Complete Thesis

University of Groningen

Better together Groenewoud, Frank

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Download date: 09-10-2021 Better Together Cooperative breeding under environmental heterogeneity

Frank Groenewoud The research presented in this thesis was carried out in the Behavioural Physiology and Eco- logy (BPE) group, which is part of the Groningen Institute for Evolutionary Life Sciences (GELIFES) at the University of Groningen and the Behavioural Ecology group at the Univer- sity of Bern, Institute of Ecology and Evolution.

This thesis is financially supported by the Netherlands Organisation for Scientific Rese- arch (NWO-TOP-854.11.003 to JK/DSR; NWO-ALW-823.01.014 to JK), the European Commu- nity’s Sixth Framework Programme (028696 to JK), the Swiss National Science Foundation (310030B_138660 and 31003A_156152 to MT; 31003A_144191 and 31003A_166470 to JGF), the Rektorenkonferenz der Schweizer Universitäten (CRUS) for their contribution within the framework of the “Cotutelles de these” program. Printing was supported by the University of Groningen and the Faculty of Science and Engineering..

ISBN (printed book): 978-94-034-1156-9 ISBN (e-book PDF without DRM): 978-94-034-1155-2 Cover: Tim Holland Illustration: Jacqueline van Rhijn Layout: Ilse Modder, www.ilsemodder.nl Printing: Gildeprint - Enschede, www.gildeprint.nl

© Frank Groenewoud, 2018 For all articles published, the copyright has been transferred to the respective publisher. No part of this thesis may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, without written permission from the author or, when appropriate, from the publisher. Better Together Cooperative breeding under environmental heterogeneity

PhD thesis

to obtain the degree of PhD of the University of Groningen on the authority of the Rector Magnificus Prof. dr. E. Sterken and in accordance with the decision by the College of Deans.

and

to obtain the degree of PhD of Science in Ecology and Evolution of the University of Bern on the authority of the Rector Prof. dr. C. Leumann and the Dean of the Faculty of Science Prof. dr. Z. Balogh.

Double PhD degree

This thesis will be defended in public on Friday 16 November 2018 at 12.45 hours

Frank Groenewoud born on 25 October 1984

in Leiden Supervisors Prof. dr. ir. J. Komdeur Prof. dr. M. Taborsky

Co-supervisors Dr. S. A. Kingma

Assessment Committee Prof. dr. I.R. Pen Prof. dr. H. Kokko Prof. dr. S. Alonzo Prof. dr. J.M. Gaillard

CONTENTS

Chapter 1 General introduction 9

Chapter 2 Predation risk drives social complexity in cooperative breeders 23

Chapter 3 Spatio-temporal resource variation, group formation and the 43 benefits of cooperative breeding in the Seychelles warbler

Chapter 4 Subordinate females in the cooperatively breeding Seychelles 67 warbler obtain direct benefits by joining unrelated groups

Chapter 5 Predation risk mediates the benefits of sociality and 87 suppresses within-group conflict in a cooperatively breeding cichlid fish

Chapter 6 Experimentally induced anti-predator responses are sex 107 specific and mediated by social and environmental factors in a cooperatively breeding passerine

Box A Box A: Anti-predator benefits drive communal breeding in the 125 Seychelles warbler

Chapter 7 Synthesis 131

References 141

Nederlandse samenvatting 159

Dankwoord/Acknowledgements 169

Chapter 1

General introduction CHAPTER 1

INTRODUCTION

How I have enjoyed watching the simple life of this happy and affectionate family. Perfect harmony reigns between all; I am beginning to believe these birds incapable of a show of anger toward each other. Better such a life in the open fields, on a diet of cockroaches and grasshoppers, than life in a palace where the board groans under the cream and honey of the land, with the constant disagreements and bickerings which so often disfigure the conduct of the wealthy. From: “Groove-billed Ani – some reflections on their family rela- tions,” Journal, Vol. 5, September 22, 1930 – Alexander F. Skutch

The passage above was written in 1930 by the then twenty six year old Alexander Skutch (who died in 2004 – just eight days short of his one hundredth birthday), where he describes the pleasantly simple life of a group of groove-billed anis (Crotophaga sulcirostris). A few years later, Skutch would formalize these and other observations in an article where he coined the term “helpers at the nest”, which is still in use today to refer to particular types of cooperative breeding (Skutch 1935). In the broadest sense, cooperative breeding is an umbrella term for any system where more than two individuals are engaged in raising offspring. Even without the aid of modern molecular techniques to confirm relatedness, and the use of banding to distinguish between individuals, Skutch appreciated by careful observations that different categories of “helpers at the nest” existed, and made the distinction between (i) juvenile helpers, which are retained offspring that provided alloparental care to their younger siblings, (ii) unmated sexually mature helpers, which cannot breed themselves due to a lack of mates or breeding vacancies, and decide to help others, and (iii), mutual helpers, which are breeding birds that assist each other in rearing their own respective fam- ilies. While many of the cooperatively breeding birds, fishes, mammals and insects known today could be assigned to one (or a combination) of these categories, our understanding of the environmental, social and genetic factors that drive these behaviours within- and between species, on both proximate and ultimate levels, has improved considerably (Koenig & Dickinson 2016). However, we are still far from a general “theory of cooperative breeding”, as it has proven difficult to find the right balance between simple, generalizable hypotheses and predictions, and the number of systems to which these would apply. Many different reasons have contributed to this conundrum. First, within-species variation (i.e. between individuals and/or between populations) is the rule rather than the norm. Different subordinates in the same species could be providing care for different reasons depending on potential future fitness benefits that may depend on sex, age, relatedness or body condition. Between-population variation poses a particular problem for studies that try to develop insights into the evolution of cooperative breeding using comparative methods. These approaches usually resort to taking some kind of average trait value, or using data only from

10 GENERAL INTRODUCTION

a single population, leading to a loss of valuable information on the ecological drivers of cooperative breeding. Second, while cooperative breeding was initially studied in birds, it also occurs in mammals, insects and fishes, further complicating generalization due to vastly different modes of reproduction (i.e. oviparity vs viviparity), and life histories (e.g. growth patterns, number of offspring; Wilson 1971; Cockburn 1998; Clutton‐Brock 2006; Ta- borsky 2016). Last, cooperative breeding encompasses a whole range of different breeding and social systems (Cockburn 1998; Hatchwell 1999; Cockburn 2006; Riehl 2013), such as groups that consist of unrelated coalitions (e.g. dunnocks) and those that form (primarily) through the delayed dispersal of offspring (e.g. Seychelles warblers), and these systems likely had very different evolutionary origins (Ligon & Burt 2004; Clutton-Brock 2009; Wong et al. 2012; Riehl 2013). Despite all these reservations, the field of cooperative breeding, and the study of its genetic, social and ecological drivers has come a long way since its first descrip- tions by early observers.

Providing a comprehensive overview of the cooperative breeding literature over the past decades is beyond the scope of this introduction. Instead I would like to highlight some important contributions that focus on the ecological drivers of cooperative breeding, specifically the environmental conditions that affect the costs and benefits of delayed dispersal and helping behaviours (i.e. alloparental care). After this more general background, I will briefly introduce my two study species: the Seychelles warbler (Acrocephalus sechellensis) and the cooperatively breeding cichlid Neolamprologus pulcher. Lastly, I will summarize the questions that will be the focus of the remaining chapters of my thesis.

Cooperative breeding: a two-step process While various evolutionary routes to cooperative breeding have been proposed, most forms of cooperation occur in family groups (Cockburn 2006; Riehl 2013). Two likely explanations exist for why this is so. First, delayed or limited dispersal of offspring is one of the primary modes by which cooperative breeding groups form (Emlen 1982; Koenig et al. 1992; Griesser et al. 2017). Second, kin selection – selection on genes through its effects on others carrying the same gene (Hamilton 1963) – is an important evolutionary driver of cooperation (West-Eberhard 1975; Foster, Wenseleers & Ratnieks 2006; Bourke 2014). It should be noted that these two statements relate to different processes: group formation in the former, and the benefits of cooperation, or helping, in the latter. This distinction is why it is generally accepted that the evolution of cooperative breeding is best approached as a two-step process where delayed dispersal is a necessary, but not a sufficient condition for the evolution of cooperative breeding. While it is difficult to overstate the importance of kin selection theory in the last half century of research in the field of cooperation (West-Eberhard 1975; Bourke 2014), its importance for the evolution of cooperative breeding has been put into

11 CHAPTER 1

question (Clutton-Brock 2002, 2009). This has generally not been because of flaws in the theory itself, but rather because most studies that invoked kin selection were correlation- al, and other (direct) benefits could therefore be in place (e.g. Wright 2007; Taborsky 2013; Kingma et al. 2014). Despite these criticisms, support for kin selection theory is strong, both within (e.g. Emlen & Wrege 1989; Komdeur 1994b; Richardson, Komdeur & Burke 2003b; Wright et al. 2010), and between species (Hughes et al. 2008; Cornwallis et al. 2010; Lukas & Clutton-Brock 2012; Dillard & Westneat 2016). Furthermore, empirical tests of the benefits of cooperative breeding in any particular species only apply to the selective forces that are currently maintaining cooperative breeding, but not necessarily to its evolutionary origins. Kin selection might therefore have been a necessary initial driver of cooperation, but once these conditions were set, other direct benefits may have evolved that were not necessarily dependent on genetic relatedness (Cockburn 2013). This thesis does not focus on the indirect (kin selected) or direct benefits of cooperative breeding per se, but rather on the ecological and environmental factors that shape the costs and benefits of dispersal and group formation, cooperative breeding and the stability of groups.

Environmental heterogeneity and the evolution of delayed dispersal Delayed dispersal is often seen as a necessary first step for the evolution of cooperative breeding, at least in so called “helpers at the nest” type systems, where the majority of helpers are the offspring of previous breeding attempts (Emlen 1982; Koenig et al. 1992; Riehl 2013). Such delayed dispersal does not necessarily lead to cooperative breeding, if there are no further benefits of helping. Consequently, many family living species exist, where subordinates do not show alloparental care (Griesser et al. 2017). Two main hypotheses have been proposed that make predictions regarding the environmental conditions under which delayed dispersal should be the preferred strategy by offspring. The “ecological constraints” hypothesis suggests that constraints on dispersal and independent breeding reduce the fitness benefits of leaving the natal territory, so that offspring achieve higher fitness by postponing breeding, and potentially staying at home (Selander 1964; Brown 1974; Emlen 1982). This hypothesis predicts that constraints on independent reproduction could arise through stable environments leading to habitat saturation and thus a lack of available suitable breeding opportunities, or alternatively, fluctuating environmental conditions leading to high costs of dispersal or rearing young in bad years (Emlen 1982). Habitat saturation has been criticized as being an insufficient explanation for the evolution of cooperative breeding, because of the observation that many, if not most species, experience severe competition for suitable breeding positions, yet do not show delayed dispersal (Stacey & Ligon 1991; Koenig et al. 1992). The “benefits of philopatry” hypothesis argues that subordinate individuals should forego dispersal if the benefits in their resident territory (e.g. food, protection) exceed the benefits of dispersal (Stacey & Ligon 1991). This hypothesis assumes that

12 GENERAL INTRODUCTION

variation in quality between territories is required to offset the cost of delayed reproduction by increased fecundity or survival when a high-quality territory is acquired. Although it has generally been agreed that these two hypotheses are effectively two sides of the same coin, and differ only in their focus on the benefits of staying versus the costs of leaving (Emlen 1994), there are notable differences. First, if the ecological constraints hypothesis only includes the costs and benefits of independent reproduction, but not dispersal, offspring should not necessarily remain philopatric. In fact, unless there are some additional benefits of philopatry, offspring could disperse and roam through the population without association to any group or territory, a strategy generally referred to as “floating” (Koenig et al. 1992; Ridley, Raihani & Nelson-Flower 2008; Kingma et al. 2016a). In contrast, the benefits of philopatry hypothesis explicitly emphasizes the benefits that can be gained on the natal territory, thereby excluding the possibility of floating as a viable option. However, most individuals will experience some combination of ecological constraints and benefits in the natal territory, potentially leading to selection for natal philopatry, and delayed reproduction (Koenig et al. 1992; Emlen 1994; Komdeur 1992).

The ecological constraints and benefits of philopatry hypotheses also differ in whether they emphasize temporal or spatial variation in environmental conditions as the primary driver of delayed dispersal. The ecological constraints” hypothesis derives its predictions mainly from environmental fluctuations (or lack thereof) through time that determine the costs and benefits for offspring to disperse or breed independently. For example, the number of breeding vacancies might be higher following a year with high breeder mortality, and years with high food availability might lead to lower costs of dispersal or independent breeding. In both examples, temporal variation in environmental conditions lead to decreased costs, or increased benefits, of dispersal. In contrast, when there is no variation in quality between territories, offspring have no prospect of obtaining a higher quality territory by initially delaying dispersal. Thus, the benefits of philopatry hypothesis requires consistent spatial variation in order for delayed dispersal to evolve.

Both the ecological constraints and the benefits of philopatry hypothesis emphasize the relative costs and benefits of dispersal vs natal philopatry for subordinates, but do not include the costs and benefits of these subordinates for the rest of the group. These can be especially important when (i) individuals have an effect on the fitness of other group members, and (ii) when a few group members (e.g. dominants) can control group membership (e.g. through eviction). While not further explored here, recent studies have taken such effects into account and have consequently provided important insights into the conditions under which groups form (Shen et al. 2017).

13 CHAPTER 1

Environmental heterogeneity and the benefits of helping In order for natal subordinates to be able to provide alloparental care, they have to be (i) present during a breeding attempt and (ii) capable of providing alloparental care. Obvi- ously, there are large differences in rates of maturation, and inter-reproductive intervals between different species and taxa that could affect these two conditions. For instance in the facultative eusocial hover wasp Liostenogaster flavolineata, nesting is year-round due to a lack of seasonality, and newly emerged females are almost immediately capable of providing alloparental care. Conversely, white-winged choughs (Corcorax melanorhamphos) only breed during the breeding season, which is a yearly occurrence. This necessitates offspring to remain with their parents for at least a year to be able to provide help. Subordinates can provide a wide range of alloparental care behaviours that are mostly an extension of the types of parental care provided by breeding pair. Help can consist of providing food to dependent young, egg-cleaning, incubation, nest-building, territory defense and territory maintenance (Brown 1987; Heinsohn & Legge 1999; Taborsky 2016).

Helping is not a necessary consequence of delayed dispersal: offspring could delay dispersal and remain in the natal group, but not provide help (Drobniak et al. 2015; Griesser et al. 2017). Thus, there need to be additional benefits that select for helping behaviour by subordinates, and these benefits – which can be broadly categorized into indirect benefits (i.e. benefits accrued through kin selection), and direct benefits – have been extensively dis- cussed and reviewed (e.g. Cockburn 1998; Clutton-Brock 2002; Bergmülleret al. 2007; King- ma et al. 2014). The costs and benefits of subordinate help can be affected by abiotic and biotic conditions. For instance, when nestling starvation is the main cause of reproductive failure, subordinates in cooperatively breeding birds are expected to have a larger impact on reproductive success when food conditions are poor than when these are high (i.e. the “hard life” hypothesis; Koenig, Walters & Haydock 2011). The main reasoning behind this is that when conditions are good and food availability is high, the additional food provisioned by helpers is less valuable than when food conditions are poor and additional food might mean the difference between reproductive failure and success. A similar argument could be made with regards to any other ecological pressure that affects the reproductive success or survival or groups that can be modulated through subordinate help, such as reducing the risk of predation. One additional benefit of improving reproductive success under harsh environmental conditions is that offspring produced under such conditions are more valuable, because fewer total offspring are produced in such years, and relative contribution to population growth (i.e. reproductive value; Fisher 1930; Taylor 1990) is therefore higher. In addition, there are other benefits of reducing variance in reproductive success that is induced by temporal variation in environmental conditions. Such strategies (i.e. reduced fecundity variance at the expense of mean fecundity) are generally referred as “bet-hedging”

14 GENERAL INTRODUCTION

strategies (Gillespie 1977; Lehmann & Balloux 2007; Starrfelt & Kokko 2012). Several studies have recently suggested that cooperative breeding might similarly be a bet-hedging strategy that buffers against fecundity variance induced by temporal fluctuations in environmental conditions (Rubenstein 2011; Koenig & Walters 2015). Further support for cooperative breeding as a bet-hedging strategy comes from comparative studies that show that the occurrence of cooperative breeding is positively associated with climatic uncertainty and variability (Jetz & Rubenstein 2011; Cornwallis et al. 2017; Lukas & Clutton-Brock 2017). Thus, while it has been suggested that the benefits of cooperative breeding can depend on (fluctuations in) the environment, how and under what conditions subordinates in cooperative groups can improve reproductive success has received little attention.

The suppression of within-group conflict Living in social groups provides many benefits for group members, but also comes with costs (Alexander 1974). One of the major costs of group living concerns conflict over the distribution of limited resources (i.e. food, reproduction) between members of these groups. Such conflict leads to behaviours that aim to secure a larger share of resources, thereby negatively affecting the stability of groups and potentially negating the benefits of sociality (Shen, Akçay & Rubenstein 2014). Investigating the factors that reduce conflict is thus important for understanding the evolutionary stability of groups (West et al. 2015). One important way by which conflict could be reduced between members of a social group, is when environmental conditions improve the fitness benefits of group living relative to leaving the group. These conditions should select for individuals refraining from using aggression to obtain a larger share of resources, because in doing so, they are reducing the fitness benefits they accrue through other group members (Alexander 1974; Brown 1982; Shen et al. 2014). While predation risk is often invoked as an important factor selecting for group-living (Inman & Krebs 1987; Krause & Ruxton 2002), its role in the evolution of more complex social organisation, such as that of cooperative breeders, has been largely neglect- ed. This is surprising, because predation risk can have substantial consequences for (i) offspring survival, which might require cooperation between individuals and (ii) the costs of dispersal and independent reproduction, selecting for limited dispersal. Predation risk can therefore influence both the benefits of group-living and cooperation, as well as the costs of leaving the group and breeding independently. Consequently, increased levels of predation risk should minimize the willingness of individuals to obtain a larger share of group resources at the expense of others, and reduce conflict between group members.

Ecological factors such as predation risk and food availability can have important consequences for group formation through delayed dispersal, the benefits of cooperation and levels of within-group conflict, all important aspects in the evolution of complex social sys-

15 CHAPTER 1

tems and cooperative breeding. Investigating how these ecological factors shape the social systems and behaviours of cooperative breeders can therefore provide insights into the processes that underlie transitions from simple to complex social organization. In the coming paragraphs, I will introduce the species that I will use throughout the rest of my thesis to address these questions, the cooperatively breeding Seychelles warbler Acrocephalus sechellensis and the social cichlid Neolamprologus pulcher.

Island life The Seychelles warbler is a small (13-19 g) facultative cooperatively breeding passerine endemic to several islands in the Seychelles archipelago (Fig. 1.1A; Komdeur et al. 2016, 2017). By the 1960’s, the last decimated population of Seychelles warblers (26-50 individuals) was confined to the island of Cousin (ca 29 ha; 04º20’S, 55º40’E). Habitat restorations and several translocations to other islands have restored the population to viable numbers and have provided a unique opportunity to study the cooperative breeding system of this once critically endangered species. Most Seychelles warblers on the island of Cousin (Fig. 1.1B), which is our main study population, live in pairs (ca 60% of all territories), but a proportion lives in groups consisting a dominant breeding pair and 1-5 subordinates (mean ± SE = 0.59 ± 0.02; 1996-2016; see chapter 3) of either sex. These helpers are usually, but not always the offspring of the dominant breeding pair (Kingma et al. 2016a; see chapter 3). Territories are defended year-round and breeding pairs often remain pair-bonded on the same territory throughout their lives. Seychelles warblers on Cousin Island typically produce single egg clutches, but around 13% of clutches contain 2-3 eggs (Richardson et al. 2001). Offspring can remain nutritionally dependent on their parents and other group members for a period of up to three months, which is extremely long for a passerine species.

The population of Seychelles warblers on Cousin Island is contained, with virtually no migration on or off the island (Komdeur et al. 2004a). Additionally, annual resighting probabilities of birds on the island are extremely high: up to 0.98 for adult birds, and 0.92 for younger individuals (Brouwer et al. 2010). This combination makes the Seychelles warbler an excellent system to study the factors associated with natal dispersal, because these are not confounded by individuals dispersing from the study site. Seychelles warblers are strictly insectivorous, taking most of their arthropod prey from the underside of leaves (Komdeur 1991). They are thus highly dependent on the relatively short peaks in abundance of these prey following monsoon rains, which occur twice per year (Komdeur & Daan 2005). Reproduction therefore mostly occurs following such rains, during June-September (major breeding season), or January-March (minor breeding season).

16 GENERAL INTRODUCTION

FIGURE 1.1 An adult Seychelles warbler (A) and a bird’s eye view of our main study site – Cousin Island – with our research station in the foreground and the neighbouring island of Cousine in the background (B). Photo (A) by Sjouke A. Kingma and (B) by

Martin Harvey, courtesy of Nature Seychelles.

17 CHAPTER 1

Detailed measurements of the abundance of prey have been collected since the start of the study on Cousin Island, and earlier studies have indicated that between-territory variation plays an important role in group formation, with offspring being more likely to delay dispersal on high quality than on low quality territories (Komdeur 1992). However, there is substantial between-year variation in arthropod abundance, which could have consequences for delayed dispersal and other aspects of cooperative breeding, which were until recently unknown (see chapter 3).

Seychelles warblers on Cousin suffer virtually no adult predation, but predation of eggs by the endemic Seychelles fody Foudia sechellarum is an important cause of nest failure (Kom- deur & Kats 1999). However, several aspects of the Seychelles warbler breeding biology reduce the risk of nest predation. First, (dominant) males perform nest guarding behaviour (i.e. remaining vigilant close to the nest during female off-bouts). Such behaviour reduces the likelihood of egg predation because eggs are only taken from unprotected nests. Nest guarding is probably costly for males since male investment into nest guarding behaviour increases with territory quality (see chapter 6; Komdeur & Kats 1999). Second, incubation by subordinate females reduces the time that the nest is unprotected, and should therefore also reduce the risk of nest predation by fodies. Third, Seychelles warblers will attack and chase off any fodies that come to close to their nest. However, several aspects of Seychelles warbler behaviour with regards to nest predation and the benefits of cooperative breeding remain elusive. For instance, the extent to which subordinate dispersal, dominant tolerance of subordinates and co-breeding by subordinate females is associated with the risk of nest predation was hitherto unknown. Additionally, we knew very little about the tradeoffs that determine anti-predator behaviours for Seychelles warbler parents. These have now been addressed in box 1 and chapter 6, respectively.

On the southern shores of Lake Tanganyika Neolamprologus pulcher is a highly social cooperatively breeding cichlid fish (Fig. 1.2A), endemic to Lake Tanganyika (Fig. 1.2B), where it inhabits the sublittoral zone between 2-40 meters depth (Konings 1998). It lives in groups that consist of a dominant pair and up to 25 subordinates of either sex (Taborsky & Limberger 1981; Groenewoud et al. 2016). Territories are centred on some kind of substrate, usually one or several small rocks, but fish have also been seen to use shells or crevices, which they use for both shelter and breeding (Josi et al. in prep.). Subordinates engage in various types of helping behaviours, including territory maintenance (i.e. removing sand and debris to create shelters), egg cleaning and fanning, defense against con- and heterospecifics space competitors and predators (Taborsky 1984).

18 GENERAL INTRODUCTION

FIGURE 1.2 A group of Neolamprologus pulcher in their territory (A) and the sunset over Lake Tanganyika as seen from the field station at Kasakalawe bay (B). Photo (A) by Dario Josi and (B) by Arne Jungwirth.

19 CHAPTER 1

Subordinates are of different sizes and show age-related task specialization: smaller, sexually immature subordinates usually engage in maintenance and defence against non-dan- gerous predators and space competitors, and large sexually mature subordinates defend against larger predators (Bruintjes & Taborsky 2011; chapter 5). Territories are aggregated into colonies, which are made up of several dozen, to several hundreds of territories (Heg et al. 2008).

The evolution of cooperative breeding in N. pulcher – and other cooperative breeding fish – is likely distinct from the evolution of cooperative breeding in most other vertebrate systems, in that it is not based on habitat saturation or increased levels of within-group relatedness. N. pulcher does not suffer from habitat saturation in the strict sense, since breeding substrate appears to be plentiful. However, most of this free habitat occurs outside of the boundaries of the colony, and individuals seem unwilling to disperse to such habitat. When similar habitat was experimentally made available inside the colony, fish usually dispersed there within a few days (Heg et al. 2008). One of the main obstacles to dispersal, and the main drivers of delayed dispersal, is the risk of predation by large predatory cichlids such as Lepidiolamprologus elongatus and L. attenuatus. These fish are highly mobile predators, swimming through N. pulcher colonies in small groups (often together with Mastacembelid eels). Individuals that do not belong to a group and are devoid of protection, are easy prey, and several studies have shown that increased predation risk leads to delayed dispersal by larger, sexually mature subordinates (Heg et al. 2004a; see chapter 2). As a result of frequent dominant turn-over, subordinate-dominant relatedness decreases with increasing subordinate size (Dierkes et al. 2005). Larger, sexually mature helpers are therefore mostly not related to the dominants in whose territory they reside and to whom they provide help. As group membership is a prerequisite for survival and large subordinates impose costs on dominant breeders, large helpers have to compensate for these costs by providing help (i.e. “pay-to-stay”; Gaston 1978; Fischer et al. 2014).

The role of predation risk in the evolution of cooperative breeding, and other forms of social complexity, have generally been understudied. The cooperative breeding system of N. pulcher offers a unique opportunity to study such effects because fish can be easily observed in the wild and there is high natural variation in predation risk (see chapter 2). The broader implications of predation risk on the structural complexity of social groups and the extent to which individuals show behavioural adjustments to increase the benefits of cooperative breeding under high predation risk were previously unexplored – but have now been addressed in chapter 2 and 5, respectively.

20 GENERAL INTRODUCTION

Environmental heterogeneity and the evolution of cooperative breeding Developing a hypothesis based on well-supported assumptions is the beginning of any investigation. I hope I have been able to provide a strong argument for the hypothesis that the ecology of cooperative breeders is an important factor determining the costs and benefits of (delayed) dispersal, helping behaviour and behavioural strategies that maximize the benefits of cooperation. In the coming chapters, I will further explore these questions. In the second chapter, I will explore the consequences of predation risk for dispersal and the social organization of N. pulcher, and discuss the general implications of our results for other cooperative breeding systems. In the third chapter, I will show that spatio temporal variation in food availability has important consequences for group formation in the Seychelles warbler, but that the benefits that are obtained through cooperative breeding are not affected by such variation. In the fourth chapter, I will presents the results of an investigation into alternative dispersal strategies in the Seychelles warbler, and show that subordinate females can disperse into unrelated group to obtain reproductive benefits. In thefifth chapter, I will return to N. pulcher to show how groups reduce within-groups conflict to maximize the benefits of cooperative breeding under high predation risk, with wider implications for evolutionary transitions to higher social complexity. In my sixth chapter, I will present results of a field experimental study showing the social and environmental factors that mediate tradeoffs in anti-predator defenses in the Seychelles warbler. Box A contains an investigation into the extent to which the risk of nest predation drives the benefits of communal breeding for females in the Seychelles warbler. In the final chapter, I will present a synthesis the results of this thesis and their implications, and offer some perspectives for future studies investigating the ecological and environmental drivers of cooperative breeding.

Chapter 2

Predation risk drives social complexity in cooperative breeders

Frank Groenewoud*, Joachim Gerhard Frommen*, Dario Josi, Hirokazu Tanaka, Arne Jungwirth and Michael Taborsky.

Published in Proceedings of the National Academy of Sciences of the United States of America, 113, 4104–4109

* Equally contributing authors CHAPTER 2

ABSTRACT

Predation risk is a major ecological factor selecting for group living. It is largely ignored, however, as an evolutionary driver of social complexity and cooperative breeding, which is attributed mainly to a combination of habitat saturation and enhanced relatedness levels. Social cichlids neither suffer from habitat saturation, nor are their groups composed primarily of relatives. This demands alternative ecological explanations for the evolution of advanced social organization. To address this question, we compared the ecology of eight populations of Neolamprologus pulcher, a cichlid fish arguably representing the pinnacle of social evolution in poikilothermic vertebrates. Results show that variation in social organization and behavior of these fish is primarily explained by predation risk and related ecological factors. Remarkably, ecology affects group structure more strongly than group size, with predation inversely affecting small and large group members. High predation and shelter limitation leads to groups containing few small but many large members, which is an effect enhanced at low population densities. Apparently, enhanced safety from predators by cooperative defense and shelter construction are the primary benefits of sociality. This finding suggests that predation risk can be fundamental for the transition toward complex social organization, which is generally undervalued.

24 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

INTRODUCTION

Predation risk is a key ecological factor selecting for adaptive responses in morphology, behavior, and life history decisions in animals (Barbosa & Castellanos 2005; Caro 2005). In particular, it constitutes a fundamental selective force for group living (Alexander 1974; Krause & Ruxton 2002). Group members benefit from predator dilution or confusion (Wro- na & Dixon 1991; Krause & Ruxton 2002) and from joint effort in antipredator behavior, such as mobbing and vigilance (Caro 2005). However, living in groups also entails costs; thus, group living should only evolve when, on average, the benefits of group living exceed its costs (Alexander 1974).

Long-term, stable groups mainly form in the context of reproduction. The most highly structured and complex groups occur when offspring are raised cooperatively, which often involves division of labor between group members (Wilson 1971; Clutton-Brock, Russell & Sharpe 2004). In such cooperative groups, sexually mature individuals typically refrain from reproduction to raise the offspring of others (Taborsky & Limberger 1981; Cockburn 1998; Jennions & Macdonald 2007), which may involve lifetime reproductive sacrifice (eusociality). The evolution of cooperative breeding is generally understood as a two-step process, where delayed dispersal is accompanied by the decision to provide alloparental brood care to dependent young (Koenig & Dickinson 2016). Limited dispersal resulting from habitat saturation may facilitate the evolution of cooperation by kin selection through the creation of kin neighborhoods (Frank 1998). Empirical evidence is provided by correlations between relatedness and helping effort (Emlen & Wrege 1989; Komdeur 1994b; Wright et al. 2010), and by interspecific correlations between monogamous mating and the incidence of cooperative breeding and eusociality (Hughes et al. 2008; Briga, Pen & Wright 2012). However, this paradigm has limited explanatory power where habitats are not saturated and where cooperation occurs between unrelated individuals, demanding alternative explanations to account for the evolution of complex social organization (Clutton-Brock 2009). Despite its central role in group formation, predation risk has rarely been recognized as an evolutionary force in the transition from simple to complex social organization, where subordinate nonbreeders provide alloparental care. This represents an important gap in our understanding of the evolution of complex social organization. It should be noted that the term “social complexity” has different connotations, especially when used in connection with different taxa, but there seems to be consensus that social complexity is not merely synon- ymous with group size. Instead, this term typically refers to social systems incorporating different types (or roles) of individuals within groups, accounting also for the nature and diversity of interactions among these individuals (Blumstein & Armitage 1997, 1998; Free- berg, Dunbar & Ord 2012). Here, we demonstrate that variation in predation risk between

25 CHAPTER 2

populations can explain social organization and complexity in cooperatively breeding fish. Predation risk may affect delayed dispersal, and hence group formation, in two possible ways. First, it increases the costs of dispersal by causing mortality when individuals disperse from their natal area to unfamiliar territory (Yoder 2004). This effect can be exac- erbated when individuals need to sample their environment for suitable dispersal options (Clobert et al. 2009; Bocedi, Heinonen & Travis 2012), as is the case in cooperative breeders keeping their territories all year round (Bergmüller et al. 2005a). Second, predation may render independent breeding unprofitable or impossible if the joint effort of group members is required for successful reproduction (Balshine et al. 2001; Caro 2005; Kingma et al. 2014). Hence, predation risk is an important ecological constraint selecting for reduced or delayed dispersal, fulfilling two of three conditions (see conditions ii and iii below) proposed by the ecological constraints hypothesis (Emlen 1982). This hypothesis predicts delayed dispersal when there is: (i) a shortage of vacant breeding territories or mates, (ii) high mortality risk during dispersal, and (iii) a low chance of independent reproduction when a breeding territory has been established. These effects may be additive and can cause strong selection for delayed dispersal under high levels of predation.

The cooperatively breeding cichlid fish Neolamprologus pulcher is a highly suited model system to unveil the role of predation risk as ecological constraint, as this species suffers from high predation (Balshine et al. 2001), but usually not from a shortage of breeding sites (Heg et al. 2008). N. pulcher breeds colonially in sandy to rocky patches along the sublittoral zone (2- to 45-m depth) of Lake Tanganyika. Individual groups consist of a dominant breeding pair and up to 30 subordinates (Taborsky 1984; Balshine et al. 2001; Bergmüller et al. 2005a). Groups are frequently attacked by predatory fish (Balshine et al. 2001), which significantly affects the survival probability of group members, especially small subordinates and fish devoid of protection through large conspecifics (Heg et al. 2004a). Hence, membership in a group is a precondition for survival. Within groups, subordinates have to pay by helping in brood care, territory maintenance (i.e., removing sand and debris from underneath rocks), and defense to compensate for the costs they impose on dominant breeders (Taborsky 1985; Balshine-Earn et al. 1998; Bergmüller, Heg & Taborsky 2005b; Fischer et al. 2014), to which they are often unrelated (Dierkes et al. 2005). The lack of relatedness between larger subordinates and dominants reduces the opportunity for selective benefits of assisting kin, which differs sharply from the situation proposed for many other cooperative breeders (c.f. Cockburn 1998; Solomon & French 2007; Hatchwell 2009). This finding suggests that other mechanisms are in place to explain helping behavior by larger subordinates (Bergmüller et al. 2005b; Taborsky 2016). We investigated the effects of predation on the social organization of N. pulcher, using natural variation in predation risk and ecological factors shaping mortality, group composition, and behavioral decisions among eight distinct populations in

26 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

Lake Tanganyika. Specifically, we focused our attention on shelter availability and sand cover as ecological factors. Shelter availability has been shown to affect group size in this species (Balshine et al. 2001), but not all group members may be equally dependent on access to shelters for their survival. In addition, territory maintenance has been shown to be one of the most costly activities in terms of time and energy expenditure (Grantner & Taborsky 1998; Taborsky & Grantner 1998), and the extent to which helpers engage in these behaviors is likely dependent on the presence of sand in their territories.

MATERIALS AND METHODS

Sampling sites, predation risk, and ecological factors We collected data on eight different populations of N. pulcher between September and De- cember 2012 and 2013 by SCUBA-diving at the southern end of Lake Tanganyika. Populations were on average 1,796 m apart (range = 150–22,450 m), with seven populations all being within 9 km of each other and one population located about 20 km away from the rest.

We estimated predation risk in each population along four transects of 10 × 1 m2 by counting the number of fish predators (Lepidiolamprologus elongatus, Lepidiolamprologus attenuatus, and Lamprologus lemairii). We repeated these scans between 6 and 10 times per population on different days to capture the variation in fish activity. For each population we estimated predation risk on adult N. pulcher by calculating the mean number of large (>10 cm) L. elongatus and L. attenuatus per transect (Heg et al. 2004a). L. elongatus and L. attenuatus are the most common predators of N. pulcher in our study area (Balshine et al. 2001; Heg et al. 2004a, 2008) and they were also the two most abundant species in the surveyed populations. These are highly mobile predators, usually observed in small groups moving through our populations at 20-30 cm above ground looking for prey, which in the case of N. pulcher consists mainly of smaller fish or fish devoid of protection by a group (Taborsky 1984; Heg et al. 2004a).

We measured the number of shelters and the percentage of sand cover per square meter (hereafter “sand cover”) for each population by surveying four transects of 10 × 1 m2 of bottom substrate, starting from the center of a colony and moving outwards in four directions at 90° angles. We also determined how many of these shelters were used by N. pulcher or other species, whether the respective square meter contained an N. pulcher territory and if so, the proportion of area covered by N. pulcher territories. To check for within- population correlations between group and habitat characteristics, we recorded the group compositions according to different size classes for all territories located within these transects, described in detail below.

27 CHAPTER 2

Group compositions, group sizes, and densities For between-population comparisons, we used data from 20 territories sampled at random from each population. We searched for N. pulcher territories in each of the eight populations until we were confident that all territories had been detected. The boundaries of N. pulcher colonies were established where no other territories were found within 5 m of the outermost territories of the colony, except for two very large populations where, because of practical considerations, artificial boundaries were established despite other territories being close by. All territories were individually marked with small numbered stones (~5 cm in diameter). In each population we determined the group composition for each randomly selected territory. We estimated the standard length (SL; from tip of the snout to the posterior end of the last vertebrae) of individuals, and assigned them to different size classes: fry (<0.5 cm), nonhelpers (0.5-1.5 cm), small helpers (1.6-2.5 cm), medium helpers (2.6-3.5 cm), large helpers (>3.5 cm) following Heg et al. (2004a). Our analyses focus mainly on the differences between small and large helpers, because these represent nonoverlapping size classes and previous studies have shown clear differences in behavior and mortality risk as a result of predation (Heg et al. 2004a; Bruintjes & Taborsky 2011). For example, small helpers typically do not disperse, whereas large helpers do disperse if conditions allow (Stiver et al. 2004; Jungwirth, Walker & Taborsky 2015b). In addition, predation risk differs markedly between small and large helpers also with regard to group size effects (Heg et al. 2004a). Medium-sized helpers, in contrast, form a transitional state that is intermediate in both life history decisions and behavior, and their predation risk is also intermediary (Heg et al. 2004a). Therefore, there are no clear hypotheses regarding the variation of their numbers according to ecological factors. However, we provide information about these relationships in Fig. S2.1. We also recorded the presence or absence of dominant breeding females and males. Dominants can easily be distinguished from subordinates based on size and behavior. Because not all subordinates in a group were always visible (e.g., as a result of time spent hiding or feeding in the water column) we estimated group composition repeatedly for each territory (median = 3 times, range = 1–4). For one population, only a single measure of group composition per territory could be obtained. From these group compositions we also calculated total group size (i.e., the total number of helpers). For each focal territory, we measured the distance to the nearest neighboring territory from the center of each territory to the nearest 5 cm and counted the total number of territories present within a 2-m radius, as a measure of territory density.

Behavioral observations In each focal group we recorded the behavior of both dominant breeders and of one haphaz- ardly selected individual from each subordinate size class. All behaviors were recorded continuously for 7 minutes using a handheld computer (Psion Teklogix Workabout Pro-7525)

28 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

in a waterproof plastic bag, running Noldus Pocket Observer (v3.0). Recorded behaviors included aggression against predators, group members, and other conspecifics, which was either overt (chasing, ramming, biting, mouth fighting, or other forms of elevated aggression) or restrained (spreading of fins or opercula, head down display, s-bend swimming, or fast approach); submissive behaviors toward dominants and other group members (tail quiver, hook swimming, and bumping); and maintenance behaviors (removal of sand and debris from the territory; Taborsky & Limberger 1981; Taborsky 1984). We also observed the spacing behavior of focal individuals continuously during the observation and recorded whether they were inside their home territory (±30-cm semispherical dome around breeding shelter; Taborsky & Limberger 1981), visiting another territory, outside of any territory, or in a shelter. In total, we collected 77 h of behavioral data of 660 individual fish in 154 different territories.

Statistical analyses We analyzed between-population effects on the total number of subordinates and the number of large and small subordinates by fitting these as separate response variables in a generalized linear mixed model (GLMM) assuming a Poisson error distribution. To see how the number of small helpers related to territory density and the number of large helpers in the territory, we fitted a Poisson GLMM. Territory defense was analyzed as a binary trait in a GLMM where we included individual class, the number of small and large helpers in the territory, nearest neighbor distance, and predation risk as predictor variables. To assess whether shelter maintenance was affected by sand cover and predation risk, and whether this relationship varied between different individuals, we fitted a Poisson GLMM with interactions between both sand cover and predation risk, and individual class and predation risk. We analyzed the time spent hiding in shelters by fitting a linear mixed model with predation risk, nearest neighbor distance, individual class, and the interaction between predation risk and individual class as predictors. For all models, we fitted varying intercepts for Territory ID, and where necessary Population ID, to account for the nonindependence of repeated measurements within these groups. We used an information theoretic model selection approach to find the most parsimonious model. Variables were removed from the model if dropping that variable resulted in a model with a minimum difference of two Akaike Information Criterion (AIC)c values (Burnham & Anderson 2002). We calculated conditional R2 based on Nakagawa and Schielzeth (Nakagawa & Schiel- zeth 2013) as an estimator of the explained variance. Parameter significance was inferred based on likelihood ratio tests of deviances assuming a χ2-distribution. All models were inspected for violations of model assumptions, such as overdispersion, deviations from normality, and het- eroscedasticity. All data were analyzed in R v3.1.2 (R Development Core Team 2008) using the packages “lme4” (Bates et al. 2014), “nlme” (Pinheiro et al. 2012), and “AICcmodavg” (Mazerolle 2013) for parameter inference and model selection.

29 CHAPTER 2

RESULTS

Between-population comparisons Habitat characteristics varied substantially between different populations (Fig. 2.1). The total number of helpers was not associated with predation risk (mean ± SE = 0.026 ± 0.020, P = 0.19). However, predation risk showed an inverse relationship with small and large helpers: the number of large helpers increased with higher levels of predation (mean ± SE = 0.093 ± 0.021, P < 0.001), whereas the number of small helpers decreased (mean ± SE = −0.07 ± 0.031, P = 0.019; Fig. 2.1A and B). The total number of helpers increased with rising numbers of shelters (mean ± SE = 0.052 ± 0.016, P = 0.001), which was mostly because of the relationship between shelter availability and the number of small helpers. The number of small helpers increased significantly with a rising number of shelters (mean ± SE = 0.063 ± 0.024, P = 0.008), and this relationship was more than twice as strong as for large helpers, where it was not significant (mean ± SE = 0.025 ± 0.017, P = 0.132; Fig. 2.1C and D). Sand cover was positively correlated to total helper number (mean ± SE = 0.011 ± 0.004, P = 0.003), again mainly because of the relationship between sand cover and the number of small helpers (mean ± SE = 0.015 ± 0.005, P = 0.004), while there was no significant correlation with the number of large helpers (mean ± SE = 0.004 ± 0.004, P = 0.293; Fig. 2.1E and F). Results of the relationship between these ecological variables and the number of medium-sized helpers are presented in Fig. S2.1 and Table S2.1.

10 A C E

4 B D F

Number of helpers 2

0 0 1 2 3 4 5 6 7 8 10 12 14 16 18 0 10 20 30 40 50 Predators transect -1 Number of shelters m-2 Sand cover m-2 (%)

FIGURE 2.1 The relationship between predation risk (A and B), the number of shelters (C and D), and sand cover (E and F) with total number of helpers (Top) and group composition (Bottom) in different populations of N. pulcher. Population means and bootstrapped 95% confidence intervals are given for total helper number (filled circles in A, C, and E), small helpers (filled circles in B, D, and F), and large helpers (open squares in B, D, and F). Data points are slightly offset horizontally to avoid overlapping confidence intervals. Solid regression lines represent the model predicted values with bootstrapped predicted 95% confidence -in tervals for total helper numbers (teal), small helpers (blue), and large helpers (green).

30 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

Within-population comparisons We used a subset of the data — all territories located within the habitat transects — to test whether these effects were also present within populations. We found a correlation between the number of shelters and the number of small helpers similar to that of the between-population comparison (mean ± SE = 0.040 ± 0.021, P = 0.049; Fig. 2.2A). However, within populations we found no significant correlation between sand cover and small helper numbers (mean ± SE = 0.006 ± 0.005, P = 0.255). The number of large helpers was not correlated with the number of shelters or sand cover, but similar to the between-population data, both relationships were significantly greater for small helpers than for large helpers (number of shelters: number of small helpers vs. number of large helpers: mean ± SE = −0.070 ± 0.023, P = 0.002; sand cover: number of small helpers vs. number of large helpers: mean ± SE = −0.022 ± 0.005, P < 0.001).

Territories had fewer small helpers at lower densities (i.e., when neighbors were further away; mean ± SE = −0.007 ± 0.002, P < 0.001), and this effect was stronger under high predation risk (nearest neighbor distance x predation risk: mean ± SE = −0.014 ± 0.005, P = 0.003; Fig. 2.3). There was no significant correlation between the number of large and small helpers within groups (mean ± SE = 0.052 ± 0.032 P = 0.11), and the number of large helpers did not depend on the distance to the nearest neighbor (mean ± SE = −0.001 ± 0.001, P = 0.413).

10 A B < 0.001 8 150

6 100 4 50 2 Time in shelter (s) Number of helpers 0 0 0 5 10 15 20 25 BrM BrF LH SH Number of shelters

FIGURE 2.2 (A) Correlation between the number of small (shaded circles, solid line) and large (open triangles, dashed line)

N. pulcher helpers with the availability of shelters. Data points are slightly offset to provide information on data density, and regression lines are drawn of mean predicted values based on mixed models accounting for between-population variance and the nonindependence of observations within territories. (B) Time spent in shelter for different individual classes of N. pulcher during

7-min observation periods. BrF, breeding female; BrM, breeding male; LH, large helper; SH, small helper. Error bars indicate 95% confidence intervals.

31 CHAPTER 2

Behaviors At higher densities, individuals showed fewer aggressive behaviors against predators (mean ± SE = 0.014 ± 0.005, P = 0.008; Fig. 2.4A), suggesting group members benefit from having nearby neighbors. In contrast, groups with more small helpers showed increased per capita predator defense rates (mean ± SE = 0.116 ± 0.051, P = 0.026), whereas there was no effect of the number of large group members on per capita defense (mean ± SE = 0.174 ± 0.127, P = 0.171), even though large helpers attack predators frequently (Fig. 2.4B). Shelter maintenance behavior increased in populations with higher average sand cover (mean ± SE = 0.071 ± 0.020, P < 0.001), and this effect was similar for all individuals (sand cover x individual class: df = 3, χ2 = 3.479, P = 0.323). Individuals lowered their shelter maintenance behavior with increasing predation risk, and small helpers decreased shelter maintenance more strongly than large helpers (slope small helpers vs. large helpers: mean ± SE = 0.301± 0.114, P = 0.008). Predation risk was positively correlated with the time spent in shelters (mean ± SE = 3.384 ± 1.689, P = 0.046), and this effect did not diverge between individuals of different sizes (predation risk x individual class: df = 4, χ2 = 6.040, P = 0.196). However, small helpers in general spent significantly more time hiding in shelters than did other group members (mean ± SE = 116.791 ± 8.839, P < 0.001; Fig. 2.2B and Table S2.2) and also showed the greatest effort in the maintenance of these shelters (Table S2.3).

20 Predation risk high low 15

0 Number of small helpers 0 50 100 150 200 Nearest neighbor distance (cm)

FIGURE 2.3 Relationship between the number of small helpers in N. pulcher groups and the distance to the nearest neighboring group. The original data points are slightly offset to provide information on data density. Conditional regression lines are plotted for high (>median) and low (

32 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

0.25 A 1.0 A B < 0.01 0.8 0.20 0.07 0.6 0.15

0.4 0.10 ense probability ense probability 0.2 0.05 De f De f

0.0 0.00 0 50 100 150 200 BrM BrF LH SH Nearest neighbor distance (cm)

FIGURE 2.4 Per capita probability of predator defense of N. pulcher in relation to nearest neighbor distance (A), and class of group members (B). BrF, breeding female; BrM, breeding male; LH, large helper; SH, small helper. The solid and dashed lines in

A indicate the predicted values and bootstrapped 95% confidence intervals, respectively. In B, means and SEs are shown. Model parameter estimates for the significance values are given in Table S4.

DISCUSSION

Habitat saturation and kin selection have been proposed as the primary explanations for the evolution and maintenance of the social complexity characteristic of cooperative breeders. Our results highlight that predation risk plays an important role in shaping the social organization and behavior of a cooperatively breeding fish, where habitat saturation and kin-selected benefits are arguably of negligible importance. Furthermore, the influence of predation risk apparently interacts with other important ecological factors. Consistent with our predictions, the social organization relates to the substantial variation between populations in predation risk and habitat characteristics. Predation risk poses a threat especially for small group members, which seem to benefit from enhanced access to shelters and from having close neighbors (Figs. 2.2A, 2.3, and 2.4A). Given that the number of small helpers within groups does not correlate with the number of large helpers, this finding suggests that small helpers may benefit more from enhanced security by the presence of close neighbors than from protection by large helpers in their own group (Jungwirth & Taborsky 2015). This pattern is consistent with our behavioral data: per capita predator defense increases with nearest neighbor distance, but not with the number of large group members (Fig. 2.4A and Table S2.4). This finding suggests that either predator dilution or benefits of shared defense are the primary contributors to the increased numbers of small helpers. A recent study on N. pulcher indeed revealed that individuals show reduced antipredator defense in response to the presence of close neighbors (Jungwirth et al. 2015a). Addition- ally, experimental data showed that a greater number of large group members increases

33 CHAPTER 2

survival in the group, except for small helpers (Heg et al. 2004a). Another positive effect of close neighbors might be improved predator detection, enabling small helpers to take refuge from incoming predators in time. Increased predator vigilance is a major benefit of living in dense aggregations and colonies, especially when predators cannot be fended off by mobbing (Krause & Ruxton 2002; Caro 2005). The importance of access to shelters for small helpers is illustrated further by the substantial time and energy expenditure that small helpers invest in creating and maintaining these shelters (Table S2.3), and by the positive relationship between shelter availability and the number of small helpers (Fig. 2.2A). Shelter maintenance has been shown to be the most energetically costly behavior in N. pulcher, raising standard metabolic rate sixfold (Grantner & Taborsky 1998), which strongly affects the helpers’ behavioral energy budget (Taborsky & Grantner 1998). In addition, a field experiment revealed that group size depends on the number of shelters in the territory (Balshine et al. 2001).

Delayed dispersal is regarded as an important first step in the evolution of cooperative breeding, and advanced sociality (Hochberg, Rankin & Taborsky 2008; but see Cockburn 2013; Riehl 2013 for alternative pathways to group formation), and our results suggest that predation can be an important ecological factor selecting for this trait. Predation risk can affect individuals both during and after dispersal, as it also influences the reproductive potential of individuals that have obtained dominance in a new group. Subordinate N. pulcher have been shown to delay dispersal when the risk of predation is increased (Heg et al. 2004a), and group members prefer to disperse to territories in the center of a colony (Heg et al. 2008), apparently to reduce the risk of predation by improved antipredator defense and vigilance. This may both increase survival of small helpers (Fig. 2.3) and decrease workload of group members in general, because of the combined antipredator defense of neighbors (Jungwirth et al. 2015a). One of the most pervasive results of this study is the obvious importance of access to shelters, especially for the survival probability of small individuals. The ability of groups to monopolize and provide access to shelters for small group members seems to be a crucial determinant of their survival and hence, of the reproductive success of breeders.

Our data show that per capita defense rates increase with the number of small helpers in the territory. Three alternative hypotheses can explain this observation. (i) Group members may be more aggressive toward potential predators when there are more juveniles present that are in need of protection. Active defense of helpers in need of protection by dominant group members has been shown experimentally in this system (Taborsky 1984). (ii) Preda- tors may preferentially target territories with a large number of small helpers, and hence they need to be repelled more often. The main predators of this species occur at higher

34 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

densities inside of N. pulcher colonies than in adjacent areas (Heg et al. 2008), and it is con- ceivable that within colonies these predators focus on small group members because they are easier prey. Size-dependent choice of prey by piscivore predators has been observed in other species, and optimal foraging theory explains this as resulting from selection on the highest yield per time spent foraging (Holmes & McCormick 2010). In addition, selection of small prey may involve a lower injury risk to predators. (iii) A large number of small helpers present in a group may increase conspicuousness to predators. The relationship between group size, conspicuousness, and predation risk has been well documented in numerous species (e.g. Botham et al. 2005). In accordance with this hypothesis, small subordinates in our study show reduced maintenance behaviors when faced with high predation risk (Table S2.3), which likely reduces conspicuousness. Similarly, in Perisoreus jays (Perisoreus spp.), subordinates seem to show helping behavior primarily under low risk of nest predation, which might reflect the necessity to conceal the nest location if predators of young are abundant (Jing et al. 2009). We should point out that these three hypotheses are not mutually exclusive. They may in fact jointly explain the observed correlation between the number of small group members and individual defense effort.

In addition to these apparent direct effects of predators on group structure and behavior, between populations the number of small helpers per group increased significantly with sand cover. Two mutually nonexclusive explanations could account for this pattern. First, shelter maintenance by digging is the most energetically costly behavior in this species (Ta- borsky & Grantner 1998), which is likely to be partly responsible for the stunted growth of helpers (Taborsky 1984; Taborsky & Grantner 1998). This might result in group compositions being skewed toward small individuals, because investment in maintenance declines with increasing body size (Table S2.3). Second, sand allows for ecological niche construction by digging out shelters, and thereby manipulating the environment (Kylafis & Loreau 2008). Although rocky habitat may provide shelters that are more easily accessible, requiring a smaller initial investment and potentially lower maintenance costs, their number and size cannot be modified. Hence, group composition in N. pulcher may partly depend on the environmental potential for niche construction, which might be an important evolutionary driver of social organization both in N. pulcher and in general.

The effects of predation risk on the transition to complex social organization have been underexplored. Our study demonstrates significant effects and interactions between predation risk and other ecological factors affecting survival, social structure, and behavior of a cooperatively breeding vertebrate in the wild. An important strength of this study is that most of our studied populations were in close vicinity to each other, therefore geographical distance and correlated patterns of gene flow cannot explain the results. In fact, the two

35 CHAPTER 2

populations that shared the smallest between-population distance showed the highest ecological differentiation in almost every aspect. The significance of the results of this study ex- tends far beyond the evolutionary ecology of cooperative breeding. Predation risk has been invoked as a prime ecological driver in the evolution of group living of primates and early hominids, mostly by relating predation risk to group size (Dunbar & Hill 1998; van Schaik & Hörstermann 2014). However, our study shows that predation may affect group composition and behavior more strongly than group size, especially when interactions between predation risk and other ecological factors are considered. Hence, this study highlights the importance of predation risk as a major factor, selecting not only for the formation of groups but for complex social organization.

Acknowledgements We thank the Department of Fisheries, Ministry of Agriculture and Livestock of Zambia, for the permission to conduct this work; Harris Phiri, Danny Sininza, and the team of the Department of Fisheries at Mpulungu for logistical help; Jan Komdeur and two anonymous referees for comments on the manuscript; and Celestine Mwewa and the staff at the Tang- anyika Science Lodge for their hospitality. This work was supported by Swiss National Sci- ence Foundation Projects 310030B_138660 and 31003A_156152 (to M.T.) and 31003A_144191 (to J.G.F.).

36 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

SUPPLEMENTARY INFORMATION

We analyzed between-population effects on the total number of subordinates and the number of large and small subordinates by fitting these as separate response variables in a GLMM assuming a Poisson error distribution. In each model, we fitted: (i) the average number of predators per transect, (ii) the average number of shelters per square meter containing a Neolamprologus pulcher territory, and (iii) the average sand cover per square meter containing an N. pulcher territory as predictor variables. We included Territory ID as a random factor in each model to account for the repeated measures of group compositions for each territory. Furthermore, we fitted the number of small helpers as a response variable in a Poisson GLMM, and added territory density, the number of small helpers, and the number of large helpers as explanatory variables. Nearest neighbor distance and the number of large group members were included as predictor variables, and Population ID and Territory ID were included as nested random effects to account for population identity and the repeated measures of territories, respectively.

Territory defense behavior was converted to a binary variable (1/0) to indicate whether individuals had or had not performed aggressive behaviors toward predators during their respective 7-min observation period. We fitted this binary response variable in a logistic GLMM with a logit-link function and included individual class (i.e., dominant male or female or subordinate size class), the number of large and small helpers in the territory, nearest neighbor distance, and predation risk as predictor variables. The interaction between nearest neighbor distance and predation risk was also included. For these purposes, we transformed predation risk into a two-level factor indicating high (>overall population median) or low (

37 CHAPTER 2

A B C 4

0 Number of medium helpers 0 1 2 3 4 5 6 7 8 10 12 14 16 18 0 10 20 30 40 50 Predators transect m-2 Number of shelters m-2 Sand cover m-2 (%)

FIGURE S2.1 The relationship between predation risk (A), the number of shelters (B), and sand cover (C) with the number of medium-sized helpers in different populations of N. pulcher. Triangles show population means with bootstrapped 95% confidence intervals.

Solid lines and shading represent the model predicted values with bootstrapped predicted 95% confidence intervals. Model estimates are provided in Table S2.1.

TABLE S2.1 Model summary showing parameter estimates for predator defence of N. pulcher. Model selection was based on an information theoretic approach (< 2 AICc values), and model terms retained in the final model are indicated in bold. Parameter significance was determined using a likelihood ratio test (LRT), and interaction terms were removed for the estimation of main effects in the model.

Predation risk was reduced to a 2-level factor with high (> median) and low (< median) predation risk. Reference categories are breeding female and high predation risk. Conditional R2 is reported based on Nakagawa and Schielzeth (2013). See subchapter statistical analysis in the Methods section for details.

Parameter estimate ± s.e. df χ2 / Z p Intercept -3.793 ± 0.704 Individual class 3 12.342 0.015 breeding male -0.016 ± 0.381 -0.041 0.967 large helper -0.499 ± 0.411 -1.214 0.225 small helper -1.502 ± 0.559 -2.685 0.007 Nearest neighbour distance 0.014 ± 0.005 1 7.043 0.008 Predation risk 0.457 ± 0.459 1 0.989 0.320 Number of small helpers 0.116 ± 0.051 1 4.983 0.026 Number of large helpers 0.174 ± 0.127 1 1.873 0.171 Nearest neighbour distance * Predation risk 0.000 ± 0.014 1 0 1.000 σ2TerritoryID 1.076 σ2PopulationID 0.000 Conditional R2 0.354

38 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

TABLE S2.2 Model summary showing parameter estimates for shelter maintenance of N. pulcher. Model selection was based on an information theoretic approach (< 2 AICc values), and model terms retained in the final model are indicated in bold. Parameter significance was determined using a likelihood ratio test (LRT), and interaction terms were removed for the estimation of main effects in the model. The reference category for individual class is small helper. Conditional R2 is reported based on Nakagawa and Schielzeth (2013).

See subchapter statistical analysis in the Methods section for details.

Parameter estimate ± s.e. df χ2 / Z p Intercept -2.619 ± 0.907 Individual class 3 9.842 0.020 breeding female -1.054 ± 0.319 -3.304 0.001 large helper -0.965 ± 0.307 -3.139 0.002 medium helper -0.715 ± 0.342 -2.091 0.037 Sand cover 0.071 ± 0.020 1 13.917 < .001 Predation risk -0.319 ± 0.139 1 1.064 0.302 Nearest neighbour distance -0.009 ± 0.006 1 1.999 0.157 Individual class * predation risk 3 9.001 0.029

breeding female 0.234 ± 0.121 1.932 0.053 large helper 0.301 ± 0.114 2.640 0.008 medium helper 0.248 ± 0.132 1.879 0.060 Individual class * sand cover 3 3.479 0.323 σ2TerritoryID 1.756 Conditional R2 0.633

TABLE S2.3 Model summary showing parameter estimates for the time spent in shelters of N. pulcher. Model selection was based on an information theoretic approach (< 2 AICc values), and model terms retained in the final model are indicated in bold. Parameter significance was determined using a likelihood ratio test (LRT), and interaction terms were removed for the estimation of main effects in the model. The reference category for individual class is breeding male. Conditional R2 is reported based on Nakagawa and Schielzeth

(2013). See subchapter statistical analysis in the Methods section for details.

Parameter estimate ± s.e. df χ2 / Z p Intercept 8.788 ± 12.242 Predation risk 3.384 ± 1.689 1 3.991 0.046 Individual class 4 182.007 < .001 Breeding female 6.431 ± 8.212 0.788 0.431 Large helper 11.635 ± 8.291 1.438 0.151 Small helper 116.791 ± 8.838 8.860 < .001 Nearest neighbour distance 0.151 ± 0.120 1 0.120 0.206 Predation risk * Individuals class 3 6.040 0.196 σ2TerritoryID 31.388

Conditional R2 0.407

39 CHAPTER 2

TABLE S4 Model summary showing parameter estimates for the relationship between population level ecological variables and the number of medium sized subordinates. Model selection was based on an information theoretic approach (< 2 AICc values), and model terms retained in the final model are indicated in bold. Parameter significance was determined using a likelihood ratio test (LRT).

Conditional R2 is reported based on Nakagawa and Schielzeth (2013). Parameter estimate ± s.e df X2 / Z p Intercept -0.832 ± 0.315 1 Predation risk 0.031 ± 0.027 1 1.260 0.262 Number of shelters 0.062 ± 0.021 1 8.355 <.001 Sand cover 0.014 ± 0.005 8.577 <.001 σ2TerritoryID 0.212 Conditional R2 0.377

40 PREDATION RISK DRIVES SOCIAL COMPLEXITY IN COOPERATIVE BREEDERS

Chapter 3

Spatio-temporal resource variation, group formation and the benefits of cooperative breeding in the Seychelles warbler

Frank Groenewoud, Sjouke A. Kingma, Martijn Hammers, Terry Burke, David S. Richardson & Jan Komdeur CHAPTER 3

ABSTRACT

Recent comparative studies suggest that environmental variability predicts the evolution of group living and cooperative breeding. Mechanisms that may explain this pattern include (1) group formation driven by spatio-temporal variation in food availability and (2) selection for cooperative breeding because it improves fecundity under adverse conditions, but these hypotheses are seldom tested in concert. Using fine-scale, long-term data on the facultative cooperatively breeding Seychelles warbler Acrocephalus sechellensis, we find evidence that spatio-temporal variation in food availability facilitates group formation, and that groups with multiple females had higher fecundity and lower fecundity variance than other groups. However, contrary to prediction, this reduction in fecundity variance was not due to subordinate females buffering the effects of adverse food availability on reproduction. Thus, spatio-temporal variation in food availability favours group formation (setting the stage for cooperative breeding), but does not favour helping behaviour per se in this species.

44 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

INTRODUCTION

Ecology has been invoked as an important driver of cooperative breeding (e.g. Stacey & Koe- nig 1990; Hatchwell & Komdeur 2000; Pen & Weissing 2000; Koenig & Dickinson 2016) – a breeding system in which individuals forgo independent reproduction to help rear non-de- scendant young within a group (Cockburn 1998; Hatchwell 1999). Recent comparative studies have shown that cooperative breeding in both birds (Rubenstein & Lovette 2007; Jetz & Rubenstein 2011) and mammals (Lukas & Clutton-Brock 2017) is positively associated with variability in environmental conditions. However, the mechanism underlying this pattern is unclear, since variability in environmental conditions can affect multiple components of cooperative breeding, such as the costs and benefits of delayed dispersal, the fecundity benefits of breeding cooperatively, or both (Griesser et al. 2017; Shen et al. 2017).

The evolution of cooperative breeding is generally considered a two-step process, whereby the formation of groups precedes the possibility of helping (Emlen 1991; Hatchwell 1999; Ligon & Burt 2004; Jennions & Macdonald 2007; Griesser et al. 2017). Constraints on dispersal and/or independent breeding may lead to higher fitness for individuals that join a group as a subordinate (Selander 1964; Brown 1974; Emlen 1982). Such constraints could arise through temporally fluctuating environmental conditions leading to increased costs of independent breeding and/or improved benefits of group living, under adverse conditions (i.e. “hard life hypothesis”; Emlen 1982; Koenig et al. 2011). Additionally, sexually mature offspring should forego dispersal if the benefits in their resident territory (e.g. food, protection) exceed the benefits of dispersal (“benefits of philopatry hypothesis”; Stacey & Ligon 1991), which may be particularly important when there is considerable and consistent spatial variation in environmental conditions. Therefore, both temporal and spatial environmental variation can play an important role in determining the costs and benefits of joining a group as a subordinate instead of dispersing and attempting to breed independently.

Temporal and spatial environmental variation may also promote cooperative breeding when it affects how subordinates improve group fecundity. The “bet-hedging hypothesis” – which has received a lot of attention recently – proposes that the benefits of cooperative breeding can arise through subordinates reducing fecundity variance, instead of increasing mean fecundity (e.g. Rubenstein 2011; Kennedy et al. 2018). Theoretical investigations have demonstrated that reducing fecundity variance can contribute as much to fitness as improving mean fecundity, especially under the conditions that are often experienced by cooperative breeders, i.e. small population size and high kin structure (Gillespie 1977; Tul- japurkar 1990; Lehmann & Balloux 2007; Sæther & Engen 2015). Consequently, the preva-

45 CHAPTER 3

lence of cooperatively breeding in regions with high climatic uncertainty has often been explained in the context of bet-hedging (Rubenstein & Lovette 2007; Jetz & Rubenstein 2011; Lukas & Clutton-Brock 2017). One commonly suggested way by which subordinates can reduce fecundity variance is by improving reproductive success under adverse conditions (i.e. “temporal variability hypothesis”; Rubenstein & Lovette 2007; Shen et al. 2017), but this has only seldom been tested (Magrath 2001; Koenig et al. 2011) Additionally, previous studies investigating cooperative breeding as a bet-hedging strategy (e.g. Rubenstein 2011; Koenig & Walters 2015) did not consider the impact of environmental conditions on delayed dispersal and group formation, which is an important prerequisite for cooperative breeding in many species (Griesser et al. 2017). Understanding how environmental variation affects group formation and fecundity benefits in cooperative breeders could prove vital in explaining why cooperative breeding has evolved in some species, but not in others.

Here we investigate how spatio-temporal variation in food availability affects delayed dispersal and the fecundity benefits of cooperative breeding, using 17 years of data from a population of facultatively cooperative Seychelles warblers Acrocephalus sechellensis (SW). Our study population is confined to the small island of Cousin. We therefore have the extensive, detailed long-term information on food availability, individual dispersal and fecundity that are necessary to investigate how spatio-temporal variation in food availability affects group formation and the fecundity benefits of cooperative breeding. In SWs, territories contain a dominant breeding pair and a variable number (1-5) of subordinates of either sex, which are mostly offspring from previous breeding attempts (Kingma et al. 2016a). Subordinates often help with the provisioning of young and improve the reproductive success of the dominant pair (Richardson, Burke & Komdeur 2002; Brouwer, Richardson & Komdeur 2012). Female subordinates generally help more than subordinate males (female subordinates provision about 80% more than subordinate males; Komdeur 1991, 1994a; Richardson et al. 2003b), including in incubation (males do not incubate) and unlike males, often co-breed with the dominant female in the territory by laying an egg in the same nest (Richardson et al. 2001; Hadfield, Richardson & Burke 2006). Therefore, female subordinates can prevent nest failure at multiple breeding stages, and are probably in a better position to improve fecundity, and reduce fecundity variance, than male subordinates.

Our study has four aims. First, we quantify how food availability varies across space and time. Second, we test how this spatio-temporal variation in food availability affects delayed dispersal and the formation of social groups. Third, we test how mean fecundity and fecundity variance change with food availability and the presence of male and female subordinates in a group. Fourth, we investigate whether the impact of male or female subordinates

46 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

on fecundity depends on food availability. These results will provide a better understanding of how cooperative breeding can be associated with fluctuating environments and provide valuable insights into the role of environmental variation in the evolution of group living and cooperative breeding.

METHODS

Study species and population monitoring The data were collected on the Cousin Island population (04º20’S, 55º40’E; ca 29 ha) of SW from 1996 to 2016. SWs live on territories that are defended year-round and stable between years (territory number: mean = 112, range = 103-123; this study). Breeding vacancies are limited and offspring of both sexes often delay dispersal after reaching sexual maturity (Kom- deur 1992; Eikenaar et al. 2007; Kingma et al. 2016a). As a result, on average 41% of territories contain subordinate group members (> 5 months old; mean number of subordinates per territory ± SE = 0.59 ± 0.02, range = 1-5, n = 2,578 “group years”; this study). Migration to or from the island is virtually absent (Komdeur et al. 2004a) and resighting probabilities between years are very high: 0.98 for birds over two years of age and 0.92 for younger individuals (Brouwer et al. 2010).

Although SWs can breed year-round, there are major (June-September) and minor (Janu- ary-March) breeding seasons, following semi-annual monsoon rains (Komdeur 1996b). For the current study, we used 17 years of data from the main breeding seasons in 1996-1999, 2003-2004, and 2006-2016. The years 2000-2002 and 2005 were excluded, because data on insect abundance (see below) were not available for these years. During fieldwork periods, birds were observed on their territories at least weekly for nesting activity and, once found, nests were visited and observed every 3-4 days to determine the onset of incubation, hatching success and fledging success. SWs on Cousin Island typically raise only a single offspring on their territory (91% of clutches contain a single egg; Komdeur 1996b; Richardson et al. 2001), and offspring can receive food from their parents and other group members for up to five months after fledging (Komdeur 1991). Unringed individuals were caught either at the nest or using mist-nets within the natal territory, and 60% of unringed individuals were caught before 5 months of age. Individuals were ringed using a unique combination of colour rings and a metal ring (British Trust for Ornithology). Over 96% of adult birds (subordinates and dominants) have been ringed in every year since 1997 (Hadfield et al. 2006; Ham- mers et al. 2015). All ringed individuals were blood sampled through brachial venipuncture for molecular sexing (Richardson et al. 2001).

47 CHAPTER 3

Food availability SWs feed on arthropods (mainly insects), taken from the underside of leaves (Komdeur 1991). Food availability can therefore be determined by estimating the density of arthropod prey using the methods described by Komdeur (1992) and Brouwer et al. (2009). In short, arthropod density was determined monthly during each main breeding season at 13 locations on the island by counting the number of arthropods on the underside of 50 leaves of each main tree species (5 leaves per tree, 10 trees per species). Vegetation cover was determined once during the main breeding season at 20 locations within each territory, by estimating the presence (>50% cover), or absence (<50% cover) of vegetation at different strata (0-0.75 m, 0.75-2 m and at 2-m intervals thereafter). In each main breeding season, arthropod density was calculated per territory as ∑ x=1(cx ix) where cx is the relative cover for species x and ix is the mean arthropod abundance per unit leaf area for species x. The resulting measure of food availability (i.e. the mean number of arthropods per unit leaf area) was log-transformed before analyses.

Statistical analyses Spatio-temporal variation in arthropod density To estimate the spatio-temporal distribution of arthropods over the island, we fitted arthropod density as a response variable in generalized additive mixed models (GAMMs) in the package “mgcv” version 1.8-16 (Wood 2011), assuming a Gaussian error distribution. Specif- ically, we fitted two nested models representing the following hypotheses about how arthropods are distributed in space and time: (i) arthropod density changes over time, but spatial variation is consistent, or (ii) both arthropod density and the spatial distribution of arthropod densities vary over time. We used a tensor product smooth with two-dimensional isotropic thin-plate regression splines to describe spatial variation, and cubic regression splines to describe temporal variation, in arthropod density (Wood 2006). All models were fitted using maximum-likelihood approximation and checked for model assumptions such as normality of residuals, homogeneity of residual variance and adequate number of knots (k; i.e. the “wiggliness” of smoothing terms) for basis construction (Wood 2006). Fitted models were compared using AIC, and AIC weights were calculated to identify the model that makes the best out-of-sample predictions. Additionally, we estimated the repeatability of arthropod density for territories by fitting a linear mixed-effects model in the package “brms” version 1.5.1 (Bürkner 2017), which is a front end for STAN (Carpenter et al. 2017). We used variance estimates to calculate the proportion of variance explained by between-territory differences, relative to within-territory differences (i.e. repeatability or intra-class correlation) according to Nakagawa and Schielzeth (2010). This model also contained varying intercepts for field periods to account for differences in arthropod density between years. To visualise the variability in arthropod density in different territories, and investigate the

48 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

possibility that variability differed across the island, we fitted the coefficient of variation (CV = standard deviation/mean) as a standardized measure of variation in arthropod density for each territory in an additive mixed model with a two-dimensional thin-plate regression spline, as explained above. CV arthropod density estimates were weighted according to how many observations (i.e. years) contributed to a particular data point (not all territories were present in all years as some disappeared and some new territories were founded; median = 13 years, range = 2–17 years).

Based on the spatio-temporal patterns that we detected using the approach described above, we partitioned arthropod density into temporal and spatial components by fitting arthropod density as a response variable in a random regression model with the package “brms” (Bürkner 2017), with year and territory as nested random effects. Estimates of these varying intercepts for years and territories were then used to obtain values for (i) between-year arthropod density (henceforth “annual food availability”), and (ii) within-year deviance in arthropod density (henceforth “territory food availability”). These estimates were used in all subsequent analyses.

Food availability and group formation We fitted a generalized linear mixed model (GLMM) with a binomial error structure to estimate the likelihood that offspring of different sex born in a given main breeding season had dispersed from the natal territory before the end of the next main breeding season (i.e. when they were approximately one year of age), using the package “brms” (Bürkner 2017). Individuals were only included if they were caught and ringed before three months of age (i.e. as a nestling or dependent fledgling) and were alive one year later (N = 193 of 339 individuals). We hypothesize that offspring are more likely to disperse (to attempt to breed independently) when annual food availability is higher, and external constraints on dispersal and independent reproduction are therefore lower. However, if benefits obtained in the natal territory are the main factor driving delayed dispersal then we predict that subordinates are more likely to disperse from territories with low food availability compared to territories with high food availability. We included sex in the model to account for potential differences in dispersal between male and female offspring and we fitted five models representing different hypotheses about the relationship between sex, annual island food availability and territory food availability (Table S3.1). We then obtained model averaged predictions based on WAIC (“Widely Applicable Information Criterion”; Watanabe 2010) by resampling predicted values of each model according to its Akaike weight. Territory ID and year ID were included as random effects in all models. To test the possibility that patterns of delayed dispersal were due to differential survival (individuals that died within a year were not included in the previous analysis), we also analysed whether an individual’s survival to

49 CHAPTER 3

the next breeding season was associated with annual island food availability, territory food availability or sex, in a generalized linear mixed model with a binomial error structure. Ter- ritory ID and year ID were included as random effects. We fitted five models, similar to the analysis of delayed dispersal (Table S3.2), and assessed models based on WAIC values.

As an additional line of evidence establishing the link between group stability and food availability, we investigated whether the proportion of cooperative breeding groups depended on food availability. Breeding groups were classified based on their group composition as having no subordinates (N = 924), having at least one female subordinate (N = 342), having at least one male subordinate (N = 186), or having at least one male and one female subordinate (N = 143). We fitted the group composition as a response variable in a multinomial logistic regression analysis, and included mean annual island food availability and the annual deviance from this mean value as predictors. We included Territory ID and year ID as random effects. These and all other models were run with 3 chains leading to 15,000 posteri- or samples (7,000 iterations with 2,000 warm-up iterations per chain). We used weakly regularizing normal priors for intercepts (μ = 0, σ2 = 5) and beta-coefficients (μ = 0,σ 2 = 2) and half-Cauchy priors for variance components (χ = 0, γ = 1; Gelman 2006). Model convergence and assumptions were checked by visual inspection of chains, Gelman–Rubin diagnostics and posterior predictive checks (McElreath 2015). All parameter estimates are reported as posterior means with 95% credible intervals (2.5–97.5%).

Mean fecundity and fecundity variance To explore whether cooperative breeding may act as a bet-hedging strategy in the SW, we tested how (per capita) mean fecundity and fecundity variance changed with sociality and with food availability. We fitted the number of fledglings produced (i.e. the number of offspring that fledged the nest) per breeding season for each breeding group as a response variable in a GLMM with a Poisson error distribution and log link function in the package “brms” (Bürkner 2017). Group composition, annual food availability and territory food availability were included as predictors. We fitted five models representing different hypothesis about the relationship between group composition, food availability and the number of fledglings produced (Table S3.3). For models assessing per capita reproductive success, we changed the Poisson exposure by including log group size as an offset in the different models. Year ID and territory ID were included as random effects.

We assessed whether fecundity variance changed with group composition and with annual food availability by parsing data according to year and group composition, and calculating the coefficient of variation for the per capita number of fledglings produced (CV young fledged = s.d. per capita young fledged / mean per capita young fledged). This was fitted as a

50 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

response in a generalized linear mixed model with a lognormal error distribution and year ID as a random effect. To assess the within-year change in fecundity variance, we included group composition and annual food availability as predictors, and fitted two separate models, one with, and one without, an interaction between the predictor variables. We calculated Akaike weights, based on model WAICs, and made averaged predictions by resampling posterior predictions from each model according to its Akaike weight (McElreath 2015).

Food availability and the benefits of cooperative breeding during different breeding stages We investigated whether annual and territory food availability, group composition, or the interaction between these predicted nest success during different breeding stages, namely (i) clutch initiation (i.e. whether an egg was laid), (ii) the probability of hatching (i.e. the proportion of nests that reached the hatching stage after an egg was laid), and (iii) the probability of fledging (i.e. the proportion of nest that reached the fledgling stage after hatching). We fitted group composition, mean annual food availability and relative territory food availability as predictors, and included year ID and territory ID as random effects. For each response variable, we fitted five models to represent different hypotheses about the interaction between group composition, annual food availability, and territory food availability (see Table S3.4). We calculated Akaike weights based on WAIC and made averaged predictions by resampling predicted values of each model according to its weight. All analyses were performed in R version 3.3.0 (R Core Team 2016).

RESULTS

Spatio-temporal variation in arthropod abundance Food availability (i.e. arthropod density) was highly variable between years and between territories (Figs. 3.1A-C). The spatial distribution of arthropods over the island varied between years, as indicated by the significant tensor product interaction (F187.83 = 2.77, p < 0.001) and the large difference in AIC between the model with and without the interaction

(ΔAIC = 641.5; AICweight for interaction model = 1). The average repeatability of arthropod density in territories across years was low (R = 0.13), but different from zero (95% CI = 0.09, 0.18). The variability in arthropod density was not consistent across the island, as indicated by a significant spatial component when modelling the coefficient of variation for each territory (F16.92 = 2.78, p < 0.001; Fig. 3.1C). Between-year differences explained almost four times 2 as much variation as differences among territories within years σ( year: mean = 0.34, 95% CI = 2 0.21, 0.53; σ territory: mean = 0.09, 95% CI = 0.05, 0.12).

51 CHAPTER 3

response response 300 300 1.9 0.24 0.3 1.7 A B C 0.34 0.26 0.28 1.6 1.8 200 0.38 0.22 3 1.8 1.5

100 1.9 0.36 1.6 100 2 1.9 0.32 1.7 2 0 1.8 0 0.28 1.8 0.38

1.3 thing.C 1.7 0.36 0.3 1.1 1.5 0.44 1.6 0.32 0.46 0.34 1.3 No r 0.42 2 1 0.36 1.4 0.44 1.2 1.3 −200 1.4

1.5 −200 0.4 1.2 1.6 (mean ± 95% CI) 200m 200m Log arthropod density N N 1 −400 −400 1995 2000 2005 2010 2015 Mean spatial variation −400Between-year−200 0 variability100 300

Year Easting.C

FIGURE 3. 1 (A) Shows the mean arthropod density (± 95% CI) on Cousin Island during the main Seychelles warbler breeding seasons over time (1996-2016, but no data were available for the years 2000-2003 and 2005). In (B) the mean spatial distribution of arthropod density over Cousin Island over 17 years is shown (yellow colours indicate high values, green colours are intermediate and blue colours are low for mean arthropod abundance). In (C) the between-year variability (i.e. coefficient of variation) of arthropod density over the same time period is shown (purple, white and blue indicate high, intermediate and low between-year variability in arthropod numbers, respectively).

Food availability and group formation Delayed dispersal WAIC-values indicated no meaningful interactions between predictors and the evidence ratio of the highest ranked (additive) model was more than two times higher than the second best ranked model (WAICweight = 0.43 vs 0.19; Table S3.1). Offspring were more likely to disperse when mean annual island food availability was higher (βannual food availability = 1.25, 95% CI = 0.21, 2.29; Fig. 3.2A). Dispersal by offspring was less likely in territories with higher food availability, but posterior estimates overlapped with zero (βterritory food availability = -0.48, 95% CI =

-1.18, 0.19; Fig. 3.2B). The likelihood of dispersal did not differ between the sexes β( sex = -0.09, 95% CI = -0.70, 0.53). Territory food availability was also positively associated with survival, and this effect was stronger in years with high island food availability β( annual food availability * territory food availability = 0.95, 95% CI = 0.02, 1.92). We found no relationship between survival and annual food availability overall (βannual food availability = -0.04, 95% CI = -0.91, 0.89), and there were no differences in survival between the sexes (βsex= -0.04, 95% CI = -0.91, 0.89).

Changes in group composition The total proportion of cooperatively breeding groups (all groups with subordinates) vs non-cooperatively breeding groups (all groups without subordinates), decreased with increasing annual island food availability (βcooperative vs non-cooperative = -1.14, 95% CI = -2.15, -0.12; Fig.

3.2C) and this decrease was strongest for groups with female subordinates only (βfemale vs no subordinates = -0.54, 95% CI = 0.96, 0.11) and weaker for groups with male subordinates and both

52 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

male and female subordinates (βmale vs no subordinates = -0.43, 95% CI = -1.07, 0.21; male and female subordinates: βfemale + male vs no subordinates = -0.16, 95% CI = -0.73, 0.42). The total proportion of cooperatively breeding groups did not change with territory food availability (βcooperative vs non-cooperative = 0.47, 95% CI = -0.16, 1.14; Fig. 3.2D). There was no change in the proportion of groups with females (female vs no subordinates = -0.05, 95% CI = -0.31, 0.20), but the proportion of groups with male subordinates and both male and female subordinates tended to increase with increasing territory food availability (male subordinates: βmale vs no subordinates = 0.23, 95% CI = -0.10, 0.56; male and female subordinates: βfemale + male vs no subordinates = 0.29, 95% CI = -0.06, 0.66).

Mean fecundity and fecundity variance Mean fecundity Mean fecundity was higher in groups with female subordinates and with both female and male subordinates (βfemale vs no subordinates = 0.44, 95% CI = 0.27, 0.60; βfemale + male vs no subordinates = 0.43,

95% CI = 0.20, 0.66; Figs. 3.3A, B), but not in groups with only male subordinates (βmale vs no subordinates = 0.11, 95% CI = -0.13, 0.35).

1.0 A B 0.8

13 0.6 12 13 54 6 14 9 0.4 17 5

(mean ± CI) 0.2 35 15

Probability of dispersal 0.0 −0.5 0.0 0.5 −1.0 -0.5 0.0 0.5 1.0 Annual food availability Territory food availability 1.0 none C D female 0.8 male both 0.6

tion of groups 0.4

0.2 Propo r 0.0 −0.5 0.0 0.5 −2 −1 0 1 Annual food availability Territory food availability

FIGURE 3.2 The upper two panels show the mean probability (± 95% CI) that Seychelles warbler offspring had dispersed at one year of age in relation to (A) mean annual island food availability and (B) relative territory food availability (i.e. territory deviance from the annual mean) at one year of age. Only individuals that were caught as a fledgling (< 3 months of age) and were still alive at one year of age were used (N = 193). Circles in (A) indicate the proportion of individuals dispersing and numbers in circles indicate sample sizes for that year. In the lower two panels, the model predicted mean proportion of groups of different compositions in relation to (C) mean annual island food availability and (D) territory food availability are shown.

53 CHAPTER 3

There was no effect of annual food availability or territory food availability on mean fecundity (βannual food availability = 0.11, 95% CI = -0.49, 0.68; βterritory food availability = 0.04, 95% CI = -0.10, 0.17; Figs. 3.3.A, B), and WAIC values indicated no meaningful interactions between food availability and group composition. There was some support for a model with an interaction between annual food availability and territory food availability (WAICweight = 0.41; Table S3.3).

Estimates for this interaction, however, overlapped with zero (βannual food availability x territory food availability = 0.15, 95% CI = -0.15, 0.45).

Per capita fecundity Compared to pairs, the mean per capita fecundity was lower in groups with only male subordinates (βmale vs no subordinates = -0.31, 95% CI = -0.55, -0.07) and in groups with both male and female subordinates (βfemale + male vs no subordinates = -0.28, 95% CI = -0.52, -0.05), but not in groups with only female subordinates (βfemale vs no subordinates = -0.01, 95% CI = -0.19, 0.15; Figs. 3.3C, D). There was no relationship between annual food availability, or territory food availability and per capita mean fecundity (βannual food availability = 0.12, 95% CI = -0.45, 0.67; βterritory food availability = 0.03, 95% CI = -0.10, 0.17; Figs. 3.3C, D). WAIC values indicated no interactions between food availability and group composition, but showed some support for a model including the interaction between annual food availability and territory food availability (WAICweight = 0.36;

Table S3.3). However, estimates for this interaction overlapped with zero (βannual food availability x territory food availability = 0.15, 95% CI = -0.16, 0.45).

Fecundity variance As predicted by the bet-hedging hypothesis, compared to pairs, fecundity variance was lower for groups with female subordinates (βfemale vs no subordinates = -0.33, 95% CI = -0.49), -0.16; Fig.

3.4, and for groups with female and male subordinates (βfemale + male vs no subordinates = -0.31, 95% CI

= -0.47, -0.15; Fig. 3.4) but not groups with only male subordinates (βmale vs no subordinates = -0.07, 95% CI = -0.24, 0.09; Fig. 3.4). Fecundity variance did not depend on annual food availability

(βannual food availability = -0.01, 95% CI = -0.40, 0.39).

Food availability and the benefits of cooperative breeding during different breeding stages Clutch initiation

Model weights indicated (WAICweight = 0.79; Table S3.4) that group composition affected nest initiation depending on annual food availability. Female subordinates had a larger effect on the likelihood that groups initiated a clutch when annual food availability was high, then when it was low compared to groups without subordinates (βfemale vs no subordinates x annual food availability = 1.47, 95% CI = 0.27, 2.79), but such effects were not present for group with males β( male vs no subordinates x annual food availability = 1.00, 95% CI = -0.58, 2,71) and were, possibly, reversed in groups with both male and female subordinates (βboth vs no subordinates x annual food availability = -1.24, 95% CI =

54 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

-2.78, 0.23; Fig. 3.5A). Territory food availability was not related to the likelihood that a group initiated a clutch (βterritory food availability = -0.02, 95% CI = -0.35, 0.32).

Subordinates present none female male both A B 0.6

0.4

0.2

Mean young fledged 0.0 0.3 C D

0.2

Per capita 0.1 mean young fledged 0.0 −0.5 0.0 0.5 −2 −1 0 1 Annual food availability Territory food availability

FIGURE 3.3 The mean total number of fledglings produced (A, B) and mean per capita number of fledglings produced(C, D) in relation to annual island food availability and territory food availability by groups with different group compositions, consisting of either no subordinates (N = 924, black line), at least one female subordinate (N = 342, red line), at least one male subordinate

(N = 186, blue line), or at least one female and one male subordinate (N = 143, green line). Lines indicate model averaged predicted mean effects based on WAIC values.

2.0

1.5 oung fledged 1.0 β = -0.07

CV y β = -0.33* β = -0.31*

0.5 none female male both Subordinates present

FIGURE 3.4 Within-year fecundity variance (CV young fledged) for groups with either no subordinates (N = 924), at least one female subordinate (N = 342), at least one male subordinate (N = 186), and both male and female subordinates (N = 143). Beta coefficients refer to the difference with groups without subordinates and estimates that do not overlap with zero are followed by an asterisk.

55 CHAPTER 3

There was some evidence that groups were more likely to initiate a clutch overall in years with higher food availability (βannual food availability = 0.85, 95% CI = -0.07, 1.78; Fig. 3.5A). Only in groups with female subordinates did the likelihood of clutch initiation increase with annual food availability βfemale = 2.18, 95% CI = 0.79, 3.67).

Subordinates present none female male both 1.0 A B

0.8

0.6 Mean probability of clutch initiation

1.0 C D

0.8 of hatching 0.6 Mean probability

1.0 E F

0.8 of fledging 0.6 Mean probability

−0.5 0.0 0.5 −2 −1 0 1 Annual food availability Territory food availability

FIGURE 3.5 The relationship between group composition, and annual and territory food availability on nest success during different breeding stages: the probability of clutch initiation (A, B), the probability of hatching given an egg was laid (C, D), the probability of fledging given a nest contained a nestling (E, F). Lines indicate model-averaged predicted mean effects based on

WAIC values. Sample sizes for each analysis are N = 1595 for clutch initiation, N = 1446 for hatching success and N = 1009 for fledging success.

56 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

Hatching success There was no association between the likelihood that a clutch would hatch and annual or territory food availability (βannual food availability = 0.02, 95% CI = -0.66, 0.68; βterritory food availability = 0.08, 95% CI = -0.11, 0.28; Figs. 3.5C, D). However, hatching success was higher when groups had a female subordinate (βfemale vs no subordinates = 0.39, 95% CI = 0.14, 0.64), but not when groups had either male subordinates, or both male and female subordinates (βmale vs no subordinates =

0.13, 95% CI = -0.17, 0.44; βmale and female subordinates vs no subordinate = 0.30, 95% CI = -0.04, 0.66; Figs. 3.5C, D). WAIC values indicated limited support for interactions between food availability and group composition (Table S3.4).

Fledging success The likelihood that nestlings would fledge was not associated with annual food availability or territory food availability overall (βannual food availability = -0.04, 95% CI = -0.83, 0.74; βterritory food availability = 0.01, 95% CI = -0.25, 0.27). However, WAIC values indicated support for the model containing an interaction between group composition and annual food availability (WAIC- weight = 0.38; Table S3.4). Fledging success improved with increasing annual food availability in groups with female subordinates, compared to groups without subordinates (βfemale vs no subordinates x annual food availability = 0.86, 95% CI = 0.06, 1.68), but not for groups with only male subordinates, or groups with both male and female subordinates (βmale vs no subordinates = 0.46, 95% CI

= -0.57, 1.49; βboth vs none = 0.68, 95% CI = -0.37, 1.74; Fig. 3.5E, F). However, fledging success did not improve overall with increasing annual food availability in groups with female subordinates (βannual food availability = -0.50, 95% CI = -0.49, 1.50), nor in groups with other group compositions.

DISCUSSION

Our study suggests that temporal and spatial variation in food availability play a key role as drivers of delayed dispersal and group formation in Seychelles warblers. Consistent with the bet-hedging hypothesis for cooperative breeding, we found that the presence of subordinate females, but not males, in a group, reduces fecundity variance. While spatio-temporal variation in food availability had no effect on the number of fledglings that were produced in a territory, female subordinates improved total reproductive success of their group, resulting in similar per capita fecundity as groups without subordinates. Converse- ly, male subordinates had no effect on fecundity, and consequently, per capita fecundity was lower in groups with male subordinates compared to group without subordinates.

57 CHAPTER 3

Food availability and group formation We show that, in the Seychelles warbler, high annual food availability increases the likelihood that offspring disperse. This is arguably due to the decreased costs of dispersal and/ or independent breeding (Emlen 1982; Kingma et al. 2016a, b). The idea of increased costs of breeding in poorer conditions is supported by our finding that overall clutch initiation tends to decline with lower annual food availability (Fig. 3.4A). These results highlight the importance of environmental variability in the formation of groups, which is often a prerequisite for the evolution of cooperative breeding (Griesser et al. 2017). Furthermore, increased dispersal during years with high food availability leads to fewer cooperative groups (Fig. 3.2C), and smaller groups in years with high food availability (Fig. S3.1B). This means that the interpretation of associations between reduced fecundity variance and average group size sensu Rubenstein (2011) and Koenig and Walters (2015), depends on the relationship between group size and annual food conditions. If there is a negative relationship between group size and environmental conditions (as in this study), large groups will tend to form under poorer conditions, which can mask, or even reverse, any mean effect of either group size, or conditions, on fecundity variance. However, if the opposite is true, and large groups tend to be associated with good conditions, than any average effect of group size on fecundity variance could be the result of improved food conditions. Temporal fluctuations in the costs of independent breeding have also been shown to lead to group formation in other cooperatively breeding species (Canario, Matos & Soler 2004; Covas, Doutrelant & du Plessis 2004; Koenig et al. 2011), which suggests that such effects are common. Future research to investigate the effect on of cooperative breeding on fecundity variance should thus be aware of such correlations, because of the potential covariance between environmental conditions and group size.

Evidence that subordinates were more likely to delay dispersal in high-quality territories than in low quality territories – which would be expected based on previous findings in the Seychelles warbler (Komdeur 1992) – was weak (Fig. 3.2B). This result could have been par- tially confounded by differential mortality risk, with subordinates from territories with low food availability being more likely to have disappeared before the next season. The fact that spatial variance in territory quality seems to play a lesser role in this study could also be due to territory quality differences becoming less pronounced as a result of vegetation recov- ery across the island since 1992 (Komdeur & Pels 2005; Eikenaar et al. 2010). Interestingly, a decrease in consistent spatial variation, in combination with increasing temporal fluctuations, could mean that the cooperative breeding system of the Seychelles warbler is shifting from being mainly benefits driven, to being mainly constraints driven. However, another analyses revealed that consistent spatial variation in food availability was positively correlated with group size, confirming that territories with high mean food availability had

58 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

larger groups on average (Fig. S3.1A). This result corroborates the earlier results of Komdeur (1992) and supports the benefits-of-philopatry hypothesis as a driver of delayed dispersal in this species. Both constraints (i.e. the costs of dispersal and/or independent breeding) and the benefits that can be obtained in the natal territory (e.g. access to food) thus play a role in dispersal and, therefore, in group formation in the Seychelles warbler.

Mean fecundity and fecundity variance If per capita fecundity increased with group size, then cooperative breeding would be more parsimoniously explained by such increases in per capita fecundity than by reducing fecundity variance (Starrfelt & Kokko 2012; Shen et al. 2017). In the Seychelles warbler, the per capita fledgling output is lower in groups that contain any male subordinates, but not groups with female subordinates, compared to groups without any subordinates (Figs 3.3C, D). Overall, group fecundity increases in groups with only female subordinates and in groups with both male and female subordinates (Figs 3.3A, B). This difference in fecundity between groups with male and female subordinates is probably because female subordinates help more, and more often than males, and also co-breed (Richardson et al. 2001; Richardson, Burke & Komdeur 2003a).

The bet-hedging hypothesis for cooperative breeding predicts that fecundity variance should decrease with increasing sociality. Here we show that while male subordinates had no effect on fecundity variance, there was a significant decrease in fecundity variance when female subordinates were present in SW groups (Fig. 3.4). Sociality has been linked to reductions in fecundity variance in superb starlings Lamprotornis superbus (Rubenstein 2011), and acorn woodpeckers Melanerpes formicivorus (Koenig & Walters 2015), but only the latter study investigated how within-year fecundity variance is reduced by groups of different composition. One notable difference is that, in the acorn woodpecker, subordinate (co-breeding) males show the highest decrease in fecundity variance, while our study shows the highest decrease for groups with female subordinates. This difference is likely due to differences in group composition and helping behaviour, since the subordinate sex ratio and helping are male biased in the acorn woodpecker (Koenig, Walters & Haydock 2016) and female biased in the Seychelles warbler (Komdeur 1996a; Richardson et al. 2002). Koenig and Walters (2015) were able to obtain fitness estimates based on the assumption that there was a linear relationship between reproductive success and the acorn crop (Frank & Slatkin 1990) and, based on these estimates, argued that the reductions in fecundity variance were probably insufficient to compensate for the overall decrease in per capita reproductive success. Due to the more complicated set of conditions encompassing reproductive success in the Seychelles warbler (e.g. density-dependence, Brouwer et al. 2009) and fecundity being expressed at the group level, we cannot deduce the effect on fitness in our current dataset.

59 CHAPTER 3

However, we point out that, for groups containing female subordinates in the Seychelles warbler, per capita fecundity does not decline in groups with female subordinates, and that the decrease in fecundity variance is stronger compared to the acorn woodpecker. This would argue in favour of bet- hedging being potentially more important as a benefit of cooperative breeding in the Seychelles warbler than in the acorn woodpecker.

Food availability and the benefits of cooperative breeding during different breeding stages A commonly proposed way in which subordinates can reduce fecundity variance is by improving fecundity during adverse food conditions (i.e. “temporal variability hypothesis”; Rubenstein & Lovette 2007), presumably by preventing nestling starvation (Rubenstein 2011). However, subordinates could also reduce nest failure during other breeding stages. In the Seychelles warbler, subordinate females most consistently prevented nest failure both during hatching and fledging (Figs. 3.5C, E). In addition, only in groups with female subordinates was there a positive relationship between the likelihood of clutch initiation and annual food availability (Fig. 3.5A). Female subordinates did not improve fecundity more during adverse food conditions, in contrast with the temporal variability hypothesis, and a commonly assumed mechanism of bet- hedging. Subordinate male SWs did not appear to reduce nest failure, although subordinate males did improve the likelihood of clutch initiation.

Interestingly, groups with subordinate females had a lower probability of hatch failure. Egg predation – an important cause of nest failure in the Seychelles warbler – is significantly reduced by female subordinate incubation (Komdeur & Kats 1999; Kingma et al. forthcom- ing). Whether subordinates could reduce fecundity variance by reducing nest predation, remains unexplored. This is an interesting possibility because nest predation potentially has a stronger effect on reproductive variance than nestling starvation through reduced food availability, because it often leads to the loss of whole broods, while starvation only leads to brood reduction (Ricklefs 1969a). Alternatively, female subordinates could buffer against other forms of stochasticity on a smaller scale than we have measured here. For example, short periods of heavy rain during the breeding season often make it difficult for Seychelles warblers to provide their offspring with enough food. Such small-scale stochastic effects are difficult to incorporate in this study, but the presence of one or more subordinates could mean the difference between breeding successfully or not.

Conclusion In conclusion, our study shows that in the Seychelles warbler, spatio-temporal variation in food availability is associated with delayed dispersal, a key step to cooperative breed-

60 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

ing. The presence of female subordinates reduces reproductive variance, and per capita fecundity does not decline in groups with female subordinates, which suggests that reduced fecundity variance does not have to compensate for a large loss in per capita fecundity to provide fitness benefits. However, the reduction in reproductive variance by subordinate females is not due to subordinates improving reproductive success under adverse conditions, as is commonly suggested by studies invoking bet hedging. In the SW, subordinate females reduce nest failure by improving the likelihood of clutch initiation, hatch success and fledging success. The extent to which reproductive variance contributes to fitness in the Seychelles warbler now requires further investigation.

So far, few studies have investigated reduced fecundity variance as a consequence of cooperative breeding (Reed & Walters 1996; Rubenstein 2011; Koenig & Walters 2015), however, data on mean reproductive success and reproductive variance are readily available for many cooperative, and non-cooperative, breeding species. It would be worthwhile to test whether species living in the same habitats and differing only in social system show differences in fecundity variance as a result of environmental fluctuations (Jetz & Rubenstein 2011; Corn- wallis et al. 2017). In addition to changing mean temperatures, climate change also affects the strength and frequency of weather extremes, thereby increasing environmental fluctuations (Garcia et al. 2014). If cooperative breeding is indeed a bet-hedging strategy that has evolved because it allows individuals to better cope with environmental perturbations, we would expect cooperatively breeding species to be less affected by changing climatic patterns than non-cooperatively breeding species. Investigating these patterns on a larger scale thus provides another important way to assess the importance of changing environments on the evolution of sociality and cooperative breeding.

Acknowledgments We thank Nature Seychelles for facilitating the long-term Seychelles warbler project and the Seychelles Bureau of Standards and Department of Environment for permission for sampling and fieldwork. We thank everyone who has helped in the field, with laboratory work and with database management, and the overall Seychelles Warbler Research Group for dis- cussions. The long-term data collection was funded by two Natural Environment Research Council (NERC) grants (NE/F02083X/1 and NE/K005502/1) and by NERC (NER/I/S/2002/00712) and Marie Curie fellowships (HPMF-CT-2000-01074) to DSR, NERC grants to TB and by grants from the Netherlands Foundation for the Advancement of Tropical Research (WOTRO, 84- 519) and the Netherlands Organisation for Scientific Research (NWO) to JK (NWO-TOP, 854.11.003). SAK and MH were funded by NWO-VENI fellowships (863.13.017 and 863.15.020).

61 CHAPTER 3

SUPPLEMENTARY INFORMATION

We investigated whether food availability predicted group size by testing whether territories with higher mean food availability have larger groups, and whether annual changes in food ability were associated with changes in group size. We fitted the number of subordinates as a response variable in a generalized linear model with a Poisson error distribution and a log link function, and fitted mean territory-level food availability and the annual deviance from this mean value as predictors. We fitted four different models (see Table S3.1) and obtained averaged predictions based on WAIC (“Widely Applicable Information Criterion”; Watanabe 2010) by resampling predicted values of each model according to its Akaike weight.

Group size was positively correlated with mean territory food availability (β = 0.48, 95% CI = 0.24, 0.72; Fig. S3.1A). Furthermore, group size declined with higher annual island food availability (β = -0.14, 95% CI = -0.24, -0.03; Fig. S3.1B). In other words, groups became smaller in years when food availability was relatively high and larger in years when food availability was relatively low, which is in agreement with our results on dispersal, where dispersal increased with mean annual food availability.

1.8 1.0 1.6 A B 1.4 0.8 1.2 1.0 0.6 0.8 0.4 0.6 0.4 0.2 (mean ± 95% CI) (mean ± 95% CI) 0.2

Number of subordinates 0.0 Number of subordinates 0.0 1.5 2.0 2.5 3.0 3.5 −1.5 −1.0 −0.5 0.0 0.5 1.0 1.5 Mean territory Annual deviance in food availability food availability

FIGURE S3.1 Changes in group size (i.e. the number of subordinates) in relation to mean territory food availability (A) and the annual deviance in food availability from the territory mean (B). Solid and dashed lines represent model predicted mean values and 95% CI, respectively.

We determined the age of all breeding females and breeding males in each year on the basis of the breeding season in which they were born with 6 month increments (i.e. individuals born during the minor breeding season were classified as being 6 months old in the next major breeding season, and one year old in the following major breeding season etc.). To investigate potential changes in breeder age as a result of patterns of dispersal, we fitted

62 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

dominant breeder age for females and males in a multivariate response model with annual food availability and group composition as predictor variables.

7 A Dominant female B Dominant male ears) y 6

5 none female male 4 both

Dominant breeder age ( −0.5 0.0 0.5 −0.5 0.0 0.5 Mean annual food availability Mean annual food availability (between-year) (between-year)

FIGURE S3.2 Changes in the average age of dominant breeding females (A) and males (B) in relation to mean annual food availability for groups containing no subordinates (black), only female subordinates (red), only male subordinates (blue) or both female and male subordinates (green).

WAIC values indicated minimal support for the model with an interaction between group composition and annual food availability on breeder age (WAIC weight = 0.05). There was a positive residual correlation between breeding female age and breeding male age (σ2 = 0.15, 95% CI = 0.10, 0.20). Breeder age decreased with lower annual food availability, for both female and male breeders (breeding females: β = -0.73, 95% CI = -1.09, -0.37; breeding males: β = -0.54, 95% CI = -0.89, -0.19; Fig. S3.2A, B), and groups with subordinate females and with both subordinate males and females had older dominant breeders (breeding females: βfemale vs no subordinates = 0.96, 95% CI = 0.58, 1.34; βfemale + male vs no subordinates = 0.76, 95% CI = 0.22, 1.30; breeding males: βfemale vs no subordinates = 0.49, 95% CI = 0.11, 0.86; ; βfemale + male vs no subordinates = 0.82, 95% CI = 0.29, 1.35; Fig. S3.2A, B)

TABLE S3.1. Comparisons for models investigating the relationship between the likelihood of dispersal, and food availability. Probability of dispersal (N = 193) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βAF + βTF + βSex 263.22 0.43 α + βTF * βSex + βAF 264.77 1.55 0.19 2.24 α + βAF * βSex + βTF 264.82 1.6 0.19 2.30 α + βAF * βTF + βSex 264.87 1.65 0.17 2.55 α + βAF * βTF * βSex 269.91 6.69 0.01 30.35 AF = annual island food availability; TF = territory food availability; Sex = sex

63 CHAPTER 3

TABLE S3.2. Comparisons for models investigating the relationship between the likelihood of survival, food availability offspring sex. Survival (N =339) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βAF * βTF + βSex 465.48 0.54 α + βAF + βTF + βSex 467.55 2.07 0.19 2.82 α + βAF * βSex + βTF 468.81 3.33 0.10 5.30 α + βTF * βSex + βAF 468.89 3.41 0.10 5.52 α + βAF * βTF * βSex 469.6 4.12 0.07 7.85 AF = annual island food availability; TF = territory food availability; Sex = sex

TABLE S3.3. Comparisons for models investigating the relationship between the number of young fledged per breed group in each year, food availability and group composition. Young fledged (N = 1595) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βGC + βAF + βTF 2682.31 0.45 α + βGC + βTF * βAF 2682.52 0.21 0.41 1.11 α + βGC * βAF + βTF 2685.62 3.31 0.09 5.22 α + βGC * βTF + βAF 2686.73 4.42 0.05 9.11 α + βGC * βAF + βGC * βTF 2690.55 8.24 0.01 61.70 GC = group composition; AF = annual island food availability; TF = territory food availability

Per capita young fledged (N = 1595) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βGC + βAF + βTF 2671.84 0.513891 α + βGC + βTF * βAF 2672.54 0.7 0.361738 1.420616 α + βGC * βAF + βTF 2675.71 3.87 0.074132 6.932106 α + βGC * βTF + βAF 2676.81 4.97 0.042919 11.97344 α + βGC * βAF + βGC * βTF 2680.34 8.5 0.00732 70.19767 GC = group composition; AF = annual island food availability; TF = territory food availability

64 SPATIO-TEMPORAL RESOURCE VARIATION AND COOPERATIVE BREEDING IN THE SEYCHELLES WARBLER

TABLE S3.4. Comparisons for models investigating the relationship between the probability of clutch initiation, hatching and fledging, in relation to food availability and group composition. Probability of clutch initiation (N = 1595) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βGC * βAF + βTF 936.02 0.79 α + βGC * βAF + βGC * βTF 939.64 3.62 0.13 6.11 α + βGC + βAF + βTF 941.49 5.47 0.05 15.37 α + βGC + βTF * βAF 943.21 7.19 0.02 36.39 α + βGC * βTF + βAF 945.33 9.31 0.01 105.02

GC = group composition; AF = annual island food availability; TF = territory food availability

Probability of hatching (N = 1446) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βGC + βAF + βTF 2220.81 0.64 α + βGC + βTF * βAF 2222.94 2.13 0.22 2.90 α + βGC * βAF + βTF 2224.54 3.73 0.10 6.45 α + βGC * βTF + βAF 2226.83 6.02 0.03 20.28 α + βGC * βAF + βGC * βTF 2230.88 10.07 0.00 153.31 GC = group composition; AF = annual island food availability; TF = territory food availability

Probability of fledging (N = 1009) Model structure WAIC ΔWAIC Weight Evidence-ratio α + βGC + βAF + βTF 1328.67 0.39 α + βGC * βAF + βTF 1328.72 0.05 0.38 1.02 α + βGC + βTF * βAF 1330.67 2 0.14 2.72 α + βGC * βAF + βGC * βTF 1331.85 3.18 0.08 4.89 α + βGC * βTF + βAF 1375.99 47.32 0.00 1.88E+10 GC = group composition; AF = annual island food availability; TF = territory food availability

Chapter 4

Subordinate females in the Seychelles warbler obtain direct benefits by joining unrelated groups

Frank Groenewoud, Sjouke A. Kingma, Martijn Hammers, Hannah L. Dugdale, Terry Burke, David. S. Richardson & Jan Komdeur

Published in Journal of Animal Ecology, 87, 1251–1263 CHAPTER 4

ABSTRACT

1. In many cooperatively breeding animals, a combination of ecological constraints and benefits of philopatry favours offspring taking a subordinate position on the natal territory instead of dispersing to breed independently. However, in many species individuals disperse to a subordinate position in a non-natal group (“subordinate between-group” dispersal), despite losing the kin-selected and nepotistic benefits of remaining in the natal group. It is unclear which social, genetic and ecological factors drive between-group dispersal.

2. We aim to elucidate the adaptive significance of subordinate between-group dispersal by examining which factors promote such dispersal, whether subordinates gain improved ecological and social conditions by joining a non-natal group, and whether between- group dispersal results in increased lifetime reproductive success and survival.

3. Using a long-term dataset on the cooperatively breeding Seychelles warbler (Acroceph- alus sechellensis), we investigated how a suite of proximate factors (food availability, group composition, age and sex of focal individuals, population density) promote subordinate between-group dispersal by comparing such dispersers with subordinates that dispersed to a dominant position or became floaters. We then analysed whether subordinates that moved to a dominant or non-natal subordinate position, or became floaters, gained improved conditions relative to the natal territory and compared fitness components between the three dispersal strategies.

4. We show that individuals that joined another group as non-natal subordinates were mainly female and that, similar to floating, between-group dispersal was associated with social and demographic factors that constrained dispersal to an independent breeding position. Between-group dispersal was not driven by improved ecological or social conditions in the new territory and did not result in higher survival. Instead, between-group dispersing females often became co- breeders, obtaining maternity in the new territory, and were likely to inherit the territory in the future, leading to higher lifetime reproductive success compared to females that floated. Males never reproduced as subordinates, which may be one explanation why subordinate between-group dispersal by males is rare.

5. Our results suggest that subordinate between-group dispersal is used by females to obtain reproductive benefits when options to disperse to an independent breeding position are limited. This provides important insight into the additional strategies that individuals can use to obtain reproductive benefits.

68 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

INTRODUCTION

In many cooperatively breeding species, ecological conditions and low breeder turnover limit the possibilities of independent breeding, leading to intense competition for breeding vacancies (“ecological constraints hypothesis”; Emlen 1982; Hatchwell & Komdeur 2000). In addition, the benefits that individuals obtain by being in a group as subordinates can outweigh the benefits of leaving and breeding independently, even if breeding vacancies are available (“benefits of philopatry hypothesis”; Stacey & Ligon 1991; Komdeur 1992). Subor- dinates therefore often delay dispersal and help with raising the offspring of the breeding pair in the natal territory during future breeding attempts, until they can disperse to an independent breeding position (Koenig et al. 1992; Hatchwell 2009; Koenig & Dickinson 2016). Subordinates may obtain important benefits by remaining in their natal territory and should only disperse when the benefits of dispersal outweigh the benefits of philopatry (Stacey & Ligon 1991; Komdeur 1992) and the costs associated with dispersal (Heg et al. 2004a; Johnson et al. 2009; Bonte et al. 2012; Kingma et al. 2016b). Subordinates often benefit through access to food resources and protection from predators, thereby increasing survival or body condition (Heg et al. 2004a; Ridley et al. 2008). These effects can be further aug- mented by nepotistic benefits, where parents preferentially allocate protection or resources towards offspring (Ekman, Bylin & Tegelström 2000; Dickinson et al. 2009; Nelson-Flower & Ridley 2016). Subordinates can also obtain indirect benefits by helping to rear related offspring (Hamilton 1964; Richardson et al. 2003b; Briga et al. 2012), or direct reproductive benefits by gaining parentage within the territory (Richardson, Burke, & Komdeur, 2002). A high likelihood of inheriting the territory (Pen & Weissing 2000), or “shifting” to a nearby vacancy (Kokko & Ekman 2002; Kingma et al. 2016a) in the future might also select for philopatry.

Despite the benefits that can be obtained through natal philopatry, in many species subordinates disperse and accept a subordinate position in other, often unrelated, groups (henceforth: “subordinate between-group dispersal”; Reyer 1982; James & Oliphant 1986; Martín-Vivaldi et al. 2002; Seddon et al. 2005; see also Riehl 2013). As nepotism and kin-selected benefits are absent or minimal, investigating why subordinates move to non-natal groups can reveal important information about the social and environmental factors that drive both philopatry and dispersal. Subordinate between-group dispersal may be a best-of- a-bad-job strategy for subordinates forced, such as by eviction, to disperse from their natal territory. Eviction is common in cooperatively breeding systems and typically occurs when there are conflicting fitness interests between dominants and subordinates (Cant et al. 2010; Fischer et al. 2014). Subordinates who cannot control the timing of dispersal are likely to disperse under suboptimal conditions, and may become floaters (i.e., roaming through the

69 CHAPTER 4

population without association with any territory). Floaters lack access to group-defended resources and protection from predators, which can reduce survival and reproduction (Berg 2005; Ridley et al. 2008; Kingma et al. 2016a). Joining an unrelated group as a subordinate could function to avoid such costs (e.g. Reyer 1980; Ridley et al. 2008; Riehl 2013). On the other hand, irrespective of the possibility of remaining in the natal territory, between-group dispersal could function to increase an individual’s fitness prospects. For instance, the fitness prospects of subordinates may increase if between-group dispersal leads to increased access to food, breeding opportunities, or a shorter queue to inherit a territory (e.g. Nelson-Flower et al. 2018). Our aim was to elucidate the proximate drivers of subordinate between-group dispersal and its fitness consequences. We do this by comparing subordinate between-group dispersal with two other common dispersal strategies (floating, and direct dispersal to a dominant position) in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis). Where previous studies on this species have emphasized the ecological and social correlates of philopatry vs. dispersal (Eikenaar et al. 2007; Kingma et al. 2016a), here we focus specifically on dispersing individuals. The majority of subordinate Seychelles warblers disperse from the natal territory at some point, even if they initially delay dispersal (Eikenaar et al. 2007; Kingma et al. 2016a). We thus provide a cross-section- al overview of the conditions under which dispersal occurs. Individuals should prefer to disperse to a dominant position over becoming a floater, because floating is costly in this species (Kingma et al. 2017). However, the proximate drivers and the fitness consequences of subordinate between-group dispersal relative to these strategies are unclear. First, we assess which social (group size, breeder replacement and population density), ecological (territory quality) and individual (sex and age) factors are associated with subordinate between-group dispersal. Second, we test whether subordinate between-group dispersers eventually inhabit a better territory than their own natal territory and better than individuals that floated or dispersed to a dominant position. Food availability, competition for breeding positions and the possibility of direct benefits are all important for survival and reproductive success in the Seychelles warbler (Komdeur 1992; Richardson et al. 2002; Brou- wer et al. 2006) and should therefore affect dispersal decisions. Lastly, we test whether subordinate between-group dispersal ultimately leads to reproductive and survival benefits compared to dispersing to a dominant position, or floating. Together, our study provides valuable insights into the benefits of subordinate between-group dispersal that are independent of natal philopatry and kin-selected benefits and therefore contributes to understanding the drivers of sociality, dispersal and cooperation.

70 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

MATERIALS AND METHODS

Study species The Seychelles warbler is a small insectivorous passerine endemic to the Seychelles archipelago in the Indian Ocean (Hammers et al. 2015; Komdeur et al. 2016). Data were collected on Cousin Island (29 ha, 04º20′S, 55º40′E) from 2002 to 2015. The Cousin Island population of Seychelles warbler fluctuates around 320 adult birds on 110-115 territories. Since 1997, ca. 96% of the adult population has been ringed in any given year, with each individual having a unique colour and metal ring combination (Hadfield et al. 2006; Hammers et al. 2015). Seychelles warblers are socially monogamous, but on Cousin, ca 50% of territories contain one to four subordinates (mean ± SE = 0.7 ± 0.02; 55% of subordinates are female) that are usually, but not always, retained offspring from previous breeding attempts (Kingma et al. 2016a). Territories are stable between years and territory boundaries are identified based on spacing behaviour and conflicts with intruding conspecifics (Komdeur 1991). Two distinct breeding seasons occur: one major breeding season (June-September) and one minor breeding season (January-March; Komdeur & Daan 2005). Clutches typically contain a single egg (91% of clutches) and many nests fail during incubation due to nest predation (Komdeur & Kats 1999). We performed regular censuses throughout the breeding season to determine (1) group membership, based on where birds are consistently seen foraging and involved in non-antagonistic interactions with other resident birds, and (2) status in the group (dominant breeder or subordinate) based on mate guarding, courtship feeding and other affili- ative behaviours (Richardson et al. 2002; Kingma et al. 2016a). Resighting probabilities are extremely high in our study population (92-98%; Brouwer et al. 2010), so individuals that are not observed over two seasons can be confidently assumed dead. Birds are caught using mist nets and unringed individuals are subsequently ringed. Blood samples (25 μl) are taken by brachial venipuncture and used for sexing and parentage analyses (see below).

Seychelles warblers take most of their arthropod prey from the underside of leaves (Kom- deur 1991). Therefore, territory quality can be accurately estimated in terms of arthropod abundance (see Komdeur 1992 and Brouwer et al. 2009 for a detailed description). In brief, arthropod abundance was estimated at 14 locations each month during the breeding season by counting the number of arthropods on the underside of 50 leaves for the most abundant plant species (mostly trees). For each territory, in each breeding season, we determined the vegetation cover of each of the plant species and the size of the territory. Territory quality was calculated by multiplying the mean number of arthropods per plant species and the relative cover of that plant species, summed over all plant species. These values were then multiplied by territory size and log-transformed. For our analyses, territory quality was mean-centred within breeding seasons by estimating the best linear unbiased predic-

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tors (BLUPs; Robinson 1991) from a random regression model to account for between-year differences due to variation in the timing and frequency of sampling. For a subset of territories (28%) for which no estimate of territory quality was available at the time of dispersal (e.g., territory quality was not always measured in winter seasons), we used the BLUPs for that territory across all seasons for which a measurement was available, which is the best approximation of territory quality in any given season (Hammers et al. 2012; Groenewoud et al. in prep).

Dispersal strategies Dispersal to dominant or non-natal subordinate positions was defined as individuals permanently leaving their natal territory and settling in a different territory for at least one season as a dominant or subordinate. Individuals that dispersed to a dominant position usually filled a vacancy after the original dominant individual had died or dispersed or they, less commonly, deposed the dominant (Richardson, Burke & Komdeur 2007). In some cases, subordinates founded a new territory, for example, by budding off part of their resident territory (Komdeur & Edelaar 2001). Individuals were assigned as floaters when they permanently left their natal territory and were recorded in at least three territories during the breeding season, without associating with any specific group (Kingma et al. 2016a). All individuals were of known sex, which was determined using molecular techniques (Rich- ardson et al. 2001).

We defined the age at which an individual dispersed using the mean date between when it was last seen in its natal territory and when first seen in its new territory. Most birds (410/461) dispersed between fieldwork periods, in which case we used the mean date between these fieldwork periods (mean ± SE number of days between fieldwork periods = 117.6 ± 50.7 days). Dispersal distance was determined as metres between the geometric centres of the natal territory and the territory to which the individual dispersed.

Genetic relatedness and reproductive success Pairwise genetic relatedness (R) was estimated based on 30 microsatellite loci (Richardson et al. 2001; Spurgin et al. 2014) using the Queller and Goodnight (1989) estimation implemented in the r-package “related” v0.8 (Pew et al. 2015). A previous study using these microsatellite loci in the Seychelles warbler has confirmed that relatedness for known parent–offspring pairs does not differ from R = 0.5 (Richardson, Komdeur & Burke 2004). To determine whether dispersers that joined another territory as non-natal subordinates (n = 3 males, n = 20 females) obtained parentage as subordinates, we assigned parentage for all offspring that were produced in that territory during a focal subordinate’s tenure using masterbayes 2.52 (Hadfield et al. 2006; Dugdale et al. in prep). Lifetime reproductive success was estimat-

72 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

ed by assigning all offspring produced per breeding female, excluding those that did not survive to subadulthood (>5 months of age). Individuals are caught at different points after hatching, including as nestlings, fledglings or juveniles, but almost all individuals are caught before reaching subadulthood. Furthermore, mortality is highest prior to subadulthood (Brouwer et al. 2010), and individuals never breed before this age (Komdeur 1995). Using this criterion therefore more accurately reflects recruitment than using all offspring produced. Lifetime reproductive success was determined only for females because almost all non-natal subordinates were female (20/23). Only females for which we had documented all lifetime reproductive events, that is, that died before the end of our study (n = 123, n = 18, n = 8 for females moving to a dominant, non-natal subordinate or floating position, respectively; mean age at death was 4.6 years and did not differ between different strategies), were included. Furthermore, we excluded all individuals that were translocated to another island (2004 and 2011; Wright et al. 2014) within a year after they dispersed for the analysis of survival, and all individuals that were translocated for the analysis of lifetime reproductive success.

Statistical analyses Proximate drivers of between-group dispersal To identify the proximate factors that determine individual dispersal strategies, we applied a multinomial logistic regression analysis using the r-package “brms” v1.5.1 (Bürkner 2017) which fits models through a Hamiltonian Monte Carlo (HMC) algorithm in STAN (Hoffman & Gelman 2014; Stan Development Team 2015). Multinomial logistic regression generalizes the logistic regression to allow for the fitting of more than two possible discrete outcomes. We fitted the three alternative dispersal strategies: dispersal to (1) a dominant position (reference category; n = 406), (2) a non-natal subordinate position (n = 23) or (3) floating (n = 32) as a response variable. We added individual (age at dispersal, sex), social (whether breeder replacement had occurred, group size, population density) and ecological (territory quality) factors in the natal territory as predictors. Group size was expressed as the number of subordinates (i.e., older than three months) present in the territory. Population density (i.e., the total number of birds >6 months on the island at the start of the breeding season) was included as a proxy for the overall degree of competition for dominant positions. In- dividuals younger than 6 months seldom disperse (Komdeur, 1996; Eikenaar et al., 2007; this study) and therefore rarely compete for breeding positions. We included “field season” as a random effect. We used weakly regularizing normal priors on all beta coefficients and half-Cauchy priors on variance components (McElreath 2015). Model convergence and assumptions (Ȓ (Gelman & Rubin 1992) and posterior predictive checks) were inspected using the package “shinystan” v2.0.0 (Chang et al. 2016; Vehtari, Gelman & Gabry 2016). All parameter estimates are reported as means with 95% Bayesian credible intervals.

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Dispersal to improve conditions We investigated whether subordinates improved their conditions by dispersing, and whether such improvements differed between dispersal strategies, using predictions de- rived from a benefits-of-philopatry framework. We tested whether subordinates with different dispersal strategies experienced a change (compared to their natal territory) in (1) territory quality, (2) group size and (3) reproductive competition (i.e., whether there was a same-sex subordinate in the group) by fitting separate (generalized) linear mixed effects models with varying intercepts for individuals (n = 461). Specifically, we fitted (1) territory quality as a response variable with a Gaussian error and included “natal vs. dispersal territory” (i.e., a dummy variable (0/1) which expresses the difference, or slope, between the natal and dispersal territory in the response), dispersal strategy, sex and the three-way interaction between “natal vs. dispersal territory,” dispersal strategy and sex as predictors. To estimate changes in group size, (2) we fitted group size as a response variable assuming a Poisson error. We included “natal vs. dispersal territory,” dispersal strategy and the interaction between “natal vs. dispersal territory” and dispersal strategy as predictors. To assess whether individuals experienced a change in reproductive competition, (3) we fitted the presence/absence of a same-sex subordinate in the group as a response variable assuming a binomial error distribution. We included “natal vs. dispersal territory,” dispersal strategy and the interaction between “natal vs. dispersal territory” and dispersal strategy as predictors. We fitted different changes between males and females only for the analysis of territory quality; a lack of variation in the response prohibited accurate estimation of sex effects in the other two models, and males and females were therefore analysed together.

Subordinates may increase their chances of territory inheritance by joining a territory where the same-sex breeder is older than the same-sex breeder in their natal territory and thus is more likely to die in the near future (Hammers et al. 2015). To test this prediction, we compared the age of the same-sex dominant breeder in the natal and dispersal territories at the time of dispersal by fitting the ages of the same-sex dominant breeders as a response variable in a linear mixed model with varying intercepts (i.e., random effects) for different birds (subordinate between-group dispersers only; n = 21 and 23, for natal and dispersal territories, respectively). We included “natal vs. dispersal territory” as a predictor. Further- more, we assessed subordinate-breeder relatedness in the natal and non-natal territory to test whether individuals that dispersed to non-natal subordinate positions did so to territories with related breeders where they could gain indirect genetic benefits. We fitted pairwise relatedness (R; see above) as a response variable assuming a Gaussian error distribution and fitted “natal vs. dispersal territory”, “dominant sex” and its interaction as predictor variables. We distinguished between female and male dominants in this analysis, because (due to extra-pair paternity) relatedness to the dominant female is higher than relatedness

74 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

to the dominant male, and the former is therefore a more reliable indicator of the indirect benefits to be gained (Richardson et al. 2003b; Komdeur, Richardson & Burke 2004b). Only subordinate between-group dispersers were included in this analysis (n = 23).

Fitness consequences of subordinate between-group dispersal We investigated the fitness benefits of becoming a subordinate on a non-natal territory by assessing (1) whether they obtained a dominant position through inheritance or “staging” (dispersing again after remaining in the non-natal territory for at least one season; Cock- burn et al. 2003) and (2) whether they gained parentage (Richardson et al. 2002). Further- more, we (3) compared lifetime reproductive success (number of independent offspring; see “genetic relatedness and reproductive success”) of females that dispersed to non-natal subordinate or dominant positions, or that became floaters. Many females in our dataset never successfully reproduced (58/149); therefore, total lifetime reproductive output was fitted as the response variable in a zero-inflated Poisson regression model. Dispersal strategy was added as a predictor and Bayes factors were calculated to assess the differences between these strategies.

Dispersal strategies might have different costs (Kingma et al. 2016a, 2017). We compared survival to the next season in the first year after an individual had left its natal territory for individuals that dispersed to non-natal subordinate or dominant positions, or that became floaters, in a generalized linear model with a binomial error structure. We included age at dispersal (in years) as a covariate in the model. We fitted separate models for males and females, because the low occurrence of male between-group dispersal prevented accurate estimation of the “sex x dispersal strategy” interaction.

All frequentist models were fitted with package “lme4” v1.1-12 (Bates et al. 2015) and checked for model assumptions such as overdispersion, homogeneity of variance and normality. We used an information theoretic model selection approach using AICc (Akaike 1973; Hurvich & Tsai 1989). We fitted full models and removed variables from the model if this resulted in a lower AICc value. Parameter estimation was based on the model with the lowest AICc value, and previously dropped variables were re-entered sequentially to be estimated. Parameter significance was estimated on the basis of likelihood ratio tests between nested models assuming a χ2- distribution or F-distribution. Similar “intermediate” model selection approaches have been advocated in Zuur et al. (2009). All higher-order interactions were dropped for the estimation of main effects, and model predictions were made using the package “aiccmodavg” v2.1-1 (Mazerolle 2013). We used to the package “multcomp” v1.4-6 (Hothorn, Bretz & Westfall 2008) and “phia” v0.2-1 (De Rosario-Martinez 2015) to obtain linear contrasts between different factor levels and interactions. All analyses were performed in R version 3.3.1 (R Core Team 2016).

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RESULTS

Subordinate dispersal strategies We identified dispersal events for 461 subordinates (n = 223 females, n = 238 males; Fig. 4.1, Table 4.1). Dispersal to a dominant position was most common (n = 406, 88%), while 23 individuals (5%) dispersed to a subordinate position in a non-natal territory and 32 individuals (7%) became floaters. Of the individuals that moved to a subordinate position, six acted as stagers, moving again to either a dominant (three females and two males) or another subordinate position (one female) after staying in the territory for only a short time (mean ± SE = 0.75 ± 0.88 years; seven inherited the dominant position after a mean of 2.54 ± 0.82 years (all females), and eight remained as subordinates in their new territory until they died (tenure as subordinate: mean ± SE = 2.77 ± 0.76 years; all females).

Proximate drivers of between-group dispersal Several proximate factors were associated with the likelihood that individuals dispersed to a non-natal subordinate position, became a floater, or dispersed to a dominant position directly (Fig. 4.2). Subordinate between-group dispersers were most often female (87%),

461 Natal subordinate

23 406 32

Non-natal Dominant Floater subordinate breeder

21 7 6 8 Dominant Inherit Staging Died as breeder subordinate

FIGURE 4.1 The fate of 461 subordinate Seychelles warblers that followed different dispersal trajectories from their original natal territory, with proportions of males (blue) and females (pink) in each category. When numbers are not carried through to the next category, this means that these individuals were seen last in that earlier position.

76 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

dispersed during periods of high population density, came from smaller groups, and were both younger (see also Table 4.1) and more likely to have experienced dominant male turnover in their natal territory than individuals that dispersed to a dominant position directly (Fig. 4.2). Individuals that became floaters were younger than those that moved to a dominant position directly, but they were not more likely to be female (Fig. 4.2; 44% of floaters are female) and the likelihood of becoming a floater was not related to population density. Similar to individuals that moved to a subordinate position, floaters often left their natal territory after replacement of the dominant male (dominant males were replaced for 9/32 (28%) floaters, 6/23 (26%) of subordinate between-group dispersers and 46/406 (11%) of individuals that dispersed to a dominant position). Replacement of the dominant female in the natal territory did not affect dispersal strategy (Fig. 4.2).

Subordinate vs dominant Floating vs subordinate Floating vs dominant

Sex

Population density

Number of subordinates

Breeder male replaced

Breeder female replaced

Territory quality

Age at dispersal −4 −3 −2 −1 0 1 2 3 4 Parameter estimate (mean±CI)

FIGURE 4.2 Parameter estimates with 50% (thick error bars) and 95% (thin error bars) credible intervals of the proximate factors that may drive the dispersal strategies of 461 subordinate Seychelles warblers. Symbols represent the mean effect (log odds ratios) that individuals will disperse to a non-natal subordinate position relative to a dominant position (triangles), become floaters relative to moving to a non-natal subordinate position (squares) or become floaters relative to the probability of moving to a dominant position (circles). The reference category for sex is “female”.

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Dispersal to improve conditions There was no difference in the quality of the natal and dispersal territory for subordinate be- 2 2 tween-group dispersing females (χ 1 < 0.01, p = 0.97; Fig. 4.3A). Females (χ 1 = 5.28, p = 0.04) and 2 males (χ 1 = 6.85, p = 0.04) that moved to a dominant breeding position had significantly lower territory quality in their new territory (Fig. 4.3A). For females that obtained a dominant position after floating, territory quality was also lower in the new territory than in the natal terri- 2 tory (χ 1 = 6.24, p = 0.04). Males that obtained a dominant position after floating experienced 2 no significant change in territory quality χ( 1 = 0.03, p = 0.97). Subordinate between-group dis- 2 2 persers (χ 1 = 0.79, p = 0.56) and individuals that obtained a position after floating χ( 1 = 0.06, p = 0.81) did not move to groups of different size than their natal territory (Fig. 4.3B). However, subordinates that dispersed directly to a dominant breeding position moved to groups that 2 contained fewer subordinates than their natal territory (χ 1 = 30.94, p < 0.001; Fig. 4.3B). Sub- ordinates dispersing directly to a dominant breeding position also moved to smaller groups relative to subordinate between-group dispersers (df = 1, z = 2.21, p = 0.03; Fig. 4.3B). The probability of having a same-sex subordinate in the natal and new territory was similar for subor- 2 dinate between-group dispersers (χ 1 < 0.001, p = 0.99; Fig. 4.3C), and there were no differences between dispersal strategies (interaction “natal vs. dispersal territory × dispersal strategy”: 2 χ 3 = 4.55, p = 0.21). Overall, the probability of having a same-sex subordinate was lower in the 2 new territory than in the natal territory (χ 1 = 19.74, p < 0.001). Subordinate between-group 2 dispersers did not move to territories with an older same-sex breeder dominant (χ 1 = 0.25, p = 2 0.61; Fig. 4.3D), and this did not differ between subordinate sexes χ( 1 = 0.06, p = 0.79).

Subordinates were highly related to the dominants in their natal group (Rnatal male: mean ± SE

= 0.29 ± 0.04, z = 6.61, p < 0.001; Rnatal female: mean ± SE = 0.39 ± 0.05, z = 8.72, p < 0.001), but not to the dominants in the territory that they joined as subordinates after dispersing (Rdispersal male: mean ± SE = −0.02 ± 0.04, z = −0.44, p = 0.99; Rdispersal female: mean ± SE = 0.03 ± 0.04, z = 0.778, p = 0.89). Subordinates were consequently less related to the dominants in the territories they joined as subordinates than they were to the dominants in their natal territory, and this decrease was similar between subordinates and the dominant female and male 2 (change in R: mean ± SE = −0.33 ± 0.04, χ 1 = 48.78, p < 0.001). Subordinate-breeder relatedness between the natal and dispersal territory showed a similar decrease when we included only between-group dispersing subordinate females (n = 20; change in R: mean ± SE = −0.36 2 ± 0.04, χ 1 = 47.12, p < 0.001). Fitness consequences of subordinate between-group dispersal About 38% (8/21) of between-group dispersing subordinate females gained parentage in their non-natal territory. Subordinate between- territory dispersing females had a moder- ate likelihood of inheriting their non-natal territory (33%; 7/21), and 57% (4/7) of these inheriting subordinates gained parentage as a subordinate in their non-natal territory. Similarly, among the between-group dispersing females that died as a subordinate in their non-natal

78 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

0.5 A 0.8 B ns ns ns ns 0.3 ** * * 0.6 y quality 0.1 ito r 0.4 −0.1 e ter r v

Mean number 0.2

−0.3 of subordinates Female Male Relati −0.5 0.0 Dominant Subordinate Floater Dominant Subordinate Floater Position after dispersal Position after dispersal 0.5 C 8 D

x sub ns ns* ns e

0.4 *** ears) x y 7 0.3 6 0.2 Same−s e 5 0.1 breeder age ( 0.0 4 Probability same−s Dominant Subordinate Floater Natal Dispersal Position after dispersal territory territory

FIGURE 4.3 Changes in model predicted means (± SE) of (A) territory quality, (B) number of subordinates and (C) the probability of having a same-sex subordinate, between the natal (circles) and dispersal territory (triangles) for subordinates that moved to a dominant position (n = 406), a non-natal subordinate position (n = 23) or that obtained a territory after floating (n = 21). Similar to that, in (D), the age of the same-sex dominant breeder in the natal (n = 21) and dispersal (n = 23) territory are given. Asterisks indicate significance of slopes. territory, 50% (4/8) reproduced as a subordinate. Stagers (n = 6/21 between-group dispersers) never obtained parentage (Table 4.2). Subordinate females produced 52% (15/29) of all offspring produced in their non-natal territories during their tenure.

Almost all floater females (93%; 13/14), but only 44% (8/18) of floater males, obtained a dominant position after floating (male vs. female floaters obtaining a dominant position after floating (Pearson’sχ 2-test with MCMC simulated p-values, n = 2,000): χ2 = 8.18, p = 0.005). This difference is explained by male floaters having a lower probability of survival to the next breeding season than males that dispersed directly to a dominant position (41% vs. 2 91% survival; βfloater-dominant: mean ± SE = −2.54 ± 0.54, χ = −2.52, p < 0.001; Fig. 4.4A). Females showed no significant differences in survival between dispersal strategiesχ ( 2 = 0.05, p = 0.97; Fig. 4.4A). Female subordinates that dispersed to a non-natal subordinate position had similar lifetime reproductive success to females that moved directly to dominant position

(βsubordinate-dominant: mean (95% CI) = 0.21 (−0.16, 0.57); Fig. 4.4B), and both had higher lifetime

79 CHAPTER 4

A B ♀ p = 0.97 ♂ p < 0.001 3.0 * 1.0 ns * 10 2.5 8 0.8 2.0 6 1.5 0.6 4 1.0 ing produced 2 0.4 0.5 Survival probability 157 19 14 178 18 123 18 8 Offsp r

Mean predicted LRS 0.0 0 Dom Sub Float Dom Float Dom Sub Float Position after dispersal Position after dispersal

FIGURE 4.4 In (A), the model predicted mean probabilities (± SE) that dispersing subordinate females and males survive to the next breeding season depending on their position after dispersal (Dom = dominant, Sub = subordinate and Float = floater). Only two males joined another group as a non-natal subordinate, which was too small a sample size to analyse and was therefore excluded. In (B), the predicted mean lifetime reproduction (number of offspring produced that survived >5 months; open circles; left axis) (± 95% CI) and distribution of the raw data (median, interquartile range and density; right axis) of all females with complete reproductive histories. Asterisks indicate significant differences according to Bayes factors.

reproductive success than female floaters β( subordinate-floater: mean (95% CI) = 0.97 (0.19, 1.84);

βfloater-dominant: mean (95% CI) = −0.76 (−1.58, −0.04); Fig. 4.4B).

DISCUSSION

In cooperatively breeding species, subordinates are expected to disperse when the fitness benefits of doing so outweigh those of natal philopatry (Stacey & Ligon 1991). In many species, individuals leave their natal territory to settle as a subordinate elsewhere, despite the lack of nepotism and kin-selected benefits on non-natal territories. Why they do so has been largely unexplored (but see Riehl 2013). Our analyses reveal that dispersal to a non-natal subordinate position and floating are associated with reduced nepotism (i.e., higher likelihood of dominant male replacement) and constraints on dispersal (i.e., higher population density). However, subordinate females can escape the costs of floating by becoming a co- breeder in an unrelated group. We discuss our results below and explain how they allow inferences about the importance of the benefits of philopatry and ecological constraints hypotheses in explaining sociality in this cooperatively breeding species.

Proximate factors promoting between-group dispersal Nepotism and parental tolerance can affect dispersal decisions and fitness (Ekman & Griess- er 2002; Eikenaar et al. 2007; Nelson-Flower & Ridley 2016). Our analyses show that the re-

80 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

placement of the dominant male, but not the female, in the natal territory is associated with subordinates joining an unrelated group or becoming a floater (Fig. 4.2). This result indicates that nepotism (tolerance by a related dominant male) plays a role in explaining philopatry in this species. Due to high rates of extra-pair paternity (ca. 40% of offspring; Richard- son et al. 2001), philopatric subordinates are on average more related to the breeding female than to the breeding male (Richardson et al. 2002). If kin-selected benefits drove philopatry, we would expect higher dispersal propensity when the breeding female, rather than the breeding male, is replaced. Thus, our results are consistent with reduced nepotistic benefits and potential eviction, but not reduced indirect benefits, driving dispersal. That eviction is responsible for subordinate dispersal to positions other than dominant ones, is further supported by between-group dispersers and floaters being younger at the time of dispersal and tending to disperse under higher population density than subordinates that dispersed to a dominant position (Fig. 4.2, Table 4.1). These results are consistent with reduced parental tolerance for natal subordinates (Nelson-Flower & Ridley 2016) and with increased competition for independent breeding positions after (forced) dispersal, such as proposed by the ecological constraint hypothesis (Emlen 1982). Interestingly, our results suggest that reduced local competition (i.e., group size) increases the probability of between-group dispersal, but not floating, relative to dispersal to a dominant position (Fig. 4.2). Previous studies in the Sey- chelles warbler suggest that this is not the result of dispersal due to increased competition (i.e., for food) in the group, because group size is not associated with the overall likelihood of dispersal (Eikenaar et al. 2007). One possibility is that small groups are an indication of poor group reproductive success and therefore of low predicted future benefits of cobreeding, which is one of the major benefits of female philopatry (Richardson et al. 2002).

Between-group dispersal as a strategy All floaters either died or gained a dominant position after floating, but none joined a group as a non-natal subordinate, which suggests that these individuals are using a different strategy. This is in contrast to pied babblers Turdoides bicolor, where floaters were more likely to regain a position as a subordinate than as dominant breeders (Ridley et al. 2008). That floating and becoming a non-natal subordinate are two different strategies in the Seychelles warbler is further supported by floaters dispersing further than subordinate between- group dispersers (Table 4.1). This suggests that between-group dispersers are un- likely to have floated before they join another territory as a subordinate. Females are also more likely than males to prospect as a subordinate (Kingma et al. 2016a), which might allow them to explore opportunities to join a territory as a non-natal subordinate in the future. Recent theoretical work has shown that, under intense competition for breeding vacancies, both strategies (i.e., obtaining a dominant position, or joining a non-natal group) can emerge and coexist in the same population (Port, Schülke & Ostner 2017).

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TABLE 4.1 Differences in age at dispersal and dispersal distances for subordinates in the Seychelles warbler with different dispersal strategies using linear models with sex, dispersal strategy and the interaction “sex x dispersal strategy” Age at dispersal (years) Dispersal distance (meters) N (mean±se) (mean±se) Position after dispersal Female Male Female Male Female Male Dominant 189 217 Dom vs Sub: Dom vs Sub: 1.23±0.05 1.34±0.04 0.27±0.14, 231.58±8.99 109.25±8.39 0.31±0.27, t = -1.96, p = 0.12 t = 1.15, p = 0.47 Non-natal 20 3 Sub vs Float: Sub vs Float: subordinate 1.05±0.14 0.52±0.36 0.03±0.18, 204.35±27.65 46.77±71.39 -1.48±0.37, t = 0.18, p = 0.98 t = -3.94, p < 0.001 Floater 14 18 Float vs Dom: Float vs Dom: 0.9±0.17 1.07±0.15 -0.30±0.12, 325.03±34.29 262.35±43.72 1.17±0.28, t = 2.58, p = 0.03 t = 4.20, p < 0.001 Total 223 238 Female vs Male: Female vs Male: 0.10±0.06, -1.21±0.12, F = 2.59, p = 0.11 F = 103.2, p < 0.001

Our results show that subordinates did not join other groups to access a territory of higher quality, reduce competition for food (i.e., group size) or improve the chances of territory inheritance (Fig. 4.2). However, subordinates that moved to a dominant position directly obtained lower quality territories than their natal territory (Fig. 4.3A), which could be partly due to newly formed territories (e.g., by budding) being smaller than territories that have been able to expand over several years (Komdeur & Edelaar 2001). Subordinates were, on average, related to the dominant male and female in their natal group, thus able to obtain indirect genetic benefits. Dominant-subordinate relatedness estimates were lower than predicted for parent-offspring dyads (R ≈ 0.5) and differed between breeding males and breeding females due to frequent extra-group paternity and subordinate cobreeding (Rich- ardson et al. 2002). Between- group dispersers subsequently moved into unrelated groups, which excludes the possibility that subordinates accrue benefits through nepotism or relatedness by dispersing, but leaves the possibility that subordinate females are allowed to join and cobreed in these territories, because they are unrelated. However, previous work on the Seychelles warbler did not find any evidence for inbreeding avoidance when finding a mate (Eikenaar, Komdeur & Richardson 2008a), and unrelated female subordinates are not more likely to reproduce than related females (Richardson et al. 2002). In consequence, non-natal subordinates do not gain any of the social or ecological benefits that we have analysed here relative to their natal territories, but do gain other (reproductive) benefits, which we discuss next.

Survival and reproductive benefits of between-group dispersal For females, all dispersal strategies have the same high level of survival (Fig. 4.4A). However,

82 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

similar to what was found in Kingma et al. (2016a) and Kingma et al. (2017), male floaters suffer higher mortality when floating compared to male dispersers that obtain a dominant position directly. Differential survival for male and female floaters suggests that being associated with a territory has important survival benefits for males, but not for females. Male subordinates, however, seldom join non-natal territories as a subordinate and never reproduce when they do (Table 4.2). One explanation for this pattern is that females are tolerated in or around other territories much more than males. This is also supported by our previous finding that males are more likely to be attacked by conspecifics when intruding into territories than females (Kingma et al. 2017). This pattern of female acceptance vs. aggression towards males concurs with what we know of the Seychelles warbler, where there can be clear benefits of female cobreeding, but dominant males frequently lose paternity to males from other territories (Richardson et al. 2001).

Our results show that female subordinates were responsible for 52% of all offspring produced in their non-natal territories (Table 4.2), similar to the 47% gained by all female subordinates reported in another study (Richardson et al. 2002). However, non-natal subordinate females had a higher likelihood of inheriting their non-natal territory than was previously reported for natal subordinates (33% of non-natal subordinates inherited the territory vs. 2% of natal subordinates (Eikenaar et al. 2008b). As a result, females that dispersed to a non-natal subordinate position had higher lifetime reproductive success than females that floated first (Fig. 4.4B; 1.98 vs. 0.79 offspring, respectively). We can speculate about several possible explanations: (1) females that join as subordinates move to higher quality territories than floaters (Fig. 4.3A); (2) these females could potentially breed directly after dispersal as cobreeding subordinates (while floaters lost time in the process of floating). While the direct lifetime reproductive success of female between-group dispersers seems to be equal to that of females that disperse directly to a dominant position, we have not taken into account any potential indirect benefits that could be accrued by natal subordinates. Although indirect

TABLE 4.2 Mean tenure duration, whether individuals help and gain reproductive success (number of individuals that gained parentage and number of offspring sired by subordinate vs total offspring produced in the territory during subordinate tenure) of non-natal subordinate Seychelles warblers (while subordinate) with different eventual fates in the territory to which they dispersed. Most (n = 20) were females, but one male was observed staging. Number of individuals Subordinate tenure duration Observed helping Gained parentage Offspring sired by subordinate (out of (mean±se years) total number of offspring) Died (n=8) 2.77±0.76 7/8 (87.5%) 4/8 (50%) 11/17 (64.7%) Inherit (n=7) 2.54±0.82 5/7 (71.4%) 4/7 (57.1%) 4/12 (33.3%) Staging (n=6) 0.75±0.88 1/6 (16.7%) 0/6 (0%) 0/0 (0%) Mean 2.11±0.49 13/21 (61.9%) 8/21 (38.1%) 15/29 (51.7%)

83 CHAPTER 4

fitness benefits are relatively low in the Seychelles warbler (Richardson et al. 2002), they might give an advantage to natal philopatry over becoming a non- natal subordinate.

Why do dominants accept non-natal subordinates? An important finding of our study is that dispersal to a non-natal subordinate position is strongly female biased. A possible explanation for this could be the benefits that both the immigrant female and the original members of the new territory can obtain from another female joining the group. Incubation by subordinate females (males do not incubate) is common in the Seychelles warbler (Richardson et al. 2001) and reduces nest predation (Komdeur 1994a; Kingma et al., in prep). In addition, dominant males may sire additional offspring with cobreeding females (Richardson et al. 2001, 2002). In most species where subordinates join unrelated groups, immigrants tend to be males that seek copulations with resident females, or wait to inherit the breeding position in exchange for help (e.g. Reyer 1982; Seddon et al. 2005; see also Riehl 2013). In the Seychelles warbler, subordinate males provide only limited help and could potentially threaten the reproduction and position of the dominant male. Subordinate males may therefore be prevented from joining non-natal groups. Although our current framework did not set out to test the reasons why individuals were accepted in territories, future work should incorporate ecological and social factors that would increase the benefits groups could obtain from accepting additional group members. This could shed light on the question why we do not see more females disperse to non-natal subordinate positions.

Conclusion Our results shed light on the benefits of cooperative breeding under varying social and ecological conditions and show how these can be independent of benefits accrued through kin selection and nepotism. We suggest that becoming a floater can be considered a “last resort” strategy. Interestingly, both floating and dispersal to a non-natal subordinate position seem to be driven by constraints on the timing and destination of dispersal, such as increased competition for breeding positions and potential eviction from the natal territory. However, some dispersing females are able to join other territories and cobreed with the dominant pair, and many of these females inherit the territory. This results in dispersal to a non-natal subordinate position leading to higher lifetime reproductive success compared to floating and similar to subordinates that disperse to a dominant position.

Acknowledgements We thank Nature Seychelles for the opportunity to work on Cousin Island, and the Sey- chelles Department of Environment and Seychelles Bureau of Standards for permits. We thank the many fieldworkers in the Seychelles warbler project who have contributed to col-

84 SUBORDINATE FEMALES IN THE SEYCHELLES WARBLER OBTAIN DIRECT BENEFITS BY JOINING UNRELATED GROUPS

lecting the long-term data, Owen Howison for help maintaining the long-term database and Marco van der Velde for microsatellite genotyping. We also thank Christina Riehl and one anonymous reviewer for valuable comments on the manuscript. The long-term data collection has been funded by various grants from the UK Natural Environment Research Council (NERC) and the Netherlands Organisation for Scientific Research (NWO) awarded to J.K., D.S.R., H.L.D. and T.B. (e.g., NWO-ALW 823.01.014, NER ⁄ I ⁄S⁄2002 ⁄00712, NE/F02083X/1, NE/I021748/1 and NE/K005502/1). F.G. was supported by a NWO-TOP grant awarded to J.K. and D.S.R. (854.11.003), S.A.K. and M.H. were funded by NWO-VENI fellowships (863.13.017 and 863.15.020), and T.B. was funded by a Leverhulme Fellowship.

Author’s contributions F.G., S.A.K. and J.K. conceived the study. F.G. analysed the data and wrote the first draft. J.K., D.S.R., H.L.D. and T.B. coordinated the long-term study and maintain the long-term dataset. All authors contributed critically to the manuscript.

85 In memory of Hirokazu Tanaka Chapter 5

Predation risk mediates the anti-predator benefits of sociality and suppresses within-group conflict in a cooperatively breeding cichlid fish

Frank Groenewoud*, Joachim G. Frommen*, Dario Josi, Hirokazu Tanaka† & Michael Taborsky

* Equally contributing authors

† This author passed away before completion of this manuscript CHAPTER 5

ABSTRACT

Social conflict is a repellent force in the evolutionary transitions to complex sociality. Thus, identifying the factors reducing such conflict is crucial in order to understand why and how such transitions occur. Predation risk, while thought to be a major factor selecting for group living, has generally been undervalued as a driver of complex sociality, despite the potential benefits of cooperation under high risk of predation. In the current study, we investigated whether predation risk leads to decreased social conflict, both within and between groups, in the cooperative breeder Neolamprologus pulcher. This highly social cichlid fish species lives in stable groups of a dominant breeding pair and several brood care helpers. We show that in nature, dominants reduce aggression towards subordinates under increased risk of predation, and that aggressive interactions between subordinates decline accordingly. Subordinates show reduced levels of submission and no changes in helping behaviour with increasing predation risk, indicating that this is not the cause of reduced aggression by dominants. In contrast, aggression between groups is independent of the level of predation risk. This coincides with significant fitness effects of the presence of subordinates in dependence of the levels of predation risk, whereas the presence of close neighbours did not affect reproductive output. Reduced aggression by dominants apparently serves to incentivize large subordinates, which are important for the defence against large predators, to remain in the group, despite the costs they inflict due to competition for resources and reproduction. We argue that that delayed dispersal by large subordinate might thus be driven by mutualistic benefits of cooperation under increased threat of predation. These results demonstrate the importance of trade-offs between predator protection and intra-group competition, highlighting the importance of predation risk for the evolution of complex social systems.

88 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

INTRODUCTION

The evolution of life on earth has been characterized by several key steps which involved previously self-replicating entities (e.g. genes, cells, individuals) to cooperate and form more complex units, which have been termed major evolutionary transitions (Smith & Sza- thmary 1995). Several processes have been identified that are necessary for such transitions to take place, including group formation, benefits of cooperation, division of labour and suppression of conflict (West et al. 2015). Conflict often occurs when there are incompat- ible fitness interests between individuals, and can diminish, or even negate, the benefits obtained through cooperation. Consequently, the factors that reduce conflict have received much attention from evolutionary ecologists (Krause & Ruxton 2002; Bourke 2011). Kin selection, i.e. fitness effects of genes accrued through its effects on relatives carrying the same genes (Hamilton 1963, 1964), can reduce conflict between individuals and thereby promote transitions to sociality (West-Eberhard 1975; Clutton-Brock 2002; Briga et al. 2012; Bourke 2014). However, it has limited explanatory power in cases where cooperation occurs mainly between non-relatives. Thus, alternative hypotheses are necessary to explain limited social conflict and the evolution of cooperation in groups consisting mainly of unrelated indivi duals.

Competition for finite resources (i.e. food or reproduction) is considered to be one of the predominant costs of group living (Alexander 1974; Reeve 2000; Shen et al. 2014). This competition is usually expressed in the form of aggression, which is aimed at obtaining a larger share of such resources at the expense of others, leading to social conflict (Shen et al. 2014). In social groups where some individuals (i.e. dominants) have control over group membership of others (i.e. subordinates) through the use of aggression (Johnstone & Cant 1999), conflict can lead to evictions. Social conflict and resulting eviction are common features of many cooperatively breeding mammals (e.g. Clutton-Brock et al. 2001; Cant et al. 2010), birds (e.g. Webster 1994; Dunn et al. 1995) and fishes (e.g. Taborsky 1985; Balshine-Earnet al. 1998; Fischer et al. 2014). Additionally, dominants can use aggression to force subordinates to provide (more) help, potentially leading to negotiations about ‘optimal’ levels of help (Gaston 1978; Quiñones et al. 2016). Conflict can also occur between subordinates in the same group, for instance over access to food or position in the hierarchy (Field & Cro- nin 2007). Regardless of the function or source of aggression, subordinates should disperse voluntarily when the costs (e.g. levels of aggression received and help provided) of being in the group exceeds its benefits (e.g. protection against predators). Social conflict and aggression are therefore expected to decrease when the benefits of having additional group members and/or cooperation, are high.

89 CHAPTER 5

Predation risk is a major ecological factor selecting for group living through passive benefits, such as increased risk dilution or predator confusion (Wrona & Dixon 1991; Lehtonen & Jaatinen 2016), or through active cooperation between group members, like joint vigilance or predator defence (Heg et al. 2004a; Bonte et al. 2012; Groenewoud et al. 2016). Furthermore, predation risk can favour the clustering of social units into colonies, when neighbours reduce the risk of predation, or the costs associated with anti-predator defence (Rolland, Danchin & de Fraipont 1998; Schädelin, Fischer & Wagner 2012; Jungwirth et al. 2015a). The anti-predator benefits of having larger groups, or more neighbours are ultimately expected to lead to increased survival or reproductive success (Krause & Ruxton 2002; Jungwirth & Taborsky 2015). Despite these benefits, having close neighbours also results in conflict, when groups compete over space or resources (Krause & Ruxton 2002). Group are therefore expected to invest less in such competition and cooperate more when neighbours provide benefits, such as increased defence against predators (Krams et al. 2010). Predation risk is therefore expected to play an important role in reducing conflict and promoting cooperation between individuals living in social groups, and facilitate the transition to complex sociality.

Here, we investigate whether predation risk is associated with reduced conflict both within and between groups, in the highly social, cooperatively breeding cichlid Neolamprologus pulcher. N. pulcher is endemic to Lake Tanganyika, where it occurs in highly variable habitats along the sublittoral zone between 2-45 m of depth (Konings 1998; Groenewoud et al. 2016). Groups consist of a dominant breeding pair and one to 26 subordinates (median = 5 subordinates, this study) of different sizes and sex, which jointly defend a territory that is used for both shelter and breeding (Taborsky & Limberger 1981; Taborsky 1984). Due to frequent breeder turnover, older and therefore larger subordinates are mostly unrelated to the dominants in their group (Dierkes et al. 2005). Low relatedness, larger body size and the fact that these individuals are often sexually mature, makes them a bigger threat to the dominants and increases the likelihood of conflict compared to smaller helpers that cannot reproduce and are mostly related to the breeders. However, larger helpers are also important to defend against large piscivorous predators, and previous studies have shown that they improve the survival of individuals in the group (Heg & Taborsky 2010). Subordinates in N. pulcher have been shown to provide help in order to be tolerated inside the relative safety of the territory (i.e. “pay to stay”; Gaston 1978; Bergmüller et al. 2005b). When the costs of eviction are higher, such as under elevated predation risk, this could favour subordinates to provide more help in order to prevent being evicted (Fischer et al. 2014). Previous studies have indicated that predation risk is an ecological constraint leading to the delayed dispersal of larger subordinates, and consequently, a higher number of large subordinates in groups under high risk of predation (Heg et al. 2004a; Groenewoud et al. 2016). These patterns have mainly been

90 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

explained in the context of increased costs of dispersal under elevated predation risk, but reduced aggression by dominants to incentivize larger subordinates to remain in the group has not yet been explored. On top of the benefits enjoyed by having subordinates, groups also benefit from increased anti-predator defence by having close neighbouring groups (Jungwirth & Taborsky 2015; Jungwirth et al. 2015a; Groenewoud et al. 2016). Predation risk should therefore increase the benefits of first order (i.e. groups) and second order (i.e. colonies) sociality and lead to reduced aggression at both levels of organisation.

In this study we address the following questions: (i) do (large) helpers and close neighbours provide fitness benefits under increased predation risk? (ii) Is conflict within- and between groups reduced under increased predation risk? (iii) Do large subordinates invest more in predator defence than small subordinates (i.e. is there division of labour)? (iv) Are potential reductions in conflict the result of changes in helping or submissive behaviours? Together, these results will shed light on the relative benefits of sociality for different individuals living under varying predation risk, and provide valuable insight into the role of predation risk as a factor to reduce conflict and facilitate transitions to complex societies.

METHODS

Study species and data collection We collected data on eight different populations of N. pulcher between September and De- cember 2012 and 2013 by SCUBA-diving at the southern end of Lake Tanganyika. Populations were between 150 m and 22.45 km apart, with seven populations being within 9 km of each other and one population located about 20 km away. Population boundaries were established where no other territories were found within five meters of the outermost territories of the colony, except for two very large populations where artificial boundaries were established despite other territories being close by. We randomly selected 20-24 territories from each population and determined the group size and composition: fry (<0.5 cm), juveniles (0.5-1.5 cm), small helpers (1.6-2.5 cm), medium helpers (2.6-3.5 cm), large helpers (>3.5 cm), similar to Heg et al. (2004a). Dominant males and females could be easily be distinguished from subordinates based on size and behaviour. Because not all subordinates in a group were always visible (e.g., as a result of time spent hiding or feeding in the water column) we estimated group composition repeatedly for each territory (median = 3 times, range = 1-4). We measured the distance to the nearest neighbouring territory from the centre of each focal territory to the nearest five cm and counted the total number of territories present within a two meter radius.

91 CHAPTER 5

Predation risk We estimated predation risk in each population by counting the number of piscivorous predators (mostly Lepidiolamprologus elongatus and L. attenuatus) along four transects of 10×1m2. These are highly mobile predators, usually observed alone or in small groups moving through the populations at 20-30 cm above ground looking for prey, which in the case of N. pulcher consists mainly of smaller fish or fish devoid of protection by a group. We -re peated these scans between 6 and 10 times per population on different days and different weeks to capture the variation in fish activity. For each population we estimated predation risk on adult N. pulcher by calculating the mean number of large (>10 cm) L. elongatus and L. attenuatus per transect, similar to Groenewoud et al. (2016).

Behaviours In each focal territory we observed the behaviours (sensu Taborsky & Limberger 1981; Ta- borsky 1984) of both breeders and one helper per size class (when present) for 7 minutes using a handheld computer (Psion Teklogix Workabout Pro-7527) running Noldus Pocket Observer (v3.0). We scored all aggressive behaviours (biting, ramming, mouth fighting, lateral displays, opercula spread and chasing) towards group members, neighbours and predators, and recorded the size class of the receiver. Furthermore, we recorded all territory maintenance (digging and removing debris from the territory), and submissive behaviours (bumping and tail quivers), and the time focal individuals spent inside the territory (i.e. within ca. 30 cm from the breeding shelter).

Statistical analyses Reproductive success We investigated whether the likelihood that a territory had produced offspring was dependent on the number of subordinates, territory density or predation risk in a generalised linear mixed model with a binomial error structure with a logit-link. We investigated the effects of different helper classes (i.e. large, medium and small helpers) separately, and for each helper class, we fitted five models representing different hypotheses (see Table S5.1) about the relationship between the numbers of subordinates, territory density and predation risk on whether a territory contained fry or juveniles (0/1). We included Population ID as a random effect in each model. We calculated Akaike weights and evidence ratios based on AICc values (Akaike 1973; Hurvich & Tsai 1989) to identify the model with the lowest out- of-sample deviance (Burnham & Anderson 2002; Burnham, Anderson & Huyvaert 2010). We then used this model to obtain parameter estimates for variables of interest. Parameter significance here and in all other models was obtained by likelihood ratio tests on nested models assuming a χ2-distribution (Zuur et al. 2009). In case two or more models had similar weights (i.e. were close in out-of-sample deviance), results from these models were also

92 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

investigated. All generalized linear mixed models were fitted with “lme4” in R (R Core Team 2016). Likelihood ratio tests were performed using the package “AICcmodavg” (Mazerolle 2013) and AICc values and Akaike weights were calculated using the “MuMin” package (Bar- ton 2018). All models were checked for violations of model assumptions by visual inspec- tions of residuals.

Within- and between group conflict We investigated whether the likelihood of dominant aggression towards subordinates decreased with increasing predation risk by fitting whether aggression had occurred during our 7-minute observation (0/1) as a response variable in a generalised linear mixed model with a binomial error and a logit-link. Predation risk, the helper class aggression was directed to, the number of helpers and the total time spent in the home territory by the dominants combined were included as predictor variables. For each territory, we only included dominant aggression towards helper classes that were present in the territory based on our estimates of group composition (see methods). We fitted five models representing different hypotheses about the relationship between predictors (Table S5.2), and calculated Akaike weights based on AICc, as before, to identify the model with the lowest out-of-sample deviance. Similarly, we investigated changes in within-group aggression between subordinates by fitting whether subordinates showed aggression to each other (0/1) as a response variable in a generalised linear mixed model. Predation risk, helper size class, and the total number of subordinates were fitted as predictors. We fitted five models representing different hypotheses about the relationship between predictors (Table S5.2). In both the model investigating dominant aggression and subordinate aggression, we included Territory ID as a random effect to account for repeated measures of individuals within territories.

To analyse changes in between-group aggression, we fitted whether aggression had occurred (0/1) between individuals belonging to different territories as a response variable in a generalised linear mixed model with a binomial error and a logit link. We included predation risk, territory density and individual class as predictors and fitted an additional model, which also included the interaction between predation risk and territory density. We then calculated Akaike weights based on AICc and estimated parameter significance.

Division of labour We fitted whether individuals showed either anti-predator defence behaviour or maintenance behaviour (0/1) in a generalised linear mixed model with a binomial error and logit-link. We included individual class and type of behaviour as predictors and fitted the interaction between these variables to allow for differences in the relative probability of anti-predator behaviour and maintenance behaviour between individuals belonging to dif-

93 CHAPTER 5

ferent classes. We included Population ID and Territory ID as random effects to account for differences between populations and repeated measures of individuals within territories. We used linear hypothesis tests implemented in the package “phia” (De Rosario-Martinez 2015) to obtain contrasts between behaviours for all individual classes. Similarly, we investigated differences in the proportion of anti-predator defence relative to total helping behaviour (all maintenance and defence against heterospecifics) between different helper classes. We fitted the number of aggressive behaviours towards predators as a binomial response variable where the number of trials was equal to the total number of helping behaviours, and we included Population ID and Territory ID as random effects.

Helping and submission We investigated whether total helping behaviour and submissive behaviours changed with predation risk by fitting whether an individual showed either helping or submission (0/1) as response variables in separate generalized linear mixed models with a binomial error and logit-link. We included predation risk and individual class as predictors and added Pop- ulation ID and Territory ID as random effects. Additionally, for both response variables, we fitted models including the interaction between predation risk and individual class and calculated Akaike weights, as before.

RESULTS

Reproductive success For models investigating the likelihood that a territory contained fry, there was considerable support for a model that included the interaction between the number of large helpers and predation risk (AICcweight = 0.59; Table S5.1). Likelihood ratio tests based on this model indicated that the number of large helpers had a larger positive effect on the likelihood of having reproduced with increasing predation risk (mean ± SE = 0.11 ± 0.05, χ2 = 5.27, DF = 1, P = 0.02; Fig. 5.1). There was no significant relationship between territory density and the likelihood of having reproduced in the highest ranked model (mean ± SE = 0.02 ± 0.03, χ2 = 0.36,

DF = 1, P = 0.55). However, the second ranked model (AICcweight = 0.20; Table S5.1) suggested a possible three-way interaction between predation risk, the number of large subordinates and territory density (χ2 = 3.20, DF = 1, P = 0.07).

A model that included the interaction between the number of medium helpers and territory density on the likelihood that a territory contained fry had the highest support (AICcweight = 0.51; Table S5.1). However, likelihood ratio tests indicated that the interaction between the number of medium helpers and territory density, was not significant (mean ± SE = 0.04 ±

94 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

0.02, χ2 = 3.39, DF = 1, P = 0.07). This model and the second ranked model did indicate that there was a significant negative relationship between predation risk and the likelihood that a territory had offspring (mean ± SE = -0.23 ± 0.09,χ 2 = 4.54, DF = 1, P = 0.03), but there were no effects of the number of medium helpers (mean ± SE = 0.06 ± 0.10,χ 2 = 0.34, DF = 1, P = 0.56) or territory density (mean ± SE = 0.02 ± 0.03, χ2 = 0.57, DF = 1, P = 0.45).

The number of small helpers showed a stronger positive relationship with the likelihood of having reproduced under high predation risk (mean ± SE = 0.11 ± 0.04, χ2 = 6.07, DF = 1, P = 0.01), and this was supported by AICc weights, which was 7.5 times higher than the second best ranked model (AICcweight = 0.75 vs 0.10; Table S5.1).

Within- and between group conflict For dominant aggression towards subordinates, there was highest support for a model without interactions (AICcweight = 0.48 vs 0.22 for the model including predation risk x helper class interaction) and this was supported by the lack of significance for this interaction (χ2 = 2.56, DF = 2, P = 0.28). Dominant aggression towards all helper classes decreased similarly with increasing predation (mean ± SE = -0.29 ± 0.08, χ2 = 14.54, DF = 1, P < 0.001; Fig. 5.2A), while overall levels of aggression differed between helper classes χ( 2 = 14.13, DF = 2, P < 0.001). Aggression of dominants was less likely to occur towards medium helpers and small helpers than towards large helpers (medium vs. large helpers: mean ± SE = -1.33 ± 0.41, DENS_HIGH DENS_L O

p(r) W 7 A B 7 1 6 6 DENS_HIGH 6 6 0.8 5 5 5 5 0.6 4 4 4 4 3 3 3 3 0.4 2 2 2 2 0.2 1 1

Number of large helpers 1 Number of large helpers 1 0

0 0 5 10 15 20 25 5 10 15 20 25 LH_LOW LH_CH Territory density TerritorLH_Ly densityOW LH_CH

FIGURE 5.1 Probability that a territory contained fry or juveniles (< 1.5 cm) – indicating successful reproduction – depending on the number of large helpers and territory density under (A) low predation risk, or (B) high predation risk. The legend on the right indicates colours associated with the probability of successful reproduction p(r). The closed circle and square in this legend give the mean (± SE) probability of reproduction under low and high predation risk, respectively. Violin plots show the distribution

(median, interquartile range and density) of raw data for territory density (top) and the number of large helpers (side) for low (< median) and high (> median) predation risk.

95 CHAPTER 5

Z = -3.25, DF = 1, P < 0.01; small vs. large helpers: mean ± SE = -1.08 ± 0.40, Z = -2.72, DF = 1, P < 0.01), and there were no differences between medium and small helpers (mean ± SE = -0.25 ± 0.45, Z = -0.56, DF = 1, P = 0.57). There was no significant relationship between the total time dominants spent in the territory and the likelihood they showed aggression towards subordinates (mean ± SE = 0.67 ± 0.44, χ2 = 2.86, DF = 1, P = 0.09).

Models investigating within-group aggression between helpers showed most support for a model without interactions (AICcweight = 0.55 vs 0.24 for the second best supported model; Table S5.2). Aggression between helpers decreased significantly with increasing predation risk (mean ± SE = -0.18 ± 0.06, χ2 = 10.85, DF = 1, P < 0.001; Fig. 5.2B) and there were no differences in the likelihood of showing aggression between different helper classes χ( 2 = 0.73, DF = 2, P = 0.70). The likelihood that helpers showed aggression towards other helpers increased with increasing group size (mean ± SE = 0.09 ± 0.03, χ2 = 10.96, DF = 1, P < 0.001).

The likelihood of between-group aggression became higher with increasing territory density (mean ± SE = 0.10 ± 0.02, χ2 = 20.48, DF = 1, P < 0.001), but was independent of the level of predation risk (mean ± SE = 0.01 ± 0.05, χ2 = 0.04, DF = 1, P = 0.83; Fig. 5.2C). There was limited support for an interaction between predation risk and density on between-group aggression as in indicated by low weights for the interaction model (AICcweight = 0.72 vs 0.28 for non-interaction vs interaction model, respectively). Individual classes differed significantly in the likelihood of showing aggression to neighbouring conspecifics χ( 2 = 58.09, DF = 4, P < 0.001). Dominant females had the highest likelihood of showing aggression towards

Dominant to subordinate Subordinate to subordinate Between groups 0.5 A Small helpers B C Medium helpers 0.6 0.4 Large helpers

0.3 0.4 0.2 0.2 (mean ± SE) (mean ± SE) 0.1

0.0 0.0 Probability of aggression Probability of aggression 0 2 4 6 8 0 2 4 6 8 0 2 4 6 8 Predators per transect Predators per transect Predators per transect

FIGURE 5.2 Counterfactual plots showing the relationship between predation risk and (A) dominant aggression to different classes of helpers, (B) aggression between subordinates in the same group and (C) aggression between individuals of different groups. Points in (A) represent mean probability of aggression for dominants to subordinates; slightly offset). In (B) points represent the mean probability of aggression between individuals of different groups. Solid and dashed lines are model predicted means (± SE). In (B) between-group aggression is plotted for dominant females.

96 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

neighbouring conspecifics, and this likelihood was not significantly different for dominant males (mean ± SE = -0.41 ± 0.29, Z = -1.38, DF = 1, P = 0.17), but lower for large helpers (mean ± SE = -0.94 ± 0.31, Z = -3.00, DF = 1, P < 0.01), medium helpers (mean ± SE = -1.84 ± 0.39, Z = -4.75, DF = 1, P < 0.001) and small helpers (mean ± SE = -2.62 ± 0.48, Z = -5.48, DF = 1, P < 0.001). Large helpers were more likely to show between-group aggression than small helpers (mean ± SE = 1.68 ± 0.48, Z = 3.51, DF = 1, P < 0.01), and tended to show more between-group aggression than medium helpers (mean ± SE = 0.90 ± 0.39, Z = 2.28, DF = 1, P = 0.06). The likelihood of between-group aggression did not differ between medium helpers and small helpers (mean ± SE = 0.78 ± 0.52, Z = 1.50, DF = 1, P = 0.29)

Division of labour Individual classes differed significantly in the type of behaviours performedχ ( 2 = 39.87, DF = 4, P < 0.001; Fig. 5.3A). Small helpers were more likely to show maintenance than anti-predator defence behaviours (mean ± SE = 1.86 ± 0.47, χ2 = 15.78, DF = 1, P < 0.001). This pattern shift- ed with helper classes increasing in body size having a lower likelihood of maintenance behaviours and higher likelihood of anti-predator defence (medium helper vs small helpers: mean ± SE = -1.50 ± 0.60, Z = -2.50, DF = 1, P = 0.01; large helpers vs small helper: mean ± SE = -1.72 ± 0.60, Z = -2.89, DF = 1, P < 0.001; dominant female vs small helper: mean ± SE = -2.32 ± 0.57, Z = -4.09, DF = 1, P < 0.001; dominant male vs small helper: mean ± SE = -3.65± 0.69, Z = -5.30, DF = 1, P < 0.001). Dominant males had a higher likelihood of showing anti-predator defence than maintenance (χ2 = 12.55, DF = 1, P < 0.01). Additionally, we found that the proportion of anti-predator defence relative to other (allo-) parental care behaviours increased in individual classes with increasing body size (χ2 = 39.80, DF = 4, P < 0.001; Fig. 5.3B). Small helpers showed the lowest proportion of anti-predator defence, while this proportion was higher for medium helpers (mean ± SE = 1.14 ± 0.50, Z = 2.29, DF = 1, P = 0.02), large helpers (mean ± SE = 1.66 ± 0.47, Z = 3.51, DF = 1, P < 0.001), dominant females (mean ± SE = 1.91± 0.45, Z = 4.24, DF = 1, P < 0.001) and dominant males (mean ± SE = 2.43 ± 0.47, Z = 5.22, DF = 1, P < 0.001)

Helping and submission The likelihood of showing submissive behaviours towards the dominants decreased with increasing predation risk (mean ± SE = -0.41 ± 0.17, χ2 = 5.48, DF = 1, P = 0.02; Fig. 5.4A). Small helpers had the lowest likelihood of showing submission towards the dominant breeders, and the likelihood of showing submission increased for medium helpers (mean ± SE = 1.10 ± 0.57, Z = 1.95, DF = 1, P = 0.05) and for large helpers (mean ± SE = 2.06 ± 0.59, Z = 3.47, DF = 1, P < 0.001). There was little evidence of an interaction between helper class and predation risk on the likelihood of showing submission to the dominants, as indicated by the low weight for the interaction model (AICcweight = 0.83 vs 0.17 for non-interaction vs interaction model, respectively).

97 CHAPTER 5

0.4 A Predator defence Maintenance 0.3

0.2

viour (mean ± SE) 0.1 Probability of helping beh a 0.0 133 136 150 162 152 0.4 B

0.3

0.2 tion anti−predator

viour (mean ± SE) 0.1 beh a

Propo r 0.0 SH MH LH DF DM Helper class

FIGURE 5.3 The mean probability (± SE) of (A) showing predator defence or maintenance behaviour for individuals of different status and size class (SH = small helper; MH = medium helper; LH = large helper, DF = dominant female, DM = dominant male).

In (B) is shown the mean (± SE) relative proportion of anti-predator behaviours to all helping behaviours (i.e. maintenance and defence against all predators and space competitors). Numbers in (A) represent sample sizes for each class.

0.5 A Large helpers 0.5 B Medium helpers 0.4 Small helpers 0.4

0.3 0.3

βpredation risk = -0.41 ± 0.17 * βpredation risk = -0.01 ± 0.05 0.2 0.2

0.1 0.1 Mean probability of helping

Mean probability of submission 0.0 0.0 0 2 4 6 0 2 4 6 Predators per transect Predators per transect

FIGURE 5.4 The mean probability of (A) submission towards the dominants and (B) providing help by different helper classes in relation to predation risk. Betas (β) represent overall conditional mean effect sizes (± SE) of predation risk on(A) the probability of submission and (B) the probability of helping. There were no significant interactions between helper class and predation risk for the probability of submission or helping (see results).

98 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

The likelihood of providing any kind of helping behaviour was independent of predation risk (mean ± SE = 0.005 ± 0.05, χ2 = 0.02, DF = 1, P = 0.90; Fig. 5.4B) and there were no indica- tions that the likelihood of providing help differed between helper classes χ( 2 = 3.61, DF = 1,

P = 0.17) or that there was an interaction between predation risk and helper class (AICcweight = 0.86 vs 0.14 for non-interaction and interaction model, respectively).

DISCUSSION

Social conflict can be a repellent force in the evolutionary transition to complex societies. Identifying the conditions that reduce social conflict are therefore important to understand why transitions occur in some species, but not in others (West et al. 2015). Our data show that dominants reduce aggression towards subordinates under increased risk of predation, presumably because subordinates provide fitness benefits under high predation risk. Similarly, conflict between subordinates in the same group decreased with increasing predation risk. In contrast, individuals did not reduce aggression towards close neighbours under increased predation risk, and reproductive success data indicated that the benefits of such neighbours are comparably small. Lower social conflict was not the result of subordinates increasing their helping effort, or submissive behaviours under increased predation risk.

Living with conspecifics can be beneficial, for example when this provides better access to food or protection against predators (Krause & Ruxton 2002). Such benefits can arise on multiple levels of social organisation – i.e. at the group and colony level (Jungwirth & Ta- borsky 2015). We show that that groups of N. pulcher benefit from the presence of helpers under increased risk of predation: small and large helpers increase the likelihood that a territory contains fry or juveniles, but only when predation risk was high (Fig. 5.1). Inter- estingly, there was no association between reproductive success and the number of medium-sized helpers. While smaller helpers invested most in the excavation of shelters (Fig. 5.3) that are important for other group members and provide safety for small fry (Balshine et al. 2001; Groenewoud et al. 2016), large helpers are important for defence against piscivorous predators, showing the highest levels of anti-predator defence (after the dominants; Fig. 5.3). Such defence has been shown to increase survival of other group members (Heg et al. 2004a). Increased group reproductive success and survival can be beneficial for all helper classes: related (mostly small) helpers can receive indirect benefits by raising kin and all group members can benefit from group augmentation effects (Kokko, Johnstone & Clut- ton-Brock 2001; Kingma et al. 2014) and improved group stability (Heg et al. 2005), which increases their chances of survival. Medium helpers were just as likely as large helpers to

99 CHAPTER 5

show anti-predator defence, or maintenance behaviours (Fig. 5.3), but large helpers likely play a more important role in defence against larger predators. A post-hoc investigating of our data also indicates this: both medium and large helpers rarely defended against large predators, but medium helpers were more likely to attack small than medium predators (56% vs 38% of attacked predators), while large helpers were more likely to attack medium than small predators (71% vs 24% of attacked predators). Such differences might explain why large helpers, but not medium helpers have a positive effect on reproduction under elevated risk of predation.

Territory density had no consistent effect on the likelihood that territories contained fry or juveniles. While there was some indication of a three-way interaction between predation risk, the number of large helpers, and territory density on the likelihood of a territory containing fry, evidence for such this model (based on AICc weights) was rather low. This interaction could be expected based on previous findings, which suggests that small groups have highest reproductive success under high territory density, while large groups have higher reproductive success under low territory density (Jungwirth & Taborsky 2015). Such trade-offs are likely the result of either large groups, or many neighbours providing the optimal number and density of fish that participate in anti-predator defence (Jung- wirth et al. 2015a; Groenewoud et al. 2016), but increased competition and lack of protection can be detrimental for large groups under high density, or small groups under low density, respectively. Predation risk is expected to shift this balance towards more defenders (i.e. group size and territory density) resulting in higher reproductive success. However, aggressive interactions between groups did not decrease with increasing predation risk (Fig. 5.2C). Previous studies on N. pulcher have found multiple benefits of having close neighbouring groups both for anti-predator defence and group persistence (Jungwirth & Taborsky 2015; Jungwirth et al. 2015a; Groenewoud et al. 2016), but effects on reproductive success were conditional on group size (Jungwirth & Taborsky 2015). Supposedly, the benefits of having neighbours under higher predation pressure does not provide sufficient additional benefits to select for reduced competition between neighbours. This might be because reduced competition (i) does not increase shared defence by neighbours, if such defence happens for purely selfish reasons (Jungwirth et al. 2015a) and/or (ii) any group that lowers investment in between-group competition loses resources to neighbouring groups.

Reduced conflict between individuals in groups is an important prerequisite in the transition to complex sociality (West et al. 2015). Previous findings in N. pulcher show that predation risk leads to reduced dispersal of large subordinates (Heg et al. 2004a) and higher acceptance of unrelated immigrants (Zöttl, Frommen & Taborsky 2013). Consequently, groups under high predation risk contain more large subordinates (Groenewoud et al. 2016). Our

100 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

data show that dominants are less likely to show aggression towards subordinates under elevated risk of predation, which likely facilitates such changes in dispersal and group composition and suggests that delayed dispersal by large subordinate might be (partly) driven by mutualistic benefits of cooperation (i.e. anti-predator defence) under increased threat of predation (Clutton-Brock 2002; Kingma et al. 2014). Reduced conflict between dominants and subordinates was not the result of increased levels of help or submissive behaviours that might appease dominants to show less aggression and which can be predicted by the pay-to-stay hypothesis (Gaston 1978; Quiñones et al. 2016). Our data is consistent with some reproductive skew models, which model within-group conflict and the partitioning of reproduction as a function of different social, genetic and ecological factors (Reeve, Emlen & Keller 1998; Kokko et al. 2001). In addition to enforcing help, dominant aggression can function to suppress or prevent competition for reproduction by larger subordinates (Di- erkes, Taborsky & Kohler 1999; Heg, Bender & Hamilton 2004b; Fitzpatrick et al. 2005). Low- ering levels of aggression would thus decrease the costs of group membership and relax the threshold at which subordinates would disperse, but increase the likelihood that large subordinate males engage in reproduction. One straightforward prediction from this line of reasoning would be that reproductive skew decreases (i.e. large subordinates obtain a larger share of reproduction) with increasing predation risk. Investigating conflict and levels of reproductive partitioning within groups in response to elevated predation risk could shed light on both the proximate and ultimate causes of sociality. We are currently not aware of any studies that have investigated the relationship between predation risk and reproductive skew, and of only one study that has shown reduced conflict and increased cooperation as a result of predation risk (Krams et al. 2010), or environmental harshness in general (Shen et al. 2012).

Aggression between subordinates in N. pulcher functions mainly to establish and maintain social hierarchies, and is mostly directed to group members that are close in rank (Wong & Balshine 2011). Levels of aggression are therefore expected to increase with the number of similar sized competitors and in fact our data shows that the likelihood of showing aggression increases with an increasing number of same size subordinates in the group. Howev- er, conflict is expected to be increasingly costly for individuals under increased predation risk because individuals invest less in helping behaviours which could negatively affect the fitness of other group members and group reproductive output. Furthermore, vigilance is lower during aggressive interactions, making individuals susceptible to predation (Ja- kobsson, Brick & Kullberg 1995; Hess, Fischer & Taborsky 2016). Accordingly, we show that subordinates reduce levels of within-group aggression towards each other with increasing predation risk. The consequences of reduced aggression and conflict for the resulting social hierarchy in N. pulcher is unknown, but it could mean that either hierarchies are established

101 CHAPTER 5

using lower levels of aggression or that social hierarchies are less well established in groups under high risk of predation, which will have substantial implications for life history traits such as dispersal and growth (Heg et al. 2004b; Jordan, Wong & Balshine 2010).

Predation risk has been undervalued as a driver of complex sociality. Our study suggests that predation risk is an important ecological factor selecting for reduced levels of conflict within- but not between groups as a result of increased benefits of having subordinates under high predation risk. Reduced levels of conflict are important in the transition to complex sociality (West et al. 2015). This study corroborates and provides a potential mechanism for a previous finding, which show that groups under high predation risk have higher numbers of large helpers (Groenewoud et al. 2016). However, the benefits of having additional neighbours might be too small to offset competition for valuable resources between neighbouring groups, and consequently, our data shown no reduction of conflict between neighbouring groups as a result of increased predation risk. We argue that high relatedness, which is generally associated with the evolution of cooperation and sociality, is not a necessary condition for cooperation to evolve, but that ecological factors can select for cooperation when it provides mutual benefits.

Acknowledgements We thank the Department of Fisheries, Ministry of Agriculture and Livestock of Zambia, for the permission to conduct this work; Harris Phiri, Danny Sinyinza, Taylor Banda, Lawrence Makasa and the team of the Department of Fisheries at Mpulungu for logistical help; Celes- tine and the late Augustin Mwewa and the staff at the Tanganyika Science Lodge for their hospitality, Pierpaolo Brena and Arne Jungwirth for help in data collection; and Jonas Walk- er and Isabel Keller for company in the field. This work was supported by Swiss National Science Foundation Projects 310030B_138660 and 31003A_156152 (to MT) and 31003A_144191 and 31003A_166470 (to JGF).

102 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

SUPPLEMENTARY INFORMATION

TABLE S5.1 Model comparisons for different helper size classes of models with varying relationships between reproductive success, predation risk, territory density and the number of helpers. Large helpers Model structure K AICc ΔAICc AICc weight Cumulative weight Evidence ratio Log-likelihood PR x LH + TD 6 314.29 0 0.59 0.59 -150.97 PR x LH x TD 9 316.42 2.13 0.2 0.79 3 -148.82 PR + LH + TD 5 317.46 3.16 0.12 0.91 4.9 -153.6 PR x TD + LH 6 319.37 5.07 0.05 0.96 11.8 -153.5 PR + LH x TD 6 319.46 5.17 0.04 1 14.8 -153.55

PR = Predation risk, LH = number of large helpers, TD = territory density

Medium helpers Model structure K AICc ΔAICc AICc weight Cumulative weight Evidence ratio Log-likelihood PR + MH x TD 6 321.56 0 0.51 0.51 -154.6 PR + MH + TD 5 322.85 1.28 0.27 0.78 1.9 -156.3 PR x TD + MH 6 324.88 3.31 0.1 0.88 5.1 -156.26 PR x MH + TD 6 324.95 3.38 0.09 0.98 5.7 -156.3 PR x MH x TD 9 327.71 6.15 0.02 1 25.5 -154.47

PR = Predation risk, MH = number of medium helpers, TD = territory density

Small helpers Model structure K AICc ΔAICc AICc weight Cumulative weight Evidence ratio Log-likelihood PR x SH + TD 6 310.45 0 0.75 0.75 -149.05 PR + SH + TD 5 314.42 3.97 0.1 0.85 7.5 -152.08 PR x SH x TD 9 315.23 4.78 0.07 0.92 10.7 -148.23 PR + SH x TD 6 316.1 5.65 0.04 0.96 18.8 -151.87 PR x TD + SH 6 316.5 6.05 0.04 1 18.8 -152.07

PR = Predation risk, SH = number of small helpers, TD = territory density

103 CHAPTER 5

TABLE S5.2 Model comparisons of social conflict (i.e. aggression) between dominants and subordinates, and between subordinates of the same social group.

Dominant to subordinate aggression

K AICc ΔAICc AICc weight Cumulative weight Evidence ratio Log-likelihood Model structure PR + GS + HC 7 310.52 0 0.48 0.48 -148.13 PR x HC + GS 9 312.12 1.6 0.22 0.7 2.18 -146.85 PR x GS + HC 8 312.51 1.99 0.18 0.88 2.67 -148.09 PR + GS x HC 9 313.54 3.02 0.11 0.99 4.36 -147.56 PR x GS x HC 14 317.78 7.26 0.01 1 48 -144.4 PR = Predation risk, GS = group size, HC = helper class (receiving)

Subordinate to subordinate aggression

Model structure K AICc ΔAICc AICc weight Cumulative weight Evidence ratio Log-likelihood PR + GS + HC 6 428.23 0 0.5 0.5 -208.01 PR x GS + HC 7 429.92 1.69 0.21 0.71 2.4 -207.82 PR + GS x HC 8 430.71 2.48 0.14 0.86 3.6 -207.18 PR x HC + GS 8 430.82 2.59 0.14 0.99 3.6 -207.23 PR x GS x HC 13 437 8.77 0.01 1 50 -205.05 PR = Predation risk, GS = group size, HC = helper class

104 PREDATION RISK MEDIATES THE ANTI-PREDTORBENEFITS OF SOCIALITY AND SUPPRESSES WITHIN-GROUP CONFLICT

105

Chapter 6

Experimentally induced anti-predator responses are sex specific and mediated by social and environmental factors in a cooperatively breeding passerine

Frank Groenewoud, Sjouke A. Kingma, Kat Bebbington, David S. Richardson & Jan Komdeur

Under review at Behavioral Ecology CHAPTER 6

ABSTRACT

Nest predation is a common cause of reproductive failure for many bird species, and various anti-predator defense behaviors have evolved to reduce the risk of nest predation. How- ever, trade-offs between current reproductive duties and future reproduction often limit the parent’s ability to respond to nest predation risk. Individual responses to experimentally increased nest predation risk can give insights into these underlying trade-offs. Here, we investigate the social and ecological factors that underlie these trade-offs by experimentally manipulating the risk of nest predation using taxidermic mounts in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis). Our results show that dominant females alarm called more often when they confront a nest predator model alone than when they do so with a partner, and that individuals that confront a predator together attacked more than those that did so alone. Dominant males increased their anti-predator defense by spending more time nest guarding after a presentation with a nest predator, compared to a non-predator control, but no such effect was found for females, who did not increase the time spent incubating. In contrast to incubation by females, nest guarding responses by dominant males depended on the presence of other group members and food availability. These results show that while female investment in incubation is always high and not dependent on social and ecological conditions, males have a lower initial investment, which allows them to respond to sudden changes in nest predation risk.

108 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

INTRODUCTION

Predation risk is an important factor driving changes in life-history and behavior in many animals (Barbosa & Castellanos 2005; Caro 2005; Creel & Christianson 2008). In birds, nest predation is one of the most common causes of nest failure, and is therefore one of the key drivers in the evolution of avian breeding biology (Ricklefs 1969b; Martin 1995). For example, individuals can vary nest site location or clutch size according to predation risk (e.g. Martin 1995; Eggers et al. 2006; Dillon, Conway & Skelhorn 2018), and parents might visit the nest less often when nest predation threat is high (e.g. Ghalambor & Martin 1999; Fontaine & Martin 2006; Ghalambor, Peluc & Martin 2013). If anti-predator behavior is costly then individuals experiencing different levels of nest predation risk should adjust their investment in such a behavior accordingly (Lima 2009). However, investment is often constrained by trade-offs between current and future reproduction, or because investment in the current breeding attempt, e.g. through anti-predator behaviors, precludes investment into others important activities, such as obtaining additional matings (Trivers 1972; Stearns 1989). Experimental studies are necessary to determine which conditions shape anti-predator responses, and the trade-offs underlying anti-predator responses, but such studies are scarce (Lima 2009). Here, we experimentally increased nest predation risk in a cooperatively breeding passerine to provide insights into the social and environmental factors that shape the costs of anti-predator responses on an ecological time-scale.

Increased nest attendance or vigilance is a common response to increased nest predation risk, and can improve predator detection (Montgomerie & Weatherhead 1988; Caro 2005) and nesting success (Komdeur & Kats 1999). Such behavior is also hypothesized to be costly, because individuals are unable to simultaneously invest in other activities, such as foraging (Komdeur & Kats 1999; Duncan Rastogi, Zanette & Clinchy 2006). Therefore individuals face a trade-off between investing in their current brood by increasing vigilance and reducing nest predation risk, or investing in self-maintenance and, thereby, potential future reproduction (Stearns 1989). However, the costs of increased investment in vigilance are not necessarily the same for all individuals. For instance, individuals in areas with high food availability may be better able to increase their food uptake after sustained periods of investment, and therefore suffer fewer costs of nest defense compared to individuals from lower quality areas (Duncan Rastogi et al. 2006). Similarly, the costs and benefits of increased anti-predator behavior can also differ between males and females, in species with bi-parental care (Montgomerie & Weatherhead 1988). For instance, males, who are larger in many passerine species (Ranta, Laurila & Elmberg 1994; Mills 2008), have been suggested to engage more in risky defense against predators than females, either because they are more effective and/or have lower risk of injury (Andersson & Norberg 1981). Thus, sex differences,

109 CHAPTER 6

and variation in environmental conditions, can alter the costs and benefits of anti-predator behavior, and shape the trade-offs between investment in current and future reproduction. A potentially important component of predator defense strategies is that individuals may respond differently to predators depending on the social context (Clutton‐Brock 1991). For instance, jointly confronting a predator might increase defense success or reduce injury risk (Weatherhead 1989). Therefore individuals that encounter predators alone could choose not to engage a predator, but to use more risk-averse tactics, such as alarm calls. The benefits of joint predator defense have been considered as one of the major benefits of group-living in many social bird species (Krause & Ruxton 2002). Moreover, the presence or additional investment by other individuals might also lead to changes in anti-predator behavior. For instance, the presence of subordinates in cooperatively breeding species could lead to lower investment for the breeders (i.e. load lightening; Johnstone 2011). However, similar and increased levels of investment by dominants in the presence of subordinates have also been shown (Hatchwell 1999; Valencia et al. 2006). The effects of the social environment on the expression of individual anti-predator behaviors are therefore complex and not well understood.

In the facultative cooperatively breeding Seychelles warbler (Acrocephalus sechellensis) egg predation is the primary cause of nest failure and an important aspect of fitness (Komdeur & Kats 1999). The main nest predator is the Seychelles fody (Foudia sechellarum; hereafter ‘fody’), an endemic weaver that has been observed taking eggs from unattended warbler nests (Komdeur & Kats 1999). Seychelles warblers on Cousin Island typically lay single egg clutches (91% of clutches; Komdeur 1996b; Bebbington et al. 2017), which means that a predation event in most cases renders the entire breeding attempt unsuccessful (Komdeur 1996b). Thus, nest predation is both common and costly for Seychelles warblers, and in response the species has evolved direct (attacks and alarms) and indirect (nest guarding) anti-predator behaviors (Komdeur 1991; Veen et al. 2000). Seychelles warblers are entirely insectivorous and insect availability is variable across the island (Komdeur & Daan 2005), consequently, local food availability may play an important role in modulating the expression of anti-predator behaviors.

Several social components of the Seychelles warbler system might be central in driving anti-predation behaviors. First, nest defense tactics are sex-specific: males are often observed nest guarding (showing vigilance behavior close to the nest; Slack 1976), which reduces the likelihood of nest predation (Komdeur & Kats 1999). Females rarely nest guard, but incubation (a female-only behavior) also prevents egg predation as it prevents fodies from gaining access to the egg (Komdeur 1991; Komdeur & Kats 1999). As such, it is the combined effort of males and females that determines the extent to which the nest is protected against pred-

110 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

ators. However, since nest guarding has evolved specifically to counter nest predation, this behavior should be much more flexible than modifications of incubation, which is also determined by the thermal requirements of the eggs. Second, males mostly guard the nest in the absence of incubation by the female, but there is some overlap between nest guarding and incubation, particularly at the beginning and end of female incubation bouts. Preda- tors can therefore be confronted by either the male or female alone, or cooperatively, and variation in anti-predator responses can indicate different costs of nest defense due to the social environment. Lastly, dominants can be accompanied by 0-4 subordinates (Komdeur 1991; Kingma et al. 2016a), which can help with incubation (females only) and provisioning (Komdeur 1991, 1994a). However, much less is known about the role of subordinate Sey- chelles warblers in mitigating predation risk.

Here we used an experimental approach to increase the perceived risk of egg predation in Seychelles warblers by using a mounted fody model in combination with fody audio playback to simulate an imminent threat at the nest. A similar method has been used in the past to successfully test for innate nest defense behaviors in this species (Veen et al. 2000). We then assessed the direct anti-predator responses of individuals to these mounted models (attacks and alarm calls), as well as the subsequent changes in indirect anti-predator behavior (incubation and nest guarding behavior), and compared these to a presentation with a non-predator control model. We ask three main questions: (i) Do parents increase anti-predator behaviors (nest guarding or incubation) in response to experimentally increased nest predation risk and are these responses dependent on the availability of food or parental sex? (ii) Do individuals respond differently to a direct predator threat depending on whether they confront a predator alone or together? (iii) Do helpers contribute towards nest defense, and how does helper presence affect the dominant birds’ anti-predator behavior? Our results shed light on how group members engage in different types of nest defense behaviors and how the trade-off between these behaviors are affected by social and/ or environmental contexts.

MATERIALS AND METHODS

Study population The Seychelles warbler is a small cooperatively breeding passerine endemic to several islands in the Seychelles archipelago. The main study island of Cousin (ca 29 ha; 4°19’53.6”S 55°39’43.3”E) is saturated with Seychelles warbler territories, and the population is relatively stable around 320 adult birds (Brouwer et al. 2009). The long-term monitoring effort on this population means that since 1997 nearly all birds (97%) on the island are individually

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identifiable by a unique combination of color rings and a metal ring (Hammers et al. 2015; Komdeur et al. 2016). The sex of all ringed individuals was confirmed by molecular sexing (Richardson et al. 2001). To find nests, dominant breeding females in each territory were followed for at least 15 minutes every 3-4 days. To determine the date of egg laying, we checked the nest in each territory at least every fourth day before nest completion and every other day after that.

Seychelles warblers are strictly insectivorous and take most of their prey from the underside of leaves (Komdeur 1991). Therefore territory quality can be accurately estimated in terms of the availability of their arthropod prey, according to the methods described in Komdeur (1992) and Brouwer et al. (2006). Briefly, we counted the number of arthropods on the underside of 50 leaves of all main tree species at 13 different locations, representative of each part of the island. We then estimated the cover of each of these tree species at different strata of the canopy for each territory. Arthropod counts per tree species were then multiplied by the cover of each tree species for each territory, and the resulting measure of territory quality (i.e. arthropod density) was log transformed and mean centered.

Nest predator presentation Predator presentation experiments were performed on Cousin Island between the 19th of July and the 2nd of September 2015, between 10-12 am or 2-5 pm. The Seychelles fody is currently listed as “near-threatened” on the IUCN red list (BirdLife International 2013), so we were unable to obtain a taxidermic model of this species, and instead used a mounted female house sparrow (Passer domesticus), which is very similar to the Seychelles fody in size and appearance. An earlier investigation into predator recognition in the Seychelles warbler showed no differences in anti-predator responses between a caged Seychelles fody and a caged mounted female house sparrow (Veen et al. 2000). Two different mounted house sparrows were used to increase generalizability (Johnson & Freeberg 2016). Similar to Veen et al. (2000), we used a mounted model of a barred ground dove (Geopelia striata), which occurs naturally on Cousin, as a non-predator control. Using an eight meter long fiberglass telescopic pole, we presented either a mounted house sparrow (N = 19) or a mounted barred ground dove (N = 11) approximately one meter from the Seychelles warbler nest during incubation. Practical constraints in the field meant that experiments were performed during different stages of nest incubation (mean number of days after onset of incubation = 8.9, range = 3–15 days). All but one nest treatment event were performed on different nests in different territories, but in one territory we used two different predator models on subsequent nests. Simultaneously with the presentation, we played calls of the species model used (obtained from the Xeno-canto bird sound database (www.xeno-canto.org)) on a portable mp3 player between 5-10 m from the nest. Audio playbacks were standardized by

112 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

removing background noise and repeating two call bouts every thirty seconds for the full length of the presentation using Adobe Audition CC (see supplementary information). We used different recordings for each of the two mounted house sparrow models. We recorded the number of attacks – pecking and dive bombing (i.e. rapidly flying overhead and pecking at the model in flight) – and alarm calls by the dominant male, dominant female and subordinates of either sex (when present) using a GoPro (Hero 3+) mounted on the telescopic pole, one meter from the model. We used a voice recorder, in addition to the video recordings, to record the identity and behavior of birds during the experiment. These recordings were later processed and the number of alarm calls and attacks was quantified using the software BORIS (Friard & Gamba 2016). The presentation ended 5 minutes after the arrival of the first territory group member at the nest area, visible to the observer.

Nest guarding was defined as individuals perching < 2.5 meters from the nest while no female was on the nest (Komdeur & Kats 1999). To assess whether individuals showed more nest guarding (males) or incubation behavior (females) after an encounter with the simulated nest predator, we recorded the behaviors of the group individuals for one hour both before and after the presentation of the mounted bird. During the second observation – which started five minutes after the end of the predator or control presentation – we used the same playback to simulate the continued presence of the predator or control bird in the territory. In all but two cases, observations before and after the presentation experiment were recorded by one of three different observers.

Statistical analyses Attacks and alarms Attacks towards the non-predator model (dove) were rare: in all 11 non-predator presentations, only three individuals (in three different territories) attacked the model. There- fore in the analysis of attacks, we focused on responses towards the predator model only, while alarm call analysis also included the non-predator model. We fitted either alarms, or attacks, as the response variable in separate generalized linear mixed models assuming a Poisson error. We fitted group member status (i.e. dominant male, dominant female, or subordinate) and the presentation type (fody versus dove; for alarms only) as predictors. To determine whether rates of alarm calls or attacks differed when individuals were alone or together, we also included the presence of other defenders as a binary variable. Individuals were counted as ‘arriving alone’ when they arrived at least 10 seconds before another group member. Individuals that ‘arrived together’ were either those that joined a partner that was already present, or that arrived with another individual within 10 seconds of each other. To account for the time spent either alone or together we included this variable as an offset in both models. We also analyzed whether there were differences between the two different

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predator models and we included territory ID as a random effect to account for the non-inde- pendence of observations within territories. We included incubation stage (i.e. the number of days after the onset of incubation) to account for potential differences in aggression as a result of motivational state affected by, for example, renesting potential. Following Veen et al. (2000), we only analyzed the behaviors during the first two minutes of observations for each individual after arrival.

Incubation and nest guarding responses To investigate whether individuals increased nest guarding (dominant males) or incubation (dominant females) after being confronted with a nest predator, we analyzed these behaviors separately using linear mixed models with varying intercepts for each territory. We included the interaction between presentation type (predator or non-predator) and watch type (before or after the presentation) to account for different responses between the nest predator and the non-predator control. We also analyzed the effect of arthropod density, and whether that territory had an incubating subordinate (since nest guarding by subordinates was uncommon; see results), on the incubation and nest guarding responses of dominants. We included the interactions watch type x arthropod density, and watch type x incubating subordinate present to test whether responses varied under these environmental and variables. We allowed for random intercepts between observers to account for between-observer variation.

We used an information theoretic model selection approach based on the Akaike Infor- mation Criterion (Akaike 1973) with small sample size correction (AICc; Hurvich & Tsai 1989)). We fitted full models as described above, and dropped variables if doing so led to a reduction in out-of-sample deviance (i.e. AICc) sensu Burnham and Anderson (2002), and Burnham et al. (2010), starting with higher level interactions. Variables that were of particular interest (e.g. presentation type) for inference were not removed. Variables that were removed, including interactions, were re-entered for estimation of their effects using likelihood ratio tests (LRT) on nested models assuming a χ2‑ distribution. All models were fitted using the package lme4 (Bates et al. 2014) and model selection and predictions performed with AICcmodavg (Mazerolle 2013). We used package multcomp (Hothorn et al. 2008) to test whether slope estimates contained in higher level interactions differed significantly from zero. All effect sizes given in the results section are means ± standard errors.

114 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

RESULTS

General results All dominant males (N = 28; one male died just prior to the experiment) and all dominant females (N = 29) showed nest guarding and incubation behavior respectively during the observation periods, and 27 dominant males and 26 dominant females were present during the actual model presentation. Of the eight subordinates seen during either stage of the experiment, three displayed both attacks/alarms and incubation behavior (all females), two showed alarms or attacks but no incubation or nest guarding, two showed nest guarding or incubation but no nest defense, and one individual did not contribute in any way (this latter individual was harassed by the dominants when he tried to participate in nest defense). Interestingly, the five subordinates that participated in direct defense (i.e. attacks or alarms) always arrived after the dominant breeding female or dominant breeding male: therefore differences in attack or alarm rates depending on whether these subordinates confronted the model presentation together or alone could not be estimated. Of the total time spent in either incubation or nest guarding, dominant females spent most of their time incubating (97.0%), while dominant males almost exclusively nest-guarded (99.2%) and subordinates (four females) showed a mixed investment (82.4% incubation and 17.6% nest guarding). One subordinate male nest guarded for 84 seconds, but showed no direct anti-predator behaviors.

Alarm calls and attacks in response to model presentation Dominant females alarm called more than breeding males (mean ± SE = -1.01 ± 0.09, z = -10.51, DF = 1, p < 0.001, Fig. 6.1A) and subordinates (-1.04 ± 0.17, z = -6.07, DF = 1, p < 0.001, Fig. 6.1A), but there was no difference in alarm calling rate between dominant males and subordinates (-0.03 ± 0.18, z = -0.16, DF = 1, p = 0.99, Fig. 6.1A). Individuals alarm called less when they confronted the mounted model together than when they were alone (-0.36 ± 0.13, χ2 = 7.97, DF = 1, p = 0.005, Fig. 6.1A), and this effect was stronger for dominant females than for dominant males (interaction effect: 0.82 ± 0.31,χ 2 = 7.18, DF = 1, p = 0.005, Fig. 6.1A). Individ- uals tended to alarm more during the predator presentation than during the non-predator presentation, but this effect was not significant (0.84 ± 0.49, χ2 = -3.02, p = 0.08, DF = 1, Fig. 6.1A), and there were no differences between the two predator models used (-0.07 ± 0.56,χ 2 = 0.12, DF = 1, p = 0.90). The number of alarms was independent of incubation stage (-0.08 ± 0.05, χ2 = 2.16, DF = 1, p = 0.14).

There was no difference in the number of attacks by the dominant females, dominant males or subordinates (χ2 = 0.45, DF = 2, p = 0.80). Individuals attacked the predator model more often when they were together than when they were alone (0.78 ± 0.27, χ2 = 9.33, DF = 1, p <

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0.01, Fig. 6.1B), but this did not differ between dominant females and dominant males (0.42 ± 0.83, χ2 = 0.51, DF = 1, p = 0.61). Individuals tended to attack one of the predator models more than the other, but this effect was not significant (1.59 ± 1.04,χ 2 = 2.83, DF = 1, p = 0.09). Individuals attacked the predator model less if the eggs had been incubated for more days (-0.29 ± 0.10, χ2 = 8.23, DF = 1, p < 0.01).

Nest guarding and incubation responses to increased nest predation risk Nest guarding Dominant males increased their nest guarding duration significantly after the nest predator presentation (0.21 ± 0.04, z = 5.47, p < 0.001), while males nest guarded less after the non-predator presentation (-0.09 ± 0.04, z = -2.03, p = 0.04). Consequently, dominant males increased their time spent nest guarding (i.e. the slope between before and after the model presentation) more after a nest predator presentation than after a non-predator presentation (0.29 ± 0.06, χ2 = 19.79, DF = 1, p < 0.001; Fig. 6.2). Although the number of territories with incubating subordinates was low (n = 4), dominant males had a significantly smaller nest-guarding response when there was an incubating subordinate present in the territory (-0.22 ± 0.09, χ2 = 5.97, DF = 1, p = 0.02; Fig. 6.3A). Consistent with previous results (Komdeur & Kats 1999), nest guarding by dominant males before the predator presentation increased with arthropod density, but was independent of arthropod density after the presentation (-0.07 ± 0.03, χ2 = 5.21, DF = 1, p = 0.02; Fig. 6.3B).

15 A Non-predator Predator 2.0 B Predator

Alone Together 1.5 10

1.0

5 0.5

Number of alarms (mean ± SE) 0 Number of attacks (mean ± SE) 0.0 DF DM SUB DF DM SUB DF DM SUB

FIGURE 6.1 The mean model predicted (± SE) number of alarm calls (A), and the number of attacks (B) per minute for Seychelles warblers when they were alone (open circles) or together (filled circles) during an experimental presentation of a nest predator (N

= 19) or non-predator (N = 11). Individuals arrived alone when they were present at least 10 seconds before the arrival of another bird. DF = dominant female, DM = dominant male, SUB = subordinate.

116 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

60 Incubation by breeding female ) Nest guarding by breeding male -1 50

40 ns 30

20 *** 10 Nestguarding/incubating (mean ± SE min hour 0 Before After Before After Predator Non predator

FIGURE 6.2 Time spent nest guarding or incubating by Seychelles warbler dominant males (blue circles) and dominant females

(red triangles), respectively, before and after a nest predator (N = 19) or non-predator (N = 11) presentation. Thick lines represent mean predicted responses with standard errors, while thin lines show individual responses. Significance indicators (*** = P <

0.001, NS = not significant) relate to the hypothesis that slopes differ from each other.

25 40 A B Before nest predator ) ) -1 without subordinate After nest predator -1 20 with subordinate 30

15 20

10 p = 0.02 10 5

(mean ± SE min hour p = 0.02

0 Time spent nest guarding (mean ± SE min hour Time spent nest guarding 0 Before After −1.5 −1.0 −0.5 0.0 0.5 1.0 1.5 Arthropod density (centered)

FIGURE 6.3 Changes in time spent nest guarding by dominant male Seychelles warblers as a result of an experimental presentation with a nest predator in relation to (A) having an incubating subordinate present in the territory (N = 4) or not (N = 15), and (B) territory food availability (i.e. centered log arthropod density). P-values relate to the hypothesis that slopes differ from each other.

Incubation In contrast to male nest guarding behavior, there was no difference in female incubation duration after presentation of a nest predator or non-predator control (-0.02 ± 0.06, χ2 = 0.14, DF = 1, p = 0.71; Fig. 6.2), and dominant females did not increase their incubation dura-

117 CHAPTER 6

tion after either the predator (0.02 ± 0.03, z = 0.58, DF = 1, p = 0.56; Fig. 6.2), or the non-predator presentation (0.04 ± 0.05, z = 0.89, DF = 1, p = 0.37; Fig. 6.2). There was some evidence that dominant females showed less incubation behavior overall when there was an incubating subordinate present in the territory (-0.11 ± 0.06, χ2 = 2.96, DF = 1, p = 0.09), but incubation responses to the model presentation were not dependent on whether there was an incubating subordinate present (interaction effect: 0.06 ± 0.10,χ 2 = 0.51, DF = 1, p = 0.48). Female incubation responses were slightly higher in territories with higher arthropod density, but this was not significant (0.06 ± 0.03,χ 2 = 3.24, DF = 1, p = 0.07). There was a small negative relationship between arthropod density and incubation duration before the model presentations (-0.11 ± 0.06, z = -2.00, DF = 1, p = 0.05), but there was no relationship between arthropod density and the duration of incubation after the model presentations (0.10 ± 0.06, z = 1.60, DF = 1, p = 0.11).

DISCUSSION

Being able to accurately assess and respond to nest predation risk is important when nest predation risk varies and anti-predator response are costly. Our results show that males increase the time spent guarding the nest – which is an effective way of reducing egg predation in natural conditions (Komdeur & Kats 1999) – after we experimentally increased the perceived risk of nest predation (Fig. 6.2). In contrast to males, females showed no change in incubation duration after being presented with a nest predator. Male nest guarding responses were lower in territories with high food availability – because males in such territories already showed high levels of nest guarding – and with subordinates present (Fig. 6.3A, B), but female incubation duration did not depend on these factors. The number of alarm calls towards the nest predator and non-predator model did not differ significantly, but physical attacks towards the non-predator model were rare, in contrast to attacks towards the predator model. This suggests that our predator model was perceived as a bigger threat than our non-predator control model (Fig. 6.1A, B) as shown before (Veen et al. 2000). Breeders showed more attacks when they confronted the nest predator together than when either of them did so alone, which suggests benefits of joint defense for Seychelles warbler parents. We discuss our results further below.

Direct anti-predator responses: alarm calls and attacks Individuals attacked more when presented with the nest predator model than the non-predator control (Fig. 6.1). No strong effect was found for alarm calls, but alarm calls were more common and occurred at higher rates than attacks. This could indicate that attacks are more costly in terms of energy expenditure, or potential injury risk, although injuries have

118 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

never been recorded as a result of nest defense against Seychelles fodies (F.G., J.K., S.A.K. D.S.R., personal observations). In contrast to Veen et al. (2000), who found that males had higher attack rates than females, we found no such differences, but we did find that females alarm called more than males overall. Subordinates did not always participate in nest defense, neither by direct defense (alarms and attacks) towards a predator, nor by incubation or nest guarding. It is possible that subordinate nest defense strategies may be conditional (e.g. perhaps based on relatedness or body condition as observed for provisioning in this species; Richardson et al. 2003b; van de Crommenacker, Komdeur & Richardson 2011) as they are less consistent than that of the breeders. This is further illustrated by the fact that even when subordinates participated in nest predator defense, they always arrived after the dominant female or dominant male. However, when they did participate in defense, they alarm called as often as dominant males, and attack rates were similar to dominant males and females (Fig. 6.1B).

In species where more than one individual provides parental care, individuals might alter their anti-predator responses depending on the social context (Chase 1980; Clutton‐Brock 1991). Interestingly, Seychelles warblers attack a nest predator model more often when they are together than when they are alone (Fig. 6.1B). Similar patterns have been found in other species, e.g. great tits Parus major (Regelmann and Curio 1986). It is likely that (i) individuals are more likely to attack together because of the benefits of additional vigilance by others. This argument is supported by our own observations, where group members would take turns in attacking the nest predator, and one individual would remain at a distance and usually alarm call (FG, personal observations). Alternatively, (ii) individuals might be signaling a willingness to invest in the current brood in the hope that their partner will also increase investment (Johnstone & Hinde 2006; Johnstone et al. 2013). Dominant females alarm called more when they were alone than when they were together, but no such effect was present for dominant males, who also showed fewer alarm calls than females overall. That individuals alarm call more when they are alone is consistent with at least two functions that have been ascribed to alarm calls in other species: (i) when alarm calls function to signal to the predator that it has been seen, but attacking alone is too risky, and (ii) to signal the presence of a threat to other group members (Caro 2005). The additional function of trying to attract other group members might thus explain the increased alarm rate of dominant females when they confronted the model alone. Interestingly, dominant males showed no differences in alarm rates depending on whether they confronted the model presentation together or alone. Dominant males generally alarm called less than females and did not compensate for this by showing more attacks than dominant females. Our results therefore suggest that Seychelles warbler breeders (females) show more risk-averse anti-predator behaviors when they are alone, switching to more direct aggression when they

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confront a nest predator when they have social support. Surprisingly, we found that attacks towards the nest predator model decreased when eggs had been incubated for more days, which is counter to the general hypothesis that nest defense should increase with increased reproductive value of the clutch or reduced nesting potential (Montgomerie & Weather- head 1988). However, results for this hypothesis have been mixed, with some species showing no change in nest defense behavior as the brood ages, and others showing decreased investment, similar to our results (reviewed in Caro 2005). One possible explanation for the decline of anti-predator responses with incubation stage, in our study and elsewhere, is a decrease in parental body condition as the brood ages due to high investment in incubation and nest guarding.

Indirect anti-predator responses: incubation and nest guarding Dominant males increased their nest guarding behavior in response to our nest predator presentations and playback, but no such response was found in terms of incubation behavior in dominant females. The lack of response in females is likely the result of the higher overall female investment and the trade-off between incubation and time spent foraging (Reid et al. 2002; Tinbergen & Williams 2002). On average females incubate ca 50% of their time, while males do not incubate and only spent 17% of their time on nest guarding (only pre-experiment nest watches), leaving males with more opportunity to respond to the increased threat, compared to females. Additionally, females are often on strict incubation schedules to create the optimal conditions for proper embryonic development, which should further limit females’ ability to respond to increased nest predation risk (Deeming & Reynolds 2015). Although we only conducted our experiment in four territories with incubating subordinates, our results suggest that males can also benefit from the presence of incubating subordinates: males without incubating subordinates showed a much stronger response after the simulated nest predation threat, while such an effect was smaller and not significant for females (Fig. 6.3A). Load-lightening is a common benefit of subordinate help, and observed in many cooperative breeders (e.g. Hatchwell 1999), including the Sey- chelles warbler (Komdeur 1994a), Our results suggest that load lightening can be exacerbat- ed under increased nest predation risk. Although we are currently unaware of any survival benefits due to load-lightening for Seychelles warbler males, it is possible that such effects only become apparent when the magnitude of nest predation risk is taken into account (Brouwer et al. 2006). Additionally, the reduced time investment by males could allow them to pursue extra-pair matings, as is the case in the superb fairy-wren Malurus cyaneus (Green et al. 1995); this is plausible in the Seychelles warbler, where extra-pair mating is common (Richardson et al. 2001).

Nest guarding responses by dominant males were also dependent on arthropod density:

120 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

time spent nest guarding in high quality territories was already high and did not change much as a result of our model presentations, while dominant males in low quality territories showed a significant increase in nest guarding (Fig. 6.3B). This result is in line with a previous study in the Seychelles warbler that showed a similar correlation between male nest guarding investment and territory quality (Komdeur & Kats 1999). Our results thus indicate that male nest guarding behavior can be temporally increased when the risk of nest predation is high, but that the trade-off between nest guarding and other activities prohib- its dominant males from keeping up such high levels of close nest guarding over a longer period of time (Komdeur & Kats 1999). Interestingly, where the latter study found no relationship between territory quality and female incubation, we found that dominant females tended to show a decrease in incubation duration with increasing territory quality, which was similar in strength to the increase in nest guarding behavior for dominant males. This suggests that at least part of female incubation behavior is compensatory and functions to reduce nest predation risk, but male removal experiments would be necessary to show this conclusively. The main difference between Komdeur and Kats (1999) and this study is that their measure of territory quality included territory size (i.e. is a measure of total arthropod abundance), while our study did not (i.e. measures arthropod density). The latter could be a better reflection of female foraging efficiency during incubation off bouts and, therefore, of the trade-off between incubation and territory quality.

Conclusion Our results show differential responses to short-term increased nest predation risk between different group members in the cooperatively breeding Seychelles warbler. In our study, we have addressed both direct responses to predators and changes in breeding and vigilance behavior, before and after a simulated nest predation threat. This study differs from previous investigations, that have looked primarily at alterations to incubation and feeding behaviors, by investigating nest guarding, a form of vigilance that has evolved specifically to reduce the risk of nest predation (Komdeur & Kats 1999). We show that direct responses by dominant males and females to nest predators in the Seychelles warbler differ depending on whether the threat is confronted together or not. Furthermore, only dominant males respond to simulated nest predation risk by increasing vigilance, while females show no such response in time spent incubating. We highlight the fact that male vigilance is likely much more flexible perhaps because, (i) it is unconstrained by thermal requirements to the egg(s) and (ii) the initial investment is much lower, leaving more opportunity for males to respond to increased risk. This is further illustrated by the finding that male nest guarding behavior is conditional on arthropod density and on subordinate help, suggesting that this behavior is costly, and that these costs can be alleviated under favorable food and social conditions. Together, these results show that anti-predator behavior can differ substantially

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according to individual, social, and environmental conditions.

Acknowledgements We thank Nature Seychelles, the Seychelles Bureau of Standards and the Department of En- vironment for making our fieldwork on Cousin Island possible, and we particularly thank Megan Pendred for help during fieldwork. We thank Alex Jansen, Moisès Sánchez-Fortún and Julia Schroeder for providing the taxidermic mounts. This research was supported by Netherlands Organisation for Scientific Research (NWO) TOP grant (854.11.003) and ALW grant (823.01.014) in the name of JK. SAK was supported by an NWO Veni fellowship (863.13.017) and KB by a Natural Environment Research Council (NERC) Ph.D. studentship. DSR was supported by a NERC grant (NE/K005502/1).

122 EXPERIMENTALLY INDUCED ANTI-PREDATOR RESPONSES ARE MEDIATED BY SOCIAL AND ENVIRONMENTAL FACTORS

123

Box A

Anti-predator benefits drive communal breeding in the Seychelles warbler

Sjouke A. Kingma, Kathryn L. Bebbington, Martijn Hammers, Frank Groenewoud, Hannah Dugdale, Marco van der Velde, Michael Taborsky, Terry Burke, Franz J. Weissing, David S. Richardson, Jan Komdeur BOX A

ANTI-PREDATOR BENEFITS DRIVE COMMUNAL BREEDING IN THE SEYCHELLES WARBLER

Mutualistic benefits, like enhanced access to food and protection against predators, are generally believed to promote group living, and can ultimately facilitate communal breeding (Krause & Ruxton 2002; Clutton-Brock 2009). Concession models (or transactional models; Reeve et al. 1998) of reproductive skew predict that dominants may grant subordinates access to reproduction if this provides a net benefit to the fitness of dominants. These reproductive concessions may persuade subordinates to stay and cooperate when they would otherwise leave or withhold help (Johnstone 2000). In the Seychelles warbler (hereafter ‘SW’), an individual can stay as a subordinate in a stable territorial group for years (Kom- deur 1992; Kingma et al. 2016a). Subordinate males sometimes stay and provision offspring, but only subordinate females participate in incubation. The main egg predator of the Sey- chelles warbler is the endemic Seychelles fody Foudia sechellarum, (hereafter ‘fody’). These small passerines approach unattended Seychelles warbler nests, rapidly toss the eggs onto the floor (within 4-17 seconds; Komdeur & Kats 1999) and consume them. Since the majority of nests contain only one egg (Komdeur 1991; Bebbington et al. 2017), predation normally results in the loss of the entire brood. Our data show that helpers substantially increase the percentage of time for which eggs are incubated (nest incubation attendance with helper: 71.0 ± 1.9% of time (n = 88) vs. no helper: 50.0 ± 0.8% (n = 301); t = 12.1, P < 0.0001; irrespective of food abundance: β = 0.009 ± 0.025, t = 0.355, P = 0.72). Fodies have a greater opportunity to predate nests with a single incubating female because these nests are unattended for longer periods than nests with multiple incubating females (time between incubation bouts; 7.2 min vs. 2.4 min). Consequently, hatching success decreased with increasing predation risk (assessed as the number of fodies) in territories without subordinates (β ± SE = -0.175 ± 0.075, Z = -2.339, P = 0.019), but was unaffected by predation risk in territories with additional subordinates (β ± SE = 0.159 ± 0.117, Z = 1.361, P = 0.173, Fig. A.1). Although having helpers may improve the dominant pair’s breeding success, they also impose costs in Seychelles warblers; adult survival decreases as a result of additional group members due to increased competition over food (Brouwer et al. 2006). Therefore, this system provides an ideal situation in which to test if females provide reproductive concessions in exchange for help, when the need for help (i.e. predation risk) is high.

We compared this plasticity in subordinate reproduction with natural variation in nest predation pressure – and hence in the benefits dominants gain from subordinate help – to test whether reproductive concessions can explain communal breeding. Our data show that subordinate females in territories with high predation risk (i.e. when subordinates provide a direct benefit to dominants) were substantially more likely to reproduce (Fig. A.2).

126 ANTI=PREDATOR BENEFITS DRIVE COMMUNAL BREEDING IN THE SEYCHELLES WARBLER

1.0 c he s t

u 0.8 c l

0.6 c hed

ha t 0.4 on i 0.2 without subordinates with female subordinate 0.0 Pr opo r t 0 1 2 3 4 5 6 7 8 9 10

Number of fodies in territory

FIGURE A.1. The effect of predator density (number of Seychelles fodies in the territory) and the presence of a subordinate female on hatching success in Seychelles warbler nesting attempts. Hatching success is lower in territories where more egg predators are present (black line; n = 385 clutches), but the presence of subordinate females (who help protect the clutch by incubation) mitigate this effect (red line; n = 146 clutches). Solid and dashed lines respectively reflect model predicted means and standard errors.

1.0 e g na t

i 0.8

0.6 s ubo r d r ep odu c i n s

on 0.4 i e l

m a 0.2 e f Pr opo r t 0.0 0 1 2 3 4 5 6 7 8 9 10

Number of fodies in territory

FIGURE A.2. Subordinate female Seychelles warblers are more likely to reproduce if the risk of egg predation is higher.

The solid and dashed lines respectively reflect model predicted means and standard errors from a logistic regression controlling for food abundance.

Importantly, the likelihood of subordinate reproduction was not related to food abundance (β ± SE = -0.011 ± 1.202, Z = -0.009, P = 0.993). Unlike subordinate females who did not reproduce, reproducing subordinates always incubated (see Richardson et al. 2002; in this study 100% of 10 individuals vs 50% of 10 non-reproducing individuals; Fisher exact test: P = 0.033; Fig. A.3) and, given they were still alive, they always stayed in the territory until the next breeding season (100% of 11 reproducing individuals vs. 67% of 12 non-reproducing stayed; P = 0.09). Thus, as female subordinates are more likely to reproduce in areas with a higher number of fodies (Fig. A.2), territories with more fodies were also considerably more likely

127 BOX A

to have two females incubating (β ± SE = 0.613 ± 0.135, Z = 4.525, P < 0.001). This was both the result of subordinates in territories with more fodies being substantially more likely to incubate (β ± SE = 0.588 ± 0.236, Z = 2.497, P = 0.013; Fig. A.3) and territories with more fodies being more likely to have a female subordinate in the first place β( ± SE = 0.383 ± 0.110, Z = 3.488, P < 0.001).

Studies of the mechanisms underlying communal breeding are often fraught with alternative explanations and potential confounds (Clutton‐Brock 1998). Kin-selection theory predicts that subordinates help if this improves the reproductive success of related dominants (Hamilton 1963), and that subordinates are more likely to stay in groups if they are related to dominants (i.e. nepotism; Kingma et al. 2016a). However, in our study, adult subordinate females were normally unrelated to one or both dominant individuals (73% of individuals). Therefore, the subordinate female’s presence and helping behaviour cannot be explained simply by kin-selected benefits or nepotism. However, concession models of reproductive skew predict that reproduction is more likely to be conceded to unrelated than to related subordinates (Johnstone 2000; Reeve 2000). If subordinate-dominant relatedness decreases with increasing predation risk as a result of e.g. differential dispersal decisions and/or breeder turn-over, than reproductive concessions might be explained by changes in relatedness. Previous studies have further indicated that reproductive success increases with age in the SW, with peak reproduction around 6 or 7 years of age (Komdeur 1995; Ham- mers et al. 2012). Subordinates that initially delay dispersal often stay to co-breed with the dominant female for several years, and increased reproduction by subordinates could thus be the consequence of increasing subordinate age. To conclusively show that reproductive concessions are the result of increased predation risk and not the consequences of age or relatedness, such effects should be taken into account.

1.0

e A g

n na t

i 0.8 i d r ba t o u b 0.6 1.0 c B u 0.8 n

s i

0.6

n s 0.4 o e 0.4 l

a rt i 0.2

m 0.2 0.0 e yes no op o f

r Subordinate reproduced?

P 0.0 0 1 2 3 4 5 6 7 8 9 10 Number of fodies in territory

FIGURE A.3 Egg predation risk promotes cooperation in Seychelles warblers.

When there are more fodies in the territory, (A) adult subordinate females are more likely help (n = 136), and (B) subordinates are almost twice as likely to help if they have reproduced. Solid and dashed lines, respectively, reflect model predicted means and standard errors.

128 ANTI=PREDATOR BENEFITS DRIVE COMMUNAL BREEDING IN THE SEYCHELLES WARBLER

Social species differ greatly regarding the mechanisms underlying cooperative breeding and the level of conflict over reproduction, ranging from no obvious conflict (this study) to infanticide (as e.g. in meerkats; Clutton-Brock, Hodge & Flower 2008). We argue that the answer to this diversity may lie in the different types of benefit (i.e., survival vs. reproduction) accruing to subordinates and dominants. Reproductive conflict is expected to be greatest in species where group formation occurs due to inherent benefits of group living, but where per capita reproduction decreases with increasing group size (i.e. resource defence benefits in Shenet al. 2017). However, in species where there are no direct benefits of being in a larger group, but per capita reproductive success increases due to mutualistic benefits (i.e. collective action benefits in Shen et al. 2017) conflict over reproduction should be small or absent. In line with this, previous studies have concluded that dominant warblers can evict subordinates from the territory (Eikenaar et al. 2007; Kingma et al. 2016a; Groenewoud et al. 2018), but that conflict over reproduction is limited (Komdeur 1991). However, in other species where there are clear benefits of group-living, such as meerkats (Clutton-Brock et al. 1999), but where per capita reproduction decreases in larger groups, reproductive conflict is rife, and the inability of dominants to fully control subordinate reproduction often leads to the occurrence of infanticide and egg destruction. Thus, overall, our results show that once groups are established, the mutual benefits of improved nest protection can explain cooperation and communal breeding as a peaceful transaction between group members, with few incentives for cheating and reproductive conflict.

129

Chapter 7

Synthesis CHAPTER 7

In this thesis, I have addressed the environmental factors affecting the formation of groups, the benefits of helping by subordinates and group stability in cooperatively breeding Sey- chelles warblers and Neolamprologus pulcher. In the Seychelles warbler, most studies had focused on the impact of differences in territory quality on delayed dispersal and the benefits of helping by subordinates, but temporal variation in food availability (chapter 3) and predation risk (chapters 6 and box A) had not yet been recognized as drivers of sociality in this species. In N. pulcher, experimental studies had shown changes in helping behavior and dispersal as a result of manipulated predation risk, but consequences of natural variation in predation risk between populations (chapter 2) and the implications for within-group conflict (chapter 5) were unknown. I will discuss these and other findings in relation to ecological drivers of cooperative breeding, further below.

DELAYED DISPERSAL

The evolution of cooperative breeding can be approached as a two-step process where group formation is a necessary, but not a sufficient, first step enabling individuals to jointly raise offspring. In many cases, these additional caregivers will be offspring from previous breeding attempts that have delayed dispersal, but other routes to group formation and cooperative breeding are also possible (see chapter 4; Riehl 2013). It has been suggested that help by unrelated subordinates is of a secondary nature – i.e. help by unrelated individuals only became possible after direct benefits became available for related subordinates that initially provided care for kin (Cockburn 2013). Several lines of evidence, such as phyloge- netic analyses (Cornwallis et al. 2010; Lukas & Clutton-Brock 2012) and the prevalence of family vs non-family groups (Riehl 2013), seem to point in the direction that this was in fact the evolutionary route to cooperative breeding for the majority of species. In this view, direct benefits of helping have played a lesser role during the initial evolution of family living, in the same way as they might do now in determining the benefits of delayed dispersal for subordinates (Drobniak et al. 2015; Griesser et al. 2017). I would add two exceptions to this scenario, for cases where unrelated subordinates either (i) provide and obtain direct (passive) grouping benefits, such as through group augmentation (Kokko et al. 2001; King- ma et al. 2014), or (ii) where helping behaviour is not strictly “altruistic”, such as territory defense or other behaviours, which are partly self-serving (e.g. Tanaka, Frommen & Kohda 2018). In these cases, it is easier to envision a situation where group formation by unrelated individuals, without evolved helping behaviours in place, is likely to occur. Nonetheless, in many cases, it seems that the factors that are currently maintaining group formation and cooperative breeding are not the same as those responsible for its initial evolution. Thus, it seems justified for researchers interested in the evolution of cooperative breeding, to inves-

132 SYNTHESIS

tigate the factors leading to delayed dispersal, that are independent from the benefits that individuals can obtain by helping.

The evolution of delayed dispersal has been attributed mainly to combinations of habitat saturation and benefits the can be obtained by remaining in the natal territory (Emlen 1982, 1994; Stacey & Ligon 1991). Most studies investigating delayed dispersal in cooperative breeders have focused on stable environments, where habitat saturation creates a shortage of breeding opportunities, and where spatial variation in territory quality generates the conditions necessary for offspring to benefit by delaying dispersal and foregoing independent breeding (Emlen 1982; Koenig et al. 1992; Komdeur 1992). However, recent studies show that cooperative breeding in mammals (Lukas & Clutton-Brock 2017) and birds (Rubenstein & Lovette 2007) is more prevalent, rather than less, in areas with high temporal variability. The extent to which this pattern is due to changes in delayed dispersal and the propensity to form family groups (i.e. “hard life” hypothesis; Koenig et al. 2011; Griesser et al. 2017), or to changes in the benefits of helping behaviour by subordinates (i.e. “bet-hedging” or “temporal variability” hypothesis; Rubenstein 2011; Shen et al. 2017), is unclear. In chapter 2, I show that in the Seychelles warbler, delayed dispersal and group formation is associated with spatial and temporal variation in food availability. Offspring are more likely to disperse from their natal group at one-year of age when food availability – and therefore the conditions for dispersal and independent breeding – is favorable, and the benefits of remaining as a subordinate in the natal territory are perhaps less important. Increased levels of dispersal and breeding as a result of improved conditions have also been found in other cooperative breeders, such as azure winged magpies Cyanopica cyanus (Canario et al. 2004), acorn woodpeckers Melanerpes formicivorus ( Koenig & Walters 2011) and experimentally in sociable weavers Philetairus socius (Covas et al. 2004). However, the extent to which the relationship between decreased dispersal and adverse ecological conditions is due to increased costs of dispersal (and breeding alone), or increased benefits of natal philopatry and breeding together (i.e. cooperative breeding arises through mutualistic benefits) is mostly unknown. Chapter 3 and box A suggest that, in the Seychelles warbler, reduced dispersal is both the consequence of increased costs of dispersal due to low food availability and the benefits that females can obtain by breeding together under high risk of predation.

Predation risk has received very little attention as a driver of complex sociality and cooperative breeding. However, this view neglects potentially important effects of predation risk on the costs of dispersal, the survival benefits of group living and the benefits of cooperation for reproductive success, which could all play a role in delayed dispersal. In N. pulcher, large subordinates are sexually mature and can potentially disperse to vacant habitat, which is plentiful at colony borders, to breed. However, an earlier study has shown experimental-

133 CHAPTER 7

ly, that individuals do not always disperse to such areas and that this is due to predation risk acting as an ecological constraint preventing dispersal (Heg et al. 2004a). In chapter 1, I show the consequences of natural variation in predation risk between different populations of N. pulcher on group composition and behaviour, which corroborates this earlier experimental study and further shows the importance of predation risk for the evolution of sociality in this system. Predation risk is also thought to play an important role in the Seychelles warbler, as egg predation by the endemic Seychelles fody Foudia sechellarum is the main cause of nest failure (Komdeur & Kats 1999). In chapter 6, I show experimentally that Seychelles warblers have evolved effective behavioural strategies to prevent egg predation by fodies, and that particularly dominant males are responsive to changes in predation risk. However, egg predation by fodies only occurs when nests are unprotected, and given that subordinate females participate in incubation, this too can be an effective strategy to reduce egg predation. In box A, I present a study into the effect of predation risk as a driver of delayed dispersal and cooperative breeding in the Seychelles warbler.

THE BENEFITS OF BREEDING TOGETHER

Limited dispersal and kin selection – i.e. selection on genes through its effects on others carrying the same gene (Hamilton 1963) – has been the predominant explanation of altruistic helping behaviour in cooperative breeding species (West-Eberhard 1975; Cockburn 1998; Foster et al. 2006). One of the appealing characteristics of this scenario, is that such selection is the automatic consequence of limited dispersal (due to e.g. ecological constraints) leading to kin neighbourhoods (but see Platt & Bever 2009). The importance of kin selection for the evolution of helping behaviour in cooperative breeders has been well documented, both between (e.g. Hughes et al. 2008; Cornwallis et al. 2010; Briga et al. 2012) and within (e.g. Emlen & Wrege 1989; Komdeur 1994b; Wright et al. 2010) species. Despite this observation, cooperation between unrelated individuals in common, and some argue that the direct benefits to subordinates in cooperative breeding species are sufficient to maintain cooperation and that indirect benefits have been overestimated (Clutton-Brock 2002; Riehl 2013). Direct benefits of cooperation can be obtained by various means such as when cooperation boosts group reproductive success and there are benefits to being in a larger group (i.e. group augmentation; Kokko et al. 2001), or when cooperation improves the reproductive success of all group members (i.e. mutualism; Clutton-Brock et al. 2001). However, environmental conditions can alter or even generate the potential of individuals to obtain direct and indirect fitness benefits through cooperative breeding, when group-living or cooperation functions to overcome some ecological or environmental obstacle (e.g. harsh abiotic conditions or high predation risk). Quantifying the costs and benefits of co-

134 SYNTHESIS

operation in relationship to such conditions is thus important to explain the evolution and maintenance of cooperative breeding.

In chapter 3 and 4, I show that there are mutualistic benefits of helping and co-breeding in the Seychelles warbler. In chapter 3, I show that per capita reproduction does not decrease in groups with female subordinates compared to Seychelles warblers that breed in pairs, which means, at least for female subordinates, cooperative breeding is not necessarily costly in terms of reproductive output. The exact reproductive benefits for subordinate females living in groups will depend on the level of reproductive sharing and within-group relatedness (b and r in Hamilton’s rule; Hamilton 1963). Furthermore, groups that contain female subordinates have lower fecundity variance, indicating more consistent reproduction, which can be an important aspect of fitness, especially under the conditions that are common for many cooperative breeders (e.g. small, kin-structured populations). The extent to which fecundity variance (i.e. bet-hedging) contributes to fitness in the Seychelles warbler, or other cooperative breeding species, remains to be discovered (Rubenstein 2011; Koenig & Walters 2015). Estimating fitness in fluctuating environments is challenging (Sæther & Engen 2015), but recently developed statistical methods have been able to assess the (long term) genetic contribution of social traits in fluctuating environments (Engenet al. 2009; Sæther et al. 2016). However, our study shows that breeding together might offer fitness gains for females, irrespective of the constraints that are placed on dispersal and independent breeding. This conclusion is also supported by chapter 3, where I investigate the proximate and ultimate factors associated with between-group dispersal by natal subordinates (i.e. subordinates joining a non-natal group as a subordinate) and show that mostly females are allowed to immigrate into another group. In the Seychelles warbler, eviction is thought to be a common phenomenon (e.g. Eikenaar et al. 2007; Kingma et al. 2016a; chapter 4 of this thesis) and groups are thus expected to only allow outsiders to join the group when such outsiders provide net benefits to the fitness of insiders (Shen et al. 2017). Since a previous study in the Seychelles warbler has shown survival costs of being in a larger group (Brouwer et al. 2006), groups allowing unrelated immigrant females to join, might be doing so for reproductive benefits.

Recent comparative studies have suggested that cooperative breeding is more common in regions with high environmental variability in temperature and rainfall (Jetz & Rubenstein 2011; Lukas & Clutton-Brock 2017). Such patterns have been explained primarily by posing that subordinates make reproduction possible under adverse conditions (i.e. “temporal variability” or “hard-life” hypothesis; Rubenstein & Lovette 2007; Koenig et al. 2011). How- ever, in chapter 3, I show that annual reproductive success is unaffected by temporal patterns in food availability, for pairs as well as groups with subordinates, but that groups with

135 CHAPTER 7

subordinate females do have higher reproductive success that those without. This result suggests that either food availability never drops under levels where it affects provisioning rates or that birds incur additional costs under low food availability. This would also mean that help by subordinates would be more important to reduce the costs of provisioning for dominant breeders when food availability is low (e.g. in terms of survival) than for reproductive success. However, an earlier study has shown that survival of dominant breeders actually declines in larger groups (Brouwer et al. 2006). This conflicting result might be explained by a preliminary analysis, which shows that subordinate females are more likely to help in years when food availability is high rather than low (Fig. 7.1), indicating that the costs of help might increase under low food conditions.

1.0

0.8

dinate helps 0.6 r

0.4

0.2 Female (R = 0.77*) Probability subo 0.0 Male (R = 0.09) −0.6 −0.4 −0.2 0.0 0.2 0.4 0.6 Log standardized food availability

FIGURE 7.1 The probability that a subordinate female (red) or male (blue) helps in relation to annual food availability. Solid and dashed lines represent model predicted means ±95% CI, respectively, and points indicate the proportion of subordinates helping in each year.

In chapter 5, I show that in N. pulcher the benefits of having subordinates only become apparent under elevated risk of predation: territories are more likely to contain small fry or juveniles (indicative of successful reproduction) when they have more large or small subordinates, but only in high predation risk populations. In low predation risk populations, reproductive success is higher overall, and independent of the number of subordinates. Previous studies have pointed out the importance of both large and small subordinates for the protection and survival of other group members (Balshine et al. 2001; Heg et al. 2004a; Groenewoud et al. 2016)

136 SYNTHESIS

GROUP STABILITY

Conflict between individuals living in social groups is common, because individuals often compete for limited resources (e.g. food or reproduction) and fitness is rarely perfectly aligned. As such, conflict can be a repellant force in the evolution of sociality and diminish or even negate the benefits of group-living or cooperation (West et al. 2015). However, individuals should invest less in competition when the benefits of cooperation (or the costs of competition) are higher. Understanding the conditions under which conflict is reduced can therefore give insights into the benefits of cooperation. InN. pulcher, conflict can occur on different levels of organisation: individuals within groups compete for limited resources such as reproduction, group membership and status, and between groups, individuals compete mainly for space and shelters needed for breeding. However, individuals living under higher density (both larger groups and more neighbours) also benefit from increased protection (Jungwirth & Taborsky 2015; chapter 2 and 5). In chapter 5, I show that within-group conflict is reduced in groups living under high risk of predation: dominants are less likely to show aggression towards subordinates and subordinates are less likely to show aggression towards each other. However, aggression towards neighbouring groups does not change with increasing predation risk. This study supports and adds to the findings of chapter 2, which show that groups under high predation risk are more likely to contain large subordinates, either through delayed dispersal (Heg et al. 2004a) or through immi- gration (Bergmüller et al. 2005a; Zöttl et al. 2013). While the findings in chapter 3 were initially attributed to increased costs of dispersal, reduced aggression might also function to incentivize large subordinates to stay in the group when dispersal decisions are influenced by such aggressive interactions. To our knowledge, this study is the first to show reduced social conflict in response to predation risk (but see Shen et al. 2012). The function of aggressive interactions between dominants and subordinates in N. pulcher has been attributed to at least two different functions, i.e. as punishment to subordinates to provide more help (Gaston 1978; Fischer et al. 2014; Quiñones et al. 2016) and as a way to suppress subordinate reproduction (Fitzpatrick et al. 2005; Heg & Hamilton 2008). If aggression functions mainly to control reproduction, reproduction by subordinates should increase under higher levels of predation risk, when the benefits of anti-predator defense by such subordinates is highest. Interestingly, concession models of reproductive skew predict that dominants should be less inclined to concede reproduction to subordinates when ecological constraints are more severe (i.e. predation risk is higher), or that alternatively, that subordinates might try to claim a smaller share of reproduction, because the costs of expulsion from the group are higher (Reeve & Keller 1997; Johnstone 2000). To square this with our current data, this would have to mean that (i) the benefits of having larger subordinates in the group for

137 CHAPTER 7

dominants increase more with predation risk, than the extent to which predation risk is an ecological constraint to large subordinates, or that (ii) dominants are less likely to show aggression to large subordinates because they do not try to reproduce under high predation risk. Future studies interested in the function of aggression and the extent to which predation risk is an ecological constraint to the dispersal of larger subordinates should include measures of reproductive skew, to test for such effects.

In the Seychelles warbler, groups can remain stable over multiple years, and aggressive interactions between group members are only seldom observed. Nevertheless, indirect evidence suggests that evictions are common and are mostly the result of the death and subsequent replacement of dominant breeding males (Eikenaar et al. 2007; Kingma et al. 2016a; Groenewoud et al. 2018). In chapter 3, I have shown that changes in annual food availability can also contribute to group stability: subordinates were more likely to disperse from their natal territory in years where food availability was high. Since reproductive success in those years (for pairs or for groups with subordinates) was not higher, this pattern is best explained by lower costs of dispersal and/or prospecting (Kingma et al. 2016b). This result adds on previous work by Komdeur (1992) who showed that subordinates were more likely to delay dispersal in high quality, rather than low quality territories. Additionally, in box A, I show that nest predation risk likely creates mutualistic benefits of communal breeding and is therefore an important driver of group formation in the Seychelles warbler. Such benefits are also supported by chapter 3 of this thesis, which show reduced reproductive variance for groups containing female subordinates, but no decrease in mean per capita reproduction. Theory predicts that given two individuals with exactly the same mean reproductive success, the one with the lowest reproductive variance, will have the highest fitness (Starrfelt & Kokko 2012). Thus, females that stay together and breed communally may outperform those that breed in groups with only a dominant breeding male present, especially under high risk of nest predation (see chapter 6).

CONCLUSIONS

In conclusion, I would like to make three important observations. First, I think that predation risk has been undervalued as a driver of cooperative breeding and transitions to social complexity (chapter 2, 5 and box I). Obtaining accurate estimates of the risk of predation can be challenging, especially in avian systems, but simple proxies of predation risk (e.g. predator densities) can sometimes be sufficient. In addition to the well documented effects of predation risk of grouping (Krause & Ruxton 2002), predation risk can also affect the costs and benefits of delayed dispersal, the division of labour and cooperation in rearing

138 SYNTHESIS

young. All of these are important aspects in the transition to complex sociality and play a crucial role in the evolution and maintenance of cooperative breeding (West et al. 2015). Second, while it has been suggested that cooperative breeding could function as a bet-hedging strategy – partly because it occurs at higher frequencies in geographical regions with high temporal variation in environmental conditions (Rubenstein & Lovette 2007; Lukas & Clutton-Brock 2017) – I argue that his conclusion could be premature. Our data shows that while years of low food availability cause offspring to delay dispersal and remain as subordinates in the natal territory, cooperative breeding does not act as buffer to prevent low reproductive success in bad years (chapter 3). Thus, high temporal environmental variation could have facilitated the transition to cooperative breeding by leading to group formation and family living (Griesser et al. 2017), but not be responsible for the benefits of collective- ly rearing offspring. Third, where many studies have concluded that delayed dispersal and helping by subordinates is making the best of a bad job, I would argue that these conclusions may change if the ecological and environmental conditions under which breeding occurs are taken into account. Subordinate females in the Seychelles warbler females might have higher fitness by breeding together under increased risk of predation, but more detailed studies of individual reproductive success and the importance of reproductive variance are necessary, to demonstrate this conclusively. Similarly, large groups are necessary for successful reproduction in N. pulcher, and the extent of reproductive sharing under high risk of predation, would therefore determine if individuals might do best by breeding cooperatively. Together, these results show that the costs and benefits of cooperative breeding can only be determined, if one considers the ecological and environmental conditions under which cooperative breeding occurs.

139

References REFERENCES

A Akaike, H. (1973) Information theory and an extension of the maximum likelihood principle. Second International

Symposium on Information Theory, pp. 267–281. Budapest.

Alexander, R.D. (1974) The evolution of social behavior. Annual Review of Ecology and Systematics, 5, 325–383.

Andersson, M. & Norberg, R.A. (1981) Evolution of reversed sexual size dimorphism and role partitioning

among raptors, with a size scaling of flight performance. Biological Journal of the Linnean Society, 15, 105–130.

B Balshine-Earn, S., Neat, F.C., Reid, H. & Taborsky, M. (1998) Paying to stay or paying to breed? Field evidence

for direct benefits of helping behavior in a cooperatively breeding fish. Behavioral Ecology, 9, 432–438.

Balshine, S., Leach, B., Neat, F., Reid, H., Taborsky, M. & Werner, N. (2001) Correlates of group size in a

cooperatively breeding cichlid fish (Neolamprologus pulcher). Behavioral Ecology and Sociobiology, 50, 134–140.

Barbosa, P. & Castellanos, I. (eds). (2005) Ecology of Predator-Prey Interactions. Oxford University Press,

Oxford.

Barton, K. (2018) MuMin: Multi-Model Inference. R package.

Bates, D., Mächler, M., Bolker, B.M. & Walker, S. (2014) lme4:P Linear mixed-effects models using Eigen

and S4.

Bates, D., Mächler, M., Bolker, B.M. & Walker, S.C. (2015) Fitting linear mixed-effects models using lme4.

Journal Of Statistical Software, 67, 1–48.

Bebbington, K., Kingma, S.A., Fairfield, E.A., Spurgin, L.G., Komdeur, J. & Richardson, D.S. (2017)

Consequences of sibling rivalry vary across life in a passerine bird. Behavioral Ecology, 28, 407–418.

Berg, E.C. (2005) Parentage and reproductive success in the white-throated magpie-jay, Calocitta formosa,

a cooperative breeder with female helpers. Animal Behaviour, 70, 375–385.

Bergmüller, R., Heg, D., Peer, K. & Taborsky, M. (2005a) Extended safe havens and between-group dispersal

of helpers in a cooperatively breeding cichlid. Behaviour, 142, 1643–1667.

Bergmüller, R., Heg, D. & Taborsky, M. (2005b) Helpers in a cooperatively breeding cichlid stay and pay

or disperse and breed, depending on ecological constraints. Proceedings of the Royal Society B, 272, 325–331.

Bergmüller, R., Russell, A.F., Johnstone, R.A. & Bshary, R. (2007) On the further integration of cooperative

breeding and cooperation theory. Behavioural Processes, 76, 170–181.

BirdLife International. (2013) Foudia sechellarum. The IUCN Red List of Threatened Species 2013.

Blumstein, D.T. & Armitage, K.B. (1997) Does sociality drive the evolution of communicative complexity? A

comparative test with ground-dwelling sciurid alarm calls. The American Naturalist, 150, 179–200.

Blumstein, D.T. & Armitage, K.B. (1998) Life history consequences of social complexity: a comparative study

of ground dwelling sciurids. Behavioral Ecology, 9, 1–7.

Bocedi, G., Heinonen, J. & Travis, J.M.J. (2012) Uncertainty and the role of information acquisition in the

evolution of context-dependent emigration. The American Naturalist, 179, 606–620.

Bonte, D., Dyck, H. van, Bullock, J.M., Delgado, M., Gibbs, M., Lehouck, V., Matthysen, E., Mustin, K., S

chtickzelle, N., Stevens, V.M., Vandewoestijne, S., Baguette, M., Barton, K., Benton, T.G., Chaput-bardy,

142 REFERENCES

A., Dytham, C., Hovestadt, T., Meier, C.M., Steve, C.F., Turlure, C. & Travis, J.M.J. (2012) Costs of dispersal.

Biological Reviews, 87, 290–312.

Botham, M.S., Kerfoot, C.J., Louca, V. & Krause, J. (2005) Predator choice in the field; grouping guppies,

Poecilia reticulata, receive more attacks. Behavioral Ecology and Sociobiology, 59, 181–184.

Bourke, A.F.G. (2011) Principles of Social Evolution. Oxford University Press.

Bourke, A.F.G. (2014) Hamilton’s rule and the causes of social evolution. Philosophical Transactions of the

Royal Society B, 369, 20130362.

Briga, M., Pen, I. & Wright, J. (2012) Care for kin: within-group relatedness and allomaternal care are

positively correlated and conserved throughout the mammalian phylogeny. Biology Letters, 8, 533–536.

Brouwer, L., Barr, I., Van De Pol, M., Burke, T., Komdeur, J. & Richardson, D.S. (2010) MHC-dependent survival

in a wild population: Evidence for hidden genetic benefits gained through extra-pair fertilizations.

Molecular Ecology, 19, 3444–3455.

Brouwer, L., Richardson, D.S., Eikenaar, C. & Komdeur, J. (2006) The role of group size and environmental

factors on survival in a cooperatively breeding tropical passerine. Journal of Animal Ecology, 75, 1321–1329.

Brouwer, L., Richardson, D.S. & Komdeur, J. (2012) Helpers at the nest improve late-life offspring

performance: evidence from a long-term study and a cross-foster experiment. PloS one, 7, e33167.

Brouwer, L., Tinbergen, J.M., Both, C., Bristol, R., Richardson, D.S. & Komdeur, J. (2009) Experimental

evidence for density-dependent reproduction in a cooperatively breeding passerine. Ecology, 90, 729–741.

Brown, J.L. (1974) Alternate routes to sociality in jays: with a theory for the evolution of altruism and

communal breeding. American Zoologist, 14, 63–80.

Brown, J.L. (1982) Optimal group size in territorial animals. Journal of Theoretical Biology, 95, 793–810.

Brown, J.L. (1987) Helping and Communal Breeding in Birds: Ecology and Evolution. Princeton University Press,

Princeton.

Bruintjes, R. & Taborsky, M. (2011) Size-dependent task specialization in a cooperative cichlid in response

to experimental variation of demand. Animal Behaviour, 81, 387–394.

Bürkner, P.-C. (2017) brms: An R package for Bayesian multilevel models using Stan. Journal of Statistical

Software, 80, 1–28.

Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodal Inference: A Practical Information-

Theoretic Approach. Springer-Verlag, New York.

Burnham, K.P., Anderson, D.R. & Huyvaert, K.P. (2010) AIC model selection and multimodel inference in

behavioral ecology: Some background, observations, and comparisons. Behavioral Ecology and Sociobiology,

65, 23–35.

C Canario, F., Matos, S. & Soler, M. (2004) Environmental constraints and cooperative breeding in the

Azure-winged magpie. The Condor, 106, 608–617.

Cant, M.A., Hodge, S.J., Bell, M.B. V, Gilchrist, J.S. & Nichols, H.J. (2010) Reproductive control via eviction

(but not the threat of eviction) in banded mongooses. Proceedings of the Royal Society B, 277, 2219–2226.

143 REFERENCES

Caro, T. (2005) Antipredator Defenses in Birds and Mammals. University of Chicago Press, Chicago.

Carpenter, B., Gelman, A., Hoffman, M.D., Lee, D., Goodrich, B., Betancourt, M., Brubaker, M., Guo, J., Li, P. &

Riddell, A. (2017) Stan: A probabilistic programming language. Journal of Statistical Software, 76, 1–32.

Chang, W., Cheng, J., Allaire, J., Xie, Y. & McPherson, J. (2016) Shiny: web application framework for R.

Chase, I.D. (1980) Cooperative and noncooperative behavior in animals. The American Naturalist, 115, 827–857.

Clobert, J., Le Galliard, J.-F., Cote, J., Meylan, S. & Massot, M. (2009) Informed dispersal, heterogeneity in animal

dispersal syndromes and the dynamics of spatially structured populations. Ecology Letters, 12, 197–209.

Clutton-Brock, T. (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science,

296, 69–72.

Clutton-Brock, T. (2009) Cooperation between non-kin in animal societies. Nature, 462, 51–57.

Clutton-Brock, T.H., Brotherton, P.N., Russell, A.F., O’Riain, M.J., Gaynor, D., Kansky, R., Griffin, A., Manser, M.,

Sharpe, L., McIlrath, G.M., Small, T., Moss, A. & Monfort, S. (2001) Cooperation, control, and concession in

meerkat groups. Science, 291, 478–81.

Clutton-Brock, T.H., Gaynor, D., McIlrath, G.M., Maccoll, A.D.C., Kansky, R., Chadwick, P., Manser, M., Skinner, J.D.

& Brotherton, P.N.M. (1999) Predation, group size and mortality in a cooperative mongoose, Suricata suri-

catta. Journal of Animal Ecology, 68, 672–683.

Clutton-Brock, T.H., Hodge, S.J. & Flower, T.P. (2008) Group size and the suppression of subordinate reproduction

in Kalahari meerkats. Animal Behaviour, 76, 689–700.

Clutton-Brock, T.H., Russell, A.F. & Sharpe, L.L. (2004) Behavioural tactics of breeders in cooperative meerkats.

Animal Behaviour, 68, 1029–1040.

Clutton‐Brock, T.H. (1991) The Evolution of Parental Care. Princeton University Press, Princeton, NJ.

Clutton‐Brock, T.H. (1998) Reproductive skew, concessions and limited control. Science, 13, 288–292.

Clutton‐Brock, T.H. (2006) Cooperative breeding in mammals. Cooperation in Primates and Humans (eds P.M. Kappeler & C.P. van Schaik), pp. 173–190. Springer, Heidelberg, Berlin.

Cockburn, A. (1998) Evolution of helping behavior in cooperatively breeding birds. Annual Review of Ecology

and Systematics, 29, 141–177.

Cockburn, A. (2006) Prevalence of different modes of parental care in birds. Proceedings of the Royal Society B,

273, 1375–1383.

Cockburn, A. (2013) Cooperative breeding in birds: toward a richer conceptual framework. Cooperation and Its

Evolution, pp. 223–245. Cambridge University Press, Cambridge, MA.

Cockburn, A., Osmond, H.L., Mulder, R.A., Green, D.J. & Double, M.C. (2003) Divorce, dispersal and incest

avoidance in the cooperatively breeding superb fairy-wren Malurus cyaneus. Journal of Animal Ecology, 72,

189–202.

Cornwallis, C.K., Botero, C.A., Rubenstein, D.R., Downing, P.A., West, S.A. & Griffin, A.S. (2017) Cooperation

facilitates the colonization of harsh environments. Nature Ecology & Evolution, 1, 1–26.

Cornwallis, C.K., West, S.A., Davis, K.E. & Griffin, A.S. (2010) Promiscuity and the evolutionary transition to

complex societies. Nature, 466, 969–972.

Covas, R., Doutrelant, C. & du Plessis, M.A. (2004) Experimental evidence of a link between breeding

144 REFERENCES

conditions and the decision to breed or to help in a colonial cooperative bird. Proceedings of the Royal Society

B, 271, 827–832.

Creel, S. & Christianson, D. (2008) Relationships between direct predation and risk effects. Trends in Ecology

and Evolution, 23, 194–201. van de Crommenacker, J., Komdeur, J. & Richardson, D.S. (2011) Assessing the cost of helping: the roles

of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis). PloS one, 6,

e26423.

D Deeming, D.C. & Reynolds, S.J. (eds). (2015) Nests, Eggs, and Incubation: New Ideas about Avian Reproduction.

Oxford University Press, Oxford, UK.

Dickinson, J.L., Euaparadorn, M., Greenwald, K., Mitra, C. & Shizuka, D. (2009) Cooperation and competition:

nepotistic tolerance and intrasexual aggression in western bluebird winter groups. Animal Behaviour, 77,

867–872.

Dierkes, P., Heg, D., Taborsky, M., Skubic, E. & Achmann, R. (2005) Genetic relatedness in groups is sex-

specific and declines with age of helpers in a cooperatively breeding cichlid. Ecology Letters, 8, 968–975.

Dierkes, P., Taborsky, M. & Kohler, U. (1999) Reproductive parasitism of broodcare helpers in a cooperatively

breeding fish. Behavioral Ecology, 10, 510–515.

Dillard, J.R. & Westneat, D.F. (2016) Disentangling the correlated evolution of monogamy and cooperation.

Trends in Ecology & Evolution, 31, 1–11.

Dillon, K.G., Conway, C.J. & Skelhorn, J. (2018) Nest predation risk explains variation in avian clutch size.

Behavioral Ecology, 29, 301–311.

Drobniak, S.M., Wagner, G., Mourocq, E. & Griesser, M. (2015) Family living: An overlooked but pivotal

social system to understand the evolution of cooperative breeding. Behavioral Ecology, 26, 805–811.

Dunbar, R.I.M. & Hill, R.A. (1998) An evaluation of the roles of predation rate and predation risk as selective

pressures on primate grouping behaviour. Behaviour, 135, 411–430.

Duncan Rastogi, A., Zanette, L. & Clinchy, M. (2006) Food availability affects diurnal nest predation and

adult antipredator behaviour in song sparrows, Melospiza melodia. Animal Behaviour, 72, 933–940.

Dunn, P.O., Cockburn, A., Mulder, R.A. & Mulder, A. (1995) Fairy-wren helpers often care for young to which

they are unrelated. Proceedings of the Royal Society B, 259, 339–343.

E Eggers, S., Griesser, M., Nystrand, M. & Ekman, J. (2006) Predation risk induces changes in nest-site selection

and clutch size in the Siberian jay. Proceedings of the Royal Society B, 273, 701–706.

Eikenaar, C., Brouwer, L., Komdeur, J. & Richardson, D.S. (2010) Sex biased natal dispersal is not a fixed trait in a

stable population of Seychelles warblers. Behaviour, 147, 1577–1590.

Eikenaar, C., Komdeur, J. & Richardson, D.S. (2008a) Natal dispersal patterns are not associated with

inbreeding avoidance in the Seychelles warbler. Journal of Evolutionary Biology, 21, 1106–1116.

145 REFERENCES

Eikenaar, C., Richardson, D.S., Brouwer, L., Bristol, R. & Komdeur, J. (2008b) Experimental evaluation of sex

differences in territory acquisition in a cooperatively breeding bird. Behavioral Ecology, 20, 207–214.

Eikenaar, C., Richardson, D., Brouwer, L. & Komdeur, J. (2007) Parent presence, delayed dispersal, and

territory acquisition in the Seychelles warbler. Behavioral Ecology, 18, 874–879.

Ekman, J., Bylin, A. & Tegelström, H. (2000) Parental nepotism enhances survival of retained offspring in

the Siberian jay. Behavioral Ecology, 11, 416–420.

Ekman, J. & Griesser, M. (2002) Why offspring delay dispersal: experimental evidence for a role of parental

tolerance. Proceedings of the Royal Society B, 269, 1709–1713.

Emlen, S.T. (1982) The evolution of helping. I. An ecological constraints model. The American Naturalist,

119, 29–39.

Emlen, S.T. (1991) Evolution of cooperative breeding in birds and mammals. Behavioural Ecology:

an Evolutionary Approach (eds J.R. Krebs & N.B. Davies), pp. 301–337. Blackwell Publishing Ltd, Oxford.

Emlen, S.T. (1994) Benefits, constraints and the evolution of the family. Trends in Ecology and Evolution,

9, 9–12.

Emlen, S.T. & Wrege, P.H. (1989) A test of alternate hypothesis for helping behaviour in White-fronted

bee-eaters of Kenya. Behavioral Ecology and Sociobiology, 25, 303–319.

Engen, S., Lande, R., Sæther, B. & Dobson, F.S. (2009) Reproductive value and the stochastic demography of

age‐structured populations. The American Naturalist, 174, 795–804.

F Field, J. & Cronin, A. (2007) Social aggression in an age-dependent dominance hierarchy. Behaviour,

144, 753–765.

Fischer, S., Zöttl, M., Groenewoud, F. & Taborsky, B. (2014) Group-size-dependent punishment of idle

subordinates in a cooperative breeder where helpers pay to stay. Proceedings of the Royal Society B, 281,

20140184.

Fisher, R.A. (1930) The Genetical Theory of Natural Selection. Clarendon, New York, NY.

Fitzpatrick, J.L., Desjardins, J.K., Stiver, K.A., Montgomerie, R. & Balshine, S. (2005) Male reproductive

suppression in the cooperatively breeding fish Neolamprologus pulcher. Behavioral Ecology, 17, 25–33.

Fontaine, J.J. & Martin, T.E. (2006) Parent birds assess nest predation risk and adjust their reproductive

strategies. Ecology Letters, 9, 428–434.

Foster, K.R., Wenseleers, T. & Ratnieks, F.L.W. (2006) Kin selection is the key to altruism. Trends in Ecology

and Evolution, 21, 57–60.

Frank, S.A. (1998) Foundations of Social Evolution. Princeton University Press, New Jersey.

Frank, S.A. & Slatkin, M. (1990) Evolution in a variable environment. The American Naturalist, 136, 244–260.

Freeberg, T.M., Dunbar, R.I.M. & Ord, T.J. (2012) Social complexity as a proximate and ultimate factor in

communicative complexity. Philosophical Transactions of the Royal Society B, 367, 1785–801.

Friard, O. & Gamba, M. (2016) BORIS: a free, versatile open-source event-logging software for video/audio

coding and live observations. Methods in Ecology and Evolution, 7, 1325–1330.

146 REFERENCES

G Garcia, R.A., Cabeza, M., Rahbek, C. & Araujo, M.B. (2014) Multiple dimensions of climate change and their

implications for biodiversity. Science, 344, 1247579–1247579.

Gaston, A.J. (1978) Evolution of group territorial behavior and cooperative breeding. The American

Naturalist, 112, 1091–1100.

Gelman, A. (2006) Prior distributions for variance parameters in hierarchical models (Comment on Article

by Browne and Draper). Bayesian Analysis, 1, 515–534.

Gelman, A. & Rubin, D.B. (1992) Inference from iterative simulation using multiple sequences. Statistical

Science, 7, 457–511.

Ghalambor, C.K. & Martin, T.E. (1999) Comparative manipulation of predation risk in incubating birds

reveals variability in the plasticity of responses. Behavioral Ecology, 13, 101–108.

Ghalambor, C.K., Peluc, S.I. & Martin, T.E. (2013) Plasticity of parental care under the risk of predation: how

much should parents reduce care? Biology letters, 9, 20130154.

Gillespie, J.H. (1977) Natural selection for variances in offspring numbers: a new evolutionary principle.

The American Naturalist, 111, 1010–1014.

Grantner, A. & Taborsky, M. (1998) The metabolic rates associated with resting, and with the performance of

agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae).

Journal of Comparative Physiology, 168, 427–433.

Green, D., Cockburn, A., Hall, M.L., Osmond, H.

& Dunn, P. (1995) Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate

helpers. Proceedings of the Royal Society B, 262, 297–303.

Griesser, M., Drobniak, S.M., Nakagawa, S. & Botero, C.A. (2017) Family living sets the stage for cooperative

breeding and ecological resilience in birds. PLOS Biology, 15, e2000483.

Groenewoud, F., Frommen, J.G., Josi, D., Tanaka, H., Jungwirth, A. & Taborsky, M. (2016) Predation risk drives

social complexity in cooperative breeders. Proceedings of the National Academy of Sciences of the United States

of America, 113, 4104–4109.

Groenewoud, F., Kingma, S.A., Hammers, M., Dugdale, H.L., Burke, T.A., Richardson, D.S. & Komdeur, J.

(2018) Subordinate females in the cooperatively breeding Seychelles warbler obtain direct benefits by join-

ing unrelated groups. Journal of Animal Ecology, 87, 1251–1263.

H Hadfield, J.D., Richardson, D.S. & Burke, T. (2006) Towards unbiased parentage assignment: Combining

genetic, behavioural and spatial data in a Bayesian framework. Molecular Ecology, 15, 3715–3730.

Hamilton, W.D. (1963) The evolution of altruistic behavior. The American Naturalist, 97, 354–356.

Hamilton, W.D. (1964) Genetical evolution of social behaviour I. Journal of theoretical biology, 7, 1–16.

Hammers, M., Kingma, S.A., Bebbington, K., Crommenacker, J. Van De, Spurgin, L.G., Richardson, D.S.,

Burke, T., Dugdale, H.L. & Komdeur, J. (2015) Senescence in the wild: Insights from a long-term study on

Seychelles warblers. Experimental Gerontology, 71, 69–79.

147 REFERENCES

Hammers, M., Richardson, D.S., Burke, T. & Komdeur, J. (2012) Age-dependent terminal declines in

reproductive output in a wild bird. PloS one, 7, e40413.

Hatchwell, B.J. (1999) Investment strategies of breeders in avian cooperative breeding systems. American

Naturalist, 154, 205–219.

Hatchwell, B.J. (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history.

Philosophical Transactions of the Royal Society B, 364, 3217–3227.

Hatchwell, B.J. & Komdeur, J. (2000) Ecological constraints, life history traits and the evolution of

cooperative breeding. Animal Behaviour, 59, 1079–1086.

Heg, D., Bachar, Z., Brouwer, L. & Taborsky, M. (2004a) Predation risk is an ecological constraint for helper

dispersal in a cooperatively breeding cichlid. Proceedings of the Royal Society B, 271, 2367–2374.

Heg, D., Bender, N. & Hamilton, I. (2004b) Strategic growth decisions in helper cichlids. Proceedings of the

Royal Society B, 271, S505-508.

Heg, D., Brouwer, L., Taborsky, M. & Bachar, Z. (2005) Large group size yields group stability in the

cooperatively breeding cichlid Neolamprologus pulcher. Behaviour, 142, 1615–1641.

Heg, D. & Hamilton, I.M. (2008) Tug-of-war over reproduction in a cooperatively breeding cichlid.

Behavioral Ecology and Sociobiology, 62, 1249–1257.

Heg, D., Heg-Bachar, Z., Brouwer, L. & Taborsky, M. (2008) Experimentally induced helper dispersal in

colonially breeding cooperative cichlids. Environmental Biology of Fishes, 83, 191–206.

Heg, D. & Taborsky, M. (2010) Helper response to experimentally manipulated predation risk in the

cooperatively breeding cichlid Neolamprologus pulcher. PloS one, 5, e10784.

Heinsohn, R. & Legge, S. (1999) The cost of helping. Trends in Ecology and Evolution, 14, 53–57.

Hess, S., Fischer, S. & Taborsky, B. (2016) Territorial aggression reduces vigilance but increases aggression

towards predators in a cooperatively breeding fish. Animal Behaviour, 113, 229–235.

Hochberg, M.E., Rankin, D.J. & Taborsky, M. (2008) The coevolution of cooperation and dispersal in social

groups and its implications for the emergence of multicellularity. BMC Evolutionary Biology, 8, 238.

Hoffman, M.D. & Gelman, A. (2014) The No-U-Turn Sampler: adaptively setting path lengths in Hamiltonian

Monte Carlo. Journal of Machine Learning Research, 15, 1351–1381.

Holmes, T. & McCormick, M. (2010) Size-selectivity of predatory reef fish on juvenile prey. Marine Ecology

Progress Series, 399, 273–283.

Hothorn, T., Bretz, F. & Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical

Journal, 50, 346–363.

Hughes, W.O.H., Oldroyd, B.P., Beekman, M. & Ratnieks, F.L.W. (2008) Ancestral monogamy shows kin

selection is key to the evolution of eusociality. Science, 320, 1213–1216.

Hurvich, C. & Tsai, C.-L. (1989) Regression and time series model selection in small samples. Biometrika,

76, 297–307.

I Inman, A.J. & Krebs, J. (1987) Predation and group living. Trends in Ecology and Evolution, 2, 31–32.

148 REFERENCES

J Jakobsson, S., Brick, O. & Kullberg, C. (1995) Escalated fighting behaviour incurs increased predation risk.

Animal Behaviour, 49, 235–239.

James, P.C. & Oliphant, L.W. (1986) Extra birds and helpers at the nest of Richardson’s merlin. The Condor,

88, 533–534.

Jennions, M.D. & Macdonald, D.W. (2007) Cooperative Breeding in Mammals (eds NG Solomon and JA French).

Cambridge University Press, Cambridge.

Jetz, W. & Rubenstein, D.R. (2011) Environmental uncertainty and the global biogeography of cooperative

breeding in birds. Current biology, 21, 72–78.

Jing, Y., Fang, Y., Strickland, D., Lu, N. & Sun, Y.-H. (2009) Alloparenting in the Rare Sichuan Jay (Perisoreus

Internigrans). The Condor, 111, 662–667.

Johnson, W.T. & Freeberg, T.M. (2016) Pseudoreplication in use of predator stimuli in experiments on anti

predator responses. Animal Behaviour, 119, 161–164.

Johnson, C.A., Fryxell, J.M., Thompson, I.D. & Baker, J.A. (2009) Mortality risk increases with natal dispersal

distance in American martens. Proceedings of the Royal Society B, 276, 3361–3367.

Johnstone, R.A. (2000) Models of reproductive skew: a review and synthesis. Ethology, 106, 5–26.

Johnstone, R.A. (2011) Load lightening and negotiation over offspring care in cooperative breeders.

Behavioral Ecology, 22, 436–444.

Johnstone, R.A. & Cant, M.A. (1999) Reproductive skew and the threat of eviction: a new perspective.

Proceedings of the Royal Society B, 266, 275–279.

Johnstone, R.A. & Hinde, C.A. (2006) Negotiation over offspring care - How should parents respond to each

other’s efforts? Behavioral Ecology, 17, 818–827.

Johnstone, R.A., Manica, A., Fayet, A.L., Stoddard, M.C., Rodriguez-Girones, M.A. & Hinde, C.A. (2013)

Reciprocity and conditional cooperation between great tit parents. Behavioral Ecology, 25, 216–222.

Jordan, L.A., Wong, M.Y.L. & Balshine, S.S. (2010) The effects of familiarity and social hierarchy on group

membership decisions in a social fish. Biology letters, 6, 301–303.

Jungwirth, A., Josi, D., Walker, J. & Taborsky, M. (2015a) Benefits of coloniality: communal defence saves

anti-predator effort in cooperative breeders. Functional Ecology, 29, 1218–1224.

Jungwirth, A. & Taborsky, M. (2015) First- and second-order sociality determine survival and reproduction

in cooperative cichlids. Proceedings of the Royal Society B, 282, 20151971.

Jungwirth, A., Walker, J. & Taborsky, M. (2015b) Prospecting precedes dispersal and increases survival

chances in cooperatively breeding cichlids. Animal Behaviour, 106, 107–114.

K Kennedy, P., Higginson, A., Radford, A.N. & Sumner, S. (2018) Altruism in a volatile world. Nature, 555, 359–362.

Kingma, S.A., Bebbington, K., Hammers, M., Richardson, D.S. & Komdeur, J. (2016a) Delayed dispersal and

the cost and benefits of different routes to independent breeding in a cooperative breeding bird. Evolution,

70, 2595–2610.

149 REFERENCES

Kingma, S.A., Komdeur, J., Burke, T. & Richardson, D.S. (2017) Differential dispersal costs and sex-biased

dispersal distance in a cooperatively breeding bird. Behavioral Ecology, 28, 1113–1121.

Kingma, S.A., Komdeur, J., Hammers, M. & Richardson, D.S. (2016b) The cost of prospecting for dispersal

opportunities in a social bird. Biology Letters, 12, 20160316.

Kingma, S.A., Santema, P., Taborsky, M. & Komdeur, J. (2014) Group augmentation and the evolution of

cooperation. Trends in Ecology and Evolution, 29, 476–484.

Koenig, W.D. & Dickinson, J.L. (eds). (2016) Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and

Behavior. Cambridge University Press, Cambridge.

Koenig, W.D., Pitelka, F.A., Carmen, W.J., Mumme, R.L. & Stanback, M.T. (1992) The evolution of delayed

dispersal in cooperative breeders. Quarterly Review of Biology, 67, 111–150.

Koenig, W.D. & Walters, E.L. (2011) Brooding, provisioning, and compensatory care in the cooperatively

breeding acorn woodpecker. Behavioral Ecology, 23, 181–190.

Koenig, W.D. & Walters, E.L. (2015) Temporal variability and cooperative breeding: testing the bet-hedging

hypothesis in the acorn woodpecker. Proceedings of the Royal Society B, 282, 20151742.

Koenig, W.D., Walters, E.L. & Haydock, J. (2011) Variable helper effects, ecological conditions, and the

evolution of cooperative breeding in the acorn woodpecker. The American Naturalist, 178, 145–58.

Koenig, W.D., Walters, E.L. & Haydock, J. (2016) Acorn woodpeckers: Helping at the nest, polygynandry, and

dependence on a variable acorn crop. Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and

Behavior (eds W.D. Koenig & J.L. Dickinson), pp. 217–236. Cambridge University Press, Cambridge.

Kokko, H. & Ekman, J. (2002) Delayed dispersal as a route to breeding: territorial inheritance, safe havens,

and ecological constraints. The American Naturalist, 160, 468–484.

Kokko, H., Johnstone, R.A. & Clutton-Brock, T.H. (2001) The evolution of cooperative breeding through

group augmentation. Proceedings of the Royal Society B, 268, 187–196.

Komdeur, J. (1991) Cooperative Breeding in the Seychelles Warbler. University of Cambridge, UK.

Komdeur, J. (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding

in the Seychelles warbler. Nature, 358, 493–495.

Komdeur, J. (1994a) Experimental evidence for helping and hindering by previous offspring in the

cooperative-breeding Seychelles warbler Acrocephalus sechellensis. Behavioral Ecology and Sociobiology, 34,

175–186.

Komdeur, J. (1994b) The effect of kinship on helping in the cooperative breeding Seychelles warbler

(Acrocephalus sechellensis). Proceedings of the Royal Society B, 256, 47–52.

Komdeur, J. (1995) Influence of age on reproductive performance in the Seychelles warbler. Behavioral

Ecology, 7, 417–425.

Komdeur, J. (1996a) Facultative sex ratio bias in the offspring of Seychelles warblers. Proceedings of the Royal

Society B, 263, 661–666.

Komdeur, J. (1996b) Seasonal timing of reproduction in a tropical bird, the Seychelles warbler: A field

experiment using translocation. Journal of Biological Rhythms, 11, 333–346.

Komdeur, J. & Daan, S. (2005) Breeding in the monsoon: semi-annual reproduction in the Seychelles

150 REFERENCES

warbler (Acrocephalus sechellensis). Journal of Ornithology, 146, 305–313.

Komdeur, J., Dugdale, H.L., Burke, T. & Richardson, D.S. (2016) Seychelles warblers: complexities of the

helping paradox. Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior (eds W.D. Koe-

nig & J.L. Dickinson), pp. 197–216. Cambridge University Press, Cambridge, UK.

Komdeur, J. & Edelaar, P. (2001) Male Seychelles warblers use territory budding to maximize lifetime fitness

in a saturated environment. Behavioral Ecology, 12, 706–715.

Komdeur, J. & Kats, R.K.H. (1999) Predation risk affects trade-off between nest guarding and foraging in

Seychelles warblers. Behavioral Ecology, 10, 648–658.

Komdeur, J. & Pels, M.D. (2005) Rescue of the Seychelles warbler on Cousin Island, Seychelles: the role of

habitat restoration. Biological Conservation, 124, 15–26.

Komdeur, J., Piersma, T., Kraaijeveld, K., Kraaijeveld-Smit, F. & Richardson, D.S. (2004a) Why Seychelles

Warblers fail to recolonize nearby islands: unwilling or unable to fly there? Ibis, 146, 298–302.

Komdeur, J., Richardson, D.S. & Burke, T. (2004b) Experimental evidence that kin discrimination in the

Seychelles warbler is based on association and not on genetic relatedness. Proceedings of the Royal Society

B, 271, 963–969.

Komdeur, J., Richardson, D.S., Hammers, M., Eikenaar, C., Brouwer, L. & Kingma, S.A. (2017) The Evolution of

Cooperative Breeding in Vertebrates. eLS, pp. 1–11. John Wiley & Sons, Ltd, Chichester, UK.

Konings, A. (1998) Tanganyika Cichlids in Their Natural Habitat. Hollywood Import & Export Inc.

Krams, I., Bērziņs, A., Krama, T., Wheatcroft, D., Igaune, K. & Rantala, M.J. (2010) The increased risk of

predation enhances cooperation. Proceedings of the Royal Society B, 277, 513–518.

Krause, J. & Ruxton, G.D. (2002) Living in Groups. Oxford University Press, Oxford.

Kylafis, G. & Loreau, M. (2008) Ecological and evolutionary consequences of niche construction for its

agent. Ecology Letters, 11, 1072–1081.

L Lehmann, L. & Balloux, F. (2007) Natural selection on fecundity variance in subdivided populations: Kin

selection meets bet hedging. Genetics, 176, 361–377.

Lehtonen, J. & Jaatinen, K. (2016) Safety in numbers: the dilution effect and other drivers of group life in the

face of danger. Behavioral Ecology and Sociobiology, 449–458.

Ligon, J.D. & Burt, D.B. (2004) Evolutionary origins. Ecology and evolution of cooperative breeding in birds (eds

W.D. Koenig & J.L. Dickinson), pp. 5–34. Cambridge university press, Cambridge, UK.

Lima, S.L. (2009) Predators and the breeding bird: Behavioral and reproductive flexibility under the risk of

predation. Biological Reviews, 84, 485–513.

Lukas, D. & Clutton-Brock, T. (2012) Cooperative breeding and monogamy in mammalian societies.

Proceedings of the Royal Society B, 279, doi: 10.1098/rspb.2011.2468.

Lukas, D. & Clutton-Brock, T. (2017) Climate and the distribution of cooperative breeding in mammals.

Royal Society Open Science, 4, 160897.

151 REFERENCES

M Magrath, R.D. (2001) Group breeding dramatically increases reproductive success of yearling but not older

female scrubwrens: a model for cooperatively breeding birds? Journal of Animal Ecology, 70, 370–385.

Martín-Vivaldi, M., Martínez, J.G., Palomino, J.J. & Soler, M. (2002) Extrapair paternity in the Hoopoe Upupa

epops: An exploration of the influence of interactions between breeding pairs, non-pair males and strophe

length. Ibis, 144, 236–247.

Martin, T.E. (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecological

Monographs, 65, 101–127.

Mazerolle, M.J. (2013) AICcmodavg: Model selection and multimodal inference based on (Q)AIC(c).

McElreath, R. (2015) Statistical Rethinking: A Bayesian Course with Examples in R and Stan. Chapman & Hall/

CRC.

Mills, A.M. (2008) Passerines are sexually dimorphic in shape as well as size. The Condor, 110, 354–358.

Montgomerie, R.D. & Weatherhead, P.J. (1988) Risks and rewards of nest defence by parent birds. The

Quarterly Review of Biology, 63, 167–187.

N Nakagawa, S. & Schielzeth, H. (2010) Repeatability for Gaussian and non-Gaussian data: A practical guide

for biologists. Biological Reviews, 85, 935–956.

Nakagawa, S. & Schielzeth, H. (2013) A general and simple method for obtaining R^2 from generalized

linear mixed-effects models. Methods in Ecology and Evolution, 4, 133–142.

Nelson-Flower, M.J. & Ridley, A.R. (2016) Nepotism and subordinate tenure in a cooperative breeder. Biology

Letters, 12, 20160365.

Nelson-Flower, M.J., Wiley, E.M., Flower, T.P. & Ridley, A.R. (2018) Individual dispersal delays in a cooperative

breeder: Ecological constraints, the benefits of philopatry and the social queue for dominance. Journal of

Animal Ecology, 87, 1227–1238.

P Pen, I. & Weissing, F.J. (2000) Towards a unified theory of cooperative breeding: the role of ecology and life

history re-examined. Proceedings of the Royal Society B, 267, 2411–2418.

Pew, J., Muir, P.H., Wang, J. & Frasier, T.R. (2015) related: An R package for analysing pairwise relatedness

from codominant molecular markers. Molecular Ecology Resources, 15, 557–561.

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Development Core Team & R Core Team. (2012) nlme: Linear

and Nonlinear Mixed Effects Models.

Platt, T.G. & Bever, J.D. (2009) Kin competition and the evolution of cooperation. Trends in Ecology and

Evolution, 24, 370–377.

Port, M., Schülke, O. & Ostner, J. (2017) From individual to group territoriality: competitive environments

promote the evolution of sociality. The American Naturalist, 189, E46-57.

152 REFERENCES

Q Queller, D.C. & Goodnight, K.F. (1989) Estimating relatedness using genetic markers. Evolution, 43, 258–275.

Quiñones, A.E., Van Doorn, G.S., Pen, I., Weissing, F.J. & Taborsky, M. (2016) Negotiation and appeasement

can be more effective drivers of sociality than kin selection. Philosophical Transactions of the Royal Society B,

371, 20150089.

R R Core Team. (2016) R: A language and environment for statistical computing.

R Development Core Team. (2008) R: A language and environment for statistical computing.

Ranta, E., Laurila, A. & Elmberg, J. (1994) Reinventing the wheel: Analysis of sexual dimorphism in body

size. Oikos, 70, 313–321.

Reed, J.M. & Walters, J.R. (1996) Helper effects on variance components of fitness in the cooperatively

breeding Red- Cockaded Woodpecker. The Auk, 113, 608–616.

Reeve, H.K. (2000) A transactional theory of within‐group conflict. The American Naturalist, 155, 365–382. Reeve, H.K., Emlen, S.T. & Keller, L. (1998) Reproductive sharing in animal societies: reproductive

incentives or incomplete control by dominant breeders? Behavioral Ecology, 9, 267–278.

Reeve, H.K. & Keller, L. (1997) Reproductive bribing and policing as evolutionary mechanisms for the

suppression of within-group selfishness. American Naturalist, 150, S42–S58.

Regelmann, K. & Curio, E. (1986) How do Great tit (Parus major) pair mates cooperate in brood defence?

Behaviour, 97, 10–36.

Reid, J.M., Ruxton, G.D., Monaghan, P. & Hilton, G.M. (2002) Energetic consequences of clutch temperature

and clutch size for a uniparental intermittent incubator : the Starling. The Auk, 119, 54–61.

Reyer, H. (1980) Flexible helper structure as an ecological adaptation in the Pied kingfisher (Ceryle rudis

rudis L.). Behavioral Ecology and Sociobiology, 6, 219–227.

Reyer, H. (1982) Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied

kingfisher (Ceryle rudis). Animal Behaviour, 32, 1163–1178.

Richardson, D.S., Burke, T. & Komdeur, J. (2002) Direct benefits and the evolution of female-biased

cooperative breeding in Seychelles warblers. Evolution, 56, 2313–2321.

Richardson, D.S., Burke, T. & Komdeur, J. (2003a) Sex-specific associative learning cues and inclusive fitness

benefits in the Seychelles warbler. Journal of Evolutionary Biology, 16, 854–61.

Richardson, D.S., Burke, T. & Komdeur, J. (2007) Grandparent helpers: the adaptive significance of older,

postdominant helpers in the Seychelles warbler. Evolution, 61, 2790–800.

Richardson, D.S., Jury, F.L., Blaakmeer, K., Komdeur, J. & Burke, T. (2001) Parentage assignment and

extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Molecular

Ecology, 10, 2263–2273.

Richardson, D.S., Komdeur, J. & Burke, T. (2003b) Altruism and infidelity among warblers. Nature, 422,

580–581.

Richardson, D.S., Komdeur, J. & Burke, T. (2004) Inbreeding in the Seychelles warbler: environment-

153 REFERENCES

dependent maternal effects. Evolution, 58, 2037–2048.

Ricklefs, R.E. (1969a) An analysis of nesting mortality in birds. Smithsonian Contributions to Zoology, 9, 1–48.

Ricklefs, R. (1969b) Natural selection and development of mortality rates in young birds. Nature, 223, 922–

925.

Ridley, A.R., Raihani, N.J. & Nelson-Flower, M.J. (2008) The cost of being alone: the fate of floaters in a

population of cooperatively breeding pied babblers Turdoides bicolor. Journal of Avian Biology, 39, 389–392.

Riehl, C. (2013) Evolutionary routes to non-kin cooperative breeding in birds. Proceedings of the Royal Society

B, 280, 20132245.

Robinson, G.K. (1991) That BLUP is a good thing: The estimation of random effects. Statistical Science, 6, 15–51.

Rolland, C., Danchin, E. & de Fraipont, M. (1998) The evolution of coloniality in birds in relation to food,

habitat, predation, and life‐history traits: a comparative analysis. The American Naturalist, 151, 514–529. De Rosario-Martinez, H. (2015) phia: Post-Hoc Interaction Analysis.

Rubenstein, D.R. (2011) Spatiotemporal environmental variation, risk aversion, and the evolution of

cooperative breeding as a bet-hedging strategy. Proceedings of the National Academy of Sciences of the United

States of America, 108, 10816–10822.

Rubenstein, D.R. & Lovette, I.J. (2007) Temporal environmental variability drives the evolution of

cooperative breeding in birds. Current Biology, 17, 1414–1419.

S Sæther, B.E. & Engen, S. (2015) The concept of fitness in fluctuating environments. Trends in Ecology and

Evolution, 30, 273–281.

Sæther, B.-E., Visser, M.E., Grøtan, V. & Engen, S. (2016) Evidence for r- and K-selection in a wild bird

population: a reciprocal link between ecology and evolution. Proceedings of the Royal Society B, 283, 20152411.

Schädelin, F.C., Fischer, S. & Wagner, R.H. (2012) Reduction in predator defense in the presence of

neighbors in a colonial fish. PLoS ONE, 7, e35833. van Schaik, C.P. & Hörstermann, M. (2014) Predation risk and the number of adult males in a primate

group: A comparative test. Behavioral Ecology and Sociobiology, 35, 261–272.

Seddon, N., Amos, W., Adcock, G., Johnson, P., Kraaijeveld, K., Kraaijeveld-Smit, F.J.L., Lee, W., Senapathi,

G.D., Mulder, R.A. & Tobias, J.A. (2005) Mating system, philopatry and patterns of kinship in the coopera-

tively breeding subdesert mesite Monias benschi. Molecular Ecology, 14, 3573–3583.

Selander, R.K. (1964) Speciation in wrens of the genus Campylorhynchus. Univ. Calif. Publ. Zool., 74, 1–224.

Shen, S.-F., Akçay, E. & Rubenstein, D.R. (2014) Group size and social conflict in complex societies. The

American naturalist, 183, 301–310.

Shen, S.-F., Emlen, S.T., Koenig, W.D. & Rubenstein, D.R. (2017) The ecology of cooperative breeding

behaviour. Ecology Letters, 20, 708–720.

Shen, S.F., Vehrencamp, S.L., Johnstone, R.A., Chen, H.C., Chan, S.F., Liao, W.Y., Lin, K.Y. & Yuan, H.W. (2012)

Unfavourable environment limits social conflict in Yuhina brunneiceps. Nature Communications, 3, 885–887.

Skutch, A.F. (1935) Helpers at the nest. The Auk, 52, 257–273.

154 REFERENCES

Slack, R.D. (1976) Nest guarding behaviour by male gray catbirds. The Auk, 93, 292–300.

Smith, J.M. & Szathmary, E. (1995) The Major Transitions in Evolution. Oxford University Press, Oxford.

Solomon, N.G. & French, J.A. (eds). (2007) Cooperative Breeding in Mammals. Cambridge University Press,

Cambridge, UK.

Spurgin, L.G., Wright, D.J., Velde, M. Van Der, Collar, N.J., Komdeur, J., Burke, T. & Richardson, D.S. (2014)

Museum DNA reveals the demographic history of the endangered Seychelles warbler. Evolutionary Appli-

cations, 7, 1134–1143.

Stacey, P.B. & Koenig, W.D. (eds). (1990) Cooperative Breeding in Birds: Long-Term Studies of Ecology and

Behaviour. Cambridge University Press, Cambridge, UK.

Stacey, P.B. & Ligon, J.D. (1991) The benefits-of-philopatry hypothesis for the evolution of cooperative

breeding: variation in territory quality and group size effects. The American Naturalist, 137, 831–846.

Stan Development Team. (2015) Stan: a C++ library for probability and sampling.

Starrfelt, J. & Kokko, H. (2012) Bet– hedging – a triple trade-off between means, variances and correlations.

Biological Reviews, 87, 742–755.

Stearns, S.C. (1989) Trade-offs in life-history evolution. Functional Ecology, 3, 259–268.

Stiver, K.A., Dierkes, P., Taborsky, M., Balshine, S. & Biology, F. (2004) Dispersal patterns and status change

in a co-operatively breeding cichlid Neolamprologus pulcher: evidence from microsatellite analyses and be-

havioural observations. Journal of Fish Biology, 9140, 91–105.

T Taborsky, M. (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits.

Animal Behaviour, 32, 1236–1252.

Taborsky, M. (1985) Breeder-helper conflict in a cichlid fish with broodcare helpers: An experimental

analysis. Behaviour, 95, 45–75.

Taborsky, M. (2013) Social evolution: reciprocity there is. Current Biology, 23, R486-488.

Taborsky, M. (2016) A model for the integrative study of social behavior. Cooperative Breeding in Vertebrates

(eds W.D. Koenig & J.L. Dickinson), pp. 272–293. Cambridge University Press, Cambridge.

Taborsky, M. & Grantner, A. (1998) Behavioural time-energy budgets of cooperatively breeding

Neolamprologus pulcher (Pisces: Cichlidae). Animal behaviour, 56, 1375–1382.

Taborsky, M. & Limberger, D. (1981) Helpers in fish. Behavioral Ecology and Sociobiology, 8, 143–145.

Tanaka, H., Frommen, J.G. & Kohda, M. (2018) Helpers increase food abundance in the territory of a

cooperatively breeding fish. Behavioral Ecology and Sociobiology, 72, 51.

Taylor, P.D. (1990) Allele-frequency change in a class-structured population. The American Naturalist, 20,

611–624.

Tinbergen, J.M. & Williams, J.B. (2002) Energetics of incubation. Avian Incubation Behaviour, Environment and

Evolution (ed D.C. Deeming), pp. 299–313. Oxford University Press, Oxford, UK.

Trivers, R.L. (1972) Parental investment and sexual selection. Sexual selection and the descent of man,

Campbell, (ed B. Campbell), pp. 136–179. Aldine press, Chicago.

155 REFERENCES

Tuljapurkar, S. (1990) Delayed reproduction and fitness in variable environments. Proceedings of the

National Academy of Sciences of the United States of America, 87, 1139–1143.

V Valencia, J., De La Cruz, C., Carranza, J. & Mateos, C. (2006) Parents increase their parental effort when aided

by helpers in a cooperatively breeding bird. Animal Behaviour, 71, 1021–1028.

Veen, T., Richardson, D.S., Blaakmeer, K. & Komdeur, J. (2000) Experimental evidence for innate predator

recognition in the Seychelles warbler. Proceedings of the Royal Society B, 267, 2253–2258.

Vehtari, A., Gelman, A. & Gabry, J. (2016) Practical Bayesian model evaluation using leave-one-out cross-

validation and WAIC. Statistics and Computing, 1–20.

W Watanabe, S. (2010) Asymptotic equivalence of Bayes cross validation and Widely Applicable Information

Criterion in singular learning theory. Journal of Machine Learning Research, 11, 3571–3594.

Weatherhead, P.J. (1989) Nest defence by song sparrows: methodological and life history considerations.

Behavioral Ecology and Sociobiology, 25, 129–136.

Webster, M.S. (1994) Female-defence polygyny in a Neotroprical bird, the Montezuma oropendola. Animal

Behaviour, 48, 779–794.

West-Eberhard, M.J. (1975) The evolution of social behavior by kin selection. Quarterly Review of Biology, 50, 1–33.

West, S.A., Fisher, R.M., Gardner, A., Kiers, E.T. & Mccutcheon, J.P. (2015) Major evolutionary transitions in

individuality. Proceedings of the National Academy of Sciences, 112, 10112–10119.

Wilson, E.O. (1971) The Insect Societies. Belknap Press of Harvard University Press, Cambridge, MA.

Wong, M. & Balshine, S. (2011) Fight for your breeding right: hierarchy re-establishment predicts

aggression in a social queue. Biology letters, 7, 190–193.

Wong, M.Y.L., Jordan, L.A., Marsh-Rollo, S., St-Cyr, S., Reynolds, J.O., Stiver, K.A., Desjardins, J.K., Fitzpatrick,

J.L. & Balshine, S. (2012) Mating systems in cooperative breeders: The roles of resource dispersion and con-

flict mitigation. Behavioral Ecology, 23, 521–530.

Wood, S.N. (2006) Generalized Additive Models: An Introduction with R. Chapman & Hall/CRC.

Wood, S.N. (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of

semiparametric generalized linear models. Journal of the Royal Statistcal Society. Series B (Statistical Method-

ology), 73, 3–36.

Wright, J. (2007) Cooperation theory meets cooperative breeding: exposing some ugly truths about social

prestige, reciprocity and group augmentation. Behavioural processes, 76, 142–148.

Wright, J., McDonald, P.G., te Marvelde, L., Kazem, A.J.N. & Bishop, C.M. (2010) Helping effort increases with

relatedness in bell miners, but “unrelated” helpers of both sexes still provide substantial care. Proceedings

of the Royal Society B, 277, 437–45.

Wright, D.J., Spurgin, L.G., Collar, N.J. & Komdeur, J. (2014) The impact of translocations on neutral and

functional genetic diversity within and among populations of the Seychelles warbler. Molecular Ecology,

156 REFERENCES

23, 2165–2177.

Wrona, F.J. & Dixon, R.W.J. (1991) Group size and predation risk: a field analysis of encounter and dilution

effects. The American Naturalist, 137, 186–201.

Y Yoder, J.M. (2004) The cost of dispersal: predation as a function of movement and site familiarity in ruffed

grouse. Behavioral Ecology, 15, 469–476.

Z Zöttl, M., Frommen, J.G. & Taborsky, M. (2013) Group size adjustment to ecological demand in a cooperative

breeder. Proceedings of the Royal Society B, 280, 20122772.

Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in

Ecology with R. Springer New York, NY.

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Nederlandse samenvatting NEDERLANDSE SAMENVATTING

INTRODUCTIE

Coöperatief broeden is een sociaal systeem waarbij meer dan twee individuen zorg dragen voor de nakomelingen. Dit systeem komt veelvuldig voor bij vogels, zoogdieren, vissen en insecten. Het ontstaan van coöperatief broeden wordt vaak toegeschreven aan een combinatie van omgevingsfactoren die het verlaten van het ouderlijk territorium (“dispersie”) belemmeren. Vaak blijven nakomelingen door een gebrek aan voldoende geschikte broedgelegenheid (“habitat saturation”), ook nadat zij reproductief volwassen zijn geworden, bij hun ouders in het territorium (“uitgestelde dispersie”). Dit stelt deze individuen vervolgens in staat om zorg te dragen voor de jongen van een volgende voortplantingspoging van de ouders (die in deze context vaak “dominanten” worden genoemd). Dit gebeurd bijvoorbeeld door het brengen van voedsel, of het be- schermen van de jongen tegen predatoren. Deze individuen worden vaak helpers of “subordinaten” genoemd. Er zijn meerdere hypotheses voorgesteld om te verklaren waarom subordinaten anderen helpen in plaats van zelf te reproduceren. Eén van de belangrijkste theorieën rust op de observatie dat subordinaten vaak verwant zijn aan de individuen die zij helpen en hierdoor dus indirecte baten ontvangen, omdat zij genen delen met deze individuen. Toch zijn er veel soorten die jongen coöperatief grootbrengen waar samenwerking vooral lijkt plaats te vinden tussen niet-verwante individuen en waarbij belemmeringen op dispersie geen rol lijken te spelen. Dit suggereert dat er – voor deze gevallen – alternatieve verklaringen voor groepsvorming en coöperatief gedrag gezocht moeten worden.

Ondanks vele voordelen, brengt groepsleven ook verschillende kosten met zich mee. Een van de meest voorkomende kosten van groepsleven is de competitie die groepsleden onderling aan moeten gaan om voldoende voedsel te bemachtigen en zelf te kunnen reproduceren. Dergelijke competitie leidt vaak tot sociale conflicten waarin individuen, door middel van agressie en ten koste van anderen, een zo groot mogelijk deel van deze middelen proberen te verkrijgen. Door dit soort conflicten kunnen de kosten van het leven in een groep uiteindelijk de baten overstijgen, waardoor groepen uit elkaar kunnen vallen. De factoren die sociale conflicten onderdrukken zijn dus belangrijk om de stabiliteit van het leven in groepen te begrijpen. Groepsvorming, helpgedrag door subordinaten en groepsstabiliteit vormen samen drie essentiële componenten van transities naar, en het behoud van, coöperatief broeden.

In mijn proefschrift onderzoek ik de invloed van variatie in omgevingsfactoren op deze drie componenten van coöperatief broeden. In het specifiek onderzoek ik hoe voedselbeschikbaarheid en het risico op predatie invloed hebben op groepsvorming, helpge-

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drag en groepsstabiliteit in twee verschillende sociale systemen: de Seychellenrietzan- ger (hierna “Seychellenzanger”; Acrocephalus sechellensis) en Neolamprologus pulcher.

Studiesystemen De Seychellenzanger De Seychellenzanger is een sociale zangvogel die voorkomt op vijf verschillende ei- landen van de Seychellenarchipel in de Indische oceaan. De meeste Seychellenzangers op het eiland Cousin – waar de studies uit dit proefschrift zijn gedaan – broeden in paartjes, maar ongeveer 40% van alle territoria hebben een of meerdere mannelijke of vrouwelijke subordinaten. Al het beschikbare habitat wordt bezet door Seychellenzan- gers en er zijn ongeveer 110 territoria, die het gehele jaar worden verdedigd. Geschikte broedplekken komen vaak dus alleen vrij als er een dominante vogel op een territorium komt te overlijden. Seychellenzangers op Cousin produceren normaal gesproken een enkel ei per legsel, maar ongeveer 13% van alle vogels legt 2-3 eieren. De jongen zijn afhankelijk van hun ouders voor een periode van drie maanden, wat erg lang is voor een zangvogel. Er is geen migratie van of naar het eiland en gezien de grootte van het eiland (29 hectare) worden bijna alle nog levende vogels elk jaar gezien. Boven- dien zijn bijna alle vogels individueel herkenbaar door het gebruik van (kleur)ringen). Deze combinatie van factoren maakt de Seychellenzanger erg geschikt om onderzoek te doen naar dispersie vanaf de geboorteplek tot de plek waar vogels voor het eerst zelf broeden (“natal dispersal”). Het dieet van Seychellenzangers bestaat bijna volledig uit ongewervelden (voornamelijk insecten) en hiervoor zijn ze afhankelijk van twee pieken in voedselbeschikbaarheid die plaatsvinden na moessonregens. Gedetailleerde metingen van voedselaanbod zijn verzameld sinds het begin van het onderzoek en een eerdere studie heeft laten zien dat nakomelingen eerder geneigd zijn om als subordinaat bij hun ouders in het territorium te blijven als dat territorium van hoge kwaliteit is. Er zijn echter ook grote verschillen in voedselbeschikbaarheid tussen jaren. De effecten van deze variatie op dispersie en de mate waarin individuen samenwerken bij het grootbrengen van de jongen waren hiervoor nog onbekend, maar zijn nu onderzocht in dit proefschrift.

Volwassen Seychellenzangers hebben geen natuurlijke vijanden, maar nestpredatie van eieren door een endemische wevervogel, de Seychellenwever (Foudia sechellarum) komt veel voor. Seychellenzangers proberen het risico op nestpredatie op verschillende manieren te verkleinen. Ten eerste bewaken dominante mannetjes het nest tijdens de incubatieperiode als hun vrouwen het incuberen tijdelijk onderbreken om op zoek te gaan naar eten. Deze strategie is erg effectief, omdat predatie alleen plaatsvind op onbewaakte nesten. Ten tweede helpen vrouwelijke subordinaten bij het incuberen

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van de eieren. Hierdoor worden de eieren minder lang en minder vaak onbeschermd achter gelaten, wat het risico op predatie verder verkleint. Ook leggen deze vrouwelijke subordinaten vaak samen met de dominante vrouw uit het territorium een ei in hetzelfde nest. De mate waarin het risico op nestpredatie een rol speelt bij de dispersie van subordinaten uit het ouderlijk territorium, incubatiegedrag door subordinate vrouwen en de kans dat zij een ei leggen in hetzelfde nest was nog niet bekend.

Neolamprologus pulcher Neolamprologus pulcher is een coöperatief broedende cichlide die endemisch is voor het Tanganyika-meer, in zuidelijk Afrika. De soort komt hier vrijwel overal voor in de su- blitorale zone vanaf 2 tot 40 meter diepte. Territoria bestaan uit een dominant paar en tot ongeveer 25 subordinaten van verschillende grootten en seksen, die meestal enkele rotsen en stenen gebruiken als vaste schuil- en broedplaats. Subordinaten in N. pulcher hebben verschillende soorten helpgedrag. Zo verwijderen ze zand om schuilplaatsen te creëren, verdedigen ze het territorium tegen o.a. predatoren en verzorgen ze de eieren door deze van extra zuurstof te voorzien. De taken die de subordinaten uitvoeren zijn grootte-afhankelijk: kleinere, onvolwassen subordinaten houden zich voornamelijk bezig met het onderhoud van het territorium en de verdediging tegen kleinere predatoren, terwijl grotere, volwassen subordinaten het territorium verdedigen tegen gevaarlijke predatoren. De territoria van N. pulcher zijn geaggregeerd in populaties die tientallen tot honderden territoria kunnen omvatten.

Een van de grootste obstakels voor dispersie door subordinaten in N. pulcher is het risico op predatie door grotere roofvissen zoals Lepidiolamprologus elongatus en L. attenuatus. Deze roofvissen jagen vaak in kleine (gemengde) groepen naar N. pulcher. Hierbij lopen vooral vissen die niet beschermd worden door een groep een verhoogd risico op predatie. Verschillende studies hebben laten zien dat een verhoogd predatie risico leidt tot uitgestelde dispersie door volwassen subordinaten. Doordat dominanten in een territorium relatief vaak vervangen worden (als gevolg van sterfte of dispersie) zijn grotere subordinaten zijn vaak niet verwant aan de dominanten in het territorium waar zij verblijven en wie zij helpen. Deze grotere subordinaten brengen echter wel kosten met zich mee voor de dominanten omdat zij concurreren voor de dominante positie en reproductie. Deze subordinaten moeten dus huur betalen in de vorm van helpgedrag om te compenseren voor deze kosten (“pay to stay”).

Uitgestelde dispersie Uitgestelde dispersie door individuen in coöperatief broedende soorten wordt voornamelijk toegeschreven aan een tekort aan geschikte broedgelegenheid en de baten

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die kunnen worden verkregen door in het ouderlijk territorium te blijven. Hierbij zorgen (temporeel) stabiele omgevingen voor lage sterfte onder broedpaartjes en dus voor een verzadiging van geschikte broedgelegenheid. Ruimtelijke verschillen in habi- tatkwaliteit zorgen er uiteindelijk voor dat het voor subordinaten loont om dispersie uit te stellen, en te wachten in het ouderlijk territorium tot ze elders een beter territorium kunnen krijgen. Recente studies laten echter zien dat coöperatief broeden in zoogdieren en vogels vaker voorkomt in gebieden waar condities het meest variabel zijn. De mate waarin dit patroon afhankelijk is van veranderingen in dispersie en de neiging tot groepsvorming, of de baten van helpen door subordinaten onder slechte omstandigheden is onduidelijk. In hoofdstuk 3 laat ik zien dat, in de Seychellenzanger, uitgestelde dispersie en groepsvorming geassocieerd zijn met variatie in voedselbeschikbaarheid. Nakomelingen zijn eerder geneigd om te vertrekken uit het ouderlijk territorium in jaren dat voedselbeschikbaarheid hoog is, en de kosten van dispersie en broeden lager.

Het risico op predatie heeft weinig aandacht gekregen als aanjager groepsvorming en coöperatief broeden. Predatie heeft echter belangrijke effecten op de kosten van dispersie, de baten van het leven in groepen op overleving en de noodzaak van samenwerking voor reproductie, die allemaal een rol kunnen spelen in uitgestelde dispersie. In hoofdstuk 2 van dit proefschrift laat ik de gevolgen zien van natuurlijke variatie in predatie-risico tussen verschillende populaties van N. pulcher voor socialiteit. Ik laat zien dat groepen in populaties waar het risico op predatie hoger is meer grote subordinaten hebben, die belangrijk zijn voor de verdediging tegen predatoren. Deze be- vinding wordt ondersteund door eerder experimenteel werk dat een relatie laat zien tussen predatierisico en uitgestelde dispersie. Predatie speelt ook een belangrijke rol in de Seychellenzanger, waar nestpredatie de belangrijkste oorzaak van reproductief falen is. In hoofdstuk 6 laat ik zien dat alleen dominante mannen bij de Seychellenzan- ger reageren op korte termijn veranderingen in predatie risico en dat hun investering lager is als zij hulp hebben van een vrouwelijke subordinaat. Nestpredatie vindt alleen plaats als nesten onbewaakt zijn. Hulp bij incubatie door vrouwelijke subordinaten kan dus ook een effectieve strategie zijn om het risico op nestpredatie te verminderen. In box A laat ik zien dat ruimtelijke variatie in dichtheden van Seychellenwevers – en dus het risico op nestpredatie – leidt tot uitgestelde dispersie van vrouwelijke subordinaten, een hogere kans dat deze subordinaten een ei leggen in hetzelfde nest als de dominant en vaker helpen bij incubatie.

De baten van coöperatief broeden De directe baten van helpgedrag voor subordinaten kunnen voldoende zijn om samen-

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werking in stand te houden. Dit soort directe baten zijn bijvoorbeeld het verhogen van de groepsgrootte (“group augmentation”) – als het hebben van een grotere groep voordelen met zich meebrengt – of verhoogd reproductief succes van alle groepsleden als gevolg van samenwerking (“mutualisme”). Ook indirecte baten – door het helpen van verwanten – vormen een belangrijke verklaring voor altruïstisch helpgedrag in coöpe- ratief broedende soorten. De directe en indirecte baten van samenwerking zijn vaak afhankelijk van omgevingsfactoren. Zo kunnen de baten van helpgedrag bijvoorbeeld alleen zichtbaar worden bij een lage voedselbeschikbaarheid, of hoge predatiedruk, waarbij subordinaten nodig zijn om succesvol jongen groot te brengen. Het kwanti- ficeren van de kosten en baten van samenwerking in relatie tot dit soort omgevingsfactoren is dus belangrijk om het behoud en de evolutie van coöperatief broeden te begrijpen.

In hoofdstuk 3 en 4 laat ik zien dat de baten van samen broeden door vrouwen in de Sey- chellenzanger waarschijnlijk mutualistisch zijn. Het per capita reproductief succes van individuen in groepen met enkel vrouwelijke subordinaten is niet verschillend van dat van paren. Verder is het zo dat deze groepen een lagere variatie in reproductief succes vertonen, wat een belangrijk onderdeel van fitness (een relatieve maat voor hoe succesvol individuen genen doorgeven naar toekomstige generaties) kan zijn, vooral onder de condities waar coöperatief broedende dieren vaak in leven. In hoeverre de mate van variatie in reproductief succes bijdraagt aan fitness in de Seychellenzanger, is nog onbekend. Het schatten van fitness in fluctuerende omgevingen is moeilijk, maar er zijn recent technieken ontwikkeld die dit in de toekomst mogelijk maken. Onze studie laat zien dat samen broeden mogelijk fitnessbaten met zich meebrengt voor vrouwelijke Seychellenzangers, onafhankelijk van beperkingen op dispersie en de mogelijkheid om alleen te broeden. Deze conclusie wordt deels ondersteund door hoofdstuk 3, waar ik laat zien dat voornamelijk vrouwelijke subordinaten in sommige gevallen toegela- ten worden tot andere groepen.

Recente studies suggereren dat coöperatief broeden vaker voorkomt in gebieden met hoge temporele variabiliteit in omgevingsomstandigheden. Zulke patronen worden voornamelijk uitgelegd door te stellen dat subordinaten reproductie mogelijk maken onder slechte omstandigheden. In hoofdstuk 3 laat ik echter zien dat jaarlijkse reproductie onafhankelijk is van voedselbeschikbaarheid, maar dat groepen met vrouwelijke subordinaten een hoger reproductief succes hebben dan groepen met een andere samenstelling. Het gegeven dat reproductief succes onafhankelijk lijkt te zijn van voedselbeschikbaarheid suggereert dat voedselbeschikbaarheid nooit onder een ni- veau komt waar reproductie hieronder lijdt, of dat vogels dit opvangen door zelf extra

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(lange termijn) kosten op te lopen. Dit laatste zou kunnen betekenen dat hulp door subordinaten belangrijker is voor de overleving van dominanten, dan voor reproductief succes. Een eerdere studie laat echter zien dat de overleving van vogels omlaag gaat in grotere groepen. Dit tegenstrijdige resultaat zou deels verklaard kunnen worden door een voorlopige analyse die laat zien dat subordinate vrouwen vaker helpen in jaren met hoge voedselbeschikbaarheid. Dit suggereert dat de kosten van hulp hoger zijn als er weinig voedsel beschikbaar is, en dat hulp dus conditie-afhankelijk is.

In hoofdstuk 5 laat ik zien dat de baten van hulp door subordinaten in N. pulcher pas duidelijk worden onder verhoogd predatierisico. Territoria in populaties met veel predatoren laten een positieve relatie zien tussen reproductief succes en het aantal subordinaten. In populaties met een laag predatierisico is het reproductief succes ge- middeld hoger, maar onafhankelijk van het aantal subordinaten in de groep. Dit is in overeenstemming met eerder werk aan N. pulcher, en laat zien dat het hebben van subordinaten belangrijk is voor de bescherming en overleving van juveniele vissen.

GROEPSSTABILITEIT

Individuen die in groepen leven zijn vaak met elkaar in conflict omdat ze concurreren om beperkte middelen. Dit soort conflict kan de fitnessbaten van groepsleven of samenwerking verminderen of zelfs ongedaan maken en daarmee dus de evolutie van socialiteit in de weg staan. Individuen worden echter geacht om meer te investeren in samenwerking als de baten van samenwerking (of de kosten van competitie) hoger zijn. In N. pulcher kan conflict plaatsvinden op meerdere organisatieniveaus: individuen in groepen concurreren om status en reproductie, en tussen groepen is er competitie om ruimte en schuilplekken die nodig zijn voor reproductie. Het leven in hogere dichtheden (grotere groepen of groepen dichter op elkaar) levert echter ook voordelen op in de vorm van een betere bescherming tegen predatoren. In hoofdstuk 5 laat ik zien dat een verhoogd predatierisico agressie tussen individuen binnen groepen vermin- dert: dominanten zijn minder agressief naar subordinaten en subordinaten tonen ook minder agressie naar elkaar. Agressie tussen naburige groepen is echter onafhankelijk van het risico op predatie. Dit is, voor zover ik weet de eerste studie die verminderd sociaal conflict laat zien als gevolg van een verhoogd predatierisico. Agressie in N. pulcher kent ten minste twee verschillende functies: als aansporing voor subordinaten om meer te helpen, en als manier om reproductie door subordinaten te onderdrukken. Als agressie voornamelijk dient om reproductie te onderdrukken, zouden subordinaten in groepen onder hoge predatiedruk een groter aandeel van de totale groepsreproductie

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moeten hebben. Er zijn echter nog geen studies die deze hypothese kunnen bevestigen of ontkrachten. Toekomstige studies die de link tussen predatierisico, sociaal conflict en subordinate reproductie onderzoeken, zouden in staat zijn om de rol van predatie op groepsvorming in N. pulcher te achterhalen.

Groepen Seychellenzangers zijn vaak stabiel over meerdere jaren en agressieve interac- ties tussen groepsleden zijn zeldzaam. Toch is er sterk bewijs dat individuen regelma- tig uit een groep gezet worden, voornamelijk nadat een mannelijke dominant in een groep wordt vervangen. In hoofdstuk 3 laat ik zien dat subordinaten minder geneigd zijn te vertrekken uit een groep in jaren dat de voedselbeschikbaarheid laag is. Om- dat reproductief succes onafhankelijk lijkt te zijn van voedselbeschikbaarheid, wordt dit resultaat waarschijnlijk het beste verklaard door lagere kosten van dispersie en het zoeken van geschikt habitat om te broeden. In box A laat ik tevens zien dat er door nest predatie waarschijnlijk mutualistische baten ontstaan voor het gemeenschappelijk grootbrengen van jongen. Nestpredatierisico is daardoor een belangrijke factor voor groepsvorming in de Seychellenzanger.

CONCLUSIE

Als conclusie van mijn proefschrift wil ik graag drie belangrijke observaties maken. Ten eerste denk ik dat het risico op predatie ondergewaardeerd is als factor die leidt tot coöperatief broeden en transities naar complexe socialiteit. Bovenop de bekende effecten van predatie op groepsvorming, kan predatie ook effecten hebben op de kosten en baten van uitgestelde dispersie, de verdeling van taken binnen groepen en samenwerking bij het grootbrengen van jongen. Dit zijn allemaal belangrijke aspecten in transities naar complexe socialiteit en deze aspecten spelen tevens een belangrijke rol in de evolutie en het in stand houden van coöperatief broeden. Ten tweede, verschillende studies wekken de suggestie dat coöperatief broeden een vorm van risicospreiding is (“bet-hedging”). Een van de bewijzen die hiervoor wordt geleverd is dat coöperatief broeden vaker voorkomt in omgevingen die erg variabel zijn. Ik denk dat deze conclusie voorbarig is. In hoofdstuk 3 laat ik zien dat uitgestelde dispersie plaatsvind in jaren van lage voedselbeschikbaarheid, maar dat subordinaten niet dienen als buffer om lage reproductie te voorkomen in dit soort slechte jaren. Temporele omgevingsvaria- tie kan dus de transitie naar coöperatief broeden hebben gefaciliteerd door te leiden tot groepsvorming, maar niet doordat het leidt tot specifieke baten van helpgedrag. Ten derde, waar meerdere studies hebben geconcludeerd dat subordinaten het beste proberen te maken van slechte omstandigheden, zou ik willen stellen dat deze con-

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clusies kunnen veranderen als rekening gehouden wordt met de omgevingsfactoren waar individuen reproduceren. Vrouwelijke subordinaten in Seychellenzangers hebben waarschijnlijk een hogere fitness door samen te broeden met een dominant in het territorium, maar meer gedetailleerde studies van individuele fitness en reproductie- ve variantie zijn nodig om hier definitieve uitspraken over te doen. In N. pulcher zijn grote groepen nodig voor succesvolle voortplanting onder verhoogd predatierisico, en de mate waarin reproductie gedeeld wordt door individuen binnen een groep bepaalt uiteindelijk of zij hierdoor beter af zijn. Deze resultaten laten het belang zien van de ecologische omstandigheden waarin individuen leven voor de kosten en baten van co- öperatief broeden.

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Acknowledgements/ Dankwoord ACKNOWLEDGEMENTS/DANKWOORD

Clichés should be avoided at all cost, but I think that many, if not most people, trying to obtain a PhD feel like time really does fly. Thus, I now find myself in the awkward position of trying to recall and accurately reflect on the last ten years of my life. I can’t promise that I will be able to thank everyone that has helped me to get to this point, but I guess that writing an acknowledgements section somehow forces me to at least try. Probably best to start at the beginning.

In early 2008, I found myself in a Sumatran jungle holding hands with a semi-wild orang- utan and had just finished Richard Dawkin’s The Selfish Gene. I became interested in biology mainly through reading about evolutionary theory, rather than by, for instance, a particular love of birds or fishes, which has led so many others that I know to take a similar path. As a child, however, I was always interested in anything animal related, and spent most of my time outdoors. When I had finally decided that I wanted to know more about evolutionary theory and animal behaviour, the choice for Groningen was straightforward. Het eerste jaar biologie was soms taai – voornamelijk door de vele niet-ecologie vakken die door aanstaande ecologen op het beste moment werden ervaren als verplichte kost en op het slechtste moment als een vorm van zelfkastijding. Gelukkig waren er veel mensen die deze marteling dragelijker maakten. Emma, Marieke, Anneleen, Anne, Annemieke, Mar- ten en Juul: bedankt voor alle mooie tijden in de Shadrak, de sigaretjes op Marieke’s dak in het ochtendgloren die hierop volgden, strandwandelingen op Schier, uitstapjes naar Tsjechië en nachtelijke autoritjes door Berlijn. Zonder jullie aanhoudende en allesomvat- tende drang naar alcohol (en sigaretten) was studeren een stuk saaier geweest.

De laatste twee jaar van de bachelor stonden steeds meer in het teken van ecologie en werd de club met gelijkgestemde studenten kleiner. Hier beginnen voor mij de eerste herinneringen aan de colleges, practica en excursies waardoor ik in eerste instantie biologie wilde studeren. Er zijn veel mensen die hier een bijdrage aan hebben geleverd – teveel om op te noemen. Toch wil ik enkelen in het specifiek bedanken, omdat ze mij allemaal iets belangrijks hebben geleerd over het doen van onderzoek. Ten eerste Joost Tinbergen. Joost was en is voor mij zowel als voor zoveel andere studenten een voorbeeld van een kritische denker met een groot hart voor onderzoek. Ik vind het spijtig dat we tijdens mijn MSc (en daarna) niet meer hebben mogen samenwerken en discussiëren over de perikel- en van de wetenschap. Marten Staal en Theo Elzenga. Ik hoop niet dat ik jullie beledig als ik zeg dat het zien van ecofysiologie van planten als een van de vakken in het curriculum niet direct mijn hart sneller liet kloppen. Toch weten jullie met jullie enthousiasme, humor en kundigheid een fantastische cursus neer te zetten waar ik oprecht van heb ge- noten en geleerd. Ik wil Maarten Schrama en Roel van Klink bedanken voor mooie tijden op Schier en Friesland buitendijks. Het had niet veel gescheeld, of door jullie toedoen had

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ik de overstap gemaakt naar community ecology, al was het alleen maar zodat ik met een bladzuiger arthropoda uit vers geknipt gras kon samplen. Deze kwelderervaring was natuurlijk niet mogelijk geweest zonder Jelle (“het beest van Bedum”) en Emma, waarmee ik elke ochtend voor zonsopgang tevergeefs op zoek ging naar veldleeuweriknesten.

In 2011, I was lucky enough to be admitted to the Top Programme in Ecology & Evolution in Groningen, which, for the first six months, followed the same curriculum as the Eras- mus Mundus Master in Evolutionary Biology, also referred to as MEME – a two year master programme where a handful of international students undergo an impressive amount of coursework at four different universities so that they can pursue PhD’s in their respective fields. Dear pinche Flora, pinche Paulina, Thibaud, Sara, Rachel, Angelica, Greta, Damian, Maryam, Angelica, Homa, Stefany, Francesco and Jelena: thanks for nights of heavy party- ing, nocturnal ice skating trips on the Groningen canals, introducing me to Que hora es? (the Mexican soap opera for people who only had three weeks of Spanish in the fourth grade), proper Mexican food, the proper names of Mexican food and for showing me that romantic feelings between two heterosexual men are completely normal (yes I’m refer- ring to you, Thibaud). I’d also like to thank the two people without whom this program would not have been possible: Irma, who was the coordinator of the MEME course at that time, was also the mainstay for the many international students that found themselves lost in bureaucratic Catch-22’s; and Franjo, who is probably one of the brightest minds that I know, but also an incredibly friendly, generous and witty person – not to mention a great teacher.

Na deze fantastische periode heb ik de rest van mijn MSc vervolgd in Groningen. Allereerst wil ik Ido bedanken voor het geven van een geweldige statistiekcursus die bij mij een ge- zonde interesse voor statistiek heeft aangewakkerd. Ik wil graag Peter Korsten bedanken, die mijn begeleider was tijdens mijn eerste MSc project aan de pimpelmezen in de Vosber- gen. Peter, je bent een uiterst gedreven en zorgvuldige onderzoeker en ik heb erg veel van je geleerd in het veld en daarbuiten. Ook wil ik mijn partner in crime Violet bedanken voor de mentale ondersteuning tijdens het veldwerk en de daaropvolgende weken van analyses achter de computer – alsmede voor het uiterst snelle gezamenlijke woon-werkverkeer van Groningen naar de Vosbergen op de racefiets.

For my second MSc project, I found myself first in Bern and shortly thereafter in Mpulun- gu in the Republic of Zambia. There are several people that I’d like to thank for this great opportunity and for providing such a positive and stimulating atmosphere under which to work. First of all Jo who really made me feel right at home at the Hasli and under whose supervision I was able to participate in the Pulcher research that turned out to be one of

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the cornerstones of my PhD thesis. Thank you for being such a fun supervisor and drag- ging me along to BBQ’s, birthdays, unihockey, Carnaval in Germany, running the Bernese Grand Prix, skiing and other such events, that usually involved beer. Good beer though; mostly good quality German beer. Thanks also to all the other people at the Hasli for being so welcoming. Arne, thanks for allowing me to watch the witchdoctor’s dog lick the puss from underneath your foot. That was great. Also, thanks for being such a cool guy; I’m really looking forward to hanging out more in Cambridge. Honorable mentions should also go out to Manon, for being such a passionate scientist and wine aficionado; Dario, for being a badass; and Leif, who was always there for the hard questions; Mattia, just for being an eccentric Italian; and Maria, for putting up with my inappropriate jokes. I’m also thankful for all the help I received from Claudia Leiser, without whom, I would still be battling a pile of Swiss paperwork. I would also like to say a few words about Hiro, whose tragic death during the writing of one of the last fish chapters came as an incredible shock to everyone at the Hasli. Hirokazu, thank you for all the great times at the lake, beers in Bern and elsewhere, and hikes in the mountains. You were one of the most passionate and knowledgeable cichlid researchers that I knew, and I will miss you dearly.

After I returned from Zambia, during a short conference in Beatenberg, Switzerland, Jan and Michael decided that a joint PhD project on both warblers and N. pulcher was warrant- ed. This seemed to me – at the time – like a great idea, so I set out to sharpen the questions that we had come up with. Unfortunately, due to completely foreseeable circumstances, I had to drop those questions about half a year into my PhD, and find a new topic. It was quite a long and bumpy road from there to here, and I want to take the opportunity to thank all the people that have in some way smoothed out that road. First, all the people that were involved in the Seychelles warbler project over the last few years: Hannah Ed- wards, Hannah Dugdale, Dave Wright, Jildou, Lewis, Dani, Michela, Sara, Owen, Kat, Ellie, Charli and Alex. Thanks for all your contributions to the data (including database days) and for all the fun times we had during our warbler meetings. I also want to thank David Richardson and Terry Burke for never being too busy to comment on one of my manu- scripts and always showing interest in new ideas. Thanks to Marco, without whom a lot of our work – including my own – would not have been possible. Also, I’d like to thank all the people who have made our office such a fun place to work: Reinaldo, Kat, Sara, Long, Martje, Lisheng, Sajad, Mehdi, Berber, Jildou, Xiaoyan, Qingtian and Owen. I’d like to thank all the people with whom I’ve shared a coffee during the coffee break – especially those that brought cake on a regular basis. I’d also like to thank the secretaries, Joyce and Inge- borg, for bringing a good dose of humor and perspective to the fifth floor, and for making everybody’s job a lot easier. Corine Eising’s office is usually visited by PhD’s in distress, and we also usually linger around much longer than we really need to, just for a chat. Thank

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you Corine for always being there to answer all of our questions and help out wherever you can; the institute could not do without you.

In het specifiek wil ik ook graag Martijn bedanken voor zijn enthousiasme en altijd pa- rate (literatuur) kennis van de Seychellenzangers en andere systemen. Jouw enthousiasme heeft mij altijd gemotiveerd en jouw scherpe blik en kritische houding hebben mij – hopelijk – tot een betere wetenschapper gemaakt. Natuurlijk kunnen mijn begeleiders niet ontbreken in deze lijst. Sjouke – ooit nog de begeleider van mijn BSc scriptie – en nu copromotor voor mijn promotieonderzoek. Helaas kan je er vanwege veldwerk niet bij zijn tijdens mijn verdediging, maar ik wil je bedanken voor alle steun over de laatste paar jaar, de input op mijn ideeën en onze gezamenlijke stukken, alle leuke avonden in de Toet- er, de Pintelier en op warbler meetings. Tot mijn grote blijdschap heb je tijdens deze periode ook de liefde gevonden. Bedankt dat Lian en ik op jullie bruiloft mochten zijn! Ik wil je ook graag feliciteren met je nieuwe baan in Wageningen en ik denk (nee, hoop) dat we elkaar in de toekomst nog vaker tegen zullen komen. I’d like to thank Michael, first and foremost for giving me the opportunity to join the Hasli team during my MSc. I admire your passion for science, and the way that during meetings you could quickly distill most of my unwieldy ideas into something concrete. I know that you will be retiring soon, and I wish you and Barbara all the best in the future – although something tells me that you will not let something as meaningless as retirement get between you and your work. Ik ken Jan al sinds hij ons – als tweedejaars broekies – college gaf over gedragsecologie en de Sey- chellenzangers. Zoals jij het altijd nog graag naverteld, zat ik meestal vooraan tijdens deze colleges. Jan, ik wil je bedanken dat je me de kans hebt gegeven om mijn promotietraject bij jou en Michael af te leggen en hierbij het privilege te hebben om op een van de mooiste plekken op aarde te werken – nee, niet de vijfde verdieping van de Linneausborg. Je hebt me altijd veel vrijheid gegeven om mijn eigen weg te gaan en fouten te maken. Dat laatste heb ik ook zeker veelvuldig gedaan. Soms was je wat ‘wetenschappelijk’ afwezig, maar dit maak je goed doordat je zo’n sociaal en empathisch persoon bent. Deze eigenschap en je eigenzinnigheid maakt je tot een bijzondere begeleider.

Verder wil ik graag al mijn vrienden bedanken. Ik weet alleen niet waarvoor: de meeste hebben het IQ van een soepstengel en weten waarschijnlijk nog steeds niet wat ik doe. In het specifiek wil ik graag mijn paranimf en enige slimme vriend Alex bedanken voor 20 jaar mooie vriendschap. Dat we dit geheel draaiende hebben weten te houden ondanks de afstand Groningen-Amsterdam spreekt boekdelen. Ik wil Jacq bedanken voor het maken van de prachtige tekeningen in mijn proefschrift waarmee ik geprobeerd heb de boel wat minder droog te maken – ik nodig de lezer uit om zelf te oordelen of dat is gelukt. Tim, bedankt voor het ontwerpen van mijn omslag; zonder jou was iedereen de belabberde in-

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houd veel eerder opgevallen. Ook wil ik iedereen van woongroep Bonobo bedanken voor hun morele en mentale steun terwijl ik al zwetend en zwoegend mijn promotie tot een succesvol einde heb proberen te brengen. Janne, bedankt dat je mijn paranimf wil zijn en voor het opzetten van de Bonobo breakfast discussion club. Stiekem zijn we het vaker eens dan niet, maar dat moeten we niet aan de grote klok hangen. Je bent super kritisch en eerlijk, vooral als het je eigen werk aangaat en dat maakt je een fantastische wetenschapper. Pieter, we hebben lang in hetzelfde schuitje gezeten, maar ik ben net iets eerder uitgestapt. Bedankt voor het gezelschap tijdens de fietsritjes naar het Zernike, de – soms wetenschappelijke – gesprekken tijdens deze ritten en dat je me af en toe nog iets over vogels hebt proberen bij te brengen.

Pa en ma, bedankt dat jullie mij van jongs af aan de vrijheid hebben gegeven om op onderzoek uit te gaan en het leven zelf te ontdekken. Jullie hebben mij altijd gesteund tijdens de keuzes die ik maakte, al waren die voor jullie soms toch wat ondoorzichtig en vooral ondoordacht. Zonder jullie was ik niet gekomen waar ik nu ben.

Lian, als laatste, maar zeker niet als minste. We hebben elkaar leren kennen op de plek waar we nu, bijna 9 jaar later, nog steeds samen wonen. In de tussentijd hebben we veel mooie herinneringen opgedaan, en ik hoop dat er nog vele mooie herinneringen bij zullen komen. We hebben elkaar vaak moeten missen als ik weer eens op veldwerk was in Afrika, of naar Zwitserland. Soms plande je dan bij terugkomst een gezamenlijk fietsweek- end in, die ik dan – 10 kilo lichter door het veldwerk – met frisse tegenzin moest trotseren. Het kwam uit een goed hart. Lieve Lian, je bent een fantastische vriendin en een nog veel betere moeder voor onze Pjotr, die we in de tussentijd ook nog maar even op de wereld hebben gezet. Bedankt voor je steun en liefde de afgelopen jaren en ik hoop dat we nog vele avonturen samen mogen beleven.

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