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An Assessment of Potential Contaminant Effects on Freshwater Mussels in the South Florida Ecosystem

Ruessler, D.S.,1* Kernaghan, N.J.2, Wieser, C.M.1, Wiebe, J.J.2, Gross, T.S.1,2

1USGS - Florida Integrated Science Center, Gainesville, Florida
2College of Veterinary Medicine, Department of Physiological Sciences
University of Florida, Gainesville, Florida

 

Abstract

     Approximately 2 million acres of the Everglades drainage system contain sediments and biota with elevated mercury and other contaminants related to human activities. The current study examined species diversity, health, and reproductive status of freshwater mussels in South Florida in relation to habitat alteration and contaminants. Mussels were present in only 23 of the 47 suitable sites examined. Although species diversity and abundance widely varied between sites, two species Elliptio buckleyi and Utterbackia imbecillis were each present at multiple sites.  Approximately 25 adult mussels of each of the two species were collected per site and health assessed using: soft tissue, mantle, total gill and shell wet weights; shell length, shell width, and mantle glycogen concentrations.  A body weight to length ratio was calculated as a body condition index (BCI).  Histological analyses were utilized to determine sex and reproductive stage.  Contaminant analyses indicated significant bioaccumulations of mercury, organochlorine pesticide residues and PCB's, which varied widely between sites.  Foot biopsy or mantle tissues were analyzed for sex steroid concentrations (Estrogen and Testosterone) to assess reproductive status and potential contaminant related endocrine disruption. Health assessments indicated decreased body condition indices and mantle glycogen concentrations for mussels from sites with elevated mercury and organochlorine pesticide exposures.  Likewise, endocrine analyses indicated decreased estrogen for females and decreased testosterone concentrations for males from sites with increased mercury and pesticide exposures. Exposure differences were also correlated to differing reproductive status.  These data are among the first to indicate potential endocrine disrupting effects of contaminants in invertebrates.  Overall, these data indicate that both habitat degradation and elevated contaminant levels from anthropogenic sources are probable causes of mussel declines.

Introduction

     Freshwater mussels are one of the most endangered groups of animals in North America. About 70 percent of the nearly 300 species in North America are classified as either endangered, threatened, extinct, or in serious decline (Williams et al, 1992).  In the United States, 42 mussel species are federally protected with another 70 species proposed and/or candidates for listing (USFWS, 1994).  Many threats have been documented for this drastic decline, such as siltation of suitable habitats, poor land management practices, channelization, host-fish declines, non-indigenous species, and decreased water quality from pollutants such as nutrients, herbicides, pesticides, and a wide variety of urban and industrial chemicals.  However, little is known about the effects of environmental contaminants on freshwater mussels.

     Much of the data indicating effects of environmental contaminants in wildlife, has focused on effects in fish, reptiles and/or other macro-faunal vertebrates.  Indeed, as with many ecosystems, the macro fauna have been studied extensively, while invertebrates have largely been ignored.  Aquatic invertebrates, such as freshwater mussels would be expected to be exposed to both sediment and water partitioning of contaminants.  Indeed, exposures to environmental contaminants and potential effects may be related to the widespread population decreases frequently reported for freshwater mussels.

     Our laboratory has recently developed freshwater mussels as models for general toxicity and as important environmental sentinels, early signals, of environmental effects for contaminants such mercury, pesticides and papermill effluents (Kernaghan et al., 1998a&b; Ruessler et al., 1998; Gross et al. 1998).  These preliminary studies have utilized freshwater mussels (Elliptio buckleyi and Utterbackia imbecillis) as models for detecting the effects of environmental contaminants within controlled and natural environments.  These efforts include the initial validation and development of several indices and biochemical assessments of health status as well as important indicators of reproductive health/function.  Indeed, these methods have included the first reported validation of sex steroid monitoring procedures for freshwater mussels.

     To assess whether chemical stressors/contaminants are significantly involved in the widespread declines in freshwater mussel populations, it is important to study populations that are potentially exposed and may be sensitive to contaminants.  The current study focused on the south Florida/Everglades ecosystem and the endemic populations of freshwater mussels as a field application of  mussels as environmental sentinels of contaminant effects and ecosystem health. These efforts include an ecosystem (Everglades) wide survey of endemic populations for initial assessments of biomarkers and bioindicators of effects such as health indices: body condition and organ somatic indices, tissue histopathology, and tissue glycogen, as well as indices of reproductive function: tissue sex steroids and reproductive success.

Site descriptions and locations - click to enlarge

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Objectives

  • To determine the current status of mussel populations in South Florida.
  • To develop and validate a battery of bioindicators for freshwater mussels which assess health, reproductive status and contaminant exposure/effects.

Materials and Methods

     Adult freshwater mussels were collected in south Florida. South Florida was defined, for this study as the area from Lake Okeechobee south, including the Everglades. Initial sites where selected based on historical records of mussel presence. Where available, 25 mussels of each species were collected and transported back to the laboratory. Five mussels from each site were analyzed for methyl mercury and organochlorine pesticides.  The remaining 20 mussels were dissected and the following measurements recorded:  Shell Length, Shell Width, Shell Wet Weight, Soft Tissue Wet Weight, Mantle Wet Weight, and Total Gill Wet Weight.  From these measurements, the following health indices were developed:  STI (Soft Tissue Index), determined as the percent of soft tissue weight to total mussel weight, BCI (Body Condition Index), determined as a ratio of total weight to shell length. Mantle tissues were digested by adding 3x volume of 30% KOH and incubated for 20 minutes in a 80oC water bath.  After digestion, samples were divided to determine mantle glycogen concentrations (mg/g) and hormone concentrations (pg/g). Mantle tissues were analyzed for estradiol and testosterone using standard radioimmunoassay (RIA) procedures.   Remaining mussel bodies were preserved in NoTox tissue fixative for histological sex determination.


indicatorIndicators of reproductive function (Elliptio buckleyi) males - click to enlargeIndicators of reproductive function (Elliptio buckleyi) females - click to enlarge

Elliptio buckleyi - click to enlarge
buckleyi aElliptio buckleyi, Glycogen concentration - click to enlargeElliptio buckleyi, Shell condition index - click to enlarge
buckleyi bElliptio buckleyi, Body condition index - click to enlarge
Elliptio buckleyi, Contaminant data - click to enlarge

Utterbackia impecillis - click to enlarge
imbecillis aaUtterbackia imbecillis, Glycogen concentration - click to enlargeUtterbackia imbecillis, Shell condition index - click to enlarge
imbecillis bUtterbackia imbecillis, Body condition index - click to enlarge
Utterbackia imbecillis, Contaminant data - click to enlarge


Results

     Freshwater mussel populations were surveyed throughout south Florida and the Everglades ecosystem.  A total of 47 sites, many with historic evidence of freshwater mussel populations, were surveyed during 1999.  Freshwater mussels were not detected at 24 sites, while only relic populations were detected at 9 sites. The remaining 14 sites had significant populations of at least one species of freshwater mussel. Of these 14 sites, Utterbackia imbecillis was present at all sites, Elliptio buckleyi at 8 sites, Villosa amygdala at 8 sites, and Anodonta couperiana at 1 site. Sites which had significant populations of Elliptio buckleyi and Utterbackia imbecillis are the focus of the current study results. These survey results demonstrate a significant decline in freshwater mussels throughout south Florida and the Everglades ecosystem.

     Indices of general health status were utilized to evaluate each of the populations. Body Condition Index was significantly reduced for C-18 and St. Lucie with E. buckleyi. However, Body Condition Index did not reveal significant differences between sites.  Shell Condition Index (SCI) revealed significant differences between sites. E. buckleyi in C-18 and U. imbecillis in Lake Osborne had reduced Shell Condition Index.  In general, these indices indicated differences for mussels from St. Lucie Canal, Lake Osborne and the C-18 Canal as compared to other sites.  These data suggest an altered or decreased health status for these populations.

     Tissue estradiol, testosterone, as well as mantle glycogen concentrations were utilized as bioindicators of reproductive and endocrine function.  In general, female mussels from the St. Lucie Canal and Lake Worth, as well as males from the St. Lucie Canal and the C-18 Canal had altered patterns of sex steroids as compared to the other sites.  These data indicate altered gonadal endocrine function, as well as potential altered reproductive status and function for these populations.  Mantle glycogen concentrations were significantly lower for Lake Osborne with E. buckleyi, but not U. imbecillis.  However, U. imbecillis showed significant increases in mantle glycogen concentration at C-18.

     Chemical residue analyses demonstrated increased tissue PCB concentrations for Lake Osborne with E. buckleyi. C-18 canal and Lake Osborne also showed increased PCB concentrations with U. imbecillis.  In general, the chlorinated pesticides (DDE, chlordane and cyclodienes) were also increased for Lake Ida, for both species, as compared to the other sites.  Mercury was significantly increased at only one of the sites, the St. Lucie Canal for E. buckleyi.

     Overall, these data indicate several correlations between health and/or reproductive/endocrine indicators and chemical residue contaminants.  High levels of PCB's were associated with decreased health status and altered endocrine indicators for mussels from the C-18 Canal. Similarly, high tissue burdens of mercury were associated with decreased health status and altered endocrine indicators for mussels from the the St. Lucie Canal. However, increased tissue concentrations of the chlorinated pesticides, as observed for Lake Ida mussels, did not appear to alter either health or reproductive indicators.

Discussion

     The current study surveyed endemic populations of freshwater mussels throughout south Florida and the Everglades ecosystem.  These results suggest significant alterations and declines in both the distribution and abundance of freshwater mussels in this critical ecosystem.  Contaminant effects in freshwater mussels could be, at least partially, responsible for these population-level effects and declines. Indeed, these results demonstrate significant alterations in health status and reproductive/endocrine indicators between populations and several correlations to contaminant concentrations and land-use patterns.  These results support our initial hypothesis that specific contaminants at ecologically relevant levels of exposure, could be responsible for adverse population effects, including decreased reproductive success/function and endocrine disruption.  For example, mussels from the St. Lucie Canal exhibit deceased sex steroid concentrations and altered health status in association with increased levels of mercury exposure. These results are similar to other recent results from this laboratory that indicate similar mercury dose dependent responses for freshwater mussels under controlled laboratory conditions.

     Freshwater mussel species have been recognized as important environmental sentinels and serve as models for a wide variety of sediment toxicity tests that utilize mortality and lethality as the endpoints of significance.  Freshwater mussels are sessile organisms and rarely move more than a few meters over the course of there entire life, usually traveling only in response to abnormal water levels or temperatures.  They spend most of there life buried in mud or sand of permanent bodies of water from lakes to large rivers to small shallow streams. It has been reported that mussels live more than ten years with certain species reaching 100 years.  These attributes make freshwater mussels an attractive model for detecting the potential non-lethal effects of environmental contaminants.  Indeed, the development and validation of freshwater mussels as indicators of ecosystem health, contaminant effects, and/or remediation/restoration success is supported by the current study results.

     Overall, the current results indicate that freshwater mussel populations in South Florida are significantly exposed to a variety of chemical stressors/contaminants, such as mercury and pesticides, as well as document non-lethal effects in multiple health, physiologic and/or endocrine endpoints.  These data demonstrate the utility and potential of freshwater mussel species as bioindicators of ecosystem health and contaminant effects. Future efforts will include the utilization of freshwater mussels as indicators of restoration/remediation success within the ongoing South Florida/Everglades Restoration Initiative.

 

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