0000000001319252
AUTHOR
Otto Seppälä
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…
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…
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…
Acanthocephalan size and sex affect the modification of intermediate host colouration
Parasitology, 136 (8)
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…
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-…
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…
Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted?
Parasitology, 136 (2)
Direct and transgenerational effects of an experimental heat wave on early life stages in a freshwater snail
AbstractGlobal climate change imposes a serious threat to natural populations of many species. Estimates of the effects of climate change-mediated environmental stresses are, however, often based only on their direct effects on organisms, and neglect the potential transgenerational effects. We investigated whether high temperature (i.e. an experimental heat wave) that is known to reduce performance of adultLymnaea stagnalissnails affects their offspring through maternal effects. Specifically, we tested whether eggs and hatched juveniles are affected by maternal thermal environment, and how strong these effects are compared with direct effects of temperature on offspring. We examined the eff…
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…
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.
Direct and transgenerational effects of an experimental heatwave on early life stages in a freshwater snail
1. Global climate change imposes a serious threat to natural populations of many species. Estimates of the effects of climate change‐mediated environmental stresses are, however, often based only on their direct effects on organisms, and neglect the potential transgenerational (e.g. maternal) effects. 2. We tested whether high temperature (i.e. an experimental heatwave), which is known to reduce the performance of adult Lymnaea stagnalis snails, affects the produced offspring (eggs and hatchlings) through maternal effects, and how strong these effects are compared with the effects of direct exposure of offspring to high temperature. We examined the effect of maternal thermal environment (15…
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…
Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan
Parasitology, 135 (5)
Quality attracts parasites: host condition‐dependent chemo‐orientation of trematode larvae
Summary Environmental factors impairing physiological condition of organisms are assumed to predispose them to parasite infections. This is because host immune function is typically condition-dependent. However, poor physiological condition has been reported to reduce host susceptibility to parasites in various systems. We examined whether such an effect can be due to altered exposure of hosts to active parasite transmission stages by investigating chemo-orientation of free-swimming cercariae larvae of a parasite Echinoparyphium aconiatum towards its snail host Lymnaea stagnalis. We used both long-term and short-term feeding treatments to manipulate the body condition and physiological trai…
Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population.
Background On-going global climate change poses a serious threat for natural populations unless they are able to evolutionarily adapt to changing environmental conditions (e.g. increasing average temperatures, occurrence of extreme weather events). A prerequisite for evolutionary change is within-population heritable genetic variation in traits subject to selection. In relation to climate change, mainly phenological traits as well as heat and desiccation resistance have been examined for such variation. Therefore, it is important to investigate adaptive potential under climate change conditions across a broader range of traits. This is especially true for life-history traits and defences ag…
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…
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…
QUALITATIVE AND QUANTITATIVE BEHAVIORAL TRAITS IN A COMMUNITY OF FURCOCERCARIAE TREMATODES: TOOLS FOR SPECIES SEPARATION?
Many trematode cercariae show distinct behavioral features, which have commonly been used in species identification in combination with morphological characteristics. However, information regarding cercariae behavior has often not been quantified in detail, or it is scattered in the literature, which is why the appropriate level of precision in behavioral identity, particularly in groups of cercariae species showing considerable morphological overlap, has not been properly established. In this study, we investigated one such group, the furcocercariae trematodes, by studying their behavior in a community consisting of 8 species (Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Coty…
An experimental heat wave changes immune defense and life history traits in a freshwater snail
The predicted increase in frequency and severity of heat waves due to climate change is expected to alter disease dynamics by reducing hosts' ability to resist infections. This could take place via two different mechanisms: (1) through general reduction in hosts' performance under harsh environmental conditions and/or (2) through altered resource allocation that reduces expression of defense traits in order to maintain other traits. We tested these alternative hypotheses by measuring the effect of an experimental heat wave (25 vs. 15°C) on the constitutive level of immune defense (hemocyte concentration, phenoloxidase [PO]‐like activity, antibacterial activity of hemolymph), and life histor…
Host manipulation by parasites : adaptation to enhance transmission?
Otto Seppälä tutki väitöskirjassaan loisten kykyä manipuloida isäntiään mahdollisena strategiana tehostaa loisten siirtymistä uusiin isäntäyksilöihin. Monien loisten on havaittu vaikuttavan mm. isäntiensä käyttäytymiseen ja ulkonäköön. Erityisesti ravintoketjuissa saaliseläimistä saalistajiin kulkeutuvilla loisilla isännän manipulointia on yleisesti pidetty loisten evolutiivisena sopeumana altistaa isännät saalistajille ja täten tehostaa loisten siirtymistä elinkierrossa eteenpäin. Manipulaatioteoriaa on kuitenkin vain harvoin testattu kriittisesti selvittämällä saalistuskokein loisten aiheuttamien käyttäytymismuutosten vaikutusta isäntien saalistusalttiuteen.Seppälä selvitti useiden eri ka…
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…
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…
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: Quality attracts parasites: host condition-dependent chemo-orientation of trematode larvae
1. Environmental factors impairing physiological condition of organisms are assumed to predispose them to parasite infections. This is because host immune function is typically condition-dependent. However, poor physiological condition has been reported to reduce host susceptibility to parasites in various systems. 2. We examined whether such an effect can be due to altered exposure of hosts to active parasite transmission stages by investigating chemo-orientation of free-swimming cercariae larvae of a parasite Echinoparyphium aconiatum towards its snail host Lymnaea stagnalis. 3. We used both long-term and short-term feeding treatments to manipulate the body condition and physiological tra…
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: 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…