Reproductive health of yellow perch Perca flavescens in selected tributaries of the Chesapeake Bay
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
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2017, Science of the Total EnvironmentCitation 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.
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2015, TheriogenologyCitation 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.