Spider Webs As Habitat Patches—The Distribution of Kleptoparasites

Home , Argyrodes, Nephila, Philoponella, Philoponella oweni

2003. The Journal of Arachnology 31:344±349

SPIDER WEBS AS HABITAT PATCHESÐTHE DISTRIBUTION OF KLEPTOPARASITES (ARGYRODES, THERIDIIDAE) AMONG HOST WEBS (NEPHILA, TETRAGNATHIDAE)

Ingi Agnarsson: Systematic Biology±Entomology, E-530, Smithsonian Institution, NHB-105, PO Box 37012, Washington, D.C. 20013-7012 & Department of Biological Sciences, George Washington University, Washington DC, 20052 USA

ABSTRACT. Most adult golden orb weavers (Nephila clavipes) have kleptoparasites of the genus Ar- gyrodes in their webs. The kleptoparasitic load correlates positively with web size. Clustered (interconnected) webs have a more predictable number of kleptoparasites than do solitary webs, but there is no difference in the mean number of kleptoparasites between the two. From the view of the kleptoparasite, host webs are habitat patches or islands. Isolated webs show characteristics of small patches, where web size is a poor indicator of kleptoparasite number and variation is high. The distribution of kleptoparasites in clustered webs, on the other hand, seems to ®t the ``ideal free distribution'' where web size nearly entirely predicts kleptoparasitic load. Thus clustered webs, as a habitat patch, are more than merely the combination of their parts. The predictability of kleptoparasite load in clustered webs may be a function of the stability (longevity) of those habitat patches, and ease of colonization, as neighboring webs act as sources. Keywords: Habitat islands, habitat stability, ideal free distribution, orb web, patch connectivity

Obligatory kleptoparasites of the genus Ar- site number? Is a cluster of interconnected gyrodes Simon 1864 are completely depen- webs equivalent to a gigantic solitary web? dent on their host webs (Kullmann 1959; Voll- Does the distribution of kleptoparasites in host rath 1987; Cangialosi 1990; Miyashita 2001); webs appear to ®t the ideal free distribution from the perspective of the kleptoparasite, model, as suggested by Elgar (1993)? host webs are thus natural habitat patches, or Many authors have studied the biology of islands. Unlike islands, however, individual kleptoparasitic Argyrodes and its interaction host webs are often interconnected, which with its hosts (see Elgar 1993 for review), yet adds another dimension to the system. Viewed understanding of the distribution of klepto- as habitat patches, host web size and kleptoparasites among host webs is fragmentary. parasite number should be correlated. The iso- Cangialosi (1990) showed a strong correlation lation, or clustering, of webs should affect the between social Anelosimus eximius (Keyser- distribution of kleptoparasites among webs. ling 1884) web size and the number of Ar- Interconnectedness should facilitate the move- gyrodes ululans O. P.-Cambridge 1880 klep- ment (immigration and emigration) of kleptoparasites residing in them. She attributed toparasites between webs. And, ease of im- this in part to the stability and longevity of migration/emigration, together with relative the larger colonies. Rypstra & Binford (1995) longevity of clustered webs, should result in found that the number of commensal Philo- either higher or more stable kleptoparasite ponella republicana (Simon 1891) was cor- load compared to solitary webs. related with web size of its social A. eximius This study is intended to examine the gen- host, and that P. republicana was more com- eral correlation (if any) between Nephila cla- mon in social A. eximius host webs than in vipes (Linnaeus 1767) host orb size and Ar- solitary host webs of Architis sp. Smith Trail gyrodes kleptoparasite load, and speci®cally, (1980) showed, similarly, that colonies of if and how the kleptoparasitic load of inter- Philoponella oweni (Chamberlin 1924) had connected (clustered) webs differs from other higher numbers of Argyrodes ®ctilium (Hentz webs. I ask three main questions: is there a 1850) kleptoparasites than did solitary P. ow- correlation between orb size and kleptopara- eni webs. Only a few studies have demonstrat-

344 AGNARSSONÐSPIDER WEBS AS HABITAT PATCHES 345 ed such correlations in Nephila Leach 1815 physically touch other webs. The distance to webs. Robinson & Robinson (1973) found the nearest web was not measured exactly, but that adult Nephila pilipes (Fabricius 1793) had was never less than one meter. I used linear more kleptoparasites than did juveniles. Elgar regression to examine the relationship of web (1989) showed a relationship between host size and kleptoparasite numbers, both for the size and kleptoparasitic load (note that host pooled data and for clustered and solitary size and orb size are strongly correlated (Witt webs separately. I used a preliminary model et al. 1968; Grostal & Walter 1999)), and that `homogeneity of slopes' test to determine the clustered webs suffered a higher parasitic load homogeneity of the regression slopes. As ho- than did solitary webs of N. edulis (Labillar- mogeneity was rejected, an ANCOVA was not dieÁre 1799) in Australia. Grostal & Walter performed. To test if web size can explain (1999) showed a weak correlation between kleptoparasite load equally in solitary and Nephila plumipes (Latreille 1804) web size clustered webs I compared the variance of (also in Australia) and kleptoparasite number, kleptoparasite load in clustered versus solitary but contrary to Elgar (1989), they found no webs, using a F-test. I used a t-test to compare special association between web aggregation the mean numbers of kleptoparasites per orb and kleptoparasitic load. area between clustered and solitary webs. This paper reports on Argyrodes kleptopar- I assigned a number to each of the Nephila asites in the webs of a fourth Nephila species, webs encountered, thereby establishing a tran- N. clavipes (Linnaeus 1767), in Costa Rica. I sect of webs which were then used for obser- look at the data from a different angle (re- vations and experiments. Webs were chosen gression variance), and in light of these results on this transect by randomly picking numbers, I propose a reinterpretation of the results of alternatively for the two parts of this study, previous studies. without replacement (so that no single web could be involved in both experiments). To METHODS obtain basic information on the distribution of The study was undertaken during the dry kleptoparasites within host webs, in particular season, over a seven day period in February during orb reconstruction, 15 Nephila webs 2001 at Cabo Blanco Absolute Reserve, and were monitored over a 6 day period for a total three day period in March 2002, in Manuel of 40 observation hours. The data collected Antonio National Park, both in Puntarenas was not quantitative, I visited the chosen webs Province, on the paci®c coast of Costa Rica. haphazardly, and noted the whereabouts (in Both study sites are in fairly open coastal hu- barrier web or in orb) and movements of the mid tropical forest. The area has approximate- kleptoparasites, and anecdotal information ly 1400 mm annual rainfall, spread mostly about the behavior of the kleptoparasites as over May±September, but with a dry season well as their interaction with the host were between January and April. All observations also noted. To compare the rates of coloniza- and data collecting were made from 0900± tion in clustered and solitary webs, I removed 1700 h. kleptoparasites from 10 solitary and 10 clus- To assess the distribution of kleptoparasites tered webs. If more than one web was chosen among host webs, N. clavipes webs were lo- from a particular cluster, I removed the klep- cated along trails and in the forest within the toparasites of only a single web daily, consec- reserves. For every web encountered, I re- utively over the six day period. I counted the corded the owner's size (body length in mm, number of kleptoparasites in these webs the excluding legs) and developmental status day after their removal and calculated the dif- (adult/juvenile based on epigynal appearance), ference in re-colonization rates using a two the orb size (height x width of orb in cm) and sample t-test. the number of kleptoparasites occupying each Voucher specimens from this study are de- web, including its associated barrier web. posited in the arachnological collection of the National Museum of Natural History, Smith- Each orb was measured in the same way sonian Institution. whether in a cluster or solitary. A web is clas- si®ed as ``clustered'' if its structural threads RESULTS attached to the threads of another Nephila I encountered 70 Nephila webs (48 solitary web. Solitary webs are any webs that do not webs, 22 clustered, in a total of 7 clusters) 346 THE JOURNAL OF ARACHNOLOGY

Figure 1.ÐKleptoparasite load is correlated with web size in both solitary and clustered Nephila clavipes webs in Costa Rica. In clustered webs the number of kleptoparasites is nearly entirely linearly predicted by web size (r2 ϭ .94). On the other hand, solitary webs have a highly variable number of kleptoparasites (r2 ϭ .29). containing close to 300 kleptoparasites. The of kleptoparasites per web area between clus- orbs of solitary webs ranged in size from tered (18.5 kleptoparasites/m2,SDϭ 13.3) 0.015±0.56 m2, while the orbs of webs that and solitary (23.1 kleptoparasites/m2,SDϭ were part of a cluster ranged from 0.015±0.77 26.4) webs (t ϭ 0.77 df ϭ 68, P ϭ 0.443). m2. In either case, I found kleptoparasites only The kleptoparasites, when not foraging, in webs larger than 0.04 m2 (i.e. about 20 ϫ spent most of their time in the host barrier 20 cm). The largest web encountered (90 ϫ web, which provides a haven outside the mon- 80 cm, located in the center of a cluster) had itoring range of the host. In two instances Ne- the highest number of kleptoparasites, 18. phila orb reconstruction was observed and in Two Argyrodes species were identi®ed: A. both cases the kleptoparasites were observed elevatus Taczanowski 1873 of the `À. argy- maintaining an association with that particular rodes'' group and A. caudatus (Taczanowski host. As Nephila rebuilt its orb the kleptopar- 1874), of the `À. cancellatus'' group (Exline asites resided in the unaltered barrier web, and & Levi 1962). Kleptoparasitic load increased no emigration was observed in these two with web size, pooling all data (r2 ϭ 0.61, F cases. The fresh orb was connected to the old ϭ 109.2, df ϭ 68, P Ͻ .001, n ϭ 70) (Fig. 1). barrier web, and after its completion the klep- Looking at clustered and solitary webs separately, web size explained nearly all the vari- toparasites rebuilt their association lines. Most ance in clustered webs (r2 ϭ 0.94, F ϭ 310.2, of the kleptoparasites were only ever seen en- df ϭ 20, P Ͻ .001, n ϭ 22) but much less so tering a single host web, even if that host web in solitary webs (r2 ϭ 0.29, F ϭ 19.8, df ϭ was connected to another. Yet, a few spiders 46, P Ͻ .001, n ϭ 48). The homogeneity of did have silk lines leading to two host webs the regression line slopes is rejected (S2 ϭ (counted only once and assigned to the nearest 42.506, F ϭ 5.861, df ϭ 1, P ϭ 0.018). The web), and thus could ``monitor'' more than difference in variance in kleptoparasitic load one web at a time and forage in either (see in clustered (S2 ϭ 2.1) and solitary (S2 ϭ 9.5) also Whitehouse & Jackson 1993). All Argy- webs is signi®cant (F(2),20,46 ϭ 4.5, P Ͻ .01). rodes instars occurred in host webs, and both There was no difference in the mean number species were observed mating in the host bar- AGNARSSONÐSPIDER WEBS AS HABITAT PATCHES 347 rier web. Argyrodes egg sacs were found cleaned of kleptoparasites in this study re- hanging from the Nephila barrier web. gained them more rapidly than did solitary A day after removal of kleptoparasites two webs. of the 10 webs in clusters had three klepto- Kleptoparasites in web clusters can easily parasites, ®ve webs had two and three webs relocate to a web that provides more prey (i.e. had one, while seven of the 10 solitary webs the ideal free distribution). An `èxtinction'' had zero and three had one kleptoparasite, re- event (disappearance of a kleptoparasite) is spectively. The re-colonization rates of clus- short-lived because the neighboring webs act tered versus solitary webs differed (t ϭ 5.737 as sources. Web clusters are, in addition, rel- df ϭ 18, P Ͻ .001). atively long lived habitat patches, increasing the probabilities of colonization by kleptopar- DISCUSSION asites. Solitary webs, on the other hand, are As in N. edulis (Elgar 1989) and N. plu- more like islands. They may ®rst of all never mipes (Grostal & Walter 1999), the number of reach an upper limit because they are rela- Argyrodes kleptoparasites correlates positive- tively short lived, immigration is more sto- ly with web size in N. clavipes (Fig. 1). If in chastic, and they will experience higher rates clusters, orb size explained nearly all variation of extinction (a solitary Nephila death will re- in kleptoparasite number whereas if solitary, sult in total extinction or emigration, whereas orb size explained much less of the variation. a Nephila death in a web cluster will result in Although the regression slope of clustered only partial extinction/emigration from the webs is steeper, solitary webs did not have cluster). Second, some solitary webs have a lower mean number of kleptoparasites (unlike higher number of kleptoparasites per web area N. edulis, see Elgar 1989). than any one in a cluster. This may be a result Elgar (1993) suggested that the distribution of a greater ``risk'' of emigrating from isolated of kleptoparasites among host webs in some webs and dif®culties of ®nding new onesÐ cases seems to follow the ìdeal free distri- isolation makes reaching an ideal distribution bution' (Milinski & Parker 1991). The ideal harder. free distribution model states that for a given Patch connectivity thus seems to be of great population size k, there exists a distribution of importance in the distribution of kleptopara- individuals such that the ``suitabilities'' de- sites among Nephila webs. A web cluster is rived from each habitat are equal and hence not merely equivalent to a gigantic solitary stable (Krebs 1994). If all individuals are web; it is rather a community of distinct webs, ``free'' to move to alternate patches, then each potentially experiencing multiple extinc- `ìdeally'' each will ®nd the place that maxi- tions and colonizations of kleptoparasites. mizes its gain. Grostal & Walter (1999) found their results The results obtained here suggest that ideal to con¯ict with those of Elgar (1989) and sug- free distribution may only be an appropriate gested that the distribution of kleptoparasites model in the case of clustered webs. It seems might be more random than Elgar had con- that the parasite load for host webs in clusters cluded. The ®ndings of this study agree with has an optimal upper limit and the low vari- Elgar's (1989) that there is a difference in ance in kleptoparasite numbers suggests that kleptoparasitic load of clustered and solitary N. clavipes webs in clusters are generally near webs. However, the difference seems to be or at that limit. Miyashita (2001) demonstrat- one of stability, therefore comparing simply ed that in Nephila clavata L. Koch 1878 webs the mean number of kleptoparasites may not in Japan, the removal of Argyrodes ¯avescens be suf®cient to detect those differences. Nei- (O. P.-Cambridge 1880) kleptoparasites re- ther Elgar nor Grostal & Walter considered the sulted in a remarkably rapid in¯ux of other regression variance in host web occupation, individuals of that and another Argyrodes spe- and thus could not have discovered the pat- cies. He interpreted this as evidence for strong terns reported here. Furthermore, both the cur- inter- and intraspeci®c competition for limited rent study and that of Elgar were ``snapshots host web space. Grostal & Walter (1999:557, in time'', done over a period of a few days, ®g. 4) also concluded that orb diameter im- whereas that of Grostal & Walter took place posed an upper limit on kleptoparasite num- over different seasons. Vollrath (1987) and bers. Furthermore, clustered webs that were Higgins & Buskirk (1998) found large sea- 348 THE JOURNAL OF ARACHNOLOGY sonal ¯uctuations in the population sizes of epitomize general ecological models, such as kleptoparasitic Argyrodes and their Nephila island biogeography (MacArthur & Wilson host. Pooling data from different seasons 1967) and metapopulation biology (Hanski could easily obscure correlations between 1999). In order to test such models, future kleptoparasite load and web size at smaller studies should include additional factors, e.g. time scales. Finally, the current study would absolute distances between webs, number of predict a greater mean number of kleptopar- webs per cluster, barrier web size, phenology asites in clustered webs if the majority of of both host and kleptoparasites, and the pat- webs considered were large (see Fig.1). Elgar terns of migration between host webs. For (1989) found a very low percentage of webs such studies Nephila webs are ideal as both without kleptoparasites (one out of 92) and a their relative longevity (thus habitat stability) high mean number of kleptoparasites per web (e.g. Wiehle 1927; Lubin 1983; Foelix 1996), (10, versus e.g. 4.2 in the current study) sug- and the extensiveness of their mesh-like bar- gesting that his study may indeed have been rier webs, may increase kleptoparasitism biased towards larger webs. Thus, reanalysis (Whitehouse 1988; Cangialosi 1990, 1997; of the data of these previous studies is likely Grostal & Walter 1999; Miyashita 2002). The to reveal more general and congruent patterns, barrier web provides a safe substrate for the the presumed con¯ict being more apparent kleptoparasites from which to monitor the than real. host web (e.g. Vollrath 1979a, 1979b; White- The structural complexity and longevity of house 1986; Cangialosi 1990), it makes the Nephila web clusters may explain, at least orb three dimensional, which may facilitate partially, the greater stability of kleptoparasite group living (Krafft 1979; Agnarsson 2002), populations in them, versus the shorter lived and it allows the kleptoparasites to stay as- solitary webs. A growing amass of evidence sociated with the host during orb reconstruc- indicates that kleptoparasites greatly prefer tion. complex, long-lived, webs (e.g. Anelosimus Simon 1891, Argiope Audouin 1826, Cyrto- ACKNOWLEDGMENTS phora Simon 1864, Diplura C.L. Koch 1850, I would like to thank Laura May-Collado Stegodyphus Simon 1873, Tengella Dahl 1901 for assistance in the ®eld and with data anal- and Nephila), to simpler webs taken down fre- yses. Jonathan A. Coddington, Gustavo Hor- quently (see Elgar 1993 for review; Miyashita miga, Agnar IngoÂlfsson, MatjazÏ Kuntner, 2002). Given that Argyrodes kleptoparasites Tony Baumert, Jeremy Miller, and Laura can signi®cantly and detrimentally affect their May-Collado provided valuable comments on hosts (Vollrath 1980; Rypstra 1981; Elgar a version of the manuscript. I thank the editor 1989; Grostal & Walter 1997; Higgins & Bus- Gail E. Stratton, and Ann L Rypstra and an kirk 1998) it is tempting to speculate that fre- anonymous reviewer for their detailed review, quent web renewal may represent an adapta- and invaluable constructive comments that tion against kleptoparasitism. Cause and effect greatly improved the paper. Support for this in this case may be hard to tease apart, as research was provided by a National Science many other factors affect web duration (e.g. Foundation grant to Gustavo Hormiga and predation by sphecid wasps). The lack of Jonathan Coddington (DOEB 9712353), a Re- kleptoparasites in ``daily webs'' seems nev- search Enhancement Fund grant from The ertheless bene®cial and further work might George Washington University to G. Hormi- pro®tably explore the idea. ga, the Smithsonian Neotropical Lowland Nephila webs are not only insect snares, but grant to Jonathan A. Coddington, a Sallee also discrete habitat islands hosting a dynamic Charitable Trust grant to Ingi Agnarsson and community of kleptoparasitic spiders depen- Matjaz Kuntner, and the USIA Fulbright Pro- dent upon them. Available studies have all gram. Further support was provided by the shown a correlation between patch (web) size Smithsonian institution and Organization for and population size, and the current study Tropical Studies. shows an increase in population stability with patch connectivityÐa cluster of small webs is LITERATURE CITED a more predictable (stable) habitat patch than Agnarsson, I. 2002. On the relation of sociality and a large solitary web. These characteristics kleptoparasitism in theridiid spiders (Theridiidae, AGNARSSONÐSPIDER WEBS AS HABITAT PATCHES 349

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