Litter-dwelling ants as bioindicators to gauge the sustainability of small arboreal monocultures embedded in the Amazonian rainforest

Ecological Indicators 82 (2017) 43–49

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Litter-dwelling ants as bioindicators to gauge the sustainability of small arboreal monocultures embedded in the Amazonian rainforest

MARK

Sarah Groca, Jacques H.C. Delabieb, Fernando Fernandezc, Frédéric Petitclerca, Bruno Corbarad, ⁎ Maurice Leponcee, Régis Céréghinof, Alain Dejeana,f, a

CNRS, UMR EcoFoG, AgroParisTech, Cirad, INRA, Université des Antilles, Université de Guyane, 97310, Kourou, France U.P.A. Laboratório de Mirmecologia, Convênio UESC/CEPLAC, C.P. 7, 45600-000, Itabuna, Bahia, Brazil c Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá D.C., Colombia d Université Clermont Auvergne, CNRS, LMGE, F-63000, Clermont-Ferrand, France e Aquatic and Terrestrial Ecology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000, Brussels, Belgium f Ecolab, Université de Toulouse, CNRS, INPT, UPS, Toulouse, France b

A R T I C L E I N F O

A B S T R A C T

Keywords: Ant diversity Community alteration Forest species Functional traits Human disturbance Tree monocultures

One of the greatest threats to biodiversity and the sustainable functioning of ecosystems is the clearing of forests for agriculture. Because litter-dwelling ants are very good bioindicators of man-made disturbance, we used them to compare monospecific plantations of acacia trees, cocoa trees, rubber trees and pine trees with the surrounding Neotropical rainforest (in contrast to previous studies on forest fragments embedded in industrial monocultures). Although the global level of species turnover was weak, species richness decreased along a gradient from the forest (including a treefall gap) to the tree plantations among which the highest number of species was noted for the cocoa trees, which are known to be a good compromise between agriculture and conservation. Species composition was significantly different between natural habitats and the plantations that, in turn, were different from each other. Compared to the forest, alterations in the ant communities were (1) highest for the acacia and rubber trees, (2) intermediate for the cocoa trees, and, (3) surprisingly, far lower for the pine trees, likely due to very abundant litter. Functional traits only separated the rubber tree plantation from the other habitats due to the higher presence of exotic and leaf-cutting ants. This study shows that small monospecific stands are likely sustainable when embedded in the rainforest and that environmentally-friendly strategies can be planned accordingly.

1. Introduction The global-scale conversion of natural ecosystems to agriculture is recognized as one of the major threats to biodiversity and the functioning and sustainability of ecosystems due both to the clearing of native vegetation and the fragmentation and destruction of natural habitats. Species richness is generally reduced as a consequence of the simplified structure of human-altered habitats. Hence, preserving high quality agricultural habitats is a priority on the biodiversity conservation agenda (Barlow et al., 2016). In native, resource-rich habitats, the complementary presence of the species making up the communities may have positive effects on ecosystem functions when ecological partitioning occurs, while increasing the growth of the populations thanks to a lower rate of competition (Turnbull et al., 2013). In perturbed habitats, the competitive advantage conferred by certain traits promotes ecologically dominant

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species that monopolize most of the available resources (Bílá et al., 2014) to the detriment of functional diversity. The functional traits of organisms in a community associates species diversity with ecosystem functioning (Mayfield et al., 2010). Functional diversity can thus reveal the link between the biological, ecological, and physiological attributes represented in communities and ecosystem functions and services. Functional redundancy (i.e., the degree to which the species in a community perform similar ecological functions) and functional structure (i.e., the composition and diversity of functional traits) are particularly important (Mouillot et al., 2011) because they likely confer ecosystem resistance and/or resilience to environmental fluctuations. In the Neotropics, multistrata agroforestry systems (e.g., shade trees in cocoa plantations) are particularly valuable for the conservation of biodiversity because the remaining native forest fragments provide refuge, thus preserving an associated biodiversity very similar to the native one. They can also play the role of template for sustainable

Corresponding author at: UPS−ECOLAB, 118 route de Narbonne, 31062 Toulouse, France. E-mail address: [email protected] (A. Dejean).

http://dx.doi.org/10.1016/j.ecolind.2017.06.026 Received 19 March 2017; Received in revised form 10 May 2017; Accepted 13 June 2017 1470-160X/ © 2017 Elsevier Ltd. All rights reserved.

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Table 1 A. Physical characteristics of the habitats sampled (for the litter: mean dry weight ± SE). B. Comparison of diversity between the Paracou forest and different naturally (treefall gaps) or anthropogenically (tree monocultures) perturbed habitats. Hill numbers, i.e., true diversities for orders 0, 1 and 2 are provided along with the rarefied number of species, the number of species occurrences recorded, and the proportion of species shared with the forest. A.

Natural rainforest Rainforest

Surface area Size of trees Canopy Age Spatial structuration of trees Understory Litter weight/m2 (in g) B. Observed richness Chao2 (0D) Completeness No. occurrences Rarefied species richness (400 occurrences) Shannon exponential (1D) Simpson inverse mean (2D) No. species shared with the forest − %

Monospecific plantations

> 40,000 Ha ≈35 m closed < 200 y ca. random

Treefall gap 1.4 Ha shrubs open 10 y ⁄

Acacia trees 4 Ha ≈20 m closed 34 y rows

Cocoa trees 8.4 Ha 6–8 m discont-inuous 25 y rows

Rubber trees 6.4 Ha ≈20 m discont-inuous 35 y rows

Pine trees 7.4 Ha ≈20 m closed 35 y ca. random

complex 404 ± 22

absent 364 ± 41

≈absent 674 ± 41

≈absent 413 ± 32

≈absent 545 ± 46

≈absent 928 ± 69

124 176.7 70% 690 101.4

101 123.4 82% 437 98.4

98 127.4 77% 759 79.1

96 114.3 79% 627 84.0

90 132.8 72% 735 72.7

96 171.0 56% 701 78.6

67.6 44.6

60.7 39.2

47.7 31.9

54.0 37.4

44.5 31.2

48.9 33.4

–

69 55.6%

50 40.3%

50 40.3%

39 31.4%

61 49.2%

than 10 ha) embedded in a tropical rainforest. Indeed, most other studies have dealt with wide industrial monocultures representing the matrix within which forest fragments are embedded (Bihn et al., 2010; Philpot et al., 2010; Liu et al., 2016). Assuming that insect diversity and community composition are tightly linked to tree diversity in rainforests (Basset et al., 2012), and that habitat structures and the physicochemical properties of the litter found in different monocultures represent different habitat filters that select certain traits, we formulated three hypotheses. (1) Ant species richness and community composition are affected by the conversion of forest to monocultures. (2) As anthropic habitats, tree monocultures induce both a shift in ant trait composition and a decrease in trait diversity compared to natural habitats. (3) The types of tree species in monocultures have a strong influence on ant community composition, including the presence of exotic species.

agricultural production systems (Schroth et al., 2011). Monocultural systems frequently concern rubber trees, a common native Amazonian species of high economic value due to the latex it yields for rubber production, or fast-growing exotic tree species. Among the latter, Acacia spp., Pinus spp. and Eucalyptus spp. are widely planted for timber production and protection against erosion. Acacia spp. are also used to rehabilitate degraded soils due to their association with nitrogen-fixing bacteria and their extraordinary ability to build organic soil matter (Orwa et al., 2009). Yet, monospecific plantations generally have a number of drawbacks in terms of ecological function, such as a deeply altered entomofauna. For example, the age, nature, size, and maintenance of a plantation, edge permeability to propagules during the (re) colonization process as well as the quality of and distance from the forest matrix are fundamental factors influencing ground-dwelling ant communities (Philpott et al., 2010; Pacheco et al., 2009; Liu et al., 2016). Ants are frequently used as bioindicators in studies dealing with natural forests and forest disturbance because they include herbivores, generalists, predators or scavengers, they respond to stress at a finer scale than many other animals, and they occupy a central place in the functioning of tropical ecosystems where they constitute the largest fraction of the animal biomass (Delabie et al., 2009; Bihn et al., 2010; Groc et al., 2014; Dejean et al., 2015a; Liu et al., 2016). We therefore used litter-dwelling ants in this study to analyze the impact of monocultures of acacia trees, cocoa trees, rubber trees and pine trees embedded in a Neotropical rainforest that served as a reference. Among the traits that are sensitive to disturbance or, on the contrary, are typical of the rainforest, we selected (1) geographical origin, as introduced species can be invasive, appearing first in disturbed areas, (2) habitat preference, including the rainforest and different types of secondary areas, (3) nesting habits, because many forest species nest in the litter between leaves or in fragments of hollow twigs, and (4) feeding habits, with special reference to leaf-cutting ants, as they attack certain tree species, and predatory ants because the presence of specialized species reflects the abundance of their prey. To the best of our knowledge, no comprehensive survey has demonstrated shifts in ant community diversity and functional traits from natural forest habitats (be they dense rainforest habitats or treefall gaps within that forest) to comparatively small tree monocultures (i.e., less

2. Materials and methods 2.1. Study sites and experimental protocol Ant sampling was conducted during the dry season of 2014 at the Paracou experimental station in French Guiana (5°16′N, 52°54′W; ≈35 m above sea level), an area characterized by ≈3300 mm of annual precipitation. We collected samples from an undisturbed area of the rainforest, a vast and expanding treefall gap and four experimental monospecific plantations: acacia trees (Acacia mangium; Fabaceae), rubber trees (Hevea brasiliensis; Euphorbiaceae), cocoa trees (Theobroma cacao; Sterculiaceae) and pine trees (Pinus caribaea; Pinaceae). Cocoa and rubber trees are native to the Neotropics, while the other species are exotic (see Table 1A for the characteristics of the habitats sampled). These experimental plantations were programmed during the Seventies shortly after the notion of sustainable development was presented by Ward and Dubos (1972). The aim of the decision-makers in agronomy was to find applications in areas where the forests were already cleared due to different human activities. When the present study was conducted, the pine tree plantation, earmarked for timber for construction, was ≈40-years old, whereas the other plantations were ≈30-years old. The rubber tree plantation was planned in an attempt to create the conditions necessary to limit attacks by the lethal, endemic fungus 44

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collected at a sampled site) were taken into account, and the percentages of species occurrences per sample were used as a proxy for ant abundance. So, six species × sample incidence matrices (one per habitat) were analyzed and compared.

Microcyclus ulei, explaining why most plantations are located outside South America, mainly in Southeast Asia (Leiberei, 2007). Native to Australasia, Acacia mangium, which fixes nitrogen in the soil and tolerates low soil fertility, helps degraded tropical soils to recover and so is used to regenerate areas particularly degraded by human activities (Voigtlaender et al., 2012). The cocoa trees were planted for agronomic purposes. The Winkler method was used because it is highly recommended for ant inventories in forest-like habitats where leaf litter abounds (Delabie et al., 2000). We collected ants from a series of 1 m2 leaf-litter samples that were weighed. Pitfall traps (left for 48 h) were also used because it is essential to combine several sampling methods to come as near as possible to an exhaustive inventory (Delabie et al., 2000). The “Ants of Leaf Litter” (ALL) protocol, which suggests using a minimum of 20 sampling points separated by 10 m intervals to collect between 45% and 70% of the ant fauna at a given site (Leponce et al., 2004), was applied. We selected 50 sampling points whenever possible (the data gathered from 50 Winkler extractions and 50 pitfall traps were pooled for each habitat, except for the treefall gap where N = 49 and the cocoa tree plantation where N = 42). Sampling in the forest was conducted far from any dirt access road (≈500 m); in the other cases, to avoid the edge effect, sampling was conducted as far as possible from the forest edge or any open area (i.e., more than 50 m). Note that this approach permitted us to limit the number of replicates and so to sample a treefall gap. Indeed, invertebrate sampling is relatively fast and surveys using this method permit a representative part of the rich litter-dwelling ant fauna to be recorded (Delabie et al., 2000; Groc et al., 2014, Fig. 1). All of the ant samples were first preserved in 70% ethanol. Then, voucher specimens and a reference collection were deposited in the Laboratório de Mirmecologia, Cocoa Research Centre CEPEC/CEPLAC (Ilhéus, Bahia, Brazil) and in the Royal Belgian Institute of Natural Sciences (Brussels, Belgium). The ants were sorted to species or morphospecies based on Bolton et al. (2006). Because ants are aggregated in colonies, contrary to non-social insects whose individuals have an equal probability of being caught during sampling, presence/absence data are preferred over abundance data in the analyses (Longino, 2000; Leponce et al., 2004). Thus, only species occurrences (i.e., the number of times that a given species was

2.2. Occurrence-based curves and comparison of ant assemblages Species rarefaction curves were plotted on the presence-absence data matrices using EstimateS 9.1.0 software (Colwell, 2013) with 100 randomizations of the sampling order without replacement. In order to standardize the comparisons between habitats and to estimate sampling completeness, these curves and the Chao2 non-parametric estimator of total species richness were calculated (Colwell et al., 2004). We calculated Hill numbers (i.e., “true diversities”) for three different orders (q) of diversity. True diversity indices obey the doubling property, preventing a misleading interpretation of results (see Jost, 2010). Order q is related to the sensitivity of the index to the frequency of the species in the community: when q = 0, all species are given the same weight (rare species are thus favored); when q = 1, species are weighted for their frequency in the community (neither common nor rare species are favored); and when q = 2, more abundant species are favored. Accordingly, species richness is a measure of diversity of order zero (0D), the exponential of Shannon’s entropy index is a measure of diversity of order one (1D), and the inverse of Simpson’s index is a measure of order two (2D) (Jost, 2010). All three indices are in units of equivalent, equally abundant species and were calculated using EstimateS 9.1.0 (Colwell, 2013). Differences in species richness between habitats were assessed using the non-overlapping of 95% confidence intervals as a conservative criterion of statistical difference in species richness between habitats (Colwell, 2013). The global turnover between the different ant assemblages was analyzed using the second version of Harrison’s indices (βH2 = [(S/ αmax)-1]/(N-1), Harrison et al., 1992) as a beta-diversity index obtained using PAST 3 software. βH2 is an improvement over Whittaker’s index (βW = (S/α)-1) which was modified to be effective in analyzing pairwise differentiation between sites; it is insensitive to species richness trends (Socolar et al., 2016). Fig. 1. Standardized comparison of ant species richness between natural habitats and monospecific tree plantations sampled with Winkler and pitfall traps. Solid lines represent occurrence-based rarefaction curves and their 95% confidence intervals.

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specialized predator Strumigenys denticulata, at only 5.6% of the overall occurrences, was the most abundant (Appendix A).

2.3. Relationships between habitat types and ant species The community composition data recorded for each habitat type allowed us to build a “291 samples x 247 ant species” matrix (presenceabsence data). These data were Hellinger-transformed prior to analysis (see equation ‘13′ in Legendre and Gallagher, 2001) to conduct analyses by linear methods when presence-absence data contain many zeros (Ramette, 2007). A Principal Component Analysis (PCA) was used to ordinate the samples according to ant species, thus summarizing community variability. Significant changes in species assemblage composition across habitats were examined by clustering samples within the PCA-component space using a k-means partitioning of sample scores. We determined the optimal number of clusters (low variance within clusters and high variance between clusters) based on the majority rule after computing 26 clustering indices. To ease interpretation, bar plots were used to show the distribution of samples from the different habitats among clusters. These analyses were conducted with the Vegan, ADE4 and NbClust packages in R software (R Development Core Team, 2015).

3.2. Occurrence-based rarefaction curves and diversity of the ant assemblages The Chao2 estimator indicated that a representative part of the leaflitter ant fauna was inventoried in total (Chao2 = 317.17 species; Sobs Mao Tau index = 247 species or ≤ 77.9% of total expected richness) and for each habitat sampled (undisturbed forest: 124 species, 70%; treefall gap: 101 species, 82%; acacia trees: 98 species, 77%; cocoa trees: 96 species, 84%; rubber trees: 90 species, 71.5%; pine trees: 96 species, 56%) (Fig. 1). Rarefied species richness was significantly higher in the forest (including the treefall gap) than in the monospecific tree plantations, whereas confidence intervals around the mean species richness of tree monocultures were overlapping, indicating no significant difference (Fig. 1). True diversities of the orders 0, 1 and 2 were systematically higher in the forest compared to the other habitats, confirming its overall higher diversity (Table 1B). The estimated total species richness calculated with the Chao2 index was surprisingly high in the pine tree plantation, reaching a value close to that of the undisturbed forest. The global beta diversity (Harrison βH2 = 0.198; a low value as this index varies between 0 and 1) denoted a large global species overlap between habitats (i.e., a small turnover). Also, the differences in the multiple comparison tests were not significant (P = 0.26 was the lowest value for the comparisons of Harrison’s indices; details not shown).

2.4. Relationships between habitat types and the functional traits of the ant species Based on previous studies of the nesting and feeding preferences of leaf-litter ant species (Delabie et al., 2007; Groc et al., 2014; Dejean et al., 2015a, 2015b) complemented by information provided by Bolton et al. (2006), the Antweb (2016) and Antwiki (2016) including ant distribution and origin, we defined nominal categories for four functional traits: (1) geographical origin (two categories: native; exotic); (2) habitat preference (three categories: forest; secondary areas; meadows or dry areas); (3) nesting habits (three categories: cryptic or subterranean; leaf-litter; arboreal); and (4) feeding habits (six categories: seeds, nectar or honeydew feeders; leaf-cutting, fungus-growing; fungus-growing from carcasses; army ants; generalist predators; specialized predators). Note that many arboreal ants forage for prey on the ground or in the leaf litter (Dejean et al., 2007). Information on the traits was structured using a fuzzy-coding technique (Chevenet et al., 1994). The scores ranged from ‘0’, indicating ‘no affinity’ for a given trait category, to ‘3’, indicating ‘high affinity’. This procedure allowed us to build the [ant species x traits] matrix. We then combined this matrix with the Hellinger-transformed [ant species x samples] matrix by matrix multiplication to upscale trait information to the community level in the form of a [samples x traits] matrix (see Dézerald et al., 2015). A Fuzzy Correspondence Analysis (FCA) was conducted on this [samples x traits] matrix. The aim was to ordinate the samples according to their abundance-weighted trait modalities and to schematize variations in the combinations of the functional traits of ant communities in the ordination space. Significant changes in functional trait composition across habitats were evaluated using a k-means clustering, as in the previous PCA analysis, using the same R packages.

3.3. Ant assemblages in the habitats sampled After the a priori clustering of samples by habitat membership in the PCA space, the k-means clustering of samples in the PCA space (Fig. 2a) revealed that ant species assemblages from the rainforest and the treefall gap were similar (cluster 5) whereas other a posteriori groups mostly matched the a priori distribution (not represented) of samples by habitats (clusters 1–4), illustrating that each tree monoculture had specific ant assemblages and that these assemblages differed from those encountered in natural forest habitats. This is reflected in the distribution of habitat types among clusters derived from the k-means algorithm (Fig. 2b) showing that each cluster corresponding to tree plantations is strongly dominated by one tree species, whereas the forest and the treefall gap share the same cluster. 3.4. Relationships between habitat types and the functional traits of the ant species In the a priori clustering of functional traits by habitat membership in the FCA space (Fig. 3a), axis 1 separates the functional composition for ants living in the rubber tree plantation from those living in natural habitats and other types of plantations. The k-means clustering of samples in the FCA space (Fig. 3b) revealed that among a posteriori groups based on functional traits, habitat preference (HA) and nesting habits (NE), there were no significant differences between habitat types. Yet, feeding habits (FE) and geographical origin (GE) significantly separated the rubber tree plantations from all other habitats. Indeed, the rubber tree plantation sheltered more leaf-cutting, fungusgrowing ants, impacting FE, and more exotic species, impacting GE, than did the natural habitats and the other types of plantations (no significant difference between them) (see also Appendix A).

3. Results 3.1. General points A total of 247 ant species belonging to 52 genera from nine subfamilies (representing 3949 occurrences) was collected (Appendix A); among them only three, non-abundant species were exotic (Tapinoma melanocephalum, Cardiocondyla obscurior and Nesomyrmex wilda). The most species-rich subfamilies were the Myrmicinae (137 species from 23 genera), the Ponerinae (35 species from 10 genera), and the Formicinae (33 species from six genera), and the most speciose genera were Pheidole (35 species), Camponotus (20 species), Solenopsis (13 species) and Strumigenys (13 species). Twenty ant species out of the 247 (8.1%) were noted in all six habitats compared, but none of them abounded. Indeed, among them, the

4. Discussion The present study proves that creating relatively small monocultural tree plantations under conditions where the surrounding tropical rainforest is mostly preserved can limit biodiversity loss and so the consequences for ecosystem services although a decline in ant species 46

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layer whereas the top-down effect of predators, including ants, indirectly accelerates litter decomposition by regulating these communities (Sayer et al., 2010; McGlynn and Poirson, 2012; Ashford et al., 2013). Among the plantations compared here, the litter of the cocoa trees had the highest number of rarefied ant species as well as the highest values for true diversities of orders 1 and 2 (Table 1B). This is in line with the fact that cocoa tree plantations are considered the best compromise between agriculture and the conservation of the native leaflitter fauna in Neotropical forests, particularly when, planted under shade trees (in which case, the leaf litter is no longer homogenous), they interconnect forest fragments (Philpott and Armbrecht, 2006; Delabie et al., 2007; Cassano et al., 2009; Schroth et al., 2011). Among the compared monocultures, the pine tree plantation surprisingly shared the largest number of ant species with the forest (Fig. 2; Table 1B), likely due to the particularly thick litter layer (more than twice as thick as that of the forest; Table 1A). A thick litter layer improves both the quantity and diversity of litter-dwelling arthropods (Sayer et al., 2010; Ashford et al., 2013) and their regulation by ant predators (McGlynn and Poirson, 2012). Heavy rainfall in French Guiana likely favors this situation as litter-ant communities are impoverished in the litter of pine trees in other, drier areas (Sinclair and New, 2004; Corley et al., 2006; Pacheco et al., 2009). A lower diversity for Pheidole appears to be a good “indicator” of disturbance in the Neotropics (Delabie et al., 2009), something confirmed here as we noted 25 Pheidole species in the forest versus nine to 15 in the plantations (Appendix A). Generally, the creation of tree plantations results in the loss of certain native forest ant species and the expansion of generalist species (Philpott et al., 2010) that take advantage of changing resource bases, especially when a disturbance makes them highly competitive (Hoffmann and Andersen, 2003) or favors non-forest species (e.g., Ectatomma brunneum; Vasconcelos et al., 2000). Yet, due to a low turnover, generalist species of the genera Brachymyrmex, Camponotus, Nylanderia, Pheidole, Solenopsis and Wasmannia, which are known to survive in altered habitat conditions (Sinclair and New, 2004; Dejean et al., 2015a), were rare in the plantations studied here. The most frequent, Wasmannia auropunctata among the rubber trees, represented only 7.1% of the occurrences (Appendix A). Solenopsis saevissima, which characterizes human-disturbed Amazonian areas (Delabie et al., 2009; Dejean et al., 2015a), was infrequently observed in this study (Appendix A), as were the three exotic species noted; T. melanocephalum and C. obscurior are pantropical, and N. wilda is an arboreal myrmicine from Central America and the southern USA (Philpott et al., 2010; Wetterer, 2012; Antweb, 2016). Functional traits separated only the rubber tree plantation from all other compared habitats (Fig. 3a), the difference being significant for the leaf-cutting ant Atta cephalotes and the exotic species T. melanocephalum which are more abundant in this kind of plantation (Fig. 3B; see also Appendix A). Therefore, at least for litter-dwelling ants used as bioindicators, the functional diversity that develops in small, old plantations embedded in the rainforest tends to be comparable to that of natural areas, particularly for cocoa, acacia and pine trees. This unexpected result, which needs to be confirmed through further studies, reinforces the idea that (1) cocoa tree plantations are the best compromise between agriculture and the conservation of the native leaflitter fauna in Neotropical forests (Cassano et al., 2009; Schroth et al., 2011), (2) A. mangium favors the regeneration of the forest in particularly disturbed areas (Voigtlaender et al., 2012), and (3) P. caribaea might be planted for timber construction in already deforested areas (provided that the areas receive large amounts of rainfall). So, if limited in size, these three types of plantations can contribute to human sustainability, particularly when an area has already been deforested. In conclusion, biotic homogenization can be prevented when tree monocultures are small and embedded in the rainforest as functional diversity was preserved in three tree species plantations and only

Fig. 2. a. Principal Component Analysis (PCA) biplot (first two axes) and k-means clustering of samples in the ordination space according to their ant species composition (1–5 = k-means clusters). b. Distribution of habitat types (number of samples from the different habitats) among clusters derived from the k-means algorithm. (1) pine trees; (2) cocoa trees; (3) acacia trees; (4) rubber trees; (5) both forest and treefall gap.

diversity was noted (Fig. 1; Table 1B). Indeed, as shown by the value for global beta diversity, turnover was low as was the loss of native forest ant species (only 36 out of 124 ant species present in the forest were absent from the plantations, 29%; Appendix A). Furthermore, functional diversity was negatively affected only for the rubber tree plantation (Fig. 3). Even in this case, the effect was limited compared to the biotic homogenization noted in a southern Chinese industrial rubber tree plantation, even though it was voluntarily interspersed with fragments of natural forest (Liu et al., 2016). The situation was worse in a large Cambodian industrial rubber tree plantation with few nearby forested areas where the sharp decline in ant diversity was associated with a high occurrence of exotic, invasive ant species (Hosoishi et al., 2013). This study also confirms the notion that man-made disturbances result in greater changes in ant species composition than those caused by natural disturbances (Philpott et al., 2010Philpott and Armbrech, 2006) because the treefall gap was much less affected compared to the rainforest than were the plantations (Fig. 1). Furthermore, the ant community composition is significantly different between the four tree plantations (Fig. 2). The main cause of these differences is likely due to a homogenous leaf litter in monospecific plantations compared to natural forests (see Cole et al., 2016). In equatorial areas where temperature and rainfall are not limiting factors, litter quantity and quality (e.g., nitrogen content) intervene in decomposition processes and nutrient release, permitting soil fertility to be maintained. The comminution of the litter by earthworms and arthropods facilitates the activity of fungi and bacteria, improving decomposition and mineralization (Sayer et al., 2010; Ashford et al., 2013). Arthropod communities benefit from a thick litter 47

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Fig. 3. Fuzzy correspondence analysis (FCA) of functional trait composition in samples originating from the various habitats (e.g., forest, treefall gap, pine plantation). a. Ordination of samples on the first two axes of the FCA, and grouping of samples according to their original habitat. b. Distribution of species trait categories on the first two FCA axes. Each panel (FE, GE, HA, NE) can be compared to (or supersimposed on) the distribution of samples represented in ‘a’ to explain the set of traits categories associated with the various areas (or habitats) in the ordination space. Trait categories are positioned at the weighted average of their species. Abbreviations for the trait categories of the ant species are as follows. Feeding habits (FE): seeds, nectar or honeydew feeders (FE1), leaf-cutting, fungus-growing (FE2), fungus-growing from carcasses (FE3), army ants (FE4), generalist predators (FE5), specialized predators (FE6); Geographical Origin (GE): native (GE1), exotic (GE2); Habitat Preference (HA): forest (HA1), secondary areas (HA2), meadows or dry areas (HA3); and Nesting habits (NE): cryptic or subterranean (NE1), leaf-litter (NE2), arboreal (NE3).

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