Freshwater Bivalves have colonized diverse habitats worldwide and have adapted to highly diverse habitat conditions; however, they also belong to the most imperilled taxonomic groups worldwide. In particular, Unionoid Bivalves, or Freshwater Mussels, which have a complex life cycle including an obligate host-Fish stage, are highly vulnerable to habitat alterations, as these can affect the Mussels directly as well as their host Fish. In Central Europe, Bivalve populations have severely declined over the last decades owing to pollution, physical habitat destruction, and land-use changes. At the same time, Bivalves are considered keystone species for the functioning of freshwater ecosystems, as they provide important ecosystem services such as filtration, bioturbation or nutrient allocation.
In a paper publiched in the journal Aquatic Conservation: Marine and Freshwater Ecosystems on 19 February 2020, Katharina Stoeckl of the Aquatic Systems Biology Unit at the Technical University of Munich, and the Bavarian Academy for Nature Conservation and Landscape Management, Marco Denic, also of the Aquatic Systems Biology Unit at the Technical University of Munich, and of Landschaftspflegeverband Passau, and Juergen Geist, again of the Aquatic Systems Biology Unit at the Technical University of Munich, presents an overview of the population status and habitat conditions in Freshwater Pearl Mussel, Margaritifera margaritifera, and Thick-shelled River Mussel, Unio crassus, streams in Bavaria and assesses the condition of populations and habitats based on the German assessment criteria within Natura 2000 areas.
In European member states, species and habitat types that are considered to be of European importance are protected under the Habitats Directive. The directive obliges member states to maintain or to reach a favourable conservation status of 200 habitat types and more than 1000 animal and plant species. All habitats and species protected under the Habitats Directive as well as under the Birds Directive form the Natura 2000 network of protected areas. Protected species and habitats are defined in Annexes II, IV and V of the Habitats Directive, depending on the means of protection. For example, for species in Annex II, core areas of protection need to be defined (‘special areas of conservation’), which are included in the Natura 2000 network. These sites must be managed according to the ecological demands of the target species. Species in Annex IV must be strictly protected not only within but also outside of protected areas, and the exploitation of species in Annex V must not endanger their favourable conservation status. Following Article 17 of the Directive, member states must report to the European Commission on the state of the habitat types and species every 6 years based on the results of monitoring programmes. In most cases, member states have developed national monitoring protocols for species and habitat assessments. As a result, methodologies and data quality can differ widely between the countries. For Freshwater Pearl Mussel, the first step to overcome this problem was taken only recently, when a group of international experts from countries with existing populations of this species came together to compile a standard, following the criteria of the European Committee for Standardization. The European Committee for Standardization brings together national standardisation bodies from 34 European countries for the development of voluntary standards at a European level. The European Committee for Standardization standard for monitoring Freshwater Pearl Mussel streams was developed by experts from 11 countries: Austria, Finland, France, Germany, Ireland, Luxembourg, Norway, Portugal, Spain, Sweden, and the UK. Based on best practice developed and used by those experts, the standard describes approaches that individual countries have adopted for survey, data analysis, and condition assessment, and provides guidance on a consistent approach to monitoring. Among the 44 mollusc species, the Freshwater Pearl Mussel and the Thick-shelled River Mussel are listed in the annexes of the Habitats Directive. Both species are relatively widespread throughout Europe but are now strongly declining. Margaritifera margaritifera is was assessed as Critically Endangered in the International Union for Conservation of Nature's Global Red List and Unio crassus is considered to be Endangered, with large viable populations remaining in northern Europe and Russia. With 46 Pearl Mussel populations and 82 Thick-shelled River Mussel populations a considerable proportion of German populations occur in the federal state of Bavaria.
Freshwater Pearl Mussels, Margaritifera margaritifera. Wikimedia Commons.
The study was conducted in 20 Margaritifera margaritifera and 14 Unio crassus streams in the state of Bavaria, Germany, between 2012 and 2015. The rivers with Margaritifera margaritifera included all types of Margaritifera margaritifera habitats in Bavaria as well as populations in various conditions. At a national level, Bavaria holds the majority of German Pearl Mussel populations. For Unio crassus, 14 study streams had been selected previously by the Bavarian Environment Agency by random draw for each Bavarian state district from the state database ArtenSchutzKartierung. As a consequence of a recent illegal pearl fishing event, the names of the Mussel rivers are treated as confidential and are not reported by Stoeckl et al. The natural distribution area of Margaritifera margaritifera in Bavaria is limited to the Eastern part of the state, which is dominated by siliceous headwater streams. In contrast, Unio crassus is widely distributed across the state, with the study sites representing all faunal regions that are populated by the species.
Distribution of Mussel populations sampled in the study area: (•) Unio crassus populations; (+) Margaritifera margaritifera populations. Stoeckl et al. (2020).
The survey area covered the colonised area of the Mussels in each stream, which was known from previous monitoring programmes, and varied between 0.2 and 18.0 km of river length. For Margaritifera margaritifera, complete census monitoring was performed where Mussel numbers were expected to be smaller than 1000 individuals. In populations of more than 1000 individuals, 5-m cross-channel transects were applied every 100 m to estimate the population size.
For Unio crassus, a systematic sampling approach was applied using cross-channel transects to estimate the population size. Systematic sampling provides good spatial coverage and is particularly useful for populations of rare species. The distance between two transects was 80 m and the length of each transect was 20 m. In all streams, visual and tactile searches were performed either by wading in an upstream direction or by snorkelling or scuba diving, drifting downstream, depending on the water depth of each stream.
Thick-shelled River Mussels, Unio crassus. Life Unio.
In areas with at least 10 Mussels per metre of stream length, at least 100 Mussels were removed from the sediment to determine their length and age. The age of the Mussels was assessed: (i) by counting the annual rings in the shells of Unio crassus; and (ii) by measuring the total length with a caliper in Margaritifera margaritifera and determining approximate ages from pre-determined age–length relationships. As the shells of Margaritifera margaritifera grow very slowly and have a dark black colour, age determination by counting the annuli is rarely possible. Therefore, the length of the Mussels was measured to distinguish between juvenile (under 65 mm) and adult Mussels. All live Mussels were returned to the river in the approximate locations where they were found. In populations with low numbers (less than 100 individuals), age structure was not determined.
Physicochemical habitat characteristics were analysed at 290 sites (5–10 sites per stream, depending on the length of the populated stretch). The sites were randomly selected and distributed across the length of each study stream. Electrical conductivity, dissolved oxygen concentration value, and temperature were measured using a handheld Multi 3430 multiparameter meter and a pH 3110 portable pH meter, with one measurement taken per site. Turbidity was measured using a Turb355 T; turbidity meter.
For water quality analysis, three replicate water samples per stream were collected from free-flowing water. A volume of 50 ml was taken and stored on ice until further processing with ion chromatography.
Flow velocity was measured with a HFA handheld flow meter at 50% water depth. Substratum texture was analysed at three sites per study stream using a box sampler. This collects the uppermost 10 cm of the substratum; it has a rectangular opening of 16.0 cm × 12.2 cm and a length of 29.3 cm. The box sampler is equipped with an adjustable metal plate on each side to ensure sampling from a well-defined substratum depth. Its use is similar to a bulkcore sampler. Grain sizes were fractioned with a Fritsch wet-sieving tower and different mesh sizes (63.0, 20.0, 6.3, 2.0, and 0.85 mm). The fractions retained on each sieve were dried at 100 °C and weighed to the nearest gram. The percentage of each grain fraction was determined, but considering the restricted grab-sample volumes, the largest fraction of over 20 mm was generally excluded from further analyses.
Redox potential was measured both in the free-flowing water and in the interstitial zone to determine the hydrological exchange of water (and oxygen) between the two compartments. The redox potential was first measured in free-flowing water and then at a depth of 10 cm into the substratum. Values above 300 mV imply oxic conditions, whereas values below indicate anoxia.
If recent data (less than 2 years old) from State Fish Monitoring by the Fachberatung fuer Fischerei – Bezirk Niederbayern and the Fachberatung fuer Fischerei – Bezirk Oberfranken on Fish populations were unavailable, electrofishing was conducted to assess host Fish availability and abundance in the streams. Fish populations were sampled with an Efko FEG 1500 1.5-kW portable electrofishing backpack unit, wading in an upstream direction with a single anode following the German standard. The area covered by electrofishing varied between 5 and 10% of the length of the river stretch that was populated by the Mussels. The stunned Fish were collected with a dip net and kept in plastic tanks with a permanent oxygen supply. After species determination and length measurements, all fish were released into the same stretch of stream from which they were sampled. Species richness and host Fish density were calculated for each stream.
To identify the main threats to Mussel populations, a qualitative assessment was conducted in each section between two transects, evaluating the following criteria: land use in the catchment area, diffuse input, pollution/water quality, indicators of predation, river maintenance, weirs, and pearl fishing. The extent of each threat was categorized in the following three classes: (i) not observed; (ii) weak, but detectable impact; and (iii) severe impact.
The monitoring results were used to classify the mussel populations and their habitats. Quantitative and qualitative parameters were recorded in an evaluation matrix following the national assessment system. Each parameter was categorized as (A) ‘good’, (B) ‘moderate’, or (C) ‘poor’. The worst score of the corresponding subcategories determined the overall assessment of habitat quality and mussel population. Data analyses were carried out with RSTUDIO 1.0.143.
Margaritifera margaritifera population size ranged from under100 to around 35 000 individuals, In three streams (15% of those examined) with previously known populations, no living individuals were detected. The mean population size of all pearl mussel streams was 3517 individuals. In 90% of the Margaritifera margaritifera populations, the population size was smaller than 10 000 individuals. Size estimates for Unio crassus populations ranged from under 100 to around 40 000 individuals, with an overall mean population size of 5566 individuals. In 92% of the studied Unio crassus populations, the population size was smaller than 10 000 individuals.
In nine Margaritifera margaritifera populations, sufficient numbers of individuals were obtained for the compilation of age profiles. The percentage of juvenile mussels (individuals under 65 mm) in the populations was very low (mean 2.2%), indicating that there has been no significant recruitment for at least 25 years. In contrast, the proportion of juvenile Mussels in Unio crassus populations was considerably higher, with a mean of 41.4%. In one population, the proportion of juvenile Mussels exceeded 90%, which results from a lack of adult age classes.
None of the Mussel populations investigated was assessed with status (A). Instead, small population size and insufficient recruitment resulted in 86% of the Margaritifera margaritifera populations and 47% of the Unio crassus populations being assessed with the lowest status class (C).
Habitat quality in Margaritifera margaritifera streams was assessed as moderate, category (B), in 24% of the streams and as bad, category (C), in 76% of the streams. In the case of Unio crassus, 7% of the streams were assessed as good, 33% as moderate, and 60% as bad in terms of habitat quality.
Fish species richness was higher in Unio crassus streams (total number of species, 28) compared with Margaritifera margaritifera streams (total number of species, 23). For both Mussel species, overall Fish species richness was higher in streams with Mussel recruitment (total number of Fish species, 28 in Unio crassus streams and 21 in Margaritifera margaritifera streams) than in streams without recruitment (total number of Fish species, 11 in Unio crassus streams and 16 in Margaritifera margaritifera streams). The average Fish species richness was similar, with 5.9 in Margaritifera margaritifera and 6.4 in Unio crassus streams. The mean density of primary hosts of Unio crassus (Three Spikes Stickleback, Gasterosteus aculeatus, Common Minnow Phoxinus phoxinus, and Common Chub, Squalius cephalus) ranged between 1.0–87.5 individuals per 100 m². The mean density of Brown Trout, Salmo trutta fario, the only host of Margaritifera margaritifera occurring in the study streams, ranged between 0.1 and 133.3 individuals per 100 m².
The Common Chub, Squalius cephalus, a host species for the larvae of the Thick-shelled River Mussel, Unio crassus. Wikimedia Commons.
The percentage of fine sediments of under 0.85 mm in size varied considerably between sites and ranged from 1.2 to 99.5% in Margaritifera margaritifera streams and from 0.2 to 99.7% in Unio crassus streams. On average, Margaritifera margaritifera sites contained 22.3% of particles of under 0.85 mm in size, whereas the mean proportion of fine particles in Unio crassus sites was twice as high, at 41.3%. In both species, texture analyses and habitat quality categories corresponded only weakly with each other: for Unio crassus, for example, samples of habitat category (A) could contain high quantities of fine sediment, and vice versa.
Physicochemical water quality was often beyond the threshold values defined in the literature for high-quality habitats. In particular, nutrient-related parameters such as electric conductivity, nitrate and orthophosphate concentrations were above or at least close to the limits suggested for intact Mussel habitats. For instance, median values for electric conductivity were 200 microsiemens per centimetre in Margaritifera margaritifera streams of category (B) and 142 microsiemens per centimetre in streams of category (C), compared with a threshold value of 180 microsiemens per centimetre in the literature. Mean orthophosphate concentrations in Margaritifera margaritifera habitats were 0.05 and 0.07 mg per litre for streams in categories (B) and (C). In Unio crassus streams of categories (A) and (C), the orthophosphate concentrations remained below detectable levels; in category (B) streams the mean orthophosphate concentration was 0.08 mg per litre.
The median values of turbidity were also twice as high in Margaritifera margaritifera streams of category (B) than in streams of category (C), with 9.13 Nephelometric Turbidity Units compared with 4.36 Nephelometric Turbidity Units, respectively. In both categories, values were clearly higher compared with a threshold value of 0.96 Nephelometric Turbidity Units for intact habitats. The turbidity values measured in Unio crassus streams were in a comparable range as the measurements made in Margaritifera margaritifera streams. The mean pH value in Margaritifera margaritifera streams was 7.2, and ranged between 6.5 and 7.5, except for one stream, where the pH reached a maximum of 8.1. In Unio crassus streams, the mean pH was 8.3 and ranged from 7.0 to 9.9. The oxygen content in free-flowing water was generally high, with an average of 10.0 and 9.9 mg per litre in Margaritifera margaritifera and Unio crassus streams, respectively; however, the deltas of redox potentials between free-flowing water and the interstitial zone were more pronounced in Unio crassus streams, with a mean of 229 millivolts, compared with Margaritifera margaritifera streams with a mean of 168 millivolts. Mean flow velocities ranged between 0.25 and 0.30 m s−1 in all habitat categories of both target species, although minimum and maximum values varied between 0.01 and 1.20 m per second. The mean total organic carbon in Margaritifera margaritifera streams was 5.1 mg per litre in category (B) habitats, which decreased to 4.7 mg per litre in category (C) habitats. In Unio crassus streams the total organic carbon was higher and increased in habitats from category (A) to (C), with means of 8.1, 8.1, and 11.5 mg per litre, respectively.
In Stoeckl et al.'s study, a total of 34 Freshwater Mussel populations and their habitats were assessed using the national evaluation methodology for species listed in the annexes of the European Habitats Directive. The results showed that both species, the Freshwater Pearl Mussel, Margaritifera margaritifera, as well as the Thick-shelled River Mussel, Unio crassus, have a ‘bad’ conservation status in the state of Bavaria, which is one of the core areas of their natural distribution in central Europe. Following the criteria of the evaluation protocol, none of the Mussel populations was rated to be of good status (A). With the exception of 7% of Unio crassus habitats, also almost all Mussel habitats were rated as being ‘poor’ (C) or in an ‘unfavourable’ status (B), with moderate (B) to strong threats (C) in the majority of the streams assessed.
Although the population status of both target species is comparable and both species need to be considered as endangered, there are several pronounced differences regarding the major drivers of their decline and species-specific tolerance against certain threats. Scientific research on the ecological requirements of Margaritifera margaritifera started in the 1980s and continued to receive great attention compared with other Mussel species, eventually resulting in the first European Committee for Standardization standard to provide guidance on monitoring a single species. The species has been characterised as a highly specialised inhabitant of oligotrophic gravel-bed streams with high water quality and a low content of fine sediment. The clogging of macropores in the interstitial zone by fine sediments was identified as the main reason for declining populations, resulting in recruitment failure, which is clearly supported by the results of this study. In most of the samples, the proportion of fine sediments exceeded the thresholds of 20% for particles under 1 mm and turbidity levels of 0.96 Nephelometric Turbidity Units, identified from investigations of intact habitats. At the same time, Stoeckl et al. observed a strong decline of redox potential from the free flowing water to the interstitial zone, which leads to a lack of oxygen in juvenile habitats, thus explaining the over-aged Pearl Mussel populations in the Bavarian study streams. Moreover, some water quality parameters, such as electrical conductivity or nitrate, were higher in several streams, but as this was also the case in some of the streams with recruitment, these parameters do not seem to have as great an impact as substratum quality.
In contrast to Margaritifera margaritifera, research activities targeting Unio crassus were rare until a few years ago. Until then, the habitat needs of both species were assumed to be similar. However, recent studies indicated pronounced differences in their ecological requirements: for example, in their sensitivity to fine sediments or in their general substratum preferences. Thus, in Stoeckl et al.'s study, recruitment of Unio crassus was observed in streams with a maximal proportion of particles under 0.85 mm of 99%. It is clear that there is no correlation between substratum structure and recruitment success in the Bavarian study streams. At the same time, even higher deltas of redox potentials were detected between free-flowing water and the interstitial zone in functional Unio crassus habitats than in nonfunctional Margaritifera margaritifera habitats. This may be explained by the shorter post-parasitic phase of Unio crassus or the lower oxygen demands of juveniles compared with Margaritifera margaritifera. Furthermore, Unio crassus does not only exhibit stronger resilience to anthropogenic habitat alteration, but also has a wider ecological range than Margaritifera margaritifera. For instance, Unio crassus is not restricted to silicate catchments and also occurs in, and even seems to prefer, limestone streams, which explains the stronger variation in electrical conductivity and the higher average pH values compared with the results for Margaritifera margaritifera streams.
Abiotic habitat conditions, especially substratum quality, mainly explain the decline of Margaritifera margaritifera. The status of Unio crassus is only weakly correlated with these parameters, however. In many of the Bavarian study streams the host Fish abundance appears too low to ensure sufficient recruitment. Particularly in the non-recruiting populations, densities are far below the recommended value of 40 individuals per 100 m². In contrast, host Fish abundance is sufficiently high in most of the Margaritifera margaritifera streams investigated, and higher densities of Fish in these situations can even be indicative of eutrophication and poor habitat quality for juvenile Mussels. An additional threat for Unio crassus is its occurrence in nutrient-enriched and often heavily modified habitats, or even in man-made ditches located in intensively used catchments. The increased nitrogen levels and the frequent observation of intensive agriculture without buffer strips along the streams studied pose a major threat to Bavarian Unio crassus streams. In some cases, direct disturbances such as dredging were observed, where Mussels can be physically harmed. The uniform stream channels with soft and steep banks are often inhabited by the Muskrat, Ondatra zibethicus. Particularly in winter, when herbal food is scarce, this non-native predator can significantly reduce Unio crassus populations, which has been observed in recent years by Stoeckl et al. in some of the streams studied.
The North American Muskrat, Ondatra zibethicus. An invasive introduced species that has been observed eating Freshwater Mussels in Bavaria. Gordon Robertson/Wikimedia Commons.
Despite the critically endangered status of both Mussel species and the legal requirement of all European member states to report their conservation status, no consistent methodologies or protocols have been used so far to do this. Thus, monitoring data may not be comparable across the European countries and data quality may vary considerably.
Although monitoring results of all species of European interest are available online via the European Environment Information and Observation Network platform, the methods applied for assessing species and their habitats remain unknown. With regard to the importance of data quality and comparability, we strongly suggest that common monitoring methods, such as those described in the European Committee for Standardization standard for Margaritifera margaritifera, should be developed. This standard is useful for designing national monitoring programmes in all European member states, because the countries represented by those who wrote the standard include all those in which Margaritifera margaritifera still occurs in Europe.
The examples of Margaritifera margaritifera and Unio crassus clearly show that even species with similar life cycles may have different habitat preferences and resilience against adverse habitat conditions. As a result, deducing the ecological requirements of one species based on another is probably rarely possible, and exact knowledge about ecological needs, population status, genetic structure, and the causes for decline is indispensable for the development of effective conservation strategies. Despite this, there is a lack of such basic information for the other native European mussel species. With respect to the important ecosystem services that Freshwater Mussel species provide. and the continuing loss of biodiversity, it is urgent to gather the missing information on species so far neglected through fieldwork and research. This will allow the design of species-specific conservation actions, as has been achieved for Margaritifera margaritifera, where several conservation projects around Europe apply a combination of artificial breeding and habitat restoration in prioritized target streams. Unfortunately, the annexes of the European Habitats Directive that list the species for special protection are not updated; hence, monitoring and conservation action for other endangered mussel species that are not listed on the annexes are rarely conducted because of an absence of supporting legislation. This may even result in the decline of tolerant and widely distributed species, with drastic effects on ecosystem functioning and the provision of ecosystem services. Furthermore, the conservation of habitats of those species already protected may also gain from legislative measures. Designated sites such as the Special Areas of Conservation selected for Mussel species in Bavaria are frequently too small to be effective, as in many cases the Special Areas of Conservation do not cover the catchment areas of the streams. This means that critical factors such as nutrient and sediment loads originating from the wider catchment cannot be reduced using the legal instruments of the Habitats Directive. The limited capacity of the Natura 2000 network to protect freshwater biodiversity seems to be true for other countries in the European Union: by assessing the coverage of protected areas on the Iberian Peninsula for more than 90 freshwater species it was shown by another study that the current areas of protection fail to provide sufficient coverage of freshwater biodiversity, with less than 20% of the range of species covered on average. Stoeckl et al. therefore recommend supplementing conservation projects with an expansion of nature reserves, wherever possible.
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