In hot and cold water: differential life‐history traits are key to success in contrasting thermal deep‐sea environments

Abstract

Summary Few species of reptant decapod crustaceans thrive in the cold‐stenothermal waters of the Southern Ocean. However, abundant populations of a new species of anomuran crab, Kiwa tyleri, occur at hydrothermal vent fields on the East Scotia Ridge.As a result of local thermal conditions at the vents, these crabs are not restricted by the physiological limits that otherwise exclude reptant decapods south of the polar front.We reveal the adult life history of this species by piecing together variation in microdistribution, body size frequency, sex ratio, and ovarian and embryonic development, which indicates a pattern in the distribution of female Kiwaidae in relation to their reproductive development.High‐density ‘Kiwa’ assemblages observed in close proximity to sources of vent fluids are constrained by the thermal limit of elevated temperatures and the availability of resources for chemosynthetic nutrition. Although adult Kiwaidae depend on epibiotic chemosynthetic bacteria for nutrition, females move offsite after extrusion of their eggs to protect brooding embryos from the chemically harsh, thermally fluctuating vent environment. Consequently, brooding females in the periphery of the vent field are in turn restricted by low‐temperature physiological boundaries of the deep‐water Southern Ocean environment. Females have a high reproductive investment in few, large, yolky eggs, facilitating full lecithotrophy, with the release of larvae prolonged, and asynchronous. After embryos are released, larvae are reliant on locating isolated active areas of hydrothermal flow in order to settle and survive as chemosynthetic adults. Where the cold water restricts the ability of all adult stages to migrate over long distances, these low temperatures may facilitate the larvae in the location of vent sites by extending the larval development period through hypometabolism.These differential life‐history adaptations to contrasting thermal environments lead to a disjunct life history among males and females of K. tyleri, which is key to their success in the Southern Ocean vent environment.We highlight the complexity in understanding the importance of life‐history biology, in combination with environmental, ecological and physiological factors contributing to the overall global distribution of vent‐endemic species.

Limitations in the Use of Archived Vent Mussel Samples to Assess Genetic Connectivity Among Seafloor Massive Sulfide Deposits: A Case Study with Implications for Environmental Management

“…SMS deposits form through hydrothermal activity and exhibit a patchy distribution along seafloor tectonic margins, with deposits occurring on average every 100 km along the oceanic plate boundaries (Hannington et al, 2011). Active deposits support chemosynthetic communities restricted to hydrothermally active areas; many of these hydrothermal fauna have limited distributions and are endemic to one region, such as the crab Kiwa tyleri, endemic to the East Scotia Ridge in the Southern Ocean (Marsh et al, 2012(Marsh et al, , 2015 and the gastropod Ifremeria nautilei, restricted to three basins in the southwest Pacific (Bouchet and Warén, 1991;Thaler et al, 2011). Such limited distributions make these species particularly vulnerable to disturbance.…”

Evidence for protracted and lecithotrophic larval development in the yeti crab Kiwa tyleri from hydrothermal vents of the East Scotia Ridge, Southern Ocean

“…The reasons for this remain unknown, but may relate to the highly un stable thermal and chemical conditions prevailing at vent chimneys, with regard to steep chemical and thermal gradients (Fisher et al 1988, Desbruyeres et al 2001, Luther et al 2001, which may negatively affect embryogenesis. Given low female fecundity (maximum N = 175 and N = 207 developing embryos, at E2 and E9, respectively; Marsh et al 2015) and the high maternal investment into offspring demonstra ted here, optimising reproductive success appears key to the species' ecology. Larval and early juvenile lecithotrophy, as discussed earlier, enables the species to employ a hypometabolic developmental mode of life whilst off the vent site.…”

“…Ovigerous females retrieved were found showing unusually (yellowbrown) dark carapace colour (see Marsh et al 2015), indicating hydrothermal deposition on the exoskeleton. Specimens also showed black spots or areas along carapace margins and on leg segments, indicative of necrosis.…”

“…The ambient water temperature at this latitude was approximately −1.3°C. For further de scription of the vent field, chemical and biological characteristics, please consult Rogers et al (2012) and Marsh et al (2012Marsh et al ( , 2015.…”

The crabs that live where hot and cold collide

“…Marsh et al . () found that this species, very shortly to be officially named Kiwa tyleri (Thatje et al . in press), inhabits different zones of the vent field depending on their sex and their reproductive stage.…”