A test of the loose-equilibrium concept with long-lived organisms: Evaluating temporal change in freshwater mussel assemblages.

The loose-equilibrium concept (LEC) predicts that ecological assemblages change transiently but return towards an earlier or average structure. The LEC framework can help determine whether assemblages vary within expected ranges or are permanently altered following environmental change. Long-lived, slow-growing animals typically respond slowly to environmental change, and their assemblage dynamics may respond over decades, which transcends most ecological studies. Unionid mussels are valuable for studying dynamics of long-lived animals because they can live >50 years and occur in dense, species-rich assemblages (mussel beds). Mussel beds can persist for decades, but disturbance can affect species differently, resulting in variable trajectories according to differences in species composition within and among rivers. We used long-term data sets (10-40 years) from seven rivers in the eastern United States to evaluate the magnitude, pace and directionality of mussel assemblage change within the context of the LEC. Site trajectories varied within and among streams and showed patterns consistent with either the LEC or directional change. In streams that conformed to the LEC, rank abundance of dominant species remained stable over time, but directional change in other streams was driven by changes in the rank abundance and composition of dominant species. Characteristics of mussel assemblage change varied widely, ranging from those conforming to the LEC to those showing strong directional change. Conservation approaches that attempt to maintain or create a desired assemblage condition should acknowledge this wide range of possible assemblage trajectories and that the environmental factors that influence those changes remain poorly understood.

Freshwater mussel conservation: A global horizon scan of emerging threats and opportunities.

We identified 14 emerging and poorly understood threats and opportunities for addressing the global conservation of freshwater mussels over the next decade. A panel of 17 researchers and stakeholders from six continents submitted a total of 56 topics that were ranked and prioritized using a consensus-building Delphi technique. Our 14 priority topics fell into five broad themes (autecology, population dynamics, global stressors, global diversity, and ecosystem services) and included understanding diets throughout mussel life history; identifying the drivers of population declines; defining metrics for quantifying mussel health; assessing the role of predators, parasites, and disease; informed guidance on the risks and opportunities for captive breeding and translocations; the loss of mussel-fish co-evolutionary relationships; assessing the effects of increasing surface water changes; understanding the effects of sand and aggregate mining; understanding the effects of drug pollution and other emerging contaminants such as nanomaterials; appreciating the threats and opportunities arising from river restoration; conserving understudied hotspots by building local capacity through the principles of decolonization; identifying appropriate taxonomic units for conservation; improved quantification of the ecosystem services provided by mussels; and understanding how many mussels are enough to provide these services. Solutions for addressing the topics ranged from ecological studies to technological advances and socio-political engagement. Prioritization of our topics can help to drive a proactive approach to the conservation of this declining group which provides a multitude of important ecosystem services.

Freshwater mussel shells (Unionidae) chronicle changes in a North American river over the past 1000years.

The Illinois River was substantially altered during the 20th century with the installation of navigational locks and dams, construction of extensive levee networks, and degradation of water quality. Freshwater mussels were affected by these changes. We used sclerochronology and stable isotopes to evaluate changes over time in age-and-growth and food sources for two mussel species: Amblema plicata and Quadrula quadrula. Specimens were collected in years 1894, 1897, 1909, 1912, 1966, and 2013, and archeological specimens were collected circa 850. The von Bertalanffy growth parameter (K) was similar between 850 and 1897, but it increased by 1912 and remained elevated through 2013. Predicted maximum size (Linf) increased over the past millennium, and 2013 individuals were over 50% larger than in 850. Growth indices showed similar patterns of continual increases in growth. Shells were enriched in 13C and 15N during the 20th century, but exhibited a partial return to historical conditions by 2013. These patterns are likely attributable to impoundment, nutrient pollution and eutrophication beginning in the early 20th century followed by recent water quality improvement.

The role of host abundance in regulating populations of freshwater mussels with parasitic larvae.

Host-parasite theory makes predictions about the influence of host abundance, competition for hosts, and parasite transmission on parasite population size, but many of these predictions are not well tested empirically. We experimentally examined these factors in ponds using two species of freshwater mussels with parasitic larvae that infect host fishes via different infection strategies. For both species, recruitment and larval survival were positively related to host abundance, but there was no apparent minimum host threshold and positive population growth occurred when an average of one fish per mussel was present. Recruitment increased rapidly with an initial increase in host abundance but appeared to approach an asymptote at moderate host abundance. Recruitment and larval survival did not differ according to whether mussel species occurred alone or in combination, providing no evidence for competition for hosts via acquired immunity. However, larval survival of the species that attracts hosts with a lure was higher than the species that infects hosts passively, but lower survival of the latter strategy was offset by higher fecundity, which resulted in comparable recruitment between the two species. The lack of evidence for competition for hosts or host saturation suggests that mussel recruitment is limited primarily by fecundity and larval transmission efficiency. Despite the lack of a minimum host abundance threshold, high variation in recruitment in all treatments suggests that population growth at low host abundance is limited by stochasticity. These results show that host-parasite interactions in natural situations may differ substantially from predictions based on models or laboratory findings.

The role of fecundity and reproductive effort in defining life-history strategies of North American freshwater mussels.

Selection is expected to optimize reproductive investment resulting in characteristic trade-offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life-history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life-history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life-history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life-history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade-off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade-off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life-history strategies. Combined with trade-offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r-selected species (e.g. tribe Anodontini and some Lampsilini) to K-selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life-history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.

Growth and longevity in freshwater mussels: evolutionary and conservation implications.

The amount of energy allocated to growth versus other functions is a fundamental feature of an organism's life history. Constraints on energy availability result in characteristic trade-offs among life-history traits and reflect strategies by which organisms adapt to their environments. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems but little is known about their growth and longevity. Generalized depictions of freshwater mussels as 'long-lived and slow-growing' may give an unrealistically narrow view of life-history diversity which is incongruent with the taxonomic diversity of the group and can result in development of inappropriate conservation strategies. We investigated relationships among growth, longevity, and size in 57 species and 146 populations of freshwater mussels using original data and literature sources. In contrast to generalized depictions, longevity spanned nearly two orders of magnitude, ranging from 4 to 190 years, and the von Bertalanffy growth constant, K, spanned a similar range (0.02-1.01). Median longevity and K differed among phylogenetic groups but groups overlapped widely in these traits. Longevity, K, and size also varied among populations; in some cases, longevity and K differed between populations by a factor of two or more. Growth differed between sexes in some species and males typically reached larger sizes than females. In addition, a population of Quadrula asperata exhibited two distinctly different growth trajectories. Most individuals in this population had a low-to-moderate value of K (0.15) and intermediate longevity (27 years) but other individuals showed extremely slow growth (K = 0.05) and reached advanced ages (72 years). Overall, longevity was related negatively to the growth rate, K, and K explained a high percentage of variation in longevity. By contrast, size and relative shell mass (g mm⁻¹ shell length) explained little variation in longevity. These patterns remained when data were corrected for phylogenetic relationships among species. Path analysis supported the conclusion that K was the most important factor influencing longevity both directly and indirectly through its effect on shell mass. The great variability in age and growth among and within species shows that allocation to growth is highly plastic in freshwater mussels. The strong negative relationship between growth and longevity suggests this is an important trade-off describing widely divergent life-history strategies. Although life-history strategies may be constrained somewhat by phylogeny, plasticity in growth among populations indicates that growth characteristics cannot be generalized within a species and management and conservation efforts should be based on data specific to a population of interest.