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Parasitism, personality and cognition in fish

Barber I, Mora AB, Payne EM, Weinersmith KL and Sih A.
Behavioral Processes, in press

It is well established that parasites can have profound effects on the behaviour of host organisms, and that individual differences in behaviour can influence susceptibility to parasite infections. Recently, two major themes of research have developed. First, there has been a growing interest in the proximate, mechanistic processes underpinning parasite-associated behaviour change, and the interactive roles of the neuro-, immune, and other physiological systems in determining relationships between behaviour and infection susceptibility. Secondly, as the study of behaviour has shifted away from one-off measurements of single behaviours and towards a behavioural syndromes/personality framework, research is starting to focus on the consequences of parasite infection for temporal and contextual consistency of behaviour, and on the implications of different personality types for infection susceptibility. In addition, there is increasing interest in the potential for relationships between cognition and personality to also have implications for host-parasite interactions. As models well-suited to both the laboratory study of behaviour and experimental parasitology, teleost fish have been used as hosts in many of these studies. In this review we provide a broad overview of the range of mechanisms that potentially generate links between fish behaviour, personality, and parasitism, and illustrate these using examples drawn from the recent literature. In addition, we examine the potential interactions between cognition, personality and parasitism, and identify questions that may be usefully investigated with fish models.

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Weinersmith KL and Earley RL
Animal Behaviour, Volume 118, Pages 123–133

Interest in how parasites shape host behaviour has increased dramatically in recent years. The main focus of behavioural ecologists has been on the negative effects of parasites on host behaviour. However, there are instances in which infected hosts express more adaptive behavioural phenotypes and have higher fitness relative to uninfected hosts, suggesting that it is sometimes beneficial to be parasitized. For example, hosts can exhibit evolved dependence, wherein the host coevolves with and comes to depend on parasites for the expression of adaptive host behaviours. Additionally, ‘conditionally helpful parasites’ modify the host phenotype in ways that benefit the host under particular conditions. These scenarios have been explored in the context of bacterial or fungal symbionts, but have been relatively unstudied with regard to metazoan parasites (e.g. trematodes, acanthocephalans, nematodes and cestodes). We explore how these scenarios apply to hosts infected by metazoan parasites, and consider implications for research in behavioural ecology. We examine conditions under which infection should result in more adaptive host behavioural phenotypes, and the implications for host fitness and evolution. We then discuss the implications of conditionally helpful parasites and parasites for which hosts have evolved dependence for laboratory studies of host behaviour and for conservation and reintroduction programmes.

The relationship between handling time and cortisol release rates changes as a function of brain parasite densities in California killifish Fundulus parvipinnis

Weinersmith KL, Hanninen AF, Sih A, McElreath R and Earley RL
Journal of Fish Biology, Volume 88, Pages 1125-1142

This study validated a technique for non-invasive hormone measurements in California killifishFundulus parvipinnis, and looked for associations between cortisol (a stress hormone) and 11-ketotestosterone (KT, an androgen) release rates and the density or intensity of the trematode parasites Euhaplorchis californiensis (EUHA) and Renicola buchanani (RENB) in wild-caught, naturally infected F. parvipinnis. In experiment 1, F. parvipinnis were exposed to an acute stressor by lowering water levels to dorsal-fin height and repeatedly handling the fish over the course of an hour. Neither parasite was found to influence cortisol release rates in response to this acute stressor. In experiment 2, different F. parvipinnis were exposed on four consecutive days to the procedure for collecting water-borne hormone levels and release rates of 11-KT and cortisol were quantified. This design examined whether F. parvipinnis perceived the water-borne collection procedure to be a stressor, while also exploring how parasites influenced hormone release rates under conditions less stressful than those in experiment 1. No association was found between RENB and hormone release rates, or between EUHA and 11-KT release rates. The interaction between EUHA density and handling time, however, was an important predictor of cortisol release rates. The relationship between handling time and cortisol release rates was negative for F. parvipinnis harbouring low or intermediate density infections, and became positive for fish harbouring high densities of EUHA.

Novel Species Interactions in a Highly Modified Estuary: Association of Largemouth Bass with Brazilian Waterweed Egeria densa

Conrad JL, Bibian AJ, Weinersmith KL, DeCarion D, Young MJ, Crain P, Moyle PB and Sih A
Transactions of the American Fisheries Society Volume 145, Pages 249-263
Frequent invasions in coastal ecosystems result in novel species interactions that have unknown ecological consequences. Largemouth Bass Micropterus salmoides and Brazilian waterweed Egeria densa are introduced species in the Sacramento–San Joaquin River Delta (the Delta) of California, a highly modified estuary. In this system, Brazilian waterweed and Largemouth Bass have seen marked increases in distribution and abundance in recent decades, but their association has not been specifically studied until now. We conducted a 2-year, bimonthly electrofishing survey with simultaneous sampling of water quality and submerged aquatic vegetation (SAV) biomass at 33 locations throughout the Delta. We used generalized linear mixed models to assess the relative influences of water temperature, conductivity, Secchi depth, and SAV biomass density on the abundance of both juvenile-sized and larger Largemouth Bass. Water temperature had a positive relationship with the abundance of both size-classes, but only juvenile-sized fish had a positive association with SAV biomass density, with highest abundances at intermediate SAV densities. In contrast, larger fish were generally ubiquitous across all sampling conditions, even when SAV was absent or present at low densities. Our results on the Largemouth Bass–SAV relationship are consistent with those of previous studies from lake systems within the Largemouth Bass’s native range, where they interact with a different SAV species assemblage. These results are supportive of the hypothesis that the proliferation of Brazilian waterweed has expanded Largemouth Bass rearing habitat in the Delta. Finally, this study has implications for tidal wetland restoration plans for the Delta, suggesting that the larger-sized Largemouth Bass may still inhabit restored areas even if invasive SAV establishment is limited.

Changes in the reproductive physiology of mangrove rivulus Kryptolebias marmoratus following exposure to environmentally relevant concentrations of ethinyl estradiol

Johnson EL, Weinersmith KL and Earley RL
Journal of Fish Biology, Volume 88, Pages 774–786

Kryptolebias marmoratus exposed to 4 ng l−1 of ethinyl oestradiol (EE2) for 30 days experienced significant changes in endogenous 17β-oestradiol (E2) and 11-ketotestosterone (KT) and qualitative changes in gonad morphology. Both hermaphrodites and males showed a significant decrease in E2, whereas only males exhibited a significant decrease in KT. Exposure to EE2 resulted in a decrease in spermatid and spermatocyte density in males and an increase in the number of early stage oocytes in hermaphrodites.

Effects of a pesticide and a parasite on neurological, endocrine, and behavioral responses of an estuarine fish

Renick VC, Weinersmith KL, Vidal-Dorsch DE, and Anderson TW
Aquatic Toxicology Volume 170, Pages 335-343

In coastal waters, pesticides and parasites are widespread stressors that may separately and interactively affect the physiology, behavior, and survival of resident organisms. We investigated the effects of the organophosphate pesticide chlorpyrifos and the trematode parasite Euhaplorchis californiensis on three important traits of California killifish (Fundulus parvipinnis): neurotransmitter activity, release of the stress hormone cortisol, and behavior. Killifish were collected from a population without E. californiensis, and then half of the fish were experimentally infected. Following a 30 day period for parasite maturation, infected and uninfected groups were exposed to four concentrations of chlorpyrifos (solvent control, 1–3 ppb) prior to behavior trials to quantify activity, feeding behavior, and anti-predator responses. Water-borne cortisol release rates were measured non-invasively from each fish prior to infection, one-month post-infection, and following pesticide exposure. Killifish exposed to 3 ppb chlorpyrifos exhibited a 74.6 ± 6.8% and 60.5 ± 8.3% reduction in brain and muscle acetylcholinesterase (AChE) activity relative to controls. The rate of cortisol release was suppressed by each chlorpyrifos level relative to controls. Killifish exposed to the medium (2 ppb) and high (3 ppb) pesticide concentrations exhibited reduced activity and a decrease in mean swimming speed following a simulated predator attack. Muscle AChE was positively related to swimming activity while brain AChE was positively related to foraging behavior. ​No effects of the parasite were observed, possibly because of low metacercariae densities achieved through controlled infections. We found that sublethal pesticide exposure has the potential to modify several organismal endpoints with consequences for reduced fitness, including neurological, endocrine, and behavioral responses in an ecologically abundant fish.

Individual differences in exploratory and antipredator behaviour in juvenile smallmouth bass (Micropterus dolomieu)

Smith KL, Miner JG, Wiegmann DD and Newman SP
Behaviour (146): 283-294

The correlation of individual behaviour in different contexts, known as a behavioural syndrome, constrains the optimization of behaviour within each context. Recent studies reveal that the strength of syndromes differs amongst populations and over individual ontogeny. In this study, exploratory behaviour in an unfamiliar environment and behavioural responses to a simulated predator attack in the presence of food were measured in juvenile smallmouth bass (Micropterus dolomieu). The results revealed a syndrome: individuals who actively explored the unfamiliar environment also behaved more boldly in the presence of the model predator. The syndrome implies a tradeoff between collecting information about one’s environment and risk of a predator attack. Additionally, the results revealed different anti-predator strategies. The simulated predator attack induced a longer period of activity (presumably to disperse away from the predator) by shy individuals, who were also more likely to utilize a refuge, had a longer latency to resume activity and were less likely to resume foraging than bold individuals. Larger conspecifics are the main predators of young-of-year smallmouth bass in the population from which subjects were collected. Predation pressure has been implicated as a cause of behavioral syndromes and the results of this study suggest that cannibalism in high density populations is sufficient to induce behavioural correlations.

Multi-attribute mate choice decisions and uncertainty in the decision process: a generalized sequential search strategy

Wiegmann DD, Weinersmith KL and Seubert SM
Journal of Mathematical Biology 60 (4): 543-572

The behavior of females in search of a mate determines the likelihood that high quality males are encountered and adaptive search strategies rely on the effective use of available information on the quality of prospective mates. The sequential search strategy was formulated, like most models of search behavior, on the assumption that females obtain perfect information on the quality of encountered males. In this paper, we modify the strategy to allow for uncertainty of male quality and we determine how the magnitude of this uncertainty and the ability of females to inspect multiple male attributes to reduce uncertainty influence mate choice decisions. In general, searchers are sensitive to search costs and higher costs lower acceptance criteria under all versions of the model. The choosiness of searchers increases with the variability of the quality of prospective mates under conditions of the original model, but under conditions of uncertainty the choosiness of searchers may increase or decrease with the variability of inspected male attributes. The behavioral response depends on the functional relationship between observed male attributes and the fitness return to searchers and on costs associated with the search process. Higher uncertainty often induces searchers to pay more for information and under conditions of uncertainty the fitness return to searchers is never higher than under conditions of the original model. Further studies of the performance of alternative search strategies under conditions of uncertainty may consequently be necessary to identify search strategies likely to be used under natural conditions.


Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis)

Cote J, Fogarty S, Weinersmith KL, Brodin T and Sih A
Proceedings of the Royal Society, Series B 277: 1571-1579

Ecological invasions, where non-native species spread to new areas, grow to high densities and have large, negative impacts on ecological communities, are a major worldwide problem. Recent studies suggest that one of the key mechanisms influencing invasion dynamics is personality-dependent dispersal: the tendency for dispersers to have a different personality type than the average from a source population. We examined this possibility in the invasive mosquitofish (Gambusia affinis). We measured individual tendencies to disperse in experimental streams and several personality traits: sociability, boldness, activity and exploration tendency before and three weeks after dispersal. We found that mosquitofish display consistent behavioural tendencies over time, and significant positive correlations between all personality traits. Most notably, sociability was an important indicator of dispersal distance, with more asocial individuals dispersing further, suggesting personality-biased dispersal on an invasion front. These results could have important ecological implications, as invasion by a biased subset of individuals is likely to have different ecological impacts than invasion by a random group of colonists.

Popular press for article: Featured in Nature’s Research Highlights and Conservation Magazine.

Personality-dependent dispersal in the invasive mosquitofish: group composition matters

Cote J, Fogarty S, Brodin T, Weinersmith KL and Sih A
Proceedings of the Royal Society, Series B 278: 1670-1678

Understanding/predicting ecological invasions is an important challenge in modern ecology because of their immense economical and ecological costs. Recent studies have revealed that within-species variation in behaviour (i.e. animal personality) can shed light on the invasion process. The general hypothesis is that individuals’ personality type may affect their colonization success, suggesting that some individuals might be better invaders than others. We have recently shown that, in the invasive mosquitofish (Gambusia affinis), social personality trait was an important indicator of dispersal distance, with more asocial individuals dispersing further. Here, we tested how mean personality within a population, in addition to individual personality type, affect dispersal and settlement decisions in the mosquitofish. We found that individual dispersal tendencies were influenced by the population’s mean boldness and sociability score. For example, individuals from populations with more asocial individuals or with more bold individuals are more likely to disperse regardless of their own personality type. We suggest that identifying behavioural traits facilitating invasions, even at the group level, can thus have direct applications in pest management.

Behavioural syndromes in fish: a review with implications for ecology and fisheries management

Conrad JL, Weinersmith KL, Brodin T, Saltz JB and Sih, A
Journal of Fish Biology 78: 395-435

This review examines the contribution of research on fishes to the growing field of behavioural syndromes. Current knowledge of behavioural syndromes in fishes is reviewed with respect to five main axes of animal personality: (1) shyness–boldness, (2) exploration–avoidance, (3) activity, (4) aggressiveness and (5) sociability. Compared with other taxa, research on fishes has played a leading role in describing the shy–bold personality axis and has made innovative contributions to the study of the sociability dimension by incorporating social network theory. Fishes are virtually the only major taxon in which behavioural correlations have been compared between populations. This research has guided the field in examining how variation in selection regime may shape personality. Recent research on fishes has also made important strides in understanding genetic and neuroendocrine bases for behavioural syndromes using approaches involving artificial selection, genetic mapping, candidate gene and functional genomics. This work has illustrated consistent individual variation in highly complex neuroendocrine and gene expression pathways. In contrast, relatively little work on fishes has examined the ontogenetic stability of behavioural syndromes or their fitness consequences. Finally, adopting a behavioural syndrome framework in fisheries management issues including artificial propagation, habitat restoration and invasive species, may promote restoration success. Few studies, however, have examined the ecological relevance of behavioural syndromes in the field. Knowledge of how behavioural syndromes play out in the wild will be crucial to incorporating such a framework into management practices.

Effects of turbidity and an invasive waterweed on predation by introduced largemouth bass.

Ferrari MCO, Ranåker L, Weinersmith KL, Young MJ, Sih A and Conrad JL
Environmental Biology of Fishes 97 (1): 79-90

Anthropogenic activities lead to changes in characteristics of aquatic ecosystems, including alteration of turbidity and addition of invasive species. In this study, we tested how changes in turbidity and the recent invasion of an aquatic macrophyte, Egeria densa, may have changed the predation pressure by introduced largemouth bass on juvenile striped bass and delta smelt, two species that have seen a drastic decline in recent decades in the Sacramento-San Joaquin Delta. In a series of mesocosm experiments, we showed that increases in vegetation density decreased the predation success of largemouth bass. When placed in an environment with both open water and vegetated areas, and given a choice to forage on prey associated with either of these habitats, largemouth bass preyed mainly on open water species as opposed to vegetation-associated species, such as juvenile largemouth bass, bluegill or red swamp crayfish. Finally, we showed that turbidity served as cover to open water species and increased the survival of delta smelt, an endemic species at risk. We also found that such open water prey tend not to seek refuge in the vegetation cover, even in the presence of an imminent predation threat. These results provide the beginning of a mechanistic framework to explain how decreases in turbidity and increases in vegetation cover correlate with a decline of open water species in the Sacramento-San Joaquin Delta.

Parasitic manipulation of hosts’ phenotype, or how to make a zombie-an introduction to the symposium

Weinersmith KL and Zen F
Integrative and Comparative Biology 54: 93-100

Nearly all animals in nature are infected by at least one parasite, and many of those parasites can significantly change the phenotype of their hosts, often in ways that increase the parasite’s likelihood of transmission. Hosts’ phenotypic changes are multidimensional, and manipulated traits include behavior, neurotransmission, coloration, morphology, and hormone levels. The field of parasitic manipulation of hosts’ phenotype has now accrued many examples of systems where parasites manipulate the phenotypes of their hosts and focus has shifted to answering three main questions. First, through what mechanisms do parasites manipulate the hosts’ phenotype? Parasites often induce changes in the hosts’ phenotypes that neuroscientists are unable to recreate under laboratory conditions, suggesting that parasites may have much to teach us about links between the brain, immune system, and the expression of phenotype. Second, what are the ecological implications of phenotypic manipulation? Manipulated hosts are often abundant, and changes in their phenotype may have important population, community, and ecosystem-level implications. Finally, how did parasitic manipulation of hosts’ phenotype evolve? The selective pressures faced by parasites are extremely complex, often with multiple hosts that are actively resisting infection, both in physiological and evolutionary time-scales. Here, we provide an overview of how the work presented in this special issue contributes to tackling these three main questions. Studies on parasites’ manipulation of their hosts’ phenotype are undertaken largely by parasitologists, and a major goal of this symposium is to recruit researchers from other fields to the study of these phenomena. Our ability to answer the three questions outlined above would be greatly enhanced by participation from individuals trained in the fields of, for example, neurobiology, physiology, immunology, ecology, evolutionary biology, and invertebrate biology. Conversely, because parasites that alter their hosts’ phenotype are widespread, these fields will benefit from such study.


A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasite

Weinersmith KL, Warinner C, Tan V, Harris DJ, Mora AM, Kuris A, Lafferty KD and Hechinger RF
Integrative and Comparative Biology (54): 184-192

For trophically transmitted parasites that manipulate the phenotype of their hosts, whether the parasites do or do not experience resource competition depends on such factors as the size of the parasites relative to their hosts, the intensity of infection, the extent to which parasites share the cost of defending against the host’s immune system or manipulating their host, and the extent to which parasites share transmission goals. Despite theoretical expectations for situations in which either no, or positive, or negative density-dependence should be observed, most studies document only negative density-dependence for trophically transmitted parasites. However, this trend may be an artifact of most studies having focused on systems in which parasites are large relative to their hosts. Yet, systems are common where parasites are small relative to their hosts, and these trophically transmitted parasites may be less likely to experience resource limitation. We looked for signs of density-dependence in Euhaplorchis californiensis (EUHA) and Renicola buchanani (RENB), two manipulative trematode parasites infecting wild-caught California killifish (Fundulus parvipinnis). These parasites are small relative to killifish (suggesting resources are not limiting), and are associated with changes in killifish behavior that are dependent on parasite-intensity and that increase predation rates by the parasites’ shared final host (indicating the possibility for cost sharing). We did not observe negative density-dependence in either species, indicating that resources are not limiting. In fact, observed patterns indicate possible mild positive density-dependence for EUHA. Although experimental confirmation is required, our findings suggest that some behavior-manipulating parasites suffer no reduction in size, and may even benefit when “crowded” by conspecifics.