The mechanisms that enable animals (and plants) to survive in reducing environments have been a fertile area for discovery of novel physiological and biochemical capabilities. Most have centered around adaptation to sulphides (e.g., Powell & Somero 1986, Arp et al. 1987, 1995, Julian et al. 1999a,b, Lee et al. 1996, 1999a) because seep and vent animals may experience exceptionally high sulphide concentrations within sediments (e.g., Figure 9). Hydrogen sulphide interferes with aerobic metabolism by disrupting the transport of oxygen by haemoglobin and inhibiting ATP production by the electron transport chain through binding to cytochrome c oxidase (CytOx) (Somero et al. 1989). Despite its toxicity, some animals have been found to tolerate relatively high sulphide levels. Adaptation to sulphides include (1) the removal of sulphide at the body wall through a layer of sulphide-oxidizing bacteria, and/or enzymatic sulphide oxidation, (2) sulphide-insensitive haemoglobin, (3) reversible sulphide binding to blood components, (4) mitochondrial sulphide oxidation to less toxic compounds (e.g., thiosulphate) with ATP synthesis and (5) reliance on anaerobic respiration at high sulphide levels (Powell et al. 1979, Grieshaber & Volkel 1998). Symbiotic sulphide oxidation is a widespread adaptation present in siboglinid annelids (formerly pogono-phorans McHugh 1997, Rouse & Fauchald 1997, Halanych et al. 1998, 2002) and a host of bivalves and annelids occurring at hydrothermal vents and methane seeps (Fisher 1990, Childress & Fisher 1992). In siboglinids, sulphide tolerance has been hypothesized to be driving the evolution of the clade (Schulze & Halanych 2003). Dorvilleid polychaetes, which exhibit high species richness at methane seeps and whale falls where sediments have porewater sulphide concentrations >10 mM, may also have radiated in sulphidic environments (G. Mendoza et al. personal communication). Differential sulphide tolerances also may drive differentiation in members of the genus Capitella (Gamenick et al. 1998). Capitella exhibits a preference for seep sediments at shelf depths off California (Levin et al. 2000).
For animals that rely on oxidation of reduced compounds by symbiotic bacteria, acquisition of oxygen and sulphide (or methane) presents a challenge. Adaptations may include separating the acquisition of oxygen and sulphide in space (by extending the body between environments, see Dufour & Felbeck 2003 for an extreme example) or in time (by moving between environments) (Fisher 1996). Seep vestimentiferans obtain oxygen from the plume and sulphide through diffusion into a 'root'-like posterior extension that penetrates deeply into the sediment (Julian et al. 1999a, Freytag et al. 2001). This adaptation allows them to persist in environments where oxygen and sulphide may be separated by 50 cm or more. Vesicomyid clams also acquire oxygen sulphide from different places, albeit over shorter distances (Childress et al. 1991). Smaller taxa (e.g., nematodes and oligochaetes) may migrate vertically between oxygen, sulphide and nitrate sources in sediments, storing one or the other. Large vacuole-bearing sulphur bacteria (e.g., Thioploca) are able to do the same, gliding vertically in sheaths. In contrast, some animals may behave in a way that promotes the production of sulphide. Downward pumping of seawater sulphate by clams (Wallmann et al. 1997) will enhance sulphate reduction, providing symbionts with a continuous source of sulphide.
Investigations of morphological adaptations that enhance fitness in sulphidic sediments have been limited mainly to megafauna. Among meiofauna, body morphology appears to reflect adaptation to limited oxygen and to be correlated with the amount of dissolved sulphide in the environment. Jensen et al. (1992) reported all thiobiotic nematodes from the East Flower Garden Brine seep to exhibit body elongation, a high surface area: volume ratio and a short body radius, relative to oxybiotic nematodes in the area.
Megafaunal activities within seep sediments (root and foot penetrations, burrowing, pumping and sulphide extraction) are certain to have significant consequences for other microbes and infauna. Dattagupta (2004) suggests that release of sulphate by roots of seep vestimentiferans in the Gulf of Mexico enhances sulphate reduction locally and thus the production of sulphide required by their symbionts. 'Second-order' interactions between megafauna and seep infauna have rarely been examined but are particularly likely to affect the distribution of Foraminifera and metazoan meio-fauna. Research in shallow-water and bathyal non-seep sediments demonstrates major influence of macrofaunal and megafaunal animal activities on the distribution and nutrition of other infauna (Reise 1985, Levin et al. 1997, Olaffsson 2003). Microbial mats may also modify the sediment geochemistry and substratum in ways that affect associated biota (Robinson et al. 2004). Given the limited oxygen and highly sulphidic nature of seep sediments, there should be extensive biotic control over geochemical microenvironments that determines physiological status, food supply, settlement cues and other ecological features for microbes and smaller infaunal invertebrates.
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