Culturing freshwater pearl mussel Margaritifera margaritifera: a breakthrough in the conservation of an endangered species

• 1. The freshwater pearl mussel Margaritifera margaritifera L. is globally endangered and is threatened by commercial exploitation, pollution and habitat loss throughout its range. Captive breeding would be a valuable tool in enhancing the status of M. margaritifera in the UK.
• 2. We have developed a semi‐natural system for successfully infecting juvenile brown trout with glochidial M. margaritifera, and culturing juvenile mussels in experimental tanks where glochidial M. margaritifera can excyst from fish gills and settle into sediment.
• 3. Infected fish had less than 1% mortality. Levels of infection varied among fish. Two yearly cohorts of juvenile M. margaritifera were identified from samples of sediment taken from each experimental tank. Individuals range in size from 1.4 mm (2000 cohort) to >3 mm in length (1999 cohort).
• 4. The number of juvenile M. margaritifera present in the two experimental tanks are estimated to be between 3600 (tank A) and 0 (tank B) for the putative 1999 cohort and between 6000 (tank A) and 13 000 (tank B) for the putative 2000 cohort.
• 5. This pioneering method for large‐scale cultivation of juvenile M. margaritifera is intermediate between the release of infected fish into rivers and the intensive cultivation systems developed in continental Europe and the USA for other species of unionid. This is the first time that large numbers of M. margaritifera have been cultured and represents a significant breakthrough in the conservation of this globally endangered Red Data List species. The method is straightforward and is most cost‐effective when undertaken alongside established hatchery processes.

Copyright © 2006 John Wiley & Sons, Ltd.     

A protocol for stocking hatchery reared freshwater pearl mussel Margaritifera margaritifera

• 1. Freshwater pearl mussel (Margaritifera margaritifera L.) populations are under serious threat of extinction throughout their geographical range and only a few remnant populations are recruiting to adulthood. Consequently, M. margaritifera is classified as endangered on the International Union for Conservation of Nature Red List.
• 2. Several institutions across many countries have set up Ark sites at hatcheries to culture and rear young M. margaritifera from population remnants, with the intention of stocking these juveniles into rivers. The release location must fulfill the habitat requirements for the full life‐cycle of the species, so they can contribute to the next generation and thus the long‐term recovery of the species. However, little research or advice exists about how to decide if river environments are suitable for stocking.
• 3. A protocol is presented for determining whether a M. margaritifera population will benefit from stocking hatchery reared juveniles and how to identify suitable areas. Stocking locations are considered from catchment scale to microscale using water quality (reach), macrohabitat (site) and microhabitat, including physicochemical properties of the substratum (spots).
• 4. A case study of the River Esk in north‐east England, is incorporated to exemplify the myriad of considerations surrounding attempts to conserve M. margaritifera, and describes how implementation of the protocol can structure and assist stocking programmes. Copyright © 2010 John Wiley & Sons, Ltd.

     

Conservation status of two endangered freshwater mussel species in Bavaria,Germany: Habitat quality,threats, and implications for conservation management

1. The freshwater pearl mussel (Margaritifera margaritifera) and the thick‐shelled river mussel (Unio crassus) are relatively widespread across Europe, but are strongly declining and are now protected by the European Habitats Directive. In the course of this study, 20 pearl mussel and 14 thick‐shelled river mussel streams in Bavaria, Germany, were investigated.
2. The mussel populations were mapped to determine population size and age structure. For the assessment of habitat quality, host fish abundance and physicochemical parameters were investigated, e.g. substratum quality, water chemistry, redox potential, and turbidity. Furthermore, potential risks for the populations such as predation or river maintenance were also recorded and assessed.
3. The average population size and recruitment rates of M. margaritifera populations were lower than in U. crassus populations, with 3517 (2.2% juveniles) compared with 5566 (41.4% juveniles) individuals, respectively. On average, 22.3% of particles were smaller than 0.85 mm in diameter at M. margaritifera sites, whereas the mean proportion of fine particles at U. crassus sites was twice as high, at 41.3%. Other parameters such as redox potential or electric conductivity also indicated more favourable habitat conditions in M. margaritifera streams. Unio crassus seems to be less vulnerable to adverse substratum texture and increased nutrient levels than M. margaritifera.
4. The main threats for U. crassus were physical habitat destruction, predation by muskrat, or a lack of host fish, whereas M. margaritifera mainly suffered from siltation leading to a lack of oxygen supply to the interstitial zone, affecting recruitment. Consequently, conservation strategies need to be species‐specific and address stream‐specific reasons for decline. As a basis, accurate and comparable monitoring data are necessary, which implies the standardization of monitoring protocols.

     

A spatially explicit approach to prioritize protection areas for endangered freshwater mussels

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The status of the freshwater pearl mussel Margaritifera margaritifera Linn. in Scotland

1. One hundred and sixty rivers in Scotland with historical records of freshwater pearl mussel Margaritifera margaritifera were surveyed between 1996 and 1999 for the presence of the species. 2. M. margaritifera populations were classed as either ‘extinct’ (no mussels remaining), ‘not currently viable’ (ranging from only dead shells present to no juveniles present, regardless of the number of adults found), or ‘functional’ (at least one juvenile was found, regardless of the overall numbers of adults present). 3. M. margaritifera populations could be classed as ‘functional’ in only 52 rivers (34% of total surveyed) and in only 17 of these were juveniles below 20 mm (5 yrs old) present. Furthermore, in only 10 of these functional rivers were mussels also still considered either to be common or abundant and these included both large easterly‐flowing rivers and small western rivers and streams. 4. In approximately two‐thirds (101) of the 155 rivers occupied 100 years ago, M. margaritifera is now extinct or is about to become extinct. Furthermore, analysis indicates that the rate of mussel population extinction has accelerated since 1970, with a recent average of two mussel river extinctions per year. 5. The predominant threat to the mussel populations has undoubtedly been pearl fishing. This has been occurring at every river, even in the most remote northwest areas, where most of the ‘functional’ populations remain. Recent legislation has provided full protection to M. margaritifera, so that all pearl harvesting is now illegal. 6. Locally, river engineering and host salmonid stock decline poses a serious threat and eutrophication has already eliminated populations in southern and eastern Scotland. 7. In every part of its global range, M. margaritifera has declined substantially and is now either threatened with extinction or is highly vulnerable. Based on recent estimates from across the species range, it appears that Scotland now probably holds at least half of the world's remaining functional M. margaritifera populations. Copyright © 2000 John Wiley & Sons, Ltd.     

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.     

Applying morphometrics to choose optimal captive brood stock for an endangered species: a case study using the freshwater pearl mussel,Margaritifera margaritifera (L.)

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Dead or alive — Old empty shells do not prompt false-positive results in environmental DNA surveys targeting the freshwater pearl mussel (Margaritifera margaritifera L.)

1. Environmental DNA (eDNA) from water samples is increasingly used to detect the presence and distribution of species in aquatic ecosystems. However, before implementing eDNA in monitoring programmes, various species-specific sampling or analytical issues remain to be resolved in order to minimize frequencies of false-positive and -negative results. For example, empty shells from freshwater pearl mussels (Margaritifera margaritifera) contain extractable DNA (chemical extraction from ground-up shells) suggesting a risk of false-positive samples at stream sites with extinct populations but with empty shell material remaining.
2. The aim of this study was to investigate whether empty and naturally degrading shells from M. margaritifera can cause false-positive eDNA signals in water samples.
3. Water samples were collected from outdoor stream channels (in Lemming, Denmark) with living freshwater pearl mussels or empty shell material (density ~10 individuals m⁻²) during a 3-week experimental period. Living freshwater pearl mussels were collected from Hemgravs stream in Sweden and transported to Denmark according to permissions granted by the Swedish and Danish authorities.
4. All water samples from stream channels containing empty shells were negative for eDNA indicating that eDNA traces in stream water are most likely to originate from living individuals located upstream of the sampling site. Water samples collected from stream channels containing living individuals of M. margaritifera were consistently positive for eDNA except for one sample (interpreted as a false negative).
5. The study shows that positive eDNA signals for freshwater pearl mussels most likely reflect the presence of living individuals. Consequently, we suggest that eDNA should be used to locate remaining population fragments of M. margaritifera in deep and turbulent streams, providing a platform for faster and more efficient decision making when launching investigative and mitigation initiatives.

     

Environmental DNA as a monitoring tool for the endangered freshwater pearl mussel (Margaritifera margaritifera L.): a substitute for classical monitoring approaches?

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Effects of aquatic weed removal on freshwater pearl mussels and juvenile salmonids in the River Spey,Scotland

• 1. Experiments were carried out in the River Spey, Scotland to determine the effects of aquatic weed (Ranunculus spp.) removal on populations of freshwater pearl mussels (Margaritifera margaritifera) and juvenile salmonids (Salmo salar, Salmo trutta) and their river‐bed habitats.
• 2. Physical removal of Ranunculus had no significant impact either on pearl mussels or on salmon and trout fry.
• 3. Regrowth of Ranunculus post‐removal was negligible for one year, indicating that hand‐removal may be an effective control measure.
• 4. Ranunculus roots appear to facilitate substantial depositions of fine sand that are detrimental both to pearl mussels and salmonid fry.
• 5. The rapid spread of invasive Ranunculus is a potential threat to the conservation status of M. margaritifera in the River Spey.

Copyright © 2007 John Wiley & Sons, Ltd.     

Genetic structure of Irish freshwater pearl mussels (Margaritifera margaritifera and Margaritifera durrovensis): Validity of subspecies,roles of host fish,and conservation implications

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The north‐west of the Iberian Peninsula is crucial for conservation of Margaritifera margaritifera (L.) in Europe

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

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Characterization of freshwater pearl mussel (Margaritifera margaritifera) riverine habitat using River Habitat Survey data

• 1. The feasibility of using River Habitat Survey (RHS) data to describe freshwater pearl mussel (Margaritifera margaritifera) macrohabitat in the River Spey, north‐east Scotland, was investigated.
• 2. Mussels were found to be positively associated with a number of RHS variables. These included: boulder/cobble river bed substrates, broken/unbroken standing waves (channel flow types), aquatic liverworts/mosses/lichens and broadleaf/mixed woodland/bankside tree cover. Negative associations with gravel‐pebble/silt substrates and emergent reeds/sedges/herbs were also found.
• 3. Two binary logistic regression models, based on seven and four variables, respectively, were constructed in order to predict the presence/absence of mussels at any given site. Predictive success rates of 83% and 78% were achieved.
• 4. Another binary logistic regression model, based on four variables, was constructed in order to predict the occurrence of ‘optimal’ M. margaritifera habitat (overall mussel densities ≥ 1 m^?2). A predictive success rate of 83% was achieved.
• 5. The results indicate two potentially important applications of RHS for the conservation management of M. margaritifera: (1) for monitoring the effects of physical changes on extant mussel beds (and predicting their effects on mussel populations), and (2) for determining the habitat suitability of historically occupied sites for re‐introductions.

Copyright © 2003 John Wiley & Sons, Ltd.     

The current distribution and status of the freshwater pearl mussel Margaritifera margaritifera L. 1758 in north-west Ireland

1. Margaritifera margaritifera populations are declining throughout its range, including Ireland, despite legislation designed to protect freshwater pearl mussels and their habitat. 2. A survey of freshwater pearl mussels was carried out on rivers in County Donegal, north-west Ireland, to determine the current distribution, size and density of M. margaritifera populations, as well as to identify potential threats to mussels there. 3. The survey revealed the freshwater pearl mussel to be widespread, particularly in the western half of the county. However, densities of mussels at most sites are low, with just two sites having mussel densities of over 5 m⁻². Furthermore, the species appears to be absent from a number of sites from which it had been previously recorded. 4. According to the literature, there is a long history of pearl fishing in Co. Donegal and neighbouring counties. Evidence from heaps of shells found on the river bed and banks at several sites and recent anecdotal reports from local people suggest pearl fishing is being practised on all rivers investigated during the present study. 5. The main conservation requirements for M. margaritifera populations in Donegal are to maintain water quality at its present high standard and, as pearl fishing appears to be a widespread and immediate threat to the remaining mussel populations, to enforce existing legislation designed to protect M. margaritifera.     

A new record of the freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia,Unionoida) from the River Narcea (Asturias,north‐western Spain)

1. A population of the freshwater pearl mussel Margaritifera margaritifera L. was found in the River Narcea in the province of Asturias (north‐western Spain). Primary analysis of the population shows that it is well distributed along the river and is particularly abundant in shady river banks with a gravel substrate. 2. The length of living mussels ranges between a minimum of 22 mm and a maximum of 116 mm, with most in the size class between 65 mm and 70 mm. There is a good proportion of young mussels, although no fertile females were found in the course of the investigation. 3. Although there is no specific legislation in Spain for the protection of M. margaritifera, it has recently been proposed to include M. margaritifera in the Spanish List of Threatened Species as ‘vulnerable’. 4. Although the River Narcea seems to provide suitable conditions for the pearl mussel (water quality, available salmonid hosts, etc.), the main conservation measures must be directed at avoiding river fragmentation from dams, channelization and organic enrichment from individual farms or towns situated close to the river bank. Copyright © 2000 John Wiley & Sons, Ltd.     

Imminent extinction of the Nore freshwater pearl mussel Margaritifera durrovensis Phillips: A species unique to Ireland

The last population of the Nore freshwater pearl mussel Margaritifera durrovensis was surveyed each year from 1990 to 1994 in the River Nore, southern Ireland. The population has fallen from a ‘flourishing colony’ in the 1920s to an estimated 2000 in 1990 and 420 in 1994. No juvenile mussels were observed in any of the surveys. If life history data for Margaritifera margaritifera are applicable to M. durrovensis, the population would need to be 20 times greater for successful recruitment. Although given special mention in the Bern Convention, M. durrovensis was omitted from the European Union Habitats Directive, perhaps due to uncertainty regarding its taxonomic status as it shares characteristics with both M. margaritifera and M. auricularia. Immediate measures are required to prevent the extinction of M. durrovensis including, (a) a captive breeding programme, (b) habitat restoration, and (c) formal recognition of its priority status within the Habitats Directive.     

Growth of wild pearl oysters <Emphasis Type="Italic">Pinctada fucata,Pinctada margaritifera</Emphasis> and <Emphasis Type="Italic">Pinctada sugillata</Emphasis> (Bivalvia: Pteriidae) in Taiwan

In order to understand growth features of pearl oysters in the genus Pinctada, i.e. Pinctada fucata, Pinctada margaritifera, and Pinctada sugillata in Taiwan, a total of 3062 wild individuals of these species from juvenile to adult were collected monthyly from March 2001 to April 2002 in Jukeng, Pingtung County, south-west Taiwan. Quantitative measurements of live oysters were conducted for shell height (SH), shell length (SL), shell width (SW), hinge length (HL), and wet weight (WW). Different cohorts were identified through multiple length frequency analysis on SH of P. fucata and P. margaritifera, and growth curves with seasonal variation were estimated for these species. Pinctada fucata in Taiwan had a different seasonal growth pattern from the Japanese population, but had similar growth rates during the high growth period. The growth rate of P. margaritifera in Taiwan was slower than in French Polynesia, the Solomon Islands, and the Red Sea. Comparisons of morphological growth features among the three species show large differences in the SW-related features. Pinctada fucata in Taiwan had larger SW than in Japan and Korea. The differences in growth rates and morphological features suggested that the wild Taiwanese oysters may retain genetically pristine characteristics, thus genetic conservation might be urgently needed.