Social integration of macroparasites in ant societies: ultimate and proximate mechanisms

Ant colonies are commonly parasitized simultaneously by several species. While some parasites are recognized and attacked by their ant hosts, others have apparently cracked the ants’ recognition code and interact mainly peacefully with their hosts. Although such apparent differences in social integration among ant parasites have been described, the underlying mechanisms resulting in differential integration remain mostly unknown. Using Leptogenys army ants and their parasites, I studied ultimate mechanisms that might be responsible for differing integration levels by comparing the strength of host defence with the negative impact of parasites. In addition, I investigated proximate mechanisms of differing integration levels by evaluating the role of chemical deception by mimicry. The interactions of several parasitic beetle species with their Leptogenys hosts revealed that particular species fed on host larvae, while others did not. The hosts’ aggressiveness was enhanced towards brood-killing species, while non-predatory species received almost no aggression, resulting in social integration. Accordingly, the fitness costs of parasites likely influence the evolution of host defences against them in a multi-parasite situation. The role of chemical mimicry has been investigated in detail for two kleptoparasites, namely the silverfish Malayatelura ponerophila and the spider Gamasomorpha maschwitzi. By analyzing the transfer of a chemical label from the host ants to the parasites, I empirically demonstrated for the first time that ant parasites are able to acquire mimetic compounds from their host. Additional biosynthesis of mimetic compounds seems unlikely in both parasites, since the concentration of each cuticular hydrocarbon decreased in individuals that were isolated from the host. In addition, a high accuracy in chemical host resemblance was shown to be beneficial for the social integration of both parasites. Reduced accuracy in chemical host resemblance resulted either in aggressive host responses towards the silverfish or elevated host inspection behaviour towards the spider. The degree of dependency on chemical mimicry to achieve social integration differed considerably between the two parasites, however. Accordingly, the parasites’ level of social integration is affected by ultimate mechanisms such as the negative impact on the host as well as by proximate mechanisms such as the degree of accuracy in chemical host resemblance

The trophic ecology of non-native ants on Round Island, Mauritius

Summary Non-native ants are implicated in the demise of native species around the world, though their trophic ecology remains poorly understood. Non-native ants have invaded Round Island, a globally significant site of biodiversity conservation located 21 km north-east of Mauritius in the Indian Ocean, but it is unclear how they are affecting the unique ecological community found there. To reveal their potential impact, I conducted a meta-analysis into the effects of non-native ants on animal community diversity in relatively undisturbed areas around the world, showing that non-native ants drive diversity declines in local animal communities by approximately 50 % on average (Chapter 2). I then examined the ecological role of non-native ants on Round Island specifically and first determined, using dietary DNA metabarcoding, whether an abundant native omnivore, Telfair’s skink, consumed non-native ants. Skinks do consume ants, though it was unclear to what degree these detections were deliberate or accidental (Chapter 3). I then identified the diet of the 12 most numerous non-native ant species on Round Island using dietary metabarcoding, revealing that all ant species showed unique generalist diet profiles and together consume over 150 species of animals and plants. The diet of the ant community was also driven by seasonal changes in food availability. This presents the first study to date detailing the diet of individual ants at the community level and that a community of generalist non-native species exhibit dietary niche separation (Chapter 4). I compared the diet of native skinks and centipedes with that of non-native ants, finding that skinks are not competing with ants for food, whilst centipedes are (Chapter 5). Overall, our results suggest, through five separate lines of evidence arising from the study, that non-native ants are having a significant impact on the Round Island ecosystem

Organisation of foraging in ants

In social insects, foraging is often cooperative, and so requires considerable organisation. In most ants, organisation is a bottom-up process where decisions taken by individuals result in emergent colony level patterns. Individuals base their decisions on their internal state, their past experience, and their environment. By depositing trail pheromones, for example, ants can alter the environment, and thus affect the behaviour of their nestmates. The development of emergent patterns depends on both how individuals affect the environment, and how they react to changes in the environment. Chapters 4 – 9 investigate the role of trail pheromones and route memory in the ant Lasius niger. Route memories can form rapidly and be followed accurately, and when route memories and trail pheromones contradict each other, ants overwhelmingly follow route memories (chapter 4). Route memories and trail pheromones can also interact synergistically, allowing ants to forage faster without sacrificing accuracy (chapter 5). Home range markings also interact with other information sources to affect ant behaviour (chapter 6). Trail pheromones assist experienced ants when facing complex, difficult-to-learn routes (chapter 7). When facing complicated routes, ants deposit more pheromone to assist in navigation and learning (chapter 7). Deposition of trail pheromones is suppressed by ants leaving a marked path (chapter 5), strong pheromone trails (chapter 7) and trail crowding (chapter 8). Colony level ‘decisions’ can be driven by factors other than trail pheromones, such as overcrowding at a food source (chapter 9). Chapter 10 reviews the many roles of trail pheromones in ants. Chapters 11 – 14 focus on the organisation of cooperative food retrieval. Pheidole oxyops workers arrange themselves non-randomly around items to increase transport speeds (chapter 11). Groups of ants will rotate food items to reduce drag (chapter 12). Chapters 13 and 14 encompass the ecology of cooperative transport, and how it has shaped trail pheromone recruitment in P. oxyops and Paratrechina longicornis. Lastly, chapter 15 provide a comprehensive review of cooperative transport in ants and elsewhere

Ownership conflicts and their resolution

Game theory has been used to investigate a wide range of evolutionary questions, and has been important in explaining apparently selfish patterns in animal behaviour, and behaviours that do not appear to benefit the individual. The modelling chapters in this thesis develop new game theory approaches to modelling animal conflict, investigating the acquisition of territories and the trade-offs that occur between behaviours. Many game theory models of conflicts between individuals make predictions regarding the duration of fights in relation to asymmetries in resource holding potential (RHP). Duration is often interpreted as a result of mutual assessment of RHP, allowing the weaker individual to avoid costly interactions. However, the duration of a contest may also be the result of each individual persisting to a threshold determined by its own RHP, in fiddler crabs, Uca mjoebergi, I show that duration of contests increases with increasing size of the loser, and decreases, but to a lesser extent, with increasing size of the winter, suggesting that neither the mutual assessment or individual threshold hypothesis can explain fight duration in this species. Instead, individual cost thresholds may determine duration, but larger opponents may inflict costs more rapidly, consistent with the cumulative assessment game of animal conflict. In animal contests, the larger opponent is often victorious, but contests are often initiated by individuals that have little chance of winning (generally smaller individuals). A number of hypotheses may explain this behaviour, including a lack of alternative options (the ‘desperado effect’). Recent work has suggested that likely losers attack first due to an error in perception: they mistakenly perceive their chances of winning as being greater than they are. Using a game theoretical model, I show that if smaller individuals can accurately assess their chance of winning, if this chance is relatively high, and if they have few alternative options, they are predicted to be as aggressive as their larger opponents. In addition, when resources are abundant, and small individuals have some change of winning, they may be more aggressive than their larger opponents. Using a game theory model, I show that avoidance of a single fight location can be adaptive if the benefits of access to the area are low compared to the costs of fighting. Low fight costs and high population densities lead to the break down of territoriality and the formation of large, overlapping home ranges

Scalable Control Strategies and a Customizable Swarm Robotic Platform for Boundary Coverage and Collective Transport Tasks

abstract: Swarms of low-cost, autonomous robots can potentially be used to collectively perform tasks over large domains and long time scales. The design of decentralized, scalable swarm control strategies will enable the development of robotic systems that can execute such tasks with a high degree of parallelism and redundancy, enabling effective operation even in the presence of unknown environmental factors and individual robot failures. Social insect colonies provide a rich source of inspiration for these types of control approaches, since they can perform complex collective tasks under a range of conditions. To validate swarm robotic control strategies, experimental testbeds with large numbers of robots are required; however, existing low-cost robots are specialized and can lack the necessary sensing, navigation, control, and manipulation capabilities. To address these challenges, this thesis presents a formal approach to designing biologically-inspired swarm control strategies for spatially-confined coverage and payload transport tasks, as well as a novel low-cost, customizable robotic platform for testing swarm control approaches. Stochastic control strategies are developed that provably allocate a swarm of robots around the boundaries of multiple regions of interest or payloads to be transported. These strategies account for spatially-dependent effects on the robots' physical distribution and are largely robust to environmental variations. In addition, a control approach based on reinforcement learning is presented for collective payload towing that accommodates robots with heterogeneous maximum speeds. For both types of collective transport tasks, rigorous approaches are developed to identify and translate observed group retrieval behaviors in Novomessor cockerelli ants to swarm robotic control strategies. These strategies can replicate features of ant transport and inherit its properties of robustness to different environments and to varying team compositions. The approaches incorporate dynamical models of the swarm that are amenable to analysis and control techniques, and therefore provide theoretical guarantees on the system's performance. Implementation of these strategies on robotic swarms offers a way for biologists to test hypotheses about the individual-level mechanisms that drive collective behaviors. Finally, this thesis describes Pheeno, a new swarm robotic platform with a three degree-of-freedom manipulator arm, and describes its use in validating a variety of swarm control strategies.Dissertation/ThesisDoctoral Dissertation Mechanical Engineering 201

Nesting Ecology, Management and Population Genetics of Bumblebees: An Integrated Approach to the Conservation of an Endangered Pollinator Taxon

Bumblebees have shown both long and short-term declines throughout their range. These declines may be attributed to a range of factors including changes in land use, alterations in climatic conditions and species introductions. However, management strategies for bumblebee conservation often focus on provision of summer forage resources and other factors are frequently overlooked. Provision of spring forage and nesting sites for bumblebee queens are rarely considered, though colony foundation and early colony growth are two of the most sensitive stages in bumblebee life history. Here, the efficacy of certain agri-environment prescriptions for providing spring forage and nest sites for bumblebees is assessed, highlighting a need for specific schemes targeted towards the provision of these vital resources in the rural environment. The nesting ecology of bumblebees is poorly understood because wild colonies are difficult to locate. However, a greater knowledge of the colony-level effects of environmental change is crucial to understanding bumblebee declines. Attracting bumblebee queens to nest in artificial domiciles could provide a valuable tool for studying colony-level responses. However, domicile trials and the findings of a literature review presented here demonstrate that this approach may be largely impractical for use in the UK. Conversely, a nationwide public bumblebee nest survey produced numerous data regarding nest site preferences among bumblebee species and also demonstrated that citizen science may also provide a sensitive method for detecting declines in currently common bumblebee species. An understanding of the ecology of species interactions and coexistence can provide valuable insights into factors that may influence declines. Data presented here suggest that coexistence between some bumblebee species may be maintained by resource partitioning based on diel activity patterns that are linked to species-specific environmental tolerances. If this is the case, the potential role of climate change in bumblebee declines may be severely underestimated. There is also increasing evidence that genetic factors may play a role in bumblebee losses, accelerating declines of small, fragmented populations as a result of reduction in genetic diversity and inbreeding depression. Here, the feasibility of reintroducing British B. subterraneus (now extinct in the UK) from New Zealand into England is assessed using population genetic techniques. The findings suggest that the population history of B. subterraneus in New Zealand has resulted in a dramatic loss of genetic diversity and high genetic divergence from the original UK population, suggesting that it may not be a suitable for use in the reintroduction attempt. This work draws together some understudied aspects of bumblebee ecology with a particular focus on nest site requirements, availability of spring forage, mechanisms of avoidance of inter-specific competition and population genetic processes. The potential role of these in bumblebee declines is considered and new data relevant to the conservation of these important species is presented. It is hoped that this work will inform future management strategies for bumblebee conservation, highlight areas in need of further study and provide a sound starting point for future research in these areas

Miniaturisation of sensory systems in ants

The main focus of this thesis is the study of sensory systems in the context of changing body-size. In particular the study of ant sensory systems and how these are shaped by miniaturisation. The study of insect visual ecology and physiology is used as a basis to develop a framework for the study of ant antennal sensilla and chemosensation, to interpret anatomical variation from a functional and organ design perspective. This thesis reviews the anatomy and nomenclature of antennal sensilla through two case studies on an extremely large species Myrmecia pyriformis and a small species Temnothorax rugatulus. These two studies additionally quantify intraspecific variation and discuss the potential functional consequences of this variation for self-organising insect societies and task allocation. A large scale comparative study takes the tools developed in previous chapters to focus in on how chemosensilla vary in their numbers, size and distribution through the Fomicid phylogeny. The gross anatomy of the antenna and changes in shape from club to filiform antennae are described in detail. Anatomical data are analysed to identify scaling trends and potential adaptations driven by miniaturisation. Ecological and phylogenetic considerations are discussed wherever relevant. The wide ranging impacts of body size changes are reviewed, incorporated into the interpretation of results and used to propose promising avenues for future research. Finally, ant body size and some of the different methods used in the literature to measure size and size variability are critically analysed. The functional implications of body size variability within species are discussed using Iridomyrmex purpureus as an example. This thesis makes use of a variety of microscopy techniques. In addition to the methods sections of each chapter a dedicated methods chapter is included. This chapter reviews some of the techniques used in the main data chapters and in the additional publications produced over the course of this thesis