European regional assessment: Critically Endangered (CR)
EU 27 regional assessment: Critically Endangered (CR)

The Freshwater Pearl Mussel occurs across much of the European region. In the EU, population information is available from EU Article 17 reporting, with no country in the region reporting 'favourable conservation status' for this species. The deficiencies in recruitment compared with losses from old age are resulting in steep population declines and population losses on an annual basis. The generation length for Margaritifera margaritifera is approximately 30 years, so the three-generation period of 90 years has been used to evaluate the population losses. Overall in the last 90 years (1993 - 2023) in Europe based on the number of viable and recruiting subpopulations left from the original subpopulations known in 1920, it is estimated that there has been a decline of 81.5% for Europe, and for EU Member States a loss of 87%. This places the species as Critically Endangered under criterion A2 for both Europe and for the EU 27 Member States.

The unknown element is the number of very large subpopulations that are recruiting as well as they did 90-100 years ago. If enough very large subpopulations (1 million +) are replacing 100-year-old mussels with the same numbers of juvenile mussels per annum, the future prospects would be for a large range reduction but some stable remaining subpopulations. However, we do not have sufficient information on the best populations to have confidence that this is the case.

The most important conservation action for any population has to be the production and thorough implementation of a catchment management plan that undertakes measures at source and/or pathway between the land activities and the habitat within the river, as well as consideration of conservation breeding in situations where subpopulations have become severely depleted.

The species has been in decline for the last century, and past conservation assessments were based on the number of known subpopulations, but without the knowledge that many of these subpopulations had failed to recruit for between 1 and 2 generations and that habitat conditions are not favourable for juvenile growth. Hence, the current assessment reflects new knowledge, and the species would have been assessed as Critically Endangered in Europe in 1996.

Margaritifera margaritifera is widespread in the European region, particularly in western parts of the Atlantic and Mediterranean areas but is largely absent from the central, eastern and southeastern parts of the region. Native extant country-level records are known from: Austria, Belgium, Czechia, Estonia, Finland, France, Germany, Ireland, Latvia, Norway, Portugal, European Russia, Spain, Sweden, and the United Kingdom. Positive e-DNA samples have been found recently in Denmark so the species may still be extant there. The species is extinct in the wild in Luxembourg (captive-bred individuals remain) and is extinct (since the 2010 assessment of the species; Moorkens et al. 2017) in Lithuania (unmapped).

This is a Holarctic species that extends out of the European region through the Russian Federation (Siberia) to North America.

This species has a large population size (with approximately 326,000,000 mature individuals/ 49,500,000 in EU27) but due to habitat degradation, has very little replacement as adults die. Functional extinction is widespread throughout most of the range. Most subpopulations are isolated and genetic exchange between sub-populations is unlikely by natural means. Across most of the range adults that die will not be replaced due to habitat changes that cannot support juveniles, and most subpopulations have not recruited for many years. The following are the most recent revised estimates of current population status and estimated past (90 years) and future (90 years) population and individual number estimates of M. margaritifera in Europe. The information is from Article 17 reporting (EU27), Lois et al. (2014), Rudzīte (2014), Rudzīte et al. (2015), Bolotov et al. (2018), Larsen and Magerøy (2019), Kalniņš et al. (2021), von Proschwitz & Wengström (2021)and from country data from Clemens Gumpinger, Daniela Csar, Pierre Yves Pasco, Samuel Esnouf, Grégory Motte, Jűrgen Geist, Bjørn Larsen, Mapas Ondina, Jon Magerøy, Frankie Thielen, Manuel Lopes-Lima, Ronaldo Sousa, Vincent Prié, Henn Timm, Katrin Kaldma, Virmantas Stunzenas, Niklas Wengström, Ted von Proschwitz, Evelyn Moorkens, Ian Killeen, Martin Österling, Tom Schiøtte, Louise Lavictoire, Panu Oulasvirta, Karel Douda, Agnija Skuja.

Overall in the last 90 years in Europe there has been a decline of 81.5% and for EU27 countries a loss of 87%. The overall Global loss over the same period is not yet calculated.

Austria: There are currently 18 sub-populations (with some sub-populations consisting of only a few, over-aged animals). The past number of sub-populations is unknown and the estimated future number of populations is three, assuming that the conservation measures take effect. There are currently 3,000 individuals. The estimated past number of individuals is 5,000,000 and the estimated future number of individuals is 10,000, assuming that the conservation measures take effect. Without conservation measures the estimated future number of individuals is zero. (Estimated loss of recruiting subpopulations 99% over last three generations).

Belgium: are currently seven sub-populations. The number of sub-populations in the past is estimated at 24. There are currently less than 400 adult individuals because the largest population of the Anlier experienced very high mortality during the historic drought of 2020. The estimate past number of individuals is > 700,000 individuals and the future estimate of individuals is dependent on captive breeding and conservation actions. (Estimated loss of recruiting subpopulations 100% over last three generations.)

Czechia: There are currently five subpopulations. The past number of sub-populations is unknown and the estimated future number of populations is three. There are currently 15,000 individuals. The estimated past number of individuals is 8,000,000 and the estimated future number of individuals is 25,000 if conservation actions work. (Estimated loss of recruiting subpopulations 100% over last three generations.)

Denmark: The species was thought to be extinct in Denmark. However, recent eDNA surveys (September 2022) have found evidence of Margaritifera presence, so targeted surveys will be undertaken (Estimated loss of recruiting subpopulations 100% over last three generations.)

Estonia: There is currently one subpopulation. The estimated past number of sub-populations is more than one and the estimated future number of populations is zero. There are currently 25,500 individuals. The estimated past number of individuals is 400,000 and the estimated future number of individuals is zero. (Estimated loss of recruiting subpopulations 100% over last zero generations.)

Finland: There are currently 151 subpopulations. The estimated past number of sub-populations is 600 and the estimated future number of populations is 25. The estimate of current individuals is 3,000,000. The estimated past number of individuals is >50,000,000 and the estimated future number of individuals is 500,000. (Estimated loss of recruiting subpopulations 78% over last three generations).

France: There are currently 159 sub-populations. Of these 63 populations have less than 10 individuals left. The estimated past number of sub-populations is 200 and the estimated future number of populations is 10. There are currently 370,000 individuals. The estimated past number of individuals is 50,000,000 and the estimated future number of individuals is dependent on the level of success with captive breeding and conservation management. (Estimated loss of recruiting subpopulations 96% over last three generations.)

Germany: There are currently 37 subpopulations. The estimated past number of sub-populations is more than 100 and the estimated future number of populations is one. There are currently 55,000 individuals. The estimated past number of individuals is 25,000,000 and the estimated future number of individuals is 10,000. In only two German subpopulations natural reproduction has led to population increases in the last 10 years. Several populations are only sustained by captive breeding.

United Kingdom: There are currently 148 subpopulations. The estimated past number of sub-populations is 200 and the estimated future number of populations is 10. There are currently an unknown number of individuals in Scotland, following the loss of a large number of individuals in Storm Frank in 2015. Estimates for England are 400,000 (13 populations), for Wales 1,500 individuals (nine populations), and in Northern Ireland 28,000 individuals (six populations). The estimated past number of individuals is 20,000,000 and the estimated future number of individuals is unknown. (Estimated loss of recruiting subpopulations 90% over last three generations.)

Ireland: There are currently 121 subpopulations. The estimated past number of sub-populations is 150 and the estimated future number of populations is zero to three. There are currently 7,000,000 individuals. The estimated past number of individuals is 120,000,000 and the estimated future number of individuals is zero unless conservation measures are sufficient to restore recruitment. (Estimated loss of recruiting subpopulations 96% over last three generations.)

Latvia: There are currently eight subpopulations. The estimated past number of sub-populations is 40 and the estimated future number of populations is zero. There are currently 18,700 individuals. The estimated past number of individuals is 5,000,000 and the estimated future number of individuals is <9,000, but depends on the ability to provide more effective conservation actions.

Lithuania: The species has gone extinct in Lithuania. (Estimated loss of recruiting subpopulations 100% over last three generations.)

Luxembourg: There are currently no extant subpopulations. The estimated past number of subpopulations is more than one and the estimated future number of populations is zero. There are currently zero individuals in the wild (ca. 500 (over eight years old) animals from captive breeding but not released in the wild). The estimated past number of individuals is 200,000 and the estimated future number of individuals is zero. (Estimated loss of recruiting subpopulations 100% over last three generations). Any improvement on this future estimate is dependent on the success of released captive-bred individuals and further conservation actions. (Estimated loss of recruiting subpopulations 100% over last three generations.

Norway: There are currently 440-460 subpopulations. The estimated past number of sub-populations is at least 600 and it is not possible to estimate the future number of sub-populations. There are currently 130 million individuals. The estimated past number of individuals is 1,000 million and it is not possible to estimate the future number of individuals. (Estimated loss of recruiting subpopulations 60% over last three generations, based on 25% loss and 35% not recruiting.)

Poland: The species is considered extinct in Poland so there are currently no subpopulations or individuals. (Estimated loss of recruiting subpopulations 100% over last three generations).

Portugal: The species was rediscovered in the early 2000s and there are currently six subpopulations (Neiva, Paiva, Beça, Mente, Rabaçal and Tuela Rivers) given the recent local extinction in the Cávado and Terva Rivers. The past number of populations is unknown and the estimated future number of populations is four (only if conservation actions are successful). A recent comprehensive survey (2022) of the M. margaritifera subpopulations in Portugal showed a 50% decline in the number of subpopulations (sites) and 57% in abundance over the last 20 years (Lopes-Lima et al., 2023).

European Russia: There are currently 53 subpopulations. The past number of sub-populations is around 100 and the estimated future number of populations is unknown. There are currently 143,600,000 individuals. The past number of individuals is unknown and the estimated future number of individuals is unknown. (Estimated loss of recruiting subpopulations 90% over last three generations.)

Spain: There are currently 63 subpopulations. The past number of sub-populations is unknown and the estimated future number of populations is unknown and dependent on conservation management implementation and success. The most recent estimate is 188,734 individuals (2014). The past, current and future number of individuals are unknown. (Estimated loss of recruiting subpopulations 89% over last three generations.)

Sweden: There are currently 646 subpopulations. The past number of subpopulations is unknown and the estimated future number of populations is unknown. There are currently 39,000,000 individuals. The past number of individuals is unknown and the estimated future number of individuals is unknown. (Estimated loss of recruiting subpopulations 81% over last three generations.)

Total estimate across Europe for 2022: 1,883 subpopulations (EU27 1,222), 327 million individuals (EU27 49.5 million individuals).

Since 2010 the number of populations has increased (due to finding previously unknown populations), but the number of individuals, taking into account estimates for new populations, has declined by 25%. Total estimate across Europe for 1920: 2613 sub-populations, 2,000 – 4,000 million individuals. Total estimate across Europe for 2100: 0 - 204 sub-populations, 0 - 47 million individuals, depending on whether conservation actions are taken soon enough and whether they are successful.

Sustainable populations of the Freshwater Pearl Mussel are restricted to near natural, clean-flowing waters, often downstream of ultra-oligotrophic lakes. A small number of records are from the lakes themselves.

The species requires stable cobble and gravel substrates with very little fine material below pea-sized gravel. Adult mussels are two-thirds buried and juveniles up to five to ten years old are totally buried within the substrate. The lack of fine material in the river bed substrate allows for free water exchange between the open river and the water within the substrate. The free exchange of water means that oxygen levels within the substrate do not fall below those of the open water. This is essential for juvenile recruitment, as this species requires continuous high oxygen levels. The clean substrate must be free of inorganic silt, organic peat, and detritus, as these can all block oxygen exchange. Organic particles within the substrate can exacerbate the problem by consuming oxygen during the process of decomposition. The habitat must be free of filamentous algal growth and rooted macrophyte growth. Both block the free exchange of water between the river and the substrate and may also cause night-time drops in oxygen at the water-sediment interface.

The open water must be of high quality with very low nutrient concentrations, in order to limit algal and macrophyte growth. Nutrient levels must be close to reference levels for ultra-oligotrophic rivers. Phosphorus must never reach values that could allow for sustained, excessive filamentous algal growth.

The presence of sufficient salmonid fish to carry the larval glochidial stage of the pearl mussel life cycle is essential.

The greatest pressure currently damaging Margaritifera margaritifera populations are inadequate water flow velocities and volumes for their needs. Water quantity and velocity needs to be natural, with hydrological drivers differing across the European range of the species. Many population flows are driven by snow melt releasing water during the demanding summer months. Other populations have water driven from surrounding wetlands, particularly the peat bogs and heaths of Atlantic regions, and the large marshes and swamps of central Europe, in the best populations large oligotrophic lakes upstream ameliorate extreme flows and supply sufficient low-nutrient food to satisfy a large adult population. Catchment wetlands constantly provide water and low-nutrient detritus food for juveniles. The final component is at least one small mountainous stream entering the river, contributing a constant supply of fresh gravels and/or larger stone to replenish the bedload that is moving slowly downstream over time, and supplying water from small rainfalls at low flows during periods of rain that are insufficient to recharge the supply from the lake or wetland/peat catchment.

Where all of the above combine, a large Margaritifera margaritifera population is expected to thrive. Many mussel populations do not have these characteristics, but at some stage in the past there was sufficient habitat and clean enough conditions to sustain a population. As catchment activities intensified, those without lakes saw the earliest and the most severe declines.

Where drivers of water have been modified, either by dam structures or by water abstraction, the delivery of the appropriate quantities and velocities of water can make the population unsustainable, in extreme cases causing drying of mussel habitat and massive die-offs.

Where open wetland catchments have been modified from natural habitats, such as through drainage and/or afforestation on peat in catchments without snow melt (especially in mild Atlantic regions), or changes of crop to water-hungry species requiring irrigation (especially in Mediterranean regions), large populations have had extreme losses over the last 10 years. Thus, the conservation targets for mussel populations include the restoration of sufficient water in both volume and discharge pattern to support sustainable recruitment and survival of juvenile mussels to maturity.

Intact natural catchments prevent fine sediment and nutrient losses to the river. As hydrological damage and catchment intensification occurs, fine sediment losses become chronic, siltation of the substrate can provide a rooting medium for higher plants. Nutrients can also accumulate in the sediment (and may be chronically or intermittently available in the open water), promoting the growth of algae and macrophytes. This exacerbates the stressful environment for the adult and juvenile mussels, and as more adults are lost, further niches for macrophyte growth become available. There is a resultant trophic cascade in the habitat, where oligotrophic conditions succeed to eutrophic conditions and the suite of invertebrate species changes accordingly. Thus, conservation targets for mussel populations must also include maintenance of free water exchange between the river and the substrate and minimal coverage by algae and weed. The most important requirement is the maintenance of recruitment i.e. the river bed structure required to breed the next generation. Nutrients in the sediment are problematic as they are used by rooted plants. Dissolved nutrients in the water column tend to lead to algal growth. Both come from chronic and/or periodic loss of dissolved nutrients from the catchment.

The species is highly demanding of very clean river habitats in order to be self-sustaining, but it lives for over 100 years, and thus non-sustainable populations of adult mussels can persist for many years after negative changes in the habitat have occurred. While a range of possible causes of decline can exist (e.g. direct habitat damage, catchment drainage or intensification, inadequate water resource management), the overwhelming majority of population declines in Europe at the receptor - i.e. the mussels in the river bed - have manifested as sediment accumulation in the river bed gravels, cutting off the supply of oxygen to juvenile mussels. New generations of mussels cannot be recruited, while older adults that were born before the habitat deterioration remain alive as they are filtering open rather than interstitial water. It is urgent that the source of pressures that lead to this decline from the catchment into the river are reversed, but in some cases, damage has been so severe that only remnant mussels in very small numbers survive in many populations. For these, captive breeding and smaller-scale targeted riparian and river measures to ensure that captive-bred mussels can be placed back in the river are essential. These populations also need to be captive-bred with techniques that maximize the genetic components of the mussels.

There are a number of factors leading to the decline and loss of pearl mussel populations (Moorkens 1999, 2020; Araujo and Ramos 2001, Geist 2010, EU Article 17 reports). The species is highly demanding of very clean river habitats in order to be self-sustaining, but it lives for over 100 years, and thus non-sustainable populations of adult mussels can persist for many years after negative changes in the habitat have occurred. A range of possible causes of decline can exist and often act together (e.g. direct habitat damage, catchment drainage or intensification, inadequate water resource management, acidification of rivers (particularly in Scandinavia), climate change and depletion of mussels from pearl fishing activities.

All direct and indirect pressures and threats result in loss of habitat function at the site of the mussel, resulting in sediment accumulation in the river bed gravels, cutting off the supply of oxygen to juvenile mussels, pollution from excessive nutrient levels causing eutrophication, or toxins causing stress or mortality. New generations of mussels cannot be recruited, while older adults that were born before the habitat deterioration remain alive as they are filtering open rather than interstitial water. The source of pressures that lead to this decline comes from the catchment into the river, thus protection and rehabilitation of mussel populations is impossible without effective catchment management that is protective to the juvenile mussel habitat. The best populations are known from low-intensively managed isolated catchments with little influence from man. However, some famous historical populations persist in low numbers in large, lowland rivers, where adults may be living in habitats that could not possibly sustain juveniles.

Juvenile mussels spend their first five to ten years buried within the river bed substrate. Other ways in which mussel populations can decline and be lost is through adult mussel kills, or loss of host fish which are essential to the life cycle of Margaritifera margaritifera. Further details of the life cycle can be found in Moorkens (1999, 2020), Geist (2010), and Taeubert et al. (2013).

Fine sediment, once introduced to a pearl mussel river, can continue to cause very serious effects on a long-term basis (Ellis 1936, Marking and Bills 1979, Killeen et al. 1998, Araujo and Ramos 2001). Direct ingestion of silt by adult mussels can lead to rapid death. Turbidity, particularly from fine peat entering the water, causes adult mussels to clam up (they close their shells tightly and do not filter water through their siphons), a response that provides protection against ingesting damaging fine particles. If the river water remains strongly turbid for a number of days, mussels can die from oxygen starvation, either from remaining clammed, or from ingesting contaminated water while stressed. During a time of year when water temperatures are high, oxygen depletion in the body occurs more rapidly, and mussels die more quickly. The evolutionarily primitive Margaritifera margaritifera gills and the annual brooding of young in all four of the gills demand a continuous, high supply of oxygen. Even if the adult mussels survive an initial silt episode, food/oxygen deprivation from clamming will have caused them to become stressed, from which they will take a long time to recover. If during that recovery period, there are further incidents of mobilisation of this or other silt, then the stressed mussels will be more susceptible to death than mussels in a cold river in unstressed conditions. Thus, they may continue to die over a period of several months. Higher temperatures throughout the summer further exacerbate this problem.

Once a silt load enters a river that holds a pearl mussel population, it can continue to cause harm. Silt causes river changes, which in turn change the dynamics of the river into the future (Dietrich et al. 1989, Colosimo and Wilcock 2005, Curran and Wilcock 2005). Increases in fine material in the bed and suspended in the water column, and consequent changes in channel form, may affect mussels in many ways and at various stages in their life cycle. The direct killing of adults is only the first stage in the damage that silt causes to the population. Sediment that infiltrates the substrate decreases the oxygen supply in the juvenile habitat, which prevents the recruitment of the next generation. The sediment subsequently provides a medium for macrophyte growth, a negative indicator in pearl mussel habitats. Macrophytes then smother the juvenile habitat even further, and the macrophytes trap more sediment, exacerbating the problem in the long term. One of the most essential requirements for pearl mussel conservation is the removal of the risk of any sediment reaching the river, as any one single incident has such long-term ramifications.

Silt infiltration of river bed gravels can also have a negative effect on the essential species of fish that host the mussel glochidial stage (Levasseur et al. 2006).

As with siltation, nutrient enrichment can have serious and ongoing impacts on both juvenile and adult mussels. Increased inputs of dissolved nutrients to mussel rivers tend to lead to filamentous algal growth unless combined with siltation, where macrophyte growth can dominate. Filamentous algae can lead to the death of juvenile mussels, by blocking oxygen exchange with the sediment, and cause adults to become stressed, as a result of nighttime drops in oxygen. Even if filamentous algae are destroyed in a flood, adult mussels may not make a full recovery before the algae re-grows. Adult mussels may eventually die as a result of oxygen/food deprivation.

Death and decomposition of filamentous algae contributes fine particulate organic matter to the river substrate. This further blocks water exchange between the river and the substrate and causes additional oxygen depletion through the process of decomposition. Decomposition also releases dissolved nutrients, promoting further primary productivity. Inputs of organic material, such as slurry, to the river have a similar effect on the mussel substrate as dying/decomposing algae and macrophytes.

Major pressures that are leading to damage of river bed substrate from infiltration of inorganic silt, organic fine peat and decaying organic detritus and from eutrophication are listed below. These are pressures that are present in many catchments and their cumulative effects have had very severe impacts on mussels.

Catchment drainage and/or intensification affecting hydrology
Explanation: Large important populations have had their most serious declines in the last 10 years from 1) intensification practices that require a higher use of catchment water, including irrigation (especially Portugal), 2) inappropriate land intensification in catchments where hydrology is driven by catchment habitats (such as peaty habitats including bogs and heaths) (Flynn et al. 2021, 2022) and 3) the culmination of older practices that have manifested most severely over the last 10 years (such as drying of catchment land from increased evapotranspiration levels from maturing forestry planted in the past) (Kuemmerlen et al. 2021). Drainage of peaty catchments has been shown to increase run-off rates and flood peaks (Müller 2000). Such hydrological changes lead to instability in mussel habitat and increased disturbance.

Damage manifests at the site of mussel habitat through inadequate water volume or level, and/or inadequate near-bed velocity at the mussel siphon level preventing sufficient oxygen and nutrition intake, and/or at the river bed preventing sufficient interstitial exchange for oxygen and nutrition intake for juvenile mussels. Low flows also concentrate sediment and nutrient levels that exacerbate mussel stress. This pressure/threat leads to adult and juvenile stress and mortality. Depending on the timescale and severity, mussel distribution and habitat may still be widespread and restorable, or mussels may be restricted to low numbers in very restricted areas of preferential and permanent flow. In the latter case the full catchment is not likely to be restorable, and captive breeding alongside targeted habitat management may be the best that can be achieved. Larger populations with restorable catchments should be prioritised before they reach a condition beyond repair.

River system modification and management: flooding, modification of hydrographic functions, management of water levels
Explanation: Dams and other holding back of water and its abstraction for human, agricultural or other use, or hydroelectric energy production have resulted in serious declines of large and important populations. This manifests at the site of mussel habitat through inadequate water volume or level, and/or inadequate near-bed velocity at the mussel siphon level preventing sufficient oxygen and nutrition intake, and/or at the river bed preventing sufficient interstitial exchange for oxygen and nutrition intake for juvenile mussels. Low flows also concentrate sediment and nutrient levels that exacerbate mussel stress. This pressure/threat leads to adult and juvenile stress and mortality. Good knowledge is needed on how mussels in their specific catchment locations respond to hydrological changes in both good catchments and poor catchments (see Hauer 2015, Killeen and Moorkens 2020, CEN Standard EN16859). Consistent but unnatural flows, particularly more prolonged low flows can cause stress to adult and juvenile mussels by raising temperature, reducing oxygen, concentrating pollutants and providing conditions for silt deposition and algal growth. Rapid changes in flow regime such as where sluices or dams are opened and closed regularly is damaging to pearl mussel populations. This may be due to the energy effort of individuals, concentrated on digging into substrate or moving around leading to a state of continuous stress. Where rapid changes are occurring at very sensitive times of the year, loss of annual glochidial production or newly dropped juvenile mussels can occur. These phases of the life cycle normally occur at periods of low flow. Dredging has taken place in the past in the large lowland pearl mussel habitats, with large numbers of dead mussels being found afterwards. Kills are likely to have included pearl mussels in the range of the dredging through habitat destruction, and mussels downstream, through siltation. Erosion of river banks is a serious cause of silt entering the river. Its cause is rarely natural, even when no immediate explanation is obvious, but rather a knock-on effect from river bed or bank changes elsewhere. Where cattle or sheep are allowed to enter the river, serious erosion can occur.

Agricultural improvement
Explanation: any practice that leads to increased drainage of catchment land, increased concentrations and pathways of nutrients or pesticides, exposure of bare ground can increase the fine sediment and nutrient load to the river. The cumulative effects of such practices can have very severe impacts on mussels.

Liming of land has a negative effect on Margaritifera margaritifera populations, through direct toxic effects, and through increased growth rates leading to shortened life expectancy and, thus, loss of reproductive years (Bauer et al. 1991, Skinner et al. 2003). In some countries, acidification problems are so severe that liming is considered to have a more positive than negative effect (Henrikson et al. 1995).

Pesticide use
Toxic pollution can have very serious and long-term effects on a Freshwater Pearl Mussel river. Of particular concern is agriculture, including forestry and pesticides. Organophosphates and synthetic pyrethroids used in sheep dipping and pouring are highly toxic to species that are a lot less sensitive to nutrient and silt pollution than Margaritifera margaritifera. The Freshwater Pearl Mussel is too endangered to justify specific laboratory toxicity testing, but this should not be used as a reason to be ambiguous about the threat such pesticides present to Margaritifera margaritifera. Evidence from studies on glochidial and juvenile stages of unionoid mussels have demonstrated lethal effects from very low doses of chlorpyrifos and permethrin, the fungicides chlorothalonil, pyraclostrobin and propiconazole, and glyphosate. Of particular concern are the severe deleterious effects of these substances in combination with surfactant blends, as found in various commercial products. The combined product is often far more toxic than the individual ingredients. The use of rotenone in Margaritifera margaritifera catchments upstream of, or close to, mussel beds should not be considered without an assessment of potential impacts on the mussels. Endocrine disrupters can potentially affect reproduction in molluscs. Investigative monitoring may need to be undertaken where brooding is found to be impaired and there is significant sewage entering the river.

Fertiliser use
Any applications of chemical fertiliser or manure can lead to direct run-off of dissolved and particulate nutrients, as well as gradual nutrient release from the soil. The most seriously damaging nutrient is most probably phosphorus, as it is the limiting nutrient in most oligotrophic pearl mussel rivers. Phosphorus promotes algal growth.

Overgrazing by livestock
Overgrazing by sheep in mountainous moor and blanket bog habitats in the upper reaches of pearl mussel catchments has led to loss of vegetation and exposure of peaty soils. The bare peaty soil erodes easily and releases fine sediment into the river. Similarly, overgrazing by cattle and other animals along the banks of pearl mussel rivers has led to, and continues to cause, bank erosion. Furthermore, drinking access for cattle causes direct damage and death to mussels, as well as encouraging further bank erosion and sediment mobilisation.

Restructuring agricultural land holding
On mineral soils, the removal of hedges, copses and scrub from lands surrounding pearl mussel rivers is linked with possible kills of adult mussels and declines in the quality of juvenile habitat. These land changes lead to exposure of bare ground that causes the release of silt into the river. They are often accompanied by drainage. Drains themselves can continuously erode and be a source of fine sediment. These newly drained areas are more conducive to agricultural practices of greater intensity than before, thus the problem is exacerbated and ongoing.

General forestry management
Forestry planting on naturally open habitats especially with wet peat soils is severely damaging to catchment hydrology. In hydrological areas where the driver is snow melt, forest is a natural habitat and can ameliorate excess flows. Even where forestry is an acceptable land use, forestry planting, drainage, ground preparation, clear-fell, replanting, thinning and all management practices associated with clear-fell plantation have been a major source of both silt and nutrients in pearl mussel catchments. The drainage and other preparations of land for planting and the practice of clear felling leads to exposure of bare ground that can erode and release silt into the river. Fertilisation of forestry leads to a release of nutrients into the watercourse, especially on peat and peaty soils. These nutrients, alone or in association with other nutrient sources, raise the trophic level of the river above limits that are tolerable for the mussel. Brash left on site during and following harvesting operations provides further, long-term inputs of damaging nutrients. Ongoing forestry operations do not allow for recovery of the Margaritifera margaritifera habitat and the future for pearl mussel rivers with continued forestry operations is bleak. Restoration of pearl mussel populations will only be possible if there are significant initiatives to remove clear-fell forestry from Margaritifera margaritifera catchments, such as forest-to-bog measures (Similä et al. 2014, Anderson 2018, Hambley et al. 2019). Even given such a commitment, major mitigation works will be necessary during the removal of the forestry and restoration to low-intensity or semi-natural land uses.

Acidification has been well documented as a threat to salmonid populations from air pollution and from forestry (e.g. Maitland et al. 1987, Lacroix 1989, Allott et al. 1990, Bowman and Bracken 1993, Henrikson et al. 1995, Kelly Quinn et al. 1997). As salmonid hosts can come from anywhere within the pearl mussel catchment, protection of the entire catchment from acidification is essential. Acidification was noted as a direct threat to Margaritifera margaritifera since the first international IUCN red data book for invertebrates (Wells et al. 1983). Work carried out in Scandinavia has provided evidence for pearl mussel decline from acidification (Eriksson et al. 1981, 1982, 1983; Økland and Økland 1986, Henriksen et al. 1995, Raddum and Fjellheim 2004). A lowering of pH directly influences pearl mussels through a gradual destruction of their calcareous shell, and also their genital organs (causing infertility), and through problems with regulation of acid-base mantle fluid homeostasis (Vinogradov et al. 1987).

Stock feeding
The introduction of nutrients to Margaritifera margaritifera catchments through the importation of artificial stock feed, e.g. silage, allows increases in the stock numbers. This in turn can cause trampling damage, soil erosion and nutrient releases. The move from outdoor rearing to indoor winter housing and associated stock feeding increases the nutrient and sediment pressures in a subpopulation, and can lead to a trophic change in the river with ongoing algal blooms and mussel mortality.

Recreational fishing
If anglers are allowed to enter rivers at pearl mussel beds, serious trampling damage can occur. Systematic physical changes to rivers for the purposes of enhancing fish numbers for angling can also be very damaging to pearl mussel habitat, including bank reinforcement, and the installation of weir and croy structures (in-river structures to manage river fisheries or provide access for fishing). Damage occurs during construction, and through changes to flow patterns, leading to scouring of stable gravels and loss of mussels and their habitat in some parts of the river. In other areas ponds are created where silt accumulates with further loss of juvenile and adult habitat.

Pearl harvesting
Pearl fishing has been a major problem in the past, and kills from pearl fishing have been observed in recent years in spite of the practice being illegal under EU law. The extent of the problem cannot be calculated due to the illicit nature of the threat.

Quarries/ Sand and gravel extraction
Freshwater Pearl Mussel subpopulations have been damaged in the past and continue to be damaged both directly through removal of gravel from pearl mussel river beds, and indirectly through silt and other pollution from quarrying activities, management of water through tailings ponds, risk of breaching of polluted ponds, changes in catchment hydrology from groundwater pumping and surface water management. Severe episodes of silt lead to adult mussel kills, large and small releases of silt destroy juvenile habitat. Another common problem is the release of calcium from limestone quarries, which increases growth rate in adult mussels, thus shortening mussel lives and reducing the long fertile period required for pearl mussel life history strategy.

Peat extraction
Hand and machine cutting of peat, including the drainage channels used in the process, leads to losses of pearl mussel juvenile habitat from hydrological change and from infiltration of river bed substrate by fine peat particles released from bare soil.

Other extractive industries
Pollution of water courses from mining and quarrying activities by mined heavy metals, and chemicals used in the process of extraction of mined products has led to the loss of Pearl Mussel subpopulations.

Pollution: urbanised areas, human habitation
The Freshwater Pearl Mussel is a species that requires near-natural conditions. Continuous urbanisation, discontinuous urbanisation and dispersed habitation have all been associated with depressed water and habitat quality in pearl mussel rivers. Lack of appropriate water treatment (water must reach the river at reference levels), including even small elevation in biological oxygen demand (BOD) levels, and even minor increases in ortho-phosphate levels can lead to loss of juvenile habitat. Inappropriately plumbed washing machines can lead to serious nutrient (phosphorus) elevations and subsequent filamentous algal growth.

Pollution: industrial and commercial areas
Freshwater Pearl Mussels have already been lost from intensively industrialised areas, but local and more rural industries such as meat processors and creameries operate adjacent some extant pearl mussel rivers. High BOD levels and other pollutants have led to loss of juvenile habitat and severe depletion of adult mussels.

Pollution: disposal of household and industrial wastes
There is evidence of reduced habitat quality for Pearl Mussels in rivers where land fill sites are present in the catchment. Decreased habitat quality is also found in rivers where household and other waste is dumped into or adjacent the river instead of being properly disposed of, and in rivers where inert materials such as builder's rubble have been used as infill within the flood plain area to raise and level the ground for more intensive usage.

Pollution: water pollution
Water pollution, particularly nutrient pollution, leading to increased primary productivity, is associated with agriculture, coniferous clear-fell forestry, industrial effluents and insufficient treatment of domestic, municipal or industrial sewage. Very small increases, above natural background nutrient loads can lead to damage. In particular, the normal background ortho-phosphate reference level (generally 0.001-0.005 mg/l P in oligotrophic rivers in Atlantic and Boreal biotopes) is considered to be essential to the maintenance of oligotrophic waters for reproducing pearl mussel rivers (Moorkens 2006). Small increases in ortho-phosphate can lead to deleterious algal and/or macrophyte growth, so maintaining low levels at all times is considered to be essential. One large input of ortho-phosphate can lead to an algal incident, which in turn leads to detritus/particulate organic matter, causing adult and juvenile deaths and increases the trophic status of the river on a long-term basis. Growing algae causes problems by blocking oxygen exchange between the substratum and the water column and through night time depletion of oxygen. Decaying algae causes detritus that not only clogs the interstices, but also causes oxygen depletion because oxygen is used up during its decomposition.

An increase in trophic status can lead to major habitat changes, particularly a change from Fontinalis-dominated flora/macrophytes to Myriophyllum and Ranunculus-dominated flora where nutrient pollution is accompanied by siltation. These macrophytes are indicative of poor Margaritifera margaritifera habitat and provide conditions for trapping further silt and continued loss of habitat as a result of changes of flow, sediment and nutrient dynamics (Masden et al. 2001, Clarke 2002, Cooper et al. 2013). Phosphorus that resulted in macrophyte growth continues to be released and mobilised as the macrophytes decompose (Barko and Smart 1980, Rooney et al. 2003).

Communication and transport networks: railways, roads, paths, tracks, cycling tracks
There is evidence of reduced habitat quality for Pearl mussels in rivers where functioning flood plain has been impeded by hard surfaces of roads or paths or where juvenile food source habitat has been destroyed or impeded. It has been reported (Hruska 1999) that juvenile mussels require a direct connection between the groundwater contributing to the interstitial gravels and the unimproved low nutrient vegetation in the flood plain, providing the type of detritus food particles that are used in captive breeding (Eybe et al. 2013). Building of hard surfaces can release damaging silt into the river. Hard surfaces near a pearl mussel population can also lead to run-off of pollutants into the river. These are permanent effects, i.e. both from construction and operation so road development is considered to present a significant threat to this species.

There is evidence of reduced habitat quality for pearl mussels in rivers where bridges have been built, even where they have clear spanned the river. In general, the most negative effects have occurred where structures were not spaced wide enough and, thus, not enough flood plain habitat has been left on either side of the river (see above). The damage is exacerbated where flow changes have occurred, and consequent hard measures such as revetments, walls or rock armouring have been built along the banks in the vicinity of the bridge to prevent bank erosion. Building of bridges can release damaging silt and nutrients into the river. The bridge and nearby road can also lead to run-off of pollutants into the river. These are permanent effects, i.e. both from construction and operation. Other permanent effects include excessive shading under the bridge and disturbance to adult mussels and reproduction on a long term basis. Where the population of mussels is dense, the mussels form an intrinsic part of the river bed structure, and damage at one area can then cause knock-on long-term damage to beds of mussels upstream and downstream of the structure.

Energy infrastructure
There is evidence of mussel kills where pipelines have been routed across river beds, from instream works in the river causing silt episodes, and also in silt from bare ground where the pipe has been dug on either side of its entry into the river. to the swathe of habitat removal required before and after it crosses the river.

Sport and leisure infrastructure
There is evidence of increased silt and nutrient releases and depressed pearl mussel habitat where golf courses, sports pitches and camp sites have been developed nearby.

River system modification and management: canalisation and drainage
Arterial drainage, canalisation, boulder removal, etc. has destroyed river habitat by replacing natural channel reach patterns of pools and riffles with more uniform runs that suit neither the pearl mussel nor its host fish (Moorkens 1999, Hastie et al. 2000, Valovirta 2001). Bank reinforcement actions often accompany or are deemed necessary following canalisation. They are a response to external damage to river banks at the site of reinforcement or that has taken place elsewhere but has had ramifications at the site of reinforcement. The reinforcement structures in themselves can affect river dynamics both upstream and downstream of the works (Fischenick 2003, O'Grady 2006). Hard reinforcement measures are considered to be damaging activities in pearl mussel rivers.

Hard measures in combination with an intensified drainage network has led to further hydrological damage and an increase in the release of silt into river channels hosting pearl mussels, with the subsequent destruction of juvenile habitat. Drainage of peaty catchments has been shown to increase run-off rates and flood peaks (Müller 2000). Such hydrological changes lead to instability in mussel habitat and increased disturbance. These inappropriate hydrological changes over time have resulted in the most serious declines of larger mussel populations over the last 10 years.

Interspecific faunal relations: genetic pollution
The loss of host fish is regularly cited as a potential reason for pearl mussel decline (Araujo and Ramos, 2001). A study on the status of host fish populations and on fish species richness in European pearl mussel populations (Geist et al. 2006) characterised typical fish communities in pearl mussel streams and revealed that a lack of host fish only seems to be limiting pearl mussel reproduction in specific areas. Intact and functional pearl mussel populations were found to occur under extremely oligotrophic conditions with lower host fish density and biomass than in disturbed populations without juvenile recruitment. However, where nutrient levels have increased, more host fish may be required as compensation for lower glochidial production rates in stressed mussels (Geist 2005). Salmon and Margaritifera margaritifera have been cited as symbiotic in their relationship, with both species providing a beneficial role for the other (Ziuganov et al. 1994). Freshwater Pearl Mussels filter the river water and increase its purity, and salmon gills host mussels during their glochidial stage. Freshwater Pearl Mussels have also been shown to prevent early senility in salmon and thus extend their life expectancy (Ziuganov 2005). It is likely that host fish numbers in ultra-oligotrophic situations were never very high, as pearl mussels are naturally adapted to live in rivers with low food levels and very low productivity (Bauer et al. 1991), but an unnatural decline in host fish will inevitably threaten Margaritifera margaritifera. As well as habitat decline and acidification, impediments to fish movement from artificial barriers can result in losses of mussel populations (Bogan 1993). Genetic pollution through the introduction of fish stocks not native to the catchment is considered to be a problem, as there appears to be a strong level of adaptation between genetic mussel and fish stocks.

Interspecific faunal relations: invasive alien species (IAS)
The potential for exotic species spreading into Pearl Mussel rivers could result in major declines of the Freshwater Pearl Mussel, such as alien fish or mussel species, and continued spread of exotic Ranunculus (Laughton et al. 2007) and invasive crayfish (Signal Crayfish Pacifastacus leniusculus)(Schmidt and Vandre 2012).

Climate change
The negative effects of climate change have manifested across the range of Margaritifera margaritifera during the last 10 years and is likely to continue to further threaten the survival of this species. Increased temperatures will lead to a higher metabolic rate and consequently a shorter life expectancy and thus reduced reproductive episodes per individual. This may exacerbate an already lowered recruitment level. The likely scenario of increased summer droughts and winter storm and flood events may negatively affect the species by increasing the frequency of stressful 'natural' events. These may result in increased siltation incidents during flooding. Habitat space may be reduced as a result of loss of river bed in drought conditions, or instability of gravel beds that are currently stable, through frequent flooding. Climate change may also threaten the salmonid host species or on the food web that they rely upon. Phenological changes may threaten the encystment of host fish through changes in interaction times between the mussels and their hosts. Changes in sea level may increase the salinity of a higher percentage of the lower reaches of some mussel rivers, which would have particularly serious ramifications for populations that have now become restricted to the bottom end of rivers. Hastie et al. (2003) predict that a number of Scottish populations may be lost as a result of climate change, and this has already manifested through large losses from hydrological pattern change.

Climate change alone is a serious threat, most particularly in the Mediterranean biotome, but in combination with catchment drainage and intensification, and in pressures on water management for abstraction the results have already been seen to be deadly.

Pearl fishing was carried out both casually and by fishermen that regularly harvested pearls for profit. Some pearl fishing continues today and is a serious threat to the species. In the EU this practice is illegal.

To date, many Freshwater Pearl Mussel rivers within the EU have been designated as Special Areas of Conservation (SACs) within the Natura 2000 network, and the species is protected under national legislation in most countries with varying levels of restriction. In most cases, both national legislation and SAC status have resulted in some improvement on direct damage to mussels such as pearl fishing, and some protection against plans or projects that would be likely to damage populations, but conservation actions are generally lacking through lack of real engagement in how such rivers and their catchments need to be managed in order to rehabilitate and sustain their mussel populations for the future.

It is obvious that if damaging activities are not removed and prevented in the future within pearl mussel catchments, the designation of SACs for the species will not have led to any protection whatsoever. Part of the problem of protection of the species within SACs is the design of the directive, which restricts SACs to habitats of importance so that buffer zones that would be of great value in conservation action cannot be part of any designation. In the EU there is a requirement to protect SACs from ex situ damage, but this has not been effectively operated to date, most direct and catchment damage through new and ongoing projects has occurred through inadequate Article 6.3 assessments.

A strong negative indicator of the future prospects of this species has been the very poor response of the competent authorities in dealing with the damaging effects of the intensification of catchments for agriculture and forestry in pearl mussel catchments. Agricultural and forestry operations continue to intensify in parts of pearl mussel catchments and need to be reduced to levels that are compatible with the life cycle of the pearl mussel. Recent intensification has resulted from both economic drivers (e.g. damaging water-demanding crops) and inappropriate environmental policy (e.g. policies of tree planting in places where open peat restoration would restore hydrological function). Pressure on dairy and fruit farmers to intensify operations has led to the use of previously marginal land. Conservation actions to restore damaged catchments and water management structures are the key priority in the largest remaining populations and are essential to the survival of the species over the next 3 generations. Planned EU legislation on habitat restoration could assist with planning for the restoration of land associated with favourable mussel conditions in the river it supports could be useful in rehabilitating populations, and such land restoration should be prioritized in these important mussel catchments. Measures to restore catchment hydrology and river flows would also be favourable climate mitigation actions.

Other conservation actions include captive breeding in situations where populations have become severely depleted. This should never take place without a detailed catchment management plan to allow for the return of captive-bred mussels to the wild. It is hoped that the Water Framework Directive (WFD) may help develop policies, legislation and management strategies that could work towards managing damaging land uses and improving water and habitat quality. However, the WFD is not yet monitored and aligned to Margaritifera margaritifera requirements and this requires urgent change. It is imperative that recoverable pearl mussel populations are given the highest priority and that everyone involved in the implementation of this Directive understands the very demanding habitat requirements of the pearl mussel.

Recent LIFE projects and European Innovation Projects (EIP) have been undertaken across the mussel’s EU range. Many included the policy of compensation of landowners for more compatible practices, and these have been very successful for ecological improvements on agricultural land, particularly those that control payments by results, such as plant indicators of increased wetness. Because they are voluntary they often miss out on actions there the biggest damage occurs.

Projects have been less successful for sectors that are more set in their ways and are reluctant to make necessary catchment-wide changes, such as the forestry sector. Proper enforcement of Article 6 of the Habitat’s Directive is a key requirement in preventing ongoing damage. The same is true of water management, Article 6 assessments or their equivalents outside the EU, if implemented properly, should lead to the required changes to sustainable practices.

It is urgently important to make long term plans for rehabilitation of mussel populations through a detailed management plan on a catchment-by-catchment basis. Over the last 10 years many countries have put much effort into improving plans and measures for conservation actions. These have not yet resulted in widespread success. It is important that efforts are put into actions deemed to be essential to prevent extinction rather than softer options that do some good but will never be enough to restore favourable status.

A CEN standard for monitoring Margaritifera margaritifera has been published and has already resulted in positive efforts to ensure survey is undertaken when needed, and is undertaken in a manner that is appropriate for assessing this species (CEN Standard EN16859; Boon et al. 2019). The standard is particularly important for populations that are not protected within the Natura 2000 network which are often ignored compared with designated populations but are important for maintaining the species' range.