Demonstrating the practical impact of studies on biotic interactions and adaptation of a threatened unionoid mussel (Margaritifera margaritifera) to its host fish (Salmo trutta)

1. To understand the ecological factors behind the decline of functionally important threatened species with complex life cycles, many different life‐cycle stages need to be investigated. The highly threatened unionoid freshwater mussels, with their complex life cycle, including a parasitic stage on host fish, often have a large influence on biodiversity and ecosystem functioning.
2. The overall aim of the present article is to summarize and discuss the impact of two articles published in Aquatic Conservation: Marine and Freshwater Ecosystems (AQC) on biotic interactions and adaptation of a threatened unionoid mussel (Margaritifera margaritifera) to its host fish (Salmo trutta).
3. The two AQC publications described research on the influence of population size and density of mussels and host fish, and host–parasite interactions between mussels and their host fish, on the recruitment of juvenile mussels.
4. The results from these publications filled gaps in knowledge and resulted in recommendations and incentives for conservation. The results and method development have been used in practical conservation work with threatened mussel species and have been implemented and cited in management handbooks. The outcome of the publications has been implemented in large conservation and restoration projects, and in several recent scientific publications.
5. Specifically, the results from one publication showed that ecological parameters such as mussel and host fish density and population size influenced recruitment of the threatened freshwater pearl mussel. The results from the second publication showed that understanding host–parasite interactions is important for comparing the suitability of host fish strains, and that host fish strains differ in their suitability for mussel infestations. In combination, the articles show that integrating ecological parameters of threatened mussels and their host fish with host–parasite interaction experiments can be an important influence on conservation recommendations, adaptive management and national management programmes for threatened species.

     

Suitability of different salmonid strains as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera L.)

• 1. The complex life cycle of endangered European freshwater pearl mussel Margaritifera margaritifera L. involves an obligatory parasitic phase on a host fish. Knowledge on the host–parasite interaction and on the suitability of different host fish species and strains is required both for the management of wild fish and mussel populations as well as for improving the efficiency of captive breeding methods.
• 2. In this study, the suitability of different salmonid strains for hosting glochidia was tested, including Danube salmon (Hucho hucho L.) and three brown trout (Salmo trutta L.) strains from inside and outside the freshwater pearl mussel distribution range. All brown trout strains as well as Danube salmon were successfully infected with freshwater pearl mussel glochidia and encystment of mussel larvae was detected.
• 3. One brown trout strain originating from the natural pearl mussel distribution range was identified as the most suitable host, revealing the highest fish‐weight‐normalized infection rates and highest glochidial growth rates, whereas endemic Danube salmon was least suitable. Under natural conditions, the role of Danube salmon may be attributed to the long‐distance dispersal of glochidia in the Danube system, whereas sedentary brown trout appear to be the most important hosts at a local scale.
• 4. Successful infection of suitable hosts and the maintenance of these host–parasite systems in calcareous water were demonstrated in this study. These results indicate that neither the infection process nor the encystment phase of freshwater pearl mussels is dependent on low lime concentrations.
• 5. The results of this study suggest that careful selection and management of appropriate host fish strains is mandatory for sustainable conservation management of freshwater pearl mussel populations. Copyright © 2010 John Wiley & Sons, Ltd.

     

Fish species composition and host fish density in streams of the thick‐shelled river mussel (Unio crassus) – implications for conservation

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Interactions between Unionida and non‐native species: A global meta‐analysis

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Effects of water temperature on the larval parasitic stage of the thick‐shelled river mussel (Unio crassus)

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Associations between stream hydrogeomorphology and co‐dependent mussel–fish assemblages: evidence from an Ohio,USA river system

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Influence of flow diversions on giant freshwater pearl mussel populations in the Ebro River,Spain

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Averting co-extinction: Successful mussel translocation rescues an endangered population of the European bitterling,Rhodeus amarus

1. Local extinctions break species interactions and have cascading effects throughout ecosystems; parasites are often severely affected. The European bitterling, Rhodeus amarus, is a cyprinid fish that parasitizes unionid mussels by laying eggs into the mussel gill cavity, where embryos develop and emerge as active juveniles; this relationship is obligatory for the bitterling.
2. This article describes a field experiment aimed at averting the secondary extinction of the European bitterling after a complete die-off of a freshwater mussel community, as a result of habitat destruction.
3. Approximately 5,000 unionid mussels were reintroduced within the short time frame in which the remnant bitterling population was still present at the site. Mussel survival was high, and bitterling resumed reproduction, with vigorous courtship observed within 24 hours of mussel release. Recruitment was successful, as evidenced by increased occupancy, densities, and relative frequencies in the fish assemblage. The frequency of sub-adults and young-of-the-year changed from 0% before mussel reintroduction to 80% a year later, and 50% 2 years later, when young-of-the-year contributed to about half of the young fish. No bitterling were observed at two control sites where mussels were not reintroduced.
4. This study exemplifies how the timely restitution of affiliate species can avert co-extinction. It also shows how the conservation of the bitterling within its historical distribution range can serve mussel conservation, including species that although not legally protected, are important keystone species and ecosystem engineers, shaping the structure and function of a broad range of freshwater habitats.

     

Invasive Chinese pond mussel Sinanodonta woodiana threatens native mussel reproduction by inducing cross‐resistance of host fish

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Fish hosts of the freshwater mussel Unio foucauldianus Pallary, 1936

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From the lab to the river: Determination of ecological hosts of Anodonta anatina

1. Coextinction is the simplest form of secondary extinction and freshwater mussels (Bivalvia, Unionida) may be particularly prone to this phenomenon as their life cycle includes an obligatory parasitic larval stage on fish hosts.
2. The main aims of this study were to determine the possible ecological fish hosts of Anodonta anatina (Linnaeus, 1758) in several rivers of the Douro basin in northern Portugal and to assess possible spatial and temporal differences in glochidial (larval) loads. In order to achieve this, electrofishing was conducted from December to April, the fish fauna was characterized, and levels of infestation with A. anatina glochidia were determined.
3. Native cyprinid species, mainly Luciobarbus bocagei (Iberian barbel) and Squalius carolitertii (northern Iberian chub), together with the non‐native Lepomis gibbosus (pumpkinseed sunfish) and Alburnus alburnus (common bleak), were found to have the highest glochidial loads. Clear differences in infestation between rivers and throughout time were detected, with an infestation period from January to March, and with the Tâmega River having the highest prevalence.
4. Anodonta anatina is able to infest a variety of fish species, and this together with earlier studies showed that the metamorphosis into juveniles occurs mainly in native cyprinid species, although non‐native species like common bleak can also be considered suitable hosts. However, the larvae infesting other non‐native species, such as the pumpkinseed sunfish, do not metamorphose and can be considered ‘dead ends’.
5. Overall, the results reported here are important for the conservation of A. anatina (and other unionoid species) because several Iberian rivers (and worldwide) have been subjected to the extirpation of native fish species and the introduction of non‐native fish species. Therefore, careful assessments of fish communities should be conducted to assess possible negative interactions with freshwater mussels.

     

Conservation status assessment and a new method for establishing conservation priorities for freshwater mussels (Bivalvia: Unionida) in the middle and lower reaches of the Yangtze River drainage

1. The freshwater mussel (Unionida) fauna of the Yangtze River is among the most diverse on Earth. In recent decades, human activities have caused habitat degradation in the river, and previous studies estimated that up to 80% of the mussel species in the Yangtze River are Threatened or Near Threatened with extinction. However, a comprehensive and systematic evaluation of the conservation status of this fauna has yet to be completed.
2. This study evaluated the conservation status of the 69 recognized freshwater mussel species in the middle and lower reaches of the Yangtze River, using the criteria published by the International Union for Conservation of Nature (IUCN). A new method for prioritizing species for conservation was then developed and applied termed Quantitative Assessment of Species for Conservation Prioritization (QASCP), which prioritizes species according to quantifiable data on their distribution and population status, life history, and recovery importance and potential.
3. IUCN assessments showed that 35 (51%) species in the study region are Threatened or Near Threatened (11 Endangered, 20 Vulnerable, 4 Near Threatened). In addition, 16 species (23%) could not be assessed owing to data deficiency. Key threats to the freshwater mussel biodiversity of the Yangtze River include pollution, habitat loss and fragmentation, loss of access to host fish, and overharvesting of mussels and their host fish. The genera Aculamprotula, Gibbosula, Lamprotula, Pseudodon, Ptychorhynchus, and Solenaia were identified as particularly threatened.
4. Data availability allowed QASCP assessment of 44 species. Only Solenaia carinata, regionally Endangered under IUCN criteria, achieved the highest QASCP rank, i.e. First Priority. The five species assessed as Second Priority were considered either regionally Endangered (one), Vulnerable (three), or Data Deficient (one) under IUCN criteria. The 23 Third Priority species were assessed as regionally Endangered (two), Vulnerable (15), Near Threatened (two), or Least Concern (four).

     

A comparison of freshwater mussel assemblages along a land‐use gradient in Minnesota

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Population consequences of behaviour in the European bitterling (Rhodeus sericeus Cyprinidae)

Abstract –  The European bitterling is a freshwater fish with an unusual spawning symbiosis with freshwater mussels. Female bitterling possess long ovipositors that they use to place their eggs onto the gills of a mussel. Males fertilise the eggs by releasing sperm into the inhalant siphon of the mussel. The embryos develop inside the mussel for approximately a month, eventually leaving the mussel as actively swimming larvae. Because they use a discrete spawning site that can be readily manipulated they represent an ideal model for linking reproductive decisions with population dynamics. Bitterling have been used in field and large-scale pool experiments, in combination with modelling and population and genetic studies to investigate the population consequences of behaviour. Here we show how male mating tactics, female mate and oviposition decisions, and aggressive interference competition among juveniles, may have significant impacts on bitterling population size and population genetics.     

Freshwater mussels in Mediterranean-climate regions: Species richness,conservation status,threats, and Conservation Actions Needed

1. The five global Mediterranean-climate regions are experiencing alarming rates of freshwater biodiversity loss. Although freshwater mussels are recognized as important functional components in aquatic ecosystems, and are among the most threatened faunal groups globally, there has been no synthesis of the plight of this group within these regions.
2. Data from the International Union for Conservation of Nature (IUCN) Red List were reviewed to compare the conservation status, threats, and conservation actions needed for freshwater mussel species occurring in Mediterranean-climate regions (med-mussels) with those of other freshwater mussel species globally. The first comprehensive catalogue of med-mussel species was compiled using existing taxonomic literature.
3. There are 41 med-mussel species, 30 of which occur in the Mediterranean basin. Many regions have just a single species, and regions where multiple species occur generally only have between one and four species per river basin. Med-mussel species are almost twice as likely to be ‘Imperilled’, are affected by 2.4 times more threats, and require 3.5 times more conservation actions than non-med mussels. In many cases, the exact threats have not been identified.
4. In combination with low species richness, this level of imperilment means that Mediterranean-climate regions are at risk of losing the benefits that mussels provide to broader ecosystem functioning. The conservation of med-mussels can be improved by increasing our knowledge of species distributions, including the identification of cryptic species and significant management units, through population genetic work. In addition, recognizing the potential of ‘novel’ habitats and refuge areas could augment the management of this important functional group.

     

Prediction of potential freshwater pearl mussel habitat aids in discovery of a large population of Margaritifera laevis in Iturup Island,Russia

1. Freshwater pearl mussels (family Margaritiferidae) are sensitive to human impact and environmental changes. Large declines in their abundance have prompted studies of distribution and estimations of population densities.
2. Iturup Island, a part of Kuril Islands, Russia, is considered to be within the distribution area of freshwater pearl mussels, but this information is based on only two specimens collected several decades ago. Detailed survey of the island is challenging as most of its territory is nearly impassable.
3. A preliminary analysis of island rivers was carried out prior to the surveys to discover potential freshwater pearl mussel habitats. Based on previous experience from European Russia, freshwater pearl mussel habitat was expected to occur in rivers flowing out of lowland lakes.
4. Live individuals of Margaritifera laevis were found during surveys in one river together with the unionid Beringiana beringiana, which were also found in two other rivers where the predicted habitat occurred. Based on prediction and surveys, the occurrence of freshwater pearl mussels in other rivers of Iturup Island is unlikely.
5. Pearl mussels were concentrated in a small section of the Zmeika River with a population of about 100,000 mussels. Present threats to the population include overharvest of host fish masou salmon (Oncorhynchus masou).
6. Surveys using similar methods can help to reveal unknown freshwater mussel populations on other Kuril Islands and on the mainland.

     

An unexpected host for the endangered giant freshwater pearl mussel Margaritifera auricularia (Spengler, 1793) as a conservation tool

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Recruitment of the threatened mussel Margaritifera margaritifera in relation to mussel population size,mussel density and host density

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Fish–habitat relationships and fish conservation in small coastal streams in southern Spain

• 1. Studies dealing with the fish fauna of coastal streams are scarce in the scientific literature, particularly those from Mediterranean climates. Owing to their small size, these systems suffer extreme seasonal fluctuations, following the typical Mediterranean flood–drought cycle and leading to a high risk of extinction to freshwater fish.
• 2. This work analyses fish distribution in 14 stream stretches belonging to eight basins in the northern sector of the Strait of Gibraltar (southern Spain). Fish–habitat relationships were studied through multivariate ordination techniques at two scales: basin and stretch.
• 3. A principal components analysis clearly discriminated larger and more sinuous basins from smaller and steeper ones. This ordination was related to the non‐migratory freshwater fish species richness and to the total number of fish species present in the middle reaches of each basin.
• 4. The main sources of variation in community composition and habitat characteristics in the different stretches were related to a clear upstream–downstream gradient, along which total species richness increased.
• 5. These small coastal basins are inhabited by two highly endangered species, Andalusian toothcarp (Aphanius baeticus) and Iberian chub (Squalius pyrenaicus), and have similar or higher overall freshwater species richness than larger adjacent basins. The near absences of flow regulation and introduced species make these streams one of the few types of Iberian aquatic system where unaltered fish–habitat relationships can be studied.

Copyright © 2005 John Wiley & Sons, Ltd.     

The status of host fish populations and fish species richness in European freshwater pearl mussel (Margaritifera margaritifera) streams

• 1. The status of host fish populations and fish species richness was investigated at 36 sites of 20 extant freshwater pearl mussel populations, including the drainages of the Elbe, Danube, Rhine, Weser, Aulne, Kemijoki and Tuuloma in Germany, the Czech Republic, France and Finland, by carrying out comparative electrofishings.
• 2. Brown trout (Salmo trutta f. fario) were found to be the available host fish for pearl mussels in all except one of the streams investigated with mean densities of 2861 ha^?1 (range 0–8710 ha^?1) and a mean biomass of 119 kg ha^?1 (range 0–478 kg ha^?1). Streams that had been frequently stocked with brown trout had higher trout biomass and densities of host fish than natural populations, but trout stocking had no positive effect in two of the streams investigated.
• 3. Fish species richness ranged from 2 to 16 species per stream and showed a negative correlation with host fish biomass and host fish densities. Undisturbed oligotrophic pearl mussel headwater streams usually only yielded a low number of fish species. Habitat degradation can reduce competitiveness of specialized trout and result in an increased abundance of ubiquitous or atypical species.
• 4. A link between the lack of juvenile pearl mussels and a lack of suitable host fish was only rarely observed. Functional pearl mussel populations with relatively high numbers of juveniles had significantly lower densities and biomass of host fish than pearl mussel populations without recent recruitment.
• 5. This study suggests that 0+ host fish are not necessarily required to sustain functional pearl mussel populations. Low densities of host fish can be compensated by the higher glochidia carrying capacity of older host fish with limited previous contact with pearl mussel glochidia, by the long reproductive period of mussels, and by low mortality rates of juvenile mussels during their post‐parasitic phase.

Copyright © 2005 John Wiley & Sons, Ltd.