American eels produce and release bile acid profiles that vary across life stage.

The American eel (Anguilla rostrata) is an imperilled fish hypothesized to use conspecific cues, in part, to coordinate long-distance migration during their multistage life history. Here, holding water and tissue from multiple American eel life stages was collected and analysed for the presence, profile and concentration of bile acids. Distinct bile acid profiles were identified in glass, elver, yellow eel and silver eel holding waters using ultraperformance liquid chromatography high-resolution mass spectrometry and principal component analysis. Taurochenodeoxycholic acid, taurodeoxycholic acid, cholic acid, deoxycholic acid, taurolithocholic acid and taurocholic acid were detected in whole tissue of American glass eels and elvers, and in liver, intestine and gallbladder samples of late-stage yellow eels. Bile acids were not a major component of silver eel washings or tissue. This study is novel because little was previously known about bile acids produced and emitted into the environment by American eels. Future behavioural studies could evaluate whether any bile acids produced by American eels influence conspecific migratory behaviour.

Reestablishing a host-affiliate relationship: migratory fish reintroduction increases native mussel recruitment.

Co-extirpation among host-affiliate species is thought to be a leading cause of biodiversity loss worldwide. Freshwater mussels (Unionida) are at risk globally and face many threats to survival, including limited access to viable host fish required to complete their life history. We examine the relationship between the common eastern elliptio mussel (Elliptio complanata) and its migratory host fish the American eel (Anguilla rostrata), whose distribution in the Chesapeake Bay watershed is limited, in part, by dams. We examined population demographics of E. complanata across locations in the Chesapeake Bay watershed, primarily in the Susquehanna River in the absence of American eels, and conducted experimental restocking of eels to assess potential impacts on mussel recruitment. Compared to surveys completed ~20 yr prior, E. complanata could be experiencing declines at several historically abundant sites. These sites also had extremely limited evidence of recruitment. Restoration of host fish improved recruitment, but results were not equivalent between stocking sites, indicating that host reintroduction alone may not be fully effective in reestablishing mussel populations. One site where eels were introduced (Pine Creek, Tioga County, Pennsylvania, USA) experienced an increase from 0 juveniles found during quantitative surveys prior to eel stocking to 151 (21% of individuals collected during quantitative surveys) E. complanata juveniles found four years after stocking. A second site (Buffalo Creek, Union County, Pennsylvania) experienced a more moderate increase from 2 to 7 juveniles found during 2010 and 2014 quantitative surveys, respectively. Continued examination of other potential interacting factors affecting recruitment, including water quality or habitat conditions, is necessary to target favorable sites for successful restoration.

A tale of two rivers: implications of water management practices for mussel biodiversity outcomes during droughts.

Droughts often pose situations where stream water levels are lowest while human demand for water is highest. Here we present results of an observational study documenting changes in freshwater mussel communities in two southern US rivers during a multi-year drought. During a 13-year period water releases into the Kiamichi River from an impoundment were halted during droughts, while minimum releases from an impoundment were maintained in the Little River. The Kiamichi observed nearly twice as many low-flow events known to cause mussel mortality than the Little, and regression tree analyses suggest that this difference was influenced by reduced releases. During this period mussel communities in the Kiamichi declined in species richness and abundance, changes that were not observed in the Little. These results suggest that reduced releases during droughts likely led to mussel declines in one river, while maintaining reservoir releases may have sustained mussel populations in another.

Species traits and environmental conditions govern the relationship between biodiversity effects across trophic levels.

Changing environments can have divergent effects on biodiversity-ecosystem function relationships at alternating trophic levels. Freshwater mussels fertilize stream foodwebs through nutrient excretion, and mussel species-specific excretion rates depend on environmental conditions. We asked how differences in mussel diversity in varying environments influence the dynamics between primary producers and consumers. We conducted field experiments manipulating mussel richness under summer (low flow, high temperature) and fall (moderate flow and temperature) conditions, measured nutrient limitation, algal biomass and grazing chironomid abundance, and analyzed the data with non-transgressive overyielding and tripartite biodiversity partitioning analyses. Algal biomass and chironomid abundance were best explained by trait-independent complementarity among mussel species, but the relationship between biodiversity effects across trophic levels (algae and grazers) depended on seasonal differences in mussel species' trait expression (nutrient excretion and activity level). Both species identity and overall diversity effects were related to the magnitude of nutrient limitation. Our results demonstrate that biodiversity of a resource-provisioning (nutrients and habitat) group of species influences foodweb dynamics and that understanding species traits and environmental context are important for interpreting biodiversity experiments.

Ontogenetic Changes in Body Shape and the Scaling of Metabolic Rate in the American Eel (Anguilla rostrata).

AbstractThe body mass (M) scaling of resting metabolic rate (RMR) may vary significantly throughout ontogeny for multiple reasons that are not perfectly understood. To compare two major geometric theories of metabolic scaling, surface area (SA) theory and resource transport network (RTN) theory, we tested whether ontogenetic shifts in metabolic scaling relate to changes in body shape in the American eel (Anguilla rostrata). To do so, we compared the log-linear scaling exponents of RMR to M (bR) and M to body length (bL) in juvenile and subadult eels (glass and yellow eel life stages, respectively). Glass eels exhibited a bL>3 and bR significantly <2/3, as predicted by SA theory. Yellow eels also had a bL>3, but their bR was not significantly different from 2/3 or 3/4. We hypothesize that two developmental changes contribute to bR being higher for yellow eels: (1) a greater reliance on branchial respiration than body-surface-dependent cutaneous respiration and (2) a lower rate of thickening during subadult growth. An ontogenetic decrease in the ratio of cutaneous to gill respiration may have increased the relative importance of the physical constraints of a single-pump, closed circulatory system on the body-size-dependent rate of resource supply to metabolizing tissues (as predicted by RTN theory) in subadult eels. Future research is needed to quantify these developmental changes and their potential mechanistic effects on metabolic scaling, especially in the elver, a critical life stage between the glass and yellow eel stages, that was not analyzed in this study.

The complete maternal mitochondrial genome sequences of two imperiled North American freshwater mussels: Alasmidonta heterodon and Alasmidonta varicosa (Bivalvia: Unionoida: Unionidae).

The freshwater mussels Alasmidonta heterodon and A. varicosa historically inhabited rivers along the North American Atlantic coast from the Carolinas, U.S.A., to New Brunswick, CA. However, many populations have been extirpated, and A. heterodon is now federally listed in the U.S.A. as endangered, and both A. heterodon and A. varicosa are listed as vulnerable on the IUCN Red List. To facilitate genetic study of these species, we sequenced the complete female mitochondrial genomes of A. heterodon (15,909 bp; GenBank accession no. MG905826), and A. varicosa (15,693 bp; GenBank accession no. MG938673). Both mitogenomes contained 14 protein coding genes, 2 rRNA genes, and 22 tRNAs with the same gene order as reported for other members of the subfamily Anodontinae. When these two genomes were put into a phylogenetic context with other members of the Unionidae, they clustered together with other species in the subfamily Anodontinae, Tribe Anodontini.

Linking otolith microchemistry and surface water contamination from natural gas mining.

Unconventional natural gas drilling and the use of hydraulic fracturing technology have expanded rapidly in North America. This expansion has raised concerns of surface water contamination by way of spills and leaks, which may be sporadic, small, and therefore difficult to detect. Here we explore the use of otolith microchemistry as a tool for monitoring surface water contamination from generated waters (GW) of unconventional natural gas drilling. We exposed Brook Trout in the laboratory to three volumetric concentrations of surrogate generated water (SGW) representing GW on day five of drilling. Transects across otolith cross-sections were analyzed for a suite of elements by LA-ICP-MS. Brook Trout exposed to a 0.01-1.0% concentration of SGW for 2, 15, and 30 days showed a significant (p < 0.05) relationship of increasing Sr and Ba concentrations in all but one treatment. Analyses indicate lesser concentrations than used in this experiment could be detectable in surface waters and provide support for the use of this technique in natural habitats. To our knowledge, this is the first demonstration of how trace elements in fish otoliths may be used to monitor for surface water contamination from GW.

Context-dependent species identity effects within a functional group of filter-feeding bivalves.

We asked whether species richness or species identity contributed more to ecosystem function in a trait-based functional group, burrowing, filter-feeding bivalves (freshwater mussels: Unionidae), and whether their importance changed with environmental context and species composition. We conducted a manipulative experiment in a small river examining the effects of mussel assemblages varying from one to eight species on benthic algal standing crop across two sets of environmental conditions: extremely low discharge and high water temperature (summer); and moderate discharge and water temperature (fall). We found strong species identity effects within this guild, with one species (Actinonaias ligamentina) influencing accrual of benthic algae more than other species, but only under summer conditions. We suspect that this effect is due to a combination of the greater biomass of this species and its higher metabolic and excretion rates at warm summer temperatures, resulting in increased nitrogen subsidies to benthic algae. We also found that Actinonaias influenced the condition of other mussel species, likely through higher consumption, interference, or both. This study demonstrates that species within trait-based functional groups do not necessarily have the same effects on ecosystem properties, particularly under different environmental conditions.

RNA sequencing analysis of transcriptional change in the freshwater mussel Elliptio complanata after environmentally relevant sodium chloride exposure.

To identify potential biomarkers of salt stress in a freshwater sentinel species, we examined transcriptional responses of the common mussel Elliptio complanata to controlled sodium chloride (NaCl) exposures. Ribonucleic acid sequencing (RNA-Seq) of mantle tissue identified 481 transcripts differentially expressed in adult mussels exposed to 2 ppt NaCl (1.2 ppt chloride) for 7 d, of which 290 had nonoverlapping intervals. Differentially expressed gene categories included ion and transmembrane transport, oxidoreductase activity, maintenance of protein folding, and amino acid metabolism. The rate-limiting enzyme for synthesis of taurine, an amino acid frequently linked to osmotic stress in aquatic species, was upregulated, as was the transmembrane ion pump sodium/potassium adenosine 5'-triphosphatase. These patterns confirm a primary transcriptional response to the experimental dose, albeit likely overlapping with nonspecific secondary stress responses. Substantial involvement of the heat shock protein 70 chaperone family and the water-transporting aquaporin family was not detected, however, in contrast to some studies in other bivalves. A subset of the most significantly regulated genes was confirmed by quantitative polymerase chain reaction in an independent sample. Cluster analysis showed separation of mussels exposed to 2 ppt NaCl from control mussels in multivariate space, but mussels exposed to 1 ppt NaCl were largely indistinguishable from controls. Transcriptome-scale analysis of salt exposure under laboratory conditions efficiently identified candidate biomarkers for further functional analysis and field validation. Environ Toxicol Chem 2017;36:2352-2366. © Published 2017 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

Regional assessment of persistent organic pollutants in resident mussels from New Jersey and New York estuaries following Hurricane Sandy.

Resident mussels are effective indicators of ecosystem health and have been utilized in national assessment and monitoring studies for over two decades. Mussels were chosen because contaminant concentrations in their tissues respond to changes in ambient environmental levels, accumulation occurs with little metabolic transformation and a substantial amount of historic data were available. Mussels were collected from 10 previously studied locations approximately a year after Hurricane Sandy. Regionally, concentrations of polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) decreased significantly, while concentrations of organochlorine pesticides (OCPs) remained unchanged, and polybrominated diphenyl ethers (PBDEs) increased compared to historic concentrations. Although concentrations of PCBs, OCPs and PAHs were at or near record low concentrations, long-term trends did not change after Hurricane Sandy. To effectively measure storm-induced impacts it is necessary to understand the factors influencing changes in mussel body burdens and have a long-term monitoring network and an ability to mobilize post event.

The effects of salinity exposure on multiple life stages of a common freshwater mussel, Elliptio complanata.

There is growing concern over the effects of increased salinization on freshwater organisms, which are largely unknown for unionid mussels. Adult and larval Elliptio complanata were exposed to low-level salt concentrations to determine the effects on mussel survival, physiology, and reproduction. Adults were exposed to salt concentrations of 0 parts per thousand (ppt), 2 ppt, 4 ppt, and 6 ppt NaCl and monitored over 7 d for mortality. Treatment groups exposed to 6 ppt and 4 ppt experienced 50% mortality at day 3 and day 4, respectively, with complete mortality by day 7. No mortality was observed in the other treatments. Adults were also exposed to sublethal salinity levels of 1 ppt and 2 ppt NaCl for 4 wk to determine physiological consequences of prolonged salinity exposure. Mussels exposed to 1 ppt and 2 ppt experienced reduced metabolic rates within the first 24 h of exposure that recovered to control levels in the 1-ppt treatment within 7 d. Metabolic recovery did not occur in the 2-ppt treatment by the end of 28 d. Glochidia exposed to 3-ppt NaCl during attachment to their host fish suffered a reduction in attachment success and metamorphosis, resulting in a 10-fold reduction in the number of juveniles produced per host fish. The present study demonstrates that low levels of salt can have a dramatic effect on the reproduction, physiology, and survival of freshwater mussels.