Discrimination and Release of Unpalatable Butterflies by Nephila

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Discrimination and release of unpalatable butterﬂies by Nephila clavipes, a Neotropical orb-weaving spider

Article in Ecological Entomology · March 2008 DOI: 10.1111/j.1365-2311.1984.tb00857.x

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João Vasconcellos-Neto Thomas M Lewinsohn University of Campinas University of Campinas, Campinas, Brazil (UNICAMP)

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Discrimination and release of unpalatable butterflies by NephiZa davipes, a neotropical orb-weaving spider

JOXO VASCONCELLOSNETO and THOMAS MICHAEL LEWINSOHN Departamento de Zoologia, Universidade Estadual de Campinas, Brasil

ABSTRACT. 1. Nephira clavipes (L.), a common spider in neotropical forests, discriminates some unpalatable prey and releases them unharmed from its web. Release is not accidental but results from a specific behavioural sequence. 2. Field trials with twenty-seven butterfly species showed that spiders respond consistently to butterfly species and higher taxa. Ithomiinae and some Danainae are almost always released while Heliconiinae, Nymphalinae, Acraei- nae, Pieridae and Papilionidae are usually eaten. 3. Paired tests showed that an immediately preceding experience with a different butterfly did not reveal any change in the spider’s usual response to a particular butterfly. 4. Warning coloration is not involved in spider response. Spiders rejected the models but ate the mimics of two different butterfly species pairs. Distasteful- ness is probably signalled by chemical cues. 5. Some unpalatable butterflies stay motionless when entangled and while the spiders release them. Motionlessness in webs seems to be a requisite to allow recognition of their distastefulness without being bitten by the spider. 6. Spiders differ from vertebrates in the prey accepted and in rejection mechanics. Although there is no indication of learning, spiders may select butterflies for distastefulness, chemical signals and motionlessness, at the individual level.

Key words. Butterfly, Ithomiinae, Heliconiinae, spider, Nephila, unpalatibifity, predation, prey rejection, prey release, thanatosis.

Introduction the experimental evidence provided for a The discrimination and rejection of unpalat- predator’s ability to discriminate and avoid able prey is a necessary condition for the evo- unpalatable prey stems from studies of lution and maintenance of aposematism and vertebrates, particularly birds (Brower & mimicry. Both of these phenomena are Brower. 1964 and references therein; Cop- classical problems for population ecology and pinger, 1970; Wiklund & Jarvi, 1982). Such genetics, and therefore the pattern of preda- studies emphasize a predator’s ability to tor responses to different prey has been ex- recognize and selectively reject brightly tensively investigated and discussed (Fisher, coloured prey. It is therefore commonly 1930; Brower, 1958; Curio, 1976). Most of held that the advertisement of unpalatability evolved to a large extent towards visual Correspondence: Dr Jolo Vasconcellos-Neto, Depto. Zoologia - UNICAMP, C.P. 6109, 13.100 signals directed at vertebrate predators, who Campinas. SP - Brazil. use colour vision, learning and memory when 337 338 Joio Vasconcellos-Neto and Thomas Michael Lewinsohn selecting prey. By contrast, arthropod pre- into a N.clavipes web in Sumard, State of dators are often considered unsuitable as Sao Paulo, Brazil. Instead of biting the butter- selective agents due to their restricted learn- fly, the spider released it alive from the web, ing capacity and apparent low prey discrimin- allowing it to fly away (Vasconcellos-Net0 & ation (Edmunds, 1974). Lewinsohn, 1982). In other webs we found Studies of arthropod predaceous behaviour remains of eaten butterflies, including several have focused mainly on mantids (Marshall, species considered to be aposematic, parti- 1902; Shelford, 1906; Gelperin, 1968) and cularly Heliconiinae and Acraeinae (Brower & spiders (e.g. Marshall, 1902; Shelford, 1906; Brower, 1964). These observations led us Bristowe, 1941; Tyshenko, 1961) and have to investigate whether N.clavipes discriminates shown them to be capable of discriminating consistently among lepidopteran groups or unpalatable prey. Nonetheless, according species, preying on some and rejecting others, to all of these studies rejected prey are usually and also whether the releasing behaviour of severely damaged or killed, except for this spider is occasional or occurs regularly

dangerous prey like reduviid assassin bugs toward certain prey species. ‘ (Shelford, 1906). If rejected prey are in- deed seriously damaged or killed, discrimination alone does not allow these predators to be considered as selective agents for un- Methods palatability or aposematism. A number of observations have been re- Observations and experiments were carried ported on the predatory habits of common out in the field, mostly in the Horto Florestal tropical spiders in the araneid genus Nephila of Sumarb, with additional observations in and its close relative Nephilengys. Belt (1 888) the Santa Genebra Forest, Campinas, and in mentions an unidentified Nephila in Nicar- the Serra do Japi, Jundiai; all of these are agua which dropped heliconiine butterflies in the state of SB Paulo, Brazil. Field work experimentally placed in its web. The rejec- was conducted from March to May in 1981 tion of noxious insects has also been des- and 1982, these being the months of maxi- cribed for Nephilengys malabarensis Walcken- mum abundance of female adult spiders with aer in South Africa by Marshall (1902) and large recently built webs. for Nephila maculata (Fabricius) in Borneo The main field experiment consisted of (Shelford, 1906) and in New Guinea (Robin- recording the responses of spiders to dif- son & Robinson, 1973). All of these report ferent butterfly species. Adult butterflies that rejected insects are usually maimed ot were caught with an insect net in the vicinity killed by the spiders. However, Eisner (1982) of the webs, not more than 30min before describes the unharmed release of the arctiid each trial, and were kept alive in a cage or moth Llfetheisa ornatrix (L.) from Nephila in the net itself until used. Each trial con- clavipes webs. Eisner also demonstrated ex- sisted of tossing a live butterfly into a Nephila perimentally that release is due to pyrrolizi- web, on the side opposite to the spider, and dine alkaloids which this moth incorporates recording the behaviour of both spider and from its Crotalaria host-plant. butterfly. The web was watched until the Nephila clavipes, a common and widely spider finished feeding on the butterfly or distributed neotropical spider, builds its or- discarded it either dead or alive. According bital webs mainly in forest gaps and corridors to the spider’s behavioural response the which are usual flying routes for insects. result of each trial was recorded as (butterfly) It commonly preys on flies, bees, wasps and ‘eaten’, ‘rejected’ or ‘released’. Further small moths and butterflies. Its predatory details on these categories are given in Results. behaviour has been described in detail by Butterfly behaviour was also noted with re- Robinson & Mirick (1971), who however gard to its movements immediately after do not mention discrimination among prey getting entangled and also while the spider by this spider. approached and handled it. All trials were In August 1976 we observed a Mechanitis conducted between 08.00 and 13.00 hours and polymnia (L.), an ithomiine butterfly, fly timed with a stopwatch. Discrimination of butterflies by Nephila 339

Different spider individuals were employed to the butterfly (Fig. lc) and finally dropped for each trial, except for a further experiment it from the web (Fig. Id). Most released designed to examine whether prior butterflies resumed normal flight before experiences influence the spider’s response hitting the ground. pattern. In this experiment we presented We performed 149 trials with twenty- sequentially a heliconiine and an ithomiine seven species of butterflies, which showed to the same spider, each of them being offered consistent responses of Ndavipes to the first in half the trials. A minimum interval of butterfly species offered (Fig. 2). Butterflies 30 min was maintained between the moment of the same subfamily induced similar res- the .spider abandoned the remains of the first ponses but there were clearcut differences butterfly or released it, and the presentation in the responses to distinct subfamilies. In of the second. the fourteen species of Ithomiinae there oc- Remains of butterflies spontaneously eaten curred ninetyseven releases and ten rejec- by N.clavipes were collected for identification tions against three eaten. In Danainae, the whenever found in or directly under the webs. six Danaus gilippus (Cramer) offered were released or rejected, while the single Lycorea cleobaea (Godart) tested was eaten. On the Results other hand, in the five species of Heliconiinae tested, twenty-three individuals were eaten The behavioural responses of the spiders to and only one rejected. The proportions of the butterflies we presented were divided into individuals released or rejected against those three distinct categories: butterflies were eaten are significantly different among these either ‘eaten’, ‘rejected’ or ‘released’. In the three subfamilies (Table 1). In the remaining first case the spider rushed towards the groups, the nine individuals of the seven butterfly, seized it with its two pairs of fore- species tried were all eaten (Fig. 2). legs and bit it protractedly, maintaining its Based on these results, we chose ithomiines, hold until the butterfly was immobilized. The which are commonly released, and heli- butterfly was then pulled out and disen- coniines, which are usually eaten, for the tangled from the web, wound up with silk second experiment in which paired trials were and carried to the spider’s resting place where designed to ascertain if an immediately pre- it was eaten. A butterfly was recorded as ceding experience with one of these would rejected whenever it was bitten by a spider influence the spider’s response to the other. without being eaten afterwards. ‘Rejection’ A total of fifteen paired trials were carried occurred either immediately after the butter- out with four different heliconiine-ithorniine fly was immobilized, by unravelling and dis- combinations: Heliconius erato (L.) x carding it from the web, or less often after Mechanitis polymnia (eleven pairs); H.erato the spider had wrapped and carried the X Hypothyris ninonia (Hiibner) (two pairs); butterfly and started feeding on it. In the Heliconius ethilla (Godart) X M.polymnia (two latter case, the butterfly was either abandoned pairs). In all of these trials the spider ate the in the web or discarded. In the ‘releasing’ heliconiine and released the ithomiine, what- response, the butterfly was freed alive and ever the order of presentation. In an addition- undamaged by the spider (Fig. 1). In a releas- al trial with a pierid (Dysmorphia ostynmne ing sequence, as soon as the spider approached (Dalman)) and an ithomiine (M.po2ymnia) the enmeshed butterfly, the spider seized the first was also eaten and the second it with the two pairs of forelegs, the pedi- released. palps and chelicerae, without however biting Butterflies showed two quite distinct be- it. The spider then touched the butterfly’s haviours when caught in the web. All the thorax and wing bases with its foreleg and Heliconiinae, Nymphalinae, Acraeinae, pedipalp tarsi. After this, the spider started Papilionidae, Pieridae and some of the carefully to unravel the butterfly (Fig. la), Danainae struggled forcefully to free thern- pulling it to the opposite side of the web with selves, eliciting a swift spider attack with a chclicerae and forelegs (Fig. Ib). The spider usually long bite. Ithomiinae, on the other cut and removed the silk threads still attached hand, typically remained motionless from the 23 340 Joio Vasconcellos-Neto and Thomas Michael Lewinsohn

FIG. 1. Release of Mechanitts lysimnia by Nephila clavipes. Total releasing sequence lasts approxi- mately 1 min. varying with the buttertly’s size and entanglement in the web. (a) The spider starts to unravel the butterfly. Note the right third leg pulling silk threads off the wing. @) The butterfly is held by the thorax and pulled to the opposite side of the web. (c) The butterfly is freed from the web and the spider removes the remaining silk threads. Note the completely extended posture of the motionless butterfly. (d) The butterfly is dropped and starts to glide with wings and legs still extended before taking off in normal flight. Horto Florestal, Sumarb, Sio Poulo, 23 March 1981 (photos by T. Lewinsohn).

moment they were caught in the web and Although we did not SUNey N.clavipes continued so while the spider touched and webs extensively for remains of butterflies, disentangled them, until they were thrown on several occasions we found identifiable out. remains of eaten individuals. The following Discrimination of butterflies by Nephila 341 species were found: Acraeinae - Actinote Discussion carycina Jordan (seven individuals); Nym- phalinae - Phyciodes lansdorfi (Godart) The trials with various butterfly species show (one), Biblis hyperia Cramer (one); Heli- that N.clavipes discriminates among different coniinae - Dryas julia (Fabricius) (one), potential prey. Rejection or release of a but- Eueides isabella (Cramer) (one), Heliconius terfly does not seem to be particularly ethilla (one); Ithomiinae - Hypothyris dependent on satiation, nor is it influenced ninonia (one); Danainae - Lycorea cleo- by an immediately preceding experience baeu (one); Morphinae - Morpho achillaenus with an acceptable butterfly; conversely, paulista Fruhstorfer (one); Hesperidae - the acceptance of a palatable butterfly is not Urbanus procne Plotz (one); Sphingidae - altered by the previous rejection of an un- Protarnbu2yx strigiris (L.) (two). palatable one. The spider’s responses thus

WYWHALIDAE ITHOMIINAE hietechanitis potymnia 27 Mechanitis lysimnia kclungia satonina Hypothyris ninonia Aeria olena Hypothyris euclea Ithnnia agMsia Nthorea hmmonia Dircennu dero Methona themisto Prit*‘teia hymeMea Epityches eupompe Ptacidula euyanaasa Pssudoacada erruca DANAINAE knaw gilippus Lycorea cteobaea I HELICONIINAE

ACRAZINAE I Actinote carycina NYMPWLINAE Biblis hyperia

PIEBIDAE Diamorphia astynane 342 Jorio Vasconcellos-Net0 and Thomas Michael Lewinsohn

TABLE 1. G contingency tests of trial outcomes with Ithomiinae, Danainae and Heli- coniinae (data from Fig. 2). Other taxa excluded because of low trial numbers, All tests are for ‘Eaten’ against ‘Released’ plus ‘Rejected’. ~~- df G P

1. Subfamily totals (Ithomiinae N = 110, Danainae N = 7, Heliconiinae N = 24) Total 2 96.14 < 0.001 Partitioning: (a) (Ithomiinae + Danainae) X Heliconiinae 1 94.54 < 0.001 (b) Ithomiinae X Danainae 1 1.60 > 0.10 2. Between the ithomiine species* Total 10 8.1 3 > 0.50

* Excluding species with less than five trials (E.eupompe,P.erruca and P.euryanasu).

seem to be determined on a case-forcase Asclepiadaceae, which make Danaus spp. basis. unpalatable to birds (Brower & Brower, Colour patterns do not appear to be 1964; Roeske et al., 1976) are probably involved in the spiders’ discrimination process. also responsible for the rejection or release Our trials included two paired presentations of D.gilippus by Nephila observed by us. with the mimics Mechanitis polymnia and Nonetheless, there is no reason to expect all Heliconius ethilla and a further pair with predators to respond similarly to a given sub- M.po1ymnia and Dysmorphia astynome. With- stance or prey species. Some birds have been out exception the Mechanitis were released observed to feed on danaines and ithomiines, while the other butterflies were eaten. Experi- which usually are rejected, under particular ments with other spiders (Marshall, 1902; conditions (Brown & Vasconcellos-Neto, Bristowe, 1941) also indicated that warning 1976; Calvert et al., 1979). Nephila accepted coloration in itself confers no protection to all but one of the Heliconiinae we offered; butterflies and other insects. by contrast one species of bird, the silver- Spider discrimination among butterflies beak tanager (Rhamphocelus carbo rnagni- seems to depend mostly on chemical signals. rostrir Lafresnaye) rejected most Heliconius Almost all prey items are touched with pedi- erato and Dryas julia as well as other Heli- palps and foreleg tarsi during the fist contact; coniinae (Brower et al., 1963). this palpation is noticeably prolonged on Thanatosis has been noted in ithomiines butterflies which subsequently are rejected and some danaines by Gilbert & Ehrlich or released. Spider tarsi are known to bear tar- (1970) and in ithomiines by Drummond sal organs and other chemoreceptive struc- (1976); however, they suggest no reason tures (Savory, 1964). Palpation probably for death-feigning in these butterflies. Our enables the spider to detect unpleasant or results indicate that this behaviour plays toxic substances in the prey before biting or an essential role in allowing the spider to feeding on it, provided that these substances identify the butterfly as unpalatable without are deposited in the integument or exuded biting it, an interpretation supported by by the prey. observations of a few ithomiiies that strug- The unpalatability of adult butterflies gled strongly against the web, which were to vertebrate predaton has been explained immediately bitten and later rejected. This by the incorporation of toxic compounds happened to all the rejected Ithorniinae (Fig. of their larval host plants (Brower & Brower, 2) except for one Mcclurrgia salonina (Hewit- 1964); such substances may also induce avoid- son) which was rejected after being wrapped ance by spiders, as demonstrated by Eisner up and tasted. The two rejected Danaus gilip- (1982) for the release of Utetheisa ornatrix pus also fought hard to free themselves, by N.clavipes. Cardiac glycosides from being repeatedly bitten until they were Discrimination of butterflies by Nephila 343

immobilized and pulled out of the web; palatable and aposematic prey both at the in- one of these died and the other recovered dividual and the kin level (Benson, 1971; after several hours. In these cases, the spider Harvey & Paxton, 1981). The detailed study bite may be due either to an immediate res- of the discrimination of distasteful prey by

ponse to a prey not yet recognized as un- invertebrate predators should , therefore palatable or to the necessity of subduing broaden our understanding of the evolution these stronger butterflies in order to handle of unpalatability in prey and of its signalling them safely and to prevent web damage. to predators. The predation of some ithomiine individuals (Fig. 2) may involve a lower concentration of deterrent substances as well as differences Acknowledgments in tolerance or hunger level of the spiders. We consider the spiders’ behaviour of We thank W. R. Silva and I. Sazima for sug- releasing butterflies alive and undamaged to gesting the Japi site, K. S. Brown for identi- be a refinement of the simple rejection of fying several butterfly species and W. W. unpalatable butterflies after biting or Benson, I. Sazima, R. Lewinsohn and two tasting them. Butterflies are obviously anonymous reviewers for critically reading favoured by being released alive; since release the manuscript. depends both on unpalatability and motionlessness in the web, such quiescence might be expected to be particularly frequent in References groups such as the Ithomiinae which fly among the undergrowth of closed vegeta- Belt, T. (1888) The Naturalist in Nicaragua. John Murray, London. tion, where there is a high risk of striking Benson, W.W. (1971) Evidence for the evolution of spider webs. Other groups including Danaus unpalatability through kin selection in the spp. inhabit more open areas and would there- Heliconiinae (Lepidoptera). American Nuturnlist, fore have less opportunity to be selected for 105,213-226. Bristowe, M.A.W.S. (1941) The Comity of Spiders, motionlessness in webs. Conversely, the Vol. 11. Ray Society, London. spider itself, by discriminating and releasing Brower. J.V.Z. (1958) Experimental studies of unpalatable prey without killing and wrap- mimicry in some North American butterflies. ping it, is able to save on venom, energy, silk Part I. The Monarch, Danaus plexippus, and Viceroy, Limenitis archippus archippus. Evo- & threads and time (Robinson Mirick, 1971). lution, 12, 32-47. The relatively common occurrence of butter- Brower, L.P. & Brower, J.V.Z. (1964) Birds, butterfly remains in Nephila webs indicates that this flies and plant poisons: a study in ecological spider’s predation on butterflies is not a chemistry. Zoologica, 49, 137-159. sporadic event and thus may represent an Brower, L.P., Brower, J.V.Z. & Collins, C.T. (1963) Experimental studies of mimicry. 7. Relative appreciable selective force in the mainten- palatability and mullerian mimicry among ance of unpalatability in insects. neotropical butterflies of the subfamily Heli- Spiders differ from vertebrate predators coniinae. Zoologica. 48.65-84. as selective agents in two fundamental aspects. Brown, K.S., Jr & Vasconcellos-Neto. J. (1976) Birds and other vertebrates respond to warn- Predation on aposematic ithomiine butterflies by tanagers (Pipmeidea melanonota). Biotropica, ing coloration, which is ignored by spiders. 8,136-141. Although ‘olfactory’ or ‘taste aposematism’ Cahrert, W.H., Hedrick, L.E. & Brower. L.P. (1979) (Eisner & Grant, 1981) may be selected for Mortality of the monarch butterfly (Danaus by spiders, prey motionlessness seems to be plexippus L.): avian predation at five over- at least as important as chemical signals wintering sites in Mexico. Science, 204, 847- 851. in allowing a spider to discriminate among Coppinger, R.P. (1970) The effect of experience prey. Secondly, since released butterflies and novelty on avian feeding behaviour with rarely show any damage from their encoun- reference to the evolution of warning colora- ters with Nephila it is likely that this pre- tion in butterflies. Part 11: Reactions of naive buds to novel insects. American Naturalist, dator will select for unpalatability only at 104,323-335. the individual level and not through kin Curio, E. (1976) The Ethology of Predation. selection, while vertebrates may select un- Springer, Berlin. 344 Jodo Vasconcellos-Net0 and Thomas Michael Lewinsohn

Drummond, B.A., 111 (1976) Comparative ecology Robinson, MN. & Robinson, B. (1973) Ecology and and mimetic relationships of Ithomiine butter- behaviour of the giant wood spider Nephila flies in Eastern Ecuador. Ph.D. thesis, University macularu (Fabricius) in New Guinea. Smith- of Florida. sonian Contributions to Zoology, 149, 1-76. Edrnunds. M. (1974) Defence in Animals. Longman, Roeske, C.N.. Seiber, J.N., Brower, L.P. & Moffitt, Essex. C.M. (1976) Milkweed cardenolides and their Eisner. T. (1982) For love of nature: exploration comparative processing by monarch butterflies and discovery at biological field stations. Bio- (Danaus plexippus L.). Biochemical Intemctions srience, 32,321-326. between Plane and Insects (ed. by J. W. Wal- Eisner, T. & Grant, R.P. (1981) Toxicity, odor aver- lace and R. L. Mansell), pp. 93-167. Plenum, sion and ‘olfactory aposematism’. Science, 2 13, New York. 476. Savory. T. (1964) Arachnidu. Academic Press, Fisher, R.A. (1930) The Genetical Theory ofNatuml London. Selection. Clarendon Press, Oxford (1958 reprint: Shelford, R. (1906) Note on a feeding experiment Dover, New York). . on the spider Nephila maculata. Proceedings of Gelperin, A. (1968) Feeding behaviour of the pray- the Entomological Society of London, 3. LXIII- ing mantis: a learned modification. Nature, LXVI. 219,399400. Tyshenko, U.P. (1961) Ob otnoshenii nekotorykh Gilbert, L.E. & Ehrlich. P.R. (1970) The affinities paukov semistiva Thomisidae K mimkriruyu- of the lthomiinae and Satyrinae (Nyrnphalidae). ohchim nasekomym i ikh modelyam. Vesrnik Journal of the Lepidoptedsts’ Society, 24,297- Leningradskogo Cosudarsfvennogo Wniversfteta 300. (Sedya Biologii). 3, 133- 139. (Abstract in Harvey, P.H. & Paxton, RJ. (1981) The evolution Biologkal Absrmcts seen.) of aposematic coloration. Oikos, 37, 391- Vasconcellos-Neto, J. & Lewinsohn, TM. (1982) 393. Comportamento de NephUa clavipes (L.) (Aran- Marshall, GA.K. (1902) Five years’ observations and eidae) em mlagio a Iepiddpteros: discriminagio e experiments (1896-1901) on the bionomics of rejeisaTo de presas. Cizncia e CU~~UM,34 (Suppl.), South African insects. chiefly directed to the 548. investigation of mimicry and warning coloun. Wiklund, C. & Jprvi, T. (1982) Survival of distaste- Transactions of the Royal Entomological Society ful insects after attack by naive birds: a re- ofLondon. Series V. 281-584. appraisal of the theory of apoaematic coloration Robinson, MH. & Mirick, H. (1971) The predatory evolving through individual selection. Evolution, behaviour of the golden-web spider Nephila 36,998-1002. clavipes (Araneae: Aranaidae). Psyche, 78, 123- 139. Accepted 10 January 1984

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