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The Direct and Indirect Effects of Maternal Nutrition on the Young Via Maternal and Allomaternal Care in Social and Subsocial Spiders

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The Direct and Indirect Effects of Maternal Nutrition on the Young Via Maternal and Allomaternal Care in Social and Subsocial Spiders The Direct and Indirect Effects of Maternal Nutrition on the Young via Maternal and Allomaternal Care in Social and Subsocial Spiders Thesis submitted in partial fulfillment of the requirements for the degree of “DOCTOR OF PHILOSOPHY” by Mor Salomon Submitted to the senate of Ben-Gurion University of the Negev April 2007 Beer-Sheva The Direct and Indirect Effects of Maternal Nutrition on the Young via Maternal and Allomaternal Care in Social and Subsocial Spiders Thesis submitted in partial fulfillment of the requirements for the degree of “DOCTOR OF PHILOSOPHY” by Mor Salomon Submitted to the senate of Ben-Gurion University of the Negev Approved by the advisor Approved by the Dean of the Kreitman School of Advanced Graduate Studies April 2007 Beer-Sheva This work was carried out under the supervision of Prof. Yael Lubin Mitrani Department of Desert Ecology Jacob Blaustein Institutes for Desert Research Ben-Gurion University of the Negev Acknowledgments I am grateful for Prof. Yael Lubin guidance during my MSc and PhD studies and for supporting me in expanding the research into the subject of nutritional ecology. My deepest thanks to Dr. David Mayntz of the University of Aarhus, Denmark, who was like a second advisor to me in all matters regarding nutrition. Special thanks to my husband, Yaniv Botner, for his support and encouragement during the long months overseas, his help in the field as a research assistant and for discussions of my research. Over the years I had the pleasure of working with three lab technicians, Ofer Eitan, Iris Musli and Sonia Rozin, whose help in gathering data in the lab and field, translating manuscripts and preparing samples for nutritional analyses was priceless. To Dr. Ally Harri, Dr. Elli Groner, Dr. Tamar Kessar, Prof. Arnon Lotem, Dr. Jutta Schnieder, Dr. Mary Whitehouse, Dr. Itamar Giladi, Daphna Gottlieb, Michal Segoli and Reut Berger-Tal for many fruitful discussions. I thank the research team I had the pleasure to work with in Namibia, Dr. Johannes Henschel, Inga Henschel, Tharina and Chris Bird, Klaus Birkhoffer, Karen and Carl Coats and Nadia Schiling. Last but not least, I would like to thank Dr. David Saltz for help with statistical analysis. The study was carried out in the Marco and Louise Mitrani Department of Desert Research, Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev. Table of contents Abstract in English……………………………………………………………………… 1 General introduction…………………………………………………………………….. 4 Chapter 1: Maternal investment in a spider with suicidal maternal care Introduction…………………………………………………………………. 10 Methods……………………………………………………………………... 12 Results………………………………………………………………………. 15 Discussion……………………………………………………………………17 Figures and Tables……………….…………………………………………. 22 Chapter 2: Effects of prey nutrient composition on reproduction in a spider showing maternal care Introduction…………………………………………………………………. 26 Methods……………………………………………………………………... 29 Results………………………………………………………………………. 34 Discussion…………………………………………………………………... 37 Figures………………………………………………………………………. 43 Chapter 3: Cooperative breeding increases reproductive success in the social spider Stegodyphus dumicola (Araneae, Eresidae) Introduction………………………………………………………………… 50 Methods…………………………………………………………………….. 52 Results……………………………………………………………………… 54 Discussion………………………………………………………………….. 56 Figures……………………………………………………………………… 61 Chapter 4: Colony nutrition affects reproductive skew in a social spider Introduction………………………………………………………………… 65 Methods…………………………………………………………………….. 67 Results……………………………………………………………………… 71 Discussion………………………………………………………………….. 73 Figures……………………………………………………………………… 77 General discussion……………………………………………………………………… 80 Cited Literature…………………………………………………………………………. 87 Abstract in Hebrew……………………………………………………………………... 99 List of Figures Chapter 1 Figure 1: Spiderling body mass in captivity and in the field at different stages of development. Figure 2: Female mass loss at the end of maternal care (after being consumed by her young) in relation to female body mass residuals. Figure 3: Female mass loss after regurgitation and after matriphagy in the different brood size treatments. Figure 4: Average spiderling mass per brood at dispersal in relation to initial female mass at hatching of her young. Figure 5: Time from hatching till dispersal in relation to average spiderling mass at dispersal. Chapter 2 Figure 6: The feeding schedule of subadult, adult females and adult females with egg sacs during the diet manipulation experiments. Figure 7: The effect of the female’s diet on her percent growth in body size (prosoma width). Figure 8: The influence of the maternal diet on the young after matriphagy. Figure 9: Nutrient composition of field-collected females relative to dry mass. Figure 10: Nutrient composition relative to dry mass of females fed on the three diets. Figure 11: Nutrient composition of young after regurgitation-feeding relative to their dry mass. Figure 12: Nutrient composition of young after matriphagy relative to their dry mass. Chapter 3 Figure 13: Average brood size and brood mass taken after the first female was eaten of young cared for by a group of females and young cared for by only their mother. Figure 14: Average brood size, brood mass and individual mass at the end of the maternal care period, for young raised by a group of females and only by their mother. Figure 15: Average brood size, brood mass and average individual mass taken at different stages after the end of the maternal care period, for young raised by a group of females and young raised only by their mother. Chapter 4 Figure 16: The percent of adult females (i.e. reproductive skew) in relation to colony size in field colonies of S. dumicola collected in 2004. Figure 17: The percent of lipids relative to dry mass found in adult and subadult females in un-supplemented field colonies of S. dumicola collected in 2004. Figure 18: The effect of colony size on the percent of adult females (i.e. reproductive skew) in colonies supplemented with either a lipid-rich or a protein-rich diet in 2005. Figure 19: The average body size and body mass of adult females under lipid-rich and protein-rich supplementation diets in 2005. Figure 20: Differential extraction of lipids from crickets by adult and subadult females in the nutrient extraction experiment. 1 List of Tables Table 1: Linear regression results of offspring vs. female variables at hatching in 2001. Table 2: Linear regression results of offspring vs. female variables at hatching in the 2002 brood manipulation experiment. Abstract Parental care is widespread in the animal kingdom and includes behaviors such as preparation of nests and burrows, production and care of eggs and the care of young. Parents provide protection for their offspring from predators and parasites and most importantly provide them with food after hatching or after birth. Providing parental care is costly for the parent, in terms of resources and energy reserves, but generally beneficial for the young whose survival, growth and reproductive value can be increased. Females of the spider Stegodyphus lineatus (Eresidae) produce a single small brood with small eggs and provide the young with regurgitated fluid and later, with their body contents via matriphagy. Selection should favor an optimal distribution of maternal resources at the egg stage versus the post-hatching stage. I investigated resource allocation of females into eggs, regurgitation feeding and matriphagy, and determined how maternal investment affects the young. By following the growth of young in the lab and in the field and measuring the young during the maternal care period, I found that females invest a small amount of their body resources into the egg stage and vary the number of eggs produced, but not their size, according to the amount of resources available to them. Females provided 95% of their body mass to the young, allocating more resources to regurgitation than to matriphagy. Heavy females provided more resources to the young, which resulted in both more and heavier young after maternal care. Achieving a large body size before dispersal from the maternal nest was suggested to increase the survival of the young and their foraging abilities, and thus is likely to increase their reproductive value as adults. My study of S. lineatus showed strong maternal effects on the body mass and development of the young, mediated by regurgitation feeding and matriphagy. These maternal effects relate to the amount of resources provided to the young by their mother. However, the nutritional composition of these resources may also affect the offspring. I hypothesized that the nutritional composition of the maternal diet may affect egg production and be crucial for the growth and development of the young through resources provided at maternal care. Therefore, I studied the influence of the maternal diet on several characteristics of the young. Females in three reproductive stages: before sexual maturation, before oviposition and before hatching of the young, were provided with three different diets varying in protein and lipid ratios. I found that maternal diet before oviposition does not affect the number of eggs produced. I suggest that females invest only a small amount of 1 proteins into the eggs by securing the amount of proteins they need from the prey and may be using protein stores from earlier life stages for egg production. Analysis of the body composition of females before hatching of the young showed that females require both
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