Hydroides elegans

Hydroides elegans (Haswell, 1883)

Figs 4E, 5

Eupomatus elegans Haswell, 1883: 633, pl. 12, fig. 1 (type locality: Port Jackson [= Sydney], Australia).

Eupomatus pectinatus Philippi, 1844: 195, pl. 6, fig. R (type locality: Mediterranean).

Hydroides abbreviata Krøyer in Mörch, 1863: 377, pl. 11, figs 6–7 (type locality: Saint Croix Island, Lesser Antilles, Caribbean Sea).

Hydroides pacificus Hartman, 1969: 759–760, figs 1–5 (type locality: Velero IV, sta. 1454–42, from ship hull; central and southern California).

Hydroides norvegica (non Gunnerus 1768) – Edmonson & Ingram 1939: 268–271 (Kaneohe Bay and Pearl Harbor, Oahu, Hawaii; pier fouling). — Edmonson 1944: 3–16 (Pearl Harbor, Oahu, Hawaii; fouling experiments; 0–4 m). — Berkeley & Berkeley 1941: 56 (Newport Bay, southern California; from piling). — Hartman 1952: 63–64, figs 1–2 (Corpus Christi Bay, Texas; bottom of a boat; some specimens with double funnel). — Renaud 1956: 35 (Miami, Florida; bottom of R/V Physalia). — Hartman 1961: 44 (Los Angeles harbor, southern California; fouling on hulls of ships). — Rioja 1961: 311 (Antón Lizardo Beach, Veracruz, eastern Mexico; on ascidians and shells). — Lakshmana Rao 1969: 5, pl. 2, figs a–g (Visakhapatnam and Madras, now Chennai, India; harbours).

Serpula vermicularis (non Linnaeus 1767) – Lakshmana Rao 1969: 2–3, pl. 1, figs a–g (Visakhapatnam and Madras, now Chennai, India; harbours).

Hydroides elegans – Zibrowius 1971: 721–725, figs 56–64 (Mediterranean, Western Africa, South Africa, Mozambique, Java, Australia, Hawaii, California, Florida; extensive revision; intertidal to 6 m; on hull of boats). — Long 1974: 28 (Pearl Harbor, Oahu, Hawaii; 9 m; with little coverage on fouling plates). — Bailey-Brock 1976: 77–78 (Oahu Island and Hawaii Island; reef flats, on chlorophyte Dictyosphaeria cavernosa (Forsskål) Børgesen, epifauna of mobile substrata (mollusks and crustaceans), boat harbors and lagoons, brackish waters and reef slope). — Imajima 1976b: 237–238, fig. 3a–n (Tokyo Bay, Kanagawa Prefecture, Shizuoka Prefecture, Mie Prefecture, Wakayama Prefecture, Osaka Bay, Hiroshima Bay, Nagasaki Harbour, Amakusa Bay and Kagoshima Bay, Kochi Prefecture, Koniya Island, Japan; on the oysters Pinctada fucata (Gould, 1850), Crassostrea gigas (Thunberg, 1793) and Pteria penguin (Röding, 1798)); 1979: 169 (around Shionomisaki Cape and Kushimoto Harbour, southern Japan; 19–75 m; on shell, gravel and rope). — Dueñas 1981: 100–101, fig. 31A–G (Cartagena Bay, Colombia; on plastic pond related to shrimp culture). — Imajima 1982: 46 (Arumizu Bay, Palau Islands). — Bailey-Brock 1987: 420– 421 (Hawaii). — Zibrowius 1992: 91 (discussion about its origin). — Nishi 1995a: 101–102 (southern Japan; on chelae and carapace of the crab Charybdis riversandersoni Alcock, 1899). — Ishaq & Mustaquim 1996: 170, fig. 5A–H (Karachi, Pakistan; intertidal, on rocks, buoy and boat hull). — Nishi 1996: 306–308 (Okinawa Island, Southwest Japan; buried in the coral Montastrea sp. and attached to dead coral, Pocillopora damicornis (Linnaeus, 1758)). — Perkins 1998: 95 (checklist of shallow-water polychaetes from Florida). — Dueñas 1999: 14 (Cartagena Bay, Colombia). — Bastida-Zavala & Salazar-Vallejo 2000b: 846–848, fig. 2e–f (eastern Mexico: San Juan de Ulúa, Veracruz; Champotón, Campeche; Celestún, Yucatán; and Contoy Island, Quintana Roo; 0.3–3.5 m; on calcareous rocks, seagrass and macroalgae, wood dock pilings, and fort wall cover with vermetids, oysters and ascidians). — Díaz-Díaz & Liñero-Arana 2001: 12 (Cariaco Gulf, Venezuela; PVC dock pilings). — Bastida-Zavala & ten Hove 2002: 164–166, figs 35A–J, 36 (Florida, Texas, Puerto Rico, Atlantic Panama, Aruba, Cura ҫao, and eastern Mexico: Veracruz, Campeche and Quintana Roo; intertidal to 7 m; 31–37‰; on coral debris, fouling of wood pier and boats). — Bastida-Zavala & ten Hove 2003: 86–87, fig. 11A–S (California and Hawaii; intertidal to 1 m; among algae and bryozoans, fouling of marina piers and ship and submarine hulls). — Rodríguez-Valencia 2004: 520 (Petacalco Bay, Guerrero, southern Mexican Pacific; 3–21 m). — Çinar 2006: 226–227, fig. 3D–E (as NIS from eastern Levantine coast of Turkey). — Bastida-Zavala 2008: 25–26, fig. 6H (California and Baja California Sur, Mexican Pacific; intertidal to 1 m,on PVC plates and hull of boats).— Carlton & Eldredge 2009: 62 (Hawaii; invasion history). — Díaz-Castañeda &Valenzuela-Solano 2009: 513 (west coast of Baja California Peninsula:Salsipuedes Bay, Baja California; vicinity of tuna farm sea-cages). — Tovar-Hernández et al. 2009: 331, figs 3l, 8a-c (as fouling species in Mazatlán, Sinaloa, Mexican Pacific). — Ben-Eliahu & ten Hove 2011: 19– 25, figs 5D–E, 6–7 (Turkey, Cyprus, Israel, Egypt, Suez Canal and Red Sea; 0.2–10 m, on algae (Cystoseira myrica C. Agardh now Polycladia myrica (S.G. Gmelin) Draima, Ballesteros, F.Rousseau & T. Thibaut, Digenea, Laurensia and Sargassum), sponges, gastropods (Murex forskoehli Röding, 1798), bivalves (Brachidontes pharaonis, Chama gryphoides Linnaeus, 1758, Chicoreus erythraeus, now Murex erythraeus P. Fischer, 1870, Crenatula picta, Fulvia fragilis (Forsskål in Niebuhr, 1775), Fusinus verrucosus (Gmelin, 1791), Malvufundus normalis (Lamarck, 1819), now Malleus anatinus (Gmelin, 1791), M. regulus (Forsskål in Niebuhr, 1775), Pinctada radiata, Spondylus spinosus Schreibers, 1793 and Pectinidae), bryozoans, barnacles, crabs, tunicates, under rocks, artificial substrates such as canal walls, a tin can submerged in mud, rubber fenders and iron frames). — Tovar-Hernández et al. 2012: 16–17 (Gulf of California: Guaymas, Sonora and Topolobampo, Sinaloa); 2014: 388, 390 (Gulf of California: Topolobampo, Sinaloa; Guaymas, Sonora; La Paz, Baja California Sur). — Schwan et al. 2015: 3–6, fig. 2A–I (southeastern Brazil; intertidal to 1 m; fouling of harbors, marinas and PVC plates). — Sun et al. 2015: 23–29, fig. 6a–b (New South Wales, Northern Territory, Queensland, South and Western Australia; intertidal to 20 m; on scallop and mussel clumps on sandy bottom, fine mud, under rocks, unvegetated sediment, Zostera, Caulerpa filiformis, brown algae, on barnacles, cement and wooden pilings, floating pontoon, fouling plates, inside air-conditioning cooling pipe, and ship hulls). — Bastida-Zavala et al. 2016: 419–420, figs 4, 11F–G (Mexican Pacific: Baja California Sur and Oaxaca; in marinas and harbors, fouling; intertidal to 1 m).

Hydroides pacificus – Díaz-Castañeda 2000: 327 (west coast of Baja California Peninsula: Todos Santos Bay, Baja California; 10 m; terracota plates).

Material examined

384 specimens: IR (123) Aug. 2005, BB (1) Aug. 2004, TB (32) Jun. and Jul. 2012, HB (1) Sep. 2003, LB (87) Sep. 2003, MI (5) Jul. 2013, SD (87) Sep. 2000 and Jul. 2013, HI (48) Aug. 2006.

Additional material

18 specimens: LACMNH s.n., colony (southern California, 33°21'03" N, 118°19'55" W, off Avalon, Santa Catalina Island, Velero III, sta. 1377, grey sand, 110 m, 3 Aug. 1941, as Serpula sp.); LACMNH s.n., 1 specimen (southern California, 33°44'02" N, 118°32'03" W, 10 km from Pt Vicente lighthouse, Velero IV, sta. 2475, peel grab, mud, specimen attached to hexactinellid sponge, 740 m, 28 Oct. 1953); LACMNH s.n., 1 specimen (southern California, 33°47'59" N, 118°33'59" W, 11.5 km from Palos Verdes Point, Velero IV, sta. 2792, Hayward grab, mud, 600 m, 22 May 1954); LACMNH s.n., 1 specimen (southern California, 33°14' N, 118°18'04" W, 6.9 km from East End Light, Santa Catalina Island, Velero IV, sta. 2850, Campbell grab, 1200 m, 23 Jun. 1954); MBL-SD s.n., 5 specimens (southern California, approx. 32°43' N, 117°13' W, San Diego, CSA P–161, 1 month plate, 7 Oct. to 7 Nov. 1974, as H. pacificus).

Diagnosis

This species is gregarious and can form small colonies. Tube white, with or without two longitudinal ridges, with or without peristomes; but not alveoli. Opercular peduncle smooth, white. Opercular funnel with 15–31 radii (21–35 in eastern Pacific specimens) with blunt tips (Fig. 4E); verticil with 11–18 spines, straight, with pointed tips (Fig. 4E); all spines with 0–4 internal spinules and 2–3 pairs of lateral spinules (2–5 in eastern Pacific specimens), without external spinules and/or wings (Fig. 4E). Special collar chaetae with two pointed-elongate teeth and a proximal rasp, distal blade with notch and many denticles.

Taxonomic remarks

Hydroides elegans now exhibits a world-wide distribution in tropical and subtropical ports, marinas and eutrophic lagoons (ten Hove 1974). Due to its rapid colonization and population growth, it is considered an invasive species (Zibrowius 1973, 1992, 1994; Tovar-Hernández et al. 2009, 2014). The main means of dispersal of this species is through fouling on boats and ships and/or as larvae in ballast water (Nelson-Smith 1967; Tovar-Hernández et al. 2009).

Although H. elegans was described from Australia (Haswell 1883), and Zibrowius (1992) and several authors speculate that it is native there (Ben-Eliahu & ten Hove 2011; Sun et al. 2015), this is not clear evidence of an Australian origin. Bastida-Zavala et al. (2016: 420) draw attention to the fact that both the Hawaiian (Long 1974; Bailey-Brock 1976) and Australian (Sun et al. 2015) records of this species were from both natural and man-made substrates, suggesting a broader Indo-West Pacific origin. However, there are also records of this species from both natural and artificial substrates in the Gulf of Mexico and Caribbean Sea (e.g., Hartman 1952; Bastida-Zavala & Salazar-Vallejo 2000b; Bastida-Zavala & ten Hove 2002). In addition, 20 years before H. elegans was described, Krøyer (in Mörch 1863) described H. abbreviata, a senior synonym of the former species, from Saint Croix, a Caribbean Island, suggesting a possible Caribbean origin as well. Finally, the oldest description of a senior synonym of H. elegans is H. pectinatus, described by Philippi in 1844, from the Mediterranean. One of these old names could take precedence over the name H. elegans (Principle of Priority, ICZN 1999, art. 23); however, nomenclatural stability will not promote the re-introduction of these oldest available names, and therefore the conditions for reversal of precedence are met (ICZN 1999, art. 23.9). To resolve the origin of this species, a molecular analysis of the different world-wide populations will be necessary. In this work, Hydroides elegans is considered a cryptogenic species.

Ecology

Intertidal to sublittoral (10 m). Some records off California (additional material from LACMNH) have questionable depth data (110–1200 m). In subtropical and tropical marine and brackish waters; salinities of 31–37‰ (Bastida-Zavala & ten Hove 2002); on reef flats, on chlorophytes, epifauna of mobile substrata (mollusks and crustaceans), boat harbors, lagoons and reef slope (Bailey-Brock 1976); on the oysters Pinctada fucata, Crassostrea gigas and Pteria (Magnavicula) penguin (Imajima 1976b); on the crab Charybdis riversandersoni, dead coral (Pocillopora damicornis) and buried in the coral Montastrea sp. (Nishi 1995 a, 1996); also on rocks, seagrass, macroalgae (Cystoseira myrica, Digenea, Laurencia and Sargassum), sponges, gastropods (Murex forskoehli), bivalves (Brachidontes pharaonis, Chama gryphoides, Chicoreus erythraeus, Crenatula picta, Fulvia fragilis, Fusinus verrucosus, Malvufundus normalis, M. regulus, Pinctada radiata, Spondylus spinosus and Pectinidae), bryozoans, barnacles, crabs, tunicates, coral debris, under rocks, and on artificial substrates such as boat and ship hulls, cement and wood dock pilings, buoys, PVC or terracotta plates, canal walls, tin cans, rubber fenders and iron frames (Hartman 1952; Long 1974; Díaz-Castañeda 2000; Bastida-Zavala & Salazar-Vallejo 2000b; Bastida-Zavala & ten Hove 2002, 2003; Ben-Eliahu & ten Hove 2011).

Distribution

Worldwide in tropical to temperate waters. Western Atlantic: Caribbean Sea, Bermuda, Gulf of Mexico, Brazil; eastern Pacific: Hawaii, southern California, Mexican Pacific, Panama; other regions: Mediterranean, Suez Canal, western and South Africa, Mozambique, Pakistan, Java, Hong Kong, Australia, southern and central Japan, Palau Islands (Mörch 1863; Fauvel 1932; Day 1967; Zibrowius 1971; Imajima 1976b, 1979, 1982; Ishaq& Mustaquim 1996; Bastida-Zavala & ten Hove2002, 2003; Çinar 2006; Bastida-Zavala 2008; Ben-Eliahu & ten Hove 2011; Sun et al. 2012, 2015). In this work, Hydroides elegans was found abundantly and frequently on fouling plates from the Indian River and Tampa Bay, Florida; Long Beach and San Diego Bay, California; and Oahu, Hawaii; and occasionally from Biscayne Bay, Florida, and Humboldt Bay and Mission Bay, California (Fig. 5). Only one specimen was found on a fouling plate from Humboldt Bay, California, in 2003, suggesting that the species may now be present in northern California. However, additional sampling is necessary to confirm that H. elegans is currently established in northern California.

Hydroides elegans was observed at Eel Pond, Cape Cod, Massachusetts, on one occasion in the summer and fall of 2011, surviving the winter 2011–2012, and found again in the spring of 2012 occurring at remarkable abundances. However, after the second winter, no live specimens were found (Fofonoff et al. 2003; Jim Carlton, pers. comm., 2011–2013) so it is not clear if the species is still established there. If so, this record extends the northward range of the species on the east coast, from the Indian River, Florida, to Cape Cod, Massachusetts (1750 km). The remarkable abundance observed by Carlton demonstrates the colonization potential of H. elegans with warming temperatures, such as those predicted under the climate change scenario. On the east coast, Eel Pond has a latitude of 41°33' N, while on the west coast, Humbolt Bay, northern California, is located at 40°45' N; both localities represent the northernmost records of this species on mainland North America, suggesting that continued monitoring is necessary to evaluate the species spread.