Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis

California killifish (Fundulus parvipinnis) infected with the brain-encysting trematode Euhaplorchis californiensis display conspicuous swimming behaviours rendering them more susceptible to predation by avian final hosts. Heavily infected killifish grow and reproduce normally, despite having thousands of cysts inside their braincases. This suggests that E. californiensis affects only specific locomotory behaviours. We hypothesised that changes in the serotonin and dopamine metabolism, essential for controlling locomotion and arousal may underlie this behaviour modification. We employed micropunch dissection and HPLC to analyse monoamine and monoamine metabolite concentrations in the brain regions of uninfected and experimentally infected fish. The parasites exerted density-dependent changes in monoaminergic activity distinct from those exhibited by fish subjected to stress. Specifically, E. californiensis inhibited a normally occurring, stress-induced elevation of serotonergic metabolism in the raphae nuclei. This effect was particularly evident in the experimentally infected fish, whose low-density infections were concentrated on the brainstem. Furthermore, high E. californiensis density was associated with increased dopaminergic activity in the hypothalamus and decreased serotonergic activity in the hippocampus. In conclusion, the altered monoaminergic metabolism may explain behavioural differences leading to increased predation of the infected killifish by their final host predators.     

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

This study validated a technique for non‐invasive hormone measurements in California killifish Fundulus 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.     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Host behaviour alteration by its parasite: from brain gene expression to functional test

Many parasites with complex life cycles modify their intermediate hosts'' behaviour, presumably to increase transmission to their final host. The threespine stickleback (Gasterosteus aculeatus) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S. solidus to determine the proximal causes of these behavioural alterations. We show that infected fish have altered expression levels in genes involved in the inositol pathway. We thus tested the functional implication of this pathway and successfully rescued normal behaviours in infected sticklebacks using lithium exposure. We also show that exposed but uninfected fish have a distinct gene expression profile from both infected fish and control individuals, allowing us to separate gene activity related to parasite exposure from consequences of a successful infection. Finally, we find that selective serotonin reuptake inhibitor-treated sticklebacks and infected fish do not have similarly altered gene expression, despite their comparable behaviours, suggesting that the serotonin pathway is probably not the main driver of phenotypic changes in infected sticklebacks. Taken together, our results allow us to predict that if S. solidus directly manipulates its host, it could target the inositol pathway.     

Reproductive potential of Schistocephalus solidus‐infected male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations

Male three‐spined stickleback Gasterosteus aculeatus from two U.K. populations with endemic infections of the cestode Schistocephalus solidus were brought into the laboratory prior to the breeding season and transferred to nesting tanks under conditions designed to stimulate sexual maturation. Nesting and courtship behaviours were scored over a 35 day period, after which fish were euthanized and the liver, spleen, kidney and gonads were weighed. Among G. aculeatus from a park pond in Leicester, U.K., infected males rarely engaged in reproductive behaviours and exhibited reduced indices of sexual development, body condition and general health, with effects being largely independent of relative parasite mass (parasite index, I_P). In contrast, the reproductive behaviour of infected fish from Kendoon Loch in Dumfriesshire, U.K. appeared to be less severely affected, with infected fish regularly building nests and courting females under laboratory conditions. This was paralleled by a more limited effect of infection on physiological indicators of development, condition and general health. Furthermore, behavioural and physiological variables typically correlated with I_P among infected fish from this population. Although comparing the performance of infected fish from the two populations directly was difficult due to potentially confounding factors, the results support the findings of recent studies showing that the effects of S. solidus on host reproduction are unlikely to be uniform across G. aculeatus populations. One possibility is that variation in the effects of infection arises from differences in the co‐evolutionary association times of G. aculeatus with the parasite.     

Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions,with particular reference to fish

1. Experimental results on the involvement of brain monoamines in agonistic behaviour and stress in fish are reviewed and discussed in relation to available data from other vertebrates.2. In fish as well as mammals, stress induces increased brain serotonergic activity, and a similar increase in serotonergic activity is seen in subordinate individuals in a dominance hierarchy.3. The brain serotonergic system appears to inhibit aggression and spontaneous locomotor activity in both fish and mammals.4. Subordinate fish show several behavioural characteristics, notably inhibition of aggressive behaviour, low spontaneous locomotor activity and decreased food intake, that are likely to be related to their increased brain serotonergic activity.5. By contrast, the brain dopaminergic system appears to stimulate aggressive behaviour in both fish and mammals, and dominant fish show signs of elevated dopaminergic activity in telencephalon.6. The similarities between fish and mammalian monoaminergic functions suggest that these are phylogenetically very old mechanisms that have been conserved during the last 400 million years of vertebrate evolution.     

Parasite‐induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal

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Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda)

The larval flatworm Microphallus papillorobustus encysts in the protocerebrum of its intermediate host, Gammarus insensibilis, and changes the gammarid's responses to mechanical and photic stimuli. The resulting aberrant escape behaviour renders infected gammarids more susceptible to predation by birds, the definitive hosts of the parasite. We used immunocytochemical methods to explore the mechanisms underlying these subtle behavioural modifications. Whole mounts of gammarid brains were labelled with fluorescent anti-serotonin and anti-synapsin antibodies and viewed using confocal microscopy. Two types of change were observed in infected brains: the intensity of the serotonergic label was altered in specific regions of the brain, and the architecture of some serotonergic tracts and neurons was affected. A morphometric analysis of the distribution of the label showed that serotonergic immunoreactivity was decreased significantly (by 62%) in the optic neuropils, but not in the olfactory lobes, in the presence of the parasite. In addition, the optic tracts and the tritocerebral giant neurons were stunted in parasitized individuals. Published evidence demonstrates changes in serotonin levels in hosts ranging from crustaceans to mammals infected by parasites as diverse as protozoans and helminths. The present study suggests that the degeneration of discrete sets of serotonergic neurons might underlie the serotonergic imbalance and thus contribute to host manipulation.     

Influence of black spot disease on shoaling behaviour in female western mosquitofish, <Emphasis Type="Italic">Gambusia affinis</Emphasis> (Poeciliidae,Teleostei)

Parasites can fundamentally alter the cost–benefit ratio of living in a group, e.g. if infected individuals increase the predation risk of shoal mates. Here, the effect of an infection with a trematode, Uvulifer sp. (Diplostomatidae) on the shoaling behaviour of female western mosquitofish, Gambusia affinis, was investigated. The parasite examined causes a direct phenotypical change of the host by forming black spots on its body surface. When given a choice between a stimulus shoal and no shoal, we found shoaling tendencies to be significantly reduced in infected focal fish. In another experiment, we tested for association preferences relative to the infection status of the stimulus fish. Given the choice between an infected and a healthy stimulus fish, both infected and healthy focal fish preferred to associate with non-infected stimulus fish. Our results suggest that (1) the cost–benefit ratio of shoaling might be different for infected and non-infected individuals. Infected fish may be more affected by competition for food within a shoal. (2) Associating with infected conspecifics appears to be costly for female mosquitofish, maybe due to increased predation risk.     

Infection of male rats with Toxoplasma gondii results in enhanced delay aversion and neural changes in the nucleus accumbens core

Rats infected with the protozoan parasite Toxoplasma gondii exhibit reduced avoidance of predator odours. This behavioural change is likely to increase transmission of the parasite from rats to cats. Here, we show that infection with T. gondii increases the propensity of the infected rats to make more impulsive choices, manifested as delay aversion in an intertemporal choice task. Concomitantly, T. gondii infection causes reduction in dopamine content and neuronal spine density of the nucleus accumbens core, but not of the nucleus accumbens shell. These results are consistent with a role of the nucleus accumbens dopaminergic system in mediation of choice impulsivity and goal-directed behaviours. Our observations suggest that T. gondii infection in rats causes a syndromic shift in related behavioural constructs of innate aversion and making foraging decisions.     

Changes in brain serotonergic activity during hierarchic behavior in Arctic charr (Salvelinus alpinus L.) are socially induced

Summary The experiment was performed in two phases. During the first phase (phase 1) the dominance hierarchy was determined in 4 groups of Arctic charr (Salvelinus alpinus L.), each group consisting of 4 fish. Phase 2 was started by rearranging phase 1 fish into 4 new groups. Group 1 consisted of previously dominant fish and groups 2, 3 and 4 of fish that previously held rank 2, 3 and 4, respectively. After phase 2 telencephalon and brain stem were analyzed with regard to their contents of serotonin (5-hydroxytryptamine, 5-HT) and 5-hydroxyindoleacetic acid (5-HIAA), the principle metabolite of 5-HT. No correlation was found between the social rank (measured as dominance index) during phase 1 and the brain serotonergic activity (measured as the ratio 5-HIAA/5-HT) determined after phase 2. However, most important, the 5-HIAA/5-HT ratio was significantly correlated with the last experienced social rank, i.e. that acquired during phase 2. These results shows that the difference in brain serotonergic activity between dominant and subordinate fish develops through social interactions. Further, we found that previous subordinate experience inhibited aggressive behavior, an effect which, in the light of available information on stress and 5-HT, could be related to the increase in brain serotonergic activity. We hypothesize that stress induces an increased serotonergic activity which in turn inhibits the neuronal circuitry which mediates aggressive behavior.Abbreviations 5-HT serotonin (5-hydroxytryptamine) - 5-HIAA 5-hydroxyindoleacetic acid     

Social rank and brain levels of monoamines and monoamine metabolites in Arctic charr,Salvelinus alpinus (L.)

Summary Dominance hierarchy was determined in 5 groups of juvenile Arctic charr (Salvelinus alpinus), each group consisting of 4 fish. Telencephalon and brain stem (remaining parts of the brain) were analyzed with regard to their content of monoamines and monoamine metabolites. No significant differences were observed in the concentrations of norepinephrine (NE), dopamine (DA), or serotonin (5-hydroxytryptamine, 5-HT) between fish with different social rank. However, the concentration of 5-hydroxyindoleacetic acid (5-HIAA), the principle metabolite of 5-HT, was significantly higher in subordinate fish, and a significant inverse linear correlation was found between 5-HIAA concentration and social rank (as measured by dominance index) in the brain stem. In the telencephalon the dominant fish had a significantly higher level of homovanillic acid (HVA), a major DA metabolite. These findings indicate a greater serotonergic activity, possibly associated with increased stress, as well as a lower dopaminergic activity, possibly associated with reduced aggression, in subordinate charr. The differences between dominant and subordinate fish could either be caused by social interactions or reflect innate individual differences in monoamine utilization, predisposing individuals for dominant or subordinate positions in the dominance hierarchy.Abbreviations DA dopamine - DI dominance index - NE norepinephrine - 5-HT serotonin (5-hydroxytryptamine) - 5-HIAA 5-hydroxyindoleacetic acid - 5-HTOH 5-hydroxytryptophol - HVA homovanillic acid     

Infection with a trematode parasite differentially alters competitive interactions and antipredator behaviour in native and invasive crayfish

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The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice

The presence of Trichinella spiralis infection in groups of male mice caused behavioural changes in both infected and uninfected mice. Also, for some behaviours, the extent of behavioural change in infected mice appeared to be determined by the number of muscle larvae they harboured. Infected mice showed a reduced frequency of exploratory and social behaviours compared with uninfected mice while uninfected mice performed more social investigatory activities towards those that were infected. Social interactions between infected and uninfected mice were also affected by familiarity. Behavioural differences shown to result from infection in mice familiar with each other were similar but more pronounced when the mice were unfamiliar. These results suggest that other factors may influence the behavioural effects of parasites on their hosts. For some behaviours, the greatest alterations in behaviour apparently caused by infection coincided with the period of infectivity to another host. The significance of this in relation to parasite transmission is considered.     

Cost of exposure to trematode cercariae and learned recognition and avoidance of parasitism risk by fathead minnows Pimephales promelas

Fathead minnows Pimephales promelas exposed to cercariae of the trematode Ornithodiplostomum sp. incurred a significant mass loss 17 days after exposure to 20 or 120 cercariae. Parasite‐naïve P. promelas showed no evidence of innate recognition or avoidance of cercariae. After a single exposure to cercariae, however, fish responded to chemical and visual cues of dead (thawed) cercariae with a reduction in activity. Encounter rate with cercariae, and hence infection rate, increased with fish activity. The data indicated that experienced P. promelas associated parasitism risk with novel chemical and visual cues that later triggered avoidance behaviour. Parallels and interactions between antiparasite behaviour and antipredator behaviour open new avenues for behavioural ecological research in risk‐sensitive decision‐making.     

Do Larval Damselflies make Adaptive Choices When Exposed to Both Parasites and Predators?

The importance of multiple enemies from different trophic levels on investment in defence by prey has, with some exceptions, received little attention. Some defences may make the victim more susceptible to other enemies; this latter situation applies to predators and parasites of larval damselflies. Baker and Smith [Oecologia 109 (1997) 622) showed that larval damselflies were as active in the presence of both mites and fish as they were when only mites were present, an apparently maladaptive behaviour that results in higher fish predation. In this paper, we further examine this maladaptive behavioural response to multiple enemies (fish predators and mite parasites) and test whether their defence responses are a result of the order in which they experience the parasite or predator, and/or if behavioural ‘personalities’ exist, such that some individuals show anti‐predator behaviours and other show anti‐parasite behaviours. Order of experience did not affect the four main behaviours (groom, crawl, turn and swim) exhibited when larval damselflies were simultaneously exposed to fish and mites. Grooming levels increased in response to mites, decreased in response to fish and when exposed to both mites and fish were similar to when they were exposed to mites alone. Duration of the other three behaviours was lower in the presence of both mites and fish. The crawling ‘personalities’ were evident. The apparently maladaptive response of high grooming levels in the presence of mites and fish is not a result of order of experience or ‘personalities’. It may be a result of relatively high encounter rates with mite parasites, compared with the encounter rates with fish. Lower encounter rates can result in diminishing investment in defence against an enemy.     

Non-Specific Manipulation of Gammarid Behaviour by P. minutus Parasite Enhances Their Predation by Definitive Bird Hosts

Trophically-transmitted parasites often change the phenotype of their intermediate hosts in ways that increase their vulnerability to definitive hosts, hence favouring transmission. As a “collateral damage”, manipulated hosts can also become easy prey for non-host predators that are dead ends for the parasite, and which are supposed to play no role in transmission strategies. Interestingly, infection with the acanthocephalan parasite Polymorphus minutus has been shown to reduce the vulnerability of its gammarid intermediate hosts to non-host predators, whose presence triggered the behavioural alterations expected to favour trophic transmission to bird definitive hosts. Whilst the behavioural response of infected gammarids to the presence of definitive hosts remains to be investigated, this suggests that trophic transmission might be promoted by non-host predation risk. We conducted microcosm experiments to test whether the behaviour of P. minutus-infected gammarids was specific to the type of predator (i.e. mallard as definitive host and fish as non-host), and mesocosm experiments to test whether trophic transmission to bird hosts was influenced by non-host predation risk. Based on the behaviours we investigated (predator avoidance, activity, geotaxis, conspecific attraction), we found no evidence for a specific fine-tuned response in infected gammarids, which behaved similarly whatever the type of predator (mallard or fish). During predation tests, fish predation risk did not influence the differential predation of mallards that over-consumed infected gammarids compared to uninfected individuals. Overall, our results bring support for a less sophisticated scenario of manipulation than previously expected, combining chronic behavioural alterations with phasic behavioural alterations triggered by the chemical and physical cues coming from any type of predator. Given the wide dispersal range of waterbirds (the definitive hosts of P. minutus), such a manipulation whose efficiency does not depend on the biotic context is likely to facilitate its trophic transmission in a wide range of aquatic environments.     

Comparison of efficiency of direct observations by scuba diver and indirect observations via video camera for measuring reef-fish behaviour

The present study investigates how the humbug damselfish Dascyllus aruanus, subject of a large number of ecological, evolutionary and behavioural studies, responds to the presence of human observers (effect of scuba diver presence-absence) and how the method of data collection (directly by a scuba diver v. indirectly via video camera) may affect the quality of behavioural data. Scuba diver presence had only subtle effects on fish behaviour. The efficiency of the method of scoring fish behaviour depended on the behaviour under consideration: those behaviours that occur in close proximity to the corals were scored more effectively directly by a scuba diver while those that are performed in a more rapid or repetitive fashion were scored more effectively indirectly via video camera. These results provide a foundation for future behavioural research on D. aruanus and other fishes where scuba divers or video cameras are the prevalent means of data collection.     

Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles

We quantified the clonal diversity of the New Zealand marine trematode Maritrema novaezealandensis (n = 1250) within Zeacumantus subcarinatus snail (n = 25) and Macrophthalmus hirtipes crab (n = 25) intermediate hosts using four to six microsatellite loci, and investigated the potential biological and physical factors responsible for the observed genetic patterns. Individual snails harboured one to five trematode genotypes and 48% of snails were infected by multiple parasite genotypes. Overall, the number of parasite genotypes did not increase with snail size, but was highest in intermediate-sized snails. Significantly larger numbers of parasite genotypes were detected in crabs (relative to snails; P < 0.001), with 16-25 genotypes recovered from individual crabs. Although crabs are typically infected by small numbers of cercariae sourced from many snails, they are occasionally infected by large numbers of cercariae sourced from single snails. The latter cases explain the significant genetic differentiation of trematode populations detected among their crab hosts (F(ST) = 0.009, P < 0.001). Our results suggest that the timing of infection and/or intraspecific competition among parasite clones within snails determine(s) the diversity of parasite clones that snails harbour. The presence of a large number of infected snails and tidal mixing of cercariae prior to infection results in crabs potentially harbouring hundreds of parasite genotypes despite the crabs' territorial behaviour.     

Cleaner fish become hosts: a novel form of parasite transmission

Adult bucephalid trematodes (Digenea) generally only occur in piscivorous fish. Within labrid fishes they are very rare, however, we have found them in labrid cleaner fish that feed on the ectoparasites of fish. We surveyed 969 labrid fishes from the tropical Pacific and found bucephalids only in cleaners (Labroides dimidiatus, L. bicolor, and Bodianus axillaris) and none in piscivores. The prevalences of bucephalids in L. dimidiatus at Lizard Island, Heron Island, Orpheus Island (all on the Great Barrier Reef), New Caledonia, and Moorea (French Polynesia) were 51, 47, 67, 56, and 67%, respectively. All of the L. bicolor examined from Moorea were infected. Bucephalids were highly prevalent in all size classes of L. dimidiatus from Lizard Island. Bucephalids were found in a 1.6-cm long juvenile L. dimidiatus, in which, piscivory is highly unlikely. We examined the literature on the worldwide bucephalid fauna in labrids and all hosts were found to be cleaners (Symphodus tinca, S. mediterraneus, L. dimidiatus, L. bicolor, and Bodianus axillaris) except Notolabrus parilus, whose ecology is unknown. We suggest that cleaners eat bucephalid metacercariae directly from the exterior surface of client fish during cleaning interactions. This is the first evidence of digeneans in the diet of L. dimidiatus, and the first study to show this novel form of parasite transmission where infective stages are eaten as a result of cleaning behaviour. Cleaning-mediated parasite transmission may result in behavioural modification of second intermediate hosts because clients and parasites both benefit from transmission. If the infection is costly to cleaners and acquired during cheating behaviour, then this parasite might regulate mutualism. Alternatively, if infective stages are targeted, infection by these bucephalids may be a negative consequence of an honest foraging strategy.Communicated by: P. F. Sale