We used spatial modelling to examine two hypotheses for the restriction of group-living Stegodyphus spiders to tropical and subtropical regions. By analysing the continental-scale environmental relationships of the genus Stegodyphus, we found clear support for the hypothesis that group-living spiders are restricted to habitats with high vegetation productivity relative to solitary congeners. This corroborates our hypothesis that habitats with high vegetation productivity support the high prey abundance that is required to sustain the food requirements of social groups. Notably, we found a strong positive relationship of social Stegodyphus species’ occurrence to vegetation productivity and a strong positive relationship between insect biomass and vegetation productivity. These results are consistent with empirical work suggesting that group living in spiders is tightly associated with high prey abundance, whether this applies to insect abundance or size, both of which correlate positively with insect biomass[18, 19, 29, 31]. We note that our results also confirmed that even social Stegodyphus spp. are absent from forest environments, just like all other species in the family Eresidae. This absence is thus not evidence for a particular constraint on the distribution of social vs. solitary species within the Stegodyphus genus, but rather indicates niche conservatism at the family level.
The multivariate analyses did not support the occurrence of social Stegodyphus in areas of low precipitation seasonality compared with their solitary congeners (Tables 1,2), although an initial comparison of habitats provided weak evidence that social spiders may be restricted to habitats of relatively lower precipitation seasonality (Figure 2 and Additional file1: Figure S2). We tested the hypothesis that social species might be limited to less variable environments to cope with demands of group living, for example continuous prey supply, as several studies have found correlations between insect abundance and biomass with seasonal rainfall patterns[32, 33]. Under low precipitation seasonality prey availability might vary less over the year, which reduces variance in prey capture rates and meets the constant demands of foraging groups. However, we did not find substantial support for this hypothesis in the regression analyses; neither did we find any consistent relationship between insect biomass and precipitation seasonality (Figure 4b). Our analyses therefore strongly indicate that prey availability per se rather than continuity in prey supply is the key factor for the formation and maintenance of social Stegodyphus groups. Moreover, this is in agreement with Stegodyphus spp. occurring in more seasonal habitats (in contrast to e.g. Anelosimus), and going dormant over times of the season when prey is particularly scarce. Thus, the quantity of food supply at certain life-stages might be more important than the constancy of prey.
While food and predators are widely recognised as two major factors underlying the formation of groups, the evolution of cooperative breeding is not necessarily facilitated by single factors alone. For example, environmental constraints such as lack of suitable habitat and genetic pre-disposition for helping relatives may act in concert to promote cooperative breeding in birds and social insects[34–36]. Sociality in spiders is favoured by enhanced survival with increasing group size, and kin-selected benefits of cooperation[6, 38], where the former is likely to result from heavy predation pressure that wipe out small colonies. However, group living is associated with fecundity costs as per capita lifetime reproductive success decreases with increasing group size[38, 40]. Hence, group living spiders face a trade-off between survival benefits and reproductive costs. Our analyses show that three independently derived social Stegodyphus species with similar life-histories also share similar habitat requirements of high vegetation productivity, suggesting that productivity needs to exceed a certain threshold to tip the balance in favour of group living. Importantly, the negligible region and region-productivity effects suggest that the three social species have consistent vegetation productivity requirements (Table 2; Additional file1: Figure S2). Only habitats that negate within-group competition which causes fitness decline should therefore be suitable to facilitate the formation and maintenance of groups. The facultative social Neotropical spider Anelosimus studiosus shows a life-history pattern consistent with this expectation: females breed solitarily under relaxed ecological conditions (i.e. higher temperature surrounding the nest sites) whereas they engage in cooperative breeding under constrained ecological conditions with increased risk of mortality.
In contrast to the patterns discussed above, where environmental constraints favour group living under certain environmental conditions, some animal species form groups in response to resources to exploit them more efficiently, in which case resource availability may be the single factor promoting group formation. This applies to colonial spiders, which differ from permanently-social spiders by sharing a common silk frame, but defend individual capture webs within the group, do not hunt communally, nor show cooperative breeding. The colonial spiders also occur mainly in the tropics and groups form through aggregations around abundant resources. In contrast, the social spiders likely evolved group living through delayed dispersal. While different proximate factors are likely involved in group formation, i.e., foraging benefits for colonial spiders and survival benefits for permanently social spiders, both groups are characterized by a distributional range within the tropics, which corroborate that prey availability in sufficient supply is an important environmental factor facilitating group living[2, 43].
Our results provide evidence that the link between the occurrence of social Stegodyphus species and vegetation productivity is related to prey availability. Notably, vegetation productivity in the general distribution area for the genus correlated positively with insect biomass. Other studies have likewise shown that the abundance of vegetation and canopy cover influences the amount and seasonal distribution of insects[44, 45]. Furthermore, multiple previous studies on arthropod distributions have found that remotely sensed vegetation structure descriptors perform well as predictors of arthropod species occurrences and species richness across large scales[46, 47].
Prey size has been hypothesized to constrain the distribution of social spiders, based on field studies showing such a pattern for four American Anelosimus species (2 social and 2 subsocial). Our data suggest that prey numbers are a major driver of Stegodyphus distribution patterns. Firstly, Stegodyphus species occur in habitats that are generally less diverse than tropical rainforests (habitats of social Anelosimus spp.), and we argue that the range of prey species is smaller and may therefore generally span a shorter body-size gradient. Secondly, we show that insect abundance is positively correlated to habitat productivity which is the most important predictor of Stegodyphus distribution in our models. Though we cannot rule out that prey body-size may be an important additional factor, we suggest that our approach provides a more general and valid explanation of the observed distribution patterns in social and solitary Stegodyphus species based on the relationship between vegetation productivity and prey biomass.
An additional explanation for the importance of vegetation productivity for the occurrence of social Stegodyphus species may be their link to vegetation complexity. Group-living Stegodyphus require certain structures for establishing colonies and capture webs, and a denser vegetation cover would offer more vertically and structurally diverse micro-niche space. Evidence for this explanation was recently found in the tropical rainforest Anelosimus species, where permanently group living species require sturdier vegetation for nest building. Structural complexity of habitats has been shown to provide important environmental cues to web-building in spiders, in particular due to their predatory function in the ecosystems. This can also have an effect on species traits in the guild through prey availability[48, 51]. Considering these factors, we could expect that social Stegodyphus should be found in areas of increasing complexity in vegetation structure - relative to their solitary congeners, respectively.