Killer algae escapes captivity, terrorizes locals!

Sounds like a well-worn horror movie plot but in fact, is the history of a creature that took hold of a tiny patch of the Mediterranean sea floor beneath the windows of the Monaco Oceanographic Museum in 1984. The warning bell tolled, but most refused to listen.

Caulerpa taxifolia, a species of tropical green algae used in aquariums and cultivated for improved cold tolerance, is among the largest single-celled organisms known. It grows up to 2 cm per day (nearly an inch), and reaches densities of over 8,000 fronds per square meter.  Even the tiniest pieces can take root and multiply vegetatively, overgrowing everything to form a lush carpet across the bottom of the sea, killing nearly everything in its tracks.


Caulerpa spreads quickly, covering every horizontal surface in its tracks....


and creeps down vertical underwater walls - it can thrive in deep habitats as long as light is available.

After 1984, as European bureaucrats argued over fault, jurisdiction, and action, the alga spread over many thousands of acres of Mediterranean sea floor off the coasts of France, Spain,  Italy, and Croatia - another story of 'too little, too late.'


Caulerpa engulfing a gorgonian coral

Across the globe, time after time, exotic species teach us hard ecological lessons. To prevent other rich coastal habitats from becoming monotypic stands of underwater astro-turf, we must learn from the European situation, taught largely by Alexandre Meinesz in 'Killer Algae.'


Caulerpa encroaching on a Posidonia meadow

The teachings of Meinesz have apparently been effective, resulting in political action in the U.S. and Australia. In July 2000, divers located ten patches of the alga off the coast of San Diego, California. Scientists covered the algal mats with tarpaulins and saturated them with chlorine or copper sulfate. SCUBA diving clubs in California and elsewhere have been mobilized to watch for more outbreaks. Continual vigilance and public input will be required to keep our coastal areas free from this leafy green monster.

 Contents

 

Taxonomy:

  • Kingdom: Protoctista
  • Phylum: Chlorophyta
  • Class: Chlorophyceae (or Ulvophyceae)
  • Order: Caulerpales (or Bryopsidiales)
  • Family: Caulerpaceae
  • Caulerpa taxifolia
  • Other names:  C. xenogigantia or godzilliana (Meinesz)
  • More information here

Contents

 

Identification Aids:

Photos - Université de Nice
Photos - RIDNIS, UC Davis
Photos - Joaco's page

Book - Littler et al. 1992.
Book - Littler & Littler 2000.
Book - Hunan 199_.

Contents

 

Similar Species:

*Also see Internet links and books listed above

C. mexicana:
Photo - Université de Nice
Photos - Joaco's page

C. sertularioides:
Photo - John Rice
Photo - Smithsonian
Photo - U. Tsukuba
Photo - C. Y. Accard

C. prolifera:
Photo - U. Catania

Other Caulerpa:
Photos - Ballantine & Aponte
Photos - Joaco's page

Contents

 

More Cool Links:

International Caulerpa taxifolia Conference, San Diego, California, USA
(Jan. 31 - Feb. 1, 2002)

Other English Sites:
Science News Online article
Essay by Maricela Yip

Other European Sites:
Université de Nice
Caulerpa on M@reNostrum 
Biocontrol on M@reNostrum
Caulerpa census
Killeralge in der Adria
IFREMER's Caulerpa site
Danger Caulerpa taxifolia
French eradication site

If you read French, check out the massive list of scientific publications compiled by the Université de Nice (through December 1996), and the even more massive list of over 1000 newspaper, magazine, and popular articles compiled by the Université de Nice (through January 2001).

Contents

 

Contacts:  

If you see this species  outside its native range, please contact:

In Europe:
Caulerpa On Line (has form for recording observations)

In Australia:
Dr. Alan Millar of Sydney Botanical Gardens, Dr. Darryl Grey of NSW Fisheries, or Dr. Britta Shaffelke at CRIMP, all listed on the Sea Slug Forum.

In the USA (west):
Phone SCCAT at (858) 467-2952, or e-mail Dr. Susan Williams of Bodega Marine Lab.

In the USA (east & Gulf):
Dr. James Carlton
Dr. Linda Walters

If all else fails, contact Todd Campbell of the Institute for Biological Invasions at lizardman@utk.edu, who will forward your message to the appropriate person.

Contents

 

Please cite this page as:
Campbell, T. S and M. Tebo. 2001. Killer algae, Caulerpa taxifolia. Institute for Biological Invasions Invader of the Month.
http://invasions.bio.utk.edu/
invaders/Caulerpa.html

 

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November, 2001
"Killer" Algae
(Caulerpa taxifolia)

By Todd Campbell and Mary Tebo

Photos courtesy of Alexandre Meinesz,
University of Nice-Sophia Antipolis

EVENT: January 31 - February 1, 2002: International Caulerpa taxifolia Conference, San Diego, California, USA


Contents:  Taxonomy - Description - Native Range & Biology - Introduced Range & Biology - Known & Potential Impacts - Identification Aids - Similar Species - Literature Cited - Contacts


Description:   Caulerpa is just one of over 7,000 species of green algae, a paraphyletic group of plant-like, green forms ranging from single-cells (Chlamydomonas) to filaments (Spirogyra) to colonies (Volvox) to various sheet-like and branching forms (Acetabularia). Like plants, green algae contain photosynthetic pigments (chlorophyl a and b), so they make their own food by synthesizing carbohydrates from carbon dioxide, water, and sunlight, and store this carbohydrate energy as starch. Algae come in many colors, but in green algae, the photosynthetic pigments are green, rather than brown or red. For general information on plants and algae, visit the Photosynthetic Life page, and for an overview of green algae, visit the Chlorophyta Page, both constructed by Dr. Charles Delwich of the University of Maryland.

Green algae are distinguished by their number and arrangement of flagella, tiny whip-like organelles that propel them, however, gametes or spores are often the only life stages that have flagella. Like plants, their cell walls are made of cellulose and pectin, but some have calcareous cell walls (Halimeda), and their cells are often very large, and often have more than one nucleus. Green algae reproduce via alternation of generations, where multicellular, haploid (1n) forms alternate with multicellular, diploid (2n) forms in every other generation. For a great synopsis of algae with lots of pictures, visit the Chlorophyta page by Dr. David Webb.

Algae in the Order Caulerpales have no internal cell walls - they are single cells with intracellular organelles floating freely in cytoplasm, a condition termed "coenocytic" (Jacobs 1994 gives a good overview). Because they can grow up to a few meters in length, algae of the genus Caulerpa are the largest known cells! Caulerpa is a group of generally tropical green algae that vary widely in morphology from bunches of grapes, to blade-like forms that look like seagrasses, to finely-branched (pinnate), almost feather-like forms. Caulerpa taxifolia is a pinnately branched form, and looks similar to C. mexicana and C. sertularioides (see links to identification sites below).


Native Range & Biology: Members of the genus Caulerpa are found worldwide in mostly warmer latitudes, but five species also occur naturally in the Mediterranean (prolifera, ollivieri, racemosa, mexicana, and scalpelliformis). Originally discovered in the Virgin Islands, Caulerpa taxifolia is native to tropical waters of the Caribbean (Virgin Islands to South America), eastern Atlantic (west coast of Africa), Indian Ocean (east coast of Africa and from Pakistan to Indonesia), and south Pacific (from Japan to Australia), and was recently discovered in the Red Sea.

In many locations, it occurs with other types of Caulerpa algae, some very similar, and some very different from C. taxifolia (see our section on similar species). For instance, C. taxifolia is found with 15 other Caulerpa species in Puerto Rican waters (see Ballantine and Aponte for a species list and photos of three species).

In the Caribbean and Pacific, C. taxifolia reproduces sexually during a short period each year. Dispersal generally takes place via fragmentation, and only a tiny piece is required for successful establishment of new patches. As a result, C. taxifolia can be transported long distances in the propulsion or anchoring systems of pleasure boats or in commercial fishing tackle (nets, trawls, long-lines, etc.).


Introduced Range & Biology: Caulerpa taxifolia has been introduced to three regions: 1) the Mediterranean Sea on the coasts of Croatia, France, Italy, Monaco, and Spain, 2) the southern California coast near San Diego, and 3) Australia near Sydney and in New South Wales. The history and biology of this green stranger in strange lands is interesting indeed...

The Mediterranean Invasion: Since it was first detected outside its native range in 1984, Caulerpa taxifolia has become widespread across the northern and western coasts of the Mediterranean and in Adriatic coastal regions, crossing the borders of five countries. The history of the invasion, the politics of identifying the source of the invasion, and the reasons control and eradication attempts failed, are revealed in detail by Alexandre Meinesz in his book, "Killer Algae" (Meinesz 1999; read an excerpt). Because of the severity of the threat to other shorelines, Dan Simberloff translated the book from French to English, so that others might learn as much as possible from the Mediterranean invasion. For the same reason, we summarize the salient historical points, cite relevant publications, and drive home the "too little too late" theme, albeit without the eloquence of Meinesz (1999).

Ironically, Meinesz and Jean Jaubert published a paper in an aquarist journal in 1977 recommending the use of green algae in the Order Caulerpales as aquarium decorations (Meinesz 1999). In 1980, a cold-resistant clone of C. taxifolia is identified at Stuttgart, Germany, and distributed to facilities in Nancy, Paris, and Monaco. In 1984, a tiny patch of C. taxifolia was found under a window at the Oceanographic Museum at Monaco - the first known introduction and the beginning of a compelling story. So the story unfolds from the very spot where Jacques Ives Costeau, inventor of the self-contained underwater breathing apparatus (SCUBA) and ambassador of the underwater world for generations of people worldwide, built his career. There is plenty of circumstantial evidence that the actions of Monaco Museum employees were the cause of the devastating Mediterranean introduction, albeit unintentionally.

By 1989, a green lawn about a hectare (2.2 acres) in size was growing in front of the Monaco Museum, and for the first time, Meinesz verbally notified Monaco and French authorities of the establishment and spread of the algae. In 1990, new populations were found in Cap Martin and Toulon, 5 and 150 km from Monaco Museum, respectively, and the first letters to French authorities and the first French newspaper articles appeared. In one article, the Monaco Museum directorate clearly minimized the problem. In 1991, the algae spreads at the existing sites, and is found at Saint-Cyprien, 350 km west of Monaco, and fishermen regularly complain of algae fouling their nets. In the press, the Monaco Museum director denies the Museum's responsibility for the introduction and touts its benefits, and IFREMER dismiss the potential impacts and risk of spread of the algae. University scientists from Nice, Marseilles, Pisa, and Trent call for eradication, but by this time, and in retrospect, it was probably already too late.

The period 1992 to 1994 was a continuation of the same - committees were formed, plans were made, research was financed, the First International Workshop was held in January 1994 (Boudouresque et al. 1994), and the Second International Workshop was held in December 1994 (Ribera et al. 1996). However, action was severely lacking, and Caulerpa continued to spread - it was found in Spanish waters around the Balearic Islands, in Italian waters at four sites, and in the Adriatic Sea off the coast of Croatia, over 1,000 km from Monaco. Now with over 1,500 ha infested in 38 sites, the "Barcelona Declaration" is finally issued, in which C. taxifolia is officially declared a major threat to Mediterranean ecosystems.

Two publications appear in the period 1995 to 1996 that epitomize the time-wasting struggle for blame that probably only exacerbated the problem: one in which the Monaco Museum researchers argue for a Red Sea origin for the algae, and another arguing against this claim. A second research program is funded, but while the players waste valuable time laying blame, arguing effects, and doing more research, the algae spreads, with over 3,000 ha infested in 68 sites by late 1996. Danger Caulerpa taxifolia presents a nice map of its distribution in the Mediterranean Sea around this time. The spread of Caulerpa taxifolia in the Mediterranean Sea was modeled by ECOSIM.

1997 brought the Third International Workshop in September, the First Workshop of the French Academy of Sciences, and the first edition of Meinesz' Killer Algae book (in French). The first United States article (Simons 1997; text here) covered the history of the invasion and Meinesz' story, and mentioned his proposed biocontrol efforts.

Not until 1998 was it determined that the Mediterranean strain and aquarium strains of Caulerpa taxifolia were one and the same. More meetings. More workshops. More spread. The U.S. takes notice, and starts political action (see text below on the California invasion).

The state of affairs in the Mediterranean since Meinesz (1999) is troubling indeed. The algae continues to spread, and eradication will surely be impossible (actually, eradication has probably been unfeasible, if not impossible, since about 1991). But if the Mediterranean situation seems bleak, it may be only the beginning - this species continues to be spread by the hand of man, and has reached at least two other continents in recent years... 

The California Invasion: In October 1998, a huge number of important scientists and others working on invasive species sent a letter to Bruce Babbitt, the Secretary of the Interior, forewarning an invasion by C. taxifolia in American waters. In November 1998, a preliminary report outlining the threat and proposing action was generated by the U. S. Fish and Wildlife Service (Keppner et al. 1998). In 1999, the USDA wisely added the aquarium clone to the Federal Noxious Weed List. Also, the ANS Task Force determined that the risk was significant, and requested the formation of an interagency Prevention Program in August 1999 (Keppner and Caplen 1999).

The prescience of the letter and prevention program was realized in the Summer of 2000 when a student of Dr. Susan Williams of Bodega Marine Lab found a small green carpet of C. taxifolia in Agua Hedionda Lagoon, a small cove off the coast of southern California north of San Diego Bay. The news spread quickly (Lazaroff 2000; Fountain 2000), and some minimal infighting reminiscent of the French situation ensued. Eventually, a joint Federal, State, and Industry effort established a control protocol, a local volunteer-based survey project was carried out, and an eradication program was initiated and studied for effectiveness by a multi-agency partnership known as the Southern California Caulerpa Action Team (SCCAT). For more alerts and continually updated information about the California invasion, visit the Internet sites for the RIDNIS Project (Reducing the Introduction and Damage of Nonindigenous Species through Outreach & Education) at UC Davis, and the San Diego Regional Water Quality Control Board; California Sea Grant.

The Australian Invasion: Patches of Caulerpa taxifolia were recently found at three locations in Australia: two small sites (1 ha total) in the Sydney region (Fishermans Bay and Gunnamatta Bay), and one large site (10 ha) in Lake Conjola, south of Jervis Bay in southern New South Wales (Millar 2000). More surveys and eradication attempts are underway. For the most recent information on the Australian invasion, including public meetings, pest alerts, and control measures, perform a search for "Caulerpa taxifolia" on the New South Wales Fisheries web site. The unfolding of scientific and political events should be very interesting to watch.

Clearly, the lags in control and eradication efforts led to the current state of affairs in the Mediterranean. However, a knowledge of the Mediterranean situation led to a heightened awareness, rapid action, and completely different outcomes in California and Australia, at least over the short term. One can only hope these efforts succeed over the long haul, that the Mediterranean invasion did not occur in vain. Although we may not be able to forever keep this species from spreading, the improvement in response efforts is a positive sign that at least we are trying to learn from past mistakes.

 

Biology of a Stranger in Strange Lands:

The introduced C. taxifolia is genetically identical to strains cultured and propagated in western European aquaria since the early 1970’s, and is believed to be a genetic clone of a single plant, exhibiting characteristics and tolerances different from its parent plant. For example, the Mediterranean strain demonstrates a different reproductive strategy, forms dense mats rather than growing in small isolated clumps, reaches much greater heights in terms of growth, and tolerates a wider range of temperatures, surviving between the isotherms of 10-31ºC. 

Like many successful invasion species, the Mediterranean strain of C. taxifolia spreads rapidly, possessing life history features enhancing its ability to spread and take over coastal areas. The Mediterranean strain of C. taxifolia exhibits vegetative or asexual reproduction - sexual reproduction has never been observed, and the gametes are apparently all males (Meinesz 1999). Small cuttings or plants fragments are capable of regenerating whole new plants. In addition, the Mediterranean strain is apparently able to adapt to a wide range of habitat conditions including substrate, light intensity, and water quality. C. taxifolia synthesizes toxic or repellent secondary metabolites as defense strategy against herbivory and epiphytism. These toxins affect local flora and fauna through both direct contact and indirect contact as the toxins are apparently released into the water causing chemical interactions with some species (see impacts section below).

Genetic research on C. taxifolia is advancing in leaps and bounds, mostly out of a need to identify the sources of invasions, but might also provide solutions for elimination and prevention.


Known & Potential Impacts: Caulerpa taxifolia made the list of the 100 worst invasive alien species (Lowe et al. 2000), and for good reason. This invader wins by attrition. At any given site, the seaweed covers all favorable, available substrates, including rock, sand, mud and natural meadows of the marine phanerogams of Posidonia or Cymodocea.

This vigorous, quasi-permanent and thick vegetable coverage colonized at a depth of 5-30 m. but has been sighted by submarine at depths of 100 m. and takes over all substrates, wiping out other algae. It even destroys the Posidonia meadows which protect the coastline, and act as a refuge, habitat, spawning ground and nursery for countless numbers of species in the Mediterranean (if you can read Spanish, visit the Posidonia page on M@re Nostrum).

The algae secretes various toxins, such as caulerpenyne (not toxic to humans) but are toxic for molluscs, sea urchins, herbivorous fish and submarine flora. In one experiment, Boudouresque (Marine Bio.Prof at the Uni Marseilles) found that sea urchins ate their own waste and resorted to pieces of plastic, rather than touching the seaweed.

 


Management:   A number of eradication techniques have been tried in different places. Any practical applications of these methods must be accompanied by the necessary authorization and precautions so that the remedy itself, should it prove effective, does not cause further unforeseen upsets to the ecosystem. For instance, although it may seem prudent to just rip C. taxifolia out by the 'roots,' remember that tiny fragments of this algae, if freed in the process, could establish new populations wherever they settle.

1. Manual uprooting by trained divers can be a solution for small algae patches measuring a few square meters, but is not 100% effective. Usually there is regrowth and the operation has to be repeated. This technique is no longer feasible due to its exorbitant cost. It might have been effective in the Mediterranean in 1991 when only a few hectares were colonized.

2. Physico-chemical elimination procedures were considered and tested in an aquariums and experimental sites: copper electrodes (copper is toxic to plants), cross-ionic dialysis, air suction, dry ice, ultrasound, hot water jets. Workers have tried ripping the seaweed out with vacuum hoses, applying seaweed-killing copper, or heavy doses of salt, but nothing has stopped it from growing. These methods do not meet one or more of the criteria (effectiveness, absence of regrowth after one month, non-dispersal of cutting, absence of secondary effects on other systems). At this stage, the only feasible strategy is not one of total eradication but rather one of slowing down the rate of spread by eradicating small, isolated patches through a combination of various techniques.

3. Biological Methods may well be a solution in the future. A sea slug (Mollusca: Opisthobranchia: Sarcoglossa = Ascoglossa) has been fingered as a potential biological control agent. A lively discussion of these issues can be found on the Sea Slug Forum. Recently, experiments with the slug Lobiger serradifalci turned up unexpected and potentially devastating results: instead of consuming the algae fronds, it cuts the fronds into tiny living pieces, which might disperse, regenerate, and colonize new areas (Zuljevic et al. 2001).

Even if these eradication efforts prove fruitful, it is generally accepted that prevention is the best and most efficient way to deal with this, and many other, exotic invasive species problems.

The continued culturing and use of Caulerpa in aquariums could be a major problem. A number of algae culture sites can be found with a basic search for "Caulerpa" on any Internet search engine. Some sites flagrantly boast the ability to get Caulerpa directly from their back yard (e.g., Seaweed Market). Clearly, this species should be restricted, or at least discouraged, from being sold for aquarium ornamentation in areas outside its native range. This has already been done in France, Spain, and Australia, and more recently in California (California Water Quality Control Board). Control measures proposed by the government of New South Wales, Australia mainly include human behavior-oriented controls on the continued spread of this species, such as boating and fishing net restrictions (NSW Fisheries).

Continued vigilance will be required in all potentially vulnerable locations, and a massive education and outreach effort will be required (e.g., Project Pacific), along with involvement of the public in survey efforts (e.g., Orange County CoastKeeper) if the establishment of this species outside its native range is to be thwarted. This might especially include contacting pet and aquarist industry organizations, recreational diving organizations, commercial and recreational fishing organizations, and various watercraft organizations. Weed alerts should be posted at key points and on relevant web sites (e.g., South Coast Divers). In the end, partnerships between industry and government will be necessary to ensure that this species will not be introduced, or if introduced, will not spread.


Literature Cited:

Boudouresque C. F., A. Meinesz, and V. Gravez, eds. 1994. First International Workshop on Caulerpa taxifolia. GIS Posidonie, Marseille, France.  ISBN 2-905540-19-2

Fountain, H. 2000. Observatory. July 18, 2000. New York Times.

Hunan, P. 199_.  Reef Creatures. (has Caulerpa pictures)

Lowe S. J., M. Browne and S. Boudjelas (2000). 100 of the World's Worst Invasive Alien Species. Invasive Species Specialist Group (ISSG).

Jacobs, W. P. 1994. Caulerpa. Scientific American 271:100-105.

Keppner, S. M. and R. T. Caplen. 1999. A prevention program for the Mediterranean strain of Caulerpa taxifolia. (www.anstaskforce.gov/Caulerpa.htm)

Keppner, S. M., M. T. Weimer, and W. J. Troxel. 1998. Caulerpa taxifolia: A Potential Threat to U. S. Coastal Waters. A preliminary report prapared for the Aquatic Nuisance Species Task Force. Unpublished report.

Lazaroff, C. 2000. Killer algae found off California coast.  Environment News Service. (ens.lycos.com/ens/jul2000/2000L-07-06-06.html)

Lehman, R. L. and J. R. Manhart. (In Press). Unique structure of the chloroplast genome of Caulerpa sertularioides (Chlorophyta) and a comparison of restriction fragment patterns in the genus Caulerpa (Chlorophyta). Journal of Phycology.

Littler, D. and M. Littler. 2001. Caribbean Reef Plants: An Identification Guide to the Reef Plants of the Caribbean, Bahamas, Florida, and Gulf of Mexico. OffShore Graphics, Inc. Washington, D.C.

Littler, D. S., M. Littler, K. E. Bucher, and J. Norris. 1992. Marine Plants of the Caribbean : A Field Guide from Florida to Brazil. Smithsonian Institution Press, Washington, DC.

Meinesz, A. 1999. Killer Algae: The True Tale of a Biological Invasion. University of Chicago Press, Chicago, IL. 360 pp. (read an excerpt) (order the book)

Millar, A. 2000. Caulerpa taxifolia - First report of its introduction to eastern Australia. Sea Slug Forum (www.seaslugforum.net/caultaxi2.htm)

Raloff, J. 1998. Rogue algae. Science News Online. July 4, 1998.

Ribera, M. A., E. Ballesteros, C. F. Boudouresque, A. Gomez, and V. Gravez, eds. 1996. Second International Workshop on Caulerpa taxifolia. Publicacions Universitat Barcelona, Spain. ISBN 84-475-1382-3

Simons, M. 1997. A delicate Pacific seaweed is now a monster of the deep. New York Times August 16, 1997, P. 1, 4. (see text on NJ Fishing site)

Woodfield, R. 2001. Noxious algae found in southern California coastal waters. 

Yip, M. 2001. Essay about Caulerpa taxifolia. Institut fur Kommunikationswissenschaft. (informative, but devoid of references)

Zuljevic, A., T. Thibaut, E. Hind, and A. Meinesz. 2001. Sea slug disperses the invasive Caulerpa taxifolia. J. Marine Biol. Assoc. UK. 8(2):343-344.


The Caulerpa page was last updated on 04/17/2002