2002. The Journal of Arachnology 30:31-38 TWO POPULATION DYNAMICS OF SPECIES OF KLEPTOPARASITIC SPIDERS UNDER DIFEERENT HOST AVAILABILITIES Tadashi Miyashita: Laboratory of Biodiversity Science, School of Agriculture and Life Sciences, University of Tokyo, Tokyo 113-8656 Japan. Email: tmiya@uf.a.U“tokyo.ac.jp ABSTRACT. Kleptoparasitic spiders are known to have a close association with host spiders, yet there have been few studies demonstrating how host availability influences the dynamics of kleptoparasites. Field surveys were conducted at five sites differing in host composition in sub-tropical areas in Japan, at about two-months intervals. Argyrodes flavescens and A. bonadea were both found more frequently on webs of two Nephila species than expected from the web areas they occupied among webs of all web spiders. Seasonal dynamics of Argyrodes changed greatly according to whether N. clavata was present or not, indicating the importance of Nephila on Argyrodes populations. The peak density ofA. bonadea came earlier than that of A. flavescens. Because A. flavescens is known to limit the number of A. bonadea on host webs, the decrease in the density ofA. bonadea may be due to the effect of interspecific competition by A. flavescens. Keywords: Interspecific competition, parasite, Theridiidae, phenology Spiders in the genus Argyrodes Simon 1864 A. flavescens O. Pickard-Cambridge 1880 and are often called kleptoparasites that rely al- A. bonadea (Karsch 1881), are commonly most exclusively on host spiders. However, found on orb-webs of various spider species. the interaction between Argyrodes and their Preliminary observations revealed that a large hosts is complex: Argyrodes can be klepto- number of the two species was found on the parasites, commensals, or predators to their webs of Nephila clavata and N. niaculata (Fa- hosts depending on the species and host con- bricius 1793). These two Nephila species have ditions (e.g., Trail 1980; Tanaka 1984; Larcher different phenologies, the former emerging & Wise 1985; Whitehouse 1986; Cangialosi later in the season. Also, the distributions of 1997). These close associations lead to the in- the two species differ, N. maculata lives all ference that population dynamics of Argyro- over the island while N. clavata inhabits only des is highly dependent on host availability. the northern part of the island. These charac- Vollrath (1987) demonstrated the dynamics of teristics enable us to estimate the importance two Argyrodes species and their host Nephila of host availability. clavipes (Linnaeus 1767). However, there In this paper I examined seasonal dynamics have been no studies showing how changes in of the two Argyrodes species and their poten- host species composition influences Argyro- tial host spiders in five sites differing in host des dynamics. Ideally such a causal relation- species compositions. I hypothesize that 1) the ship should be evaluated by field experiments Nephila species are the preferred host for Ar- in which a particular host is removed, but pop- gyrodes, and 2) the presence or absence of ulation manipulation on a large scale suffi- Nephila clavata changes population dynamics cient to change host availability is impractical. of Argyrodes greatly. Examining the variation of kleptoparasite dy- METHODS namics in areas differing in host availability seems to be the only way to estimate the Field studies were conducted at four sites strength of associations between the host and on Okinawa Island, Nakagusuku (NK), Nan- kleptoparasite at the population level. gusuku (NG), Shoshi (SH), Nakijingusuku On Okinawa Island located in the south- (NJ), and at one site on Iheya Island (IH), western part of Japan, two Argyrodes species, southwestern Japan. The climate of these sites 31 — THE JOURNAL OF ARACHNOLOGY 32 is sub-tropical, with an average temperature of and Nj is the total number of Argyrodes sp. j 22.6 °C and an annual rainfall of 2,100 mm. on host species j. Hosts harboring at least ten Previous observations revealed that Nephila Argyrodes or those occupying more than 30% clavata, a major host for Argyrodes, lives at of the total web areas of all species combined NK all sites except for which is located at the were used for the analysis. Significance level southern part of Okinawa Island, Iheya Island was adjusted by the sequential Bonferroni lies about 60 km away from Okinawa Island method (Sokal and Rohlf 1995) for each sea- and is much smaller (about 20 km^) than that son. of Okinawa Island (about 1,199 km^). Thus I RESULTS expected densities and/or species richness of host spiders to be low on that island. Dynamics of Argyrodes and their host. m I established two 50 lines along the road- The kleptoparasitic spiders found in this sur- side in forests at each site, and surveyed these vey were mostly A. flavescens and A. bona- transects five times (four times for IH) from dea. Figure 1 shows seasonal changes in the July 1997 to April 1998 at intervals of ap- density of the two Argyrodes spp. and web NK proximately 2-3 mo. I recorded all web spi- areas of host spiders in five study sites. In mm ders with body lengths larger than 4 liv- where N. clavata is absent, the dynamics of m m ing within 2 from the transect and 2 from web area were mostly determined by N. ma- the ground. I recorded the spider body length, culata. Although the peak density of A. fla- the vertical and horizontal web diameters, any vescens was delayed relative to that of host prey being consumed, and any small insects web area, its density decreased abruptly in remaining in the web. At the same time I November when N. maculata disappeared. In counted and recorded the body length of all NG, SH and NK, however, N. clavata is abun- Argyrodes found on the spider webs with cal- dant in November, and Argyrodes maintained ipers. Because it was difficult to know the high densities in November. It is noteworthy stage of Argyrodes in the field, I used body that the timing of peak density of the two Ar- length as an indicator for the stage and deter- gyrodes species differed, with A. bonadea mm mined the smallest size of adults, viz., 3 reaching the peak earlier. Another important mm for A. flavescens and 2.5 for A. bonadea. point is that both Argyrodes densities declined In this study, web areas of hosts instead of to low levels in January and April when web density of host individuals was used for rep- areas of spiders other than Nephila remained resenting host availability because the body at levels similar to those in November. The size of host spiders varies greatly depending main species in this period were Leucauge on the species and seasons. For instance, the blanda (L. Koch 1878), Cyclosa confusa Bos- web of Nephila maculata is much larger than enberg & Strand 1906 and Neoscona scylla that of most other spiders, so that the amount (Karsch 1879). In IH where N. clavata was of habitat and food resources available to Ar- not found on the census route, the density of gyrodes may vary greatly. Argyrodes showed a peak in August and then The density of each Argyrodes on a partic- dropped sharply in November, which is simi- ular host species (no./cm^) was calculated as lar to the situation in NK. Unlike other study follows, S N,/S Aj, where N, is the number of sites, the density of A. bonadea was much Argyrodes on the web of a particular host higher than that of A. flavescens. i'*^ species and Aj is the web area of the web. Percentage of adult Argyrodes.—The per- Data from the two transects were combined at centage of adult individuals was calculated A each site. binomial test was performed to separately for areas where both Nephila spe- ascertain whether each Argyrodes prefers a cies were present (NG, SH, NJ) and Nephila particular host spider species. The null hy- clavata was absent (NK, IH). In areas where pothesis was that the total number of Argy- both Nephila species were present, seasonal rodes on webs of host species (Nj) is deter- change in the percentage of adults differed j mined by the proportion of the web area of greatly between the two Argyrodes (Fig. 2). that host, i.e., The peak occurrence of adult A. flavescens = Ays S was found in autumn while that ofA. bonadea N, A, Nj, • was in spring and early summer. In areas where Aj is the total web area of host species where Nephila clavata was absent, the differ- MIYASHITA—DYNAMICS OF KLEPTOPARASITIC SPIDERS 33 in sites 5 in spiders web other and species Nephila two the of areas web and species, Argyrodes two the of numbers the of dynamics Seasonal — 1. Figure Okinawa. S9poj^8jY JO ’o^ THE JOURNAL OF ARACHNOLOGY 34 BothNephila present Nephila clavata absent Month — Figure 2. Percentage of adult Argyrodes in areas ;vith and without Nephila clavata. Numerals in the figure represent sample size. ence was less conspicuous due to the high per- in November were small plant hoppers in all centage of adult A. flavescens in spring. Ar- study sites. gyrodes bonadea showed a similar seasonal DISCUSSION pattern in the two types of areas. — A Host preference ofArgyrodes. total of The dynamics of the two Argyrodes species 18 species of web spiders was recorded in- were largely affected by the phenologies of cluding all sites and seasons (Table 1). Twelve Nephila species. This is clearly illustrated by species were found to be hosts for A. flaves- the following findings: 1) where there is no cens, and 14 were hosts for A. bonadea. N. clavata (NK and IH), densities of Argyro- The results of the binomial tests (Table 2) des declined rapidly in November when N. revealed that A. flavescens had a strong ten- maculata had disappeared; but where both Ne- dency to prefer Nephila clavata in August and phila species were present, the density in- November, although no preference was found creased in November for A. flavescens and de- in July when Nephila clavata was still small creased slightly for A. bonadea’, 2) preference in body size. Nephila maculata was preferred for Nephila webs was prominent, especially in July probably because Nephila was already by A. flavescens. The first finding is particu- large. Besides the two Nephila species, only larly good evidence for the importance of Ne- Argiope minuta was preferred significantly. phila on Argyrodes dynamics because this can Leucauge blanda^ and Cyclosa confusa had be viewed as a “natural experiment” in which significantly fewer A. flavescens on their webs one major host was “removed”. Grostal & than expected from their web areas. Walter (1999) revealed a similar result show- Argyrodes bonadea also preferred N. cla- ing that Nephila spp. were the preferred hosts vata in August and November, but the pref- for A. antipodianus. The reason why Nephila erence for N. maculata was obscure. Unlike webs are suitable for Argyrodes may be that A. flavescens, Cyrtophora moluccensis, which these webs have a barrier web on both sides builds large, horizontal and tightly-meshed of the capture web, providing a space for liv- webs, was a preferred host for A. bonadea. ing. The significance of barrier webbing for Leucauge blanda had fewer A. bonadea than Argyrodes has already been argued by several & expected from its web area. — researchers (Whitehouse 1986 1997; Can- Prey density on host webs. Figure 3 gialosi 1997). Comparing the two Nephila shows seasonal changes in prey density on species, N. clavata has a more elaborate bar- Nephila webs. In all areas, prey density on rier web and N. maculata sometimes lacks a host webs increased in November and then de- barrier web (unpub. obs.). This may explain creased markedly in January. The main prey why N. clavata was preferred more frequently > A— MIYASHIT DYNAMICS OF KLEPTOPARASITIC SPIDERS 35 ^ & S+ r C3 Cu S c^ K •a e ^ S ^3 •2 ^ ^ ^ ^ " Eg + + + + ^ " II S ^ +s ^ S + + + CO S S O 3 "O 5: Q ”0 U + + + CO oa ,§• DO cC« Cj S ^ O ^ to + + + + + + + +I + IIII II o 00 S " ^ s CO CO o + + + + + + + 3 C3O ffi Oi -^§ G O0) SS KQ - (U -S -Cl + + + + + + I O'llO) S TC3 K !3S3 3 + + + + + + 3 A I I 5 CO ^ " II 'o o ^ ^ (DU- Us + c co Co Co o 3 ^ -a ^ + + + s § U s?,p I CO ^^ 5 Co s o o CeX) ^<5 +=i -I-' 3 CoO (U U t-* ^ ^o ^II II 0 C+^ + + + + + s S D CO ^ 5^ s 0) -g u CSo" ^0CC0OO- ^-g3oo CeCoo + + + ^ +-r -+r -+r soa •'CC2Clo *- e 3 s ffi O c> 1 ^ -Ci I Co 1 H Co Co +I + + + 2 + + + + + S s0) g Cl g H oo O 4=9 ^ Z Sp:^ K^-, S 2i 36 THE JOURNAL OF ARACHNOLOGY — Table 2. Results of binomial test to assess whether each Argyrodes species prefers a particular host spider. The null hypothesis is that an Argyrodes chooses a host spider in proportion to its web area. Positive signs mean preference (+ ++ = p < 0.001, ++ = p < 0.01, + = p < 0.05), negative signs mean avoidance ( = P < 0.001, = P < 0.01, — = p < 0.05). Abbreviations for species name are the same as in Table 1. Argyrodesflavescens Host species Site Month Nm Nc Av Cm Lb Ns Cc Am NK Aug +++ — ns — NG .Jul ns ns ns Aug ++ + Nov ++ ns ns SH Jul ++ + ns —ns ns Aug ns + + + ns Nov ns + + + + + NJ Jul Aug ns ns + Nov ++ — -h IH Aug Argyrodes bonadea Host species Site Month Nm Nc Av Cm Lb Ns Cc Am NK Aug ++ — ns NG — Jul ns ns ns Aug ns +++ ns Nov — + ns ns SH Jul ns ns ns — Aug + + A Nov ns ns ns ns ns NJ Jul ns ns -h Aug ++ + + ns Nov + ns IH Aug ns ns than N. maculata by the two Argyrodes, Other that of A. flavescens. This difference may be studies have shown that Argyrodes spiders oL due to interspecific competition between the ten live in Nephila webs (e.g., Elgar 1993) but two Argyrodes species. Miyashita (2001) only a few of them have demonstrated the sea- demonstrated that experimental removal of A. sonal dynamics of Nephila-Argyrodes sys= flavescens increased number of A. bonadea terns. Vollrath (1987) showed that the dynam- within only 2 d, and the number of individuals ics of A. elevatus and A, caudatus were removed was positively correlated with the closely related to the number of N. clavipes in rate of increase in A. bonadea. Although this Panama, yet no evidence was provided show- experiment indicated interspecific competition ing that alternative host spiders were not re- on a small spatial scale, this effect is likely to sponsible for this pattern. The present study extend up to regional scales. There is addi- clearly demonstrates the importance of Ne- tional circumstantial evidence supporting the phila as hosts for Argyrodes both from the likelihood of interspecific competition. In a “natural experiment” and preference analysis. temperate area where only A. bonadea was Another interesting point in the population present, Yasuda (pers. comm.) found that this dynamics of the two Argyrodes is that the species is most abundant in mid-October peak density of A. bonadea was earlier than which is the late adult period of N. clavata A— MIYASHIT DYNAMICS OF KLEPTOPARASITIC SPIDERS 37 by consuming prey abundant on host webs but adjusts its life cycle by retarding its develop- ment. It appears that A, flavescens has a more opportunistic life cycle strategy than A. bonadea. From winter to spring when the main hosts were absent, Argyrodes spiders were found to live on the webs of smaller orb-weavers such as Leucauge blanda, Cyclosa confusa and Gasteracantha mammosa, which were not preferred in the presence of Nephila. White- house (1988) found that the host range of A. — antipodiana in winter was larger than that in Figure 3. Seasonal change in prey density (no./ growing and reproductive seasons, probably web area) on host spider webs. The 3 sites shown here have both of the two Nephila species. because overwintering individuals need webs for shelter only. However, the situation of Ar- gyrodes in the present study is quite different because I often observed Argyrodes ingesting and 2 mo behind the peak of the web area. silk of host webs as well as stealing prey (un- On Okinawa, however, A. bonadea showed a pub. obs.). The difference is mainly due to peak in late August and the density decreased climate conditions: the present study was in November, the beginning of the adult pe- made in the sub-tropics whereas the study by riod in Okinawa. This means that A. bonadea Whitehouse was in a temperate region. Al- living in regions without A. flavescens showed though it seems unlikely that sub-tropical Ar- host-parasite dynamics similar to A. flaves- gyrodes can obtain sufficient food in winter, cens. Accordingly, interspecific competition they may be able to survive the harsh period by A. flavescens may have shifted the dynam- by living on unfavorable hosts. Grostal & ics of A. bonadea to earlier seasons. An alter- Walter (1999) found no A. antipodianus on native explanation is that the life cycle of A. webs of Leucauge sp. and Gasteracantha sp. bonadea in sub-tropical Okinawa is different in Australia but the season they studied was from that of the temperate area, which is un- the period when the main host Nephila was related to competitive interactions with A. fla- present. It seems necessary to clarify the role vescens. It would be difficult to test whether of non-preferred host for the maintenance of there is a causal relationship between the dy- Argyrodes populations. namics of the two Argyrodes species because ACKNOWLEDGEMENTS large scale experimental manipulation is necessary. I thank Mary Whitehouse for comments on Host composition appears to have a minor the manuscript, and Akira Shinkai, Takafumi impact on the age structure of Argyrodes, es- Chida, Aya Shimazaki, Yasunori Maezono pecially for A. bonadea (Fig. 2). The increase and Claire Cartan for assistance in the field. in the proportion of adults in spring in areas This research was supported by Eujiwara Nat- without N. clavata might have been an artifact ural History Foundation. due to the small sample size (N = 8). Adults LITERATURE CITED of A. flavescens were found throughout the year but the peak was in autumn when prey Cangialosi, K.R. 1997. Foraging versatility and the on host webs were most abundant. If the in- influence of host availability in Argyrodes tri- crease in prey availability had already been gonum (Araneae, Theridiidae). Journal of Arach- nology 25:182-193. initiated in October, this can explain the high- Elgar, M.A. 1993. Inter-specific associations involv- er proportion of adults in November, because ing spiders: Kleptoparasitism, mimicry and mu- spiderlings ofA. flavescens can reach maturity tualism. Memoirs of the Queensland Museum and produce egg sacs in a month (unpub. 33:411-430. obs.). Contrarily, adults of A. bonadea were Grostal, P. & D.E. Walter. 1999. Host specificity rarely found in autumn, suggesting A. bona- and distribution of the kleptoparasitic spider Ar- dea does not accerelate its developmental rate gyrodes antipodianus (Araneae, Theridiidae) on THE JOURNAL OF ARACHNOLOGY 38 orb webs in Queensland, Australia. Journal of Vollrath, F. 1987. Kleptobiosis in spiders. In Eco- Arachnology 27:522-530. physiology of Spiders. Nentwig W. ed, pp 274- & Larcher, S.R. D.H. Wise. 1985. Experimental 286, Springer-Verlag, Berlin. studies of the interactions between a web-invad- Whitehouse, M.E.A. 1986. The foraging behaviours ing spider and two host species. Journal of Ar- of Argyrodes antipodiana (Theridiidae), a klep- achnology 13:43-59. toparasitic spider from New Zealand. New Zea- Miyashita, T. 2001. Competition for a limited space land Journal of Zoology 13:151-168 in kleptoparasitic Argyrodes spiders revealed by Whitehouse, M.E.A. 1988. Factors influencing field experiments. Population Ecology 43:97- specificity and choice of host in Argyrodes an- 103. tipodiana (Theridiidae, Araneae). Journal of Ar- & Sokal, R.R. F.J. Rohlf. 1995. Biometry, 3rd ed., achnology 16:349-355. W.H. Freeman, New York. Whitehouse, M.E.A. 1997. The benefits of stealing Tanaka, K. 1984. Rate of predation by a kleptopar- from a predator: foraging rates, predation risk, asitic spider, Argyrodes fissifrons upon a large and intraspecific aggression in the kleptoparasitic host spider, Agelena limbata. Journal of Arach- ?,^'\dQVArgyrodes antipodiana. Behavioural Ecol- nology 12:363-367. ogy 8:663-667. Trail, D.S.S. 1980. Predation by Argyrodes (Theri- diidae) on solitary and communal spiders. Psy- Manuscript received 1 August 2000, revised 10 che 87:349-355. May 2001.

POPULATION DYNAMICS OF TWO SPECIES OF KLEPTOPARASITIC SPIDERS UNDER DIFFERENT HOST AVAILABILITIES

Similar POPULATION DYNAMICS OF TWO SPECIES OF KLEPTOPARASITIC SPIDERS UNDER DIFFERENT HOST AVAILABILITIES