Nonindigenous Ascidians in Tropical Waters1

Gretchen Lambert2

Abstract: Ascidians (invertebrate chordates) are abundant in many ports aroundthe world. Most of them are nonindigenous species that tolerate wide fluctua­tions in temperature, salinity, and even pollution. These sessile suspensionfeeders have a rapid growth rate, usually a short life span of a few months, reachsexual maturity when only a few weeks old, and produce large numbers of short­lived nonfeeding planktonic larvae. They thrive on marina floats, pilings, buoys,and boat bottoms in protected harbors where there is reduced wave action andenhanced nutrients from anthropogenic activities. Nonindigenous ascidiansfrequently overgrow oysters and mussels, which are often cultivated in or nearbusy harbors. Adult ascidians on ship or barge hulls may survive transport overthousands 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 largemasses of fouling nonindigenous taxa, including ascidians. Transfer betweenculture sites of oysters, mussels, and associated lines and nets may provide anadditional mode of transport. Once nonindigenous ascidians become estab­lished, they provide large local sources of larvae for further possible invasionsinto additional harbors and nearby natural marine communities. Invasive speciesinclude both solitary and colonial forms, with a preponderance of large solitaryspecies that thrive in highly disturbed habitats. In Guam, for example, mostnonindigenous ascidians are confined to harbor structures and have not as yetsignificantly colonized natural reefs. In contrast, healthy natural benthic regionsboth inside and outside the harbors of Guam are usually stable coral reef com­munities containing a high diversity, but very low biomass, of native colonialascidian species. However, in several areas of the Caribbean a native colonialdidemnid has recently begun overgrowing coral reefs. In the Gulf of Mexico anonindigenous didemnid now covers many offshore oil rigs and may become athreat to neighboring natural reefs. Additional data on nonindigenous ascidiansin Australia, Palau, Hawai'i, and the Mediterranean are included. Although se­rious invasion of coral reefs has not yet been reported, more studies and regularmonitoring are needed.

INTRODUCTIONS OF nonindigenous ascidiansinto harbors in both tropical and temperatewaters are now commonplace, with the tempo

1 Paper presented at the Ninth International CoralReef Symposium, Bali, Indonesia, 27 October 2000.Manuscript accepted 2januar;r2002. -

2 University of Washington Friday Harbor Labo­ratories, Friday Harbor, Washington 98250. Mailingaddress: 12001 11th Avenue NW, Seattle, Washington98177 (phone: 206-365-3734; E-mail: glambert®fullerton;edu).

Pacific Science (2002), vol. 56, no. 3:291-298© 2002 by University of Hawai'i PressAll rights reserved

of introductions increasing (for reviews seeMonniot et al. 1991, Lambert and Lambert1998, Coles et al. 1999). Ascidians are in­vertebrate members of the phylum Chordata,with a sessile suspension-feeding adult and ashort-lived nonfeeding motile larva. Colonialspecies brood theiryoung and release mature­larvae into the water, but most others spawneggs and sperm that develop in about 24 hrinto swimming larvae with an average larvalduration of 12-24 hr. Because the larval stageis so short (perhaps only a few minutesbetween release and settlement in colonialforms), their primary mode of anthropogenictransport is probably boat hulls or other

291

292 PACIFIC SCIENCE· July 2002

fouled surfaces. Movement between culture having the ability to attach tenaciously tosites 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 organismstransport nonindigenous ascidians (unpubl. that are transported, it can rapidly colonizedata), as were burrowing polychaetes on oys- a new substrate and may already be in re­ters imported from Maine into Hawai'i in productive mode. Because many colonies are1990 (Bailey-Brock 2000). Although ascidian actually chimeras, the gametes of zooids with­larvae 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 colonizenot be their major mode of human-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 oftenacross thousands of kilometers in the Pacific nearly completely composed of nonindige­(including Honolulu to Guam in July 1999 nous species of various taxa, frequently dom­and San Diego to Honolulu in December inated by huge numbers and biomass of1999) has shown that many adult ascidians nonindigenous ascidians (Lambert and Lam­arrive alive (G. Paulay and S. Godwin, pers. bert 1998). The important question is, docomm.). When a bridge collapsed in Palau in these invaders also colonize neighboring nat­1996, a floating pontoon bridge was towed ural reef areas, outcompeting and replacingthere from China the following year; it ar- native species, or do they remain confined torived carrying many live fouling organisms artificial surfaces within harbors? This ques­including ascidians (P. Colin, pers. comm.). tion is highly relevant not only because of theBy whatever means they achieve transport, increasingly large number of artificial surfacesthe same nonindigenous ascidians are often associated with ever-expanding marinas torecorded 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 fishniot and Monniot 1994, 1996,2001, Lambert and wildlife and parks departments are estab­and Lambert 1998). lishing artificial reefs to attract fish for sports

Many nonindigenous ascidians reach sex- fishermen and snorkeling and scuba divingual maturity in just a few weeks and have long hobbyists.breeding seasons (Lambert and Lambert Only a few comparative studies, especially1998). They tolerate wide fluctuations in long-term, of neighboring natural versus ar­temperature and salinity and acclimate rap- tificial habitats have been done. Glasby andidly to these changes (Sims 1984, Nomaguchi Connell (Connell and Glasby 1999, Connellet al. 1997). Nonindigenous ascidians also 2000, Glasby 2000) concluded after manytolerate various types of pollution and are years of study of Sydney Harbour in Australiaknown to sequester or use metal ions (Mon- that pilings and floating pontoons provide aniot et al. 1993, 1994, Naranjo et al. 1996, unique set of habitats that cannot be consid­Sings et al. 1996). Diplosoma listerianum pro- ered equivalent to adjacent natural benthicvides an excellent example of a potential substrates. The environmental conditionsnonindigenous ascidian; it now has a global they are subject to, the particular surfaces ex­distribution. 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 overlapthe resulting chimeras have been shown to in species composition even after severalhave enhanced adaptability (Sommerfeldt and years. Connell (2000) showed that it is not theBishop 1-9-9-9). The -zeeids ean -store €xeg€- natuF€efth€ sUF-faG@--its~Mbut-its-IeGatien that­nous sperm for several weeks (Bishop and is most important in determining which spe­Sommerfeldt 1996), and like other colonial cies will colonize it. Surfaces composed of ei­ascidians the larvae are brooded and released ther artificial or natural materials attached toonly 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 crite­pontoons; similarly, both artificial and natural ria, nine are listed as introduced and 18 assurfaces placed in a benthic ecosystem will be cryptogenic. An additional four included ascolonized by the same types of organisms as cryptogenic were found predominantly onoccur in that ecosystem. In Sydney Harbour, artificial substrates with only a few very smallpilings and pontoons have increased the specimens collected from natural areas (Per­overall 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- Of the 31 species considered introduced orported similar results in a large-scale com- cryptogenic in Guam (Table 1), 16 are colo­parison of the epibiota of artificial structures nial and 15 are solitary. Half of the colonialin and around Apra Harbor, Guam, with forms belong to the order Aplousobranchia.natural reef areas. Although there is some The Phlebobranchia are also well representedoverlap of species, for the most part the biota with five species, two of which are colonialof these adjoining habitats are very different; and three are solitary. The largest group isbased on the work of Glasby and Connell (as the Stolidobranchia, with seven colonial andmentioned earlier), we can assume that these 12 solitary species. All of the 78 species oc­artificial and natural habitats are subjected to curring only on natural substrates are con­very different environment conditions. Float- sidered native/indigenous. Of these 78, 69ing docks, buoys, and pilings are primarily (88%) are colonial. Thus 48% of introduced!colonized by nonindigenous ascidians, where- cryptogenic species are solitary, but most ofas 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 speciesficial surfaces only, 78 species (67%) are found of ascidians from the Channel Islands offon 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 be­known invasive ascidian species in Guam that tween mainland and islands, they found aare also reported as nonindigenous in many preponderance of viviparity in the island spe­other areas (Monniot et al. 1991, Monniot cies and concluded that this was a strategy toand Monniot 1994, 1996, Coles et al. 1999), reduce gamete loss. However, nearly all theall were found on artificial surfaces; three of viviparous species were colonial. Thus an­these also occurred on nearby reefs: Botryllus other ecological factor that must be consid­niger, Cnemidocarpa irene, and Herdmania pal- ered is growth form: colonial species are lowlida. On natural reefs these three species were encrusting mats; solitary species project intosmall, sparse, and formed only a negligible the water column. The high-energy surf zonepart of the reef fauna, in striking contrast to environment present around the Channel Is­their larger size and numbers on artificial lands as well as on the reef edges aroundsubstrates. (One immature Microcosmus sp., Guam favors ascidians with both a low en­possibly M. exasperatus but too small to iden- crusting form and viviparous mode of repro­tify, 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 pil­four 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. Theof introduced are that the species (1) be re- epibionts that colonize these structures, andstricted to artificial surfaces and (2) have an indeed the large-scale fouling communitiesextra-Indo-West-Pacific distribution; if only that form, can do so only because of the pro­one 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- RestrictionWest-Pacific to Artificial

Species Status Apra Harbor Distribution Substrates Solitary/Colonial

AplousobranchiaGold-green compound Cryptogenic 1 1 CDidenmum perlucidum Introduced 1 1 1 CDidemnum psammathodes Cryptogenic 0 1 0 CDiplosoma listerianum Introduced 1 1 1 CDiplosoma "fluffy" Cryptogenic 1 ? 1 CLissoclinum fragile Introduced 1 1 CPolyclinum consteltatum Introduced 1 1 C

PhlebobranchiaPerophora multiclathrata Cryptogenic 1 0 CPerophora sagamiensis Cryptogenic 0 0 CAscidia sydneiensis Introduced 1 1 SAscidia sp. B Cryptogenic ? 1 SPhallusia nigra Introduced 1 S

StolidobranchiaBotryllus cf. simodensis Cryptogenic 1 0 1 CBotryllus niger Cryptogenic 1 1 0 CBotryllus sp. A Cryptogenic 1 ? 1 CBotryllus sp. B Cryptogenic 1 ? 1 CCnemidocarpa irene Cryptogenic 1 1 0 SPolyandrocarpa sagamiensis Cryptogenic 1 0 1 CPolycarpa aurita Cryptogenic 1 0 1 SStyela canopus Introduced 1 1 1 SSymplegma brakenhielmi Introduced 1 1 1 CSymplegma sp. A Cryptogenic 1 ? 1 CHerdmania insolita· Cryptogenic 1 ? 1 SHerdmania pallida Cryptogenic 1 1 0 SMicrocosmus exasperatus Introduced 1 1 1 SMicrocosmus helleri Cryptogenic 1 1 0 SMicrocosmus pupa Cryptogenic 1 0 1 SPyura confragosa Cryptogenic 1 0 1 SPyura curvigona Cryptogenic 1 0 0 SPyura honu Cryptogenic 1 0 0 SPyura cf. robusta Cryptogenic 1 0 0 S

31 total

out, budding in colonial ascidians is "primar­ily a means of extending the living, repro­ducing ascidian entity in two rather thanthree dimensions, in relation to the exploita­tion of flat surfaces on which uniform three-

- Oiinensional growth leads to-mcreasmgc fnse"curity of foothold."

In Palau, preliminary data indicate that, asin Guam, the artifical structures of MalakalHarbor are dominated by large, solitary spe­cies of nonindigenous ascidians (unpubl.obs.), while the ascidians of the reefs are pri­marily native colonial species (Monniot andMonniot 2001).

Naranjo et al. (1996) analyzed the ascidiandistribution in the large Mediterranean portof Algeciras Bay, Spain, and separated thespecies into three fairly distinct groups thatdiffer considerably in their physiological tol-

--er:m-c'es--rowave-;rction;- pollutants;-sedinren~ -­tation, and other environmental factors: (a)"exclusively in the outer zone of the baywhich settle mainly on natural rock sub­strates, Eb)species more abundant in the in­ner zone of the bay which settle mainly onartificial substrates, and (c) species foundthroughout the bay." The same nonindige­nous 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% ofmon or abundant on artificial structures in the rig superstructure that had previouslyAlgeciras Bay, but were generally not present been out of water. A quick survey of the twoelsewhere in the bay. Naranjo et al. (1996) underwater reefs just mentioned during sum­concluded that fouling species, which are mer 2000 appears to indicate that D. perluci­primarily nonindigenous ascidians, dominate dum is so far restricted to the oil rigs and hasartificial substrates in the harbor, are tolerant not invaded the reefs, but it is a situation thatof sedimentation and water stagnation, and needs to be closely monitored. Any degrada­grow rapidly in water highly enriched by or- tion of the natural reefs might give the asci­ganic material from runoff and sewage treat- dian the competitive advantage it needs to getment effiuents; thus they can be considered a foothold.indicators of regions of intense environmental Didemnum perlucidum apparently breedsstress. Native species prefer natural benthic throughout the year, daily releasing largesubstrates, 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.). Di­thus can be considered indicators of relatively 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 andwe can be unconcerned about controlling the natural substrates. It was not listed by Vanintroduction of nonindigenous ascidians in Name (1945) or Plough (1978) for any regiontropical waters? Some available information in the United States. Thus it may be a recentsuggests otherwise. In the Gulf of Mexico, introduction to the Caribbean or was a minorthe Texas Parks and Wildlife Department has member of the fauna until its rapid increaseutilized decommissioned offshore oil and gas and spread within the past few years. Di­rigs as artificial reefs (J. Culbertson, pers. demnum perlucidum is now a common foulercomm.). While the rigs are still in place in of artificial surfaces in harbors in Brazil (dawater up to 70 m deep, they are cut in half. Rocha and Monniot 1995) as well as through­The bottom half (about 35 m in height) may out the Indo-West Pacific, including Guambe 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 (reviewedture (walkways, etc.) of the top halves now in Monniot and Monniot 1996). It is oftenalso becomes available for colonization by abundant, overgrowing other epibionts (es­marine organisms. In all cases, all of the epi- pecially solitary ascidians) and sometimesbiota that had been growing for many years hanging in long, thick strands that easilyon the underwater legs of the rigs is left break off and drift away; this may be an im­in place and thus may be transported to new portant method of spreading, as it appears tolocations. 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 Trididemnumbeautiful underwater reefs such as Flower solidum are facultative hosts to unicellularGarden Banks and Stetson Bank, both pro- photosymbionts such as Prochloron; thus nottected under the National Marine Sanctuary only can the photosymbionts be transported

-program~-In-the-past'several- years'a--non~---alorrg-w:iththeir-hostascidian-colony-but theyindigenous colonial ascidian, Didemnum per- may make it easier for the host to becomelucidum, has completely overgrown all sides of established in a new area.a number of these oil rigs, covering hundreds Healthy communities with a high diversityof" square meters and smothering the sponges, - of-speeiesseem -able to prevent ()f-limit thebivalves, and other invertebrates that for- establishment of nonindigenous ascidiansmerly grew on the structures. On a rig that (Stachowicz et al. 1999), though there is somewas cut in half in 1997, the upper half sunk disagreement about this theory. When reefsnext to the lower half and then surveyed 14 become degraded or when bacterial levels

296 PACIFIC SCIENCE· July 2002

Literature Cited

ACKNOWLEDGMENTS

overgrowth of other sessile organisms. Morefrequent dry dock cleaning of boat hullsmight help prevent the spread of fouling spe­cies (Brock et al. 1999), and perhaps handremoval of invaders in an early stage of inva­sion might prevent their establishment. Al­though the mostly nonindigenous biota onartificial structures in harbors has apparentlynot affected nearby natural areas (Connelland Glasby 1999), there is still the possibilityof long-term and as yet unforeseen changes inadjacent natural ecosystems (Bak et al. 1996,Glasby and Connell 1999), and careful regu­lar monitoring ofsensitive natural areas shouldbe carried out.

Bailey-Brock, J. H. 2000. A new record of thepolychaete Boccardia proboscidea (Family

rise, certain species of ascidians may undergorapid increases. Ascidians are efficient sus­pension feeders. Bak et al. (1981, 1996, 1998)studied the coral reefs of the Caribbean islandof Cura~ao for over 15 yr. Before 1980 thenative didemnid Trididemnum solidum waspresent in small numbers, did not appear tocompete with native corals for food andspace, and preferred to settle on dead coralwith a thin algal turf. However, by 1996 Baket al. found a 900% increase in T. solidum,which they attributed at least in part to greatlyincreased densities of suspended bacteria inthe water resulting from a big increase in an­thropogenic activities during the 15 yr be­tween the two studies. Trididemnum solidumnow actively outcompetes the corals, over­growing and killing live coral. A similar situ­ation is occurring in the Bay Islands off thecoast of Honduras, about 1800 km from Cu­ra~ao, where large mats of T. solidum haveappeared in the past 2-3 yr and are coveringand killing the corals (J. Keck and R. Hous­ton, pers. comm.).

I am greatly indebted to G. Paulay and theentire staff of the University of Guam MarineLaboratory for their willing and cheerful as­sistance in all matters large and small duringmy stays in Guam, funded by a Sea Grant toG. Paulay. G. Paulay aided by L. Kirkendale,C. Meyer, R. Ritson-Williams, J. Starmer, T.

CONCLUSIONS Rongo, and P. Houk collected ascidians byAlthough 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 Coralthey are often the dominant species with an Reef Research Foundation provided all nec­

essary support for the work in Palau. Manyincredibly high biomass, they rarely colonizeadjacent natural benthic ecosystems. Healthy thanks to L. G. Eldredge of the Pacific Science

Association for obtaining financial supportnatural ecosystems such as coral reefs com- for my work in Honolulu and participation atpri~e a high biodiversity, with cOl?~lex inter- the Ninth International Coral Reef Sympo­aCTIons among the speCIes, and this IS thought. d S G d' R D F l' d S

b " £" "th SlUm, an to . 0 wm, . e e Ice, an .to e 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 loresta IS ent 0 mva mg speCIes. owever, 11' f . J C lb f th

1 f b · d d d co eCTIon 0 speCImens. . u ertson 0 emany cora ree areas are ecommg egra e T P ks d W'ldli1: Dd th .. " , 1 b 1 exas ar an 1 Ie epartrnent pro-ue to an ropogemc 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 emg mc u mg e recent warmmg ue to G If f M' Th " .

N "-) d h th Abu 0 eXlCO. e manuscnpt was lm-mo ,an per aps 0 er causes. num er d b th . fohepurts- mosr-of-them-unpublished-as7 et __ Jlro.ve y (:..s.!!gg~.!lons_Q.._an ~Q..I!Y!!!0us _

d ' . th "d d f l' reVlewer. I am especIally grateful to C. Lam­are ocumennng e rapl sprea 0 severa b 1 f, h' "' ·d·th allascidian species over the past several years in ert as afwthiafs or

kIS unsnnnng at Wl

. d' 1 . f th aspects 0 s wor .varlOUS temperate an tr0plca reglOns 0 eworld. The reasons for this change -are flotknown, but they do coincide with the latest ElNino event. These ascidians have not de­clined with the return of cooler water; on thecontrary they continue their rapid spread and

Nonindigenous Ascidians in Tropical Waters . Lambert 297

Spionidae), imported to Hawai'i with oys­ters. Pac. Sci. 54:27-30.

Bak, R P. M., J. Sybesma, and F. C vanDuyl. 1981. The ecology of the tropicalcompound ascidian Trididemnum solidum.n. Abundance, growth and survival. Mar.Ecol. Prog. Ser. 6:43-52.

Bak, R P. M., D. Y. M. Lambrechts, M.Joenje, G. Nieuwland, and M. L. J. VanVeghel. 1996. Long-term changes on coralreefs in booming populations of a com­petitive colonial ascidian. Mar. Ecol. Prog.Ser. 133:303-306.

Bak, R P. M., M. Joenje, I. de Jong, D. Y. M.Lambrechts, and G. Nieuwland. 1998. Bac­terial suspension feeding by coral reefbenthic organisms. Mar. Ecol. Prog. Ser.175:285-288.

Berrill, N. J. 1955. The origin of vertebrates.Clarendon Press, Oxford.

Bishop, J. D. D., and A. D. Sommerfeldt.1996. Autoradiographic investigation ofuptake and storage of exogenous spermby the ovary of the compound ascidianDiplosoma listerianum. Mar. BioI. (Berl.)125:663-670.

Boyd, H. C, 1. L. Weissman, and Y. Saito.1990. Morphologic and genetic verifica­tion that Monterey Bottyllus and WoodsHole Bottyllus are the same species. BioI.Bull. (Woods Hole) 178:239-250.

Brock, R, J. H. Bailey-Brock, and J. Goody.1999. A case study of efficacy of freshwaterimmersion in controlling introduction ofalien marine fouling communities: TheUSS Missouri. Pac. Sci. 53:223-231.

Carlton, J. T, and J. B. Geller. 1993. Eco­logical roulette: The global transport ofnonindigenous marine organisms. Science(Washington, D.C) 261:78-82.

Coles, S. L., R C DeFelice, L. G. Eldredge,and J. T Carlton. 1999. Historical and

-- receiii:- introductions of non=illdlgenousmarine species into Pearl Harbor, Oahu,Hawaiian Islands. Mar. BioI. (Berl.)135:147-158.

Coiiliell; S. D. 2000. Floatiilg poritoons cre­ate novel habitats for subtidal epibiota. J.Exp. Mar. BioI. Ecol. 247:183-194.

Connell, S. D., and T M. Glasby. 1999. Dourban structures influence local abundance

and diversity of subtidal epibiota? A casestudy from Sydney Harbour, Australia.Mar. Environ. Res. 47:373-387.

da Rocha, R M., and F. Monniot. 1995.Taxonomic and ecological notes on someDidemnum species (Ascidiacea, Didernni­dae) from Sao Sebastiao Channel, south­eastern Brazil. Rev. Bras. BioI. 55:63 9-649.

Fay, R C, and J. A. Vallee. 1979. A survey ofthe littoral and sublittoral ascidians ofsouthern California, including the Chan­nel Islands. Bull. South. Calif. Acad. Sci.78:122-135.

Glasby, T. M. 2000. Surface composition andorientation interact to affect subtidal epi­biota. J. Exp. Mar. BioI. Ecol. 248:177­190.

Glasby, T M., and S. D. Connell. 1999. Ur­ban structures as marine habitats. Ambio28:595-598.

Lambert, C C, and G. Lambert. 1998. Non­indigenous ascidians in southern Califor­nia harbors and marinas. Mar. BioI. (Berl.)130:675-688.

Monniot, C, and F. Monniot. 1994. Addi­tions to the inventory of eastern tropicalAtlantic ascidians; arrival of cosmopolitanspecies. Bull. Mar. Sci. 54:71-93.

Monniot, C, F. Monniot, and P. Laboute.1991. Coral reef ascidians of New Cale­donia. ORSTOM, Paris.

Monniot, F. 1983. Ascidies littorales de Gua­deloupe 1. Didernnidae. Bull. Mus. Natl.Hist. Nat., 4th ser., 5:5-49.

Monniot, F., and C Monniot. 1996. Newcollections of ascidians from the westernPacific and southeastern Asia. Micronesica29:133-179.

Monniot, F., and C Monniot. 2001. Asci­dians from the tropical western Pacific.Zoosystema 23:201-383.

MO!1J:llot, _F'1J.. Martoj~, _aI!d C:;. M.9!11li9l­1993. Tin aCCUlllulation in tissues of asci­dians from Mediterranean harbours (Cor­sica, France). C R Acad. Sci. 316:588­592.

---. 1994. Cellular sites of iron and niCkelaccumulation in ascidians related to thenaturally and anthropic enriched New Ca­ledonian environment. Ann. lust. Ocean­ogr. 70:205-216.

298

Naranjo, S. A., J. L. Carballo, and J. c.Garcia-Gomez. 1996. Effects of environ­mental stress on ascidian populations inAlgeciras Bay (southern Spain). Possiblemarine bioindicators? Mar. EcoI. Prog.Ser.144:119-131.

Nishikawa, T., J. D. D. Bishop, and A. D.Sommerfeldt. 2000. Occurrence of thealien ascidian Perophora japonica at Ply­mouth. J. Mar. BioI. Assoc. u.K. 80:949­950.

Nomaguchi, T. A., C. Nishijima, S. Minowa,M. Hashimoto, C. Haraguchi, S. Ame­miya, and H. Fujisawa. 1997. Embryonicthermosensitivity of the ascidian, Ciona sa­vignyi. Zool. Sci. (Tokyo) 14:511-516.

Paulay, G., L. Kirkendale, G. Lambert, andJ. Starmer. 2001. The marine invertebratebiodiversity of Apra Harbor: Significantareas and introduced species, with focus onsponges, echinoderms and ascidians. Pre­pared for Naval Activities Guam, underCooperative Agreement N68711-97-LT­70001.

Plough, H. H. 1978. Sea squirts of the At­lantic continental shelf from Maine to

PACIFIC SCIENCE· July 2002

Texas. Johns Hopkins University Press,Baltimore.

Sims, L. L. 1984. Osmoregulatory capabilitiesof three macrosympatric stolidobranch as­cidians, Styela clava Herdman, S. plicata(Lesueur), and S. montereyensis (Dall). J.Exp. Mar. BioI. Ecol. 82:117-129.

Sings, H. L., K. C. Bible, and K. L. Rinehart.1996. Acyl tunicWorins: A new class ofnickel chlorins isolated from the Ca­ribbean tunicate Trididemnum solidum.Proc. Natl. Acad. Sci. U.S.A. 93:10560­10565.

Sommerfeldt, A. D., and J. D. D. Bishop.1999. Random amplified polymorphicDNA (RAPD) analysis reveals extensivenatural chimerism in a marine proto­chordate. Mol. EcoI. 8:885-890.

Stachowicz, J. J., R. B. Whitlatch, and R. W.Osman. 1999. Species diversity and inva­sion resistance in a marine ecosystem.Science (Washington, D.C.) 286:1577­1579.

Van Name, W. G. 1945. The North andSouth American ascidians. Bull. Am. Mus.Nat. Rist. 84:1-476.