Elsevier

Science of The Total Environment

Volume 447, 1 March 2013, Pages 198-209
Science of The Total Environment

Reproductive health of yellow perch Perca flavescens in selected tributaries of the Chesapeake Bay

https://doi.org/10.1016/j.scitotenv.2012.12.088Get rights and content

Abstract

Reduced recruitment of yellow perch has been noted for a number of years in certain urbanized watersheds (South and Severn Rivers) of the Chesapeake Bay. Other rapidly developing watersheds such as Mattawoman Creek are more recently showing evidence of reduced recruitment of anadromous fishes. In this study, we used a battery of biomarkers to better document the reproductive health of adult yellow perch collected during spring spawning in 2007–2009. Perch were collected in the South and Severn Rivers, Mattawoman Creek and the less developed Choptank and Allen's Fresh watersheds for comparison. Gonadosomatic indices, plasma reproductive hormone concentrations, plasma vitellogenin concentrations and gonad histology were evaluated in mature perch of both sexes. In addition, sperm quantity (cell counts) and quality (total and progressive motility, spermatogenic stage and DNA integrity), were measured in male perch. Many of these biomarkers varied annually and spatially, with some interesting statistical results and trends. Male perch from the Choptank and Allen's Fresh had generally higher sperm counts. In 2008 counts were significantly lower in the perch from the Severn when compared to other sites. The major microscopic gonadal abnormality in males was the proliferation of putative Leydig cells, observed in testes from Severn and less commonly, Mattawoman Creek perch. Observations that could significantly impact egg viability were an apparent lack of final maturation, abnormal yolk and thin, irregular zona pellucida. These were observed primarily in ovaries from Severn, South and less commonly Mattawoman Creek perch. The potential association of these observations with urbanization, impervious surface and chemical contaminants is discussed.

Highlights

► Reduced recruitment of yellow perch has occurred in urban tributaries of Chesapeake Bay. ► We compared reproductive health biomarkers in perch from two urban, one developing, two less developed watersheds. ► Lack of final maturation, abnormal yolk and zona pellucida were noted in females. ► Leydig cell proliferation was noted in males.

Introduction

The native range of yellow perch (YP) Perca flavescens includes much of Canada, from central Canada east and southeast through the Great Lakes–St. Lawrence and the upper Mississippi basins and on the Atlantic slope from Maine to Georgia (Grzybowski et al., 2010). Historically, YP populations in Chesapeake Bay and the Great Lakes supported major recreational and commercial fisheries (Piavis, 1991, Wells, 1977). However, at selected sites or tributaries in both geographic regions, major population declines and a lack of recruitment have occurred (Yellow Perch Work Group, 2002, Clapp and Dettmers, 2004, Wilberg et al., 2005).

In the Chesapeake Bay (Fig. 1), commercial YP harvest began to decline during the mid-1960s and reached its nadir during 1976–1982 (Yellow Perch Work Group, 2002). Declines in YP recreational fishing participation in the urbanizing subestuaries within the Baltimore–Washington corridor became evident in the 1980s (O'Dell 1987) and these declines were attributed to habitat degradation by urban/suburban development (Yellow Perch Work Group, 2002, Uphoff et al., 2005). Subestuaries, including the Severn and South Rivers, closed to YP fishing for nearly 20 years, were reopened for recreational fishing in 2009. The rationale (for the Severn, South and West Rivers) being that these watersheds are extremely degraded habitat, reproductive output is low, while the adult population appears stable and therefore recreational harvest would not impact the total reproductive capacity (Maryland Fisheries Service, 2012).

Yellow perch are semi-anadromous in the Chesapeake Bay watershed and adults remain in their natal tributaries. As a result, they are exposed to chemical mixtures and stressors typical of their respective tributaries. Upstream spawning migration of adults and the subsequent downstream dispersal of juveniles are their primary movements (Muncy, 1962, Piavis, 1991). The adults migrate from the lower parts of the tributaries to the upper regions in search of suitable spawning habitat in late February–early March. Males tend to reach the freshwater spawning areas first and do not migrate downstream until the females leave. In the 1950s studies in the Severn River indicated YP first appeared when water temperatures were 3.9–6.7 °C and peak spawning occurred at water temperatures of 5.6–7.2 °C (Mansueti, 1964). Later studies indicated peak spawning occurs when water temperatures reach sustained levels of 8.5 to 11 °C (Hardy, 1978). Peak spawn is usually fewer than five days and in some years two to three days (S. Minkkinen, personal observation).

During spawning females extrude distinctive, long, accordion-like strands of eggs, which have a thick gelatinous egg membrane (Mansueti, 1964). Two indicators that have been used to assess reproductive success and year class strength in selected tributaries are egg mass surveys and larval abundance. The Coastal Conservation Association of Maryland conducts egg mass surveys in YP spawning reaches. These surveys are performed by volunteers making counts or semi-quantitative estimated counts (i.e. > 100 or > 300 egg masses per 50 m of shoreline) by walking along the shore or on the water by kayak or other watercrafts. These data are not consistently collected annually for all tributaries; however, they provide useful comparative observations suggestive of differential spawning success. For instance, counts from survey data in 2005–2009 were consistently high in the Choptank (> 200) and Mattawoman (> 100 except 82 in 2008). Counts in Allen's Fresh (a tributary of the Wicomico River on the western shore of the Chesapeake Bay) varied annually from 350 in 2006 to 40 in 2009. Counts have been consistently low (< 100 and often < 50) in the South and Severn with none observed in the South in 2009 and only seven in the Severn in 2006 (Coastal Conservation Association Maryland, Ken Hastings, personal communication).

Larval presence, Lp, is defined as the proportion of 0.5 m plankton tows with larvae during the peak weeks from late March through early May, and is used as an indicator of year class strength. The Lp index integrates egg production, egg hatching success, and survival of first-feeding larvae. Brackish systems with small watersheds and high levels of development (South, Severn and Magothy Rivers) have exhibited a persistent depression in Lp, below a reference minimum since 2002. Regression analyses indicated that development (percent of impervious surface in the watershed, i.e. pavement, rooftops and compacted soils) was negatively related to Lp. Other systems may exhibit wide variation in larval presence, but the low levels similar to those seen in these urbanized subestuaries are not common. However, since 2008 spawning site loss for anadromous fishes is evident in the developing Mattawoman Creek (Uphoff et al., 2010, Uphoff et al., 2011).

Neither excessive adult mortality nor reduced growth has been observed in Severn River YP. Additionally, Severn River broodstock induced to spawn in the hatchery produced visually abnormal egg chains and too few viable eggs to support hatchery production. Hence, the depressed egg and larval survival are hypothesized to be critical factors suppressing resident YP populations in western shore subestuaries subject to high levels of development (Uphoff et al., 2005). However, neither the biological basis for the depressed egg and larval survival, nor specific chemicals or other stressors leading to these effects has been documented. Hence, the goal of the current study was to compare the reproductive health of spawning adult YP from historically important spawning reaches in the Chesapeake Bay watershed to better understand the biological effects leading to reduced reproduction. Yellow perch from two developed tributaries (South and Severn) with evidence of population declines were compared to those from Mattawoman Creek with intermediate but increasing development and the less developed Choptank River and Allen's Fresh. A broad suite of indicators including gonadal histology, plasma vitellogenin (Vtg), sex steroid hormone concentrations and sperm quality parameters was assessed in multiple years.

Section snippets

Site descriptions

Yellow perch were collected during spawning runs in the Choptank River (CH) at Mill Creek near Route 16; South River (SO) near Defense Highway; Severn River (SE) at Severn Run; Mattawoman Creek (MA) at Mason's Branch and Allen's Fresh (AF), Zekiah Swamp above Route 234. Watersheds for the areas sampled (Fig. 1) were delineated using 12-digit level hydrologic units developed as part of the National Watershed Boundary Database (USGS and USDA, 2011) except the Choptank River, where only the upper

Site comparisons

Landuse categories (estimated for 2010) indicated the CH (8.2%) and AF (22.1%) had fairly low percentages of developed land, while MA (44.7%) was intermediate and SE (69.3%) and SO (81.2%) were high. The percent of impervious surface showed the same pattern with CH (1.7%) and AF (4.8%) low, MA (10.2%) intermediate and SO (24.6%) and SE (20.7%) high. The SO and SE also have low percentages of forested land, 2.0 and 9.1% respectively (Table 1).

Morphometric observations

Yellow perch were collected from four rivers in 2007,

Discussion

Reports of reproductive endocrine disruption/modulation of aquatic organisms are increasing worldwide. Chemical disruption or modulation of the hypothalamic–pituitary–gonadal axis can result in numerous adverse effects. The most commonly reported effects are those resulting from exposure to estrogenic/antiandrogenic chemicals. Feminization of male fishes as evidenced by testicular oocytes or intersex (Jobling et al., 1998, Kavanagh et al., 2004, Dietrich and Krieger, 2009, Blazer et al., 2012)

Acknowledgments

Funding for this project was provided by the U.S. Fish and Wildlife Service, Chesapeake Bay Field Office, Mirant Corporation and the U.S. Geological Survey's Chesapeake Bay Priority Ecosystems, Fisheries and Toxic Substances Hydrology Programs. The authors thank Deb Iwanowicz and Emily Chambers for assistance with perch necropsies; Kathryn Spring and Darlene Bowling (USGS National Fish Health Research Laboratory) for histological slide preparation; E. Theall and H. Olivier (USGS National

References (84)

  • D.G. Kaufman et al.

    Aspiration flow cytometry of the testes in the evaluation of spermatogenesis in the infertile male

    Fertil Steril

    (1987)
  • I.A. Khan et al.

    PCB congener-specific disruption of reproductive neuroendocrine function in Atlantic croaker

    Mar Environ Res

    (2006)
  • E. Lubzens et al.

    Oogenesis in teleosts: how fish eggs are formed

    Gen Comp Endocrinol

    (2010)
  • T.V. Madureira et al.

    The toxicity potential of pharmaceuticals found in the Douro River estuary (Portugal): assessing impacts on gonadal maturation with a histopathological and stereological study of zebrafish ovary and testis after sub-acute exposures

    Aquat Toxicol

    (2011)
  • C.J. Martyniuk et al.

    Effects of acute dieldrin exposure on neurotransmitters and global gene transcription in largemouth bass (Micropterus salmoides) hypothalamus

    Neurotoxicol

    (2010)
  • R.W. Schulz et al.

    Gonadotropins, their receptors, and the regulation of testicular functions in fish

    Comp Biochem Physiol B. Biochem Mol Biol

    (2001)
  • M.M. Schultz et al.

    Selective uptake and biological consequences of environmentally relevant antidepressant pharmaceutical exposures on male fathead minnows

    Aquat Toxicol

    (2011)
  • S.A. Sower et al.

    Steroid and thyroid hormones during sexual maturation of coho salmon (Oncorhynchus kisutch) in seawater or fresh water

    Gen Comp Endocrinol

    (1982)
  • A.M. Vajda et al.

    Demasculinization of male fish by wastewater treatment plant effluent

    Aquat Toxicol

    (2011)
  • W. An et al.

    Extinction risk of exploited wild roach (Rutilus rutilus) populations due to chemical feminization

    Environ Sci Technol

    (2009)
  • G.T. Ankley et al.

    Ketoconazole in the fathead minnow (Pimephales promelas): reproductive toxicity and biological compensation

    Environ Toxicol Chem

    (2007)
  • C.L. Arnold et al.

    Impervious surface coverage: emergence of a key environmental factor

    J Am Plan Assoc

    (1996)
  • B.E. Ballachey et al.

    The sperm chromatin structure assay relationship with alternate tests of semen quality and heterospermic performance of bulls

    J Androl

    (1988)
  • N. Basu et al.

    Pulp and paper mill effluents contain neuroactive substances that potentially disrupt neuroendocrine control of fish reproduction

    Environ Sci Technol

    (2009)
  • V.S. Blazer

    Histopathological assessment of gonadal tissue in wild fishes

    Fish Physiol Biochem

    (2002)
  • V.S. Blazer et al.

    Reproductive endocrine disruption in smallmouth bass (Micropterus dolomieu) in the Potomac River basin: spatial and temporal comparisons of biological effects

    Environ Monit Assess

    (2012)
  • E. Brabec et al.

    Impervious surfaces and water quality: a review of current literature and its implications for watershed planning

    J Planning Lit

    (2010)
  • B.W. Brooks et al.

    Determination of select antidepressants in fish from an effluent-dominated stream

    Environ Toxicol Chem

    (2005)
  • J.F. Casey et al.

    Characterization of Choptank River populations of white (Morone americana) and yellow (Perca flavescens) perch

    Final Report FY 1986

    (1988)
  • Claggett PR, Irani FM, Thompson RL. Estimating the extent of impervious surfaces and turf grass across large regions. J...
  • D.E. Clapp et al.

    Yellow perch research and management in Lake Michigan: evaluating progress in a cooperative effort, 1997–2001

    Fisheries

    (2004)
  • T. Colburn et al.

    Aquatic ecosystems: harbingers of endocrine disruption

    Ecol Appl

    (2000)
  • J.C. Cook et al.

    Rodent Lyedig cell tumorigenesis: a review of the physiology, pathology, mechanisms, and relevance to humans

    Crit Rev Toxicol

    (1999)
  • H.A. Crissman et al.

    Rapid simultaneous measurement of DNA, protein and cell volume in single cells from large mammalian cell populations

    J Cell Biol

    (1973)
  • N.D. Denslow et al.

    Vitellogenin as a biomarker of exposure to estrogen or estrogen mimics

    Ecotoxicology

    (1999)
  • D.R. Dietrich et al.

    Histological analysis of endocrine disruptive effects in small laboratory fish

    (2009)
  • D.P. Evenson et al.

    Flow cytometric analysis of mouse spermatogenic function following exposure to ethylnitrosourea

    Cytometry

    (1985)
  • Glenn III DW. Effect of osmolality, extender and temperature on gamete storage of koi carp (Cyprinus carpio). Master's...
  • H.J. Grier et al.

    The ovary, folliculogenesis, and oogenesis in teleosts

  • M. Grzybowski et al.

    Genetic variation of 17 wild perch populations from the Midwest and East Coast analyzed via microsatellites

    Trans Am Fish Soc

    (2010)
  • L.J. Guillette

    Endocrine disrupting contaminants — beyond the dogma

    Environ Health Perspect

    (2006)
  • J.D. Hardy

    Development of fishes of the mid-Atlantic bight. Vol. III. Aphredoderidae through Rachycentridae

    (1978)
  • Cited by (18)

    • Sperm quality biomarkers complement reproductive and endocrine parameters in investigating environmental contaminants in common carp (Cyprinus carpio) from the Lake Mead National Recreation Area

      2018, Environmental Research
      Citation Excerpt :

      Additionally, neoplastic foci in livers were more evident at Willow Beach (WB) below Hoover Dam than either in Lake Mead or Lake Mohave (Patiño et al., 2003). Even with clearly diverse environmental EDC and fish biological response profiles, linking environmental EDC exposure with endocrine and reproductive outcomes is challenging (Blazer et al., 2013; Jenkins et al., 2015; Patino et al., 2015; Sopinka et al., 2012). Cellular and molecular biomarkers of sperm quality contribute to fertilization capacity (Blazer et al., 2013; Jenkins, 2011; Jenkins et al., 2011, 2014) and developmental outcomes (Pagano et al., 2016).

    • Histopathology of brown bullhead (Ameiurus nebulosus), smallmouth bass (Micropterus dolomieu), and yellow perch (Perca flavescens) in relation to polychlorinated biphenyl (PCB) contamination in the Hudson River

      2017, Science of the Total Environment
      Citation Excerpt :

      As demonstrated in the literature and in the current study, there are dramatic differences among species in field studies of the prevalence of ovotestis. Smallmouth bass are among the most sensitive species (e.g., Hinck et al., 2009; Iwanowicz et al., 2016), whereas no cases have been reported in yellow perch (current study, Blazer et al., 2013); none in brown bullhead in the Baldigo et al. (2006) study and only one case in the current study. Bahamonde et al. (2013) in a literature review stated that it is uncertain whether field studies are distinguishing between natural intersex background and intersex due to stressors, and recommended further studies in geographic areas not subjected to chemical loading.

    • Flow cytometric method for measuring chromatin fragmentation in fixed sperm from yellow perch (Perca flavescens)

      2015, Theriogenology
      Citation Excerpt :

      In addition to effecting individuals at any stage of life by mimicking, replacing, or interfering with sex hormone activities, environmental endocrine disrupting compounds (EDC) can modify the germ line [29,36]; some EDC are genotoxic [37]. Evidence in the Chesapeake Bay watershed points to reproductive impairment, including endocrine disruption in yellow perch (YP; Perca flavescens), largemouth bass (Micropterus salmoides), and smallmouth bass (Micropterus dolomieu) [38–40]. This study addressed the hypothesis of whether gametes of male YP collected from tributaries of Chesapeake Bay could be fixed and analyzed later for DNA quality.

    View all citing articles on Scopus
    View full text