Host‐specificity of the endangered thick‐shelled river mussel (Unio crassus,Philipsson 1788) and implications for conservation

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Glochidial infestation by the endangered mollusc Unio crassus in rivers of north‐eastern France: Phoxinus phoxinus and Cottus gobio as primary fish hosts

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

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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.

     

Local adaptation studies and conservation: Parasite–host interactions between the endangered freshwater mussel Unio crassus and its host fish

1. Parasite–host interactions can involve strong reciprocal selection pressure, and may lead to locally adapted specializations. The highly threatened unionoid mussels are temporary parasites on fish, but local adaptation has not yet been investigated for many species.
2. Patterns of local adaptation of one of Europe's most threatened unionoids, the thick‐shelled river mussel (Unio crassus) were investigated. Eurasian minnows (Phoxinus phoxinus) from two rivers (separate drainage areas) were cross‐infested in the laboratory with sympatric and allopatric mussel larvae, while bullheads (Cottus gobio), inhabiting only one of the rivers, were infested with sympatric or allopatric mussel larvae. Larval encystment, juvenile mussel excystment and survival were measured.
3. For one river, but not the other, juvenile excystment from P. phoxinus was highest when infested with sympatric mussels. The opposite pattern was found for C. gobio in this river, where juvenile excystment and post‐parasitic juvenile survival from allopatric C. gobio were highest. The results thus cannot confirm local adaptation of U. crassus to P. phoxinus in the study rivers, as excystment was not consistently higher in all sympatric mussel–host combinations, whereas there were potential maladaptive signs of U. crassus in relation to C. gobio. There was no loss of encysted larvae 3 days after infestation until juvenile excystment. Most juveniles were excysted between 17 and 29 days after infestation, and the numbers of excysted juveniles increased with fish size.
4. The results have implications for parasite–host ecology and conservation management with regard to unionoid propagation and re‐introduction. This includes the need to (1) test suitability and adaptation patterns between U. crassus and multiple host fish species, (2) evaluate the suitability of certain unionoids and host fish strains after more than 3 days, and (3) determine whether large fish produce more juvenile mussels than smaller fish.

     

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

1. The effects of invasive alien species (IAS) on host–affiliate relationships are often subtle and remain unnoticed or insufficiently quantified. The global decline of freshwater unionid mussel species has been attributed to many causes, but little is known about the interactions of IAS, with their complex life cycle, which includes an obligatory parasitic stage (the glochidium) that develops on fishes.
2. The capacity of a European freshwater mussel, Anodonta anatina, to develop on its widespread fish host, Squalius cephalus was tested experimentally, after previous infestations by the IAS, Sinanodonta (Anodonta) woodiana. The initial attachment of glochidia, the length of the parasitic period, and the metamorphosis success rate of A. anatina glochidia were compared among treatments of different priming infestation intensities.
3. The metamorphosis success rate of the native A. anatina glochidia was strongly reduced (Wilcoxon Signed‐Rank Test, P < 0.001) and declined by 42.1 and 45.4% on fish hosts that were previously exposed to S. woodiana by single and multiple priming infestations, respectively, in comparison with the control group. Such cross‐resistance is expected to decrease significantly the quality of the host resources available to native mussels.
4. This study provides the first evidence of the host‐mediated adverse impact of invasive S. woodiana on native mussel species. These results also highlight the importance of potential competition for hosts between threatened groups of affiliate species and their invasive counterparts, which should be reflected in conservation strategies.

     

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

1. The giant freshwater pearl mussel Margaritifera auricularia (GFPM) is one of the most endangered bivalve species in the world. Originally occurring in many European rivers, the GFPM is a relict now restricted to a few ageing populations in France and Spain in which natural reproduction is almost absent.
2. Like most unionoid mussels, the GFPM needs host fish for the development of their parasitic larvae (glochidia). The European sturgeon (Acipenser sturio), the only known native host fish of the GFPM in France, is essentially extinct. Therefore, the aim of this study was to identify other hosts that could be responsible for the few cases of recent recruitment.
3. Natural infestation of wild fishes in three French rivers was assessed to identify potential hosts of M. auricularia, while artificial infestation experiments were conducted on the sea lamprey (Petromyzon marinus) and the wels catfish (Silurus glanis) to determine their compatibility as hosts.
4. Among the 29 fish species assessed for natural infestation, only the three‐spined stickleback (Gasterosteus aculeatus) and the European eel (Anguilla anguilla) carried M. auricularia glochidia. In the artificial infestation experiments, living juvenile mussels were collected from both P. marinus and S. glanis. The number of juveniles collected from a single P. marinus specimen (13,827) suggests that this species is a highly efficient host. As with previously known hosts, newly identified ones also appear to have a relationship with marine environments.
5. The present findings suggest that P. marinus has played a key role in preventing the total extinction of M. auricularia in France, and indicate the potential use of P. marinus in conservation strategies aimed at reintroducing or stabilizing populations of this rare mollusc.

     

Interspecific comparison of experimental and natural routes of Lepeophtheirus salmonis and Caligus elongatus challenge and consequences for distribution of chalimus on salmonids and therapeutant screening

Although the gills have been reported as a site for settlement by sea lice attached stages in experimental challenges, the prevalence and abundance of infection on gills have not been reported in farmed fish and have been reported only rarely in wild salmonids. Disproportionate attachment to the gills may be significant in evaluation of new therapeutants and this study asks whether the efficacy data from studies of therapeutants based on experimental challenge can be extrapolated to the fish farm arena. The distribution of chalimus on gills, body and fins of farmed first sea year Atlantic salmon were examined in two Scottish sea lochs, each on two occasions (30 fish on each sampling date), fish from one farm with infection with Lepeophtheirus salmonis only and the other farm with exclusively Caligus elongatus. The dorsal fin was the primary attachment site of L. salmonis (50% and 33% in two samples respectively) with 29% and 32% on other fins and 20% and 29% on the body and head. Only one of 56 chalimus (1.8%) and four of 75 chalimus (5.3%) were attached to the gills. In contrast, the chalimus distribution of C. elongatus was predominantly on fins other than the dorsal, including the tail, 74% and 71%, on two sampling occasions, respectively, with only 4.2% and 3.6% of chalimus located on the dorsal fin. The pectoral fins were the most common location with 32%, followed by the tail 23%, pelvic fins 14% and only 3% on the anal fin. None of 287 and 111 chalimus in two samples, respectively, of C. elongatus was attached to the gills. The low abundance of lice on the gills indicated that non‐destructive sampling methods adequately represented lice infection. In three experimental challenges with L. salmonis, the gills were a major attachment location with 19.9–36.3% of chalimus, 9.9–26.9% on the body, 22–27% on the dorsal fin and 19–23% on the other fins. These differences with natural challenge in L. salmonis reported here and also in the literature suggest that the importance of the gills for chalimus location in the experimental model is atypical and an artefact of reduced host swimming speed in tanks that permits copepodids to attach to the gills. In natural infection, the flow over the gills is high and reduced flow is required for copepodid settlement. Greatest reductions (96%) in chalimus bath treated with cypermethrin occurred on the gills with no significant reductions in those located on the dorsal and other fins. It is possible that the efficacy of therapeutants may be higher in chalimus attached to the gills because of the higher concentration encountered of bath therapeutant and extrapolation of efficacy to farms may be misleading and progression to field testing is essential.     

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

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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.     

Influence of the excystment time on the breeding success of juvenile freshwater pearl mussels (Margaritifera margaritifera)

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Electrofishing as a new method to search for unknown populations of the endangered freshwater pearl mussel Margaritifera margaritifera

1. The freshwater pearl mussel Margaritifera margaritifera is threatened throughout its Holarctic range, but the occurrence of this species is insufficiently mapped. For the conservation of M. margaritifera, it is important to identify populations more comprehensively. 2. Traditionally mussels have been searched for visually using techniques such as diving and aquascope, both of which are potentially time‐consuming and demanding survey methods. 3. In this study, a new search method is presented. As glochidia of M. margaritifera are larval parasites on the gills of salmonid fish, electrofishing and non‐destructive examination of salmonids with the naked eye may reveal the presence of glochidia and therefore the occurrence of M. margaritifera in watercourses. This method was tested in both the field and laboratory in northern Finland. 4. In summer, when M. margaritifera glochidia were large, the status of salmonids being infected or uninfected by M. margaritifera was correctly identified with the naked eye with 62, 80, 88 and 93% accuracy in four streams sampled, 96% accuracy in the laboratory, and 100% accuracy in all cases when at least 20 glochidia per fish were present. Intensity of infection was also assessed successfully; a specifically tailored, qualitative abundance score correlated significantly with the real number of glochidia. However, during autumn with small glochidia freshly attached to fish, glochidia infection could be observed only under microscopic examination. 5. When the method was used in 40 previously incompletely surveyed tributaries, three M. margaritifera populations were found. The infection in salmonids was observed always with the naked eye, being subsequently confirmed microscopically. The existence of adult mussels in two of these rivers was also confirmed. 6. The results indicate that electrofishing and a relatively quick naked‐eye check of salmonids provides a new, non‐destructive, and potentially cost‐effective way to search for new, previously unrecorded M. margaritifera populations. Copyright © 2016 John Wiley & Sons, Ltd.     

Evaluating the upper thermal limits of glochidia for selected freshwater mussel species (Bivalvia: Unionidae) in central and east Texas,and the implications for their conservation

1. Understanding the temperature tolerances of organisms is critical because the thermal regimes of freshwater ecosystems are changing globally. Native freshwater mussels are sensitive to increasing water temperatures because of their physiology and unique life history. Detailed knowledge on lethal temperatures for mussels has been limited to less than 5% of the species known to occur in North America, and little is known about the thermal tolerances of mussel species from rivers within the south‐western USA.
2. To determine the effects of elevated water temperature on mussels, the upper thermal tolerances of larvae (glochidia) for the following species across four basins in Texas (Neches, Guadalupe, San Antonio, and Colorado) were tested: Amblema plicata, Cyclonaias necki, Fusconaia mitchelli, Lampsilis bracteata, Lampsilis hydiana, Lampsilis satura, Lampsilis teres, and Obovaria arkansasensis.
3. Glochidia were acclimated to 27°C across a range of experimental temperatures (30–39°C) in 24‐h standard acute laboratory tests. The median lethal temperature (LT50) among glochidia averaged 32.4°C and ranged from 26.9 to 36.4°C.
4. Thermal tolerances differed significantly among and within species, and by season. Comparing these results with current water temperatures in central and east Texas indicated that populations of the focal species studied are at risk from rising environmental temperatures and, as a consequence, their long‐term viability will be challenging in future years.

     

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

1. Understanding the multiple agents of decline is important for the conservation of globally threatened Unionida (Class Bivalvia), but threats from non‐native species have received limited attention. To address this gap, a global meta‐analysis was conducted aimed at identifying known interactions and mechanisms of impact and informing potential effect pathways for the New Zealand unionid fauna.
2. The main non‐native groups identified as interacting with unionids were fish (38% of published studies), macrophytes (33%), and vertebrate predators (30%), with ~70% of interactions leading to adverse impacts on mussels. Most studies used field surveys (~50%) and were conducted in rivers (~50%).
3. Impacts occurred across the unionid life cycle (adult, glochidia, host, and juvenile), and primarily affected processes that determine the transitions between life‐cycle stages (fertilization, infestation, settlement, and maturation). The impacts of non‐native macrophytes and fish were predicted to be greater for transitional stages than the impact of vertebrate predators, which mostly affected adult mussels.
4. New Zealand Unionida are most likely to be affected by interactions with non‐native species in lowland lakes and waterways, where connectivity for diadromous native fish hosts and high bioinvasion potential intersect.

     

Heavy loads of parasitic freshwater pearl mussel (Margaritifera margaritifera L.) larvae impair foraging,activity and dominance performance in juvenile brown trout (Salmo trutta L.)

The life cycle of the endangered freshwater pearl mussel (Margaritifera margaritifera) includes a parasitic larval phase (glochidia) on the gills of a salmonid host. Glochidia encystment has been shown to affect both swimming ability and prey capture success of brown trout (Salmo trutta), which suggests possible fitness consequences for host fish. To further investigate the relationship between glochidia encystment and behavioural parameters in brown trout, pairs (n = 14) of wild‐caught trout (infested vs. uninfested) were allowed to drift feed in large stream aquaria and foraging success, activity, agonistic behaviour and fish coloration were observed. No differences were found between infested and uninfested fish except for in coloration, where infested fish were significantly darker than uninfested fish. Glochidia load per fish varied from one to several hundred glochidia, however, and high loads had significant effects on foraging, activity and behaviour. Trout with high glochidia loads captured less prey, were less active and showed more subordinate behaviour than did fish with lower loads. Heavy glochidia loads therefore may negatively influence host fitness due to reduced competitive ability. These findings have implications not only for management of mussel populations in the streams, but also for captive breeding programmes which perhaps should avoid high infestation rates. Thus, low levels of infestation on host fish which do not affect trout behaviour but maintains mussel populations may be optimal in these cases.     

Fish hosts of the freshwater mussel Unio foucauldianus Pallary, 1936

1. The life cycle of Unio foucauldianus Pallary, 1936, a critically endangered freshwater mussel species (Bivalvia: Unionida), includes a parasitic phase using fish as hosts. Therefore, to develop more efficient conservation strategies it is essential to know which are the suitable fish hosts of U. foucauldianus.
2. In this study, two approaches were used to assess the fish hosts of U. foucauldianus: the determination of infestation rates of fishes under natural conditions through monthly sampling (from January to June) in the Laabid River (Oum Rbia basin) and the N'Fis River (Tensift basin), and artificial infestation in laboratory trials using fish species from both rivers.
3. The natural infestation of fish was detected from February to June, with a peak in May. Fully metamorphosed juveniles were only detected in native fish species, i.e. Luciobarbus ksibi (Boulenger, 1905), Carasobarbus fritschii (Günther, 1874), Luciobarbus zayanensis Doadrio, Casal‐lopez & Yahyaoui, 2016, Labeobarbus maroccanus (Günther, 1874), and Luciobarbus magniatlantis (Pellegrin, 1919). The two non‐native fish species used do not function as effective hosts.
4. Given the increasing human pressure on native fish species in the Mediterranean biodiversity hotspot, including the increased number of non‐native fish introductions, urgent conservation measures are discussed for this and other freshwater mussel 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.

     

Early stages of Margaritifera margaritifera glochidiosis in Atlantic salmon: Morphopathological characterization

Freshwater mussels of the order Unionida encyst into the fish mucosa to metamorphose and complete their life cycle, causing a parasitic disease known as glochidiosis. This parasitic stage represents a bottleneck for the survival of naiads, particularly for critically endangered species as Margaritifera margaritifera; however, little is known about the events occurring during this critical stage. Therefore, this study aimed to histologically characterize the development of M. margaritifera glochidiosis in Atlantic salmon to get insight into the pathogenesis of this interaction. Fish exposed to glochidia were sampled during the first 44 days post-exposure, and organs were observed by stereomicroscopy and light microscopy. Glochidia attached to the gills by pinching the lamellar epithelium, whereupon an acute proliferative branchitis engulfed most of the larvae. However, during the first 14 days, a severe detachment of unviable glochidia occurred, associated with the presence of pleomorphic inflammatory infiltrate and epithelial degeneration. In the cases where larvae remained attached, a chronification of the lesions with none to scarce inflammation was observed. These results provide key information to better understand the complex host–parasite interaction during the early stages of glochidiosis and provide valuable information to optimize artificial rearing of naiads in conservation of threatened freshwater mussel populations.     

An investigation of salmonid host utilization by the endangered freshwater pearl mussel (Margaritifera margaritifera) in north‐west Scotland

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Geographic variation in host fish use and larval metamorphosis for the endangered dwarf wedgemussel

1. Host fishes play a crucial role in survival and dispersal of freshwater mussels (Unionoida), particularly rare unionids at conservation risk. Intraspecific variation in host use is not well understood for many mussels, including the endangered dwarf wedgemussel (Alasmidonta heterodon) in the USA.
2. Host suitability of 33 fish species for dwarf wedgemussel glochidia (larvae) from the Delaware and Connecticut river basins was tested in laboratory experiments over 9 years. Relative suitability of three different populations of a single host fish, the tessellated darter (Etheostoma olmstedi), from locations in the Connecticut, Delaware, and Susquehanna river basins, was also tested.
3. Connecticut River basin A. heterodon metamorphosed into juvenile mussels on tessellated darter, slimy sculpin (Cottus cognatus), and Atlantic salmon (Salmo salar) parr. Delaware River basin mussels metamorphosed using these three species, as well as brown trout (Salmo trutta), banded killifish (Fundulus diaphanus), mottled sculpin (Cottus bairdii), striped bass (Morone saxatilis), and shield darter (Percina peltata). Atlantic salmon, striped bass, and sculpins were highly effective hosts, frequently generating 5+ juveniles per fish (JPF) and metamorphosis success (MS; proportion of attaching larvae that successfully metamorphose) ≥ 0.4, and producing juveniles in repeated trials.
4. In experiments on tessellated darters, mean JPF and MS values decreased as isolation between the mussel source (Connecticut River) and each fish source increased; mean JPF = 10.45, 6.85, 4.14, and mean MS = 0.50, 0.41, and 0.34 in Connecticut, Delaware, and Susquehanna river darters, respectively. Host suitability of individual darters was highly variable (JPF = 2–11; MS = 0.20–1.0).
5. The results show that mussel–host fish compatibility in A. heterodon differs among Atlantic coastal rivers, and suggest that hosts including anadromous Atlantic salmon and striped bass may help sustain A. heterodon in parts of its range. Continued examination of host use variation, migratory host roles, and mussel–fish interactions in the wild is critical in conservation of A. heterodon and other vulnerable mussel species.