Nonindigenous Ascidians in Tropical Waters 1

Gretchen Lambert2

Abstract: Ascidians (invertebrate chordates) are abundant in many ports around the world. Most of them are nonindigenous species that tolerate wide fluctua­ tions in temperature, salinity, and even pollution. These sessile suspension feeders have a rapid growth rate, usually a short life span of a few months, reach sexual maturity when only a few weeks old, and produce large numbers ofshort­ lived nonfeeding planktonic larvae. They thrive on marina floats, pilings, buoys, and boat bottoms in protected harbors where there is reduced wave action and enhanced nutrients from anthropogenic activities. Nonindigenous ascidians frequently overgrow oysters and mussels, which are often cultivated in or near busy harbors. Adult ascidians on ship or barge hulls may survive transport over thousands of kilometers to harbors with conditions similar to those they left; occasionally live larvae have also been recovered from ships' ballast water. U.S. Navy dry dock movements between major Pacific ports have transported large masses of fouling nonindigenous taxa, including ascidians. Transfer between culture sites of oysters, mussels, and associated lines and nets may provide an additional mode of transport. Once nonindigenous ascidians become estab­ lished, they provide large local sources of larvae for further possible invasions into additional harbors and nearby natural marine communities. Invasive species include both solitary and colonial forms, with a preponderance of large solitary species that thrive in highly disturbed habitats. In Guam, for example, most nonindigenous ascidians are confined to harbor structures and have not as yet significantly colonized natural reefs. In contrast, healthy natural benthic regions both inside and outside the harbors of Guam are usually stable coral reef com­ munities containing a high diversity, but very low biomass, of native colonial ascidian species. However, in several areas of the Caribbean a native colonial didemnid has recently begun overgrowing coral reefs. In the Gulf of Mexico a nonindigenous didemnid now covers many offshore oil rigs and may become a threat to neighboring natural reefs. Additional data on nonindigenous ascidians in Australia, Palau, Hawai'i, and the Mediterranean are included. Although se­ rious invasion of coral reefs has not yet been reported, more studies and regular monitoring are needed.

INTRODUCTIONS OF nonindigenous ascidians of introductions increasing (for reviews see into harbors in both tropical and temperate Monniot et al. 1991, Lambert and Lambert waters are now commonplace, with the tempo 1998, Coles et al. 1999). Ascidians are in­ vertebrate members of the phylum Chordata,

1 Paper presented at the Ninth International Coral with a sessile suspension-feeding adult and a Reef Symposium, Bali, Indonesia, 27 October 2000. short-lived nonfeeding motile larva. Colonial Manuscript accepted 2januar;r2002. - species brood theiryoung and release mature­ 2 University of Washington Friday Harbor Labo­ larvae into the water, but most others spawn ratories, Friday Harbor, Washington 98250. Mailing address: 12001 11th Avenue NW, Seattle, Washington eggs and sperm that develop in about 24 hr 98177 (phone: 206-365-3734; E-mail: glambert® into swimming larvae with an average larval fullerton;edu). duration of 12-24 hr. Because the larval stage is so short (perhaps only a few minutes Pacific Science (2002), vol. 56, no. 3:291-298 between release and settlement in colonial © 2002 by University ofHawai'i Press forms), their primary mode of anthropogenic All rights reserved transport is probably boat hulls or other

291 292 PACIFIC SCIENCE· July 2002

fouled surfaces. Movement between culture having the ability to attach tenaciously to sites of fouled nets and shells used in mari- substrates, the tunic is flaccid and tears easily. culture, for example, may inadvertently If even a small bit adheres to any organisms transport nonindigenous ascidians (unpubl. that are transported, it can rapidly colonize data), as were burrowing polychaetes on oys- a new substrate and may already be in re­ ters imported from Maine into Hawai'i in productive mode. Because many colonies are 1990 (Bailey-Brock 2000). Although ascidian actually chimeras, the gametes ofzooids with­ larvae are known to survive transport in bal- in a single colony can cross-fertilize. last water (Carlton and Geller 1993), this may Nonindigenous ascidians rapidly colonize not be their major mode ofhuman-influenced artificial substrates in harbors, such as pilings, transport. Sampling of U.S. Navy dry dock floating marina docks, boat hulls, and buoys. hulls both before and after their movement The epifauna on these structures is often across thousands of kilometers in the Pacific nearly completely composed of nonindige­ (including Honolulu to Guam in July 1999 nous species of various taxa, frequently dom­ and San Diego to Honolulu in December inated by huge numbers and biomass of 1999) has shown that many adult ascidians nonindigenous ascidians (Lambert and Lam­ arrive alive (G. Paulay and S. Godwin, pers. bert 1998). The important question is, do comm.). When a bridge collapsed in Palau in these invaders also colonize neighboring nat­ 1996, a floating pontoon bridge was towed ural reef areas, outcompeting and replacing there from China the following year; it ar- native species, or do they remain confined to rived carrying many live fouling organisms artificial surfaces within harbors? This ques­ including ascidians (P. Colin, pers. comm.). tion is highly relevant not only because of the By whatever means they achieve transport, increasingly large number ofartificial surfaces the same nonindigenous ascidians are often associated with ever-expanding marinas to recorded from widely separated localities service the rapidly growing pleasure boat in­ (Boyd et al. 1990, Monniot et al. 1991, Mon- dustry, but also because more and more fish niot and Monniot 1994, 1996,2001, Lambert and wildlife and parks departments are estab­ and Lambert 1998). lishing artificial reefs to attract fish for sports Many nonindigenous ascidians reach sex- fishermen and snorkeling and scuba diving ual maturity in just a few weeks and have long hobbyists. breeding seasons (Lambert and Lambert Only a few comparative studies, especially 1998). They tolerate wide fluctuations in long-term, of neighboring natural versus ar­ temperature and salinity and acclimate rap- tificial habitats have been done. Glasby and idly to these changes (Sims 1984, Nomaguchi Connell (Connell and Glasby 1999, Connell et al. 1997). Nonindigenous ascidians also 2000, Glasby 2000) concluded after many tolerate various types of pollution and are years ofstudy of Sydney Harbour in Australia known to sequester or use metal ions (Mon- that pilings and floating pontoons provide a niot et al. 1993, 1994, Naranjo et al. 1996, unique set of habitats that cannot be consid­ Sings et al. 1996). Diplosoma listerianum pro- ered equivalent to adjacent natural benthic vides an excellent example of a potential substrates. The environmental conditions nonindigenous ascidian; it now has a global they are subject to, the particular surfaces ex­ distribution. In addition to having many of posed, and many other variables result in an -the- traits--listed--above,geneticaHy different- - epibiota-quite-different-from-that-of-adjacent---­ colonies of D. listerianum frequently fuse and benthic areas, and there is very little overlap the resulting chimeras have been shown to in species composition even after several have enhanced adaptability (Sommerfeldt and years. Connell (2000) showed that it is not the Bishop 1-9-9-9). The -zeeids ean -store €xeg€- natuF€efth€ sUF-faG@--its~Mbut-its-IeGatien that­ nous sperm for several weeks (Bishop and is most important in determining which spe­ Sommerfeldt 1996), and like other colonial cies will colonize it. Surfaces composed of ei­ ascidians the larvae are brooded and released ther artificial or natural materials attached to only when competent to settle. Although or suspended from floating pontoons will be Nonindigenous Ascidians in Tropical Waters . Lambert 293

colonized by the same species as inhabit the considered cryptogenic. Based on these crite­ pontoons; similarly, both artificial and natural ria, nine are listed as introduced and 18 as surfaces placed in a benthic ecosystem will be cryptogenic. An additional four included as colonized by the same types of organisms as cryptogenic were found predominantly on occur in that ecosystem. In Sydney Harbour, artificial substrates with only a few very small pilings and pontoons have increased the specimens collected from natural areas (Per­ overall biodiversity and biomass without any ophora sagamiensis, Pyura curvigona, P. honu, apparent changes in the benthic ecosystems and P. cf. robusta), though their distribution is (Connell and Glasby 1999). not extra-Indo-West-Pacific. Paulay et al. (2001 and unpubl. data) re- Ofthe 31 species considered introduced or ported similar results in a large-scale com- cryptogenic in Guam (Table 1), 16 are colo­ parison of the epibiota of artificial structures nial and 15 are solitary. Half of the colonial in and around Apra Harbor, Guam, with forms belong to the order Aplousobranchia. natural reef areas. Although there is some The Phlebobranchia are also well represented overlap of species, for the most part the biota with five species, two of which are colonial of these adjoining habitats are very different; and three are solitary. The largest group is based on the work of Glasby and Connell (as the Stolidobranchia, with seven colonial and mentioned earlier), we can assume that these 12 solitary species. All of the 78 species oc­ artificial and natural habitats are subjected to curring only on natural substrates are con­ very different environment conditions. Float- sidered native/indigenous. Of these 78, 69 ing docks, buoys, and pilings are primarily (88%) are colonial. Thus 48% of introduced! colonized by nonindigenous ascidians, where- cryptogenic species are solitary, but most of as native species dominate the natural reefs. the native/indigenous species are colonial. Twenty-one species (18%) are found on arti- Fay and Vallee (1979) reported 39 species ficial surfaces only, 78 species (67%) are found of ascidians from the Channel Islands off on natural substrates only, and 18 species the southern California mainland. Fourteen (15%) are found on both artificial and natural (36%) were solitary; 25 (64%) were colonial. substrates, a total of 117 species. Of the 15 In comparing the ascidian distribution be­ known invasive ascidian species in Guam that tween mainland and islands, they found a are also reported as nonindigenous in many preponderance ofviviparity in the island spe­ other areas (Monniot et al. 1991, Monniot cies and concluded that this was a strategy to and Monniot 1994, 1996, Coles et al. 1999), reduce gamete loss. However, nearly all the all were found on artificial surfaces; three of viviparous species were colonial. Thus an­ these also occurred on nearby reefs: Botryllus other ecological factor that must be consid­ niger, Cnemidocarpa irene, and Herdmania pal- ered is growth form: colonial species are low lida. On natural reefs these three species were encrusting mats; solitary species project into small, sparse, and formed only a negligible the water column. The high-energy surf zone part of the reef fauna, in striking contrast to environment present around the Channel Is­ their larger size and numbers on artificial lands as well as on the reef edges around substrates. (One immature Microcosmus sp., Guam favors ascidians with both a low en­ possibly M. exasperatus but too small to iden- crusting form and viviparous mode of repro­ tify, was also found on a reef but not included duction. All 69 colonial native/indigenous ------"1fflable-l~tFiveohheremaining9-of-t:ll:e-21-- species of-Guam-asciOiiillToccurring olllyon-- ­ species recorded only from artificial surfaces natural substrates are viviparous. In constrast, are as yet identified only to genus; the other artificial structures such as buoys, wharf pil­ four are considered cryptogenic. ings, and floating docks are located in harbors -In Table 1 the criteria for a designation where- there-is much less wave actilJU. The of introduced are that the species (1) be re- epibionts that colonize these structures, and stricted to artificial surfaces and (2) have an indeed the large-scale fouling communities extra-Indo-West-Pacific distribution; if only that form, can do so only because of the pro­ one of these criteria apply, the species is tected environment. As Berrill (1955) pointed 294 PACIFIC SCIENCE· July 2002

TABLE 1 Guam Ascidians Considered Introduced or Cryptogenic

Extra-Indo- Restriction West-Pacific to Artificial Species Status Apra Harbor Distribution Substrates Solitary/Colonial

Aplousobranchia Gold-green compound Cryptogenic 1 1 C Didenmum perlucidum Introduced 1 1 1 C Didemnum psammathodes Cryptogenic 0 1 0 C Diplosoma listerianum Introduced 1 1 1 C Diplosoma "fluffy" Cryptogenic 1 ? 1 C Lissoclinum fragile Introduced 1 1 C Polyclinum consteltatum Introduced 1 1 C Phlebobranchia Perophora multiclathrata Cryptogenic 1 0 C Perophora sagamiensis Cryptogenic 0 0 C Ascidia sydneiensis Introduced 1 1 S Ascidia sp. B Cryptogenic ? 1 S Phallusia nigra Introduced 1 S Stolidobranchia Botryllus cf. simodensis Cryptogenic 1 0 1 C Botryllus niger Cryptogenic 1 1 0 C Botryllus sp. A Cryptogenic 1 ? 1 C Botryllus sp. B Cryptogenic 1 ? 1 C Cnemidocarpa irene Cryptogenic 1 1 0 S Polyandrocarpa sagamiensis Cryptogenic 1 0 1 C Polycarpa aurita Cryptogenic 1 0 1 S Styela canopus Introduced 1 1 1 S Symplegma brakenhielmi Introduced 1 1 1 C Symplegma sp. A Cryptogenic 1 ? 1 C Herdmania insolita· Cryptogenic 1 ? 1 S Herdmania pallida Cryptogenic 1 1 0 S Microcosmus exasperatus Introduced 1 1 1 S Microcosmus helleri Cryptogenic 1 1 0 S Microcosmus pupa Cryptogenic 1 0 1 S Pyura confragosa Cryptogenic 1 0 1 S Pyura curvigona Cryptogenic 1 0 0 S Pyura honu Cryptogenic 1 0 0 S Pyura cf. robusta Cryptogenic 1 0 0 S 31 total

out, budding in colonial ascidians is "primar­ Naranjo et al. (1996) analyzed the ascidian ily a means of extending the living, repro­ distribution in the large Mediterranean port ducing ascidian entity in two rather than of Algeciras Bay, Spain, and separated the three dimensions, in relation to the exploita­ species into three fairly distinct groups that tion of flat surfaces on which uniform three- differ considerably in their physiological tol- - Oiinensional growth leads to-mcreasmgc fnse" --er:m-c'es--rowave-;rction;- pollutants;-sedinren~ -­ curity offoothold." tation, and other environmental factors: (a) In Palau, preliminary data indicate that, as "exclusively in the outer zone of the bay in Guam, the artifical structures of Malakal which settle mainly on natural rock sub­ Harbor are dominated by large, solitary spe­ strates, Eb)species more abundant in the in­ cies of nonindigenous ascidians (unpubl. ner zone of the bay which settle mainly on obs.), while the ascidians of the reefs are pri­ artificial substrates, and (c) species found marily native colonial species (Monniot and throughout the bay." The same nonindige­ Monniot 2001). nous ascidians that occur in numerous warm- Nonindigenous Ascidians in Tropical Waters . Lambert 295

temperate ports of the world were also com- months later, D. perlucidum covered 100% of mon or abundant on artificial structures in the rig superstructure that had previously Algeciras Bay, but were generally not present been out of water. A quick survey of the two elsewhere in the bay. Naranjo et al. (1996) underwater reefs just mentioned during sum­ concluded that fouling species, which are mer 2000 appears to indicate that D. perluci­ primarily nonindigenous ascidians, dominate dum is so far restricted to the oil rigs and has artificial substrates in the harbor, are tolerant not invaded the reefs, but it is a situation that of sedimentation and water stagnation, and needs to be closely monitored. Any degrada­ grow rapidly in water highly enriched by or- tion of the natural reefs might give the asci­ ganic material from runoff and sewage treat- dian the competitive advantage it needs to get ment effiuents; thus they can be considered a foothold. indicators ofregions ofintense environmental Didemnum perlucidum apparently breeds stress. Native species prefer natural benthic throughout the year, daily releasing large substrates, especially those near the outside of numbers of mature brooded larvae (unpubl. the bay. They are more sensitive to stress and data and J. Culbertson, pers. comm.). Di­ thus can be considered indicators ofrelatively demnum perlucidum was described by F. undegraded environmental conditions. Monniot (1983) from Guadeloupe in the Ca- Do the results of these studies mean that ribbean, where it grows on both artificial and we can be unconcerned about controlling the natural substrates. It was not listed by Van introduction of nonindigenous ascidians in Name (1945) or Plough (1978) for any region tropical waters? Some available information in the United States. Thus it may be a recent suggests otherwise. In the Gulf of Mexico, introduction to the Caribbean or was a minor the Texas Parks and Wildlife Department has member of the fauna until its rapid increase utilized decommissioned offshore oil and gas and spread within the past few years. Di­ rigs as artificial reefs (J. Culbertson, pers. demnum perlucidum is now a common fouler comm.). While the rigs are still in place in of artificial surfaces in harbors in Brazil (da water up to 70 m deep, they are cut in half. Rocha and Monniot 1995) as well as through­ The bottom half (about 35 m in height) may out the Indo-West Pacific, including Guam be left in place while the top half is sunk (Paulay et al. 2001), Palau (unpubl. data), either nearby or after being towed to an- French Polynesia, Indonesia, New Caledonia, other site. The newly submerged superstruc- Zanzibar, and many other areas (reviewed ture (walkways, etc.) of the top halves now in Monniot and Monniot 1996). It is often also becomes available for colonization by abundant, overgrowing other epibionts (es­ marine organisms. In all cases, all of the epi- pecially solitary ascidians) and sometimes biota that had been growing for many years hanging in long, thick strands that easily on the underwater legs of the rigs is left break off and drift away; this may be an im­ in place and thus may be transported to new portant method of spreading, as it appears to locations. Some of these locations are within be for Perophora japonica (Nishikawa et al. 1-2 Ian or so of exceptionally rich and 2000). Both D. perlucidum and Trididemnum beautiful underwater reefs such as Flower solidum are facultative hosts to unicellular Garden Banks and Stetson Bank, both pro- photosymbionts such as Prochloron; thus not tected under the National Marine Sanctuary only can the photosymbionts be transported -program~-In-the-past'several- years'a--non~---alorrg-w:iththeir-hostascidian-colony-butthey indigenous colonial ascidian, Didemnum per- may make it easier for the host to become lucidum, has completely overgrown all sides of established in a new area. a number of these oil rigs, covering hundreds Healthy communities with a high diversity of" square meters and smothering the sponges,- of-speeiesseem -able to prevent ()f-limit the bivalves, and other invertebrates that for- establishment of nonindigenous ascidians merly grew on the structures. On a rig that (Stachowicz et al. 1999), though there is some was cut in half in 1997, the upper half sunk disagreement about this theory. When reefs next to the lower half and then surveyed 14 become degraded or when bacterial levels 296 PACIFIC SCIENCE· July 2002 rise, certain species of ascidians may undergo overgrowth of other sessile organisms. More rapid increases. Ascidians are efficient sus­ frequent dry dock cleaning of boat hulls pension feeders. Bak et al. (1981, 1996, 1998) might help prevent the spread offouling spe­ studied the coral reefs ofthe Caribbean island cies (Brock et al. 1999), and perhaps hand of Cura~ao for over 15 yr. Before 1980 the removal of invaders in an early stage of inva­ native didemnid Trididemnum solidum was sion might prevent their establishment. Al­ present in small numbers, did not appear to though the mostly nonindigenous biota on compete with native corals for food and artificial structures in harbors has apparently space, and preferred to settle on dead coral not affected nearby natural areas (Connell with a thin algal turf. However, by 1996 Bak and Glasby 1999), there is still the possibility et al. found a 900% increase in T. solidum, oflong-term and as yet unforeseen changes in which they attributed at least in part to greatly adjacent natural ecosystems (Bak et al. 1996, increased densities of suspended bacteria in Glasby and Connell 1999), and careful regu­ the water resulting from a big increase in an­ lar monitoring ofsensitive natural areas should thropogenic activities during the 15 yr be­ be carried out. tween the two studies. Trididemnum solidum now actively outcompetes the corals, over­ growing and killing live coral. A similar situ­ ACKNOWLEDGMENTS ation is occurring in the Bay Islands off the I am greatly indebted to G. Paulay and the coast of Honduras, about 1800 km from Cu­ entire staff of the University ofGuam Marine ra~ao, where large mats of T. solidum have Laboratory for their willing and cheerful as­ appeared in the past 2-3 yr and are covering sistance in all matters large and small during and killing the corals Keck and R. Hous­ (J. my stays in Guam, funded by a Sea Grant to ton, pers. comm.). G. Paulay. G. Paulay aided by L. Kirkendale, C. Meyer, R. Ritson-Williams, J. Starmer, T. CONCLUSIONS Rongo, and P. Houk collected ascidians by Although nonindigenous ascidians are ex- scuba. M. Hadfield, director of the University of Hawai'i Kewalo Laboratory, provided lab- ~~::da;':i~:r:o~~t~~:~:-:~~1~,:~:;~ oratory space; P. and L. Colin of the Coral they are often the dominant species with an Reef Research Foundation provided all nec­ essary support for the work in Palau. Many incredibly high biomass, they rarely colonize adjacent natural benthic ecosystems. Healthy thanks to L. G. Eldredge ofthe Pacific Science Association for obtaining financial support natural ecosystems such as coral reefs com- for my work in Honolulu and participation at pri~e a high biodiversity, with cOl?~lex inter- the Ninth International Coral Reef Sympo­ D aCTIons among" the speCIes,£"and this IS thought."th SlUm, andto S. G 0d'wm, R. eF el'Ice, and S. to be an Important actor m prevenTIng e C 1 f th B" h M . H 1 1 1: bl" hm f "d" "H 0 es 0 e IS op useum mono u u lor esta IS ent 0 mva mg speCIes.· dowever, d d co11'eCTIon 0fspeCImens. . J.C ulbertson 0f th e many cora1reefareas are becommg egra e T P ks d W'ldli1: D .. ", 1 b 1 exas ar an 1 Ie epartrnent pro- due to anthropogemc aCTIVlTIeS, goa warm- 'd d th d D"d l"d' th . (. 1 d' th . d El Vl e e ata on 1 emnum pe~ UCl um m e mg mc u mg e recent warmmg ue to G If f M' Th ". N mo"-),andper haps 0ther causes. Abunum er d0 b theXlCO. e.manuscnpt f was lm- ohepurts- mosr-of-them-unpublished-as7 et__ Jlro.ve y (:..s.!!gg~.!lons_Q.._ an ~Q..I!Y!!!0us _ '. th "d d f l' reVlewer. I am especIally grateful to C. Lam­ are documennng e rapl sprea 0 severa b 1 f, h' "' ·d·th all ascidian species over the past several years in ert as afwthiafs or IS unsnnnng at Wl k varlOUS. temperate and'tr0plca1reglOns . 0f th e aspects 0 s wor . world. The reasons for this change -are flot known, but they do coincide with the latest El Literature Cited Nino event. These ascidians have not de­ clined with the return of cooler water; on the Bailey-Brock, J. H. 2000. A new record ofthe contrary they continue their rapid spread and polychaete Boccardia proboscidea (Family Nonindigenous Ascidians in Tropical Waters . Lambert 297

Spionidae), imported to Hawai'i with oys­ and diversity of subtidal epibiota? A case ters. Pac. Sci. 54:27-30. study from Sydney Harbour, Australia. Bak, R P. M., J. Sybesma, and F. C van Mar. Environ. Res. 47:373-387. Duyl. 1981. The ecology of the tropical da Rocha, R M., and F. Monniot. 1995. compound ascidian Trididemnum solidum. Taxonomic and ecological notes on some n. Abundance, growth and survival. Mar. Didemnum species (Ascidiacea, Didernni­ Ecol. Prog. Ser. 6:43-52. dae) from Sao Sebastiao Channel, south­ Bak, R P. M., D. Y. M. Lambrechts, M. eastern Brazil. Rev. Bras. BioI. 55 :63 9-649. Joenje, G. Nieuwland, and M. L. J. Van Fay, R C, and J. A. Vallee. 1979. A survey of Veghel. 1996. Long-term changes on coral the littoral and sublittoral ascidians of reefs in booming populations of a com­ southern California, including the Chan­ petitive colonial ascidian. Mar. Ecol. Prog. nel Islands. Bull. South. Calif. Acad. Sci. Ser. 133:303-306. 78:122-135. Bak, R P. M., M. Joenje, I. de Jong, D. Y. M. Glasby, T. M. 2000. Surface composition and Lambrechts, and G. Nieuwland. 1998. Bac­ orientation interact to affect subtidal epi­ terial suspension feeding by coral reef biota. J. Exp. Mar. BioI. Ecol. 248:177­ benthic organisms. Mar. Ecol. Prog. Ser. 190. 175:285-288. Glasby, T M., and S. D. Connell. 1999. Ur­ Berrill, N. J. 1955. The origin of vertebrates. ban structures as marine habitats. Ambio Clarendon Press, Oxford. 28:595-598. Bishop, J. D. D., and A. D. Sommerfeldt. Lambert, C C, and G. Lambert. 1998. Non­ 1996. Autoradiographic investigation of indigenous ascidians in southern Califor­ uptake and storage of exogenous sperm nia harbors and marinas. Mar. BioI. (Berl.) by the ovary of the compound ascidian 130:675-688. Diplosoma listerianum. Mar. BioI. (Berl.) Monniot, C, and F. Monniot. 1994. Addi­ 125:663-670. tions to the inventory of eastern tropical Boyd, H. C, 1. L. Weissman, and Y. Saito. Atlantic ascidians; arrival of cosmopolitan 1990. Morphologic and genetic verifica­ species. Bull. Mar. Sci. 54:71-93. tion that Monterey Bottyllus and Woods Monniot, C, F. Monniot, and P. Laboute. Hole Bottyllus are the same species. BioI. 1991. Coral reef ascidians of New Cale­ Bull. (Woods Hole) 178:239-250. donia. ORSTOM, Paris. Brock, R, J. H. Bailey-Brock, and J. Goody. Monniot, F. 1983. Ascidies littorales de Gua­ 1999. A case study of efficacy offreshwater deloupe 1. Didernnidae. Bull. Mus. Natl. immersion in controlling introduction of Hist. Nat., 4th ser., 5:5-49. alien marine fouling communities: The Monniot, F., and C Monniot. 1996. New USS Missouri. Pac. Sci. 53:223-231. collections of ascidians from the western Carlton, J. T, and J. B. Geller. 1993. Eco­ Pacific and southeastern Asia. Micronesica logical roulette: The global transport of 29:133-179. nonindigenous marine organisms. Science Monniot, F., and C Monniot. 2001. Asci­ (Washington, D.C) 261:78-82. dians from the tropical western Pacific. Coles, S. L., R C DeFelice, L. G. Eldredge, Zoosystema 23:201-383. and J. T Carlton. 1999. Historical and MO!1J:llot, _F'1J.. Martoj~, _aI!d C:;. M.9!11li9l­ -- receiii:- introductions of non=illdlgenous 1993. Tin aCCUlllulation in tissues of asci­ marine species into Pearl Harbor, Oahu, dians from Mediterranean harbours (Cor­ Hawaiian Islands. Mar. BioI. (Berl.) sica, France). C R Acad. Sci. 316:588­ 135:147-158. 592. Coiiliell; S. D. 2000. Floatiilg poritoons cre­ ---. 1994. Cellular sites ofiron and niCkel ate novel habitats for subtidal epibiota. J. accumulation in ascidians related to the Exp. Mar. BioI. Ecol. 247:183-194. naturally and anthropic enriched New Ca­ Connell, S. D., and T M. Glasby. 1999. Do ledonian environment. Ann. lust. Ocean­ urban structures influence local abundance ogr. 70:205-216. 298 PACIFIC SCIENCE· July 2002

Naranjo, S. A., J. L. Carballo, and J. c. Texas. Johns Hopkins University Press, Garcia-Gomez. 1996. Effects of environ­ Baltimore. mental stress on ascidian populations in Sims, L. L. 1984. Osmoregulatory capabilities Algeciras Bay (southern Spain). Possible of three macrosympatric stolidobranch as­ marine bioindicators? Mar. EcoI. Prog. cidians, Styela clava Herdman, S. plicata Ser.144:119-131. (Lesueur), and S. montereyensis (Dall). J. Nishikawa, T., J. D. D. Bishop, and A. D. Exp. Mar. BioI. Ecol. 82:117-129. Sommerfeldt. 2000. Occurrence of the Sings, H. L., K. C. Bible, and K. L. Rinehart. alien ascidian Perophora japonica at Ply­ 1996. Acyl tunicWorins: A new class of mouth. J. Mar. BioI. Assoc. u.K. 80:949­ nickel chlorins isolated from the Ca­ 950. ribbean tunicate Trididemnum solidum. Nomaguchi, T. A., C. Nishijima, S. Minowa, Proc. Natl. Acad. Sci. U.S.A. 93:10560­ M. Hashimoto, C. Haraguchi, S. Ame­ 10565. miya, and H. Fujisawa. 1997. Embryonic Sommerfeldt, A. D., and J. D. D. Bishop. thermosensitivity of the ascidian, Ciona sa­ 1999. Random amplified polymorphic vignyi. Zool. Sci. (Tokyo) 14:511-516. DNA (RAPD) analysis reveals extensive Paulay, G., L. Kirkendale, G. Lambert, and natural chimerism in a marine proto­ J. Starmer. 2001. The marine invertebrate chordate. Mol. EcoI. 8:885-890. biodiversity of Apra Harbor: Significant Stachowicz, J. J., R. B. Whitlatch, and R. W. areas and introduced species, with focus on Osman. 1999. Species diversity and inva­ sponges, echinoderms and ascidians. Pre­ sion resistance in a marine ecosystem. pared for Naval Activities Guam, under Science (Washington, D.C.) 286:1577­ Cooperative Agreement N68711-97-LT­ 1579. 70001. Van Name, W. G. 1945. The North and Plough, H. H. 1978. Sea squirts of the At­ South American ascidians. Bull. Am. Mus. lantic continental shelf from Maine to Nat. Rist. 84:1-476.