Wendell R. Haag

Biodiversity on the brink: an assessment of conservation strategies for North American freshwater mussels

The North America freshwater mussel fauna has suffered an inordinately high recent extinction rate, and the small size and isolation of many remaining populations portends a continued diminishment of this fauna. Causes of extinction and imperilment are varied but revolve around massive habitat loss, deterioration, and fragmentation. The National Strategy for the Conservation of Native Mussels, published in 1997, has guided efforts to address this crisis. Considerable progress has been made toward several of the Strategies’ goals, particularly increasing our knowledge of mussel biology, promoting mussel conservation, and development of techniques for captive mussel propagation. However, mussel conservation should focus more directly on reducing fragmentation through bold and aggressive habitat restoration. In addition to dam removal, improvement in dam tailwater flows, and restoration of channelized streams, identification of factors that eliminated mussels from many otherwise intact streams is critical. Translocation and captive propagation will be key elements in reestablishing mussel assemblages in restored habitats, but these techniques should be used with caution and primarily to increase the occurrence of a species throughout its historical range. Conserving mussel diversity in an ever-changing world is dependent on promoting the natural, long-term sustainability and evolutionary potential of mussel populations.

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 organisms 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.

Pervasive Hydrologic Effects on Freshwater Mussels and Riparian Trees in Southeastern Floodplain Ecosystems

We present long-term growth trends for 13 freshwater mussel species from two unregulated rivers and one regulated river in the southeastern U.S. Coastal Plain. We also collected baldcypress (Taxodium distichum (L.) Rich.) tree cores adjacent to mussel collection sites in one river and directly compared tree and mussel chronologies in this river. To extend our analysis spatially, we examined published baldcypress chronologies from six other unregulated rivers throughout the region. Biochronologies were developed using standard dendrochronology techniques and we explored relationships between annual growth and a suite of streamflow variables in each river. Growth of mussels in unregulated rivers was negatively correlated with annual flood pulse count and May and June discharge, but positively correlated with annual low pulse count and annual number of hydrographic reversals. Baldcypress growth in unregulated rivers was positively correlated with May and June discharge and negatively correlated with annual low pulse count. Mussel growth in the regulated river was not correlated with any streamflow variable suggesting that biological rhythms are decoupled from hydrologic variations in this system. This study shows how interannual variability in streamflow can benefit diverse taxa in floodplain rivers over long periods and how river regulation can disrupt these relationships.

Spatio-temporal patterns of the decline of fresh water mussels in the Little South Fork Cumberland River,USA

The Little South Fork Cumberland River, Kentucky and Tennessee, USA, was a globally important conservation refugium for freshwater mussels (Mollusca: Unionidae) because it supported an intact example (26 species) of the unique Cumberland River mussel fauna including imperiled species. We used previous surveys and our 1997–1998 survey to reconstruct the historical fauna, to describe spatio-temporal patterns of density and number of species, and to evaluate the probable sequence and cause of observed mussel declines. We were specifically interested in better understanding how mussel assemblages respond to chronic disturbances, and how these changes manifest in persistence patterns. Density and numbers of species declined steadily from 1981 to 1998, but declines occurred first in the lower river (early 1980s), followed by declines in the upper river (late 1980s to early 1990s). Of the total species recorded from the Little South Fork, 17 (65%) are seemingly extirpated and five others appear near extirpation. Declines are associated with at least two, temporally distinct major insults. Lower river declines are associated with surface mining, whereas, oil extraction activities are implicated in upper river declines. Regardless of causal factors, species persistence was primarily a function of predecline population size with only the most numerous and widespread species surviving. At this time, the river appears lost as a conservation refugium for mussels despite its remoteness, predominantly forested watershed, and several layers of existing statutory and regulatory environmental safeguards. We suggest that the river could be restored and mussels reintroduced if an interagency task force is formed to identify and mitigate specific stressors now affecting most mussel species in the river.

High suspended solids as a factor in reproductive failure of a freshwater mussel

Abstract. Elevated suspended solids are a widespread stressor of aquatic ecosystems, but their effects on growth and reproduction in freshwater mussels are largely unknown. We fertilized experimental ponds to create a gradient in total suspended solids (TSS) and examined the effects of TSS on growth, nutritional status, reproduction, and clearance rate in Ligumia subrostrata. The number of females that became gravid declined sharply with increasing TSS, and no gravid females were found in the highest TSS treatments. The proportion of gravid females was not related to the TSS organic∶inorganic ratio. Fertilization was an all-or-nothing phenomenon. In all females that did become gravid, 98 to 99% of eggs were fertilized regardless of TSS, and total fecundity was unrelated to TSS. Clearance rates declined sharply as TSS increased but showed a threshold relationship in which clearance was uniformly low at TSS > ∼8 mg/L. Reproductive failure probably was not caused by poor body condition or nutritional status because growth (length and mass) and energetic status (measured as caloric density) were not related to TSS. We propose 2 mechanisms that implicate interference of TSS with fertilization as the cause of reproductive failure. Reduced clearance rate could decrease the chance of females encountering suspended sperm during filter feeding, or an increase in pseudofeces production could bind sperm in mucus and lead to its egestion before fertilization. Interruption of fertilization coincident with high TSS is a potential mechanism to explain the lack of mussel recruitment in many locations. Monitoring and reduction of TSS, especially during the spawning season, may help create conditions necessary for maintenance and recovery of mussel populations. More research is needed to explore the generality of this pattern across a broad range of mussel species including those adapted to lotic environments or that use different brooding strategies.

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.

Effects of temperature and photoperiod on lure display and glochidial release in a freshwater mussel

Abstract Freshwater mussels use an array of strategies to transfer their parasitic larvae (glochidia) to fish hosts. We examined the effects of temperature, photoperiod, and female gravidity on mantle lure display and conglutinate release by Ligumia subrostrata (Say, 1831) in 2 laboratory experiments. In the 1st experiment, we examined the use of these strategies in 4 temperature treatments (5, 15, 25, 35°C) and 3 photoperiods (10∶14, 12∶12, and 14∶10 h light∶ dark). In the 2nd experiment, we observed infection strategies under ambient conditions with flow-through pond water. Water temperature appeared to be the primary cue governing use of these strategies. Lure display occurred over a protracted period, but the highest display frequency occurred between ∼11 and 20°C. Lure display declined rapidly above this range and ceased altogether >28°C. Release of conglutinates increased coincident with the decrease in lure display but, at ambient temperatures, occurred over a protracted period similar in duration to lure display. Females that were not gravid at the beginning of the experiment did not display lures, and gravid females whose gills were flushed of glochidia displayed for only a short period during which frequency of display was much lower than gravid individuals. Ligumia subrostrata exhibits a temperature-mediated switch between alternate host strategies. We present evidence that lure display is a primary strategy for host infection and conglutinate release is a secondary, bet-hedging strategy to reduce wastage of glochidia that ultimately must be cleared from the gills at the end of the reproductive season.

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

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.

Age and Growth in the Australian Freshwater Mussel, Westralunio carteri, with an Evaluation of the Fluorochrome Calcein for Validating the Assumption of Annulus Formation

Abstract: Growth and longevity of freshwater mussels (Unionida) are important for defining life-history strategies and assessing vulnerability to human impacts. We used mark—recapture and analysis of shell rings to investigate age and growth of the hyriid, Westralunio carteri, at 5 sites in southwestern Australia. We tested the utility of the in situ marker calcein for validating the assumption of annulus formation in adults. Calcein was incorporated into the shells of all recovered individuals, but it provided an interpretable reference mark in only 4 of 16 individuals. These 4 individuals produced 1 shell ring subsequent to the mark, supporting the assumption of annulus production during the austral winter. Maximum age ranged among populations from 36 to 52 y and maximum size ranged from 72.9 to 82.8 mm. Mean age and length did not differ between sexes, and growth trajectories differed between sexes at only 1 site. Estimates of growth measured by the von Bertalanffy growth constant, K, ranged from 0.021 to 0.336 among sites. Estimates from mark—recapture experiments were 20 to 52% lower than values from shell annuli at all sites except 1 where K from shell annuli was ∼½ that estimated from mark—recapture. Both methods showed a positive relationship between K and mean water temperature among sites, suggesting a role of riparian shading in regulating stream temperature, and hence, indirectly influencing mussel growth. Mussel growth and mean N or P concentrations were not related among sites, but total N at the site with highest mussel growth was >2× higher than at any other site. Westralunio carteri is a long-lived, slow-growing bivalve. Maximum age, K, and probable age at maturity (4–6 y) are similar to other slow-growing freshwater bivalve groups. This suite of life-history traits is considered an adaptation for stable aquatic habitats. Therefore, W. carteri can be expected to adapt poorly to human impacts, such as riparian clearing and water extraction, which increase the temporal variability of environmental conditions in streams.