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5. Control Measures, Strategies and Prevention

Various attempts that range from manual uprooting, mechanical means (underwater suction devices), physical control with dry ice, to chemical intervention utilizing household bleach (chlorine) and other chemicals have been tried to halt the spread of this invasive species. Accidentally, Meinesz and his colleagues stumbled over a more promising alternative, involving some selected predators that are able to feed on this particular mutant.

5.a Biocontrol via potential predators of C.taxifolia: Since 1994, the potential use of four ascoglossans (Mollusca: Opisthobranchia) as biological control agents against C.taxifolia (and C.racemosa) have been examined. These mollusks make incisions on all parts of C.taxifolia. They perforate the cell wall with its uniserial radula and sucks up a small portion of the algal contents, leaving light colored markings on the alga. Most ascoglossan sequester secondary metabolites from its diet for their own defense (5.1Paul & Hay, 1986; 5.2Jensen, 1994) thus storing and using caulerpenyne (CYN) from C.taxifolia as a feeding deterrent.

One of the more unspecific predators is Berthelina chloris. Infestation with this snail over a period of a few months creates a booming bivalve population that pierce into the thalli and cause the algae to bleed. Under such pressure and within a few days Caulerpa attains a vitreous appearance that triggers collapse of entire sections. This predator is especially inconspicuous as it is a flat, only 8mm long, with a greenish bivalve shell and thereby well camouflaged among the jumble of thalli. It is usually found in the tropics of the Caribbean sea where predation pressure keeps this Opistobranch in check. Sexually mature animals of B.chloris are usually found in pairs, with regular copulation being observed resulting in 150-300 eggs. After hatching from the gelatinous mass and aided by water currents, they distribute quickly. Juveniles use a sticky mucus for adherence in order to search for their preferred prey any species of the genus Caulerpa (5.1aDebelius & Baensch, 1997).

Oxynoe olivacea is a Mediterranean ascoglossan species, which is scarce in meadows of their usual food (strictly stenophagous on C.prolifera). It has become an adapted feeder on the invading tropical alga C.taxifolia (5.3Thibaut & Meniesz, 2000). It has a partial shell to protect its reproductive organs and digestive glands. Unfortunately, its grazing pattern is correlated with water temperature. Feeding at and above 22C the number of incisions is almost double that observed at 16C (at and above 16C it is still three times that observed at 13C). A single specimen can destroy 0.7-1.6cm/day of the alga's frond (5cm in 3-7 days). Its larval stage is planktothrophic, rendering a possible use as a biological control against C.taxifolia only possible through an artificial enhancement of its populations after cultivation of the veligers and release of juveniles during the winter season.


Fig.5.b Oxynoe olivacea (55kB)

Oxynoe azuropunctata is also a shelled species feeding exclusively on Caulerpales (stenotrophic). This species has a higher feeding rate than either O.olivacea or L.serradifalci; an individual is able to destroy a 3-4.5cm of frond per day (5.3aMeniesz et al., 1996). Unfortunaltey, this species has a brevipelagic larval phase (5.4Clark et al., 1979; 5.5Clark & Jensen, 1981), diluting the recruitment of progenic predation by this species.


Fig.5.c Oxynoe azuropunctata (30kB)

Lobiger serradifalci, another shelled species native to the Mediterranean that naturally feeds on C.prolifera has been observed to settle and feed on C.taxifolia. However, rather than helping to control the spread of this introduced algae it may in fact be hastening its spread. In the Mediterranean, at least, C.taxifolia is reproducing vegetative, by small pieces breaking off and growing into new plants. Unfortunately, L.serradifalci feeds by piercing holes in the cell wall, which weakens the plant and allows pieces to break off, so hastening the spread of the algae. Like O.olivacea and O.azuropunctata it has a planktothrophic larval stage; thus requires artificial enhancement of their populations after cultivation of the veligers and release of juveniles during the winter season.


Fig.5.d Lobiger serradifalci (50kB)

Elysia subornata, a Caribbean species lacking a shell; it feeds only on Caulerpa species by causing incisions with the radula - incised algal thalli rapidly become necrotic and die. The grazing rates correspond to the destruction of 5-6cm/day of frond at 21C; this is 2-11 times higher than those recorded for the Mediterranean ascoglossan species (5.3Thibaut & Meinesz, 2000). Being a tropical species it no longer reproduces at 17C and dies at 15C. Dietary switching is possible on some Mediterranean caulerpales but feeding on other algae and sea grass is unlikely. According to Thibaut et al., (5.62001) only 30% of the E.subornata individuals tested survived when fed a diet made up of C.prolifera exclusively, whereas 100% of individuals tested survived when fed with C.racemosa. Incisions were observed on the Ulvaceae, Enteromorpha compressa and Ulva sp. but the ascoglossans were unable to survive beyond 40 days when exclusively fed on these algae. Only this species is able to ingest and store resistant chloroplasts (kleptoplasty) to allow individuals to survive if food is lacking (5.7Clark et al., 1990); this explains the high degree of stenotrophy of E.subornata towards Caulerpa sp. Another important aspect speaking for E.subornata is its benthic larval development (5.4Clark et al. 1979) allowing it to quickly establish locally dense populations.


Fig.5.e Elysia subornata (50kB)

Unless species are found that are more temperature tolerant, molluscan species that would not survive the winter period in the Mediterranean Sea where temperatures are below 15C, and where feeding and reproduction are only significant above 20C, would require breeding to be performed under laboratory conditions prior to the release window stretching from May to October. With feeding rates of around 5cm of frond per day (E.subornata), still more than 1000 slugs/m2 of C.taxifolia are required to obtain a significant effect on a dense colony with approximately 5000 fronds/m2 (5.8Meniesz et al., 1995). Regardless of planktothrophic larval stage (Oxynoe, Lobiger) or lower thermal viability (Elysia), yearly treatments may be required to maintain a sufficient level of predation on the alga and thus reduce its biomass in the long run (5.9Coquillard et al., 2000).

Already now, biologists have bred thousands of snails, which includes also the tropical variant in laboratories around Nice (France). Teams of scientists are waiting for permission from the French authorities to unleash the snail army. But critics fear that the remedy may introduce new bio-troubles. As recommended by the International Council for the Exploration of the Sea (ICES) and the Food Administration Organization's (FAO) guidelines on biological control or the introduction of species (5.10FAO, 1997; 5.11ICES, 1997) this study on nonnative ascoglossans from the Mediterranean Sea should not be undertaken in open sea. The French Ministry of Environment shares the same attitude. As far as the risks associated with the introduction of non-native species, four of these are identified below:

  • switching to non-target species - unlikely in the case of E.subornata as it is strictly stenotrophic;
  • introduction of pathogens - with species imported from the Caribbean (Elysia) no disease transfer was observed even after one year of quarantine (5.12Pierce et al. 1999);
  • competition with indigenous Mediterranean ascoglossan - theoretically possible, but due to thermal limitations in their reproductive cycle, annual intervention is necessary; thus limiting competition to the time window an eventual trial is running;
  • spreading across the Mediterranean - anti-Lessepsian migration is possible (into the Red Sea and eastern Atlantic).

Meinesz, an advocate of the operation, is convinced that it is safe. Due to its stenotrophic spectrum, dietary switching is not very probable. Furthermore, releasing it in the spring will result only in a temporary invasion as it will die out during the cooler winter months.

5.b Vectors aiding in the spread of C.taxifolia: Although natural (wind & ocean currents) vectors aid in its distribution, the main dispersal agent spreading C.taxifolia across the globe is human-mediated. The aquarium trade in particular, is the most likely source of introduction to the Australia, Oceania, and the Americas. Similar species are sold on the Internet, although far too often the exact species traded is not even known.
As outlined before, dissemination essentially takes place by fragmentation. All sites of infestations far from the introduction area are either close to a harbor, common sites of leisure activity (anchored), or extensively harvested fishing areas (compare fig.5.h, 5.13aCreese et al., 2004). A fact that confirms dispersion of plant fragments attached to boat anchors, fishing gear (including those of commercially operating enterprises) and other equipment. Although unlikely, Caulerpa can be introduced in ballast water or on vessel hulls (NZFMB)5.14. However, even a barely visible piece can regenerate a new plant (fig. 5.f). At 25C, formation of a whole small plant including fronds, stolons and rhizoids, from a cutting as small as a few mm in size (5.34McClary, 2001), occurred within 10 days following a similar pattern of regeneration (5.13Zuljevic & Antolic, 2002). This has rendered all but useless any attempt to eradicate the algae, either by hand or by using the underwater equivalents of plows. The spreading of the alga is facilitated by fishing activity, in particular by bottom trawlers and trammel nets. Fishermen are themselves strongly affected by the spreading, not only because of the decrease in valuable fish, but also because the massive presence of the alga interferes with the use of the gear. In the shallow, bottom trawling is forbidden by EU and Italian laws, but illegal fishing is not uncommon and so a trawler can easily transport algal fragments for several kilometers on a single day (5.15Relini et al., 2000). The same authors go even further by attesting that fishermen harm themselves with these fishing practices in two ways:
i) First, because of the qualitative change in catch composition, commercially important species such as Pagellus erythrinus, Pagrus pagrus, and Solea lascaris decrease and may ultimately disappear when the sea grass is replaced by the green alga.
i) And secondly, because the massive presence of C.taxifolia interferes with fishing activities. In particular, the large quantity of algal fronds affects the deployment and performance of the gear.


Fig.5.f Viability size of floating C.taxifolia fragment (150kB)
 

Fig.5.g Vectors of dispersion (130kB)
 

Fig.5.h Anthropogenic influence (90kB)

5.c Countermeasures - What has been done so far? In Italy, except for a few eradication attempts made at the onset of the invasion, and Tunisia alike, no control strategy has been established (5.16Thibaut & Meinesz, 2002).
Many methods to control this plant have been tested throughout the Mediterranean. Some have tried to tear up the patches of algae but one torn leaf that gets away can generate a whole new outbreak. Divers have used pumps to pull out the plant but it seems to regenerate in the same place at a rate quicker than its original growth rate. Other eradication methods include poison, smothering the algae with a cover that lets in no light, and using underwater welding devices to boil the plant.

Manual uprooting has been executed by trained and motivated divers. It is a solution for small algal patches measuring a few square meters, but even then it is not 100% effective. Sometimes there is re-growth and the operation has to be repeated. In France, regular control of the alga only occurs in the waters of the national park of Port-Cros, where control efforts (manual removal) have been performed annually since 1994. Fifteen tiny isolated colonies have been successfully eradicated (5.17Riera et al, 1994; 5.16Thibaut & Meinesz, 2002). This technique is unfeasible, and tends to be a lost cause from the outset in-depth growth, guaranteed re-growth and exorbitant cost. It could have been effective in 1991 when only a few hectares were colonized.
Physico-chemical elimination procedures were considered and tested either in an aquarium or at an experimental site. These involve certain chemicals, cross-ionic dialysis, vacuum hoses, airlift sediment suckers, suction pumps, dry ice, ultrasound, hot water jets, etc. Although not very efficient with larger patches, these methods can be applied in areas with smaller infestations; e.g. being smaller in extension, annual control measures in Croatia have been implemented by covering isolated colonies with black plastic sheets and removing the alga with a suction pump.


Fig.5.i Development of C.taxifolia species invasion (135kB - 5.35Allendorf & Lundquist, 2003)

  • Smothering with rock salt (sodium chloride, NaCl) has shown partial success in that it kills the C.taxifolia assimilators, but the health of the rhizoids imbedded in the soft sediment has yet to be determined (Millar & Talbot, 2002). Smothering techniques are currently being tested in Australian's West Lakes and may prove to be a suitable management tool for small, isolated patches of the weed. Fresh water is an option when C.taxifolia is encountered in lagoons that can be sealed off. Indeed Australian authorities investigated the possibility whether the affected area could be turned into a fresh water body. The weed dies in fresh water with salinity levels less than 10 parts per thousand. However, trials performed with NaCl in Lake Macquarie showed that a concentration of 50kg/m2 of salt could remove all C.taxifolia fronds for a period of at least 6 months if applied during autumn (fig.5.j, 5.13aCreese et al., 2004).
  • Copper (Cu): is known to be toxic not only to plants, but also to the entire underwater ecosystem. Since the first discovery in 1992, Spanish authorities have been shown to slow down the spread of the alga by using Cu-electrodes, and Cu-salts (ions). Similar efforts were undertaken by French authorities in the Port Cros region since 1994, by applying cloths soaked in copper salts, (5.16Thibaut & Meinesz, 2002).
  • Chlorine: As part of the eradication effort in Agua Hedionda and Huntington Harbour (California-USA) each patch of Caulerpa was covered with a heavy plastic tarpaulin, sealed to the bottom at the edges and fitted with a small port on top that allowed the introduction of liquid chlorine into the mud and water. Chlorine not only killed C.taxifolia but also any other life form present under the tarps. The tarpaulins were left in place to prevent re-growth below ground material and other parts that may not have been fully treated, while preventing loss of herbicide to lagoon waters (5.19Withgott, 2002). Long-term monitoring will be necessary at least for the next five years on a monthly bases to assure complete eradication. Financially, the eradication program at the Californian site (Agua Hedionda Lagoon) in the first two years of the program amounted to approx. U$1.9E6. With the amount of Caulerpa being reduced as work progressed, surveillance has replaced treatment. Therefore another U$800E3/year has been estimated as a minimal requirement to declare the eradication program a success (5.20Merkel & Woodfield, 2003).
  • Algacide have proven to be ineffective.


Fig.5.j NaCl treatment of C.taxifolia (110kB)
 

Fig.5.k Manual Control of C.taxifolia (115kB)
 

Fig.5.l Eradication Success in California (45kB)

Since these methods do not meet one or more of the criteria (effectiveness, absence of re-growth after one month, non-dispersal of cutting, absence of secondary effects on other systems), 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.

Biological Methods may well be the only feasible solution in the future for the Mediterranean. The evaluation of laboratory trials involving Mediterranean specialist grazing exclusively on this species (e.g. Mollusca, Opisthobranchia) showed that indigenous species are inefficient to halt its spread. On the other hand, the tropical counterpart Elysia subornata provides some hope, if a cold-resistant strain of this species could be cultivated (5.16Thibaut & Meinesz, 2002). According to the optimal foraging theory (5.21Hugues, 1980), total eradication of all the Caulerpa spp. by biological control methods is ecologically not possible. Any practical applications of these methods, already being studied, 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 already stressed ecosystem. There are no universal and reliable rules, which can predict whether a biological control organism will be effective (5.22Carlton, 1997).

  1. Genetic research, which is advancing in leaps and bounds, could also provide solutions for local elimination and prevention. Though, one should keep in mind, that once released, a genetically modified organism can never be withdrawn any more!
  2. Mapping C.taxifolia's expansion in the Mediterranean Sea is necessary for a number of reasons (even though, as the extent of colonization increases, mapping precision decreases, 5.23Vaugelas et al., 1999):
    (i) to follow its progression from one year to the next;
    (i) to assess its environmental impact and analyze the regression of out-competed species;
    (i) to estimate C.taxifolia biomass and other related biological data;
    (i) to calibrate computer models to simulate its spread;
    (i) to describe the situation to decision-makers for possible control measures.
    Eventually, the left over smaller patches could be treated with physico-chemical means.

The present state of the Mediterranean invasion is critical and any attempt of eradication of the alga seems useless. A realistic option would be to preserve the biodiversity of selected sanctuaries against the invasion by regular control of new C.taxifolia recruitment. In addition, modeling the spread can help decision makers with their choice of strategy. A selection of simulation models taking into account the biology of C.taxifolia, the seasons, and the spatial characteristics of the Mediterranean are used. Modeling results are accurate over 4-5 year time periods (5.24Aussem & Hill, 1999; 5.25Leme et al., 1997).

5.d. Preventive Methods: Emptying aquarium contents facilitates short distance spread as fragments transported by currents quickly establish newly colonized sites; these are usually harbors, marinas and other places where boats anchor (5.26Ribera & Boudouresque et al 1995). The long distance spread of C.taxifolia can be the result of cleaning anchors and fishing nets as well as ballast water (5.27Meinesz, 1992; 5.28Sant et al., 1996). Hence, being asexually in reproduction, this is important information for resource management and conservation. The uppermost aim though, must be prevention, and this not only involves local authorities but every individual that has to do directly or indirectly with this algae. Thus the guidelines listed herein, should be strictly followed:

  1. Home-Aquaria: As alternatives are available, every owner of a salt-water aquarium should refrain from using this seaweed! Salt-water aquaria and other contents should never be emptied into or near any gutter, storm drain, creek, lagoon, bay, harbor, or the ocean. Aquarium water should be disposed off only in a sink or toilet connected to a wastewater treatment plant. Rock and other solid material from an aquarium should be disposed off in a trash-can. C.taxifolia from an aquarium (and anything it is attached to), should be either dried out for several days under the sun or placed in a plastic bag, put in a freezer for at least 24 hours, and then disposed in a landfill.
  2. Fishing: If any seaweed suspected to be C.taxifolia is found on fishing gear it should be removed, carefully bagged (definitely not thrown back into the sea, since even a small fragment has the potential to regenerate into a new plant), and reported. In order to prevent new infestations and comply with the law, C.taxifolia should not be purchased, sold, or distributed. The legal provisions adopted in France and Catalonia (ban on buying, selling, transporting and storing of C.taxifolia) should be adopted by all countries around the Mediterranean.
  3. Boat: Long-distance spread should be avoided by informing owners of private vessels of the need to check and clean their anchors, trailers, rudders, after mooring in contaminated areas. Like with the above, algal fragments should be removed, carefully bagged (not thrown back into the sea or carried to a new location), dumped into a trash-can and reported to the authorities. Mooring should be prohibited in highly contaminated areas, all national and international regulations and legislation on the introduction of species will have to be adapted.
  4. Water Sports: Sun-lovers, snorkellers, divers, and fishermen should be instructed to inform their local authorities and environmental services each time they sight new patches or populations of C.taxifolia. Such information is essential for the continued monitoring and its spread as well as the adoption of any necessary measures and must also include active involvement of the tourist industry.
  5. Everybody's help is needed! Your help is critical to the success of containing and prevent further infestation by this destructive marine seaweed (refer to contact details in Chapter 6).

5.e. Caulerpa and the Law: Boudouresque & Verlaque (5.292002) recommend that steps be taken at once to slow down the rate of introduction of non-native species. In particular, it seems necessary to implement national legislation, to set up quarantine conditions (aquaculture), to control the flow of ballast waters and the aquarium trade and to ban all species, which prove to be invasive in other parts of the world ("black list" or "dirty list"). Subsequently, it will be necessary to move from a "dirty list" to a "clean list" approach: only the species mentioned on the ''clean list'' will be allowed to be imported. In addition, it is clear that laws should be enforced and that particularly lax practices should be stopped.
At the same time, the spread of an aquarium strain of C.taxifolia in the Mediterranean has led several governments (Australia, France, Spain and USA) to ban its use in the aquarium trade in order to prevent it from escaping to new geographical areas (Jousson et al., 1998).

EU: In a decree dated 4th of March 1993, the French Minister for the Environment and the State U ndersecretary for the Sea banned the offering, the sale, buying, use and dumping into the sea of all or parts of the specimens of the algae Caulerpa taxifolia. Collection and transport of the algae are also subject to a system of authorization granted on presentation of a well-grounded request. The appearance and spread of C.taxifolia are covered at Mediterranean level by the two provisions of article 13 of the Barcelona convention's Protocol on Specially Protected Areas which was adopted in 1996 but has not yet come into force (entitled: The introduction of non-indigenous or genetically modified species).
AUS: The risk of an introduction of non-native C.taxifolia to Australian waters has been recognized by the Australian Quarantine and Inspection Service with the implementation of an import ban of the species in 1996 (5.30Schaffelke et al., 2002). The alga was listed as a Noxious Species by the parliament of New South Wales (NSW) on 1st of October 2000; it cannot be bought, sold, traded, or kept in an aquarium in NSW (5.18Millar & Talbot, 2002).
NZ: The New Zealand government put the aquaria strain of C.taxifolia to the list of species on the Plant Pest Accord for surveillance of retail outlets by Regional Councils. The so-called aquarium strain of C.taxifolia, referring to the Mediterranean invasion, is on the interim species list to trigger a marine pest incursion emergency response in Australia (5.31Schaffelke et al. 2002).
USA: Assembly Bill 1334 (Harman), signed into law by the Californian Governor in September 2001, prohibits the possession, sale, and transport of C.taxifolia throughout that state. This bill also establishes the same restrictions on several other species of the genus Caulerpa that are similar in appearance to C.taxifolia and that are believed to have the ability to become invasive. Furthermore, the importation, interstate sale (including Internet sale), and transport of the Mediterranean strain (i.e., aquarium strain) of C.taxifolia is prohibited under the federal Noxious Weed Act (5.321999) and the federal Plant Protection Act (5.332003).

Please continue with the final PART-6 - Conclusion, Contact details and Bibliography