Reproductive health and endocrine disruption in smallmouth bass (Micropterus dolomieu) from the Lake Erie drainage, Pennsylvania, USA

Smallmouth bass Micropterus dolomieu were sampled from three sites within the Lake Erie drainage (Elk Creek, Twentymile Creek, and Misery Bay, an embayment in Presque Isle Bay). Plasma, tissues for histopathological analyses, and liver and testes preserved in RNALater® were sampled from 30 smallmouth bass (of both sexes) at each site. Liver and testes samples were analyzed for transcript abundance with Nanostring nCounter® technology. Evidence of estrogenic endocrine disruption was assessed by the presence and severity of intersex (testicular oocytes; TO) and concentrations of plasma vitellogenin in male fish. Abundance of 17 liver transcripts associated with reproductive function, endocrine activity, and contaminant detoxification pathways and 40 testes transcripts associated with male and female reproductive function, germ cell development, and steroid biosynthesis were also measured. Males with a high rate of TO (87–100%) and plasma vitellogenin were noted at all sites; however, TO severity was greatest at the site with the highest agricultural land cover. Numerous transcripts were differentially regulated among the sites and patterns of transcript abundance were used to better understand potential risk factors for estrogenic endocrine disruption. The results of this study suggest endocrine disruption is prevalent in this region and further research would benefit to identify the types of contaminants that may be associated with the observed biological effects.

Ecological genomics of divergence, admixture, and fitness in the smallmouth bass (Micropterus dolomieu)

The Smallmouth Bass (Micropterus dolomieu) is one of the most highly targeted sport fishes in the world. Anglers vie for the opportunity to catch Smallmouth Bass recreationally and competitively, spending billions of dollars every year on travel, equipment, and conservation permits. Along with their extreme popularity, they are of central importance in their native ecosystems throughout central and eastern North America. They are voracious apex predators, controlling top-down food web dynamics among fishes and invertebrates in both streams and natural lakes, and they act as obligate hosts in the life cycles of several freshwater mussels. A great deal is known about the general ecology of Smallmouth Bass and their role in aquatic communities across their extensive native distribution. Much less is known about levels and distribution of diversity within the species. In 1940, Carl Hubbs and Reeve Bailey published descriptions of two distinct subspecies: the Northern Smallmouth Bass (M. d. dolomieu), inhabiting the central and eastern portion of the range, and the Neosho Smallmouth Bass (M. d. velox), which is range-restricted to the Arkansas River Basin in the Central Interior Highlands. While the subspecies classification was largely accepted among taxonomists, it was predicated on only a few subtle morphological traits, including differences in coloration, body size, and the presence of glossohyal teeth. Researchers began to investigate genetic divergence among Smallmouth Bass populations at the end of the twentieth century. Some genetic structure has been detected, but the overall diversity and the evolutionary forces generating contemporary patterns have been considered extremely complex and therefore unresolved, especially where the Neosho and Northern subspecies ranges meet in the Central Interior Highlands. To address the need for a robust understanding of the divergence and evolution history of Smallmouth Bass in the Central Interior Highlands, I addressed three broad areas concerning the phylogeography and conservation of the species using a combination of morphological, genetic, and genomic data: 1) patterns of genetic and morphological differentiation between the Neosho and Northern Smallmouth Bass subspecies, 2) lineage diversification and the extent and origins of admixture within the subspecies, and 3) effects of admixture on individual growth and fitness in two streams within the Neosho Smallmouth Bass native range. Using neutral microsatellite markers and a combination of three independent Bayesian analysis methods, I detected complex and hierarchical population structure of Smallmouth Bass in the Central Interior Highlands. The broadest level of structure indicated two distinct genetic clusters corresponding to the Neosho and Northern subspecies, but with substantial and heterogenous patterns of admixture within some streams in the Neosho native range. At finer levels of structure, clusters corresponded to river drainages and to potentially distinct populations within drainages. The Northern and Neosho subspecies were morphologically distinct overall based on principal component analysis of five morphometric traits, but they significantly differed only in head length. Based on genome-wide variation at over 50,000 single nucleotide polymorphisms, the Neosho and Northern subspecies represented two diverged, monophyletic clades, each comprising two additional monophyletic lineages. Populations in Big Piney Creek and the Illinois Bayou within the Neosho range also showed signatures of local adaptation based on outlier FST analysis. Admixture in the Illinois River system within the Neosho range originated from a hatchery strain of Northern Smallmouth Bass found in Skiatook Lake, Oklahoma, while admixture in the Elk River, upper Arkansas River tributaries, and the Illinois Bayou and Big Piney Creek system originated from the White River in the Northern range. Demographic analysis revealed that admixture in these streams has occurred on different time scales, in some cases likely due to historic migration, and in other cases likely due to secondary contact, possibly as a result of anthropogenic introductions. In Big Sugar Creek and the Elk River, two Neosho Smallmouth Bass native streams known to be admixed with White River Northern Smallmouth Bass, individual growth did not differ between genetically pure Neosho, pure Northern, or admixed fish. However, in the Elk River alone, average length-at-infinity (maximum length) was lower for admixed fish than for either pure Neosho or pure Northern fish. We also found a significant negative relationship between multi-locus heterozygosity (based on fourteen microsatellite loci) and body condition, suggesting that increased intermixing may be causing outbreeding depression in these streams. The Neosho and Northern Smallmouth Bass constitute highly differentiated, locally adapted, and independently evolving lineages in the Central Interior Highlands. Despite divergence, there are also complex and extensive patterns of admixture in the Neosho range which may be contributing to lower fitness in two Neosho Smallmouth Bass streams. It will be crucial to consider these patterns and their potential outcomes in the development of management protocols for the preservation of endemic diversity within this economically and ecologically vital sportfish.

Perfluoroalkyl Substances in Plasma of Smallmouth Bass from the Chesapeake Bay Watershed

Smallmouth bass Micropterus dolomieu is an economically important sportfish and within the Chesapeake Bay watershed has experienced a high prevalence of external lesions, infectious disease, mortality events, reproductive endocrine disruption and population declines. To date, no clear or consistent associations with contaminants measured in fish tissue or surface water have been found. Therefore, plasma samples from two sites in the Potomac River and two in the Susquehanna River drainage basins, differing in land-use characteristics, were utilized to determine if perfluoroalkyl substances were present. Four compounds, perfluorooctane sulphonic acid (PFOS), perfluoroundecanoic acid (PFUnA), perfluorodecanoic acid (PFDA) and perfluorododecanoic acid (PFDoA), were detected in every fish. Two additional compounds, perfluorooctane sulphonamide (PFOSA) and perfluorononanoic acid (PFNA), were less commonly detected at lower concentrations, depending on the site. Concentrations of PFOS (up to 574 ng/mL) were the highest detected and varied significantly among sites. No seasonal differences (spring versus fall) in plasma concentrations were observed. Concentrations of PFOS were not significantly different between the sexes. However, PFUnA and PFDoA concentrations were higher in males than females. Both agricultural and developed land-use appeared to be associated with exposure. Further research is needed to determine if these compounds could be affecting the health of smallmouth bass and identify sources.

Host diet and parasitic helminth infections within native, established and introduced fish of Algonquin Park

Freshwater fish biodiversity loss has been attributed to many reasons, including invasive species infectious diseases. I examined 112 invasive Rock Bass (Ambloplites rupestris), 59 established Smallmouth Bass (Micropterus dolomieu), and 60 native Pumpkinseed sunfish (Lepomis gibbosus) from 8 different lakes in Algonquin Park, ON, Canada to evaluate their endohelminth parasites. My results indicate that established and native fish are not only more likely to be infected with trophically-transmitted parasites such as cestodes (tapeworms) and acanthocephalans (thorny-headed worms) than invasive Rock Bass, but they also have a higher infection intensity and greater diversity of endohelminths. There was also a significant difference between the three fish species with respect to non-trophically transmitted larval trematodes (flatworms), which reflect the habitat of fish. Along with host size, I examined fish diet and habitat use to demonstrate how the ecology of different species influences their probability of infection, parasite communities, and possible ease of establishment in novel environments.

Host diet and parasitic helminth infections within native, established and introduced fish of Algonquin Park

Freshwater fish biodiversity loss has been attributed to many reasons, including invasive species infectious diseases. I examined 112 invasive Rock Bass (Ambloplites rupestris), 59 established Smallmouth Bass (Micropterus dolomieu), and 60 native Pumpkinseed sunfish (Lepomis gibbosus) from 8 different lakes in Algonquin Park, ON, Canada to evaluate their endohelminth parasites. My results indicate that established and native fish are not only more likely to be infected with trophically-transmitted parasites such as cestodes (tapeworms) and acanthocephalans (thorny-headed worms) than invasive Rock Bass, but they also have a higher infection intensity and greater diversity of endohelminths. There was also a significant difference between the three fish species with respect to non-trophically transmitted larval trematodes (flatworms), which reflect the habitat of fish. Along with host size, I examined fish diet and habitat use to demonstrate how the ecology of different species influences their probability of infection, parasite communities, and possible ease of establishment in novel environments.

Natal and intergenerational dispersal of riverine smallmouth bass Micropterus dolomieu

Quantifying the scale of offspring dispersal is essential for understanding demographic connectivity across landscapes and rates of population spread. However, characterizing natal dispersal in fishes is complicated by the difficulties of tracking origins and movement during early life-history stages. We combined direct observation of natal dispersal based on otolith chemistry with indirect estimates of dispersal from population genetics to quantify intergenerational dispersal of smallmouth bass inhabiting a river network. Average parent-offspring dispersal was estimated as 7.7 km from genetic isolation-by-distance and demographic population data. Otolith chemistry indicated that adults were captured an average of 8.3 km from their natal tributary, supporting the genetics-based estimate. Our estimate of intergenerational dispersal is higher than previous estimates for lotic fishes and considerably higher than estimates for smallmouth bass in lake systems. Differences in availability of seasonal habitats for smallmouth bass may account for the contrasting scales of dispersal between lake and river populations. The large intergenerational dispersal distance of riverine smallmouth bass should be considered in conservation of fisheries or efforts to control invasive populations in river networks.

Is energetics or competition a stronger driver of male smallmouth bass seasonal reproductive timing?

ABSTRACTIntraspecific competitive ability is often associated with body size and has been shown to influence reproductive timing in many species. However, energetic constraints provide an alternative explanation for size-related differences of reproductive timing. In temperate fishes that experience a winter starvation period, for instance, a negative allometric relationship between body size and winter energy loss might explain why larger males spawn earlier in a season than smaller males, especially in fishes that exhibit paternal care, which is energetically costly and limits parental foraging opportunities. Male smallmouth bass, Micropterus dolomieu, defend nesting territories in which they care for offspring over an extended period. In northern populations, males rely on energy reserves over a winter starvation period and in spring must recoup energy losses before initiating reproduction, making them ideal systems in which to study contributions of competition and energetic allometry on differences of reproductive timing. Here, we harness data on parental male M. dolomieu from a 10-year study and show that larger males required fewer degree days-a measure of thermal energy experienced-in spring before they spawned each year and that the time of peak seasonal reproduction in the population was negatively related to the number of degree days accumulated before reproduction started. Furthermore, we found that growth of individual males between seasons better predicted changes in timing of reproduction than changes in size relative to competitors. Together, these results suggest that timing of reproduction in this population is more strongly influenced by energetic constraints than size-based competition amongst males.