No abstract

Parasitism is ubiquitous in the animal kingdom. Although many fundamental aspects of host-parasite relationships have been unravelled, few studies have systematically investigated how parasites affect organismal movement. Here we combine behavioural experiments of Schistocephalus solidus infected sticklebacks with individual-based simulations to understand how parasitism affects individual movement ability and thereby shapes social interaction patterns. High-resolution tracking revealed that infected fish swam, accelerated, and turned more slowly than did non-infected fish, and tended to be more predictable in their movements. Importantly, the strength of these effects increased with increasing parasite load (proportion of body weight), with more heavily infected fish showing larger changes and impairments in behaviour. When grouped, pairs of infected fish moved more slowly, were less cohesive, less aligned, and less temporally coordinated than non-infected pairs, and mixed pairs were primarily led by the non-infected fish. These social patterns also emerged in simulations of self-organised groups composed of individuals differing similarly in speed and turning tendency, suggesting infection-induced changes in mobility and manoeuvrability may drive collective outcomes. Together, our results demonstrate how infection with a complex life-cycle parasite affects the movement ability of individuals and how this in turn shapes social interaction patterns, providing important mechanistic insights into the effects of parasites on host movement dynamics. Parasitism is ubiquitous across the animal kingdom, with parasites often exerting considerable influence on their hosts by consuming energy and inducing morphological, physiological, and behavioural changes 1-3. Parasites have been best studied in terms of their ecological and evolutionary effects on hosts 1,4 , but may also have large effects on host behaviour 2. Besides potential manipulation of the host, parasites also often change their host's morphology and physiology, which may strongly alter its movement dynamics 2,5 , such as by reducing the energy available to allocate to movement or by compromising their movement capacity and mobility. So far, few studies have systematically investigated the mechanistic basis of such potential behavioural modifications 2,5 or considered the repercussions this may have for social interactions and collective outcomes via self-organising effects 6,7. Three-spined sticklebacks (Gasterosteus aculeatus) infected with the flatworm Schistocephalus solidus are a host-parasite model system with well-documented parasite effects on host behaviour 8,9. S. solidus is a complex life-cycle parasite that has to sequentially infect a copepod, the three-spined stickleback, and a fish-eating bird to survive and reproduce. It is often proposed that parasites with complex life cycles manipulate their host's behaviour in order to increase their probability of transmission to their final host 4. However, the parasite may also affect behaviour via energ...

Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly-dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide insights into predator decision-making, but show which key spatial and kinematic features of predator and prey predict the risk of individuals to be targeted and to survive attacks. We found that pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal 'strike zone' the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks were successful (70%), targeted individuals that did manage to avoid being captured exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey underlying the predation risk within mobile animal groups.

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Parasitism is ubiquitous in the animal kingdom. Although many fundamental aspects of hostparasite relationships have been unravelled, few studies have systematically investigated how parasites affect organismal movement. Here we combine behavioural experiments of Schistocephalus solidus infected sticklebacks with individual-based simulations to understand how parasitism affects individual movement ability and how this in turn influences social interaction patterns. Detailed movement tracking revealed that infected fish swam slower, accelerated slower, turned more slowly, and tended to be more predictable in their movements than did non-infected fish. Importantly, the strength of these effects increased with increasing parasite load (% of body weight), with the behaviour of more heavily infected fish being more impaired. When grouped, pairs of infected fish moved more slowly, were less cohesive, less aligned, and less coordinated than healthy pairs. Mixed pairs exhibited intermediate behaviours and were primarily led by the non-infected fish. These social patterns emerged naturally in model simulations of self-organised groups composed of individuals with different speeds and turning tendency, consistent with changes in mobility and manoeuvrability due to infection. Together, our results demonstrate how infection with a complex life cycle parasite affects the movement ability of individuals and how this in turn shapes social interactions, providing important mechanistic insights into the effects of parasites on host movement dynamics.

To effectively balance the need to forage against the need to avoid predation, animals should utilize information from both their physical and social environments. However, most studies have considered these factors in isolation and few have investigated how animals change the use of these cues temporally. Using novel 3D modeling of the environment and 3D observations of fish movement, we investigated how local abiotic and biotic features of the environment, along with tidal patterns, impacted risk‐related behaviors using humbug damselfish, Dascyllus aruanus, in coral reef habitats as a model system. We found that damselfish balance risk by utilizing cues from both the physical and the social environment, although the relative importance of these cues changes according to tide. At flowing tide, when food resources are typically more abundant, damselfish increased their foraging behavior, but only when their external social environment offered protection from predation. At slack tide, when food resources are typically less abundant, damselfish were not responsive to their external social environment. Regardless of tide, damselfish living in smaller corals showed more risk‐averse behavior, emphasizing the importance of local refuge availability on risk perception. Our results underscore the flexible use of social and physical information along temporal scales and how both biotic and abiotic features influence the trade‐off adopted between foraging and refuging behavior.

Sexual conflict occurs when selection to maximize fitness in one sex does so at the expense of the other sex. In the burying beetle Nicrophorus vespilloides, repeated mating provides assurance of paternity at a direct cost to female reproductive productivity. To reduce this cost, females could choose males with low repeated mating rates or smaller, servile males. We tested this by offering females a dichotomous choice between males from lines selected for high or low mating rate. Each female was then allocated her preferred or non-preferred male to breed. Females showed no preference for males based on whether they came from lines selected for high or low mating rates. Pairs containing males from high mating rate lines copulated more often than those with low line males but there was a negative relationship between female size and number of times she mated with a non-preferred male. When females bred with their preferred male the number of offspring reared increased with female size but there was no such increase when breeding with non-preferred males. Females thus benefited from being choosy, but this was not directly attributable to avoidance of costly male repeated mating.

Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly-dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide detailed insights into predator decision-making but show which key spatial and kinematic features of predator and prey influence individual's risk to be targeted and survive attacks. Pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal "strike zone" the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks (70%) were successful, targeted individuals that did manage to avoid capture exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey in determining predation risk in mobile animal groups.