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Individual Cognition and Collective Behaviour in Ants

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Individual Cognition and Collective Behaviour in Ants Individual cognition and collective behaviour in ants DISSERTATION ZUR ERLANGUNG DES DOKTORGRADES DER NATURWISSENSCHAFTEN (DR. RER. NAT.) DER FAKULTÄT FÜR BIOLOGIE UND VORKLINISCHE MEDIZIN DER UNIVERSITÄT REGENSBURG vorgelegt von Felix Benjamin Oberhauser aus Linz, Oberösterreich im Jahre 2019 Das Promotionsgesuch wurde eingereicht am: 12.07.2019 Die Arbeit wurde angeleitet von: Dr. Tomer J. Czaczkes Unterschrift: Lasius niger foragers drinking at a sucrose drop, filling their crop before returning to the nest to unload the collected fluid to their nest mates. While feeding, the crop extends and leads to swelling of the gaster, forcing the rigid sclerites apart and revealing the soft membrane underneath. © Oberhauser FB | iv Abstract Eusocial insects are impressive on individual and collective level. Collectively, they build nests and efficiently exploit and monopolise nearby resources by sharing information amongst their members. Such collective behaviours are shaped by remarkable and multi-facetted individual abilities and decision-making processes. By revealing and investigating factors which influence individual decision making, this thesis provides a deeper insight into the cognitive lives of ants while contributing to a more cohesive understanding of colony behaviour as a whole. In chapter 2, we demonstrated that foraging ants form expectations about value-neutral qualities of a food source – such as its taste – and dislike food which deviates from those expectations. As such dislike is translated into reduced recruitment, it will have a direct impact on colony-level behaviour. Expectations are thus a potential driver of foraging decisions. Ants excel in navigation, and we showed in chapter 3 that ants can rapidly learn olfactory or spatial cues to localise food sources. Moreover, when those two types of private information where put into conflict, ants exclusively relied on olfaction. This demonstrates that one type of information can entirely dominate decisions in certain situations. While we demonstrated that ants learn simple associations rapidly, nothing was known about their ability to learn abstract relations between stimuli, although concept learning has been reported in honeybees. Thus, in chapter 4, we trained ants to learn a relational rule of same/different, but found that the ants, instead of solving such a complex task via learning, resorted to heuristics such as ‘go left’ or ‘go to the more salient cue’. Intriguingly, the heuristics used varied between individual ants. Learning is dependent on reward and motivation and in chapter 5 we investigated whether those factors alone could explain individual and collective foraging behaviour. While we only found small effects of reward magnitude and motivation on learning, persistence rates varied dramatically in lower motivated colonies. An agent-based model using the empirical data further demonstrated that individual decisions alone can cause ecologically sensible colony-level foraging behaviour. Finally, in chapter 6 we explored whether colonies could make sensible collective decisions in the context of trail-clearing by Australian meat ants. We found that ant colonies preferentially cleared trails toward a food source if the alternative detours were long. The underlying mechanisms seem to be dependent on individual propensities to remove obstacles which leads to the emergence of paths. Taken together, the results of this thesis broaden our understanding of individual cognition in ants and demonstrate that properties inherent to individuals, such as experience or task propensities, systematically influence decisions and thus impact the collective. v | Work arising from this thesis This thesis is composed of the following five manuscripts, three of which are published, one is in revision and one in preparation for publication: A. Oberhauser FB, Czaczkes TJ (2018) Tasting the unexpected: Disconfirmation of expectations leads to lower perceived food value in an invertebrate. Biol Lett 14. doi: 10.1098/rsbl.2018.0440 B. Oberhauser FB, Koch A, Czaczkes TJ (2018) Small differences in learning speed for different food qualities can drive efficient collective foraging in ant colonies. Behav Ecol Sociobiol 72:1–10. doi: 10.1007/s00265-018-2583-6 C. Oberhauser FB, Schlemm A, Wendt S, Czaczkes TJ (2019) Private information conflict: Lasius niger ants prefer olfactory cues to route memory. Anim Cogn. doi: 10.1007/s10071-019-01248-3 D. Oberhauser FB, Middleton EJT, Latty T, Czaczkes TJ (under review, J Exp Biol) Meat ants cut more trail shortcuts when facing long detours. E. Oberhauser FB, Koch A, de Agrò M, Czaczkes TJ (to be submitted) Ants resort to heuristics when facing complex tasks. During the course of this thesis I also contributed to manuscripts and projects which are not part of this work: F. Jones S, Czaczkes TJ, Gallager AJ, Oberhauser FB, Gourlay E, Bacon JP (accepted) Copy when uncertain: Lower light levels increase trail pheromone deposition and reliance on pheromone trails in ants. Anim Behav G. de Agrò M., Oberhauser FB, Loconsole M, Galli G, Dal Cin F, Moretto E, Regolin L (In preparation) Episodic-like memory and information integration in the black garden ant. H. Oberhauser FB, Wendt S, Czaczkes TJ (In preparation) Social information in the form of pheromone trails does not distort perceived value in ants. I. Oberhauser FB, Bogenberger K, Czaczkes TJ (In preparation) Primacy effect in ants. | vi Author contributions Manuscript A Tomer J. Czaczkes (TJC) and Felix B. Oberhauser (FBO) conceived the experiment, FBO collected, analysed and visualised the data, FBO wrote the manuscript, FBO and TJC revised the manuscript. Manuscript B TJC conceived the experiment, FBO and Alexandra Koch (AK) collected the data, TJC wrote the agent-based model, FBO analysed the data, FBO and TJC visualised the data, TJC and FBO wrote ESM5-1 & ESM5-2, FBO wrote the manuscript, FBO and TJC revised the manuscript. Manuscript C TJC and FBO conceived the experiments, Annika Schlemm (AS) and Stephanie Wendt (SW) collected the data, FBO analysed and visualised the data, FBO wrote the manuscript, FBO, TJC, AS and SW revised the manuscript. Manuscript D TJC, Tanya Latty (TL) and FBO conceived the experiment, FBO and Eliza J. T. Middleton (EJTM) collected the data, FBO analysed and visualised the data and wrote the ant tracker, FBO wrote the manuscript, FBO, TJC, TL and EJTM revised the manuscript. Manuscript E FBO and TJC conceived the experiment, FBO and AK collected the data, FBO and Massimo de Agrò (MdA) analysed the data, FBO visualised the data, FBO wrote the manuscript, FBO, TJC and MdA revised the manuscript. vii | Table of contents Abstract ............................................................................................................................... v Work arising from this thesis ....................................................................................................... vi Author contributions ................................................................................................................... vii Table of contents ........................................................................................................................ viii How this thesis developed ........................................................................................................... xi Chapter 1 General introduction .................................................................................................................. 1 1.1 Overview ....................................................................................................................... 1 1.2 Foraging and signalling ................................................................................................. 2 1.3 Value perception ........................................................................................................... 3 1.4 Learning in social insects .............................................................................................. 5 1.5 Collective behaviour ..................................................................................................... 9 1.6 Lasius niger as a model organism ............................................................................... 10 1.7 Aims of this thesis ....................................................................................................... 11 Chapter 2 Tasting the unexpected: disconfirmation of expectations leads to lower perceived food value in an invertebrate ....................................................................... 13 2.1 Abstract ....................................................................................................................... 13 2.2 Introduction ................................................................................................................. 14 2.3 Methods overview ....................................................................................................... 15 2.4 Results ......................................................................................................................... 16 2.5 Discussion ................................................................................................................... 17 2.6 Supplementary manuscript (shortened version of ESM2-1) ....................................... 20 Chapter 3 Private information conflict: Lasius niger ants prefer olfactory cues to route memory .... 29 3.1 Abstract ......................................................................................................................
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