Kleptoparasitism: a cost of aggregating for an orb-weaving spider

Animal

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Behaviour,

during the second half of the releases.It appears to be an immediate outcome of the treatment itself, probably of traumatic nature. This interpretation is in agreement with the observation that the greater shock of the first treatment resulted in a greater effect, while repeated application of the anaesthetic reduced it. Schmidt-Koenig & Phillips (1978) reported a similar finding. All of this evidence points to a non-specific effect rather than to an effect based on altered informational input. It should be mentioned, however, that this type of non-specific effect was not observed when the local anaesthetic was applied after the birds had been prevented from smelling by plugging their nostrils. In a test seriesin which the experimental birds wore cotton tampons in their nostrils during displacement and while waiting at the site, we rarely found an effect when we sprayed them with Gingicain; in particular, we did not find a difference in orientation at the four releasesites used in this study (Fig. lb in Wiltschko et al. 1987a). Why the same treatment frequently causes changes in orientation when applied to unimpaired pigeons, as in the present study, is unclear. Yet these different reactions have to be considered when local anaesthetics are applied, especially when birds are treated for the first time. Even if they have had ample opportunity to collect sufficient olfactory information beforehand, one can never be sure that their performance represents ‘normal’ behaviour. This work was supported by the Deutsche Forschungsgemeinschaft in the program SFB 45; all calculations were carried out by the Hochschulrechenzentrum of the Universitgt Frankfurt a.M. We thank the Farbwerke Hoechst AG for providing a free supply of Gingicain and its propellant. ROSWITHA WOLFGANG

WILTSCHKO WILTSCHKO UTE KOWALSKI Fachbereich Biologic der Universitiit, Zoologie, Siesmayerstraj’e 70, D 6000 Frankfurt a.M, Federal Republic of Germany

References Batschelet, E. 1981. Circular Statistics in Biology.-. London: Academic Press. Benvenuti. S. & Wallraff. H. G. 1985. Piaeon navigation: site simulation by means of atmospheric odours. J. camp. Physiol. A, 156,731-746. Kiepenheuer, J. 1985. Can pigeons be fooled about the actual release site position by presenting them with information from another site? Behav. Ecol. Sociobiol.,

l&75-82. Papi,

F. 1976. The

olfactory

navigation

system

of the

37,6

homing pigeon. Verh. Dtsch. Zool. Ges. Hamburg, 1976, 184-205. Papi, F. 1986. Pigeon navigation: solved problems and open questions. Monit. Zool. Ital. (N.S.) ,20,47 l-5 17. Schmidt-Koenig, K. & Phillips, J. B. 1978. Local anaesthesia of the olfactory membrane and homing in pigeons. In: Animal Migration. Navigation, and Homing (Ed. by K. Schmidt-Koenig & W.T. Keeton), pp. 119124. Berlin: Springer-Verlag. Wiltschko, W., Wiltschko, R. & Jahnel, M. 1987a. The orientation behaviour of anosmic pigeons in Frankfurt a.M., Germany. Anim. Behav., 35, 1324-1333. Wiltschko, W., Wiltschko, R. & Walcott, C. 1987b. Pigeon homing: different effects of olfactory deprivation in different countries. Behav. Ecol. Sociobiol., 21, 333-342. (Received

8 November 1988; revised 30 November MS. number: ~~582)

Kleptoparasitism: a Cost of Aggregating Orb-weaving Spider

1988;

for an

One possible cost of living in groups or aggregations is an increased transmission of parasites and disease (Alexander 1974): for example, positive correlations between group sizeand parasite intensity (i.e. the number of parasites per host, following Margolis et al. 1982) have been reported in prairie dogs, Cynomys spp. (Hoogland 1979), cliff swallows, Hirundo pyrrhonota (Brown & Brown 1986), mangabeys, Cercocebus albigena (Freeland 1979), and bobwhite quail, Colinus virginianus (Moore et al. 1988). Theridiid spiders of the genus Argyrodes are kleptoparasites, living on the webs of orb-weaving spiders, where they feed on the prey that is caught in the web of the host spider (e.g. Robinson & Robinson 1973; Vollrath 1979; Rypstra 1981). It is assumed that the fecundity of the host spider is reduced by kleptoparasitism, although this has not been verified experimentally (but see Rypstra 1981). Kleptoparasitic Argyrodes are associated with both solitary and communal speciesof orb-weaving spiders (Exline & Levi 1962). While many studies have examined the association between host spiders and kleptoparasites (Vollrath 1987) and social behaviour in spiders (Buskirk 1981), the relationship between kleptoparasitism and aggregating in spiders has not been explored. Here, I report a study on aggregation sizeand kleptoparasite intensity of an orb-weaving spider. The Australian golden orb-weaving spider, Nephila edulis Koch, is widely distributed throughout the continent and, where it occurs, is relatively common. It is a large spider: the female may reach a body length of 35 mm, with orb-webs that exceed

Short Communications

1 m in diameter and support threads extending beyond 5 m. Only one spider occupies a web, but the webs are sometimes found in loose aggregations with individual webs less than 20 cm apart, supported by structural threads that are often shared by several spiders.The webs of N. edulis are host to at least two speciesof kleptoparasitic Argyrodes. Further details of the biology of N. edulis were described by Austin & Anderson (1978). The kleptoparasitic silver-drop spider, Argyrodes antipodianus Cambridge (between 1 and 2 mm long) is commonly found on the web of N. edulis, although it is not host-specific. Both males and females may be present on the host web. Argyrodes antipodianus are usually found around the edge of the orb-web, venturing on to it only when collecting prey items. Observations of adult females of N. edulis and its kleptoparasite A. antipodianus were made during May and June of 1988, in the mangrove swamps at the Towra Point Nature Reserve, Botany Bay, Sydney. The webs of N. edulis are suspended between branches of either the same or adjacent mangrove trees, Avicennia marina, between 0.5 and 4 m above ground level. The following data were recorded from each web that was found along transects into the mangroves: the size of the aggregation, the body length of N. edulis, and the number of A. antipodianus present on each web. An individual N. edulis web was deemed to belong to an aggregation if the structural threads of its web were attached to the threads of another web, or the web was less than 30 cm from the web of another spider. In thesecases,A. antipodianus was observed moving freely between the webs of individual

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The kleptoparasite intensity of A. antipodianus was positively correlated with the size of the host (r, = 0.376, N = 96 webs, P < O.OOl),but the correlation between aggregation size and kleptoparasite intensity, although positive, was not significant (r, = 0.124, N= 96 webs, NS). However, this correlation was confounded by the negative correlation between aggregation size and body size; when the effects of body size were partialled out (Conover 1980) there was a significant correlation between aggregation sizeand the number of kleptoparasites per web (partial r = 0.26, P < 0.01). Thus, aggregating females of N. edulis of any sizesuffered a higher kleptoparasite intensity than solitary females. The higher kleptoparasite intensity for N. edulis in aggregations may be due to a higher colonization rate of kleptoparasites. Alternatively, this rate may not alter with aggregation size, but individuals in aggregations may remain at a particular web site for longer than solitary individuals, resulting in a higher kleptoparasite intensity. A removal experiment was undertaken in the field to test whether the colonization of A. antipodianus is higher for aggregating N. edulis than for solitary N. edulis. Solitary and aggregating individuals of N. edulis were selectedaccording to their size,the location of the web and the number of kleptoparasites per web, and subsequently paired for statistical analysis. One N. edulis was randomly chosen from each aggregation, since the colonization rate for individuals within aggregations could not be assumed to be independent. The number of A. antipodianus on each web were counted, removed and then releasedabout 50 m from the site. The host spiders’ webs were then censusedfor kleptoparasites on the N. edulis. following day and 4 days after removal of the Aggregations of N. edulis range up to five webs, kleptoparasites. with a mean aggregation size of 1.42 (SD =0.79, The results of the removal experiment showed N=96 groups). The frequency distribution of that N. edulis in aggregations suffered a higher aggregation sizes was not significantly different colonization rate of A. antipodianus than solitary from a truncated Poisson distribution (1=0.75, N. edulis. After 24 h, N. edulis in aggregations had a Cohen 1960; x2=2.24, df=?, NS). This suggests significantly higher proportion of the original that the formation of aggregations is largely ran- number of kleptoparasites than solitary N. edulis dom, and individuals do not selectspecificaggrega- (Table I). However, these differences were no tion sizes. Nevertheless, there was a significant longer significant after 4 days. The mean kleptonegative correlation between the body size of N. parasite intensity for both solitary and aggreedulis and aggregation size (r, = -0.284, N=96 gating N. edufis at the end of the experiment webs, P< 0.01). (8+ SD = 12f 5 kleptoparasites/web, N = 16) was At least one A. antipodianus was found on all but not significantly different from the number at the one of the webs examined (N=96) and the maxi- start of the experiment (Rk SD = 10 + 3 kleptoparamum number of kleptoparasites on a single web sites/web, N=20, t,= 1.97, NS). was 30. The mean kleptoparasite intensity (number The removal experiment was not designed to of kleptoparasites per web) was 10 (SD = 5, N =96 distinguish between the two explanations for the webs). These kleptoparasite intensities are higher higher kleptoparasite intensity for aggregating than those reported for other speciesof Nephila females of N. edulis. Nevertheless, it demonstrated (Robinson & Robinson 1973; Vollrath 1979; that spiders in aggregations suffered a higher colonization rate of kleptoparasites. Furthermore, Rypstra 1981).

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Animal

Behaviour,

Table I. Colonization of the kleptoparasite nus on the webs of Nephila edulis

37, 6 Argyrodes

Mean

Treatment Solitary Aggregation t-test

Number of webs 10 10

Mean number removed 8.0 f 3.5 10.6& 3.0

antipodia-

colonization frequency

Day 053+0,29 0,86&0.31 7.89*

1

Day 4 l.lOf0.58 1.40+0.39 1.68

Colonization frequency is the kleptoparasite intensity for that day, divided by the number of kleptoparasites that were initially removed from that web. Values given are meansks~. *p
there was no association between aggregating and web-site tenacity; eight out of 10 solitary spiders had remained at the same web site after 5 days, compared with seven out of 10 aggregating spiders (Fisher’s exact probability =0.5). The dispersal mechanism of A. antipodianus may explain the higher colonization rate for aggregating spiders. Argyrodes antipodianus travel between webs by ‘ballooning’: the kleptoparasites exude a gossamer thread which is caught up and drawn by wind currents, eventually allowing them to drift between the webs of hosts. This largely random method of dispersal means that A. antipodianus are more likely to land on the larger surface area of an aggregation of webs than on a solitary web of N. edulis. Movement between the webs in an aggregation can then be made on connecting threads that have been built by either N. edulis or A. antipodianus.

Variation in the kleptoparasite intensity may depend upon several factors; for example, the kleptoparasites may leave a web as a result of insufficient food intake, due to competition among kleptoparasites (Vollrath 1979), the poor location of the host web, or the web-site tenure of the host. Nephila edulis at Towra Point did not always remain at the same web site for long periods. While inclement weather may account for some of their mobility (webs are dismantled during periods of heavy rain or strong winds), N. edulis may also move as a result of heavy kleptoparasite intensity, as has been shown for other species of Nephila (Rypstra 1981; Larcher & Wise 1985). Several studies have shown that in web-building spiders, individuals in aggregations benefit from increased prey capture (e.g. Lubin 1974), even under experimental conditions that controlled for prey availability (Uetz 1988). The results of this study suggest that individuals in aggregations may have their food intake reduced as a result of higher

kleptoparasite intensity. Clearly the extent to which a prey-capture advantage is translated into reproductive success for any species of spider that aggregates may depend upon the intensity and subsequent cost of kleptoparasitism. I thank Belinda Chang, Michael Crosland, Ross Crozier, Christian Peeters, Andrew Read and Fritz Vollrath for their helpful comments on the manuscript, Mike Gray for identifying the spiders, and the N.S.W. National Parks and Wildlife Service for permission to work in the Towra Point Nature Reserve. Financial support was provided by a University of New South Wales Research Fellowship, and a small project grant from the Association for the Study of Animal Behaviour. MARK

A. ELGAR

School of Biological Science, University of New South Wales, P.O. Box I, Kensington, Sydney, New South Wales 2033. Australia.

References Alexander, R. D. 1974. Theevolution ofsocial behaviour. A. Rev. Ecol. Syst., $325-383. Austin, A. D. & Anderson, D. T. 1978. Reproduction and development of the spider Nephila edulis (Koch) (Araneidae: Araneae). Austral. J. Zool., 26, 501-5 18. Brown, C. R. & Brown, M. B. 1986. Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology, 67, 1206-1218. Buskirk, R. E. 1981. Sociality in the Arachnida. In: Social Insects. Vol. ZZ (Ed. by H. R. Hermann), pp. 281-367. New York: Academic Press. Cohen, A. C., Jr. 1960 Estimating the parameter in a conditional Poisson distribution. Biometrics, 16, 203211. Conover, W. J. 1980. Practical Nonparametric Statistics. New York: John Wiley.

Short

Communications

Exline, H. & Levi, H. W. 1962. American spiders of the genus Argyrodes (Araneae, Theridiidae). Bull. Mm. Comp.

Zool.,

Harvard,

121,15-202.

Freeland, W. J. 1979. Primate social groups as biological islands. Ecology, 60, 719-728. Hoogland, J. L. 1979. Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behauiour, 69, l-35. Larcher, S. F. &Wise, D. H. 1985. Experimental studies of the interactions between a web-invading spider and two host species. J. Arachnol., 13,43-59. Lubin, Y. D. 1974. Adaptive advantages and the evolution of colony formation in Cyrtophora (Araneae: Araneidae). Zool. J. Linn. Sot., 54, 321-339. Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. & Schad, G. A. 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J. Parasitot., 68, 899-902. Moore, J., Simberloff, D. & Freehling, M. 1988. Relationships between bobwhite quail social group size and intestinal helminth parasitism. Am. Nat., 131,22-32. Robinson, M. H. & Robinson, B. 1973. Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithson. Contr. Zool., 149, l-76. Rypstra, A. L. 1981. The effects of kleptoparasitism on prey consumption and web relocation in a Peruvian population of the spider Nephila clavipes. Oikos, 37, 179-182. Uetz, G. W. 1988. Group foraging in colonial webbuilding spiders: evidence for risk sensitivity. Behau. Ecol.

Sociobiol.,

22, 2655270.

Vollrath, F. 1979. Behaviour of the kleptoparasitic spider Argyrodes elevatus (Araneae, Theridiidae). Anim. Behav.,

21,515-521.

Vollrath, F. 1987. Kleptobiosis in spiders. In: Ecophysiology of Spiders (Ed. by W. Nentwig), pp. 274-286. Berlin: Springer-Verlag. (Received

20 July 1988; revised 3 October MS. number: x-472)

1988;

Do Anuran Larvae Retain Kin Recognition Abilities Following Metamorphosis? Ontogenetic analyses provide a powerful tool for the study of kin recognition mechanisms (e.g. see Fletcher & Michener 1987). Amphibians have been studied extensively (reviewed by Waldman 1986; Blaustein et al. 1987), largely because their larval development is easily examined and manipulated. Yet functional explanations of their kin recognition abilities cannot be limited to the larval stage. Amphibians have complex life cycles: selection on adults to discriminate their kin, for example in mate choice (see Bateson 1983), might drive the acquisition and expression of kin recognition abilities by larvae. Waldman (1982b) suggested that kin recognition

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abilities might be retained through metamorphosis. Subsequently, Blaustein et al. (1984) showed that recently metamorphosed Cascades frogs, Rana cascadae, discriminated between siblings and nonsiblings to the same extent as did the tadpoles. Wood frogs, Rana sylvatica, are ecologically similar to Cascades frogs in several respects, and wood frog tadpoles recognize and associate with familiar siblings in preference to familiar non-siblings (Waldman 1984), and with unfamiliar siblings rather than unfamiliar non-siblings (Cornell et al., in press). During 1985 and 1986, I tested recently metamorphosed wood frogs in an apparatus virtually identical to that used by Blaustein et al. (1984) to determine whether they too discriminate between siblings and non-siblings. I collected R. sylvatica egg masses during March of each year from communal oviposition sites (see Waldman 1982a) in Carlisle, Massachusetts. Egg masses were brought to the laboratory, and at hatching, larvae were reared in groups of 25 in 20litre containers either solely with their siblings or with non-siblings (individuals from 25 sibships were mixed). Tadpoles were fed spinach daily ad libitum, and water was changed twice weekly. At metamorphosis (tail completely resorbed, stage 46, Gosner 1960), groups of 10 froglets were transferred to shallow rectangular trays (30 x 20 x 10 cm high), and were fed live Drosophilia melanogaster ad libitum. Individuals were tested either soon after metamorphosis (4-18 days; mass 240-l 110 mg, snout-vent length 13-20 mm) or a month later (3448 days; 620-2140 mg, 15-23 mm). The testing apparatus consisted of a plastic tube measuring 84 cm in length and 5.5 cm in diameter (Habitrail@, Metaframe). The tube’s interior was slightly wetted prior to each test. Subjects were tested singly. Ten froglets from the subject’s sibling group (or same mixed group) and 10 froglets from a non-sibling group (or different mixed group) were placed in opposite end chambers (8 cm long), separated from the subject by 1.5-mm fibreglass mesh (see Fig. 1 in Blaustein et al. 1984). Test subjects and stimulus groups had been reared together in the same containers as larvae, but were separated into different trays at metamorphosis. The tube was marked in thirds, corresponding to areas near each of the stimulus groups, and a central (neutral) area. Subjects were released in the centre, mesh (see diagram in Blaustein et al. 1984). Test subjects and stimulus groups had been reared together in the same containers as larvae, but were separated into different trays at metamorphosis. The tube was marked in thirds, corresponding to areas near each of the stimulus groups, and a central (neutral) area. Subjects were released in the centre, oriented