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The ecological role of the Bonobo : seed dispersal
service in Congo forests
David Beaune
To cite this version:
David Beaune. The ecological role of the Bonobo : seed dispersal service in Congo forests.
Agricultural sciences. Universit´e de Bourgogne, 2012. English. <NNT : 2012DIJOS096>.
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UNIVERSITE DE BOURGOGNE
UFR Sciences de la Vie, de la Terre et de l'Environnement
THÈSE
Pour obtenir le grade de
Docteur de l’Université de Bourgogne
Discipline : Sciences Vie
par David Beaune
le 28 novembre 2012
The Ecological Role of the Bonobo
Seed dispersal service in Congo forests
Directeurs de thèse
Pr Loïc Bollache, uB
Pr François Bretagnolle, uB
Dr Barbara Fruth, MPI
Jury
Bollache, Loïc Prof. Université de Bourgogne Directeur
Bretagnolle, François Prof. Université de Bourgogne Directeur
Hart, John Dr. Lukuru Research Fundation Rapporteur
Krief, Sabrina Dr. MNHN Paris Examinateur
McKey, Doyle Prof. Université de Montpellier Rapporteur
©
1
Aux jardiniers des forêts. Puissent-ils encore vivre… tout simplement
2
Remerciements
Financeurs :
Le projet « Rôle écologique des bonobos » a bénéficié de diverses sources de financements :
Le conseil régional de Bourgogne
Le Max Planck Institute
Le laboratoire Biogéosciences
L’université de Bourgogne
La société française d’écologie
La société francophone de primatologie
D’autres entités ont aussi permis ces recherches et en sont remerciées:
3
Personnel :
Mes sincères remerciements vont tout d’abord à ceux qui ont cru en ce projet et se sont lancés dans
l’aventure avec moi. Merci Gottfried et Barbara pour votre foi dans ce nouveau volet de la vie des bonobos :
leur écologie, leur rôle dans cette fantastique forêt du Congo. Merci à Lolo qui a découvert un drôle de mail
en 2009 et y a répondu… Idem pour François. Votre curiosité et ouverture scientifique ont permis ce projet.
Je suis heureux et honoré de vous avoir eu comme superviseurs. Mais aussi comme amis. Car outre vos
qualités scientifico-intellectuelles, je vous ai apprécié pour vos qualités humaines, humanistes et de
générosité. Pour ma vie au Congo : je suis reconnaissant à Mara pour ses conseils et sa sagesse. Mes
assistants de terrain, pisteurs et puits de connaissance : Lovis, Djaman, Mangos et Lambert (spécialistes des
bonobos) ; Kabemba, Kabongo et encore Mangos (botanistes). Reconnaissance aux peuples Nkundu et les
villageois de Lompole. Ils ont choisi d’abandonner la chasse ancestrale dans leur forêt pour la science. Merci
à mes amis de LuiKotale et du MPI : Osamu, Amandine, Paulina, Chlo, Heidi, Martin, Robin (of the wood),
Isaac, Juan, captain Andrew, Delta Force, Alan, Baas the pruner, Katy, Tim, Sonja, Ben, Luc. Merci aux
amis de biogéosciences et de l’expé : merci à Jéjé, Christine, p'tit et grand Séb, Alouexe, Émilie, Coco, Julia,
Adrien, Juliette, Aude, Romain, Lucile, Caro, Anne, Thierry, ↔annick, Mathias, F↓, et bien d’autres du labo.
Élise, Lionel, Marie Laure. Merci à Roger, FX et Mathias pour les conseils en stat. Merci à Carmela, Liz,
Sam, Janet, Kerry, Didier, Liza Moscovice, PM Forget, François Feer, John Hart, Doyle McKey,
Sabrina Krief, Benjamin Borgy pour les conseils et suggestions. Merci à mes chéris : Zoé, Zizou, Zed,
Ben, Olga, Opale, Émile, Uma, Ulric, Iris, Ida, Opale, Olga, Suzie, Solea, Luna, Wilma, la grosse Paula,
Poly, Peggy, et tous les autres. Vivez ! Cette thèse je vous la dois. Merci à ma famille adorée et mes amis. Je
vous aime, vous le savez et ne lirez pas cette thèse en anglais. J’en oublie (Gaëlle, Benoit, Mich’, Fab, Am’,
Yannoch, Tony, Aurore …) et ces remerciements sont bien fades par rapport à la gratitude que vous
m’inspirez tous. Mais j’ose croire que vous connaissez déjà la sincérité de mes sentiments. Et de toute façon
il est 3 heures du mat’ je divague, et personne ne lira cette page.
Tiens d'ailleurs, je remercie Dark Vador pour m’avoir montré la force. Dudulle le champion de saut
périlleux sur bordure de trottoir. Jean Michel qui vomit plus vite que son ombre. Pablo Kadifa mon
fournisseur de cocaïne. Régina et ’les filles’ pour ces soirées mémorables (c’est bon je suis négatif). Jack
Tanner pour mon initiation homme canon sans parachute : c’était super. Mais j’ai perdu les dents de devant!
Séb et Tony Montanna les rois de la soirée cuire à moustache (maman : je fais mon coming-out ! je devais te
l’avouer). Raoul le routier polonais, tu as bien réussi ta conversion en homme, elle est bien loin ta vie de
nonne. On s’est connue à l’hôpital John Travlota lors de ma transformation trans. Eh oui j’étais une femme
moi aussi. Je m’appelais Jeannette. Je ne l’ai jamais avoué. Voici mon exutoire (et ceci explique cela, voire
plus haut). Merci à tata Giselle qui m’a tout appris dès l’âge de 7 ans, de comment égorger un poulet à mon
éveil sexuel. Pardon Karlos pour avoir déserté des camps d’entraînement, mais les grenades me faisaient mal
aux tympans. Merci à Jimmy d’avoir parsemé de références bibliographiques imaginaires cet ouvrage pour
le rendre scientifique pendant des journées entières. C’est très réussi. Tu mérites bien 6 €uros. Merci à
Helmut Cold de m’avoir accepté en apprentissage de chocolatier, après cette thèse je pourrais réaliser un rêve
de toujours : ouvrir ma boutique de sexe en chocolat sucette. Ça va marcher, la banque m’offre un prêt de
1203€ et j’ai fait une percée sur le marché kirghize (demandez-moi le braquemart au lait noisette, mmh).
Merci Julia de m’avoir aidé à me débarrasser de Martine à la ferme, souviens-toi : 1 kg de chaux pour 2 kg
de viande. Ah qu’est-ce qu’on a ri. Et pour finir merci aux membres du jury. Oups ! J’espère que vous ne
lisez pas les remerciements. C’est une perte de temps ! Bon cette partie permettra de voir ceux qui lisent un
peu trop scrupuleusement une thèse.
4
Abstract
B
Bonobos (Pan paniscus) are threatened with extinction. They are the largest primates, and the
only apes (except human), of the southern bank of the Congo Basin. Along with chimpanzees, they
are our closest living relatives and are studied by anthropologists to include/understand our hominid
origins; but what about their functional role in the forest? Would their disappearance have serious
consequences for forest ecology? Answering this question is the aim of this new project, with
several years of observations of a free-ranging habituated group of bonobos on the LuiKotale
research station (DR Congo). In this tropical rainforest, the very great majority of plants need
animals to reproduce and disperse their seeds. Bonobos are the largest frugivorous animals in this
region, after elephants. During its life, each bonobo will ingest and disperse nine tons of seeds, from
more than 91 species of lianas, grass, trees and shrubs. These seeds will travel 24 hours in the
bonobo digestive tract, which will transfer them over several kilometers (mean 1.3 km; max: 4.5
km), far from their parents, where they will be deposited intact in their feces. These dispersed seeds
remain viable, germinate better and more quickly than unpassed seeds. For those seeds, diplochory
with dung-beetles (Scarabaeidae) imrpoves post-dispersal survival. Certain plants such as Dialium
may even be dependent on bonobos to activate the germination of their seeds, characterized by
tegumentary dormancy. The first parameters of the effectiveness of seed dispersal by bonobos are
present. Behavior of the bonobo could affect the population structure of plants whose seeds they
disperse. The majority of these zoochorous plants cannot recruit without dispersal and the
homogeneous spatial structure of the trees suggests a direct link with their dispersal agent. Few
species could replace bonobos in terms of seed dispersal services, just as bonobos could not replace
elephants. There is little functional redundancy between frugivorous mammals of the Congo, which
face severe human hunting pressures and local exctinction. The defaunation of the forests, leading
to the empty forest syndrome, is critical in conservation biology, as will be illustrated here. The
disappearance of the bonobos, which disperse seeds of 65% of the tree species in these forests, or
11.6 million individual seeds during the life of each bonobo, will have consequences for the
conservation of the Congo rainforest.
Keywords Congo Basin, coevolution, conservation, ecological service, forest ecology, mutualism,
seed dispersal.
5
Résumé
L
Les bonobos (Pan paniscus) sont menacés d’extinction. Ils sont les plus grands primates et les
seuls grands singes de la rive sud du bassin du Congo. Ils sont nos plus proches parents avec les
chimpanzés et sont étudiés dans l’urgence par les anthropologues pour comprendre nos origines
Hominidé. Mais qu’en est-il de leur rôle fonctionnel dans la forêt ? Leur disparition aurait-elle des
conséquences graves sur l’écologie forestière ? Telles sont les questions de ce projet inédit, dont les
réponses sont apportées par plusieurs années d’observations d’un groupe en liberté habitué au site
de recherche LuiKotale (RD Congo). Dans cette forêt tropicale humide, la très grande majorité des
plantes a besoin des animaux pour se reproduire et disperser leurs graines. Les bonobos sont les
plus grands frugivores après les éléphants. Au cours de sa vie, chaque bonobo ingèrera et dispersera
9 tonnes de graines, de plus de 91 espèces de lianes, herbes, arbres et arbustes. Ces graines
voyageront 24 heures dans le tube digestif des bonobos, qui les transporteront sur plusieurs
kilomètres (≈1.3km; max : 4.5 km), loin de leur plante mère, où ils seront déposées intactes dans
leurs fèces. Ces graines dispersées restent viables, germent mieux et plus rapidement que les graines
non passées par le tube digestif d’un bonobo. La diplochorie, impliquant les bousiers
(Scarabaeidae), favorise leur survie post dispersion. Certaines plantes comme les Dialium
pourraient même être dépendants du bonobo pour activer la germination de leurs graines en
dormance tégumentaire. Les premiers paramètres de l’efficacité des bonobos comme disperseurs de
graines sont présents. Leurs comportements pourraient affecter la structure des populations
végétales. La majorité de ces plantes zoochores ne peuvent recruter sans dispersion et la structure
spatiale homogène des arbres laisse penser à un lien direct avec leur agent de dispersion. Peu
d’espèces remplaceraient les bonobos en terme de leur rôle fonctionnel, tout comme les bonobos ne
remplacent pas les éléphants. Il y a peu de redondance fonctionnelle entre les mammifères
frugivores très différents du Congo, qui doivent faire face aux pressions de chasse des hommes et
disparaissent localement. La défaunation des forêts, résultant dans le syndrome des forêts vides, est
un problème grave de biologie de la conservation illustré ici. La disparition des bonobos qui
dispersent les graines de 65% des arbres de leur forêt, ou encore 11.6 millions de graines au cours
de la vie d’un bonobo, est liée à la conservation des forêts tropicales humides du Congo.
Mots clefs Bassin du Congo, coévolution, conservation, dispersion de graines, écologie forestière,
mutualisme, service écologique.
6
7
Contents
Throughout the electronic version you can find
hyperlinks. CTRL+clic for linking.
LIST OF TABLES ............................................................................................................................................................ 8
LIST OF FIGURES ........................................................................................................................................................ 11
CONTRIBUTORS AND AFFILIATIONS ................................................................................................................... 16
INTRODUCTION .......................................................................................................................................................... 18
BONOBO: A BRIEF PRESENTATION .............................................................................................................................. 28
Pan paniscus myths and realities ........................................................................................................................... 29
THE CONGO FOREST ................................................................................................................................................... 41
Seed dispersal strategies and the threat of defaunation in a Congo forest .......................................................... 42
PART I ............................................................................................................................................................................. 57
SEED DISPERSAL BY BONOBOS .................................................................................................................................... 58
Seed dispersal services performed by bonobos (Pan paniscus) in tropical forest ............................................... 59
in the Democratic Republic of Congo.................................................................................................................... 59
The Bonobo-Dialium positive interactions ............................................................................................................ 85
How bonobos deal with tannin-rich fruits. Coprophagy and re-ingestion technique for Canarium
schweinfurthii ....................................................................................................................................................... 103
EXAMPLE OF APPLICATION IN PLANT CONSERVATION ............................................................................................ 115
Artificial germination activation of Dialium corbisieri by imitation of ecological process ............................... 116
PART II ......................................................................................................................................................................... 127
LONG-DISTANCE DISPERSAL ..................................................................................................................................... 128
Can fruit traits control the distance that animals move seeds during dispersal? ............................................... 129
PART III ........................................................................................................................................................................ 143
OTHER ACTORS INFLUENCING THE SEED FATE ........................................................................................................ 144
8
Bush pig (Potamochoerus porcus) seed predation of bush mango (Irvingia gabonensis) and other plant species
in Democratic Republic of Congo ........................................................................................................................ 145
Dung beetles are critical in preventing post-dispersal seed removal by rodents in Congo rain forest .............. 152
A BONOBO DOES NOT REPLACE AN ELEPHANT ......................................................................................................... 159
Doom of the elephant-dependent trees in a Congo tropical forest ..................................................................... 160
CONCLUSION ............................................................................................................................................................. 183
SYNTHESE ................................................................................................................................................................... 186
LIST OF ABBREVIATIONS ...................................................................................................................................... 191
GLOSSARY .................................................................................................................................................................. 192
APPENDIX.................................................................................................................................................................... 199
Density-dependent effects on recruitment of Irvingia gabonensis ..................................................................... 200
Daily differences in bonobo activities: More sex in the morning? ..................................................................... 205
Few organizations for bonobo conservation ....................................................................................................... 211
BIBLIOGRAPHY ......................................................................................................................................................... 213
9
List of tables
Table 1 Deforestation rate for all countries harbouring populations of ape species (1990-2010). “-“:
unavailable data. ................................................................................................................................. 27
Table 2 List of fruit-eating vertebrates categorized as seed dispersers in the study site. IUCN status
of each species was consulted in June 2011, indicating status of threat as follows: LC: Least
Concern, DD: Deficient Data, V: Vulnerable, NT: Near Threatened, E: Endangered, : stable
population trends; decrease, ? = population trend unknown. .......................................................... 53
Table 3 List of seed predators in the study site. IUCN status of each species was consulted in June
2011, indicating status of threat as follows: LC: Least Concern, DD: Deficient Data, : stable
population trends; decrease, ? = population trend unknown. .......................................................... 54
Table 4 Mean recruitment under canopy of adults of 22 tree and liana species in LuiKotale, DR
Congo. ................................................................................................................................................ 76
Table 5 Plants consumed by bonobo in LuiKotale, DRC.
W
indicates that the species exists in and is
consumed by bonobos at Wamba (Kano & Mulavwa 1984);
L
= same for Lomako (Badrian &
Malenky 1984); Fruth, unpub data); I = seeds were found intact in feces, V = seeds were tested and
found viable in nursery trials but ratio is not posted because census was interrupted. NID = not
identified. ........................................................................................................................................... 84
Table 6 Nutritional values of fruits consumed by bonobos at LuiKotale. Column Dialium and Other
fruits show mean nutritional values or concentration of macronutrients expressed as % of dry
matter. Direction of difference indicates > (higher), < (lower), or = (no difference) revealed by
application of the Wilcoxon’s signed-rank test. Nutritional values of other highly consumed fruits
(Cissus dinklagei and Greenwayodendron (Polyalthia) suaveolens) are presented for comparison.
.......................................................................................................................................................... 101
Table 7 Main plant species characteristics for feeding ecology (seven tree species, one liana: Cissus
dinklagei). Average diameter at breast high (dbh) based on 12-ha plots inventory; average foraging
session time based on 1879 h of field observation, average fruit weight and largest diameter (n =
10) and mean nutritional value. Values are mean ± SE ................................................................... 136
10
Table 8 Seed species recorded to be predated by Potamochoerus porcus in LuiKotale (DR Congo).
Tree density is estimated among 12 ha of heterogeneous terra firme forest. Tree species such as
Gilbertiodendron or Guibourtia are more abundant in homogenous forests. .................................. 150
Table 9 Elephant-dependent tree species: characteristics show averages of fruit and seed size,
species density, trunk diameter in breast-height (DBH). seed-handliong of bonobos as well as
current human interests. Fruit-size is average length, seed size is largest width or passage size
according to the morphology and passage in a digestive tract, indicated as diameter ø or length ↔
(n=10). Human usage is specified as F (fruit consumption), W (wood), TM (traditional medicine).
.......................................................................................................................................................... 168
Table 10 Recruitment of the megafaunal & control species, with mean pole recruitment under the
parent trees and density under other species. Poles density is compared with adults (from the 13-ha
plots) using Wilcoxon signed rank test (> =poles density> adults density (and reverse with <); *:p-
value<0.05, **:<0.01, ***<0.001) ................................................................................................... 178
Table 11 Examples of great ape populations eating bush mango and local elephant status (ref: 1:
this study, 2: (Hohmann and Fruth 2000), 3: (Kano and Mulavwa 1984); Furuichi pers. comm. , 4:
Renaud & Jamart pers. comm., unpub. data., 5: Boesch comm. pers., 6: (White and Abernethy
1997)) ............................................................................................................................................... 182
11
List of figures
Figure 1 Map of the field site: LuiKotale in DRC. ............................................................................ 18
Figure 2 Trail network (76 km) of the LuiKotale field site. South-west of the Salonga NP.
DRCongo. .......................................................................................................................................... 19
Figure 3 An habituated bonobo community with identifiable individuals: Bonobos of the Bompusa
community are indifferent to human observers, allowing collection of behavioral data (left : Zed
felling asleep in front of me ; right : Ida eating Haumania stem) ...................................................... 20
Figure 4 Interactive effects between frugivores and fruiting plants .................................................. 22
Figure 5 Percentage forest area losses between 1990 and 2010 for regions within the ranges of ape
species. Percentage values express the total area deforested between 1990 and 2010 relative to
forest cover in 1990............................................................................................................................ 23
Figure 6 Charcoal-making and agriculture are the main causes of deforestation linked to human
encroachment. (here for manioc cultivation, DR Congo). ................................................................. 24
Figure 7 Female Olga and her daughter Opale eating a red colobus (Procolobus tholloni),
opportunistically killed by the group. ................................................................................................ 36
Figure 8 Female bonobos’ swellings ................................................................................................. 37
Figure 9 Female-female genito-genital (GG) rubbing ...................................................................... 39
Figure 10 Map of the field site and location of plots (white dots), with main transects shown as
black lines. ......................................................................................................................................... 47
Figure 11 Proportions of species characterized by the different seed-dispersal strategies among tree,
shrub and liana species of LK. Grey = animal-dispersed, white = autochorous, black = wind-
dispersed............................................................................................................................................. 50
12
Figure 12 Proportion of different dispersal modes for all species (dark bars), and for all individuals
(light bars) present in 12x1-ha plots. Error bars indicate SE. ............................................................ 51
Figure 13 Relative parts of the interactions among the feeding sessions (22 months; 1879 hrs
continuous group scans); Error bars indicate SE. Others are honey, mushrooms, soil and unknow. 70
Figure 14 Dispersal distance kernel with fat-tailed dispersal kernel infered by bonobos (N = 75
dispersal events recorded) .................................................................................................................. 71
Figure 15 Germination rate of seven species (Cissus dinklagei, Diospyros sp., Grewia sp., Guarea
laurentii, Manilkara yangambiensis, Uapaca sp., Zeyherella longepedicellata) with (white) and
without diaspore (grey bars). ***: p < 0.001; **: p < 0.01 after t-test; Error bars indicate SE.
Numbers on the x axis are N. ............................................................................................................. 73
Figure 16 Germination rate of eight species (Cissus dinklagei, Cola gigantea, Dacryodes
yangambiensis, Dialium corbisieri, Garcinia ovalifolia, Grewia sp., Guarea laurentii, Manilkara
yangambiensis) comparing passed (dark) and unpassed seeds without diaspore (grey bars). ***: p <
0.001, *: p < 0.05 after t-test. Error bars indicate SE. Numbers on the x axis are N. ........................ 73
Figure 17 Tree species richness (dark) and abundance (grey) of seeds handled, consumed and
dispersed by bonobos. The Y-axis depicts the average proportion of tree species (diversity) or tree
individuals (abundance) per hectare (N = 12 1-ha plots). Error bars indicate SE. ............................ 74
Figure 18 Mean recruitment of pole (<10 cm DBH) under the parent crown for three control
species (autochorous) and 19 species dispersed by bonobo. The dotted line is the threshold for self-
replacement of the parent. Error bars indicate SE. ............................................................................ 77
Figure 19 Germination rates of Dialium seeds for different preconditions. Columns along X-axes
show seeds of different preconditions: Control seeds, passed seed through human and bonobos’
digestive tracts, naturally transformed and artificially activated seeds. Number in brackets indicates
sample size (N). Error bars indicate SE. Horizontal brackets indicate significance of differences
(Multiple pairwise comparisons, binomial test, Power analysis=100%). .......................................... 94
Figure 20 Time spent feeding on Dialium fruit. Bars indicate feeding sessions of Dialium fruit as
proportion of overall time spent feeding for 43 months between December 2007 and June 2011. .. 96
13
Figure 21 Bonobos eating Dialium leaves out of the fruiting season of Dialium. LuiKotale, DR
Congo. ................................................................................................................................................ 97
Figure 22 Map of the field sites: LuiKotale (LK) (S2°47’- E20°21’), Lomako (Loma) (N0°51’,
E21°5’) and Wamba (W) (N0°11’, E22°37’), Democratic Republic of the Congo ........................ 107
Figure 23 Condensed tannin (% in dry matter) in fruit. Outliers are Autranella congolensis,
Canarium schweinfurthii, Musanga cecropioides and Strombosia glaucescens. Parinari excelsa is
the maximum value of the range. S. glaucescens fruits are not consumed by bonobos. ................. 110
Figure 24 Emile chewing wadges of Parinari excelsia. LuiKotale, DR Congo. ............................. 112
Figure 25 Seeds transformation of intact (left) versus perforated seed coat (right), after 48h of
immersion in water. (a): Weight ; (b): Length ; (c): Breadth. .......................................................... 123
Figure 26 Germination in relation to time in Dialium corbisieri according to treatment (perforated
seed coat).......................................................................................................................................... 124
Figure 27 Illustration of the mechanistic seed dispersal estimation with an example of dispersal
event (Gambeya lacourtiana). Identified bonobo feeding trees are georeferenced during group
observations (2007-2011) and bonobo movement daily recorded (dark track log). Theoretical seed
deposition site are determined by actual bonobo position (dark track log) after 24 h corresponding
to the seed transit time. .................................................................................................................... 134
Figure 28 There is no correlation between feeding time spent on the fruiting plant and the dispersal
distance by bonobo. For 22 fruiting species analysed as whole (n=278) or other species as Dialium
sp. (122) or Cissus dinklagei (50). ................................................................................................... 138
Figure 29 Size effect on the transit time (35 small:<2mm, 28 medium-sized:2-10mm and 61 large
seeds:>10mm). No significant effect (F
2,119
= 0.38, P = 0.68). Mean Transit time = 24:00 h. ........ 139
Figure 30 Seed dispersal distribution infered by bonobo based on movement behavior (n = 1200
dispersal events with all plant species) and mean transit time for seed (24:00 h). .......................... 140
14
Figure 31 Seed dispersal distances infered by bonobos for eight plant species. (Cissus dinklagei,
Dialium sp., Gambeya lacourtiana, Grewia sp., Pancovia laurentii, Placodiscus paniculatus,
Polyalthia suaveolens, Treculia africana). ...................................................................................... 141
Figure 32 Picture of bush pig (Potamochoerus porcus) camera trapped in LK, 2011. ................... 148
Figure 33 Seed predation rate within a 100 m radius around the parent bush mango (I. gabonensis).
There was no distance effect (p-value>0.33). .................................................................................. 151
Figure 34 Infrared records on faecal odour attraction: Arrows point at bonobo faecal odour and
control stick with giant pouched rat (Cricetomys emini) (a) and African brush-tailed porcupine
(Atherurus africanus) (b) each sniffing at the treated wooden stick. ............................................... 155
Figure 35 Effect of seed burial on seed predation: Percentage of buried (dotted line) vs. unburied
(continuous line) seeds in relation to time of Cissus dinklagei, Polyalthia suaveolens and Dialium
corbisieri. ......................................................................................................................................... 157
Figure 36 Demography of 6 control tree species censused in 13-ha plots. Y-Axes shows proportion
of survivors. X-axes shows cohort size. ........................................................................................... 171
Figure 37 Demography of 18 megafaunal tree species censused in 13-ha plots. Bars indicate cohorts
starting with saplings. Red cross shows absence of the first cohort. Y-Axes shows proportion of
survivors. .......................................................................................................................................... 173
Figure 38 Morisita’s index (I
M
) of adults, poles, saplings and seedlings of three autochoric (blue),
three zoochoric (green) and six megafaunal species (yellow) of 13 one-ha-plots. The index-value is
1 when individuals are randomly dispersed, values greater than one indicate clumping, values
between 0 and 1 indicate uniformity.The higher the value, the more clumped the distribution. ..... 174
Figure 39 Mean number of poles present (or recruited) under parent tree. For autochoric (blue),
zoochoric alternative partners (green) and zoochoric megafaunal partners tree species (red). The
dotted line is the theoretical value of pole recruitment necessary for self replacement of the parent
tree. Y-error lines in bars indicate standard errors. .......................................................................... 176
Figure 40 Empty forest syndrome and the possible effect on the plant community scenario. ........ 183
15
Figure 42 Nombre de publications scientifiques par année contenant le terme « Pan paniscus »
référencé par ISI Web of Knowledge THOMSON REUTERS, dans le titre (vert) et dans le sujet
(rouge). ............................................................................................................................................. 187
Figure 43 Sampling area. Red spots representing adult trees .......................................................... 202
Figure 44 The density dependent effect of Irvingia gabonensis. No recruitment under the parental
trees (n=54) ...................................................................................................................................... 203
Figure 45 Seedling and adult tree of Irvingia gabonensis ............................................................... 204
Figure 46 AM (left) and PM (right) comparison, 1. feeding activity, 2. average speed, 3. group size,
4.female composition, 5. copulation rate, 6.GG rubbing rate,. NS= non significant difference. ... 208
Photos by David Beaune
16
Contributors and affiliations
David Beaune Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
Laboratoire Biogéosciences, UMR CNRS 5561, Université de Bourgogne, 6
blvd Gabriel, 21000 Dijon, France
Loïc Bollache Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6
blvd Gabriel, 21000 Dijon, France
Chloé Bourson Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6
blvd Gabriel, 21000 Dijon, France
François Bretagnolle Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6
blvd Gabriel, 21000 Dijon, France
Pamela Heidi Douglas Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
Barbara Fruth Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
Gottfried Hohmann Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
Musuyu Désiré Muganza Institut National de Recherche Biomédicale. Avenue de la Démocratie,
Kinshasa-Gombe B.P. 1197, RDC
Tetsuya Sakamaki Primate Research Institute, Kyoto University, Kanrin 41, Inuyama, Aichi,
484-8506, Japan
Martin Surbeck Max Planck Institute for Evolutionary Anthropology, Department of
primatology, Deutscher Platz 6, Germany
17
Field contributors
Alan Cowlishaw ; Amandine Renaud ; Andrew Fowler ; Bas Van Der Veer ; Ben Buckley ; Booto
Rigobert (Rigo) ; Delphine Ronfot ; Isaac Schamberg ; Juan Salvador Ortega Peralejo ; Kabemba
Imanawanga ; Kabongo Bobanza ; Katalin Csatadi ; Lambert Booto (Tata Mulee) ; Lovis Loseka
(Tati Waata) ; Luke Ward ; Mangos Longomo ; Mara Etiké ; Mobembo Apoluke (Djaman) ; Osamu
Terao ; Pauline Toni ; Robin Loveridge ; and others…
18
Introduction
T
T
T
his project was born in the middle of the Congo in 2008, in one of the few free-ranging
bonobo communities studied by a permanent team of scientists. I was camp manager in the Max
Planck Institut‘s field station: Luikotale (LK,
Figure 1, Figure 2). Looking at the bonobos and how
they behave in the wild, obvious questions arise for an ecologist. ‘These animals interact with many
plants and seem to be very important, but how? For how many species? What is the effect on forest
structure and on ecological network?’ Additionally, these great apes are critically threatened by
extinction (IUCN 2012). They might disappear from the system. What risk would their extinction
entail for the ecosystem? The project on the ecological role of the bonobo was thus born, profiting
from the expertise of the
Max Planck institute for evolutionary anthropology in primatology and the
Biogéosciences laboratory in ecology. This project is an international collaborative project focusing
on an original chapter in the life of bonobos: their ecological services in the ecosystem.
Figure 1 Map of the field site: LuiKotale in DRC.
19
Only recently described by science (Coolidge 1933) and studied in the wild only since the late
1970s (Kano 1980), the bonobos gained popular interest only recently. They gained interest because
of their phylogenic proximity to humans and their peculiar social behavior (de Waal 1997). They
were thus mainly studied by anthropologists without a particular interest in ecology and forests.
Since the appearance of the young field of “bonobology”, only two short notes published in Journal
of Tropical Ecology stated the understandable role of these large frugivores in seed dispersal; with
seeds found in feces and remaining viable, and secondly about the long dispersal distance infered
by bonobos (Idani 1986; Tsuji, Yangozene & Sakamaki 2010).
Figure 2 Trail network (76 km) of the LuiKotale field site. South-west of the Salonga NP. DRCongo.
The goal of this study is to investigate these questions and eventually analyze the ecological
role of the bonobo in the ecosystem.
Bonobos are frugivores and primates are well known to be important seed dispersers
(Sussman 1991; Lambert & Garber 1998; Poulsen, Clark & Smith 2001a; Vulinec, Lambert &
2km
20
Mellow 2006; Gross-Camp, Masozera & Kaplin 2009). Not surprisingly, the main ecological
service investigated is seed dispersal.
To do this, a wild bonobo group exists and can help to improve our knowledge on plant-
animal interactions. Near the Salonga National Park, the Bompusa community is a free-ranging
group of 25-30 bonobos habituated by scientists beginning a decade ago (Hohmann & Fruth
2003c);
Figure 3). Plant biodiversity has been studied over the long term and the great majority of
trees, shrubs, lianas and herbs are identified to species level (Fruth 2011).
Figure 3 An habituated bonobo community with identifiable individuals: Bonobos of the Bompusa community are
indifferent to human observers, allowing collection of behavioral data (left : Zed felling asleep in front of me ; right :
Ida eating Haumania stem)
This thesis is organised in sections which can be read independently. Each section is based on
a paper submitted or in the process of being submitted, to a peer-reviewed journal in ecology,
conservation biology or primatology. The introductive part is an introduction the studied model,
Pan paniscus, in which I review the most recent research on bonobos. The second sub-section
21
introduces the different seed dispersal strategies of plants in the LuiKotale forest and the importance
of frugivores in this system. This sub-section also identifies the seed disperser and seed predator
guilds and the human pressure on each of them.
Part I is the core of the project, presenting data on the ecological role of the bonobo. The first
sub-section is a general analysis of how bonobos affect seed survival, germination rate and speed,
and examines the number of plant species whose reproduction is affected by bonobos. The
functional redundancy with other primates is also tested, in addition to an estimation of the seed
rain infered by a bonobo population and an examination of how plants deal with the absence of seed
dispersal. The second sub-section focuses more specifically on a dominant tree genus in examining
the mutualism between bonobo and Dialium (Fabaceae: Caesalpinioideae). This part documents the
bonobo’s positive effect in this animal-plant interaction (
Figure 4). Another investigation (third sub-
section) focuses on fruits that produce chemical components such as tannins that deter consumers
(direct deterrence hypothesis) and how these chemicals affect interaction with bonobos.
The last sub-section ends with an examination of the effect of bonobos on seed germination. In this
section the seed dormancy of a dominant tree species, important ecologically, economically and in
conservation, was broken by imitation of an ecological process. Artificial activation of seed
germination in Dialium corbisieri is tested.
Part II examines more fundamental aspects of the ecology of bonobos. Dispersal distances are
compared among plant species dispersed by bonobos, in order to see whether fruit traits can affect
the dispersal behaviour of this dispersal vector.
22
Figure 4 Interactive effects between frugivores and fruiting plants
Part III includes other actors of the ecological network that affect post-dispersal seed fate.
One subsection starts with the biggest seed predators of the system, bush pigs (Beaune et al. 2012a),
and the second introduces rodents and dung beetles (Beaune et al. 2012b). Other important actors in
the Congo forest are elephants (Campos-Arceiz & Blake 2011). However, forest elephants are
seriously threatened with extinction in Africa (Blake et al. 2007). It is thus critical to assess if
another animal vector, such as bonobo, can replace the ecological service of seed dispersal that was
previously assured by elephants. Functional overlap between the two biggest frugivorous mammals
of the forest is then investigated
This project does not fill the gap in data on processes occurring between seed deposition and
the arrival to maturity of an adult plant. However, it provides a base for future work on seed
dispersal processes in Congo forests, and new evidence for the urgent need to protect our cousin,
the bonobo, and the other animals of the forest.
23
4%
13%
8%
11%
8%
32%
18%
14%
0%
10%
20%
30%
40%
Democratic
Republic of
the Congo
West Africa Central Africa East Africa Central Africa East Africa Southeast
Asia
Southeast
Asia
Forest lost (1990-2010)
Bonobo
Chimpanzee
Gorilla
Orangutan
Gibbon
Figure 5 Percentage forest area losses between 1990 and 2010 for regions within the ranges of ape species. Percentage
values express the total area deforested between 1990 and 2010 relative to forest cover in 1990. Calculation based on
FRA FAO 2010
In forest conservation, deforestation is the most obvious and visible fact. Based on FAO data
(FAO 2010), we can see the deforestation rate of countries hosting apes
. Figure 5 shows major
forest area loss for all ape species over the last two decades. However, tropical forests face another
threat: defaunation. Many countries conserve rare primary forests and relatively large forested areas
(
Table 1), but without protection, hunting pressures empty the forest of its large and medium-sized
animals and thus affect ecological functions such as seed dispersal (Redford 1992). The forests
remain structurally intact, with large healthy trees and large areas of ‘intact’ forest that we can
assess in tables. Nevertheless the functional effects of emptying the forest of its animals (Terborgh
et al. 2008) are not revealed by tables and deforestation reports. Forest conservation should be
considered not only in terms of surface area protected against deforestation but in temrs of survival
of the entire system that assures ecological services, and this is the point of the main chapter of this
thesis.
24
Figure 6 Charcoal-making and agriculture are the main causes of deforestation linked to human encroachment. (here
for manioc cultivation, DR Congo).
25
Species
Countries
Extent of forest
in 2010 (1000ha)
Forest
% of
land
area
Primary forest
annual change
rate (2005-
2010)
Forest annual
change rate
(2005-2010)
Forest
area lost
(1990-
2010)
Population
status
Primary
All
forest
1000ha/yr
%
1000ha/yr
%
1000ha
Pan
paniscus
Central
Africa
Democratic Republic of
the Congo
-
154135
68
-
-
-311
-0.2
-6228
Pan
troglodytes
West Africa
Benin
0
4561
41
0
-
-50
-
1.06
-1200
extinct
Burkina Faso
0
5649
21
0
-
-60
-
1.03
-1198
extinct?
Ivory Coast
625
10403
33
0
0
-
-
181
Gambia
1
480
48
-
-
4.36
2
0.38
38
extinct
Ghana
395
4940
22
0
0
-115
-
2.19
-2508
Guinea
63
6544
27
0
0
-36
-
0.54
-720
Guinea-Bissau
0
2022
72
0
-
-10
-
0.49
-194
Liberia
175
4329
45
0
0
-30
-
0.68
-600
Mali
0
12490
10
0
-
-79
-
0.62
-1582
Senegal
1553
8473
44
-9
-
0.57
-40
-
0.47
-875
Sierra Leone
113
2726
38
-4
-
3.21
-20
-0.7
-392
Togo
0
287
5
0
-
-20
-
5.75
-398
extinct
Central
Africa
Angola
0
58480
47
0
-
-125
-
0.21
-2496
Cameroon
-
19916
42
-
-
-220
-
1.07
-4400
Central African Republic
2370
22605
36
-76
-
2.94
-30
-
0.13
-598
Congo
7436
22411
66
-6
-
0.08
-12
-
0.05
-315
Democratic Republic of
the Congo
-
154135
68
-
-
-311
-0.2
-6228
Equatorial Guinea
0
1626
58
0
-
-12
-
0.71
-234
Gabon
14334
22000
85
-330
-
0
0
0
26
2.16
Nigeria
-
9041
10
-65
-
-410
-4
-8193
East Africa
Burundi
40
172
7
0
0
-2
-
1.01
-117
Rwanda
7
435
18
0
0
10
2.47
117
Sudan
13990
69949
29
-11
-
0.08
-54
-
0.08
-6432
Uganda
0
2988
15
0
-
-88
-
2.72
-1763
United Republic of
Tanzania
0
33428
38
0
-
-403
-
1.16
-8067
Zambia
0
49468
67
0
-
-167
-
0.33
-3332
extinct
529558
-51506
Gorilla
Central
Africa
Angola
0
58480
47
0
-
-125
-
0.21
-2496
Cameroon
-
19916
42
-
-
-220
-
1.07
-4400
Cameroon
-
19916
42
-
-
-220
-
1.07
-4400
Central African Republic
2370
22605
36
-76
-
2.94
-30
-
0.13
-598
Congo
7436
22411
66
-6
-
0.08
-12
-
0.05
-315
Democratic Republic of
the Congo
-
154135
68
-
-
-311
-0.2
-6228
Western=
extinct?
Equatorial Guinea
0
1626
58
0
-
-12
-
0.71
-234
Gabon
14334
22000
85
-330
-
2.16
0
0
0
Nigeria
-
9041
10
-65
-
-410
-4
-8193
East Africa
Rwanda
7
435
18
0
0
10
2.47
117
Uganda
0
2988
15
0
-
-88
-
2.72
-1763
333553
-28510
Pongo
Southeast
Asia
Indonesia
47236
94432
52
-103
-
0.22
-685
-
0.71
-24113
Malaysia
3820
20456
62
0
0
-87
-
0.42
-1920
114888
-26033
Hylobatidae
Southeast
Asia
Bangladesh
436
1442
11
0
0
-3
-
0.18
-52
Brunei Darussalam
263
380
72
-2
-
0.89
-2
-
0.47
-33
Cambodia
322
10094
57
0
0
-127
-
1.22
-2850
East India
-
-
-
-
-
-
-
-
Indonesia
47236
94432
52
-103
-
-685
-
-24113
27
0.22
0.71
Lao People's Democratic
Republic
1490
15751
68
0
0
-78
-
0.49
-1563
Malaysia
3820
20456
62
0
0
-87
-
0.42
-1920
Myanmar
3192
31773
48
0
0
-310
-
0.95
-7445
Thailand
6726
18972
37
0
0
15
0.08
-577
Viet Nam
80
13797
44
-1
-
1.21
144
1.08
4434
Yunnan (south China)
-
-
-
-
-
-
-
-
Table 1 Deforestation rate for all countries harbouring populations of ape species (1990-2010). “-“: unavailable data.
28
Bonobo: a brief presentation
29
Pan paniscus myths and realities
David Beaune
Published in Revue de primatologie
30
Abstract
Bonobos are our closest living relatives along with chimpanzees. They attract much attention
from anthropologists who want to better understand our primate origins and more recently from the
public because of their remarkable behavior and matriarchal social system. New published insights
from recent years allow us to better know Pan paniscus. This review describes the most recent
findings: bonobos, chimpanzees, and humans ought to be part of the same genus (Homo or Pan)
according to our genetics. bonobos have impressive cognitive ability to communicate with lexigram
and sign-language, solve problems and use tools. Females have high social status in the group due
to female association and coalition. The society is not really characterized by female dominant but
rather by co-dominance of associated females. They are not purely egalitarian but non-violent and
tolerant. Neither lethal aggression nor infanticide were observed and are not expected. Sex has a
pivotal role in this pacifist society, which lacks sexual restrictions with the one exception of incest.
Bonobos are probably a key species in forest ecology through their seed dispersal mutualism with
plants whose fruits they eat. We continue to discover fascinating biological facts about our cousins
who are in danger of extinction. A few of these are described here.
Key words: Great apes, Hominid, homosexuality, matriarchal, Pan, sexual behavior.
Résumé
Les bonobos sont nos plus proches parents vivants avec les chimpanzés. Ils attirent beaucoup
d'attention de la part des anthropologues qui cherchent à comprendre nos origines simiesques. Plus
récemment, ils attirent l’attention du grand public en raison de leur comportement remarquable et
de leur système social matriarcal singulier. Les médias et certaines aspirations philosophiques ont
rapidement érigé les bonobos comme nos plus proches parents, vivant en société pacifique de
végétariens féministes, et gouvernée par le sexe. Mais la barrière entre l’homme et l’animal était
sauve pour beaucoup tant que ce lubrique primate ne manifestait aucune capacité à exécuter ce qui
fait le propre de l’homme. Or les nouvelles découvertes publiées ces dernières années nous
permettent d’en savoir plus sur Pan paniscus. Cette revue décrit les résultats les plus récents : Selon
les généticiens, bonobos, chimpanzés et humains appartiennent au même genre (Homo ou Pan)
avec plus de 98% de gènes communs et un ancêtre partagé il y à 5 à 6 millions d’années. Il est
récemment prouvé que les bonobos possèdent les capacités cognitives pour communiquer mais sans
pharynx (langage des signes, lexigramme). Les bonobos peuvent résoudre des problèmes complexes
et utiliser des outils. En captivité certains bonobos taillent des pierres, allument du feu avec un
briquet ou utilisent une pelle pour creuser. Les femelles ont le statut social le plus élevé du groupe
31
grâce à l'association et à la coalition entre femelles. La société n'est pas vraiment femelles-
dominantes, mais plutôt co-dominante. La société n’est pas purement égalitaire, mais non violente
et tolérante. Ni les agressions mortelles ni l'infanticide n'ont été observés à ce jour en milieu naturel
ou en captivité. Le sexe a un rôle primordial dans cette société pacifique. Il n’y a pas de restriction
sexuelle excepté l'inceste. Les bonobos sont une espèce clef dans leur écosystème, grâce au service
écologique fournit de dispersion de graines. De plus en plus de découvertes fascinantes naissent au
sujet de nos cousins qui sont en danger d'extinction et pourraient disparaître d’ici quelques
décennies.
Mots clefs : Comportement sexuels, grands singes, Hominidé, homosexualité, matriarchale, Pan
32
Introduction
Bonobos are one of the large mammal species most recently discovered by science. First
informally described in 1929, they were named Pan paniscus in 1933 (Coolidge 1933). Since
Robert Yerkes in the thirties, bonobos were studied in captivity and more recently in the wild
beginning in 1973 with Takayoshi Kano at Wamba field site, DR Congo (Kano 1980). With
Congolese wars and political instability, studies in the field were slowed down but research teams
persevered and new exciting discoveries about this great ape allow us to better know our cousins’
biology and also allow insights into our own origin. This paper reviews the latest news from the
bonobos. Some old views of bonobos are obsolete; some previous questions have been answered
while others remain unsolved. This review based on recent literature is also punctuated by my own
observations with an habituated free-ranging bonobo community at the LuiKotale field site
(Hohmann & Fruth 2003c). My main research focused on the bonobo ecology. I recorded 1879
hours of behavioral data within this community of 25-35 identifiable bonobos, through 22 months
of field work (2008-2011). Other discoveries, I hope, will astonish you with new insights about one
of the planet’s most fascinating animals and one of our closest living relatives.
Our closest living relative?
Within our own family of the Hominidae, great apes of the genus Pan, including bonobos (Pan
paniscus) and chimpanzees (Pan troglodytes), are our closest living relatives. Chimpanzees live in
four major populations, including those located in western Africa (P. t. verus), equatorial Africa (P.
t. troglodytes and P. t. schweinfurthii), and the Gulf of Guinea region (P. t. ellioti); with distinct and
full species proposed and still debated today (Gonder et al. 2011). Described as pygmy
chimpanzees in literature before the 1980s, bonobos have more gracile limbs than chimpanzees but
are similar in many other morphological traits and in body size (♀≈33-36kg, ♂≈43-46kg; (Coolidge
& Shea 1982; Parish 1996)) to the other Pan species. However, their frequently bipedal posture
(D’Août et al. 2004), their morphology, and neotenic characteristics (Shea 1983) which they share
with us (Homo sapiens sapiens), caused many anthropologists to propose the bonobo as the best
model for our closest living relative.
However, contrary to popular belief, bonobos are not more closely related to us than are
chimpanzees. We share a common ancestor with both Pan which dates to 5-6 million years ago, and
approximately 98% of our DNA (Wildman et al. 2003; Patterson et al. 2006; Prufer et al. 2012)
with both species. Bonobos and chimpanzees diverged from 0.93 (Won & Hey 2005) to 2 million
years ago (Raaum et al. 2005) and are separated by the Congo River, which acts as a biogeographic
barrier by splitting the Congo basin. Therefore, both are genetically equidistant to us.
33
Pan troglodytes and P. paniscus are so close to us that an increasing number of scientists propose a
fusion of the genus of our cousins Pan, with our own genus Homo; with the proposed classification:
Homo sapiens (humankind), Homo troglodytes (chimpanzee), and Homo paniscus (bonobo)
(Wildman et al. 2003). This little taxonomic revolution could be difficult for the general public to
accept, but an extraterrestrial taxonomist would not hesitate. One day we might accept ourselves as
the third chimpanzee (Diamond 1991). Another more philosophical rapprochement is the Great Ape
Project (GAP) launched in the 1990s (Cavalieri & Singer 1993). It is an appeal of 36 scientists from
different disciplines aiming at the legal equalization of the non-human great apes with humans. The
central point of the initiative is the "Declaration on Great Apes", claiming the inclusion of great
apes in the "community of equals" and thus securing three basic rights for all great apes: 1. The
Right to Life; 2. Protection of Individual Freedom; 3. The Prohibition of Torture. Furthermore, the
project pleads for the idea of conferring the "moral status of person" on great apes. But beyond
religion and ethics, rejection of this idea is mainly due to pressure for maintaining the use of living
apes as “biological material” for experimentation in industry (Carlsson et al. 2004). We can note
that the United States and Gabon are the only remaining countries allowing such research.
A tool maker?
Chimpanzees are well recognized as tool makers in the wild, with cultural variation in usage among
populations across Africa (Whiten et al. 1999). For bonobos, tool-related behaviors are observed in
wild populations but are rare and less sophisticated than those observed in chimpanzees (Kano
1982; Ingmanson 1996; Hohmann & Fruth 2003a). This bonobo difference could be explained by
the fact that they inhabit a less challenging environment than chimpanzees with no need for
weapons, or may simply the general lack of studies of this species compared to chimpanzees.
However, in captivity, tool making and usage by bonobos have both been well described (Jordan
1982; Toth et al. 1993; Gold 2002; Mulcahy & Call 2006; Gruber, Clay & Zuberbühler 2010).
Kanzi and Pan-Banisha, a famous male and female who have gained widespread attention for their
skills in language and have lived in the stimulating environment of the Great Ape Trust of Iowa
since 2005 (Savage-Rumbaugh & Lewin 1994). They can light a fire with a lighter, cook a meal,
roast marshmallows and perform other impressive tasks. They have the basic stone-tool making
skills required to produce usable flakes and fragments by hard-hammer percussion (Toth et al.
1993) and their techniques are improving (Schick et al. 1999). Their reported tool production and
utilization for food retrieval (digging or breaking wooden logs) exhibits Homo-like technological
competencies (Roffman et al. 2012).
The most recent results appear to describe bonobos as having a similar repertoire in captivity, and
tool-using capabilities equal to those of chimpanzees (Herrmann, Wobber & Call 2008; Gruber,
34
Clay & Zuberbühler 2010). Bonobos as chimpanzees use less dramatic tools for social purposes,
games or comfort (cleaning with specific leaves, use of leaves as an umbrella against rain), while
chimpanzees use also impressive reported tool techniques in the context of difficult food-
acquisition tasks. Another remarkable point is that just like chimpanzees, female bonobos are more
willing to use tools than males (Gruber, Clay & Zuberbühler 2010). Because wild and captive
bonobos share the same cognitive abilities required for tool use, such behavior is expected to occur
in wild bonobos as well.
Communication
Bonobos, like gorillas and chimpanzees, show a human-like asymmetry in language-related brain
areas, which has been correlated with language dominance (Cantalupo & Hopkins 2001). But
articulation of speech is physically impossible and language is restricted to vocalizations and
gestures (Pika, Liebal & Tomasello 2005; Pollick & de Waal 2007). We share several
communicative roots like the gestural NO by head shaking (Schneider, Call & Liebal 2010) and
almost all of these are understood by humans. Gestural communications include sexual invitation
with body posture and hand raising, begging, embracing, mouth/tongue kissing, kicking, slapping,
etc. with facial nuance and context dependence (Pika, Liebal & Tomasello 2005).
Apes cannot ‘speak’. They can however communicate a wide range of information and are even
able to talk with us with the help of technology. Kanzi understands spoken English and
communicates with a lexigram keyboard. He also modulates his vocalization with evident structural
differences produced within a specific semantic context (Taglialatela, Savage-Rumbaugh & Baker
2003). A similar structural difference was observed in other captive bonobos which use a specific
acoustic structure in long and complex call sequences related to a precise type of food. This
suggests that bonobo food-calling sequences convey meaningful information to other group
members (Clay & Zuberbuhler 2009).
In the wild, bonobos exchange long distance calls (high hoot) between groups (Hohmann & Fruth
1994). What kind of information do they exchange? The study of communication in wild bonobos
is promising and may lead to fascinating discoveries.
A female dominant society?
Bonobos live in a male-philopatric structure. This means that males are born and die in the same
group while females of 6–13 years emigrate to neighboring groups (Furuichi et al. 2012). Males
will stay all their lives with their mothers. Females are accepted into new groups weaving future
alliance bonds. Female chimpanzees do not have frequent social interactions with other females,
whereas female bonobos maintain close social associations with one another (Furuichi 2011).
35
The result is a singular primate society: a matriarchal bonobo society in clear contrast with the
patriarchal societies of chimpanzees, other primates and most human societies (Parish 1996;
Sommer et al. 2011). This unique trait attracted feminists, public attention and debate about male-
female dominance. In early studies (mainly male) scientists described this behavior as “strategic
male deference” or males being chivalrous to females as a strategy to obtain sex. This made it
easier to admit female dominance in bonobo groups (Parish, De Waal & Haig 2000). Females most
often initiate sexual interactions and ranging behavior (Furuichi 2011), have priority of access to
preferred food (Hohmann & Fruth 1993; White & Wood 2007) and will sometimes chase or be
aggressive towards males (i.e. the definition of ‘dominance’; NB: not within chimpanzees). Females
are so influential in the groups that mothers improve the mating success of their sons when present
(Surbeck, Mundry & Hohmann 2011). In male-male aggression, mothers and females can intervene
and decide the outcome of the situation, and eventually influence their son’s rank in the hierarchy
(Furuichi 2011). Despite modest physical dimorphism (female body size is 82.5% that of males)
females gain power by cooperation and coalition formation (Parish 1996; White & Wood 2007).
However, female dominance over males is not a rule. Males are consistently dominant in dyadic
interactions (White & Wood 2007). To conclude, it is clear that adult females occupy high
dominance status in bonobo societies and that females are rather co-dominant to males (Surbeck et
al. 2012). Differences in dominance among individuals are slight but measurable (see below) but
we should keep in mind that bonobos show nothing that is comparable to the strong dominance with
submission enforced by violence that is characteristic of chimpanzee societies. Are we close to an
egalitarian society? Not really, but non-violence gives us this impression.
A peaceful vegetarian society?
Because they use sexual behavior in several contexts where other species use aggression, bonobos
may be viewed as peaceful. However several injuries have been observed in captivity and in the
wild, resulting from beatings, or biting on fingers, faces, or genitals (Parish, De Waal & Haig
2000), pers. obs). Recently, the public was shocked by a case of cannibalism among wild bonobos
where a baby was consumed by a group, including the mother (Fowler & Hohmann 2010). We
should note that the cause of death remains unknown and violence was not observed. Before the
carcass was eaten (it was, after all, meat), the mother, with great affection, carried her offspring’s
body around with her for a whole day. Indeed, bonobos are not the pure vegetarians that we first
thought them to be (
Figure 7). Bonobos kill and eat duikers, birds, rodents and monkeys (Hohmann
& Fruth 1993; Hohmann & Fruth 2008; Surbeck & Hohmann 2008; Surbeck et al. 2009). However,
although bonobos appreciate and are excited by meat, they are not organized hunters and carnivory
36
thus remains opportunistic and accounts for only a marginal part of their diet (Oelze et al. 2011),
i.e., 0.9% ± SE 0.2 of feeding sessions; N = 1879 hrs of observation (Beaune 2012).
Although linear dominance can be determined by agonistic interactions, bonobos are non-violent
and mainly engage in chasing acts, submissive behaviours and deference (Hohmann & Fruth 2003b;
Surbeck, Mundry & Hohmann 2011). Bonobos are highly tolerant and cooperative (Hare et al.
2007). While most primate groups have territorial conflicts, bonobos behave peacefully with
neighbouring community, with a large inter-group home range overlap (at Wamba 66% of the
group’s home range overlaps with those of neighbour groups (Kano & Mulavwa 1984)). When two
groups meet, they often engage in inter-group sexual relations (often female-female), grooming,
feeding and foraging together, and sometimes sleeping at the same nesting place (Hohmann & Fruth
2002; Furuichi 2011). So far, infanticide and lethal aggression have never been observed in Pan
paniscus. We can definitively say that the bonobo has a peaceful nature.
Figure 7 Female Olga and her daughter Opale eating a red colobus (Procolobus tholloni), opportunistically killed by
the group.
The most lascivious hominid?
For the public, the bonobo is our lubricous cousin, performing Kama Sutra positions all day long
(de Waal 1997). Actually, the frequency with which bonobos engage in sex is less than an average
37
of 0.3 copulation/hour (Furuichi & Hashimoto 2002), with intercourse lasting less than a minute
(usually a few seconds). Compared to us, bonobos’ frequency of intercourse is definitely higher,
with humans averaging 1 to 3 marital coitus per week, the freqeuncy declining with age (Kinsey
Institute 2012). The length of coitus fo rhumans is generally longer than a minute with an average
of 5 min for humans (Kinsey Institute 2012). Bonobos do not have more sex than chimpanzees,
nevertheless females of this species do have more sex and start earlier in life than male bonobos
(Takahata, Ihobe & Idani 1999; Hashimoto & Furuichi 2006). Most importantly females have sex
during non-fertile periods or in non-swelling episodes (Furuichi & Hashimoto 2004). And when
fully tumescent, sexual swelling signals occur even during non-conceptive periods. This is called
“pseudo-estrus” (Furuichi 2011). Thus females with true and confusing estrus signals are
proportionally more numerous than females displaying no estrus signals so they are less
monopolizable by an alpha male (preventing sexual harassment and infanticide) (Furuichi 2011).
See
Figure 8 for swellings). Male bonobos do not sexually coerce females (Hohmann & Fruth
2003b) and therefore, their sexual solicitation has to be accepted by the female for intercourse to
occur. This strategy, contrasting with chimpanzees, is evolutionarily stable and quite similar to
behaviour in most human societies (except that our species lost the receptive signals potentially as a
result of similar selective pressures).
Sex is routinely used for non-reproductive goals (tension-reduction, reconciliation, bartering for
social favors, and sex for food exchanges). Behavioral observations support the hypothesis that sex
reduces tension and is the basis of this largely peaceful society (Hohmann & Fruth 2000; Palagi,
Paoli & Tarli 2004; Hare et al. 2007) and now scientists are trying to test this hypothesis through
hormonal experimentation (Hohmann, Mundry & Deschner 2009; Wobber et al. 2010).
Figure 8 Female bonobos’ swellings
38
Sexual taboos? Homosexuality does not matter…
Bonobos practice public sex (Clay & Zuberbühler 2012) rather than the more secretive sexuality of
humans and chimpanzees. Bonobos are bisexual apes and homosexual encounters are common,
especially among females (Fruth & Hohmann 2006). Female bonobos engage in a unique sexual
behavior also found in humans (tribadism) termed genito-genital (GG) rubbing in which they
embrace ventro-ventrally and rub their genital swellings together with rapid sideways movements
(Hohmann & Fruth 2000) (Figure 9). Sex seems to be the cement for social bonds. This is why
females use it predominantly for their alliance. Sex with high-ranking females could be strategic for
subordinates, who can call loudly an audience to acknowledge the scene (Clay & Zuberbühler
2012). Bonobos can have oral, manual and foot sex. They perform multiple positions not found in
other non-human primates (such as ventro-ventral or missionary position in humans). Males can be
observed mounting other males without intromission, dorso-dorsally rubbing their scrota with
sideways movements, or performing face to face ersatz fencing with erect penises. Juveniles can
also be involved (de Waal 1997), pers. obs). Bonobos seem to have no limits to the choice of sexual
partners with the exception of incest.
Gardener of the forest?
The ecological role of the bonobos has been recently studied at LuiKotale (Beaune 2012). Bonobos
are efficient seed dispersers; they spend ≈3.5 hrs/day swallowing the seeds of trees, lianas and herbs
of more than 91 species and disperse them at very long distances (0-4.5km). In its entire lifespan, a
bonobo should disperse almost 12 million seeds (or 9 tons; excluding seeds <2 mm such as Ficus
spp). The great majority of the seeds passed through the gut is viable (34/35 tested species).
Compared with seeds not passed through the gut, bonobos’ seeds germinate faster and at a higher
rate. Furthermore, seeds disseminated by endozoochory with bonobos are better able to escape seed
predators, thank to dung beetles attracted by bonobos’ feces (Beaune et al. 2012a). For certain
species such as the velvet tamarind, bonobos are germination activator (Beaune et al. submitted). In
a Congo forest we estimate that 65% of the individual trees in the forest community are
disseminated by bonobos. The great majority of the tree species does not recruit and self-replace
without seed dispersal (18/19 plant species). Bonobos seem to be tree planters of the Congo forest.
39
Figure 9 Female-female genito-genital (GG) rubbing
Threatened by extinction
Bonobos are limited to areas south of the Congo River. Their survival depends on the conservation
policies and decisions of the one country were they live: the Democratic Republic of Congo. The
species’ range covers 500,000 km² of the Cuvette Centrale (Thompson, Hohmann & Furuichi
2003). Deforestation in DRC occurs at an average rate of 311,000 ha/year (FAO 2010), but human
hunting and bush meat trafficking is the main cause of bonobo extinction (Hart et al. 2008b).
Bonobo numbers are hard to estimate. They could number between 10,000 and 50,000 but it is also
possible that there are fewer than 10,000 (Thompson, Hohmann & Furuichi 2003). Bonobo
populations are decreasing and the species is in danger of extinction (IUCN 2012).
40
Conclusion
Myths… and realities
Bonobos are our closest living relatives…
No more than chimpanzees.
Bonobos do not use tools…
They do. Sophisticated tools (such as chimpanzees’) were not observed in wild populations
but bonobos do use and built tools.
Girls’ power is within bonobos…
Not really. Females’ alliance in this matriarchal society allows dominance towards males.
But bonobos are rather co-dominant.
Bonobos are peacefull…
Yes. Lethal aggression was never reported, although aggressions exist.
Bonobos are the primate sex-champion….
No. Bonobos use sex for social issues in various ways and without taboos but no more often
than chimpanzees in frequency.
Homosexuality is common in bonobos…
Yes. Especially female-female.
Bonobos can disappear…
Yes.
41
The Congo forest
42
Seed dispersal strategies and the threat of defaunation in a Congo forest
Authors
David Beaune, François Bretagnolle, Loïc Bollache, Gottfried Hohmann,
Martin Surbeck, Barbara Fruth
Published in Biodiversity and Conservation
43
Abstract
Seed dispersal mode of plants and primary interactions with animals are studied in the
evergreen Afrotropical forest of LuiKotale, at the south-western part of Salonga National Park (DR
Congo). We first analysed seed dispersal strategies for a) the plant species inventoried over a
decade at the study site and b) the tree community in 12 × 1-ha census plots. Our analyses of
dispersal syndromes for 735 identified plant species show that 85% produce fleshy fruits and rely
on animals for primary seed dispersal. Trees depending on animals for primary dispersal dominate
the tree community (95%), while wind-dispersed and autochorous trees are rare in mixed tropical
forests. A list of frugivorous vertebrate species of the ecosystem was established. Among the fruit-
eating vertebrate species identified in the ecosystem, forest elephants and bonobos are threatened
with extinction (IUCN 2012). Although most of the species listed previously are internationally and
regionally protected, ALL the species we observed dispersing seeds are hunted, fished or trapped by
humans in the area. With the exception of bush pigs, seed predators, mainly small-sized animals,
are generally not targeted by hunters. As a consequence, we expect human pressure on key animal
species to impact the plant community. We suggest defaunation to be considered as major
conservation problem. Thus, not only for the sake of animal species but also for that of plant species
conservation, anti-poaching measures should have priority in both “protected” and unprotected
areas. Defaunation could bring a new impoverished era for plants in tropical forests.
Résumé
Dans la forêt tropicale humide de LuiKotale, au sud-ouest du parc national de la Salonga (RD
Congo), nous avons analysé a) l’ensemble des stratégies de dispersion des plantes inventoriées dans
le site d’étude depuis une décennie, puis b) des plantes recensées dans l’inventaire de la
communauté d’arbres sur 12 parcelles de 1 ha. D’après l’analyse des syndromes de dispersion de
735 espèces de plantes identifiées, 85 % produisent des fruits adaptés pour la consommation par des
animaux qui dispersent leurs graines. Les arbres dont la dispersion primaire est zoochore dominent
la communauté (95%), alors que les arbres autochores et dispersés par le vent sont rare. Nous
avons identifié les espèces de vertébrés frugivores de l’écosystème, parmi lesquelles les éléphants
de forêts et les bonobos qui sont menacés d’extinction (IUCN 2012). Bien que protégés
internationalement, tous ces animaux sont chassés, pêchés ou piégés. Les prédateurs de graines,
principalement des petits animaux (rongeurs et oiseaux), ne sont pas des espèces cibles pour la
chasse à l’exception des potamochères. La pression humaine devrait affecter la communauté
végétale par l’élimination d’espèces clefs de l’écosystème. La défaunation risque d’être la cause
d’une nouvelle ère d’appauvrissement spécifique des plantes de forêt tropicale. Cette défaunation
doit être considérée comme un problème majeur de conservation. Les mesures anti-braconnage
44
doivent être une priorité dans les zones protégées et « non protégés » et ceci non pas seulement pour
la conservation des espèces animal mais aussi pour la conservation des espèces végétales.
Keywords: bush meat; seed dispersal; defaunation; Democratic Republic of the Congo; forest
ecology; frugivores; human pressure; seed predators; tropical rainforest; zoochory
45
Introduction
A critical problem in tropical forest conservation is hunting and poaching for the commercial
bush meat trade, and this is particularly true in the Congo Basin (Bowen Jones & Pendry 1999;
Wilkie & Carpenter 1999; Fa, Peres & Meeuwig 2002). The Congo Basin is of particular interest
investigating the link between defaunation and forest conservation, as it is home to the second
largest rainforest block in the world. Almost half of its forests (about 154 million ha) are located in
the Democratic Republic of Congo (DRC) (FAO 2010). A total of 60% of the DRC is covered by
forest with high biodiversity, but these areas where defaunation is particularly severe are among the
least studied in Africa (Bowen-Jones and Pendry 1999; Hart et al. 2008). With a total extraction of
4.9 tons of wild mammal meat each year (vs. 0.15 in Neotropical forests (Fa, Peres & Meeuwig
2002)), the rate of exploitation has been judged unsustainable for Afrotropical forests. Causes and
consequences of the on-going “bush meat crisis” (Peres & Palacios 2007) are similar across Africa,
and where still available, large and medium-sized animals are the most targeted species (Wright et
al. 2007; Poulsen et al. 2009). This impact on animal species and populations has an impact on
plants (Terborgh et al. 2008): Ecosystems are shaped by animal-plant interactions, and many plant
species depend on animals for seed dispersal (Forget et al. 2006; Dennis 2007; Forget et al. 2011).
To evaluate the impact of hunting on plant species, we need to 1) estimate how many plant
species are dependent on animals for seed dispersal; 2) census primary seed dispersers and seed
predators; and 3) assess their relative hunting pressure.
1) In tropical areas, zoochory is dominant and seems to outperform other dispersal modes such
as barochory (by gravity), hydrochory (by water), anemochory (by wind) or autochory (by ballistic
mechanisms) (Gautier-Hion et al. 1985; Willson 1993; Jordano 2000; Levey, Silva & Galetti 2002).
However, community-scale assessments are rare in the Afrotropics. Studies must therefore assess
the abundance and diversity of zoochorous plant species in the ecosystem.
Recent studies indicate that seed dispersal plays a prominent role in recruitment limitation, gene
flow, metapopulation dynamics, colonisation potential and plant migration in response to past and
future climate change, maintenance of biodiversity, and more (Schupp, Jordano & Gomez 2010).
As predicted by models (Muller-Landau 2007) and shown in field surveys (Forget & Jansen 2007;
Stoner et al. 2007; Wright et al. 2007; Terborgh et al. 2008; Brodie et al. 2009; Vanthomme, Bellé
& Forget 2010), defaunation leads to the empty forest syndrome (Redford 1992; Terborgh et al.
2008) with noticeable consequences for the structure and dynamics of the habitats concerned.
Currently, three not mutually exclusive conclusions are possible concerning the impact of hunting
for tropical forest plant communities: (1) Hunting reduces the amount and efficiency of seed
dispersal for plant species whose seed dispersal agents include hunted animals (Beckman & Muller-
46
Landau 2007; Wang et al. 2007); (2) Hunting alters the species composition of the seedling and
sapling layers (Stoner et al. 2007); (3) Selective hunting (i.e. pressure on large/medium-sized
instead of small animals) leads to differential predation on seeds, with more predation on small
seeds (Mendoza & Dirzo 2007). As a consequence of hunting pressure, the tropical forest with plant
species disseminated by animals might change with regard to biodiversity, species dominance,
survival, demography, and spatial and genetic structure (Wright et al. 2007). Although studies have
assessed diversity and abundance of plant species in Central African ecosystems such as the Congo
Basin (Howe & Smallwood 1982; Idani et al. 1994; Boubli et al. 2004), certain areas are
underexplored and require urgent assessment due to the continuing rapid decline in biodiversity.
2) Plants can interact with many different animals, such as seed predators and/or seed
dispersers (Gautier-Hion et al. 1985; Jordano, Bascompte & Olesen 2003). Some of these animals
are prey for hunters while others are not (or are caught opportunistically). Differential human
pressure on fauna could affect plant reproductive parameters. Seed predators (e.g. small rodents)
may be less affected by human predation than primary seed dispersers (such as primates, bats, and
birds (Wilkie & Carpenter 1999)). Therefore, a census of primary seed dispersers and seed
predators is required.
Among the seed predator guild, some species are strictly seed predators (e.g., bush pigs: (Beaune et
al. 2012b) while others are also secondary dispersers (scatter hoarders, ruminants: (Feer 1995;
Vander Wall, Kuhn & Beck 2005; Nyiramana et al. 2011; Beaune et al. 2012a).
3) The relative hunting pressure on seed predators depends on a variety of factors such as a
species’ conspicuousness, its arboreality, or body mass. The latter i.e. shows a large variation not
only between but also within species (with weights from < 1kg to > 100kg, e.g., bush pig). Within
the seed predator community, the seed size panel predated is thought to be linked to seed predator
size: the differential predation hypothesis (DPH). The removal of large/medium-sized seed
predators such as bush pigs (one of the preferred prey of hunters (Wilkie & Carpenter 1999)) could
trigger differential predation on seed species; with large-seeded plants escaping predation with
consequences on seed mortality and recruitment (Mendoza & Dirzo 2007).
Here we provide an assessment of seed dispersal strategies within a plant community in a Congo
forest. In this study (1) we determine plant strategies and estimate the number of species within a
tree community that are dependent on animals for seed dispersal and the relative importance of their
abundance/dominance relative to other strategies; (2) we inventory the community of vertebrates
interacting with seeds (primary seed dispersers and seed predators) and assess whether or not an
animal is hunted by humans; (3) we present the first data on ichthyochory in Africa.
Reports on
fruit-eating fish are limited although fruits of some trees that inhabit
riverine and seasonally
inundated forests are already known to be eaten by fish (Hulot 1950; Horn et al. 2011).
47
Methods
Figure 10 Map of the field site and location of plots (white dots), with main transects shown as black lines.
Study site
The LuiKotale research site (LK) is located within the equatorial rainforest at 2°47’ S - 20°21’ E, at
the south-western fringe of the Salonga National Park (DRC), and in the same continuous forest
block as that park. (
Figure 10). Classified as a world heritage site, Salonga Naational Park is the
largest protected rain forest area in Africa and the second largest protected rainforest in the world
(33.346 km², (Grossmann et al. 2008). The study site is a primary evergreen tropical lowland
rainforest ancestrally owned and used by Lompole village (17 km away). The site covers >60km²
with a network trail of 76km. Since 2001, subsistence hunting and harvesting within the site has
ceased for the sake of research (Hohmann & Fruth 2003). The climate is equatorial with abundant
rainfall (>2000mm/yr), a short dry season in February and a longer one between May and August.
Mean temperature at LuiKotale ranges between 21°C and 28°C, with a minimum of 17°C and a
48
maximum of 38°C (2007-2010). Five major vegetation types are distinguished in the site: (1) mixed
tropical forest on terra firme, (2) monodominant forest dominated by Monopetalanthus sp. (3)
monodominant primary forest dominated by Gilbertiodendron dewevrei (4) temporarily inundated
mixed forest (5) permanently inundated mixed forest. Well-drained habitats (1-3) dominate site
cover, with 73% of heterogeneous forest composition and 6% of homogeneous composition.
Seasonally or permanently flooded habitats (4, 5) represent 17% and 4% of the cover respectively
(Mohneke & Fruth 2008).
Plant species & dispersal mode
Between 2002 and 2010, botanical data collection took place as part of the long-term project «The
Cuvette Centrale as a Reservoir of Medicinal Plants»: Fertile plant material was collected at least in
triplicate along natural trails (31 km), standardized transects (8 km), in plots, and opportunistically.
Each plant was identified by vernacular name, described, tagged with a unique collection number,
and herborised. The dried vouchers were shipped to Kinshasa, taxonomically determined and
incorporated into the herbarium of the INERA at Kinshasa University. Duplicates of specimens
were shipped to herbaria in Belgium (Jardin National Botanique de Belgique, Meise) and Germany
(BSC, Munich) for verification and identification by specialists. By May 2010, the herbarium
consisted of 7300 vouchers (Fruth 2011). For the purpose of our study, the dispersal strategies of
each inventoried species from LK were categorized through diaspore anatomy and tissue analysis as
(1) zoochore (fleshy fruit indicating zoochory by primary dispersers), (2) hydrochore (drift fruit),
(3) anemochore (achene or samara) or (4) autochore. (dehiscent tissue). If fruit was unavailable,
dispersal strategy was inferred from literature (Gautier-Hion et al. 1985; White & Abernethy 1997;
Geerinck 2005).
Abundance and diversity of animal-dispersed trees
From February to June 2011, 12 plots of 1 ha (100×100m) were randomly positioned in mixed
tropical forest. Within these plots, all trees ≥ 10cm DBH (diameter at breast height) were measured
and identified in order to assess the relative importance of zoochorous trees in the community. Plot
difference was tested with a Shapiro-Wilk normality test. and tree densities and average DBH were
calculated by one-way analysis of variance (ANOVA) (Boubli et al. 2004).
The proportional abundance of zoochorous trees found in the plots was compared to the
theoretical proportion according to the number of zoochorous species censused on the plots, using a
Binomial test (with power analysis of the test specified if H
0
rejected). Analyses were performed
using R 2.13 (R Development Core Team 2011).
49
Vertebrate seed dispersers and predators
Mammals: From January 2010 to June 2011, a list of terrestrial frugivorous mammals was compiled
from ad libitum direct visual observation and camera traps (Two Wildeview series3 & three
Bushnell
®
Trophy Cam™: Video mode 60s/1s interval/normal sensitivity, were installed for 82 days
and nights) at the LK site. The LK site was explored on and off the trail system (>10km/day) and
species were recorded opportunistically. To identify seed predators, camera traps were randomly
positioned throughout the forest and baited with different seeds (Beaune et al. 2012b).
Birds: Frugivorous birds were directly observed from January 2010 to June 2011 and from earlier
studies (Surbeck in (Fruth & Hohmann 2005; BirdLife-International 2011).
Fishes: Fishes were captured for market by local fishermen in the Lokoro River and affluents.
Catches were brought to scientists for census. Stomach contents were analysed from March to June
2011 in order to find seeds in the bolus.
Animal species were identified and their main interaction with seeds (1-primary seed disperser; 2-
seed predator; 3-neutral) inferred from literature, video records and unpublished data observation
from the field-site (Gautier-Hion et al. 1985; Kingdon 1997; Bourson 2011; Beaune et al. 2012a;
Beaune et al. 2012b). Observed frugivores were considered to be seed dispersal vectors when intact
seeds were horizontally moved in space by endo- or ectozoochory. Seed predators were observed
destroying seeds (Beaune et al. 2012b). Through lack of evidence of secondary dispersal, only
primary dispersal was considered. Species status followed the IUCN red list of threatened species
(IUCN 2012). The local threat was assigned for each species (poached, hunted or fished) by
crosschecking questionnaires from experienced local hunters (n=28), the literature (Wilkie &
Carpenter 1999; Poulsen et al. 2009) and ad libitum observation of catches from January 2010 to
June 2011.
Results
How many plant species are zoochorous?
Within the LK area, dispersal syndromes of a total of 735 species were analysed. These included
403 tree, 130 shrub and 202 liana species belonging to 77 plant families. Of these species, 85.0%
produce fleshy fruits and are primarily dispersed by animals (zoochory).
Zoochory is the dominant seed dispersal strategy among trees (83.9%), shrubs (97.7%) and lianas
(79.2%). Figure 11. The proportion of zoochorous shrubs is significantly higher than for trees and
lianas (test of proportion, χ²=15.65 and 21.51 respectively df=1, p-values<0.001; power
50
analysis=100%). There was no significant difference in the proportion of trees and lianas dispersed
by animals (χ²=1.70 df=1, p-value=0.2).
Herbaceous species were excluded from this study because it was difficult to distinguish species
dispersed by multiple vectors (such as wind+ant, water+fish, etc.). Nevertheless, we identified 123
herbaceous species which may use animals as dispersal vectors (first or secondary).
0%
20%
40%
60%
80%
100%
Tree (403
species)
Shrub (130) Liana (202)
Figure 11 Proportions of species characterized by the different seed-dispersal strategies among tree, shrub and liana
species of LK. Grey = animal-dispersed, white = autochorous, black = wind-dispersed.
Abundance and diversity of animal-dispersed trees
All 12 plots were similar in structure (size-class distribution: no significant difference in DBH class
size: ANOVA, F = 1.3, p-value = 0.25; normal distribution of tree density: W = 0.93, p-value =
0.43). Within the 12 1-ha plots, zoochorous species accounted for a much greater proportion than
did other dispersal strategies. Zoochorous species accounted for a mean of 88.1%, ± SE 0.7, CI
95%
=
[86.6-89.6%] of all species present in the plots. Autochorous species accounted for a mean of
10.6%, ± 0.7, CI
95%
= [9.0-12.1%], while wind-dispersed species were nearly absent (0.5%, ± 0.2,
CI
95%
= [0.0-1.0 %]) (
Figure 12). If tree species dispersed by different vectors tend to be equally
abundant, then proportions of individual trees dispersed by different vectors should reflect the
proportions of species dispersed by these vectors. However, trees belonging to zoochorous species
accounted for a higher proportion of all individual trees than that expected under equal abundance
of species with different dispersal strategies (p-value < 0.001, power analysis = 100%). A
proportion of 95.1% ± 0.7 of all individual trees in the plots belonged to animal-dispersed species
(CI
95%
= [93.5-96.6%]). Anemochorous and autochorous species account for smaller proportions of
all individual trees present in the 12 1-ha plots compared to the proportion of all species that they
51
account for (p-values < 0.001, power analysis = 100%). Among the 25 most dominant species (i.e.
from the genera Dialium, Polyalthia, Chaetocarpus, Drypetes, Strombosiopsis, Strombosia,
Sorindeia, etc.) representing +78% of individual trees (4098/5234 trees), only one is autochorous:
Scorodophloeus zenkeri, 23
rd
in rank with a total of 63 individual trees.
Figure 12 Proportion of different dispersal modes for all species (dark bars), and for all individuals (light bars) present
in 12x1-ha plots. Error bars indicate SE.
Vertebrate seed dispersers and predators
Thirty eight non-aquatic vertebrates eating fruit were identified at LK. Some of these fruit-eating
species, namely bushbuck (Tragelaphus scriptus), common genet (Genetta genetta), potto
(Perodicticus potto), tree hyraxe (Dendrohyrax dorsalis), water chevrotain (Hyemoschus
aquaticus), and west African linsang (Poiana leightoni), so far did not show evidence of seed
dispersion, and thus were not classified as seed dispersers. Other identified species, namely Afep
pigeon (Columba unicincta), African green pigeon (Treron calvus), Congo peacock (Afropavo
congensis), crested guineafowl (Guttera pucherani), grey parrot (Psittacus erithacus), streaky-
throated barbet (Tricholaema flavipunctata), may both eat and disperse seeds of different plant
species. Thus, it was not possible to assign a clear category to these animals. Finally, 31 fruit-eating
species (including a non-exhaustive list of fishes) were identified as seed dispersers. All of them are
exploited for meat (
52
Table 2), including threatened species protected by law such as elephants and bonobos. Smaller
frugivorous birds and bats which are usually not hunted are probably present but were not recorded.
Five vernacular species of fish belonging to five genera (Xenocharax, Distichodus, Clarias,
Malapterurus, Schilbe) were recorded to swallow fruits and seeds. Fruits from the forest gallery are
used as bait by local people. Intact seeds of Parinari congensis, Treculia africana, Uapaca sp., etc.
have been found in either stomach, intestines, or close to the anus of several fishes (n = 23 content
analyses). The last three genera mentioned in Table 1 are catfishes (order Siluriformes) reaching
+1m. No amphibians or reptiles were observed to feed on fruits in LK but this cannot be excluded.
The seed predator guild comprises 19 identified species (
Table
3). It is mainly comprised of seed-eater specialists such as rodents and birds (family
Estrildidae with Estrilda paludicola, Nigrita bicolour, N. canicapillus, Spermophaga haematina).
Snare trapping targets specifically the largest terrestrial rodents (Kingdon 1997), such as porcupines
(Atherurus africanus, 1.5-4kg) or giant pouched rats (Cricetomys emini, 1-1.4kg). Squirrels (family
Sciuridae) and anomalures (Anomalurus derbianus) are hunted with weapons when encountered, as
are birds (francolin: Francolinus lathami). Bush pigs (Potamochoerus porcus) with their large body
mass (45-115kg) are among hunters’ preferred prey ((Wilkie & Carpenter 1999; Poulsen et al.
2009). The proportion of seed predator species hunted in their guild is with only 1/3
rd
as important
of the seed disperser species significantly less important (37% to 100%, χ²=22.4, df = 1, p-
value<0.001, power analysis=100%). Yet, unlike the bonobos and the forest elephants, none of the
seed predators are threatened by extinction (
Table
2). According to hunters, seed predator species such rodents and passerines are not targeted
preys of hunting expeditions, owing to their small size. Most seed predator species are
opportunistically shot or trapped, except for P. porcus, the largest seed predator, favouring the
hypothesis that frugivores are hunted more intensively than seed predators and by that the
differential predation hypothesis.
53
Class
Familly
Species
Name
Status
Population
trends
Threats
Mammalia
Bovidae
Cephalophus callipygus
Peter’s duiker
LC
Hunted
Cephalophus dorsalis
Bay duiker
LC
Hunted
Cephalophus monticola
Blue duiker
LC
Hunted
Cephalophus nigrifrons
Black-fronted duiker
LC
Hunted
Cephalophus silvicultor
Yellow-backed
duiker
LC
Hunted
Cercopithecidae
Allenopithecus nigroviridis
Allen’s swamp
monkey
LC
?
Hunted
Cercocebus chrysogaster
Golden-bellied
mangabey
DD
Hunted
Cercopithecus cephus
ascanius
Red-tailed monkey
LC
?
Hunted
Cercopithecus mona wolfi
Wolf’s monkey
LC
?
Hunted
Cercopithecus neglectus
De Brazza’s monkey
LC
?
Hunted
Lophocebus aterrimus
Black mangabey
NT
Hunted
Hominidae
Pan paniscus
Bonobo
E
Poached
Elephantidae
Loxodonta africana
cyclotis
Forest elephant
V
↑
Poached
Pteropodidae
Epomophorus grandis
Epauletted fruit bat
DD
?
Hunted
Hypsignathus monstrosus
Hammer-headed bat
LC
?
Hunted
Lissonycteris angolensis
Angola fruit bat
LC
Hunted
Viverridae
Civettictis civetta
African civet
LC
?
Hunted
Nandinia binotata binota
African palm civet
LC
?
Hunted
Aves
Bucerotidae
Bycanistes albotibialis
White-thighed
hornbill
LC
?
Hunted
Ceratogymna atrata
Black-casqued
hornbill
LC
?
Hunted
Tockus camurus
Red-billed dwarf
hornbill
LC
?
Hunted
Tockus fasciatus
African pied hornbill
LC
?
Hunted
Tropicranus albocristatus
White-crested
hornbill
LC
?
Hunted
Musophagidae
Musophaga rossae
Ross's turaco
LC
?
Hunted
Tauraco schuettii
Black-billed turaco
LC
?
Hunted
Corythaeola cristata
Great blue turaco
LC
?
Hunted
Actinoptery
gii
Citharinidae
Distichodus sp
"Mboto"
Fished
Xenocharax sp
"Loboli"
Fished
Clariidae
Clarias sp
"Ngolo"
Fished
Malapteruridae
Malapterurus sp
"Nina"
Fished
Schilbeidae
Schilbe sp
"Lolango"
Fished
Table 2 List of fruit-eating vertebrates categorized as seed dispersers in the study site. IUCN status of each species was
consulted in June 2011, indicating status of threat as follows: LC: Least Concern, DD: Deficient Data, V: Vulnerable,
NT: Near Threatened, E: Endangered, : stable population trends; decrease, ? = population trend unknown.
54
Class
Familly
Species
Name
Status
Population
Trends
Threats
Mammalia
Anomaluridae
Anomalurus derbianus
Lord Derby’s
Anomalure
LC
?
Hunted
Hystricidae
Atherurus africanus
Brush tailed
porcupine
LC
?
Hunted
Muridae
Hylomyscus sp
African wood mouse
LC
?
Malacomys sp
Long footed rat
LC
?
Mus sp
Common mouse
LC
?
Praomys sp
Soft-furred rat
LC
?
Stochomys longicaudatus
Target rat
LC
?
Nesomydae
Cricetomys emini
Giant pouched rat
LC
Hunted
Sciuridae
Funisciurus congicus
Congo rope squirrel
LC
Hunted
Protoxerus aubinnii
African giant
squirrel
DD
?
Hunted
Suidae
Potamochoerus porcus
Bushpig
LC
Hunted
Estrildidae
Estrilda paludicola
Fawn-breasted
waxbill
LC
?
Nigrita bicolour
Chestnut-breasted
nigrita
LC
?
Nigrita canicapillus
Grey-headed nigrita
LC
?
Spermophaga haematina
Western bluebill
LC
?
Phasianidae
Francolinus lathami
Forest francolin
LC
?
Hunted
Ploceidae
Malimbus nitens
Blue-billed malimbe
LC
?
Malimbus cassini
Cassin's malimbe
LC
?
Malimbus rubricollis
Red-headed malimbe
LC
?
Table 3 List of seed predators in the study site. IUCN status of each species was consulted in June 2011, indicating
status of threat as follows: LC: Least Concern, DD: Deficient Data, : stable population trends; decrease, ? =
population trend unknown.
Discussion
Seeds of most plant species in tropical forests are dispersed by animals, rather than by wind, water
or ballistic mechanisms (Jordano, Bascompte & Olesen 2003; Forget et al. 2006; Dennis 2007;
Forget et al. 2011). In the LK forest systems of the Congo Basin, zoochorous species currently
dominate plant communities (85% of the referenced plant species in LK areas). More specifically,
in the mixed tropical forest we sampled, the abundance of anemochorous and autochorous tree
species (4.9%) is lower than expected from the respective proportions of anemochorous and
autochorous species in the tree community (11.1%).
Zoochorous tree species are among the dominant trees in this Afrotropical forest, indicating the
dominance of this dispersal strategy. However, adaptations for zoochory leads to dependence on
55
animals, so zoochorous plants may become trapped in a coevolutionary dead-end if their partners
become extinct (Jordano, Bascompte & Olesen 2003; Muller-Landau 2007; Muller-Landau et al.
2008). This is particularly important in tropical forests, where numerous animals, predominantly
large vertebrates, are unsustainably overhunted (Wright et al. 2007). The importance of the largest
seed dispersers in our study site, bonobos and elephants, has already been noted (Yumoto et al.
1995; Blake et al. 2009), and elephants have been described as the ‘megagardeners’ of the forest
(Campos-Arceiz & Blake 2011). Some of the seed dispersers such as bonobos are endemic, rare,
and threatened (Fruth et al. 2008) and others such as Allen’s swamp monkeys, are insufficiently
known (Oates and Groves 2008). Fruiting plants can have several consumers and seed dispersers
with functional redundancy. However this does not help when all dispersal vectors are hunted. In
the studied ecosystem all primary seed dispersers are hunted, trapped or fished; while seed
predators are less impacted. Ecosystem resilience might be compromised.
Human pressure on animals providing seed dispersal services and large seed predators such as bush
pigs should increase in the future with human demography and population increase (Brashares,
Arcese & Sam 2001; Poulsen et al. 2009). In central Africa, consumption rates are estimated at 0.16
kg of bushmeat per person per year (Delvingt 1997) and extraction of bushmeat is estimated at 213–
248 kg/km²/yr (Wilkie & Carpenter 1999). Bushmeat demand is increasing steadily as the
population increases and cities expand (Poulsen et al. 2009). Many parks have failed to prevent
poaching, including the adjacent Salonga National Park, where organized poaching is rife (Hart et
al. 2008). Beyond the survival of animals, the entire ecosystem dominated by plants dependent on
animal-mediated seed dispersal is also at risk.
This study also highlights the risk of the differential predation hypothesis (Mendoza &
Dirzo 2007). While bush pigs are the biggest seed predators of the system, with dramatic effects on
the mortality of large and hard protected seeds (Beaune et al. 2012b), they suffer greater hunting
pressure than small seed predators eating small-seeded species. Large-seeded species such as
(Irvingia gabonensis, Mammea africana, etc.) could benefit from reduced seed predation, This
differential could modify plant reproduction and dominance in the forest. Similarly, the
disappearance or decline of populations of large frugivores such as elephants and bonobos, which
disperse large seeds, seems to alter recruitment of large-seeded plant species (Wang et al. 2007;
Vanthomme, Bellé & Forget 2010). Of plant species with putative “megafaunal syndromes”, many
are ecologically disrupted by the loss of megafauna, but some show resilience (Janzen & Martin
1982; Guimarães, Galetti & Jordano 2008; Johnson 2009).
If animal density decreases, animal-dependent plants could be replaced by autochorous and
anemochorous species. Although this will be a slow and not immediately detectable process,
ultimately a possible scenario in this forest is a radical change in the composition of the dominant
56
species. With this inventory of seed disperser species and pressures on them, we can estimate the
proportion of plants potentially affected by their loss as follows: 85% of all plant species, and 88%
of tree species (but 95% of individual trees). Thus, hunting is likely to trigger changes in forest
structure and composition, as well as in population demography and genetics.
Tree density might stabilise, with autochorous and anemochorous trees occupying vacant
space (Chapman & Onderdonk 1998) but biodiversity would decrease as a result (Muller-Landau
2007). More studies determining whether zoochorous plants can reproduce in the absence of
animals are urgently required, as are conservation and management plans for these forests.
Conservationists have focused on the direct consequences of habitat loss, animal species decline as
well as consequences of habitat loss on animal species decline. However, a growing body of
literature shows the increasing need to focus in addition on the reverse argument, the consequences
of animal species’ loss on habitat. In this respect, defaunation has to be considered as major
conservation problem (Redford 1992; Terborgh et al. 2008). Its consideration is urgent in
unprotected areas but even more in “protected” areas, where timber exploitation is banned but
poaching still continues due to a lack of law enforcement (Hart et al. 2008).
57
Part I
58
Seed dispersal by bonobos
59
Seed dispersal services performed by bonobos (Pan paniscus) in tropical forest
in the Democratic Republic of Congo
Authors
David Beaune, François Bretagnolle, Loïc Bollache, Chloé Bourson,
Gottfried Hohmann & Barbara Fruth
60
Abstract
Conservation of Afrotropical forests depends not only on habitat protection but also on the
protection of animal species such as frugivorous primates, recognized as the most important seed
dispersers for many plants. Here we investigate seed dispersal by bonobos (Pan paniscus) in
evergreen lowland tropical rainforest of the Congo Basin. Bonobos are mainly frugivores (66% of
all feeding sessions), spending about 3.5 hrs/day swallowing seeds that are transported for an
average of 24hours. During the behavioral study (22 months), bonobos dispersed seeds of more
than 91 plant species by endozoochory in the gut, carrying them to an average distance of 1.2 km
from the parent tree. Seeds passed by bonobos germinated more rapidly, at higher rates and had
greater post-dispersal survival than unpassed seeds. Bonobo-dispersed plants account for 40 % of
tree species and 65 % of individual trees in the study site. Almost all bonobo-dispersed species
investigated (95% of 19 species) are unable to self-recruit without dispersion.
Since bonobos show little functional overlap with other frugivores, loss of their seed dispersal
services is likely to affect forest structure and dynamics. Our results justify description of the
bonobo as the gardener of the Congo forest.
Keywords Africa, Congo basin, forest ecology, long dispersal distance, seed dispersal, seed rain,
seed shadow, zoochory
Résumé
La conservation des forêts d'Afrique tropicale dépend non seulement de la protection des habitats,
mais également de la protection des espèces qui la composent telles que les primates frugivores,
identifiés parmi les disperseurs de graines les plus importants pour de nombreuses plantes. L’étude
de la dispersion de graines par des bonobos (Pan paniscus) dans une forêt tropicale humide du
bassin du Congo est ici présentée. Les bonobos sont principalement frugivores (66% de toutes les
sessions d'alimentation). Ils passent environ 3.5 h/jour à avaler des graines qui sont transportées
24hrs en moyenne. Pendant l'étude comportementale (22 mois), les graines de plus de 91 espèces de
plantes ont été identifiées comme étant dispersées par endozoochorie dans l’estomac à une distance
moyenne de 1,2 km de l'arbre-parent. Les graines passées germent plus rapidement, à des taux plus
élevés et avec une plus grande survie post-dispersion que les graines non passées par le tube digestif
d’un bonobo. L'influence du bonobo dans le réseau écologique devrait affecter 40 % des espèces
d’arbres et 65 % des arbres individuels. Presque toutes les plantes dispersées par les bonobos dont
61
le recrutement a été étudié (95% des 19 espèces) ne peuvent pas autorecruter suffisamment de
jeunes individus sans dispersion des graines. Puisque les chevauchements fonctionnels avec d'autres
frugivores sont faibles, le bonobo en tant que vecteur de dispersion de graines est susceptible
d'affecter la structure et la dynamique des forêts. Nos conclusions classifient le bonobo comme
probable jardinier de la forêt du Congo.
Mots clefs Congo, écologie de forêt, longue distance de dispersion, dispersion de graines, pluie
de graines, zoochorie
62
Introduction
I
In tropical forests of Africa, Asia, South America, and Australia, between 70.0% and 93.5% of
all tree species owe their existence to vertebrate seed dispersal. Fishes, birds, bats and terrestrial
mammals are cited as endozoochorous vertebrates responsible for primary seed dispersal, the
predominant mode of dispersal in these ecosystems (Janson 1983; Gautier-Hion et al. 1985;
Jordano 2000). Many tropical plants have evolved fruits that are attractive to only a limited subset
of frugivores, with colors, antifeedants, and seed dimensions being adapted to a specific group of
dispersers (Fleming 1979). In Africa, Asia, and South America, frugivorous primates are
recognized as the most important primary seed dispersers for many fruit-bearing species (Chapman
& Onderdonk 1998a; Lambert & Garber 1998; Sato 2011).
Increased rates of successful germination of seeds following passage through the gut have
been documented in all great apes, namely chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla
gorilla), bonobos (Pan paniscus), and orang-utans (Pongo pygmaeus) (Idani 1986; Wrangham,
Chapman & Chapman 1994; Poulsen, Clark & Smith 2001a; Gross-Camp & Kaplin 2011; Nielsen
et al. 2011). The role of seed dispersal by large primates in forest dynamics and structure has been
highlighted in few studies and the impact of their loss by over-hunting on vegetation patterns and
plant diversity has become an increasingly urgent question (Nuñez-Iturri & Howe 2007; Peres &
Palacios 2007; Wright et al. 2007; Nunez-Iturri, Olsson & Howe 2008; Brodie et al. 2009). Indeed,
there is a general agreement that along with the physical destruction of habitats, the impoverishment
of seed disperser communities has a considerable influence on an important ecosystem service,
primary seed dispersal, and thus constitutes a major threat for the regeneration of the ecosystem
(García & Martínez 2012). In the tropics, many forests are successfully protected from logging, but
are insufficiently protected from hunting. For example, Wang and colleagues (2007) were able to
show that the extinction of large primates in Cameroonian forests has altered seed deposition
patterns of the tree species Antrocaryon klaineanum, with the majority of seeds falling beneath the
parent trees (Wang et al. 2007). In a comparative study of forest regeneration between forests
protected and unprotected from primate hunting, Nuñez-Iturri et al. (2008) found significant
differences in the composition of tree seedling and sapling assemblages. Great apes, the largest
primates, are known to ingest a considerable diversity of fruit, including some with large seeds, and
are widely involved in their dissemination processes (Lambert & Garber 1998). Thus, their
disappearance may disproportionately affect large-seeded tree species (Vanthomme, Bellé & Forget
2010; Gross-Camp & Kaplin 2011).
Despite studies on the diversity of plants dispersed by great apes or the effect of gut
passage on seed germination (Idani 1986; Wrangham, Chapman & Chapman 1994; Voysey et al.
63
1999a), our understanding of how great apes contribute to seed dispersal or forest regeneration is
limited.
For example, seed deposition patterns, considered to be among the crucial components
affecting Seed Dispersal Effectiveness (SDE) (Schupp, Jordano & Gomez 2010), have rarely been
investigated in the field.
The dispersal kernel (
the function that describes the probability of dispersal to different
distances
from the source (Nathan & Muller-Landau 2000a)), is frequently used as a quantitative
descriptor of seed dispersal in plants and is another important factor in plant dissemination;
combining information on movements (distances, positions) and gut passage time, that can be
measured as either transit time (TT) or mean retention time (MRT) of seeds (Poulsen, Clark &
Smith 2001a; Holbrook, Smith & Hardesty 2002; Tsuji, Yangozene & Sakamaki 2010). So far, gut
passage time of seeds in primates has been investigated primarily in captivity (for a synopsis see
(Lambert 1998)). Ranges in gut passage time within and between species are considerable and
depend on various factors at both the individual and environmental levels (Lambert 1998).
Individual factors include age, sex, health, reproductive status, hormonal fluctuations, stress, time
since last feeding bout, hunger/satiation, and activity level. Environmental factors include
temperature, time of day, content of macro-, micronutrients and fiber, and degree of ripeness.
Despite the magnitude of influencing factors, local ecological conditions are considered to be
crucial in determining dispersal distances (Russo, Portnoy & Augspurger 2006). Additionally in
great apes, the general use of large home ranges, extended daily movements, and return to food
patches for re-use are expected to strongly influence seed deposition patterns and the probability of
dispersal to different distances from short to long (Cain, Milligan & Strand 2000; Bohrer, Nathan &
Volis 2005). Long Distance Dispersal (LDD), for example, has been shown to influence survival
and genetic patterns of plant species, with ultimate effect on forest structure (Bohrer, Nathan &
Volis 2005).
In the Congo basin south of the Congo River, the biggest primate and the only
representative of the great ape family is the bonobo (Pan paniscus (Schwarz 1929). Population
estimation of this threatened species fluctuates between 29,500 and 50,000 animals (Fruth et al.
2008. In: IUCN 2012). In the Democratic Republic of Congo (RDC), to which bonobos are
endemic, forest fragmentation and the bushmeat traffic seriously undermine their survival. Despite
international protection in law, and occasional local taboos, they are still killed in their natural
habitats, including protected areas such as the Salonga National Park (Hart et al. 2008a). Pan
paniscus has been studied in the wild since 1979. Previous studies have shown that, with over 83%
fruit in their diet, bonobos are important fruit consumers (Kano & Mulavwa 1984), but little is
known about their role in seed dispersal. The plants ingested and their potential benefits for the
64
bonobo are comparatively well studied, but the costs or benefits for the ingested plants remain
largely unknown (Badrian & Malenky 1984; Kano & Mulavwa 1984). Idani (1986) carried out
pioneering work investigating seed dispersal by wild bonobos (Idani 1986), conducting germination
experiments on bonobo-passed seeds of 17 fruit-bearing species over 2.5 months. This subject was
taken up again only recently by Tsuji et al. (Tsuji, Yangozene & Sakamaki 2010) during
preliminary investigations over a two-month period. The lack of knowledge concerning the role of
Pan paniscus in seed dispersal can be explained by the fact that bonobos have predominantly
generated interest in anthropology, behavioral ecology and sociobiology (Wrangham 1993; Parish
1996; Hohmann et al. 1999; Hohmann & Fruth 2000; Hohmann & Fruth 2003a; Fruth & Hohmann
2006; Surbeck, Mundry & Hohmann 2011), and not in basic tropical ecology with the objective of
understanding animals’ functions in ecosystems. Our investigations thus have the potential to make
an important contribution to a better understanding of the ecological role of this great ape within its
natural habitat. The results could be applicable to all other large frugivorous primates. Our
investigations have three major goals:
First, we quantify the primary parameters for seed dispersal effectiveness of the bonobos:
(1) Are the seeds transported by bonobos and do they remain viable? (2) What is the transit time for
seed transport? (3) What is the dispersal curve/kernel and LDD? (4) Is seed germination affected by
passage through the bonobo gut? (5) How does gut passage affect post-dispersal survival? Second,
we assess the ecological importance of bonobos in the ecosystem by investigating the plant
community’s diversity, abundance and ability to recruit without seed dispersal. How many tree
species could be affected by the loss of bonobo seed dispersal services? Third, we compare seed
rain resulting from dispersal by bonobos with that produced by other seed dispersers by reviewing
the literature. Our hypothesis is that large frugivores such as bonobos disperse to considerable
distances seeds of species that are adapted to transport through the gut of this ape and are dispersed
by few other animals.
Materials and methods
Ethics Statement
The studied apes are free ranging bonobos observed without invasive methods, constraint, contact
or any interaction with the researchers. Animal welfare had greater priority than scientific interests.
The methods used to collect data in the field are in compliance with the requirements and guidelines
of the Institut Congolais pour la Conservation de la Nature, and adhere to the legal requirements of
the host country, the Democratic Republic of Congo.
65
Study site
Field work took place between September 2009 and June 2011 at the Max-Planck-Institute research
site LuiKotale (LK) (S2°47’- E20°21’) that is located within a continuous block of equatorial
rainforest at the south-western fringe of Salonga National Park (DR Congo,
Figure 1). The study
site consists of > 60km² of primary evergreen lowland tropical forest with a trail network of about
76km (Figure 2). The climate is equatorial with abundant rainfall (> 2000mm/year) interrupted by a
short, relatively dry season in February and a longer one between May and August. Mean
temperature at LuiKotale ranges between 21°C and 28°C with a minimum of 17°C and a maximum
of 38°C (2007-2010). Two major habitat types are distinguished: 1-Dry (Terra firma); and 2-Wet
forest (temporarily and permanently inundated). The dry habitat dominates the area with 73% of
mixed and 6% of single-dominant (Monopetalanthus sp. or Gilbertodendron sp.) primary forest.
The wet habitat includes temporarily inundated mixed forest, which covers 17% of the area,
permanently inundated mixed forest which covers 4% (Mohneke & Fruth 2008).
Studies investigating bonobo behavior have been ongoing since 2002 with one bonobo community
of 25-35 individuals habituated by researchers since 2007 (Hohmann & Fruth 2003c). Bonobos are
identifiable by individual physical traits (genital, face, pilosity, color).
Bonobo feeding behavior
From September 2009 to June 2011 behavioral data was recorded for bonobos over 22 months,
corresponding to 1879 hrs of observations over 315 days. Bonobos have a fission-fusion society in
which, depending on season and time of day, the community splits up into smaller foraging
subgroups called parties. As parties are largely cohesive (most animals conducting the same
activities at the same time), we considered group activity to be that of the majority (> 50% of the
bonobos) of the visible animals during a continuous record of feeding activities (i.e. continuous
focal sub-group (Altmann 1974)). The continuous record stopped when the group went out of view
or contact was lost. In order to record the part of feeding sessions (starting with the first hand-to-
mouth movement, stopping with another behavior) in daily activities and among feeding sessions
we analyzed interactions with consumed plants (i.e. granivory, herbivory, frugivory with positive or
neutral seed dispersal effect). We recorded the duration of the feeding session, the item consumed
and how seeds were processed when they were not consumed (e.g. spitting, handling, and
swallowing). Food items were classified into five categories: fruits (including either the whole fruit
ingested or the pulp without its seeds), leaves/stem/bark/gum, seeds, animals and other items
(honey, mushrooms, soil).
66
Transit time & dispersal distance
Whenever possible, bonobos were followed daily from nest to nest (approx. 05:30 to 17:30). Daily
travel routes of parties were tracked with a GPS (Garmin
®
60CSX) using 1 point position /5
minutes for georeferencing. Both bonobo transit time and dispersal distance were calculated from
direct observation. Whenever an individual bonobo swallowed a new fruit species not eaten in the
previous 36 hours, its seed was considered as a markerseeds and the individual was monitored
continuously (not at night) until the seeds of the newly ingested species were found in its feces. The
time between ingestion of the markerseeds and appearance of its first seed in the dung was taken as
gut transit time (TT). Influences of the sex and seed size on transit time were tested with students t-
test and analyses of variance (ANOVA) with all the effects considered as fixed and
homoscedasticity tested (Breusch–Pagan test). Seed size was arbitrary categorized as follows:
small: < 2mm; medium-sized: 2-10mm; large: > 10mm).
The straight-line dispersal distance was calculated with GPS positions from the parent tree
to the georeferenced seed deposition. When several bonobos of the group had ingested new
markerseeds, only one random individual was included in the dispersal model to avoid bias in the
dispersal distance, while all were included in the calculation of transit time.
Plants ingested
Plants ingested by bonobos were identified by vernacular name and determined post hoc with data
from the herbarium collection of the long term project «The Cuvette Centrale as Reservoir of
Medicinal Plants», consisting of 7,300 vouchers by May 2010 (Fruth 2011). The dried vouchers
were shipped to Kinshasa, taxonomically determined and incorporated into the herbarium of the
INERA at Kinshasa University (herbarium code: IUK). Copies of specimens were shipped to
herbaria in Belgium (National Botanic Garden of Belgium : code BR, Meise) and Germany
(Botanische Staatssammlung München : code M, Munich) for verification and identification by
specialists. If unknown, samples were recorded as NID (non identified), and collected for later
species identification. All feeding plants (trees, lianas and bushes) were marked. Plant species were
considered as dispersed by endozoochory when seeds were observed to be swallowed and defecated
intact. Such cases were classified as frugivory with seed dispersal mutualism and constituted our list
of bonobo-dispersed species. When seeds were not ingested but spat in place without primary
horizontal dispersal we classified this as frugivory with seed dispersal neutralism (effective
dispersal = horizontal displacement). Bonobo-dispersed plant species of the LK community were
compared to those of communities from Wamba (Kano & Mulavwa 1984) and Lomako (Badrian &
Malenky 1984), the two longest field sites for bonobo research, to assess cross-site similarities.
67
Representation of bonobo-dispersed trees
To assess the impact of bonobo seed dispersal on the forest tree community, we calculated both
relative biodiversity and abundance of bonobo-dispersed species within 12 plots of mixed terra
firme forest. Plots were positioned randomly within the home range of the bonobo community.
From February to June 2011 all trees > 10cm DBH (diameter at breast height) were censused in
these 12 plots of 1 ha (100×100m) each. Relative biodiversity was calculated as the number of
species within the plot observed at least once to be effectively dispersed by bonobos, divided by the
total number of species found in the plot. Relative abundance was calculated as the total number of
individual trees of all species dispersed by bonobos, divided by the total number of trees in the plot.
Seed dispersal/viability/germination/survivorship
Bonobo feces were collected at the study site between April 2002 and June 2011 (N = 1152). Feces
and seeds therein were weighed (fresh mass); the number of seeds per feces was counted for each
species.
To test germination viability of seeds that passed the bonobos’ digestive tracts, we
extracted seeds from feces collected between January 2010 and June 2011. These seeds were
packed in leaves of Haumania spp. and depositited in a nursery within the same day. The nursery
was an elevated platform (height 170cm) in situ under natural canopy cover. It was 200 cm long ×
100 cm wide, was filled with natural soil (6cm deep), and was secured with predator-proof table
legs. Each seed was marked and observed daily. We recorded emergence of the radicle
(germination) (Heß 1999) and viability ratio (proportion of seeds that germinated).
To assess the influence of gut transit on germination, we compared the germination rate of
seeds from the same parent and with three different treatment mimicking three dispersal modes, (1)
by barochory (Fruit lot = seed + diaspore); (2) by seed spitting zoochory (spitting lot = diaspore
removal); and (3) by swallowing endozoochory (swallowing lot = seeds collected after gut passage).
Whenever bonobos were observed ingesting new fruit species (see above), mature fruits were
directly collected from the respective parent tree (fruit lot and spitting lot). Ingested seeds
(swallowing lot) were collected the next day in the feces from identified bonobos. Seeds were
marked, alternately positioned in line in the nursey platform (mixing local effects) the evening of
collection (D
0
), and monitored daily.
To assess actual viability and recruitment of seeds embedded in bonobos’ feces in situ, 45
feces defecated between January 2010 and May 2011 (and not collected for the above experiments)
were monitored from one to 18 months. Seed species composition was determined by visual
inspection of the dung. Seedling recruits were counted once a week.
68
Seed rain
The daily seed rain dispersed by bonobos was calculated according to (Poulsen, Clark & Smith
2001a):
Seed rain (Seed nb/day/km²) = avg Seed nb/dung pile × avg dung pile/day/ind × avg bonobo density/km²
Population density was taken from (Mohneke & Fruth 2008) where it was calculated to be 0.73
bonobos/km². Dung production was calculated on the basis of continuous follows of individual
bonobos during which each defecation was recorded. Influences of sex and age (adult, sub-adult)
were tested with analyses of variance (ANOVA), with factors considered as fixed effects.
Recruitment under parental trees
To assess seed recruitment under the parental crown, mature trees of 22 species previously observed
to fruit (thus excluding males of dioecious species), were investigated between May 2010 and June
2011 following the methodology of (Chapman & Chapman 1995). All seedlings (< 50cm high),
saplings (50cm-200cm high), and poles (> 200cm high- < 10cm DBH (Diameter at Breast Height))
were censused in the corresponding fruit-fall zone of trees > 10cm DBH, opportunistically selected
in the LK forest. Average numbers of seedlings, saplings and poles were calculated from a
minimum of five adult trees/species. We considered a population to be able to self-replace when the
average pole production/tree was ≥ 1. For confirmation that a species was able to recruit outside its
fruit fall zone, density of its recruits was calculated in the total area censused for all species with
exclusion of the conspecific fruit-fall zones.
Functional overlap – the primate community
In addition to bonobo, 41 other species of frugivorous vertebrates occur in LuiKotale, including
birds, fruit bats, civets, monkeys and others. We assessed seed handling and overlap in food-plant
species among seven species of the diurnal primate community of LK from February to June 2011.
Observations were simultaneously performed by two teams (one observing bonobos, the other
monkeys). In contrast to bonobos, monkeys were not habituated (Bourson 2011). Feeding and seed
handling were assessed by the above-mentioned protocol. The functional overlap was calculated
using the Jaccard similarity coefficient (Real & Vargas 1996)
Results
69
Bonobo food qualified and quantified
A total of 133 plant species were recorded in the bonobo diet during the 22-month study period
(Table 1). Feeding behavior represented 992 hrs of continuous records (from 1879 hrs of
observation). The bonobo group spent 52.8% ± SE. 1.1% of its daily activity engaged in feeding
sessions. During these feeding sessions, we recorded fruits of 91 species to be ingested with their
seeds being swallowed. These species belonged to 45 genera of 25 plant families. Seeds of 56 of
these species were found intact in feces, confirming endozoochory.
Among all feeding sessions observed (315 days, average continuous records ≈ 05h 57 min
± 0h 10 min), 54.5% ± 4.4% included the ingestion of fruit with subsequent seed dispersal (i.e.,
frugivory with seed ingestion and deposition observed,
Figure 13), 0.6% ± 0.2% included the
ingestion of fruit but deposition of seeds was not confirmed (insufficient data) and 7.3% ±3.0%
consisted of the ingestion of fruit but with large seeds that were not swallowed (e.g. Mammea
africana with average seed size = 324 ± SE. 12 mm, Anonidium mannii = 42 ± 2 mm, Irvingia
gabonensis 55 ± 2 mm) (for each of these species, N ≥ 10). We exceptionally observed transport of
these large seeds over distances of about 100 meters by hand or mouth (max = 426 m). Ingestion of
food other than fruit such as leaves, terrestrial herbaceous vegetation, flowers, stems, and bark
consisted of 30.0% ± 3.3% of the feeding sessions. The remainder could be attributed to granivory
(3.4% ± 2.4%), carnivory (squirrels, monkeys: Procolobus tholloni, bird chicks, duiker:
Cephalophus spp.) (0.9% ±0.2%) and other foods (honey, termite soil, digging session for truffles
and probably insect larvae, etc. (3.3% ± 0.9%).
70
0%
10%
20%
30%
40%
50%
60%
70%
Frugivory
with seed
dispersal
service
Frugivory
with
probable
seed
dispersal
service
Frugivory
with seed
dispersal
neutralism
Herbivory Granivory Carnivory Other
Feeding sessions
Figure 13 Relative parts of the interactions among the feeding sessions (22 months; 1879 hrs continuous group scans);
Error bars indicate SE. Others are honey, mushrooms, soil and unknow.
Seed dispersal by bonobos
Of the 1152 bonobo feces collected between April 2002 and June 2011, 97.8% ± 0.3 contained
seeds. Feces weighed on average 93.5 g ± 3.0. Seeds represented 67% ± 2.4 of the feces weight (N
= 146). A dung-pile contained on average 1.9 ± 0.1 species of seeds (range = 0-6) with 79.8 ± 7.9
seeds (size > 2 mm. i.e. Ficus spp. and Musanga cecropioides excluded).
Transit time We recorded 124 markerseeds from ingestion to first deposition. Markerseeds were
identified from twelve different genera. These markerseeds were swallowed and defecated by 19
different bonobos, seven males and 12 females. The resulting transit time was 24hrs00min on
average ± SE. 9 min; (range: 20 hrs 03 min-28 hrs 17 min). Neither sex nor seed size affected
transit time (t = 0.0253, df = 15.285, p = 0.9801; F = 0.382, df = 119, p = 0.683).
71
Figure 14 Dispersal distance kernel with fat-tailed dispersal kernel infered by bonobos (N = 75 dispersal events
recorded)
Dispersal distance To assess the dispersal distance of seeds, we used georeferenced records of 75
events from 12 different plant species, when observation was continuous from first ingestion to first
defecation. The average distance of dispersal from the parent tree was 1183 m ± SE. 88 m (CI
95%
[1007 m-1358 m]; range: 0 m-2995 m (
Figure
14). The resulting dispersal distance kernel is a probability density function, characterized by
a unimodal leptokurtic distribution, with a fat-tailed dispersal kernel (right skewness = 0.63;
Kurtosis = 2.61; see (Nathan & Muller-Landau 2000a) for the different shapes of dispersal kernels).
Bonobos disperse seeds over long distances, with 93.3% of the dispersal events longer than 100 m.
Seed viability/survivorship
72
Ex-situ (in the nursery): Of the 56 species whose seeds were observed to be swallowed and
defecated intact, seeds of 35 species were submitted to a viability census (it was not possible to
bring samples of the other 21 species due to field conditions). Of these, 97% were viable, that is, we
were able to observe emergence of the radicle (N.B. for the ungerminated species only five seeds of
Momordica foetida were monitored).
Table 5 shows the 24 genera from 18 families, as well as four
tested species that remained unidentified, that were scored as viable.
To assess the effect of fruit manipulation on germination, germination rate of unpassed
seeds, as simulation to a situation of spitted seeds (spitting lot) was compared to that of seeds from
unmanipulated fruit (fruit lot). Overall germination rate was higher for manipulated than for
unmanipulated seeds, although differences were significant for only four out of seven species with
sufficient sample size (p < 0.001; power analyses = 100% (Figure 15).
To assess the role of gut passage on germination, germination rate of unpassed but
manipulated seeds, as simulation to a situation of spitted seeds (spitting lot) was compared to that of
passed seeds (swallowing lot). Overall germination rate was higher for passed than for unpassed
seeds. Here as well, differences were significant for only four out of eight species with sufficient
sample size (p < 0.05; power analyses ≥ 99% (
Figure 16).
In situ: To assess the viability of seeds in situ, a total of 45 bonobo feces (defecated from
January 2010 to May 2011 and not collected for the above experiments) was localized, marked and
monitored. Each dung pile was monitored for one to 18 months. Of all these dung piles, 67% ± 8
produced seedlings CI
95%
=[53-81%]. Overall, we identified seedlings of 8 genera. We think it
highly likely that feces continued to yield seedlings after monitoring ceased (the shorter monitoring
of a dung lasting one month). In an unpublished experiment the T
50
(= time when 50% of the
seedlings germinated) of Zeyherella longepedicellata seeds passed in bonobo was equal to 50 days;
for Diospyros sp., T
50
= 7 d; for Guarea laurentii, 20 d; for Garcinia sp., 63 d; and for Manilkara
yangambiensis, 44 d.
73
0%
20%
40%
60%
80%
100%
Cissus
Diospyros
Grewia
Guarea
Manilkara
Uapaca
Zeyherella
Germination rate
***
***
***
**
41
25
110
125
135
116
44
42
50
70
43
47
45
45
Figure 15 Germination rate of seven species (Cissus dinklagei, Diospyros sp., Grewia sp., Guarea laurentii, Manilkara
yangambiensis, Uapaca sp., Zeyherella longepedicellata) with (white) and without diaspore (grey bars). ***: p < 0.001;
**: p < 0.01 after t-test; Error bars indicate SE. Numbers on the x axis are N.
0%
20%
40%
60%
80%
100%
Cissus
Cola
Dacryodes
Dialium
Garcinia
Grewia
Guarea
Manilkara
Germination rate
***
***
***
*
25
45
24
23
58
100
133
110
74
532
406
135
20
44
162
101
Figure 16 Germination rate of eight species (Cissus dinklagei, Cola gigantea, Dacryodes yangambiensis, Dialium
corbisieri, Garcinia ovalifolia, Grewia sp., Guarea laurentii, Manilkara yangambiensis) comparing passed (dark) and
unpassed seeds without diaspore (grey bars). ***: p < 0.001, *: p < 0.05 after t-test. Error bars indicate SE. Numbers on
the x axis are N.
74
Diversity & abundance of trees dispersed by bonobos
Focusing on trees only, we found 5,233 adults in the 12 1-ha plots. A total of 40.1% ± 0.8 of these
tree species are dispersed by bonobos via endozoochory through the gut (
Figure 17). These account
for a total of 64.7% ± 1.3 of all tree individuals recorded in these plots. Abundance of
endozoochorous species is not equally distributed. A few species only account for the majority of
individuals, such as Greenwayodendron suaveolens and Dialium spp., which together account for
32% of individual trees.
0%
25%
50%
75%
100%
endozoochory ectozoochory granivory
% tree per ha
Figure 17 Tree species richness (dark) and abundance (grey) of seeds handled, consumed and dispersed by bonobos.
The Y-axis depicts the average proportion of tree species (diversity) or tree individuals (abundance) per hectare (N = 12
1-ha plots). Error bars indicate SE.
Seed rain
To assess defecation interval, we observed 16 individuals, five males and 11 females. A total
of 74 defecations were recorded (01/05/10 to 31/05/11), resulting in an average of 7.55 dung piles
between dawn and dusk of a day. Thus, the interval of defecation for each individual was on
average 1h35 ± 3 min. We detected no effect of sex (t = 0.2438, df = 12.511, p = 0.8113) or of age
(adult, sub-adult) (t = -0.3324, df = 4.369, p = 0.7549) on the interval between two defecations.
Taking into account bonobo population density, the average seed rain infered by bonobos in the
75
LuiKotale area is estimated to be 441.1 seeds/day/km². Extrapolating based on their average
lifespan in the wild (50-55 yrs), an individual bonobo disperses 9.1 tons of seeds or 11.6 million
seeds (not including seeds < 2mm length such as those of Ficus spp. and Musanga cecropioides).
Recruitment under parental trees
Table 4 shows 19 plant species, including three liana and 16 tree species used for the assessment of
self-recruitment under the parent tree. Further, a total of three species considered to be autochorous
were included in the assesment (control species), the other 19 are zoochorous. The autochorous
species, used as controls, recruited on average more than one pole under the parents, thus fulfilling
the criterion for self-replacement. In contrast, the fleshy-fruited species dispersed by bonobo did
not recruit enough poles for self-replacement under the parents, except for Drypetes sp. (
Table 4,
Figure 18). While seedlings, saplings and poles were found under other tree species (5.13 ha
censused), the majority of endozoochorous species was not able to self-replace without seed
dispersal beyond the fruit-fall zone.
76
Dispersal
mode
Tree species
N
mean
DBH
(cm)
mean recruitment
seedling
sapling
pole
autochory
Hymenostegia mundungu
10
73.7
4.4
4.1
2.5
Scorodophloeus zenkeri
10
48.4
16.3
2
3.4
Strombosiopsis zenkeri
11
35.6
2
2.1
1.2
zoochory with Pan paniscus
Anonidium mannii
10
46.7
0.5
0.6
0.4
Blighia welwitschii
5
62.8
0
0.2
0.4
Canarium schweinfurthii
5
109.4
0
0
0
Cissus dinklagei
5
-
0.8
0
0
Drypetes sp.
10
30.9
0.7
1.9
2.6
Enantia olivacea
6
15.4
0
1.8
0.8
Ficus sp.
7
-
0
0
0
Gambeya lacourtiana
10
92.2
1
0
0
Grewia oligoneura
6
38.4
0.2
0.3
0.3
Irvingia gabonensis
54
83.1
1.7
0.0
0
Irvingia grandifolia
10
110
0
0
0
Klainedoxa gabonensis
10
124.5
0
0
0
Landolphia forestiana
5
-
0
0.2
0
Landolphia sp.
5
-
0
5.6
0.4
Mammea africana
10
117.6
0.1
0.9
0
Manilkara yangambiensis
10
40.4
0.6
0.2
0.1
Pancovia laurentii
10
27
0.1
1
0.5
Parinari excelsa
10
113.1
19.8
0.1
0.1
Greenwayodendron (Polyalthia) suaveolens
10
29
0.1
1.6
0.5
Table 4 Mean recruitment under canopy of adults of 22 tree and liana species in LuiKotale, DR Congo.
77
Figure 18 Mean recruitment of pole (<10 cm DBH) under the parent crown for three control species (autochorous) and
19 species dispersed by bonobo. The dotted line is the threshold for self-replacement of the parent. Error bars indicate
SE.
Functional overlap – the primate community
The diurnal primate community of the study area is composed of members of three families:
Hominidae: P. paniscus; Colobidae: Colobus angolensis, Piliocolobus tholloni; Cercopithecidae:
Lophocebus aterrimus, Cercopithecus wolfi, Cercopithecus ascanius, Cercopithecus neglectus and
Allenopithecus nigroviridis. In 16 feces of C. angolensis that were investigated, and 124 feces of P.
tholloni, we did not discover a single seed. Allen’s swamp monkey (A. nigroviridis) and de
Brazza’s monkey (C. neglectus) are restricted to riparian forests. While bonobos can visit these
habitats and feed on riparian plants, we cannot assume functional overlap due to insufficient data.
We investigated 124 dung piles of L. aterrimus. Of these, 11.3% contained intact seeds, 62.9%
fragmented seeds. The average number of intact seeds per feces was 0.19 ± 0.06 (N=124). The only
species indicating food overlap and dispersal of intact seeds was Dialium sp. For C. wolfi, we
investigated 78 dung piles. Of these, 17.9% contained intact seeds of six different species. On
78
average, each dung pile contained 0.39 ± 0.99 seeds/feces. For C. ascanius, we investigated 118
feces, discovering seeds in 35.2% of them, originating from 16 species. On average, each dung pile
contained 2.8 ± 0.15 seeds. Based on direct observations, both species disperse additional species
by ectozoochory. Thus, the total number of dispersed species during the observation period was N =
18 for C.wolfi and N = 23 for C.ascanius. Based on five months of daily survey, the values of
Jaccard’s index show that functional overlap between monkeys and bonobos seems to be low.
Bonobos shared 17.1% of species dispersed with C. ascanius and 16.1% with C. wolfi. Only 4.8%
of the plants dispersed by L. aterrimus were also dispersed by bonobos.
Discussion
Here we investigated seed dispersal by bonobos (Pan paniscus), a large mainly frugivorous great
ape species inhabiting the evergreen lowland forests of the Central Congo Basin, restricted to the
area south of the Congo river.
For our study site LK we compiled a list of 133 plant species whose fruits were observed to
be ingested by bonobos, of which 91 were ingested including seeds. Among these plant species
shown to be bonobo-dispersed the trees represent 40% of all tree species found in the area and
account for 65% of all adult trees. Examining data from the two other long term field sites, Wamba
and Lomako (Table 1), shows that our findings are in line with plant species observed to be
consumed in these sites. Kano and Mulavwa (Kano & Mulavwa 1984) reported 113 species for the
Wamba site, representing an overlap of 44% at the genus level with our site. Badrian and Malenky
(Badrian & Malenky 1984) reported 81 species for Lomako, of which 40% overlap at the genus
level with our site. The fact that the overlap at the species level is small (8% and 9% respectively)
merits further investigations, suggesting a much higher diversity across the Congo Basin than
usually anticipated.
We are aware that there may be several dispersers per plant species and that primary dispersal can
be followed by secondary or tertiary dispersal and followed by post dispersal predation.
Nevertheless, we single out the bonobo to illuminate seed dispersal services performed by a single
vector in the extremely complex system of the tropical rain forest under consideration.
Almost all bonobo feces (98%) contained seeds, which represented over half of the dung’s weight,
with an average of two different species in each defecation.
With regard to the quality and viability of passed seeds, our results show that ingested seeds
remained viable after gut transit (97%). These seeds germinated faster and in higher frequency than
unpassed seeds, suggesting removal of tegumentary dormancy and endozoochorous processes
79
shaped by co-evolutionary interactions (Howe & Smallwood 1982; Robertson et al. 2006; Bradford
& Nonogaki 2007). Similar results have been documented for all other great ape species;
highlighting their crucial role in regeneration of the forests they inhabit (Poulsen, Clark & Smith
2001; Gross-Camp & Kaplin 2011; Nielsen et al. 2011). Although we did not quantify all the
aspects of seed dispersal effectiveness, in particular the probability that a viable dispersed seed
survives, germinates and produces an adult tree, our study shows that bonobos fit many crucial
criteria characterising efficient dispersers of tree species. Like other large primates, bonobos exploit
a large home range and consequently may disperse seeds to relatively long distances from parent
plants. Our study shows that the seeds ingested are dispersed to an average distance of 1.2 km from
the parental tree. Nevertheless, we have to note that after first seeds found in feces, other seeds can
follow after Time of Last Appearance (TLA = 63 h for chimpanzees (Lambert 1998)). Our estimate
of dispersal distance is thus likely to underestimate actual dispersal distances. Overall, 93.3% of
dispersal events were longer than 100 m. Long dispersal distance (LDD, (Nathan et al. 2003) is of
critical importance in plant population dynamics (Cain, Milligan & Strand 2000) and in LuiKotale,
the majority of zoochorous plants dispersed by bonobos (95% of the investigated species) could not
self-recruit without dispersal beyond the parent tree’s crown. This can be due either to the
incapacity of seeds to germinate without handling and/or to higher mortality under the parental
crown due to density-dependent effects (Janzen 1970b; Connell 1971; Schupp 1992).
Furthermore, and not reported here, endozoochory by bonobos is in fact often the first stage
of diplochorous seed dispersal, with dung beetles as secondary dispersers. Tunnellers such as
Catharsius sp. bury seeds to a maximum of 3.5 cm(Beaune et al. 2012a) thereby enhancing the
probability that a seed will escape predators, when compared to seeds that remain on the surface (by
>50%, (Beaune et al. 2012a). Thus, small changes in predation pressures can have a large effect on
plant demography (Fenner 2000).
A large gap exists between seed production and the growth of a reproductive adult tree. This
gap is not assessed here (secondary/tertiary/quaternary dispersal, post-dispersal mortality,
competition, abiotic and biotic factors, etc. (Forget et al. 2005; Forget et al. 2011). But we assess
here the first steps of the seed dispersal loop set in march by the bonobo. According to Schupp’s
definition, the bonobo seems to be an efficient seed disperser for the majority of fruiting plants in
our site. What we found here is probably applicable to other ecosystems in which large primates are
important frugivores. But here our system is simplified by the fact that bonobo is the only ape and
the only large primate of the area.
If we compare seed rain produced by bonobo with that produced by other Afrotropical
primates (Poulsen, Clark & Smith 2001), bonobos outperform them in seed dispersal. Accounting
for density, seed rain effected by chimpanzees turns out to be less than that effected by bonobos.
80
With only 96.5 seeds/day/km² chimpanzees of a Cameroonian site dispersed merely a quarter of
what bonobos dispersed in our study site (441.1 seeds/day/km²). Seed rains reported for Gorillas
calculated with high density of this ape (1.7 Gorilla/km²) are similar to our results (464.7
seeds/day/km²). The entire arboreal monkey community, with four species of Cercopithecidae,
disperses 568 seeds/day/km² (Poulsen, Clark & Smith 2001). The unique and irreplaceable dispersal
service provided by bonobo cannot be proved here. However, five months of observation show little
functional redundancy for seed dispersal with other primates. A general correlation is found
between body size of frugivores and the size of fruits/seeds that are ingested (Howe & Smallwood
1982), and very few animals reach the size of bonobos. Thus, it becomes evident that the bonobo is
certainly a key seed disperser for many tree species and can be considered – next to the elephant –
as gardener of the Congo forests.
Conclusion
Pan paniscus is the biggest ape within its geographic range and the second largest frugivore after
the elephant. In general, fruit species are dispersed by many frugivorous species (Gross-Camp &
Kaplin 2011) such as hornbills, monkeys, and bats. However, for fruit with large seeds, the
potential dispersal vectors are scarce, suggesting that the fate of large frugivorous species such as
the bonobo may disproportionately affect the regeneration process of these plants (Vanthomme,
Bellé & Forget 2010a). Apes with their medium-sized body size category are specialized in a
certain seed size range (Forget et al. 2007). Moreover, in the LK primate community, very few
species that are dispersed by bonobo endozoochory through the gut are also dispersed by monkeys.
The overlap in dispersal services seems to be low. Monkeys (mainly Cercopithecus) disperse
principally by seed spitting zoochory, which is an different mechanism in terms of recruitment
(Dominy & Duncan 2005), with different effects on seed fate (Gross-Camp & Kaplin 2011).
Finally, a monkey’s home ranges and daily travel distances are different in monkeys than in
bonobos (several km/days), with consequences for dispersal distances and LDD. In Afrotropical
forests, birds and primates consume and disseminate plants located in different canopy strata and
exhibit low plant species overlap in the seeds they disperse (Fleming 1979; Clark, Poulsen & Parker
2001; Poulsen et al. 2002). In the absence of functional overlap between the bonobo and other
dispersers, the extirpation of this primate from the system might lead to an irreplaceable loss of
ecosystem services.
With the large size of the bonobo and its peculiar behavior, our hypotheses are verified:
bonobos disperse adapted seeds to considerable distance with low functional vector overlap.
81
Strategies for conserving Congo forests inhabited by bonobos should therefore include strong
measures for conserving this key species, which is currently threatened by extinction (IUCN 2012).
82
interaction
Family
Genus
Species
Life
Form
Leaf
Flower
Fruit
Seed
Stem
Sap
Bark
Seed
handling
Intact
passed
seed
viability
census
germinated
/total
seed dispersal
Achariaceae
Caloncoba
welwitschii
W L
tree
1
swallow
I
Anacardiaceae
Antrocaryon
nannanii
tree
1
spit
I
Anacardiaceae
Sorindeia
zenkeri
tree
1
swallow
I
Anacardiaceae
Trichoscypha
arborescens
tree
1
swallow
I
Anacardiaceae
Trichoscypha
acuminata
tree
1
swallow
Annonaceae
Anonidium
mannii
W L
tree
1
handle
I
15/15
Annonaceae
Enantia
olivacea
tree
1
swallow
Annonaceae
Enantia
pilosa
tree
1
swallow
Annonaceae
Greenwayodendron
suaveolens
W L
tree
1
swallow
I
1/4
Annonaceae
Isolona
bruneelii
tree
1
swallow
I
Annonaceae
Monanthotaxis
myristicifolia
liana
1
swallow
Annonaceae
Thonnera
congolana
tree
1
swallow
I
5/19
Annonaceae
Uvaria
acabrida
liana
1
swallow
Annonaceae
Uvaria
acabrida
tree
1
swallow
I
6/18
Annonaceae
Uvaria
engleriana
liana
1
swallow
Annonaceae
Uvariastrum
pynaertii
tree
1
swallow
Apocynaceae
Landolphia
forestiana
liana
1
swallow
I
V
Apocynaceae
Landolphia
congolensis
W L
liana
1
swallow
I
Apocynaceae
Landolphia
owariensis
W
liana
1
swallow
Burseraceae
Canarium
schweinfurthii
W L
tree
1
swallow
I
Burseraceae
Dacryodes
yangambiensis
tree
1
swallow
I
69/142
Burseraceae
Dacryodes
sp.
tree
1
swallow
Burseraceae
Dacryodes
buettneri
tree
1
?
Burseraceae
Santiria
trimera
W
tree
1
swallow
Burseraceae
tree
1
swallow
Burseraceae
tree
1
swallow
Caesalpiniaceae
Dialium
corbisieri
W L
tree
1
1
swallow
I
41/542
Caesalpiniaceae
Dialium
sp.
tree
1
1
swallow
I
Caesalpiniaceae
Dialium
sp.
tree
1
1
swallow
I
Caesalpiniaceae
Dialium
sp.
tree
?
1
swallow
I
Caesalpiniaceae
Dialium
sp.
tree
?
1
swallow
I
Cecropiaceae
Musanga
cecropioides
tree
1
1
1
swallow
I
V
Chrysobalanaceae
Parinari
excelsa
W L
tree
1
spit
I
Clusiaceae
Garcinia
chromocarpa
tree
1
swallow
Clusiaceae
Garcinia
ovalifolia
L
tree
1
swallow
I
52/101
Clusiaceae
Mammea
africana
W L
tree
1
handle
I
Cucurbitaceae
Momordica
foetida
liana
1
swallow
I
0/5
Ebenaceae
Diospyros
sp.
tree
1
swallow
I
V
Ebenaceae
Diospyros
sp.
tree
1
swallow
I
Ebenaceae
Diospyros
hoyleana
L
tree
1
?
Euphorbiaceae
Drypetes
sp.
tree
1
?
Euphorbiaceae
Drypetes
Ieonensis
tree
1
spit
I
Euphorbiaceae
Maesobotrya
bertramiana
tree
1
spit
I
Euphorbiaceae
Phyllanthus
muellerianus
tree
1
?
Euphorbiaceae
Plagiostyles
africana
tree
1
?
Guttifereae
Garcinia
punctata
L
tree
1
swallow
Icacinaceae
Icacina
sp.
shrub
1
swallow
Irvingiaceae
Irvingia
grandifolia
tree
1
handle
I
Irvingiaceae
Irvingia
gabonensis
W L
tree
1
handle
I
5/100
83
Irvingiaceae
Irvingia
sp.
tree
1
handle
I
Irvingiaceae
Klainedoxa
gabonensis
L
tree
1
handle
I
Malvaceae
Cola
sp.
shrub
1
swallow
Malvaceae
Cola
gigantea
tree
1
swallow
I
24/24
Malvaceae
Cola
bruneelii
W
shrub
1
swallow
I
Malvaceae
Cola
sp.
shrub
1
swallow
I
Malvaceae
Cola
clamidandtha
tree
1
swallow
Malvaceae
Cola
sp.
tree
1
swallow
Malvaceae
Grewia
sp.
tree
1
swallow
I
29/79
Malvaceae
Grewia
pinnatifida
W
tree
1
swallow
I
13/77
Malvaceae
Grewia
sp.
tree
1
swallow
I
15/40
Malvaceae
Grewia
sp.
tree
1
swallow
I
9/20
Marantaceae
Maranthacloa
leucantha
herb
1
swallow
Melastomataceae
Dissotis
brazzeana
shrub
1
1
1
?
Meliaceae
Guarea
laurentii
tree
1
swallow
I
68/74
Mimosaceae
Parkia
filicoidea
tree
1
?
Moraceae
Ficus
sp.
liana
1
1
swallow
I
V
Moraceae
Ficus
cyathistipula
liana
1
swallow
I
V
Moraceae
Ficus
exasperata
L
liana
1
swallow
I
V
Moraceae
Ficus
sp.
liana
1
swallow
I
V
Moraceae
Ficus
sp.
liana
1
swallow
I
V
Moraceae
Ficus
sp.
liana
1
swallow
I
V
Moraceae
Morus
nigrum
tree
1
swallow
I
Myristicaceae
Pycnanthus
angolensis (=kombo)
tree
1
swallow
Myristicaceae
Staudtia
kamerunensis
tree
1
swallow
I
3/67
NID
tree
1
swallow
I
NID
tree
1
swallow
NID
tree
1
swallow
I
NID
1
swallow
I
6/83
NID
tree
1
swallow
I
1/100
NID
tree
1
swallow
I
NID
1
swallow
I
NID
1
swallow
I
2/100
NID
1
swallow
I
V
NID
tree
1
swallow
Olacaceae
Olax
sp.
tree
1
swallow
I
Olacaceae
Strombosiopsis
tetrandra
L
tree
1
swallow
Olacaceae
Strombosiopsis
tetrandra
L
tree
1
spit
I
Rubiaceae
Mitragyna
stipulosa
tree
1
swallow
I
V
Rubiaceae
tree
1
swallow
Sapindaceae
Blighia
welwitschii
tree
1
swallow
Sapindaceae
Chytranthus
macrobotrys
tree
1
swallow
Sapindaceae
Eriocoelum
microspermum
tree
1
swallow
Sapindaceae
Haplocoelum
congolanum
shrub
1
swallow
Sapindaceae
Pancovia
laurentii
W L
tree
1
swallow
I
54/74
Sapindaceae
Placodiscus
paniculatus
tree
1
1
swallow
I
V
Sapotaceae
Autranella
congolensis
tree
1
spit
I
Sapotaceae
Gambeya
lacourtiana
tree
1
swallow
I
2/50
Sapotaceae
Manilkara
yangambiensis
tree
1
swallow
I
30/133
Sapotaceae
Manilkara
malcoleus
tree
1
swallow
Sapotaceae
Manilkara
obovata
tree
1
swallow
Sapotaceae
Manilkara
sp.
tree
1
swallow
Sapotaceae
Pachystela
bequaertii
tree
1
?
Sapotaceae
Synsepalum
sp.
tree
1
swallow
84
Sapotaceae
Zeyherella
longepedicellata
tree
1
swallow
I
V
Verbenaceae
Vitex
sp.
tree
1
swallow
Vitaceae
Cissus
dinklagei
W
liana
1
swallow
I
12/45
Zingiberaceae
Aframomum
sp.
herb
1
1
swallow
I
V
Zingiberaceae
Aframomum
daniellii
herb
1
swallow
Zingiberaceae
Aframomum
sp.
herb
1
swallow
I
Zingiberaceae
Renealmia
africana
W L
herb
1
swallow
I
granivory/herbivory
Caesalpiniaceae
Cynometra
alexandri
W
tree
1
Caesalpiniaceae
Cynometra
sessiliflora
L
tree
1
Caesalpiniaceae
Cynometra
sp.
tree
1
Caesalpiniaceae
Dialium
gossweileri
tree
1
?
Caesalpiniaceae
Erythrophloeum
suaveolus
tree
1
Caesalpiniaceae
Gilbertiodendron
dewevrei
W L
tree
1
?
Caesalpiniaceae
Gilbertiodendron
ogouense
tree
1
Caesalpiniaceae
Hymenostegia
mundungu
tree
1
Caesalpiniaceae
Julbernardia
seretii
tree
1
Caesalpiniaceae
Monopetalanthus
microphyllus
L
tree
1
Caesalpiniaceae
Scorodophloeus
zenkeri
W L
tree
1
1
1
Euphorbiaceae
Manniophyton
fulvum
W
liana
1
1
Marantaceae
Haumania
leonardiana
liana
1
Marantaceae
Haumania
liebrechtsiana
W L
liana
1
Marantaceae
Megaphrynium
macrostachyum
L
herb
1
Melastomataceae
Ochtocharis
ancellandroides
shrub
1
1
Melastomataceae
Ochtocharis
dicellandroides
shrub
1
1
?
Melastomataceae
Tristemma
mauritianum
shrub
1
1
?
Mimosaceae
Pentaclethra
macrophylla
W
tree
1
Mimosaceae
Piptadeniastrum
africanum
tree
1
Moraceae
Treculia
africana
W L
tree
1
1
NID
epiphyte
1
Nymphaeaceae
Nymphaea
lotus
herb
1
Table 5 Plants consumed by bonobo in LuiKotale, DRC.
W
indicates that the species exists in and is consumed by
bonobos at Wamba (Kano & Mulavwa 1984);
L
= same for Lomako (Badrian & Malenky 1984); Fruth, unpub data); I =
seeds were found intact in feces, V = seeds were tested and found viable in nursery trials but ratio is not posted because
census was interrupted. NID = not identified.
85
The Bonobo-Dialium positive interactions
David Beaune, François Bretagnolle, Loïc Bollache, Gottfried Hohmann,
Martin Surbeck & Barbara Fruth
Published in the American Journal of Primatology
86
Abstract
A positive interaction is any interaction between individuals of the same or different species
(mutualism) that provides a benefit to both partners such as increased fitness. Here we focus on
seed dispersal mutualism between an animal (bonobo, Pan paniscus) and a plant (velvet tamarind
trees, Dialium spp.). In the LuiKotale rainforest south-west of Salonga National Park, DR Congo,
seven species of the genus Dialium account for 29.3% of all trees. Dialium is thus the dominant
genus in this forest. Dialium fruits make up a large proportion of the diet of a habituated bonobo
community in this forest. During the six months of the fruiting season, more than half of the
bonobos’ feeding time is devoted to Dialium fruits. Furthermore, Dialium fruits contribute a
considerable proportion of sugar and protein to bonobos’ dietary intake, being among the richest
fruits for these nutrients. Bonobos in turn ingest fruits with seeds that are disseminated in their feces
(endozoochory) at considerable distances (average: 1.25km after 24hrs of average transit time).
Endozoochory through the gut causes loss of the cuticle protection and tegumentary dormancy, as
well as an increase in size by water uptake. Thus, after gut passage, seeds are better able to
germinate. We consider other primate species as a potential seed disperser and conclude that
Dialium germination is dependent on passage through bonobo guts. This plant-animal interaction
highlights positive effects between two major organisms of the Congo basin rainforest, and
establishes the role of the bonobo as an efficient disperser of Dialium seeds.
Keywords Congo basin, forest ecology, germination activation, plant-animal interaction, seed
dispersal, velvet tamarind, zoochory
Résumé
Le mutualisme est une interaction entre des individus de deux espèces qui fournit un avantage
sélectif aux deux partenaires. Ici nous présentons un exemple de mutualisme de dispersion de
graines entre un animal : le bonobo (Pan paniscus) et un arbre : les tamarins africains (genre
Dialium). Au sud-ouest du parc national de la Salonga, dans la forêt tropicale humide de LuiKotale,
sept espèces du genre Dialium représentent 29.3% de tous les arbres et sont ainsi le genre dominant
de cette forêt. Les fruits de Dialium composent une grande proportion du régime alimentaire de ces
grands singes. Pendant les six mois de la saison de fructification, plus de la moitié du temps
d'alimentation des bonobos est consacré aux fruits de Dialium. En outre, les fruits de Dialium sont
parmi les plus riches des fruits analysés pour les sucres et protéines. Ils sont une source importante
de ces nutriments dans le régime des bonobos. Les bonobos ingèrent en contrepartie les fruits avec
leurs graines qui sont disséminées via leurs fécès (endozoochorie). Cette endozoochorie affecte la
87
protection tégumentaire des graines qui gonflent et brisent ainsi la dormance germinative. Ainsi,
après le passage dans l’intestin, les graines ont un meilleur taux de germination. Les autres espèces
de la communauté diurne de primates semblent ne pas avoir le même rôle que les bonobos dans la
dispersion de graines de Dialium. Nous proposons par conséquent une certaine bonobo-dépendance
pour les graines de Dialium. Cette interaction plante-animale est un autre exemple
d’interdépendance biologique entre deux organismes d’importance majeure dans le bassin du
Congo, et place le bonobo comme disperseur efficace de graine pour des arbres du genre Dialium.
Mots clefs Activation de la germination, bassin du Congo, bonobo dépendance, coévolution,
écologie forestière, interaction plante-animale, zoochorie
88
Introduction
Seed dispersal mutualism between fruiting trees and frugivores is an important interaction in
rainforest ecology (Howe & Smallwood 1982; Lambert & Garber 1998; Nathan & Muller-Landau
2000; Levin et al. 2003; Howe & Miriti 2004; Forget et al. 2011). Fruiting plants bear fruit that
attracts frugivorous animals. Animals in turn disperse the seeds by zoochory. Animals seem to be so
efficient that the majority of tropical plants use zoochorous strategies for seed dispersal (Howe &
Miriti 2000).
Within tropical rainforests, birds, mammals and to a lesser extent reptiles and even fishes are known
to be frugivores and seed dispersers (Asquith, Wright & Clauss 1997). In particular, primates have
been cited to be efficient seed dispersers in tropical rainforest ecosystems, as they often occur in
high densities, show high rates of frugivory and are often of considerable body size (Chapman
1995; Lambert & Garber 1998). Studies from Cameroon (Clark, Poulsen & Parker 2001) and Ivory
Coast (Koné et al. 2010) show that seed dispersal services provided by primates are often taxon-
specific. These processes have been shaped by sophisticated evolutionary histories and the
disappearance or declining abundance of one partner may raise serious challenges for conservation
(Chapman 1995; Chapman & Onderdonk 1998). For a wide range of plant species in African
rainforests, great apes such as chimpanzees and gorillas play key roles in seed dispersal
(Wrangham, Chapman & Chapman 1994; Voysey et al. 1999a; Voysey et al. 1999b). In a
comprehensive study investigating the diurnal primate community in the Dja reserve, Poulsen and
colleagues [2001] were able to show that despite lower densities compared to monkeys, apes
accounted for one-half of all seeds dispersed by primates, highlighting their major role as dispersal
agents.
Of the 32 species of the tree genus Dialium (Caesalpinioideae) known worldwide, 16 occur
in tropical Africa (Senesse 1995). Dialium trees are tall, sometimes more than 40 meters, and reach
the highest level of the canopy. They produce black-brown velvety pods, each enclosing a single
seed embedded in luscious sugary fruit that is produced throughout most of the year. These trees
provide food for populations of many apes in Africa including gorillas, chimpanzees and bonobos
(Kuroda et al. 1996; White & Abernethy 1997), not only when in fruit, but also with flushes of
young leaves. In the southern part of the Congo basin, south of the Congo River, in the Democratic
Republic of Congo (DRC), the bonobo (Pan paniscus) is the only great ape. Like gorillas and
chimpanzees on the northern bank of the Congo River, this primate is thought to play an important
role in seed dispersal [Idani 1986]. So far, however, their role in seed dispersal and germination
processes has been poorly addressed (Idani 1986; Tsuji, Yangozene & Sakamaki 2010).
89
Across all field sites where food plant inventories have been published and some
investigations conducted, Dialium has been mentioned as a major food resource for Pan paniscus.
In terms of time the apes spend feeding on them and the availability of foods they produce
throughout the year, Dialium trees make up a major part of the diet of the bonobos inhabiting
LuiKotale (Hohmann et al. 2006). At Wamba, fruit pulp of Dialium spp. is eaten as a staple food
during several periods of the year (Kano & Mulavwa 1984). In the Lomako long-term field site,
Dialium is one of the most important bonobo foods (Badrian & Malenky 1984). Although Dialium
is widely considered to be an important resource for bonobos, and thus plays an important role in
the daily foraging activities of the groups, the relative importance of species of this genus compared
to species of other genera with which these animals interact is largely unknown. Moreover, the role
of the bonobo in the regeneration process of Dialium spp. is largely unknown. The aim of the
present paper is to investigate the interactions between Dialium and bonobos, testing the hypothesis
that they are engaged in a positive interaction (seed dispersal mutualism), by studying both (A) the
efficiency of seed dispersal by bonobos, including Dialium seed rain and the effects of interactions
with bonobos on seed viability and germination, and (B) the benefits that bonobos receive by
including Dialium in their diet, indexed by comparing the nutritional value of Dialium fruit to those
of other plants at the site.
In addition, to investigate the importance of interactions of bonobos with Dialium compared
to other primates, we (C) explore how other primates of the community at LuiKotale interact with
Dialium. Our objective is to quantify the possible functional redundancy between primate species,
addressing the question of whether other primates could replace the ecological services provided by
bonobos in Dialium seed dispersal. We hypothesise that bonobos and Dialium trees are mutually
interdependent.
We consider bonobo-mediated seed dispersal as being efficient, if the number of seeds
spread through endozoochory by bonobos exceeds that spread by other consumers (here, monkeys).
We predict that Dialium provides critical food resources for bonobos, as its fruits are among the
most important items in the animals’ annual diet in terms of both, quantity and quality.
METHODS
Study site
The LuiKotale research site (LK) is located within the equatorial rainforest (2°47’ S, 20°21’ E), at
the south-western fringe of Salonga National Park (DR Congo), within the same continuous forest
block. The study site comprises > 60 km² of primary evergreen lowland tropical forest with a trail
network of 76 km. The climate is equatorial with abundant rainfall (>2,000mm/year). Mean
90
temperatures at LuiKotale range between 21°C and 28°C with a minimum of 17°C and a maximum
of 38°C (2007-2010). Investigations were conducted with a habituated group of 35 bonobos. Field
work with these primates has been carried out since 2002 (Hohmann & Fruth 2003).
Impacts of Bonobos for Dialium
Dialium seed rain
A total of 1152 bonobo feces were collected between April 2002 and June 2011 to contribute to the
project’s long-term data base. These samples were analysed for the presence of Dialium seeds. In
addition, the number of Dialium seeds per feces was counted for 160 feces collected between 2009
and 2011.
Seed transformation & viability
To assess seed transformation allowing control for both intake and output, seeds were ingested by
the first author and measured again after passage through the digestive tract. A total of 112 seeds
from a bonobo feeding tree were collected. Seed diameter (length & breadth) in mm was measured
using a slide calliper (0-10cm ± 1μm). Retention time was 24 hours, which is similar to that
calculated in the wild bonobo population of LK (24hrs00min ±SE. 9min, see below).
We collected Dialium fruit samples during bonobo feeding sessions. The trees where
feeding was observed were our target trees. To avoid other confounding factors such as the
genotype of the fruiting plant, fruit samples were used from these target trees as controls. We took
only intact fruit that had fallen to the ground incidentally as the bonobos moved through a feeding
tree. Fruit that was clearly discarded by a feeding animal was not collected. If bonobos had not been
observed feeding in any other Dialium tree 36hrs prior to and 24hrs after the feeding bout under
investigation, we collected their feces the next day to obtain seeds from the target tree. The seeds
were extracted manually from the feces. Unchanged seeds, i.e., seeds that were identical in size and
shape to fresh seeds, were separated from transformed seeds, i.e., seeds that were visibly swollen
(imbibed). All seeds were placed on an elevated platform (1×2m, 1.70 m high with predator-proof
legs) in natura in LuiKotale forest (under canopy) and monitored daily.
To assess seed viability, we scored germination as defined by radicle emergence (Heß 1999;
Knogge, Herrera & Heymann 2003). We monitored the germination rate of seeds that had passed
the human digestive tract as mentioned above and seeds collected from target trees artificially
activated by scraping the hard testa responsible for physical seed dormancy, in an attempt to imitate
processes occurring in the bonobos’ gut [Beaune 2012, Beaune et al., submitted].
91
Transit time & dispersal distance
The probability distribution of Dialium seeds is based on empirical bonobo movements,
georeferenced from 15
th
of January 2008 to the 21
st
of September 2011. With bonobo movements
after feeding sessions in Dialium trees georeferenced and mean transit time of seeds known, a
mechanistic model of seed dispersal distance can be calculated (Westcott et al. 2005; Tsuji,
Yangozene & Sakamaki 2010; Côrtes & Uriarte 2012). Whenever possible, bonobos were followed
daily from nest to nest (approx. 05:30 to 17:30). Daily travel routes of parties were tracked with a
GPS (Garmin
®
60CSX) using 1 point position /5 minutes for georeferencing [Beaune 2012].
Bonobo transit time was calculated from direct observations. Whenever an individual bonobo
swallowed a new fruit species not eaten in the previous 36 hours, its seed was considered as a
marker seed indicating the onset of passage-time, and the individual was monitored continuously
(except at night) until the seeds of the newly ingested species were found in its feces. The time
between ingestion of the marker seeds and appearance of the first seeds in the dung was taken as gut
transit time (TT). Influences of the sex and seed size on transit time were tested with students t-test
and analyses of variance (ANOVA) with all the effects considered as fixed and homoscedasticity
tested (Breusch–Pagan test). Seed size was arbitrarily categorized as follows: small: < 2mm;
medium-sized: 2-10mm; large: > 10mm).
Data analysis
To test the germination success of different Dialium seeds, the R program (R Development Core
Team 2011) was used. Each relevant statistical test is specified in the results section.
Impact for the apes
Dialium as part of the bonobo diet
Bonobos have a fission-fusion society. Depending on season and time of day, the community splits
up into smaller foraging subgroups called parties. From December 2007 until July 2009 we
preferentially followed parties containing males and performed hourly scans on the activity of
individuals (n=5,605). If they were observed feeding, the food item and species were determined.
Based on these scans we calculated the proportion of observations of Dialium feeding relative to
feeding on other items. From August 2009 until June 2011, we considered group activity to be that
of the majority (> 50% of the bonobos) of the visible animals during a continuous record of feeding
activities (i.e., continuous focal sub-group sampling, Altmann 1974). Start and end times of feeding
for each plant species and part consumed were recorded starting from August 2009 for focal
subgroups. We thereby assessed the proportion of feeding sessions on Dialium relative to those of
92
feeding on other plant species. We distinguished fruit from leaves and sap consumption. Dialium
tree and seed species have subtle differences, making them difficult to distinguish. The genus level
Dialium was used for all seven of the species, considering that seed biology was similar among
species.
Nutritional value of Dialium compared to that of other fruits
Collection of plant samples
Data collection covered 25 months between February 2002 and July 2010. The study included 95
species whose fruits were observed to be eaten by bonobos. Samples were preferably collected from
individual plants that were visited by bonobos and, whenever possible, came from feeding patches
while the animals fed. When this was impossible, we collected a sample either from the same
feeding patch after the animals had left, or from a patch that was similar in size and phenophase. As
for the Dialium control fruits, samples were made up of intact fruit that had fallen to the ground.
The samples were brought back to camp within a few
hours. Samples were processed the same day
and stored in liquid nitrogen until lyophilisation.
For further details see (Hohmann et al. 2010).
Phytochemical analyses
Macronutrient analyses of all samples were performed at the Nutritional Lab of the Leibniz Institute
for Zoo and Wildlife Research (Berlin). Analyses of antifeedants such as phenols and tannins were
carried out at Hamburg University following the protocol described in [Hohmann et al. 2006]. For
methodological details see (Hohmann et al. 2010).
Functional overlap – preliminary report on the primate community
To assess the importance of monkeys as dispersers of Dialium seeds, we investigated seed handling
and food plant overlap among seven species of the diurnal primate community of LK from February
to June 2011 as a preliminary report. The following species were involved: Allenopithecus
nigroviridis, Colobus angolensis, Piliocolobus tholloni, Lophocebus aterrimus, Cercopithecus
neglectus, Cercopithecus ascanius, and Cercopithecus wolfi. For reasons of sample size and
because C. angolensis, A. nigroviridis and C. neglectus are restricted to riparian forest where
Dialium does not occur, we included only data for four species: P. tholloni, L. aterrimus, C.
ascanius, and C. wolfi. Observations were simultaneously performed by two teams, one focusing on
bonobos and one focusing on the monkey species. In contrast to bonobos, monkeys were not
habituated (Bourson 2011). Feeding and seed handling of Dialium fruit were assessed by direct
observation. Fecal samples were collected whenever possible. Seeds were collected from feces as
93
described above. A total of 440 monkey feces were collected between February and June 2011. In
addition, we collected seeds that had been spat out by monkeys.
Ethics Statement
The studied apes are free-ranging bonobos and monkeys observed without invasive methods,
constraint, contact and any interaction with the researchers. Animal welfare was of higher priority
than scientific interest. The methods used to collect data in the field are in compliance with the
requirements and guidelines of the ICCN, and adhere to the legal requirements of the host country,
the Democratic Republic of Congo and to the American Society of Primatologists principles for the
ethical treatment of primates.
Results
Impacts of Bonobos for Dialium
Dialium seed rain
Among the 1152 feces analysed from April 2002 to June 2011, 36.1 ± SE 0.0 % contained Dialium
seeds. Of 416 feces that contained seeds, the number of Dialium seeds varied greatly between 1 and
781. The median was 50.0 Dialium seeds/feces with an average of 82.9 ± SE 14.3, right-skewed (=
3.52). By extrapolation, an individual bonobo should disperse 82,623, 471 Dialium seeds/year.
Considering 40 years as an average lifespan (Rowe 1996), and an average number of dung produced
per day (7.55; this study), a bonobo may disseminate about 3.3 million Dialium seeds in its lifespan.
Seed transformation & viability
In the human-gut passage experiment, a total of 112 measured Dialium seeds were swallowed, 85 of
these were excreted and found 24 hours later. Of these 85 seeds, only five had transformed into
bigger seeds (from 1148 to 1502 µm of length, Wilcoxon rank-sum test: W=1, P<0.05; and from
542 to 739µm of breadth: W=0, P<0.05), whereas the remainder of 80 seeds remained unchanged
(length: W = 4107.5, P = 0.72; breadth: W = 4244.5, P = 0.9912). In the transformed seeds, the
protective cuticle was partially removed, and the cotyledon reserve was visible. In the rest of passed
seeds no change was visible, which is similar to what we observed in bonobo dung (Wilcoxon rank-
sum test for length (µm): W= 91, P = 0.09). See
Figure 19.
None of the control seeds (n= 406) germinated during the eight months of monitoring (Fig. 1). Only
seeds transformed by passage through the human or bonobo digestive tract and artificially treated
seeds germinated. One third (37.6% ± SE 4.7) of these transformed seeds showed radicle
94
emergence becoming visible between 24 and 96 hrs after plantation. All of the other transformed
seeds that did not germinate were infected with pathogens. Of 532 seeds collected from bonobo
feces, 109 were transformed, and 423 were untransformed. The germination rate was 7.7% ± 1.3 for
seeds that passed through the bonobo digestive tract. This rate was not significantly different from
the germination rate of seeds that passed through the human digestive tract (chi squared test =
2.4019, df = 1, P = 0.1212).
0
25
50
75
100
Control
seeds (406)
Passed
human (85)
Passed
bonobo (532)
Passed
bonobo
transformed
(109)
Treated (92)
germination rate %
P=0.11
a
b
d
c
Figure 19 Germination rates of Dialium seeds for different preconditions. Columns along X-axes show seeds of
different preconditions: Control seeds, passed seed through human and bonobos’ digestive tracts, naturally transformed
and artificially activated seeds. Number in brackets indicates sample size (N). Error bars indicate SE. Horizontal
brackets indicate significance of differences (Multiple pairwise comparisons, binomial test, Power analysis=100%).
Transit time & dispersal distance
Transit time
We recorded 124 marker seeds from ingestion to first deposition. Marker seeds were identified from
13 different genera. These marker seeds were swallowed and defecated by 19 different bonobos,
seven males and 12 females. The resulting transit time was 24hrs00min on average ± SE. 9 min;
(range: 20 hrs 03 min-28 hrs 17 min). Neither sex nor seed size affected transit time (t = 0.0253, df
= 15.285, p = 0.9801; n=61 large, 28 medium-sized, 35 small; F
2,119
= 0.382, p = 0.683).
Dialium dispersal distance
In the fission-fusion bonobo society, sub-groups (parties) are often composed of males and females
of various ages. Thus movement behavior ought to be similar for both sexes. Based on 344 bonobo
95
travel distances from 344 Dialium feeding session in trees, the average dispersal distance for
Dialium seeds was: 1248 ± 45 m, median= 1115; range = 1-4151 m.
Impact for the apes
Proportion of Dialium in the bonobo diet
Fruit: Bonobos consume Dialium fruit during several months of the year (32/43 months studied,
from December 2007 to June 2011.
Figure 20. This includes times when we observed bonobos
eating unripe fruits before the start of the fruiting season. However, this consumption is negligible
compared with the high consumption of ripe fruit during the season. During the 43 months of
feeding ecology assessment, Dialium fruit feeding sessions made up 25.5 % ± SE 1.0 of the overall
time spent feeding. By excluding months when Dialium was not in fruit the average proportion of
feeding sessions on Dialium fruit rose to 34.2 % ± 1.5. During certain months of the year, Dialium
fruit also made up the majority of feeding time such as in December 2008 and October 2009, when
it accounted for 82.4 % and 83.4% of the feeding time respectively. On certain days, Dialium fruits
were the only fruits eaten by the group. From September 2009 to June 2011, 951hrs of group
feeding sessions were recorded across 22 months (totaling 315 days). Among all fruit species eaten
during this period, Dialium were the most consumed fruits (19.0%); beyond Cissus dinklagei
(7.9%); Grewia spp. (4.7%); Polyalthia (=Greenwayodendron) suaveolens (3.8%); and others.
Bonobos were observed eating more than 100 plant species (see (Beaune 2012)).
Leaves: Bonobos also ate young leaves of this tree. Therefore, bonobos also feed on Dialium trees
outside the fruiting season (
Figure
21). Considering Dialium leaf-consumption, the species appears to be present in the bonobo
diet all year round.
Sap: Bonobos were anecdotally observed feeding on Dialium sap (n=1). After removing a dozen or
so centimetres of bark, bonobos ate the leaking sap.
96
0
10
20
30
40
50
60
70
80
90
100
12/07
2/08
4/08
6/08
8/08
10/08
12/08
2/09
4/09
6/09
8/09
10/09
12/09
2/10
4/10
6/10
8/10
10/10
12/10
2/11
4/11
6/11
months
Time spent feeding (%)
on Dialium fruit
Figure 20 Time spent feeding on Dialium fruit. Bars indicate feeding sessions of Dialium fruit as proportion of overall
time spent feeding for 43 months between December 2007 and June 2011.
Nutritional value of Dialium compared to that of other fruits
Table 6 shows nutritional values of Dialium seeds in comparison to the averaged values of 94 other
fruits. It becomes clear that Dialium has a special place within the bonobo diet with respect to
macronutrients such as protein (145.7 mg/g) and sugar (101.4mg/g). Although not reaching
significance, Dialium also shows the tendency to contain less antifeedants than the average fruit.
When compared with other important fruit consumed by bonobos (Cissus dinklagei and
Greenwayodendron suaveolens), Dialium fruits still provide more protein while the other two fruits
are richer in sugar.
Functional overlap – preliminary report on the primate community
The diurnal primate community of the study area is composed of three families: Hominidae: P.
paniscus; Colobidae: Colobus angolensis, Piliocolobus tholloni; Cercopithecidae: Lophocebus
aterrimus, Cercopithecus wolfi, Cercopithecus ascanius, Cercopithecus neglectus and
Allenopithecus nigroviridis. Based on five months of daily survey: L. aterrimus, C. wolfi, C.
ascanius were observed eating Dialium fruits, while C. neglectus and A. nigroviridis did not.
97
Although we could not confirm that the two latter species interact with Dialium, these monkeys
were mainly restricted to riparian forest where the genus Dialium is not present. The monkeys
mainly spit out the Dialium seeds as they did with seeds from other species. Overall, 440 feces from
four monkey species were collected. Of these, only 12.5% (N=55) contained intact seeds. . Of these,
only two feces contained Dialium seeds: one feces of L. aterrimus (1/124) with three Dialium seeds
and one feces of C. ascanius (1/118) with one Dialium seed. The number of all plant seeds per feces
was low (L. aterrimus: 0.19 ± SE. 0.06 (N= 124), C. wolfi: 0.39 ± 0.99 (N= 78), C. ascanius: 2.80
± 0.15 (N= 118). Dialium seed handling by monkeys is different than that of bonobos. Seeds were
mainly dispersed by seed spitting. Whether spit our or passed, Dialium seeds resulting from
monkey foraging activity never germinated.
Figure 21 Bonobos eating Dialium leaves out of the fruiting season of Dialium. LuiKotale, DR Congo.
Discussion
98
In this study, we investigated ecological interactions between an animal (bonobo, Pan paniscus)
and a plant (velvet tamarind trees, Dialium spp.). Concerning the impact for the tree, we
investigated Dialium seed rain, seed transformation and seed viability. With ingestion observed
during almost 75% of all months investigated, Dialium is consumed over long periods of the year.
Over 1/3 of all feces collected between 2002 and 2011 contained Dialium seeds. We showed that
the majority of Dialium seeds are adapted to survive digestion in apes and to a lesser extent in
monkeys (Lophocebus aterrimus and Cercopithecus ascanius). One of the major risks for a tree
using the endozoochorous strategy is the passage through a digestive system, where seeds are
exposed to a high level of acidity. Adaptation to these endozoochorous partners implies a trade-off
for the cuticle, which must be thin enough to be removed by acid attack and strong enough to
survive digestion. This is the case for Dialium seeds. Here, Dialium seeds seem to be adapted to
resist acid erosion of the primate’s gut. However, seed protection decreases with time in the
digestive tract. This affects some of the seeds, which become porous. When hermetic protection of
the coat is perforated, seeds swell and probably become digestible. Prolonged retention in the gut
may increase the likelihood of perforation. This can explain the coprophagy described in young
chimpanzees (Krief, Jamart & Hladik 2004) and bonobos at Wamba (Sakamaki 2009). In addition
this may explain the coprophagy observed in bonobos in times of reduced food abundance and
extended Dialium availability (own observations), although these observations remain exceptional.
The number of seeds passing through the bonobo’s digestive tract is considerable and exceeds by
far that of L. aterrimus, the monkey with the highest proportion of Dialium seeds found in feces.
Of the seeds that passed through the digestive tract, a small proportion (8%) had become porous and
managed to start germination within 24 to 96hrs from the moment of being positioned on the
ground. This effect is known as germination activation by animals, and this was the first example
observed in bonobos. In mammals, elephants are best known for germination activation. Detarium
or Balanites seeds are able to germinate only after passing through the elephant’s digestive tract,
and the consequences of the considerable decline in elephant populations for these trees has already
become apparent (Chapman, Chapman & Wrangham 1992; Cochrane 2003; Babweteera, Savill &
Brown 2007).
In seed dispersal mutualisms, dispersal by animal partners shows high dependence on population
survival. In cases when the animal partner becomes extinct (e.g. elephants by poaching) and when
no alternative partner exists, the dependent plant population cannot recruit effectively and the
number of seedlings falls (Babweteera, Savill & Brown 2007); this is more difficult to demonstrate
for the dispersal of medium-sized and small seeds such as Dialium, which involves many
consumers and is thus multi-vectorial. In Afrotropical forests, birds and primates consume and
disseminate plants located in different canopy strata and there is thus low overlap in dispersed seed
99
species (Fleming 1979; Clark, Poulsen & Parker 2001; Poulsen et al. 2002). In LK neither birds nor
bats have so far been observed feeding on Dialium. However, we showed that other frugivorous
primates consume and disperse Dialium seeds, although to a much lesser extent than bonobos. Even
though monkey densities in LK are larger than bonobo densities, Dialium endozoochorous seed rain
through the gut from monkeys might be lower than seed rain from bonobos. This phenomenon has
been observed in other sites (Poulsen, Clark & Smith 2001). We cannot prove that Dialium trees are
dependent on the bonobo, but monkeys, as a dispersal vector for Dialium, are surely different from
bonobos in terms of handling techniques, seed treatment and dispersal distance and thus seed
dispersal effectiveness.
Monkeys disperse seeds by seed spitting and endozoochory. Seed spitting by monkeys also allows
plant reproduction, although the quantity and quality of seeds are different from those dispersed by
bonobos (Lambert & Garber 1998; Gross-Camp, Masozera & Kaplin 2009; Gross-Camp & Kaplin
2011). Thus Dialium may be able to survive even without bonobos, although the process of
reproduction would be slowed down, and this would probably have an impact on Dialium
populations, and their genetic and spatial structures (Schupp, Jordano & Gomez 2010). The role of
monkeys in Dialium seed dispersal deserves further exploration. The current data are a preliminary
report and more observations and data collection during other seasons are required before final
conclusions are made.
Thanks to the dormancy coat, Dialium seeds can resist pathogens until germination after being
dispersed by any primate. However, they are highly vulnerable to seed predators when on the
ground. In other experiments, we showed that, when on the ground, Dialium seeds are often
removed by seed predators such as the giant pouched rat (Cricetomys emini) (Beaune et al. 2012a).
In addition, herds of bush pigs (Potamochoerus porcus), which are important seed predators, are
regularly observed foraging beneath Dialium trees (Beaune et al. 2012b) and they readily ingest and
chew available seeds. The same is true for forest duikers (Cephalophus nigrifrons, Cephalophus
callipygus), which are often found in the company of troupes of monkeys eating fruit and/or seeds
that has fallen to the ground. In these cases, the seeds are a valuable source of nutrients to their
predators. However, such seeds will no longer be able to germinate.
In contrast, seeds swallowed by bonobos avoid this dangerous period on the ground. First, passage
through the gut and seed dormancy both reduce the risk of predation. Secondly, diplocory also
occurs: bonobo feces attract dung beetles (Scarabidae, tunnellers as Catharsius spp.) that bury the
seeds and thus hide them from nocturnal predators (Hanski & Cambefort 1991; Feer 1999). At LK,
we showed that thanks to tunnelers, Dialium seeds dispersed by bonobo endozoochory through the
gut disappeared from the surface of the ground in less than an hour and were better able to avoid
seed predators and pathogens. A high proportion (97%) of Dialium seeds dispersed by diplochory
100
first by bonobos and then by dung beetles remained in place, while 74% of the surface seeds were
removed by nocturnal rodents (Beaune et al. 2012a).
Furthermore, based on the follow-up of 344 Dialium seed dispersal events, we judged Dialium seed
dispersal to be very long (1.25km ±SE. 0.045). Considering this very long dispersal together with
home range size and post-dispersal survival, bonobos are more likely to affect the spatial structure
of the trees than are sympatric primates (Westcott et al. 2005; Seidler & Plotkin 2006; Schupp,
Jordano & Gomez 2010). Although there is a gap between seedlings and adult trees that remains to
be explored, bonobos seem to play an important role in Dialium seed dispersal, reproduction and
population biology, and thus have an impact on the evolution of Dialium spp. populations.
However, bonobos, like all great apes, are rare and threatened in their area of distribution (Dupain
et al. 2000; Walsh et al. 2003; Hart et al. 2008; Tranquilli et al. 2012). A decrease in the numbers,
or worse, the disappearance of this species might have consequences for the ecosystem. Although
other mammals such as monkeys are probable dispersers of these attractive trees, their ability to
activate Dialium germination still remains to be demonstrated.
For Dialium species, this adaptation related to bonobo-facilitated germination, namely the strong
protection against digestion, could become a dangerous dependence (Howe 1984; Chapman 1995;
Chapman & Onderdonk 1998). In our experiment, none of the 406 seeds that had not gone through
the bonobo digestive tract germinated during eight months of monitoring. Such seeds probably
germinate, though at a much lower rate and after a long and dangerous dormancy period.
Considering this and other studies, the genus Dialium (African velvet tamarind) seems to be a key
resource for apes. Dialium trees have developed a highly nutritive fruit available during a long
fruiting period, and thus provide food for apes and other members of the frugivore community.
Although the two other great apes, chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla)
overlap with the Dialium’s home range in their areas of distribution (White & Abernethy 1997),
only chimpanzees have a positive Dialium-ape interaction. Gorillas have been observed chewing
the seeds and thus act as seed predators (Kuroda et al. 1996) or have been observed eating unripe
fruit (Rogers et al. 1990).
In LuiKotale, Dialium trees represent 29.3% ± SE 2.3 of the tree community in the terra firme
heterogeneous primary forest and are thus dominant (Beaune 2012). Dialium plays a considerable
role in bonobo feeding ecology. Dialium is known to be an important plant in the bonobo food
repertoire for the other long-term sites Lomako and Wamba (Badrian & Malenky 1984; Kano &
Mulavwa 1984), but no study has attempted to assess the relative importance of Dialium in terms of
quality and quantity. Here, we showed not only that Dialium serves bonobos as staple food for more
than half of the year but also that once in fruit, bonobos spend more time feeding for Dialium than
for any other food item in their diet. However, we cannot exclude other exceptional fruiting species
101
during other season not followed during our 43 months of monitoring. The extraordinary abundance
of these trees across bonobo study sites and the important nutrients contained in the fruit may
explain why the bonobos have this predilection. Furthermore, the fruits are richer in protein and
sugar than are other fruits available in the forest. In addition to eating Dialium fruit, bonobos also
eat the young leaves, even outside the Dialium fruiting season (Fig. 3). Dialium trees could thus be
considered one of the bonobos’ staple foods and are certainly of crucial importance. This
importance should be highlighted in bonobo conservation plans, with regard to the assessments of
suitable places for bonobo conservation or reintroduction (André et al. 2008).
Future investigations should focus on Dialium recruitment, population biology, spatial and genetic
structure and survival in forests where their ape partners are now extinct. In addition, to assess
potential coevolution between apes and Dialium trees, a comparison of their respective ranges is
needed. If some of the Dialium spp. ranges overlap with the range of bonobos and chimpanzees, the
coevolution hypothesis would be reinforced.
Dialium
spp
Other fruits
average
±SE
Direction
of
difference
Wilcoxon’s
signed-
rank test
Cissus
dinklagei
Polyalthia
suaveolens
Macronutrient
Protein (mg/g)
145.7
92.8 ±43.1
>
p<0.001
106.1
96.8
Crude Protein/ADF-Ratio
1.7
0.8 ±0.7
>
p<0.001
0.4
0.4
Protein
14.6%
9.3% ±4.3
>
p<0.001
10.6%
9.7%
Sugar (mg/g)
101.4
84.8 ±70.5
>
p<0.001
119.2
128.5
Starch (mg/g)
3.0
37.8 ±86.8
<
p<0.001
14
9.9
Crude fat
1.8%
6.4% ±8.8
<
p<0.001
10.6%
NA
Energy
Energy (kJ/g dry matter)
16.3
18.2 ±2.8
<
p<0.001
20.4
18.3
Fiber
Neutral Detergent Lignin
32.0%
29.1%
±15.9
=
p = 0.05
38.7%
29.7%
Acid Detergent Fiber (ADF)
8.6%
18.5%
±11.5
<
p<0.001
27.3%
22.2%
Acid Detergent Lignin
0.5%
6.2% ±5.3
<
p<0.001
7.4%
7.6%
Cellulose
8.1%
12.3% ±7.1
<
p<0.001
19.9%
14.6%
Hemicellulose
23.3%
10.6% ±7.0
>
p<0.001
11.4%
7.5%
Anti feedant
Total Phenol
0.4
0.7 ±1.2
=
p = 0.09
0.7
0.5
Total Tannin
0.3
0.6 ±1.2
=
p = 0.32
0.6
0.3
Condensed Tannin
4.5
4.9 ±9.3
=
p = 0.06
8.3
1.2
Table 6 Nutritional values of fruits consumed by bonobos at LuiKotale. Column Dialium and Other fruits show mean
nutritional values or c
oncentration of macronutrients expressed as % of dry matter. Direction of difference indicates >
(higher), < (lower), or = (no difference) revealed by application of the Wilcoxon’s signed-rank test. Nutritional values
of other highly consumed fruits (Cissus dinklagei and Greenwayodendron (Polyalthia) suaveolens) are presented for
comparison.
102
103
Undesired consumer: directed deterrence hypothesis with Tannin
How bonobos deal with tannin-rich fruits. Coprophagy and re-ingestion
technique for Canarium schweinfurthii
David Beaune, Tetsuya Sakamaki, François Bretagnolle, Loïc Bollache,
Gottfried Hohmann & Barbara Fruth
104
Abstract
This note describes the bonobo (Pan paniscus) adaptation to process fruits with high tannin
level. In the direct deterrence hypothesis, tannin should discourage certain seed dispersers. This is
not the case for bonobos that consume and disperse some of these species rich in polyphenol
compound. Apes’s saliva can neutralize tannin and then bonobo chew Parinari and Musanga edible
pulp. Another original adaptation for Canarium schweinfurthii is described. Bonobos of Wamba
and Lomako swallow and crunch the pulp. The LuiKotale community performs a peculiar handling
technique: bonobos ingest the entire fruit. The next day they check their feces, extract the intact
fruit, re-ingest the pulp and spit the seed. We do not know if this treatment 24 hours in the digestive
tract affect polyphenols but this softens the pulp and allows endozoochory. This peculiar
coprophagy could be a cultural behavior not shared with other group (while present at Wamba).
Potentially, bonobo of LuiKotale could use this technique for self-medication with tannin of this
fruit. Furthermore this potential LuiKotale’s handling technique of eating Canarium schweinfurthii
fruits implies learning, transmission and concept of anticipation.
Keywords Zoochory, coprophagy, seed dispersal, anticipation concept, directed deterrence
hypothesis.
Résumé
Cette note décrit l'adaptation des bonobos (Pan paniscus) pour traiter et consommer les fruits
hautement concentrés en tannins. La salive des singes peut neutraliser le tannin des fruits de
Parinari et Musanga, les rendant comestibles par mastication. Une adaptation originale pour
Canarium schweinfurthii est ici décrite. Pour neutraliser les niveaux élevés de tannin de ces fruits,
les humains qui consomment C. schweinfurthii les font bouillir. Tandis que les chimpanzés et les
bonobos de la communauté de Wamba et Lomako rongent la pulpe. La communauté de LuiKotale
exécute une technique de traitement particulière : les bonobos ingèrent le fruit entier. Le jour
suivant ils vérifient leurs fécès, extraient le fruit intact, re-ingérent la pulpe et crachent la graine.
Ceci a pu traiter les composés polyphénolés 24hrs dans le système digestif. Ce comportement de
coprophagie particulier semble être un comportement culturel non partagé avec d'autres groupes.
Les bonobos pourraient potentiellement utiliser cette technique à des fins d’automédication avec les
tannins contenus dans le fruit. En outre, cette technique de consommation complexe des fruits de
Canarium par la communauté de LuiKotale implique l’apprentissage, la transmission et le concept
d'anticipation.
105
Mots-clés Anticipation, coprophagie, dispersion de graine, hypothèse de dissuasion direct,
zoochorie.
106
Introduction
In the seed dispersal effectiveness (SDE) framework, a plant can have several consumers with
different qualities (Schupp, Jordano & Gomez 2010). Plants might be able to ‘choose’ higher-
quality seed dispersal vectors and discourage lower-quality ones. The directed deterrence
hypothesis proposed that fruits’ secondary compounds or chemical defense mediated by plant
secondary metabolites (PSMs) have evolved to discourage damaging vertebrates such as seed
predators while not inhibiting helpful frugivores such as seed dispersers (Cipollini & Levey 1997;
Levey et al. 2006). The secondary chemistry used by plants against animals, such as alkaloids,
various glycosides, and saponins, are potentially toxic to consumers (Johns 1999). Others, such as
lectins, enzymatic inhibitors and tannins reduce digestion and nutrient availability (Robbins et al.
1991). The latter are one of the most well-studied groups and primates seem to have tannin sense
(astringency with textural perception, (Dominy et al. 2001) and avoid food with the polyphenolic
compounds, in both condensed and hydrolysable forms (Oates, Swain & Zantovska 1977; McKey et
al. 1981; Wrangham & Waterman 1981; Glander 1982). However, apes’ saliva contains
‘prolinerich’ proteins, known as tannin-binding salivary proteins. These proteins allows nutrient
assimilation even with tannin presence because of their high affinity with tannin that is neutralised
after binding (Lambert 1998).
In southern bank of the Congo tropical forest the sole apes are bonobos (Pan paniscus) and are
important fruigivores interacting with plants as seed disperser mutualists (Idani 1986; Tsuji,
Yangozene & Sakamaki 2010; Beaune 2012). How do bonobos deal with tannin concentrated fruit?
Does a concentration threshold exist to repulse these fruit consumers?
In this study, we 1) analyse tannin concentrated fruits among fruits of the forest (potential bonobo
food), 2) explore the threshold where bonobo avoid tannin concentrated fruits and 3) describe how
bonobos (Pan paniscus) are adapted to handle the most tannin concentrated fruits of their diet.
Because complex food processing behaviour can imply local knowledge and transmission (Whiten
et al. 1999), we give a preliminary comparison of different bonobo communities and their food
processing within the community. The ongoing long term field site of LuiKotale provides
observations since one decade and allows comparisons with Wamba and Lomako, the two oldest
bonobo field sites.
4) We finally analyse the bonobos’ handling process and its effect on seed dispersal (either neutral,
positive or negative) to test the directed deterrence hypothesis with tannin on bonobos. If bonobos
disperse horizontally the seeds by endo or ectozoochory out of the fruit fall zone, (positive effect on
seed dispersal), we can say that a bonobo is a seed dispersal vector not repulsed by the plant. If
107
bonobos eat the fruit without horizontal seed dispersal (neutral effect) or eat the seed (negative), the
plant fails for the direct deterrence hypothesis to discourage neutral consumers.
Methods
Study sites
All field sites are situated in the Cuvette centrale (DR Congo), south of the Congo River within the
same lowland equatorial rainforest block, that is the home range of Pan paniscus. LuiKotale (LK)
(S2°47’- E20°21’), Lomako (Loma) (N0°51’, E21°5’) and Wamba (W) (N0°11’, E22°37’) are
about 400 km apart each (
Figure 22). All sites receive rain >2000 mm/yr with average temperature
of 24°C. See (Hohmann & Fruth 2003c; Furuichi et al. 2008) for more details. In all sites,
habituated groups of bonobos were daily observed by research teams. Food species overlap is high
across sites (Badrian & Malenky 1984; Kano & Mulavwa 1984; Beaune 2012). We can consider
that these bonobo populations share the same genotype and same ecosystem (Eriksson et al. 2004).
Figure 22 Map of the field sites: LuiKotale (LK) (S2°47’- E20°21’), Lomako (Loma) (N0°51’, E21°5’) and Wamba
(W) (N0°11’, E22°37’), Democratic Republic of the Congo
108
Ethics Statement
The studied apes are free ranging bonobos observed without invasive method, constraint, contact
and any interaction from the researchers. Animal welfare is the top priority beyond scientific
interests. The methods used to collect data in the field are in compliance with the requirements and
guidelines of the ICCN, and adhere to the legal requirements of the host country, the Democratic
Republic of Congo.
Tannins content analysis
Ninety five species of fruit from LuiKotale forest were collected for nutrients analyses (see
(Hohmann et al. 2006b; Hohmann et al. 2010).
Analyses of antifeedants such as phenols and
tannins were carried out at Hamburg University following the protocol described in Hohmann et al.
(2006).
Feeding process
From September 2009 to June 2011 behavioral data of LK bonobos was recorded across 22 months
corresponding to 1879 hrs of observations or 315 days. Bonobos have a fission-fusion society that
is depending on season and time of day the community splits up into smaller foraging subgroups
called parties. As parties are largely cohesive going for the same activities, we considered group
activity to be that of the majority (>50% of the bonobos) of the visible animals during a continuous
record of feeding activities. (i.e. continuous focal sub-group (Altmann 1974). The continuous
record stopped with group loss or out of view (Beaune 2012). We analysed interactions (granivory,
herbivory, frugivory with or without seed dispersal mutualism) for tannin concentrated fruits.
Comparisons with Wamba and Lomako are indicated based on long term observations: Wamba
(TS) and Lomako (GH, BF).
Results
Fruits with high tannin
The average percentage of condensed tannin in dry matter of fruit (100 mg) is 4.9 ±SE.1.3% (CI95%
= [2.1-7.7%]). Four species are outliers with significantly higher levels of condensed tannin in the
flesh than the other fruits (Wilcoxon signed rank) see Figure 23. Autranella congolensis (A.Chev.
& De Wild.) (51%; V=0, P<0.001), Canarium schweinfurthii (Engl.) (30%; V=6, P<0.001),
Musanga cecropioides (R.Br.apud Tedlie) (57%; V=53, P<0.001) and Strombosia glaucescens
(Engl.) (16%; V=58, P<0.001). Another fruit, Parinari excelsa (Sabine) is the highest value of the
range with 12% of condensed tannin in the flesh. A.congolensis fruits are also outliers for total
109
phenol and total tannins with 2.45 and 1.89% respectively. These values are significantly different
from the averages total phenol found in fruits: 0.75±1.17%; CI95% = [0.38-1.12%]; and average total
tannin: 0.55± 1.16%; CI95% = [0.21-0.92%].
110
Figure 23 Condensed tannin (% in dry matter) in fruit. Outliers are Autranella congolensis, Canarium
schweinfurthii, Musanga cecropioides and Strombosia glaucescens. Parinari excelsa is the maximum value of
the range. S. glaucescens fruits are not consumed by bonobos.
Bonobo handling techniques
The following handling processes from LK are based on observations of 992 hrs of feeding
sessions. The feeding techniques for dealing with tannins were observed on Canarium
schweinfurthii, Musanga cecropioides and Parinari excelsia from January 2009 to June 2011
(DB). Autranella congolensis in 2005 (BF). Strombosia glaucescens were not observed and is
not reported as fruit consumed (Kano & Mulavwa 1984). Nevertheless seed consumption was
noticed in Lomako (Badrian & Malenky 1984; Kano & Mulavwa 1984).
Saliva neutralization:
Parinari excelsa: (LK) In June-July 2007 and June-July 2010, 54 feeding sessions were
observed with the bonobos on 27 different P. excelsa trees. To eat the fruit (44 mm ø, N=10),
the bonobos scrape the mesocarp around the seed (35mm ø, N=10) of several fruits and chew
the wadges (
Figure 24) which is then spat out. Bonobos stay under the crown corresponding
to the fruit fall zone. Horizontal seed dispersal is limited comparing to endozoochory, but
111
seeds may be carried at several meters. Apes are not endozoochoric seed disperser of these
trees. Consequently, P. excelsa failed to discourage this primate in the direct deterrence
hypothesis and bonobos are neutral or limited seed dispersers (ectozoochory).
(W): Similar technique (NB: bonobos carry the wadges of the fruits including seeds
sometimes about 100 meters).
(Loma): Similar technique.
Autranella congolensis: (LK) feeding session was not observed since 2005 with the last
fruiting season of these trees (Fruth unpub data). To eat the fruits (7cm ø, n=10), the bonobos
eat the yellow mesocarp around the seed (5.5cm ø, n=10). Chewing behaviour was not
reported during this research season but not excludable. Bonobos stay under the crown
corresponding to the fruit fall zone. Horizontal dispersal of the seeds is extremely limited
when considering dispersal effectiveness. The apes are not endozoochoric seed disperser of
these trees. Consequently, A. congolensis failed to discourage this primate in the direct
deterrence hypothesis and bonobos are neutral/limited seed dispersers.
(W): species absent (Idani et al. 1994)
(Loma): Similar technique.
Musanga cecropioides: (LK): From January 2008 to July 2010, 27 feeding sessions were
observed on 14 different trees. Bonobos ate the young stem, the flower and fruit. Bonobos
chew for several minutes the flat fruit entirely (5-15cm long), that contain thousands of seeds
(<2mm ø, n=10). Wadges were swallowed with viable seeds found in dung or occasionally
spat out (Fowler pers. com.). Swallowing or spitting behavior is probably linked with ripeness
stage of the fruit. The bonobos can be considered as endozoochoric seed disperser for
Musanga trees.
(W): Similar technique
(Loma): Similar technique
Canarium schweinfurthii: (LK): In July 2007, January 2008, April 2009 & 2010 and February
2011, 14 feeding sessions were observed on 10 different trees. Bonobos swallowed the entire
fruits without biting or chewing. The next day, the dung was checked. C. schweinfurthii fruits
were extracted intact from the dung. After this first passage, bonobos bit the pulp, spat out the
seeds and re-ingest the pulp. Independent juvenile bonobos did the same, similarly to all
members of the observed parties. Infants observed the mother when she held and checked her
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own dung. After the second ingestion, the necked seeds of C. schweinfurthii are dropped on
the ground. Through this local behaviour the bonobo is an endozoochoric disperser of C.
schweinfurthii at LK.
(W): Bonobos at Wamba first bite or chew the flesh around the seeds, and then eat the pulp if
ripen or drop it out without eating if unripen. They may taste the astringency first. Therefore
they are not endozoochoric and have limited horizontal dispersal. However the similar
technique described in LK was observed (N=???). This feeding technique is not "customary"
or "habitual" but just "present" in Wamba population (see the terms in (Whiten et al. 2001).
(Loma): Similar to Wamba.
Figure 24 Emile chewing wadges of Parinari excelsia. LuiKotale, DR Congo.
Discussion
The directed deterrence hypothesis
The main dispersers of: Parinari excelsa and Autranella congolensis are elephants (Yumoto
et al. 1995; White & Abernethy 1997); Musanga cecropioides: birds, rodents and primates
(Gautier-Hion et al. 1985), while Canarium schweinfurthii seems to be hornbill dependant
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(White & Abernethy 1997). The tannin of this different fruit species could be discouraging
enough for seed predators and neutral seed disperser as flesh consumers. However, bonobo
adaptability with its apes’ saliva and sophisticated handling behavior can eat the fruit and deal
with chemical defense. In this study, different seed dispersal interactions are described.
Where bonobos avoid Strombosia glaucescens, are ectozoochoric with P. excelsa and A.
congolensis, bonobos are alternative endozoochoric partners with birds, rodents and monkeys
for M. cecropioides or even locally for C. schweinfurthii. Seed dispersal in the fruit fall zone
with seed spiting can be dangerous for seeds such as P. excelsa and A. congolensis, due to
the density dependant effect and predation of both species by bush pigs (Beaune et al. 2012b).
While seeds embedded in feces and dispersed by endozoochory (Musanga cecropioides)
escape seed predators with dung beetles (Beaune et al. 2012a) Because bonobos are efficient
seed dispersers in term of quality and quantity (Tsuji, Yangozene & Sakamaki 2010; Beaune
2012), the population structure of the Canarium from LuiKotale (seed dispersal vectors =
Hornbill + bonobo) could be different than Wamba and Lomako’s population (seed dispersal
vector = Hornbill). For the reason that long dispersal distance and seed dispersal effectiveness
are different between these birds and apes (Whitney et al. 1998; Holbrook, Smith & Hardesty
2002; Poulsen et al. 2002), this should impact populations’ biology and structure of C.
schweinfurthii at LuiKotale, Wamba and Lomako.
The Canarium handling technique
Among 1879 hrs of observation in LuiKotale, other coprophagic behaviours were not
observed within the context of C. schweinfurthii. Nevertheless, exceptional coprophagy
events were observed with juveniles and subadults eating the matrix or picking some Dialium
seeds (Douglas unpub data, similarly reported at Wamba (Sakamaki 2010) and for juvenile
chimps (Krief, Jamart & Hladik 2004). Coprophagy and re-ingestion technique seems to be
specifically used to process fruits of C. schweinfurthii. This peculiar adaptation to high tannin
levels is vivid and original in apes. While humans boil Canarium fruit, to soften the flesh and
maybe neutralize tannins, bonobos process the fruit for 24hrs in the digestive tract. The fruit
still intact could diffuse the antifeedant in the bolus. This uncommon technique was possibly
accidentally learnt from rare coprophagy events occurring in bonobos. Then this technical
acquisition needed to be transmitted to the group. This re-ingestion behaviour could have
emerged in other independent bonobo groups, but is apparently not widespread though
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populations. As demonstrated with the Wamba and Lomako population which does not
process Canarium fruit or exceptionally. Could this technique be cultural?
Another explaination is that condensed tannins have antiseptic, antibacterial, antiviral and
caustic properties (Robbins et al. 1991; Min & Hart 2003). Animal use self-medication
(Huffman 2003). Self-medication with leaf folding was reported in free ranging bonobos
(Dupain et al. 2002). Thus bonobo could possibly use this handling technique to treat
parasites or other self-medication with tannin. In the Canarium case, bonobos swallow the
pill that unfolds its phytochemical properties where they may be required in the intestines.
Further investigation are required.
Nevertheless the simplest explanation is that bonobos found an original handling technique to
process difficult food. Without tools, bonobo can deal with indigestible food. This processing
has neither been described in chimpanzee (Pan troglodytes) nor in other primates.
Furthermore, cognitive function of prospection seems to be involved. The bonobos have to
anticipate a food that they will eat without direct digestion but delayed. This undigested food
encumbers the bolus and is a clear trade-off (i.e. bad meal today for a better tomorrow). With
prospective ability, they should ‘remember’ the next day to check the feces containing
appetizing food from the day before. This holding process of Canarium fruits is the first case
described in Pan paniscus.
115
Example of application in plant conservation
116
Artificial germination activation of Dialium corbisieri by imitation of
ecological process
David Beaune, Loïc Bollache, Musuyu D. Muganza, François Bretagnolle,
Gottfried Hohmann & Barbara Fruth
Submitted to the Journal of Sustainable Forestry
117
Abstract
Species of the genus Dialium commonly are trees found in Central African rainforests.
They produce tasty sugary fruits, feeding numerous frugivores, but are despite their valuable
nutritional value, rarely exploited by humans. Potential reason for this could be the
complexity of symbiotic dependence between trees and pollinators, germination activators,
and dispersers causing problems in ancestral and contemporary domestication. We
investigated Dialium corbisieri (Staner-1932) reproduction in DRCongo, Bandundu province.
Here we give a key for an artificial activation of germination of these trees ecologically
adapted to the digestive system of their ape dispersers: by perforation of the impermeable
seed coat protection water assimilation and subsequent activation of germination becomes
possible. By this nicking pretreatment germination increases from 0 to 96%, representing an
inexpensive and simple treatment to be used under natural conditions and in developing
countries. The use of this mechanical activation for forest management, conservation and
economical use is discussed.
Keywords Dialium corbisieri, African velvet tamarind, seed pre-treatment, germination
activation, seed dormancy, endozoochory, domestication.
Résumé
Les espèces du genre Dialium sont généralement des arbres trouvés dans les forêts tropicales
humides d’Afrique centrale. Ces arbres produisent des fruits sucrés savoureux, qui nourrissent
de nombreux frugivores. Mais en dépit de leur importante valeur nutritive, ces espèces sont
marginalement exploitées par des humains. La raison potentielle pourrait être la complexité de
la dépendance entre les arbres et leurs pollinisateurs, leurs disperseurs de graine et activateurs
de germination. Ceci posant des problèmes pour la domestication passée et contemporaine de
ces arbres fruitiers. Nous avons ici étudié la reproduction de Dialium corbisieri (Staner-1932)
en RD Congo, province de Bandundu. Ici nous donnons une clef pour l’activation artificielle
de la germination de ces arbres écologiquement adaptés au système digestif des grands singes,
leur vecteur de dissémination : la perforation du manteau tégumentaire imperméable permet
l’absorption d’eau et l'activation de la germination qui devient possible. Ce traitement par
scarification augmente le taux de germination de 0 à 96%. Ce traitement est peu coûteux et
simple d’utilisation dans des conditions de terrains et dans les pays en voie de développement.
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L'utilisation de cette activation mécanique pour la gestion des forêts, la conservation et un
usage économique de l’espèce est discutée.
Mots clefs Activation de la germination, Dialium corbisieri, domestication, dormance
tégumentaire, endozoochorie, prétraitement de graines, tamarin africain.
119
Introduction
T
The family of the Leguminosae got an important ecological role in forests with their
ability to directly absorb atmospheric azotes (N
2
) and to release it for the rest of the ecosystem
(Roggy & Prevost 1999). Of particular interest are Dialium species belonging to the sub
family of Caesalpinioidae. They dominate parts of the tropical evergreen lowland rainforests
of the Central Congo Basin, DRC. Species of this gender are medium sized to very tall trees
(up to 40 meters) with a very hard wood, highly valued in timber, and fruit providing an
edible pulp (Janick & Paull 2008), p. 391). Some of them are considered of particular interest
for their mono-lobed fruit consisting of a slightly flattened seed protected by a hard endocarp,
imbedded into a pithy and luscious sweetly sour edible mesocarp and enclosed by a black-
brown velvety, thin and brittle exocarp (capsule). Fruits stand erect at the end of branches and
ripen over an extended period of the year, usually coinciding with dry seasons. Availability of
fruit has been reported between February and May for Nigeria and, between November and
July for Gabon (White & Abernethy 1997). These fruits are important for a lot of frugivorous
species in rain-forest biocenoses and we can observe a strong interaction between plants and
animals (Beaune, unpubl. data). To attract animals as seed dispersers, angiosperm fruit
coevolved with fruit-predators adapting to the taste and digestive system of their partners
(Thompson 1991; Jordano 1995). Partners include birds, ungulates, monkeys and great apes
including Bonobo (Pan paniscus) (Hohmann et al. 2006b) ; Beaune et al., in prep),
Chimpanzee (Pan troglodytes) and Gorilla (Gorilla gorilla) (Kuroda et al. 1996; White &
Abernethy 1997). Dialium seeds are adapted to endozoochory by their strong endocarp (i.e.
seed coat dormancy) in order to survive through the frugivorous’ gut passage. This potentially
avoids or inhibits the ability to self germinate and thus may be considered as displaying
dependency to endozoochory.
Dialium fruit are not only of importance to forest dwelling animals, particularly non-human
primates, but also to humans. Particularly Dialium guineense, known in Africa as Black
Velvet Tamarind, is used by people in West and Central Africa. Fruit is popular and traded in
Benin and of regular use in Nigeria (Arogba, Ajiboro & Odukwe 1994). It is known to contain
high levels of Vitamin C, sugars, essential oils and other nutritive components (Achoba et al.
1993; Arogba, Ajiboro & Odukwe 1994; Ude et al. 2002; Onwuka & Nwokorie 2006; Essien
et al. 2007).
However traditional use of Dialium fruits across Africa is not widespread, and attempts to
enhance cultivation or incite industrialisation so far was constrained by their ecology. In
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addition, certain Dialium species are at risk by habitat loss and registered on the IUCN red list
as follows: D. bipindense (lower risk/near threatened); D. cochinchinense (lower risk/near
threatened); D. excelsum (endangered); D. holtzii (vulnerable); D. lopense (lower risk/near
threatened); D. orientale (lower risk/near threatened); D. travancoricum (critically
endangered) (IUCN 2010). An increasing risk that has been so far underestimated is the loss
of seed dispersers. Commercial hunting and the bush meat trade cause a considerable decline
in seed dispersers. Overhunted forests, stigmatized by the empty forest syndrome, become
disturbed in the reproduction and dynamic of their current vegetation (Terborgh et al. 2008).
To conserve and support Dialium progeny therefore is not only of interest for the purpose of
agriculture but also for the purpose of habitat conservation.
In this study, we propose an artificial activation of the Dialium corbisieri seeds, with
regard to the natural activation in great apes, trying to mechanically replace what is
chemically happening in the apes’ digestive tract. Dialium seeds recovered from apes’ dung
are either intact or swollen and show coat removal. The major hypothesis is that strong seed
protection (i.e. endocarp or seed coat dormancy) is perforated by mechanical or chemical
digestive processes. Consequently, seeds become porous and absorb water. Previous studies
tried different chemical (Razanamandranto et al. 2004; Tanaka-Oda, Kenzo & Fukuda 2009)
or chemical as well as mechanical methods (Todd-Bockarie & Duryea 1993; Sozzi & Chiesa
1995; Razanamandranto et al. 2004; Vari et al. 2007; Nwaoguala & Osaigbovo 2009; Tanaka-
Oda, Kenzo & Fukuda 2009). Both sulphuric acid bath (H
2
SO
4
) and nicking of seeds appear
to be the most effective pre-treatments. However, the chemical effects seem to be similar to
the mechanical treatment in that they cause perforation of the seed coat tissue improving
water absorption by the embryo. While chemical incitement is expensive, dangerous and
needs peculiar equipment for usage in nurseries (Todd-Bockarie & Duryea 1993; Olufunke &
Gbadamosi 2009), mechanical treatments are simple, harmless and available to all.
Here we apply a mechanical treatment as a simple and cheap way to test the potential of
Dialium reproduction in artificial nurseries as replicable procedure for countries containing
tropical rainforests.
Material and methods
Study area
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The study was carried out from April to May 2009 within the LuiKotale research site
(S2°47’- E20°21’), located within the equatorial rainforest, south-west of Salonga national
park (Figure 1), Bandundu Province, Democratic Republic of Congo (Hohmann & Fruth
2003c). The climate is equatorial with abundant rainfall (2016 mm for the year 2008; 448 for
April and May 2009) and a relatively dry season from February to July. Mean temperature at
LuiKotale ranges between 21°C to 28°C with a minimum of 17°C and a maximum of 38°C
(n=360 days for 2008). For April and May the range was 21°C to 29.3°C with a minimum of
20°C and a maximum of 33°C.
Sample collection an measurements
We used one species only: Dialium corbisieri. For genetic similarity, fruits were collected
from the same branch at 25m height. Collection was done the 8
th
of April 2009 when seeds
were fully ripe. Entire fruit were taken back to Lui Kotale camp field laboratory where they
were manually opened by breaking the brittle exocarp. Seeds were isolated by manually
removing the mesocarp. Seeds were separated into three groups (see below) to undergo a
different treatment each. Seed transformation was measured before and after 48h of
immersion in water (see below) in order to test the coat permeability and potential water
assimilation. For this, seed weight was taken in mg using an electronic balance (KERN-
Taschenwaage 0-300mg ± 10μg), seed diameters (length and breadth) were taken in mm
using slide calliper (0-10cm ± 1μm).
Groups of seed treatment for activation and monitoring of artificial germination
Group 1: Artificial seed coat perforation: In accordance to the seed enhancement technique
(Taylor et al. 2008) seed protection was interrupted in 92 seeds by scratching with a knife a
piece of endocarp (< 1mm) until the endosperm appeared. These nicked seeds were immersed
in rain water for 48h;
Group 2: Intact seed coats: A total of 92 seeds were left with intact endocarp. These intact
seeds were immersed in rain water for 48h and served as control for Pw;
Group 3: A total of 100 seeds neither underwent mechanical treatment nor was it immersed in
rain water. These seeds were considered being similar to dropped seeds in natura such as
seeds spread by ectozoochory of monkeys (pers. obs.) and served as overall control group.
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All seeds were randomly positioned on a sieve with absorbent paper. For distinction
between treatments, each seed was flagged with a bamboo stick next to it. Sieves were kept
under the canopy with a grid protection against predators, under in situ climatic conditions.
Every day at 6:00 hours, all seeds were monitored in order to detect the emergence of the
radicle and subsequently hydrated with rain water. Radicle emergence was used rather than
flushing of the cotyledons because radicle emergence is considered to be the first sign of
germination and thus demonstrates viability of seeds (Heß 1999; Knogge, Herrera &
Heymann 2003).
Statistical analysis
After testing the data’s normality (Shapiro-Wilk normality test), parametric data of the size
and weight were tested by Student’s t-test. Germination rate between groups were compared
using Binomial test. The power analysis of the tests is specified when a difference is detected.
Analyses were performed using R 2.11R (R Development Core Team, 2005) was used for
statistical analysis.
Results
Seed transformation
Already after the first hours of immersion, all perforated seeds started to swell. Figure 25a-c
shows weight and size dimensions of perforated (n=92) and intact seeds (n=92) before and
after 48hours of immersion in rain water.
In terms of weight, perforated seeds were on average twice (× 2.21) as heavy as were intact
seeds of the control group. While they weighed 0.27mg±se. 0.01mg on average before, they
weighed 0.59mg± 0.01mg on average after immersion, resulting in a highly significant
difference (Fig1a: t-test: t = -31, df = 112, p<0.001. power analysis=100%).
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Figure 25 Seeds transformation of intact (left) versus perforated seed coat (right), after 48h of immersion in
water. (a): Weight ; (b): Length ; (c): Breadth.
In terms of size, perforated seeds were significantly larger than intact seeds of the control
group: This was reflected by increase in length by 1.35 times of perforated seeds in
comparison to intact seeds. While length measured 10.28mm± 0.09mm on average before,
they measured 13.93mm± 0.09mm on average after immersion (
Figure 25b: t-test: t = -28, df
= 132, p<0.001. power analysis=100%) as well as by increase in breadth by 1.39 times
between these two groups of seed treatment. While breadth measured 4.02mm± 0.06mm on
average before, they weighed 5.63mm± 0.07mm on average after immersion (Fig 1c: t-test: t
= -17, df = 128, p<0.001. power analysis=100%).
In summary, all 92 perforated seeds were swollen after 60 hours, there was neither an
effect on intact seeds immerged for 48hours in rain water as shown by the control group nor
was there any measurable effect on the overall control group without any treatment. (weight: t
= -0.7, df = 132, p-value = 0.5; length (t = 1.5, df = 132, p-value = 0.1); breadth: t = 0.2, df =
128, p-value = 0.9).
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0
20
40
60
80
100
1 6 11 16 21 26 31
Time (d)
% of germination
perforated (n=92)
intact (92)
control (100)
Figure 26 Germination in relation to time in Dialium corbisieri according to treatment (perforated seed coat).
Artificial germination activation
Figure 26 shows the results of the monitoring of radicle emergence in 284 seeds divided
according to the treatments described above, into three test-groups, Perforated (n=92), Intact
(n=92) and Control (n=100). After 24h in nursery, 27% of the treated seeds showed
appearance of their radicle. After four days 96% of the perforated seeds germinated whereas
all other seeds did not. The proportion of germinated perforated seed is significantly different
since the first day (p<0.001).
Discussion
As shown in our results, only Dialium seeds with seed coat perforation were able to swell and
germinate. These results may illustrate a clear adaptation of the seed coat impermeable to rain
water on endozoochory. By coat perforation the seeds absorb water and the germination rate
is triggered by 0 to 96%. Dialium corbisieri recruitment shows dependence of seeds passing a
partners’gut to be not condemned to everlasting dormancy in the forest (Beaune et al., in
prep). In the absence of natural seed dispersers, seed dormancy can be broken by imitation of
125
the natural process, allowing the seed to absorb water, to swell and activate germination. This
is what happens with endozoochoric partners as apes: the digestive acid nicks the coat and
induces germination. Seeds found in bonobo dung are similar in size and shape to
transformed seeds as obtained by artificial seed coat perforation and water immersion (Pw)
(pers. obs). However not all frugivores can act as partner for this effect. Cheek pouch
monkeys such as crested black mangabeys (Lophocebus aterrimus) spit the Dialium seeds
apparently unharmed onto the ground (pers. obs). Teeth may scratch the coat, but whether or
not this is enough to induce water absorption needs to be investigated by focusing on seeds
dispersed by ectozoochoric partners. In addition, transit time across the dispersers’ gut
passage may effect perforation. While bonobo’s gut passage time appears to be appropriate,
we do not know if the transit time of birds or bats is long enough to perforate Dialium seed
coats. Moreover, the question remains, whether or not after spiting the seed on the ground,
the ambient moisture absorption (versus: digestive bath) is rapid enough to avoid pathogens
infection of the dormant seeds. Indeed, fast germination can help to skip seed predators and
start the race against seedling pathogens.
This result is a good example for application of ecological processes to ecological and
economical management. Pretreatment for tree breeding of Dialium species could be of use
for both the a) restoration and conservation of natural forests and the b) potential for future
nutritional use.
Restoration and conservation
Tree nurseries are used for forest restoration and conservation (Dumroese & Riley 2009). In
the restoration of forest impacted by logging, or other ecological catastrophes, fruiting trees
are important resources for maintaining or restoring frugivorous populations such as primates,
birds, or bats (Dew & Boubli 2005) that consequently, may regain their keystone role in the
ecosystem (Terborgh 1986). However in a disturbed system, natural colonisation of these
dependant trees could be difficult if populations of animal partners have decreased or partners
are already exterminated (Chapman 1995; Chapman & Onderdonk 1998b). Human
interventions may be the last solution with Dialium nurseries becoming now possible with
this artificial method for the breeding of shoots.
Potential for future nutritional use
Focusing on the larger environments of our study site, indigenous people of the Bolongo area
in Bandundu province, south West of the Salonga National Park in DRC, have a profound
126
knowledge of the trees species of their surroundings. Among 56 local people asked during
visits to adjacent villages, all knew the “Maku” which is the vernacular name for all Dialium
trees. The majority of these people distinguishes between two ethnospecies “Maku rouge”
and “Maku pembe”, comprising seven species taxonomically described for Lui Kotale study
area (Fruth et al. unpubl. data): the “Maku rouge” (Dialium corbisieri and D. zenkeri) and
“Maku pembe” (D. gossweileri, D. kasaiense, D. pachyphyllum, D.angolensis, D. tessmannii)
with reddish and clear bark respectively. With their large naturalist knowledge, “Maku rouge”
stays for the consumption of caterpillars feeding on Dialium leaves, as well as for the use of
wood in construction or treesap in medicine, fruits of “Maku rouge”, however, despite their
highly nutritive value, are not on their menu. In our study area this lack of consumption of
Dialium fruit by local people, can be easily explained by the availability of fruits of other
species that are much easier to access. In contrast, explanations may differ for areas where
Dialium is part of the human diet such as in Benin. Here, the symbiotic dependence between
tree and dispersers, which is a barrier for domestication, may explain the difficulty of this
fruit becoming a diet widespread among people inhabiting tropical zones of subsaharian
Africa. The system, however, is even more complex: In addition to great apes and dung
beetles as dispersers (Beaune et al. in prep.), Dialium trees are highly symbiotic with a lot of
partners such as nitrogen fixing bacteria for nitrogen absorption, insects for pollination (Kato
et al. 2008), or apes for germination activation. All these dependences could be an obstacle
for domestication.
There are two potential ways to successfully domesticate plants: either randomly by trial
and error of seed recruitment or by detailed understanding of the complex ecological
processes such as shown for Ficus requesting a specific wasp for pollination (Murray 1985)
and specific manipulations for horticulture thereafter (Kjellberg & Valdeyron 1984).
This example may show the high ecological interdependence of rainforest-species and the
problem of domestication of species in these areas despite their great potential for nutritional
or economic use. Increase in overall population size of homo sapiens and the related
challenge to face nutritional requirements for all, asks for the domestication of new plants by
help of modern agriculture paired with scientific knowledge.. As we have shown here, the
problem of the activation of germination of Dialium seeds can be overcome artificially. Will
we find the luscious Dialium fruit in our organic supermarket from the African agriculture in
50 years?
127
Part II
128
Long-distance dispersal
129
Can fruit traits control the distance that animals move seeds during
dispersal?
David Beaune, François Bretagnolle, Loïc Bollache
& Barbara Fruth
Submitted to Behaviour
130
Abstract
In an Afrotropical forest, the test hypothesis was that fleshy-fruited plants with interspecific
difference in fruit quality affect the behaviour of their seed dispersers, thus affecting seed
dispersal distance. From 2007 to 2011, an extensive movement survey was conducted on an
important and common seed disperser in Congo forests: the bonobo (Pan paniscus), with GPS
georeferencing daily movements. Transit times were calculated; dispersal distance was
estimated, using 1200 georeferenced dispersal events, and results were compared for species,
seasons and years (ANOVA). An exact mechanistic model compared dissemination for eight
plant species dispersed by bonobo through its ranging behaviour; the only variant factor being
the fruiting species. We tested the trade-off for plants: attracting dispersers by means of fruit
quality/quantity versus retaining them in the patch because of the same quality/quantity value
that attracted them. Transit time (mean ± SE) is similar among species (24h00 ±00min).
Dispersal distance is not affected by year, season or species trait. Although a difference exist
for the average feeding time spent per fruiting species, and for the fruit nutrient contents, they
are no relation time spends on the feeding patch and the dispersal distance that that follow.
The average bonobo dispersal distance is (1332 ± 24 m). Feeding time invested in the patch,
fruit quality and abundance had no apparent effect on bonobo ranging behaviour and therefore
did not affect dispersal distance.
Keywords African forest, bonobo, Congo Basin, forest structure, long-distance dispersal,
mutualism, Pan paniscus, seed dispersal, tropical rain forest, zoochory
Résumé
Dans une forêt Afrotropical humide, l'hypothèse testée est que les plantes à fruit avec leurs
différences interspécifiques en qualité et quantité affectent différentiellement leur partenaire
animal disperseur de graines. Ce qui aurait un impact sur la distance de dispersion. De 2007 à
2011, une analyse des mouvements quotidiens et géoréferencés (GPS) a été conduit sur un
disperseur important et commun de graines dans une forêt du Congo : le bonobo (Pan
paniscus). Les temps de passage ont été calculés; la distance de dispersion a été estimée
empiriquement et par modélisation de 1200 événements de dispersion géoréferencés, et des
résultats ont été comparés entre espèces de plantes à fruits, entre les saisons et les années
(ANOVA). Un modèle mécanistique exact a comparé les distances de dispersion de huit
131
espèces de plantes dispersées par les bonobos : le seul facteur variable étant l'espèce fruitière.
Nous avons examiné le compromis évolutif pour ces plantes à fruits : attirer des disperseurs
au moyen de fruit qualitativement et quantitativement coûteux sans les retenir à proximité
pour permettre la dispersion de leurs graines à bonne distance. Le temps de passage (moyen
±ES) est similaire entre les espèces (24h00 ±00min). La distance de dispersion n'est pas
affectée par les variables années, saisonnalité ou espèce. Bien qu'une différence existe
pendant le temps d'alimentation moyen passé par espèce fruitière, et pour le contenu nutritif
des fruits, ceci ne semble pas affecter la distance parcourue après nourrissage et donc la
distance de dispersion des graines. La distance moyenne de dispersion des graines
transportées par les bonobos est (1332 ± 24 m). Les temps d’alimentation, la qualité et la
quantité des n'ont eu aucun effet apparent sur le comportement de déplacement des bonobos et
n'ont donc pas affecté la distance de dispersion des graines de ces espèces.
Mots clefs Bassin du Congo, bonobo, dispersion de graine, distance de dispersion, forêt
tropicale humide, mutualism, structure forestière, Pan paniscus, zoochory
132
Introduction
The spatial pattern of seed deposition such as dispersal distance is an aspect of dispersal
ecology that have theoretically major consequences on several aspects of plant population
dynamics as well as on plant community structure and dynamics (Jordano 1995; Levin et al.
2003; Howe & Miriti 2004; Schupp, Jordano & Gomez 2010). However experimental data
that quantify real dispersal patterns are scarce, particularly concerning forest species those are
dispersed through endozoochory (Clark et al. 2005; Russo, Portnoy & Augspurger 2006;
McConkey & Chivers 2007; Cousens et al. 2010). For zoochoric plants, the spatial
distribution of seed deposition (i.e. seed shadows, (Willson 1993) results from the movement
and behaviour of animals that feed on the fruit and transport the seeds (Westcott et al. 2005).
Frugivores can shape plant populations in numerous interactive ways such as spatial
configuration of fruiting plants, foraging decisions and the characteristics of the disperser
(Jordano et al. 2007; Spiegel & Nathan 2007; Carlo & Morales 2008). The behaviour of
dispersers after feeding on a fruiting parent plant will influences the shape of the probability
distribution of dispersal distance because it will depends on how far the disperser moves away
from the source while retaining the seeds (Westcott et al. 2005; Russo, Portnoy & Augspurger
2006; Cousens et al. 2010). The gut transit time of the seed is another parameter that could
potentially affect the probability distribution of dispersal and very few studies showed that
this parameter could be affected by seed size and chemical components of the fruit that can
increase or decrease seed transport time (Westcott et al. 2005). The seed dispersal distances
for animals with short gut passage time, such as birds is related to the time spent in fruiting
trees (Lenz et al. 2010). The quantity and the quality of fruits produced by a plant as well as
the level of aggregation of the fruiting plants in a landscape can also affect the probability
distribution of seed dispersal (Carlo & Morales 2008). If the food patch can sustain the
dispersers for a time superior to the transit time, or if the dispersers frequently come back to
the patch, and remain in its vicinity, the amount of seed transported could be high although
with low dispersal distance. For example, orang-utans can select large fruiting trees that they
repeatedly visit staying around between feeding bouts (Leighton 1993).
Large and medium frugivores, such as elephants or apes disperse numerous plant species
(Campos-Arceiz & Blake 2011; Forget et al. 2011). In Congo rainforest, bonobo (Pan
paniscus Schwarz) are efficient seed dispersers that transport seeds of several fruiting species
by endozoochory (Idani 1986; Tsuji, Yangozene & Sakamaki 2010). Bonobo in particular
have a long gut passage and are wide-ranging animals that forage many fruiting plants during
133
a day although being sometimes able to stay around a big fruiting plant or frequently come
back to this patch (own observations).
The hypothesis of the present paper is that plant species with different fruit production
strategies can affect their disperser behaviour and, consequently, their seed dispersal distance.
Fruiting trees that produce large quantities and/or highly nutritive fruit could attract but
maintain the disperser in place, resulting in lower seed dispersal distance. Conversely, trees
with limited fruit production could perform in higher dispersal distance although being less
attractive.
To test this hypothesis, we first analyzed whether bonobos exhibit variation in the times they
spend in fruiting trees. Hence, we compared the difference in fruit quality and quantity
provided by the fruiting species with analyse of the fruit nutrient composition, traits and the
average feeding duration of the bonobo groups in the fruiting species. Secondly a mechanistic
estimation of seed dispersal incorporating transit time for seed and the empirical movement
behaviour of a common disperser for several zoochoric plant species is developed here. Many
tropical plants have evolved fleshy fruit that are attractive to only a limited subset of
frugivores (Fleming 1979). Afrotropical forest frugivores use different canopy strata with low
feeding overlap (Fleming 1979; Clark, Poulsen & Parker 2001b; Poulsen et al. 2002).
Consequently, in certain rainforest of the Congo, bonobo can be considered as main seed
disperser for specifics fruiting species selected here, but alternative dispersers among birds,
rodents and other primates cannot be excludable.
The long-term project of LuiKotale with a habituated bonobo group which can be daily
observed, identified, followed and georefenced allowed us to build empirical seed dispersal
estimation. We compared dispersal distances for several tree species with different species
traits and fruit production strategies (see Table 1). Those dispersal distances can be used to
test whether plants affect frugivore ranging behaviour and thus control their zoochoric
partners for seed dispersal distance.
Study species and site
Pan paniscus is restricted to the tropical rain forest of the Democratic Republic of Congo
(DRC) on the southern bank of the Congo River. The bonobo is mainly frugivores, feeding on
and disseminating hundreds of plant species (Beaune unpubl. data; Tutji et al. 2010). Around
134
40% of the tree species in the forest are dispersed by bonobos (Beaune unpubl. data).
Bonobos live in matriarchal groups with fission of subunit groups (parties) during the day
while foraging, and fusion in the nesting place before night (Fruth & Hohmann 1993). In the
Congo Basin, at the south-west fringe of the Salonga National Park, there is a habituated
group of free-ranging bonobos, tracked by research teams at the LuiKotale field site (LK)
(Hohmann & Fruth 2003c). Since 2007, groups have been followed from nest to nest and
daily travels are georefenced with GPS (Garmin
®
60CSX) using one point position per 5 min.
Bonobo feeding trees are georefenced when identified during group feeding sessions. The
most abundant fruiting species eaten by bonobo (allowing normality with sufficient sample
size) were selected and compared (i.e. eight species with dispersal events recorded >30).
Figure 27 Illustration of the mechanistic seed dispersal estimation with an example of dispersal event
(Gambeya lacourtiana). Identified bonobo feeding trees are georeferenced during group observations
(2007-2011) and bonobo movement daily recorded (dark track log). Theoretical seed deposition site
are determined by actual bonobo position (dark track log) after 24 h corresponding to the seed transit
time.
135
Methods
Variation in feeding time session
Feeding duration were estimated by direct observation of the LK bonobo group. From
September 2009 to June 2011 behavioral data of bonobos were recorded for 315 days across
22 months of observations. Bonobos are a fission-fusion society that is depending on season
and time of day the community splits up into smaller foraging subgroups called parties. As
parties are largely cohesive going for the same activities, we considered group activity to be
that of the majority of the visible animals during a continuous behavioural records. A total of
573 hours of feeding session with fruiting species was analysed. Among these feeding
sessions, the potential correlation of 278 dispersal events linked with feeding duration from
22 different fruiting species was analysed.
Interspecific fruit differences
Fleshy-fruited plant species are different in fruit production and quality (Hohmann et al.
2006b; Hohmann et al. 2010). The aim of this study is to test whether fruit production and
quality affect the probability of seed dispersal distance. We have contrasted medium-sized
tree species with relatively low fruit production (i.e. Polyalthia suavoelens, Placodiscus
paniculatus) and large-sized fruiting trees which support and maintain dispersers for longer
periods (i.e. Dialium corbisieri, Gambeya lacourtiana). To estimate the mean fruit abundance
of each selected species we have calculated the diameter at breast height (dbh) (Chapman et
al. 1992). The mean dbh was calculated for the main species, based on a 12-ha plot inventory
(Beaune et al. In press). One liana, Cissus dinklagei, was added to the test and compared with
the seven tree species, for a total of eight species analysed. Fruits from LK forest were
collected for nutrient analyses (Hohmann et al. 2006b; Hohmann et al. 2010). Average fruit
mass and diameter were measured on at least ten mature fruits.
Dispersal analysis
The probability distribution of seeds is based on empirical bonobo movements (
Figure 27),
georeferenced since 2007. Mean transit time (Tt) was calculated by continuously observing
individually identified bonobos from the moment they swallowed seeds of a new species (not
previously ingested in the past 36 h), until seed deposition in feces. Theoretical dispersal
136
distance is taken to be the distance between the parent tree on which the bonobo fed and the
bonobo’s position after mean transit time (Tt). Effect of sex and seed size (categorized as: (1)
small <2 mm, (2) large >1 cm and (3) medium (2-10 mm) on Tt were tested with analysis of
variance (ANOVA) using R (R Development Core Team 2011), with all the effects
considered as fixed. Distances of dispersal with annual, seasonal and species effects were also
tested with ANOVA, with all the effects considered as fixed.
Familly
Species
average feeding
session (min) n
Energie
kJ/g dry
matter
Protein
mg/g
Sugar
mg/g
mean fruit
weight (g)
mean fruit
diameter
(mm)
average DBH (cm)
n
Annonaceae
Polyalthia
suaveolens
16 ± 3
75
18.3
96.9
128.5
3.2 ± 0.2
19.4 ± 0.7
18.3± 0.4
408
Caesalpiniaceae
Dialium sp
47 ± 3
230
16.3
145.7
101.4
0.9 ± 0.1
22.2 ± 0.5
31.3± 1.1
761
Moraceae
Treculia
africana
78 ± 19
16
19.8
106.9
17.3
>8000
>800
37± 0
1
Sapindaceae
Pancovia
laurentii
27 ± 5
58
14.6
65.5
160.3
15.1 ± 1.2
29.0 ± 1.3
26.7± 1.5
31
Sapindaceae
Placodiscus
paniculatus
46
1
16.4
125.9
101.6
2.4 ± 0.1
17.3 ± 0.5
16.7± 0.5
104
Sapotaceae
Gambeya
lacourtiana
16 ± 2
81
-
-
-
207.1 ± 28.6
70.7 ± 3.7
96.3±
34.2
4
Tiliaceae
Grewia sp
27 ± 2
89
18.9
80.2
172.4
9.2 ± 0.3
32.9 ± 0.4
22.6± 1.6
50
Vitaceae
Cissus
dinklagei
22 ± 1
204
20.4
106.2
119.2
8.3 ± 0.5
26.5 ± 0.6
-
-
Table 7 Main plant species characteristics for feeding ecology (seven tree species, one liana: Cissus dinklagei).
Average diameter at breast high (dbh) based on 12-ha plots inventory; average foraging session time based on
1879 h of field observation, average fruit weight and largest diameter (n = 10) and mean nutritional value.
Values are mean ± SE
Results
Table 7 reports differences in nutritional values, fruit size, weight and dbh for adult trees, and
mean feeding duration in fruiting species. There are no correlation between the feeding time
spent on a fruiting plant and the dispersal distance infered by the bonobo ranging behaviour
(
Figure 28).
137
22 fruiting species
R
2
= 0.0051
0
500
1000
1500
2000
2500
3000
3500
4000
4500
0:00 1:00 2:00 3:00
Feeding duration (h)
Dispersal distance (m)
R
2
= 0.0003
0
500
1000
1500
2000
2500
3000
3500
4000
4500
0:00 1:00 2:00 3:00
Feeding duration (h)
Dispersal distance (m)
Dialium sp
138
R
2
= 0.0521
0
500
1000
1500
2000
2500
3000
3500
0:00 0:30 1:00 1:30
Feeding duration (h)
Dispersal distance (m)
Cissus dinklagei
Figure 28 There is no correlation between feeding time spent on the fruiting plant and the dispersal distance by
bonobo. For 22 fruiting species analysed as whole (n=278) or other species as Dialium sp. (122) or Cissus
dinklagei (50).
Transit time: 124 transit times (from 13 different genera) from seed ingestion to deposition
were recorded, with continuous observation of the dispersers. Mean transit time is 24:00hrs
±SE. 00:09hrs (SD=01:20h; range = 20:03-28:17h). There was no significant effect of seed
size (Figure 29; n=61 big, 28 medium, 35 small; F
2,119
= 0.38; P = 0.68) or bonobos’ sex
effect (t = 0.0253, df = 15.3, P = 0.98) on transit time.
139
Figure 29 Size effect on the transit time (35 small:<2mm, 28 medium-sized:2-10mm and 61 large
seeds:>10mm). No significant effect (F
2,119
= 0.38, P = 0.68). Mean Transit time = 24:00 h.
Based on 1200 bonobo travel distances from the 8
th
July 2007 to 22
nd
September 2011, the
dispersal curve fitted a unimodal leptokurtic distribution (
Figure 30). The average dispersal
distance is: 1332 ± 24 m, median= 1198; CI
95%
= 1282-1380 m; range = 1-4492 m. This
estimation is not significantly different to the actual estimation based on 75 actual seed
dispersal events observed (t = -1.4442, df = 1273, P = 0.1489). Annual (F
4,1195
= 1.87; P =
0.248) and seasonal effects (F
10,1189
= 1.24; P = 0.26) are not significant. The main species
tested (height fruiting species; 890 dispersal events), from large G. lacourtiana to medium
tree species (P. paniculatus, P. suaveolens) (see Table 7 for average dbh) do not significantly
affect the dispersal distance by the bonobo (F
7,882
= 0.77; P = 0.61.
Figure 31). The hypothesis
on interspecific difference in seed dispersal distance is rejected.
140
Figure 30 Seed dispersal distribution infered by bonobo based on movement behavior (n = 1200 dispersal events
with all plant species) and mean transit time for seed (24:00 h).
141
Figure 31 Seed dispersal distances infered by bonobos for eight plant species. (Cissus dinklagei, Dialium sp.,
Gambeya lacourtiana, Grewia sp., Pancovia laurentii, Placodiscus paniculatus, Polyalthia suaveolens, Treculia
africana).
Discussion
Our findings provide the first analysis based on long-term data, of differences in dispersal
distance among fleshy-fruited plants disseminated by the same endozoochoric partner.
Surprisingly, all the fleshy-fruited species are dispersed at the same average distance,
whatever the feeding time on the fruiting plant, their fruit quality and abundance: 1.3 km.
Bonobos move at homogenous and regular distances from food patches. This is due to the
regular ranging behaviour and consistent travel times of bonobo groups, whatever the year,
season or fruiting season. One potential explanation is the stochastic phenology of fruiting
species at the site (Fruth et al. unpubl. data). This unpredictability could force bonobos to
forage permanently for food and then regularly disperse the seeds at long distances. Another
unverified hypothesis is differential ripening for these species. With asynchrony in ripe fruit
availability, frugivores cannot forage for long sessions in the same area. However, further
studies are needed on differential ripening in tropical plants. Surprisingly in our study, seed
size does not seem to affect transit time, unlike in other animals, where a shorter gut passage
142
is induced by smaller seed size (Westcott et al. 2005). Bonobo physiology and foraging
behaviour result in similar dispersal distances for disseminated plants whatever their
differences in size, colour, fruit quality and quantity or species traits.
Extensive seed dispersal among communities homogenises species composition, and
eventually makes competitive ability dependent on global rather than local abundances, thus
facilitating domination by the single most abundant species (Levin et al. 2003). This study
tends to confirm that finding. Seed dispersal limitation in distance (Muller-Landau et al.
2008) does not exist for different plants species sharing the same dispersers.
The assumption in the theoretical dispersal model that animals move randomly in space
(Levin et al. 2003) is supported by our finding for the distance parameter, which is consistent
and without any plant species effect. This is coherent with mechanistic models of zoochoric
seed dispersal (Cousens et al. 2010).
However we did not explore post-dispersal fate for seed, which surely shapes species
distribution (Réjou-Méchain et al. 2011). Several studies have shown that the interaction
between environmental heterogeneity and the biological characteristics of species can
influence distribution patterns at various spatial scales (Muller-Landau 2004; ter Steege et al.
2006). Negative density dependence with environmental filtering contributes to community
assembly (Paine et al. 2012). Nevertheless, it has also been shown that dispersal syndrome
predicts spatial distribution, which is relatively dispersed for zoochoric species (Seidler &
Plotkin 2006b). For species using large mammals such as the bonobo, we show that seed
dispersal is long-distance but without interspecific differences; although interspecific
difference in fruit characteristics is wide. Do species dispersed by the same partner share the
same distribution pattern? Studies have hypothesised that spatial patterns are highly context
dependent but can be predicted by dispersal syndrome (Réjou-Méchain et al. 2011) and plant
traits (Muller-Landau et al. 2008). Our hypothesis goes further with spatial prediction, trait-
based generalisation and modelling of seed dispersal in tropical forests, based not on fruit
characteristics, but rather on the disperser variable itself (elephant, bonobo, guenon, bat,
hornbill, etc.).
To conclude, fruit quantity and quality do not seem to affect disperser behaviour in relation to
dispersal distance. Our finding leads to new questions about possible plant adaptations to
force zoochoric partners to move constantly within their range.
143
Part III
144
Other actors influencing the seed fate
145
Bush pig (Potamochoerus porcus) seed predation of bush mango (Irvingia gabonensis)
and other plant species in Democratic Republic of Congo
Authors
David Beaune, Loïc Bollache, Barbara Fruth, François Bretagnolle
Published in African Journal of Ecology
146
Introduction
Bush pigs (otherwise known as Red river hogs, (Potamochoerus porcus) are known seed
predators in Afrotropical forests (Ghiglieri et al. 1982; Whitesides 1985; Blake & Fay 1997;
White & Abernethy 1997). Seed predators are key species affecting plant population
demographics by influencing the survival of early successional stages, such as seeds and
seedlings thereby playing a pivotal role in the regeneration, colonisation ability and spatial
distribution of plants (Hulme 1998). While largely omnivorous (Kingdon 1997) bush pigs are
also the largest member of the granivore guild in the Democratic Republic of Congo (DRC),
and their relative impact on structuring plant communities could be significant. To assess the
nature of bush pig seed predation we firstly recorded all plant species predated by bush pigs at
the long-term LuiKotale field site, in the DRC, over a period of eighteen months. This new
list was used to estimate how many tree species (species richness) and how many trees
(abundance) within the tree community are affected by bush pig predation, based on a plot
census of heterogeneous primary forest (12-ha plots). We also assessed the role of bush pigs
on seed fate in the fruit fall zone, focusing on the bush mango (Irvingia gabonensis), an
Afrotropical tree of local and western world economic value (White & Abernethy 1997). We
estimated seed predation and pathogen infection on seeds in the fruit-fall area and tested the
density dependent hypothesis: The density-dependent hypothesis suggests that predation and
pathogen levels will be elevated in the vicinity of the parent plant (Janzen 1970b; Connell
1971; Schupp 1992), becoming less prevalent the further one moves away from the parent
plant as seeds escape such pressure (Hubbell 1980; Howe & Smallwood 1982). We
consequently tested for potential distance effects within 100 m of parent plants to assess the
relative impact of bush pigs.
Methods
Study site
The LuiKotale research site (>6000 ha) is located within equatorial rainforest (2°47’ S -
20°21’ E), along the south-west fringe of the Salonga National Park, in DRC (Hohmann &
Fruth 2003c). The climate is equatorial with abundant rainfall (>2000 mm/yr), and a relatively
dry season from February to July. Mean temperature at LuiKotale ranges between 21°C to
28°C with a minimum of 17°C and a maximum of 38°C (2007-2010). Local people agreed in
147
2001 to stop all exploitation in the forest (Hohmann & Fruth 2003c). In this hunting-free
forest reserve, animals are less wary and more easily observable. A long-term project initiated
in 2002 at the site catalogues plant species and allows plant identification (Fruth, 2011).
Seed species predated by bush pigs
Seed predation by bush pigs was recorded by: i) opportunistic observations recorded during
315 days of field work focusing on bonobo feeding behaviour, 1879 hrs from January 2010 to
June 2011; ii) camera traps installed to capture medium to large seed predators, randomly
positioned in the study site in fruiting places and sites baited with all available seeds of the
forest (two Wildview series3 & three Bushnell
®
Trophy Cam™: Video mode 60s/1s
interval/normal sensitivity, set for a total of 82 consecutive days and nights during the study
period;
Figure 32); and iii) confirmation by trackers and experienced bush pigs hunters from
the province. Seed predation of the plant species was identified when seed destruction
(crunching sounds) was observed or heard on seed species (identified by direct observation at
distance with binocular and/or by collection of seed remains after the observed passage), and
there was no seed regurgitation. Bush pig feces were opportunistically collected and analysed
(N=8).
Estimation of mean tree number and tree diversity per hectare was made by surveying all
adult trees (>10 cm DBH, diameter at breast height) in each of 12 one hectare plots of
heterogeneous terra firme forest from February to June 2011. The estimated percentage of
trees and tree species seed predated by bush pigs were based on the above list of seed species
identified as being predated.
148
Figure 32 Picture of bush pig (Potamochoerus porcus) camera trapped in LK, 2011.
Predation under parent trees
Fifty-four fruit-producing adult Irvingia gabonensis trees were monitored from January 2010
to June 2011, to calculate the predation rate occurring on seeds under parents by counting the
ratio of open endocarps (i.e. predated by bush pigs, the only species able to open the
endocarp). Unopened seeds with pathogens tracks were also counted to estimate the role of
pathogens in seed mortality
To measure survival probability in relation to distance from the parent, we positioned a fruit
every 10 m along a 100 m transect in a marked place (square of branches), with care to avoid
conspecifics within 200 m. Each transect started at the parent trunk. This experiment started at
the end of the fruiting season when all the fruits had fallen (February 6
th
and 7
th
, 2010). Five
trees were studied, with two transects marked out per tree. For estimating the survival
probability, we sampled the remaining fruits five months later on July 6
th
and 7
th
, 2010 (when
germination occurred in the control nursery where 100 seeds of I. gabonensis were observed
from the beginning of the season (Beaune unpub. data)). We hypothesise that seed survival
would increase with distance from the parent tree with decrease of granivore pressure.
Statistical analyses were performed using R (R Development Core Team 2011) for GLM.
149
Results and discussion
Seed species predated by bush pigs
Twenty-six tree species and two liana species were recorded as being predated by bush pigs in
LuiKotale (
Table
8). This result is conservative given the brief study and infrequent fruiting periods of
some tropical species. Herds of 2-6 animals were observed predating large quantities of seeds
beneath the parent trees, within the fruit-fall zone where fruit drop by gravity (barochory).
Based on the 12-ha plot census and the conservative list of seed species predated, we estimate
that 15.5% ± SE. 0.9 of the tree species are seed predated by bush pigs. These species
represent 33.3% ± 1.7 of the trees in the LuiKotale community. Eight feces were collected,
undetermined fragments were visible but none of them contained whole seeds. However,
given the small sample size we cannot exclude that certain seed species of LuiKotale may
pass through the digestive tract and remain viable. While recognised as seed predators, studies
from Asia, Australia and Africa have shown that suids also pass seeds intact through the
digestive system (Corlett 1998; Castley et al. 2001; Westcott et al. 2005), and act as important
seed dispersers in some habitats (Kerley, McLachlan & Castley 1996). Their role as seed
dispersers in other ecosystems within Africa remains to be determined (Geldenhuys 1993;
Seufert, Linden & Fischer 2010), but bush pigs can therefore have both beneficial and
detrimental functional roles within African landscapes.
Species
Family
tree nb/ha ± SE
Anonidium mannii
Annonaceae
8,8 ± 1,6
Autranella congolensis
Sapotaceae
0,1 ± 0,1
Colletoecema dewevrei
Rubiaceae
2,6 ± 1
Colletoecema sp.
Rubiaceae
0,1 ± 0,1
Crotonogyne manniana
Euphorbiaceae
0
Dacryodes buettneri
Burseraceae
0,4 ± 0,2
Dialium gossweileri
Caesalpiniaceae
2,1 ± 1,4
Dioscorea praehensilis
Diocoreaceae
N/A (Liana)
Drypetes gossweileri
Euphorbiaceae
8,3 ± 2
Gambeya lacourtiana
Sapotaceae
0,3 ± 0,3
Gilbertiodendron dewevrei
Caesalpiniaceae
0
Gilbertiodendron mayombense
Caesalpiniaceae
0
150
Guibourtia demeusei
Caesalpiniaceae
0
Irvingia gabonensis
Irvingiaceae
1,7 ± 0,6
Irvingia grandifolia
Irvingiaceae
0,1 ± 0,1
Lasianthera africana
Rubiaceae
2,6 ± 1
Mammea africana
Guttifereae
0,3 ± 0,2
Manilkara yangambiensis
Sapotaceae
0,9 ± 0,3
Parinari excelsa
Chrysobalanaceae
0,3 ± 0,1
Pentaclethra macrophylla
Mimosaceae
0,1 ± 0,1
Pycnanthus marchalianus
Myristicaceae
0,2 ± 0,1
Synsepalum longecuneatum
Sapotaceae
10,1 ± 1
Tetracarpidium conophorum
Euphorbiaceae
N/A (Liana)
Treculia africana
Moraceae
0,1 ± 0,1
Tridesmostemon omphalocarpoides
Sapotaceae
0,1 ± 0,1
Vitex sp.
Verbenaceae
3,4 ± 0,9
Xylopia aethiopica
Annonaceae
0,2 ± 0,2
Zeyherella longepedicellata
Sapotaceae
0,9 ± 0,3
Table 8 Seed species recorded to be predated by Potamochoerus porcus in LuiKotale (DR Congo). Tree density
is estimated among 12 ha of heterogeneous terra firme forest. Tree species such as Gilbertiodendron or
Guibourtia are more abundant in homogenous forests.
Predation under parent trees
Bush pigs have powerful jaws adapted to crush hard food like seeds (Herring 1985). For
example, even seeds protected by thick shells, such as I. gabonensis, can be crushed. The
mean force needed to crack an Irvingia shell was calculated to be 2.06 to 3.67 kN (Ogunsina,
Koya & Adeosun 2008). This ability to destroy seeds could lead to bush pig mediated density-
dependent effects (sensu Schupp, 1992), thereby affecting seed survival for many tree species
in DR Congo. We calculated that for each adult bush mango monitored (N=54) an average of
54% ± SE. 3 of the seeds present in the fruit fall zone were opened and predated by bush pigs;
CI
95
=[40-67%]. Among remaining unpredated seeds, 76% ± 3 were rotten, reflecting
pathogen attacks; CI
95
=[62-90%].
Figure 33 shows that the probability of seed survival does
not increase significantly with distance from the parent tree within a 100 m radius (GLM:
F
108,-4
=-4.53; p=0.3392 for distance, no tree effect: F
105-1
=-1.46; p=0.2274). Within this zone,
seed mortality remains high. For all the parent trees, 87% ± 3 of the monitored seeds were
predated within a 100 m radius around the trunk. Irvingia gabonensis exemplify the high
mortality rate in the fruit fall zone where fruit fall beneath the canopy by gravity (barochory)
151
and in the vicinity (at least 100 m). For I. gabonensis, intense predation and pathogen effects
within 100 m from the parent tree do not appear to conform to the Janzen-Connell model of
density-dependent effects. However, the effects on seedling survival remain to be tested. (see
appendix 1 : Density dependent effect affecting Irvingia gabonensis recruitment)
Bush pigs are important seed predators in LuiKotale, DRC. However, their importance as
keystone species within the broader landscape is likely to be affected by a number of
anthropogenic factors, primarily hunting as bush pig are a target species in the DRC (Wilkie
& Carpenter 1999). The potential impacts of bush pig hunting activities could have direct
effects on the dynamics of plant communities (Muller-Landau 2007; Vanthomme, Bellé &
Forget 2010a) but are as yet untested.
0
25
50
75
100
0 20 40 60 80 100
distance (m)
% predation
mean predation rate = 87% ±3
Figure 33 Seed predation rate within a 100 m radius around the parent bush mango (I. gabonensis). There was
no distance effect (p-value>0.33).
152
Dung beetles are critical in preventing post-dispersal seed removal by
rodents in Congo rain forest
Authors
David Beaune, Loïc Bollache, François Bretagnolle, Barbara Fruth
Published in Journal of Tropical Ecology
153
Abstract
Seed dispersal with seed deposited by animal in feces attracts dung beetles. In the Congo
forest of LuiKotale (DRC), granivores such as the giant pouched rat (Cricetomys emini) or
porcupine (Atherurus africanus) are attracted to bonobo dung in order to forage for seeds.
These nocturnal seed predators are preceded by diurnal dung beetles (Scarabaeoidea feeding
on feces) while feces are deposited by frugivores during the day, like bonobos (Pan paniscus).
The largest Scarabaeidae from the genus Catharsius bury feces and seeds (≤3.5cm) within
two hours of deposition by apes. For three plants species tested, burial effect reduced post
dispersal removal and mortality of seeds. This race for dung between granivores and
coprophages is probably critical for plant survival and thus demography.
Keywords Congo, Cricetomys emini, dung beetle, Scarabaeidae, secondary dispersal, seed
predation, zoochory
Résumé
La dispersion de graine via les animaux et leurs fécès attire les bousiers. Dans la forêt du
Congo, à LuiKotale (RDC), les granivores tels que le rat géant d’Emin (Cricetomys emini) ou
le porc-épic (Atherurus africanus) sont attirés par les fécès de bonobo afin de trouver des
graines. Ces prédateurs nocturnes de graine sont précédés dans leurs recherches de fécès par
les coléoptères (Scarabaeoidea coprophage) qui atterrissent sur les fécès déposées par les
frugivores comme le bonobo (Pan paniscus) pendant le jour. Le plus grand Scarabaeidae du
genre Catharsius peut ensevelir des graines (≥3.5cm) deux heures après le dépôt par les
grands singes. Sur trois espèces de plantes étudiées, l’effet d'enterrement réduit le
déplacement post-dispersion des graines par les prédateurs. Cette course pour les crottes entre
les granivores et les coprophages est probablement un facteur influent dans les paramètres de
survie et la démographie des populations de plantes.
Mots clefs bousiers, dispersion secondaire, Cricetomys emini, Scarabaeidae, prédation de
graine, zoochory
154
Dung beetles (Scarabaeidae subfamily Scarabaeinae) are ubiquitous and play an important
role in the removal of animal dung and the dispersal of seeds embedded therein. They exhibit
a range of dung-acquisition and burying behaviours, from burying dung directly beneath the
dung deposit or to rolling dung balls at several metres. Dung beetles act as important agents
for secondary seed dispersal and seed survival: the burial of seeds is said to be of advantage
against predators and desiccation (Feer 1999; Andresen & Feer 2005; Culot et al. 2009). In
addition, burial of seeds by dung beetles is considered beneficial as seeds are not only
deposited within the range of depths that are favourable for seedling establishment but
also among organic fertilizer that is said to increase seedling growth rates (Estrada &
Coates-Estrada 1991; Shepherd & Chapman 1998; Andresen 1999; Andresen 2002).
However, post-dispersal seed fate with and without the effects of dung beetles is a challenge
and for a better understanding more detailed investigations are required (Vander Wall &
Longland 2004); especially in Africa where research is far less developed than in Neotropical
systems. Here we explore experimentally under in situ conditions, how dung beetle burial can
affect seed removal by predators in an undisturbed forest. Research took place at the
LuiKotale research site, Central Congo Basin, Democratic Republic of Congo (DRC). Here,
the bonobo (Pan paniscus Schwarz) is the primary seed disperser. The giant pouched rat
(Cricetomys emini Wroughton) is the most common seed predator and dung beetles are
secondary dispersers. For the seeds, post-dispersal mortality is affected by seed predators and
dung beetles. Thus, seeds embedded in feces could have both, advantages and disadvantages.
Advantages as mentioned above, and disadvantages as dung specifically may attract seed
predators. In order to assess the impact of seed burial by dung beetles, we tested two
hypotheses as follows: (1) Seed predators are attracted by faecal odours; and (2) Seeds buried
by dung beetles escape the seed predators. In addition, we investigated dung beetle presence,
behaviour and efficiency as well as dung beetle-related seedling establishment.
The LuiKotale research site is located at the south-western fringe of the Salonga National
Park, DRC, within evergreen lowland equatorial rain forest (2°47’S, 20°21’E) (Hohmann &
Fruth 2003c). The climate is equatorial with abundant rainfall (>2000 mm y
-1
), and two dry
seasons, a short one in February and a longer one between May and August. Mean
temperature at LuiKotale ranges between 21°C and 28°C with a minimum of 17°C and a
maximum of 38°C (2007-2010).
155
Figure 34 Infrared records on faecal odour attraction: Arrows point at bonobo faecal odour and control stick
with giant pouched rat (Cricetomys emini) (a) and African brush-tailed porcupine (Atherurus africanus) (b) each
sniffing at the treated wooden stick.
For the first hypothesis, two sticks from the same wood of 50 cm length, were placed 1 m
apart 4 m in front of a camera trap (Wildview series3 & Bushnell
®
Trophy Cam™: Video
mode 60s/1s interval/normal sensitivity) to test faecal olfactory attraction in animals: one
stick was covered in fresh bonobo manure (without seeds or faecal material >1 mm;
Figure
34) 2 cm of the top end, the other stick was without treatment serving as control. The
experiment started at 17h00 and lasted for 24 h. It was run 30 times between January and
March 2011 with new sticks each time. Sticks were randomly positioned where giant pouched
rats had been observed previously. Only sites visited by predators were analysed. Olfactory
attraction was considered when the rat rose on its hind legs and pointed its nose towards the
top of the stick (at less than 5 cm) (
Figure 34). From these 30 runs, a total of nine showed seed predators. Of these, eight
recordings contained giant pouched rats at night. All of the eight videos showed a rat sniffing
the stick with faecal odour (
Figure 34a). None of the control sticks was sniffed. During their nocturnal activities, giant
pouched rats were significantly attracted by bonobo faecal odour (non-parametric Wilcoxon
signed rank paired test = 36, P = 0.01; power analysis = 91%, software: R 2.11.). One video
recorded an African brush-tailed porcupine (Atherurus africanus Gray) sniffing the stick with
faecal odour (
Figure
34b).
In order to investigate granivore behaviour towards unburied bonobo feces, fresh bonobo
feces collected during the day were positioned at night (19h00), 4 m away from a camera trap.
The experiment was conducted twice in January 2011 at different sites. Both times fresh
bonobo feces were visited by C. emini which ate the seeds (19h32 and 02h19). For the second
156
visit, dung beetles had probably started to bury the material because the rat was filmed
digging.
For the second hypothesis, we investigated the removal rate of five seeds on the ground
compared to five seeds of the same species buried at 5 cm depth with 40 replicates. Seeds of
three plant species from three different families, Cissus dinklagei Gild & Brandt, Vitaceae;
Polyalthia suaveolens Engl. & Diels, Annonaceae; Dialium corbisieri Staner,
Caesalpiniaceae, were extracted manually from several bonobo feces collected the previous
day and tested from January to June 2010 and 2011. Seed dimensions were measured for 10
seeds each during their fruiting season between 2010 and 2011 as follows: C. dinklagei:
weight 0.7 g, length 18 mm, diameter 10 mm; P.suaveolens: 0.6 g, 11 mm, 6 mm; and D.
corbisieri: 0.6 g, 14 mm, 10 mm. Manure was removed manually to mimic dung beetle
consumption but not washed to keep faecal odour. This experimental manipulation mimics a
situation in which seeds primarily dispersed by bonobos (endozoochory) are secondarily
dispersed by dung beetles and represents the two possible outcomes for these seeds: all dung
removed by dung beetles but seed not buried vs. all dung removed and seed buried. The seeds
of each species (n = 5 buried and n = 5 unburied 15 cm apart) were deposited in the forest and
replicated along a transect of 1.2 km length, resulting in three transects. The surface seeds
were deposited in a surface depression (2 cm deep, 8 cm diameter, manually created) in order
to avoid seed removal by rain. They were checked daily before and after the night (17h00 and
05h00). Presence and scratches of surface seeds were monitored daily, and presence of buried
seeds was checked every 30 d by excavation. Seeds were reburied after each control. Camera
traps were installed for identifying the seed removers and predators.
Buried seeds remained unaffected by seed predators. After 69 and 78 d of monitoring, 100%
of the buried seeds from P. suaveolens and C. dinklagei, and after 154 d of monitoring, 94%
of the buried seeds from D. corbisieri were still present (Proportion tests = 217, df = 1, P <
0.001; 154, df = 1, P < 0.001; 172, df = 1, P < 0.001 respectively; power analyses =100%). In
contrast, more than half of all surface seeds was removed by nocturnal seed predators: (P.
suaveolens: 56%; C. dinklagei: 58%; and D. corbisieri: 74%;
Figure 35). All removal events
occurred at night.
157
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
1 50 99
Time (d)
% of seed remaining in place
Dialium
Cissus
Polyalthia
Dialium
Polyalthia
Cissus
Figure 35 Effect of seed burial on seed predation: Percentage of buried (dotted line) vs. unburied (continuous
line) seeds in relation to time of Cissus dinklagei, Polyalthia suaveolens and Dialium corbisieri.
In order to investigate dung beetle presence, behaviour and efficiency, between January 2010
and April 2011 we baited a total of 45 pitfall traps (10 cm diameter, 15 cm depth) with fresh
bonobo feces (100 g each) exposing each to nature for 24 h in random places of the forest
undergrowth. Of these, 36 were found with several dung beetle species. The biggest identified
was possibly Catharsius gorilla Thomson (P. Moretto pers. comm.). Catharsius sp. was also
observed under natural conditions feeding on bonobo feces (n = 45). Freshly deposited
bonobo feces were georeferenced and monitored directly or by help of camera-traps. Arrival
time, burial time and burial behaviour were recorded. Catharsius sp. was able to bury
numerous and large seeds (max: 3.5 cm diameter e.g. Grewia spp.) in an average depth of 5
cm in large tunnels of 3.5 cm diameter. Mean (± SE) time between bonobo faecal deposition
158
and Catharsius sp. arrival was 42 ± 25 min (range = 5-188 min; n = 7). Catharsius sp. buried
the feces completely (average weight of bonobo feces: 111 ± 76.1 g, n = 407) within an
average of 56 ± 10 min (range = 27-89 min; n = 5).
In order to investigate dung beetle related seedling establishment, 45 feces were monitored
between March 2010 and June 2011. Of these, 67% ± 7% (CI
95%
= 53%-81%) were observed
to recruit seedlings between 1 and 18 mo from the beginning of monitoring. The following
plant species were identified: C. dinklagei, Dacryodes yangambiensis Louis ex Troupin, Ficus
spp, Grewia spp, Guarea laurentii De Wild, Landolphia spp, Manilkara sp., Pancovia
laurentii Gild ex De Wild.
In the forest ecosystem of LuiKotale, the bonobo eats fruits and swallows seeds of hundreds
of plant species (unpubl. data). Nocturnal seed predators such as the giant pouched rat or
porcupine are attracted by faecal odour likely to indicate seeds dispersed by endozoochory.
However, seeds are usually deposited by apes during the day, attracting tunnellers such as
species from the genus Catharsius in less than 1 h. Seedling establishment is likely to occur in
a narrow range of depths (3–10 cm), where seed removal by rodents is low but seedlings can
still emerge (Estrada & Coates-Estrada 1991; Shepherd & Chapman 1998).
Deposited feces disappear from the surface in less than 1 h due to tunnellers that can bury
seeds of up to 3.5 cm diameter such as seeds of Grewia spp, allowing seeds to avoid nocturnal
rodents and surface pathogens.
The net outcome of these plant-animal interactions is highly context-specific and deserves
attention, particularly in the Afrotropics where related research appears to be
underrepresented, further attention. This note, however, allows confirming the following
Neotropical findings: dung beetles decrease the probability of seed predation by rodents and
favor seedling establishment (Andresen & Levey 2004; Santos-Heredia, Andresen & Zárate
2010; Culot et al. 2011; Lawson, Mann & Lewis 2012). However, more emphasis needs to be
put on distinguishing rodent seed predation from secondary dispersal. Indeed, seeds removed
by granivores such as rodents cannot be considered as 100% predated (Nyiramana et al.
2011). A minority could be secondarily dispersed but the majority of the removed seeds is
food for seed predators (Crawley 1992). In DRC, dung beetles such as Catharsius spp. and
other large tunnellers are involved in secondary seed dispersal and thus play a critical role in
post-dispersal seed survival.
159
A bonobo does not replace an elephant
160
Doom of the elephant-dependent trees in a Congo tropical forest
Authors
David Beaune, Barbara Fruth, Loïc Bollache,
Gottfried Hohmann & François Bretagnolle
Published in Forest Ecology and Management
161
Abstract
In an evergreen lowland rain forest of the Cuvette Centrale, DR Congo, at the LuiKotale
Max-Planck-Institue research site, forest elephants (Loxodonta cyclotis) are close to
extinction. Between January 2009 and June 2011 we investigated the influence of elephant
decline on sustainability of elephant-dispersed tree populations.
For this, we explored how trees with the megafaunal syndrome reproduce without seed
dispersal, what is the recruitment under other tree species, and eventually what are the effects
on the population demography and on the spatial structure. We estimated dispersal
effectiveness of alternative partners for functional replacement of the elephant.
Overall, 18 tree species presenting the megafaunal syndrome were identified. They represent
4.5% of the local tree diversity with a density of 28.2 ±2.7 tree/ha. Seventy-eight percent
(14/18) of these tree species are elephant-dependent and do not recruit enough poles for self
replacement, neither under the parent nor beneath other tree species. For 12 species
populations, the first cohorts were absent in our plots. For species able to recruit, the spatial
structures of the young generations are more clumped than adults while they are no difference
for control tree species.
The second biggest seed disperser of the forest, the bonobo (Pan paniscus), does not replace
elephant dispersal effectiveness. Thus, there is no alternative partner for seed dispersal for the
majority of the megafaunal trees which are actually elephant dependent.
We discuss the likely consequences of the loss of elephants dispersed tree species and propose
alternatives for species survival to bridge the time until efficient conservation strategies take
effect.
Keywords Congo basin, defaunation, ecosystem decay, forest ecology, Loxondota cyclotis,
Pan paniscus, poaching, recruitment, seed dispersal
Résumé
Dans une forêt tropicale humide de la Cuvette centrale du Congo (RDC), dans le camp de
recherche LuiKotale du Max Planck Institut, les éléphants de forêt (Loxodonta cyclotis) sont
proches de l'extinction. Entre janvier 2009 et juin 2011, nous avons étudié l'influence du
déclin des éléphants sur la reproduction et la survie des populations de plantes dont les graines
sont dispersées par ces pachydermes.
162
Pour ceci, nous avons étudié comment les arbres au syndrome de megafaunal se reproduisent
sans dispersion de graine, ce qui implique l’étude du recrutement sous les arbres-parents, nous
avons étudié le recrutement sous les autres arbres (impliquant une dispersion) et enfin les
effets potentiels sur la démographie et la structure spatiale de ces populations d’arbres. Nous
avons par ailleurs estimé l'efficacité de dispersion des partenaires alternatifs qui pourraient se
substituer au rôle fonctionnel des éléphants.
De façon générale, 18 espèces d'arbre présentant le syndrome de megafaunal ont été
identifiées. Ces espèces représentent 4.5 % de la diversité locale d'arbre avec une densité de
28.2 ±2.7 arbres/ha. Soixante-dix-huit pour cent (14/18) de ces espèces d'arbre sont éléphant-
dépendant et ne recrutent pas assez de jeune pour le remplacement des parents. Le
recrutement est insuffisant sous les arbres-parents comme sous les autres espèces d’arbres.
Chez 12 espèces, les premières cohortes sont absentes de nos parcelles d’étude. Pour les
espèces capables de recruter, les structures spatiales des jeunes générations sont plus groupées
que la structure aléatoire, voire uniforme, des adultes.
Le deuxième plus grand disperseur de graine de la forêt : le bonobo (Pan paniscus), ne
remplace pas les éléphants. Ainsi, il n'existe pas de partenaire alternatif pour la majorité des
arbres au syndrome mégafaunale qui sont par conséquent : éléphant-dépendants.
Nous discutons les conséquences probables de la perte d'espèce d'arbre dispersées par les
éléphants et proposons des solutions alternatives d’urgence pour la survie des espèces
éléphant dépendantes jusqu'à ce que les stratégies efficaces de conservation entrent en
vigueur.
Mots clefs Bassin du Congo , braconnage , défaunation , dispersion de graine , écologie
forestière , Loxondota cyclotis, Pan paniscus, recrutement.
163
Introduction
The elephant is the largest terrestrial animal and one of the last megafauna represented on
earth. African Elephants (Loxodonta cyclotis Matschie and L. africana Cuvier) currently
occur in 37 countries in sub-Saharan Africa (Blanc 2007) while extinct from many former
ranging areas (Bouché et al. 2011), Blanc 2008 in (Bouché et al. 2011; IUCN 2012).
Rarefaction and possible extinction of elephants in many countries may have implications
beyond the loss of the species itself. These large herbivores are known to consume a huge
amount of food and interact with many plants, both quantitatively and qualitatively (White,
Tutin & Fernandez 1993; Blake et al. 2009). Recently Campos-Arceiz & Blake (2011)
compiled a food list of 335 elephant dispersed species from 213 genera in 65 families across
several African research sites. In Afrotropical forests, many of these plant species are
disseminated by forest elephants (Loxodonta cyclotis) sometimes at very long dispersal
distances (Blake et al. 2009), a mutualism that matters to the population dynamics of plants
and to the structure of forest tree communities (Cain, Milligan & Strand 2000). Moreover, the
rate of seed germination of many forest plant species has been increased significantly after
passage of the elephant’s gut (reviewed in Campos-Arceiz and Blake, 2011). Therefore,
elephants are widely recognized as a keystone species (Western 1989; Power et al. 1996), and
are qualified as “megagardeners of the forest” (Campos-Arceiz & Blake 2011). Many of the
plants the elephants interact with as fruit consumers are generalists and hence dispersed by
other animals. To date, obligate relationships have been only demonstrated for Balanites
wilsoniana (Cochrane 2003; Babweteera, Savill & Brown 2007) but based on different
evidences, many other African plant species are suspected to be largely or exclusively
elephant dependant in their seed dispersal and regeneration (reviewed in Campos-Arceiz and
Blake, 2011) (Cochrane 2003; Babweteera, Savill & Brown 2007). One of the most appealing
evidence is based on the traits of the fruits and of the seeds consumed by the elephants that
constitute a megafaunal syndrome (Alexandre, 1978, Feer 1995a; Guimarães et al. 2008).
Following Alexandre (1978) megafaunal fruits have been defined by Guimaraes et al. (2008)
as the fruits produced by plant species that interact with large bodied frugivore species. These
authors have classified these fruits as either big fleshy fruits (4-10cm in diameter) producing
big (>2cm) seeds with a hard coat or bigger fleshy fruits (>10cm) producing numerous small
seeds. These fruits are generally brown, green or yellow and smelly (Guimaraes et al. 2008;
Campos-Arceiz and Blake, 2011) . Moreover, the fruits are commonly very noisy when
dropping and hitting the soil at maturity, thus likely to be localised acoustically by potential
164
seed-dispersers. Several plant species share these megafaunal syndromes in African forests
historically inhabited by elephants. Considering the massive decline of elephant forest
populations in Africa these last decades, many authors have suggested that the phenomenon
would seriously impact the regeneration process of many plant species in particular those
presenting megafaunal syndromes ((Blake et al. 2007; Guimarães Jr, Galetti & Jordano 2008;
Blake et al. 2009; Campos-Arceiz & Blake 2011) although these dramatic predictions are still
debated (Campos-Arceiz & Blake 2011). However, it is difficult to evaluate the
consequences of the decrease of forest elephant populations in forest ecosystem dynamics
because it would necessitate to compare the demography of long generation trees in forests
where the elephants are still present with those in forests where they have been extirpated.
One approach consists in comparing regeneration and conspecific spatial aggregation patterns
of plant species that present megafaunal syndrome at different age classes in forests where
elephants have been hunted. Indeed, a strong relationship between dispersion syndromes and
spatial aggregation was found among 561 tree species in a 50 ha plot in Malaysia (Seidler &
Plotkin 2006b). Barochore and ballistic species with short dispersal distance are more
aggregated than species dispersed by large animals and this pattern was found for saplings
and adult trees ((Seidler & Plotkin 2006b). Our hypothesis is that in a forest where elephants
have been extirpated we should detect either the disappearance of young age classes or a shift
in aggregation patterns between old age classes (that have been dispersed by elephants) and
young age classes that have been dispersed without elephants for species that present a
megafaunal syndrome. These changes should not be detected for barochorous species or for
species dispersed by other animals. Hence, if tree species showing the megafaunal syndrome
depend on elephants for seed dispersal, one would expect no alternative seed-dispersers and
thus a high mortality of seedlings and poles due to the density dependent effect (Janzen
1970b; Connell 1971; Beaune et al. 2012b; Paine et al. 2012). Very few studies have
investigated the consequences of the disappearance of the elephants on the spatial distribution
of different age classes of tree species dispersed by these animals. The seedling and the
sapling spatial distributions of Balanites wilsoniana, a species dependant on elephants for
dispersal and germination, differ between forests with and without elephants, with seedlings
being more aggregated under adult plants when elephants are absent (Babweteera, Savill &
Brown 2007).
In the Salonga National Park (NP) (DR Congo), the largest forested NP in Africa and the
second largest on earth, forest elephants have been severely poached for decades (Alers et al.
165
1992; Van Krunkelsven, Bila-Isia & Draulans 2000; Blake et al. 2007). Compared to other
NP in the Congo Basin, mean forest elephant density of 0.05 individuals km
-
² in Salonga NP
deriving from 1900 remaining individuals is considered being low. In contrast, mean
estimated forest elephant densities in the other NP in this area ranged from 0.4 individuals
km
-
² in Nouabalé-Ndoki NP and Dzanga-Sangha NP to 2.9 elephants km
-
² in the Minkébé NP
(Blake et al. 2007). Thus, forest African elephant population in Salonga NP can be considered
as one of the most limited in the Congo basin with severe potential consequences for the
elephant-dependent tree community.
In this paper, we examine the potential impact of a reduced density of forest elephants on the
recruitment for several trees species presenting the megafaunal syndrome in the Salonga NP.
Overall, we aim to assess the ability of the megafaunal tree community at LuiKotale to
reproduce without elephant seed dispersal service.
To test these hypotheses, we compare the spatial distribution of different age classes of tree
species (adults, poles, saplings and seedlings) among species with different dispersion
syndromes (megafaunal, zoochoric and autochoric), in a forest where elephants have been
almost extirpated 30 years ago , still suffer from illegal poaching and are far from having
recovered from this serious impact. Moreover we have quantified the recruitment of
megafaunal syndrome species under parental trees (without seed dispersal) and other trees;
and (2) alternative dispersal partners and their dispersal effectiveness (Schupp 1993; Schupp,
Jordano & Gomez 2010) in order to judge ecological redundancy and alternative survival.
Here, we focus on the second largest fruit consuming mammal after the elephant and potential
dispersal partner, the only great ape of the Cuvette Centrale South of the Congo River, the
bonobo (Pan paniscus Schwarz); (3) current tree-population demography including recent
cohorts born after elephants’ disappearance and old cohorts born in the past, when visits of
elephants were still regular (before the eighties). For tree-populations with alternative seed-
dispersers, we expect different spatial structures of recent generations. For this we (4)
compare spatial structure of adults dispersed during the elephant era (potentially long
dispersal distances) with that of new recruits not dispersed by elephants (potentially shorter
dispersal distances; after the eighties).
Materials and methods
Study site
166
The LuiKotale research site (LK) is located within the equatorial rainforest (2°47’S, 20°21’E),
at the south-western fringe of Salonga NP, in the same continuous forest block. Salonga NP
has a size of 33.346 km², and has been classified as UNESCO world heritage site (Grossmann
et al. 2008). The study site covers >60km² of primary evergreen lowland tropical forest. This
forest traditionally belongs to Lompole village (17 km away) and has been used for hunting,
fishing and the collection of forest products. Since 2001 Lompole agreed to stop all
exploitation and devote it for the purpose of research (Hohmann & Fruth 2003c). The climate
is equatorial with abundant rainfall (>2000mm/yr) and two dry seasons, a short one around
February and a longer one between May and August. Mean temperature at LuiKotale ranges
between 21°C to 28°C with a minimum of 17°C and a maximum of 38°C (2007-2010). Two
major habitat types can be distinguished: 1-Dry (terra firme forest) and; 2-Wet (temporarily
and permanently inundated forest). The dry habitat dominates with heterogeneous species
composition covering 73%, and homogenous species composition (e.g.Gilbertodendron spp)
covering 6% of the site. The wet habitat consists of heterogeneous forest temporarily (17%)
and permanently (4%) inundated (Mohneke & Fruth 2008).
Tree species
Between 2002 and 2010, botanical data collection took place in the frame of the long term
project “The Cuvette Centrale as Reservoir of Medicinal Plants” (Fruth 2011): Fertile plant
material was collected in at least triplicate along natural trails (31 km), standardized transects
(8 km), in plots, and opportunistically. It was identified by vernacular name, described, tagged
with a unique collection number, and herborized. The dried vouchers were shipped to
Kinshasa, taxonomically determined and incorporated into the herbarium of the INERA at
Kinshasa University (herbarium code: IUK). Copies of specimens were shipped to herbaria in
Belgium (National Botanic Garden of Belgium : BR, Meise) and Germany (Botanische
Staatssammlung München : M, Munich) for verification and identification by specialists. By
May 2010, the herbarium consisted of 7,300 vouchers. So far, ≥403 tree species from 40
families were identified for LuiKotale (Fruth unpub. data). Among the tree species censused,
the diaspores were analysed and dispersal strategies defined as (1)-zoochore (animal dispersed
species), (2)-anemochore or (3)-autochore. Species were assigned zoochory when an edible
part of the fruit that promotes swallowing or transport of seeds was found. Anemochory (wind
dispersal) was assigned when wings or other structures (e.g. plumes) favouring wind transport
were found. Finally, autochory was assigned to species that lack any obvious dispersal
structure. (Howe & Smallwood 1982). We distinguished the species with megafaunal
167
syndrome following the criteria of (Feer 1995a; Guimarães, Galetti & Jordano 2008).
Effective seed dispersal of these species by elephants was confirmed by literature (White,
Tutin & Fernandez 1993; Yumoto et al. 1995; White & Abernethy 1997; Theuerkauf et al.
2000; Nchanji & Plumptre 2003; Morgan & Lee 2007; Blake et al. 2009; Campos-Arceiz &
Blake 2011). See Table 9.
Family
Species name
vernacular
name
size (cm)
of fruit &
seed
Mean
density
(tree/ha)
Mean
DBH
(cm)
Bonobo seed
handling
Human usage
Anacardiaceae
Antrocaryon nannanii
Bokongwende
5ø
4ø
<0.1
97
Dropped
F
Annonaceae
Anonidium mannii
Bodzingo
30
6
8.8
47
Dropped
F, TM
Apocynaceae
Picralima nitida
Botolo
17
3
5.2
19
Fruit not
consumed
W
Chrysobalanaceae
Parinari excelsa
Bodzilo Mpongo
5ø
3ø
0.3
113
Dropped
W
Euphorbiaceae
Drypetes gossweileri
Bopambe
10
4
8.3
46
Fruit not
consumed
TM, W
Guttifereae
Mammea africana
Bokodzi
10
6
0.3
118
Dropped
TM, W
Irvingiaceae
Irvingia gabonensis
Boseki
7
5
1.7
83
Dropped
F
Irvingia grandifolia
Loote
7
5
0.1
110
Dropped
TM
Klainedoxa gabonensis
Boseki ya
Moindo
6ø
4
2
125
Fruit not
consumed
Mimosaceae
Tetrapleura tetraptera
Bolese
16
<1
ø
<0.1
82
Fruit not
consumed
F, TM
Moraceae
Treculia africana
Boimbo
35ø
1
0.1
60
Swallow/Crunc
h
F
Rubiaceae
Massularia acuminata
Welo
6
<1
0.8
11
Fruit not
consumed
W, TM
Poga oleosa
Ememo
7ø
5ø
<0.1
68
Fruit not
consumed
poison
Sapotaceae
Autranella congolensis
Bonianga
9
6
<0.1
185
Dropped
TM, W
Gambeya lacourtiana
Bopambu
90ø
4
0.3
92
Sawallow/spit
F, TM
Omphalocarpum letestui
Boiliki
14ø
3
0.2
69
Fruit not
consumed
Omphalocarpum procerum
Bosanga
20ø
4
<0.1
73
Fruit not
consumed
Tridesmostemon
omphalocarpoides
Boyoko
10ø
3
<0.1
27
Fruit not
consumed
168
Table 9 Elephant-dependent tree species: characteristics show averages of fruit and seed size, species density,
trunk diameter in breast-height (DBH). seed-handliong of bonobos as well as current human interests. Fruit-size
is average length, seed size is largest width or passage size according to the morphology and passage in a
digestive tract, indicated as diameter ø or length ↔ (n=10). Human usage is specified as F (fruit consumption),
W (wood), TM (traditional medicine).
Tree population demography
In order to investigate the impact of elephant decline on the actual tree population
demography at LuiKotale, we censused all adults trees ≥10cm DBH in 13 plots of 1-ha
(100×100m) each, as well as all seedlings (<50cm high), saplings (50cm-200cm high), and
poles (>200cm high and <10cm DBH) in 400 subplots of 4m² (2×2m) /ha plot. The plots were
randomly positioned in heterogeneous primary forest, haphazardly without previous
knowledge of the area. The closest plot pair is separated by 250m and the most distant one by
6km. From February to June 2011, all trees were spatially referenced with compass and
hectometer, using the South-Western plot-corner as origin. Tree populations are normally
characterized by type III demographic curves because the species produce a huge number of
seeds and seedlings but the greatest mortality due to predation and pathogens is experienced
early on in life followed by an exponentially decrease of the rates of death (Demetrius 1978;
Makana et al. 2011). Consequently, with class age cohorts being equivalent to class size
cohorts, tree demography is an exponential of Type III curve in viable populations. Our
hypothesis is that if the dispersion and the reproduction of a tree species has been impacted by
the disappearance of the elephant population we should detect a crash in the youngest cohorts
and hence a strong departure from a classical type III curve. In this study we have excluded
seedlings (<50cm) from the youngest cohort because of the huge fluctuations observed in the
annual factors regulating seedling density such as production, predation, drought, etc.
(Beaune, unpub. data). DBH and fruit dimensions have been measured for all species
investigated.
Recruitment under parental tree (without seed dispersal) and under non-parental tree (seed
dispersal)
To assess the actual recruitment of megafaunal trees elephant dependent for dissemination,
both megafaunal and control tree species were chosen from the Max-Planck-projects’ long-
term inventory of plants and exploration of the realm. As control we included six tree species
169
known to be independent of elephant-dispersal, (a) three autochoric, and (b) three zoochoric.
(a) Scorodophloeus zenkeri Harms, and Hymenostegia mundungu Pellegr, J.Léonard
(Caesalpiniaceae with ballistic seed dispersal able to propel seeds 30m away), and
Strombosiopsis zenkeri Engl. (Olacaceae, with barochory and probable secondary
dispersal);(b) Enantia olivacea Robyns & Ghesq., Polyalthia suaveolens Engl. & Diels
(Annonaceae), and Pancovia laurentii Gilg ex De Wild. (Sapindaceae), which are dispersed
by frugivores still present in LK including primates and birds (Beaune et al. in prep).
Between May 2010 and June 2011 a minimum of 10 adult individuals of both megafaunal and
control species that were previously observed to produce seeds were censused for actual
recruitment under the parental crown (without conspecific within 200m radius) as follows: All
seedlings (<50cm high), saplings (50cm-200cm high), and poles (>200cm high and <10cm
DBH=Diameter at Breast Height) were counted in the corresponding fruit-fall zone. The
surface of the fruit fall zone (=A) was calculated according to A=r²π, where r is the measured
radius of the crown.
Mean production of seedling, sapling and pole were calculated subsequently (=nb per
tree/fruit-fall zone). We considered a population being able to self replace when the average
pole production/tree was ≥1. In order to assess actual seed dispersal, the average density of
nineteen species-specific seedlings, saplings and poles from twelve families was calculated
for each parental and non parental tree species. The average densities calculated under non
parental species were compared with adult species densities inferred from 13×1ha-plots
(details below). In viable populations pole density should exceed adult density (see
demography below). Recruitment abilities were categorized according to (Chapman &
Chapman 1995) as follows: 1-Autorecruit (recruits under the parent, characteristic of the
autochoric species); 2-Dispersal dependent (no recruit under the parent but high recruits
densities (>to adults) under other trees); 3-Polyvalent (able to recruit more than one pole
under the parent and other trees); 4-Unable to recruit (insufficient recruits under the parent
and other trees (density<to adults’).
Bonobos as alternative dispersal partners
Bonobos (Pan paniscus) are the biggest frugivores after elephants. Field work with these
primates has been ongoing since 2001 (Hohmann & Fruth 2003c). Day-to-day follows of
individuals of one habituated community (n=35 mature bonobos) have been conducted since
2007. In order to investigate their role as potential alternative seed disperser, DB observed for
22 months between January 2009 and June 2011, fruit and seed handling of the megafaunal
170
plants using continuous behavioural group observations and ad libitum observations (Beaune
et al. in prep).
Spatial analyses
The spatial distribution of the different cohorts of the megafaunal and control were
investigated. For determining the degree of clumping for each species, we calculated
Morisita’s Index (I
M
) within the censused 1-ha quadrates (Morisita 1959). The index
corresponds to the scaled probability that two plants randomly selected from the entire
population are in the same quadrate. The index varies from 0 to n. In uniform patterns the
index varies between 0 and 1, where values >1 indicate clumping, with the distribution being
more clumped, the higher the value. When the index value is 1, the distribution of the plants is
random irrespective of plot-size or mean density of individuals per plot. Calculations were
performed using PASSaGE (Pattern Analysis, Spatial Statistics, and Geographic Exegesis;
(Rosenberg & Anderson 2008). For control species we expect no difference of spatial
structure among generations. Statistical analyses are specified in results. Analyses were
performed using R 2.13 (R Development Core Team 2011).
Results
Tree species
Table 9 shows the eighteen tree species from eleven families identified as megafaunal. This
megafaunal tree community represents 4.5% of the local tree species diversity. In terms of
abundance, the megafaunal tree density represents with 28.2 trees/ha ±2.7, a total of 7.8%
±0.7 of all trees/ha.
171
Figure 36 Demography of 6 control tree species censused in 13-ha plots. Y-Axes shows proportion of survivors.
X-axes shows cohort size.
Population demography
Control species show demographic curves Type III (
Figure 36).
Among the 18 megafaunal species tested at LuiKotale, only two species, A. mannii and D.
gossweileri, follow Type III demographic curve (Figure 37). Four species (P. excelsa, M.
africana, K. gabonensis, I. grandifolia) show higher numbers of recruits in the first cohort
than in the next one, although the fit is not exponential. For the other twelve species the first
cohort is absent. No seedlings at all were found for A. congolensis, A. nannanii, G.
lacourtiana, I. grandifolia, M. acuminata, M. africana, O. letestui, O. procerum, P. nitida, P.
oleosa and T. tetraptera either in the 13-ha plots or in the realm where attention was focused
on these species during the study period.
172
173
Figure 37 Demography of 18 megafaunal tree species censused in 13-ha plots. Bars indicate cohorts starting
with saplings. Red cross shows absence of the first cohort. Y-Axes shows proportion of survivors.
Spatial analyses
Of all 19 control tree-species, three autochoric and three zoochoric were analysed. For
megafaunal species, only populations able to recruit with existing cohorts of poles, sapling
and poles were analyzed. Consequently, analysis included A. mannii, D. gossweileri, and P.
excelsa. Three species, I. grandifolia, K. gabonensis and M. africana, while reported, could
not be analysed completely due to a lack of entire cohorts and recruit numbers <2. The spatial
patterning is similar among cohorts for the control species with clumped distribution, with I
M
>1.8 for autochoric trees and a random distribution for zoochoric trees with a mean I
M
=1.2
[1-1.7] (
Figure 38). However, the spatial patterning of the megafaunal species varies among
cohorts. Young generations tend to be more clumped than adult generations. The spatial
patterning of the six adults is similar to the other zoochoric species with a dispersed
distribution (uniform and random, I
M
range: 0-1.5), while the young cohorts are much more
similar to autochoric spatial patterns with clumped distribution (I
M
>>1). Our hypothesis is
supported: young generations dispersed by alternative seed dispersers are more clumped than
adults probably dispersed by elephants during time of highest elephant density.
174
Figure 38 Morisita’s index (I
M
) of adults, poles, saplings and seedlings of three autochoric (blue), three
zoochoric (green) and six megafaunal species (yellow) of 13 one-ha-plots. The index-value is 1 when individuals
are randomly dispersed, values greater than one indicate clumping, values between 0 and 1 indicate
uniformity.The higher the value, the more clumped the distribution.
Recruitment under parental tree (without seed dispersal) and under non-parental species
(seed dispersal)
A total of 302 trees from 37 species were censused (18 megafaunals+19 controls). The
cumulative fruit fall zone of these trees represents 5.13 ha, with an average fruit-fall zone for
each tree of 207 m² ± SE.19). For eight of the 18 megafaunal species, we were unable to find
10 specimens within the study area. This was the case for Antrocaryon nannanii (n=2),
Autranella congolensis (1), Omphalocarpum procerum (6), Tetrapleura tetraptera (2),
Treculia africana (7), Tridesmostemon omphalocarpoides (2), Omphalocarpum letestui (5),
and Poga oleosa (2). Both
Figure 39 and Table 10, show that none of the megafaunal species
can recruit enough poles for self replacement. Sixty seven percent (12/18) of the elephant-
dependent tree species did not recruit any pole neither under the parent nor beneath other
trees, resulting in the recruitment category 4 (unable to recruit). Only four megafaunal species
(Anonidium mannii, Drypetes gossweileri, Picralima nitida and Treculia africana) were able
to disperse and recruit poles under non parental trees resulting in the recruitment category 2
(dispersal dependent). However for D. gossweileri and P. nitida, pole recruit densities were
significantly lower than the adults’ ones (1.2 pole/-ha<<8.3 trees/ha; Wilcoxon signed-rank
175
test: p-value = 0.01 and 0.8 pole/ha <<5.2 trees/ha; p-value <0.01 respectively). Our
hypothesis of population viability is challenged by the last two megafaunal species, A. mannii
and T. africana, being the sole dispersal dependent trees that recruit beneath other non
parental trees with higher pole densities than adult (falling in category 2: dispersal
dependent). However, adult density of T. africana is extremely low explaining the extreme
difference between adult and pole densities.
Except for Antrocaryon nannanii, negative effects of adult megafaunal trees such as growth
inhibition of seedlings, saplings and poles within the fruit fall zone can be excluded.
Seventeen elephant-dependent tree species censused for recruits from other species beneath
their crown, showed an abundance and diversity of other plant species not significantly
different from what is found beneath control trees (Wilcoxon rank sum test, p-values>0.05).
Control species in contrast exhibited significantly different patterns. Of 19 species from 12
families, all resulted in the recruitment category 1, 2 or 3. A typical example of autochoric
tree-recruitment is illustrated by the control-species H. mundungu, Scorodophloeus zenkeri
and Strombosiopsis zenkeri. These species are able to recruit beneath the parental crown on
average 2.5 poles/parent ± 0.4; 3.4 ± 0.9; 1.2 ± 0.3 respectively resulting in the recruitment
category 1 (autorecruit). A typical example of dispersal dependent tree-recruitment is
illustrated by the control species E olivacea, P. suaveolens, P.laurentii, which are dispersed
by primates and birds. These were able to disperse and recruit poles under non parental trees
resulting in the recruitment category 2 (dispersal dependent).
176
Figure 39 Mean number of poles present (or recruited) under parent tree. For autochoric (blue), zoochoric
alternative partners (green) and zoochoric megafaunal partners tree species (red). The dotted line is the
theoretical value of pole recruitment necessary for self replacement of the parent tree. Y-error lines in bars
indicate standard errors.
The Bonobo as an alternative partner
Table 9 presents the megafaunal fruits that have been observed to be consumed by bonobos at
LuiKotale. Of the 18 species identified as megafaunal, nine are consumed by this second
largest frugivore. Bonobos consumed fruits of A. mannii in 1.6% ±0.2 of the feeding sessions
(based on 1879 hrs of continuous group observation), A. nannanii (0.2% ±0.7), I. gabonensis
(2.3% ±0.2) & grandifolia (<0.1%), M. africana (0.4% ±1.1) and P. excelsa (2.5% ±0.3). A.
congolensis consumptions were observed in 2007. These big size fruits are usually consumed
within or beneath the crown. Fruits become available by bonobos’ harvest or dropping by
gravity when ripe. Depending on the species, the fibrous mesocarp is chewed and swallowed,
or the juice extracted fabricating wadges and the fibrous remainders or the seeds dropped on
the spot with no differences from dispersal induced by barochory (no horizontal movement).
Sometimes individuals took one or more fruits (species: I. gabonensis, M. africana, A.
mannii), transporting them in their mouth and/or hands to eat while travelling, documenting
seed dispersal by ectozoochory. From our observations, seeds were transported in the 100 m
radius zone, with a maximum considered to be exceptional, where a bush mango was carried
for 426 m from the parent tree. Only G. lacourtiana (2.3% ±0.2 of the feeding sessions) seeds
177
were observed to be swallowed and found in feces and also spat. The size of this species
seems to be the limit for bonobo endozoochory with its ovoid shape (3cm long and 1cm
wide). The bonobo could be considered as a partner for endozoochoric seed dispersal of G.
lacourtiana. Bonobos were observed eating T. africana in flower, unripe and ripe including
the soft seeds (2.6% ±4.5). The bonobo is not considered as a dispersal partner for these trees.
Nevertheless, the megafaunal community is part of the bonobo diet representing 11.8% ± 0.1
of their feeding sessions.
Bonobos were not observed interacting with the other megafaunal species which do not seem
to be attractive for a primate. T. tetraptera, observed to be eaten by black mangabeys
(Lophocebus aterrimus Oudemans) in LK, are an exception.
178
Recruitment
Species
average recruitment under parent tree
recruitment density/ha
under other trees
seedlings
saplings
poles
poles
Control
Polyvalent
Hymenostegia mundungu
4.4
4.1
2.5
11.8>**
Scorodophloeus zenkeri
16.3
2
3.4
25.0 >**
Strombosiopsis zenkeri
2
2.1
1.2
1.3>**
Dispersal
dependent
Enantia olivacea
0
1.8
0.8
7.6>**
Pancovia laurentii
0.1
1
0.5
34.4>**
Polyalthia suaveolens
0.1
1.6
0.5
96.4 >**
Megafaunal species
Anonidium mannii
0.5
0.6
0.4
27.7 >**
Treculia africana
0.1
-
-
1.4 >***
Unable to
recruit
=
Elephant
dependent
Antrocaryon nannanii
3
4.5
-
-
Autranella congolensis
-
-
-
-
Drypetes gossweileri
-
0.2
0.1
1.2 <*
Gambeya lacourtiana
1
-
-
-
Irvingia gabonensis
1.7
0
-
-
Irvingia grandifolia
-
-
-
-
Klainedoxa gabonensis
-
-
-
-
Mammea africana
0.1
0.9
-
-
Massularia acuminata
-
-
-
-
Omphalocarpum procerum
0.2
-
-
-
Parinari excelsa
19.8
0.1
0.1
-
Picralima nitida
-
-
0.3
0.8 <**
Tetrapleura tetraptera
2
-
-
-
Tridesmostemon
omphalocarpoides
1.5
-
-
-
Omphalocarpum letestui
0.6
-
0.2
-
Poga oleosa
-
-
-
-
Table 10 Recruitment of the megafaunal & control species, with mean pole recruitment under the parent trees
and density under other species. Poles density is compared with adults (from the 13-ha plots) using Wilcoxon
signed rank test (> =poles density> adults density (and reverse with <); *:p-value<0.05, **:<0.01, ***<0.001)
179
Discussion
Here we analyzed 18 species of the megafaunal community to test the megafaunal tree
population’s ability to survive without elephants in an evergreen lowland rainforest of the
Cuvette Centrale. Without seed dispersal none of the 18 studied megafaunal species can
recruit enough poles for self replacement. Twelve of those species did not recruit poles under
other species, resulting in the recruitment category 4 (unable to recruit). These results can be
explained by the density dependent effect also named the Janzel-Connel effect, where the
seed mortality is correlated with seed density which attracts predators and pathogens (Janzen
1970b; Connell 1971; Beaune et al. 2012b). In the absence of an endozoochoric partner such
as the elephant, this “putting all your eggs in one basket” adaptation is likely to turn out as a
maladaptation, unless a tree-species has alternative dispersal partners or mechanisms. Within
the megafaunal community we found four species with recruits beneath non parental trees
demonstrating alternative seed dispersal. However their pole density was lower than the
current adults’ density found in the forest except for one species: A. mannii.
With demographic analysis, six species seem to be resilient without elephants: A. mannii, D.
gossweileri, I. grandifolia, P. excelsa and K. gabonensis. But only A. mannii and D.
gossweileri show an exponential demography characteristic of trees. These species are likely
to be dispersed by other agents that are efficient enough to allow a high recruitment of the
first cohort. Duiker species are known to disperse several large-seeded plants in African
tropics (Gautier-Hion et al. 1985; Feer 1995b). And scatter-hoarding rodents such as
Cricetomys emini for example can be secondary dispersers for some plants usually dispersed
by megafauna. In our site, this nocturnal rodent was observed and camera trapped catching
seeds >3cm. As demonstrated with Cricetomys kivuensis in an afromontane forest (Nyiramana
et al. 2011), this genus transports and buries seeds for later consumption. Part of these seeds
can germinate due to superabundant reserves, obliviousness or death of the animal. The 12
other described species currently seem to not recruit sufficiently to maintain their population
and could be qualified as elephant-dependent. Therefore, elephant decrease affects the largest
proportion of megafaunal-tree reproduction, not yet visible in the grown-up forest, however
already visible in the understory looking at several generations of recruits.
For resilient species able to recruit without elephants, the spatial patterning could change.
New generations of megafaunal species are distributed differently from the adults. The spatial
pattern of the young cohort is more similar to autochoric species (clumped) while the adult
pattern is more similar to animal-dispersed species (random). Even if secondary dispersers
180
such as rodents allow certain megafaunal species to recruit, the next population would be
clumped with consequences for inter-populational genetic exchange (Hamrick & Trapnell
2011) and increased mortality due to density effects (Burkey 1994). In addition to seed
dispersal, absence of gut passage could affect germination success. As (Nchanji & Plumptre
2003) showed, unpassed seeds revealed both a longer germination time and a lower growth
rate compared to seeds passed in elephants.
These results illustrate that megafaunal species cannot rely on barochory for recruitment.
However, even if it was possible to recruit in the surrounding area of the adult trees as for A.
mannii, D. gossweileri, P. excelsa, etc. , this dispersal pattern would be different and
problematic for range expansion, genetic structure and metapopulation dynamics (Levin et al.
2003). In the megafaunal community, we can conclude that all the species, except A. mannii,
seem to be elephant-dependent. In summary, our results show that the first step in population
dynamics is compromised without elephants, with weaker or even non-existent self
recruitment for the elephant-dependent species.
In the southern area of the Congo River, bonobos, the second biggest frugivores, are unable to
replace elephants as seed dispersers, as the seeds are too large to be swallowed. They may
contribute in some cases to dispersal outside the fruit fall zone by short distance
ectozoochoric transport, similar to what can be dispersed by rodents (Forget & Wall 2001).
For I. gabonensis, M. africana, A. mannii, bonobos can be considered as a poor disperser,
dispersing over much shorter distances than elephants and omitting passage through their
digestive tract.
Unfortunately for the elephant-dependent tree community, elephants have vanished from
numerous forests. Healthy adult trees producing fruits remain in structurally intact in forests,
empty of elephants and often of other large/medium fauna (Wilkie & Carpenter 1999). This so
called empty forest syndrome (Redford 1992; Terborgh et al. 2008) occurs everywhere in
overhunted forests giving the illusion that plant communities are still fine despite the lack of
animals. Since recruitment and population dynamics of trees take longer than animal
dynamics and go beyond human life time, ignorance to the change is widespread. Several
studies described the first changes in recruitment due to changes in seed dispersal (Asquith,
Wright & Clauss 1997; Chapman & Onderdonk 1998a; Andresen & Laurance 2007;
Babweteera, Savill & Brown 2007; Muller-Landau 2007; Wright et al. 2007; Terborgh et al.
181
2008; Vanthomme, Bellé & Forget 2010a), and recent models of forest defaunation show
alteration of plant reproduction, with changes after each generation and clear consequences
for the future of our forests (Muller-Landau 2007). This study closes the loop by
demonstrating the decline or absence of the last cohort likely to have been produced during
the decades of elephant massacres (after the 1980s). The doom of the large dispersal vector
might trigger a radical change in the forest composition, probably with a new era for the wind
and ballistic dispersed trees (Beaune et al. in prep).
Looking closely at the primate-Irvingia seed dispersal commensalism, however, it’s not only
the tree species that is on the losing side. Numerous primate species include fruits of Irvingia
in their diet. Certain populations use it massively during the fructification season as shown
with drill (Mandrillus leucophaeus) (Astaras, Muhlenberg & Waltert 2008), bonobos and
chimpanzees (see. Annex 2). Irvingia is only one of many elephant dependent tree species
that highlight the cascade effect that is likely to occur with elephant extinction: first on the
direct mutualists, such as the elephant-dependent trees, second on their consumers, third on all
species depending on the consumers for endo- and ectozoochory, et cetera. However, this will
take at least a tree lifespan’s time. At Gashaka for example, a study site in Nigeria, where
elephants have been extinct for more than 50 years, chimpanzees still eat bush mangos
(Fowler personal communication), as do bonobos in some areas in DRC such as at Wamba
and other sites (see appendix 1).
Taking into consideration that some of these trees, already on the 1
st
level of this cascade, are
valuable for humans with respect to supplies such as nutrition, medicine construction material
and economic aspects (
Table 9), the following steps have to be included in conservation
management plans. There are several strategies to investigate.
1) artificial nurseries in National Parks, scientific stations, forest concessions and other places
where elephant preservation is not ensured in order to bridge the time till effective
conservation measures allow the elephant to rebuild viable populations; 2) law enforcement;
3) reintroduction.
The park, classified as a World Heritage Site in Danger since 1999, may soon turn into
another 33,346 km² of empty forest.
We invite all partners to join and contribute of the creation list of the species which cannot
reproduce without their endangered partners (contact authors). In order to create a web red list
of the species that needs artificial reproductive assistance for conservation in their ecosystem.
182
Species
location
elephant local status
P. paniscus
LuiKotale, DRC
1
poached
P. paniscus
Lomako, DRC
2
poached
P. paniscus
Wamba, DRC
3
extinct
P. troglodytes verus
Conkouati Douli, Congo
4
preserved
P. troglodytes verus
Gashaka, Nigeria
5
extinct
P. troglodytes verus
Tai, Ivory Coast
6
poached
P. troglodytes verus
Lopé, Gabon
7
poached
G. gorilla gorilla
Lopé, Gabon
poached
Table 11 Examples of great ape populations eating bush mango and local elephant status (ref: 1: this study, 2:
(Hohmann and Fruth 2000), 3: (Kano and Mulavwa 1984); Furuichi pers. comm. , 4: Renaud & Jamart pers.
comm., unpub. data., 5: Boesch comm. pers., 6: (White and Abernethy 1997))
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Conclusion
The most visible threat on tropical forest is habitat loss with deforestation. From 1990 to 2010
the world lost 135 million ha of forest area, including 75 million ha for Africa only (FAO
2010). However another serious problem although less visible is defaunation with the empty
forest syndrome (Redford 1992; Terborgh et al. 2008,
Figure 40). Defaunation affect all
large/medium animals in tropics, including apes in Africa (Bowen-Jones & Pendry 1999). In
DRC, at the southern bank of the Congo River, bonobos are the largest primates and sole
representing of apes.
Figure 40 Empty forest syndrome and the possible effect on the plant community scenario.
The ecological role of the bonobo project shows that bonobos are important seed disperser
(Part I). They provide seed dispersal service to the majority of the fruiting plants (probably
more than a hundred of plant species; 65% of the trees). All these plants are adapted to the
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bonobo endozoochory showing probable coevolution process with the apes. One of these
adaptations is the seed coat adapted to the apes’ gut passage and the need to be scarified to
activate or improve germination. As demonstrated with the Dialium mutualism, both partners
take advantage of the interaction. By imitation of these ecological processes we can
artificially trigger the germination of Dialium corbisieri as probably the great majority of the
Congo trees.
In this ecological story, numerous animals interact in the seed fate. For primary seed
dispersal, very low functional overlap occurs with bonobo and other primates. After
deposition: rodents, birds, Suidae and others can affect post dispersal survival (Part II). But
endozoochory with bonobo imply dung effect which attract secondary dispersers (dung
beetle) such as Catharsius that burrow the seeds and improve survival rate (Andresen & Feer
2005). Granivores are both seed predators and can act as secondary/tertiary seed dispersers
(Forget & Milleron 1991; Forget 1996; Forget et al. 2005; Forget & Cuiljpers 2008;
Nyiramana et al. 2011). However, while bonobos have crucial role in seed dispersers,
bonobos do not replace elephant ecological service for species with megafaunal syndrome and
by consequent elephant dependant. We show in this Congo forest specialized dispersal
(Nathan et al. 2008) for certain plants with elephant as vector.
The bonobo seed dispersal induce long dispersal events at an average distance >1km; thus
probably affecting populations’ structure. It is surprising to see that a fruit character does not
affect the behavior of their dispersal vector. Differential dispersal distance does not exist for
plant species sharing the same vector: bonobo (Part III).
To conclude, bonobo are important animals of the forest providing irreplaceable ecological
service. Unfortunately, bonobo are threatened of extinction (IUCN 2012) and their fate does
not improve with time. They are threatened by bushmeat trafficking (Hart et al. 2008a;
Reinartz et al. 2008) which growth with human demography. The forest might change unless
bonobo efforts for conservation are not seriously managed.
See appendix for few organizations involved in bonobo conservation.
185
186
Synthèse
L’étude des derniers grands singes découverts par la science est récente ; et l’intérêt
porté à Pan paniscus ne cesse de croître depuis ses quelques décades d’existence scienifique.
Figure 41. Or très peu de sujets concernent le rôle écologique de cette espèce (cf : Pan
paniscus myths and realities) gravement menacée d’extinction par le braconnage, les maladies
humano-simiennes et la dégradation de l’habitat (Dudley et al. 2002; Hart et al. 2008a; IUCN
2012; Tranquilli et al. 2012) : (Deforestation throughout the ape’s range). Les bonobos
peuplent une vaste partie des forêts du bassin du Congo, et ce, depuis plusieurs millions
d’années. Quels sont les risques de la disparition annoncée de ces grands singes sur
l’écosystème ? Jusque-là les réponses restèrent incertaines. Les arguments en faveur de la
conservation des bonobos étaient principalement d’origines philosophiques, morales (avec la
proximité filiale que nous autres humains partageons avec les bonobos, et scientifiques (pour
comprendre nos origines communes d’il y a 5 à 6 millions d’années (Cavalieri & Singer
1993). Évidemment, le caractère frugivore des bonobos n’a pas échappé aux écologistes et
leur rôle dans la dispersion de graines a été souligné (Caldecott & Miles 2005; Tsuji,
Yangozene & Sakamaki 2010). Cependant, la quantification de la dispersion de graine,
l’efficacité (viabilité, distance de dispersion, etc.), la diversification et la complexité des
interactions écologiques des bonobos n’a pas été étudiée. L’histoire écologique des bonobos
avec leur milieu est une ébauche. Grâce à la communauté habituée de bonobo à LuiKotale, le
projet ‘rôle écologique des bonobos’ apporte des réponses.
Nous avons vue dans la partie introductive (Seed dispersal strategies and the threat of
defaunation in a Congo forest) que dans la forêt mixe de LuiKotale la grande majorité des
plantes utilise les animaux comme vecteur de dispersion de leurs graines. L’inventaire quasi
exhaustif des plantes de l’écosystème a permis une estimation de la part des plantes zoochores
de 88 % dans la communauté végétale. Peu d’études ont permis une telle estimation dans un
écosystème Afrotropical (Gautier-Hion et al. 1985). De plus, cette partie montre bien le
problème de pression de chasse humaine qui vise essentiellement les animaux de grandes
tailles et les frugivores disperseurs de graine. Cette défaunation sélective pourrait défavoriser
la majorité des plantes à fruits dispersées par les bonobos, éléphants, cercopithèques et autres
coq congolais. Mais pour cela il est nécessaire de quantifier la dispersion de graine des
vecteurs tels que les bonobos : l’objet de la présente thèse.
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0
10
20
30
40
50
60
70
80
90
1985
1987
1989
1991
1993
1995
1997
1999
2001
2003
2005
2007
2009
2011
Years
Number of publication/year
Figure 41 Nombre de publications scientifiques par année contenant le terme « Pan paniscus » référencé par ISI
Web of Knowledge THOMSON REUTERS, dans le titre (vert) et dans le sujet (rouge).
L’écologie de la dispersion des graines est une science jeune mais vigoureuse (Forget et al.
2011). Ces travaux ne sont pas révolutionnaires dans le domaine. Mais ils apportent une
vision large, proche de l’exhaustivité, des interactions de Pan paniscus avec les autres espèces
de l’écosystème : plantes à fruits, compétiteurs, granivores, disperseurs secondaires et
alternatifs de graines, etc. Les études des interactions plante-animal concernent souvent un
modèle à deux espèces (Jordano 2000; Jordano, Bascompte & Olesen 2003b). Néanmoins, les
observations en milieux naturelles, la discrétion, la rareté des espèces ou la difficulté du
terrain d’étude permettent rarement d’aller au-delà de la description d’un mutualisme entre les
deux espèces (Schupp, Jordano & Gomez 2010). Or les interactions avec d’autres espèces, la
quantification de ces interactions, et les paramètres de l’efficacité des bénéfices réciproques
sont essentiels à la compréhension des interactions écologiques. Dans la partie I (Bonobo
(Pan paniscus) seed dispersal service in tropical forest in the Democratic Republic of
Congo), nous pouvons estimer avec combien d’espèces de plantes les bonobos agissent
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comme vecteurs de dispersion des graines : 91 espèces. Grâce à l’inventaire botanique
effectué sur le site d’étude (Fruth 2011), nous pouvons estimer à 40 % les nombres d’espèces
d’arbres dont les graines sont dispersées par les bonobos. Par ailleurs des données inédites sur
la biologie de l’espèce, le comportement alimentaire et de déplacement ont été étudié. Ainsi,
les différents paramètres permettent d’estimer la pluie de graines induites par un bonobo au
cours de sa vie : 11,6 millions de graines dispersées. La zoochorie récemment décrite chez les
bonobos (Hohmann & Fruth 2008; Surbeck & Hohmann 2008; Surbeck et al. 2009) peut être
ici quantifiée dans le régime alimentaire grâce à 1879 heures d’observations
comportementales : 0.9 %. Avec les analyses fécales, nous pouvons noter le biais induit par
l’utilisation seule des fèces dans les études d’écologie alimentaire chez les primates et le
risque de conclusions inexactes (McGrew et al. 2007; Hofreiter et al. 2010; Hohmann et al.
2010).
Déterminer quels sont les interactions plantes-bonobos est une chose, mais il faut déterminer
l’exclusivité de ces interactions : d’autres disperseurs peuvent ils remplacer les bonobos ou les
plantes peuvent-elles tout simplement se passer de disperseurs ? Dans cette première partie,
nous constatons que la grande majorité des arbres dispersés par les bonobos ne peuvent
recruter de nouvelles plantules sans dispersion. Par ailleurs, la redondance fonctionnelle avec
les autres singes de la communauté de primates semble faible aux vues des résultats
préliminaires d’une étude de 5 mois de terrains (Bourson 2011).
Le second chapitre de la première partie (Bonobo-Dialium mutualism) se concentre plus
spécifiquement sur le couple d’espèces : Bonobo et arbres du genre Dialium afin d’estimer
quantitativement et qualitativement les interactions plante-animal. Cette étude montre que
pour le grand singe, les fruits de Dialium sont une ressource importante de nourritures, au
cours de l’année et en termes de nutriments. Pour l’arbre, les graines sont dispersées
efficacement (selon les critères d’efficacité de dispersion (Schupp, Jordano & Gomez 2010))
et le passage des graines dans le tube digestif des bonobos briserait la dormance tégumentaire
et activerait ainsi la germination. Ce constat permettrait l’activation artificielle des graines de
Dialium par imitation du processus écologique. Les applications en biologie de la
conservation sont intéressantes et prometteuses (Artificial germination activation of Dialium
corbisieri by imitation of ecological process).
L’étude du comportement des bonobos ne fut pas en reste dans ce projet. Le comportement
animal et ses effets sur la pluie de graines, et donc la biologie des plantes, sont avérés
(Lambert & Garber 1998; Robertson et al. 2006; Russo, Portnoy & Augspurger 2006;
Kitamura et al. 2008). Le troisième chapitre de la partie III (How bonobos deal with tannin
189
concentrated fruits. Re-ingestion technique for Canarium schweinfurthii) montre que les
bonobos grâce à un comportement élaboré (ingestion et re-ingestion des fruits de Canarium
schweinfurthii) peuvent être des vecteurs de dispersions malgré la haute teneur en tannins qui
écartent certains consommateurs : mais pas les bonobos de LuiKotale. En effet, malgré la
présence des arbres sur leur territoire, il est intéressant de noter que ces fruits de Canarium
schweinfurthii ne sont pas consommés par la communauté de Lomako ou consommés de
manière différente (wadge technique) par les bonobos de la communauté de Wamba. Cette
recherche en cours pourrait être la première description d’une culture chez les bonobos vivant
en liberté (voir(Hohmann & Fruth 2003a), pour une revue sur la culture chez les bonobos).
Le comportement de déplacement alimentaire d’un animal influence la dispersion des graines
qu’ils transportent (Russo, Portnoy & Augspurger 2006; Nathan et al. 2008). Ici il est
surprenant de constater que la qualité et la quantité des fruits consommés par les bonobos ne
semble pas influencer la distance de dispersion des graines, toutes dispersés 24heures en
moyenne après ingestion, à 1.3 km en moyenne de l’arbre-parent. Ce fait assez étonnant ne va
pas en faveur de la limitation de recrutement des différences espèces dans la forêt comme
moteur de maintien de la biodiversité (McEuen & Curran 2004; Muller-Landau et al. 2008).
En effet, nos analyses préliminaires en écologie spatiale (données non publiées, en
collaboration avec le Dr B. Borgy (INRA)) semblent montrer qu’il n’existe pas d’agrégation
spatiale particulière des arbres à fruits. Les arbres dispersés par les bonobos auraient une
structure homogène dans la forêt. Mais le fossé entre la déposition d’une graine et sa survie à
l’âge adulte est grand et restera difficile à combler (Balcomb & Chapman 2003; Vander Wall
et al. 2005; Schupp, Jordano & Gomez 2010). Les perspectives de recherche sont donc
nombreuses : survie post dispersion des plantules ; influence du microsite ; écologie spatiale
avec analyse d’associations interspécifiques (les espèces dispersées par le même vecteur sont-
elles associées spatialement ?) ; le rôle des rongeurs dans la dispersion secondaire ; etc.
D’autres perspectives de recherche sont à envisager : l’étude de forêt jumelle avec et sans
bonobos (forêt de Lompole avec population de bonobo éteinte) ; quantification de la
défaunation avec recensement des prises ; défaunation diffreretielle ; carte mentale de
déplacement des bonobos ; icthyochory dans le bassin du Congo et effet de la pêche ;
zoochory des singes ripisylves (singes de Brazza : Cercopithecus neglectus ; singes des
marais : Allenopithecus nigroviridis) ; effet du passage des graines dans le tube digestif des
éléphants de forêts ; etc.
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Les interactions biotiques impliquant deux espèces sont rares dans les forêts tropicales
(Gautier-Hion et al. 1985). Ce projet explora naturellement les interactions avec d’autres
disperseurs (éléphants de forêt, cercopithèques, etc.), les disperseurs secondaires (bousiers) et
les prédateurs (Cricétomes, potamochères, etc.). Pour les graines, le premier chapitre de la
troisième partie montre que les potamochères sont d’importants prédateurs de graines à
LuiKotale et doivent être des espèces clefs pour la reproduction d’un tiers des arbres de la
communauté de LuiKotale. (Bush pig (Potamochoerus porcus) seed predation of bush mango
(Irvingia gabonensis) and other plant species in Democratic Republic of Congo). Les
rongeurs, bien que probable disperseurs secondaires à LuiKotale comme dans d’autres forêts
(Forget et al. 2005; Forget et al. 2006; Nyiramana et al. 2011) sont des prédateurs de graines
pour beaucoup de plantes. Or nous avons montré que la zoochory induite par les bonobos
attire les bousiers qui dans leur course aux matières fécales (NB : qui attirent aussi les
rongeurs) enterreront les graines et leur permettent d’échapper aux rongeurs de manière
efficace (deux fois plus (Dung beetles are critical in preventing post-dispersal seed removal
by rodents in Congo rain forest). Finalement, la présence de nombreux fruits présentant le
syndrome mégafaunale (Feer 1995a; Guimarães, Galetti & Jordano 2008) à LuiKotale, attira
l’étude des éléphants et les effets de leur disparition sur les populations de plantes
ancestralement dispersées. Ce dernier chapitre (Doom of the elephant-dependent trees in a
Congo tropical forest) montre que la majorité des espèces végétales présentant le syndrome
mégafaunale, sont en fait éléphants dépendants : ces arbres ne recrutent plus assez de jeunes
pour permettre la viabilité de leur population sans les irremplaçables éléphants de forêt. Les
bonobos ne remplacent pas les éléphants. Serait-ce une crise écologique similaire qui menace
les plantes dispersées par les derniers bonobos si ces derniers venaient à disparaître ?
De nouveaux et solides arguments viennent s’ajouter pour la préservation de Pan paniscus,
actuellement menacé d’extinction (IUCN 2012). Mais les mesures de conservation des
bonobos vont au-delà de la conservation de ces grands singes : il en va de la conservation de
l’ensemble de ces forêts du bassin du Congo.
191
List of abbreviations
ANOVA: ANAlysis of Variance
CI: Confidence interval
CNRS: Centre National de la Recherche Scientifique
DBH: Diameter at Breast Height
DPH : Differential Predation Hypothesis
df: degree of freedom
FRA : Forest Ressources Assessment
FAO : Food and Agriculture Organization
GPS : Global Positioning System
ha : Hectare (100 m by 100 m)
ICCN: Institut Congolais pour la Conservation de la Nature
IUCN: International Union for Conservation of Nature
LDD: Long Dispersal Distance
LK: LuiKotale
MPI: Max Planck Institute
MTT: Mean Transit Time
N: Sample size (number)
P: P-value
RDC: Democratic Republic of Congo
SE: Standard error
TT: Transit Time
UB: University of Burgundy/ Université de Bourgogne
192
Glossary
Some of the definitions are based on (Wang & Smith 2002; Vander Wall & Longland 2004;
Nathan et al. 2008)
Abundance: the number of individuals in a species that are found in a given area; abundance
is often measured by population size or population density.
Anemochory: seed dispersal by wind.
Arboreal: tree-living; referring to animals that are adapted to life in the trees.
Ballistic dispersal: abiotic dispersal by mechanical ejection of a seed from a fruit (does not
work as weapon).
Biodiversity: a term used to describe the diversity of important ecological entities that span
multiple spatial scales, from genes to species to communities.
Bonobology: studies of bonobos.
Coprophagy: feeding on excrement. Not tasty for most of the human.
Defaunation: extirpation of the medium/large animals from the system, often by overhunting.
Density-dependent: of or referring to a factor that causes birth rates, death rates, or dispersal
rates to change as the density of the population changes.
Diaspore: any propagative structure of a plant, especially one that is easily dispersed, such as
a seed.
Dispersal kernel: a probability density function characterizing the spatial distribution of
dispersal units originating from a common source. The ‘dispersal distance kernel’ describes
193
the probability of seed deposition at a certain distance, whereas the ‘dispersal density kernel’
describes the same probability per unit area. We use the former type throughout this review.
Dispersal limitation: recruitment limitation resulting from the failure of seeds to arrive at
favorable sites.
Dispersal vector: an agent transporting seeds or other dispersal units. Dispersal vectors can
be biotic (e.g. birds) or abiotic (e.g. wind). (A spacecraft is biotic).
Displays: visual messages, or body language, used by primates and other animals primarily to
communicate anger, fear, and other basic emotions.
Diurnal: being awake and active during the daylight hours but sleeping during the
nighttime. Most of the apes are diurnal exept certain night workers, insomniacs, perverts or
students.
Dominance hierarchy: a group of individuals arranged in rank order. In some non-human
primate species, each community has a distinct male and female dominance hierarchy. Every
individual is ranked relative to all other community members of the same gender. In the case
of rhesus macaque females, rank is determined by the relative rank of their mothers.
Depending on the species, male ranking may be similarly determined by the mother's rank or
it may be earned in competition with other males. Individuals who are higher in the
dominance hierarchy usually have greater access to food, sex, and other desirable things.
Ecological interaction: the relation between species that live together in a community;
specifically, the effect an individual of one species may exert on an individual of another
species.
Ecological niches: specific micro-habitats in nature to which populations or organisms
adapt. They are usually seen in terms of being food getting opportunities in the environment.
Ecosystem services: the beneficial outcomes, for the natural environment, or for people, that
results from ecosystem functions. Some examples of ecosystem services are seed dispersal,
support of the food chain, harvesting of animals or plants, clean water, or scenic views.
194
Egalitarian: (Primatology) lack of hierarchy or pecking order. Resources likely to be
obtained by whoever gets there first, rather than any social order.
Endozoochory: seed dispersal by vertebrates that ingest fruit and either regurgitate or
defecate seeds unharmed.
Estrus: the period of time when female animals are sexually excited and receptive to mating.
Estrus occurs around the time of ovulation in many species.
Ethogram: The behavioral repertoire of a species.
Fat-tailed dispersal kernel: a highly leptokurtic dispersal kernel, indicating relatively high
levels of LDD, formally defined as a kernel with a tail that drops off more slowly than that of
any negative exponential kernel.
Fission-Fusion: Chimp-like social structure where small groups go off together for periods of
time but then join up again later.
Foraging group: a group of animals that seek food together. In the case of non-human
primates, this group may consist of all community members or only some of them.
Free-ranging population: a non-captive group of primates or other animals that is living in
its natural habitat, largely free from constraints imposed by humans.
Frugivore: any animal that eats fruit.
Frugivory: consumption of fruits by animals. In this context, a broad definition is used
whereby frugivory need not involve ingestion and encompasses all seeds removed from the
plant by animals, including seeds in cheek pouches of primates or attached to coats by burs.
Fruiting/flowering phenology: the timing of the production of flowers and fruits.
Gene flow: the transfer of alleles from one population to another via the movement of
individuals or gametes.
195
Granivore: any animal that eats seeds.
Great apes: the gorillas, common chimpanzees, and bonobos of Africa and the orangutans of
Southeast Asia. These species are referred to as great apes because they are the largest apes.
Grooming: carefully picking through hair looking for insects, twigs, and other debris.
Guild: a subset of the species in a community that use the same resources, whether or not
they are taxonomically related.
Habitat fragmentation: the breaking up of once continuous habitat into a complex matrix of
spatially isolated habitat patches amid a human-dominated landscape.
Habitat loss: conversion of an ecosystem to another use by human activities
Habituation: The process where animals cease to change their behaviour because of the
presence of human observers.
Haplochory: seed dispersal by a single dispersal vector.
Hydrochory: seed dispersal by water.
Janzen–Connell hypothesis: postulates that a main benefit of seed dispersal is that it allows
seeds and seedlings to escape the high density-dependent mortality owing to pathogens, seed
predators, and/or herbivory that can occur directly under the parent plant.
Keystone species: a strongly interacting species that has a large effect on energy flow and on
community structure and composition disproportionate to its abundance or biomass.
Kurtosis: descriptor of the shape of a probability distribution, measure of the "peakedness" of
the probability distribution of a real-valued random variable.
Mutualism: A form of symbiosis in which both species benefit.
196
Non-equilibrium seed dispersal system: a seed dispersal system in which the relationships
between the animal species and plant species vary either in time and/or space. The relative
importance of the various subprocesses and constituent factors can also vary seasonally,
yearly or spatially.
Nonstandard dispersal vector: a dispersal vector different from the one that can be inferred
from the phenotypic characters of the plant.
Olfactory: the sense of smell.
Party: subgroup of bonobo after fission of the main group. No link with dancefloor or BBQ.
Philopatry: (Primatology) Where an individual stays in the natal group.
Polychory: seed dispersal by multiple dispersal vectors.
Primatology: the study of primates and their behavioral patterns.
Recruitment limitation: the failure of a species to establish in all sites that are favorable to
its growth and survival.
Quadrat: a sampling area (or volume) of any size or shape.
Scatter hoarding: a primary or secondary dispersal process by which an animal deposits food
resources (often seeds) in caches for later use. Unrecovered cached seeds are candidates for
germination.
Secondary dispersal: process by which seeds that are already on the ground are moved to
other locations; this dispersal is often mediated by ground-dwelling mammals (e.g. rodents,
tapirs, and forest antelopes) and insects (e.g. ants and dung beetles).
Seed deposition/placement: process by which seeds carried by dispersal agents are dropped
in new locations.
197
Seed dispersal cycle: a succession of processes whereby fruits produced by a plant are
removed by animals that disperse the seeds, some of which might germinate to seedlings and
recruit to adult plants, influencing the fruit availability of the next .
Seed dispersal: movement of seeds away from parent plants, usually by animal agents or by
wind, water, or intrinsic explosive mechanisms. Directed dispersal occurs when seeds are
deposited disproportionately in favorable locations.
Seed predation: action on seeds that renders those seeds nonviable for germination. Often
this predation occurs through ingestion by animals or by infestation of pathogens.
Seed rain: the pattern of seedfall to the ground. (more poetic than dung rain, isn’t it).
Seed shadow: the area on the ground where the seeds of a single tree either fall to the ground
or are placed by dispersers.
Seed: in a strict sense, the fertilized ovule of spermatophytes consisting of embryo,
endosperm and testa. We follow here the typical use of this term in the plant dispersal
literature as a synonym for a reproductive propagule.
Sexual dimorphism: referring to anatomical differences between males and females of the
same species. Primate males are usually significantly larger and more muscular than
females. Humans are also sexually dimorphic (usually).
Skewness: describe asymmetry from the normal distribution in a set of statistical data.
Skewness can come in the form of "negative skewness" or "positive skewness", depending on
whether data points are skewed to the left (negative skew) or to the right (positive skew) of
the data average.
Subadult: the stage of maturation in which animals are beyond infancy and early childhood
but are not yet fully grown.
198
Specialized dispersal: a dispersal system in which the plant exhibits phenotypic characters
that are interpreted as adaptations for dispersal by a particular vector. This vector is also
called the ‘standard dispersal vector.’
Terrestrial: referring to animals that spend most of their time on the ground rather than in the
air, water, or trees.
Type I survivorship curve: a survivorship curve in which newborns, juveniles, and young
adults all have high survival rates and death rates do not begin to increase greatly until old age
(e.g : modern human).
Type II survivorship curve: a survivorship curve in which individuals experience a constant
chance of surviving from one age to the next throughout their lives (e.g : bacteria).
Type III survivorship curve: a survivorship curve in which individuals die at very high rates
when they are young, but those that reach adulthood survive well later in life (e.g : tree).
Waypoint: a coordinate that is input into a navigation device, such as a GPS receiver,
representing a position that a vessel, aircarft, vehicle or person has to navigate to, with the aid
of GPS (and/or any other position fixing device).
199
Appendix
200
Density-dependent effects affecting elephant seed-dispersed tree recruitment (Irvingia
gabonensis) in Congo Forest
Authors
David Beaune, Loïc Bollache, Barbara Fruth, Gottfried Hohmann
François Bretagnolle
Accepted in Pachyderm
201
Several species are known to be important for local wildlife, rural communities (White &
Abernethy 1997) and even the “western world”. However little is know about the ecology of
these species and biodiversity crisis could change the population survival. Among these, the
bush mango (Irvingia gabonensis), widespread in West and Central Africa, is of major
importance for rural communities (Atangana et al. 2001; Leakey et al. 2005). Recently, the
plant is used as a slimming supplement in western world. Elephants are widely recognised as
the most important Irvingia seed dispersers in Africa (Theuerkauf et al. 2000; Nchanji &
Plumptre 2003; Morgan & Lee 2007). In this study we focus on this species as the example to
illustrate seed fate without dispersion and thus density dependence effect affecting tree
recruitment.
Here we conduct investigation on this megafaunal tree population’s ability to survive without
elephants in the evergreen lowland rainforest of the Max-Planck research site, LuiKotale, on
the South-Western fringe of the Salonga National Park, DRCongo. In and around Salonga
National Park, elephants (Loxondota cyclotis) have been severely poached for decades (Van
Krunkelsven, Bila-Isia & Draulans 2000; Blake et al. 2007), and poaching has increased with
increasing availability of automatic weapons (AK47) and ammunition after war. The current
nationwide elephant population is said to have declined by as much as two-thirds to that of the
1990’s and the remainder are said to survive in fragmented subpopulations (Alers et al. 1992).
Across 10 years of continuous presence at the research site at LuiKotale, the pressure on the
species became evident when leftovers from massacres were documented.
Overall, we aim to assess the ability of the I. gabonensis tree community at LuiKotale to
reproduce without elephant dispersal. If megafaunal trees depend on elephants for seed
dispersal, one would expect no alternative seed-dispersers and thus a high mortality of
seedlings and poles due to the density dependent effect (Paine et al. 2012).
202
Figure 42 Sampling area. Red spots representing adult trees
Methods
To investigate the density dependent effect on seed survival of this elephant-dependent tree,
we focused on all adult trees of Irvingia gabonensis inventoried since 2007 (LK-research-site
data base: all feeding trees within the bonobo-communities’ range, observed to be used by
Pan paniscus are geo-referenced (
Figure 42) that produced ripe fruits during the survey from
January 2010 to June 2011. We i) counted (1) seeds, (2) seedlings, (3) saplings, and (4) poles
in the fruit fall zone of each individual,. and ii) judged the state of each of the 4 stages of
growth, assessing pathogens and folivory by visual inspection (absence/presence of traces).
203
Figure 43 The density dependent effect of Irvingia gabonensis. No recruitment under the parental trees (n=54)
Results
We investigated 54 adult trees of Irvingia gabonensis (83.1cm± SE. 0.7 DBH) producing ripe
fruit.
Figure 43 shows the presence and state of (1) seeds, (2) seedlings (Figure 44), (3)
saplings, and (4) poles.
1) Seeds: Seeds were present within all fruit fall zones. Seeds revealed a loss rate of 54% ±
SE 3 due to seed predation and among the unopened seeds, 76% ± 4 were rotten or showed
signs of pathogen attacks. Red river hogs (Potamochoerus porcus) in herds of 2-6 animals
were found responsible for predating on large quantities of seeds cracking the endocarps.
2) Seedlings: Only 6 of the 54 trees (11%) showed seedling recruitment. Of these, all 90
seedlings were infested by pathogens or showed traces of folivory whereas some other
surrounding seedling species and the Irvingia of the nursery did not (unpub. data). Although
these adult trees reproduced, no established offspring (i.e. producing fruit) was found beneath
the adults’ crowns. A total of 48% (n=26) of the fruit fall zones clearly showed tracks of
animals’ road leading to the feeding place.
3) Saplings: A single sapling recruit (<2m high) was found below an adult crown.
4) Poles: No pole was found below an adult crown.
204
Figure 44 Seedling and adult tree of Irvingia gabonensis
Conclusion
Our results showed a high mortality for Irvingia seeds and recruits on all levels with a loss of
1) seeds, 54% due to predation and 76% due to pathogens; and 2) seedlings , 100% due to
predation and pathogens. These results can be explained by the density dependent effect also
named the Janzel-Connel effect (Janzen 1970b; Connell 1971; Burkey 1994) where the
mortality of seeds, eggs, or other immobile organisms is correlated with their density which
attracts predators and pathogens. In the absence of an endozoochoric partner such as the
elephant, this “putting all your eggs in one basket” adaptation is likely to turn out as a
maladaptation, unless a tree-species has alternative dispersal partners or mechanisms.
In the southern area of the Congo River, bonobos, the second biggest frugivores, are unable to
replace elephants as seed dispersers, as the seeds are too large to be swallowed. They may
contribute in some cases to dispersal outside the fruit fall zone by short distance
ectozoochoric transport, similar to what can be dispersed by rodents (Forget & Wall 2001).
For I. gabonensis, bonobos can be considered as a poor disperser, dispersing over much
shorter distances than elephants and omitting passage through their digestive tract.
205
Daily differences in bonobo activities: More sex in the morning?
Authors
David Beaune, Pamela Heidi Douglas
& Gottfried Hohmann
206
Abstract
This technical note for field primatologists demonstrates that behavioral activities are not
consistent throughout the day. In LuiKotale (DR Congo), a habituated group of bonobo (Pan
paniscus) was continuously followed in 2010 and 2011 (38 and 124 entire days of analyzable
data) for comparison of the morning and afternoon activities (midday=11 :30). While group
size, number of females, and feeding activity are similar, bonobos travel more in the
afternoon. Furthermore sexual activities show differences: bonobos copulate more in the
morning and homosexual interaction between females (GG rubbing) seems to be consistent
between morning and afternoon. This fact highlights the risk of bias in studies based on
number of hours observation. Preliminary observation during entire days is a prerequisite for
generalization of a behavior with bonobos and probably, other primates and animals.
Introduction
In behavioural studies, and particularly with primates, following free-ranging groups is
always an adventure. Habituation is an important stage, allowing scientists to follow animal
groups and collect relatively undisturbed behaviours. Often in remote areas with sampling
effort limitations, continuous data collection embracing twelve hours of daily activities is
challenging and unbalanced data can result from these logistical constraints. In primatology
literature, observation hours are sometimes indicated without precision of time consistency,
accepting the hypothesis that behaviours are similar and consistent throughout the day.
However, if daily activities are not regular throughout the day, and if observations are mainly
taken during a certain window of time, results will be biased: minored or majored. This note
tests this last hypothesis: no difference between morning and afternoon behavioural activities;
in a habituated group of wild bonobos in LuiKotale MPI field station (Hohmann & Fruth
2008; Surbeck & Hohmann 2008; Fowler & Hohmann 2010; Oelze et al. 2011). Morning and
afternoon activity budgets are compared through an examination of the following: 1) feeding
session; 2) travel (average speed); 3) group size; and 4) copulation rate. Since 2007, several
observers followed standardised methods of behavioural observation during bonobo daily
activities (between 5:30 AM and 5:30 PM).
207
Materials and methods
The study was carried out at the LuiKotale research site (S2°47’- E20°21’), located within the
equatorial rainforest, South West of Salonga National Park (DRCongo) (Mohneke & Fruth
2008). Field work with bonobos has been conducted since 2001 (Hohmann & Fruth 2003c)
with one habituated community of 35 bonobos (the Bompusa community) on a realm range of
60km² crossed by 76km of trails for access. Parties of bonobos were followed and observed
on a daily basis. However, during fieldwork, logistical limitations reduced the data length on
certain days and observations were stopped when the bonobos were lost. Only continuous
observations from nest to nest were compared. In this equatorial area, sunrise varies
minimally over the year, and bonobo activity can be split at midday, i.e., 11:30 AM.
For feeding activity, continuous feeding group scan observations (Altmann 1974) were used.
For travel activity, GPS Garmin
®
60CSX with track log (1 georeference/5mins) recorded the
bonobo position and average speed. Parametric data were tested by Student’s paired t-test.
The power analysis of the tests is specified when a difference is detected. Analyses were
performed using R 2.11 (R Development Core Team 2005).
Results
Feeding session
Fifty-one complete days were analysed and do not show a significant difference in bonobo
feeding activity, which represents more than half of the daily activities (i.e. 51%, see
Figure
45.1
). Paired t-test (t = -1.4899, df = 50, p-value = 0.14).
208
Figure 45 AM (left) and PM (right) comparison, 1. feeding activity, 2. average speed, 3. group size, 4.female
composition, 5. copulation rate, 6.GG rubbing rate,. NS= non significant difference.
209
Travel (average speed)
A hundred and twenty four complete days were analysed and average speed is significantly
different (Figure 45.2) (t = -3.7832, df = 123, p-value = 0.001, test power=90%).
Bonobo travel
15% (+0.07km/h) more in afternoon than in morning; from 0.40±0.17km/h in the morning to
0.46±0.16km/h in the afternoon.
Group size
Forty complete days were analysed and do not show any difference in group size with an
average of 9 individuals per group. (Fig1.3) Paired t-test: (t = 0.0058, df = 39, p-value =
0.99). The proportion of females does not change neither during between morning and
afternoon (Figure 45.4) (t = -0.1441, df = 38, p-value = 0.89)
Copulation rate
Forty complete days were analysed and show a significant difference in copulation rate
between morning and afternoon (Figure 45.5).
Paired t-test: t = 4.3071, df = 39, p-value < 0.001; test power=90%). The mean difference is
0.05 copulation/ind/hrs from AM to PM. The copulation peak occurs during the first hours of
daily activities.
GG rate
Thirty eight complete days were analysed and do not show significant difference in GG rate
between morning and afternoon (
Figure 45.6).
(t = 1.6792, df = 37, p-value = 0.1015)
Conclusion
Certain bonobo daily activities vary, such as travel or social activities. These data lead to two
conclusions: First, we logically cannot announce a behavioural rate, percentage or average
based solely on behavioural hours collection. Authors should assess the consistency of the
behaviour over the day before making comparisons such as those between bonobos and
chimpanzees because if the behaviour varies over the day, just recording hours of observation
1
210
does not give an accurate representation of the rate of the behaviour. An example might
concern the numerous debates about copulation rate comparison between bonobos and
chimpanzees (Takahata, Ihobe & Idani 1999; Hashimoto & Furuichi 2006) or among apes
population). We can remark that some of these rates are based on observation hours without
precision of daily consistency.
For the LK bonobo, the Bompousa community show a clear unbalanced copulation rate and a
calculation of the copulation rate based on the morning observation would be overestimated
and lead to numerous false hypothesis regarding the literature’s rates (0.11, 0.13, 0.18, 0.19
copulation/hours, (Stevens, Vervaecke & Elsacker 2008).
Secondly, behaviourists could improve their data collection effort by focusing their
observations in the best behavioural window regarding their need. If the study concerns
comparison (inter individual, inter communities) for example, researchers can focus on the
best time period where maximal activities needed occurs. This time window has to be
validated by preliminary daily collection. Similarly, if the behaviour of interest does not show
daily change, researchers can acquire data hours without daily time constraint.
211
Few organizations for bonobo conservation
Bonobo Alive
http://www.bonobo-alive.org
Bonobo Alive is an organisation initiated by bonobo researchers dedicated to the protection of
wild bonobos and their habitat in the south-western part of Salonga National Park, DR Congo.
The Bonobo Conservation Initiative
http://www.bonobo.org/
(BCI) is dedicated to ensuring the survival of the bonobo (Pan paniscus) and its tropical
forest habitat in the Congo Basin. By working with indigenous Congolese people through
cooperative conservation and community development programs, as well as on the national
and international levels, BCI is establishing new protected areas and leading efforts to
safeguard bonobos wherever they are found.
Lola ya Bonobo
http://www.friendsofbonobos.org/
212
http://www.lolayabonobo.org/
Founded by Claudine Andre in 1994, Lola ya Bonobo is the sanctuary of the NGO, Les Amis
des Bonobos du Congo (ABC). Since 2002, the sanctuary has been located at Les Petites
Chutes de la Lukaya, just outside of Kinshasa in the Democratic Republic of Congo.
And also:
http://mboumontour.org
http://www.worldwildlife.org/species/finder/bonobo/bonobo.html
http://www.awf.org/section/wildlife/bonobos
http://www.awely.org/fr/programmes/casquettes-vertes/republique-democratique-du-congo
213
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