Seed-dispersal networks on the Canaries and the Galápagos archipelagos

27 Pages·2015·3.91 MB·English

GlobalEcologyandBiogeography,(GlobalEcol.Biogeogr.)(2015)
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Seed-dispersal networks on the Canaries
SPECIAL
ISSUE and the Galápagos archipelagos:
interaction modules as
biogeographical entities
M.Nogales1*,R.Heleno2,B.Rumeu1,3,A.González-Castro1,4,A.Traveset5,
P.Vargas3andJ.M.Olesen6
1IslandEcologyandEvolutionResearchGroup ABSTRACT
(CSIC-IPNA),LaLaguna,Spain,2Centrefor
Aim Mutualistic network parameters, such as modularity and nestedness, show
FunctionalEcology,DepartmentofLife
non-random linkage patterns. Both increase network stability in different ways.
Sciences,UniversityofCoimbra,Coimbra,
Modularity hampers extinction cascades,whereas nestedness resists network dis-
Portugal,3RealJardínBotánico(CSIC-RJB),
assembly.Weexploretheseparametersinseed-dispersalnetworksintwoarchipela-
Madrid,Spain,4DepartamentodeCienciasde
gosandthesignificanceoflifehistory,habitat,geographyandphylogenyasdrivers
laTierra,UniversidadEstatalAmazónica,
Puyo,Ecuador,5InstitutMediterranid’Estudis oflinkagepatternsandtheapplicabilityofmodulesasbiogeographicalentities.
Avançats(CSIC-UIB),PalmadeMallorca,
Location Canaries(AtlanticOcean)andGalápagos(PacificOcean).
Spain,6DepartmentofBioscience,Aarhus
University,Aarhus,Denmark Methods We compiled data on plant–seed disperser interactions from own
observationsandtheliterature,estimatednetworkparametersdescribinginterac-
tion patterns (connectance,nestedness and modularity) and constructed a back-
bonephylogenyfortheanalyses.
Results The Canarian network was highly nested but weakly modular,whereas
the Galápagos network showed the opposite characteristics. Most key network
species are native and have a favourable conservation status. Modularity in the
Canariesiscorrelatedwithhabitats(indirectlyaffectedbyaltitudeandorientation),
whereasintheGalápagositmainlyreflectsthefunctionalrolesofspecies.
Mainconclusions Thedivergentlinkpatternsforthearchipelagosimplythatthe
highlynestedCanariannetworkisstableagainstdisassembly,whereasthemodular
Galápagos network may show strong resistance against extinction cascades.This
differencemaybedrivenbythespecificevolutionarydynamicsonthearchipelagos.
*Correspondence:M.Nogales,IslandEcology
andEvolutionResearchGroup(IPNA-CSIC),
Keywords
C/AstrofísicoFco.Sánchezno.3,38206La
Animal–plant interaction, fleshy fruit, food web, frugivory, insular network,
Laguna,Tenerife,CanaryIslands,Spain.
E-mail:[email protected] modularity.
andmodularity(Olesenetal.,2007).Theirapplicabilityinthe
INTRODUCTION
context of biogeography and system stability is the focus of
Biodiversityismuchmorethanmerespecieslists,particularly this paper.
asitalsoincludesthemyriadofwaysinwhichspeciesinteract Ifanetworkhasahighlyheterogeneousstructureofspecies
(Pococketal.,2012)andformspatio-temporallydynamicnet- andtheirinteractions,itismostoftenbothnestedandmodular.
works (e.g. Rasmussen etal., 2013). During the last two Inanestedlinkpattern,acoreofgeneralistspeciesinteractwith
decades, this upscaling in focus from species to networks each other and with specialists (Bascompte etal., 2003). In a
has contributed significantly to our comprehension of the modularlinkpattern,eachmoduleisagroupof highlyinter-
complexity of biodiversity (Bascompte & Jordano, 2013). connected species, often sparsely linked together into a larger
There are plenty of important milestones along this route, network(Olesenetal.,2007).Inecology,modulesareextremely
especially the concepts of nestedness (Bascompte etal., 2003) useful for our understanding of mutualistic systems such as
©2015JohnWiley&SonsLtd DOI:10.1111/geb.12315
http://wileyonlinelibrary.com/journal/geb 1
M.Nogalesetal.
Table1 GeneralcharacteristicsoftheCanarianandGalápagosarchipelagosandpotentialconsequencesforbiodiversity.
Characteristics Canaries Galápagos Biodiversityconsequences
Abioticcharacteristics
Landarea(km2) c.7900 c.7500 Largeareaforimmigration
Numberofislands(>10km2) 9 13 Largeareaforallopatricspeciation
Highestpeak(masl) 3718 1707 Largetopographicareaforimmigration
andspeciation
Maximumageofcurrentislands(Ma) 21 4–6 Widespanofgeologicalage
Currentminimumdistancebetweenarchipelago c.98 c.1000 Verydifferentlevelofisolation
andmainland(km)
Volcanicactivityinthelastcenturies High High Recurrentextinctionevents
Climate Subtropical Equatorial Hotspotsofdiversity
Mediterranean
Bioticcharacteristics
Mainbiomes 5 3 Highhabitatdiversity
Biodiversity(no.ofspecies) High Medium Highinteractionpotentiality
No.ofseed-plantendemicspecies(%)withrespecttonatives 537(40.3%) 168(38%) Strongsignalforuniqueinteractions
No.offleshyfruitedspecies(%)withrespecttonatives 76(5.7%) 34(7.6%) Importantplantcomponentfor
ecologicalnetworks
No.ofvertebratedisperserspecies(%)withrespect 30(35.7%) 28(65%) Importantanimalcomponentfor
tonativelandvertebrates ecologicalnetworks
plant–pollinator(Travesetetal.,2013)andplant–seed-disperser Hereweintegratenetworktheoryandbiogeographyinastudy
networks(Donattietal.,2011),butalsoinantagonisticsystems of seed-dispersal networks on two oceanic archipelagos, the
suchasfoodwebs(Dunneetal.,2002)andhost–parasitenet- Canaries (Atlantic Ocean) and the Galápagos (Pacific Ocean).
works(Anderson&Sukhdeo,2011).Withinamodule,species Thesearchipelagosdifferingeographicalpositionandisolation,
operateindynamicecological–evolutionarysynchronybecause age,elevationandmainlandspeciessource,buthavequiteasimi-
of theirhighinterconnectivity.Thusif modularityisstrong,a larlandsurfaceareaandhighinteractionpotentiality(Table1).
morerelevantscaleofanalysismightbethemoduleandnotthe Wefocuseduponseed-dispersalmodulesinordertoshowtheir
individualspeciesorthewholenetwork.Amodulemaybeseen valueasfunctionalentitiesinbiogeographicalanalyses.
asacoevolvingniche(Gómezetal.,2015),aconceptwithwide The aims of our study were to: (1) estimate levels of
implications for the study of coevolution, ecological conver- nestedness and modularity, identify modules and quantify
gence,localco-occurrence,systemstability,invasion/extinction, intermoduledistances;(2)comparespeciesandlinkcomposi-
migration/dispersal, geography and phenological uncoupling/ tionofmodulesfromthetwoarchipelagos;and(3)identifylocal
climate change (Thébault & Fontaine, 2010; Stouffer & andregionaldriversofmodularity.Finally,wediscusstheresults
Bascompte, 2011; Aizen etal., 2012; Høye etal., 2013; for a inrelationtosystemstabilityandtheapplicabilityofthemodule
reviewofmodularity,seeBascompte&Olesen,inpress).Thus, conceptasabiogeographicalentityinstudiesoftheecologyand
insightintothelinkstructureallowsadeeperunderstandingof evolutionofislandinteractions.
biodiversity,forexamplewithrespecttoregional/geographical
patterns (e.g. Carstensen & Olesen, 2009; Dalsgaard etal., METHODS
2013), the impact of alien species (Valdovinos etal., 2009;
Rodriguez-Cabal etal., 2013; Traveset etal., 2013) and system Studysites
stability (Stouffer & Bascompte, 2011; Bascompte & Jordano,
ThearchipelagosoftheCanariesandtheGalápagos(Appendi-
2013;Rodriguez-Cabaletal.,2013).
cesS1 & S2 in Supporting Information) differ in several
Seeddispersalisanessentialphaseintheprocessofregenera-
respects, but also show important similarities (Table1), for
tionofplantcommunitiesandastrongdriveroflocalbiodiver-
exampleintotallandsurface(7900vs.7500km2,respectively)
sity (Bascompte & Jordano, 2007).At the network level,most
and number of islands (9 vs. 13 islands >10km2) and
studies of seed dispersal have been carried out in mainland
palaeoislands (6 vs. 7); however, the Canaries are older and
communities(Jordanoetal.,2003),andonlyafewonoceanic
richer in plant species and main biomes (see Heleno etal.,
islands (Heleno etal., 2011a, 2013; González-Castro etal.,
2011b;Padillaetal.,2012)(AppendixS3).
2012). This retards rigorous island–mainland comparisons
(Schleuningetal.,2014),althoughasageneralpatternweknow
Interactionmatricesandnetworkparameters
birds and mammals are major mainland biotic dispersers
(Herrera,1995)whereasbirdsandreptilesoftenplaythisroleon We compiled data about interactions from own field observa-
oceanicislands(Nogalesetal.,2005). tionoffrugivory(overatimespanof10yearsintheCanaries
2 GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd
Modularityofseed–dispersalnetworksonoceanicislands
and6yearsinGalápagos)andalsoincludedallrecordsfroman fornetworkcohesionbygluingmodulestogether;(3)module
exhaustiveliteraturereview(Helenoetal.,2011bandreferences hubs(z≥2.5,c<0.62)havemanylinkstootherspeciesintheir
therein).Wealsoincludedallinteractionsinvolvingnon-native ownmodule,andareimportantformodulecohesion,and(4)
species,withtheexceptionofcaptive/cultivatedspecies.Aseed- network hubs or super-generalists (z≥2.5, c≥0.62) are both
dispersal interaction was recorded if fruit was swallowed or connectorsandmodulehubs(Olesenetal.,2007).
removedfromaplantbyananimal,if undamagedseedswere Networks were visualized using the software Pajek v.2.05
foundindroppingsorpelletsorifgutsampleswithintactseeds (Batagelj & Mrvar, 1998). The basic principle behind Pajek
were obtained. In the Canaries, predatory birds such as the visualization is that distance between species expresses their
kestrelandthemeridionalshrikeindirectlydispersemorethan numberoflinkstootherspecies.
60 species by their predation of frugivorous lizards (Padilla
etal.,2012).Suchrecordsofseedsinregurgitationpelletswere
Testingforphylogeneticsignalin
alsoincludedinthenetwork.Onbotharchipelagos,interactions
networkcomposition
were gathered all year round with a greater effort during the
mainfruitingseasons. Thephylogeneticsignalofatraitinasampleofspeciesexpresses
Interactionswerecompiledintotwo-modebinaryadjacency theextenttowhichthephylogeneticstructureofthecommunity
matricesofAanimalspecies(matrixcolumns)interactingwith accountsformorphologicalcharactersofthespecies.Inorderto
Pfleshyfruitedplantspecies(matrixrows)(TablesS1&S2).If estimatetheimportanceofthephylogenyinexplainingthevari-
aninteraction Ibetweenaplantandananimalspeciesisrec- ationof traitvaluesof ourfourcommunities(plantsanddis-
orded,itspresenceinthematrixcellisscoredas‘1’,ifnotas‘0’. persersintheCanariesandintheGalápagos),weconstructeda
We estimated three network parameters: connectance, backbone phylogeny for each community. Plant phylogenies
nestedness and modularity. Connectance C=100I/AP is the were based on the supertree from APG III (Angiosperm
percentageofrealizedinteractionsoutofthetotalpossibleinter- Phylogeny Group, III, 2009), bird phylogenies from http://
actionsinthenetwork.Levelofnestednesswasmeasuredwith birdtree.org/ and Gallotia lizard phylogenies from Cox etal.
the NODF algorithm (Almeida-Neto etal., 2008), and the (2010).Asinformationonbranchlengthwasnotavailableforall
NODFvaluebelongstotheinterval[0(not-nested);1(perfectly taxa and phylogenies, we used a taxonomic proxy, equalizing
nested)].EmpiricalNODFvalueswerecomparedwithdistribu- branchlengthsbetweenspecies,generaandfamilies.Inorderto
tionsof NODFvaluesfrom1000randomnetworksof similar runtheRscripts,afewpolytomieswereresolvedtaxonomically
size(Almeida-Netoetal.,2008).Totestformodularityweused intodichotomiesusingbranchlengths<<1.
the software netcarto (Guimerà & Amaral, 2005), which We used two measures of phylogenetic signal, K and λ.
assigns all plants and seed dispersers to modules.The level of Blomberg’sKcomparestheobservedtraitsignalwithasignal
modularityMofanetworkexpresseshowstronglythenetwork underaBrownianmotion(BM)evolutionarymodel(Blomberg
ispartitionedintomodules.AsMapproaches0or1,thelevelof etal.,2003).IfK≈1,thetraitisphylogeneticallyclusteredinthe
modularitybecomesweakerorstronger,respectively.Empirical sample of species. K≈0 indicates a convergent or random
M-values were compared with distributions of M-values from pattern, whereas K>1 indicates a strong phylogenetic signal.
100randomnetworksofsimilarsize(Olesenetal.,2007).The ThesignificanceofKistestedbycomparingtheobservedsignal
nullmodelassumesthattherankingofthespecieslinkagelevels withthemeanofthesignalfromrandomizationsbasedonanull
L (i.e.the number of links of each species) is like that of the model,which shuffles species randomly across the phylogeny.
empiricalnetwork.Wealsorecordedthesizeandcompositionof KwascalculatedusingthepackagepicanteinR(Kembeletal.,
each module and the number of links between and within 2010).
modules. We calculated the distance between each pair of Pagel’s λ measures how much trait correlations among
modules (intermodule distance), defined as the number of speciestellusabouttheirsharedevolutionaryhistory.Thevalue
sharedlinksbetweenapairofmodulesdividedbythesumofall of λrangesbetween0and1;if λ≈0,thetraitstructureisnot
theirlinks.If amodule,onaverage,hasashortdistancetoall influenced by phylogeny, whereas λ≈1 implies that the trait
othermodules,ithasahighmodulecentrality. followsaBMmodel.Thelowerandupperboundsof Kandλ
Inaddition,netcartoalsoassignstopologicalnetworkroles (TableS3)indicatewhichofthetwoscenariosisthemostlikely.
toallspeciesbasedontheirpatternof intra-andintermodule This analysis was performed using the packages picante and
links (Guimerà & Amaral, 2005).The assignment of a role to geigerinR(Harmonetal.,2008).
a species is determined by relative within-module degree or Wetestedforphylogeneticsignalineachofthefourcommu-
hubability (z), quantifying how well connected a species is to nities with respect to the distribution of a set of five network
otherspeciesinitsmodule,andamong-moduleconnectivity(c), traits(moduleaffinity,modulecentrality,linkagelevelL,con-
whichquantifieshowwelldistributedthelinksofaspeciesare nectivity c and relative within-module degree or hubability z)
amongmodules.Wesortedallspeciesintofourcategories:(1) andfivespeciestraits[bodyweight,fruitsize,preferredhabitat,
peripherals (z<2.5, c<0.62) have few links inside their own origin (i.e. native or alien) and geographic distribution (i.e.
module and rarely any to other modules; (2) connectors number of islands on which the species was present); see
(z<2.5,c≥0.62)haveafewlinksbothtospeciesintheirown Table S3]. Species of the same module show module affinity,
moduleandtospeciesinothermodules,i.e.theyareimportant whereas species of different modules do not. A phylogenetic
GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd 3
M.Nogalesetal.
Table2 Descriptiveparametersofseed-dispersalnetworksinthe Table3 Intermoduledistance.Distancebetweenmodulesiandj
CanariesandGalápagos. calculatedastheirsharednumberoflinks×100/(theirtotal
numberoflinks).Themodule“Geospizaconirostris-Opuntia
Canary Galápagos helleri”isanunconnectedsatellitemoduletothemainnetwork
Islands Islands andthereforeisnotpossibletocalculate“intermoduledistance”
withtherestofmodules.
Numberofseed-disperserspecies,A 30 28
Numberoffleshyfruitedplantspecies,P 65 34 Canarianmodules 1 2 3 4 5 6
Animalstoplantsratio(A/P) 0.46 0.82
Networksize(S=AP) 1950 952 1 Laurelforestandlargebirds 6.3 5.2 5.5 1.1 7.0
Numberofrecordedinteractions,I 325 153 2 Medium–largelizards 8.8 9.7 1.7 12
Modularity,M 0.31** 0.39** 3 Coastalshrubland 9.5 1.0 6.5
Numberofmodules,N 6 6 4 Secondaryseeddispersal 1.1 8.9
M
Connectance,c(100I/AP) 16.7 16.1 5 Highmountain 1.7
NestednessNODF 27.8** 12.6** 6 Thermophilousforest
Averagedistance 5.7
Modularity (based on 100 randomizations) and nestedness (1000
randomizations); significance indicated by **P<0.01 (Almeida-Neto Galápagosmodules 1 2 3 4 5 6
etal.,2008).
1 Geospizaconirostris–Opuntia – – – – –
helleri
signalwithrespecttomoduleaffinitytellsusthattaxonomically 2 Small–mediumdispersers/ 21 14 13 23
relatedspeciestendtobeinthesamemodule. SanCristóbal
As a measure of the phylogenetic signal for plant origin, 3 Westernislands 3.0 12 15
we used Fritz and Purvis’ D (Fritz & Purvis, 2010), which 4 Tortoise–largemammals 5.0 7.8
was calculated using the R package caper (Orme, 2013): 5 Largefinches/endemicrodent 8.6
D=(d –mean d)/(mean d –mean d), where d is the 6 Smallfinches/passerines
obs b r b obs
Averagedistance 12.24
numberof characterstatechangesneededtogettheobserved
characterstatedistributioninourphylogeny,d istheexpected
b
distributionof dunderaBMmodel(1000runs)andd isthe
r
expecteddistributionofdifcharacterstatesarerandomlydis- ‘laurelforestandlargebirds’modulewasthemostisolated.A
tributedamongspecies.Wescaledd byd andd inordermake high proportion (49%) of all links were between modules
obs r b
comparisons possible across communities and archipelagos. (Table4),i.e.intermodule distance was low.The network was
D=1ifthedistributionofatraitinacommunityisindepend- formed by two network hubs or super-generalists (the lizard
ent of the phylogeny of the species; D>1 if the trait is Gallotiagalloti andthekestrelFalcotinnunculus),twomodule
phylogenetically overdispersed; D=0 if the trait is distributed hubs(thepigeonsColumbabolliiandColumbajunoniae)and30
according to a BM model; and D<0, if the trait is more connectors (six seed dispersers and 24 fleshy fruited plants)
phylogenetically clustered than expected according to a BM (Figs1a & 2, AppendixS5). Besides, four of the six modules
model(Nunn,2011). were habitat-specific, namely high mountain, laurel forest,
We also tested for any correlations between traits using thermophilousforestandcoastalshrubland.Thus,anextensive
phylogeneticallyindependentcontrasts(PIC),bymeansofthe elevational habitat zonation enforced modularity (Appen-
apepackageinR(Paradisetal.,2004). dixS3).Theothertwomodulesweredominatedbylizardsand
secondaryseeddispersers(shrikesandkestrels;AppendixS5).
TheGalápagosnetworkalsoconsistedofsixmodules(Fig.1b;
RESULTS
seeTableS5forinformationaboutmodulesandAppendixS6for
TheCanarianandGalápagosnetworkshadsimilarconnectance informationaboutspeciesincludedinFig.1b).Onlythemodules
(Table2).However,speciesrichnessandnestednesswerehigher ‘small–medium dispersers/San Cristóbal Island’ and ‘western
intheCanaries,whereasmodularityandintermoduledistance islands’and‘small-mediumdispersers/SanCristóbal’and‘small
were higher in the Galápagos (Tables2 & 3; see also Appen- finches/passerines’ were strongly connected to each other. By
dixS4). In other words, the different modules operated more contrast, the modules ‘western islands’ and ‘tortoise/large
independently in the Galápagos.We also confirm the value of mammals’,andthe‘tortoise/largemammals’and‘largefinches/
theseed-dispersalmodulesasstudyentitiesinbiogeographical endemicrodentandlarge-seededplants’moduleswerepoorly
analyses. connected. The cactus Opuntia helleri and the finch Geospiza
The Canarian network consisted of six interconnected conirostrismadeanindependentsmallsatellitemodule,uncon-
modules (Fig.1a;see TableS4 for information about modules nectedtothemainnetwork.Only37%ofalllinkswerebetween
and AppendixS5 for information about species included in modules(Table4).ThegianttortoiseChelonoidisnigrawasthe
Fig.1a). The‘medium–large-sized lizards’and‘thermophilous onlynetworkhub,theplantMiconiarobinsonianawastheonly
forestandpasserines’moduleswerecloselyconnected,whilethe modulehub,and10specieswereconnectors(fourdispersersand
4 GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd
Modularityofseed–dispersalnetworksonoceanicislands
(A) * * *
*
* MODULES
Medium-large lizards
* * High mountain
*
*
Thermophilous forest
& passerines
*
* Coastal xerophytic shrubland
* & bird/mammal
* Laurel forest & large birds
*
Secondary seed dispersal
*
*
(B) *
* MODULES
Figure1 Modularstructureofthe Tortoise/large mammals
seed-dispersalnetworkintheCanary * *
Islands(A)andtheGalápagos(B).The * * Geospiza conirostris-
outerringofnodesrepresentfleshy * * Opuntia helleri (satellite)
*
fruitedplantspeciesthatareconnectedto Small-medium dispersers/
seed-disperserspecies(innerring)by S. Cristóbal Island
links,representingfrugivorous Large finches/endemic
interactions.Modulesareshownin rodent & large-seeded plants
differentcolours/shadesandspeciesroles
* Western islands
arelabelledbydifferentsymbols.
Asterisksindicateintroducedspecies.For
Small finches/passerines
alistofthespeciesincludedinthe & small-seeded plants
interactionnetworksseeAppendicesS5&
*
S6fortheCanaryIslandsandthe
Galápagos,respectively. peripherals connectors module hubs network hubs
sixplants)(Figs1b&2,AppendixS6).Onemodulewasdomi- Othertraitsshowedphylogeneticsignals,e.g.fruitsize(‘fruit
natedbythegianttortoise,togetherwithcattle,pigsandgoats, dm’).Phylogenyalsoinfluencedgeographicdistribution(‘no.of
whiletheothermoduleswerecharacterizedbybirdandreptile islands’) of Canarian seed dispersers and Galápagos fruiting
seed dispersers. Thus, in contrast to the Canaries, functional plants.
group affinity in the Galápagos disperser guild was a stronger In the phylogenies of Canarian plants and dispersers, and
driverthanhabitatspecificity. Galápagosdispersers,thetrait‘nativeversusalien’wasdistrib-
Withregardtothedriversofmodularity,Kandλgavequali- uted according to a Brownian motion model of evolution
tativelysimilarresults;networktraitsonlyshowedsomesignifi- (D≤0),indicating a phylogenetic signal.However,native and
cant phylogenetic signals (TableS3). Canarian plants showed alienGalápagosplantspeciesweredistributedindependentlyof
phylogeneticclusteringwithrespecttotheirabilitytolinkdif- theirphylogeny(Dwascloserto1thanto0).
ferentmodules(relatedplanttaxawereimportantconnectors), Severaltraitswerecorrelatedaftercorrectingforphylogenetic
andrelatedtaxa(e.g.speciesoffinches)inGalápagoshadahigh dependency(Table5),butthepatterndifferedstronglybetween
linkagelevel.Bodyweightwasatraitthatwasaffectedbyphy- communitiesandbetweenarchipelagos.IntheGalápagos,dis-
logeny among both Canarian and Galápagos dispersers; the perserspeciessharingamodule(‘moduleaffinity’)hadamore
‘tortoise/largemammals’modulefromGalápagosstronglycon- similarextentofgeographicaldistribution(‘no.ofislands’)than
tributed to this.Habitat specificity (‘main habitat’) was influ- arandomspeciesset;bycontrast,theothercommunities(Galá-
encedbyphylogenyintheCanariandispersercommunityand pagosplantsandCanarianplantsanddispersers)didnotshow
boththeplantandthedispersercommunitiesontheGalápagos. this correlation. The Canarian modules were more associated
GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd 5
M.Nogalesetal.
Table4 Numberofspeciesandlinksinmodulesofseed-dispersalnetworksoftheCanaryIslandsandtheGalápagos.Moduleconnectance
C istheproportionofrealizedlinksinsidethemodule(i.e.numberofobservedlinks/numberofpossiblelinksinthemodule,excluding
M
linkstoothermodules).
No.of No.of
No.of No.of within- between-
plant disperser module module
Module species species links links C
M
CanaryIslands
Medium-largelizard 20 3 34 76 0.57
High-mountain 2 1 2 7 1.00
Thermophilousforestandpasserines 11 4 37 70 0.84
Coastalxerophyticshrublandandbird/mammals 8 12 36 58 0.38
Laurelforestandlargebirds 14 7 35 44 0.36
Secondaryseeddispersal 10 3 22 63 0.73
Total 65 30 166 318* −
GalápagosIslands
Tortoise–largemammaldispersers 8 4 13 11 0.41
Geospizaconirostris–Opuntiahelleri 1 1 1 0 1.00
Small–mediumdispersers/SanCristóbalIsland 9 4 27 36 0.75
Largefinches/endemicrodentandlarge-seededplants 2 3 4 13 0.67
Especiallytwopasserines(GeospizascandensandMimusparvulus),onedove 8 6 26 25 0.54
(Zenaidagalapagoensis),theiguanaConolophussubcristatusandrichflora
Especiallyfivesmallpasserines(Certhideaolivacea,Certhideafusca,Camarhynchusparvulus, 6 10 26 27 0.43
Geospizafuliginosa,Dendroicapetechia)andendemictree-likeMiconiarobinsoniana
Total 34 28 97 112* −
*Numberofbetween-modulelinksisequaltothehalfofthesevalues,becauseeachbetween-modulelinkiscountedtwice,i.e.frommodulesAtoB,and
fromBtoA.
Canaries Galápagos
8
Module hubs Network hubs Module hubs Network hubs
ze ()6 Figure2 Distributionofseeddispersers
e
gr andfleshyfruitedplantsaccordingto
e de4 theirnetworkrole(symbolsasinFig.1)
dul intheCanarianandGalápagos
o2
m archipelagos.Cut-offvalues(2.5forzand
n-
hi 0.62forc,seeMaterialandMethods);
Wit0
eachdotrepresentsaspecies;whitedots
-2 Peripherals Connectors Peripherals Connectors arefleshyfruitedplantsandgreydots
0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1
Among-module connectivity (C) Among-module connectivity (C) frugivores.
with habitats within islands.Large Canarian dispersers (‘body
DISCUSSION
weight’) had a central position in their modules (high z),
whereas those specific large Galápagos dispersers had a high Althoughbothoceanicarchipelagosharbourrichcommunities
habitat preference (‘main habitat’) and were dominated by with similar diversity of dispersers,connectance level,and the
invasive alien mammals. The three main network parameters samenumberofmodules,theydifferedconsiderablyonoverall
(l,candz)werepositivelycorrelatedinallcommunitiesexcept plantdiversityandonnetworktopology.Therobustnessagainst
candzfortheGalápagosplants.ThemostwidespreadCanarian disturbancesofanetworkisinfluencedbylevelsofnestedness,
fruitingplants(‘no.ofislands’)hadmorelinks(L)andshowed modularity and connectance. High nestedness (Thébault &
more connectivity (c). Thus we see relationships between Fontaine,2010),andalsohighmodularity,mayaddstabilityto
modular structure and body weight, habitat preference and a mutualistic network, but they do it in different ways
native/alienstatus,andalsobetweennetworkcharacteristicsand (Sebastián-González etal., 2015). The Canarian network was
geographicaldistribution. highlynestedandthusstronglycoherent,resistingcommunity
6 GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd
Modularityofseed–dispersalnetworksonoceanicislands
Table5 Coefficientofdeterminationbetweentraits(continuous/categorical)incommunitiesofseeddispersersandtheirfruitingplantsin
theCanaryIslandsandtheGalápagosaftercorrectingfortheinfluenceofphylogeny(includingintroducedspecies).
Module log(body Main Native/ log(linkage Connectivity, Hubability, No.of
centrality weight) habitat invasive level,L) c z islands
CanaryIslands
Seeddispersers
Moduleaffinity – n.s. n.s. n.s. 0.16* 0.27** n.s. n.s.
Modulecentrality n.s. (−)0.46*** n.s. 0.14* 0.20** n.s. n.s.
log(bodyweight) n.s. n.s. n.s. n.s. 0.19* n.s.
Mainhabitat n.s. n.s. (−)0.11* n.s. n.s.
Native/invasive n.s. n.s. n.s. n.s.
log(linkagelevel,L) 0.87*** 0.75*** n.s.
Connectivityc 0.48*** n.s.
Hubability,z n.s.
GalápagosIslands
Seeddispersers
Moduleaffinity – n.s. n.s. n.s. n.s. n.s. n.s. 0.30**
Modulecentrality (−)0.40*** n.s. (−)0.18* 0.14* 0.21** n.s. 0.14*
log(bodyweight) 0.34*** 0.31** n.s. n.s. n.s. n.s.
Mainhabitat 0.36*** n.s. n.s. n.s. n.s.
Native/invasive (−)0.34*** (−)0.37*** (−)0.17* n.s.
log(linkagelevel,L) 0.82*** 0.82*** n.s.
Connectivity,c 0.63*** n.s.
Hubability,z n.s.
CanaryIslands
Fruitingplants
Moduleaffinity – (−)0.07* n.s. n.s. 0.16*** 0.17*** n.s. n.s.
Modulecentrality n.s. (−)0.12** n.s. (−)0.28*** (−)0.21*** n.s. (−)0.05*
Fruitdm n.s. 0.12** n.s. n.s. n.s. n.s.
Mainhabitat n.s. n.s. n.s. (−)0.10** n.s.
Native/invasive n.s. (−)0.08* n.s. n.s.
log(linkagelevel,L) 0.80*** 0.22*** 0.30***
Connectivity,c n.s. 0.15**
Hubability,z n.s.
GalápagosIslands
Fruitingplants
Moduleaffinity – n.s. n.s. n.s. n.s. n.s. n.s. n.s.
Modulecentrality (−)0.11* n.s. n.s. 0.16* n.s. n.s. n.s.
Fruitdm n.s. 0.13* n.s. (−)0.13* n.s. (−)0.48***
Mainhabitat 0.14* n.s. n.s. n.s. n.s.
Native/invasive n.s. n.s. n.s. n.s.
log(linkagelevel,L) 0.64*** 0.45*** n.s.
Connectivity,c n.s. n.s.
Hubability,z (–)0.09*
Significancelevel:*P<0.05;**P<0.01;***P<0.001;n.s.,notsignificant.Moduleaffinityisabinaryvariable,indicatingifaspeciesismemberofthe
samemoduleornot;modulecentralityisthenumberofbetweenlinksofamodule/(totalnumberoflinksinamodule),i.e.linksfromagivenmodule
toallothermodules,dividedbythetotalnumberoflinksofthemodule(no.linkstoothermodules+no.linkswithinthemodule).Minussignsin
bracketindicatethedirectionofthecorrelation.
disassembly,especiallytheextinctionofrarespecies(Bascompte press).ThestrongcoherenceoftheCanariannetworkisdueto
etal.,2003;Rodriguez-Cabaletal.,2013),whereastheGalápa- itsmanyconnectors(threetimesasmanyasintheGalápagos);
gosnetworkconsistedofwell-separatedmodules(intermodule these are animals moving between habitats,and plants with a
distancewastwiceaslargeastheCanarianandtheproportionof wide elevational range. In general, the Galápagos network is
between-module links was considerably lower). According to functionallystructured(assemblagesof birds,lizards,tortoises
that,thedifferentmodulesoperatemoreindependentlyinthe andtheirplants,andoneintroducedmammalmodule),whereas
Galápagos. This pattern reduces the risk of coextinction cas- the Canarian network mainly reflects the underlying habitat
cades (Rodriguez-Cabal etal., 2013; Bascompte & Olesen, in diversity(elevationalzones:mountains,forests,coastland).Both
GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd 7
M.Nogalesetal.
aregeographicallywellstructured,andeachmodulewasoften fortunatelystillmostlyintact,withtheexceptionoflocalextinc-
locatedononeorafewislands. tionsofgianttortoisesonGalápagos.However,acloserlookat
theinfluenceofdifferencesinnetworkstructure,asobservedon
the Canaries and the Galápagos, upon extinction dynamics,
Seed-dispersalnetworksandmodules
mightbeafruitfulfutureresearchprogrammethatmayexpose
The general trend that more diverse networks have more differentcolonization–extinctiondynamics.
modules (Olesen etal., 2007) was not observed in our study,
even though the Canarian network had twice as many plant
speciesastheGalápagosone.Thereasonsforthisare:(1)the
Thedriversofmodularity
largeintermoduledistanceandthushighmodularitylevelofthe
Galápagosnetwork;and(2)thehighertopologicalrank(con- The drivers of modularity appear to be quite different on the
nectors,moduleandnetworkhubs)ofCanarianspeciesinpar- twoarchipelagos.Habitatdiversityandnumberof biomesare
ticular–Canarianconnectorsweremorefrequent.Bothfeatures higher on the Canaries,perhaps due to a considerably higher
tendtoreducethenumberofmodules.Ifweregardamoduleas elevationcoupledwithamuchwidergeologicalagespan.Fleshy
a kind of niche shared by a set of strongly interacting species fruitedplantswerewellrepresentedinallhabitats,exceptinthe
(Gómez etal., 2015), then our results demonstrate that the pineforest.Birdsweremoreimportantinforestenvironments,
Galápagoshaveamoreclearlydelimitedandfine-grainedniche whilelizardsweremoresointheopenhabitatmodules,inboth
structure than the Canaries. Finally, the stronger Galápagos coastalandhigh-mountainhabitats(Validoetal.,2003;Rumeu
modularity was further enhanced by invasive alien mammals, etal.,2011).Thetwomodulesdifferedbecausetheywereorgan-
whichformedtheirownmodule. izedaroundlizardsandsecondaryseeddispersers,confirming
In the Canaries, the kestrel and the lizard G.galloti were theroleoftheseanimalsinmutualisticinsularsystems(Olesen
network hubs.The wide foraging range of the kestrel and the &Valido,2003;Nogalesetal.,2007;Padillaetal.,2012).
wideelevationalrangeofthelizard(Padillaetal.,2012)circum- In the Galápagos,each module was formed by species with
ventthehabitatspecificityof theirmodules,incontrasttothe somewhat similar traits,selecting similar functional groups of
other four modules. A key role was also played by the two species,especially birds and lizards (but see the‘tortoise/large
endemic laurel forest pigeons, both being hubs in the ‘laurel mammals’ module). Most modules included sauropsid repre-
forest and large birds’module.Their central role (10–15 fruit sentativesandtheimportanceofseeddispersalbybirds,lizards
plants)emphasizestheimportanceofthesebirdstothisunique andtortoisesiswellknownfromislands(e.g.Guerrero&Tye,
forest.Furthermore,thepigeonswereresponsiblefortwo-thirds 2009;Helenoetal.,2011b,2013;Blakeetal.,2012).
ofalldispersallinksintheforestandsuchamodularstructure Ingeneral,thepaucityofwell-resolvedstudiesofseeddisper-
couldperhapsbesaidtohavethesignatureofboththeconsid- sal modularity (two exceptions from mainland environments
erableageoftheforestandthestrongelevationalzonationofthe being Donatti etal., 2011; and Schleuning etal., 2011) still
islands.Fortunately,bothspeciesofpigeonhavehealthypopu- hampers comparisons of island and mainland networks.
lationsandnoimmediatethreatsareknown. However, we hypothesize that modularity could be higher in
In the Galápagos, the tortoise C.nigra constituted the sole continents, where rich species assemblages tend to have been
networkhub,whiletheplantMiconiarobinsonianawastheonly interacting for longer evolutionary periods, forcing species to
module hub, and both are endemic. The role played as seed specialize and occupy smaller realized niches. In contrast, the
disperser by C.nigra (see Blake etal., 2013) is due to its large poorer biodiversity of oceanic islands allows some species to
bodysize,homerangeandcapacitytodispersebothsmallseeds become very common (density compensation), broadening
and the largest fleshy fruited plants such as Hippomane theirtrophicniche(interactionrelease;Travesetetal.,2015)to
mancinella (Euphorbiaceae) (Blake etal., 2012; Heleno etal., becomesuper-generalists,andthustomakethenetworkmore
2013). Populations of this tortoise are, in general, recovering coherent.Inspiteofthisreasoning,thenumberofmoduleswas
their former size with the eradication of competing feral rathersimilarbetweenourtwooceanicarchipelagosandthetwo
mammalsoccupyingthesamemodule.Modularitywouldcer- mainland sites (Donatti etal., 2011; Schleuning etal., 2011),
tainlyincreasefurtherifthepopulationsoftortoiseweretreated though the island networks were smaller.Detailed studies are
taxonomically as distinct species (Jiménez-Uzcátegui etal., neededinordertodelvedeeperintotheinterpretationofmodu-
2014).Followingtherecentreleaseof tortoisestonewislands, laritybetweeninsularandcontinentalenvironments.
forexamplePintaandSantaFe,wecanexpectstrongnetwork Irrespective of the two main causes of modularity in the
changes,particularlywiththereintroductionofan‘extinctfunc- Canaries(environmentalheterogeneity)andGalápagos(species
tion’ within these communities. Miconia robinsoniana is the functionalroles),thesixmodulesdetectedoneacharchipelago
dominantplantthroughoutthehighlandMiconiazone.Here,it mayproducestrongisolationovertime.Ontheotherhand,itis
isoneof thefewspeciesproducingfleshyfruits(Helenoetal., possiblethatislandshavehighmodularityduetotheimportant
2013) and is a key resource for most dispersers in its module habitat diversity in the different archipelagos and the strong
(TableS5). temporaldynamics(e.g.vulcanism).Thesetwofactorsareprob-
Althoughhuman-inducedextinctionisrelativelycommonon ablythebasicdriversoffastspeciationoccurringwithinremote
oceanicislands,thefrugivoreassemblageofbotharchipelagosis territories isolated in the middle of the two largest oceans.
8 GlobalEcologyandBiogeography,©2015JohnWiley&SonsLtd
Modularityofseed–dispersalnetworksonoceanicislands
Indeed,wesuggestthatislandstudiesfocusingupontheimpor- Bascompte,J.&Jordano,P.(2013)Mutualisticnetworks.Prince-
tanceofmodularityforspeciationratecouldbeamostprom- tonUniversityPress,Princeton.
isingresearchavenue. Bascompte, J. & Olesen, J.M. (in press) Mutualistic networks.
Mutualism (ed. by J.L. Bronstein). Oxford University Press,
Oxford.
CONCLUDING REMARKS
Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003)
This is the first detailed study of the modularity of seed- The nested assembly of plant–animal mutualistic networks.
dispersal networks on oceanic islands. We demonstrate that Proceedings of the National Academy of Sciences USA, 100,
insularseed-dispersalnetworksmaydifferprofoundlyintheir 9383–9387.
linkage structure among oceanic archipelagos. In this sense, Batagelj, V. & Mrvar, A. (1998) Pajek: a program for large
modulesformpromisingbiogeographicalentitiesforexploring networkanalysis.Connections,21,47–57.
the interplay between ecology and evolution on islands and Blake, S., Wikelski, M., Cabrera, F., Guezou, A., Silva, M.,
elsewhere. Thus the evolutionary history of insular networks Sadeghayobi, E., Yackulic, C.B. & Jaramillo, P. (2012) Seed
mightalsodifferwithimportantconsequencesforourgeneral dispersalbyGalápagostortoises.JournalofBiogeography,39,
understanding of island biogeography,colonization/extinction 1961–1972.
dynamicsandspeciationpatterns. Blake, S., Yackulic, C.B., Cabrera, F., Tapia, W., Gibbs, J.P.,
Kümmeth, F. & Wikelski, M. (2013) Vegetation dynamics
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ACKNOWLEDGEMENTS
ingacrossaltitudinalgradients.JournalofAnimalEcology,82,
ManycolleaguesintheCanariessharedwithustheirobserva- 310–321.
tionsoninteractionsbetweendispersersandfruitingplants,but Blomberg, S.P., Garland, T. & Ives, A.R. (2003) Testing for
especially Alfredo Valido, Félix M. Medina, Juan D. Delgado, phylogeneticsignalincomparativedata:behavioraltraitsare
DavidP.Padilla,PatriciaMarrero,AiramRodríguezandMarta morelabile.Evolution,57,717–745.
López.IntheCanaries,wealsoexpressourgratitudetopublic Carstensen, D.W. & Olesen, J.M. (2009) Wallacea and its
institutions at national (Parques Nacionales) and autonomic nectarivorousbirds:nestednessandmodules.JournalofBio-
level (Gobierno de Canarias and Cabildos insulares). In the geography,36,1540–1550.
Galápagos,we thank the Charles Darwin Foundation and the Cox, S.C., Carranza, S. & Brown, R.P. (2010) Divergence
ParqueNacionaldeGalápagosforofferingusmuchinformation times and colonization of the Canary Islands by Gallotia
andlogisticsupport.Theeditorsandtwoanonymousreferees lizards. Molecular Phylogenetics and Evolution, 56, 747–
provided useful comments and suggestions to improve this 757.
manuscript.R.H.wasfundedbyFCTgrantIF/00441/2013and Dalsgaard, B., Trøjelsgaard, K., Martín González, A.M.,
the Marie-Curie CIG-321794. This study is framed within a Nogués-Bravo, D., Ollerton, J., Petanidou, T., Sandel, B.,
biodiversityprojectintheGalápagosIslands,financedbyBBVA Schleuning, M., Wang, Z., Rahbek, C., Sutherland, W.J.,
Foundation (Spain) and by projects CGL2012-C02-01 and Svenning,J.C.&Olesen,J.(2013)Historicalclimate-change
CGL2013-44386-P financed by Ministerio de Economía y influences modularity and nestedness of pollination net-
Competitividad(Spain). works.Ecography,36,1331–1340.
Donatti,C.I.,Guimarães,P.R.,Galetti,M.,Pizo,M.A.,Marquitti,
F.M.D. & Dirzo, R. (2011) Analysis of a hyper-diverse seed
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