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Decreased biodiversity in soil springtail communities: the importance of dispersal and landuse history in heterogeneous landscapes

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Jean-François Ponge at Muséum National d'Histoire Naturelle
Jean-François Ponge
Florence Dubs
Florence Dubs
Servane Gillet
Servane Gillet
Servane Gillet
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Jose Paulo Sousa at University of Coimbra
Jose Paulo Sousa
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Abstract

In previously published papers it had been demonstrated that at the local level the species richness of soil springtail communities was negatively influenced by landuse diversity. When the dispersal rate of soil animals was taken into account, quite opposite trends were displayed by species having poor or high dispersal capabilities. At the local level, species with short legs, non functional jumping apparatus and reduction of visual organs were distinguished against by landuse diversity, while species with long legs, functional jumping apparatus (furcula) and complete eyes, thus able to disperse at the soil surface, were not. It was verified, through aerial photographs taken 50 years ago, that landuse changes, expected to be more frequent in heterogeneous landscapes, may contribute to explain this phenomenon.
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1
Type of contribution: Short communication 1
2
Date of preparation of the revised version: 2005-09-02 3
4
Number of text pages: 8 5
6
Number of tables: 2 7
8
Number of figures: 1 9
10
Title: Decreased biodiversity in soil springtail communities: the importance of dispersal 11
and landuse history in heterogeneous landscapes 12
13
Jean-François Ponge1, Florence Dubs2, Servane Gillet1, Jose Paulo Sousa3, Patrick Lavelle2 14
15
1Muséum National d’Histoire Naturelle, CNRS UMR 5176, 4 avenue du Petit-Chateau, 91800 16
Brunoy, France 17
2Institut de Recherche pour le Développement, UMR 137 BioSol, 32 rue Henri Varagnat, 93143 18
Bondy Cédex, France 19
3Universidade de Coimbra, Instituto do Ambiente e Vida, Lg. Marquês de Pombal, 3004-517 20
Coimbra, Portugal 21
22
Correspondence: Jean-François Ponge, Muséum National d’Histoire Naturelle, CNRS UMR 5176, 4
avenue du Petit-Chateau, 91800 Brunoy, France. E-mail: jean-francois.ponge@wanadoo.fr
2
Abstract 1
2
In previously published papers it had been demonstrated that at the local level the species 3
richness of soil springtail communities was negatively influenced by landuse diversity. When the 4
dispersal rate of soil animals was taken into account, quite opposite trends were displayed by 5
species having poor or high dispersal capabilities. At the local level, species with short legs, non 6
functional jumping aparatus and reduction of visual organs were distinguished against by landuse 7
diversity, while species with long legs, functional jumping apparatus (furcula) and complete eyes, 8
thus able to disperse at the soil surface, were not. It was verified, through aerial photographs taken 9
fifty years ago, that landuse changes, expected to be more frequent in heterogeneous landscapes, 10
may contribute to explain this phenomenon. 11
12
Keywords: Landuse intensification, Springtails, Landuse diversity, Dispersal rate 13
14
In a previous study conducted within the BioAssess EC program, we have shown that the 15
springtail species richness of core samples (local biodiversity) was inversely related to landuse 16
diversity along a gradient of landuse intensification (Ponge et al., 2003), while an opposite trend 17
was displayed by plant species (Fédoroff et al., 2005). We hypothesized that, in the studied region, 18
heterogeneous landscapes were most subject to changes in landuse history, to which soil animals 19
were lesser adapted than plant forms. To test this hypothesis we decided to revisit our data set, by 20
taking into account the dispersal abilities of the different springtail species, and the landuse 21
changes that occurred over the last half century. 22
23
Sampling took place in the Morvan Regional Nature Park (western Burgundy, Centre of 24
France). Six landuse units (LUUs), one square kilometer each, have been chosen on the basis of 25
aerial photographs, taking into account the distribution of forested areas (coniferous, deciduous), 26
meadows and agricultural crops. LLUs 1 to 6 depicted a gradient of increasing influence of human 27
3
activities. Soil and climate conditions, as well as landuses, were described in two previously 1
published papers (Ponge et al., 2003; Fédoroff et al., 2005). The distribution of landuse types in the 2
six LUUs is shown in Table 1. In each LUU the diversity of landuse types was expressed by the 3
Shannon Index. 4
5
Using aerial photographs, a grid of 16 regularly spaced plots (200 m) was identified in each 6
of the six LUUs. Sampling of Collembola took place in June 2001. Methods used for sampling, 7
extraction, sorting and identification of Collembola at the species level were detailed in Ponge et al. 8
(2003). One sample was discarded for extraction, because of waterlogging at the time of sampling. 9
10
Collembolan species were classified in two groups, according to their ability to disperse 11
actively or not (Table 2). Species with long legs and antenna, a developed jumping apparatus 12
(furcula) and complete visual apparatus (8 ocella per eye spot) were considered able to disperse 13
rapidly by their own means (Hopkin, 1997). All other species, because of a reduction in motion or 14
vision organs, were considered as having poor dispersal capabilities. It has been demonstrated that 15
fully functional visual organs allow springtails to move directionally over long distances (Hågvar, 16
1995). Conversely, springtails showing a reduction in their eye number, even when fully motile, 17
exhibit negative phototaxis and thus cannot disperse easily (Salmon and Ponge, 1998). 18
19
Ecological requirements of Collembolan species were derived from the distribution of 20
species over all samples (n = 95), which was studied by multivariate analysis (Ponge et al., 2003). 21
Axis 1 coordinates of correspondence analysis (CA) in Ponge et al. (2003) were used to separate 22
forest from agricultural species (Table 2). It should be noted that the environmental gradient 23
depicted by the first axis of CA was a combination of all factors which contrasted woodland and 24
agricultural land, humus type included. 25
26
4
Ancient aerial photographs (1948 IGN campaign) were examined for each LUU, in order to 1
identify the landuse type which prevailed at the place where sampling took place in 2001. Black 2
and white photographs easily distinguished woodland, agricultural land, and hedgerows, but could 3
not be used for finer resolution. Thus landuse types were gathered into two gross categories, 4
namely woodland (deciduous and coniferous forests) and agricultural land (hay meadows, pastures, 5
arable crops, recent fallows). Hedgerows (one sample) and clear-cuts (two samples) were not taken 6
into account in the census. Afforested land was comprised of 10- to 50-yr-old coniferous 7
plantations (Douglas fir, Norway spruce) and old fields (wooded fallows). 8
9
When landuse units were ordered according to increasing landuse diversity (Table 1), the 10
balance between the two springtail categories changed markedly (Fig. 1). Slow-dispersal species 11
were largely dominant in forested areas, decreasing from LUU 1 to LUU 4, while the fast-dispersal 12
species increased. In the most diverse landscape (LUU 4) fast-dispersal and slow-dispersal species 13
were at the same richness level. In areas dominated by agriculture (LUU 5 and LUU 6), slow-14
dispersal species were also dominant, but to a lower extent than in areas dominated by forests 15
(LUU1 and LUU2). The mean species richness of slow-dispersal Collembola was negatively 16
correlated with landuse diversity (r = -0.93, P = 0.003), while fast-dispersal species were positively, 17
but poorly correlated with landuse diversity (r = 0.68, P = 0.07). 18
19
Examination of past landuse revealed that some changes took place over the last half 20
century. Eight samples were taken in places where there was a shift from agricultural land to 21
woodland (afforestation), while two samples were taken in places where woodland was replaced by 22
agricultural land (deforestation). Calculation of the impact of landuse change on local species 23
richness of springtail communities was only possible in afforested sites. It revealed a deficit of 24
species richness in sites where agricultural land was afforested (8.4±1.1), compared to stable 25
woodland (13.2±0.6, Mann-Whitney U = 54.5, P = 0.001). When springtail species were separated 26
in two dispersal groups, still clearer features appeared. In afforested land, the richness of slow-27
5
dispersal species was equal to that of the original agricultural land (i.e. near half that of woodland), 1
while the richness of fast-dispersal species decreased to the level typical of woodland, i.e. near half 2
that of agricultural land. While dominance of slow- over fast-dispersal species was prominent in 3
woodland as well as agricultural land, afforested land displayed the reverse phenomenon. The 4
examination of ecological requirements of species (forest vs agricultural species) showed that in 5
afforested land fast-dispersal species were shared between forest (57%) and agricultural species 6
(43%), while nearly all slow-dispersal species were still those typical of agricultural soils (88%). 7
8
We found that (i) the heterogeneity of the landscape exerted a negative influence on slow-9
dispersal collembolan species, (ii) at least part of these effects could be explained by time-related 10
processes, acting differentially on organisms with distinct life habits. 11
12
Soil collembolan communities are negatively affected by deforestation as well as 13
afforestation and this impact was shown to be durable (Jordana et al., 1987; Deharveng, 1996). The 14
contrast between closed and open habitats is one of the chief complex of factors which govern the 15
species composition of most soil animal groups (Nordström and Rundgren, 1974; Ponge, 1993). 16
Soil and climate factors are in play in the influence of landuse change on soil animal communities, 17
more especially when agricultural land shifts to woodland, or the reverse. However, in the present 18
state of our knowledge of ecological requirements and dispersal abilities of Collembola, only 19
cursory explanation can be found for the observed changes in species composition and diversity, 20
which are summarized below. 21
22
In the present study, the passage from agricultural land to woodland was accompanied by 23
soil acidification (Ponge et al., 2003). In mixed landscapes, the higher acidity of the soil in woody 24
areas is not solely due to the acidifying influence of forest growth (Nilsson et al. 1982) but also to 25
(i) the choice of more fertile (thus less acidic) soils for agriculture and (ii) the fertilization 26
associated with the permanent use of land for agriculture (Brady and Weil, 1999). Soil acidity and 27
6
associated factors influence the species composition of most soil animal communities (Nordström 1
and Rundgren, 1974; Wauthy, 1982; Ponge, 1993), but they affect primarily species in permanent 2
contact with humified organic matter (Ponge, 1993). 3
4
Micro-climate changes affect primarily soil animal species living at the soil surface or not 5
far from it, with agricultural land exhibiting more contrasting thermic and hygric conditions than 6
woodland at the ground surface (Coffin and Urban, 1993). In springtails, it has been demonstrated 7
that the first instar, i.e. the first stage of development following egg hatching, was more sensitive to 8
desiccation that further instars and that this phenomenon was more pronounced in woodland than in 9
agricultural land species (Betsch and Vannier, 1977). 10
11
Slow-dispersal Collembola, contrary to fast-dispersal species, are favoured by forest 12
environments. Most of them need a protection towards desiccation, because they are badly 13
equipped for jumping rapidly from a micro-site to another in a changing environment (Bauer and 14
Christian, 1987). Most species classified in the slow-dispersal category are soil-dwelling species, to 15
the exception of small surface species, such as Xenylla spp. and Brachystomella parvula, which 16
live under the protection of mosses and lichens or exhibit anhydrobiosis (André, 1976; Poinsot-17
Balaguer, 1976). 18
19
In a complex landscape where forest and agricultural land are intimately mixed, two 20
categories of underground biodiversity should be considered apart: those organisms which are able 21
to disperse at the scale of landscape heterogeneity (these communities will be positively or not 22
affected by heterogeneity, here fast-dispersal springtails), and those unable to do that, which will be 23
negatively affected except those tolerant of landuse changes. Examination of literature shows that 24
most springtail species which are considered of particular interest, because they are endemic or 25
rare, fall into the slow-dispersal category, thus are threatened by landuse changes (Barrocas et al., 26
1998; Deharveng, 1996; Lauga-Reyrel and Deconchat, 1999). 27
7
1
Acknowledgements 2
3
The authors thank the staff of the Morvan Regional Nature Park and numerous private 4
owners for facilities during choice of sites and sampling operations. This study was part of the 5
European Community program BioAssess EVK2-CT-1999-00041, coordinated by A. Watt (UK), 6
who is gratefully acknowledged for financial support and fruitful exchange of ideas between 7
participants. 8
9
References 10
11
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Bauer, T., Christian, E., 1987. Habitat dependent differences in the flight behaviour of Collembola. 19
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Betsch, J.M., Vannier, G., 1977. Caractérisation de deux phases juvéniles d’Allacma fusca 22
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Brady, N.C., Weil, R.R., 1999. The Nature and Properties of Soils, 12th edn. Prentice Hall, Upper 26
Saddle River. 27
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dynamics: comparisons of a grassland and a forest. Ecological Modelling 67, 147-178. 3
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Pyrenees (France). Conservation Biology 10, 74-84. 6
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Fédoroff, E., Ponge, J.F., Dubs, F., Fernández-González, F., Lavelle, P., 2005. Small-scale 8
response of plant species to land-use intensification. Agriculture, Ecosystems and 9
Environment 105, 283-290. 10
11
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Hypogastrura socialis (Uzel). Acta Zoologica Fennica 196, 200-205. 13
14
Hopkin, S.P., 1997. Biology of the Springtails. Oxford University Press, Oxford. 15
16
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(Northern Spain). Revue Suisse de Zoologie 94, 491-502. 19
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Lauga-Reyrel, F., Deconchat, M., 1999. Diversity within the Collembola community in fragmented 21
coppice forests in south-western France. European Journal of Soil Biology 35, 177-187. 22
23
Nilsson, S.I., Miller, H.G., Miller, J.D., 1982. Forest growth as a possible cause of soil and water 24
acidification: an examination of the concepts. Oikos 39, 40-49. 25
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Sweden. Pedobiologia 14, 1-27. 2
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Poinsot-Balaguer, N., 1976. Dynamique des communautés de Collemboles en milieu xérique 4
méditerranéen. Pedobiologia 16, 1-17. 5
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Ponge, J.F., 1993. Biocenoses of Collembola in atlantic grass-woodland ecosystems. Pedobiologia 7
37, 223-244. 8
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Ponge, J.F., Gillet, S., Dubs, F., Fédoroff, E., Haese, L., Sousa, J.P., Lavelle, P., 2003. Collembolan 10
communities as bioindicators of landuse intensification. Soil Biology and Biochemistry 35, 11
813-826. 12
13
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Soil Biology 34, 199-201. 15
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19
10
LU U 1 LU U 2 LU U 6 LU U 3 LU U 5 LU U 4
Dec iduo us forest 16 1 0 8 3 0
Con ifer ous forest 0 14 0 2 2 3
Clear-cut 0 1 0 0 0 1
Hedgerow 0 0 0 0 1 0
Hay m eadow 0 0 0 4 4 4
Past u re 0 0 2 1 6 3
Fallow 0 0 5 0 0 1
A rable crop 0 0 9 1 0 3
Not sam pled 0 0 0 0 0 1
Shannon Index 0 0 .6 7 1.3 7 1.8 8 2.1 1 2.4 2
Table 1. D istributio n of land use types am ong the six land use unit s (LUUs), ordered acco rdin g to
in creasing landuse div ers ity. Sixteen sam ples w ere tak en in each LU U, ex cept LUU 4 w it h f ifteen
sam ples only
1
2
3
11
AA nu rid a granaria FA llacm a fusc a
AA nu rid a unif orm is ADeu teros mint hurus sulp hu reu s
FA rrhopalit es bifid us ADic yrtom a fusca
FA rrhopalit es sp. ADic yrtom ina minut a
ABrachy st om ella parvula ADic yrtom ina ornat a
FCerat op hy sella ar mat a AEntom ob rya m ult ifas ciat a
ACerat op hy sella den ticulata FEntom ob rya n ivalis
FCerat op hy sella lu teospina AFasc iosm in th urus q uinquef asc iat us
ACyphoderus alb inus AIsotom a an tennalis
AFolso mia c andid a AIsotom a tig rin a
AFolso mia f im etaria AIsotom a vir idis
FFolso mia q uadrioculata AIso to muru s palustris
FFriesea c lav iset a ALepid oc yrt us cyan eus
FFriesea m irabilis FLep idocyrtus lan ugin osus
FFriesea t ru ncata ALepid ocy rtus lig no rum
AHet eromurus nitid us FLipothrix lu bb ocki
FIsotom iella m inor FOrc hesella c incta
FIsotom od es p roductus AOrc hesella q uinquef asc iat a
AKalap horura burm eisteri AO rches ella v illos a
FM egalot horax m inim us FPogonognat hellus flav escen s
FM esap ho rura bet sc hi FPseu diso to ma sen sibilis
FM esap ho rura jevanica ASmin th urid es parvulu s
FM esap ho rura leit zaensis ASm inthurides schoet ti
FM esap ho rura m acro ch aet a ASmin th urin us aur eus
FM esap ho rura yosii ASmin th urin us nig er
FM icran urid a pygmaea FSmin th urin us sig natus
FM icran urid a sensillat a ASm inthuru s nig rom aculatus
FM icrap horura ab solo ni ASm inthurus viridis
FNeanura m uscorum ASphaeridia pu milis
FNeelides m inutus ASten acidia vio lac ea
ANeo tu llberg ia ram ic uspis FTo mocerus m in or
FOncopodu ra cr ass ico rnis FV ert agopus arboreus
FOnychiu roid es pseu do gran ulosu s AW illow sia nig rom aculata
FOnychiu rus c eben narius
AOnychiu rus jubilariu s
FParatullbergia callipygos
AParisotoma n ot abilis
FProisotom a m inim a
AProtap ho rura ar mat a
AProtap ho rura m eridiata
AProtap ho rura prolata
FPseu dachoru tes parvulu s
APseu danuro ph orus binoculatus
APseu do sin ella alba
APseu do sin ella illiciens
FPseu do sin ella mauli
ASpinonychiu rus edin ensis
ASten aphor ura denisi
ASten aphor ura quadrisp ina
FW illemia an op ht halm a
FW illemia den isi
FW illemia in termedia
FX enylla grisea
FX enylla t ullberg i
FX enyllodes arm atus
Slow -dispersal
Table 2. Lis t of collem bolan s pecies fo und in t he st ud y sites, classified
ac cordin g to their abilit y ot d isperse (estim at ed by append age and ey e
dev elo pm ent ). F = forest species. A = agricult ural species
1
12
Figure captions 1
2
Fig. 1. Local species richness of fast- and slow-dispersal springtail communities along a gradient of 3
increasing landuse diversity. The two springtail categories were compared at each LUU by 4
Mann-Whitney non-parametric tests. N.S. = not significant, ** = P<0.01, *** = P<0.001. 5
Bars are standard errors of the means. Within each category, LUUs were compared by 6
repeated Mann-Whitney non-parametric tests, the significance of differences between 7
groups (at P 0.05) being indicated by common letters (a, b for fast-dispersal species, x, y, z 8
for slow-dispersal species) 9
10
13
0
1
2
3
4
5
6
7
8
9
10
11
12
13
LUU 1
LUU 2
LUU 6
LUU 3
LUU 5
LUU 4
Species richness of a Collembolan sample
Slow-dispersal species
Fast-dispersal species
***
***
**
N.S.
***
***
a
bb
ab ab
a
x
xy
y
z
y
y
1
Fig. 1 2

Supplementary resource (1)

Collembola Morvan
Data
October 2022
Servane Gillet · Jean-François Ponge
... Previous studies showed that moister micro-climate conditions provided by tree canopies affects positively Collembola richness and influences community structure towards a higher relative abundance of euedaphic species (Martins da Silva et al., 2012, 2016Salmon et al., 2014;Rossetti et al., 2015;Joimel et al., 2021). In contrast, the relative abundance of epigeics species is usually higher in open habitats, such as grasslands and open landscapes (Alvarez et al., 2000;Ponge et al., 2006;Martins da Silva et al., 2012;Salmon et al., 2014;Harta et al., 2021), as they are usually faster dispersers and more resistant to desiccation and disturbances in the upper soil layers (Verhoef and Van Selm, 1983;Alvarez et al., 1999;Ponge et al., 2006;Bokhorst et al., 2012;Salmon and Ponge, 2012). Yet, the findings above are focused on the Mediterranean, Temperate or Boreal regions. ...
... Previous studies showed that moister micro-climate conditions provided by tree canopies affects positively Collembola richness and influences community structure towards a higher relative abundance of euedaphic species (Martins da Silva et al., 2012, 2016Salmon et al., 2014;Rossetti et al., 2015;Joimel et al., 2021). In contrast, the relative abundance of epigeics species is usually higher in open habitats, such as grasslands and open landscapes (Alvarez et al., 2000;Ponge et al., 2006;Martins da Silva et al., 2012;Salmon et al., 2014;Harta et al., 2021), as they are usually faster dispersers and more resistant to desiccation and disturbances in the upper soil layers (Verhoef and Van Selm, 1983;Alvarez et al., 1999;Ponge et al., 2006;Bokhorst et al., 2012;Salmon and Ponge, 2012). Yet, the findings above are focused on the Mediterranean, Temperate or Boreal regions. ...
... We expected that community traits of life-form would accurately indicate the influence of tree canopy on collembolan functional diversity. Based on previous observations in temperate and Mediterranean regions (e.g., Ponge et al., 2006;Salmon and Ponge, 2012;Salmon et al., 2014;Martins da Silva et al., 2016), we predicted that tree canopy influence collembolan richness and diversity in forested environments due to an increase in the relative abundance of euedaphics. Most euedaphics are expected to be particularly favored by local suitable microhabitat conditions promoted by closed canopy environments, as they are slower moving and are not equipped with traits protecting them against desiccation (Ponge et al., 2006;Bokhorst et al., 2012;Winck et al., 2017), such as larger body size or cuticular impermeability (Salmon and Ponge, 2012). ...
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... But additionally, their larger body size, longer appendages and fully functional visual organs provide these epigeic species with a greater dispersal capacity (Ojala & Huhta, 2001), which allows them to migrate to avoid adverse conditions and choose more favourable micro-habitats within their home range (Chauvat et al., 2014;Ponge et al., 2006), ultimately making them more resilient against local disturbances (Lindberg & Bengtsson, 2006;Malmström, 2012). ...
... This behavioural difference may be behind the observed relative edaphization of springtail assemblages under the experimental drought. Atmobiotic and epigeic species may have dispersed seeking for better patches nearby (Chauvat et al., 2014;Ojala & Huhta, 2001;Ponge et al., 2006) after experiencing between 2 up to 4 years of drought, while euedaphic species were still there likely retreated below and perhaps migrating across the soil profile tracking the daily variation in moisture (Detsis, 2000;Hopkin, 1997). Indeed, the soil matrix provides a remarkable buffering capacity against environmental variation (Geiger et al., 2009). ...
Trait‐mediated responses to aridity and experimental drought by springtail communities across Europe
Article
Full-text available
The capacity to forecast the effects of climate change on biodiversity largely relies on identifying traits capturing mechanistic relationships with the environment through standardized field experiments distributed across relevant spatial scales. The effects of short‐term experimental manipulations on local communities may overlap with regional climate gradients that have been operating during longer time periods. However, to the best of our knowledge, there are no studies simultaneously assessing such long‐term macroecological drivers with local climate manipulations. We analysed this issue with springtails (Class Collembola), one of the dominant soil fauna groups, in a standardized climate manipulation experiment conducted across six European countries encompassing broad climate gradients. We combined community data (near 20K specimens classified into 102 species) with 22 eco‐morphological traits and reconstructed their phylogenetic relationships to track the evolution of adaptations to live at different soil depths, which is key to cope with desiccation. We then applied joint species distribution models to investigate the combined effect of the regional aridity gradient with the local experimental treatment (drought and warming) over the assembly of springtail communities and tested for significant trait–environment relationships mediating their community‐level responses. Our results show (1) a convergent evolution in all three major collembolan lineages of species adapted to inhabit at different soil strata; (2) a clear signature of aridity selecting traits of more epigeic species at a biogeographical scale and (3) the association of short‐term experimental drought with traits related to more euedaphic life‐forms. The hemiedaphic condition would be the plesiomorphic state for Collembola while the adaptations for an epigeic life would have been secondarily gained. Epigeic springtails are not only more resistant to drought, but also have a higher dispersal capacity that allows them to seek more favourable micro‐habitats after experiencing drier conditions. The observed relative edaphization of the springtail communities after short‐term experimental drought may thus be a transient community response. The disparity between macroecological trends and fast community‐level responses after climate manipulations highlights the need of simultaneously assessing long‐term and short‐term drivers at broad spatial scales to adequately interpret trait–environment relationships and better forecast biodiversity responses to climate change. Read the free Plain Language Summary for this article on the Journal blog.
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... The moss layer provided favourable habitats especially for very large surface-dwelling species (Cronberg, 2006;Rusek, 2007), including some highly mobile species (e.g., epigeic Entomobryomorpha, see Table S1 of Turnbull and Lindo, 2015). Species of this type are usually tolerant to disturbance (Farská et al., 2014;Ponge et al., 2006), but they are almost absent in our experimental field. Therefore, our study indicates that the functional composition of soil fauna in agroecosystems is more sensitive to intense rainfall than that in Fig. 3. Collembola density (upper row), CWM body size (mid row), and CWM eye number (lower row) along a soil water content gradient. ...
... Notably, the communities in manure-treated plots showed a bias towards species with well-developed furca but against those without furca. This response conforms to a general pattern observed under multiple land use effects (Farská et al., 2014;Ponge et al., 2006), and supports that Collemobla with a more active life form and higher dispersal ability are more tolerant to anthropogenic disturbance. ...
Ecological intensification alters the trait-based responses of soil microarthropods to extreme precipitation in agroecosystem
Article
  • Sep 2022
  • GEODERMA
Soil biodiversity is of key importance to many essential ecosystem functions, but currently it is severely threatened by both intensive agriculture and climate changes. Ecological intensification, including organic amendments and less disturbance, is expected to buffer the degradation of biodiversity and ecosystem functioning induced by intensive agriculture, but its effects in the context of climate changes are poorly understood. In the present work, we studied the responses of agricultural soil biodiversity to ecological intensification under different natural rainfall intensities in a subtropical field. We focused on a numerically dominant group of soil microarthropods, the Collembola, and three conservation managements, i.e., straw, manure, and no-tillage. The experimental site was established with a full-factorial design of different managements. Soil physiochemical parameters and the density, taxonomic diversity, and morpho-functional traits of the collembolan community were measured over three consecutive years. Results showed that rainfall intensification markedly reduced collembolan density and had severe impact on large euedaphic species. Straw amendment buffered the detrimental effect of dense rainfall on collembolan density, but aggravated the body size reduction caused by the rainfall. Manure input and no-tillage mainly affected the community functional composition, in which manure favours more active and mobile species characterised by a well-developed furca, whereas no-tillage favoured surface-dwelling species. These results support the hypothesis that external resource enrichment and reduced disturbance would shape the functional traits of soil fauna, and further modified their response to climate change events. Our findings call for more attention on the functional consequences of ecological intensification and the interactions among soil biodiversity, agricultural managements and climate changes.
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... Ancient versus recent above-ground forest differences may however be hidden by recent transformation (e.g., logging, plantation). Nevertheless, beech is often present and major differences have been observed in specific lichen (Fritz et al. 2008), beetles (Assmann 1999;Desender et al. 1999), vascular plants (Hermy et al. 1999) and springtails species (Ponge et al. 2006). These organisms share common traits such as a low dispersal capacity and high sensibility to habitat stability. ...
Influence of habitat fragmentation and habitat amount on soil fungi communities in ancient forests
Article
Full-text available
  • Feb 2024
  • LANDSCAPE ECOL
Context Fungi represent a large part of soil biodiversity as well as an essential role for tree hydromineral nutrition, survival, and carbon cycling. While their local diversity has proven to be shaped by abiotic and biotic factors related to soil, climate and vegetation, their response to landscape fragmentation is still debated. Objectives In this paper, we focus on ancient forests characterized by the presence of beech at low elevation, a habitat particularly fragmented in South-West France. We aim to assess the effect of past and present forest fragmentation and quantity on soil fungal and functional group diversity. We expect a negative impact of fragmentation and a positive effect of forest quantity on soil fungal diversity, in addition to an influence of local soil factors. Methods Soils from 41 1ha ancient forest plots across South-West France were sampled along gradients of past and present forest fragmentation and quantity, before their fungal diversity was characterized by metabarcoding of environmental DNA. Hill numbers have been computed and applied to all fungi, trophic guilds and growth forms. Results We find that past forest fragmentation negatively impacts on soil fungal diversity and in particular for symbiotrophs, while the present forest quantity has a positive impact. In contrast, the species richness of pathotrophic fungi shows a negative correlation with past forest fragmentation. The diversity of fungal groups with lower dispersal abilities (e.g., corticioid, microfungi) is negatively impacted by past forest fragmentation, while the diversity of wind-dispersed fungi (e.g., agaricoid) is not influenced by any landscape descriptors. Conclusions Our results show the complexity of fungal responses to past and present forest fragmentation and demonstrate the long-lasting effect of past fragmentation as well as the positive impact of recent forest quantity in the landscape on fungal diversity associated with ancient forest soils. Our study also highlights the huge diversity of fungi unraveled by eDNA metabarcoding in this habitat and the potential of such techniques to study the landscape ecology of soil communities.
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... Les auteurs n'ont cependant pas observé de différences de communautés pour les invertébrés vivant à la surface du sol (Peña et al. 2016). L'ancienneté du couvert forestier influencerait également positivement la richesse spécifique des collemboles (Heiniger et al. 2014) et favoriserait des espèces peu dispersives et typiquement forestières (Ponge et al. 2006), mais il semblerait que le pH soit le principal facteur structurant ces communautés (Chauvat et al. 2007 ;Martins da Silva et al. 2016 ;Janssen et al. 2017). Les vers de terre quant à eux, ne semblent pas particulièrement impactés par la continuité forestière et les communautés des forêts post-agricoles se rapprochent de celles des forêts anciennes après seulement un demi-siècle (Sigurðsson & Guðleifsson 2013 ;Palo et al. 2013). ...
Ecologie historique et conservation de la biodiversité des forêts anciennes dans les espaces protégés de montagne : une approche multi-taxonomique
Thesis
Full-text available
  • May 2023
In France, the forest area decreased continuously until the middle of the 19th century, then increased rapidly following the industrial revolution. This forest minimum marks the limit between pre-existing "ancient forests" and the "recent forests" that were established later, because it makes it possible to assume a much longer forest continuity and to estimate precisely the historic forest areas thanks to the existence of complete historical maps (Napoleonic cadastre and Ordnance Survey maps among others). This temporal continuity of ancient forests induces a stability likely to favor the presence of particular species with low dispersal capacity and sensitive to disturbances.If the French forest area has almost doubled since 1850, it is estimated that 15 % of the forests present in 1840 has disappeared today at a national scale. Despite IUCN recommendations to protect ancient forests, conservation actions are still poorly defined and fall under the precautionary principle. This thesis project is part of a partnership with five French national parks located in mountain areas (Pyrenees, Cevennes, Mercantour, Ecrins and Vanoise) which have already vectorised and identified ancient forests on their territory. It aims to answer three main research questions :1- What is the role of ancient forests for the conservation of threatened species?2- Does the type of ancient land use influence the biodiversity of recent forests?3- Does forest management impact the biodiversity of ancient forests?The first question was addressed through statistical analysis of naturalist data collected by different networks of observers in the areas of adhesion of the five national parks in our study area. This work showed that threatened spermaphytes, pteridophytes, bryophytes, and forest beetles were more responsive to historical forest area than to current forest area, highlighting a 150-year lag in response to landscape change. The second part of the study was based on botanical surveys carried out in the forests of the Vanoise national park on four types of ancient use: forest, pasture, hay meadow and crop. This study showed that there was no difference in edaphic conditions between ancient forests and recent forests developed on former pastures and hay meadows, whereas forests located on former cropland had richer soils. On the other hand, differences in taxonomic and functional composition of understory plant communities were also smaller between ancient forests and former pastures than between ancient forests and former cropland. Finally, the third question was treated using metabarcoding surveys of fungal communities in the public forests of Vanoise with a gradient of time elapsed since the last harvest from one to 75 years. This study showed that the low-intensity silvicultural management of the Vanoise forests had little impact on soil fungal communities and confirmed the weak long-term traces left by grazing in recent forests.This work therefore highlights the importance of old-growth forests for the conservation of biodiversity, particularly forest species, but also emphasizes that the type of ancient land use is important to consider in recent forests. Former pastures in particular, which represent an important part of recent forests in mountain areas, have a lower impact than other land uses.
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... Specifically, euedaphic species may be less exposed to temperature variability (smaller temperature ranges) and extreme weather events compared to hemiedaphic and epedaphic species, which live closer to or on the soil surface (Bokhorst et al., 2012;Holmstrup et al., 2018). By contrast, Ponge et al. (2006) suggested that Collembola living in the soil and being characterized by limited active dispersal may suffer more from intensified land use, than species living on the soil surface. Based on previous work at the same experimental field site, however, the abundance of surface-dwelling species might be less negatively affected by global change drivers than that of soil-living Collembola (Yin et al., 2019b). ...
The responses of Collembola biomass to climate and land-use changes vary with life form
Article
  • Jan 2023
  • SOIL TILL RES
The biomass of invertebrate detritivores is an important driver of multiple ecosystem functions, yet little is known about how it changes in the context of global change. Taking Collembola communities as our focal groups, we conducted a study at the Global Change Experimental Facility (GCEF) in central Germany to assess how climate change (i.e., increased temperature by ∼0.55 °C across seasons, and the altered precipitation patterns by ∼9 % increase in spring and autumn, and ∼21 % reduction in summer) and intensive land use (i.e., from extensively-used grassland to conventional cropland) would shift the biomass patterns of Collembola and their different life forms. Our results show that the biomass of different Collembola life forms differed in their response to the changes in climate and land use. Specifically, the population biomass of surface-dwelling Collembola significantly decreased under future climate scenario and intensive land use, while the biomass of soil-living Collembola responded less. Importantly, Collembola biomass was decreased by (i) climate change-induced body size shrinkage, and (ii) intensive land use-induced density reduction. These results suggest that different environmental change drivers are able to reduce soil microarthropod biomass via dissimilar mechanisms.
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... Based on primary literature, catalogues, and reference work (Gruss et al., 2019;Malmström, 2012;Moretti et al., 2017;Vandewalle et al., 2010), seven traits of collembolans were selected, which are likely to respond to variations in environmental conditions, and to provide complementary information to taxonomic information. The traits included life-history traits (life-form), behaviour trait (dispersal ability) and morphological traits (body size, length of furca, number of ocelli, pigmentation, and coverage by scales, Jagatap et al., 2019;Ponge et al., 2006;Saifutdinov et al., 2018). Life-history traits are among the most sensitive traits responding to environmental change, while morphological traits such as body size are likely to respond to both the abiotic and biotic environment Moretti et al., 2017;Rusek, 2002). ...
Urbanization and greenspace type as determinants of species and functional composition of collembolan communities
Article
  • Dec 2022
  • GEODERMA
Urban regions are rapidly expanding worldwide resulting in biotic homogenization and loss of ecological functions in urban ecosystems due to management practices targeting at satisfying aesthetic and health demands of urban residents. These practices also modify living conditions and food recourses of soil invertebrates thereby affecting the structure and functional diversity of soil animal communities including collembolans. Here, we assessed the response of the community composition and functional diversity of collembolans as a major component of soil food webs to urbanization (suburban vs urban region) and greenspace types (including forest and four park-associated greenspaces: lawn, lawn with shrubs, lawn with trees, and lawn with shrubs and trees). Our results highlight that both urbanization and greenspace type significantly affect soil properties and community structure of collembolans. The negative effect of urbanization and park-associated greenspaces on species and functional composition of collembolan communities were likely due to both changes in soil abiotic conditions and bacterial community composition, whereas the reduction of collembolan functional traits likely resulted from changes in soil abiotic conditions and fungal community composition. In park-associated greenspaces richness and diversity of bacterial communities were highest in lawns with trees and lowest in forests. By contrast, species richness and diversity of fungal communities were highest in lawns with shrubs, but, similar to bacteria, lowest in forests. Community composition and functional traits of collembolans were more homogeneous in urban than suburban greenspaces pointing to reduced functioning of collembolan assemblages in urban areas. Overall, our results suggest that changes in soil properties and bacterial communities caused by urbanization and greenspace type are important factors contributing to taxonomic homogenization of collembolan communities, while the loss of functional traits of collembolan communities in urban greenspaces is likely caused by changes in soil properties and fungal community composition.
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Invertebrate communities (Collembola and Acari) in soil cover treatments for mine tailings in a long‐term field experiment
Article
  • Jun 2023
Assessment of mine rehabilitation strategies including soil cover treatments rely mainly on soil physico‐chemical properties or plant performance indices, while much less is known about the response of biological soil properties. This field study evaluated the response of soil mesofauna (Collembola and Acari) in soil cover treatments (mainly subsoil and subsoil) on mine tailings, with or without organic amendments. The field experiment was conducted in large (1 m ³ ) units rehabilitated in 2014, and mesofauna in soil cores was assessed 7 years later. The richness of Collembola and Acari as well as the density of Acari increased with organic amendments. Collembola community composition changed with the addition of soil cover and organic amendments. The density and community composition of Acari were strongly positively associated with organic carbon. The density of Euedaphic Collembola decreased, whereas Hemiedaphic and Epedaphic forms increased with soil cover. The contribution of generalist and metal‐tolerant species explained the high density of Euedaphic life forms in tailings. Species‐specific traits for Collembola and Acari could play an essential role in explaining the response of populations to treatments, such as affinity for C‐enriched habitats, food preferences, and sensitivity to heavy metals. Overall, it is recommended to use a multiple diversity indices approach, to collect data on the density and assemblage of mesofauna species to investigate the response of mesofauna communities to soil cover treatments. Mine tailings rehabilitation strategies should focus on improving the nutrient content of soil covers, since it benefits diversity and density of soil fauna.
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Mitogenome selection in the evolution of key ecological strategies in the ancient hexapod class Collembola
Article
Full-text available
  • Aug 2022
A longstanding question in evolutionary biology is how natural selection and environmental pressures shape the mitochondrial genomic architectures of organisms. Mitochondria play a pivotal role in cellular respiration and aerobic metabolism, making their genomes functionally highly constrained. Evaluating selective pressures on mitochondrial genes can provide functional and ecological insights into the evolution of organisms. Collembola (springtails) are an ancient hexapod group that includes the oldest terrestrial arthropods in the fossil record, and that are closely associated with soil environments. Of interest is the diversity of habitat stratification preferences (life forms) exhibited by different species within the group. To understand whether signals of positive selection are linked to the evolution of life forms, we analysed 32 published Collembola mitogenomes in a phylomitogenomic framework. We found no evidence that signatures of selection are correlated with the evolution of novel life forms, but rather that mutations have accumulated as a function of time. Our results highlight the importance of nuclear-mitochondrial interactions in the evolution of collembolan life forms and that mitochondrial genomic data should be interpreted with caution, as complex selection signals may complicate evolutionary inferences.
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The Nature and Properties of Soils. 15th edition
Book
Full-text available
  • Apr 2017
This edition updates a narrative that has been at the forefront of soil science for more than a century. The first edition, published in 1909, was largely a guide to good soil management for farmers in the glaciated regions of New York State in the northeastern U.S. Since then, it has evolved to provide a globally relevant framework for an integrated understanding of the diversity of soils, the soil system and its role in the ecology of planet Earth. The 15th edition is the first to feature full-color illustrations and photographs throughout. These new and refined full color figures and illustrations help make the study of soils more efficient, engaging, and intellectually satisfying. Every chapter has been thoroughly updated with the latest advances, concepts, and applications. Hundreds of new key references have been added. The 15th edition, like preceding editions, has greatly benefited from innumerable suggestions, ideas, and corrections contributed by soil scientists, instructors, and students from around the world. Dr. Nyle Brady, although long in retirement and recently deceased, remains as co-author in recognition of the fact that his vision, wisdom and inspiration continue to permeate the entire book. This edition,1082 pages in length, includes in-depth discussions on such topics of cutting edge soil science as the pedosphere concept, new insights into humus and soil carbon accumulation, subaqueous soils, soil effects on human health, principles and practice of organic farming, urban and human engineered soils, cycling and plant use of silicon, inner- and outer-sphere complexes, radioactive soil contamination, new understandings of the nitrogen cycle, cation saturation and ratios, acid sulfate soils, water-saving irrigation techniques, hydraulic redistribution, cover crop effects on soil health, soil food-web ecology, disease suppressive soils, soil microbial genomics, indicators of soil quality, soil ecosystem services, biochar, soil interactions with global climate change, digital soil maps, and many others. In response to their popularity in recent editions, I have also added many new boxes that present either fascinating examples and applications or technical details and calculations. These boxes both highlight material of special interest and allow the logical thread of the regular text to flow smoothly without digression or interruption. For students: This book provides both an exciting, accessible introduction to the world of soils as well as a reliable, comprehensive reference that you will want to keep for your professional bookshelf. What you learn from its pages will be of enormous practical value in equipping you to meet the many natural-resource challenges of the 21st century. The book demonstrates how the soil system provides many opportunities to see practical applications for principles from such sciences as biology, chemistry, physics, and geology. Throughout, the text highlights the countless interactions between soils and other components of forest, range, agricultural, wetland, and constructed ecosystems. As the global economy expands exponentially societies face new challenges with managing their natural resources. Soil as a fundamental natural resource is critical to sustained economic growth and the prosperity of people in all parts of the world. To achieve balanced growth with a sustainable economy while improving environmental quality, it will be necessary to have a deep understanding of soils, including their properties, functions, ecological roles and management. I have tried to write this textbook in a way designed to engage inquisitive minds and challenge them to understand soils and actively do their part as environmental and agricultural scientists, in the interest of ensuring a prosperous and healthy future for humanity on planet Earth. It is my sincere hope that this book, previous editions of which have served so many generations of soil students and scientists, will continue to help future generations of soil scientists to benefit from a global ecological view of soils.
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Habitat dependent differences in the flight behaviour of Collembola
Article
Full-text available
  • Jul 1987
  • PEDOBIOLOGIA
Atmobiotic species should escape by a single long distance, rapid jump that catapults them out of the range and field of view of an attacker. Litter-inhabitants execute short jumps but more jumps per unit time. The bark-inhabiting Entomobrya corticalis behaved differently. Even when touched it escapes by running quickly and very rarely employs a short jump. Tree inhabitants are characterized by greater resistance to desiccation while inhabitants of deeper litter layers show low resistance. Among species that live on or in the uppermost litter layer there is no conspicuous difference in resistance to dryness between long distance and short distance jumping species. -from Authors
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The Nature and Properties of Soil
Book
Full-text available
  • Jan 1996
Thoroughly updated and now in full color, the 15th edition of this market leading text brings the exciting field of soils to life. Explore this new edition to find: A comprehensive approach to soils with a focus on six major ecological roles of soil including growth of plants, climate change, recycling function, biodiversity, water, and soil properties and behavior. New full-color illustrations and the use of color throughout the text highlights the new and refined figures and illustrations to help make the study of soils more efficient, engaging, and relevant. Updated with the latest advances, concepts, and applications including hundreds of key references. New coverage of cutting edge soil science. Examples include coverage of the pedosphere concept, new insights into humus and soil carbon accumulation, subaqueous soils, soil effects on human health, principles and practice of organic farming, urban and human engineered soils, new understandings of the nitrogen cycle, water-saving irrigation techniques, hydraulic redistribution, soil food-web ecology, disease suppressive soils, soil microbial genomics, soil interactions with global climate change, digital soil maps, and many others Applications boxes and case study vignettes bring important soils topics to life. Examples include “Subaqueous Soils—Underwater Pedogenesis,” “Practical Applications of Unsaturated Water Flow in Contrasting Layers,” “Soil Microbiology in the Molecular Age,” and "Where have All the Humics Gone?” Calculations and practical numerical problems boxes help students explore and understand detailed calculations and practical numerical problems. Examples include “Calculating Lime Needs Based on pH Buffering,” “Leaching Requirement for Saline Soils,” "Toward a Global Soil Information System,” “Calculation of Nitrogen Mineralization,” and “Calculation of Percent Pore Space in Soils.”
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Long distance, directional migration on snow in a forest collembolan, Hypogastrura socialis (Uzel)
Article
  • Jan 1995
H. socialis is well known for its mass occurrence on snow during mild weather. This behaviour has been considered to have a migratory function, allowing the animals to identify suitable, snow-free patches below trees where reproduction can start early. Detailed studies in the present work on the migratory behaviour of single individuals and populations indicate directional movements over long distances, 200-300 m per day. Each individual repeatedly jumps in a certain direction and keeps a steady course on the snow surface. Before each jump, the animal rotates horizontally, probably using the sun for navigation. -from Author
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Forest Growth as a Possible Cause of Soil and Water Acidification: An Examination of the Concepts
Article
  • Jun 1982
Acidity consequent on root uptake was calculated as the excess cation accumulation in both stems and all above-ground tree components in a range of forest types, and values were derived for acidity resulting from the accumulated humus. In addition data from one pine stand was used to construct models of rate of accumulation of excess cations in trees and humus throughout the forest rotation. Rates of hydrogen ion production reaches a maximum very early in the life of a forest and the average annual permanent acidification resulting from removal of harvested material covers a wider range than either measured inputs in rainfall, including throughfall and stemflow, or estimated weathering rates. However, it is suggested that because rainwater inputs are episodic, include a mobile anion and may be channelled through the profile, whereas root generated acidity varies only gradually, does not involve the movement of an anion and occurs in intimate contact with the soil surfaces, rainwater acidity is the more likely to lead to streamwater acidification whereas root uptake will primarily acidify the soil. /// Динамика кислотности, создающаяся в результате корневого всасывания, рассчитывалаь как аккумуляция избитка катионов в стволе и других надземных частях деревьев в ряду типов леса; результаты использованы для определения кислотности в накапливающемся гумусе. Кроме того, использовали данные по одному сосняку для построения моделей скорости аккумуляции избытка катионов деревьями и гумусом в ходе смены лесных пород. Скорость образования ионов водорода достигает максимума на ранних этапах развития леса, а средне-годовая перманентная ацидификация в результате удаления созревшего матириала колеблется в более широких пределах, чем величины постеплений с осадками, включая просачивание и стволовой сток и скорости выщелачивания. Однако, это показывает, что так как поступления с осадками эпизодичны, они содержат подвижные анионы и могут просачиваться по профилю почвы, а кислотность, создаваемая активностью корней, изменяется постепенно, не увеличивает подвижности анионов и тесно связана с поверхностью почвы; кислотность осадков наиболее вероятно влияет на ацидификацию текучих вод, а корневая активность - прежде всего на кислотность почвы.
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Biology of the Springtails (Insecta: CollEMBOla)
Book
  • Feb 1997
The book is organized into 10 chapters: general introduction; review of the literatire on springtails; evolution, systematics and biogeography; ecomorphology and anatomy; taxonomic methods and the species concept in Collembola; interactions between Collembola and the abiotic environment; interactions between Collembola and the biotic environment; reproduction, development and life histories; ecology and conservation; and ecotoxicology. There are three appendices: World genera of Collembola; regional checklists of Collembola; and laboratory/field studies on the effects of chemicals on Collembola.
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