Hormonal Signaling in Cnidarians: Do We Understand the Pathways Well Enough to Know Whether They Are Being Disrupted?
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Ecotoxicology (2007) 16:5–13 DOI 10.1007/s10646-006-0121-1 Hormonal signaling in cnidarians: do we understand the pathways well enough to know whether they are being disrupted? Ann M. Tarrant Accepted: 4 October 2006 / Published online: 18 January 2007 Ó Springer Science+Business Media, LLC 2007 Abstract Cnidarians occupy a key evolutionary posi- level, and the potential for signal disruption is largely tion as basal metazoans and are ecologically important unknown. This review considers the state of knowledge as predators, prey and structure-builders. Bioregulato- on hormonal signaling, chemical bioregulation and ry molecules (e.g., amines, peptides and steroids) have signal disruption in cnidarians, focusing particularly on been identified in cnidarians, but cnidarian signaling advances since the publication of the results of the pathways remain poorly characterized. Cnidarians, Endocrine Disruption in Invertebrates: Endocrinology, especially hydras, are regularly used in toxicity testing, Testing and Assessment workshop (deFur et al. 1999). but few studies have used cnidarians in explicit testing for signal disruption. Sublethal endpoints developed in cnidarians include budding, regeneration, gametogen- Why cnidarians: diversity, evolutionary significance esis, mucus production and larval metamorphosis. and ecological role Cnidarian genomic databases, microarrays and other molecular tools are increasingly facilitating mechanis- The phylum Cnidaria contains four extant classes, the tic investigation of signaling pathways and signal Hydrozoa (e.g., hydras), Scyphozoa (‘‘true’’ jellyfishes), disruption. Elucidation of cnidarian signaling processes Cubozoa (box jellies) and Anthozoa (e.g., corals and in a comparative context can provide insight into the anemones). The number of cnidarian species has not evolution and diversification of metazoan bioregula- been rigorously assessed, but is estimated to be around tion. Characterizing signaling and signal disruption in 10,000 (Brusca and Brusca 1990). A definitive cnidar- cnidarians may also provide unique opportunities for ian species inventory is currently being established evaluating risk to valuable marine resources, such as (D.G. Fautin, personal communication, December 30, coral reefs. 2005), and progress to date indicates that the subclass Hexacorallia (that includes anemones and corals) Keywords Bioregulation Á Cnidaria Á Coral Á alone contains 2,899 valid species (Fautin 2005). Endocrine Á Signal disruption Cnidarians are usually classified as basal metazoans that form a sister group to the bilaterians, although these ancient evolutionary relationships are a subject Introduction of active research (Holland 1998; Gro¨ ger and Schmid 2001; Martindale 2005; Rokas et al. 2005). Because of Hormonal signaling in cnidarians has not been fully their basal position and simple organization, it is characterized on either a molecular or a biochemical sometimes assumed that bioregulation of cnidarian physiology must also be simple and that vertebrate features absent from model protostomes (e.g., nema- & A. M. Tarrant ( ) todes and insects) are likely to have evolved after the Woods Hole Oceanographic Institution, Mailstop 32, Woods Hole, MA 02543, USA divergence of the protostomes and the deuterostomes. e-mail: [email protected] Somewhat surprisingly, a comparative study indicated 123 6 Tarrant that more than 10% of genes shared between cnida- circulation (Xian et al. 2005). The role of hormonal or rians and humans have apparently been lost from pheromonal signals in regulating jellyfish blooms is model protostomes (Kortschak et al. 2003). Thus, it is unknown. Similarly, it is unknown whether environ- not possible to use conserved features between verte- mental chemicals affect jellyfish signaling and bloom brates and model invertebrates alone to predict the dynamics. complexity of cnidarian signaling processes (Miller Cnidarians also provide three-dimensional structure et al. 2005; Technau et al. 2005). Further, elucidation of to benthic ecosystems, most notably tropical coral cnidarian signaling processes in a comparative context reefs. Reef ecosystems provide habitat for diverse taxa, can provide insight into the evolution and diversifica- protect shorelines and provide commercial and recre- tion of metazoan bioregulation. ational resources for humans. Scleractinian coral biol- In addition to their key evolutionary position, ogy is of particular interest due to the importance of cnidarians are also important as both predators and corals in maintaining tropical reefs and increasing prey in aquatic ecosystems. Gelatinous cnidarians human concerns about reef degradation (Gardner et al. serve as prey for diverse taxa including other cnidari- 2003; Hughes et al. 2003; Pandolfi et al. 2003). The ans, fishes and turtles. While gelatinous cnidarians are chemical signals that regulate coral gametogenesis and sometimes regarded as relatively unpalatable or of low spawning are poorly understood, and it is unknown nutritional value (e.g., Avent et al. 2001), cnidarians whether environmental chemicals may disrupt these may be widely underestimated as prey sources because signals. they tend to be rapidly digested (Arai et al. 2003; Arai 2005). As predators, cnidarians can dramatically change the composition of plankton and may impair Routes of exposure fisheries yield through dietary overlap and direct predation (Arai 1988; Purcell and Arai 2001; Purcell Cnidarians may be exposed to chemicals through and Sturdevant 2001). As an example, the hydroid, uptake of dissolved compounds, ingestion of food Clytia gracilis, can remove up to 40% of copepod particles, or contact with suspended solids and sedi- nauplii daily production in a region of the Georges ments. The relative importance of these routes of Bank (Atlantic coast of the United States, Madin et al. exposure varies with life history parameters, particu- 1996). Copepod nauplii are a primary food source for larly habitat and mode of nutrition. Adult cnidarians larval cod and haddock, so hydroids can significantly may be benthic or pelagic, cnidarian gametes may be reduce food availability and may also prey directly on brooded or spawned, and larvae spend varying times the larval fish (Madin et al. 1996). Suspension-feeding (hours to months) in the water column. Cnidarians may benthic cnidarians also impact planktonic composition be entirely carnivorous or may contain algal symbionts and may play an important role in benthic–pelagic that fill some or all of their energetic needs. Exposure coupling. For example, a Mediterranean gorgonian was of scleractinian corals to chemicals is of particular found to consume large numbers of eggs and inverte- concern because reef ecosystems are often located near brate larvae, particularly larval bivalves, with unknown highly populated coasts and may be exposed to effects on bivalve recruitment and population dynam- contaminants through riverine input, sewage effluent, ics (Rossi et al. 2004). run-off, groundwater discharge, marine activities and Jellyfish (medusae, which may be hydrozoan, spills (reviewed by Peters et al. 1997). scyphozoan or cubozoan) aggregations or blooms are Cnidarians can take up dissolved chemicals through common episodic events, and the frequency and extent diffusion. The freshwater Hydra spp. are commonly of blooms may be increasing (Mills 2001). Jellyfish used (Blaise and Kusui 1997; Holdway et al. 2001; blooms can have major ecological consequences. For Pascoe et al. 2003) and other cnidarians are occasion- example, an exotic jellyfish recently accounted for 98% ally used (e.g., anemones Mercier et al. 1997; colonial of total fisheries sampling in the Yangtze estuary in hydroids Chicu et al. 2000) in toxicity testing with China (summarized by Xian et al. 2005). Jellyfish dissolved contaminants. One explanation for the blooms are caused and maintained by a combination of observed sensitivity of hydras to a range of chemicals physical and poorly understood behavioral and phys- is their diploblastic organization, which allows all cells iological processes (Lotan et al. 1994; Purcell et al. potentially to be exposed to the surrounding medium 2000; Graham et al. 2001; Lucas 2001). Jellyfish blooms and associated contaminants (Ingersoll et al. 1999). may also be aggravated by anthropogenic factors (Mills Similarly, Peters et al. (1997) suggested that reef- 2001) including overfishing of competitors (Brodeur building corals might be particularly sensitive to et al. 2002), eutrophication and changes in estuarine lipophilic contaminants because corals typically 123 Hormonal signaling in cnidarians 7 possess thin lipid-rich tissues, facilitating direct uptake. determine whether accumulated lipophilic contami- Incubations with radiolabeled compounds have dem- nants are mobilized during spawning events. In addi- onstrated that corals can remove estrogens (Tarrant tion to organic chemicals, heavy metals can also et al. 2001), petroleum hydrocarbons (Solbakken et al. accumulate in cnidarian tissues (Mitchelmore et al. 1984), and benzo [a]pyrene (Kennedy et al. 1992) from 2003) and can be transferred up the food chain. For the surrounding seawater. example, high levels of cadmium and other metals in Few studies have examined the bioavailability of leatherback turtles are thought to be derived from particle-associated contaminants to cnidarians. Harter their jellyfish prey (Caurant et al. 1999). and Matthews (2005) suggested that the burrowing anemone Nematostella vectensis could be used in sediment toxicity testing.