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Bioaccumulation and Metabolic Effects of the Endocrine Disruptor Methoprene in the Lobster, Homarus americanus1
Integrative and Comparative Biology, Feb 2005 by Walker, Anna N, Bush, Parshall, Puritz, Jonathan, Wilson, Thomas, Et al
SYNOPSIS. Methoprene is a pesticide that acts as a juvenile hormone agonist. Although developed initially against insects, it has since been shown to have toxic effects on larval and adult crustaceans. Methoprene was one of several pesticides applied to the Western Long Island Sound (WLIS) watershed area during the summer of 1999; the other pesticides were malathion, resmethrin, and sumethrin. These pesticides were applied as part of a county-by-county effort to control the mosquito vector of West Nile Virus. Subsequently, the seasonal lobster catches from the WLIS have decreased dramatically. The lethality of the pesticides to lobsters had been unknown. We studied the effects of methoprene while other investigators studied effects of the other pesticides. We questioned whether methoprene, through its effects on larvae, adults or both, could have contributed to this decline. We found that low levels of methoprene had adverse effects on lobster larvae. It was toxic to stage II larvae at 1 ppb. Stage IV larvae were more resistant, but did exhibit significant increases in molt frequency beginning at exposures of 5 ppb. Juvenile lobsters exhibited variations in tissue susceptibility to methoprene: hepatopancreas appeared to be the most vulnerable, reflected by environmental concentrations of methoprene inhibiting almost all protein synthesis in this organ.
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Our results indicated that methoprene concentrates in the hepatopancreas, nervous tissue and epidermal cells of the adult lobster. Methoprene altered the synthesis and incorporation of chitoproteins (cuticle proteins) into adult postmolt lobster explant shells. SDS PAGE analyses of adult post-molt shell extracts revealed changes in the synthesis of chitoproteins in the methoprene-treated specimens, suggesting that methoprene affects the normal pathway of lobster cuticle synthesis and the quality of the post-molt shell. Although it is likely that a combination of factors led to the reduced lobster population in WUS, methoprene may have contributed both by direct toxic effects and by disrupting homeostatic events under endocrine control.
INTRODUCTION
Juvenile hormone (JH) is a regulator of insect development. It modifies the response to the molting hormone, 20-hydroxyecdysone, at the molecular, cellular and organismal level. In larval insects, the presence of JH promotes larval-larvae molts, while its absence results in a pupal or adult molt (Riddiford, 1993, 1996). Methyl farnesoate (MF), synthesized in the mandibular organ of crustaceans, is the unepoxidated equivalent of Juvenile Hormone III (JH III) found in insects. The pesticide methoprene is a JH agonist (Staal, 1986; Wilson, 2004) and also mimics the action of MF in crustaceans (Laufer et al., 1987).
During the warm weather months of 1999, concerns about the spread of the mosquito-borne West Nile Virus led to increased application of pesticide compounds in the New York City and Connecticut area. In mid-September of that year, the region experienced extremely heavy rainfall due to Hurricane Floyd. One month later, lobstermen in Western Long Island Sound (WLIS) began to report sightings of gravid female lobsters dying in the throes of abortive molts. The environmental concentrations of methoprene and of the other pesticides in WLIS during that time are unknown. The combination of circumstances and observations, however, led us to question whether methoprene, known to have been applied to the WLIS watershed, had disrupted the normal hormonal balance in ovigerous female lobsters and triggered molting at inappropriate times. The subsequent decrease since 1999 in the seasonal lobster catches would likewise indicate that one or more harmful events had increased morbidity and mortality among adult lobsters and their offspring. We undertook study of the acute effects of methoprene exposure on the survival of larval lobsters and to determine whether such an exposure would exert changes in the tissues of adult animals. The purpose of this paper is to provide a preliminary communication of our findings, as of January, 2004. A detailed report will be presented elsewhere.
MATERIALS AND METHODS Culture
All larval experiments were conducted at the Darling Marine Center, University of Maine, Walpole, ME. Gravid female lobsters were obtained from local fishermen and maintained in flowing seawater tanks equipped with an outlet screen to retain larvae. As they hatched, larvae were collected with a dip net and transferred to cylindrical tanks (0.3 × 1.5 m) equipped with a similar flow-through system. A large airstone at the bottom of each tank provided adequate suspension of the larvae throughout the entire water column. The ambient water temperature was 18°C; all experimental work with larvae was conducted at the same temperature. Larvae were fed live adult brine shrimp twice daily; the photoperiod was 12 L: 12 D. Developmental stages of larvae were identified according to Factor (1995).
Acute exposure studies
All solutions for larval exposure studies were prepared using filtered seawater. S-Methoprene (Welmark International, Schaumburg, IL) was dissolved and diluted in acetone (10 mM) prior to adding it to seawater; seawater used to maintain control animals contained an equivalent amount of neat acetone. Plastic development trays (Pfaff; B&H Photo, New York, NY) were half filled with various concentrations of methoprene in seawater (see Results) and aerated with a small airstone. Trays were maintained at 18°C under fluorescent light in a walk-in cold room. Plastic tackle boxes with 1 mm holes drilled in the bottom were used for exposure studies: each compartment (4×5 cm, with a depth of 3 cm seawater) housed one larval lobster. Thirty larvae were exposed to each concentration of pesticide tested (see Results). For postlarvae (Stage IV), 18 individuals were tested at each concentration. Larvae were fed adult brine shrimp ad lib. and were scored daily for molting and survival. Dead animals were removed from the trays immediately. Animals were maintained in the original volume of pesticide laden seawater for 7 days; thereafter animals were changed to normal seawater and the experiment was continued for an additional 7 days.
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