Ulva reticulata (ribbon sea lettuce)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Plant Type
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Biology and Ecology
- Latitude/Altitude Ranges
- Water Tolerances
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Impact Summary
- Economic Impact
- Environmental Impact
- Social Impact
- Risk and Impact Factors
- Uses List
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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IdentityTop of page
Preferred Scientific Name
- Ulva reticulata Forsskal, 1775
Preferred Common Name
- ribbon sea lettuce
Other Scientific Names
- Phycoseris reticulata Kützing
International Common Names
- English: sea lettuce
Local Common Names
- Philippines: lumot
Summary of InvasivenessTop of page
U. reticulata normally grows attached to rocky substrates but mature thalli easily detach and become free living vegetative algae. Massive growth or ‘green tides’ of the free-living forms is a result of high nutrient influx. However, invasiveness is localized when growth penetrates coral reefs and competes with other benthic species.
The green tide caused by this species in the island of Mactan (Cebu, Philippines), with outbreaks from March to May, has been documented by Largo et al. (2004). The species also has been reported to cause seasonal massive blooms in the Boracay Islands (Aklan, Philippines; Largo, unpublished report submitted to the Department of Science and Technology, Republic of the Philippines). In both Philippine cases, massive growth of this species may have been promoted by eutrophication from untreated sewage.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Plantae
- Phylum: Chlorophyta
- Class: Chlorophyceae
- Order: Ulvales
- Family: Ulvaceae
- Genus: Enteromorpha
- Species: Ulva reticulata
Notes on Taxonomy and NomenclatureTop of page
U. reticulata belongs to the cosmopolitan genus Ulva, one of the first seaweed genera described by Linneaus in 1753, which includes species with foliose and tubular thalli. The genus Ulva is distinguished morphologically from closely related ulvalean Enteromorpha by its flat, two-cell layer (distromatic) morphology, in contrast to the latter with its tubular, single-cell (monostromatic) structure. However, Ulva and Enteromorpha are, as first thought by Linnaeus, not distinct genera after all, based on ITS nrDNA analysis (Hayden et al., 2003).
Ulva contains more than 140 species but only about 50 are currently recognized, including U.reticulata. First described by Forsskal in 1775, based on collection from Gomphodae’ (Al-Qunfudhah), in the Saudi Arabian part of the Red Sea, U.reticulata has not undergone any major taxonomic revision except for the synonym Phycoserisreticulata given to the same species by Kützing. With molecular techniques becoming a more common approach in algal taxonomy, the species has been widely used for comparative alignment with other species (Hiraoka et al., 2003; Prasad et al., 2009; Flagella et al., 2010). U. reticulata seems to be a well-defined species both morphologically and molecularly.
DescriptionTop of page
The genus Ulva is classified under order Ulvales, class Ulvophyceae, which includes morphologically variable forms that have a life history involving alternation of isomorphic generations consisting of haploid gametophyte and diploid sporophyte. Ulva spp. can grow abnormally in bacteria-free culture but develop normal morphology in the presence of their bacterial floras (Provasoli and Pintner, 1980; Nakanishi et al., 1996).
Mature thalli have irregular shapes, light to dark green in colour, forming masses of perforated blades from a few centimeters in size to about a meter across. Juveniles usually attached with a small discoid holdfast, becoming detached into free-living individuals that could be entangled with other seaweeds, seagrasses, rocks or corals. Cross section of blades will show the distromatic blade consisting of cells which are squarish, rectangular to polygonal in shape, uninucleate, containing a single parietal chloroplast with one to several pyrenoids.
U. reticulata has reproduction occurring in small patches in the middle of blades which are two cells thick. During or after spore release, these patches fall out of the blade leaving a small hole. These holes become larger to form the characteristic pattern of holes in the blades.
Plant TypeTop of page Annual
DistributionTop of page
Algaebase gives the centre of distribution for U. reticulata as the Indo-west Pacific region. It is found in southeast Asia (Indonesia, Malaysia, the Philippines, Singapore, and Vietnam), eastern Indian Ocean (Andaman and Nicobar Islands), southwest Asia (Bahrain, India, Kuwait, Pakistan, Persian Gulf, Saudi Arabia, Sri Lanka), western Indian Ocean (Kenya, Tanzania, Madagascar islands, Somalia, and Mauritius), northern Indian Ocean (southern Red Sea, Eritea, Egypt, eastern Saudi Arabia), east Asia (southern Japan and Korea), mid-Pacific Ocean (Hawaiian Islands), and in Oceania (Papua New Guinea, north Australia).
The occurrence of U. reticulata in the subtropical waters of Japan (Yamada, 1934), Hong Kong (Harder et al., 2004) and Taiwan (Lewis and Norris, 1987; Tsai et al., 2004), which are influenced by the warm Kuroshio Current, makes these areas its northern geographical boundaries. Its eastern Pacific limit could be Chile (Etcheverry, 1960), although it is not recorded in a more recent study by Ramirez (2010) in the same country. It is therefore possible that the species did not survive after being introduced to Chile. Its occurrence in New Zealand (Naylor, 1954; Batham, 1956) and the Antarctic Ocean (Papenfuss, 1964) remains suspect and highly unlikely considering the low temperature in these areas. Therefore, the more established southern limit of U. reticulata will be north Australia (north of Cape Tribulation and in Thursday Island, both in Queensland; http://biocache.ala.org.au) and Papua New Guinea (Coppejans et al., 2001; Lewis,1987).
Westward, U. reticulata was reported in the Venezuelan waters of the Atlantic Ocean. With the assumption that the Indo-west Pacific region is its centre of distribution, it must have crossed the Atlantic via the Mediterranean Seas, before it reached the Venezuelan waters and become one of the exotic species in that area (Perez et al., 2007; Ardito and Garcia, 2009), including as an associated species with mangrove Rhizophora mangle (Barrios et al., 2004). Eastward, the species was reported to have also occurred in Chile as early as the 1950s (Etcheverry, 1960). Assuming that a Pacific stock successfully crossed and reached the eastern Pacific, through Hawaii, there is, however, a disjunct in its distribution as there is so far no report of this species from any of the South Pacific island countries.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Djibouti||Present||Silva et al. (1996)|
|Eritrea||Present||Ateweberhan and Prud'homme Reine (2005); Lipkin and Silva (2002)||Assab Bay, Eddi, Mandola Island|
|Kenya||Present||Native||Papenfuss (1964); Silva et al. (1996); Bolton et al. (2007); Nyunja et al. (2009); Sjöö and Mörk (2009)|
|Madagascar||Present||Silva et al. (1996)|
|Mauritius||Present, Widespread||Native||Jagtap (1993); Ballesteros (1994); Silva et al. (1996)||Present in 5 out of 10 stations (south, east, north and west coast) of Mauritius|
|Somalia||Present||Silva et al. (1996)|
|Tanzania||Present||Native||Silva et al. (1996); Lugendo et al. (2001); Semesi et al. (2001); Msuya et al. (2006)|
|-Zanzibar Island||Present||Msuya et al. (2006)|
|Togo||Present||Msuya et al. (2006)|
|Tunisia||Present||Msuya et al. (2006)|
|Uganda||Present||Msuya et al. (2006)|
|Western Sahara||Present||Msuya et al. (2006)|
|Zambia||Present||Msuya et al. (2006)|
|China||Present||CABI (Undated)||Present based on regional distribution.|
|Hong Kong||Present||Introduced||Harder et al. (2004)||Collected from Port Shelter (22° 19’ N, 114° 16’ W) as source of antifoulants; peak growth from Feb to June|
|India||Present||Silva et al. (1996)|
|-Andaman and Nicobar Islands||Present, Widespread||Native||Jagtap (1992)||Car, Nicobar (within Nicobar Islands)|
|-Goa||Present||Native||Dhargalkar (1986)||Chapora Bay|
|-Kerala||Present||Native||Varghese et al. (2010)||Bakel, Kasaragod|
|-Maharashtra||Present||Native||Umashankar Prasad et al. (2009)||Present in Dahanu, Mumbai, Shriwardhan, Murud, Ratnagiri, Malvan|
|-Tamil Nadu||Present||Native||Raghavendra Rao et al. (2004); Vijayaraghavan et al. (2004); Manivannan et al. (2009); Shanmugan and Palpandi (2010); Felix and Pradeepa (2011)|
|Indonesia||Present||Native||Puspawati et al. (2011)||Segara Beach|
|-Irian Jaya||Present||Native||Takeshi et al. (2005)||Seribu Is.|
|-Java||Present, Widespread||Native||Coppejans and Prud'homme van Reine (1992)||Northeast coast of Sumba, east of Melolo; east of Komodo Selat Linta|
|-Maluku Islands||Present||Native||Gerung et al. (2006)||Ambon Is. (Galala, Latuhalat, Leahari, Rutong, Hutumuri); highest density (of 2.82 ind/m2) and frequency (0.82) among species in the Islands|
|Iran||Present||Sohrabipour and Rabiei (2007)||Iranian coastlines of the Persian Gulf and Oman Gulf|
|Israel||Present, Widespread||Native||Lipkin and Silva (2002)||Dahlak Archipelago; more common in Southern Red Sea (Al Qunfudhah, Saudi Arabia; Al Mukha, Yemen); reported from only one locality in northern Red Sea (Al Qusayr, Kosseir); never been reported in the northernmost reaches of the Red Sea|
|Japan||Present||CABI (Undated)||Present based on regional distribution.|
|-Kyushu||Present, Localized||Native||Yamada (1934)||Kyushu, in the vicinity of Nawa. Grows abundantly|
|Malaysia||Present||CABI (Undated)||Present based on regional distribution.|
|-Peninsular Malaysia||Present, Widespread||Native||Phang (1998); Ahmad et al. (2011)||Man-made island, Penang bridge|
|Pakistan||Present||Native||Sabina et al. (2005)||Studied only for antileishmanial activity with indication of collecting site in Buleji, Karachi coast|
|Philippines||Present, Widespread||Native||Largo et al. (2004); Taylor (1977)||Mactan (Cebu), Boracay (Aklan)|
|Saudi Arabia||Present, Localized||Native||Aleem (1978)||Obhor, Jeddah|
|Singapore||Present||Native||Chou and Wong (1984)||Pulau Salu reef|
|Sri Lanka||Present||Native||Mageswaran et al. (1985); Coppejans et al. (2009)||Studied as source of boron; collected from Mandaitivu|
|Taiwan||Present||Native||Lewis and Norris (1987); Huang (1990); Tsai et al. (2004)||Nanwan Bay, southern Taiwan Hsiao-Liuchiu Island|
|Thailand||Present||Native||Lewmanomont (1998); Ratana-arporn and Chirapart (2006); Ruangchuay et al. (2007)|
|Vietnam||Present||Native||Nang and Dinh (1998); Abbott et al. (2002); Hong et al. (2007); Hong et al. (2011)|
|United States||Present||CABI (Undated)||Present based on regional distribution.|
|-Hawaii||Present, Widespread||Native||Kenzie (2008); Santelices (1977)||Abundant in Natatorium Reef, Waikiki|
|Australia||Present||CABI (Undated)||Present based on regional distribution.|
|-Queensland||Present||Native||Lewis (1987); Bostock and Holland (2010)||North of Cape Tribulation and in Thursday Island|
|Papua New Guinea||Present, Widespread||Native||Coppejans et al. (2001)||Madang Harbor, North coast of PNG|
|Venezuela||Present||Introduced||Invasive||Perez et al. (2007); Barrios et al. (2004); Ardito and Garcia (2009)||Isla Larga, Bahia de Mochima and Guayacan|
History of Introduction and SpreadTop of page
From the Indo-west Pacific region as its distribution centre, U. reticulata has spread the furthest into Venezuela (South America) in just the last decade or so. So far, this is the only documented Atlantic reach of this species, probably travelling from the Red Sea via the Mediterranean Sea. It is also reported in Chile, probably in the 1950’s, as the only documented eastern Pacific record (Santelices, 1989).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Antarctica||Papenfuss (1964)||Need verification as to its occurence|
|Chile||1950's?||Etcheverry (1960)||To determine origin, need to conduct molecular analysis between Indo-Pacifi, Hawaii and South American strains|
|New Zealand||Batham (1956); Naylor (1954)||Need verification as to its occurence|
|Venezuela||2000||Hitchhiker (pathway cause)||Yes||Barrios et al. (2004); Perez et al. (2007)||Need to conduct molecular analysis between Indo-Pacific and Atlantic Strains.|
Risk of IntroductionTop of page
So far, the only non-Indo-west Pacific countries where U. reticulata is confirmed or reported to be present are Venezuela and Chile. It is highly possible that this species may also establish in neighbouring countries where local conditions of temperature and salinity are within the same range of conditions as the species’ origin. The export of farmed species to other countries, as in the case of the red seaweed Kappaphycusalvarezii, may provide a convenient vehicle for U.reticulata to be also transferred to new destinations where the alga is not known to exist. A list of countries where Kappaphycus has been introduced can be found in Ask et al. (2003).
Countries like the South Pacific islands Fiji, Samoa, Micronesia, Solomon Islands, French Polynesia, and even Brazil, have attempted or established seaweed farming for carrageenan production. The northern part of Brazil is now producing K.alvarezii from the Philippines. The temperature range in these countries approximates that of the Philippines during most times of the year. Unless strict quarantine procedures similar to those established for the south Pacific island countries (Sulu et al., 2003) are implemented for new materials entering these countries, the accidental introduction of U. reticulata as an exotic species into the eastern Pacific, Brazilian waters and elsewhere in the Atlantic is highly possible.
Another possible course for introducing U. reticulata is through the ballast water of ships (as monitored by Flagella et al. (2010) in the harbour of Naples, Italy) plying between the Indo-west Pacific and eastern Pacific side and even the Atlantic Ocean.
HabitatTop of page
U. reticulata, like most Ulva species, typically grows on hard substrates. The spores or zygotes (after fertilization) find suitable substrates for attachment such as rocks, coral rubbles, or even on the back of marine turtles, mollusc shells and carapace of crabs where they can be carried wherever these animals go (based on personal observation, D. Largo). As soon as they are mature, their thalli are easily detached by water movement and become free living/floating fronds, or become loosely intertwined with other vegetation structures such as seagrasses and seaweeds.
Habitat ListTop of page
|Inland saline areas||Present, no further details||Harmful (pest or invasive)|
|Inland saline areas||Present, no further details||Natural|
|Lagoons||Present, no further details||Harmful (pest or invasive)|
|Lagoons||Present, no further details||Natural|
|Terrestrial – Managed||Disturbed areas||Present, no further details||Harmful (pest or invasive)|
|Coastal areas||Present, no further details||Harmful (pest or invasive)|
|Coastal areas||Present, no further details||Natural|
|Mangroves||Present, no further details||Harmful (pest or invasive)|
|Mangroves||Present, no further details||Natural|
|Mud flats||Present, no further details||Harmful (pest or invasive)|
|Mud flats||Present, no further details||Natural|
|Intertidal zone||Present, no further details||Harmful (pest or invasive)|
|Intertidal zone||Present, no further details||Natural|
|Inshore marine||Present, no further details||Harmful (pest or invasive)|
|Inshore marine||Present, no further details||Natural|
|Coral reefs||Principal habitat||Harmful (pest or invasive)|
|Coral reefs||Principal habitat||Natural|
|Benthic zone||Present, no further details||Harmful (pest or invasive)|
|Benthic zone||Present, no further details||Natural|
Hosts/Species AffectedTop of page
Ulva species in general quickly respond to an increase in nutrient concentration (eutrophication) from anthropogenic sources, increasing their biomass to bloom proportion (Morand and Merceron, 2005). In such events their large biomass competes for space with other bottom-dwelling organisms, by overcrowding and shading thus limiting other species’ mobility to feed and to find mates, in the case of animals, or the ability to photosynthesize, in the case of plants. In an experimental study by Bolam et al. (2000), wherein an ulvalean species (Enteromorpha intestinalis) was artificially implanted in a moderately exposed intertidal sand flat, it caused marked changes in the macrobenthos, together with significant changes in all the measured sediment variables. Some benthos such as the polychaete Capitella capitata increased in density after weed treatment while other species decreased in number.
In another experiment by Cardoso et al. (2004), comparing between eutrophic and undisturbed areas of the seagrass bed, there was a marked difference in the eutrophic area in terms of abundance of species. Decomposed macroalgal mats of Ulva and other green algae cause the underlying sediments to become anoxic with the accumulation of toxic hydrogen sulphide. This in turn causes a general decline in species richness and an increase in opportunists (Bolam et al., 2000, and authors cited therein). The resulting changes may have direct effects on the numbers of birds and fish that these areas are able to support.
Ulva spp. can cover a wide area of coral reefs, limiting growth of corals and their associated benthic species. They can also cover patches of seagrass beds and their soft bottom communities (e.g. Tsai et al., 2004). This could potentially affect biodiversity in certain areas where nutrient levels are high, which can lead to the alga exceeding its normal growth pattern.
Biology and EcologyTop of page
The sporophyte (spore-producing) generation of U. reticulata produces containers called sporangia which release haploid, quadriflagellated zoospores through meiosis at the middle portion of a mature thallus. When released, the zoospores leave the reticulated/perforated thallus typical of U. reticulata. The released spores directly germinate, first, into a filamentous germling, and then into foliose gametophytes. Gametophytes in turn produce another container called gametangia in the mature thallus which releases haploid, biflagellated gametes through mitosis. Gametes are isomorphic (isogametes) hence there is no distinct male or female; rather they pair to form quadriflagellated zygotes at fertilization, developing into a filamentous germling, then into a perforated, foliose thallus. Unmated gametes are typically capable of functioning as asexual reproductive cells, attaching to substrates and growing into new (haploid) multicellular gametophytes (Graham and Wilcox, 2000).
Physiology and Phenology
By possessing an alternation of sporophytic and gametophytic generations, Ulva has certain advantages of shifting strategies for survival. How these two isomorphic generations differ between each other is not clear in these algae in general. However, a heteromorphic alternation of generations in algae, where the sporophyte is morphologically diminutive and the gametophyte assumes a macroscopic size, as in the case of advanced brown algae, is an adaptation for survival against seasonal changes in temperature and all other factors, especially in regions with clear climatic shifts (Graham and Wilcox, 2000).
Like most Ulva species, U. reticulata possesses antifouling (Harder et al., 2004), inhibitory (Harder and Qian, 2000), and antimicrobial properties (Vairappan and Suzuki, 2000; Karthikaidevi et al., 2009; Kolanjinathan and Stella, 2011) which are probably strategies that enable the alga to survive competition.
U. reticulata does not have any specific intimate macrofloral or macrofaunal association it can be identified with. It does, however, harbour bacteria that may have a significant influence on its growth and development such as those documented for related species of Ulva, (U. pertusa, U. (=Enteromorpha) intestinalis), where the alga develops normal thallus morphology only in the presence of bacterial associates and not when they are absent in an axenic culture (Provasoli and Pintner, 1980; Nakanishi et al., 1996; Marshall et al., 2006).
U. reticulata is an established tropical species that thrives well in clear, shallow waters. It requires warm water temperature of between 25 and 30°C, with growth occurring at a faster rate when inorganic nutrients, especially ammonia and phosphorous, are high due to its efficient nutrient uptake ability (Ahmad et al., 2011). It is likely that U. reticulata after macroalgal blooms alternates in occurrence with other species of algae that are common in eutrophied waters. In Mactan Island (Cebu, Philippines), for instance, the species has been found to be commonly in succession with Enteromorphaintestinales and E. clathrata (Largo et al., 2004).
U. reticulata is conspicuously present during peak growth in protected marine habitats, estuaries, bays and lagoons, where salinity is around 34-35 ppt. The only exception is the Red Sea where salinities as high as 36.5 to 39 ppt (average of 38 ppt; Ateweberhan and Prud’homme van Reine, 2005) seems to be at the extreme end of tolerance for U. reticulata.
Generally, the geographical distribution of U. reticulata is influenced mainly by water temperature. It can be found at quite a wide range of temperatures, from as low as 20 to 30°C to as high as 38°C in the southern part of the Red Sea (Eritrea) during mid-summer (Ateweberhan and Prud’homme van Reine, 2005). In Sri Lanka (Indian Ocean), surface water temperature all around the island is between 26 and 28°C (Coppejans et al., 2009) while that in southeast Asia it could range between 20 and 29°C. Vietnam which is connected to continental Asia, has a surface water temperature in winter of 20-23°C in its northern region and 25-29°C in the southern part (Nang and Dinh, 1998), while in Thailand, Malaysia and the Philippines, temperature is normally about 28-30°C (Trono and Ganzon-Fortes, 1988; Lewmanomont, 1998; Phang, 1998).
In Ryukyu Islands (Okinawa islands) which is probably the northern geographical limit of U. reticulata in the Pacific Ocean, water temperature is influenced by the north branch of the Kuroshio Current, resulting in a warmer range of approx. 20°C in winter to 29°C in summer, with an annual average of 25°C typical of tropical waters (Ohno and Largo, 1998).
In Venezuela, U. reticulata is found near the Caribbean Sea, where the average surface water temperature is 27°C (with a variation of + 3°C) and a salinity of 34.5 – 36.5 ppt (Smith, 1998). In Chile where U.reticulata has been reported by Etcheverry (1960), temperature in latitudes 18°S (Arica) to 27°S (Caldera) is around 18-20°C (Alveal, 1998) which is similar to temperature at its northern limits in the Pacific Ocean (Okinawa Islands).
ClimateTop of page
|Am - Tropical monsoon climate||Preferred||Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))|
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Water TolerancesTop of page
|Parameter||Minimum Value||Maximum Value||Typical Value||Status||Life Stage||Notes|
|Depth (m b.s.l.)||1||3||Optimum||4-10 m tolerated|
|Salinity (part per thousand)||33||34||Optimum||Tolerates 32-38 ppt|
|Water temperature (ºC temperature)||26||30||Optimum||Can occur between 20 and 35°C. Most extreme water temperatures and salinities where U. reticulata has been reported to occur are in the Red Sea (Ateweberhan and Prud'homme van Reine, 2005).|
Notes on Natural EnemiesTop of page
Ulva spp. in the tropics are grazed by sea urchins and rabbitfish or siganids (Siganus spp.) which abound in the coral reefs and seagrasses. In places where Ulva population size in normal, sea urchins and rabbitfish may sometimes consume a sizable area of their natural occurrences. Traditional fishing for rabbitfish in the tropics includes the use of Ulva as bait (Basson et al., 1989).
Means of Movement and DispersalTop of page
Natural Dispersal (Non-Biotic)
Like any alga, U. reticulata is dispersed mainly through water current. Dispersal may be restricted by range of temperature tolerance and geographical boundaries.
Spores or gametes of U. reticulata could be transferred with ballast water discharged from ships moving from the port of origin of the species, where the water is filled in. U. ohnoi and U. fasciata have been identified from ballast water collected in the West Mediterranean harbor of Naples (Italy) (Flagella et al., 2010).
The other possibility of Ulva reticulata being carried by seedlings of Kappaphycusalvarezii introduced to farming areas outside of its origin is very likely. This is happening in the South Pacific Island countries where the unintentional transfer of U. reticulata through K. alvarezii ‘seedlings’ prompted these countries to adopt a common quarantine protocol (Sulu et al., 2003).
While intentional introduction of U. reticulata can be through its use as animal feed, as fish bait (Jaikumar et al. 2011), as fertilizer, and as human food, these are mainly in non-living forms that present very little or harmless consequence to the introduced site. Otherwise, no record exists in the literature documenting this species as having been intentionally transferred for any culture purposes.
Pathway CausesTop of page
|Aquaculture||Can be transferred with introductions of Kappaphycus alvarezii||Yes||Yes||Ask et al., 2003|
|Research||May be brought to other destinations dead or alive for various experimental purposes||Yes||Yes||Paula et al., 1998; Takeshi et al., 2005; Varghese et al., 2010|
Pathway VectorsTop of page
|Aquaculture stock||Yes||Yes||Ask et al., 2003|
|Host and vector organisms||Kappaphycus alvarezii introduction in areas outside its natural occurrence may bring U. reticulata||Yes||Yes||Ask et al., 2003|
|Ship ballast water and sediment||Spores, zygotes, germlings||Yes||Yes||Flagella et al., 2010|
|Ship hull fouling||Attached germlings, spores, zygotes||Yes||Yes||Piola and Conwell, 2010|
Impact SummaryTop of page
|Cultural/amenity||Positive and negative|
|Economic/livelihood||Positive and negative|
|Environment (generally)||Positive and negative|
Economic ImpactTop of page
No specific attribution to U. reticulata was found in the literature regarding any positive economic impact of the seaweed. Algal blooms in general could have detrimental effects on aquaculture. In Macajalar Bay, northern Mindanao Islands, Philippines, Ulva blooms have been reported as having affected the fishing grounds, producing foul odour from rotting seaweeds. Blooms can also impact tourism by making the coast less attractive to tourists and reducing visitor numbers.
Environmental ImpactTop of page
Impact on Habitats
Ulva blooms alter water and sediment quality due to organic decomposition and deposition. Lack of water movement in a bloom area could increase sedimentation rate, resulting in the accumulation of more organic detrital matter leading to anoxic mud and accompanying noxious smell of hydrogen sulfide. This condition renders the area inhospitable for most benthic organisms while favouring those that can tolerate anoxic conditions. Such a case of macroalga bloom affecting the benthic community was observed by Bolam et al. (2000) and Cardoso et al. (2004) in Scotland and Portugal, respectively. In addition, not only are the benthic organisms affected but this may also affect their predators, such as water birds. For example the Yatsu tidal flat in Japan is often visited by migratory birds because of abundant food species, making the area a part of the East Asian-Australasian Shorebird Site Network under the Ramsar Convention (Yabe et al., 2009).
Impact on Biodiversity
So far, there has been no documented case of the effects on biodiversity directly attributed to U. reticulata blooms. But effects of macroalgal assemblages are underscored by a study of Tsai et al. (2004) wherein a shift of coral reefs to algal domination caused a dramatic decline in biodiversity in the reef ecosystem of Nanwan Bay, southern Taiwan. It seems to be also the case in Mactan, Cebu, Philippines where rotting Ulva causes fish and other invertebrates to swim away from waters with very highly anoxic sediments.
Benthic organisms, such as shelled molluscs that thrive in soft sea bottoms, as well as other sedentary invertebrates that feed on detritus, or that filter seawater for food, are likely to be affected when there is little oxygen available, especially in areas when there is limited water circulation. Lack of food and oxygen, therefore, are key factors that could lead to poor biodiversity resulting from an algal bloom (Jonge et al., 2002). Such an environment is also devoid of other trophic components of the food web. On the other hand, detrital matter coming from bloom areas, flushed away by water current may also be transported elsewhere if water circulation is good and therefore the accumulation of an otherwise anoxic organic sediment that could stimulate the above conditions may not be possible.
If the intertidal zone is in an enclosed bay where there is limited water circulation, the entire area could become a biodiversity-poor environment and only organisms adapted to such an environment may survive, such as certain shelled molluscs such as cockles, manila clams (Venerupis philippinarum), and mud snails (Giannotti and McGlathery, 2001). Blooms of Ulva and other macroalgae (Cladophora, Chaetomorpha and Gracilaria) also contribute to the decline of seagrass in nutrient enriched coastal waters (McGlathery, 2001).
Social ImpactTop of page
Perhaps the most important economic and social impact caused by an Ulva bloom is on tourism. Massive growth of U. reticulata in the intertidal zone is detrimental to aesthetic value, and reduces the attractiveness of the coast to visitors who want sandy beaches and clear water. In the Philippines, green tides caused by U. reticulata in the beaches of Boracay Islands (central Philippines) caused tourist arrivals to drop in the early 2000’s. Algal blooms occur in beach resorts with inadequate wastewater treatment. In Mactan Island (Cebu, Philippines) beach operators have to meet the expense of cleaning beachcast materials of U.reticulata during green tide events.
Viscusi (2011) reported on Bloomberg.com that green tides were keeping tourists away from the coast in Brittany, France. However, actual monetary value of this impact on tourism has not been estimated.
In China Ulva ‘green tide’ threatened the sailing event of the 29th Olympics held in Qingdao (Leliaert et al., 2009).In this celebrated case, more than 10,000 people and 1400 boats were mobilized in the fight to clean up a vast algal bloom which appeared shortly before the Olympics. The bloom started in late May and covered 13,000 square kilometers of sea.
Risk and Impact FactorsTop of page Invasiveness
- Invasive in its native range
- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Is a habitat generalist
- Pioneering in disturbed areas
- Benefits from human association (i.e. it is a human commensal)
- Fast growing
- Has high reproductive potential
- Reproduces asexually
- Damaged ecosystem services
- Ecosystem change/ habitat alteration
- Modification of natural benthic communities
- Modification of successional patterns
- Negatively impacts aquaculture/fisheries
- Negatively impacts tourism
- Reduced amenity values
- Reduced native biodiversity
- Transportation disruption
- Negatively impacts animal/plant collections
- Damages animal/plant products
- Antagonistic (micro-organisms)
- Competition - shading
- Competition - smothering
- Competition - strangling
- Competition (unspecified)
- Interaction with other invasive species
- Rapid growth
- Highly likely to be transported internationally accidentally
- Highly likely to be transported internationally deliberately
- Highly likely to be transported internationally illegally
- Difficult to identify/detect as a commodity contaminant
- Difficult/costly to control
UsesTop of page
U. reticulata has a range of potential nutritional and health benefits. It has antihepatotoxic (Raghavendra Rao et al., 2004), anticoagulant (Nisizawa, 2002), analgesic and anti-inflammatory (Hong et al., 2011) effects, which, if exploited, can be a potential source of pharmaceutically important compounds.
The potential benefit of U. reticulata as human food is related to some findings that show high calorific (2828-3725 cal/g) and protein contents based on studies in India (Dhargalkar, 1986) and in Thailand (Ratana-arporn and Chirapart, 2006), respectively. In Japan, Philippines and Indonesia, Ulva is utilized as food in the form of fresh salad or used as ingredients in various food preparations (Kim et al., 2011).
Its high protein content, although it may vary from place to place, means that this species can be used as a functional food for human diets (Hong et al., 2007) or as source of ingredients with high nutritional values (Ratana-arporn and Chirapart, 2006). Single cell detritus (SCD) - a product prepared by decomposing seaweed to a cellular level - has been explored as a potential fish-diet in India in place of unicellular algae (Felix and Pradeepa, 2011) and in Tanzania (Mmochi et al., 2002). It is also being used as feed for rabbitfish in India (Jaikumar et al., 2011).
Harvesting of economically important species of Ulva is a potential activity that will have a social impact in places where it could develop, both in the short- and long-term. This will be dependent, however, on Ulva’s utilization that could lead to the development of an industry where more people participate and stand to benefit from it, as has happened to Tanzania’s farming of Kappaphycus alvarezii adopted from the Philippines. Seaweed farming in Tanzania has resulted in the elevation of the social status of women who were engaged in seaweed farming, normally an activity that is unattractive to men in that country (Mshigeni, 1998). Some species of Ulva, including U. reticulata, which shows promise of utilization for various economic purposes, have this potential. In Japan, Ulva pertusa is harvested and made into dried seaweed powder as an additive in soup, pasta (okonomiyaki), and crispy crackers.
Studies on Ulva, including U. reticulata, have mainly focused on the alga’s ability to absorb excess nutrients and toxic heavy metals as biofilters. Hence in Tanzania, this ability was found to be effective when tested with effluents from tidal fishponds (Msuya and Neori, 2002; Msuya et al., 2006). U. reticulata has also been found to absorb heavy metals such as nickel from synthetic and electroplating industrial solutions (Vijayaraghavan, 2008), zinc (Senthilkumara et al., 2006), and copper (Mamboya et al., 2009). The species has also been found to possess antifouling ability that prevents larval metamorphosis (Bhadury and Wright, 2004).
Uses ListTop of page
Animal feed, fodder, forage
- Fodder/animal feed
- Invertebrate food
- Research model
Human food and beverage
- Emergency (famine) food
- Food additive
- Spices and culinary herbs
- Green manure
- Source of medicine/pharmaceutical
Detection and InspectionTop of page
U. reticulata has the potential of being transported to non-traditional grounds such as in the Atlantic Ocean. It is thought of having spread more recently in the vicinity of Venezuela when Perez et al. (2007) reported its occurrence in that country, probably through accidental introduction from the Red Sea and Indian Ocean via the Mediterranean Sea. Flagella et al. (2010) have attempted to determine the cryptic species of Ulva transported by ballast water of ships and discovered that the species found in the West Mediterranean harbor of Naples, Italy was that of the green tide species U. ohnoi from Japan determined through morphological and molecular approaches.
Accidental introduction of U.reticulata is also possible through the transport of seedlings of farmed seaweeds such as the case of Kappaphycus alvarezii introduced from the Philippines to South Pacific island countries such as Fiji, Tonga and the Solomon Islands. These countries have adopted a common quarantine protocol for this carrageenan-producing red seaweed to prevent exotic species, such as U. reticulata, from entering these isolated island countries (Sulu et al., 2003). The protocol involves the following steps:
- Seaweed propagules should be selected from the young healthy portion of the plant and are free of epiphytic algae
- Minimal quantities of seaweed are to be selected (10-30 kilograms)
- The surface of propagules is free of sediment, macrofauna and flora (ie any entangled drift seaweed)
- The respective quarantine authorities of the importing country are to be notified in advance of transshipment
- Airline and freight agents are to be notified that the shipment contents contain live plant specimens
3. Quarantine facilities
- Seawater supply is pre-treated by filtration through 1 micron sieve
- Seawater is from a source with sufficient nutrient levels (preferably not oceanic water)
- Seawater salinity is at least 28 parts per thousand
- Seawater temperature is stable and in the range of 25-30°C
- Aeration is provided to generate adequate water flow
- The seaweed quarantine unit is isolated from other aquaculture facilities
- Access to the quarantine facility is restricted to authorised personnel only
- All other fauna or flora to be excluded from the quarantine facility
- The seawater outflow is discharged into a sump pit which is out of range of the high tide water mark, at a location that can safely treated with herbicide
- Equipment used in the quarantine facility, such as scrubbing brushes, thermometers, filters and etc, are to be treated with a chlorine dip after use
- Holding tanks are to be drained and scrubbed clean at least twice a week
- Upon arrival the seaweed is to be thoroughly rinsed with fresh seawater before placement into holding tanks
- Seaweed stock are to be held under quarantine for at least two weeks
- Seawater in the holding tanks are to be changed twice per week
- Discharged water is treated with chlorine bleach for 24 hours at 125 ml m-3 dose
- Stress of seaweed stock is to be minimized
- Seaweed are to be visually examined by hand daily for unusual signs
- Seaweed samples are to be sacrificed for a surface microscopic examination using a magnifying glass (5x) for signs of epiphytes
- A daily log to be kept, recording details of treatment, observations and clinical abnormalities
5. Criteria for not releasing imported seaweed into the local environment
- The presence of unexplained flora or fauna associated with the seaweed
- Unexplained unusually high mortality of the seaweed
- Unexplained lesions on the seaweed
- Fungal infections on the seaweed
- Suspicion that non-endemic organisms associated with the seaweed may be introduced into the wild
6. Ecological monitoring
- Prior to out planting a baseline survey of species biodiversity is to be conducted within an area of 0.5 kilometers vicinity from the proposed farm site
- Upon placement the seaweed are to be visually examined for abnormal signs of stress and mortality
- The location of the seaweed is to be surveyed to see if the site is host to any unusual parasites
- An area of 0.5 km vicinity surrounding the seaweed farm is to be monitored over a 1 year period for signs of unusual ecological disturbances or of loose seaweed becoming established in the wild in significant quantities.
Similarities to Other Species/ConditionsTop of page
U. reticulata has perforated thallus and shares this character with four other Ulva species: U. pulchra,U. ohnoi, U. pertusa, and U. fenestrata. U.reticulata differs, however, from these four species in having perforations of mixed diameters, which, according to Coppejans et al. (2004) occur up to the blade margin in contrast to U. pulchra where the perforations are limited to the central part, becoming gradually smaller towards the margin of the perforated part. It also differs from U.fenestrata which has irregular, crenulate perforations, and U. pertusa for its irregularly placed small perforations of different sizes.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Aquatic marine assemblages such as Ulva that could potentially develop into massive biomass or blooms (‘green tides’) have no established control or eradication measures available. Ulva blooms normally die a natural death after nutrient supply, in which it thrives well, is exhausted.
Gaps in Knowledge/Research NeedsTop of page
Blooms of Ulva or ‘green tides’ in general are becoming a common phenomena and are well-documented in highly eutrophied marine waters such as in Brittany, France; Yasu, Japan; and Qingdao, China (Nelson et al., 2003; Yabe et al., 2009; Lellaert et al., 2009). Blooms of U. reticulata have been documented in the Philippines (Largo et al., 2004) but there is an apparent gap in information on blooms caused by this species in many other parts of the world especially in the Indo-west Pacific region where increasing human activities contribute to the degradation of the marine environment. For instance massive U. reticulata blooms seem to be occurring in Singapore as indicated in Wildfactsheets Singapore (http://www.wildsingapore.com/wildfacts/plants/seaweed/chlorophyta/reticulata.htm) but, so far, no literature is available on this topic. This may also be the case for Hong Kong and Malaysia.
ReferencesTop of page
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30/4/12 Original text by:
Danilo Largo, University of San Carlos, Cebu City, Philippines
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