Annelid Endocrine Disruptors and a Survey of Invertebrate FMRFamide-Related Peptides1

SYNOPSIS.

There is a growing body of literature describing the actions of endocrine disruptors on annelids. These pollutants cause decreases in growth and reproductive output, delay sexual maturation, and inhibit the immune system in annelids. More studies are needed to determine the mechanisms that underlie these responses. Most invertebrate endocrine disruptor research focuses on steroids. In recent years many new invertebrate peptide hormones including those related to the molluscan peptide FMRFamide have been identified. Since the storage of these peptides can be inhibited by steroids during insect metamorphosis, they may be affected by endocrine disruptors. Therefore, it is worthwhile to give a brief overview of this peptide family to those studying endocrine disruption in invertebrates with the hope that they may begin to consider these peptides in their future research. In 1977 Price and Greenberg isolated FMRFamide from the cerebral ganglia of the clam, Macrocallista nimbosa. Since then researchers have used bioassays and immunoassays to identify a large number of FMRFamide-related peptides (FaRPs) from many invertebrate phyla. Even more peptides are predicted by the FaRP genes that have been sequenced. FaRPs have a variety of functions and act as neurotransmitters, neuromodulators, or neurohormones. Each function is species and tissue specific. Most FaRP receptors are linked to a second messenger system. However, at least one is a ligand gated sodium channel. On going studies are examining FaRPs from the molecular to organismal level.

INTRODUCTION

This presentation will discuss two topics. The first part will review the effects of endocrine disruptors on annelids. The second part will consider the ever increasing family of invertebrate neuropeptides related to FMRFamide. Although there is currently no evidence that suggests these neuropeptides are targets of endocrine disruption in annelids or any other invertebrate, in insects the levels of these peptides can be regulated by steroid hormones during metamorphosis. Therefore, endocrine disruptors may have an effect on these peptides and this review can serve to bring them to the attention of researchers in the field of invertebrate endocrine disruption.

ANNELID ENDOCRINE DISRUPTORS

There are many chemicals which have been implicated in endocrine disruption in invertebrates. These include heavy metals, polychlorinated biphenyls (PCBs), alkylphenols, insectisides, synthetic and natural vertebrate steroids, and industrial effluents that contain chemical mixtures (Depledge and Billinghurst, 1999). Most studies have examined the uptake, accumulation, and toxicity of these materials in annelids; however, there are some studies that have examined the physiological impacts of these substances on the animals.

Heavy metals can affect the density, viability, cocoon production, growth and sexual development of terrestrial annelids (Spurgeon et al., 1994). Juvenile worms are more sensitive to these pollutants. When juvenile specimens of the earthworm Eisenia fetida are exposed to zinc they have a decreased growth rate, delayed sexual maturation, and a reduction in cocoon production (Spurgeon and Hopkin, 1996). Adult worms exposed to the same doses displayed none of these abnormalities. The researchers suggest that these responses may be due to the excess energy the animals must expend to void these metals, however they may also elicit other changes in physiology. Metals may also affect invertebrate immune systems. Copper has been shown to suppress immune system function in E. fetida by decreasing phagocytosis in the coelomocytes '(Burch et al., 1999).

Tributyltin (TBT) is the active ingredient in marine antifouling paints. Hagger et al. (2002) exposed embryos and larvae of the polychaete Platynereis dumerilii to various TBT concentrations. The results showed that TBT had dose-dependent genotoxic, cytotoxic, and developmental effects on these worms. When juveniles of the polychaete Armandia brevis, a deposit feeder, were exposed to sediment-associated TBT growth was inhibited by twenty-five percent (Meador and Rice, 2001).

Herbicides and pesticides also can affect reproduction. When the earthworm Eisenia andrei was exposed to either the herbicide terbuthylazine or the pesticide carbofuran there was a concentration-dependent decrease in cocoon production and biomass (Viswantahan, 1997). Interestingly, the offspring of the terbuthylazine exposed worms exhibited enhancement of growth, development, and cocoon production when exposed to terbuthylazine. The offspring from parents exposed to carbofuran also had enhanced growth when treated with carbofuran; however cocoon production was below control values. When the larvae of the estuarine polychaete, Streblospio benedicti were treated with the pesticide disulfan there was a significant decrease in settlement and juvenile growth (Chandler and Scott, 1991).

Nonylphenol is an alkylphenol that mimics estrogen and disrupts sexual development in some invertebrates (Depledge and Billinghurst, 1999). Bettinetti and Provini (2002) exposed the benthic annelid Tubifex tubifex to 4-nonylphenol in the sediment. The production of cocoons and young worms decreased with increasing concentrations of nonylphenol. A histological examination of the clitellum revealed that damage occurred to both male and female gonads.