Scytodes socialis Miller, 2006
Cooperative behavior is known for a minute fraction of spider species. Yet various forms of sociality have evolved repeatedly in spiders (Avilés 1997). Two attributes are commonly used to classify spider sociality: territoriality and permanence (Avilés 1997; D'Andrea 1987). Individuals either defend individual territories from colony mates or move freely throughout a colony of unaggressive conspecifics, and social behavior either persists throughout the life of the spider or alternates with an obligate solitary phase. All four permutations of these conditions are known in spiders (see Avilés 1997 for review). Seasonal colonies of non-territorial individuals typically consist of extended mother to offspring maternal care. Such spiders are referred to as subsocial. Territorial sociality, whether periodic or permanent, is typically manifested by clusters of individuals within discrete webs connected to other webs in the colony. There is controversy over whether such spiders should be considered social at all because they are not cooperative (Agnarsson 2002, 2004; Kullmann 1972). Non-territorial permanent social spiders are referred to as quasisocial. These include the best studied social spiders (e.g., Avilés 1994; Avilés and Maddison 1991; Johannesen and Lubin 2001; Lubin 1991, 1995; Riechert 1985; Roeloffs and Riechert 1988; Rowell and Avilés 1995; Seibt and Wickler 1988; Smith and Engel 1994). Most quasisocial spiders are highly inbred and exhibit a strongly female biased sex ratio (e.g., Avilés 1993; Avilés 1997; Avilés and Bukowski 2006; Avilés and Maddison 1991; Bilde et al. 2005; Lubin 1991; Riechert and Roeloffs 1993).
Scytodids are best known for their ability to trap prey at a distance by expelling a mixture of venom and gluey silk from their chelicerae (Foelix 1985, 1996). Most scytodids are cursorial, although some species build webs. A small body of literature on sociality in Scytodidae documents two forms of sociality in the group: subsociality, involving extended maternal care (Eberhard 1986; Li 2002; Li et al. 1999; Li and Kuan 2006) and communal territorial web building (Bowden 1991; Bowden and Jackson 1988).
Miller (2006) described a species of web-building scytodid where webs may contain multiple males, females, and juveniles. Multiple nest mates participate in the capture of large prey items (Figs. 7-8). Participants and non-participant web mates are allowed to feed. No aggression between web mates was observed. The sex ratio among adults is unbiased. Webs contain from 1 to 16 individuals. Prey remains found in webs included ants, roaches, and moths. Webs usually incorporate dead leaves and other debris as well as living leaves and branches (Figs. 5-6). Mean web volume is estimated at 218.6 cm3 (8.4×5.8×4.5 cm).
Contrast with Other Social Spiders
The questions most relevant to compare S. socialis to the other social spiders concern colony permanence and whether one or more mothers contribute offspring to the colony. A female biased sex ratio is a well-studied phenomenon among highly social spiders that is expected under conditions that favor inbred, strongly subdivided populations where colony growth rate and proliferation is under group selection (e.g., some species of Achaearanea, Agelena, Anelosimus, Stegodyphus, etc., see Avilés 1993; Avilés 1997; Avilés and Maddison 1991; Lubin 1991; Riechert and Roeloffs 1993). Scytodes socialis falls into a small class of social spiders where multiple juveniles and adults of both sexes coexist cooperatively while maintaining an unbiased sex ratio.
These include the oxyopid Tapinillus sp. (Avilés 1994), the sparassid Delena cancerides (Rowell and Avilés 1995), and the subsocial thomisid Diaea ergandros (Evans 1995). Among the non-territorial permanent social (quasisocial) spiders, only Tapinillus sp. and Delena cancerides have an unbiased sex ratio (Avilés 1994, 1997; Rowell and Avilés 1995). Colonies of both species can consist of multiple juveniles and adults of both sexes. Outbreeding in Tapinillus is accomplished by dispersing males. So, colonies consist mostly of siblings plus a few immigrant males. Reproduction within colonies is apparently the result of mating between a single male-female pair. In spite of this reproductive monopolization, colonies may contain a few dozen spiders and one atypical web contained hundreds of individuals (Avilés 1994).
Delena cancerides is the only permanent social spider that does not use a prey capture web. While there is no aggression among colony mates, these spiders are unique among non-territorial social spiders in being extremely aggressive toward conspecifics from other colonies. Given this intercolony aggression, it is unclear how outbreeding is accomplished. Multiple females within the colony contribute offspring (Avilés 1997; Rowell and Avilés 1995).
Unlike Tapinillus sp. and Delena cancerides, Diaea ergandros colonies are non-permanent. While thomisids are not typical web-building spiders, social Diaea use silk in nest construction (Evans 1995; Main 1988; see also Jackson et al. 1995). Adult females disperse to establish new colonies after mating. Diaea ergandros are unique among subsocial spiders in that offspring continue to cooperate through maturity. Subsocial spiders typically avoid inbreeding by dispersing before they reach sexual maturity (e.g., Avilés 1997; Brach 1977; Nentwig and Christenson 1986). In D. ergandros, males mature first, then disperse to other colonies; females mate with siblings or immigrants, then disperse to found new colonies (Avilés 1997; Evans 1995). It is interesting to note that two other social species of Diaea exhibit female sex ratio bias. In these species, mating takes place among siblings before dispersal (Avilés 1997; Evans 1995; Main 1988).
How is S. socialis similar to or different from these outbred social spiders? One critical question is that of colony permanence. Diaea ergandros are atypical subsocial spiders because colonies persist beyond the maternal care phase into adulthood, yet there is a solitary phase as males disperse for mating and inseminated females disperse to found new colonies. There is no obligate solitary phase in Tapinillus sp. or D. cancerides. Reproduction in colonies of Tapinillus sp. and D. ergandros are the product of a single female. The relatively small population size of S. socialis colonies could indicate that colony members are the offspring of a single female founder. In fact, colony population size is small in S. socialis relative to both Tapinillus sp. and D. ergandros (Avilés 1994, 1997; Rowell and Avilés 1995). More observations from across the phenological cycle will be required to determine whether sociality in S. socialis conforms better to the Tapinillus sp. model (permanent sociality) or the D. ergandros model (periodic sociality), or perhaps differs from both of these in important ways.
Evolution of Sociality
While sociality is often discussed in terms of discrete classes, it is really a continuum of behaviors involving increasing levels of maternal investment in offspring and conspecific tolerance (Agnarsson 2002, 2004; Avilés 1997; Kullmann 1972; Shear 1970). Subsociality and quasisociality can gradually evolve by extension of maternal care to older and older offspring. This is known as the "maternal care pathway" to sociality and it predicts that subsociality should precede quasisociality on a phylogenetic tree (Agnarsson 2002, 2004; Avilés 1997). Recent phylogenetic analyses of Theridiidae are consistent with the "maternal care pathway" (Agnarsson 2002, 2004; Arnedo et al. 2004; Miller and Agnarsson 2005).
The evolution of sociality is usually preceded by two adaptations: web building and maternal care (Agnarsson 2002; Avilés 1997; Shear 1970). With rare exceptions (e.g., Sparassidae, Thomisidae), sociality tends to occur within lineages where web building is the norm (e.g., Theridiidae, Eresidae, Agelenidae). Even social members of the typically cursorial family Oxyopidae have non-social congeners that build prey-capture webs (Avilés 1997; Griswold 1983; Mora 1986). Sociality and web building in scytodids are both rare attributes, yet they seem to be tightly correlated.
Expressions of sociality in Scytodidae are surprisingly diverse, including subsociality with extended maternal care (Eberhard 1986; Li 2002; Li et al. 1999; Li and Kuan 2006), a communal territorial species (Bowden 1991; Bowden and Jackson 1988), and the non-territorial multiple-adult species S. socialis. Scytodid colonies with males, females, and juveniles living together in webs have also been observed in South Africa. It is not known if observations of this phenomenon in the Blyde River Canyon region, Mpumalanga and Tonquani Gorge, Magaliesberg Mountains, Northwest Province represent one or two more species (Astri and John Leroy, pers. comm; I. Engelbrecht, pers. comm.). The Blyde River species at least is superficially not very similar to the Kirindy species, raising the possibility of multiple independent origins of non-territorial multiple-adult sociality in scytodids. Sociality is thought to have evolved multiple times within the eresid genus Stegodyphus (Kraus and Kraus 1988, 1990), and the theridiid genera Anelosimus (Agnarsson 2006) and Achaearanea (Agnarsson et al. 2006) so such a scenario is hardly unprecedented. Hence, Scytodidae may offer another independent opportunity within spiders to explore the association of sociality with putative social preadaptations such as maternal care and web building, and the consequences of sociality for mating system and sex ratios. The answers to these questions will depend on new advances in the study of scytodid natural history, phylogeny, and systematics.
MALE: Carapace brown with dark markings (Fig. 11); abdomen light brown with pattern of dark obliquely transverse markings (Fig. 11). Legs light brown with dark markings; femora I–III with one ventral longitudinal stripe, femur IV with two ventral longitudinal stripes; tibiae and metatarsi with dorsal longitudinal stripe for proximal ~¾ of length, distal tip dark; tarsi without distinct markings.
Palpal bulb with basal part nearly spherical with an elongate, gently tapering stalk; distal part narrows abruptly to a glossy black tip; no apophyses present (Figs. 15-16). Tip of cymbium with tight cluster of three strong prolateral macrosetae.
FEMALE: Markings as in male (Figs. 12, 13, 14). Tip of palpal tarsus with tight cluster of four strong prolateral mactosetae subtending the palpal claw.
Vulva covered by oblong lightly sclerotized plate (Figs. 17-18). Duct leaves bursa ectally, curves mesally toward spermatheca (Fig. 18). Pair of positioning plates located posterior to epigastric furrow (Fig. 17). Positioning plates striated, wider than long with longest axis obliquely transverse (Figs. 17-18).
CHAETOTAXY: Tibiae I–III with two retrodorsal, one mediodorsal, two prodorsal trichobothria; tibia IV with one additional prodorsal trichobothrium. Retrodorsal and mediodorsal trichobothria distal; one prosorsal trichobothrium distal, others proximal. Distal-most trichobothrium is mediodorsal; distal prodorsal trichobothrium positioned between retrodorsal trichobothria. Metatarsi with one trichobothrium near distal tip. Palpal tibia with three retrodorsal, one mediodorsal, two (rarely three) prodorsal trichobothria.
Adult females are larger than adult males (mean carapace length: female = 2.75 mm, male = 2.43 mm) but males have longer legs (mean patella plus tibia I: female = 4.55 mm, male = 5.35 mm).
Male holotype specimen from Forêt De Kirindy, Toliara, Madagascar: Total length 5.70. Carapace 2.71 long, 2.04 wide; sternum 1.54 long, 1.03 wide; prosoma 1.94 high; Palpal bulb 0.78 long, 0.29 wide at the base.
Female specimen from Forêt de Kirindy, Toliara, Madagascar: Total length 6.77. Carapace 2.95 long, 2.28 wide; sternum 1.58 long, 1.09 wide; prosoma 2.49 high.
VARIATION: Female (n = 86): carapace length 2.3–3.2, patella-tibia I length 3.9–5.3. Male (n = 93): carapace length 1.8–3.1, patella-tibia I length (4.1–6.7).
Ecology and Distribution
Known only from Forêt de Kirindy field station, 46 km NE Morondava, elev. 50 m, 20°04.026'S, 44°39.434'E, Toliara, Madagascar. 179 males, 184 females, and 98 juveniles were collected from 109 colonies between 20–30 January 2006 by H. Wood and J. Miller.