Multiple stressors and recruitment failure of long-lived endangered freshwater mussels with a complex life cycle

Abstract

Multiple stressors can interactively affect the population of organisms; however, the process by which they affect recruitment efficiency remains unclear for empirical populations. Recruitment efficiency can be regulated at multiple stages of life, particularly in organisms with complex life cycles. Understanding the interactive effects of multiple stressors on recruitment efficiency and determining the bottleneck life stages is imperative for species conservation. The proportion of <20-year-old juveniles of the endangered freshwater pearl mussel Margaritifera togakushiensis, which has an obligate parasitic larval stage, was investigated in 24 rivers from eastern Hokkaido, northern Japan to reveal the influence of nutrients, fine sediment, and their combined effects on juvenile recruitment efficiency. The following indices for recruitment at adult, parasitic, and post-parasitic juvenile stages were obtained from 11 of these rivers: gravid female density, glochidia density (the number of glochidia infections per stream area), and juvenile survival rate. This study explored the bottleneck stages of recruitment efficiency and the interactive effects of the two stressors on these stages. Twenty-four population status assessments determined that the proportion of juveniles ranged from 0.00 to 0.53, and juveniles were absent from four rivers. The results showed that the parasitic and post-parasitic juvenile stages were bottlenecks for recruitment efficiency. Juvenile survival rates had a more significant positive effect on recruitment efficiency in rivers with a high glochidia density. Juvenile survival rate was decreased by the synergistic interaction of nutrients and fine sediment, although factors limiting glochidia density were not found. The nutrient concentration of rivers in the study region was well explained by the proportion of agricultural land cover and urban areas in the watersheds, but no relationship was detected between fine sediment abundance and land use. This study suggests that nutrient management at a catchment scale can be effective for re-establishing the recruitment of M. togakushiensis, particularly in rivers with a high content of fine sediments. The results also emphasise the importance of considering both parasitic and post-parasitic juvenile stages of mussels to maximise the positive effects of stressor mitigation.

Does winterkill explain contrasting demographics of winter-breeding freshwater mussel populations in Ishikari River floodplain?

“…Under such conditions, a chain of adult abundance decreases in winter, high mortality of gravid mussels and newly born juveniles occurs in summer, and population size decreases with a lack of juveniles at annual or longer timescales. Recent studies have indicated that multiple stressors can limit the community structure, distribution, and reproduction of freshwater species, including freshwater mussels, in complex ways (Birk et al, 2020;Miura et al, 2023a). Our findings extend the multiple-factor paradigm and underscore the importance of considering survival limitation factors acting at multiple life stages of freshwater mussels at different times of the year.…”

“…One of the most prevalent signs of population decline in freshwater mussels is the cessation of their reproduction, which can often be reflected in disproportionately fewer juveniles in population demography and small population sizes (i.e., abundance) (Österling et al, 2010;Negishi & Kayaba, 2010). Efforts have been made to identify how population decline and reproduction cessation occur by examining single or multiple life-history stages of species in relation to various external environmental factors (Geist et al, 2006;Österling et al, 2010;Strayer & Malcom, 2012;Tremblay et al, 2016;Brian et al, 2021;Miura et al, 2023a). Furthermore, as intrinsic properties of mussels, demographics, including size frequency, age structure, sex ratios, and survival rates, are among the key parameters in inferring impaired populations and projecting how and whether the populations would change in the future (Ferreira-Rodríguez et al, 2019).…”

Recruitment status and host-fish-limitation threats to endangered freshwater pearl mussel (Margaritifera laevis) in eastern Hokkaido, northern Japan

“…In the next step, other limiting factors of M. laevis recruitment and their relative importance should be determined in detail to recover M. laevis recruitment more effectively. In particular, the post-parasitic juvenile stage could also be a bottleneck for freshwater mussel recruitment together with the parasitic stage (Miura et al 2021a). Evaluating the performance of this stage and its bottleneck factors is especially important for improving M. laevis recruitment.…”

“…Margaritifera kurilensis (Zatravkin & Starobogatov, 1984) also occurred at study sites (Miura et al, 2019b). Margaritifera kurilensis has a different reproductive season (March to May) and suitable host-fish species (white-spotted char Salvelinus leucomaenis leucomaenis (Pallas, 1814) and perhaps Dolly Varden char S. malma krascheninnikovi Taranetz, 1933) with M. laevis (Kobayashi and Kondo 2009;Miura et al 2021a).…”