Table Of ContentINTER-SPECIFICASSOCIATIONS INVOLVING SPIDERS;
KLEPTOPARASITISM, MIMICRY .ANDMUTUALISM
MARK A ELGAR
Elgar, M.A. 1993 11 11: Inter-specific associations involving spiders: klcptoparasiusin,
mimicry and mutualism. Memoirs ofthe Queensland Museum 35i2): 41 1-430. Brisbane.
ISSN 0079-SS35
Manyspidershavelife-styles thatinvolve arelativelycloseandprolongedassociation with
anotherspecies;forexample,betweenaspecialistpredatoranditspreyspecies, oraspecies
mayrelyonanotherforeitherprotectionfrompredatorsorprovidingasuitableplacetolive.
Inasymmetric relationships, where individuals ofone speciesbenefitat the expenseofthe
other,eachspeciesmayactasaselectionpressureontheotherspecies.Thiscanresultinthe
evolution ofspecific adaptations and counter-adaptations thaiare evident in at least three
kinds of inter-specific associations between spiders. These associations, namely klep-
toparasitism,mimicryandmutualismare reviewedhere.Ourunderstandingoftheevolution
ofthesefascinatingsystemsremainslimited,despitenumerousanecdotalaccounts, because
onlyafew studiesareexperimental. Thepurpose ofthis review istwo-fold: U3 Illustratethe
useofcomparativeandexperimentalstudiesforunderstandinglheevolutionarysignificance
oftheseinter-specificrelationships,andtohighlightthuscgaps inourknowledge that might
benefitfrom\h\happtvacU.C\Inter-spedftcassociations,spiders,kleptoparasithm,mimicry,
mutualism.
MwkA. Lii>ar, DepartmentqfZoology, UniversityofMelbourne, Parkvilie, Vtcxeri
Australia; 18January, 199X
Individuals of one species can affect in- (e.g. Endlcr, 1986; Daviessai, 1989;TofttiaU
dividuals of another as a result of competition, 1991),butthereisalsosomeevidence forsimilar
predation, parasitism or mutualism. The evolu- processes in predalor-prev systems (eg Brodie
tionary implications ofany association between and Brodie, 1991; Endlerf 1991).
two or more species depends critically on the
frequency and nature ofthe interaction* For ex- INTER SPECIFICASSOCIATIONS IN
ample,aspeciesmaybetheprey ofmanyspecies SPIDERS
of generalist predators. While these predators
may represent an important selective pressure
Research on the behaviour and ecology of
favouring anti-predator responses in the prey
spiders has, with a few notable exceptions,
species, the adaptations of the prey may have
focussedon issues involving single species (e.g
little impact on the reproductive success of the Humphreys, 19S8).includingforagingbehaviour
predators. In contrast, a predator that preys on
(Reichert*and Luczak, 1982; VollrauY 1987a;
only one species can be an important selective
Uetz, 1992), habitat choice (e.g. Reichert and
force favouring anti-predator adaptations in that Giltespie, 1986), intraspecific competition (e.g.
species. In turn, the prey species anti-predator Reichert, 1982), courtship and mating (e.g.
adaptations can exert a selective pressure on the Robinson and Robinson. 1982; Elgar, 1992) and
predator, favouring improvedpredatoryabilities social behaviour (Buskirk, 1981; Elgar and
Thus, each species acts asa selectionpressure on Godfrey, 1987; Uett, 1988). Nevertheless, some
the other, favouring adaptations and counter- spiders have relatively specific and prolonged
adaptations, perhaps leading to characteristics relationships with other species. These relation-
that are increasingly specific to the relationship. ships often involve predation or avoiding preda-
However, these improvements need not neces- tion, and perhaps a reason why inter-specific
sarily change the relative position of each interactions involving spiders have been
protagonist (Dawkins and Krebs, 1979). The neglected is thatspiders arefrequentlyperceived
evolution of these specific adaptations and as generalist predators; cursorial or wandering
counter-adaptationsdependsonboththefrequen- spiders attack any vulnerable prey that they can
cy of the interactions and the effects of each find, while web-building spiders simply capture
protagonist. Host-parasite systemsprovide arich anypreythatiscaughtintheirweb. However,(he
seamofexamplesofsuchevolutionaryprocesses view that spiders are generalist predators is mis-
MEMOTRSOFTHEQUEENSLAND MUSEUM
113
leading. Many spiderspreyononlyafewspecks Mysmenidae, Symphytognaihidae and
using foraging techniques that include building Theridiidae (Table I).Ofthesespiders,thegenus
specialised webs; producing chemical com- Argyroses (Theridiidae) is the best documented
pounds that attract prey; utilising the webs or (see Vollrath. 1984T 1987b).
capturing capabilities ofother spiders; mimick-
ingpreybehaviour;andcooperativeforaging{see EVttJGNCe OP KLEPTOPARASmSM
reviewsinStowe. 19S6:Nenrwig, 1987).Clearly, Argyrodes were originally described as com-
the survival and reproductive success of both
mensals: Argyrodes benefit by feeding on the
predaior and prey will depend on theirpredatory
prey items that are caught in the host's web. but
and defensive behaviours, and the degree to
lil tohfe fporoedd.atNorotdeapllenadsssoocinattihoensprbeeytwaesena tiHhtoeewmhesovsdetor,insosntuobftsoderiqmsupaeadnrvttabonefthaiatgvseiddoiuehrtea(clea.aug.snedBeetlchtoe.lsoe1g8pi7r4ce)a.yl
spidersand otherinvertebrates are predator-prey
studies revealed that individual Argyrodes
relationships, some species depend on other
remove prey that might otherwise be consumed
speciesforprotection from p&daiOtti 01 provid-
by thepredator. These observations suggest that
ing suitableplaces10 live. Thisreview will focus the relationship between Argyrodes and their
ospnidtehrrese: mktleicpstpoepciafriacsirteilastmi.onsmhiipmsicinrvyolvainndg hosts is more accurately described as klep
toparasiiic rather than commensal (see Vollrath,
mutualism.
1984,1987b).
Adetailed understanding ofthe nature ofthese In fact, klcptoparasitism may also be an inap-
inier-specific associations will benefit fromboth A
propriate description. kleptoparasiiic relation-
experimental and companiiive studies The
ship implies that one partner in the symbiosis
former can provide insight into both 1h<? fitness benefits at the expense ofthe other, and Uiat the
effects ofthe association on individuals ofeach
klcptopurasite hascertain characteristics that are
species,andtheimportanceofparticularspecies'
adaptations to this lifestyle. Studies of several
traits for maintaining the association. Compara-
nd species associations leave liule doubt that the
studies can provide further insight into the
IanercontentioDiscorrectForexample,dicsym-
lion pressures responsible for theevolution
phytognathid Curimagua inhabits the
• iftheassociation;revealtheimplicationsofthese Webs of a large mygalomorph Diplura, i-iihet
i.tiiuns foi other aspects ofthe species life- climbing about the funnel web or remaining on
history characteristics; and help formulate ideas
the host (Vollrath. 3978). After a Dipiunt has
thatcanbesubsequentlyexaminedexperimental-
caught, masticatedand enveloped a prey item in
ly IseeHarveyandPagel, 1992 forreviewi.While digestive fluids, the kleptoparasite descends to
emphasising the evolutionary dynamic nature of
the prey item and imbibes the liquidized prey
inter-specificassociations,acentralthemeofthis
Interestingly, the anatomy of the mouth of C.
review is to illustrate the use ofcomparative and
experimentalstudiesforunderstandingthesesys- bayanoapparently prevents it from being able to
knowl, eadngdeaolfsaoratcohnhiidghilnitgerh-tsptehcoisfeicagsasposciiantions cianpgttuhraet,ihtoilsdanorobmlaisgtaitceatkeleipttsoopwarnaspirteey,(Vsoulglgreastth-,
1978),
ght benefit from this evolutionary ap-
Several behaviours ofArgyrodes appear to be
proach.
adaptations that arc specifically related to
KLEPTOPARASmCASSOCIATIONS kleptoparasiticlifestyle.These spiderscanmove
throughouttheweb,apparentlyundetectedbythe
host and the attempts of the kleptoparasites to
The webs of spiders arc host to numerous in- obtain prey items mav vary according to the
sects, including flies, damselfies and wasps (see behaviour of the host (Vollrath, 1984. 1987b).
reviews in Vollratfi, 1984. 1987b; Nentwig and There are several mechanisms by which klep-
Heimer, 1987).Most descriptionsoftheseguests toparasiticArgyrodes avoid detection or capture
areanecdotal, andconsequently thenatureofthe by the host: many species drop from the web
relationship is poorly understood. The webs of when challenged by the host, A. antipodfanuA
many spiders are also host to numerous other swings away from the web when the host is
spidersthai obtain food from prey caught in the agitated (Whitehouse, 1986). andA. ultdanscnl&
host's web. These spider guests commonly holes in the tangle web of its social spider bosfl
referred to as kleptoparasites, arc represented in Anelosinms eximius, forming a tunnel that ap-
at least four families, including the Dictynidae, parently facilitates escape (Cangialosi, 1991).
.
INTER-SPECIFICASSOCIATIONS 413
Surprisingly, the evidence that thepresence of number of kleptoparasites per web is greater in
Argyrodeshasa negative effectonthe reproduc- larger colonies. For example, Nephila edulis
tive success of the host has not been directly builds webs in aggregations, and webs in ag-
sed. Forexample, therearenoexperimental gregations have higher kleptoparasite loads and
t -knee that the growth rate or fecundity ofthe infestation rates than those found alone fElgar.
hostis reduced by the presence ofArgyrodc 1989).Re-locating a tyefc away froman aggi
any other generaofklep(oparasiles). Instead, the tion may reduce kleptoparasite load, butthehost
negativeimpactofArgyrosesonitshosthasbeen Subsequently does no( bench! from the foraging
inferred primarily from either the behaviour of and predatordefense advantagesoflivingwithin
the host ie.g. Larcher and Wise, 1985), or from anaggregation(e.g.seeUfctK, 1988) Movingweb
estimates ofthe energetic costs derived from the In reduce kleptoparasite load may not be
loss of prey items obtained by Argyrades. For possible frit some stX ul ••
example, the numberofprey itemsconsumedby Aneiositnus thai build substantial, permanent
Neplrilaclavipesisreducedwithincreasingnum- Webs, Indeed, high klcpttt; re ap-
bers of Argyrcxlcs on the web (Rypstra, 1981). parently responsible for tftc demise of some
and A. uMattsremoves around 26% ofthe prey Anelosiniuscolonics (Cangialosi, 1990b) but not
items that are caught in the web of its hosi others(Vollrath, 1982).
Anelosimuy exitnhts (Cangialosi, 199' Liketheirho^K individual klcptoparasites
Vollrath (1981> examined the potential costs of also react 10 variation in prey capture rates. |The
Argyroses by estimating the energetic require-
feeding rates of klcptoparasites ^rc Likely w* be
mentsofasinglekleptoparasite Thedailyen
influenced by both Ihe prey capture rate or the
requirements ofthe 3-4 mgA. elevaius is 0.82J, host and the number ofotherkierxoparasites on
abouti>.5%ofthedailyrequirementsofits975mg theweb.Hostwebcaptureralesmayvary at
(ftephih clavipes] post This proportion in- ing toboth the location and the size of the: web.
creases with larger numbers of kleptoparasites Thenumberofkleptoparasitesincreases withthe
per web; over 40 individuals have been counted websueofseveralhost species leg. Elgar, 1989;
on asingle Nephila web (although the average is Cangliosi. 1990a), possibly because larger
2.2 klcptoparasites perweb),suggesting apoten- have higher web capture rates that can support
tially high energetic cost of this relationship morekleptoparasites.Web-buildingspidersrelo-
(Vollrath, 1981). cate their webs Btf to prc> capture pates
IfKJeptoparasitesexactacostonhostreproduc- (e.g. Gillespie andCaraco. 1987),dndArgyrodes
tive success, then selection should favour any may behave similarly by moving to differ* r,i
trait that enables the hosts to reduce ihat cost. webs(hut see lurcherandWise, 1985). Itwould
There are several mechanisms by which be interesting to establish experimentally
I
might reduce the cost of kleptoparasilism: whether the emigration rate of individual Ar-
recovering the prey from the kleptoparasite; ^TOi#s»ncreasesasaresultonowerwebcapture
reducingthekleptoparasitesaccesstotheprey;or rates orincreased numbers ot conspecifics. Ifthe
Mmplyabandoning the webandbuilding another latter, it is possible that the distribution or Ar
elsewhere. Interestingly, hosts appear td be inef- gyroJeswithinapopulationofhosts, particularly
ficient at recovering prey (Vollrath, 1979a, b; those hosts that aggregate, could be predictedby
Rypstra, 1981) although several host species the ideal tree distribution (see Milinski and
reduce access to their prey by chasing the klep- Parker, 1991 j.
toparasites (Cangialosi, 1990b)orconcealingthe A possible option for klcptoparasites thar e*
prey in retreats [see Cangialosi. 1990b). Larcher perience a low feeding rate is b capture and
.m.l Wise (1985) demonstrated experimentally consume the host before moving tn tbe web of
that hostsare more likely to abandon webs when another host (e.g. Tanaka. 1984). Some species
Argyroses are present ihun absent. Nephila
of Argyti either obligate or facultative
lcalragveipneusmrbeelrocsaotfesklitcsptwoepbarwashietnesit(Risypisntfreas,te1d9w8i1t)h, pArregdyatwodrestocfatnheciarpthuorsetsth(eseheoTstabtlhero1u1ghPrmeidratory
arnleutsmhpbooeunrgssheottfhoekllbeoepwtheoarpvMiifaoesueirdtito-nfsg,/Vr.atcelsa,virpaetshermatyhabnetao aindgvaanpcrienygittoewma(red.g.thWehhiotsetboaunsdea.tt19ac8k6i)ngo it. Such
aspecialisedform ofprcdation i¬ uncomni*m
Social or communal spiders appear to have in spiders, and has been recorded in several
fewer defensive options against high klep- families leg. Jackson, 1987; Jacksonand b
roparashe loads,andthiscostmaybe higherifthe 1982. Jackson and Bras-sington, |9g7
414 MEMOIRS OFTHEQUEENSLANDMUSEUM
TABLE 1: Spiders thai are presumed to be kleptoparasites ofweb-building spiders. Families; Ag, Agelenidae;
Am, Amaurobiidae; Ap, Aphantochilidae; Ar, Araneidae; CI, Clubionidac; Co, Corinnidac; De, Deinopidae;
DPir,odDiidpolmuirdiadcae;^SaE,r,SaElrleisciiddaaee;; TGdn,,ThGenraipdhioisdiacd;aeT;mLTiTn,hoLmiinsyipdhaiei;daUel;,LUiloo,boLriiodcarea;niZdoa,e;ZoPdharTiiPdhaoel.ciAdageg;, PArgo-,
gregates; Soc, Social; Sol, Solitary Web types: O, orb; T, tangle; S, sheet; F, funnel; Sp, spacc.Body sizes in
mm.
Kleptopar*si(iclaxa BiodysNize Family Species Host Size Web Social pGeureswtesb AssoclSource
Dicrynidae
GnsNsuld&Metkle-
Archaeodicrynantova Er Siegodyphus T Soc K Gnswold(1987)
Heteropodida*
Oliosd'tana Urn BadumnaCandida Soc 20 K Jackson(1987)
'O{.'.s(n«a.rnianndeti.i !lA;rm BStaedguomdnvpahCuasnsdairdaasinorum TT 'SSoocc 1100 KK JJaacckkssoonn((11998S77))
O. obesulus B. Steeodvphussarasinorum It Soc :: K Jackson(19871
M
vsmenidoe
Iselaokuncaiui Di AUotheleterreth F Sol K Ciriswold(19S5i
KtUfuitntpiitiiui Di Thelerfwriskanclii F K Coylcetal.(1991)
Mysmenopsisarcheri Ph T K Baptisa(l988)
M.copue Ar Cvrfophora O K Baert(1990)
M citlrelicotu Di K Coylee-la/.(1991)
M.cienga Ar Cyrtophora (.) K Baert(1990)
M-dipluroamiga Di Diplura s K Vollnllh(1978)
M.furfiva L5 J_Di Jschnothelexera T Sol 14 K Coylcetal.(1991)
M.gamboa Di Dipiun S K Vollralh(1978)
!
M.hauscar Di K Co\\celat(1991,1
-
M- isthnamigo Di Diplura S K VolIrath(I97H)
M.monticata Di IsclmoiheUsp. T Sol 4 K C(1o9y8J9)e&Meigs
M-pachacutec Di K Coy]cetal.(1991>
M palpatis Di K Coylcc(at l 1991i
M tibialis Di K Coylecfa/.II99D
M.<p- indet. Di hchnothelereggae K Coyte«a/.(l99l)
Qndapidac
Ootwpspukher >2.0 | 1.5 |Am Amanrobinsfenestralis 8 |T |k Briitowe(I95S3
SaUicidAe
Sinmeihapaetuta 7 7,0 Am BadtunnaCandida Soc KP Jackson(1985)
Symphvlognathidae
Ofrirttapuabaxano ] 3 1.3 1Di Diplurasp. 140 |S Sol K VoHraihi 1978)
Theridiidae
Ag Cambridgeasp. F Sal KP Whiiehuuse(1988a)
antipodianus
A.antipodianus Ag Stipiudion !" Sol KP Wmiehouscl1988a)
A.antipodianus Am Badumnatonginquus Sp Sol KP Wh)ieboiiscll9KKai
A.antipodianus I Ar Araneuscrassa Sul KP Whnehou5e(19SSa)
A.antipodianus fi Ar Lriopharanustulosi. 13 Sol KP Whiiehou^ei l9SKa)
A.unfipudiatms Ar Cvclosatrilobata 8 o Sol KP V.Iiiiehousei >9S8aj
A. antipodianus Ar hcucaugcdromedoria o Sol KF Whitehousel1988a)
A.(uUipodiantts Ph Phafcusphalangioides SP Sol KP Wbi(ehouse(T988a,l
A.antipodianus Td Achaearanea T Sol KIJ Whitehousc(1988a)
A.antipodianus 3 : s ... Cyrtophorafurta !: O Sol K mgzierat(1983)
-Vantipodianus 3,0 2-5 \r Septulaeduhs 21 O Agg K Elear(19B»j
INTER-SPECIFICASSOCIATIONS 415
Bodysize Host Guests Assoc*
Kleptoparasitictaxa 6 v Family Species Size Web Social perweb Source
A.argyrodes Ar ' Cyrtophoracitricola O K Vollrath(1984)
A.atopus 2.4 3.4 Ar Nephilaclavipes 25 O Agg 5 K Vo!!rath(1987)
A.attenuatus 17.0 9.3 none Eberhard(1979a)
A.baboquinari 3.7 3.5 Td Latrodectus T Sol K Exline&Levi
(1962)
A.baboquivari 3.7 3.5 Ul Philoponellaoweni 6 O Agg KP SmithTrail(1980)
A.cancellatus 3.2 3.8 Ag Agelenopsis F K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ar Argiopeaurantia 22 O K Exline&Levi
(1962)
A,cancellatus 3.2 3.8 Ar Araneusstrix O K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ar Mecynogealernniscata O K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ar Metepeiralabyrinthea O Sol K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ar Nephilaclavipes 25 O Agg K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ar Verrucosaarenta 9 O K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Li Frontinellapyramitela 4 S K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Ph Pholcus space Sol K Exline&Levi
(1962)
A.cancellatus 3.2 3.8 Td Theridiontepidariorum 7 T K Exline&Levi
(1962)
A.caudalus 3.1 3.9 Ar Argiopeargentata 16 O Sol K SmithTrail(1980)
A.cochleaforma 2.7 3.7 Ar Argiope O K Exline&Levi
(1962)
A.cochleaforma 2.7 3.7 Ar Gasteracantha O K Exline&Levi
(1962)
A.colubrinus 25.0 none Eberhard(1986)
A.cordillera 3.6 3.1 Ar Gasteracantha O K Exline&Levi
(1962)
A.cxlindratus Ar Araneusventricosus O Sol K Shinkai(1988)
A.dracus 2.3 2.6 Ar Nephilaclavipes 25 O Agg 5 K Vollrath(1987)
A.elevatus 3.4 4.0 Ar Argiopeargentata id 4 K Vollrath(1979)
A.elevatus 3.4 4.0 Ar Gasteracantha o K Exline&Levi
(1962)
A.elevatus 3.4 4.0 Ar Nephilaclavipes 25 o Agg 5 K Vollrath(1979
A.fictilium 10.0 5.0 Ar Araneus o KP Exline&Levi
(1962)
A.fictilium 10.0 5.0 Li Frontinellacommunis 4 s Agg KP Wise(1982)
A.fictilium 10.0 5.0 Ul Philoponellaoweni 6 Agg KP SmithTrail(1980)
Exline&Levi
A.fictilium 10.0 5.0 none
(1962)
A.fissifrons 7.0 Ag Agelenalimbata 16 F Agg 2 KP Tanaka(1984)
A.fissifrons 7.0 Lin Linyphia s KP Tanaka(1984)
A.fissifrons 7.0 Td Theridionjaponicum T KP Tanaka(1984)
A.fissifrons 7.0 Ul Philoponellasp. 3 O Agg 3 KP Elgar(persobs)
A.fissifrons 7.0 Ul Uloborusvarians KP Tanaka(1984)
A.flagellum none Eberhard(1986)
A.globosus 2.3 2.3 Ar Nephilaclavipes 25 o Agg K Exline&Levi
(1962)
A.incisifrons Ar Cyrtophorahirta 14 Sol K Elgarera/.(1983)
Table continued
1.
C
416 MEMOIRS OFTHEQUEENSLAND MUSEUM
Table 1. continued
Kleptoparasitictaxa B6odysiz9e Family Species Host Size Web Social Gpeureswtesb Assoc4 Source
A.incursus 3.8 2.2 Td Achaearaneamundula 6 T Sol 5 KP G(1r9a8y9)&Anderson
Exline&Levi
A.longissimus 24.0 19.0 none (1962)
A.miniaceus Ar Nephilamaculata 43 O K RRoobbiinnssoonn(&1973)
A.nephilae 1.7 2.2 Ar Argiope O K (Ex1l9i6n2e)&Levi
A.nephilae 1.7 2.2 Ar Cyrtophoramotuccensis 19 O Agg K Berry(1987)
A.nephilae 1.7 2.2 Ar Gasteracantha O K (Ex1l9i6n2e)&Levi
A.nephilae 1.7 2.2 Ar Neoscona O K (Ex1l9i6n2e)&Levi
A.nephilae 1.7 2.2 Ar Nephila O K (Ex1l9i6n2e)&Levi
A.nephilae 1.7 2.2 Ar Nephilamaculata 43 O K RRoobbiinnssoonn&(1973)
A.pluto 3.9 3.7 Ar Argiopeaurantia 22 O K E(x1l9i6n2e)&Levi
A.pluto 3.9 3.7 Ar Metepeiralabyrinthea O Sol K Exline&Levi
(1962)
A.pluto 3.9 3.7 Td Latrodectus T Sol K (Ex1l9i6n2e)&Levi
A.proboscifo 2.6 2.9 Ar Gasteracantha O K (Ex1l9i6n2e)&Levi
A.projiciens 4.0 3.2 Ar Metazygiasp. O Sol KP Eberhard(1986)
A. sp.A Ar Nephilaclavipes 25 O Agg 2 K Rypstra(1981)
A. sp.B Ar Cyrtophoramoluccensis 19 O Agg KP Lubin(1974)
A. sp. Ar Gasteracantha O 23 Vollrath(1981)
A.subdolus 2.6 2.8 Ul Philoponeilaoweni 6 O Agg K SmithTrail(1980)
A.trigonum 4.2 2.5 Ag Agelenalimbata 16 F Agg KP Suleretal.(1989)
A. trigonum 4.2 2.5 Ag Agelenopsis F E(x1l9i6n2e)&Levi
A. trigonum 4.2 2.5 Ar Mecynogealemniscata O KP Wise(1982)
A. trigonum 4.2 2.5 Ar Metepeiralabyrinthea O Sol KP (L1a9r8c5h)er&Wise
A.trigonum 4.2 2.5 Lin Linyphiamarginala 5 S KP E(x1l9i6n2e)&Levi
A.trigonum 4.2 2.5 Lin Nerieneradiata 5 S Sol KP L(1a9r8c5h)er&Wise
A,trigonum 4.2 2.5 Td Latrodectus T Sol E(x1l9i6n2e)&Levi
A.trigonum 4.2 2.5 Td Theridionzelotypum 4 T KP Exline&Levi
(1962)
A.trigonum 4.2 2.5 Lin Frontinellapyramitela 4 S KP Suterera*.(1989)
A.ululans 4.0 3.7 Ar Nephilaclavipes 25 o Agg K Exline&Levi
(1962)
A. ululans 4.0 3.7 Td Anelosimuseximius T Soc K Cangialosi(1990a)
Exline&Levi
A.weyrauchi 4.3 3.8 none
(1962)
Twocategoriesofrelationship('Assoc')aredefined: 'K' isKleptoparasiteonly,and 'KP' means thattheguest
may alsocapturethehost. Some speciesofArgyrodesmay be incorrectly categorised as 'Kleptoparasite only
becausetheirpredatory behaviourhas notyetbeenobserved.
Taxonomy ofArgyrodesfollows Levi and Exline (1962) and thusArgyrodes,Ariamnesand Rhomphaeaare
notdistinguished.
.
INTERSPECIFICASSOCIATIONS *11
Bodylength! thatalso prey on theirhosts ITable 2). How
kJcptoparasilc Uepiupjrasite tstatistic males of these two groups of species are not
only 3ndpredaior significantly different in body size (Tabic 2).
¥ Argyrfhies 1,M±I»-2(14) 5.0±1.1(6) 9.41** Argyrodesthat-prvyon theirhosts also specialise
A Argyroses 3.2+0.2TM) 3.7+0.4(5) 1.21 on smaller hosts, compared with the size of the
Dimorphismi.d/v) J M+fiOSfH) |u.82±0.I4<5) 2.5H* hosts ofthose species ofArgyrodesthat are only
ti<81 21.5±2.6 6.7+0.S(5i 3.47*• kleptoparasites {Table 2). These compar.
datashow that,aspredicted,ihedifferenceinsin-
TABLE2: Differencesinkleptopaiasiteandhostbody between Argyrodes and its host is greater for
length according to whetherihe kleptuparasite does
those species that are primarily kleptoparv;
lvoarlduoeessaxneotmaeNaonplernegythosn t±heSirEh(ossta-mplesizes), Values compared wiih those that are also predatory.
comparedusingl-test withpooledvariance. Average Thesecomparativedatasuggestthatselectionhas
hostbodysizemeasureswereobtainedfor,4rgyrodes either favoured larger body size for species ihai
thathavemultiplehosts. *p<0,05; ** p<(Mm are bothkJeptoparasitic and prey on their hosts,
ofithasfavouredafurtherreduction inbody size
andJackson, 1986:Jacksonand Hallas, 1990) A inthose speciesthatarcprimarilyklcptopara
potential cost ofthis foraging strategy isthat the The laHer argument is consistent with the
Meptoparasitc may become prey to the host At that kVcploparasitrsm is a specialised foraging
one host specie*:- has a relatively effective strategy that evolved from a more general klep
defensive behaviour: when the predatory Ar- toparasitie and predatory lifestyle (VollratL
>!i:\ is detected- the host simply cuts the web 1984).
thereby collapsing it and ensuring that the Theevolutionarysequenceleadingtothedi
predator cannot proceed further (eg, Eberhard.
genee of these two foraging strategies within
1979bm)i,teSiuatcearnetdiasicr(i1mi9n8a9t)erbeepotrwteetnhaetofnespmeacliefihc Argyrodes is not known; oi>e may have evolved
males, prey items and predatory A. trigonum, a cotmhemootnher,woerbb-obtuhimldaiynhgavaendcievsetrgoerd '
apparently using chemical cues, and respond jc- |
cordingjy. Whitehouse, 1986). Thus, it is not possible,
without an accurate phylogeny. to establish
whether selection has favoured an increase in
COMPARATIVEPATTERNS WiltllNAftGr/t.OOiS body size with the predatory- lifestyle, or a
What evolutionary sequences arc responsible decrease in body size is associated wiih a klcp
tor the diversity of predator)' specialisations hi toparasitie lifestyle. Indeed, the species placed
Argyrodesl Smith Trail 11080) stresses the im- within the single genus Argyrodeshy Exlineand
portanceofthekleptoparasites' ability toidentify Le\ 1 1 1962)havebeenplacedbyothersintothree
the vibratory signals generated by the host, thus genera; the Annnmes, the Rhomphaca. and the
allowingthemtostalkandsafelycapturethehost Argyrodes. In this classification, the Ariamncs
However, kleptoparasites that also attempt to and Rhampluu-a groups arc primarily fl
capture their hosts nsk being captured the? ' predators and the Argyrodes group are klcp-
ves. Consequently they may be more likely to topar (Whitehouse, 1987) Thus, the
attempttocapturevulnerable hosts,suchasthose differencesdescribed above may be confounded
that are smaller (e.g. Smith Trail, 1980; Larcher by taxonomic associations (sec below) Resolv-
and Wise, 1985). moulting (e.g. Vollrath, 1984). ing some ofthese issues is most likely achieved
ven the spiderHnp.s of the host by experimental manipulation of individuals
Whiterrouse, 1986. within a species that shows both kleplopar
and predatory behaviour.
Ifrelativebodysizeisimportantindetermining
theoutcomeofattackingthe host, then predatory An additional pattern revealed by comparative
speciesofArgyttufesiiiaybelargerthanprim analysis also deserves experimental ioveslign
kleptoparasitic species,orthe fi aytend to Hon. Thedegreeofsexual size dimorphism(male
specialiseon smallerhosts. Thesepredictionsare lenguVfemak length)eovaries significantly with
supported by comparative data of body length ihe foraging strategics ofArgyrodes, Males are
measures for20 species o\ Argyrodes (see Tabic smallerthanfemalesinthose speciesthatprey on
I). Species ofArgyrodes were divided into two theirhost, consistent with patternsofsize dmuu
gioups.accordingiowhethertheypreyedontheir phisminalmostallotherspidersIe.ij. Elearetat..
hosts: females elArgyroses that are only klep- 199CV; Elgar, 1991, 3992; Vollrath and Parker.
toparasitic are significantly smaller than those 1992). However, males of those species of Ar-
'
418 MEMOIRS OFTHEQUEENSLANDMUSEUM
Hosttaxa |Kleploparasite* Biology Hostrange
Ageienidae Kleptoparasite Kleptoparasite tstatistic
ACgatenlberniadg(2e)a,,ASgteilpehniodpisotns, Argyrodes(4) KP No.species* only 18 andpredat6or
Amaurobiidae Family 1.6±0.3 2.8±0.7 ] 89
Badumna(2) ASrimgayertohdae,s KK Species 2.7±0.7 3.5±1.3 0.57
Amaurobius Oonops K
Araneidae TABLE 4: Mean host-ranges of Argyrodes that are
eitheronlyprimarilykleptoparasiticortheyalsoprey
ACryartnoepuhso(r5a),(A2)r,giGaosptee(r4a)c,aCnytchlao,sa, on theirhost.* referstoArgyrodes.
Leucauge,Mecynogea,Metazygia, Argyrodes(18) KP
Metepeira,Neoscona,Nephila(3), ofArgyrodes. Itis likelythatbothhost-rangeand
Verrucosa parasite-range will expand as more records be-
Cyrtophora Mvsrnenopsis(2) KK comeavailable. Incontrast, many species appear
Dipluridae to be host specific, with one species of klep-
Allothele Isela K toparasite recorded from the web of only one
Diplura,Ischnothele Mvsrnenopsis KK speciesofhost. Forexample, incertainPeruvian
(U) habitats,Argyrodes ululans is found only on the
Diptura Cuhmagua K webs of the social spider Anelosimus eximius,
Thelechons Kilifia K despite considerable effort searching for this
Linyphiidae kleptoparasite on other potential hosts (Can-
Frontinella(2),Linyphia,Neriene Argyrodes(4) KP gialosi, 1990a).
Phulcidae
Vollrath (1984) argued that Argyrodes can be
Photcus Argyrodes(2) KK placed in two general categories; specialists that
Pholcus Mysmenopsis K
arehost specific butbehaviourally versatile, and
Theridiidae generaliststhatinvadethewebsofmanydifferent
AAncehlaoesairmaunse,a,LaTthreordiedcitouns(3), Argyrodes(7) KP species but use relatively few techniques to ob-
tain food. Thus, Whitehouse (1988a) considers
Uloboridae
Argyrodes antipodianus a specialist, primarily
Uloborus,Philoponella Argyrodes(4) KP because its behaviour is versatile, and adults are
found primarily on the webs of Eriophorapus-
TABLE 3: Summary of taxonomic distribution of tulosa. Dichotomies likethesecanbemisleading
spiders that arc host ofkleptoparasites (see Table 1 because both host-specificity and behavioural
for further details). KP= Kleptoparasites and versatility are most likely continuous ratherthan
predators; K=kleptoparasites. * No. species in each
genusinparentheses. discretevariables;A.antipodianusisfoundonthe
webs of several other hosts (Table 1). Further-
gyrodes that are primarily kleptoparasitic are more, host-specificity may also vary between
generally larger than their conspecific females populations, depending on the diversity and
(see Table 2). What factors are responsible for abundanceofpotential hosts in differentpopula-
this reversal of size dimorphism patterns within tions. For example, A. antipodianus in
this group of spiders? One explanation is that Whitehouse's (1988a) study may be found
competitionbetweenmalesforaccess tofemales primarily onEriophorapustulosabecausethatis
may be more intense for kleptoparasitic spiders, the most common host in her New Zealand
and consequently sexual selection has favoured population.
large male size in these species (see also The hostrange ofArgyrodesmay vary accord-
Whitehouse, 1988b).
ingto whetherthe species isbothkleptoparasitic
Thereisconsiderablevariationinboththenum- and predatory or whether it is only klep-
ber of species that are host to each species of toparasitic. Purely kleptoparasitic Argyrodes
kleptoparasite and the number of kleptoparasite may escape host-detection through specialised
species found oneach web-buildinghost species behaviours, but these behaviours may be effec-
(see also Vollrath, 1984, 1987b). For example, tiveforrelativelyfew hostspecies. Ifso, thehost
Argyrodes cancellatus are found on the webs of ranges of primarily kleptoparasitic Argyrodes
at least ten different host species from five maybelessthanforspeciesofArgyrodesthatare
families (see Table 3), while the orb-weaver also predatory. The comparative data provide
Nephila clavipes is host to at least seven species little support for this prediction (Table 4); al-
INTERSPECIFICASSOCIATIONS 419
though the host-range of primarily klep- described aJlopatricIschnothelemorphsthatalso
tnpaiasitic species is less than the range of appeartobe sisterspecies. Third, diplurids may
predatoryspecies,thedifferenceisnotstatistical- be more sensitive to web invaders than thehosts
ly significant. of Argyrodes* and thus the kleptoparasitk be-
Theresults ofthese inter-specific comparative haviours required to avoiddetection by one host
analyses within the genus Argyrodes should be species are not appropriate for another. In this
interpreted cautiously. These patterns may be regard, it is noteworthy that Argyrodes are not
confounded by an association between foraging known to invadedipluridwebs,despitethetH
strategy andtaxonomicaffinity, and thus thedif- taxonomic range oftheirhosts.
ferencesinbodysizeorhost rangemay be dueto The relatively permanent nature of the host's
Other,unknownfeaturesthatdifferbetweenthese web isacommoncharacteristicofthehostsofall
twogroups.Thispossibility isespecially relevant klepioparasites (Table I) Kleptoparasites that
given the ambiguity of the taxonomic arrange- liveonpermanent webs maybenefitbyspending
mentofthis genus. Furthermore, somespeciesof less lime searchingfornew webscompared with
Argyrodes may be incorrectly assigned to thosethatareassociatedwithhoststhatfrequent-
primarily kleptoparasite status simply through ly move their webs However, it may not be the
lack of observations. Thus, the patterns may permanent structureoftheweb thatisimportant,
change when more data and/or a more accurate but rather the tenacity of the web site. For ex-
phylogeny become available. Nevertheless, the ample, the large, nocturnal, Australian orb
mssuggestseveral interestingquestionsthat weaverEriophoratransmarinabuildsanewweb
could be resolved by an experimental approach every evening and then destroys itthe following
dawn. Despite the temporary nature of its web,
TSPBCJRCm OFK1EPTOPARASITH5 this spider is alsu hosi to many individual Ar-
Both Argyrodes and Mystnenopsis belong to gyrodes,(prMobably because it has a high web-site
tenacity Hcrbcrstcin. unpublisheddata)
web-building families and thus are relatively
e phylogenetically (Coddington and Levi,
MIMICRY BY SPIDERS
1991). However, the range and taxonomic af-
finities of their hosts are substantially different
1 hie i).Argyrodeshave been recorded on the Many species of animals, including spiders,
webs of 29 host genera from eight families resemble other, unrelated species. These
(Ageienidae, Amaurobiidae, Araneidae, resemblances may be visual, chemical, be
Linyphiidae,.Pholcidae.PsechridacTheridiidae. havioural oracousticand are usuallyreferred to
UJoboridac), and some species have many hosts as mimicry. There are many different types H
• sre above), in contrast, !! ofthe 14 species of mimicry,whwrhhasprccipitaiedsomecontra
Mystnenopsis are found on diplurid hosts, with syover itsdefinition (e.g. Endler, 1981; Pasteur.
the remaining species found on Cyrtopltora 1982). Two general forms ofmimicry axe di
(Araneidae) and Pholcus (Pholcidae). A com- guished in this review: defensive mimicry and
parativeanalysisrevealsa significant difference; aggressive mimicry. In the former, the mboetfc
every species ofMysmerwpsis has only one host form is presumed to have evolved because the
species, while thehostrange forArgyrodesis2.7 risk ofpredation (or parasitism) on the mimic bfi
<±0.7. n*l*) species, or 1.6 (±0.3) host reduced as a resuJt of IIS resemblance to the
families. model. The lower mortality occurs because the
Why is Mystnenopsis more host-specific than receiver (the predator) does not usually prey on
Argyrodes? There are several possible explana- the model,andfails to distinguishbetween it and
tions. First, kleptoparasitism may have evolved the mimic. Aggressive mimics resemble some
morerecentlyinMysmenopsisthan inArgyrodes, feature o{ (heir prey species thereby increasing
and therefore the former klcptoparasitc has had the chance of capturing the prey model. Both
Ie3$ time to expand its host tangc. Second, the forms of mimicry occur in several families of
present associations between Mysmenopsis and spid:
dipllifids may have evolved from a common an- The relationship between mimic, model and
cestor and subsequently spcciatcd as host/klcp- receiver is asymmetric; only the mimic benefits
toparasitepairs. Consistent will)this isCoyieand and any improvement in the mimic will be
Meigs(1989)descriptionoftwosisterspeci favoured rapidly by natural selection. Both the
kleptcparasttes (Mysmcrt</f»i.y ntomicola and M. model and the receiver may lose, in defensive
furtiva) that live on the webs of a pair of tin- mimicry, through increased attack rate and lost
i j
420 MEMOIRS OFTHEQUEENSLANDMUSEUM
Spider(axon Afit Taxa i V.UTll
Fain Subfamily Species
Caxtianeiradubium CI Ponerinae Pachxcnndvhobscuricornis Reiskind(t977)
Mazaxpax Co Ponerinae Ectatommaruidum Reiskind(l970)
Mvrmeciumbifaxciatum Co Formieinac Ctunponntusfemoratus OHveOT([988)
Myrmeciumbifusciatum. <„ Mvmucinae Megalomyrmexmodesfa OhvcirafWS81
Myrrnt'OU-i Cn Ponerinae Pachxcoodvlaunideniata OftveirH<l988]
Mvrmeciumvelulutum Co Ponerinae Ectatommalugens Dimmil i'-'"';-
Myrtnecorypaxcubanas Co Formieinac Camponotusplanatus MyersandSail(1926) —
M\rmeiot\pusfuligmosux Co Forrnicinae Camponotusplanatus Jackson&Dnininumd1.1974)
Myrmecotypairettenmeyert Cn Fonnieinae CamponotussericeWeturis Reiskind(l977)
Sphecoivpusrtiger Co Ponerinae Pacfrvcotidvlavilloxa Olivcira(!988)
Micariapulicariu Gn Myrmicmac AcurUhomyrme.xniger Bristowfl(l958j
Micaria:.p. Un Myrmiemae Aphaencgasterbeccarii HingMon(l927)
Micariascintillans Gn Rormicinje Formicafusca Hristowe(19411
Phrurolithusfestivus Lio Formieinac Lasias*N>'r Bnslowt i 1941 i
Phrurelithusminimus Lin Forrnicinae FormicaJttxia Hri\Mwc(l94I)
Mariettafurva Sa Forrnicinae Camponotusbrevis Rcisiund(1977)
ANT
MIMICRY Mariettafurva Sa Formieinac Campanulasfastigams Reisttjnd(1977)
ONLY Mvrmarachnee}vn$ota Sa Pseudomvrmecinae Tftruponeraanthracina Edmunds1.1978)
Mxrmaruchnvfoetuses Sa htnnicinae Qecophvllalongwoda Fdmundsi 1978)
Myrmarachneforrmraha Sa Formieinac Formicarufa Bris1owe(194l)
Mxrmaruchntlegpn Sa Forrnicinae Camponolusacvapimensh Edmund*(1978)
Mvrmarachn?lupala v. Forrnicinae Polyrhachis Jackson(1986'i
M'vftnurachneparalUta Sa Ponerinae Pachxiondylacaritmlata Reiskind(1977j
Mvmuirachn%'paraileio Sa r'vwrmac j'utvlttstriatinodis Rciskmd(1977)
Mymmrachneplataleotdes Sa Fonnicmae Ocropbyilasmaragdina Maihcw(I954l
Myrmarachnesp. ij Forrnicinae Foivrharhissimplei Hingslon(I927)
Myrmarachnesp. Sj Fonnieinne Prrnolepislongicornis Minpsion0927)
Mvrmarachnes^ Sa Myrmlcinae ioteindica UfngstOn(192-7)
'., -.',.. Sa Forrnicinae Cft'npt'KOiUipUivanv; .lavkson._ Dnimmond i 1974
S\naj,'eh's:otxidenuilis Sa Fonivianae Myrmicaemetiauui Cullcr(l99M
SvnagelestwiJentidts Sa Forrnicinae LasiusaUenus Cmlcr(199J)
Syiuinelftvettdior Sa Forrnicinae LashlSniger l:iigelhaidniJ970)
Svnemosvna>;p Sa PseudontyntiActnae PsetuU'tnvrmexme.xicaiui'j ReiskJnd»1977)
S\aemosynaamericana Sa Psendomynnevmac Pseudomvrmesboapis R.;i;l-in-m97;i
Synemosynaauratitiacti Sa Pseudomvrmetinae Fseudnntyrmes OIiveira(]988)
Synemoxynasmithi Sa Pscudumymieeinae f'yruihjmyrrtuivlo'i^ma MyersandSail(1926)
Sytiemoxvnasmithi Sa Psciidoinvrmccinae PseMdomymuiJlaiiitu MyeisandSail(1926)
Zunieataeta Sa Formicinac Camponotusfemoratus 01ivdra(l988)
Zunigamagna Sa Ponerinae Pachvcotutylaviltosa 0]ivcira(J9S3,)
Altuteafbffmcaria n\ Mvnnicinac Cheianercroccenentre RcisltindandLevi(1967)
Dipoenu |Td MyrnVicinac Pheidoleindica Hinpston(1927)
TABLE5(part).Taxonomicdistributionofspidersthatmimicants,includingthosethatalsopreyon themodel,
* spiders observedwithdeadants.Family abbreviationsgiveninTable 1.
foodrespectively (see Endler. 1991), and natural ves will depend upon the benefits to the mimic
selection will favour models that have less and the costs ofmimicry to the model. The costs
resemblance to the mimic (although the strength to the model in aggressive mimicry are more
of this selection will depend on the frequency complicated,anddependuponwhetherthemodel
with which the model is attacked) Thedegreeof and the receiver (in this case, the potential prey)
resemblancebetweenmodel andmimicthatcvol- isthe same individual.
