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BIOLOGICAL CONTROL of IOLLER ALGAE, CAULERPA TAXIFOLIA '' Lars WJ Anderson USDA- ARS Exotic and Invasive Weed Research Davis, CA

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BIOLOGICAL CONTROL of IOLLER ALGAE, CAULERPA TAXIFOLIA '' Lars WJ Anderson USDA- ARS Exotic and Invasive Weed Research Davis, CA '. BIOLOGICAL CONTROL OF IOLLER ALGAE, CAULERPA TAXIFOLIA '' Lars WJ Anderson USDA- ARS Exotic and Invasive Weed Research Davis, CA ABSTRACT Caulerpa taxifolia, a marine alga, has invaded Mediterranean subtidal ecosystems from small founder populations in 1984 to present expanse of about 6,000ha, including coasts of France, Monaco, Italy, Spain and I, Croatia, and Tunisia. It was recently found in Australia and Southern California in 2000. It has successfully displaced several native, benthic communities and can establish on a variety of substrates from sand to rocky shores. Reproduction and spread is clonal via stolons supporting fronds from 0.2 to 3 meters long. The small, California populations have been under vigorous containment and eradication since their discovery under the direction of the Southern California Caulerpa Action Team (SCCAT). Four species of herbivorous gastropods (mollusks) have been examined in Europe for potential reduction of th extensive Mediterranean C. taxifolia populations ( Oxytnoe azuropunctata, Elysia subornatat, Oxynoe olivacea and Lobiger serradifalci) E. suboranata, a tropical species, though unable to survive below 15C, has direct, benthic development (no pelagic larvae), feeds well at higher (e.g.>20C) temperatures, and appears to be the best candidate. However, since it is not native, further testing of host-specificity and potential for switching is required. L, serraedifalci, a native to the Mediterranean, feeds on C. taxifolia, but also tends to produce fragments, which can spread the population further. At present, there is no ' ' proven, effective biological control agent for C. taxifolia. INTRODUCTION Nearly 20 years ago, one of the most interesting and aggressive marine invasive species, Caulerpa taxifolia, entered Mediterranean waters off Monaco and began its dominance of subtidal habitats there (Meinesz, 1999). This alga has many biological characteristics that facilitate its successful establishment, dispersal, and displacement of native species. C. taxifolia, (Byropsidales) a green siphonous alga, is a true single-celled coenocytic organism possessing adequate architectural strength to form large, persistent colonies in spite of the wave and tidal action of coastal environments (Fig. 1.) This strain can grow in very low light, yet does well in moderately high light of clear, shallow waters. It tolerates a wide range of water temperatures 10 to 31 °C, but has maximum growth in temperatures at 20°C and above (Komatsu et al. 1997, Gacia et al. 1996). Thus, it could become established in coastal waters of Mexico both U.S. coasts. (However, it will not tolerate fresh water.) Note: The genetic relationships of Caulerpa taxifolia was recently reported by Jousson et al. (2001), who showed that the introduction in the US (California) was indeed the same as the Mediterranean strain. Dispersal and spread is through elongation of rapidly growing stolons as well as from fragments of the thalli (fronds) that may be produced from wave action, foraging fish or human activities such as fishing and anchoring. Very small, sub-centimeter sized pieces can produce new plants. However, reproduction appears to be exclusively vegetative in the Mediterranean strain- only male gametes have been observed (Zuljevic and Antolic 2000). Growth rates of one to a few several cm/day have been observed. In addition, Williams and Grosholz (2002) reported the presence of many "proliferations", or second-order branch points on fronds in one of the California populations. The importance of recruitment via fragments was examined by Ceccherelli and Cinelli (1999), who showed, through release of fragments at 3 and 10 m depths during different seasons, that successful establishment was greatest from June to September at the margins of native seagrass, Posidonia oceanica stands. Deep water fragment movement off Monaco (45m to 100 m) was shown by Belsher and Meinesz (1995). This raises the interesting question of how grazers feed, not just how much they feed. For example, grazing in the Mediterranean by a native gastropod, Lobiger serradifalci, appears to disperse the plant by creating fragments (Zuljevic et al. 2001). Displacement of native algae, and general dominance of benthic substrate, is achieved through elongation and proliferation of anchoring stolons, dense canopy formation, and through the presence of the toxin, caulerpenyne, which appears to deter grazing by most organisms. 79 Fig. 2. Locations of Caulerpa ta:xifolia in the USA. (Agua Hedionda and Huntington Harbor) ... 'l. '. 61\H of C.t.rxffolil> (Aliff aetlOldna 10 al~ ono yoM) ~'.;r::.4:=UM~'fJS,1.91) 2.:T---..(q l : Z,..,4"$'-Rl~,-(~-1><-9.1) 4 :t-•w-1oo(lf) J : p•ruh s.,.~.. (91) •: fl,l"<U'( Pl-94) 1 :11!\p,,u, Po,i,,-:n:Jo~ *:""'4» IMq-...(~~· :Sb-Eo-=t-h't--Allit•~•.,_,, lO: M4wqoo,c.,.~•& !>SJ 11 ,u-<n93·&• it tl: DllMIM.airia,. (I)) I.!".... de.M>•, ,........ .,, .,_...,(9'/J 1• : J,oporia. OIHjlo 1>·'> 1$ ; McHlllO, """11ri61l) J6; s...--•.. -l"'l 11 San-/µ/ IS : po,, ... Tl,Oool..t.(• (1131 !) : C..,, k fl-..W<l~( N-QS} • l0:Aa44', (~l) :; 11 : V..iiroi~.. l,o · AA,...,(9<) • 22; lJ.4op411. Qi,.,(9')·.,.,.___, 2J : &....G,,d.11,4,-(9l) 2A : MJibJl.fb..t.. 4'J!rAl(93) 15 ' b,."-1-(lll) · .l.Dlit.• ...u--.. .. c.,.,~ , M, : V1l1wif. (k,U11"""' 0-$ 3$~:.S•M•odl,.ot,l>c~ ' =·<,Cl .)Q~C.Nl... ,d4.tfl•~ (Ultl'c l.udu.4 'Nlii'f ~,,a Fig. 3. Spread of C. ta:xifolia in the Mediterranean areas. It is clear that, with the fortuitous advantage of having observed the prolific spread of C. taxifolia in Europe, the USA reaction was both reasonable and offered. the best hope for long-term prevention of further incursions in coastal waters here. It is important to note that in addition to the immediate containment and eradication effort, the California state legislature passed a bill banning the sale, transport and possession of C. taxifolia and eight other "look-alike" species in Caulerpa genus. Thus, from an operational as well as political perspective, the response to these first (last?) populations was very quick. 81 ... .. Table 1. Some characteristics of four potential biological control agents for C. taxifolia. ... Species Provenance Larval Opt. Host-Specificity Feeding Development Temp ("preferences") Characteristics Range for Feedin2 Lobiger Mediterranean Pelagic l 7-25C C.prolifera Incisions lead to serradifaclci C.taxifolia wholes and (w/she/1) fragments; low feedine: rate. Elysia subornata Tropical Direct, 17-25 C C. taxifolia Incisions on all parts; (wlo shell) Benthic <15C is C. racemosa kleptoplasty; stores lethal caulerpenin; high feeding rate ( 1Ox others). Oxynoe Tropical Direct, 17-25C C. taxifolia Incisions on all parts; azuropunctata Benthic C. racemosa stores caulerpenin; (w/shel/) medium feedine: rate. Oxynoe olivacea Mediterranean Pelagic 12-25C C. prolifera Feeds on individual (w/she/1) C. taxifolia pinnules; low feedine: rate. Caulerpa taxifolia and C. racemosa are not the only siphonous algae that have expanded beyond native ranges, nor which are readily consumed by sacoglossans. The alga, Codium fragile and various sub-species (some of which are now prolific in, but not indigenous to, Europe) have been the subject of a large body of work by Cynthia Trowbridge at Oregon State University. She has examined several aspects of sea slug feeding (e.g. Placida dendritica), reproduction and responses in grazed species, and "switching" behavior of more catholic sea slug foragers. The approaches Trowbridge has taken (see Trowbridge, 199la,b; Trowbridge, 1993; Trowbridge and Todd, 2001; Trowbridge, 2002 ) are models for more in-depth work on potential agents to control invasive Caulerpa species. Clearly, the complexities of host-attractants, deterrents, physical responses to feeding (e.g. location of radula incision and cytoplasm extraction), and group feeding behavior will be important to understand as part of developing a strategy for a Caulerpa biocontrol program. .Allochtonous species J - - ~ Ernbryonn!c stdge 20 lf;,ys Direct dcvclop,)111~::11 Fig. 4. Life cycle of Elysia subornata (From Theirry Elysia subomata Thibaut). Benthic - juvenile Lile time 9 month r,,einosz et al 1996, Thibaut ot al. 2001 83 Piazzi, L., G. Ceccherelli, and Fr. Cinelli. 2001. Threat to macroalgaldiversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol. Prog. Ser. 210: 149-159. Thibaut, T. and A. Meinesz. 2000. Are the Mediterranean ascoglossan molluscs Oxynoe olivacean and Lobiger serradifalci suitable agents for a biological control against the invading tropical alga Caulerpa taxifolia? C.R. Acad. Sci. Paris. 323:477-488. Thibaut, T., A. Meinesz, P. Amade, S. Charrier, K. De Agnelis, S. Ierardi, L. Mangialazo, J. Melnick and Vidal. 2001. Elysia subornata (Molusca) a potential control agent of the alga Caulerpa taxifolia (Chlorophyta) in the Mediterranean Sea. J. Mar. Bio. Ass. U.K. 81:497-504. Trowbridge, C. D. 1991a. Diet specialization limits herbivorous sea slug's capacity to switch among food species. Ecol. 72: 1880-1888. Trowbridge, C.D. 1991b. Group memberfshop facilitates feed of the herbivorous sea slug Placida dendritica. Eco. 72: 2193-2203. Trowbridge, C.D. 1993. Interactoins between an ascoglossan sea slug andits green algal host: branch loss and role of epiphytes. Mar. Ecol. Prog.Ser. 101: 263-272. Trowbridge, C.D. and C.D.Todd. 2001. Host plant change in marine specialist herbivores: Ascoglossan sea slugs on ... introduced macroalgae. Ecol. Monogr. 71: 219-243 . ' Trowbridge, C.D. 2002. Northeastern Pacific sacoglossan pisthobrancs: Natural history review, bibliography, and prospectus. The Veliger 45: 1-24. Uchimura, M., A. Ribal, A. Mato, R. San deaux, J. Sandeaux, and J.C.Baccou. 2000. Potential use of Cu2+, K + and Na+ for the destruction of Cau/erpa taxifolia: Differential effects of photosynthetic parameters. J. Applied Phycology 12: 15-23. Williams, S. and E. D. Groscholtz. 2002. Preliminary reports from the Caulerpa taxifo/ia invasions in southern California. Marine Ecol. Progress Series (in press). Zuljevic, A. and B. Antolic. 2000. Synchronous release of male gametes of Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean Sea.
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