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The Society for Integrative and Comparative Biology
The Influence of Insect Juvenile Hormone Agonists on Metamorphosis and Reproduction in Estuarine Crustaceans1
1 U.S. Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Gulf Ecology Division, 1 Sabine Island Dr., Gulf Breeze, Florida 32561-5299
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Comparative developmental and reproductive studies were performed on several species of estuarine crustaceans in response to three juvenile hormone agonists (pyriproxyfen, methoprene and fenoxycarb). Larval development of the grass shrimp, Palaemonetes pugio, was greater than two orders of magnitude more sensitive to disruption by methoprene and fenoxycarb than was embryonic development. Developing larvae of the mud crab, Rhithropanopeus harrisii, exhibited reduced metamorphic success at lower concentrations of methoprene and pyriproxyfen than grass shrimp larvae. These responses suggest that the more rigidly controlled metamorphic process in crabs is more sensitive to compounds acting as endocrine disruptors than is the more flexible metamorphic pattern in shrimp. The final crab larval stage, the megalopa, was more sensitive to methoprene and fenoxycarb exposure than earlier zoeal stages. Mud crab larvae exposed to fenoxycarb had reduced biomass and lipid content, particularly triglycerides and sterols. Concentrations of fenoxycarb which reduced the reproductive capacity in single life-cycle exposures of the estuarine mysid, Americamysis bahia, were similar to those concentrations which inhibited metamorphosis in grass shrimp. Juvenile mysids released by exposed adults and reared through maturation without further exposure produced fewer young and had altered sex ratios (lower percentages of males) at lower parental-exposure concentrations than directly affected parental reproduction. These transgenerational responses may well be a product of irreversible effects during developmental exposures which become apparent following maturation and initiation of reproduction. These findings support using a functional approach as an appropriate screening procedure to evaluate potential environmental endocrine-disrupting chemicals in aquatic environments.
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INTRODUCTION |
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Increased understanding of the endocrine control of developmental and reproductive processes in insects has led to the introduction of insect hormones and their analogues as insecticides known as insect growth regulators (IGRs) with the largest group being juvenile hormone analogues (Keeley et al., 1990
; Riddiford, 1994). Yet, juvenile hormone (JH)-like compounds function in crustaceans in a manner similar to that seen in insects and may have roles in the regulation of crustacean reproduction and development (Laufer and Borst, 1988; Laufer et al., 1993; Charmantier et al., 1997). More recently the scientific community has become aware of the value of invertebrates in alerting us to potential environmental compounds acting as endocrine disruptors and of the ecological significance of endocrine disruption in invertebrates (Fingerman et al., 1998; deFur et al., 1999; Depledge and Billinghurst, 1999; McKenney, 1999).
The main effects of compounds acting as JH agonists (JHAs) in insects are disruption of normal embryogenesis and interference with the process of metamorphosis by inhibiting insect development at the end of larval or pupal development (Downer and Laufer, 1983; deFur et al., 1999). A number of studies has shown that compounds with JH activity, which interrupt developmental processes in insects, also affect these processes in crustaceans (for recent reviews refer to deFur et al., 1999 and McKenney, 1999). JHAs have been shown to influence crustacean larval development (McKenney and Matthews, 1990; McKenney and Celestial, 1993; Celestial and McKenney, 1994; Cripe et al., 2003; McKenney et al., 2004), egg maturation (Templeton and Laufer, 1983) and reproductive timing and capacity (McKenney and Celestial, 1996).
Given the critical role that crustaceans have in the trophodynamics of aquatic ecosystems as dominant secondary producers and similarities in the endocrine control of developmental processes between insects and crustaceans, it is important to assess the potential impact of these novel acting pesticides on this ecologically important group of invertebrates. The objectives of this paper are to synthesize, compare and contrast developmental and reproductive studies performed at our laboratory (U.S. Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Gulf Ecology Division) (GED) on three species of estuarine crustaceans in response to three JHAs (methoprene, pyriproxyfen and fenoxycarb) (Fig. 1). Since larval shrimp generally have a more labile developmental pattern with a variable number of larval stages for completion of metamorphosis than crabs which have a more stable developmental pattern with a fixed number of larval stages through metamorphosis (McKenney, 1999), developmental responses to JHAs were compared between an estuarine shrimp (Palaemonetes pugio) and an estuarine crab (Rhithropanopeus harrisii). Reproductive responses to these same JHAs were evaluated using life-cycle exposures of the estuarine mysid, Americamysis bahia.
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Comparative embryonic and larval sensitivities to JHAs
Comparative sensitivity of embryos and larvae of decapod crustaceans to a variety of pesticides, including JHAs, have shown developing larvae to be more sensitive than embryos. Exposure concentrations of the JH agonist, methoprene, which inhibited successful completion of metamorphosis of larval P. pugio (
8 ug liter–1) (McKenney and Celestial, 1993) were greater than two orders of magnitude lower than those concentrations in which embryos successfully hatched (Horst and Walker, 1999). Embryos of P. pugio successfully hatched under exposure to 1 mg liter–1 methoprene (Wirth et al., 2001), a concentration of methoprene which would result in total mortality in larvae of this same species (McKenney and Matthews, 1990). Comparative exposures of P. pugio during both embryonic and larval development demonstrated that metamorphic success of larvae was two orders of magnitude more sensitive to fenoxycarb exposure than embryonic hatching success (McKenney et al., 2004). Exposure of larval grass shrimp to fenoxycarb concentrations 4 ug liter–1 inhibited successful metamorphosis, while exposure to fenoxycarb concentrations 
502 ug liter–1 had no significant effect on complete embryonic development. A more extensive review of the literature demonstrating the more sensitive toxic nature of crustacean larval stages to a variety of classes of pesticides compared to developing embryos is provided in McKenney et al. (2004).
Larval development through completion of metamorphosis
Even though embryos of P. pugio were more resistant to acute toxicity by diflubenzuron than were larvae (Wilson and Costlow, 1987), there were many delayed toxic effects seen in the hatched larvae following exposure as embryos to sublethal concentrations of diflubenzuron. These effects included decreased larval viability dependant on the embryonic stage of exposure (Wilson, 1985), larval morphological abnormalities (Wilson, 1985), decreased phototaxis (Wilson et al., 1985) and altered swimming patterns and vertical distribution of larvae (Wilson et al., 1987). This phenomenon of stress associated with embryonic P. pugio exposure to a pesticide being expressed subsequently during larval development was not seen with exposure to the JHA fenoxycarb (McKenney et al., 2004). Rearing grass shrimp larvae which had been exposed throughout embryonic development to sublethal fenoxycarb concentrations ranging from 28 to 502 µg liter–1 resulted in no significant modifications in their complete larval development. The lack of a delayed response in larvae exposed as embryos to fenoxycarb may be a reflection of the different modes of action of these two pesticides. Unlike diflubenzuron, which acts as a chitin synthesis inhibitor by interfering with the endocrine-regulated process of molting through a nonendocrine mechanism, the mode of action of fenoxycarb is as an endocrine disruptor functioning as a JHA in targeted insects (LeBlanc et al., 1999).
Differential toxicity was found between the metamorphic processes for shrimp and crabs in response to JHA exposure (Table 1). For the majority of JHAs studied, developing larvae of the mud crab, Rhithropanopeus harrisii, exhibited reduced metamorphic success at lower concentrations than grass shrimp (Palaemonetes pugio) larvae. The more rigid developmental pattern of the crab compared to the shrimp suggests greater endocrine control of metamorphosis in the crab and perhaps a greater sensitivity to endocrine disruption of this process.
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Differential stage-sensitivity to JHA exposure was also reported for larvae of the mud crab. As previously shown with R. harrisii exposed through complete larval development to methoprene (Costlow, 1977
), the final megalopae larval stage was shown to be more sensitive to toxicity from the JHAs, fenoxycarb (Cripe et al., 2003) and pyriproxyfen (McKenney, unpublished data) than the earlier zoeal stages. This greater sensitivity in late larval stages of the crab could indicate a similar progressive lowering of the endogenous JH titer through the various larval stages as seen in insects (Downer and Laufer, 1983) with an elevated sensitivity to JHAs at the period just prior to the completion of the metamorphic process when endogenous hormone titers are the lowest.
A number of studies have measured the inhibitory effects of pesticides acting as JHAs on successful completion of the metamorphic process in crustacean larvae (see references herein and in McKenney, 1999). In general, toxicity of these pesticides on the larvae of several crustaceans are similar to those toxicity values for the larvae of insect pests targeted by these pesticides. Furthermore, the low µg liter–1 concentrations of these compounds shown to inhibit successful completion of metamorphosis in estuarine crustaceans represent some of the lowest toxicity values reported for these registered pesticides to non-target biota. In most cases, concentrations of these JHAs that limited metamorphic success in crustacean larvae were two to three orders of magnitude lower than lethal concentrations for fish and other non-target organisms. Greater resistance among fish to fenoxycarb relative to crustaceans attests to the specific nature of pesticides acting as endocrine disruptors and the phylogenetic similarities between the endocrinology and structure of hormones from two dominant members (Insecta and Crustacea) of the Arthropoda (deFur et al., 1999) (Fig. 1). Similarities in the sensitivity of crustacean larvae and certain mosquito larvae to these pesticides acting as JHAs are consistent with earlier warnings (Grenier and Grenier, 1993) that compounds like these JHAs can create potential problems associated with their chronic toxicology because of the more insidious nature of chronic effects and the problems associated with analytical detection, especially if effects are high at very low but continuous exposure levels (Retnakaran et al., 1985).
These findings support an analogous functional approach in the selection of appropriate screening procedures to evaluate potential endocrine-disrupting chemicals in aquatic environments. Use of a bioassay protocol which measures the metamorphic success of crustacean larvae would be a valuable adjunct to the hazard assessment of newly developed pesticides that target endocrine control of metamorphosis in insects for control of insect pests and possibly other endocrine disrupting compounds as well.
Developmental stages and rates
At exposure concentrations of JHAs that allowed for successful completion of metamorphosis other developmental abnormalities have been reported in crustacean larvae (Table 2). Additional developmental intermediates or supernumerary larval stages were seen in the barnacle Eliminius modestus exposed to a JHA (Tighe-Ford, 1977). Cyprid larvae of the acorn barnacle, Balanus galeatus, metamorphosed prematurely when exposed to either the pesticide hydroprene, a JH analogue (Gomez et al., 1973) or synthetic JH1 (Ramenofsky et al., 1974). Morphological abnormalities have been reported in both crab (Costlow, 1977) and lobster (Charmantier et al., 1988) larvae exposed to JH analogues.
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The most common sublethal response reported for crustacean larvae exposed to JHAs is an increase in the time required for larval development through successful completion of the metamorphic process (Table 2). It is interesting to note that for comparative studies between larval crabs and larval shrimp with the same JHA (McKenney and Matthews, 1990
; Celestial and McKenney, 1994; Cripe et al., 2003; McKenney et al., 2004), developmental rates of larval crabs were delayed while shrimp larval developmental rates were unaffected. Preferential impacts of these compounds acting as endocrine disruptors on delaying developmental rates during crab metamorphosis and not shrimp, as with differential impacts on metamorphic success, suggest a more important role of hormones in the regulation of crab metamorphosis than that of shrimp with a greater potential for hormone disruption of these processses in crabs by compounds acting as JHAs.
Altered growth and energy metabolism
Juvenile Hormone is also thought to play a functional role in the regulation of insect energy metabolism (Downer and Laufer, 1983). It is not surprising, therefore, to find alterations in the growth rates and energy metabolism of crustacean larvae exposed to JHAs, suggesting similar endocrine control of these functions in this closely-related group of organisms. McKenney and Celestial (1993) showed that although methoprene inhibited growth in early larval and postlarval development of the shrimp P. pugio, this JHA actually enhanced growth in the premetamorphic stages. Reduced growth rates in early larvae were associated with elevated respiration rates and lower net growth efficiency rates suggesting that increased metabolic demands reduced assimilated energy available for growth of early larval stages. Lower O:N ratios in premetamorphic shrimp larvae than in early larval stages suggests a shift from greater utilization of lipid substrates during early larval development toward more protein usage as larvae approach the conclusion of metamorphosis. However, both premetamorphic larvae and postlarval grass shrimp utilized significantly greater amounts of lipid material during exposure to methoprene. Similarly the JHA fenoxycarb had a significant influence on growth, lipid class and fatty acid composition in developing crab larvae (Nates and McKenney, 2000). The first postlarval crab stages of R. harrisii, reared through complete larval development in fenoxycarb, weighed less, contained less lipid (primarily as a result of less triglycerides and free sterols) and had different fatty acid profiles that larvae not reared in fenoxycarb.
Exposure to synthetic analogues of insect JH altered the energy utilization patterns of crustacean larvae during the metamorphic process in a manner similar to the mechanism of action of this hormone in insects. Endocrine control of metamorphosis in developing insect larvae is thought to include control of such processes as the accumulation, mobilization, and use of nutrient reserves, including regulation of lipid and protein metabolism (Laufer and Borst, 1988). Lipid reserves in pupae of yellow fever mosquitoes (Aedes aegypti) were depleted following treatment with methoprene (Downer et al., 1976). Application of methoprene to early fourth-instar larvae of the same mosquito lowered protein and carbohydrate levels in the fat body, suggesting modifications in the mobilization and utilization of these energy substrates as a plausible explanation for the failure of treated mosquitoes to undergo normal metamorphosis (Gordon and Burford, 1984). Similar alterations in the utilization patterns of energy reserves in JHA-exposed crustacean larvae may at least partially explain the toxicosis of crustacean larvae to JHAs.
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Life cycle effects
Mysids have been used in regulatory toxicity testing for more than 20 years and during this time have been shown to be more sensitive to chemical contaminants at environmentally relevant concentrations than most other aquatic test species (Nimmo and Hamaker, 1982
; McKenney, 1998; Verslycke et al., 2004). Taking into consideration their ecological importance, cosmopolitan geographic distribution, availability in the field throughout the year, ease of culture in the laboratory, and proven sensitivity to various xenobiotics, mysids are generally considered amenable and highly desirable as estuarine and marine toxicity tests organisms (McKenney, 1998; Verslycke et al., 2004). Moreover, as a representative aquatic crustacean, mysids have been proposed as suitable test organisms for the evaluation of endocrine disruption by several researchers and regulatory bodies (deFur et al., 1999; Verslycke et al., 2004). The United States Environmental Protection Agency (USEPA) and the American Society for Testing of Materials (ASTM) have adopted the estuarine sub-tropical Americamysis (formerly Mysidopsis) bahia as a primary testing species for coastal and estuarine monitoring and standard guidelines for conducting life-cycle toxicity tests with A. bahia as a model have been developed by these groups (e.g., ASTM, 1999; USEPA, 1997).
The estuarine mysid A. bahia was exposed to the JHA methoprene from release as one-day-old juvenile through juvenile growth and maturation and production of young as an adult (Fig. 2). This life-cycle exposure to methoprene, a JHA used in mosquito control, produced mortality at concentrations similar to those preventing adult emergence of several mosquito species in the laboratory and in the field (McKenney and Celestial, 1996). Unlike the inhibitory effects of traditional chemical pesticides on growth of A. bahia at low sublethal concentrations, growth of A. bahia was reduced only at higher methoprene concentrations. In contrast, reproductive endpoints proved to be quite sensitive to methoprene exposure. Release of the first brood was significantly delayed by as much as 3 days for mysids exposed to low µg L–1 concentrations of methoprene. These delays in brood production could result from slowing of sexual maturity and/or embryogenesis as seen in daphnids exposed to methoprene (Templeton and Laufer, 1983). The most sensitive response of mysids to methoprene exposure was a significant reduction in the number of young produced per female. Both individual female fecundity and total young production by discrete mysid populations were significantly reduced by exposure to single-digit µg L–1 concentrations of methoprene. Since chemicals with JH activity have been shown to affect these same reproductive processes in crustaceans and since mysid responses in this study to very low concentrations of methoprene resemble responses of insects to JH and JHAs, it is plausible that this compound may be functioning through interference with an endogenous endocrine system in crustaceans which utilize JH-like compounds.
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Transgenerational effects
Recent efforts in ecotoxicology have focused on linking effects of contaminants on individuals with population-level consequences. Some of the tools used to support this linkage are structured population models, studies measuring life-history responses and multi-generational studies. As previously discussed, protocols have been developed for determining single life-cycle responses of mysids to xenobiotic chemicals. There exists, however, a need to identify groups of organisms that could be evaluated in transgenerational (multigenerational) exposures to detect ecologically relevant effects of xenobiotics on progeny of exposed organisms. Longer-term studies spanning critical life stages over multiple generations can identify and characterize possible latent or cumulative adverse effects occurring in an organism's life history.
A two-generation mysid toxicity protocol was developed which extends the single life-cycle test such that juveniles, released by adults exposed since 1-day-old juveniles, were reared through maturation and young production without further exposure (Fig. 3). Survival, growth, development and reproduction of this estuarine mysid were monitored through an entire life cycle during flow-through laboratory exposures to a range of concentrations (1–43 ug/liter) of fenoxycarb and during the second generation without additional exposure. The life-cycle exposure was initiated with triplicates of 15 <24-hr-old juveniles for each treatment which were monitored daily for survival and reproductive condition (appearance of a marsupial indicated maturation of females). Upon maturation, F0 males and females were paried and daily records maintained for young production of each pair. Triplicates of 5 <24-h-old F1 juveniles were reared in unexposed sea water and observed daily through maturation for survival, maturation and young production as previously described for exposed F0 mysids.
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Preliminary transgenerational responses of A. bahia to fenoxycarb, a pesticide acting as a juvenile hormone agonist, have been reported (McKenney et al., 1999
). Exposure to 43 ug/liter significantly reduced mysid survival through first brood production (Fig. 4). At these exposure concentrations neither sex ratios nor young production were altered significantly during the life-cycle exposure. However, second generation adults, exposed to fenoxycarb only as developing embryos and larvae, produced fewer young when developing in 6 µg L–1 and contained significantly less males when developing in 1 µg L–1 (Fig. 5). Therefore, juvenile mysids released by fenoxycarb-exposed adults and reared through maturation without further exposure produced fewer young and had altered sex ratios (reduced percentages of males) at lower parental-exposure concentrations than directly impacted parental reproduction. Interestingly, these results indicate that compounds with JH-like activity may be acting like other endocrine disrupting chemicals with exposure during developmental periods (in this case during ovarian, embryonic and larval development) producing irreversible reproductive dysfunction in adults. These findings strongly suggest the importance of developing, at least, two-generational exposure protocols for adequately predicting the ecological risk of endocrine-disrupting chemicals on aquatic organisms.
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ACKNOWLEDGMENTS |
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The collaborative interactions and technical assistance of David Celestial, Geraldine Cripe, Peggy Harris, Marilynn Hoglund and Edward Matthews are greatly appreciated during various portions of the work summarized herein.
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FOOTNOTES |
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1 From the Symposium EcoPhysiology and Conservation: The Contribution of Endocrinology and Immunology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 E-mail: mckenney.chuck{at}epa.gov
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