Taxonomic and functional composition of arthropod assemblages across contrasting Amazonian ...

13 Pages·2015·2.36 MB·English

JournalofAnimalEcology2016,85,227–239 doi:10.1111/1365-2656.12445
Taxonomic and functional composition of arthropod
assemblages across contrasting Amazonian forests
Greg P. A. Lamarre1,2,3*, Bruno He(cid:1)rault4, Paul V. A. Fine5, Vincent Vedel2,3,
Roland Lupoli3, Italo Mesones5 and Christopher Baraloto2,6
1Universite(cid:1)Antilles-Guyane, UMR Ecologiedes Fore^ts deGuyane,97310Kourou, FrenchGuiana; 2INRA, UMR
Ecologie desFore^ts deGuyane,97310, Kourou,French Guiana;3Socie(cid:1)te(cid:1)Entomologique Antilles-Guyane, 97354
Re(cid:1)mire-Montjoly, FrenchGuiana; 4CIRAD, UMR Ecologie desFore^ts deGuyane,97310Kourou, FrenchGuiana;
5DepartmentofIntegrative Biology, University ofCalifornia, Berkeley, 1005Valley LifeSciences Building #3140,
Berkeley, CA 94720,USA; and 6International Center forTropical Botany,Departmentof BiologicalSciences,
International Center forTropical Botany,FloridaInternational University, Miami, FL33199,USA
Summary
1. Arthropods represent most of global biodiversity, with the highest diversity found in tropi-
cal rain forests. Nevertheless, we have a very incomplete understanding of how tropical
arthropod communities are assembled.
2. We conducted a comprehensive mass sampling of arthropod communities within three
major habitat types of lowland Amazonian rain forest, including terra firme clay, white-sand
and seasonally flooded forests in Peru and French Guiana. We examined how taxonomic and
functional composition (at the family level) differed across these habitat types in the two
regions.
3. The overall arthropod community composition exhibited strong turnover among habitats
and between regions. In particular, seasonally flooded forest habitats of both regions com-
prised unique assemblages. Overall, 17(cid:1)7% (26 of 147) of arthropod families showed signifi-
cant preferences for a particular habitat type.
4. We present a first reproducible arthropod functional classification among the 147 taxa
based on similarity among 21 functional traits describing feeding source, major mouthparts
and microhabitats inhabited by each taxon. We identified seven distinct functional groups
whose relative abundance contrasted strongly across the three habitats, with sap and leaf
feeders showing higher abundances in terra firme clay forest.
5. Our novel arthropod functional classification provides an important complement to link
these contrasting patterns of composition to differences in forest functioning across geograph-
ical and environmental gradients. This study underlines that both environment and biogeo-
graphical processes are responsible for driving arthropod taxonomic composition while
environmental filtering is the main driver of the variance in functional composition.
Key-words: Amazon, arthropod community, environmental filtering, forest habitat, French
Guiana, functional composition, mass sampling, Peru, trophic cascades
quantify arthropod diversity. Moreover, we have little
Introduction
idea how arthropod communities are structured across
Arthropods represent most of the world’s biodiversity, geographical and environmental gradients. In megadiverse
with the highest species richness totals found in tropical tropical forests, an important component of plant diver-
rain forests. Yet with less than 1(cid:1)5 million species sity is the turnover of species composition across geo-
described out of the estimated 6 million insect species graphical regions and contrasting habitats (i.e. beta
globally (Hamilton et al. 2011; Basset et al. 2012), we diversity, Condit et al. 2002; Tuomisto et al. 2003). Cur-
have hardly scratched the surface in our attempt to rent evidence suggests that herbivorous insects may vary
in abundance because of changing environmental condi-
tions across habitat gradients (Novotny et al. 2005;
*Correspondenceauthor.E-mail:[email protected]
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety
228 G. P.A. Lamarre
Rodriguez-Castan~eda et al. 2010), or due to geographical evolutionary trade-offs in allocation to growth and
variation in co-evolutionary dynamics (Thompson & Cun- defence against herbivores (Fine, Mesones & Coley 2004;
ningham 2002). However, contrasting predictions have Fine et al. 2006). We therefore predict that arthropod
been made for the contribution of beta diversity to regio- community composition varies strongly among habitats
nal diversity within lowland tropical forests. For instance, types because of differences in resource availability, plant
Novotny et al. (2007) present evidence for a greater num- composition andhabitat structure.
berofgeneralistherbivoresresultinginalowspeciesturn- Complementary insights into the role of environmental
over across relatively large areas in Papua New Guinea. filteringincommunityassemblycanbegleanedusinganal-
In contrast, Dyer et al. (2007) suggest that tropical low- yses of functional composition (Cadotte, Carscadden &
land forests should have a high arthropod beta diversity Mirotchnick2011).Moststudiesexamininginsectdiversity
because of higher host specificity than in temperate havefocusedonspeciesrichnessortaxonomiccomposition
forests. (Erwin1982; Novotnyet al. 2002,2007; May2010; Basset
Pioneering attempts tostudytropical insectassemblages et al. 2012). Yet the literature on assembly rules in plant
involvedfoggingseveralindividualsofasingletreespecies communities has underlined contrasts between patterns of
(Erwin 1982). Recently, studies have employed hand col- taxonomic and functional diversity and composition (Bar-
lections of known host plant lineages to estimate alpha alotoet al.2012;Lavorelet al.2013).Itisnotuncommon
and beta diversity and the degree of host specialization for unrelated taxonomic groups of arthropods to share
(Novotny et al. 2002, 2006; Ødegaard, Diserud & Ostbye similar functions, such as the leaf-chewing habit of Nym-
2005; Dyer et al. 2007; Rodriguez-Castan~eda et al. 2010; phalidaelarvae(Lepidoptera)andChrysomelidae(Coleop-
Basset et al. 2012). While these studies have revealed tera). If food substrates vary across forest types, as
important patterns of diversity and specificity of particu- suggested by studies showing denser leaf, stem and roots
lar arthropod lineages, they are far from representative of tissuesinwhite-sandforests(Fortunelet al.2014),thenwe
complete arthropod communities (Ødegaard et al. 2000; would predict higher turnover in arthropod functional
Sobek et al. 2009; Rodriguez-Castan~eda et al. 2010; De compositionthanmightbeexpectedfrompatternsofturn-
Vries et al. 2012) or are very restricted in geographical over in taxonomic composition. Turnover in functional
area (Novotny et al. 2005; Basset et al. 2012). A more compositionmayalso provideamoremeaningfulassay of
comprehensive macroecological approach would sample the role of arthropod communities in ecosystem processes
entire arthropod communities at large geographical scales such as decomposition (Lavorel et al. 2013). In this study,
using a combination of traps in a wide variety of habitat we sampled representative arthropod communities across
types. Yet to our knowledge, no such community-level white-sand, terra firme and flooded forests in lowland
arthropod compositionstudyhasbeen conductedintropi- Amazonian rain forests of Peru and French Guiana. We
cal rain forests, and therefore, the factors governing then used these collections to investigate how taxonomic
assembly rules in tropical arthropod communities are still and functional composition varied across the three con-
poorlyunderstood. trasted tropical forest habitats at broad geographical
In the Amazon basin, three broad types of lowland for- scales.
est habitats have been distinguished based on soil texture
and fertility and seasonal water stress, and associated for-
Materials and methods
est structure (Baraloto et al. 2011): (i) nutrient-poor and
dry soils of the white-sand forest (hereafter WS) that are
study sites and environment
often surrounded by (ii) terra firme clay forest with high
soil nutrient content (TF); and, in low-lying areas nears
This study was conducted in 12 plots within four representative
rivers and streams (iii) seasonally flooded forests (SF) in sites (Fig.1) that represent the entire range of variation in cli-
which episodic flooding often submerges soil surfaces dur- matic, edaphic and forest structure factors observed in a larger
ing periods of high precipitation or Andean snowmelt plot network in lowland tropical forests of South America in
(Baraloto et al. 2007). A unique floristic composition Loreto, Peru, and French Guiana (Baraloto etal. 2011). Each
among these three habitats has been detected, with a high plotconsistsoften10950mtransectsdistributedthroughouta
spatial turnover among tree species (Baraloto et al. 2007; 2-haareathatischosenforhomogeneityandtorepresentagiven
Fine et al. 2010; Wittmann, Scho€ngart & Junk 2010), forest habitat in a given region. UTM coordinates for each plot
(Universal Transverse Mercator system using WGS 1984 datum)
including host plant species on which arthropods rely for
were collected using handheld Garmin 60csx units. Environmen-
nourishment and shelter (Price 2002). A recent study con-
tal variables describing climate, soil and forest structure were
ducted among habitat-specialist tree species has shown
used in order to define the environmental conditions of each
contrasting patterns in leaf production and insect her-
studied plot (for complete details, see Baraloto etal. 2011). Soil
bivory rates across habitats (Lamarre et al. 2014), with physicalandchemicaldescriptionswereconductedontenbulked
consistently higher rates of leaf production in seasonally samplesofsurfacesoil(0–20cmdepth)collectedthroughouteach
flooded forests (Lamarre et al. 2012a). Contrasting plot. Climatic variables were calculated using M(cid:1)et(cid:1)eo-France data
environmental conditions may therefore select for differ- in French Guiana and from IIAP weather stations in Peru. Cli-
ent ecological strategies in tropical trees, including mate in the Guianas is driven by a marked seasonal alternation
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
Drivers ofAmazonian arthropod assemblages 229
(a)
(e) (b)
(d) (c)
Fig.1. SamplingsitesandtrapmethodsinstalledintheAmazonBasin.(a)MapoftheAmazonregionwithmajorwatersheds,illustrat-
ingsites(circles)andplots(dots)establishedinthenorthern(Porvenir)andsouthern(JenaroHerrera)regionsofLoreto,Peru;andthe
western (Laussat) and eastern (Regina) regions of French Guiana. (b) Automatic light trap. (c) Malaise trap. (d) The new type of
windowpanetrapdevelopedinFrenchGuiana.(e)Aerialfruittrap.
between a wet season (December to August) and a dry season (Lamarreetal.2012b).Tocapturemultidirectionaltrajectoriesof
(September to November). In French Guiana, the intertropical insectsflyingthroughtheforestunderstorey,weinstalledonepair
convergence zone results in heavy rains with up to 120mm on ofeachMTandWTinoraroundgapsineachplot.Thesetraps
somedaysinDecembertoFebruaryandApriltoJuly.Amarked were collected every 6days during the study period in each
and short dry season in March is also characteristic of the Gui- region.
anas, in addition to a long dry period during August to Novem- Eachfruit trap (4FTs perplot) was installedand fixed in tree
ber (Wagner etal. 2011). In contrast with the Guianas, there is branches between 3 and 5m high and collected every 2days.
no distinctive dry season in northern Peru, although it also can Thesetrapsconsistofa1-mmosquitonetcylinderinwhichafer-
have short periods of heavy precipitation for several days (Mar- mented mixture of banana, sugar and rum actively attract fruit-
engo 1998). Each habitat type was separated by 1km to avoid feedingbutterfliesandtoalesserextendnectar-feedingbutterflies
collecting specimens (i.e. avoiding the ‘tourist’ issue, see andafewothertaxa(i.e.grasshoppers,beetlesandwasps).
Ødegaard2004)fromadjacenthabitats. Finally, we installed one portable automatic light trap (ALT)
with an 8-W backlight tube to collect light-attracted arthropods
sampling arthropod communities during each new moon of the study period (+/(cid:3)2days). We
installedALTsinthemiddleofeachplotandtrappedforatotal
Arthropod communities were sampled weekly in the twelve per- of 24 sampling nights over the study period. Each of the trap
manent plots from August to November 2010 in French Guiana typeswasseparatedbyatleast20mtoavoidspatialinterference
andbetweenMayandSeptember2011inPeru,correspondingto both between and within traps. We employed equal sampling
drier periods in each region. We employed a multiple trapping effort in terms of number of day–night periods for each trap in
method composed of two types of flight interception trap (FIT), eachplotandineachcountry.
the malaise trap (MT) and the windowpane trap (WT); and two
types of attractive traps: the fruit trap (FT) and the automatic taxonomic sorting and collections
lighttrap(ALT)(Fig.1). Foreachplot,onepairofeachFIT(2
MTs+2WTs)andtwopairsofFTwereinstalledwithinthefor- For each plot (aggregating the collections of multiple traps),
est understorey of the 2-ha surface area covered. Malaise and adult arthropods including five important major insect orders in
windowpane traps represent wide interception surfaces that are Insecta (Coleoptera, Lepidoptera, Hemiptera, Hymenoptera and
together collecting a representative portion of flying arthropods Orthoptera) in addition to spiders (Araneae) were counted and
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
230 G. P.A. Lamarre
identified to the family level. This level of taxonomic resolution Table1. Listofthe21functionaltraitsusedinthisstudy
hasbeenfoundtobesufficientfordetectingsomesignificantpat-
terns of community composition and beta diversity in temperate Categories Functionaltraits Detailsb
systems(Timmsetal.2013).Moreover,family-levelidentification
Feedingsource Leaf Leaf-feedinginsect
has provided ecologically adequate surrogates for species in the
Sap Includingphloem,
study of functional diversity (see also Cardoso etal. 2011 for
xylemandmesophyll
both temperate and tropical systems). Because of strong diver-
cellsucker
gence in life histories within some family-level taxa, eight diverse
Wood-related Includingdecayed
groupsweresortedfurthertothesubfamilylevel(Lawrenceetal. vegetation
1999): Ceratocanthinae (Hybosoridae), Colydiinae (Zopheridae), (saproxylophagous)
Malachiinae (Melyridae), Paussinae (Carabidae), Platypodinae, Invertebrates Predatorandparasitoid
Scolytinae(Curculionidae),Noctuinae(Erebiidae)andScydmaen- Organicmatter Includingdung
inae (Staphylinidae). Three hymenopteran taxa (Chalcidoidea, FruitandFlower Includingseed,nectar
IchneumonoideaandProctotrupoidea)couldbeidentifiedonlyto andpollenfeeder
Fungi-related Fungivore
thesuper-familyduetoourinabilitytoconsistentlyseparatethem
Scavenge Insectsthatscavenge
further.Duetothelackofknowledgeinidentificationandclassi-
asresource-use
fication of some groups, we excluded all Diptera, Odonata and
Mouthparts Mandibulates Aninsecthavingmandible
specimensinsmallorders(Phasmatodea,Mantodea).Mostspeci- Piercing–sucking Insectwithmouthpart
mens in Gryllacrididae, Anostostomatidae, Rhaphidophoridae modifiedforpiercing
andGryllidaefamilies(Orthoptera)werehighlydamagedbecause andsucking
of the windowpane trap collecting methods and were therefore Siphoning Insectwithmouthpart
excludedfromtheanalysis.Becauseoftheirimportantfunctional modifiedforsiphoning
role in ecosystems (Cardoso etal. 2011), we included spiders in Habitats Terrestrial Insectsthathave
our sample and were able to capture a representative portion of terrestrialhabit
Aquatic Insectsthathaveaquatic
themwithourflightinterceptiontraps(Vedel,Camus&Lamarre
orsemi-aquatichabit
2011). Samples were sent to taxonomists that are collaborating
Riparian Livinginrivershore,sand
along with the Socie(cid:1)te(cid:1) Entomologique Antilles-Guyane (SEAG)
andmuddyhabitat
representing hundreds of taxonomists from institutes, universities
Litter Insectsinhabitingthefirst
andmuseumsworld-wide.Distributionrecordswereaddedtothe layerofsoilprofile
lists of French Guiana (SEAG, Labex CEBA) and Peru (IIAP Wood Xylophageinsectsincluding
Iquitos). insectinhabitingunderbark
Endophagy Insectsperformingleaf
mining,stemboring,
arthropod functional classification
gallforming
Deadtree Decayingwood
Each arthropod family was described using 21 functional and Free-living Definedas‘tourist’insecta
ecological traits belonging to three trait categories (Table1, Dungandcarrion Insectsinhabitingdung
AppendixS3,SupportingInformation).Basedonthesefunctional andcarrionmatter
attributes, we constructed a matrix of binary functional traits
using the literature (Gauld & Bolton 1988; Delvare & Aberlenc aDefinitionfromMor(cid:1)an&Southwood(1982)
1989; Browne & Scholtz 1999; Lawrence etal. 1999) and con- bWe tried to add all details concerning functional attributes for
bothadultandlarvaewheninformationwasavailable.
firmedbyexpertsoftheSEAGnetwork.First,inordertoextend
the designation of arthropods into major ecological guilds, we
part of the world or those available for other related taxonomic
classified each group by its most frequent food source. Secondly,
group. Despite the coarse taxonomic resolution of our data set
we described the general type of insect mouthparts as a comple-
(i.e.mostlyfamilylevel),thisapproachfocussedonresource-cap-
mentarymeasureoffeedingmodeandmorphologicalfeaturethat
ture and resource-use traits that are expected to capture most of
emphasizes resource use. We recognize that insect mouthparts
the evolutionarily conserved functional attributes at the family
represent a complex structure in which variation may be con-
level(seeTimmsetal.2013for discussiononoptimaltaxonomic
tributed to by at least 34 fundamental mouthpart types (Laban-
resolution).
deira 1997). Nevertheless, we chose to distinguish three major
types of mouthparts (siphoning, piercing–sucking and mandibu-
lates) that represent the ecological attributes of insect feeding statistical analyses
strategyamongourstudiedarthropodtaxa.Thirdly,wedescribed
the different habitats and microhabitats inhabited by each taxa. Ataxonomicapproachwasfirstconstructedbasedonthesumof
We classified ‘free-living’ insects in this third category because the relative abundance of each collected arthropod taxa for each
thesetaxaarebelievedtobe‘touristinsects’asdefinedbyMor(cid:1)an plot(i.e.mostlyatthefamilylevel,inadditiontosevensubfami-
&Southwood(1982),implyinghighmobilityacrossawiderange lies and three super-families). Dissimilarity in community-level
of habitats. Some generalization of ecological characteristics was arthropod abundance among plots – that is community turnover
made because detailed trait information is not yet available for – was measured using Bray–Curtis indices. Correlations between
some invertebrate taxa and/or not in South America. In some taxonomic arthropod dissimilarity among habitat and countries
cases, when information was missing in the Amazon for a given were visualized with a NMDS ordination and tested for signifi-
family,weusedthedataavailableforthesamefamilyinanother cantdifferencesamonghabitatsand across countrywithanalysis
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
Drivers ofAmazonian arthropod assemblages 231
of variance (ANOVA on NMDS coordinates). We then explored between pairs of plots calculated from the UTM coordinates of
how arthropod taxa differ in abundance among the three differ- eachpermanentplot.Anenvironmentaldistancematrixofthe24
entforesthabitatsandbetweencountries.Theimpactofhabitats environmental variables (i.e. forest stand, climatic and edaphic
and countries was modelled using a generalized linear model variables, see Baraloto etal. 2011) was calculated for each plot
framework. Because our response variable, that is the number of pairfollowingaprincipalcomponentanalysisoftheenvironmen-
individuals recorded in a plot, was discrete with positive values, taldatasetoftheentire74plotnetwork.Wefirstcalculatedtwo
wemodelledthemwithaPoissondistribution.Thesignificanceof principal coordinates of neighbour matrices (PCNM), the first
both habitat and country effects was assessed through the Wald one on the community composition and the second one on the
statisticZ(Rsoftware;RDevelopmentCoreTeam,2013): geographical distance matrices. We then extracted the first five
eigenvectors of each PCNM and used these eigenvectors in two
logðEðIndchÞÞ¼h0þhcþhh partial constrained correspondence analyses (pCCA), the first in
whichcommunitycompositionwasconstrainedbyenvironmental
whereInd isthenumberofindividualsofagiventaxaincoun- eigenvectors while partitioning out the effect of geographical
ch
try c and habitat h and h the model parameters. To counteract eigenvectors, and the second in which community composition
theproblemofmultiplecomparisons,weusedtheHolm–Bonfer- was constrained by geographical eigenvectors while partitioning
roni method (Holm 1979) to correct the significance values. out the effect of environmental eigenvectors. We were able to
Secondly, in order to evaluate the degree of arthropod habitat partition the variance in community composition that is solely
associations across the studied forests, we calculated indicator attributable to environmental effects, to geographical effects and
taxa values (IndVal) for each arthropod taxon after Dufrene & to ‘shared’ variation among environment and geography
Legendre(1997). (Table2).
Thetrait-basedapproachintegratedthematrixof21functional
traits(Table1)tocreateapairwisefunctionaldissimilaritymatrix
for the studied plots. Functional distances between all taxa were Results
computedaccordingtotheirtraitvalueusingtheGower’smetric
(Gower1966).Then,weconstructedafunctionaltypologyofthe changes in arthropod taxonomic composition
overallarthropodcommunityusingWard’smethod(Everittetal.
2011). We then computed the KGS penalty function (Kelley, In total, 60 123 specimens of arthropods were collected
Gardner & Sutcliffe 1996) to decide where to prune the tree in and assigned to 147 taxonomic groups, representing 108
order to delimit arthropod functional groups. The minimum of super-families in seven arthropod orders (Appendix S1).
this function represents the suggested pruning size. The consis- Variance partitioning showed that geographical distances
tency of each arthropod taxon’s membership to a given func- and environmental dissimilarity among plots explained
tionalgroup(i.e.suggestedpruning)wascomputedandvalidated most of the variation in arthropod community taxonomic
usingasilhouetteplot(Rousseeuw1987).Wethentestedfordif-
composition (Table 2). Geographical distance (controlling
ferencesinfunctionalgroupabundancesamongthethreehabitats
for environment) explained slightly more (39% vs 34%)
using a GLM Poisson model in the same way as for the taxo-
of the variation in community composition than environ-
nomicapproach.
mental distance(controlling for geography).
Finally,wepartitionedthedegreetowhichspatial variationin
These results can be visualized in the ordinations pre-
community composition (taxonomic and functional group com-
position)was explainedby environmentaland geographical com- sented in Fig. 2, which show a clear separation in arthro-
ponents using a canonical partitioning procedure (Legendre, pod composition between SF forest and the two other
Borcard & Peres-Neto 2005). We used geographical distances foresthabitats(axis2;F = 41(cid:1)8;P = 0(cid:1)0003).Wealso
(1,6)
Table2. Partitioningtheeffectofenvironmentandgeographyonvariationinarthropodcommunitytaxonomicandfunctionalcomposi-
tion.Weusedpartialcanonicalcorrespondenceanalyses.Afirstcorrespondenceanalysis(CA)wasrunonthetaxonomicandfunctional
compositionmatricestoquantifyallvariationinthedata.Then,canonicalcorrespondenceanalyses(CCA)wereruntodecipherthepart
variancethatcanbeexplainedbyoneconstraint(environmentorgeography)whilecontrollingfortheother.Thefirst5axessummarize
morethan99%oftheobservedvariationinconstraints
Inertiaa Axis1b Axis2b Axis3b Axis4b Axis5b MSCc
Taxonomiccomposition
CA 0(cid:1)88
CCAEnvironment 0(cid:1)30 0(cid:1)11 0(cid:1)07 0(cid:1)06 0(cid:1)03 0(cid:1)02 34(cid:1)3%
CCAGeography 0(cid:1)35 0(cid:1)12 0(cid:1)10 0(cid:1)08 0003 0(cid:1)02 39(cid:1)3%
Functionalcomposition
CA 0(cid:1)27
CCAEnvironment 0(cid:1)12 0(cid:1)10 0(cid:1)01 0(cid:1)01 0(cid:1)00 0(cid:1)00 42(cid:1)6%
CCAGeography 0(cid:1)07 0(cid:1)03 0(cid:1)03 0(cid:1)01 0(cid:1)00 0(cid:1)00 26(cid:1)0%
asumofeigenvalues.
beigenvalues.
cMSC=(inertia of CCA/inertia of CA)*100; it provides an indication of the proportion of the variance accounted for by environment
orgeography.
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
232 G. P.A. Lamarre
Fig.2. Non-metric dimensional scaling
(NMDS)ordinationsillustrating similarity
in arthropod taxonomic composition
among plots of different habitats, regions
and countries. French Guiana plots are
coloured in blue and Peruvian plots in
red. Habitats include terra firme clay for-
est (circles), white-sand forest (triangles)
and seasonally flooded forest (squares).
Lightanddarkbluesymbolsrepresentthe
Laussat and Regina regions of French
Guiana, respectively. Light and dark red
symbolsrepresentthePorvenirandJenaro
Herrera regions of Peru, respectively (see
Fig.1).Thecolourversionofthisfigureis
availableonline.
found convergent patterns of dissimilarity among habitat tles were collected in TF forest (see Table 1). These
types between Peru and French Guiana. In particular, patterns are consistent with the results of the general-
overall community composition in SF forest was remark- ized linear model (Appendix S1) in which we found
ably similar in the two countries, mainly because of a
consistent dominance of aquatic insect communities in Table3. Arthropod taxa with significant associations with each
these habitats (Appendix S1 and Table 3). We observed a ofthestudiedforesthabitats.IndicatortaxavaluesafterDufrene
high similarity in taxonomic composition in terra firme & Legendre (1997) and the probability of obtaining as great an
indicatorvalueasobservedover1000iterations
clay forest and to a lower extent in white-sand forest
habitats within each country (Fig. 2). Taxonomic compo-
Preferred
sitionwasstrongly andsignificantlydifferentiated between forest Indicator
Peru and French Guiana (axis 1; F = 200(cid:1)4; Order Taxa habitat value P
(1, 6)
P < 0(cid:1)001). The partitioning analysis clearly showed that
Coleoptera Carabidae Flooded 0(cid:1)738 0(cid:1)007
the effect of geographical variation in community taxo-
Coleoptera Cicindelidae Flooded 0(cid:1)912 0(cid:1)013
nomic composition was stronger than the effect of envi- Coleoptera Heteroceridae Flooded 0(cid:1)891 0(cid:1)013
ronment (Table 2), a pattern also confirmed by the visual Coleoptera Hydrophilidae Flooded 0(cid:1)805 0(cid:1)016
inspection ofthe NMDS ordination. Coleoptera Hydrochidae Flooded 0(cid:1)864 0(cid:1)019
Coleoptera Dytiscidae Flooded 0(cid:1)967 0(cid:1)066
Hemiptera Gerridae Flooded 0(cid:1)933 0(cid:1)006
arthropod habitat associations Isoptera Termitidae Flooded 0(cid:1)852 0(cid:1)008
Lepidoptera Hesperiidae Flooded 0(cid:1)593 0(cid:1)047
Overall, arthropod taxa exhibited striking contrasts in Coleoptera Scarabaeidae terrafirme 0(cid:1)681 0(cid:1)007
habitat associations acrossthe studied forestcommunities, Coleoptera Ptilodactylidae terrafirme 0(cid:1)588 0(cid:1)019
with more than 17% (26 out of 147) of arthropod taxo- Coleoptera Nitidulidae terrafirme 0(cid:1)63 0(cid:1)038
Coleoptera Phengodidae terrafirme 0(cid:1)7 0(cid:1)05
nomic groups having significant preferences for a single
Coleoptera Curculionidae terrafirme 0(cid:1)483 0(cid:1)067
habitat type (Table 3). Arthropod families that showed Coleoptera Erotylidae terrafirme 0(cid:1)579 0(cid:1)089
clear habitat associations were mostly detected in high- Coleoptera Mordellidae terrafirme 0(cid:1)656 0(cid:1)006
resource habitats (e.g. TF and SF). Nevertheless, white- Hemiptera Cicadellidae terrafirme 0(cid:1)46 0(cid:1)071
sand forest communities were preferred habitats for two Hemiptera Flatidae terrafirme 0(cid:1)7 0(cid:1)073
Lepidoptera Nymphalidae terrafirme 0(cid:1)496 0(cid:1)01
moth families (Dalceridae and Nolidae), in addition to
Lepidoptera Saturniidae terrafirme 0(cid:1)611 0(cid:1)01
two Auchenorrhyncha families (Delphacidae and Fulgo- Orthoptera Acrididae terrafirme 0(cid:1)567 0(cid:1)02
ridae). Ground beetles (i.e. Carabidae) were the beetle Araneae Salticidae terrafirme 0(cid:1)634 0(cid:1)045
family exhibiting the strongest association with a partic- Hemiptera Delphacidae Whitesand 0(cid:1)824 0(cid:1)013
ular forest habitat, with nearly two-thirds of all individ- Hemiptera Fulgoridae Whitesand 0(cid:1)81 0(cid:1)019
Lepidoptera Dalceridae Whitesand 1 0(cid:1)007
uals collected in SF forests. We also found that more
Lepidoptera Nolidae Whitesand 0(cid:1)675 0(cid:1)059
than 60% of the individuals in Mordellidae flower bee-
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
Drivers ofAmazonian arthropod assemblages 233
Fig.3. Cluster functional dendrogram of
the overall arthropod community. Results
for the functional-based approach inte-
gratedthematrixof21functionaltraitsto
create a pairwise functional dissimilarity
matrix. Functional distances between all
taxa were computed according to their
trait value using the Gower’s metric.
Arthropodordersarecolouredtovisualize
phylogenetic conservatism in functional
attributes; red=Hemiptera, green
=Coleoptera, blue=Lepidoptera, yel-
low=Araneae, orange=Orthoptera, bla
ck=Hymenoptera,purple=Scutigeromor-
phaandburgundy= Isoptera.Thecolour
versionofthisfigureisavailableonline.
changes in arthropod functional composition
that 82 out of 147 taxonomic groups (i.e. 55(cid:1)8 %) dif-
fered significantly in their abundance among the three The functional typology of the 147 taxa identified seven
studied forest habitats. distinct functional groups (Fig. 3), or clusters of taxo-
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
234 G. P.A. Lamarre
nomic groups sharing similar ecological and functional approach also discriminated different feeding sources (e.g.
attributes and that are therefore likely to be similar in groups 1 and 4 feed on leaf tissue) from morphological
their response to their environment and/or their effects on traits related to foraging (hemipterans from Group 1 but
ecosystem functioning (Diaz & Cabido 2001). Figure 3 also Group 2harbour the same piercing–suckingstylet).
illustrates the clear separation between arthropod groups Each of the seven functional groups had contrasting
related to leaf resources (groups 1 and 4), those repre- distributions across the three forest habitat types (Fig. 4).
sented by predators and parasitoids (groups 2 and 3) and Most groups exhibited higher abundance in high-resource
those feeding on wood and fungi (groups 5 and 6). Our environments (i.e. SF and/or TF). Herbivores (leaf feeders
(a) (e)
(b) (f)
(c) (g)
(d)
Fig.4. Relative abundances of arthropod functional groups differ among contrasted types of habitats (TF= terra firme clay forest,
SF=seasonally flooded forest, WS= white-sand forest). (a) Sap-sucker; (b) leaf-feeder; (c) wood–fungi feeder; (d) mixed beetle; (e)
aquaticbeetle;(f)hemipteranpredator(+Araneae)and(g)insectpredatorandparasitoid.Differentlettersindicatesignificantdifferences
inmeanabundanceamonghabitatsatP<0(cid:1)05.
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
Drivers ofAmazonian arthropod assemblages 235
and sap suckers), mixed beetles and insect predators availability (Fine et al. 2013). Because of higher resources
showed a higher abundance of individuals in TF than in andpresumablygreater nichepartitioning(food, seasonal-
both SF and WS forests. Wood–fungi feeders and aquatic ityandspace),wealsofoundsignificantdifferencesincas-
insects weremost abundantin SF forests. cading trophic level structure with higher abundances in
Variancepartitioningshowedthatgeographicaldistance high-resource habitats than low-resource habitats (e.g.
and environmental dissimilarity among plots also white-sand forest). For example, rove beetles (Staphylin-
explained most of the variation in arthropod community idae) had nearly five times more individuals in high-
functional composition (Table 2). However, functional resource habitats (both SF and TF) than in white-sand
composition was much more clearly linked to environ- forests(Appendix S1).
mentaleffectsthantogeographicaldistance.Geographical Previousstudieshaveshownthatplantspeciescomposi-
distance (controlling for environment) explained only tion shows strong turnover among local communities
26% of the variation in community functional composi- (Tuomisto et al. 2003) and across different habitats types
tion, whereas environmental distance (controlling for in the Amazon (Fine et al. 2010). Indeed, each habitat
geography) explained 43% of variation in arthropod com- considered in our study harbours a unique floristic com-
munity functionalcomposition. position (Baraloto et al. 2007; Fine et al. 2010) that
includes many habitat specialists (Lamarre et al. 2012a).
Finally, we believe that host plant functional traits may
Discussion
be influencing herbivore community structure. Leaf traits
promoting higher resource conservation are expected in
habitat filtering shapes arthropod
low-resource habitats, whereas terra firme tree species are
taxonomic composition
allocating, in turn, more resources into growth with
In our study, arthropod community composition varied higher specific leaf area and higher nutrient concentra-
markedly across contrasting tropical forest habitats. This tions (Baraloto et al. 2010; Fortunel et al. 2014; Lamarre
strong pattern of turnover among habitat types is concor- et al. 2014). We would therefore expect strong turnover in
dant with the few previous studies of arthropod commu- arthropod communities dependent on plant community
nity composition in tropical forests (Smith, Hallwachs & composition, especially host-specialist herbivores (Nov
Janzen 2014). For instance, Novotny et al. (2005) found a otny et al. 2006). In general, we found a high turnover of
highturnoverin caterpillarsassociatedwiththehostplant arthropod communities across forest communities with
genus Ficus along altitudinal gradients. Rodriguez-Cas- different floristic composition (Fine et al. 2010). For
tan~eda et al. (2010) also found high beta diversity in both instance, leaf beetle (Chrysomelidae) and weevil (Cur-
plant and insect communities across a tropical montane culionidae), which are the most diverse insect families,
gradient in four distinct elevation zones (see also Smith, support, respectively, 2(cid:1)7 and 2(cid:1)1 more individuals in TF
Hallwachs & Janzen 2014 for ants). Our study therefore forests than in WS forests (Appendix S1). Furthermore,
confirms that marked shifts in environmental conditions moth and butterfly communities also showed striking dif-
can strongly influence spatial patterns in arthropod com- ferences in abundance between habitat types with a clear
munities,hereinlowlandNeotropicalforests.Wesampled dominance in high-resource habitats (for Nymphalidae,
a limited number of sites as comprehensively as possible. Notodontidae, Saturniidae,Sphingidaeand Noctuidae).
Nevertheless, our statistical approach allowed us to com-
pare the relative contributions of geography and environ-
arthropod habitat association
ment in shaping arthropod community composition,
which were relatively equal and explained most of varia- Most arthropod families in both regions showed striking
tion (Table 2). differences in their relative abundances among the three
The low overlap in overall arthropod composition studied habitats. In particular, we found strong differ-
between highly contrasted forest habitats may be driven ences in arthropod composition between seasonally
by differences in habitat structure, changes in host plant flooded forests and the two other forest habitats (Fig. 2).
species richness and composition and host plant func- In particular, the ground beetle family (Carabidae) exhib-
tional traits. The three forest habitats we studied differ ited 4(cid:1)3 more individuals in SF than in TF forests
markedly in forest structure and soil texture and fertility (Appendix S1). Seasonally flooded forests exhibited a con-
(Baraloto et al. 2011), with potential consequences for vergent effect on overall community composition that was
arthropod community composition. For instance, forests remarkably similar in the two countries. A recent study
withlesslimiting mineralnutrientsandamorerapidturn- found a high rate of treefall disturbances in French Guia-
over of plant tissue (Lamarre et al. 2012a, 2014) support nan flooded forests, resulting in a more rapid forest turn-
higher abundances of herbivorous insects and associated over than in terra firme forests (Ferry et al. 2010). We
predators.A recentstudyshowedthat asingle tree species speculate that the more rapid forest dynamics in flooded
may host different assemblages of insect herbivores in forests may increase resources available for specific feed-
white-sand and terra firme sites and that this pattern ing guilds such as predators. Disturbance caused by
might be directly linked to variations in soil nutrient water-table fluctuation in seasonally flooded forests is
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239
236 G. P.A. Lamarre
likely to influence arthropod community composition Lamarre et al. 2014). For example, insects associated with
(Ellis et al. 2001; Baccaro et al. 2013). Additional expla- wood and fungi resource uses are found to be more com-
nations to the trend observed may lie in physiological mon in seasonally flooded forest, in which more forest
stressors among host plant assemblages subjected to regu- dynamics,microclimate(e.g.moisture)andnaturalpertur-
lar flooding regimes that may drive herbivore and associ- bation occur and are favourable for specific insect guilds.
atedhighertrophic levelin lowland tropical forests. Our results are thus consistent with recent research con-
ducted in some of the same forest sites that showed a sig-
nificantly lower wood density in seasonally flooded plant
towards a functional classification of
specialists (Fortunel et al. 2014). The pattern found on
tropical arthropods
functional Group 5 (see Fig. 3) would not have been
Several authors first described the guild concept for detected unless using a functional approach (Group 5
arthropods based on feeding strategy (Mor(cid:1)an & South- includes 21taxonomically distinctbeetle families).
wood 1982). As a novel application to the feeding guild The strength of environmental filtering on functional
approach, we propose a functional composition approach community composition may be even stronger because we
based on feeding, habitat and mouthpart traits that are included white-sandforeststhatare characterizedbyvege-
inherent to each arthropod family. Although we recognize tation with pronounced sclerophylly, low diversity and
that the functional traits assigned in our study (e.g. at the high endemism in plant species (Medina, Garcia & Cue-
family level) may be a simplistic representation of insect vas 1990; Fine et al. 2010). We predicted that a unique
ecological niches, we believe this is a novel approach that assemblage of insect herbivores would be able to feed on
may help investigating arthropod community patterns. thethickerandtougherleaves,forexamplethewhite-sand
Based on trait-based similarity, each of the 147 taxa was habitat specialists such as Delphacidae and Fulgoridae
classified and grouped into seven functional groups. The (Table 3). Our functional approach confirmed this gener-
visual inspection of the silhouette plot, a graphical aid for ally as we found that functional composition in leaf-
validation of cluster analysis, showed high consistency of chewer and sap-sucker taxa clearly differed in relative
affiliation for each taxon within each functional group abundance among the three contrasted habitats with a
(Appendix S2). Such a functional tree can be considered higher abundance in terra firme clay forest (Fig. 4 and
asafirststeptowardsdescribingmoreaccuratelytheroles Table 2). A high allocation to secondary compounds
of arthropods in ecosystem functioning. For instance, the restricts the relative abundance of leaf and sap feeders,
functionalclustering obtainedfromourdatasethighlights and these properties are more characteristic of white-sand
that Coleoptera (in green), one of the most diverse groups forests (Coley, Bryant & Chapin 1985; Fine et al. 2006).
of arthropods, comprise taxa with highly contrasting Further investigations are needed on the functions of dif-
functional roles in lowland tropical forests. We believe ferent plant tissues (resource conservation and/or defence)
that a refined approach to functional characterizations that would allow us to test whether plant functional
(Flynn et al. 2009; Moretti et al. 2009), in concert with trade-offs are directly influencing arthropod functional
phylogenetic data (Smith, Hallwachs & Janzen 2014; community structure in tropical forests. We envision a
Lamarre et al. in press), will allow enhancing and gen- bottom-up model by which herbivore species and associ-
eralizing this functional approach for future studies of ated natural enemies are filtered among habitat types
arthropods. based on shifts in host plant community functional com-
positioncorrelated withenvironmental changes.
contrasting functional composition across
lowland tropical forests partitioning effects on arthropod community
composition
Overall, our functional approach using simple functional
and ecological traits at the family level reveals strong pat- The NMDS ordination clearly suggests that arthropod
terns of dissimilarity in functional structure among taxonomic assemblages are partitioned in two regions,
arthropod communities collected in terra firme, flooded Loreto, Peru, and French Guiana, representing distinct
forest and white-sand forest plots (Fig. 4). Environmental biogeographical regions that differ in geological and
filtering should translate taxonomic turnover into func- edaphic histories in addition to highly contrasted rainfall
tional turnover across these steep habitat gradients (e.g. seasonality (Hoornet al. 2010).The considerable turnover
low functional redundancy, see Flynn et al. 2009; but see found between countries is also consistent with the results
Vill(cid:1)eger et al. 2012). In our study, we observed that taxo- of the generalized linear model in which we found that
nomic turnover was accompanied by marked changes in nearly 47%of the arthropod taxonomic groups (69 out of
functional composition. Most of the functional groups 147) differed significantly in their abundance between
showed greatest abundance in high-resource habitats com- French Guiana and Peru (Appendix S1). We believe this
pared to low-resource habitats (Fig. 4). This result is con- pattern is particularly evident because of the contrast in
sistent with previous studies that have reported greater soil profiles at both ends of the Amazon that are expected
herbivory rates in high-resource habitats (Fine et al. 2006; to influence both host plant and associated arthropod
©2015TheAuthors.JournalofAnimalEcology©2015BritishEcologicalSociety,JournalofAnimalEcology,85,227–239