Individual variation in cooperation is a striking yet poorly understood feature of many animal societies, particularly in cooperative breeders where individuals assist in the care of young that are not their own. While previous research on these systems has emphasised the plasticity of helping and how it varies with current environmental and social conditions, in this dissertation I examine how individual variation is constrained and influenced by trade-offs with other behaviours and experiences in early life. I demonstrate that variation in cooperative pup care (babysitting and provisioning) is consistent within individuals over time (Chapter 3). Provisioning is more consistent than babysitting, although the two behaviours are highly correlated within individuals. I then focus on the variation in helping that remains once current factors, such as condition, group size and food availability, are taken into account. In Chapter 4, I explore the possibility that variation in helping can be explained by personality, or consistency in behavioural traits such as exploration or risk-taking. I find little evidence for consistent individual differences in field measures of personality traits, however, with such behaviours instead being group-specific. Early social experiences are known to have important and lasting effects on later fitness and behaviour: in Chapter 5, I demonstrate that, in female meerkats only, growing up in a group with more helpers is correlated with reduced cooperation later in life. This result suggests the importance of future fitness in influencing current cooperative behaviour, as females raised in larger groups are more likely to attain dominance. Finally, I examine the extent to which vocal communication between carers and young is influenced by variation in contributions to cooperation. Females are more sensitive to increased begging rate (Chapter 6), which reflects general sex differences in cooperative behaviour. Carers modify their vocalizations but not their foraging behaviour in the presence of pups, and the way in which they vocalize during provisioning events suggests these calls serve to increase efficiency of prey transfer (Chapter 7).

The red-cockaded woodpecker (Picoides borealis) is a federally endangered species. As such, populations need to be increased in order to achieve recovery goals outlined by the U.S. Fish and Wildlife Service. My thesis is composed of two chapters that represent opposite sides of this issue. The first chapter investigates whether military training activity negatively affects red-cockaded woodpeckers. Military installations in the southeastern United States contain several of the largest remaining red-cockaded woodpecker populations. Six of the 15 installations harboring these birds are designated primary core populations; thus, population increases on these sites are critical to recovery of the species. However, restrictions on military training activity associated with red-cockaded woodpecker protection are a cause of concern on military installations that sometimes constrains management for population growth. Current restrictions are based on assumptions of potential impacts rather than scientific evidence, so we evaluated two different restriction regimes to test for training activity effects. The second chapter concerns how to induce populations to grow more rapidly through natural processes. As a cooperative breeder, red-cockaded woodpeckers preferentially compete for existing breeding positions and queue in the form of helping or floating to obtain a breeding vacancy, rather than create new territories. I used 20 years of demographic data collected as part of a long-term monitoring study of red-cockaded woodpeckers to investigate mechanisms that stimulate territory creation in this cooperatively breeding species. / Master of Science

The measurement of stress hormone levels in wild free-living animals is becoming an increasingly effective method for examining proximate mechanisms of animal behavior and the physiological impacts of human activities on wildlife. In these studies I measured plasma levels of the stress hormone corticosterone in the endangered red-cockaded woodpecker (Picoides borealis) to determine their role in the reproductive behavior of individuals in this species, and whether they are affected by human disturbance. In chapter one, I provide an introduction to the vertebrate stress response and I describe the natural history of the red-cockaded woodpecker. In chapter two, I compare corticosterone and reproductive hormone levels between breeding males and helper males to examine hormonal mechanisms of reproductive suppression in helper males. No hormonal differences existed between breeding and helper males. However, baseline corticosterone levels were lower in all males living in groups with two or more helper males, suggesting that male helpers reduce the workload of all other group members. In chapter three, I compare corticosterone levels between birds living in clusters subject to two different training restriction regimes on a military installation. Males living in clusters without training restrictions had lower baseline corticosterone than those living in clusters with training restrictions, suggesting that males habituate to chronic disturbance by downregulating baseline corticosterone levels. / Master of Science

Oxidative stress has recently been highlighted as a potential physiological mechanism underpinning life-history trade-offs in animals. While the role of oxidative stress in mediating such trade-offs is receiving increasing attention, its importance in wild populations remains poorly understood. In this thesis, I use a wild population of cooperatively breeding white-browed sparrow weavers (Plocepasser mahali) to investigate the role that oxidative stress plays in mediating the costs of reproduction and immune defence. Cooperative animal societies offer a unique opportunity to investigate the costs of reproduction, because dominants frequently monopolise breeding opportunities (exhibiting higher reproductive effort than subordinates), and subordinate cooperative contributions frequently lighten reproductive workloads. My findings reveal, first, that dominants’ reproductive monopolies do not arise because they exhibit superior oxidative balance, as no such rank-related differences in oxidative state exist prior to breeding (Chapter 2). However, the higher reproductive effort of dominant females may underpin their differential declines in antioxidant protection after the breeding season (Chapter 2). Second, experimental manipulation of reproductive effort reveals marked oxidative damage and body mass costs incurred during reproduction. However, these costs are entirely mitigated in large social groups, suggesting that the cooperative contributions of helpers may offset the costs of reproduction for all group members (Chapter 3). While this represents rare evidence of an oxidative stress cost of reproduction in the wild, longitudinal data suggests that these costs do not endure after the breeding season (Chapter 4), highlighting that circulating markers of oxidative balance are unlikely to mediate long-term costs of reproduction. Finally, an immune activation experiment reveals that, while mounting an immune response causes no net change in oxidative balance, the scale of the response can be adjusted according to baseline antioxidant protection in an oxidative-condition-dependent manner (Chapter 5). Together my results provide support for the role of oxidative stress in shaping life histories in the wild. Furthermore, evidence of rank-related disparities in oxidative balance and the avoidance of reproductive costs in large social groups may have important implications for our understanding of both the evolution of cooperative breeding and the patterns of health and ageing in societies.

Telomeres are increasingly used as biomarkers of somatic maintenance and could conceivably play a causal role in life history trade-offs. In this thesis, I use longitudinal telomere measures from a wild population of cooperatively breeding white-browed sparrow weavers (Plocepasser mahali) to further our understanding of the causes and fitness consequences of individual variation in somatic maintenance, with particular focus on hitherto unexplored effects of the social environment. In Chapter 2, I start by investigating the key prediction of life-history theory that shortfalls in somatic maintenance in early life entail later-life costs, and find supporting evidence. Nestlings with higher within-individual rates of telomere attrition show reduced survival to the following season, even after controlling for the effects of variation in body mass. In Chapter 3, I then investigate the effects of the social and abiotic environment on nestling telomere length and attrition rates and find the first support, to my knowledge, for the key prediction that helpers in cooperatively breeding societies alleviate telomere attrition rates in growing offspring (consistent with the expectation that helper contributions to nestling feeding relax resource allocation trade-offs in offspring). In addition, I find that rainfall prior to egg-laying has a positive effect on hatchling telomere length; an effect that most likely arises via egg- or incubation-mediated maternal effects. In Chapter 4, I investigate the causes of variation in telomere attrition rates in adults, and while there are no overall differences in telomere length or long-term within-individual telomere dynamics between dominant and subordinate birds, my findings are suggestive of dominance-related differences in the short-term regulation of telomere length. In addition, and in concordance with predictions of life-history theory regarding trade-offs between somatic maintenance and reproduction, I find that annual rainfall (a proxy for reproduction-related activity during the breeding season) negatively predicts the within-individual rate of change in telomere length in adults specifically over the breeding season; there was no such relationship in the non-breeding season. Finally, in Chapter 5, I investigate the extent to which natural variation in oxidative state predicts variation in within-individual rates of change in telomere length over time. This chapter provides evidence suggestive of associations between oxidative state and telomere dynamics in a natural population, and highlights complexity in the nature of these relationships. Together my findings provide novel support for key predictions of life-history theory regarding the causes and consequences of variation in somatic maintenance, and lend strength to the view that longitudinal field studies of telomere dynamics can offer useful insights in this regard. Furthermore, my findings highlight the potential for diverse effects of the social environment on patterns of somatic maintenance, and specifically hitherto unexplored downstream effects of helping behaviour on later-life performance and ageing trajectories.

The social mole-rats have often been typecast as extreme examples of mammalian sociality. With their pronounced reproductive skew, status-related contrasts in lifespan and morphology, and the suggestion of a division of labour amongst helpers, mole-rat societies have repeatedly been likened to the structurally complex societies of some eusocial insects. However, because few studies of mole-rats have quantified individual variation in growth and behaviour across long periods of development, it has remained unclear the extent to which mole-rat societies, and the features of individuals within them, should be considered unique amongst social vertebrates. In this thesis, I examine life history variation in Damaraland mole-rats Fukomys damarensis from three perspectives- growth, behaviour, and ageing- to explore how individual developmental trajectories contribute to, and are influenced by, the structure of mole-rat societies. First, I use a large longitudinal dataset to test for the presence of behavioural specialisation in non-breeding mole-rat helpers. I find no indication of individual specialisation in cooperative activities. Instead, individual differences in helping behaviour are largely the result of age-related changes in the extent to which individuals commit to all forms of helping (Chapter 3); refuting the notion of helper castes. I then focus on the variation in growth across non-breeders, developing a novel biphasic model to accurately quantify sex differences in growth and explore the influence of social effects on growth trajectories (Chapter 4). Despite the proposition of intense intrasexual competition in mole-rat societies, there was no clear signature of sex-specific competition on helper growth trajectories. A more conspicuous form of socially-mediated growth in mole-rats is the secondary growth spurt displayed by females that have acquired the dominant breeding position, causing them to become larger and more elongated. By experimentally controlling reproduction in age-matched siblings, I show that rather than being stimulated by the removal from reproductive suppression, this adaptive morphological divergence is achieved through a lengthening of the lumbar vertebrae when breeding is commenced (Chapter 5). With contrasts in size and shape following the acquisition of the breeding role, this status-related growth pattern shares similarities with growth in naked mole-rats and other social vertebrates. Breeders also show a twofold greater lifespan than non-breeders in Fukomys mole-rats, prompting the suggestion that the transition to dominance also sets individuals onto a slower ageing trajectory. To date, there is little evidence to support a physiological basis to lifespan extension in breeders. This assertion is bolstered by the absence of longer telomeres or slower rates of telomere attrition in breeding females compared to non-breeding females residing in groups (Chapter 6), each of which might be expected if breeders age more slowly. I argue that previous studies exploring status-related ageing in captive Fukomys mole-rats have overlooked the importance of demographic processes (and associated behavioural influences) on mortality schedules. Irrespective of the proximate basis of the longer lifespan of breeders, at an interspecific level the social mole-rats are unusually long-lived for their size. A recent large-scale comparative analysis concluded that prolonged lifespan is a general characteristic of all mammalian cooperative breeders, but this conclusion is premature, as in most of the major clades containing both cooperative and non-cooperative species there is no consistent trend towards lifespan extension in cooperative species (Chapter 7). In the case of mole-rats, it seems more likely that their exceptional longevity arises principally from their subterranean habits and related reductions in extrinsic mortality. Overall, these findings demonstrate that cooperative breeding has important consequences for individual life histories, but there is no strong basis for the claim that Damaraland mole-rat societies are markedly different in form than other cooperative breeding societies.

All human societies process their food extensively by thermal and non-thermal means. This feature distinguishes us from other species, and may even be compulsory given that humans are biologically committed to an energy-rich diet that is easy to chew and digest. Yet the energetic consequences of food processing remain largely unknown. This dissertation tests the fundamental hypothesis that thermal and non-thermal processing lead to biologically relevant increases in energy gain from protein-rich meat and starch-rich tubers, two major caloric resources for modern and ancestral humans that present divergent structural and macronutrient profiles. The energetic consequences of food processing are evaluated using three indices of energy gain, each of which account for costs not currently captured by conventional biochemical assessments of dietary energy value. Chapter 2 investigates the effects of cooking and pounding on net energy gain as indexed by changes in body mass, controlling for differences in food intake and activity level. Chapter 3 examines the effect of cooking and pounding on diet-induced thermogenesis, the metabolic cost of food digestion. Chapter 4 considers the effort required to engage in food processing, arguing that the advantageous ratio of benefit to cost has likely had important effects on human life history. By each of these definitions of energy gain, food processing is shown to have substantial energetic significance. Overall, energetic gains due to thermal processing exceeded those of non-thermal processing, consistent with recent proposals that the adoption of cooking had a particularly important influence on human biology. Gains due to food processing were observed in both meat and tuber substrates, supporting a transformative role for habitual food processing in the evolution and maintenance of the human energy budget. / Human Evolutionary Biology

Das Tierreich zeichnet sich durch eine große Diversität an Sozialsystemen aus, die von einer einzelgängerischen Lebensweise bis hin zum Leben in komplexen sozialen Gruppen reicht. Diese Variation in Sozialsystemen liefert den perfekten Rahmen um die evolutionäre Entwicklung von sozialen Merkmalen zu untersuchen. Ein besonders erfolgsversprechender Ansatz besteht darin, eng verwandte Arten, die sich durch einen unterschiedlichen Grad der Vergesellschaftung auszeichnen, miteinander zu vergleichen. Die Charaktersierung von Sozialsystemen wird für verschiedene taxonomische Gruppen unterschiedlich gehandhabt. Bei Vögeln wird das Sozialsystem normalerweise durch das Brut- und das soziale Paarungssystem charakterisiert. Die meisten Vogelarten sind paarlebend, aber man findet auch komplexere Gruppen welche im Allgemeinen durch das Verbleiben der Jungen am Aufwuchsort und kooperatives Brüten charakterisiert sind. Bisher wurden verschiedene Hypothesen im Zusammenhang mit Demographie, Ökologie, Lebensgeschichte und Verwandtschaftsverhältnissen vorgeschlagen um den Übergang von Paarbrütern zu kooperativen Brutsystemen in Vögeln erklären. Kurzfuß-Stelzenrallen (Mesitornis variegata) sind mittelgroße, am Boden lebende Vögel, die zur Familie der Mesitornithidae gehören. Diese Vogelfamilie ist endemisch in Madagaskar und beinhaltet zwei weitere allopatrische Arten, welche sich hinsichtlich des Grades der Vergesellschaftung unterscheiden: Die Einfarb-Stelzenralle (Mesitornis unicolor) des östlichen Regenwaldes welche in Paaren brütet und die Monias-Stelzenralle (Monias benschi) des südlichen Dornenwaldes welche in Gruppen lebt und kooperativ brütet. Die Kurzfuß-Stelzenralle hingegen kommt im westlichen Trockenwald vor und lebt für gewöhnlich in Paaren oder kleinen Gruppen von denen angenommen wird, dass es sich um Familiengruppen handelt, wobei allerdings nur wenig Informationen über das Brutsystem vorhanden ist und bisher keine Studie die genetischen Verwandtschaftsverhältnisse innerhalb der kleinen sozialen Einheiten untersucht hat. Das Hauptziel dieser Arbeit war es erstens die verschiedenen Komponenten des Sozialsystems der Kurzfuß-Stelzenrallen zu beschreiben, ein Art für welche bisher angenommen wurde das sie kooperativ brütet, deren Jungen jedoch Nestflüchter sind und prinzipiell nur wenig elterliche Fürsorge benötigen. Zweitens sollten die proximaten und ultimativen Ursachen untersucht werden, die dieses Sozialsystem geformt haben könnten. Um dieses Ziel zu erreichen habe ich genetische, morphologische, räumliche sowie Verhaltensdaten von 10 bis 15 sozialen Einheiten von M. Variegate während fünf Feldsaisonen (Oktober 2009 bis April 2012) im Kirindy-Wald im Westen von Madagaskar gesammelt. Das Ergebnis dieser Studie zeigt, dass die Kurzfuß-Stelzenralle in sehr kohäsiven stabilen Paaren oder kleinen Familien lebt, die durch eine verspätete Abwanderung der Jungtiere entstehen, und dass nur die Elterntiere sich um die Aufzucht der Brut kümmern. Außerdem versorgen die Eltern ihre Jungen entgegen bisherigen Vermutungen in den ersten zwei Lebensmonaten intensiv mit Nahrung, und auch darüber hinaus bis zum 12. Lebensmonat obwohl mit viel geringerer Häufigkeit. Diese lange Periode der elterlichen Fürsorge hängt wahrscheinlich mit der langsamen Entwicklung der Jungtiere hinsichtlich der für die Nahrungssuche erforderlichen Fertigkeiten zusammen. Die hohe Kohäsion sozialer Einheiten mit inter-individuellen Abständen von selten mehr als drei Metern steht eher mit einer Strategie der Raubfeindvermeidung als einer Strategie zur Verhinderung des Fremdgehens in Verbindung. Dennoch kann die hohe Kohäsion zwischen Paarpartnern das streng monogame Paarungssystem erklären. Die Untersuchung des Abwanderungsverhaltens hat ergeben, dass männliche Nachkommen länger in ihren Familien bleiben als weibliche, was mit der beobachteten langsameren Fluktuation der erwachsenen männlichen Population und dem Vorhandensein von „Stiefmüttern“ in einigen Familien übereinstimmt. Darüber hinaus konnte ich durch den Vergleich von Paaren mit und ohne Nachwuchs zeigen, dass Familienleben für die Eltern hinsichtlich der Effizienz der Nahrungsbeschaffung und hinsichtlich der Investitionen in zukünftige Reproduktion kostspielig ist. Dies könnte die Intoleranz der Eltern gegenüber älteren Nachwuchs erklären, welche ich beobachten habe. Zusammenfassend kann gesagt werden, dass die Einschränkungen bezüglich unabhängigen Brütens und einzelgängerischen Umherstreifens in Kombination mit der langsamen Entwicklung der Fähigkeiten die im Zusammenhange mit der Nahrungsbeschaffung stehen und elterliche Kosten wichtige Faktoren sind, welche das Abwanderungsverhalten der Jungtiere, die Bildung von Familien und die Familienstabilität in dieser Art erklären. Zusätzlich beeinflusst die Gefahr von Raubfeinden, die mit der starken Kohäsion innerhalb sozialer Einheiten einhergeht, das Paarungssystem bei Kurzfuß-Stelzenrallen und legt eine Verbindung zwischen genetischer Monogamie und Raubfeindruck bei sozial monogam lebenden Arten nahe. Basierend auf einem Vergleich mit den anderen Arten der Familie der Mesitornithidae könnte das Brutsystem der Kurzfuß-Stelzenralle als Übergansstadium zwischen einem allein auf den beiden Elternteilen basierenden und einem kooperativen Brutsystem erachtet werden in dem einige Jungen fähig wären Hilfe zu stellen, aber von den Eltern daran gehindert werden.

Group-living sets the scene for complex social behaviours such as cooperative breeding, and exploring the factors that shape group-living is crucial in understanding these behaviours. This thesis explores the ecology of a population of the facultative cooperative breeding southern anteater-chat (Myrmecocichla formicivora), a group-living bird species endemic to southern Africa. It reveals a breeding system based around a breeding pair and up to three auxiliary males. Despite equal numbers of males and females produced as fledglings there was a surplus of adult males, which remained philopatric. Dispersal was strongly female biased. Females dispersed within their first year, they dispersed further than males, and they lost the benefits of the natal site. The sex skew in the population suggested that these factors drive differential mortality, with juvenile females having much lower annual survival than juvenile males. Adult survival was higher, with female survival only slightly lower than male survival. Dispersal distances suggested that males selected the breeding location, nearer to their natal site. There was no evidence of surplus non-breeding females. On the loss of a breeding female there was no replacement until new females entered the population, yet if a breeding male disappeared the female promptly re-paired with a male from another group. There was no indication of birds floating in the population, and if males were orphaned or widowed they joined other groups as unrelated helpers in preference to floating. There was no sign of inter-group or individual aggression among chats, and unrelated helpers were peacefully accepted into groups, suggesting mutual benefits. In fact all birds in a group helped raise offspring of the breeding pair, and groups with more helpers fledged more offspring, which implies that both direct and indirect fitness benefits can be gained through joining a group and helping. There was surprisingly little inheritance of breeding position by auxiliaries, and strikingly low levels of extra-pair paternity. This study suggests that the Southern anteater-chat group structure arises through male philopatry due to a shortage of breeding females, the benefits of remaining on the natal site and helping, and the potentially high costs of living alone.

Thesis (Ph. D.)--State University of New York at Binghamton, Department of Biological Sciences, 2009. / Includes bibliographical references.