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Natural History Miscellany Altitudinal Patterns of Spider Sociality and the Biology of a New Midelevation Social Anelosimus Species in Ecuador

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Natural History Miscellany Altitudinal Patterns of Spider Sociality and the Biology of a New Midelevation Social Anelosimus Species in Ecuador vol. 170, no. 5 the american naturalist november 2007 ൴ Natural History Miscellany Altitudinal Patterns of Spider Sociality and the Biology of a New Midelevation Social Anelosimus Species in Ecuador Leticia Avile´s,1,* Ingi Agnarsson,1,2,† Patricio A. Salazar,1,‡ Jessica Purcell,1,§ Gabriel Iturralde,3,k Eric C. Yip,4,# Kimberly S. Powers,5,** and Todd C. Bukowski5,†† 1. Department of Zoology, University of British Columbia, are one to two orders of magnitude smaller than those of a low- Vancouver, British Columbia V6T 1Z4, Canada; elevation congener of similar body size. We suggest that the absence 2. Department of Botany, University of British Columbia, of subsocial Anelosimus species in the lowland rain forest may be Vancouver, British Columbia V6T 1Z4, Canada; due to an increased probability of maternal death in this habitat due 3. Escuela de Biologı´a, Pontificia Universidad Cato´lica del to greater predation and/or precipitation, while absence of a sufficient Ecuador, Quito, Ecuador; supply of large insects at high elevations or latitudes may restrict 4. Department of Entomology, Cornell University, Ithaca, New social species to low- to midelevation tropical moist forests. We refer York 14853; to these as the “maternal survival” and “prey size” hypotheses, re- 5. Department of Ecology and Evolutionary Biology, University of spectively, and suggest that both in combination may explain the Arizona, Tucson, Arizona 85721 geographical distribution of sociality in the genus. Submitted March 7, 2007; Accepted July 2, 2007; Keywords: biogeography of sociality, elevation, latitude, social evo- Electronically published September 21, 2007 lution, social spiders, sex ratio, group foraging, Theridiidae. Online enhancements: appendix tables, figure. Spider sociality is a rare phenomenon (about 0.06% of spider species) but one that has nonetheless evolved re- peatedly (Avile´s 1997; Agnarsson et al. 2006; Johannesen abstract: To the extent that geography correlates with particular et al. 2007). Nonterritorial permanent-social spiders, also environmental parameters, the geographical distribution of phylo- known as quasi-social or simply “social” (e.g., Avile´s 1997; genetically related social and nonsocial organisms should shed light Lubin and Bilde, forthcoming), are scattered in several on the conditions that lead to sociality versus nonsociality. Social distantly related families and hence differ in many mor- spiders are notorious for being concentrated in tropical regions of phological, behavioral, and physiological traits. They are the world, occupying a set of habitats more restricted than those available to the phylogenetic lineages in which they occur. Here we found in diverse habitats and on most continents and document a parallel pattern involving elevation in the spider genus hence experience a variety of environments. Many species Anelosimus in America and describe the biology of a newly discovered occur in tropical moist forests (e.g., Levi et al. 1982; Riech- social species found at what appears to be the altitudinal edge of ert et al. 1986; Avile´s et al. 2001), while others inhabit dry sociality in the genus. We show that this is a cooperative permanent- thornbush or semideserts (e.g., Kraus and Kraus 1988; social species with highly female-biased sex ratios but colonies that Crouch and Lubin 2000). Despite these differences and multiple independent origins, social spider species exhibit * Corresponding author; e-mail: [email protected]. striking similarities in their behavior and population struc- † E-mail: [email protected]. ture (reviewed in Avile´s 1997). Colony members cooperate ‡ E-mail: [email protected]. in nest building and maintenance, prey capture and feed- § E-mail: [email protected] ing, and brood care. Unlike most social insect societies, k E-mail: [email protected]. where individuals disperse out of the natal nest to mate # E-mail: [email protected]. (Wilson 1971), social spider colonies grow through the ** E-mail: [email protected]. internal recruitment of new offspring generations pro- †† E-mail: [email protected]. duced by male and female spiders who remain within their Am. Nat. 2007. Vol. 170, pp. 783–792. ᭧ 2007 by The University of Chicago. natal nest to mate. New colonies arise through the budding 0003-0147/2007/17005-42446$15.00. All rights reserved. or fission of existing colonies. Colonies are thus isolated DOI: 10.1086/521965 population lineages that grow, proliferate, and become ex- 784 The American Naturalist tinct without mixing with one another. As shown by Avile´s Methods (1993), such population structure and dynamics, com- Altitudinal Patterns of Anelosimus Sociality bined with the greater proliferation success of more female-biased (i.e., faster-growing) colonies, may have al- Through surveys along several hundred kilometers of lowed the evolution of the highly female-biased sex ratios roads and visits to natural reserves and other point lo- that characterize the permanent-social spiders (reviewed calities in Ecuador, we recorded the presence of Anelosimus in Avile´s 1997). In contrast, related subsocial (or periodic- species at elevations ranging from 4 to 3,000 m (table A1 social) species form colonies that contain the offspring of in the online edition of the American Naturalist). Areas a single female, disperse before mating, and have 1 : 1 sex surveyed included several main and secondary roads on ratios (Kraus and Kraus 1988; Avile´s and Maddison 1991; the eastern slopes of the Andes, three roads on the western Avile´s and Gelsey 1998; Evans 2000; Bilde et al. 2005; slopes, six natural reserves or other point localities in east- Agnarsson 2006; Avile´s and Bukowski 2006; Viera et al. ern Ecuador, 10 in the highlands, and three in the west. 2006). Areas visited below 700 m elevation correspond to lowland Interestingly, all social spider species appear to occupy tropical rain forest and those between 700 and 2,500 m, a set of habitats more restricted than those available to east and west of the Andes, to lower montane rain forest the phylogenetic lineages in which they occur. Most no- or cloud forest (see Neill 1999). Highland areas surveyed tably, they are all concentrated in tropical regions of the ranged from 2,200 to 3,000 m, with vegetation types rang- world (reviewed in Avile´s 1997), while related subsocial ing from upper montane rain forest to semidesert. Voucher species extend into the temperate zones (e.g., Kraus and specimens have been deposited in the collections of the Kraus 1988; Avile´s and Gelsey 1998; Agnarsson 2006; Viera Museum of Comparative Zoology, the Museo Ecuatoriano et al. 2006; Jones et al. 2007). Here we demonstrate a de Ciencias Naturales, the Museo de Invertebrados de la parallel pattern involving elevation. We show that social Pontificia Universidad Cato´lica del Ecuador, the Smith- species in the genus Anelosimus (Agnarsson 2006) in Ec- sonian Natural History Museum, and the University of uador occur exclusively in the lowland rain forest up to British Columbia (see table A2 in the online edition of midelevation cloud forests, while subsocial species are ab- the American Naturalist). sent from the lowland rain forest but are common at higher elevations. We also report on a newly discovered Anelosimus guacamayos Biology social species, Anelosimus guacamayos Agnarsson 2006 (for its taxonomic description, see Agnarsson 2006), found at We obtained data on the age composition and tertiary sex higher elevations than previously studied species in the ratio (juveniles to young adults) of Anelosimus guacamayos genus. We first show that this is a cooperative permanent- colonies through the collection of entire (N p 15 in 1999; social species by demonstrating that it forms colonies that N p 7 in 2002) or partial (15%–50% ofN p 4 nests in contain multiple adult females and their offspring, exhibits 2002) nests from the area in eastern Ecuador where we cooperative prey capture and feeding, and has female- first discovered the species in August 1999, that is, Co- biased sex ratios. We then test the hypothesis that this codrilos, in the Napo Province, 0.63Њ–0.65ЊS, 77.8ЊW, species is somehow “less social” than a lower-elevation 1,740–1,940 m elevation. We also obtained a preliminary social congener of similar body size, Anelosimus eximius estimate of A. guacamayos’s primary sex ratio from cy- Keyserling 1884 (Agnarsson 2006), by comparing the col- tological preparations of 45 embryos randomly chosen ony size distribution and spacing of spiders within nests from five egg sacs collected from the Cocodrilos area in in these two species. Uetz and Hodge (1990), in comparing 1999 (four sacs from a colony with 39 adult females and two species of orb-weaving colonial (noncooperative) spi- one from a colony with three adult females). Clutch size ders from Mexico in the genus Metepeira (Araneidae), data were obtained from four of these sacs (three from found that spiders in a prey-poor environment, where they the large colony and one from the small colony), plus three were predicted to be less social, lived solitarily or in small sacs collected in 2003. groups, with greater spacing among group members, when We collected nests after measuring and drawing their compared with spiders in a prey-rich environment, where aerial and lateral cross sections (as in Purcell and Avile´s groups were bigger and spacing smaller (Uetz and Hodge 2007, their fig. 1) and classified the spiders they contained 1990). We thus consider that the presence of a greater by instar and sex on the basis of size and secondary sexual proportion of nests with solitary females, smaller colony characters. Males were distinguishable from females be- sizes, or greater spacing of spiders within the nests, a pos- cause of their enlarged palpi starting in their fourth instar sible indicator of mutual tolerance (Uetz and Hodge 1990), outside the sac. Females matured in their seventh instar, may be indicative of a “lower” level of sociality in the one instar later than males.
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