Contrasting Effects of Plant Diversity Across Arthropod Trophic Groups In

Basic and Applied Ecology 17 (2016) 11–20

Contrasting effects of plant diversity across arthropod

trophic groups in plantain-based agroecosystems

a,b a,b c

Anicet Gbèblonoudo Dassou , Sylvain Dépigny , Elsa Canard ,

d e a,f,∗

Fabrice Vinatier , Dominique Carval , Philippe Tixier

CIRAD, UPR GECO, TA B-26/PS4, Boulevard de la Lironde 34398, Montpellier Cedex 5, France

CARBAP, African Research Centre on Bananas and Plantains, BP 832 Douala, Cameroon

IRD, UMR MIVEGEC, 911 Avenue Agropolis BP 64501, 34394 Montpellier Cedex 5, France

INRA, UMR LISAH, 2 place Pierre Viala, 34060 Montpellier Cedex 2, France

CIRAD, UPR GECO, CAEC, Petit Morne, BP 214, 97285 Le Lamentin Cedex 2, Martinique, France

CATIE, Departamento de Agricultura y Agroforesteria, 7170, Cartago, Turrialba 30501, Costa Rica

Received 15 December 2014; accepted 9 September 2015

Available online 25 September 2015

Abstract

Previous biodiversity studies have shown that plant diversity increases the complexity of arthropod food webs. However, only

a few studies have addressed this issue in tropical ecosystems, in which the small annual variations allow the community to

approach a steady state. With the goal of optimizing pest management, we studied the effect of plant diversity on the arthropod

community in 20 plantain-based ﬁelds in Cameroon. Plantain-based agroecosystems are especially useful for studying the

effects of plant diversity because they contain few to many non-plantain crop plants and are treated with few or no pesticides or

fertilizers. We measured the diversity of cropped plants and the abundance of ground-dwelling arthropods. Five trophic groups

13 15

of arthropods were identiﬁed based on stable isotopic signatures (␦ C and ␦ N). At the ﬁeld scale, predator abundance was

positively correlated with plant diversity while herbivore abundance displayed the opposite pattern. These strong and inverse

effects of plant diversity on predator and herbivore abundances suggest that top-down forces and resource concentration structure

the arthropod community in plantain ﬁelds. Our ﬁndings are consistent with other studies that showed a reduction of interaction

and interference between predators in more structured habitats. These ﬁndings will help in the design of plantain agroecosystems

that enhance pest control.

Zusammenfassung

Frühere Untersuchungen zur Biodiversität haben gezeigt, dass die Pﬂanzendiversität die Komplexität von Arthropoden-

Nahrungsnetzen erhöht. Indessen haben sich nur wenige Studien mit dieser Fragestellung in tropischen Ökosystemen befasst,

in denen geringe saisonale Umweltveränderungen der Gemeinschaft erlauben, einen Gleichgewichtszustand zu erreichen. Mit

dem Ziel einer optimierten Schädlingskontrolle untersuchten wir den Effekt der Pﬂanzendiversität auf die Arthropodengemein-

schaften von 20 Kochbananenfeldern in Kamerun. Diese Felder sind besonders gut für solche Untersuchungen geeignet, weil

zusammen mit der Kochbanane einige bis viele andere Nutzpﬂanzen angebaut werden und weil Pestizide oder Dünger kaum

oder gar nicht eingesetzt werden. Wir maßen die Diversität der angebauten Pﬂanzen und die Abundanz von bodenbewohnenden

Arthropoden. Fünf trophische Gruppen wurden anhand der Signaturen von stabilen Isotopen (13 C and 15 N)

∗

Corresponding author at: CATIE, Departamento de Agricultura y Agroforesteria, 7170, Cartago, Turrialba 30501, Costa Rica. Tel.: +33 467617152;

fax: +33 467615688.

E-mail address: [email protected] (P. Tixier).

http://dx.doi.org/10.1016/j.baae.2015.09.003

12 A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20

identiﬁziert. Auf der Felds kalawar die Abundanz der Räuber positiv mit der Pﬂanzendiversität korreliert, während die Abundanz

der Herbivoren einen entgegengesetzten Trend zeigte. Diese starken gegenläuﬁgen Effekte legen nahe, dass top-down-Kontrolle

und Ressourcen-Konzentration die Arthropodengemeinschaften von Kochbananenfeldern strukturieren. Unsere Befunde stim-

men mit anderen Untersuchungen überein, die einen Rückgang von Interaktion und Interferenz zwischen Räubern in stärker

strukturierten Habitaten gezeigt hatten. Diese Ergebnisse werden sich bei der Gestaltung von Kochbananen-Agrosystemen, die

die Schädlingskontrolle verbessern, als nützlich erweisen.

Keywords: Arthropod food webs; Field scale; Multitrophic interactions; Habitat structure; Cameroon; Musa spp. AAB group

Introduction crucial in the provision of pest control. Here, we investi-

gated the effect of plant diversity on the abundance of trophic

High functional diversity in agroecosystems provides and groups, and we assumed that their connections ranged from

promotes important services to human society such as bio- strong to weak. Based on the response of each trophic group

logical control, pollination, and nutrient cycling (Cardinale and of the studied taxa in terms of abundance, we assessed

et al. 2012). The effect of biodiversity on ecosystem char- the relative effects of bottom-up vs. top-down forces in struc-

acteristics, including belowground biomass, pollination, and turing the food web.

predation and parasitism of pests, is mediated by the hetero- The use of stable isotopes of C and N can be useful for

geneity of resources and their spatial organization (Tylianakis identifying homogeneous trophic groups and for generating

et al. 2008). Currently, there is a critical need to better hypotheses about their linkages. Because values of ␦ C (see

understand the effect of plant diversity on the functioning of “Materials and methods” section for details on the ␦ nota-

agroecosystems so as to enhance production and ecosystem tion) are relatively conserved along trophic chains, ␦ C is a

services. good marker of the resources consumed by a given organism

Plant diversity determines the structure of food webs (DeNiro & Epstein 1978). Basal resources have contrasting

(Eisenhauer et al. 2013; Haddad, Crutsinger, Gross, Haarstad, values of ␦ C, ranging from −30‰ to −5‰ for C3 and

& Tilman 2011) and affects the abundance, diversity, and C4 plants, respectively (Swap, Aranibar, Dowty, Gilhooly, &

functioning of species at higher trophic levels (Ebeling, Macko 2004; Yakir & Israeli 1995); this enables researchers

Klein, Weisser, & Tscharntke 2012; Loranger et al. 2014; to separate primary consumer taxa that feed on different basal

Unsicker et al. 2006). Scherber et al. (2010) documented resources. At the same time, the regular enrichment of N

a positive effect of plant diversity on the abundance and along trophic chains allows researchers to use ␦ N values to

diversity of most trophic groups (except invasive groups), estimate the trophic level of organisms (Minagawa & Wada

and this effect decreased with increasing trophic height. 1984; Ponsard & Arditi 2000). Taxa with similar values of

13 15

␦

Plant diversiﬁcation of agroecosystems is currently receiv- C and ␦ N are thus in the same trophic niche and con-

ing considerable attention from agroecologists (Fahrig et al. stitute a relatively homogeneous group (Newsome, Martinez

2011; Isbell 2015). More speciﬁcally, ecosystems with higher del Rio, Bearhop, & Phillips 2007).

plant diversity are expected to support increased levels of In the humid tropics of Africa, plantains (cooking bananas

pest regulation (Letourneau et al. 2011; Quijas, Schmid, with Musa AAB genome) are cropped in association with

& Balvanera 2010). Plant diversity helps sustain arthropod annual crops (roots, tubers, and vegetable crops) and peren-

populations, including increased abundances of natural ene- nial crops (cocoa, coffee, palm, and others). Plantain ﬁelds

mies (Tylianakis, Tscharntke, & Lewis 2007), and often may be planted with >20 kinds of other crop plants and are

supports increased levels of pest predation (Landis, Menalled, mainly managed with few or no inputs of fertilizer or pes-

Costamagna, & Wilkinson 2005). Pests can be controlled ticide. In most banana and plantain production areas, the

by both bottom-up effects from plants and by top-down most important pest is the banana weevil, Cosmopolites sor-

effects by natural enemies (Rosenheim 1998). Theory sug- didus (Coleoptera, Curculionidae) (Germar., 1825) (Gold,

gests that plant diversity enhances pest control by stabilizing Pena, & Karamura 2001). In a simple banana agroecosystem,

natural enemy communities (Tylianakis & Romo 2010) and previous studies have shown that the addition of a primary

by providing resources that have indirect effects on higher resource (a cover crop) altered the structure of the arthro-

trophic levels through bottom-up trophic cascades (Power pod community (Duyck et al. 2011), increased the abundance

1992). Diversiﬁed systems, however, do not always exhibit of a potential predator of C. sordidus (Solenopsis geminata,

decreases in pest numbers and damage (Letourneau et al. Myrmicinae), and increased S. geminata predation of C. sor-

2011). Indeed, in diversified agroecosystems, the predators didus eggs that were artificially placed in the fields (Mollot,

may feed on more abundant alternative prey, thus decreasing Tixier, Lescourret, Quilici, & Duyck 2012). We expect that

their control of pests (Holt 1977). The connectivity (i.e., the presence of multiple crops may also change the struc-

consumption intensity) between trophic groups is thus ture of arthropod food webs in plantain systems and should

A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20 13

consequently change the control of herbivores, including C. ants were collected with an aspirator. Ants were counted in

sordidus, by predators. digital photographs of the samples. Just after the bait trap

We studied the effects of plant diversity on the arthropod was removed, we deployed one banana stem trap (made of

community in plantain-based, multi-species agroecosystems one-half of a 20-cm-long segment of a plantain stem) in the

in Cameroon. We focused on the local scale, which has same position to capture other arthropods. After 48 h, all of

recently received less attention than the landscape scale even the arthropods that sheltered under the stem traps were col-

though it is the primary scale at which farmers manage plant lected with an aspirator. The combination of these two types

diversity. We determined the structure of arthropod food webs of trap provided more information about the ground-dwelling

13 15

in 20 farmer ﬁelds. Based on ␦ C and ␦ N isotopic signa- arthropod community, including ants that may interact with

tures, we identiﬁed arthropod trophic groups, i.e., arthropods C. sordidus, than a single type of trap. All samples of both

that shared the same food resources and consumers. We tested traps were kept for taxonomic description in the laboratory

the hypothesis that plot-scale plant diversity has different and were frozen for isotopic analysis. Ants were identiﬁed

effects on arthropods depending on their trophic level and with the aid of the Bolton key (Bolton 1974) and the PIAkey

their connectivity to each other. (Sarnat 2008). Other arthropods were identiﬁed based on the

literature (Appert & Deuse 1988; Lavabre 1992). Overall,

we determined the location of 8325 plants belonging to 31

Materials and methods

species (see Appendix A) and captured 19,946 ants belonging

to 11 species with bait traps and 1730 arthropods belonging

Study sites

to 19 species with banana stem traps. We retained for fur-

ther analysis the arthropods that were present in at least three

The study was conducted in the Moungo Department of the

ﬁelds with a total abundance in each ﬁeld >6 individuals;

Littoral Region of Cameroun (Central Africa) from June 2012

these criteria resulted in sufﬁcient replicates for statistical

to February 2013. We selected 20 ﬁelds in 20 farms located

≤ ◦ analysis in the case of 15 species of arthropods (Table 1).

5 km from the CARBAP Research Station (4 34 11.33

◦

N; 9 38 48.96 E; 79 m a.s.l.); the environmental conditions

are similar for all of the ﬁelds, which have a young brown Isotopic analyses

soil derived from a volcanic platform (Delvaux, Herbillon, &

Vielvoye 1989). The climate is humid tropical with a monthly We used isotopic analyses to determine the trophic niche

◦

mean temperature ranging from 25.0 to 27.4 C and a mean of each taxon, i.e., the primary producer that directly or indi-

annual rainfall of 2610 mm. All ﬁelds contained plantain rectly provides its carbon source, and its trophic height. This

crops (Musa AAB genome) and a diverse array of other annual evaluation of trophic niche was used to constitute homoge-

crops (roots, tubers, and vegetable crops) and perennial crops neous trophic groups. Changes in a consumer’s diet may be

(cocoa, coffee, palm, and others crops). These ﬁelds were indicated by changes in the isotopic signatures of C and

extensively managed, and no pesticide was applied during N (Oelbermann & Scheu 2002; Ponsard & Arditi 2000;

the study or in the 12 months preceding the study. Vanderklift & Ponsard 2003).

Once identiﬁed, arthropods were lyophilized for 48 h and

then ground into a ﬁne powder before a 1-mg sample of the

Identiﬁcation and enumeration of plants and

powder was placed in a tin capsule for analysis. For each

arthropods

of the 15 arthropod taxa that were identiﬁed and kept for

analyses, we measured one pooled sample per plot, lead-

In each ﬁeld, we determined the abundance of each arthro-

ing to 300 samples. Isotope ratios were determined with an

pod taxon and plant species once during two periods: the

isotope ratio mass spectrometer EA2000 (Eurovector) cou-

rainy season (mid-March 2012 to mid-November 2012) and

pled to an Isoprime mass spectrometer (elemental analyser)

the dry-season (mid-November 2012 to February 2013). In

at the Biochemistry and Plant Molecular Physiology Labo-

the centre of each ﬁeld, we delimitated one 12 m × 12 m zone,

ratory of the Integrative Biology Institute for Plants (IBIP)

which we subdivided into 2.4 m × 2.4 m quadrats, leading

at SupAgro-INRA of Montpellier-France. All stable isotope

to 25 measures per plot. In each quadrat, we identiﬁed all 13 15

values are reported in the ␦ notation, with ␦ C or ␦ N calcu-

crop plants. In these cropping systems, weeds are managed 13 12

lated as [(Rsample/Rstandard) − 1] × 1000, where R is C/ C

mechanically; thus the crop diversity was very close to the 15 14

or N/ N. Standards were PeeDee Belemnite (Peterson &

whole plant diversity. To measure the diversity and abundance

Fry 1987) and atmospheric air (Mariotti 1983) for C and N,

of the whole community of arthropods, we used two types of

respectively.

traps placed in the centre of each quadrat. First, we used

an attractive trap composed of 30 cm × 30 cm white ceramic

tiles, each of which had at its centre a 4 cm spot of bait com- Data processing and statistical analysis

posed of honey mixed with canned tuna. This ﬁrst type of

trap (the bait trap), which was designed to detect the diver- We deﬁned ﬁve trophic groups of arthropods based

13 15

␦ ␦ sity and abundance of ants, was deployed for 30 min before on their mean C and N values using the ‘hclust’

14 A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20

Table 1. Systematic classification of the most abundant arthropod taxa identified in 20 plantain fields in Cameroon.

No. Taxon name Trophic group Class Order Family

1 Cosmopolites sordidus 1 Insecta Coleoptera Curculionidae

2 Metamasius hemipterus 2 Insecta Coleoptera Curculionidae

3 Pachybolidae 2 Diplopoda Spirobolida Pachybolidae

4 Termitidae 2 Insecta Blattodea Termitidae

5 Gryllus spp. 3 Insecta Orthoptera Gryllidae

6 Porcellionidae 3 Malacostraca Isopoda Porcellionidae

7 Camponotus acvapimensis 4 Insecta Hymenoptera Formicidae

8 Tenebrionidae 4 Insecta Coleoptera Tenebrionidae

9 Monomorium spp. 4 Insecta Hymenoptera Formicidae

10 Odontomachus troglodytes 4 Insecta Hymenoptera Formicidae

11 Paratrechina longicornis 4 Insecta Hymenoptera Formicidae

12 Pheidole megacephala 4 Insecta Hymenoptera Formicidae

13 Pheidole spp. 4 Insecta Hymenoptera Formicidae

14 Araneae 5 Arachnida Araneae

15 Dermaptera 5 Insecta Dermaptera

Not identiﬁed.

function from the package ‘cluster’ version 1.14.1 (Maechler,

Rousseeuw, Struyf, Hubert, & Hornik 2011) of the R soft-

ware (R Development Core Team 2012). The clustering was

performed through a hierarchical analysis using a set of

dissimilarities with the “Ward” method (Ward 1963). The

abundance of each trophic group was calculated by summing

the abundance of arthropods belonging to the group. Plant

diversity was assessed with the Shannon index (Shannon

1948), which was calculated with the ‘diversity’ function of

the ‘vegan’ package, version 2.2-1 (Oksanen et al. 2015).

We analyzed the effect of the ﬁeld-scale plant diversity

on the abundance of arthropod species and trophic groups

based on the sum of the capture of the 50 traps in each ﬁeld.

Poisson generalized linear mixed-effects models (GLMM,

Bolker et al. 2009) were used to examine the relationship

between plant diversity and arthropod abundances. When

overdispersion was >5 (Venables & Ripley 2002), we used

negative binomial GLMMs, which provide an improved ﬁt

to overdispersed count data (Zuur 2009). We considered

13 15

the ‘season’ (dry or rainy) as a random intercept factor. Fig. 1. Values of ␦ C and ␦ N for the studied taxa (means ± SE)

The effect of the plant diversity was tested against a null and identiﬁcation of ﬁve arthropod trophic groups. The number next

model with a Chi-square test. The GLMMs were ﬁtted by to each point corresponds to the taxon number presented in Table 1.

the Laplace approximation using the ‘glmer’ function in the

‘lme4 package (Bates, Maechler, & Bolker 2011). All statis- 15

an isotopic signature for ␦ N of 5‰ for species means, was

tical analyses were performed with R 2.15.0 (R Development

composed only of C. sordidus. Trophic group 2, whose iso-

Core Team 2012) and with an alpha level of 0.05. 15

topic signatures for ␦ N ranged from 5 to 8‰ for species

means, was composed of the herbivore/detritivore taxa Meta-

masius hemipterus, Pachybolidae, and Termitidae. Trophic

Results 15

group 3, which had isotopic signatures for ␦ N ranging from

Determination of trophic groups 9 and 10‰ for species means, was composed of the detriti-

vore/omnivore taxa Gryllus spp. and Porcellionidae. Trophic

The isotopic signatures of arthropods ranged from −15 group 4, which had isotopic signatures for ␦ N ranging

13 15

to −35‰ for ␦ C and from 0 to 25‰ for ␦ N. Cluster- from 8 and 13‰ for species means, included the omni-

13 15

ing based on ␦ C and ␦ N led to the deﬁnition of ﬁve vore/predator ants Camponotus acvapimensis, Monomorium

trophic groups (Fig. 1, Table 1). Trophic group 1, which had spp., Odontomachus troglodytes, Paratrechina longicornis,

A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20 15

& Wada 1984). Our results show that the abundances of

the herbivore and omnivore trophic groups were negatively

correlated with plot-scale plant diversity, while the abun-

dance of the predator trophic group was positively correlated

with plot-scale plant diversity. These results are therefore

consistent with the hypothesis that plot-scale plant diversity

differentially alters arthropods depending on their trophic

level in plantain-based agroecosystems. That plant diver-

sity positively affects arthropods at higher trophic levels but

negatively affects arthropods at lower trophic levels sug-

gests that top-down forces are important in structuring the

arthropod community (Dyer & Letourneau 2003). Further-

more, the connectivity of the trophic groups (as indicated

by their ␦ C signatures) seems to be important in mediat-

ing top-down forces. Another study reported similar results

for predator and herbivore abundance (Haddad et al. 2009)

but with a weaker negative effect of plant diversity on the

lowest trophic levels. Our results support the general ﬁnding

Fig. 2. Predicted effect of plant diversity on the abundance of arthro-

that areas with high plant diversity enhance predator pres-

pod taxa. Only signiﬁcant effects are shown. See Table 2 for details

ence and abundance (Letourneau et al. 2011). In our case,

concerning the statistical analysis.

the results also suggest that abundant predators represent a

pressure on the lowest trophic levels to which they are con-

nected, and consequently keep their abundance at low levels.

Pheidole megacephala, and Pheidole spp., and omnivorous

The positive effect of plant diversity on predators may be

taxa of the Tenebrionidae. Trophic group 5 had high isotopic

15 explained by the provision of more diversiﬁed resources but

signatures for ␦ N (the mean values for species ranged from

also by non-trophic effects, i.e., increased plant diversity is

13 to 14‰) and included generalist predators belonging to

likely to increase habitat diversity and thus reduce interfer-

Dermaptera and Araneae.

ence between predators. Non-trophic effects can also alter

trophic interactions, e.g. the moderation of intraguild pre-

Relationship between plant diversity and the dation that may dampen the control of lower trophic levels

abundance of taxa and trophic groups (Finke & Denno 2002, 2006).

Although theory predicts that trophic cascades are most

Plant diversity was positively related to the abundance of likely to occur in less diverse systems (Polis & Strong 1996),

C. acvapimensis, M. hemipterus, and Dermaptera and was other effects such as the accessibility of plant resources and

negatively related to the abundance of the Porcellionidae, the structure of habitats should be considered by researchers

Rhinocricidae, P. longicornis, Pheidole sp., and Termitidae attempting to unravel multitrophic interactions (Polis, Sears,

(Table 2, Fig. 2). The relationship between plant diversity Huxel, Strong, & Maron 2000). Because herbivores often

and abundance was nearly signiﬁcant for C. sordidus but was depend on speciﬁc plant hosts as food sources, herbivore

not signiﬁcant for the Araneae, Gryllus spp., Monomorium numbers could decline with increasing plant diversity simply

spp., O. troglodytes, P. megacephala, or the Tenebrionidae because the percentage of preferred plant hosts in the com-

(Table 2). Plant diversity was positively related to the abun- munity decreases as plant diversity increases. In our study,

dance of trophic group 5 (generalist predators) but was however, this effect was probably weak, because the herbi-

negatively related to the abundances of trophic groups 2 (her- vore taxa that were negatively affected by increasing plant

bivores/detritivores) and 4 (omnivores/predators) (Fig. 3). diversity (trophic group 2) are generalists, i.e., they feed on

The relationship was nearly signiﬁcant for trophic group 1 many plant/detritus resources. We suggest that the top-down

but was not signiﬁcant for trophic group 3 (Table 2). control might be the main reason of their decrease as plant

diversity increased. Plant diversity in polycultures increases

herbivore movement (Straub et al. 2014), which probably

Discussion increases herbivore vulnerability to predation (Root 1973).

Predators, in contrast, may directly beneﬁt from increased

In all cases, the trophic levels that we observed for plant diversity because a more diversiﬁed plant community

the arthropod taxa were consistent with those previously may provide predators with favourable habitats. To assess the

reported. The difference in trophic level between the taxa at relative importance of the change in the basal food resource

the lowest levels (groups 1 and 2) and those at the highest level vs. the change in habitat with change in plant diversity, lab-

(group 5) was consistent with the ␦ N enrichment usually oratory experiments may be useful (Kalinkat, Brose, & Rall

observed between a consumer and its resource (Minagawa 2013).

16 A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20

Table 2. Effect of plant diversity on the abundance of ﬁve arthropod trophic groups at the plot scale. Statistics presented are the result of

comparison of the null model with models that include plot-scale plant diversity as an explicative variable.

Trophic group Df Estimate SE estimate AIC dAIC logLik χ Pr (>χ )

1. Cosmopolites sordidus 3 −0.06 0.03 330.22 1.38 −162.11 3.38 0.0661

2. Herbivorous and detritivores* 4 −0.14 0.07 403.94 5.12 −197.97 7.12 0.0076

Metamasius hemipterus 3 0.32 0.06 186.74 23.28 −90.37 25.28 <0.0001

Pachybolidae* 4 −0.32 0.10 360.61 13.56 −176.30 15.56 <0.0001

− −

Termitidae 3 0.18 0.07 229.18 3.72 111.59 5.72 0.0168

3. Herbivores 3 0.09 0.08 110.13 −0.99 −52.07 1.01 0.3148

Gryllus spp. 3 −0.04 0.07 152.14 −1.56 −73.07 0.44 0.5067

Porcellionidae* 4 −0.47 0.17 234.40 24.16 −113.20 26.16 <0.0001

4. Omnivores and predators* 4 −0.13 0.09 373.49 2.52 −182.74 4.52 0.0334

Camponotus acvapimensis* 4 0.28 0.12 252.12 7.04 −122.06 9.04 0.0026

−

Tenebrionidae 3 0.09 0.07 135.16 0.42 −64.58 1.58 0.2086

−

Monomorium spp.* 4 0.02 0.17 247.17 1.95 −119.59 0.05 0.8229

Odontomachus troglodytes 3 0.03 0.04 255.32 −1.41 −124.66 0.59 0.4441

Paratrechina longicornis 3 −0.57 0.08 224.62 57.97 −109.31 59.97 <0.0001

Pheidole megacephala* 4 0.07 0.16 195.70 −1.40 −93.85 0.60 0.4375

Pheidole spp.* 4 −0.28 0.19 196.95 2.85 −94.48 4.85 0.0277

5. Generalist predators 3 0.14 0.04 199.89 13.63 −96.95 15.63 <0.0001

Araneae 3 0.03 0.05 163.10 −1.53 −78.55 0.47 0.4952

Dermaptera 3 0.29 0.05 189.34 26.26 −91.67 28.26 <0.0001

Models of taxa or trophic groups marked with ‘*’ were ﬁtted using a negative binomial distribution to account for the overdispersion of errors; others were

ﬁtted with a Poisson distribution.

Our trapping method captured most of the ground-dwelling stable over years, and the presence of a perennial crop rein-

arthropods in plantain ﬁelds, especially those that interact forces this stability. Another factor that contributes to the

with C. sordidus, and the diversity of captured taxa was at establishment of a relatively stable arthropod community

least as great as in other studies conducted in banana ﬁelds in the studied plantain systems is the absence of pesticide

(Duyck et al. 2011; Tixier, Dagneaux, Mollot, Vinatier, & treatments.

Duyck 2013). It would be useful, however, to complement Our results also support the hypothesis that plant diver-

the banana stem and bait traps with other methods such as sity increases herbivore control only for trophic groups

pitfall traps and vacuum sampling. well-connected to predators. We inferred the connection

While our results are consistent with some experiments strength of herbivores to predators from their C signa-

that show strong top-down and cascading effects of preda- tures because C signatures are relatively well-conserved

tors (Dyer & Letourneau 2003), our results also differ across trophic levels (DeNiro & Epstein 1978). Thus, C

from those of other biodiversity experiments. For instance, signatures indicate that the herbivores/detritivores of trophic

Scherber et al. (2010) showed that plant diversity had a pos- group 3 are far less connected than those of group 2 to

itive effect on the abundance of most trophic groups and the omnivores and predators of groups 4 and 5 (Fig. 1).

that this effect tended to decrease with trophic level, sug- This apparent disconnection of group 3 with the rest of the

gesting that bottom-up effects controlled the community. food web perhaps explains why the abundance of group 3

Similarly, the recent grassland biodiversity experiment of taxa was not signiﬁcantly affected by differences in plant

Rzanny, Kuu, and Voigt (2013) showed that the composi- diversity.

tion of the arthropod community was mainly determined by We hypothesize that the positive effect of plant diversity

plant-mediated, bottom-up forces. In contrast to our trop- on predators (trophic group 5) can be attributed to an increase

ical study, however, the latter two studies were conducted in primary resources and to more suitable habitats. Inversely,

in temperate regions. Whereas winters in a temperate cli- the negative effect of plant diversity on the abundance of

mate induce an annual collapse in the abundance of all omnivores (trophic group 4) may be attributed to a reduced

taxa, a tropical climate is relatively stable and therefore sup- suitability of habitat for ants, which are the main component

ports a relatively less perturbed community. We argue that of this group, and to predation from higher trophic levels

the relatively stable conditions in the plantain-based sys- (probably trophic group 5). Our results show that in plant-

tems of the current study (these systems were at least 5 diversiﬁed systems, higher trophic levels play a major role

years old) allowed top-down forces to structure the com- in the structure of the arthropod community and in the reg-

munity. In plantain-based systems, the plant community is ulation of herbivores. These results are consistent with the

A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20 17

Fig. 3. Abundance of trophic groups 1–5 as a function of plant diversity measured at the plot scale. Symbols indicate measured abundance

(ﬁlled circles and open squares show the dry and wet season, respectively), and lines indicate abundance predicted by GLMM when the

GLMM analysis was signiﬁcant (the line is in grey when it was nearly signiﬁcant, i.e., with p < 0.07). See Table 2 for details concerning the

statistical analysis.

meta-analysis from Letourneau et al. (2011), which showed we can expect a low to null bottom-up effect of plant diver-

that an increase in plant diversity reduces the abundance sity on its abundance. However, plant diversity may play a

of herbivores and increases the abundance of their preda- role in its spatial dispersion. Previous research has shown

tors. that plant diversity (other than Musacea) creates patches of

The weak effect of plant diversity on the control of our habitats that may alter the perception range of C. sordidus

main pest (C. sordidus, trophic group 1) may be explained (Vinatier et al. 2010, 2011) and also fragment its resources

by its speciﬁcity for Musacea and by a moderate connectivity (Vinatier, Lescourret, Duyck, & Tixier 2012), thereby chang-

to potential predators. Because C. sordidus is oligophagous, ing its population dynamics. C. sordidus was moderately

18 A.G. Dassou et al. / Basic and Applied Ecology 17 (2016) 11–20

connected to trophic group 4 and 5 in the current study, Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen,

suggesting a weak top-down effect. Among predators that J. R., Stevens, M. H. H., et al. (2009). Generalized linear mixed

are likely to consume C. sordidus, only the taxa of the models: A practical guide for ecology and evolution. Trends in

Ecology and Evolution, 24, 127–135.

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Bolton, B. (1974). The ant genera of West Africa: A syn-

diversity. Because taxa in the Dermaptera consume C. sor-

onymic synopsis with keys (Hymenoptera: Formicidae). Bulletin

didus (Mollot et al. 2014), we hypothesize that the predation

of the British Museum (Natural History) entomology, 27,

by taxa in this order partly explains the weak, negative

319–366.

response of C. sordidus to plant diversity. Future manage-

Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings,

ment options might attempt to better connect C. sordidus

C., Venail, P., et al. (2012). Biodiversity loss and its impact on

to the Dermaptera, perhaps by identifying and removing the

humanity. Nature, 486, 59–67.

potential resources of alternative prey of Dermaptera to mini- Delvaux, B., Herbillon, A. J., & Vielvoye, L. (1989). Characteriza-

mize the apparent competition between C. sordidus and these tion of a weathering sequence of soils derived from volcanic ash

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depending on trophic group. Consistent with results from

Duyck, P. F., Lavigne, A., Vinatier, F., Achard, R., Okolle, J. N., &

temperate studies, we found that plant diversity tended

Tixier, P. (2011). Addition of a new resource in agroecosystems:

to increase the abundance of predators and to reduce

Do cover crops alter the trophic positions of generalist predators?

the abundance of lower trophic groups. Our results sug-

Basic and Applied Ecology, 12, 47–55.

gest that both trophic and habitat effects structure the

Dyer, L. A., & Letourneau, D. (2003). Top-down and bottom-up

arthropod community and that increases in plant diversity diversity cascades in detrital vs. living food webs. Ecology Let-

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Multitrophic effects of experimental changes in plant diversity

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169, 453–465.

Acknowledgements Eisenhauer, N., Dobies, T., Cesarz, S., Hobbie, S. E., Meyer, R.

J., Worm, K., et al. (2013). Plant diversity effects on soil food

The authors thank Pascal Tillard from SupAgro-INRA webs are stronger than those of elevated CO2 and N deposi-

Montpellier for help with the isotopic analysis; Gabriel Fansi tion in a long-term grassland experiment. Proceedings of the

National Academy of Sciences of the United States of America,

and Justin Lowé from CARBAP for help in the plantain

110, 6889–6894.

ﬁelds; and Zéphirin Tadu, Régis Babin, and Léila Bagny

Fahrig, L., Baudry, J., Brotons, L., Burel, F. G., Crist, T. O., Fuller,

Beilhe for help in the identiﬁcation of arthropod taxa. We

R. J., et al. (2011). Functional landscape heterogeneity and ani-

also thank the plantain farmers for allowing us to work in

mal biodiversity in agricultural landscapes. Ecology Letters, 14,

their ﬁelds. This work is part of a PhD thesis of Anicet

101–112.

Gbèblonoudo Dassou and was funded by CIRAD (AIRD

Finke, D. L., & Denno, R. F. (2002). Intraguild predation dimin-

grant).

ished in complex-structured vegetation: Implications for prey

suppression. Ecology, 83, 643–652.

Finke, D. L., & Denno, R. F. (2006). Spatial refuge from intraguild

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Appendix A. Supplementary data

cades. Oecologia, 149, 265–275.

Gold, C. S., Pena, J. E., & Karamura, E. B. (2001). Biology and

Supplementary data associated with this article can be

integrated pest management for the banana weevil Cosmopolites

found, in the online version, at http://dx.doi.org/10.1016/ sordidus (Germar) (Coleoptera: Curculionidae). Integrated Pest

j.baae.2015.09.003. Management Reviews, 6, 79–155.

Haddad, N. M., Crutsinger, G. M., Gross, K., Haarstad, J., Knops, J.

M. H., & Tilman, D. (2009). Plant species loss decreases arthro-

pod diversity and shifts trophic structure. Ecology Letters, 12,

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