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Sociality of Spiders of the Genus Anelosimus (Araneae: Theridiidae), with Focus on Species in Southeast and East Asia

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Sociality of Spiders of the Genus Anelosimus (Araneae: Theridiidae), with Focus on Species in Southeast and East Asia SOCIALITY OF SPIDERS OF THE GENUS ANELOSIMUS (ARANEAE: THERIDIIDAE), WITH FOCUS ON SPECIES IN SOUTHEAST AND EAST ASIA GOH SEOK PING A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY NATIONAL UNIVERSITY OF SINGAPORE 2014 SOCIALITY OF SPIDERS OF THE GENUS ANELOSIMUS (ARANEAE: THERIDIIDAE), WITH FOCUS ON SPECIES IN SOUTHEAST AND EAST ASIA GOH SEOK PING B.Sc. (Hons.), NUS A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES NATIONAL UNIVERSITY OF SINGAPORE 2014 DECLARATION I hereby declare that this thesis is my original work and it has been written by me in its entirety except the phylogenetic tree in Chapter 1 which was analyzed by Dr. Ingi Agnarsson from the University of Vermont, USA. I have duly acknowledged all the sources of information which have been used in the thesis. This thesis has also not been submitted for any degree in any university previously. Goh Seok Ping 31 May 2014 i ACKNOWLEDGEMENTS To God, the Creator of all things. To my parents, for giving me the freedom and support I needed to follow my interest. To Matthew, thank you for your patience, support, encouragement and ‘naggings’, which I needed. To my family and friends, Thank you for standing by me and believing in me. Your prayers and encouragement have carried me this far. I would like to thank many who have helped me in this dissertation: Special thanks to my supervisor Assoc. Prof. Li Daiqin, for allowing me to pursue my topic of interest and supporting me in the completion of this dissertation. Thanks to fellow lab mates (past and present): Shiyu, Junhao, Diego, Zhanqi, Shichang, Jeremy, Laura, Stanley, Mindy, Joelyn, Jiafen, Ganison and Yuan Ting for making lab a fun filled place and for the company through lunches, tea breaks and late nights. Special thanks to Junhao, Laura, Shiyu, Wendy, Xu Xin and Yingying for enduring the hot sun, downpours, mosquitoes and leeches with me during field trips. Thanks to Mr. Chong and Mdm. Loy, for their help in usage of the S.E.M. I would also like to thank the National Parks Board and Agri-Food & Veterinary Authority of Singapore for the issuing of research and import permits. For those who taught and inspired me, Dr. Ingi Agnarsson and lab members, for an opportunity to work and learn in the lab and for providing me with invaluable advice and specimens from Borneo and Indonesia. David Court, for his help and enthusiasm and in providing specimens from Singapore. Dr. Matjaž Kuntner and members of EZ lab, for the opportunity to participate in 27th European Congress of Arachnology and for inspiring me with his passion for research and his encouragement. Prof. Rudolf Meier and Dr. Kwong Shiyang, for guiding me and getting me started on the daunting task of molecular genetics. ii TABLE OF CONTENTS SUMMARY vi LIST OF TABLES x LIST OF FIGURES xii INTRODUCTION Sociality in the animal kingdom 1 Evolution of sociality in spiders 3 The genus Anelosimus 8 Research objectives 10 References 13 CHAPTER 1: SYSTEMATICS AND PHYLOGENY OF SOUTHEAST AND EAST ASIAN SPIDERS OF THE GENUS ANELOSIMUS (ARANEAE: THERIDIIDAE), WITH THE DESCRIPTIONS OF TEN NEW SPECIES Abstract 28 Introduction 29 Materials and Methods 31 Spiders collection 31 Taxonomy 31 Phylogenetics 32 Results 36 Morphology 36 Phylogeny 36 Natural History 37 Discussion 40 Taxonomy 43 References 123 CHAPTER 2: NATURAL HISTORY AND BEHAVIOURAL OBSERVATIONS OF ANELOSIMUS SPECIES WITH FOCUS ON SOCIAL AND REPRODUCTIVE TRAITS Abstract 129 Introduction 131 Materials and Methods 137 Colony survey in the field 137 Spider collection and maintenance in laboratory 137 Behavioural observations in laboratory 142 Reproductive traits 145 Data analyses 145 Results 148 Colony survey in the field 148 Colony structure 152 Life cycle 153 Maternal care 155 Cooperative prey capture and food sharing 156 Natal dispersal 160 Reproductive traits 161 iii Discussion 171 References 183 CHAPTER 3: SENSORY RECEPTORS AND SOCIALITY IN SPIDERS OF THE GENUS ANELOSIMUS (ARANEAE: THERIDIIDAE) Abstract 192 Introduction 193 Materials and Methods 198 Study subjects 198 Sample preparation 198 Data analyses 199 Results 201 Tactile hair 201 Chemoreceptor 204 Slit sensillum 205 Trichobothrium 207 Discussion 216 References 224 CHAPTER 4: ENVIRONMENTAL FACTORS AFFECTING THE GEOGRAPHICAL DISTRIBUTION OF ANELOSIMUS SPECIES Abstract 233 Introduction 234 Materials and Methods 238 Species and spatial data 238 Environmental data 240 Data processing and analyses 241 Results 244 Species distribution 244 Variation partitioning 245 Environmental variables 246 Discussion 252 References 257 CHAPTER 5: PARASITES AND SOCIALITY OF ANELOSIMUS SPIDERS Abstract 266 Introduction 267 Materials and Methods 272 Nest collection and examination 272 DNA extraction and detection of Wolbachia 276 Data analyses 277 Results 278 Nest contents 278 Wolbachia detection 279 Discussion 284 References 290 iv OVERALL DISCUSSION Overall Discussion 301 Future directions 305 References 307 APPENDIX Table 1 310 Table 2 312 v SUMMARY The formation of groups is pervasive in the animal kingdom. Groups formed may be temporal or permanent and are sometimes made up of related individuals or unrelated ones. The purpose of group formation can also vary from predator defense and brood fostering to increased foraging efficiency. While group formation is generally rare in spiders, the occurrence of closely related social spider groups is exceptionally unusual. Out of 44,000 spider species, less than 25 species have been documented as social. Social behaviour is believed to have evolved 12 times in spiders, of which three derivations have occurred in the family Theridiidae. To date, the genus Anelosimus (Araneae: Theridiidae) consists of 64 nominal species, of which six are social, 14 subsocial and five solitary living, while the sociality of the remaining species are unknown. Whilst intensive work has been conducted on spiders of this genus in North and South America, little is known about Anelosimus in Asia. A comprehensive study of spiders of this genus is important due to its cosmopolitan distribution as well as its composition of spiders with a spectrum of social behaviour. Therefore, the goal of this thesis is to supplement the knowledge of spiders of the genus Anelosimus, with concentration on species found in Southeast and East Asia. While 13 species of Anelosimus has been described in Southeast and East Asia to date, the natural history of many remains undetermined. Moreover, almost half of these species were described before the year 2000. With the advancement of technology, I thus re- described 11 of these species, supplementing past taxonomic descriptions with photographs, updates of missing male/female descriptions and information on natural history. Furthermore, I also included description of nine new species collected from Malaysia and Indonesia. vi In order to gain a better understanding of the evolution of sociality within this genus of spiders, I further examined the natural history of ten species of Anelosimus collected from China, Malaysia and Singapore, with special focus on traits such as habitat and colony structure, maternal care, cooperative behaviour, dispersal and a number of reproductive traits. I determined that seven of these species are solitary living, while the remaining three species are subsocial. Solitary species dispersed from the natal nest by 3rd instar but exhibited prey sharing amongst siblings before dispersal. In contrast, subsocial species disperse from the natal nest before reaching maturity, between 4th to 6th instars. Females of all species studied displayed maternal care through guarding of egg sacs and provision of prey for 2nd instar spiderlings. Interestingly, I found that even solitary Anelosimus possessed traits such as reduced dispersal distance and maternal care that suggest that this group of spiders may be predisposed to the development of social behaviour. In Chapter 3, I looked at the sensory receptors of eight Anelosimus species (six solitary and two subsocial) to determine if a reduced sensitivity to external signals corresponds with the evolution of social behaviour. I found that subsocial species possessed lower mechanoreceptor densities as compared to solitary species although there is no significant difference in total mechanoreceptor densities between solitary and subsocial spiders. Besides morphological and behavioural disposition to the evolution of sociality, abiotic factors in the habitat may also affect the evolution of social behaviour in Anelosimus. Social spiders tend to occur in lowland tropical rainforests, while subsocial species occur at higher latitudes and altitudes. A number of environmental factors similarly vary according to changes in latitudes and altitudes. Therefore, in Chapter 4, I analyzed the worldwide distribution of 35 Anelosimus vii species and determined that solitary species tend to occur in habitats with high rainfall and temperature, subsocial species occur in areas with low rainfall and temperatures while social species are commonly found in areas with high rainfall and intermediate temperatures. Possible explanations for this observation are associated with ability of web structure to withstand rain damage, prey abundance and effects of temperatures on metabolism and growth of spiders. Finally, parasitism has been closely associated with social groups across different animal taxa. The rate of parasitism is therefore examined in Chapter 5. In this chapter, I investigated the prevalence of parasites in nests of eight Anelosimus
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