Ecology Letters, (2003) 6: 13-18 LETTER Are three-dimensional spider webs defensive adaptations? Abstract Todd A. Blackledge1*, Jonathan Spider webs result from complex behaviours that have evolved under many selective A. Coddington2 and Rosemary pressures. Webs have been primarily considered to be foraging adaptations, neglecting 1 G. Gillespie the potential role of predation risk in the evolution of web architecture. The ecological 1 University of California - success of spiders has been attributed to key innovations in how spiders use silk to Berkeley, Environmental capture prey, especially the invention of chemically adhesive aerial two-dimensional orb Science, Policy and webs. However, araneoid sheet web weavers transformed the orb architecture into three- Management, Division of Insect dimensional webs and are the dominant group of aerial web-building spiders world-wide, Biology, 201 Wellman Hall, both in numbers and described species diversity. We argue that mud-dauber wasps are Berkeley, CA 94720-3112, USA 2National Museum of Natural major predators of orbicularian spiders, and exert a directional selective pressure to History NHB 105, Smithsonian construct three-dimensional webs such that three-dimensional webs are partly defensive Institution, Washington, DC, innovations. Furthermore, patterns of diversification suggest that escape from wasp 20560-0105, USA predators may have facilitated diversification of three-dimensional web-building spiders. *Correspondence and present address: Department of Keywords Entomology, Comstock Hall, Adaptive radiation, Araneidae, key innovation, Linyphiidae, orb web, sheet web, silk, Cornell University, Ithaca, NY Sphecidae, Theridiidae. 14853, USA E-mail: [email protected] Ecology Utters (2003) 6: 13-18 1982), but may better protect spiders against predators (see INTRODUCTION below). Diversification of arthropods and their subsequent dom- Construction of spider webs involves a complex series of inance of earth's biodiversity have been attributed to shifts behaviours that have evolved under many selective factors, and expansions in exploitation of food (Ehrlich & Raven among which predation risk has received little consideration. 1964; Farrell & Mitter 1994). Within spiders, whose Here, we examine the hypothesis that 3-D webs may be 37 000+ described species are all predators of arthropods, adaptations against predation by mud-dauber wasps that innovations in the use of silk in foraging, such as specialize upon spiders in the Orbiculariae. chemically adhesive two-dimensional (2-D) orb webs, may have been especially important (Bond & Opell METHODS 1998). Aerial orb webs allow exploitation of abundant flying insects, require little silk, and allow spiders to change Six sphecid genera hunt spiders exclusively (Bohart & foraging patches efficiently through recycling of silk Menke 1976), capture 20 or more spiders daily for larval (Janetos 1982; Shear 1986). food (Coville 1987; Rayor 1997; Blackledge & Wenzel 2001), However, 2-D orb weaving is an ancient behaviour and occur in most terrestrial ecosystems. Because paralysed (Coddington & Levi 1991; Griswold et d. 1998), and the spiders can be recovered from wasp nests, selection on araneoid sheet web weavers have transformed the orb spider defensive behaviours can be elucidated by comparing architecture into typically three-dimensional (3-D) sheet or behavioural phenotypes of prey with the background tangle webs (Fig. 1; Coddington & Levi 1991; Griswold frequency of spiders in the habitat. et al. 1998). This change is associated with a 43% increase in We compiled all known captures of spiders by sphecid described species diversity of araneoid sheet web weavers wasps from studies published over the last century. These (Platnick 2001) and a 400% increase in numerical abundance studies encompassed a variety of ecosystems from around in ecosystems across the world (see below). 3-D webs are the world. Several techniques were used to collect wasp not recycled daily, constraining spider mobility (Janetos prey, mainly excavation of provisioned prey from natural ©2003 Blackwell Publishing Ltd/CNRS 14 T. A. Blackledge, J. A. Coddington and R. G. Gillespie Figure 1 Two types of aerial spider webs, (a) Two-dimensional orb webs provide spiders with very efficient traps to capture flying insects and the silk is easily recycled from day to day. However, orb-weaving spiders must rest either at the centres of webs where spiders are vulnerable visually and physically to predators or in retreats next to webs, (b) The 'araneoid sheet web weavers' build three-dimensional sheet or tangle webs. These relatively permanent webs surround spiders with three-dimensional networks of silk that can give advanced warning about attacks by predators or physically block predators. and wooden tfap nests, but also opportunistic observations Other spiders included non-orbicularian taxa from 24 on burrow-nesting taxa. These data collectively provide the families, of which only Agelenidae (4 prey), Dictynidae best available evidence on the threat predatory wasps pose (197 prey), and Pholcidae (18 prey) typically build webs. to spiders, but are biased in various ways, particularly by discrepancies in sample sizes between wasp genera. How- RESULTS ever, within each genus the relative frequencies of spider behavioural phenotypes probably reflect wasp prey prefer- We recorded 30 375 records of identified spider prey from ences with reasonable accuracy. 70 publications (130 observations differentiated by wasp We used faunal surveys to estimate background frequen- species and/or localities) and 164 118 records of potential cies of behavioural phenotypes of potential spider prey. prey available in habitats from 26 faunal surveys. Aerial web- Fifty percent of surveys (70% of all data), used standardized building orbicularians comprised 76% of all prey (Table 1), techniques, including direct searching, beating, sweeping, most of which built the ancestral 2-D orb architectures pitfall trapping, canopy fogging, and litter sifting (see (Table 1 and Fig. 2a). Araneoid sheet web weavers, with Coddington et al. 1991, 1996; Sorensen et al. 2002 for their 3-D web architecture, accounted for only 17% of methodology). These methods are not ideal for estimating predation within the Orbiculariae, even though these spiders relative abundances of spiders, but are probably least biased constitute 81% of the numerical abundance and 59% of within web-building spiders at shrub, herb and ground species diversity within the Orbiculariae (Fig. 2a). Wasps levels, which is the comparison of interest here. We captured more orb-weavers than araneoid sheet web classified spiders into three behavioural phenotypes (Figs 1 weavers in 86 of 111 studies (sign test P < 0.0001; 19 and 2b). (1) 3-D web-builders included a single apomorphic studies lacked orbicularian taxa), even though sheet web clade within the Orbiculariae, the 'araneoid sheet web weavers were more abundant in 21 of 26 faunal surveys weavers', which construct diverse but usually highly three- (sign test P < 0.005). There was a significant difference in dimensional webs. (2) 2-D web-builders included all other the numbers of 2-D vs. 3-D web weaving spiders in each orbicularian taxa that retain plesiomorphic orb webs. (3) study when comparing the prey captured by wasps and ©2003 Blackwell Publishing Ltd/CNRS Spider webs as predator defences 15 (a) (C^tests, P < 0.05). Sphecid wasps are significantly biased web architecture towards two-dimensional orb weavers as prey. | two-dimensional H three-dimensional DISCUSSION C. M No doubt three-dimensional web architectures influence * 50 many aspects of spider biology, which we cannot discuss or even begin to enumerate here. However, these data are consistent with the hypothesis that 3-D web architectures provide a defensive advantage against wasps compared to available to hunting wasps captured by hunting wasps plesiomorphic 2-D orb webs. It is further plausible that 3-D web architecture may have originated in part due to selective pressures from wasps and that escape from wasp predation may have facilitated the evolutionary diversification of araneoid sheet web weavers. The role of predatory wasps in web-building spider evolution has not been considered heretofore. • 65 mya Wasps are a significant danger to spiders Invertebrates, such as sphecid wasps, are often primary predators of web-building spiders (Coville 1987; Blackledge & development of three-dinicnsuMKil Wenzel 2001). Pompilid wasps capture up to 99% of adult WCDS& burrowing wolf spiders (McQueen 1978). One study that first sphecid wasp specialists that prey •125 mya considered multiple predatory taxa found that wasps (Pomp- on spiders ilidae and Sphecidae) accounted for 93% of all attacks on colonial orb-weaving spiders in Mexico, with 500 h of biculariae - first aerial two- observation yielding 465 attacks by 15 or more species of dimensional webs wasps (Rayor 1997). In small colonies, individuals risked a 1.5% chance of capture by wasps each day (Uetz & Hieber 1994). Finally, outbreaks of pompilid wasps reduced island Figure 2 Wasps exert directional selection that favours three- populations of web-building spiders by 54•77% (Polis et al. dimensional web architectures, (a) 'Araneoid sheet web weavers' 1998). are 400% more abundant than ancestral orb-weaving spiders in the Birds also prey on spiders (e.g. Rypstra 1984; Gunnarsson environment, but orb-weaving spiders are 476% more common as 1996), but many studies have failed to find a significant