Predicting climatic threats to an endangered freshwater mussel in Europe: The need to account for fish hosts

Abstract

1. The freshwater pearl mussel Margaritifera margaritifera has been suffering major population declines in Europe. This endangered species is a host specialist and exclusively requires salmonid species (Salmo trutta and Salmo salar) to complete its life cycle. In theory, obligatory biotic interactions should deserve special conservation attention, because the loss or massive decline of fish hosts may elicit the extirpation of their affiliated species. While many threats disturbing M. margaritifera are similarly affecting salmonids, climate change is particularly alarming, with the potential to significantly change the fish-mussel dynamics.2. To evaluate the importance of including the occurrence of fish hosts for predicting the distribution of M. margaritifera in Europe, three datasets were used to build species distribution models (SDMs) with a maximum entropy (MaxEnt) approach: (1) environmental variables (ENV); (2) probability of fish hosts occurrence (FH); and (3) environmental variables and probability of fish hosts occurrence (ENV + FH). We identified the environmental variables that better explain M. margaritifera distribution and modelled its current and future distribution under a suite of climate change scenarios. Furthermore, projections were used to evaluate the adequacy of current networks of European protected areas in covering the suitable habitats for M. margaritifera. 3. Results showed that incorporating data about fish hosts into M. margaritifera SDMs avoided the overprediction of geographical projections and, to a minor extent, improved model performance (area under the curve: ENV = 0.851; FH = 0.848; ENV + FH = 0.867). The distribution range of M. margaritifera in Europe | 843 da SILVa et aL.

Joint species distribution models unveil co‐occurrences between freshwater mussels and their fish hosts

“…Accordingly, A. anatina and U. delphinus can occur in most river systems, while P. littoralis occurs in middle to downstream stream sections but only in lotic stretches (Araujo et al, 2009; Lopes‐Lima et al, 2014, 2017). On the other hand, M. margarifera seemed to only occur far from cropland areas, which follows previous findings that associate this species with pristine streams with a low human disturbance within Europe (da Silva et al, 2022; Inoue et al, 2017; Lopes‐Lima et al, 2017). Furthermore, regardless of the different contribution of cropland extent for each one of these species, we found a consistent pattern across all mussels and most of the fish species inhabiting the Douro River basin, that being their negative response to this variable.…”

Applying genomic approaches to delineate conservation strategies using the freshwater mussel Margaritifera margaritifera in the Iberian Peninsula as a model

“…Peripheral populations have a high importance from a conservation point of view, as they have been considered as potential reservoirs of adaptive genetic variation, even if they usually retain low genetic diversity 62 . It is a matter of fact that genetic diversity is the basis of evolutionary change and, consequently, it is decisive for organisms to adapt to changing environmental conditions under the current global warming scenario, especially when the potential impact is significant, as is the case of M. margaritifera 16 . Even though our study supports a high differentiation among populations, it does suggest the occurrence of recent gene flow events, either through the fluvial connectivity within rivers and basins, or through past paleogeomorphological/tectonic events such as river captures.…”

“…Indeed, during the last century, its European populations have suffered an estimated decline of around 90% because of habitat loss and fragmentation, overexploitation for pearl extraction, pollution and the introduction of invasive species 8 , 13 . The decline of host fish (salmonids) in most of the rivers inhabited by the freshwater pearl mussel, especially in southern European regions 14 , 15 , could also have contributed to the decline of M. margaritifera populations and must be considered in the future trend of the species 16 . In the Iberian Peninsula, populations of this species have an additional constraint, as southern regions might be more susceptible to climatic change associated to a stronger decrease in precipitation and an increase of more unstable hydrological conditions than in northern latitudes, which has been reported as a potential extinction risk for M. margaritifera 16 .…”

Ecological marginality and recruitment loss in the globally endangered freshwater pearl mussel

“…This suggests that the optimal habitat suitability of FPM may shift to higher altitude and/or more northern areas over time and ultimately result in local extinctions and a reduced southern distribution range of FPM (Bolotov et al, 2018). A warming climate may also lead to changes in catchment processes that can have effects on hydrology, fine sediment dynamics and on the host fishes, which may all directly, indirectly and interactively affect FPM (Baldan et al, 2021; da Silva et al, 2022). The increased sediment and nutrient input predicted from global warming will lead to a decrease in the availability of interstitial oxygen, which will be particularly hazardous for juvenile mussels (Baldan et al, 2021).…”

“…In Sweden for instance, about 30% of all populations are believed to have become extinct since the beginning of the 20th century and out of the remaining populations only 50% are expected to be viable (ongoing recruitment as indicated by the presence of mussels that are less than 50 mm and approximately 20‐year‐old) (Arvidsson et al, 2012). Yet, despite previous attempts to identify environmental conditions that may explain the presence of FPM populations using SDMs (Baldan et al, 2020; da Silva et al, 2022; Lois et al, 2015; Prié et al, 2014; Wilson et al, 2011), none have incorporated mussel recruitment status in their analyses, which have constrained conclusions regarding differential sensitivity to various environmental disturbances that may impact recruitment. Moreover, due to the extreme longevity of FPM this system offers a unique, but overlooked, opportunity to gain novel insights on the consequences on biodiversity of long‐term and gradual changes in environmental conditions.…”