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Species traits and habitatsin springtail communities: a 1
regional scale study 2
3
S. Salmon,J.F. Ponge 4
5
Muséum National d’Histoire Naturelle, CNRS UMR 7179, 4 avenue du Petit-Château, 6
91800 Brunoy France 7
8
Running title: Trait-habitat relationshipsin springtails 9
10
Corresponding author. Tel.: +33 6 78930133.
E-mail address:ponge@mnhn.fr (J.F. Ponge).
2
Abstract 1
Although much work has been done on factors patterning species trait assemblages in 2
emblematic groups such as plants and vertebrates, more remains to be done in 3
belowground invertebrate species. In particular,relationships between species traits and 4
habitat preferences are still a matter of debate. Springtails were sampled in a 5
heterogeneous landscape centered on the Sénart forest, near Paris (northern France), 6
embracingthe largest possible array of five environmental gradients (humus forms, 7
vegetation, moisture, vertical strata, and seasons) over which Collembola are known to 8
be distributed. Distances between samples varied from a few cm to several km. 9
Canonical correspondence analysis using species (128) as observations and species trait 10
attributes (30) and habitat indicators (82) as dependent and independent variables, 11
respectively, allowed to discern whether species habitats and species trait assemblages 12
were related and which trends could be found in trait/environment relationships. It was 13
concluded that, within the studied area, species habitatswere significantly associated 14
with species trait assemblages. The main gradient explaining the distribution of species 15
traits combined the vertical distribution of habitats (from the mineral soil to plant aerial 16
parts), and the openness of the environment, i.e. a complex of many ecological factors. 17
In the ecological traits of Collembola, this gradient corresponded to anincreasing 18
contribution of sensory and locomotory organs, bright color patterns, size and sexual 19
reproduction, all attributes associated with aboveground life under herbaceous cover. 20
Another important, although secondarycontrast concerned traits associated with habitats 21
far from soil but concealed (corticolous vs all other habitats). Soil acidity and water did 22
not contribute significantly to trait distribution, at least within the limits of our database. 23
Keywords:Collembola; species trait assemblages; habitats; trait-environment 24
relationships 25
3
Introduction 1
The indicative power of species trait assemblages has been intensively studied in 2
plants, birds and beetles and most species traits could be clearly related to habitat 3
preferences of species in these groups (Graves and Gotelli 1993; Ribera et al. 4
2001;Cornwell and Ackerly 2009; Mayfield et al 2009; Pavoine et al. 2011). 5
Surprisingly, although this is common sense and was reported for a long time in soil 6
zoology (Bornebusch 1930), few studies questioned whether the extraordinary diversity 7
of species traits which prevail in soil animal communities could be explained, and 8
potentially could have been selected, by differences in habitat use (Vandewalle et al. 9
2010; Decaëns et al. 2011; Bokhorst et al. 2011).Moreover, these studies focused either 10
on a restricted number of traits, or a restricted number of habitats which does not allow 11
providing general trends in relationships between species traits and habitat use. 12
The aim of our study was to determine trends that emerge from trait-13
environment relationships, i.e. how species traits vary along environmental gradients 14
(e.g. vegetation, soil, depth). 15
Among soil invertebrates, we selected springtails (Hexapoda, Collembola) as an 16
abundant and diversifiedmonophyletic group for which a great deal of work has been 17
devoted to the study of species/environment relationships at the community level (Poole 18
1962; Hågvar 1982; Ponge 1993; Chagnon et al. 2000; Auclerc et al. 2009). The Sénart 19
forest (Ile-de-France, northern France) and its vicinity were selected because they 20
display a great variety of soil and soil-related habitats (e.g. woodland, heathland, 21
grassland, ponds, paths, tree trunks) composing a little more than 3,000 ha of 22
heterogeneous landscape, now totally included in the Paris area. Data collected from 23
1973 to 1977, at a time when agriculture was still practiced both inside and outside the 24
4
forest, were revisited for a statistical analysis taking into account species 1
trait/environment relationships. The same pool of data (370 samples, 127 species) has 2
been already used in several studies dealing with species/environment relationships 3
(Ponge 1980, 1983, 1993) and was included in the COLTRAIT data base 4
[http://www.bdd-inee.cnrs.fr/spip.php?article51&lang=en], which also comprises data 5
about twelve morphological and life-history traits of more than 300 collembolan 6
species. 7
Materials and Methods 8
Site description 9
The Sénart state forest (3,000 ha) is located 20 km south-east of Paris on the 10
western border of the Brie plateau, delineated by a meander of river Seine and by a 11
tributary, the river Yerres, at an altitude ranging from 50 to 87 m a.s.l. At the time of 12
sampling it was mainly bordered by urbanized areas (communes of Quincy-sous-Sénart, 13
Boussy-Saint-Antoine, Brunoy, Yerres, Montgeron, Draveil) on its western and 14
northern parts, and by agricultural areas (communes of Soisy, Étiolles, Tigery, 15
Lieusaint, Combs-la-Ville) on its eastern and southern parts. Nowadays, the forest is 16
totally included in the metropolitan area of Paris. Private peripheral woods and 17
agricultural areas (cultures and meadows) were included in the study. Most of them 18
have now been incorporated into the state forest, to the exception of peripheral 19
agricultural areas which have been built or transformed into golf courses or other 20
recreational areas.A number of soil types can be observed in the Sénart forest, varying 21
according to the nature of quaternary deposits (loess or gravels) and permanent or 22
seasonal waterlogging resulting from clay migration (perched water tables) or 23
5
underlying impervious clay strata (permanent water tables). More details were given in 1
previously published papers (Ponge 1980, 1983, 1993). 2
Sampling procedure 3
Sampling took place from 15th October 1973 to 10th October 1977 in every 4
season and every kind of weather, our purpose being to embrace all climate conditions, 5
except when the soil was deeply frozen and could not be sampled at all. At each 6
sampling time, a point was randomly selected, around which all visible sitespotentially 7
available to springtails were investigated, from deep soil (leached mineral horizons) to 8
tree trunks two meters aboveground and to floating vegetation in water-filled ponds. No 9
effort was made to standardize sampling, the only requirement being to collect enough 10
litter (at all stages of decomposition), vegetation (aerial and subterranean parts), bark 11
(naked or covered with lichens or mosses) or soil (organo-mineral to mineral horizons) 12
to have enough animals as possible in each sample, the aim of the study being to know 13
which species were living together in the same micro-habitat and which species were 14
not.The volume sampled varied from 100 mL for moss cushions, which are particularly 15
rich in springtails (Gerson 1982) to 1 L for bleached mineral soil horizons which are 16
strongly impoverished in fauna (Hågvar 1983). Care was taken not to undersample 17
some poorly represented habitats. For that purpose some additional sampling was done 18
in agricultural areas, calcareous soils and dumping places. This procedure allows 19
environmental gradients to be better described (Gillison and Liswanti 2004). 20
Samples were taken with the help of a shovel for soil, and with fingersfor above-21
ground samples, care being taken not to lose too many jumping animals in particular 22
when sampling aerial parts of erected plants. No attempt was done to force a corer into 23
the soil. Samples were immediately put in plastic bags then transported to the nearby 24
6
laboratory, to be extracted on the same day. Extraction was done by the dry funnel 1
(Berlese) method over 10 days, using 25 W bulb lamps in order to avoid too rapid 2
desiccation of the samples, known to prevent slowly moving animals from escaping 3
actively the samples (Nef 1960). Animals were collected and preserved in 95% ethyl 4
alcohol in plastic jars. A total of 310 samples were collected and kept for the analysis. 5
Species identification 6
Animals were sorted in Petri dishes filled with ethyl alcohol then springtails 7
were mounted and cleared in chloral-lactophenol to be identified under a light 8
microscope at x 400 magnification. At the time of study the only key available for 9
European springtails was that of Gisin (1960), to which were added numerous detailed 10
published studies at family, genus or species level (complete list available upon 11
request), and miscellaneous (unpublished) additions by Gisin himself. Color patterns 12
were noted before animals were discolored in chloral-lactophenol. Young specimens, 13
when not identifiable to species level, were allocated to known species by reference to 14
adults or subadults found in the same sample, or in samples taken in the vicinity. For 15
instance in the genus Mesaphorura, where several species may cohabit and diagnostic 16
characters are not revealed in the first instar (Rusek 1980), unidentified juveniles were 17
proportionally assigned to species on the base of identified specimens found in the same 18
sample. Gisin’s nomenclature was updated using Fauna Europaea 2011 19
[http://www.faunaeur.org/]. A total of 128 species were found (Table 1). 20
Trait data 21
Twelve traits, mostly extracted from the COLTRAIT data base and collected 22
from numerous identification keys or synopses, describe morphology and reproductive 23
mode of the 128 species used in the analysis. Attributes of each trait (Table 3) were 24
7
considered as variables, and were coded as binary (dummy) variables, resulting in a list 1
of 30 attributes: mode of reproduction (parthenogenesis dominant, sexual reproduction 2
dominant), body size (small, medium, large), body form (cylindrical body, stocky body, 3
spherical body), body color (pale-colored, bright-colored, dark-colored), scales (absent, 4
present), antenna size (short, long), leg size (short, long), furcula size (absent or 5
vestigial, short, long), eyenumber (0, 1-5, > 5), pseudocella (absent, present), post-6
antennal organ (absent, simple, compound), and trichobothria (absent, present). 7
Antennae, eyes, post-antennal organsand trichobothria are supposed to play a sensory 8
role (Hopkin 1997). 9
Species habitat data 10
Field notes were used to classify habitat features (sensu lato, including micro-11
habitat and season) in 82 categories (Table 2). To each sample was thus assigned a set 12
of 82 habitat indicators which describe its main features at varying scales, from landuse 13
(heathland, grassland, woodland) to sampling plot (e.g. ditch, plain ground, pond, 14
vegetation, soil pH) then to within-plot scale (e.g. plant part, litter, earthworm casts, 15
mineral soil). Species presence was indicated by dummy variables (coded as 0 or 1) for 16
each of the 82 habitat categories. 17
Statistical treatment of the data 18
Canonical correspondence analysis was used to analyze trait-habitat 19
relationships (species as observations, species trait attributes as dependent variables, 20
species habitatsas constraining variables), permutation tests being used to test trait-21
habitat associations. 22
Rarefaction curves were calculated to estimate the exhaustiveness of our 23
sampling method.Rarefaction curves and jacknife estimators were calculated using 24
8
EstimateS (version 8.2.0).All other calculations were done using XLSTAT® 1
(Addinsoft®, Paris, France). 2
Results 3
The rarefaction curve of the 128 observed species showed that sampling had 4
approached an asymptote. Estimating the number of missing species according to Chao 5
(1987) put the expected total number of species for the Sénart forest to 133 and 6
indicated that the sampling was relatively exhaustive. 7
Canonical Correspondence Analysis (CCA)with species trait attributes as 8
explained variables and species habitats as explanatory variables showed that traits were 9
significantly explained by habitats (number or permutations = 500, pseudo-F = 0.94, P < 10
0.0001). Constrained variance (variance of species traits explained by species habitats) 11
represented 72.9% of the total variance. 12
The first two canonical components of CCA extracted 54% of the constrained 13
(explained) variance (40% and 14% for F1 and F2, respectively). The projection of trait 14
attributes and species in the F1-F2 plane is shown in Figures 1a and 1b, respectively. 15
Both species and trait attributes were distributed along three dimensions. Species with 16
pseudocella and post-antennal organ present (of compound type), parthenogenesis 17
dominant, regressed locomotory (furcula, legs) and sensorial organs (eyes, antennae, 18
thichobothria), and pale color were opposed to species displaying opposite attributes 19
along F1. According to principal coordinates of species habitats (Table 2) this 20
corresponded to opposite habitats: woodland vs grasslandand depth versus surface, from 21
negative to positive sides of F1. Heathland was in an intermediate position between 22
woodland and grassland (Table 2). Mineral soil, organo-mineral soil, humus (organic), 23
litter, plant aerial parts ranked in this order along F1. Sunlight was projected on the 24
9
positive side of F1 (open environments).The second canonical component F2 was more 1
specifically linked to corticolous microhabitats (trunks, wood and associated mosses 2
and lichens): associated trait attributes were short furcula, stocky and dark-colored 3
body, eyes present but in regressed number (1-5), post-antennal organ present but 4
simple. Acidity and humus type, as well as water, did not exhibit any pronounced 5
influence on species trait attributes. Partial CCA, allowing only water and soil acidity 6
(including humus type) to vary, showed that they did not influence the distribution of 7
trait attributes (pseudo-F = 0.17, P = 0.99). 8
Discussion 9
Previous studies showed that a limited number of ecological factors could 10
explain the distribution of collembolan species when collected in the same geographical 11
context, at a regional scale (Ponge 1993; Ponge et al. 2003). Vertical distribution is the 12
main gradient along which most springtail species are distributed (Hågvar 1983; Faber 13
and Joosse1993; Ponge 2000a), followed by the contrast between woodland and 14
grassland (Ponge et al. 2003), and other factors such as water availability (Verhoef and 15
Van Selm 1983) and soil acidity (Loranger et al. 2001). We showed that grassland and 16
epigeic habitats were mostly characterized by traits adapting species to surface life: big 17
size, high mobility, protection against desiccation by round shape or cuticular clothing 18
(Kaersgaard et al. 2004), avoidance of predation by flight and color signaling, and 19
sexual reproduction (Fig. 1, Table 2, F1 component, positive side). On the oppositeside, 20
woodland and endogeic habitats were mostly characterized by traits associated with 21
subterranean life: small size, small locomotory appendages, poor protection from 22
desiccation, avoidance of predation by toxic excreta (pseudocella), and parthenogenesis. 23
10
Much life in woodland is more concealed than in grassland: smaller forms, more 1
sensitive to environmental stress because of a higher surface/volume ratio (Kærsgaard et 2
al. 2004;Bokhorst et al. 2012), and less motile species (Auclerc et al. 2009), can find in 3
woodland better conditions for survival and reproduction. Mebes and Filser (1997) 4
showed that surface dispersal of Collembola was much more intense in agricultural 5
fields compared to adjoining shrubby fallows where litter began to accumulate, and 6
Alvarez et al. (1997, 2000) highlighted the role of hedgerows as temporary refuges for 7
species living at the surface of arable fields.Sexual reproduction needs easy-to-visit sites 8
for the deposition of spermatophores by males (Chahartaghi et al. 2006), and movement 9
in search of mating partners using olfactory or tactile clues (Chernova et al. 2010), 10
which is easier in surface than in depth, in the same sense as escape from predators 11
needs visual or tactile sensory organs to detect their presence (Baatrup et al. 2006) and 12
needs jumping movements (ensured by furcula acting as a spring) for fleeing away 13
(Bauer and Christian 1987). The fractionation of space within leaf or needle litter 14
horizons makes the forest floor improper to rapid surface movements (Bauer and 15
Christian 1987), while protecting soil-dwelling animals from surface predation by 16
carabids and vertebrates (Hossie and Murray 2010) and offering a variety of food 17
resources such as fungal colonies and animal excreta (Bengtsson et al. 1991; Salmon 18
and Ponge 2001). Other predators are subterranean and cannot be avoided through 19
active movements, hence the use of chemical repellents excreted by pseudocella 20
(Dettner et al. 1996; Negri 2004). 21
Despite clear trends of trait/habitat relationships exhibited by our results, 22
possible biases due to escape movements during sampling, in particular from the part of 23
big-size animals with long furcula, should not be overlooked. If such biases differ from 24
a habitat to another, this may flaw trait/habitat relationships. However, concerning the 25
11
association between big size and agricultural environments, which is novel to science, it 1
must be highlighted that it was less easy to collect vary motile specimens in the absence 2
of litter (i.e. in agricultural areas) than when litter was present (i.e. in forest areas), 3
stemming in a bias in quite opposite direction to the observed association. This made us 4
confident that such biases were not present in our dataset. 5
The second canonical component of trait-environment relationships (Fig. 1, 6
Table 2, F2 component) distinguishes traits associated with life in bark and associated 7
mosses and lichens: the combination of short furcula, dark color, stocky body, eyes 8
present but in limited number is an original adaptation to life in concealed environments 9
(hence small size and limited movements) but far from soil (hence the need to be 10
protected from UV radiation through pigmentation and possibilities offered by vision). 11
The structure of the post-antennal organ, opposing simple to compound structure (more 12
typical of edaphic habitat) is worthy of note, since no other studies considered its 13
ecological correlates. The exact role played by this organ is still unknown, but 14
anatomical observations on the innervation of these pitted porous plates located not far 15
from the protocerebrum point to sensory activity (Altner and Thies 1976). Differences 16
between simple and compound post-antennal organs concern the number of dendritic 17
branches, which are more numerous in compound organs (Altner and Thies 1976), 18
suggesting that compound post-antennal organs are more sensitive to chemical features 19
of the immediate environment. The higher sensitivity of the compound post-antennal 20
organ could be more adapted to deeper horizons by compensating the reduction or the 21
complete absence of other sense organs such as eyes. 22
The fact that we did not discern any association between traits and obvious 23
factors such as water and soil acidity (or humus type) does not preclude any further 24
scrutiny of such relationships. Two reasons could be invoked.First, that, in its present 25
12
state, our database did not cover the traits needed to establish this relationship. Ponge 1
(2000b) showed that acidophilic and acidophobic species cohabited within the same 2
lineage, pointing to corresponding traits as mainly based on physiology (mechanisms 3
counteracting oxidative stress) rather than on anatomy and reproduction mode. Traits 4
associated with aquatic life concern mainly the form and size of claws (Gisin 1960), and 5
of course physiology (resistance to desiccation), which were not considered here. 6
Second, in the particular case of the Senart forest, traits adapting species to habitats 7
varying in terms of water availability and/or soil acidity could be masked by landuse or 8
vertical stratification effects, pointing to the need for studying trait/habitat relationships 9
on a wider geographic scale, as suggested by Lepetz et al. (2009). 10
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18
1
Code Species name Abundance
Number of
samples
Code Spe cies name Abundance
Number of
samples
ACA Arrhopalites caecus 23 6 MKR Mesaphorura krausbaueri 813 69
AEL Anurida ellipsoides 12 4MMA Mesaphorura macrochaeta 2962 102
AFU Allacma fusca 1 1 MMI Megalothorax minimus 963 105
AGA Allacma gallica 5 2 MMS Mesaphorura massoudi 31 2
APR Arrhopalites principalis 9 7 MMT Micronychiurus minutus 1 1
APY Arrhopalites pygmaeus 13 7MMU Micranurophorus musci 5 1
ASE Arrhopalites sericus 24 8 MPY Micranurida pygmaea 829 72
BPA Brachystomella parvula 1036 33 MSE Micranurida sensillata 2 2
BVI Bourletiella viridescens 50 15 MYO Mesaphorura yosii 158 13
CAL Cyphoderus albinus 3 2 NDU Neonaphorura duboscqi 2 1
CBE Ceratophysella bengtssoni 436 4 NMU Neanura muscorum 115 53
CBI Cryptopygus bipunctatus 2 1 NNO Neonaphorura novemspina 1 1
CDE Ceratophysella denticulata 117 16 NRA Neotullbergia ramicuspis 28 2
CEX Cryptopygus exilis 4 3 OAM Onychiurus ambulans 2 2
CMA Caprainea marginata 9 2 OCI Orchesella cincta 1460 81
CSC Cryptopygus scapelliferus 22 3 OCR Oncopodura crassicornis 5 3
CTH Cryptopygus thermophilus 13 2 OPS Onychiuroides pseudogranulosus 347 13
DFL Deuterosminthurus flavus 7 5 OVI Orchesella villosa 167 44
DFI Deuteraphorura fimetaria 1 1 PAL Pseudosinella alba 279 51
DFU Dicyrtoma fusca 34 19 PAQ Podura aquatica 410 7
DJU Detriturus jubilarius 1 1 PAS Pseudachorutella asigillata 16 5
DMI Dicyrtomina minuta 56 30 PAU Protaphorura aurantiaca 740 24
DTI Desoria tigrina 1192 5 PCA Paratullbergia callipygos 430 53
EAL Entomobrya albocincta 120 17 PDE Pseudosinella decipiens 7 6
ELA Entomobrya lanuginosa 39 13 PLO Pogonognathellus longicornis 7 5
EMA Entomobrya multifasciata 166 11 PMA Pseudosinella mauli 430 48
EMU Entomobrya muscorum 17 15 PMI Proisotoma minima 156 25
ENI Entomobrya nivalis 74 8 PMU Proisotoma minuta 212 10
EPU Entomobryoides purpurascens 11 2 PNO Parisotoma notabilis 6095 180
FCA Folsomia candida 60 9PPA Pseudachorutes parvulus 229 35
FCL Friesea claviseta 67 11 PPE Pseudosinella petterseni 1 1
FMA Folsomia manolachei 6274 101 PPO Pseudosinella pongei 12 4
FMI Friesea mirabilis 109 13 PSE Pseudisotoma sensibilis 1464 12
FPA Folsomides parvulus 145 13 PSU Protaphorura subuliginata 193 20
FQU Folsomia quadrioculata 1810 45 SAQ Sminthurides aquaticus 1 1
FQS Fasciosminthurus quinquefasciatus 2 2 SAS Sminthurides assimilis 78 12
FTR Friesea truncata 361 57 SAU Sminthurinus aureus aureus 1054 75
GFL Gisinianus flammeolus 98 6 SDE Stenaphorurella denisi 32 5
HCL Heterosminthurus claviger 3 1 SEL Sminthurinus elegans 95 21
HIN Heterosminthurus insignis 33 7 SLA Superodontella lamellifera 4 3
HMA Heteromurus major 594 71 SMA Sminthurides malmgreni 591 43
HNI Heteromurus nitidus 28 18 SNI Sminthurus nigromaculatus 16 9
HPU Hypogastrura purpurescens 1 1 SPA Sminthurides parvulus 82 13
IAN Isotomurus antennalis 1 1 SPS Subisotoma pusilla 82 5
IMI Isotomiella minor 2136 116 SPU Sphaeridia pumilis 1566 107
IPA Isotomurus palustris 1483 101 SQU Stenaphorurella quadrispina 7 3
IPR Isotomodes productus 4 1 SSC Sminthurides schoetti 401 44
ISP Isotomodes sp. 2 2 SSE Schaefferia sexoculata 1 1
IVI Isotoma viridis 54 13 SSI Sminthurinus aureus signatus 2407 97
KBU Kalaphorura burmeisteri 30 5 STR Sminthurinus reticulatus 1 1
LCU Lepidocyrtus curvicollis 72 26 SVI Stenacidia violacea 6 2
LCY Lepidocyrtus cyaneus 889 35 TBO Tomocerus botanicus 35 9
LLA Lepidocyrtus lanuginosus 3399 160 TMI Tomocerus minor 312 45
LLI Lepidocyrtus lignorum 565 63 VAR Vertagopus arboreus 788 31
LLU Lipothrix lubbocki 15 6 WAN Willemia anophthalma 577 35
LPA Lepidocyrtus paradoxus 2 2 WBU Willemia buddenbrocki 5 3
LVI Lepidocyrtus violaceus 4 4 WIN Willemia intermedia 1 1
MAB Micraphorura absoloni 3 2 WNI Willowsia nigromaculata 3 1
MBE Mesaphorura betschi 12 6 WPO Wankeliella pongei 2 1
MGR Monobella grassei 32 14 XBR Xenylla brevisimilis 2 1
MHG Mesaphorura hygrophila 1 1 XGR Xenylla grisea 361 19
MHY Mesaphorura hylophila 633 42 XSC Xenylla schillei 18 5
MIN Megalothorax incertus 12 9 XTU Xenylla tullbergi 4673 68
MIT Mesaphorura italica 21 9XXA Xenylla xavieri 33 5
Table 1. Codes and species names of springtails collected in the Senart forest from 1973 to 1977, total abundance, and number of samples in
which the species was found. Species names according to Fauna Europaea 2011
19
1
2
Number of
samples
F1 F2
Number of
samples
F1 F2
Autumn 96 0.045 0.084 Hornbeam 42 -0.046 0.037
Winter 108 0.162 0.051 Linden 22 -0.012 0.001
Spring 88 0.091 0.035 Maple 8 0.053 0.049
Summer 46 0.109 0.030 Ash 8 0.011 0.026
Grassland 50 0.136 -0.021 Cherry 9 0.097 -0.066
Woodland 279 -0.124 0.006 Elm 3 0.170 0.057
Heathland 9 0.064 0.029 Elder 3 0.112 -0.012
Ditch/brook 44 0.106 0.059 Hazel 11 -0.027 -0.040
Pond 64 0.140 0.056 Pine 12 0.007 0.021
Plain ground 230 0.027 -0.011 Calluna 6 0.009 0.076
Water 107 0.078 0.023 Blackberry 5 0.124 -0.002
Sunlight 141 0.230 0.074 Ivy 4 0.013 0.036
pH < 5 32 0.030 0.102 Peat moss 18 0.022 0.071
pH 5-6 35 0.024 -0.003 Hair moss 5 0.183 0.008
pH > 6 32 -0.052 -0.069 Feathermoss 8 0.030 0.102
Limestone 48 0.002 -0.009 Liverwort 1 0.156 -0.041
Sand 20 -0.062 -0.009 Lichens 4 0.082 0.140
Pebbles 23 0.057 -0.004 Algae 3 0.155 0.023
Mull 57 -0.121 -0.036 Bracken 21 0.014 0.044
Moder 24 -0.090 0.046 Purple moor grass 21 0.108 0.039
Mor 2 0.086 -0.027 Hair-grass 5 0.084 -0.028
Hydromull 6 -0.019 -0.019 Fescue-like grass 8 0.201 -0.016
Hydromoder 3 -0.030 0.004 Rushes 6 0.219 -0.013
Hydromor 3 -0.017 0.021 Waterlilies 10 0.132 0.021
Trunk 33 0.108 0.143 Hawksbeard 1 0.121 -0.003
Herbs (aerial parts) 58 0.296 0.077 Sedges 4 0.078 0.016
Mosses (aerial parts) 74 0.163 0.146 Wood anemone 20 -0.037 0.045
Superficial soil 17 0.146 0.003 Bluebell 20 -0.037 0.045
Litter 80 0.213 0.068 Duckweed 1 0.121 0.007
Humus 41 0.136 0.043 Mustard 1 0.062 0.024
Organo-mineral soil 18 -0.049 -0.032 Chamomile 1 -0.013 -0.008
Mineral soil 68 -0.172 -0.111 Chickweed 9 0.053 -0.078
Mole hill 4 0.028 -0.007 Yarrow 4 0.003 -0.051
Vertebrate dung 3 0.181 0.010 Nettle 5 -0.046 -0.047
Garbage deposits 11 -0.045 0.058 Mercury 16 0.036 0.022
Wood 35 0.093 0.132 Solomon's seal 8 0.053 0.049
Earthworm casts 7 -0.036 -0.013 Wheat 7 -0.011 -0.051
Tree roots 5 0.067 0.053 Buttercup 1 0.142 -0.041
Herb roots 8 0.083 -0.006 Knotweed 1 0.091 0.037
Oak 142 -0.048 0.015 Clover 5 -0.091 -0.038
Birch 41 0.113 0.026 Mint 1 0.123 0.001
Table 2. Habitat indicators, number of samples where indicators were quoted as 1 and principal coordinates
along the two first components of CCA. F1 component (40% of explained variance) is linked to landuse and
depth. F2 component (14% of explained variance) is linked more specifically to corticolous micro-habitats
20
1
2
Trait Attribute
Number of
species
Mode of reproduction Parthenogenesis dominant 36
Sexual reproduction dominant 89
Body size Small 86
Medium 28
Large 14
Body form Slender 92
Stocky 6
Spheric 30
Body color Pale-coloured 60
Bright-coloured 30
Dark-coloured 38
Scales Absent 109
Present 19
Antenna size Short 65
Long 63
Leg size Short 61
Long 67
Furcula size Absent or vestigial 35
Short 25
Long 68
Eye number 0 42
1-5 24
> 5 62
Pseudocella Absent 105
Present 23
Post-antennal organ Absent 69
Simple 21
Compound 38
Trichobothria Absent 72
Present 56
Table 3. Trait attributes of the 128 springtail species collected in the Sénart
forest, and number of species where attributes were found
21
Figure legends 1
Figure 1.Canonical correspondence analysis of species trait attributes: projection of 2
traits (a) and habitat indicators (b) in the plane of the first two canonical factors 3
F1 and F2. 4
5
22
1
Fig. 1 2
Parthenogenesis dominant
Sexual reproduction
dominant
Small Medium
Large
Slender body
Stocky body
Spheric body
Pale-colored body Bright-coloured body
Dark-colored body
Scales absent
Scales present
Short antennae
Long antennae
Short legs
Long legs
Furcula absent or vestigial
Short furcula
Long furcula
Eyes absent
Eyes 1-5
Eyes > 5
Pseudocella absent
Pseudocella present
Post-antennal organ
absent
Post-antennal organ
simple
Post-antennal organ
compound
Trichobothria absent
Trichobothria present
F1
F2
a)
Autumn
Winter
Spring Summer
GRASSLAND
WOODLAND
HEATHLAND
Ditch/broo k Pond
Plain ground
Water
Sunlight
Limestone
Sand Pebbles
Trunk
Mole hill
Vertebrate dung
Garbage deposits
Superficial soil
Litter
Humus
Organo-miner al soil
Mineral soil
Wood
Earthworm casts
Tree roots
Herb roots
pH < 5
pH 5-6
pH > 6
Mull
Moder
Mor
Hydromull
Hydromoder
Hydromor
Oak
Birch
Hornbeam
Linden
Maple
Ash
Cherry
Elm
Willow
Elder
Hazel
Pine
Calluna
Blackberry
Ivy
Mosses (aerial parts)
Peat moss
Hair moss
Feathermoss
Liverwort
Lichens
Algae
Herbs (aerial parts)
Bracken Purp le moor grass
Hair-grass
Fescue-like grass
Rushes
Waterlilies
Hawksbeard
Sedges
Wood anemone
Bluebell
Duckweed
Mustard
Chamomile
Chickweed
Yarrow
Nettle
Mercury
Solomon' s seal
Wheat
Buttercup
Knotweed
Clover
Mint
F1
F2
b)
