Impacts of Xenobiotics on Crustacean Molting: The Invisible Endocrine Disruption1

SYNOPSIS.

Aquatic pollution has led to the accumulation of various xenobiotics in crustaceans. A number of these environmental chemicals have been found to interfere with molting of crustaceans. Results of initial mechanistic studies with Uca pugilator suggest that the disruption of molting results from the disturbance to the Y-organ-ecdysteroid receptor (EcR) axis by xenobiotics. Such disturbance to the Y-organ-EcR axis can be caused by interference with epidermal ecdysteroid signaling and/or alterations in ecdysteroidogenesis and/or ecdysteroid disposition. Because the adverse impacts on crustacean molting cannot be readily seen in the wild, the disruption of molting represents an invisible form of endocrine disruption.

INTRODUCTION

Because of agricultural and industrial activities, aquatic environments are increasingly contaminated with various kinds of pollutants, many of which can interfere with hormonal signaling in vertebrates. Through feeding and direct uptake from water and sediments, these endocrine-disrupting contaminants have been found to accumulate in crustaceans living in various aquatic environments. Because of the generally high lipophilicity of organochlorine compounds, these organic contaminants can readily accumulate in the fatty tissue, such as hepatopancreas, of crustaceans. For instance, Mattig et al. (1997) reported the accumulation of organochlorine compounds, including polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs), hexachlorocyclohexanes (HCHs), and hexachlorobenzene (HCB), in the shore crab, Carcinus maenas, and the sand shrimp, Crangon crangon. Organochlorine contaminants, including toxaphene, chlordane and metabolites, HCHs, HCB, dieldrin, and PCBs, were found in the opossum shrimp, Mysis relicta, from the great lakes (Kucklick and Baker, 1998). Heptachlor epoxide, dieldrin, endosulfan, chlordane, DDT and metabolites, and HCHs were found to accumulate in the burrowing crab, Chasmagnathus granulata (Menone et al., 2000). Borga et al. (2002) detected DDTs, PCBs, chlordance, HCB, and HCH in several amphipods from the Arctic Ocean. PCBs, DDTs and metabolites, endosulfan, heptachlor epoxide, HCHs, and HCB were detected in the tissues of the amphipod, Gammarus lacustris, inhabiting a high-altitude lake (Biais et al., 2003). Like organochlorines, polycyclic aromatic hydrocarbons (PAHs), the pollutants from activities of petroleum and smelter industries, are also highly lipophilic and can easily accumulate in crustaceans tissues (Kayal and Connell, 1995; Eickhoff et al, 2003). Besides, cadmium, a metal capable of disrupting estrogen functions in vertebrates (Le Guevel et al., 2000), has been found to accumulate in the tissues of crustaceans in appreciable quantities (Paez-Osuna and Tron-Mayen, 1996; Mattig et al., 1997; Mouneyrac et al., 2001; Turoczy et al., 2001).

Earlier, the possibilities of the adverse effect of environmental chemicals on crustacean molting had been investigated. Weis and Mantel (1976) found a stimulatory effect of p, p' DDT on molting of Uca pugilator. Fingerman and Fingerman (1977) reported the inhibitory effect of the PCB mixture Aroclor 1242, on molting of Uca pugilator. Schimmel et al. (1979) found that blue crabs, Callinectes sapidus, fed oysters contaminated with kepone, molt less frequently than crabs fed kepone-free oysters. Aromatic hydrocarbons benzene (Cantelmo et al., 1981) and dimethylnaphthalene (Cantelmo et al., 1982) were found to delay the molting of juvenile Callinectes sapidus. In recent years, with the emergence of a new subdiscipline of ecotoxicology, endocrine disruption, also called environmental signaling (McLachlan, 2001), new attention is being paid to the disrupting effects of environmental chemicals on crustacean molting. More molt-interfering chemicals have been identified and the pervasiveness of molt-inhibition by xenobiotics has been reexamined. Zou and Fingerman (1997a), in their study on the effects of vertebrate endocrine disrupters on sex differentiation in Daphnia magna, found that estrogenic agents diethylstilbestrol (DES) and endosulfan do not affect male differentiation but delay the molting of this cladoceran. A further study by these investigators found that other environmental chemicals, such as Aroclor 1242, 2,4,5-trichlorobiphenyl (PCB29), and diethyl phthalate, can also inhibit molting of Daphnia magna (Zou and Fingerman, 1997e). Baer and Owens (1999) found that the pesticide methoxychlor delays the molting of Daphnia magna. Snyder and Mulder (2001) reported that exposure of Homarus americanus larvae to the cyclodiene pesticide heptachlor can cause a delay in molting. Molt-inhibition by heavy metal cadmium has also been reported in the estuarine crab, Chasmagnathus granulata (Rodriguez Moreno et al., 2003).

ACTION ROUTES OF MOLT-DISRUPTING XENOBIOTICS

As is mentioned above, a number of xenobiotics that readily accumulate in the tissues of crustaceans can adversely impact molting in crustaceans. Now, the question is: how is crustacean molting adversely affected by environmental chemicals? To seek an answer to such a question, we must first examine the endocrine control of molting in crustaceans. Since the endocrine system for regulation of molting in decapods is best understood, only the endocrine control for molting of these animals is described.