Species richness of Costa Rican Cenocoeliini (Hymenoptera: Braconidae): a latitudinal and altitudinal search for anomalous diversity

10 Pages·1998·3.4 MB·English

by  L J Van Der Ent

J.HYM.RES.
Vol.7(1),1998,pp.15-24
Species Richness of Costa Rican Cenocoeliini (Hymenoptera:
Braconidae): a Latitudinal and Altitudinal Search for
Anomalous Diversity
Leendert-JanvanDF.REntandScottR.Shaw
DepartmentofPlant,SoilandLIanrsaecmtieS,ciWenYces8,20P7.1O,.UBSoxA3354,UniversityofWyoming,
Abstract.—LatitudinalpatternsofspeciesdiversityofNewWorldBraconidaehavebeenscarcely
surveyedtodate.Suchpatternsmaybeofbiogeographicalandecologicalinterestbecausesome
literaturedatasuggestthatsomebraconidsubfamiliesdonotshowanincreaseinspeciesdiversity
towardstheequatordespiteanincreaseofpotentialhostspecies(i.e.,"anomalousdiversity").In
thepresentstudy,speciesdiversityofa"presumptive"anomalousdiversebraconidtaxa,Ceno-
coeliini,wassurveyedinCostaRica.Theresultswerecomparedwithpublisheddistributiondata
olfevNelorttoh34A0m0ermicaalntiCteundoecionelCioisnit.aARliscoa,wsepreceieasnarliyczhneedsstoacnodmapbaurnedalantcietuodifnCaelnaocnodelailitnitiudfirnoamlgsreaa--
dientsinspeciesdiversity.CostaRicanCenocoeliiniwerefivetimesmorespeciosethanthosein
CanadaandUSAcombined.Theincreaseinestimatedspeciesrichnessperunitareatowardsthe
equatorofNorthAmericanCenocoeliiniwassimilartothatoftheirmostcommonhosts,Cer-
ambycidaeandScolytidae,butexceededthatofthepotentialhostsinCostaRica.Diversification
inCostaRicanCenocoeliiniwaspartlyinfluencedbyadaptationtodifferenthostfamiliesand
hmo)stinsuCbosstrtaateRsi.caM.oCsetnoscpoeecliieisnianwderiendniovtidueanlcsouonfteCerneodcoaebloivieni1w6e0r0emfoiunnCdosattaloRiwcaa,lttihtiusdebsei(n<g50i0n
contrasttotheirmostlikelyhosts, CerambycidaeandScolytidae, whichalsooccurredathigh
asletmiattuidecs.fuLnacrtgieorn-stiozweadrCdosstvaisuRailclayn-oCreineonctoeedlipirneidawtoerrse.oNfteewnbWroirghltdlyCecnoolcooreeldiisnuiggaepspteiangreadntaopboe-
tropicallowland-centeredandthisisexpectedtoberatheraneffectoftemperaturerequirements
thananeffectofhost-limitation.
Anomalousdiversityisdefinedasapat- thetropicsmayprovidebiasedresultsfor
tern in species richness "counter to the large-sized parasitoids (>3 mm) in areas
prevalenttrendofincreasingspeciesnum- where small-sized parasitoids may be
ber in a taxon with decreasing latitude" abundant (Hespenheide 1979; Morrisson
(Rathcke and Price 1976). Owen and etal. 1979).Morerecently, resultsofMal-
Owen(1974)werethefirstinvestigatorsto aise trap sampling revealed that some
show anomalous diversity for parasitic subfamilies of Ichneumonidae displayed
Hymenoptera of the family Ichneumoni- anomalous diversity (Gauld 1986, 1987,
dae,despiteanincreaseofnumbersofpo- 1995b). Several theories toexplain latitu-
tential host species towards the equator, dinal patternsinspeciesdiversityofpar-
Janzen and Pond (1975) found a similar asiticHymenopterahavebeenformulated:
pattern in species richness for parasitic resourcefragmentation(Janzenand Pond
Hymenoptera; they were less or equally 1975; Janzen 1981), predation on hosts
specioseinCostaRicacomparedtothose (Rathcke and Price 1976), predation on
occurring in a meadow in England. Sev- parasitoids(Gauld 1987),andthe"nasty"
eral investigators noted that sweep-sam- hosthypothesis(Gauldctal. 1992;Gauld
pie studies of parasitic Hymenoptera in andGaston1994).Accordingtothesethe-
16 JournalofHymenopteraResearch
ories, differentecologicalgroupsofpara- evaluated carefully. Specialistparasitoids
sitic Hymenoptera are expected to show (i.e.,koinobionts)associatedtoendophytic
differentpatternsinlatitudinalspeciesdi- hostsmayshow,aspredictedbythethe-
versity(Hawkins1994). ories of resource fragmentation and pre-
To date, anomalous diversity has not dationonparasitoids, a (very)strongde-
bcoeneindafeu.llyQuaincakleyzaenddfoKrruNfetw(1W9o95r)ldfoBurnad- cpreeraasteetiontsrpoepciiceaslrziocnhenses(sTafbrloem4.t2h,eHtaewm--
somesubfamiliesofBraconidae(e.g.,Aly- kins 1994). At the other hand, these
siinae,Aphidiinae,Cheloninae)tobeless parasitoids may also show, as predicted
speciosefromnorthern(zone3,4)towards by the theory of predation on hosts and
southern (zone 5) latitudes in the USA. thatofthe"nasty"hosts,aweakdecrease
This suggests anomalous diversity, how- toincreaseinspeciesrichnesstowardsthe
ever, theseanalysesdidnotincludeneo- equator. Thus, based on parasitizing be-
tropicalregions.Speciesrichnessofanoth- havior, contrasting predictions could be
er group, Cenocoeliinae (i.e., Cenocoeli- madeforspeciesrichnessofCostaRican
ini), increased fromnortherntosouthern Cenocoeliini.
temperate regions, but did not increase Species richness along altitudinal gra-
frommiddletolowerlatitudesintheUSA dients may demonstrate patterns similar
(Quicke and Kruft 1995). Also, species to those of latitudinal gradients (Brown
richnessofCenocoeliiniinsoutherntem- 1988; Stevens 1992). Noyes (1989) noted
perateregionswasequaltothatofnorth- that in general species diversity ofpara-
ernand central Mexicocombinedand to sitic Hymenoptera in an Indonesian rain
thatofsouthernMexico(datafromSaffer forestwasthehighestatlowaltitudes(<
1982).Todate,notmorethantwospecies 1000m).Alsothehighestdiversityoftheir
ofCenocoeliinihavebeendescribedfrom hosts,e.g.Lepidoptera,wasfoundatlow
Costa Rica (Saffer 1977, 1982). Previous altitudes (Holloway 1986). This suggests
data,therefore,suggestapatternofanom- that, if patterns in latitudinal and altitu-
alousdiversityinCenocoeliini.Thedistri- dinalspeciesrichnessaresimilar,anoma-
butionofCentral AmericanCenocoeliini, lous diversity should not occur among
however, is less well documented than parasiticHymenoptera.Resultsofanalti-
thatofNorthAmerica(Saffer1982). tudinal transect study in theVenezuelan
Cenocoeliini are diurnally activeendo- AndesbyJanzenetal. (1976)showedthat
plaarravsaieti(cvaknoiAncohbtieonrtbserogf1e9n9d4o;pShayftfiecrb1e9e8t2)l.e wspaescieassrhiicghhneasts2o0f0pamrasaisticatHy1m60e0nomp,tebruat
In North America, Cenocoeliini were that it was lower at high altitudes (3550
foundtoparasitizeCerambycidae(68%of and3600m). The declineofspeciesrich-
raencdordBeudprehossttidsapeeci(eSsa)f,feSrcol1y98t2i)d.aeK(o2i2n%o)-, n1e6s0s0aonfdp3ar5a5s0itmicwHaysmsemnaolpletrertahanbetthewedeen-
biontsareparasitoidswhichlettheirhosts cline of species richness of most other
continue to be mobile and defend them- groupsofinsectssuchasotherHymenop-
selvesfora whileafterbeingparasitized. tera(ants,bees,aculeatewasps)andother
Koinobionts are expected to have more insect orders (e.g., Coleoptera and Lepi-
narrow host ranges than idiobionts doptera).Thissuggeststhatsomegroups
(AskewandShaw1986;Gauld1987;Haw- of parasitic Hymenoptera show anoma-
kins 1994) and are often referred to as lousdiversity alongaltitudinalgradients.
"specialist" parasitoids. Sheehan and At a lower taxonomic level, tropical alti-
Hawkins(1991),however,notedthatcom- tudinal species diversity ofIchneumono-
parisons ofaverage host rangesbetween ideawasfound todifferamongsubfami-
koinobionts and idiobionts have to be lies(Gauld1985;GastonandGauld 1993;
Volume7,Number1,1998 17
Gauld and Hanson, in press). Also, Nacional de Biodiversidad, Costa Rica).
Ophioninaewerefound tohavedifferent Malaise traps were located in different
patterns in altitudinal species diversities habitat types and at different altitudes
betweentropicalregions(GauldandHan- throughout Costa Rica as described by
son,inpress). Gauld(1991, 1995a).Ouranalysesinclud-
As noted earlier, anomalous diversity ed ca 70 Malaise trap-yearsofsamplings
hasnotbeencompletelyanalyzedforNew atca 60differentsites.Therefore,sample
WorldBraconidae.Literaturedatasuggest coverage was expected to be reasonably
that the braconid tribe Cenocoeliini may representative fortheCosta Rican fauna.
showadecrease,oratleastnoincrease,in From these samples, Braconidae were
species diversity towards the equator. sorted and sentto theUniversity ofWy-
Therefore, the aims of the present study oming for identification. Cenocoeliini
were: 1) to determine whether species were sorted and individuals were deter-
richness and a-index of diversity of the minedtomorphospeciesusingthefollow-
Cenocoeliini in temperate regions were ing set of characters: hindwing venation
higherthanthoseintropicalregions,2)to (relativelengthvein IM-l-CU to IM, and
determinewhetherpotentialhostsofCen- IM to Ir-m); colorpatterns ofhead, me-
ocoeliini increased more in species rich- sosoma, metasoma, legs, ovipositor
nesstowardstheequatorthantheirpara- sheathsandantennae;bodysize;oviposi-
sitoids,3)torelatelatitudinalspeciesrich- tor length relative to forewing length;
nesswithaltitudinalspeciesrichness,and number of flagellomeres; and shape of
4) to determine whether abundance and apical flagellomeres. Additional charac-
species richness of Cenocoeliini were ters, like sculpture patterns on the pro-
higher at intermediate and high than at episternum, apexofthepropodeum, and
lowaltitudesinCostaRica.Thisresearch vertex, were included to distinguish
isthefirstinaseriesofanalysesofdiffer- among presumptive sibling species com-
entgroupsofBraconidaetobeexamined plexes.DatabySaffer(1982)wereusedto
for species diversity in Costa Rica in re- comparespeciesrichnessofBraconidaein
lationtoaltitudes. North America with that in Costa Rica.
MATERIALSANDMETHODS SMaexmipcloecwoavserraegleataivnedlysalmopwleanindtelnessistyrefpo-r
ThetribeCenocoeliiniisamonophyletic resentativefortheareathanthoseofCan-
groupinthe Helconinae (Shaw 1995), al- ada,USAandCostaRica.
though several authors placedtheCeno- Twoformulaewereusedtoestimateex-
coeliiniasthemaintribeinaseparatesub- pected species richnessofthefaunae(S')
family, Cenocoeliinae (van Achterberg based on thenumbersofindividualsper
1984,'l993; Shaw and Huddleston 1991; speciesinasample:
bWliyhinaivrastpnoencAic1eh9st93ew)re.breBeregfcoo(rn1es9i9t4dh)ee,rgemedonestroticbCeerenwvoiictsohieio-nn s1.peSc^i'es=wSi-t/h(Son-eSi,n)di(Sv,id=uatlo)talnumberof
tlheceItnegddeinvwuiidstuhaClensMoaclooafeilisCueesn.torcaopesli(i8ni5%)wearnedctohle- o2.fsS"p-ec=ieSsw+it(h(S,t)wVo2Si,n)di(Sv;id=uatlost)alnumber
restbyhandnettinginCostaRica,mostly Thefirstformulaofexpectedspeciesrich-
during the last 10 years. Hand collected ness (S'') is derived from the formula of
specimensforthisstudywerefromH.A. sample coverage (1-(N,/I): Fagen and
Hespenheide (University of California, Goldmann 1977). Inthisformula, Iisthe
Los Angeles), F. Parker (University of total number ofbehavior types observed
Utah) and J.A. Ugalde (INBio, Instituto and N| is the total behavior types ob-
18 JournalofHymenopteraResearch
bsaiTneynhvrdeevtrehNssde,eecoonwonfiulntydtmhhboefenSo,csr.rea.mmSo"up"If'llwaewoabasocssfoesvruceevbaxreslpatcdegiucetltsuapmetteudeecldditsewiapspiseltci(thiSehe)Sdes. v(nsaSepen"res'Tds,csaiibtUSe(yl'sSS-,e);,Anr1s.uiteccmweohboNnmemeubaersimtsssnbetereio(diSmfr,a,a,sll^tos)MecoesafoalxfnioiitfdnciCdeoeeismnxveao(pitclndeoohducceoat)ldlCeisasodi)nsn(,dtsiNap)aae,f-vRcrsiieicponeraesdma.cegirxeCeidasconhflrnaoiecdcdsaihals--
richness (S'"'), is that of Chao 1 as de-
scribedinColwellandCoddington(1994).
Inadditiontospeciesrichness,a-indexof
diversityofthelogarithmicserieswascal-
culated because of its good discriminant
ability and its low sensitivity to sample
size(Magurran1988).Toestimatespecies
richness per unit area the formula S, =
px/ear°-u^niwtasareuas,edx(=S, n=unmubmebrerofoofbsspeercvieeds
speciesincountryorregion, a = areaof
country or region (10' km-): MacArthur
and Wilson 1967, Gastonetal. 1996). We
also estimated species richness per unit
area for the most important temperate
hosts of Cenocoeliini, the Cerambycidae
(datafromMonneandGiesbert1994)and
the Scolytidae (data from Wood 1982;
Woodetal. 1991).
Toexaminetheeffectofaltitudeonspe-
ciesrichnessofCenocoeliini,wedefined4
altitudeclasses:low(0-500m),lowinter-
mediate (500-1500 m), high intermediate
(1500-2500 m) and high (>2500 m) alti-
tudes. These altitude classes reflect the
distribution of different habitat types as
describedbyGauld (1995a).Weassumed
that there was a linear relationship be-
tween sample effort (i.e.. Malaise trap-
months) and number of individuals
caughtinMalaisetraps.Becauseseasonal
variationin abundanceofneotropicalin-
sects occurs (Owen and Chanter 1970;
Wolda1988,1989;WoldaandWong1988),
only Malaise traps which operated three
ormoreconsecutivemonthswereinclud-
edintheanalysis,andabundancesofCen-
ocoeliini were summed for several year-
roundMalaisetrapsamples.Weestimated
expected numbersofCenocoeliini peral-
titudeclassbymultiplyingthetotalnum-
berofobservedCenocoeliiniwiththepro-
portionofnumberofMalaisetrap-months
of a particular altitude class to the total
Volume7,Number1,1998 19
Table2. Estimatedspeciesrichnessperunitarea(S,)ofparasitoids(Cenocoeliini)andtheirmostcommon
rticieacm,hpnueesrsiasntegesShw.,ohs=etsnx(/taCh"ee-r'easmatbsiyamcaistdteaadensdapanercddieSsscpoerlciyictehisnd-eaasers)eaofforrCedlaianftfaiedornaesnhtwiapgse(ossgeeretaptaehtxitc1)..a0l.BeretgwieoennsopfarNeonrtthhesaensdaCreentthrealreAlmaetirv-e
Geographical Area Cenocoeliini Cerambycidae ScolvHciae
region (10'km-') S. S,"
Canada(+Alaska)
20 JournalofHymenopteraResearch
Table3. Totalspeciesrichness(S),numberofMalaisetrap-months{#tm),observed(N„i,Jandexpected
o(Np^.e,rj,a)tendummboerrestohfanintdhrieveidcuoanlssecouftiCveenomcooneltihisniwepreerianlctlituuddeedcilnastsheiannaCloysstias.RIitcwa.asOntelsytedMailfatihseeobtsraeprsvewdhaincdh
expectednumbersofCenocoeliiniwereequalatlowaltitudes(<500m)andathigheraltitudeclassescom-
binedusingchi-squaretest.
Altitudecl
Volume7,Number1,1998 21
Lezama, pers. comm.). Scolytidae are in Malaise traps. The observed 24 Ceno-
known to be regularly encountered at coeliinispeciesinthePacificlowlandrain
high altitudes in Costa Rica (Wood etal. forest around Golfo Dulce in Puntarenas
1991). It is unlikely, however, that alter- Provinceshared9specieswiththe25Cen-
nativehostsforCenocoeliini,likelarvaeof ocoeliini species in the Atlantic lowland
seed-boringbeetlesdooccurathigh alti- rain forest of La Selva in Heredia Prov-
tudes. Legume trees, of which the fruits ince.ThisspeciesdistributionofCenocoe-
are among the most frequently attacked liini may suggest that manyCosta Rican
by seed-boring beetles (Janzen 1980), are Cenocoeliini have a restricted geographi-
scarceatintermediateandabsentathigh cal distribution according to Rapoport's
altitudes(Holdridgeetal.1971).Also,Gas- Rule (Stevens 1989, 1992). Itmay alsobe
tonandGauld(1993)notedthatPimplinae a sample artifact due to the low number
(Icneumonidae) were more abundant at ofindividuals.
high altitudes than at low altitudes. In Inthe present study it was found that
bcaeseensppreecsieenstofatCehniogchoeallitiintiudwesouilndChoasvtea htahlofseoflartgheer tCehnaonco5elmiimniwaenrde bersipgehctialolry-
Rica,theylikelywouldhavebeencollect- angeandblackcolored,oftenwithpartly
edintheMalaisetraps.Thissuggeststhat or completely darkened wings. Saffer
hostpresencedoesnotexplainabsenceof (1982) described 2 similar bright colored
Cenocoeliini at high altitudes in Costa CenocoeliinifromsoutherntropicalMex-
Rica. ico,butnosuchcoloredspeciesfromtem-
Inthepresentstudy,itcouldnotbede- perate North America. Bright colors are
termined if Cenocoeliini were scarce in common in tropical parasitoids (Quicke
CostaRicaorthatitisdifficulttosample 1986a;Shaw 1995). Brightcolorsoccurin
thembyusingMalaisetraps.Onaverage, several other neotropical braconid sub-
oneindividualofCenocoeliiniwascaught familiessuchasAgathidinaeandBracon-
per3to4Malaisetrap-months.Trapeffi- inaeand theyarecharacteristicforlarger
ciencyforCenocoeliiniwastwiceashigh sized (>5 mm) diurnally active Braconi-
at low altitude rain forests than at low dae with long ovipositors, which likely
middlealtituderainforestorlowaltitude parasitizeconcealedhosts(Shaw1995).In
dry forest. Also Cenocoeliini were most general,brightcolorsarecharacteristicfor
frequently caught during the dry season lowland insects where it occurs in up to
(Feb.-May;unpublisheddata).Butevenin 25% ofinsects and do not occur at high
theoptimalhabitattypeandseason,Cen- altitudes in Costa Rica (Janzen 1973).
ocoeliiniwasneverfoundtobeabundant Quicke (1986b) noted that in general
suggesting that they occur in low popu- brightcolorshaveawarningfunctionto-
lationdensities. wards visually-oriented predators (i.e.,
Anotherremarkableresultwasthat77% aposematic coloration). Bright colored
oftheMexicanand60%oftheCostaRican tropicalparasiticwaspsmaymimicsting-
species of Cenocoeliini were represented ingaculeatesandsomelargersizedpara-
byoneor2individuals.Estimatedspecies sitoids are capable of stinging by them-
richness of Mexican Cenocoeliini may selves (Quicke 1986b). Otherauthors hy-
havebeenunderestimatedassamplecov- pothesized that parasitoids may mimic
eragebytheMalaisetrapsinMexicowas unpalatablehostssuch asChrysomelidae
lowcomparedtothoseinCostaRicaand (Gauld,pers.comm.)orSymphyta(anon,
theUSAandCanadacombined. rev., pers. comm.). Gauld and Gaston
Analysesofgeographicaldistributionof (1994), suggested that parasitoids with
CostaRicanCenocoeliinicouldnotbejus- brightcolorsmaybeunpalatableforpred-
tified duetolownumbersofindividuals ators after sequestering "nasty" tasting
22 JournalofHymenopteraResearch
secondary plant chemicals from their ed number of species have adapted to
hosts.Ifthelatteristrueandthe"nasty" year-roundcoolconditionsatlowermon-
hosthypothesishasvalidityforCenocoe- tanerainforestsandnonetomontanefor-
liini, bright colored Cenocoeliini may at- ests. Someotherspecieshaveadapted to
tackseed-eatingorphloephageousbeetle climatological conditions in temperate
larvae,ratherthanwood-livingScolytidae regionsandevolvedoverwinteringmech-
or Cerambycidae. Quicke (1986a) found anisms(Saffer1982).
homeochromatic assemblages for some ACKNOWLEDGMENTS
largesizedBraconidaeandtheirpotential
h(o1s9t9s6)(is.e.h,owCeerdamtbhyactidacoel)o.rHpeastpteenrhnesidoef GaWuledfwoorusledttilnigkeuptothethMaanlkaisPeautlrapHannestwoonrkanindCoIsa-n
uMCnhodrreyerslorymeiesnlegairddcaehefeimsnsaneyeembdeeecdhsautnbositesrlmaustcei-odrraetloeatthteehder. JtlieainfkvfeRoilLtcovoaectdkahwnaiodnnokidfdoI,eranntMhiaGafavriuickalntdgSi,ohtnDaheaowfvUiaBndnridavKecaroazsnnmiitdeayarne,.oofnDWayWevmyeoowumLoseiugnlrgegd,-
meaning of bright colors in large sized viewerfortheircriticalcommentsonearlierversions
neotropicalwood-boringbraconidparasit- ofthemanuscript.
oids. LITERATURECITED
ThesmallersizedCostaRicanCenocoe-
liini from our survey were mostly less Achterberg,C,van.1984.Essayonthephylogenyof
conspicuouscoloredthanthelargersized Braconidae(Hymenoptera:Ichneumonoidea)£ii-
oconeelsi.inMiamnayyobfethaenste-msimmailclse,rwshiizecdhCiseneox-- Achteftroabmmeoillroigge,iscCo,TfuMvBrarnia.fcto1n919i035d.:ae4I1lu-(s5Ht8yr.mateendopkteeyrato:tIhcehsnuebu--
pected to occur frequently inneotropical monoidae).ZoologischeVerhamkiiiigen283:1-189.
Braconidae (Shaw 1995). This color pat- Achterberg,C,van.1994.Genericrevisionofthesub-
tern of presumably ant-mimics also oc- family CenocoeliinaeSzepligeti (Hymenoptera:
cliuirnire(dSafafmeron19g82)N.orTtohdaAtmee,rpiocsasniblCeenboechoaev-- AskeBmwru,anciRto.ineiRsd.:aea)tnh.deiZMro.oslioRzg.ei,sScshhtaeruwVcet(ru1hr9ae8n6d)a.enldPianrdgaeesvniet2lo9oi2p:dmc1e-on5mt2-..
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itudinal species richness (Fisher 1960; Colwell,R.K.and].A.Coddington.1994.Estimation
TPsheiurasvn,ekdaa1fno9or6m6a;CleSnotoucesoveeldniisivne1ir9.s8i9tT;yhWewialissnocrnneoa1ts9e9o2b)i-.n CondidtPtehor,inrleoR(s.sst,oerpriShi.aeilscPa.Blb)HiTuo3rbd4abi5ne:vslealr1c,s0ti1iJt-o.y1nVs1.8to.LfhartfohreuangRkhoiyea,elxRtS.roaScpiuoektluyatmLiaoornn,-.
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liinifromtemperateNorthAmericatothe 1996.Species-areaandspecies-individualrela-
Nhu1oae6slo0tst0sr.oomfpICinecanlCsotoicestoxtuecadleei,eRiidncteiahd,iwsteshipraneetccionofeonsttthrafeanoisrdutnpiodtntodeainbtvthoiievdaie-lr Fagen5tc2,i60ao1-tRn-ha.s2alh7oMi1pg.pl.uosetasfna,ondrajltoRyru.osrpniNias.clamGloeofttlhrEdecoemodsla:son.agnyAc.n8o4im1:m9p7aa57l4r.9iB-Bse5eho6ahn2oai.voofiioiturhrr2ae5le:
TpnaloehttseiestnuCtdiieenanslo.CcehoTnoehoslictisosiensliwuihgiaignpecipshatirssaelnntsthoolattyohcsiocpssuetraciletaisrtmoiprhtiiieccgdahh.l- GFiasscthodcdeniiare,v,ese)rKAs.o.aifrtJeyG...patiEnhm1vedp9or6lle0Iiu..ntiDienLo.sanCtGoi(1ast4Hutu:yldamd6ie4.nR-ani8lo1c19pa.9v?t3ae.rjrioaHaut:roinowaInlcmhionfnaenTouryrmogpoasinnpciiea--cl
lowland-centeredgroupofwhichalimit- Ecology9:491^99.
Volume7,Number1,1998 23
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