Freshwater Mollusk Biology and Conservation 22:43–60, 2019 Ó Freshwater Mollusk Conservation Society 2019 REGULAR ARTICLE REASSESSING ENIGMATIC MUSSEL DECLINES IN THE UNITED STATES Wendell R. Haag1* 1 U.S. Forest Service, Southern Research Station, Center for Bottomland Hardwoods Research, 3761 Georgetown Road, Frankfort, KY 40601 USA ABSTRACT Freshwater mussels have disappeared from many U.S. streams since the 1960s. These declines are enigmatic: there are no clear causes and other components of aquatic communities appear unaffected. I review the characteristics, spatial occurrence, timing, and potential causes of enigmatic mussel declines. They share some or all of the following characteristics: (1) fauna-wide collapse, affecting all species; (2) recruitment failure, leading to a senescent fauna; (3) no well-documented impact sufficient to affect all species rapidly; (4) specific to mussels; (5) recent occurrence, since the 1960s; (6) rapid action, often leading to faunal collapse within 10 yr; and (7) upstream progression in some cases. Enigmatic declines are largely restricted to upland regions south of maximum Pleistocene glaciation and north or west of the Gulf and Atlantic coastal plains, and they appear restricted to small- to medium-sized streams. In contrast, mussel declines with different characteristics are reported nationwide. Their consistent characteristics, restricted spatial occurrence, and similar timing suggest that enigmatic declines represent a distinct, diagnosable phenomenon. Many commonly invoked factors are not plausible explanations for enigmatic declines, and others are vague or poorly supported. Other factors are plausible in some cases (e.g., agricultural effects) but cannot explain declines across the affected area. I identified only two factors that could broadly explain enigmatic declines: disease and introduction of Corbicula fluminea, but these factors are poorly understood. The occurrence of enigmatic declines overlies the region with the highest mussel species richness on Earth, but I believe their severity and importance are underappreciated. Streams affected by enigmatic declines are vital research and management opportunities, deserving of increased attention; I propose ways that research can be focused to rigorously evaluate the specific mechanisms for these declines. Until we understand the causes of enigmatic declines, mussel conservation in affected areas is substantially hamstrung. KEY WORDS: Unionida, conservation, extinction, disease, invasive species, sediment, fragmentation INTRODUCTION long, downward trend in mussel populations that began over The dramatic and widespread decline of North American 100 yr ago, and, as such, they are conflated with declines freshwater mussels is well recognized. Many mussel declines attributable to other, clearly supported causes. Explanations in the first half of the 20th century are clearly attributable to for enigmatic declines consist of a long list of potential threats massive habitat destruction, mainly by dams. In contrast, more or causal factors that has changed little over time. Hereafter, I recent declines are enigmatic: there are no clear causes, and refer to this body of explanations as ‘‘the conventional wisdom’’ (Table 1). Several factors in the conventional other components of the aquatic communities in these streams wisdom seem unrelated to enigmatic declines, the importance are relatively unaffected (Haag 2012). Despite more than three of many factors is untested, and the precise nature of other decades of research, we are still far from understanding the factors is unspecified. Nevertheless, much of the conventional causes of such declines. Enigmatic declines are rarely viewed wisdom has become accepted as proven fact. as distinct events; rather, they usually are considered part of a Our understanding of enigmatic declines, and mussel declines in general, has been hampered by three related issues. *Corresponding Author: [email protected] First, a lack of clarity about the characteristics of enigmatic 43 44 HAAG Table 1. The conventional wisdom: factors invoked to explain mussel declines. poundment (Taylor et al. 2001). Throughout this period, Adapted from Bogan (1993), Strayer et al. (2004), and FMCS (2016). mussels and other aquatic life also were nearly eliminated Dams and Impoundment locally by severe water pollution or other specific, documented insults (Ortmann 1909; Forbes and Richardson 1913). Dredging and channelization As late as the 1960s, many streams that escaped ‘‘Habitat degradation’’ impoundment or other severe insults continued to support ‘‘Poor land use practices’’ spectacular mussel faunas. We know about the condition of ‘‘Pollution,’’ water quality degradation, contaminants the fauna at that time in large part because of the efforts of Sedimentation two remarkable individuals, David H. Stansbery, of The Ohio Loss of riparian buffers State University, and Herbert D. Athearn, a private shell ‘‘Run-off,’’ impervious surfaces collector, both of whom collected mussels extensively across Eutrophication the eastern USA and whose large collections survive (Ohio Coal mining, oil and gas extraction State University Museum of Biological Diversity and North Exotic species Carolina Museum of Natural Sciences, respectively). These Hydrologic change and most other historical collections were not quantitative in Overharvest any sense, and they have several potential sources of bias. Lack of fish hosts; changes in fish assemblages First, sampling methods and effort are rarely recorded. Climate change Second, species that were common and widespread at the Endocrine disrupters time (e.g., Eurynia dilatata) often appear to be underrepre- Disease sented numerically in collections unlike rarer species for which most encountered individuals apparently were retained and catalogued (e.g., Epioblasma spp.). Third, many declines makes it difficult to distinguish them from other types collections came mainly from muskrat middens, which may of declines and establish their spatial distribution and timing. provide a biased depiction of the fauna that occurred at the Second, we are uncertain about whether enigmatic declines site (Tyrrell and Hornbach 1998; Owen et al. 2011). together represent a single, widespread phenomenon or a Nevertheless, these collections clearly show that abundant, collection of largely unrelated events. Third, we have failed to diverse, and largely intact mussel assemblages continued to critically evaluate the evidence for factors invoked to explain exist across much of the USA (Table 2). Furthermore, these mussel declines and thus have tended to perpetuate poorly collections often contain a wide range of age classes, supported speculation about causes (see Downing et al. 2010). including juveniles. These issues have hampered the search for causes and may Throughout this paper, I illustrate examples of enigmatic have encouraged management actions that have little chance of declines by comparing historical collections with contempo- reversing declines. rary survey data. Such comparisons must be made cautiously I provide a critical analysis of enigmatic mussel declines because of the unknown extent to which they are influenced by and the factors invoked to explain them. First, I review the sampling artifacts at different times. To minimize this characteristics of enigmatic declines and assess their spatial problem, the examples I provide consist of collections made occurrence and timing. Second, I evaluate how well the at the same locations at different times, and I used only conventional wisdom explains these declines and discuss other qualitative contemporary survey data. Contemporary qualita- potential explanations. Finally, I propose ways that mussel tive survey methods are similar to methods used by Stansbery, research and management can be focused to provide more Athearn, and others (Athearn 1969; J. Jenkinson, personal specific information about the causes of enigmatic declines communication), and Stansbery trained or advised many and more specific guidance for addressing them. contemporary mussel biologists. If anything, contemporary surveys probably are more exhaustive than historical surveys because today’s agency-supported mussel programs provide OVERVIEW OF ENIGMATIC MUSSEL DECLINES resources that were largely absent in the past (Haag and In the first half of the 20th century, a frenzy of dam Williams 2014). construction across the USA destroyed or radically altered Even considering potential sampling artifacts, collections thousands of kilometers of riverine habitat and profoundly from the 1960s contrast starkly with contemporary survey affected aquatic communities. To date, most extinctions of data. These comparisons show that the condition of the mussel North American mussel species are directly attributable to fauna in many streams has deteriorated dramatically since the habitat destruction by dams (Haag 2012). Substantial mussel 1960s. In the Red River, Tennessee, species richness declined assemblages survived in some impounded streams, but they 44% between 1966 and 1990, the total number of individuals shifted to dominance of impoundment-tolerant species and reported declined 90%, and a subsequent survey showed now bear little resemblance to the pre-impoundment fauna further deterioration (Table 2). Furthermore, the 1966 (e.g., Garner and McGregor 2001). Fish assemblages and other collection contains multiple age classes, but the 1990 survey aquatic organisms showed similar radical shifts after im- reported