Isotopic niche differentiation in benthic consumers from shallow-water hydrothermal vents and nearby non-vent rocky reefs in northeastern Taiwan

Highlights

• The shallow-water hydrothermal vents off the Kueishan (KS) Islet, Taiwan, are known to emit the most acidic fluid (pH 1.52).

• The predominant vent crab Xenograpsus testudinatus mainly feeds on dead zooplanktons. In this sulfur-rich ecosystem and nearby non-vent rocky reefs (NV), the trophic niche width of benthic organisms with different feeding guilds was compared.

• We found that the contribution of plankton-derived production (i.e., dead zooplankton killed by sulfurous plumes) plays a significant role in providing food to benthic consumers, not only scavengers, such as vent crabs but also carnivores in SV off KS Islet.

Abstract

Shallow-water hydrothermal vents (SVs) off Kueishan (KS) Islet are located along the northeastern coast of Taiwan. Although the trophic relationships of the sublittoral (15–30 m) and upper bathyal (200–300 m) vents in this region have been investigated, a comparison of SVs and adjacent non-vent ecosystems has not been undertaken. We compared the trophic structure and isotopic niche width of consumers in benthic communities around SVs off KS Islet with nearby non-vent rocky reefs (NV) to address this gap. The trophic structures for both SV and NV habitats were categorized into four trophic levels based on δ¹³C and δ¹⁵N signatures. SV sites ranged from −27.7 to −14.3‰ (δ¹³C) and from −7.3 to 12.2‰ (δ¹⁵N), whereas NV sites ranged from −20.2 to −13.1‰ (δ¹³C) and from 2.2 to 11.9‰ (δ¹⁵N). We found a notable difference in δ¹³C and δ¹⁵N values for primary producers and sediment organic matter between the two habitats indicating that available nutrient sources were different and more diversified in SV than those in NV. Based on the types of consumer feeding guilds, no difference in niche width of filter feeders between SV and NV was detected by ellipses analysis. Besides, a narrower niche width for scavengers in SV and differentiated niche positions for carnivores in both habitats were found. We conclude that plankton-derived production (i.e., dead zooplankton killed by sulfurous plumes) plays a significant role in providing food to benthic communities. These include not only scavengers, such as vent crabs, but also carnivores in SVs off KS Islet where extreme values of pH (1.52), temperature (116 °C), and H₂S (172 mmol/mol) are known to occur.

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.