Host-parasite interactions between freshwater pearl mussels (Margaritifera margaritifera) and their salmonid hosts

The freshwater pearl mussel, Margaritifera margaritifera, is an endangered bivalve which has suffered a serious decline across its Holarctic distribution. It has a complex life cycle which involves an obligate parasitic stage on a suitable host. M. margaritifera populations are very host specific, and they are able to metamorphose only on the gills of Atlantic salmon (Salmo salar), sea trout (Salmo trutta f. trutta) or brown trout (S. trutta f. fario). Currently, the main concern is the lack of juvenile recruitment and survival in organically enriched river sediments. Consequently, several conservation programmes are rearing mussels in hatcheries, for eventual release back into their natural habitat when they are older and better able to survive. Although M. margaritifera do not reproduce on their hosts, their survival is highly dependent on the presence of suitable hosts. The main purpose of this study was to improve our understanding of the host-parasite interactions and their influence on glochidial or juvenile mussel fitness, with the aim of providing information that could be used to refine future conservation strategies. In the first experiment, the duration of the parasitic phase had a significant positive influence on post parasitic fitness of juvenile mussels in eight populations in Norway. Fitness was measured as size at excystment, post parasitic growth and survival. The strong positive relationship observed between the test variables clearly indicated that glochidial growth and development were dependent on individual host-parasite compatibility. In the same experiment, temperature was also observed to be an important factor governing excystment of juvenile mussels, with higher temperatures decreasing the duration of the parasitic phase. The variation in host suitability has been linked to environmental conditions, host age and/or size, genetic composition of the host and parasite, or a combination of these factors. Therefore, in the second experiment, the effect of host age on glochidial infestation was examined under common garden conditions. Hosts (0+ and 1+) were infested with glochidia from closely related mothers in order to remove the confounding effects of genotype-specific host interactions. A host age dependent immune response was observed, i.e. the 0+ hosts displayed a resistant strategy, whereas the 1+ hosts displayed a tolerant one. In the second and third experiments, the virulent effects of glochidia on their hosts were examined, and measured as haematocrit values and host mortality respectively. Haematocrit values were significantly elevated in heavily infested hosts, which indicated respiratory distress (Chapter 3). In addition, glochidia were highly virulent on the less suitable host species, resulting in high mortalities of infested hosts (Chapter 4). Both these results display the parasitic nature of M. margaritifera in the host-parasite interaction. In the third experiment, the hypothesis that glochidia from a single mother could infest both salmon and trout hosts was examined. The results showed that glochidia from a population that uses salmon as its principal host were able to infest both species, but some mothers displayed a bias for either salmon or trout. These observations were probably a result of the higher genetic diversity observed in salmon-mussel populations. Individual and population level genetic diversity is associated with species fitness and an ability to adapt to a changing environment, which can help ensure long-term survival. All the results of this study clearly indicate that the degree of host-parasite compatibility has an influence on glochidial and juvenile mussel fitness. Further studies should investigate factors that influence host-parasite interactions, for example the diversity of the genes of the host major histocompatibility complex (MHC). Based on the results, it is recommended that naive 1+ hosts are preferably used in captive breeding programmes, as this will maximise the production of juvenile mussels. The use of high quality hosts will also minimise the possible selection and genetic drift effects. Such effects lead to a deterioration in the evolutionary potential to adapt to a changing environment. Since glochidial development and successful metamorphosis into juvenile mussels is highly dependent on good host condition and survival, it is recommended that conservation efforts should focus on methods that can guarantee this

Higher mortality of the less suitable brown trout host compared to the principal Atlantic salmon host when infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia

The freshwater pearl mussel (Margaritifera margaritifera) is a highly host-specific parasite, with an obligate parasitic stage on salmonid fish. Atlantic salmon (Salmo salar) and brown trout (Salmo trutta f. trutta and Salmo trutta f. fario) are the only hosts in their European distribution. Some M. margaritifera populations exclusively infest either Atlantic salmon or brown trout, while others infest both hosts with one salmonid species typically being the principal host and the other a less suitable host. Glochidial abundance, prevalence and growth are often used as parameters to measure host suitability, with the most suitable host species displaying the highest parameters. However, it is not known if the degree of host specialisation will negatively influence host fitness (virulence) among different host species. In this study we examined the hypothesis that glochidial infestation would result in differential virulence in two salmonid host species and that lower virulence would be observed on the most suitable host. Atlantic salmon and brown trout were infested with glochidia from two M. margaritifera populations that use Atlantic salmon as their principal host, and the difference in host mortality among infested and control (sham infested) fish was examined. Higher mortality was observed in infested brown trout (the less suitable host) groups, compared to the other test groups. Genetic assignment was used to identify offspring from individual mother mussels. We found that glochidia from individual mothers can infest both the salmonid hosts; however, some mothers displayed a bias towards either salmon or trout. We believe that the differences in host-dependent virulence and the host bias displayed by individual mothers were a result of genotype × genotype interactions between the glochidia and their hosts, indicating that there is an underlying genetic component for this parasite-host interaction.publishedVersio

Host-parasite interactions between freshwater pearl mussels (Margaritifera margaritifera) and their salmonid hosts

The freshwater pearl mussel, Margaritifera margaritifera, is an endangered bivalve which has suffered a serious decline across its Holarctic distribution. It has a complex life cycle which involves an obligate parasitic stage on a suitable host. M. margaritifera populations are very host specific, and they are able to metamorphose only on the gills of Atlantic salmon (Salmo salar), sea trout (Salmo trutta f. trutta) or brown trout (S. trutta f. fario). Currently, the main concern is the lack of juvenile recruitment and survival in organically enriched river sediments. Consequently, several conservation programmes are rearing mussels in hatcheries, for eventual release back into their natural habitat when they are older and better able to survive. Although M. margaritifera do not reproduce on their hosts, their survival is highly dependent on the presence of suitable hosts. The main purpose of this study was to improve our understanding of the host-parasite interactions and their influence on glochidial or juvenile mussel fitness, with the aim of providing information that could be used to refine future conservation strategies. In the first experiment, the duration of the parasitic phase had a significant positive influence on post parasitic fitness of juvenile mussels in eight populations in Norway. Fitness was measured as size at excystment, post parasitic growth and survival. The strong positive relationship observed between the test variables clearly indicated that glochidial growth and development were dependent on individual host-parasite compatibility. In the same experiment, temperature was also observed to be an important factor governing excystment of juvenile mussels, with higher temperatures decreasing the duration of the parasitic phase. The variation in host suitability has been linked to environmental conditions, host age and/or size, genetic composition of the host and parasite, or a combination of these factors. Therefore, in the second experiment, the effect of host age on glochidial infestation was examined under common garden conditions. Hosts (0+ and 1+) were infested with glochidia from closely related mothers in order to remove the confounding effects of genotype-specific host interactions. A host age dependent immune response was observed, i.e. the 0+ hosts displayed a resistant strategy, whereas the 1+ hosts displayed a tolerant one. In the second and third experiments, the virulent effects of glochidia on their hosts were examined, and measured as haematocrit values and host mortality respectively. Haematocrit values were significantly elevated in heavily infested hosts, which indicated respiratory distress (Chapter 3). In addition, glochidia were highly virulent on the less suitable host species, resulting in high mortalities of infested hosts (Chapter 4). Both these results display the parasitic nature of M. margaritifera in the host-parasite interaction. In the third experiment, the hypothesis that glochidia from a single mother could infest both salmon and trout hosts was examined. The results showed that glochidia from a population that uses salmon as its principal host were able to infest both species, but some mothers displayed a bias for either salmon or trout. These observations were probably a result of the higher genetic diversity observed in salmon-mussel populations. Individual and population level genetic diversity is associated with species fitness and an ability to adapt to a changing environment, which can help ensure long-term survival. All the results of this study clearly indicate that the degree of host-parasite compatibility has an influence on glochidial and juvenile mussel fitness. Further studies should investigate factors that influence host-parasite interactions, for example the diversity of the genes of the host major histocompatibility complex (MHC). Based on the results, it is recommended that naive 1+ hosts are preferably used in captive breeding programmes, as this will maximise the production of juvenile mussels. The use of high quality hosts will also minimise the possible selection and genetic drift effects. Such effects lead to a deterioration in the evolutionary potential to adapt to a changing environment. Since glochidial development and successful metamorphosis into juvenile mussels is highly dependent on good host condition and survival, it is recommended that conservation efforts should focus on methods that can guarantee this

Data from: Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera)

Host–parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long-lived and highly host-specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter-lived host fish (Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness-related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts

Higher mortality of the less suitable brown trout host compared to the principal Atlantic salmon host when infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia

The freshwater pearl mussel (Margaritifera margaritifera) is a highly host-specific parasite, with an obligate parasitic stage on salmonid fish. Atlantic salmon (Salmo salar) and brown trout (Salmo trutta f. trutta and Salmo trutta f. fario) are the only hosts in their European distribution. Some M. margaritifera populations exclusively infest either Atlantic salmon or brown trout, while others infest both hosts with one salmonid species typically being the principal host and the other a less suitable host. Glochidial abundance, prevalence and growth are often used as parameters to measure host suitability, with the most suitable host species displaying the highest parameters. However, it is not known if the degree of host specialisation will negatively influence host fitness (virulence) among different host species. In this study we examined the hypothesis that glochidial infestation would result in differential virulence in two salmonid host species and that lower virulence would be observed on the most suitable host. Atlantic salmon and brown trout were infested with glochidia from two M. margaritifera populations that use Atlantic salmon as their principal host, and the difference in host mortality among infested and control (sham infested) fish was examined. Higher mortality was observed in infested brown trout (the less suitable host) groups, compared to the other test groups. Genetic assignment was used to identify offspring from individual mother mussels. We found that glochidia from individual mothers can infest both the salmonid hosts; however, some mothers displayed a bias towards either salmon or trout. We believe that the differences in host-dependent virulence and the host bias displayed by individual mothers were a result of genotype × genotype interactions between the glochidia and their hosts, indicating that there is an underlying genetic component for this parasite-host interaction

MarMa_dataset

Size and survival data collected from juvenile mussels (Margaritifera margaritifera) from 8 river populations from southern Norway