0000000001303048
AUTHOR
Anssi Karvonen
Susceptibility of eye fluke-infected fish to predation by bird hosts.
Host manipulation by trophically transmitted parasites may predispose infected hosts to predation and in this way enhance parasite transmission. In most study systems, however, the evidence comes from laboratory studies, and therefore knowledge of the effect of manipulation on parasite transmission efficiency in the wild is still limited. Here we examined the effect ofDiplostomum spathaceum(Trematoda) eye flukes on the susceptibility of fish intermediate hosts to predation by bird definitive hosts. Our earlier studies have shown that the parasite alters fish phenotype and increases their susceptibility to artificial predation under laboratory conditions. In the present field study, we allow…
Experience and dominance in fish pairs jointly shape parasite avoidance behaviour
There is increasing evidence that the composition of a social group influences the fitness of its members. For example, group member identities can determine the exposure risk to contact-transmitted parasites and consequently impact the health of all group members. Here, we propose that group composition may also affect host exposure to parasite propagules prevailing in the environment via collective parasite avoidance behaviours. We explored the spatial avoidance of a trematode parasite, Diplostomum pseudospathaceum, using the simplest form of host groups, pairs of sea trout, Salmo trutta trutta. These pairs showed either (1) between-group heterogeneity in their experience with the parasit…
HELMINTH ASSEMBLAGES OF WHITEFISH (COREGONUS LAVARETUS) IN INTERCONNECTED LAKES: SIMILARITY AS A FUNCTION OF SPECIES SPECIFIC PARASITES AND GEOGRAPHICAL SEPARATION
This article examined the composition of parasite assemblages of whitefish (Coregonus lavaretus) in 8 interconnected lakes in northeastern Finland and evaluated the role of coregonid specific parasites and the geographical distance between populations in determining the similarity of the assemblages. Parasite assemblages were compared using the Jaccard qualitative similarity index and a quantitative similarity index and by incorporating the allogenic-autogenic species concept and the effects of 2 corresponding measures of geographical distance between the lakes. The majority of the parasite species found (10 of 14) were specific to salmonids. Similarity of assemblages of autogenic parasites…
Diplostomiasis ( Diplostomum spathaceum and related species).
This book chapter describes various aspects of diplostomiasis caused by Diplostomum spathaceum: diagnosis, epidemiology, life cycle, transmission, developmental stages, population dynamics, effects of climate change on parasite distribution, and disease control and prevention. peerReviewed
Parasite assemblages of crucian carp (Carassius carassius) – is depauperate composition explained by lack of parasite exchange, extreme environmental conditions or host unsuitability?
Recent studies on parasite communities have considered the factors which contribute to variability in parasite infections among populations of one host species. This paper examined parasite assemblages of crucian carp (Carassius carassius) in a natural set-up of two distinctive environments inhabited by the same host species and differing in respect to composition of other fish species: ponds, where extreme conditions prevent other fish species from occurring and lakes, where crucian carp coexist with other fish species. Our aim was to evaluate the significance of parasite exchange, environmental conditions and host suitability for the depauperate parasite assemblages observed in pond cruci…
FOOD MAKES YOU A TARGET: DISENTANGLING GENETIC, PHYSIOLOGICAL, AND BEHAVIORAL EFFECTS DETERMINING SUSCEPTIBILITY TO INFECTION
Genetics, physiology, and behavior are all expected to influence the susceptibility of hosts to parasites. Furthermore, interactions between genetic and other factors are suggested to contribute to the maintenance of genetic polymorphism in resistance when the relative susceptibility of host genotypes is context dependent. We used a maternal sibship design and long- and short-term food deprivation treatments to test the role of family-level genetic variation, body condition, physiological state, and foraging behavior on the susceptibility of Lymnaea stagnalis snails to infection by a trematode parasite that uses chemical cues to locate its hosts. In experimental exposures, we found that sna…
Spatiotemporal and gender‐specific parasitism in two species of gobiid fish
Abstract Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish…
Multispecies coinfections and presence of antibiotics shape resistance and fitness costs in a pathogenic bacterium
Increasing antimicrobial resistance (AMR) poses a challenge for treatment of bacterial diseases. In real life, bacterial infections are typically embedded within complex multispecies communities and influenced by the environment, which can shape costs and benefits of AMR. However, knowledge of such interactions and their implications for AMR in vivo is limited. To address this knowledge gap, we investigated fitness-related traits of a pathogenic bacterium (Flavobacterium columnare) in its fish host, capturing the effects of bacterial antibiotic resistance, coinfections between bacterial strains and metazoan parasites (fluke Diplostomum pseudospathaceum) and antibiotic exposure. We quantifie…
Host immunization shapes interspecific associations in trematode parasites
1. Individuals of free-living organisms are commonly infected by multiple parasite species. Under such circumstances, positive or negative associations between the species are possible because of direct or indirect interactions, details in parasite transmission ecology and host-mediated factors. One possible mechanism underlying these processes is host immunity, but its role in shaping these associations has rarely been tackled experimentally. 2. In this study, we tested the effect of host immunization on associations between trematode parasites infecting eyes of fish. We first analysed the associations between three species (Diplostomum spathaceum, Diplostomum gasterostei and Tylodelphys c…
Within‐host interactions shape virulence‐related traits of trematode genotypes
Within-host interactions between co-infecting parasites can significantly influence the evolution of key parasite traits, such as virulence (pathogenicity of infection). The type of interaction is expected to predict the direction of selection, with antagonistic interactions favouring more virulent genotypes and synergistic interactions less virulent genotypes. Recently, it has been suggested that virulence can further be affected by the genetic identity of co-infecting partners (G × G interactions), complicating predictions on disease dynamics. Here, we used a natural host-parasite system including a fish host and a trematode parasite to study the effects of G × G interactions on infection…
Eye fluke infection and lens size reduction in fish: a quantitative analysis.
Parasites have a variety of harmful effects on their hosts, some of which may be overlapping or complementary and thus easily overlooked but which are still important for the overall severity of infection. We investigated the effect of Diplostomum sp. eye fluke infection on the size of the eye lens in a range of wild and farmed fish species and those exposed to controlled parasite infection. We found that asymmetry in intensity of infection between the right and left lens of an individual fish affected lens size such that the lens with the higher intensity of infection was smaller. Interestingly, however, this was observed only in 3 of the 10 species studied (whitefish, smelt and sea trout)…
Impaired crypsis of fish infected with a trophically transmitted parasite
Trophically transmitted parasites may enhance their transmission by altering the phenotype of infected hosts to increase their vulnerability to predation by the next hosts in the life cycle. In an experimental study, we investigated whether the parasite Diplostomum spathaceum (Trematoda) alters cryptic coloration and cryptic behaviour of infected rainbow trout, Oncorhynchus mykiss, so that they would be more conspicuous to avian predators. The parasite reduces the vision of fish by lodging in the eyes and inducing cataract formation, which gives it an opportunity to affect fish crypsis. We examined the effect of the parasite on the ability of fish to adjust their coloration to the environme…
supplementary information and data from Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentration of antibiotic affects the co-infection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum, in their fish host. We found that antibiotic in fee…
Host infection history modifies co-infection success of multiple parasite genotypes.
Co-infections by multiple parasite genotypes are common and have important implications for host-parasite ecology and evolution through within-host interactions. Typically, these infections take place sequentially, and therefore, the outcome of co-infection may be shaped by host immune responses triggered by previous infections. For example, in vertebrates, specific immune responses play a central role in protection against disease over the course of life, but co-infection research has mostly focused on previously uninfected individuals. Here, we investigated whether sequential exposure and activation of host resistance in rainbow trout Oncorhynchus mykiss affects infection success and inte…
Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar)
AbstractOne of the most important life-history continuums is the fast–slow axis, where “fast” individuals mature earlier than “slow” individuals. “Fast” individuals are predicted to be more active than “slow” individuals; high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription co-factor, explains ∼40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with increased a…
Relative reproductive success of co-infecting parasite genotypes under intensified within-host competition.
In nature, host individuals are commonly simultaneously infected with more than one genotype of the same parasite species. These co-infecting parasites often interact, which can affect their fitness and shape host-parasite ecology and evolution. Many of such interactions take place through competition for limited host resources. Therefore, variation in ecological factors modifying the host resource level could be important in determining the intensity of competition and the outcome of co-infections. We tested this hypothesis by measuring the relative reproductive success of co-infecting genotypes of the trematode parasite Diplostomum pseudospathaceum in its snail host Lymnaea stagnalis whil…
Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity
Trophically transmitted parasites may predispose infected hosts to predation by altering host behaviour, which can be either an adaptation of the parasites to enhance transmission to the next hosts in the life cycle or a nonadaptive side-effect of infection. In an experimental study, we investigated host manipulation by Diplostomum spathaceum (Trematoda), an eye fluke of fish, to evaluate its adaptive value as a parasite strategy to increase transmission efficiency to bird hosts. The parasite induces cataract formation in the lenses of fish eyes, and predisposes fish to predation by reducing their escape response. We examined the effect of developmental stage and the number of parasites on …
Reciprocal Interaction Matrix Reveals Complex Genetic and Dose-Dependent Specificity among Coinfecting Parasites
Understanding genetic specificity in factors determining the outcome of host-parasite interactions is especially important as it contributes to parasite epidemiology, virulence, and maintenance of genetic variation. Such specificity, however, is still generally poorly understood. We examined genetic specificity in interactions among coinfecting parasites. In natural populations, individual hosts are often simultaneously infected by multiple parasite species and genotypes that interact. Such interactions could maintain genetic variation in parasite populations if they are genetically specific so that the relative fitness of parasite genotypes varies across host individuals depending on (1) t…
Are Sick Individuals Weak Competitors? Competitive Ability of Snails Parasitized by a Gigantism-Inducing Trematode
Parasitized individuals are often expected to be poor competitors because they are weakened by infections. Many trematode species, however, although extensively exploiting their mollusc hosts, also induce gigantism (increased host size) by diverting host resources towards growth instead of reproduction. In such systems, alternatively to reduced competitive ability due to negative effects of parasitism on host performance, larger size could allow more efficient resource acquisition and thus increase the relative competitive ability of host individuals. We addressed this hypothesis by testing the effect of a trematode parasite Diplostomum pseudospathaceum on the competitive ability of its sna…
Interactions among co-infecting parasite species: a mechanism maintaining genetic variation in parasites?
Individuals of free-living organisms are often infected simultaneously by a community of parasites. If the co-infecting parasites interact, then this can add significantly to the diversity of host genotype×parasite genotype interactions. However, interactions between parasite species are usually not examined considering potential variation in interactions between different strain combinations of co-infecting parasites. Here, we examined the importance of interactions between strains of fish eye flukes Diplostomum spathaceum and Diplostomum gasterostei on their infectivity in naive fish hosts. We assessed the infection success of strains of both species in single-strain exposures and in co-…
Opposing health effects of hybridization for conservation
The continuing decline of many natural plant and animal populations emphasizes the importance of conservation strategies. Hybridization as a management tool has proven successful in introducing gene flow to small, inbred populations, but can be also associated with health risks. For example, hybridization can change susceptibility to infection in either direction due to heterosis (hybrid vigor) and outbreeding depression, but such health effects have rarely been considered in the genetic management of populations. Here, we investigated the effects of experimental outcrossing between the critically endangered Saimaa landlocked salmon (Salmo salar m. sebago) and the genetically more diverse A…
Vertebrate defense against parasites: Interactions between avoidance, resistance, and tolerance
Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade‐offs with other life‐history traits. Trade‐offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host–parasite system, the trematode eye‐fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host ind…
Ecological divergence of closely related Diplostomum (Trematoda) parasites.
Parasite life-cycles present intriguing model systems to study divergence in resource use and ecology between parasite taxa. In ecologically similar taxa, consistent selective forces may lead to convergence of life-history traits, but resource overlap and similarity of life-cycles may also promote divergence between the taxa in (1) use of host species or (2) specific niche within a host. We studied the life-history characteristics of 2 sympatric species of Diplostomum parasites, D. spathaceum and D. gasterostei, concentrating particularly on differences in intermediate host use and characteristics of the infective stages between the species. This group of trematodes is a notoriously difficu…
Infracommunity level aggregation in the monogenean communities of crucian carp (Carassius carassius).
Aggregation is one of the distinctive features in parasite-host relationships, which has generally been studied at the level of host communities. Parasite aggregation at the infracommunity level may nevertheless be important for intraspecific interactions such as parasite mating success and opportunities for cross-fertilization. In the present paper, we studied the infracommunity aggregation of 3 highly abundantDactylogyrus(Monogenea) species occurring on the gills of crucian carp (Carassius carassius). In line with the previous work on monogenean communities, we observed no competition between the species. At the species level, parasites were distributed unevenly on the gills showing aggre…
Infection, specificity and host manipulation of Australapatemon sp. (Trematoda, Strigeidae) in two sympatric species of leeches (Hirudinea)
SUMMARYFactors that drive parasite specificity and differences in infection dynamics among alternative host species are important for ecology and evolution of host–parasite interactions, but still often poorly known in natural systems. Here, we investigated spatiotemporal dynamics of infection, host susceptibility and parasite-induced changes in host phenotype in a rarely explored host–parasite system, theAustralapatemonsp. trematode infecting two sympatric species of freshwater leeches,Erpobdella octoculataandHelobdella stagnalis. We show significant variation in infection abundance between the host species in both space and time. Using experimental infections, we also show that most of th…
Within-host interactions shape virulence-related traits of trematode genotypes
Within‐host interactions between co‐infecting parasites can significantly influence the evolution of key parasite traits, such as virulence (pathogenicity of infection). The type of interaction is expected to predict the direction of selection, with antagonistic interactions favouring more virulent genotypes and synergistic interactions less virulent genotypes. Recently, it has been suggested that virulence can further be affected by the genetic identity of co‐infecting partners (G × G interactions), complicating predictions on disease dynamics. Here, we used a natural host–parasite system including a fish host and a trematode parasite to study the effects of G × G interactions on infection…
Parasite avoidance behaviours in aquatic environments
Parasites, including macroparasites, protists, fungi, bacteria and viruses, can impose a heavy burden upon host animals. However, hosts are not without defences. One aspect of host defence, behavioural avoidance, has been studied in the terrestrial realm for over 50 years, but was first reported from the aquatic environment approximately 20 years ago. Evidence has mounted on the importance of parasite avoidance behaviours and it is increasingly apparent that there are core similarities in the function and benefit of this defence mechanism between terrestrial and aquatic systems. However, there are also stark differences driven by the unique biotic and abiotic characteristics of terrestrial …
Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite
Characterizing genetic variation in parasite transmission traits and its contribution to parasite vigor is essential for understanding the evolution of parasite life‐history traits. We measured genetic variation in output, activity, survival, and infection success of clonal transmission stages (cercaria larvae) of a complex life cycle parasite (Diplostomum pseudospathaceum). We further tested if variation in host nutritional stage had an effect on these traits by keeping hosts on limited or ad libitum diet. The traits we measured were highly variable among parasite genotypes indicating significant genetic variation in these life‐history traits. Traits were also phenotypically variable, for …
Shoaling with infected conspecifics does not improve resistance to trematode infection
Group‐living animals can gain protection against parasitic infections through social contacts with previously infected conspecifics (social immunization). Recent research suggests that such protective effects can be induced through visual or chemical cues released by infected individuals, resulting in anticipatory immune upregulation among group members. Here, we study cue‐induced social resistance in rainbow trout Oncorhynchus mykiss exposed to a trematode parasite, the eye‐fluke Diplostomum pseudospathaceum. We established groups of naïve individuals (receivers) that were paired with previously infected individuals (donors) at different ratios of donors to receivers and at different time …
supplementary information and data from Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentration of antibiotic affects the co-infection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum, in their fish host. We found that antibiotic in fee…
Between-population Similarity in Intestinal Parasite Community Structure of Pike (Esox Lucius)—Effects of Distance and Historical Connections
The effect of geographical distance on similarity in parasite communities of freshwater fish has received considerable attention in recent years, and it has become evident that these apparently simple relationships are influenced by, among other things, colonization ability of parasites and degree of connectivity between the populations. In the present paper, we explored qualitative and quantitative similarity in the intestinal parasite communities of pike (Esox lucius) in a particular system where previously interconnected groups of lakes became isolated ca. 8,400 yr ago. Contrary to our expectations, we did not find differences in similarity between the lake groups or a negative effect of…
Infectivity of trematode eye flukes in farmed salmonid fish — Effects of parasite and host origins
Abstract Parasites cause significant economic losses in fish farming, and knowledge of the mechanisms underlying their effects on hosts is an essential prerequisite of preventative procedures for the parasite problem in hatcheries. One such mechanism is local adaptation of parasites, which should lead to higher infectivity of parasites in sympatric host–parasite combinations compared to corresponding allopatric combinations. In this study, we investigated the infectivity of two ubiquitous species of trematode eye flukes, Diplostomum sp. and Tylodelphus clavata, in their farmed salmonid fish hosts with respect to origin of the parasite and the host. First, we exposed two anadromous and one l…
Supplementary tables and figures from Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon (Salmo salar) and sea trout (an anadromous form of brown trout, Salmo trutta) were raised under common garden conditions and infected with the eye fluke …
Eye fluke-induced cataracts in natural fish populations: is there potential for host manipulation?
SUMMARYManipulation of host phenotype (e.g. behaviour, appearance) is suggested to be a common strategy to enhance transmission in trophically transmitted parasites. However, in many systems, evidence of manipulation comes exclusively from laboratory studies and its occurrence in natural host populations is poorly understood. Here, we examined the potential for host manipulation by Diplostomum eye flukes indirectly by quantifying the physiological effects of parasites on fish. Earlier laboratory studies have shown that Diplostomum infection predisposes fish to predation by birds (definitive hosts of the parasites) by reducing fish vision through cataract formation. However, occurrence of ca…
Spatiotemporal and gender-specific parasitism in two species of gobiid fish
Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence, for example, host population dynamics and behavior such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behavior and mate choice. We found that both fish species harbored parasite communities dominated by taxa transmitted to fish through …
Differences in parasite community composition support ecological differentiation in a freshwater gadoid fish
Several northern freshwater fishes have gone through rapid adaptive radiation after the last glacial period, resulting in new species or intraspecific morphs with distinct life histories. Parasite infections can promote adaptive radiations and spatiotemporal differences in patterns of infections can potentially reveal incipient or ongoing speciation processes. We investigated intraspecific differentiation in a freshwater gadoid fish, burbot (Lota lota), by exploring differences in parasite infections between two potential life-history morphs in Lake Konnevesi, Central-Finland, one reproducing species characteristically in shallow littoral waters in February and the other possibly in deep pr…
Phenotypic variation in infectivity of Diplostomum spathaceum cercariae within a population.
The present study examined phenotypic variation in infectivity of Diplostomum spathaceum (Trematoda) cercariae within a natural population. Twelve infected Lymnaea stagnalis were collected from the field, and the infectivity of cercariae from individual snails was assessed under constant laboratory conditions. At a water temperature of 16.3 C, the mean infectivity of cercariae from the snails varied between 55.5% and 87.5%. Depending on the source of variation, this may have important ecological and evolutionary implications for both natural parasite populations and those occurring in aquaculture.
Interactions among bacterial strains and fluke genotypes shape virulence of co-infection.
Most studies of virulence of infection focus on pairwise host–parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co-infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of the effects of genotype by genotype (G × G) interactions between unrelated parasite species on virulence of co-infection is limited. Here, we tested such a relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mo…
The role of parasitism in adaptive radiations – when might parasites promote and when might they constrain ecological speciation?
Research on speciation and adaptive radiation has flourished during the past decades, yet factors underlying initiation of reproductive isolation often remain unknown. Parasites represent important selective agents and have received renewed attention in speciation research. We review the literature on parasite-mediated divergent selection in context of ecological speciation and present empirical evidence for three nonexclusive mechanisms by which parasites might facilitate speciation: reduced viability or fecundity of immigrants and hybrids, assortative mating as a pleiotropic by-product of host adaptation, and ecologically-based sexual selection. We emphasise the lack of research on specia…
Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host?
Due to their particular way of life, dispersal of parasites is often mediated by their host's biology. Dispersal distance is relevant for parasites because high degree of dispersal leads to high gene flow, which counters the rate of parasite local adaptation in the host populations. Parasites with complex life cycles need to exploit sequentially more than one host species to complete their life cycle. Most trematode parasites have such complex life cycles involving invertebrate and vertebrate hosts. The spatial scales of invertebrate and vertebrate host populations are often different, which may decrease the probability that the parasite cycles locally in the intermediate host population. W…
Quantity and Quality of Aquaculture Enrichments Influence Disease Epidemics and Provide Ecological Alternatives to Antibiotics
Environmental heterogeneity is a central component influencing the virulence and epidemiology of infectious diseases. The number and distribution of susceptible hosts determines disease transmission opportunities, shifting the epidemiological threshold between the spread and fadeout of a disease. Similarly, the presence and diversity of other hosts, pathogens and environmental microbes, may inhibit or accelerate an epidemic. This has important applied implications in farming environments, where high numbers of susceptible hosts are maintained in conditions of minimal environmental heterogeneity. We investigated how the quantity and quality of aquaculture enrichments (few vs. many stones
Enriched rearing environment and wild genetic background can enhance survival and disease resistance of salmonid fishes during parasite epidemics
Summary 1. The importance and volume of aquaculture is increasing world-wide. Rearing practices play a key role in determining growth rate, survival and disease resistance in aquaculture fishes. Recent evidence suggests that in comparison with a standard stimulus-poor rearing environment, an enriched or variable rearing environment has significant positive effects on several traits underlying growth and well-being of fish. However, the effect of enriched rearing on one of the most important threats for aquaculture development, occurrence of parasitic infections, remains unknown. 2. We used surveillance data of experimental salmonid populations of wild and hatchery origin under semi-natural …
Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite.
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentrations of antibiotic affects the co-infection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum , in their fish host. We found that antibiotic in …
Schistosomes in the north: a unique finding from a prosobranch snail using molecular tools.
article i nfo Samples of schistosome cercariae from three different snail species (Lymnaea stagnalis, Radix auricularia and Valvata (Tropidina) macrostoma) collected from lakes in Central Finland were analyzed using molecular techniques. Based on sequences of ITS region of rDNA, the parasite isolates from L. stagnalis and R. auricularia belong to Trichobilharzia szidati and T. franki, respectively. This confirms a wide distribution of these two species in Europe. On the other hand, the isolates from V. macrostoma represent a unique finding — they belong to yet unknown schistosome species falling into the bird schistosome clade. Therefore, identification of natural final hosts and morphologi…
supplementary information and data from Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentration of antibiotic affects the co-infection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum, in their fish host. We found that antibiotic in fee…
Prevalence of infection as a predictor of multiple genotype infection frequency in parasites with multiple-host life cycle.
In nature, parasites commonly share hosts with other conspecific parasite genotypes. While adult parasites typically show aggregated distribution in their final hosts, aggregation of clonal parasite genotypes in intermediate hosts, such as those of trematodes in molluscs, is not generally known. However, infection of a host by multiple parasite genotypes has significant implications for evolution of virulence and host-parasite coevolution. Aggregated distribution of the clonal stages can increase host mortality and reduce larval output of each infecting genotype through interclonal competition, and therefore have significant implications for parasite epidemiology. The aim of this study was …
Intestinal distribution and fecundity of two species ofDiplostomumparasites in definitive hosts
This paper investigated the intestinal distribution and fecundity of 2 species ofDiplostomumparasites,D. spathaceumandD. pseudospathaceum, in 2 species of definitive hosts, herring gull (Larus argentatus) and common gull (L. canus), using both empirical field data and experimental infections. At the level of individual hosts, the parasite species occupied different parts within the intestine, but the fecundity of the worms, measured as the number of eggs in the uterus, did not differ between the parasite species except in wild common gulls. Interestingly, egg numbers in individual hosts were positively correlated between the parasite species suggesting that some birds provided better resour…
Priming of host resistance to protect cultured rainbow trout Oncorhynchus mykiss against eye flukes and parasite-induced cataracts
In the present study, immunologically naive rainbow trout Oncorhynchus mykiss were experimentally exposed to a low-level Diplostomum spathaceum (Trematoda) infection to stimulate acquired resistance and, along with unexposed controls, were subsequently exposed to natural infection for 8 weeks. The priming of the host resistance, designed to simulate a procedure applicable in aquaculture, decreased the number of establishing parasites compared to untreated controls by the end of the experiment. This effect was slow and did not protect the fish against the parasite-induced cataracts. The results suggest that this type of priming of host resistance is probably inefficient in preventing the del…
Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites
Co-infecting parasite genotypes typically compete for host resources limiting their fitness. The intensity of such competition depends on whether parasites are reproducing in a host, or using it primarily as a transmission vehicle while not multiplying in host tissues (referred to as ‘competition hypothesis’). Alternatively, simultaneous attack and co-infection by several parasite genotypes might facilitate parasite infection because such a diverse attack could present an additional challenge to host immune defence (referred to as ‘facilitation hypothesis’). We tested the competition hypothesis by comparing the production of transmission stages (cercariae) from snails infected with one or …
Rearing background and exposure environment together explain higher survival of aquaculture fish during a bacterial outbreak
1.Parasitic diseases represent one of the greatest challenges for aquaculture worldwide and there is an increasing emphasis on ecological solutions to prevent infections. One proposed solution is enriched rearing, where traditional stimulus‐poor rearing tanks are equipped with different types of structures to increase habitat complexity. Such spatial enrichment is known to increase survival of fish during parasite epidemics, but the underlying mechanisms are still unclear. 2.We studied whether enriched rearing affected infection of an important fish pathogen Flavobacterium columnare in young Atlantic salmon (Salmo salar) and sea‐migrating brown trout (Salmo trutta). First, we used natural b…
Being successful in the world of narrow opportunities: transmission patterns of the trematode Ichthyocotylurus pileatus.
SUMMARYParasites with complex life cycles face 2 major challenges for transmission in northern latitudes. They have to cope with the general unpredictability associated with the series of transmission events required for completion of the cycle, and transmission has to be completed within a narrow temporal window because of strong seasonality. Despite this, some parasites show high transmission success, suggesting the operation of effective transmission mechanisms. We explored the transmission of Ichthyocotylurus pileatus (Trematoda) from its snail (Valvata macrostoma) to fish (Perca fluviatilis) hosts by examining some key characteristics in the dynamics of the cercarial emergence from sna…
Within-lake dynamics in the similarity of parasite assemblages of perch (Perca fluviatilis).
Although parasite communities have been studied extensively in recent years, spatial and temporal variation in factors affecting the communities has received less attention. This paper examined the similarity of parasite assemblages of perch (Perca fluviatilis) in 18 locations within a single lake in relation to geographical distance and temporal dynamics in the host and parasite populations. We expected that in the present study-scale where distinct but potentially interacting host subpopulations could occur, similarity of the assemblages could be affected by seasonal dynamics in host movements particularly during the spawning period. Parasite species showed differences in infection levels…
Spatial and temporal structure of the trematode component community inValvata macrostoma(Gastropoda, Prosobranchia)
SUMMARYWe conducted the first comprehensive study on the spatiotemporal structure of trematode communities in the large-mouthed valve snail,Valvata macrostoma. A total of 1103 snails were examined monthly between May and October 2007 from Lake Konnevesi, Central Finland, from a shallow (1–2 m deep) and an offshore site (5–6 m deep), located ca. 50–70 m apart. Snails were infected by 10 trematode species. The species composition and prevalence were strikingly different between the sites with high species diversity in the shallow site (all 10 species; total prevalence of sporocysts/rediae 12·1%, metacercariae 55·4%) compared to the deeper site (3 species; prevalence 15·0% and 1·9%, respective…
Variation in parasite resistance of Arctic charr, Salvelinus alpinus, between and within sympatric morphs
Abstract Genetic variation in resistance against parasite infections is a predominant feature in host–parasite systems. However, mechanisms maintaining genetic polymorphism in resistance in natural host populations are generally poorly known. We explored whether differences in natural infection pressure between resource‐based morphs of Arctic charr (Salvelinus alpinus) have resulted in differentiation in resistance profiles. We experimentally exposed offspring of two morphs from Lake Þingvallavatn (Iceland), the pelagic planktivorous charr (“murta”) and the large benthivorous charr (“kuðungableikja”), to their common parasite, eye fluke Diplostomum baeri, infecting the eye humor. We found t…
Ultraviolet B Irradiation Affects Resistance of Rainbow Trout (Oncorhynchus mykiss) Against Bacterium Yersinia ruckeri and Trematode Diplostomum spathaceum
Ultraviolet B (UVB) radiation is known to have various effects on the immune system of fish, but the effect on the actual disease resistance has remained largely unknown. Here we studied the effect of UVB on the resistance of rainbow trout (Oncorhynchus mykiss) against a bacterium Yersinia ruckeri, the causative agent of enteric red mouth disease, and a trematode parasite Diplostomum spathaceum, which causes cataracts in fish. The fish were exposed to UVB irradiation seven times in 14 days, and inoculated intraperitoneally with Y. ruckeri on day 5 after the first irradiation. On day 2 postinfection (p.i.), the number of viable bacteria in the kidney was lower in UVB-exposed than in unexpose…
Cold water reduces the severity of parasite-inflicted damage : support for wintertime recuperation in aquatic hosts
The reduction in host fitness caused by parasite infections (virulence) depends on infection intensity and the degree of damage caused per parasite. Environmental conditions can shape both virulence components, but in contrast to infection intensity, environmental impacts on per-parasite damage are poorly understood. Here, we studied the effect of ambient temperature on per-parasite damage, which is jointly determined by the ability of parasites to induce harm (per-parasite pathogenicity) and the ability of hosts to limit damage (tolerance). We experimentally exposed two salmonid species, Atlantic salmon (Salmo salar) and sea trout (Salmo trutta), to replicated genotypes of the eye fluke Di…
Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies
AbstractThe link between climate changes and disease risks from various pathogens has been increasingly recognized. The effect of climatic factors on host–parasite population dynamics is particularly evident in northern latitudes where the occurrence and transmission of parasites are strongly regulated by seasonality-driven changes in environmental temperatures. Shortened winter periods would increase growth potential of many parasite populations. The ways in which climate warming could affect life history dynamics of the directly transmitted crustacean ectoparasite Argulus coregoni and complex life cycle trematode Diplostomum spathaceum, which frequently cause problems in northern fish far…
Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon ( Salmo salar ) and sea trout (an anadromous form of brown trout, Salmo trutta ) were raised under common garden conditions and infected with the eye fl…
Host Developmental Stage Effects on Parasite Resistance and Tolerance.
Hosts can defend themselves against parasites either by preventing or limiting infections (resistance) or by limiting parasite-induced damage (tolerance). However, it remains underexplored how these defense types vary over host development with shifting patterns of resource allocation priorities. Here, we studied the role played by developmental stage in resistance and tolerance in Atlantic salmon (Salmo salar). This anadromous fish has distinct life stages related to living in freshwater and seawater. We experimentally exposed 1-year-old salmon, either at the freshwater stage or at the stage transitioning to the marine phase, to the trematode Diplostomum pseudospathaceum. Using 56 pedigree…
Parasite infection in a central sensory organ of fish does not affect host personality
Among the ecological factors acting on the evolution and expression of animal personalities and behavioral syndromes, parasitism has received comparatively little attention. However, infection and host behavior are often strongly intertwined, because host behavior can predict the risk of infection and can also be changed by an infection. We conducted a controlled experimental infection study to explore the effects of infection on host boldness, exploration and activity using rainbow trout Oncorhynchus mykiss and its trematode parasite Diplostomum pseudospathaceum, which infects a central sensory organ of the fish, the eye lens. Contrary to our expectation, infection did not change the withi…
Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging?
In the production of the infective cercariae of trematodes, the terminal investment hypothesis of life-history theory predicts that the rate of host exploitation and cercarial production should increase during the period of cercarial shedding since the reproductive value of the parasite decreases during this period. In contrast, a bet hedging hypothesis that focuses on the success of transmission when host contact rate is variable predicts that cercarial production should decrease in an attempt to keep the host alive for longer and thus would increase the probability of successful transmission. We examined these two hypotheses under laboratory conditions and recorded the production ofDiplos…
Shoaling behaviour of fish under parasitism and predation risk
Shoaling is a common antipredatory adaptation in several fish species. However, parasite infections may alter shoaling behaviour of fish by impairing fish sensory/motor systems and by reducing the net benefit of shoaling. In an experimental study, we investigated whether Diplostomum spathaceum (Trematoda) eye flukes alter shoaling behaviour of rainbow trout, Oncorhynchus mykiss, and if this has an interaction with predation risk. The parasite reduces the vision of fish by inducing cataract formation, which in previous studies has been shown to alter fish escape responses and crypsis. We found that the shoals of infected fish contained fewer individuals and they divided into separate groups …
Effect of eye fluke infection on the growth of whitefish (Coregonus lavaretus) —An experimental approach
Abstract Effect of the eye fluke Diplostomum spathaceum on fish growth has remained somewhat unclear because 1) the question has not been subjected to experimental examination with treatment-control setup and 2) growth has not been related to the coverage of parasite-induced cataracts in a quantitative manner. We examined effects of the parasite on growth and competitive ability of whitefish ( Coregonus lavaretus ) in experimental conditions resembling those at fish farms by maintaining groups of exposed and control fish, as well as mixed groups from both treatments, under optimal conditions for 8 weeks. Contrary to our expectations, we did not observe differences in fish growth between the…
Interspecific and intraspecific interactions in the monogenean communities of fish: a question of study scale?
SUMMARYMonogenean communities of fish have generally been considered non-interactive as negative interspecific interactions have rarely been reported. Most of the earlier studies on monogenean communities, however, have been conducted not only in systems with relatively low parasite abundances but, more importantly, at study scales where microhabitat-level interactions between the parasites are easily overlooked. We examined the communities of 3 abundant Dactylogyrus (Monogenea) species on the gills of crucian carp (Carassius carassius) by analysing the interactions at the scale of individual gill filaments, where interactions between the species, if any, should most likely take place. Cont…
Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope
We examined the parasite-induced cataract formation in rainbow trout (Oncorhynchus mykiss) using slit-lamp microscopy to determine the relationship between cataract intensity and number of Diplostomum spathaceum parasites that were established in the lens. Cataract intensity increased significantly with parasite burden, but was also affected by the pattern of exposure to the parasite cercariae. The slit-lamp methodology proved useful in scoring the cataracts since it provides a 3-dimensional view into the lens and gives an actual picture of the location and intensity of the cataracts, which allows detailed investigations of mechanisms underlying cataract formation in various fish species. P…
Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA.
Infections by multiple parasite species are common in nature and have important consequences for between species interactions and coevolutionary dynamics with the host populations. For example ecological and evolutionary factors underlying the structure of parasite communities determine the range of hosts a parasite can infect and set the basis for both evolution of host defences and parasite virulence as well as management of diseases. Studies investigating these factors have been facilitated in the recent past by genetic methods which surmount difficulties of traditional morphological taxonomy in identifying individual parasite species. Here we take a step further and present a novel meth…
Increasing water temperature and disease risks in aquatic systems: Climate change increases the risk of some, but not all, diseases
Global warming may impose severe risks for aquatic animal health if increasing water temperature leads to an increase in the incidence of parasitic diseases. Essentially, this could take place through a temperature-driven effect on the epidemiology of the disease. For example, higher temperature may boost the rate of disease spread through positive effects on parasite fitness in a weakened host. Increased temperature may also lengthen the transmission season leading to higher total prevalence of infection and more widespread epidemics. However, to date, general understanding of these relationships is limited due to scarcity of long-term empirical data. Here, we present one of the first long…
Importance of Sequence and Timing in Parasite Coinfections
Coinfections by multiple parasites predominate in the wild. Interactionsbetween parasites can be antagonistic, neutral, or facilitative, and they canhave significant implications for epidemiology, disease dynamics, and evolu-tion of virulence. Coinfections commonly result from sequential exposure ofhosts to different parasites. We argue that the sequential nature of coinfectionsis important for the consequences of infection in both natural and man-madeenvironments. Coinfections accumulate during host lifespan, determining thestructure of the parasite infracommunity. Interactions within the parasite com-munity and their joint effect on the host individual potentially shape evolution ofparasi…
Divergent parasite infections in sympatric cichlid species in Lake Victoria
Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species‐rich communities and as a driver of post‐speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiatio…
Sequential infection can decrease virulence in a fish–bacterium–fluke interaction: Implications for aquaculture disease management
Hosts are typically infected with multiple strains or genotypes of one or several parasite species. These infections can take place simultaneously, but also at different times, i.e. sequentially, when one of the parasites establishes first. Sequential parasite dynamics are common in nature, but also in intensive farming units such as aquaculture. However, knowledge of effects of previous exposures on virulence of current infections in intensive farming is very limited. This is critical as consecutive epidemics and infection history of a host could underlie failures in management practises and medical intervention of diseases. Here, we explored effects of timing of multiple infection on viru…
Sensitivity of bipartite network analyses to incomplete sampling and taxonomic uncertainty
Bipartite network analysis is a powerful tool to study the processes structuring interactions in ecological communities. In applying the method, it is assumed that the sampled interactions provide an accurate representation of the actual community. However, acquiring a representative sample may be difficult as not all species are equally abundant or easily identifiable. Two potential sampling issues can compromise the conclusions of bipartite network analyses: failure to capture the full range of interactions (sampling completeness) and use of a taxonomic level higher than species to evaluate the network (taxonomic resolution). We asked how commonly used descriptors of bipartite antagonisti…
Divergent parasite infections in sympatric cichlid species in Lake Victoria
Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species-rich communities and as a driver of post-speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiatio…
Transmission of Diplostomum spathaceum between intermediate hosts
FM Anssi Karvonen tutki väitöskirjassaan kalojen silmän linssissä elävän Diplostomum spathaceum -imumatoloisen ekologiaa. Tutkimus tarjoaa uutta tietoa lois-isäntä -suhteiden evoluutiosta sekä perustietoa, jonka avulla voidaan suunnitella loisen torjuntamenetelmiä kalanviljelyssä. Tutkimukset ovat lisäksi osa laajempaa projektia, jossa tutkitaan D. spathaceum -loisen elinkierron ekologiaa ja evoluutiota kaikissa elinkierron vaiheissa. Sen yhtenä päämääränä on kehittää elinkierron matemaattinen malli, jonka avulla on mahdollista kehittää ekologisesti kestäviä menetelmiä D. spathaceum -loisen torjuntaan.D. spathaceum on yksi luonnonkalojen yleisimmistä loisista Suomessa ja sitä esiintyy myös …
Transmission, infectivity and survival of Diplostomum spathaceum cercariae
The transmission dynamics of the cercariae of Diplostomum spathaceum were investigated under laboratory conditions using cercariae collected from naturally infected Lymnaea stagnalis. Cercariae were kept in a constant temperature of 20 °C and the survival and infectivity to naïve young rainbow trout recorded at 3-h intervals until few cercariae were alive. Mortality initially remained constant but increased rapidly after 20 h. While a model of constant mortality fitted the survival data, an age-dependent model provided a better fit and implied that cercariae tended to carry similar quantities of resources and once these were exhausted the cercariae died. Cercarial infectivity also showed an…
Supplementary tables and figures from Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations
Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon (Salmo salar) and sea trout (an anadromous form of brown trout, Salmo trutta) were raised under common garden conditions and infected with the eye fluke …
Diplostomum spathaceum metacercarial infection and colour change in salmonid fish
Colour changes in two salmonid fish, the salmon (Salmo salar) and sea trout (S. trutta), were examined in relation to infection with the trematode Diplostomum spathaceum. This parasite had no effect on the rate of colour change in these fish, although species specific differences in colour adjustment times were observed. Increasing asymmetry in parasite numbers between the right and left eye, which could lead to the retention of vision in one eye, nevertheless tended to reduce the colour change time in salmon with moderate infection (P=0.08). This first experimental attempt to examine colour changes in fish in relation to eye fluke infections provides grounds for future investigations. The …
Learned parasite avoidance is driven by host personality and resistance to infection in a fish-trematode interaction
Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum , we asked whether sea trout ( Salmo trutta trutta ) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased af…
Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish.
This paper examines the efficiency of acquired resistance in protecting the fish host, rainbow trout (Oncorhynchus mykiss), against the trematode parasite Diplostomum spathaceum, and the hypothesis that fish recognize areas where infective stages are aggregated and show avoidance behaviour. We found that when fish with a low level of infection were held in restricted cages in natural conditions they became infected and developed cataracts as a result of this infection. This suggests that acquired resistance is insufficient in protecting fish against the parasite or the deleterious effects of infection in conditions where fish could not avoid the parasite. Behavioural experiments in the labo…
Water temperature, not fish morph, determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)
Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the hos…
Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus)
Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most hostparasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in populationpairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide…
Supplementary figures
Supplementary figures S1-S3.
supplementary information and data from Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentration of antibiotic affects the co-infection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum, in their fish host. We found that antibiotic in fee…
Reciprocal interaction matrix reveals complex genetic and dose-dependent specificity among coinfecting parasites
Understanding genetic specificity in factors determining the outcome of host-parasite interactions is especially important as it contributes to parasite epidemiology, virulence, and maintenance of genetic variation. Such specificity, however, is still generally poorly understood. We examined genetic specificity in interactions among coinfecting parasites. In natural populations, individual hosts are often simultaneously infected by multiple parasite species and genotypes that interact. Such interactions could maintain genetic variation in parasite populations if they are genetically specific so that the relative fitness of parasite genotypes varies across host individuals depending on (1) t…
Establishment and interspecific associations in two species of Ichthyocotylurus (Trematoda) parasites in perch (Perca fluviatilis)
Abstract Background Co-infections of multiple parasite species in hosts may lead to interspecific associations and subsequently shape the structure of a parasite community. However, few studies have focused on these associations in highly abundant parasite species or, in particular, investigated how the associations develop with time in hosts exposed to co-infecting parasite species for the first time. We investigated metacercarial establishment and interspecific associations in the trematodes Ichthyocotylurus variegatus and I. pileatus co-infecting three age cohorts of young perch (Perca fluviatilis). Results We found that the timing of transmission of the two Ichthyocotylurus species was …
Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction
Abstract Trophically transmitted parasites may increase their transmission efficiency by altering the behaviour of infected hosts to increase their susceptibility to predation by target hosts (the next host in the life cycle). The parasite Diplostomum spathaceum (Trematoda) reduces the vision of its fish intermediate hosts: its metacercariae lodge themselves in the eyes of fish and induce cataract formation, which gives them the opportunity to affect fish behaviour. We examined whether D. spathaceum eye flukes change the preference of fish for the surface layers of the water column or their escape behaviour, which could make the fish more vulnerable to predation by bird hosts. We also studi…
Data from: Spatiotemporal and gender-specific parasitism in two species of gobiid fish
Parasitism is considered a major selective force in natural host populations. Infections can decrease host condition and vigour, and potentially influence e.g. host population dynamics and behaviour such as mate choice. We studied parasite infections of two common marine fish species, the sand goby (Pomatoschistus minutus) and the common goby (Pomatoschistus microps), in the brackish water Northern Baltic Sea. We were particularly interested in the occurrence of parasite taxa located in central sensory organs, such as eyes, potentially affecting fish behaviour and mate choice. We found that both fish species harboured parasite communities dominated by taxa transmitted to fish through aquati…
Data from: Parasite infection in a central sensory organ of fish does not affect host personality
Among the ecological factors acting on the evolution and expression of animal personalities and behavioral syndromes, parasitism has received comparatively little attention. However, infection and host behavior are often strongly intertwined, because host behavior can predict the risk of infection and can also be changed by an infection. We conducted a controlled experimental infection study to explore the effects of infection on host boldness, exploration and activity using rainbow trout Oncorhynchus mykiss and its trematode parasite Diplostomum pseudospathaceum, which infects a central sensory organ of the fish, the eye lens. Contrary to our expectation, infection did not change the withi…
Data from: Interactions among bacterial strains and fluke genotypes shape virulence of co-infection
Most studies of virulence of infection focus on pairwise host-parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of effects of genotype by genotype (G×G) interactions between unrelated parasite species on virulence of co infection is limited. Here we tested such relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mortality) …
Data from: Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite
Characterizing genetic variation in parasite transmission traits and its contribution to parasite vigor is essential for understanding the evolution of parasite life-history traits. We measured genetic variation in output, activity, survival, and infection success of clonal transmission stages (cercaria larvae) of a complex life cycle parasite (Diplostomum pseudospathaceum). We further tested if variation in host nutritional stage had an effect on these traits by keeping hosts on limited or ad libitum diet. The traits we measured were highly variable among parasite genotypes indicating significant genetic variation in these life-history traits. Traits were also phenotypically variable, for …
Data from: Rearing background and exposure environment together explain higher survival of aquaculture fish during a bacterial outbreak
1. Parasitic diseases represent one of the greatest challenges for aquaculture worldwide and there is an increasing emphasis on ecological solutions to prevent infections. One proposed solution is enriched rearing, where traditional stimulus-poor rearing tanks are equipped with different types of structures to increase habitat complexity. Such spatial enrichment is known to increase survival of fish during parasite epidemics, but the underlying mechanisms are still unclear. 2. We studied whether enriched rearing affected infection of an important fish pathogen Flavobacterium columnare in young Atlantic salmon (Salmo salar) and sea-migrating brown trout (Salmo trutta). First, we used natural…
Data from: Enriched rearing environment and wild genetic background can enhance survival and disease resistance of salmonid fishes during parasite epidemics
The importance and volume of aquaculture is increasing world-wide. Rearing practices play a key role in determining growth rate, survival and disease resistance in aquaculture fishes. Recent evidence suggests that in comparison with a standard stimulus-poor rearing environment, an enriched or variable rearing environment has significant positive effects on several traits underlying growth and well-being of fish. However, the effect of enriched rearing on one of the most important threats for aquaculture development, occurrence of parasitic infections, remains unknown. We used surveillance data of experimental salmonid populations of wild and hatchery origin under semi-natural parasite expos…
Data from: Minor environmental concentrations of antibiotics can modify bacterial virulence in co-infection with a non-targeted parasite
Leakage of medical residues into the environment can significantly impact natural communities. For example, antibiotic contamination from agriculture and aquaculture can directly influence targeted pathogens, but also other non-targeted taxa of commensals and parasites that regularly co-occur and co-infect the same host. Consequently, antibiotics could significantly alter interspecific interactions and epidemiology of the co-infecting parasite community. We studied how minor environmental concentration of antibiotic affects the coinfection of two parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum, in their fish host. We found that antibiotic in feed…
Data from: Learned parasite avoidance is driven by host personality and resistance to infection in a fish–trematode interaction
Cognitive abilities related to the assessment of risk improve survival. While earlier studies have examined the ability of animals to learn to avoid predators, learned parasite avoidance has received little interest. In a series of behavioural trials with the trematode parasite Diplostomum pseudospathaceum, we asked whether sea trout (Salmo trutta trutta) hosts show associative learning in the context of parasitism and if so, whether learning capacity is related to the likelihood of infection mediated through host personality and resistance. We show that animals are capable of learning to avoid visual cues associated with the presence of parasites. However, avoidance behaviour ceased after …
Data from: Food makes you a target: disentangling genetic, physiological, and behavioral effects determining susceptibility to infection
Genetics, physiology and behavior are all expected to influence the susceptibility of hosts to parasites. Furthermore, interactions between genetic and other factors are suggested to contribute to the maintenance of genetic polymorphism in resistance when the relative susceptibility of host genotypes is context dependent. We used a maternal sibship design and long- and short-term food deprivation treatments to test the role of family-level genetic variation, body condition, physiological state and foraging behavior on the susceptibility of Lymnaea stagnalis snails to infection by a trematode parasite that uses chemical cues to locate its hosts. In experimental exposures, we found that snail…
Data from: Host infection history modifies co-infection success of multiple parasite genotypes
1. Co-infections by multiple parasite genotypes are common and have important implications for host-parasite ecology and evolution through within-host interactions. Typically, these infections take place sequentially and therefore, the outcome of co-infection may be shaped by host immune responses triggered by previous infections. For example, in vertebrates specific immune responses play a central role in protection against disease over the course of life, but co-infection research has mostly focused on previously uninfected individuals. 2. Here, we investigated whether sequential exposure and activation of host resistance in rainbow trout Oncorhynchus mykiss affects infection success and …
Data from: Reciprocal interaction matrix reveals complex genetic and dose-dependent specificity among coinfecting parasites
Understanding genetic specificity in factors determining the outcome of host-parasite interactions is especially important as it contributes to parasite epidemiology, virulence, and maintenance of genetic variation. Such specificity, however, is still generally poorly understood. We examined genetic specificity in interactions among coinfecting parasites. In natural populations, individual hosts are often simultaneously infected by multiple parasite species and genotypes that interact. Such interactions could maintain genetic variation in parasite populations if they are genetically specific so that the relative fitness of parasite genotypes varies across host individuals depending on (1) t…
Data from: Sequential infection can decrease virulence in a fish-bacterium-fluke interaction: implications for aquaculture disease management
Hosts are typically infected with multiple strains or genotypes of one or several parasite species. These infections can take place simultaneously, but also at different times, i.e. sequentially, when one of the parasites establishes first. Sequential parasite dynamics are common in nature, but also in intensive farming units such as aquaculture. However, knowledge of effects of previous exposures on virulence of current infections in intensive farming is very limited. This is critical as consecutive epidemics and infection history of a host could underlie failures in management practises and medical intervention of diseases. Here, we explored effects of timing of multiple infection on viru…
Data from: Divergent ectoparasite infections in sympatric cichlid species in Lake Victoria
Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species rich communities, and as a driver of post-speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked if host niche, host abundance or host genetic differentiation ex…
Original data for manuscript: Quantity and Quality of Aquaculture Enrichments Influence Disease Epidemics and Provide Ecological Alternatives to Antibiotics
The data processed and analyzed in this study are given in a single file: Karvonen et al. exposure data.xlsx. For detailed description of the material, methods and results of the study, see the article.
Alkuperäinen aineisto julkaisulle: Differences in parasite community composition support ecological differentiation in a freshwater gadoid fish
The data file contains original data from burbot (Lota lota), captured from two sampling depths, littoral and profundal, in Lake Konnevesi during the breeding season of the fish in 2019-2020. The other variables indicate total body length of the fish (mm), gender, and abundance of 9 metazoan parasite taxa observed in the fish. Column F indicates the mean coverage of cataracts caused by Diplostomum parasites found in the eye lenses (column E).