Ecotoxicology (2007) 16:61–81 DOI 10.1007/s10646-006-0115-z Crustacean endocrine toxicology: a review Gerald A. LeBlanc Accepted: 4 October 2006 / Published online: 18 January 2007 Ó Springer Science+Business Media, LLC 2007 Abstract Crustaceans are major constituents to aqua- differentiation. Population studies have revealed dis- tic ecosystems that provide a variety of ecological and ruptions in crustacean growth, molting, sexual devel- economic services. Individual crustacean species are opment, and recruitment that are indicative of adept at occupying diverse niches and their success, in environmental endocrine disruption. However, envi- part, stems from neuro-endocrine signaling cascades ronmental factors other that pollution (i.e., tempera- that regulate physiology in response to environmental ture, parasitism) also can elicit these effects and and internal cues. Peptide hormones are major signal definitive causal relationships between endocrine dis- transducers in crustaceans. The crustacean hypergly- ruption in field populations of crustaceans and chem- cemic hormone family of peptides regulates various ical pollution is generally lacking. aspects of growth, reproduction, and metabolism. These peptides may function as the terminal hormone Keywords Crustacean Á Endocrine Á Ecdysteroid Á to regulate some physiological activities or may func- Terpenoid Á Methyl farnesoate Á Intersex tion as intermediates in a signaling cascade. Ecdyster- oids and terpenoids are two major classes of terminal signaling molecules in these cascades. Hormones from Introduction these two classes function independently or in concert to regulate various processes. Ecdysteroid signaling is The planet Earth is the domain of the arthropods and subject to toxicological disruption through distur- the aquatic environments are dominated by members bances in ecdysteroid synthesis or binding of toxicants of the arthropod subphylum Crustacea. Arthropod-like to the ecdysteroid receptor. Methyl farnesoate is the creatures (anomalocarids) first appear in the fossil major terpenoid hormone of crustaceans and also is record during the late Precambrian period. Early in the susceptible to disruption by environmental chemicals. subsequent Cambrian period (~500 million years ago), However, the methyl farnesoate signaling pathway is when speciation occurred at an unparalleled rate, poorly understood and only limited mechanistic con- crustacean-like trilobites emerged in abundance, firmation for disruption of this endocrine signaling accompanied by minute creatures of undisputed crus- pathway exists. Disruption of the ecdysteroid/terpe- tacean lineage (i.e., Bradoriid ostracods of the Chen- noid signaling pathways in crustaceans has been jiang fauna) (Hou and Bergstrom 1997) (Fig. 1). associated with aberrations in growth, metamorphosis, Crustaceans have undergone dynamic species radiation reproductive maturation, sex determination, and sex through evolutionary time (Brusca and Brusca 2003). The first decapods to appear in the fossil record were free swimming shrimp-like creatures of the Devonian G. A. LeBlanc (&) period (~400 million years ago). Benthic, lobster- Department of Environmental and Molecular Toxicology, shaped decapods appear in the record around the North Carolina State University, 27695-7633, Raleigh, NC, USA Triassic-Permian border (~250 million years ago) e-mail: [email protected] following the extinction of the previously abundant 123 62 G. A. LeBlanc Fig. 1 Phylogeny of Anomalocarda contemporary crustacean classes Agnostida (trilobites) Subphylum: Crustacea Class: Remipedia Class: Cephalocarida Class: Branchiopoda Class: Maxillopoda Class: Malacostraca trilobites. The true crabs are late editions to the interact with neuro-endocrine signaling cascades, crustacean species repertoire, having appeared in the resulting in signal perturbations (Colborn and Clement fossil record roughly 1 million years ago (Cretaceous 1992). Such altered signaling can result in modifications period). to development, maturation, reproduction, and other Over 66,000 crustacean species are known to exist neuro-endocrine-regulated processes that hinder pop- today. Members of this subphylum (Phylum: Arthro- ulation sustainability (Spence et al. 1990). Continued poda) are largely aquatic, though a few species are exposure to such environmental contaminants can exclusively terrestrial (i.e., some Isopoda), while others result in the emergence of genetically modified popu- utilize both the aquatic and terrestrial environment lations that can tolerate this new environment (Huet (i.e., some Decapoda). Crustaceans are the major et al. 1996). The evolution of contaminant-tolerant constituent of zooplankton, either as minute species species is reasonably common among arthropods (i.e., (i.e., some Branchiopoda and Maxillopoda) or as larval insecticide-resistant insect populations; ffrench-Con- forms of larger species (i.e., Malacostraca). The largest stant et al. 2004) due to the high fecundity and short crustaceans include the American lobster (Homarus generation time of many arthropod species. However, americanus) which can attain a body length of ~1m just as trilobites and other species encompassing 85% and the giant spider crab (Macrocheira kaempferi) of the marine species succumbed to environmental which has a claw span of up to ~3 m (Barnes 1987). changes of the Permian period, adaptation to chemicals The diversity in crustacean morphology (Fig. 2) that interfere with neuro-endocrine signaling is likely reflects their success in occupying diverse ecological to be the exception rather than the rule among niches. Incumbent in this diversification has been the contemporary species. Herein, basic neuro-endocrine evolution of various strategies for detecting environ- signaling among crustaceans is reviewed along with mental cues and using these signals to regulate aspects documentation (both laboratory and field) of pertur- of survival (i.e., development, maturation, and repro- bations in such signaling by environmental influences. duction) that ensure population sustainability. Neuro- Finally, the potential utility of crustaceans to serve as endocrine pathways are critical to transducing these sentinels of environmental endocrine disturbance is signals (Beltz 1988). Changes in these signaling cas- discussed. cades through mutation may prove advantageous to a population by enhancing sustainability in a changing environment, resulting in the evolution of the popula- Crustacean physiology and systematics tion. More likely, such changes have no effect (neutral) or prove disadvantageous, conferring some liability to The ancestral pre-crustacean Anomalocarus exhibited sustainability, and are purged from the population little resemblance to any contemporary crustaceans gene pool. with its wing-like formation of swimming appendages Changes in signaling cascades also can occur due to and toothed, circular mouth (view a ‘‘swimming’’ environmental influences. Human activities over the Anomalocarus at http://www.calstatela.edu/faculty/ac- past half-decade have introduced a myriad of chemi- olvil/sediments.html). Morphologies diverged consid- cals into the environment that have the potential to erably among and even within the crustacean classes 123 Crustacean endocrine toxicology 63 Fig. 2 The major morphotypes among the Crustacea. Significant variability in structure exists even within classes though all contemporary crustaceans share several Critical body parts of crustaceans are (with a few common characteristics (Barnes 1987; Smith 2001; exceptions) shielded within a chitinous carapace. Brusca and Brusca 2003) (Fig. 2). The body of most Crustaceans typically possess one or two compound crustaceans is composed of three parts, a head (ceph- eyes and, depending upon the species and life stage, a alon), a thorax and an abdomen, though the thorax and simple eye call an ocellus. All crustaceans possess an abdomen are indistinguishable in some species and, open circulatory system. together, are often referred to as a trunk. Each body According to most contemporary phylogenic con- part consists of multiple segments and each segment structs, using both morphometric and DNA analyses, commonly bears a pair of appendages. Head segments modern crustaceans are segregated into five classes bear the first antennae (minor antennae or antenn- (Figs. 1, 2); although, inter- and intra-class relation- ules), second antennae (major antennae), mandibules, ships remain equivocal (Brusca and Brusca 2003; maxillules, and maxillae. The thorax and abdomen Koenemann and Jenner 2005). Crustaceans commonly bear appendages that contribute to various functions encountered by field biologists can typically be including movement, respiration, and reproduction. assigned to one of three classes: Branchiopoda, 123 64 G. A. LeBlanc Maxillopoda, and Malacostraca. Basic body forms shrimp have a bivalved carapace along with concentric associated with the different crustacean classes are growth striations that confer significant overt resem- depicted in Fig. 2. blance to small bivalved mollusks (i.e., clams). Clam shrimp are typically bottom dwellers that filter organic Class: Branchiopoda particles from the water column or scrapped off of bottom substrates. Clam shrimps have limited swimming These small invertebrates are dominant crustacean mobility. residents of ephemeral habitats. Most are freshwater inhabitants, have a short life span, and are capable of Water fleas producing desiccation-resistant resting eggs. The trunk appendages of the