Isotopic niche differentiation in benthic consumers from shallow-water hydrothermal vents and nearby non-vent rocky reefs in northeastern Taiwan
Introduction
There are twenty-two shallow-water hydrothermal vents (SVs; depth < 200 m) found globally (Zhang et al. 2020). Since initial research began in the 1970s (Takeda and Kubata 1977), many aspects of these unique regions have been investigated. These include biodiversity (e.g., Aegean Sea, Greece; Thiermann et al. 1997), community structure (e.g., Tyrrhenia Sea, Italy; Hall-Spencer et al. 2008), and trophic structure (e.g., Kueishan Islet, Taiwan; Wang et al. 2014). It is well understood that the waters surrounding these vents are enriched with nutrients and heavy metals (e.g., Zhang et al. 2020), primarily containing reduced sulfur compounds, methane, and hydrogen gas; these vent emissions can affect ambient biota (Jeng et al. 2004). Despite SVs having been explored for decades, there is a lack of studies that compare the food webs of SVs to nearby non-vent (NV) ecosystems.
In Taiwan, SVs are located along the northeastern coast, near Kueishan (KS) Islet (Fig. 1). There is a cluster of over 30 vents at depths of 10 to 20 m within a 0.5 km2 area (Chen et al. 2005a). The sulfur-rich plumes emitted from the SV are usually white or yellow. These vents register some of the most extreme pH values (1.52) and temperatures (116 °C) in the world (Chen et al. 2005a, b). Discharged gas bubbles contain carbon dioxide, nitrogen, oxygen, sulfur dioxide, and hydrogen sulfide (Yang et al. 2005). Micro- and macrofauna found here include Epsilonproteobacteria, Gammaproteobacteria, filamentous bacteria, red algae, hexacoral (Tubastraea aurea), sea anemones (Anthopleura spp.), snails (Anachis misera and Nassarius sp.), chitons, serpulid polychaetes, and vent crabs (Xenograpsus testudinatus) (Chan et al., 2016, Chang, 2006, Chen et al., 2015, Jeng et al., 2004, Tang et al., 2013, Wang et al., 2014, Wang et al., 2015). The SV benthic communities near KS Islet were reported to have three trophic levels (Chang et al., 2018, Wang et al., 2014).
The northeast coast of Taiwan is characterized by rocky reefs (Dai, 2018, Huang, 1999). There are 153 species of stony corals along the northeastern coast (Jeng et al. 1997), and 89 of which can be found near KS Islet (Hwang and Li 2003). At the southwestern end of KS Islet, coral coverage ranges from 30 to 90%, and 134 fish species have been documented (Huang 2007). Based on a trophic study conducted within Kuosheng Bay in northern Taiwan (Lin et al. 2004), the source of organic carbon in this rocky reef ecosystem was predominately from primary producers and detritus. The 2nd trophic level was comprised of barnacles, gastropods, bivalves, holothuroids, and detritivorous fish. Carnivorous zooplankton, zooplanktivorous fish, and benthic-feeding fish occupied the 3rd trophic level, and piscivorous fish was at the 4th trophic level.
Trophic niche width of animals is strongly dependent on food resources (Layman et al. 2007a), whereby if resources are scarce, niche width expands to include alternative resources. In the Caribbean Sea off the coast of Mexico, herbivores on degraded reefs (i.e., a reef with increased algal cover) occupied a broader niche width than those in non-degraded reefs (Morillo-Velarde et al. 2018). In the benthic communities of Comau Fjord (Chile), the niche width of grazers from X-Huinay (chemosynthetic site) was broader and more heterogeneous than those from Punta Gruesa (NV site; Zapata-Hernández et al. 2014). Along the northeast coast of Taiwan, the benthic food web in SVs (Chang et al. 2018) off KS Islet exhibited chemosynthetic and photosynthetic production. Chang et al., 2018, Jeng et al., 2004 suggest that dead zooplankton killed by sulfurous plumes is the primary food source for benthic vent crabs (X. testudinatus). Although benthic communities may benefit from additional food sources, they may also be exposed to harmful vent fluids. However, comparisons of trophic structure and niche width of benthic organisms with different feeding guilds between this unique ecosystem and nearby non-vent rocky reefs (NV) are unexplored.
Natural biological tracers, such as stable isotopes of carbon (δ13C) and nitrogen (δ15N), are often used in trophic ecology studies to elucidate feeding relationships between species (Levin 2005). Primary producers tend to use lighter inorganic carbon and nitrogen in photosynthesis and consequently produce lower values than sources of inorganic carbon and nitrogen (Fry 2007). In consumers, through processes of assimilation, increases in stable isotope values based on trophic level for δ13C (0.0–1.3‰) and δ15N (1.4–5‰) (DeNiro and Epstein, 1978, DeNiro and Epstein, 1981, McCutchan et al., 2003, Post, 2002) allow for estimation of trophic position, niche width, and contribution of potential food sources to various consumers in the food web (Cabana and Rasmussen, 1996, Carlier et al., 2007).
We aimed to understand better the benthic community's trophic structures in SVs and nearby NV rocky reefs. Specifically, we compared the carbon and nitrogen stable isotope compositions, trophic position, and isotopic niche width of consumers representing different feeding guilds from SV and NV habitats to evaluate the chemosynthetic production and dead zooplankton contribution to the vent ecosystem.
Section snippets
Sampling sites
This study focused on examining the benthic community in SV and NV; two sites were assessed in each habitat. Details of the sampling sites are listed in Table 1.
The SV sites included White vent (WV, 24.83404 N, 121.96172 E) and Yellow vent (YV, 24.83553 N, 121.96361 E), which are located southeast of KS Islet (Fig. 1). At WV, white fluids are emitted from a 2 m wide hole surrounded by rocks. The ambient substrate is sand with many deposited sulfur globules (~0.05–0.10 cm in diameter). At YV,
Results
A total of 172 samples from WV, YV, Tail, and Dali, were classified into 20 groups (Table 2 and S1). The numbers of examined species obtained from the four sites were 40, 6, 25, and 56, respectively (Table S2). Species diversity was lowest at YV. The seven species present in both SV and NV habitats include the fish Prionurus scalprum, snails Thylacodes dentiferus, Bostrycapulus gravispinosus and Ergalatax contractus, macroalgae Ulva lactuca and Codium intricatum, and Sargassum spp. Within SV
Discussion
The trophic structure in both SV and NV was comprised of four trophic levels. The range of carbon and nitrogen stable isotope values of primary producers and SOM was significantly broader in SV than in NV, indicating a notable difference in available nutrient sources between the two habitats with higher diversification in SV. Dead zooplankton killed by sulfurous plumes (as plankton-derived production) is an essential food source in SV, as demonstrated by niche width comparisons of consumers
Conclusions
In this study, the trophic structures of benthic communities in SVs off KS Islet and nearby NV were categorized into four levels based on δ13C and δ15N signatures. The contribution of chemosynthetic production in SVs was demonstrated as low δ13C and δ15N values in SOM and algae. It was also identified that the plankton-derived production plays an essential role in providing food not only to scavengers, such as Xenograpsus crab, but also carnivores living in environments with low pH, high
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work described in this paper.
Acknowledgements
We are grateful to anonymous reviewers for their constructive comments, which have substantially improved the manuscript. We thank the Stable Isotope Facility of the University of California (Davis) for analyzing our samples. We also thank Mr. Jhih-hui Hung, Mr. Jeng-Ren Lia, Ms. Yalan Chou, and the SeaWatch Company for help with sample collection and Dr. Koh-Siang Tan, Dr. Kotaro Tsuchiya, Dr. Chienhsun Chen, Mr. Swee-Cheng Lim, and Mr. Chin-Wen Wang for species identification. This study was
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