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Costs and Benfits of Group Living in an Unusual Social Spider

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Costs and Benfits of Group Living in an Unusual Social Spider COSTS AND BENFITS OF GROUP LIVING IN AN UNUSUAL SOCIAL SPIDER, DELENA CANCERIDES A Dissertation Presented to the Faculty of the Graduate School of Cornell University in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Eric Chun-Ngam Yip August, 2012 i ii COSTS AND BENFITS OF GROUP LIVING IN AN UNUSUAL SOCIAL SPIDER, DELENA CANCERIDES Eric Chun-Ngam Yip, Ph.D. Cornell University 2012 Virtually all spiders are predators, and many are cannibalistic. Of the handful of species that tolerate conspecifics and sustain long-term associations, nearly all spin a web or silken retreat. Previous research on these social spiders showed that many of the benefits they derive from group living depend on these silken structures. The social huntsman spider of Australia, Delena cancerides, is the exception and only lives under the bark of trees. I studied the costs and benefits of group living in this species, given that many of the benefits ascribed to other species are impossible without a web, in three contexts: (1) predator defense, (2) foraging, and (3) dispersal. I examined predator defense by introducing potential predators into field colonies that had been manipulated to allow observations and into captive colonies in the laboratory. The single adult female of the colony was the primary defender of the colony, while younger spiders were ineffective at repelling predators. I examined foraging by observing natural prey capture in the field, introducing prey into field colonies, and recording the condition of field spiders at the time of collection. Spiders predominantly foraged individually; however, some prey captured inside the retreat was shared, and younger iii spiders benefited from sharing prey captured by their older siblings. I examined dispersal into neighboring colonies through a combination of allozyme analyses and direct observations in the field and laboratory. Young spiders can and do immigrate into foreign colonies; however, older spiders were usually attacked in foreign colonies, and thus their dispersal options are constrained. Through the use of nest boxes, I showed that competition for a new bark retreat is intense and that spiders should wait in their natal retreat until they are larger and better competitors for a new retreat. Together, these data show that the bark retreat is indeed critical to the social biology of D. cancerides. Without the web some forms of cooperation found in other social spiders never evolved, yet the reliance on a rare bark retreat also promotes group cohesion, as is found in many social vertebrates. iv BIOGRAPHICAL SKETCH In May of 2005, Eric C. Yip graduated with a B.S. in Ecology and Evolutionary Biology from the University of Arizona, summa cum laude and with honors. His honors thesis on the relationship between colony size and foraging success in the social spider, Anelosimus eximius, sparked his interest in the evolution of social behavior in spiders and would eventually be published in The Proceedings of the National Academy of Sciences, USA. He chose to continue his work on social spiders with Dr. Linda S. Rayor at Cornell University’s Department of Entomology. From 2005 to 2012, he has studied the costs and benefits of group living in the unusual social spider, Delena cancerides. Eric is grateful to the Fulbright Fellowship, the National Science Foundation’s Graduate Research Fellowship, Cornell University’s Sage Fellowship and Liu Memorial Fund, in addition to smaller awards, that have funded his research. These grants have allowed him to spend three years conducting field work in Australia as a visiting fellow at The Australian National University. He has presented his work at meeting by the American Arachnological Society, the International Arachnology Congress, the International Society for Behavioral Ecology, and the Animal Behavior Society. He was awarded second place Best Student Oral Presentation at two International Arachnology Congresses in 2007 and 2010. He was also selected to compete in the Animal Behavior Society’s Allee Competition in 2012. He has been awarded the Blaustein Fellowship and the Kreitman Fellowship to conduct post-doctoral work at Ben-Gurion University of the Negev with Dr. Yael Lubin. v AKNOWLEGEMENTS Funding for my dissertation research was provided by The Australian-American Fulbright Association, The National Science Foundation Graduate Research Fellowship, Cornell University’s Sage Fellowship, Cornell University’s Liu Memorial Fund, The Rawlins Endowment, and Cornell’s Graduate School. I would like to thank my adviser, Dr. Linda S. Rayor for her guidance on all aspects of this work. I would also like to thank my other co-authors, Shannon Roberts (formerly Shannon Clarke) and Dr. David M. Rowell. Dr. Rowell was also my gracious host at The Australian National University. My work would not have been possible without the help of the faculty and staff of The Australian National University’s School of Research Biology. I thank my committee members Drs. Thomas D. Seeley and Hudson Kern Reeve for their comments on the chapters of this dissertation. Finally, I would like to thank the many undergraduates of the Rayor lab who have provided animal care and stimulating conversation over the years. vi TABLE OF CONTENTS Biographical Sketch v Acknowledgements vi Chapter 1: Aliens among us: Nestmate recognition in the social huntsman spider, Delena cancerides. 1 Chapter 2: Do social spiders cooperate in predator defense and foraging without a web? 28 Chapter 3: Molecular and behavioural evidence for selective immigration and group regulation in the social huntsman spider, Delena cancerides. 67 Chapter 4: The influence of siblings on body condition in a social spider: Is prey sharing cooperation or competition? 106 Chapter 5: Saturated habitats promote philopatry in a social huntsman spider. 137 Chapter 6: Maternal care and subsocial behavior in spiders 159 vii CHAPTER 1 Aliens among us: Nestmate recognition in the social huntsman spider, Delena cancerides E.C. Yip, S. Clarke, L.S. Rayor Published in Insectes Sociaux/ Received: 22 May 2008/ Revised: 28 January 2009/ Accepted 21 April 2009/ Published online: 13 May 2009 © Birkhäuser Verlag, Basel/Switzerland 2009 Abstract. Unlike all other social spiders, the social huntsman spider, Delena cancerides has been reported to rapidly respond to non-nestmates with lethal aggression, similar to the behavior of some eusocial insects. We tested for the presence of nestmate recognition in D. cancerides under laboratory conditions by introducing 105 unrelated alien conspecifics into foreign colonies and comparing their behavior to 60 control spiders removed and returned to their natal colony. Spiders demonstrated nestmate recognition by investigating alien spiders far more than nestmates and by resting closer to nestmates than to aliens. Serious attacks or deaths occurred in 23% of all trials; however, aggression was not directed significantly more toward aliens than to nestmates. Most notably, aggression was largely mediated by the adult females (resident or alien), who were most likely to attack or kill other subadult or mature individuals. Young individuals (resident or alien) were largely immune from serious aggression. Spiders recently collected from the field tended to be more 1 aggressive than spiders born and raised in the laboratory, possibly due to blurring of recognition cues related to laboratory husbandry. Our findings support the prediction that nestmate recognition should evolve when there is a benefit to discriminating against non-kin, as in this social spider system where foraging individuals may enter a foreign colony and the colony retreat is a limited resource. Key words: Social spiders, Nestmate recognition, aggression Introduction The ability to discriminate kin from other conspecifics is a common trait among social animals, as it allows altruistic behaviors to be preferentially directed toward kin (Hamilton 1964; Hölldobler & Wilson 1990; Holmes 2004). Most eusocial insects recognize their nestmates, with the resolution of kin discrimination at the level of the colony (Breed et al. 1994; Clément & Bagnères 1998; Strassmann et al. 2000; Tarpy et al. 2004). While nestmate recognition is common among the eusocial insects (Wilson 1971; Singer & Espelie 1992; Clément & Bagnères 1998; Vander Meer & Morel 1998) nestmate recognition is rare or absent in the subsocial and social arachnids (Lubin & Bilde 2007). There is a continuum of social behavior in the spiders from small subsocial mother-offspring-sibling groups to complex, cooperative societies of thousands of individuals (Buskirk 1981; Avilés 1997; Lubin & Bilde 2007). Most social spiders, despite multiple evolutionary origins, share a suite of traits that includes the acceptance of alien spiders (unrelated and unfamiliar conspecifics) into the group without overt 2 aggression (Lubin & Bilde 2007). These social spider species do not appear to differentiate between conspecific aliens and members of their own colony (Pasquet et al. 1997), silk from kin or non-kin (Bilde et al. 2002; Buser 2002), or even heterospecific from conspecific spiders in the same genus (Seibt & Wickler 1988a). Most social spiders may have never evolved nestmate recognition because the costs of sharing resources are relatively small, and non-relatives are encountered only rarely. While there is undoubtedly competition for resources within social spider colonies (Ward 1986; Seibt & Wickler 1988b; Avilés & Tufiño 1998; Bilde et al. 2007), the benefits
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