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Keywords:

  • cooperation;
  • group foraging;
  • group living;
  • insect size;
  • social spiders

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • 1
    Social species in the spider genus Anelosimus predominate in lowland tropical rainforests, while congeneric subsocial species occur at higher elevations or higher latitudes.
  • 2
    We conducted a comparative study to determine whether differences in total biomass, insect size or both have been responsible for this pattern.
  • 3
    We found that larger average insect size, rather than greater overall biomass per se, is a key characteristic of lowland tropical habitats correlating with greater sociality.
  • 4
    Social species occupied environments with insects several times larger than the spiders, while subsocial species nearing dispersal occupied environments with smaller insects in either high or low overall biomass.
  • 5
    Similarly, in subsocial spider colonies, individuals lived communally at a time when they were younger and therefore smaller than the average insect landing on their webs.
  • 6
    We thus suggest that the availability of large insects may be a critical factor restricting social species to their lowland tropical habitats.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The characteristically tropical distribution of social taxa in a variety of animal groups, from wasps and social spiders to communal breeding birds, has long been a puzzle for evolutionary biologists and ecologists (e.g. Brown 1987; Reeve 1991; Avilés 1997). The association between low latitudes and sociality is particularly striking` in spiders, as all currently known cooperatively social species are primarily tropical (Krafft 1979; Buskirk 1981; Avilés 1997). In these species, variously named quasisocial (Wilson 1971), non-territorial, permanent social (D’Andrea 1987; Avilés 1997), cooperative (Avilés 1997; Whitehouse & Lubin 2005), or simply social (this paper), colony members cooperate in building and maintaining a communal web, sharing their food, and caring for brood. In contrast, only subsocial species (also known as non-territorial periodic-social) occur in the temperate zones (Avilés 1997; but see Furey 1998 and Jones et al. 2007, for a partial exception). In cases where such patterns have been studied (L. Avilés, in press), the latitudinal association with level of sociality is mirrored by an altitudinal one. In America, social Anelosimus (Theridiidae) species in lowland tropical rainforests (e.g. Avilés et al. 2001) are substituted progressively by subsocial species as either elevation or latitude increase, with social and subsocial species coexisting in some areas of intermediate latitude or elevation (Agnarsson 2006; L. Avilés, in press).

In subsocial species, females typically establish nests as solitary individuals and raise their offspring without the aid of others (reviewed in Kullman 1972; Krafft 1979; Buskirk 1981; D’Andrea 1987). Following their mother's death, siblings remain together for variable periods of time cooperating in prey capture and sharing food, but they disperse prior to reaching reproductive maturity. Subsocial spider colonies contain at the most a few dozen individuals. Social spider colonies, in contrast, may grow to contain hundreds to tens of thousands of spiders as colony members typically reproduce within the natal nest generation after generation. Dispersal to establish new nests occurs only after a colony has reached a relatively large size and involves females who have been inseminated within their natal nest (reviewed in Avilés 1997). Recent phylogenetic analyses (Agnarsson 2006; Agnarsson et al. 2006; Johannesen et al. 2006; Agnarsson, Maddison & Avilés 2007) support the long-held view that social spiders arose from subsocial ancestral lineages and that subsociality arose from solitary living (Kullman 1972; Krafft 1979; Kraus & Kraus 1988; Avilés 1997). Thus, extant subsocial species not only exhibit an intermediate form of sociality, but they also resemble the ancestral system from which their social congeners originated.

Here, we examine the hypothesis that the latitudinal and altitudinal patterns of sociality observed in the spider genus Anelosimus may be related to the availability and size of prey in different environments. We explore whether total biomass, insect size or both are characteristic of areas of greater spider sociality. Social spiders might be absent from environments that are low in available prey biomass because of a lack of sufficient resources to support large social colonies (e.g. Rypstra 1986; Ruttan 1990; Avilés & Gelsey 1998; Powers & Avilés 2003) and because group foraging, with its reduction in prey consumption variance (Caraco 1981; Clark & Mangel 1986; Caraco et al. 1995), should be disfavoured in such environments (e.g. Uetz & Hodge 1990; Uetz 1992). Alternatively, even in environments with abundant resources, spiders may live solitarily if they are able to access those resources without the aid of others, i.e. prey biomass is contained for the most part in insects that are small enough to be caught by single individuals. Because social and subsocial spiders cooperate in the capture of insects that are too large for single individuals to subdue (Nentwig 1985; Ward 1986; Rypstra 1990; Rypstra & Tirey 1991; Pasquet & Krafft 1992; Jones & Parker 2000; Kim, Krafft & Choe 2005), the distribution of available prey sizes becomes an additional parameter to be considered when trying to understand the geographical distribution of spider sociality.

To discriminate between these possibilities, we assessed the abundance and size of insects captured by colonies and present in the habitats where either social or subsocial Anelosimus species occur – a dry riparian temperate habitat in Arizona where one subsocial species occurs, a relatively high-elevation (~2100 m) cloudforest site in eastern Ecuador where one subsocial species occurs, and a lowland tropical rainforest site in eastern Ecuador (~450 m) with at least two social species (Table 1). Four predictions can be made based on our hypotheses: (1) if high total biomass is a key characteristic favouring sociality, we expect that social species will be exposed to higher overall biomass, but not necessarily larger insects, than subsocial species in their respective environments; (2) alternatively, if large prey size is the primary requirement, we expect that social species will be exposed to larger insects, in either low or high total biomass, than subsocial species; or (3) if both total biomass and prey size matter, we expect that social species will be exposed to both greater biomass and larger insects than subsocial species. Similarly, when comparing early and late stages in the life cycle of subsocial species, we expect that (4) subsocial colonies in their early communal stage will experience higher prey abundance and/or larger relative prey sizes than subsocial colonies approaching the dispersal phase.

Table 1.  Study localities: for the social A. eximius and A. domingo: Jatun Sacha, Napo, Ecuador, 1·07° S, 77·61° W, 450 m, lowland tropical rainforest, average daily temperature 25 °C; for the subsocial A. baeza: Yanayacu, Napo, Ecuador, 0·60° S, 77·87° W, 2073 m, cloudforest edge, 17 °C except in July–August when 15·5 °C; for the subsocial A. arizona: Garden, Canyon, Arizona, USA, 31·49° N 110·32° W, 1524 m, Arizona riparian, average monthly precipitation 33 ± 16 mm, but highly variable across months and years
Field siteSeasonality*Spider phenologyDates and no. of colonies studied
  • *

    Approximate average monthly precipitation or temperature.

Jatun SachaOct.–Feb.: ‘dry’ (232 ± 20 mm)Aseasonal, all stages available at all times.Jan. 2002: n = 6 exi; n = 3 dom
March–June: rainy (364 ± 23 mm) June 02: n = 4 exi, n = 3 dom
July–Sept.: intermediate (286 ± 22 mm) May–June 03: n = 5 exi August 01: n = 14 exi; n = 3 dom
YanayacuDec.–Feb.: dry (146 ± 22 mm)Maternal care and early communal phaseFeb. 2002: n = 83
March–Sept.: rainy (327 ± 33 mm)Communal, late communal, early dispersalJune 2002, n = 66; June 03, n = 38 August 01, n = 94
Oct.–Nov.: intermediate (207 ± 23 mm)Late dispersal and mating 
Garden CanyonSept.–Nov.: autumn (17 °C)Maternal care and early communal phaseOct. 2000: n = 60; Sept. 2003: n = 30
Dec.–Feb.: winter (10 °C)Communal phase 
March–May: spring (17 °C)Late communal phase and dispersalApril–May 2001: n = 61
June–August: summer (24 °C)Mating and egg laying 

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

study system

We studied the social Anelosimus eximius Keyserling and A. domingo Levi (Levi 1963; Agnarsson 2006) at the Estación Biológica Jatun Sacha in eastern Ecuador (Table 1). At this site, A. domingo builds nests in the forest understorey, while A. eximus builds them both in the forest understorey and along the forest edge (Purcell & Avilés 2007). Both species have a similar social system, with colonies that last for multiple generations (reviewed in Avilés 1997 and Avilés et al. 2001). A. domingo, however, is a much smaller spider (female total length 3·2 mm vs. 4·7 mm for A. eximius, Avilés et al. 2001) and its colonies grow only into the thousands, while those of A. eximius may grow into the tens of thousands. The life cycles of both species are not correlated with seasonal patterns or with each other, as colonies in different stages co-occur at all times (L. Avilés, unpublished observations) (Table 1). We studied these species at times of the year corresponding to rainy, dry, and transition from rainy to dry seasons (Table 1).

In contrast, the subsocial species that we studied, A. arizona Agnarsson and A. baeza Agnarsson (Agnarsson 2006), exhibit seasonally synchronized phenologies at our study sites (Avilés & Gelsey 1998; K. S. Powers, unpublished observations; for other publications on these species, with different taxonomic names, see Powers & Avilés 2003; Klein, Bukowski & Avilés 2005; Avilés & Bukowski 2006, for A. arizona, and Nentwig & Christenson 1986, for A. baeza). We studied A. arizona at a dry riparian area in southern Arizona (Table 1). At this site, colonies are most abundant within 10–20 m of a perennial creek. Colonies are initiated in late summer by solitary females who lay a single egg sac (Avilés & Gelsey 1998). Mothers care for their offspring during early offspring development, but mothers die before the onset of winter. Spiderlings remain together until late spring, when they disperse as late-stage juveniles to young adults and establish individual webs. We studied this population during the early communal stage, when colonies contained adult females and their offspring, and during the late communal stage when later instar juveniles and subadults approached dispersal (Table 1).

We studied the subsocial A. baeza at a tropical mid- to high-elevation (2100 m) cloudforest site in eastern Ecuador (Table 1), where colonies occur in secondary growth and along roads but not inside the forest. At this site, A. baeza forms larger colonies and exhibits more cooperation and nest sharing among older instars than A. arizona (K. S. Powers, unpublished data). Females produce new clutches during the dry season (Table 1), with multiple females occasionally sharing a nest. Colonies are less synchronized during the rainy season, when older juveniles and subadults can be found in communal nests and also in solitary webs. Communal webs may also be cohabited by adult males, adult females and spiderlings at this time. We studied the Yanayacu population once during the early communal phase and three times when colonies containing either late juveniles and subadults (June 2002 and June 2003) or subadults and adults (August 2001) approached dispersal (Table 1).

insects in the environment

We used no-kill Malaise traps (Malaise 1937 and Marston 1965, cited in Buskirk & Buskirk 1976) to assess the abundance and size of insects in the habitats occupied by the social and subsocial spiders. In a separate study, we found that Malaise traps compare favourably with other methods in their effectiveness at detecting insect size differences across environments (Guevara & Avilés 2007). We positioned traps (trapping area = 6244 cm2) within 2–3 m of and at a similar height to the social or subsocial spider colonies. Every 3 h throughout the day for 3–5 days during each field expedition (Table 1), we recorded the order and length of insects caught in the traps (all insects were removed from a trap prior to a new 3-h period). We extended our censuses into the night for a subset of the observation periods at each site (cloudforest, June 2003; rainforest, May–June 2003; Arizona, April–May 2001). For the three Ecuadorian species in May 2003 and for A. arizona in September 2003, we conducted additional hourly censuses in which we did not remove insects between censuses to determine how long they remained in traps. Because we found variability in the time that different taxonomic orders remained in the traps (F9,177 = 3·28, P = 0·0007; Figure S1 in supplementary material), when estimating average number of insects caught per hour per unit area, we weighted each insect recorded by the inverse of the estimated time that insects of that order remained in traps. We estimated prey dry biomass from insect length using Sage's (1982) regression equations, which take into account the different shapes characteristic of insects of different orders.

prey caught by colonies

We assessed independently prey caught by colonies. For each species, the number of colonies monitored (Table 1) was a function of how many could be reached within the 3-h census interval and the frequency at which colonies caught prey. In subsocial species, colonies occur at high densities and capture prey rarely, so many colonies were monitored. In social species, colonies occur at low densities but capture prey frequently, so fewer colonies were monitored. As with insects caught in traps, we recorded the order and body length of captured prey, with prey capture being characterized by freshly dead insects on which at least one spider was feeding. To account for prey items that may have been consumed during the intercensus interval, a correction factor was applied based on the relationship between prey size and feeding duration (see Appendix S1, Supplementary material).

colony size and biomass estimations

We estimated the numbers and ages of spiders in a nest by either counting spiders directly in the field when nests were small with few spiders (the two subsocial species), by collecting nests and sorting spiders from their nests materials when nests were larger or had complex age structures (some nests of both subsocial species), or by using previously determined relationships between nest size and spider number (Fig S2, Supplementary material), along with observed proportions of the different age classes in the nests (the two social species and the largest nests of A. baeza). To estimate colony biomass, we measured to the nearest 0·1 mg the wet weight of a sample of individuals of different age classes – adult females, subadult females, adult males, subadult males, older juveniles, younger juveniles and spiderlings – using an AG104 Metler Toledo (Columbus, OH, USA) balance. We then multiplied the appropriate mass – converted to dry mg using a relationship derived from Sage (1982) – by the estimated numbers of spiders in each age class in a colony.

data analysis

We estimated four aspects of insects sampled from the environment and caught by colonies: probability of capture (at least one insect), number of insects and total biomass caught per hour, and mean insect mass (in mg). For traps, number of insects and biomass per hour were analysed per m2. For colonies, insects per hour was analysed per capita, while prey biomass per hour was analysed per unit colony biomass (prey mg hour−1 colony mg−1) to account for body size differences across species. Prey sizes were also analysed relative to mean size of the spiders in a colony at the time of prey capture observations (mean prey mg mean spider mg−1). Given the lack of seasonality of the spiders themselves (Table 1) and lack of significant differences in our insect abundance and size measures across seasons at our lowland tropical site (F1,65 = 0·68, P = 0·51 for prey density; F1,58 = 0·56, P = 0·57 for prey size, F1,65 = 0·01, P = 0·99 for prey biomass h−1), we combined year-round samples of this habitat for further analyses.

Analyses of insects sampled from the environment use averages of our insect size and abundance measures caught by a trap over a day or night period. We tested the effect of habitat type with a mixed-model analysis of variance (anova) followed by Tukey–Kramer (a posteriori) multiple comparisons tests to determine which means were significantly different from one another. In order to account for the repeated measures taken from each trap over several day and night periods, day–night was nested within trap ID, and trap ID, nested within habitat type, was set as a random effect. In the analyses, daily average insect sizes were natural log-transformed and weighted by the number of insects entering into the estimate and daily density and total biomass were square root-transformed and weighted by the number of hours the traps were up (range 3–12 h day−1 or night period). Weighting accounts for the fact that a greater number of insects or more hours of observation should produce more precise estimates.

For prey caught by colonies, we averaged across all census periods to obtain a single colony estimate of our prey capture variables (day and night censuses were combined in a single estimate following a preliminary mixed-model anova that yielded no significant day–night effect on our variables: F3,204 = 2·1, P = 0·10 size of prey caught; F3,249 = 1·8, P = 0·16 for number of insects captured per hour, with day–night and colony ID nested within species and the latter set as a random effect). In our analyses, we weight colony means by the number of insects entering into the estimates (for the absolute and relative insect size analyses) or by the number of times a colony was censused (for the probability of capture by colonies, number of prey caught per spider, and total prey biomass per spider biomass analyses). We used one-way anova, followed by independent contrasts (social vs. subsocial species), to compare those variables whose distributions could be normalized by means of log-transformations (absolute and relative prey sizes). Because prey capture was not observed for many of the subsocial spider colonies even after several days of being monitored, distributions involving frequency of prey capture could not be normalized, so nonparametric tests were performed. All means are reported ± standard error.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

subsocial species approaching dispersal vs. social species

Insects sampled from the social species lowland tropical rainforest habitat were considerably larger on average than those from the cloudforest or Arizona riparian habitats (Fig. 1a) (F2,54 = 7·4, P = 0·0014, R = 0·33, for the comparison across the three habitats). Insect density (insects h−1 m−2) and overall biomass (mg h−1 m−2), however, were greater in samples from the cloudforest than in samples from the other two habitats (Fig. 1b,c) (insect density F2,56 = 13·1, P < 0·0001, R = 0·36; total biomass: F2,56 = 6·1, P = 0·004, R = 0·23).

image

Figure 1. Insect size, density and total biomass in the habitats of A. eximius and A. domingo (rainforest), A. baeza (cloudforest) and A. arizona (temperate riparian). Shown are least square means of malaise trap sample averages (insects collected by a trap during a day or night period) estimated using mixed model anovas (see Methods) on (a) natural log-transformed average insect sizes (dry mg), (b) square root-transformed insect density (number of insects flying per hour through a 1 m2 area) and (c) square root-transformed total insect biomass (insect dry mg flying per hour through a 1 m2 area). Means that are significantly different in a posteriori multiple comparisons (Tukey–Kramer honest significance difference test) shown with different letters.

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Considering prey caught by colonies (social species all year, subsocial species approaching dispersal), the social species captured much larger insects relative to the average size of spiders in their nests than did the subsocial species (contrast A. eximius vs. A. baeza: F1,75= 33·2, P < 0·0001; vs. A. arizona: F1,75 = 42·9, P < 0·0001; contrast A. domingo vs. A. baeza: F1,75 = 5·0, P = 0·03; vs. A. arizona: F1,75 = 13·9, P = 0·0004) (Fig. 2a). The two social species captured prey on average six times their body size (prey to spider ratio, A. eximius: 6·1, 4·8–7·7, 95% CI; A. domingo: 6·3, 1·6–24·0, 95% CI), while the subsocial species captured prey the same size or slightly smaller than the average spider in their nests (A. baeza: 1·3, 0·8–1·9, 95% CI; A. arizona prey to spider ratio: 0·3, 0·1–0·8, 95% CI). Prey to spider ratios (prey mg−1 spider mg−1) reflected both differences in the size of the spiders and of the insects they caught (Fig. 2b,c).

image

Figure 2. Sizes of prey captured by colonies in relation to spider body mass during colony census periods (all year for socials, period approaching dispersal for subsocials). Shown are back-transformed (from natural logarithms) mean colony averages of (a) relative prey mass (back-transformed from mean ln(mean prey mg/mean spider mg), (b) mean prey mg and (c) mean spider mg. Spider mass reflects number and size of the spiders present in a nest at the time of prey capture observations; insect biomass are colony averages obtained over several day/night observation periods. Bars represent standard error.

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Failure of a colony to capture any prey during the observation periods was also much less frequent in the social than in the subsocial species, despite the lower insect density in the environment of the social species (% colonies failing to capture any prey: 13 vs. 48 vs. 70 vs. 77, for A. eximius, A. domingo, A. baeza and A. arizona, respectively, likelihood ratio χ2 = 499·0, P < 0·0001; all pairwise comparisons P < 0·008, which adjusts for six comparisons). On a per capita basis, however, because prey had to be divided by a greater number of individuals, social species overall did not necessarily perform better than subsocial ones. Variance in colony prey capture success (number of insects and biomass captured h−1 per spider or per spider mg) was greatest in A. arizona, followed by A. baeza and A. eximius, and was lowest in A. domingo (Barlett test F3,211 = 42·5, P < 0·0001, for prey numbers; F3,211 = 7·9, P < 0·0001, for prey biomass).

early vs. late colony stages in subsocial species

In both subsocial species, colonies in the early communal stages containing young juveniles and their mother exhibited greater probability of capturing prey (A. baeza likelihood ratio χ2 = 88·7, P < 0·0001; A. arizonaχ2 = 130·0, P < 0·0001) and captured more prey items per capita (A. baeza: χ2 = 10·7, 1 d.f., P = 0·001; A. arizona: χ2 = 6·2, 1 d.f., P = 0·01) and greater prey biomass per colony biomass (A. baeza: χ2 = 13·5, 1 d.f., P = 0·0002; A. arizona: χ2 = 11·2, 1 d.f., P = 0·0008) than later-stage colonies with older juveniles and subadults approaching dispersal. These differences were present, even though the environments of both species did not differ in the density or overall biomass of insects caught by traps at these two times (insect numbers h−1 m−2, cloudforest F1,26 = 1·4, P = 0·26; Arizona riparian F1,27 = 1·2, P = 0·28; mass h−1 m−2, cloudforest F1,26 = 0·1, P = 0·74; Arizona riparian F1,27 = 0·01, P = 0·91).

In both species colonies in their early communal phase caught prey that was considerably larger relative to the average size of the spiders in the nests than colonies approaching dispersal (prey to spider ratio A. baeza, early: 4·4, 2·7–7·1, 95% CI; late: 1·3, 0·8–1·9; F1,61 = 15·4, P = 0·0002; A. arizona, early: 4·8, 2·5–9·0; late: 0·3, 0·1–0·7; F1,27 = 28·0, P < 0·0001) (Fig. 3). In A. baeza, this effect reflected the smaller size of spiders in young colonies, as prey caught by colonies did not differ in size between the early and late colony stages (F1,83 = 2·3, P = 0·13). In A. arizona the effect was due both to the smaller size of young spiders as well as to the larger absolute size of prey caught by colonies in the early communal stages (F1,28 = 30·4, P < 0·0001). The latter effect is particularly interesting, given that insects in the Arizona riparian trap samples did not differ in size between these two time-periods (F1,20 = 0·3, P = 0·61).

image

Figure 3. Size of captured prey relative to mean spider size in colonies of the subsocial species A. baeza and A. arizona during their early communal phase vs. the stage when spiders were approaching the dispersal phase. Units as in Fig. 2a.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

By studying social and subsocial Anelosimus species and their habitats, we examined the hypothesis that the geographical distribution of spider sociality may reflect differences in potential insect prey in different environments. In particular, we explored whether high overall insect biomass, large insect size, or both, may be involved in enabling the development of large social colonies in areas where only social species occur. We found that large insect size, rather than greater overall insect biomass per se, is a key characteristic of lowland tropical habitats that correlates with greater spider sociality. Consistent with this observation, we found that during the early communal phase of the subsocial species, when spiders are small, the relative size of the insects they caught was comparable to prey caught by fully grown social spiders in their lowland tropical habitat. As subsocial species approached the dispersal phase, however, spiders were no longer smaller than the average insect landing on their webs. We suggest, therefore, that lack of a sufficient supply of large insects at higher elevations and higher latitudes may be a critical factor restricting social species to their lowland tropical habitats.

prey abundance and size in relation to spider sociality

Insect samples from a lowland tropical habitat in Ecuador where only social Anelosimus species occur were characterized by large average insect sizes, but not necessarily high overall insect biomass, while samples from a higher elevation habitat in Ecuador and a higher latitude habitat in the southern United States, where only subsocial species occur, were characterized by smaller average insect sizes and either high or low total biomass. In contrast to the expectation that subsocial species would be found inhabiting environments with low overall biomass, the cloudforest habitat of the subsocial A. baeza had the highest numbers of prey and greater total prey biomass than the other two habitats.

The latter finding contrasts with the prediction of risk-sensitive foraging theory that group foraging would be favoured in environments where resources are high enough to meet the needs of the average individual (Caraco 1981; Clark & Mangel 1986; Uetz & Hodge 1990; Caraco et al. 1995). Cooperative social spiders, however, may not meet the assumptions of risk-sensitive foraging theory because their groups concentrate individuals in spaces that are orders of magnitude smaller than those occupied by the equivalent number of individuals living solitarily (J. Purcell & L. Avilés unpublished data). Given that spider colonies are limited to capturing prey that contact their webs, the concentration of individuals into smaller spaces should reduce per individual prey encounter rates and, other things being equal, per capita prey intake rates.

Other things would not be equal, however, in environments where there is a sufficient supply of prey that are too large for solitary individuals to capture, as in the lowland tropical rainforest (Fig. 1a). In such environments, cooperative prey capture would allow individuals in dense social groups access to resources that are inaccessible to solitary spiders. This would magnify what can be extracted from the environment in relatively small physical spaces, facilitating the development of groups that grow over multiple generations. For a variety of cooperative foragers, including lions (Caraco & Wolf 1975), wolves (Nudds 1978), tree-killing bark beetles (Berryman et al. 1985; Raffa & Berryman 1987), killer whales (Baird & Dill 1996) and others, groups are predicted to occur and are often found in environments with resources that require coordinated group efforts for their capture (see also Packer & Ruttan 1988). Competition is reduced in such systems by prey being too large and/or too ephemeral for single individuals to consume solitarily (Clark & Mangel 1986; Rypstra & Tirey 1991).

The idea that environments with large potential insect prey favour sociality in spiders is supported further by the patterns observed within the subsocial species. Although insect availability and size changed little between the early communal stage and the predispersal stage in the subsocial species (see Results), the way in which spiders experienced prey differed between these stages by virtue of their growth as the season progressed. Spiders lived communally and cooperated when they were small relative to insects contacting their webs, but dispersed once they matched or surpassed the size of the typically available prey (Fig. 3).

We note that the use of malaise traps in our study provides a conservative test of the large prey hypothesis because malaise traps are likely to miss the largest insect size classes, which multiple sampling techniques confirm are considerably more common in the lowland rainforest (Guevara & Avilés 2007). Inclusion of such large size classes in our samples would thus only magnify the patterns we have detected. Absence of the largest insect size classes in our samples may also result in underestimation of the total biomass potentially available to the spiders, especially in the lowland rainforest. Such underestimation, however, would not affect our conclusion that high total biomass alone is not sufficient to enable the formation of large social colonies, as social spiders are absent from the upper elevation cloudforest, where we found total biomass to be high but insects small. We also note that our argument does not imply that the lowland rainforest does not contain enough small insects to support solitary spiders, as there are plenty of solitary species in this habitat. Our argument is, rather, that the existence of a large supply of large insects in this habitat provides an incentive for the development of cooperative spider societies and that the absence of such a supply in higher elevations or latitudes may preclude the expansion of species with large social groups into those areas, at least in the genus Anelosimus.

sociality and prey capture

The ability to access large prey is a well-known benefit of cooperative foraging in spiders (Nentwig 1985; Rypstra 1990; Rypstra & Tirey 1991; Uetz 1992; Kim et al. 2005) and other organisms (Caraco & Wolf 1975; Nudds 1978; Raffa & Berryman 1987; Baird & Dill 1996). Group foraging may also increase prey capture efficiency in general (e.g. McMahon & Evans 1992). In the colonial non-cooperative spiders, which form a network of closely packed individual webs, insects that may have otherwise escaped ‘ricochet’ between webs until they become ensnared and captured by a spider (Uetz & Hodge 1990; Uetz 1992). In the cooperative spiders, increase in efficiency results not only from the cooperative nature of prey capture itself, but also because social groups, albeit concentrated in smaller physical spaces than the equivalent number of solitary individuals, present a greater surface for the interception of flying insects than single solitary webs do. Therefore, even though the lowland tropical rainforest had lower insect densities than the high elevation cloudforest (Fig. 1b), the fraction of colonies failing to capture any insects during the study periods was significantly lower in the social than in the subsocial species (see Results). Similarly, in the subsocial species the cooperative nature of prey capture during early communal stages of the colonies may have contributed to the greater number of prey per capita the colonies captured during those stages relative to phases approaching dispersal (see Results) or relative to solitary individuals following dispersal (data not shown). Given size differences between the spiders and their potential prey, either because insects in some areas are large or because young spiders are small, the net result in both of these comparisons was more efficient extraction of the available resources in the social species or in the communal phase of the subsocial species.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Funding was provided by the National Science Foundation of the United States (research grant NSF-DEB 9815938 to L. A. and a research training grant to the University of Arizona), the Center for Insect Science and the Department of Ecology and Evolutionary Biology of the University of Arizona, the Harvard Travelers’ Club, the Explorer's Club and the American Arachnological Society. D. Papaj, W. P. Maddison, D. Wheeler, B. Enquist, C. Martínez del Rio, T. Bukowski, A. Cutter, A. Danielson-François, I. Agnarsson, P. Salazar and J. Fletcher offered feedback on this project. We thank the Department of Biology of the Pontificia Universidad Católica del Ecuador for sponsoring our research and the Ministerio del Ambiente del Ecuador for research permits. We thank Eric Yip, Eric Higgins, Harold Greeney, Jatun Sacha and Yanayacu biological stations, Patricio Salazar, Patricia Salazar, Cecilia Puertas and Gabriel Iturralde for technical assistance and support in the field. Writing of this manuscript was completed while L. Avilés was on sabbatical at the Wissenschaftskolleg, in Berlin, Germany.

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  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Figure S2. Relationship between nest and colony size in the study species.

Appendix S1. Estimation of total prey capture rates

Table S1. For each species, the relationship between a prey item???s size and the amount of time that spiders could be observed feeding on it in the web. The measure of prey size (length vs. mass) used depended on which was a stronger predictor of feeding time as indicated by r-square values.

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