University of Groningen Better together Groenewoud, Frank IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2018 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Groenewoud, F. (2018). Better together: Cooperative breeding under environmental heterogeneity. University of Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. 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 by 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 con- duct 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 coop- erative 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 be- tween 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 sub- ordinates 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 ap- proaches 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 like- ly 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, spe- cifically 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