The Influence of Insect Juvenile Hormone Agonists on Metamorphosis and Reproduction in Estuarine Crustaceans

Abstract

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.

Mysid crustaceans as standard models for the screening and testing of endocrine-disrupting chemicals

“…The primary reasons for its selection over other mysid species are the high degree of standardization, its year-round availability, the availability of commercial cultures, the relative ease of maintenance and culture in the laboratory, and its well known biology and test requirements. Furthermore, the potential for full life-cycle (A. bahia has a life cycle of about 17-20 days) and multigenerational exposures are other important advantages (McKenney, 2005). Major disadvantages that preclude the general utility of A. bahia are a limited relevance for cold water and low salinity (including freshwater) systems.…”

“…As such, any chemical that has the capacity to mimic or interfere with the action of these signaling molecules can be expected to cause significant physiological disruption. This is exemplified by the many effects on non-target arthropods of certain insect growth regulators (a class of pesticides) which are developed to intentionally mimic, block or otherwise interfere with insect ecdysteroid and juvenoid systems (insect growth regulator effects on non-target animals are reviewed by Oehlmann and SchulteOehlmann, 2003;Oetken et al, 2004;McKenney, 2005). Unfortunately, basic endocrinological studies using lower crustacean models, such as copepods, amphipods, and mysids, remain extremely limited.…”

“…For example, sexual maturity (Khan et al, 1992), intersexuality and sex determination (McKenney, 2005), time to first brood release (McKenney, 1996), time required for egg development (Gentile et al, 1983), fecundity (Gentile et al, 1982), and alterations in reproductive characteristics in populations have all been used as endpoints (Raimondo and McKenney, 2005a).…”

“…For A. bahia, standard life cycle test protocols have been developed, applied and evaluated (e.g., McKenney and Celestial, 1996;USEPA, 1997;ASTM, 1999). 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 (McKenney, 2005). For this purpose, a transgeneration mysid toxicity protocol was developed which extends the single life-cycle test such that juveniles, released by adults exposed since <24h-old juveniles, are reared through maturation without further exposure.…”

“…Survival, growth, development and reproduction of A. bahia were monitored through an entire lifecycle exposure to fenoxycarb and during the second generation without additional exposure (McKenney, 2005). Neither maturation time, sex determination nor young production was significantly altered during the life-cycle exposure.…”