Parasites alter their host behaviour and vice versa as a result of mutual adaptations in the evolutionary arms race. One of these adaptations involves changes in host thermoregulation, which has the potential to harm the parasite and thereby act as a defence mechanism. We used a model of the brown trout (Salmo trutta) experimentally parasitised with glochidia ectoparasitic larvae from the endangered freshwater pearl mussel (Margaritifera margaritifera) to reveal whether parasitisation alters fish behavioural thermoregulation. A study using radiotelemetry temperature sensors was performed during almost one year of the M. margaritifera parasitic stage. Glochidia-infested S. trutta altered their thermoregulation through active searching for habitats with different thermal regimes. The general preference for temperatures in infested fish varied and was either above or below the temperature preferred by uninfested individuals. Infested fish also preferred different temperatures across localities, whereas uninfested fish maintained their thermal preference no matter which stream they inhabited. Glochidia further induced the expression of a behavioural syndrome among S. trutta personality traits, suggesting that it might increase the probability that the fish host would occur in the glochidia temperature optimum. Our findings present the first evidence that thermoregulation plays a fundamental role in the relationship of affiliated mussels and their fish hosts. Incorporating thermoregulation as a factor in the study of this relationship can help to interpret results from previous behavioural studies, as well as to optimise management measures related to endangered mussels.
- MeSH
- Acclimatization MeSH
- Host-Parasite Interactions MeSH
- Larva growth & development physiology MeSH
- Bivalvia growth & development physiology MeSH
- Fish Diseases parasitology MeSH
- Trout * MeSH
- Body Temperature Regulation * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Parasitic infections elicit host defences that pose energetic trade-offs with other fitness-related traits. Bitterling fishes and unionid mussels are involved in a two-way parasitic interaction. Bitterling exploit mussels by ovipositing into their gills. In turn, mussel larvae (glochidia) develop on the epidermis and gills of fish. Hosts have evolved behavioural responses to reduce parasite load, suggesting that glochidia and bitterling parasitism are costly. We examined the energetic cost of parasitism on both sides of this relationship. We used intermittent flow-through respirometry to measure (1) standard metabolic rate (SMR) of individual duck mussels Anodonta anatina (a common bitterling host) before and during infection by embryos of the European bitterling Rhodeus amarus, and (2) SMR and maximum oxygen uptake (MO2max) of individual R. amarus before and during infection with glochidia of the Chinese pond mussel Sinanodonta woodiana (a mussel species that successfully infects bitterling). As predicted, we observed an increase in mussel SMR when infected by bitterling embryos and an increased SMR in glochidia-infected bitterling, though this was significantly mediated by the time post-infection. Contrary to our predictions, glochidia infection did not impair MO2max and the number of glochidia attached to gills positively (rather than negatively) correlated with MO2max. The results suggest that tolerance is the prevailing coping mechanism for both fish and mussels when infected, while resistance mechanisms appear to be confined to the behavioural level.
- MeSH
- Cyprinidae * MeSH
- Host-Parasite Interactions MeSH
- Oxygen MeSH
- Parasites * MeSH
- Oxygen Consumption MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Parasitization by the larvae (glochidia) of freshwater mussels can cause harm to a fish's gills, resulting in less effective respiration and/or reduced activity by the host fish. The impact of glochidia infections on the host's physiology remains poorly understood, and no information is available concerning energy consumption in parasitized fish. Hence, we obtained glochidia of the invasive unionid mussel Sinanodonta (Anodonta) woodiana and experimentally infected common carp, Cyprinus carpio, tagged with physiological sensors to measure energy consumption. We tested the hypothesis that parasitization affects energy consumption in the host fish, reflected as higher energy costs for movement and reduced movement activity over eight days post-infection within a twenty-four-hour cycle. Parasitized fish showed higher energy costs of movement; however, no changes in movement activity were found compared with activity in control fish. Significantly increased biochemical indices were measured in host fish blood samples, including aspartate (AST) and alanine (ALT) aminotransferase levels, indicating liver injury, and high concentrations of potassium (K(+)), signifying kidney injury (hyperkalemia). Increased Cl(-) concentrations indicate gill dysfunction. Our results show that the energy costs due to glochidia parasitization are independent of overall movement activity patterns and vary in time according to the parasitic phase and the diurnal cycle. Moreover, the side effects of parasitization have a more important impact on fish hosts than has been shown in previous reports.
- MeSH
- Alanine Transaminase blood MeSH
- Analysis of Variance MeSH
- Aspartate Aminotransferases blood MeSH
- Chlorides blood MeSH
- Potassium blood MeSH
- Electromyography MeSH
- Energy Metabolism physiology MeSH
- Carps blood parasitology physiology MeSH
- Parasites pathogenicity MeSH
- Movement physiology MeSH
- Probability MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Interspecific relationships frequently determine the effect a pollutant can have on an organism, and this is especially true in closely interacting species such as hosts and parasites. The high spatial and temporal variability of contaminant concentrations combined with the movement of aquatic biota can further influence the consequences that are associated with contamination. We used a full factorial design for the exposed and unexposed partners of the relationship between the parasitic larvae (glochidia) of the European freshwater mussel (Anodonta anatina) and its host fish (Squalius cephalus) to identify the sources of variation in the sublethal endpoints of species interaction (the intensity of parasite attachment, the spatial position of glochidia on the host body, and encapsulation success). We used the water-borne human pharmaceutical compounds methamphetamine (a central nervous system stimulant) and tramadol (an opioid) at environmentally relevant concentrations (˜ 6.7 and 3.8 nmol L-1 of methamphetamine and tramadol, respectively) as a proxy for contaminant exposure because these compounds are emerging aquatic stressors that are known for high spatial and temporal variability in their detected concentration levels. The relationship between the bivalve and the fish species was influenced by the preceding contact with both methamphetamine and tramadol, but this effect was highly asymmetric. Our experimental design enabled us to identify the specific changes in the relationship outcome that are elicited by the exposure of individual partners, such as the significant increase in glochidia infection success rate from 59.6 ± 3.9% to 78.7 ± 2.8% (means ± s.e.) that was associated with host exposure to methamphetamine. Additionally, the significant interaction effect of the exposure was demonstrated by the lowered proportion of glochidia attached to gills after the coexposure of both partners to tramadol. The impact of pharmaceuticals on wild aquatic host-parasite relationships provides an example of the risks that are associated with the unintentional discharge of biologically active compounds into freshwater habitats. Given the increasing evidence showing the ecological impact of waste pharmaceuticals, the use of multitrophic interaction endpoints after joint and unilateral exposures provides an important step towards the realistic risk assessment of these compounds.
- MeSH
- Anodonta drug effects growth & development MeSH
- Water Pollutants, Chemical toxicity MeSH
- Cyprinidae parasitology MeSH
- Host-Parasite Interactions drug effects MeSH
- Larva growth & development MeSH
- Environmental Monitoring methods MeSH
- Fresh Water chemistry MeSH
- Toxicity Tests MeSH
- Gills parasitology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
The glochidium larvae of freshwater mussels of the family Unionidae need to find suitable hosts to attach themselves and metamorphose into free-living juveniles. The specificity of the host-parasite relationship was investigated for the Iberian Unio tumidiformis Castro, 1885 by means of experimental infections and also by analyzing naturally infected fish. The process of encapsulation of glochidia was studied using scanning electron microscopy. Unio tumidiformis has proven to be an unusual host-specific unionid mussel, apparently parasitizing only fish of the genus Squalius Bonaparte, 1837. Successful encapsulation or complete metamorphosis was observed in five fish taxa: S. aradensis (Coelho, Bogutskaya, Rodrigues et Collares-Pereira), S. caroliterti (Doadrio), S. pyrenaicus (Günther), S. torgalensis (Coelho, Bogutskaya, Rodrigues et Collares-Pereira) and S. alburnoides (Steindachner) complex (only for the nuclear hybrids with at least one copy of the S. pyrenaicus genome). Complete metamorphose was achieved in 6 to 14 days at mean temperatures ranging from 21.8 to 26.1 degrees C. The current study provides support for cell migration being the main force of cyst formation and shows the influence of potential host's genome in response to the infection process to determine the success of the metamorphosis.
- MeSH
- Metamorphosis, Biological physiology MeSH
- Epithelium physiology MeSH
- Host-Parasite Interactions physiology MeSH
- Larva growth & development physiology ultrastructure MeSH
- Bivalvia growth & development physiology ultrastructure MeSH
- Fishes parasitology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Portugal MeSH
The Chinese sleeper (Perccottus glenii), an invasive Asian fish, was first registered in Germany in 2009 (westernmost extent of its invasive range). We sampled Chinese sleepers from two localities on the Bücherlgraben creek (a tributary of the River Naab) in south-eastern Germany in November 2015 and examined them for parasite infection. Twelve taxa were registered, including ciliates (unidentified Trichodina), a monogenean, three cestode species, two digenean taxa, two acanthocephalan species, two nematode species and one mollusc glochidia. Infracommunities consisted of 1-5 species, with 10% of fish uninfected. Three parasite species (Acanthocephalus anguillae, Gyrodactylus luciopercae and Pseudocapillaria tomentosa) were recorded on Chinese sleepers for the first time. The results highlight the important role of the Chinese sleeper as a second intermediate host in the life cycle of heron and grebe parasites. The Chinese sleeper parasite community displayed low homogeneity at both localities sampled, with allogenic parasites (metacercariae and mesocercoids) mostly shared. Differences between localities were mainly caused by autogenic parasites. No invasive parasites associated with the Chinese sleeper were observed in the study area, all parasites being representatives of European fauna. This supports the hypothesis of introduction via the aquarium trade or through transport with commercial fish.
- MeSH
- Cestoda classification genetics isolation & purification MeSH
- Cestode Infections parasitology veterinary MeSH
- Trematode Infections parasitology veterinary MeSH
- Fish Diseases parasitology MeSH
- Rivers parasitology MeSH
- Fishes MeSH
- Trematoda classification genetics isolation & purification MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Germany MeSH
