Hydroids (Cnidaria, Hydrozoa) from marine environments in Taiwan

Abstract

Background

Hydroids were identified from extensive surveys of benthos, and especially from worm tubes, in the Danshuei River estuary (DRE), in the northeast Taiwan Strait (NETS), and on a reef in Nanwan Bay (NWB), Taiwan.

Results

A total of 33 species (12 of them identified to generic and 1 to family rank only), referable to 22 genera, 12 families, and 2 orders, were distinguished. The majority of them were referable to order Leptothecata (84.8%) with the remainder being assigned to order Anthoathecata (15.2%). The only species found at NETS was Monoserius pennarius (Linnaeus, 1758). Plumularia habereri (Stechow, 1909) was recorded at both DRE and NWB. The known range of Dynamena nanshaensis (Tang, 1991), recorded for the second time, is extended further north. Six species (Aglaophenia latecarinata, Plumularia floridana, Diphasia palmata, Dynamena brevis, Dynamena obliqua, Synthecium elegans) are recorded for the first time in waters adjacent to the Chinese mainland.

Conclusions

Species composition and abundances varied considerably from one environment to another and especially between DRE and NWB. This study provides the first taxonomic account of the hydroid fauna inhabiting the eastern Taiwan Strait region.

Background

Hydroids are largely sessile epibenthic cnidarians that inhabit all marine habitats from shallow to abyssal waters (Vervoort [1966]). Since hydroids feed on plankton, they likely play an important role in marine ecosystems (Gili and Hughes [1995]). Hydroids are often found growing on other marine organisms, including sponges (Calder [1991b]), other hydroids (Tang [1991b]), deep-sea corals (Henry [2001]), molluscs (Kubota et al. [1999]), arthropods (Genzano [2002]), and macroalgae (Fraschetti et al. [2006]; Cunha and Jacobucci [2010]; Oliveira and Marques [2007]). Except for the well-known association between proboscidactylid polyps and sabellid polychaetes (Schuchert [2009]), relatively, little attention has been given to worm tubes as substrates for hydroids.

Several studies on hydroids from temperate and tropical waters of the northwest Pacific have been carried out over the past few decades. These include the fauna of Japan to the north (e.g., Hirohito [1988], [1995]), the Yellow Sea (Tang and Huang [1986]), the East China Sea (Tang and Xu [1978]; Liu and Li [2002]), the Taiwan Strait (Kubota et al. [1999]; Xu and Huang [2004]), the Philippine Islands (Hargitt [1924]), and the South China Sea (Tang [1991a], [b], [1998]; Yeh [1995]; Zhao [1998]). Liu ([2008]) and Huang and Lin ([2012]) provided checklists and illustrations of Hydrozoa in waters adjacent to mainland China. A number of earlier reports explored the rich hydroid fauna of the western Pacific Ocean (for some references, see Vervoort [1995]). Literature is scanty on hydroids from waters of northeast Taiwan (Jäderholm [1903]), from the coast of southern Taiwan (Yeh [1995]), around Taiwan (Hwang and Shao [1998]), in the middle part of the western coast of Taiwan (Kubota et al. [1999]), in the Taiwan Strait (Xu and Huang [2004]), and from coral reef areas of the country (Fontana et al. [2012]). So far, distribution and species composition of hydroids have not been explored in the eastern Taiwan Strait. The present study was undertaken to establish a baseline of information on the group in waters of Taiwan.

Methods

Field sampling and samples treatment

Investigations on hydroids were undertaken in three environmentally distinct regions: (1) the Danshuei River estuary (DRE, 25°10′ N, 121°24′ E) in north Taiwan, (2) the northeastern Taiwan Strait (NETS, 24°48′ N, 119°55′ E), and (3) the reef zone in Nanwan Bay (NWB, 21°56′ N, 120°46′ E), south Taiwan (Figure 1, Table 1). Samples from DRE and NETS were collected by bottom trawl onboard the Ocean Research Vessel II and from a fishery vessel, respectively. At NWB, hydroid sampling on a coral reef was undertaken at 12 to 15 m depth using self-contained underwater with breathing apparatus (SCUBA) and at 100 m depth using a remotely operated vehicle (ROV). A total of 24 worm tube specimens collected at the coral reef site by SCUBA diving, and two additional ones using the ROV, were examined for hydroid associates. Specimens were preserved in seawater with 5% to 10% buffered formalin immediately after collection.

Figure 1

Map of Taiwan and vicinity, showing the three sampling locations. DRE, Danshuei River estuary; NETS, northeastern Taiwan Strait; NWB, Nan-Wan Bay.

Table 1 Sampling location, date, depth, and methods

Hydroids identification

In the laboratory, each sample for taxonomic identification was dissected on a glass slide with the help of a dissecting microscope. Identification of species was undertaken using recent taxonomic keys and relevant references, including Vervoort ([1966]), Millard ([1975]), Rees and Vervoort ([1987]), Calder ([1988], [1991a], [1997], [2012]), Hirohito ([1988], [1995]), Cornelius ([1995a], [1995b]), Schuchert ([1996], [1998], [2001], [2003], [2004]), Marques ([2001]), and Vervoort and Watson ([2003]).

Results

Hydroids from DRE and NETS, collected by bottom trawl, were often found together with rocks. However, those actually attached to rock at DRE represented less than 30% (N > 100) of the total number of specimens. At NETS, hydroids were found tangled in the trawl net because most colonies were fragmented and longer than 40 cm. Worm tubes, an important substrate at NWB, supported a substantial growth of sessile organisms including hydroids, soft corals, ascidians, and red algae (Figure 2). As for hydroids, they were associated with worm tubes at the rate of 100% (N = 24). Most hydroids attached to middle and distal surfaces of the tube, while fewer were present at the base.

Figure 2

Photographs of worm tubes in field (a) and colony size (b) taken from the coast of Nan-Wan Bay.

In our samples, 22 species were identified from riverbed environments at DRE, 11 epizoic species were found on worm tubes at NWB, and 1 species occurred in samples from NETS (Table 2). Overall, a total of 33 hydroid species (12 of them identified solely to generic level and 1 to family level) referable to 22 genera, 12 families, and 2 orders, were discovered. Most of the species belonged to order Leptothecata (84.8%), with the remainder being referable to order Anthoathecata (15.2%). Taking samples from all study areas together, hydroids of the family Sertulariidae (comprising 14 species, with 3 identified to generic level only) contained the largest number of species. Six species (Aglaophenia latecarinata Allman, 1877; Plumularia floridana Nutting, 1900; Diphasia palmata Nutting, 1905; Dynamena brevis (Fraser, 1935); Dynamena obliqua Lamouroux, 1816; and Synthecium elegans Allman, 1872) are recorded here for the first time from waters adjacent to mainland China (Table 2).

Table 2 Taxonomic list of hydroids collected from north and south Taiwan

Hydroid species composition and abundance varied considerably between DRE and NWB. Only one species, Plumularia habereri Stechow, 1909, was found at both locations. Species found in the deep zone at NWB by the ROV were P. habereri and Dynamena nanshaensis Tang, [1991a]. At NETS, only one species was found, the robust aglaopheniid Monoserius pennarius (Linnaeus, 1758). Its colony had a single stem, with pinnate side branches.

Discussion

Historical records of hydroids in coastal waters around Taiwan are limited. Yeh ([1995]) reported seven species of Plumulariidae collected in the southern part of the island. Hwang and Shao ([1998]) described two venomous hydroids from the same location. Kubota et al. ([1999]) provided the first record of Eugymnanthea japonica (Yamada, 1950) (Leptothecata, Eirenidae), from western Taiwan, where it was associated with two bivalve species (Crassostrea gigas (Thunberg, 1793), Perna viridis (Linnaeus, 1758)). Recently, Fontana et al. ([2012]) reported what was believed to be a cosmopolitan and possibly genus-specific association between Zanclea spp. and its coral hosts, based in part on hydroids from Acropora corals on reefs in Kenting and the Penghu Islands, Taiwan. Previous literature provided li`mited data of hydroids in this area, as shown in the extensive review on hydroid species in Chinese waters by Liu ([2008]). His report recorded 615 species of Hydrozoa in waters adjacent to mainland China, including the East China Sea, western Taiwan Strait, and South China Sea. Shortly after, Huang and Lin ([2012]) provided illustrations of 829 species of Hydrozoa in waters adjacent to mainland China. However, hydroids in the eastern Taiwan Strait were still inadequately known, and our study is the first to document the hydroid fauna in waters of the region.

The stinging hydroid Aglaophenia cupressina Lamouroux, 1816 is widely distributed on the coral reefs of the Bunaken area (Ricciardi [2007]). Tang ([1991a]) noted that the sting of A. cupressina, frequent on reefs in the Indo-West Pacific area, produces an itchy rash in humans. Hwang and Shao ([1998]) reported A. cupressina and the feather hydroid Halocordyle disticha (a synonym of Pennaria disticha Goldfuss, 1820), both venomous to humans, in Taiwan. Eldredge and Smith ([2001]) noted that the sting of P. disticha causes mild irritation in humans. The two species were recorded on worm tubes from NWB in our study.

The colonial hydroid P. habereri was found in a riverbed environment at DRE and by ROV in NWB. This species is widely distributed in the South China Sea, Indonesia, and Japan (Liu [2008]) at varied depth ranges, e.g., 10 to 35 m (Schuchert [2003]) and 1 to 4 m (Calder and Kirkendale [2005]). In our study, the species was collected at a depth of 100 m, the deepest ever recorded. In addition, waters in the estuarine environment at DRE have a wide range of salinities. We conclude that P. habereri is a euryhaline species.

A noteworthy discovery in our samples was D. nanshaensis, collected from hard substrates on the reef at NWB. This is only the second record of the species since its original description from the Nansha Islands (Tang [1991a]). Thus far, D. nanshaensis is known only from the South China Sea, specifically from the type locality (Nansha Islands, about 10° N) and now from our study in Nanwan Bay (about 21°56′ N), south Taiwan, the northernmost record of the species.

The macrobenthic hydroid M. pennarius was especially abundant at Nansha Island (Zhao [1998]; Tang [1991b]). Its dense population there establishes an ecological environment described as an ‘imitative steppe on sea floor’ (Zhao [1998]) and a ‘sea-floor prairie’ (Tang [1991b]). M. pennarius is widely distributed in the Indo-Malayan and Sino-Japanese subregions of the Indo-West Pacific region (Tang [1991b]), including India, Ceylon, Indonesia, Philippines, Taiwan, southern Japan, Palau, and New Zealand (Schuchert [2003]). It is a species of warm waters and high salinity in the East China Sea (Liu and Li [2002]). Common macrobenthic communities there include: Callianassa spp., M. pennarius-Stellaster equestris (Tang and Xu [1978]), and S. equestris, M. pennarius-Callianassa japonica (Liu and Li [2002]). Our material from NETS confirmed that colony length of M. pennarius ranges from 30 to 100 cm and that it inhabits muddy-sandy seabeds at depths of 50 to 100 m (Tang [1991b]; Schuchert [2003]; Vervoort and Watson [2003]).

Samples from DRE included the cosmopolitan species Dynamena disticha (Bosc, 1802). Liu ([2008]) reported D. disticha from the East China Sea, South China Sea, Indonesia, Japan, Bermuda, and Brazil. Puce et al. ([2009]) reported that D. disticha can be found in association with algae, hydroids, barnacles, rocks, and concretions in the Mediterranean Sea. This suggests high adaptability to diverse environments, and indeed, D. disticha has a broad distribution. Some hydroids form communities in association with other co-occurring marine organisms. Fraschetti et al. ([2006]) reported D. disticha and Obelia dichotoma (Linnaeus, 1758) in association with brown algae Cystoseira amentacea (C.Agardh) Bory de Saint-Vincent, 1832 in the Mediterranean Sea. Both hydroid species were recorded from DRE in this study. Cunha and Jacobucci ([2010]) reported 16 species of hydroids on fronds of the alga Sargassum cymosum C.Agardh, 1820 in subtropical Brazil. Among species in their list, A. latecarinata, D. disticha, and O. dichotoma were also found in our study. Gravier-Bonnet and Bourmaud ([2006]) recorded 95 hydroid species from a reef zone in the southwest Indian Ocean, with P. disticha, A. cupressina, Macrorhynchia philippina, and Dynamena crisioides being common to abundant. Three of these species (P. disticha, A. cupressina, and D. crisioides) were also identified from samples in the reef zone at NWB.

Notably, six species (A. latecarinata, P. floridana, D. palmata, D. brevis, D. obliqua, and S. elegans) identified from DRE have never been recorded previously in seas of China (Liu [2008]). This reveals that the assemblage of hydroids in the eastern Taiwan Strait differs significantly from those in coastal waters of mainland China. Shao ([1998]) estimated that the number of marine species around Taiwan represented 10% of the total number known worldwide. The island of Taiwan, located in the west Pacific Ocean, has a total of 1,566 kilometers of coastline (including the Penghu Islands) (Tung [2006]), and complex current systems influence the island (Tseng et al. [2013a], [b]). Diverse water masses of the East China Sea, South China Sea, China Coastal Current, and Kuroshio Current have a pronounced effect on the endemic marine biota. Varied marine habitats promote a highly diversity biota around Taiwan Island (Shao [2009]). Expanding the geographic scope and frequency of marine surveys would potentially show that the indigenous hydroid fauna in waters around Taiwan is even richer.

Conclusions

The study documents a unique and heterogeneous assemblage of hydroids found in three quite dissimilar marine environments in Taiwan (DRE, NETS, and NWB). The DRE riverbed system supports a comparatively richer hydroid fauna than a group of species associated with worm tubes from NWB. The three sampling sites differed significantly in faunal composition and numbers of species. Differences are attributed primarily to disparities in substrate types and salinity characteristics among the sites. Studies on developmental stages of hydroids under laboratory conditions are needed to better understand their life cycles in nature.