Date Published: February 7, 2019
Publisher: Public Library of Science
Author(s): Jia-Jang Hung, Shao-Hung Peng, Chen-Tung Arthur Chen, Tsui-Ping Wei, Jiang-Shiou Hwang, Hans-Uwe Dahms.
The vent crab Xenograpsus testudinatus was firstly discovered in 2000 at the hydrothermal vent field off the coast of Kueishan Island. The present study attempts to understand the adaptive reproduction of this crab living in an extreme environment by examining its spatial and temporal distribution and isotopic signatures. The seasonal variation of the female-male ratio suggests that ovigerous females may migrate from beneath the vent orifice to the vent-periphery region to release their larvae to avoid the larvae contacting high toxic plumes, and then returns to the vent orifice habitat. We used variation of the isotopic crab signatures as indicators for this unique female migration. Our results showed that this vent crab evolved an adaptive modulation of reproductive behavior to successfully survive and propagate in an oceanic shallow hydrothermal vent field.
Hydrothermal vents exist in locations ranging from coastal ridges to the abyss. Light is most likely absent at depths beyond 200 meters, and biological communities are dominated by numerous symbiotrophic forms, sustained by chemosynthesis using sulfide compounds as their primary energy source [1, 2]. In contrast, shallow hydrothermal vents may erupt within the euphotic zone and the species living around them are not obligate taxa; few organisms exist near these shallow vents [2, 3].
In this study we analyzed seawater, sediment, and biological samples collected by researchers through three independent samplings from shallow water hydrothermal vents, conducted in April 2010, July 2010, and July 2011 at four sites (Fig 1). The crab Xenograpsus testudinatus and linked organisms were caught in April and July 2010. Crabs were not caught at site ‘B’ in the April sample because of extremely bad weather. Site ‘A’, with a vent orifice, is located on the eastern side of Kueishan Island. Site ‘B’ is also a vent location, emitting fluids likely from crevices, but located some distance from site ‘A.’ Meanwhile, site ‘C’ is located on the edge of the vent field where X. testudinatus can be found with other organisms. Finally, site ‘D’ is a coral reef area located in the north of Kueishan Island where no vent crabs can be found. Additionally, a home-made sediment trap (S1 Fig) was deployed in both vent field and coral reef sites for eight days during September 2011 to collect settling materials.
Comparing the female ratio and ovigerous female ratio of the vent crabs at the three collection sites during different seasons (Fig 2) demonstrated that the crabs from beneath the vent orifice (site ‘A’) have total female and ovigerous female ratios of 22% and 0% in April, respectively. The total female and ovigerous female ratios increased to 65% and 2.04% in July 2010. In contrast, the total female and ovigerous female ratios at site ‘C’ in April were 72% and 46.15%, respectively. Both ratios decreased to 48% and 28.87%, respectively, in July 2010. The results indicate that spring is the main reproductive season of X. testudinatus, and the mature female crab may exhibit unique seasonal-migration behavior during this period. The isotopic signatures of collected female and male crabs also indicated the unique migratory behavior of female crabs (Fig 3).
Analysis of stable isotopic signatures of δ13C and δ15N is a common method used to identify the food web structure of organisms. Since the variation of δ13C and δ15N isotopic signatures reflects the longer term changes in food sources coming from the same food organism, these signatures were also applied to study the geographic migration or translocation of marine organisms, including crustaceans [13, 14]. δ13C and δ15N data of different organisms collected from Kueishan Island (Fig 3) suggested that the food web structures consisted of primary producers and secondary consumers. For the female crab, the isotopic signatures of specimens collected from site ‘A’ were categorized into groups ‘B’ and ‘C’ but not group ‘A’. Apparently, the non-ovigerous female individuals at site ‘A‘ were recent migrants from sites ‘B’ or ‘C’ in July 2010. This adaptive behavior may be related to the physical, chemical and biological characteristics of their habitats.