Population trends and ecological community interactions of freshwater mussels

Abstract

Freshwater mussels (order Unionida) are a globally widespread taxon which have been described as ecosystem engineers due to their capacity to modify freshwater habitats and facilitate other taxa, with effects on wider biodiversity. At the same time, freshwater mussels rank among the most threatened taxa globally. As a result, building a better understanding of mussel population dynamics and the interactions of mussels with other taxa is important to understanding potential impacts on freshwater ecosystems in the era of anthropogenic global environmental change. This thesis addresses three broad questions. First, I ask how mussel populations are changing over time and in response to anthropogenic ecosystem alteration, addressed in Chapters 2 and 3. Secondly, I investigate the ways freshwater mussels affect wider freshwater communities, discussed in Chapters 4-6. Finally, in Chapters 5 and 6 I consider the possible implications of changes to mussel populations for freshwater communities. I begin by exploring the changes that have occurred in freshwater mussel populations in southern England over the long and short term, using a variety of evidence types. In Chapter 2 I compare archaeological mussel shells from a Bronze Age site to modern populations. I show that present-day mussels grew faster and with more year-to-year variation than Bronze Age equivalents, and showed differences in δ18O and δ13C isotopic composition indicative of anthropogenic changes to habitats, in particular a shift to a deeper and more regulated waterway and a possible influence of elevated nutrient inputs. The now-Vulnerable Pseudanodonta complanata also appears to have been lost from the site. In Chapter 3 I further investigate historical changes to mussel populations, revisiting a study of mussel populations in the River Thames, one of the earliest studies to quantify mussel population dynamics. I show that mussel population density has fallen dramatically across nearly all species, with declines of over 95% in both Anodonta anatina and Unio pictorum; once more Pseudanodonta complanata appears to have been lost. Here too I show changes to mussel growth rates likely linked to anthropogenic nutrient enrichment, although in the opposite direction – mussel growth rates are now significantly lower than those recorded in the 1960s, which may reflect declining nutrient loading associated with improvements in sewage treatment. I then address the role of mussels as ecosystem engineers in shaping wider ecological communities, with a focus on benthic macroinvertebrates. In Chapter 4 I analyse the associations between two mussel species, Lamellidens marginalis and Indonaia (Parreysia) caerulea, and macroinvertebrate families in a lake in central Dhaka, Bangladesh. I show associations between mussels and invertebrates for the larger, more abundant Lamellidens but not the rarer Parreysia, with which it was negatively associated. Lamellidens density was associated with community composition, such that sites with higher mussel density had invertebrate communities which more strongly resembled one another. Lamellidens was also positively correlated with the scraper and predator functional feeding groups and associated taxa, lending support to the idea that mussels can structure freshwater communities. In Chapter 5 I link the themes of mussel declines and ecosystem engineering by comparing mussel and invertebrate populations in the same lake in Bangladesh in 2010 and 2023. I show that even in this short timescale mussel populations have again declined by around 90%. Invertebrate diversity and abundance also fell, and at the much lower mussel population densities now observed there were no significant relationships between mussels and invertebrate community composition. At the same time, in a broader survey of mussels in lakes across Dhaka, I show that rarer species appear to have declined or been lost from multiple locations, being represented in samples by shells but no live individuals. Finally, in Chapter 6 I test the association between mussels (native Unio tumidus) and invertebrates experimentally, as well as examining how this relationship is impacted by several conservation-relevant factors – unionid mussel density, the presence of live mussels versus empty shells, and the effect of invasive zebra mussels, Dreissena polymorpha. I find that while unionid mussel density and zebra mussels presence did not have any significant effect on invertebrate communities in this experiment, the presence of live Unio tumidus increased invertebrate abundance, while the presence of shells reduced diversity, a potentially important effect given that mussel die-offs often lead to large assemblages of empty shells. Community composition also differed between shell, live and control enclosures, and live Unio tumidus was associated with greater abundance of the predator and collector functional groups. Taken together these studies provide insights into the effects of anthropogenic environmental change on freshwater mussels, with impacts ranging from the individual level (altered growth rates in response to nutrient enrichment) to the population level (loss of rare species and declines in density of common ones). I also suggest how these impacts might extend to wider freshwater ecosystems, showing that mussels can shape benthic invertebrate communities, but that this effect is species- and context-dependent, and can be lost with mussel decline or die-offs. This highlights the importance of collecting data to enable a better understanding of the population trajectories of overlooked and common species, which may be undergoing catastrophic declines, as well as of conserving ecosystem engineers like freshwater mussels to mitigate against cascading effects on wider biodiversity.