Ecological Study on Community of Exotic Invasive Seaweed Caulerpa
prolifera in Suez Canal and its Associated Macro Invertebrates
Ali A-F. A. Gab-Alla
Caulerpa prolifera (Forsskal) Lamouroux, a green
alga, widespread in tropical and subtropical seas is now invading species
to the Suez Canal during last recent years after 2000; it is widely spread,
colonizing its western sandy shore at shallow waters of 1-2 m depth. It
has the potential to supplant native vegetation, thereby altering the
structure and function of the subtidal marine landscape, supplant seagrass
H. stipulacea. According to the present study, based on biometric
parameters, the frequency of occurrence, abundance and density analyses,
the seaweed C. prolifera is more frequent, abundant and dense in
Suez Canal than the seagrass H. stipulacea, which is very rare.
Instead C. prolifera forming extended dense meadows with percentage
cover nearly 100% m–2 at many sites. This mainly happened;
due to the competitive success of C. prolifera which seems to be
related to its big size, high density, rapid growth, high efficiency in
dim light conditions, high tolerance to severe nutrient limitation and
salinity and temperature fluctuations and to the production of toxic secondary
metabolites. The presence of these toxic secondary metabolites explains
why C. prolifera is avoided by many of macro invertebrates as a
habitat or feeding grounds.
The Suez Canal extends 172 km from Port Said in the north to the Suez in the South. About 80 km south of Port said it passes through Lake Timsah, some 5 km long and then after a further 15 km, through the 25 km of the Bitter lakes. The Canal and these lakes comprise the area of this study. These lakes contain nearly 90% of the water in the system and have predominantly sedimentary substrate (Por, 1978) and consequently support most of the fishing grounds. The hydrographic regime in these lakes is stable now with salinity of 43-47 at Bitter Lakes and 43 at Lake Timsah (Gab-Alla et al., 1990) with some freshwater input and agriculture run off which could lower the salinity at some sites near the western shore of both lakes ( Gab-Alla et al., 1990).
Invasive species of the algal genus Caulerpa have garnered much attention
in recent years (Sanchiz et al., 2001; Sanchez-Moyano et al.,
2001) as they have the potential to supplant native vegetation, thereby altering
the structure and function of the subtidal marine landscape. Caulerpa prolifera
(Forsskal) Lamouroux is a green alga, widespread species in tropical and subtropical
seas. It is a relative of the Mediterranean invasives of Caulerpa taxifolia
and Caulerpa racemosa (Meinesz and Hesse, 1991; Meinesz, 1992; Meinesz
et al., 1993a; Vaugelas et al., 1994) and commonly occurring,
native, rhizophytic algal species along the Mediterranean (Taplin et al.,
2005). Suez Canal began to be colonized by this seaweed (Caulerpa prolifera)
as exotic invasive species since few years ago, after 2000 (Personal observation),
where this species was not recorded before in the Suez Canal (El Manawy, 1987,
1992, 2000). But, last years, the progression of C. prolifera has been
very rapid, expanding to cover most sandy substrate of Suez Canal, nowadays.
This species has a record of stress on marine habitats (Sanchez et al.,
2001; Sanchez-Moyano et al., 2001), with a great impact on different
species and communities of algae, seagrasses, marine invertebrates and fishes.
The presence of toxic secondary metabolites explains why C. prolifera
is avoided by other marine biota.
In this study, we conducted a field survey to investigate the distribution of C. prolifera versus the seagrass Halophila stipulacea at different sites along Suez Canal to provide a potential explanation for pattern observed for the C. prolifera along Suez Canal according to marine environmental conditions related to its distribution. Also, to assess the associated diversity and the ecology of different associated macroinvertebrate fauna.
MATERIALS AND METHODS
Sampling was conducted at fourteen sites during April 2004 along the western coast of Suez Canal (Fig. 1).
Pilot survey showed that the seaweed C. prolifera was the most spreading flora on the sandy areas of Suez Canal.
|| The sampling sites along the Suez Canal
At each sampling site, temperature (glass mercury thermometer), salinity (refractometer), water's depth were recorded. Quantitative sampling of the vegetation as well as, semi-quantitative visual observations of the epiphytes and macro-invertebrates of C. prolifera vegetation was carried out.
The abundance of vegetation was quantified by three methods: 1) total biomass in grams dry weight or ash free dry weight per square meter (gdwm2) 2) percentage cover (%m2) and 3) a modified Braun-Blanquet Cover-abundance Scale (Braun-Blanquet, 1965).
Vegetation density and biomass: Samples of seaweed or seagrass were obtained at each site by using 0.25 m2 quadrat. To optimize the sampling process, four randomized samples were taken at each site (Kershow, 1980). Each sample consisted of all plant material with its roots and rhizomes to a depth of 15-20 cm in the substratum. After the quadrat was placed on the sea bottom, a knife was used to cut around its inside edge. This ensured that attached plant material outside the quadrat was not taken in the sample. Each quadrat was placed in a bag (5 mm mesh) and rinsed free of sediment. Macroscopic epiphytes (if present) were carefully scraped from the leaves.
In the laboratory, the plant material was rinsed in 5% phosphoric acid, to digest adhering carbon materials, then placed in an oven at 60°C and dried to a constant weight, then burned at 600°C in muffle ferns for determination of ash-free dry weight.
Braun-blanquet cover-abundance scale: Aach site, a minimum of four 1 m2 (H. stipulacea or C. prolifera) quadrats were arbitrarily laid on the bottom. The seagrass or the seaweed occurring within the quadrats were assigned a cover-abundance scale value: 0.1-solitary, with small cover; 0.5-few, with small cover; 1-numerous, but less than 5% cover; 2-numerous, with 5-25% cover; 3-numerous, with 25-50% cover; 4-numerous, with 50-75% cover; 5-numerous, with more than 75% cover. Frequency of occurrence, abundance and density of the seagrass and seaweed were calculated by the following three formulae:
Frequency = No. of occupied quads/total No. of quads.
Abundance = Sum of Braun-Blanquet scale values/No. of occupied quads.
Density = Sum of Braun-Blanquet scale values/total No. of quads.
Benthic invertebrates: To investigate benthic communities at studied sites, belt transects (1x10 m) was established. The survey technique was done by observing and recording the distribution and the ecological status of different species (absent, rare, common) along transect.
Statistical analysis: Data of biometric parameters of the seaweed C. prolifera (percentage cover and biomass) and seagrass H. stipulacea (percentage cover, shoot number and biomass) at different sites were statistically tested by analysis of variance (One-Way ANOVA). Mean values were considered significant when p<0.05.
Environmental conditions: In the water column of Suez Canal, the salinity ranged from 10 to 44% and temperature from 23 to 26°C at different sites (Table 1). Sites with low salinity have usually access to fresh water input e.g., sites 12 (10%) and 13 (11%), or agriculture run off e.g., sites 5 (26%), 6 (32%) and 14 (37).The bay bottom is mainly sedimentary, with fine sand at uncovered sites or very fine sand at Caulerpa or seagrass sites except the second site which is rocky shore (Table 2). The depth at different sites is ranged from 1 to 2 m. The percentage of total organic carbon was high (6.94; 8.18%) at sites 7 and 11, while it was low (1.14, 1.18%) at sites 6 and 12, respectively.
|| Status, water depth, temperature and salinity of different
sampling sites along Suez Canal
|| Percentage of grain size (mm) and total organic carbon (%
dry weight) of the bottom sediments of different sampling stations at Suez
|*Stations 1, 4, 5, 6, 12, and 13 are sandy without any vegetation
of seaweed or seagrass, **Station 2 is rocky substrate
|| Biometric parameters of seaweed Caulerpa prolifera
and seagrass Halohpila stipulacea at different sampling sites of
Suez Canal site
Vegetation density and biomass: C. prolifera has a wide distribution
at sites 3, 7, 8, 9, 10, 11 and 14 along the Suez Canal. While, it was absent
at sites 1, 2, 4, 5, 6, 12 and 13. The percentage cover (%m2) ranged
from 22% at site 14 to 100% at site 11 (Table 3) with lowest
biomas 87 gm2 (AFDW) and highest biomass of 916 gm2
(AFDW) at both sites, respectively.
||Summary of Braun-Blanquet data on frequency of occurrence,
abundance and density for seaweed Caulerpa prolifera and seagrass
Halophila stipulacea along Suez Canal
At sites 8, 10 and 14 which showed less percentage cover and biomass of the
seaweed where it was newly growing.
Seagrass H. stipulacea was recorded only at sites 10 and 14 in much localized patches with a percentage cover of 23 and 76% in their patches at both sites. The shoot density was higher at site 14, represented by 163±20 shoots m2; than site 10 which represented by 72±17 shoots m2. The total biomass of H. stipulacea at site 14 was 63.43 g m2 (AFDW), while at site 10 was 30.14 g m2 (AFDW).
The difference between percentage cover and biomass for the seaweed C. prolifera at different sites was statistically significant (p<0.05). Also, there was obvious difference between percentage cover, shoot density and biomass of the seagrass H. stipulacea at site 10 and site 14 (p<0.05). The difference may be attributed to the suitable environmental conditions at sites 8, 10 and 14 of low salinity and input of fresh water leading to low biometric data for C. prolifera and H. stipulacea and C. racemosa at these sites.
Braun-blanquet cover-abundance: Braun-Blanquet Cover-abundance (Table 4) showed that the seaweed C. prolifera occurred with the highest frequency, abundance and density both at the sites 7, 9 and 11; while, at other sites 8, 10 and 14, the seaweed was with lowest frequency, abundance and density.
Seagrass H. stipulacea was relatively frequent, dense and abundant at the site 14, than the site 10 (Table 4). The complete absence of seagrass from Lake Timsah and other sites is possibly due to the presence of unstable sediments covering the coast, which is unsuitable for the development of these plants, also, the anaerobic conditions at these sites and the discharge of herbicides and pesticides through Western Lagoon of Lake Timsah or other discharge points at Bitter Lakes.
Other ecological aspects and macroinvertebrates: The seaweed community at the sites 8, 10 and 14 was growing newly and consisted of delicate new blades. Recently grown rhizome apical meristems and central branches were also developing.
The blades of the investigated seaweed species were very clean, nearly free from macro-epiphytes. The microscopic examination showed very clean leaves in almost cases.
Invertebrate fauna of the seaweed community was less diverse than seagrass and sandy sites (Table 5). Thirty four species were recorded at different sampling sites. Only 14 species were recorded at Caulerpa sites, the most common species were mollusks C. ruppelli, Trochus erythreus, crustaceans and represented by the caridean shrimp Alpheus audouini, the crab Eucrate crenata, Trapezia sp. the amphipod Gammarus sp. and the isopod Sphaeroma walkari. Other habitats, seagrass and sandy areas were represented by 23 invertebrate species each. The most common species were the molluscs Brachidontis variabilis, Cerithium erythraeonense, Modiolus auriculatus and M. tribulus, crustaceans Alpheus audouini, Gammarus sp. L. signata and Sphaeroma walkari and polychaetes Nereis persica, N. willeyi and echinoderm Ophicoma scolopendrina at seagrass at sites 10 and 14. While at sandy areas, the most common species were mollusks Bulla ampulla, Gafrarium pectinatum Murex tribulus, Venerupis pullastra and Tapes decussata, crustaceans Metapenaeus stebbingi and the crab Portunus pelagicus, polychaetes Branchiosyllis uncinigera, Glycinde bonhourei, Nereis persica, Phllodoce sp. and Syllis exilis and echinoderms Astropecten polyacanthus, Ophiactis savigyni and Ophicoma scolopendrina.
||A list of invertebrate species of seaweed Caulerpa prolifera,
seagrass community and sandy subtidal sites of Suez Canal during the present
|(-) Absent; (+) Rare, <1 up to 3 individuals 10 m-2;
(++) Common = 4 individuals 10 m-2;
Seagrass Halophila stipulacea known to occur in shallow waters along the western coasts of the Suez Canal (Fox, 1926; Lipkin, 1972), sometimes, this seagrass is intermingled to some extent with seagrass H. uninervis and seaweed Caulerpa racemosa (Lipkin, 1972). According to the present study, based on biometric parameters, the frequency of occurrence, abundance and density analyses, H. stipulacea is very rare seagrass now along the western coast of Suez Canal, which was recorded at two sites only from 14 sites investigated, while the other species H. uninervis was not recorded at all.
Now, H. stipulacea is replaced by the most frequent, dense competitive seaweed C. prolifera, which recorded at 50% of investigated sites, forming expanding dense meadows with percentage cover nearly 100% at many sites, especially at Bitter lakes. Last recent years after 2000, this species invaded and competed with the seagrass of Suez Canal, supplant them. This mainly happened; due to the competitive success of C. prolifera which seems to be related to some specific characters to this seaweed which are its big size, the high density of its populations (Meinesz and Hesse, 1991), its rapid growth (Komatsu et al., 1994), its high efficiency in dim light conditions (Gacia et al., 1994), its tolerance to the lack of severe nutrient limitation (Delgado et al., 1994), its wide temperature tolerance (Gacia et al., 1994) and its production of toxic secondary metabolites (Guerriero et al., 1992, 1993). The presence of these toxic secondary metabolites explains why C. prolifera is avoided by many of macro invertebrates. Many authors (Lemee et al., 1993; Dini et al., 1994, Fancour et al., 1994; Harmielin-Vivien et al., 1994; Pesandro et al., 1994) considered the discontinuity in the trophic chain from microbes to metazoans and ichtyofauna must exist in ecosystems dominated by C. prolifera.
The structure and flux of organic matter on the new ecosystem dominated by C. prolifera could be probably different to other Suez Canal infralittoral ecosystems. Its plant biomass is not very high conversely to its appearance and percentage cover. Productivity of C. prolifera is probably low. Studies (Romero et al., 1992; Pergent et al., 1994) confirm that Caulerpa being siphonalean algae, part of the new blades and stolon growth may be sustained by organic matter translocation from the senescent to the young, actively growing parts and it is not attributable to new growth. C. prolifera meadows do not act as a carbon sink, conversely to seagrass beds as confirmed by studies on Posidonia oceanica beds in Mediterranean (Romero et al., 1992; Pergent et al., 1994) according to a hypothesis would be that a great part of the produced organic matter is transferred to the water column as dissolved organic carbon. Thus, benthic production of Caulerpa beds would be exported to the pelagic system, conversely to what happen in seagrass meadows, where the transfer is from the pelagic to the benthos.
It was very clear during field investigation that macro-invertebrates community of Caulerpa was obviously low in biodiversity than seagrass and sandy habitat. This is due to its toxicity, which prevents grazing for some species (Guerriero et al., 1992, 1993) or to be a habitat for other biota (Lemee et al., 1993; Dini et al., 1994, Ferrer et al., 1994; Gianotti et al., 1994; Merino et al., 1994; Pesandro, et al., 1994; Talpin et al., 2005).
Sediments of the investigated sites were sandy ranging from very fine sand at Caulerpa sites to fine at sandy sites. Also, water was clearer at Caulerpa beds. C. prolifera have a great sediment retention capacity, favoring stabilization and organic enrichment of the environment (Walker and McComb, 1992). Due to this, plant density may affect the granulometric composition, shifting it to very fine sand and clay and increasing percentage of organic matter of the sediment, through slow down of water movements by seaweed blades.
The manifestation of a negative interaction of C. prolifera on Halophila stipulacea is consistent with other studies done using other species of seagrass (Talpin et al., 2005) and/or other members of the Caulerpa genus. The bulk of this prior work comes from the Mediterranean where exotic species of Caulerpa have been invading native seagrass beds (e.g., de Villele and Verlaque, 1995; Meinesz et al., 1993b; Boudouresque and Verlaque, 2002; Ceccherelli et al., 2002; Belsher et al., 2003). Also, Talpin et al. (2005). C. prolifera is an invasive species in Suez Canal, its interaction is similar to those observed in Mediterranean. In both Suez Canal and Mediterranean, interactions with Caulerpa sp. Resulted in a decrease in seagrass abundance under a variety of situations. In addition, anthropogenic alterations to coastal systems of Suez Canal may alter the outcome of these interactions.
In many conventions, signed by many countries on the environment and biological diversity. The issues regarding the exotic invasive organisms are taken into consideration. All countries ratifying the international conventions take responsibilities for controlling and monitoring the expansion of these species. Briefly speaking, Our goals in a combat against this invasive species is to monitor the spreading of the plant; forecasting the probable places that the species can colonize and to control already established colonies and to slow down development and spreading of the plant. Consequently, a current project in Suez Canal should be started by Ministry of Environment in order to protect biological diversity in our seas and to determine the present status of C. prolifera species along coasts as well as to plan action to undertake.
Belsher, T., M. Lunven, E. LeGall, X. Caisey, O. Dugornay and C. Mingant, 2003. Observations conserning the expansion of Caulerpa taxifolia and Caulerpa racemosa in Rade d'Hyeres and Rade of Toulon (France). Oceanol. Acta, 26: 161-166.
Direct Link |
Boudouresque, C.F. and M. Verlaque, 2002. Biological pollution in the Mediterranean Sea: Invasive versus introduced macrophjytes. Mar. Pollut. Bull., 44: 32-38.
Direct Link |
Braun-Blanquet, J., 1965. Plant Sociology: The Study of Plant Communities. Hafner Publ. Comp., New York.
Ceccherelli, G., L. Piazzi and D. Balata, 2002. Spreed of introduced Caulerpa species in macroalgal habitats. J. Exp. Mar. Biol. Ecol., 280: 1-11.
Direct Link |
De-Villele, X. and M. Verlaque, 1995. Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the North West Mediterranean. Bot. Mar., 38: 79-87.
Direct Link |
Delgado, O., C. Rodriguez-Prieto, E. Gacia and E. Ballesteros, 1994. Nutrient-limited productivity of Caulerpa prolifera agardh, an allian weaweed invading the North-Western Mediterranean: Preliminary results. Proceedings of the 1st International Workshop on Caulepa prolifera GIS Posidonie, (CPGISP'94), Marseille, pp: 295-299.
Dini, F., G. Rosati, F. Erra, F. Verni and F. Pietra, 1994. The environmental toxicity of secondary metabolites product by the mediterranean adapted seaweed Caulerpa prolifera. Using marine ciliates protests as a model. Proceedings of the 1st International Workshop on Caulepa prolifera, GIS Posidonie, (CGISP'94), Marseille, pp: 290-294.
El-Manawy, I. and M.A. Shafik, 2000. Ecological and morphological studies on Genus Caulerpa from Egyptian Red Sea coasts. Egypt. J. Phycol., 1: 71-86.
El-Manawy, I., 1987. Ecological studies on the seaweeds of the Suez Canal. M.Sc. Thesis. Suez Canal University, Ismailia, Egypt, pp: 166.
El-Manawy, I., 1992. Ecological studies on the benthic flora of the Bitter Lake (Suez Canal). Ph.D. Thesis. Suez Canal University, Ismailia, Egypt, pp: 155.
Fancour, P., M. Harmelin-Vivien, J.G. Harmelin and J. Duclec, 1994. Evolution des peuplementes des poisons, entre 1992 et 1993, dans les zones colonisees par Caulerpa prolifera a menton. Proceedings of the 1st International Workshop on Caulepa prolifera, GIS Posidonie, (CPGISP'94), Marseille, pp: 309-313.
Ferrer, E., M.A. Ribera and G. Garreta, 1994. Effet de la diffusion des toxins de Caulerpa prolifera. Agardh sur la productivite dauters macroalgues. Proceedings of the 1st International Workshop on C. prolifera. GIS Posidonie, (CPGISP'94), Marseille, pp: 223-227.
Fox, H.M., 1926. 1-General part. Zoological results of Cambridge expedition to the Suez Canal, 1924. Trans. Zool. Soc. Lond., 22: 1-64.
Gab-Alla, A.A.F.A., R.G. Hartnoll, A.F. Ghobashy and S.Z. Mohammed, 1990. Biology of penaeid prawns in the Suez Canal lakes. Mar. Biol., 107: 417-426.
CrossRef | Direct Link |
Gacia, E., C. Rodriguez-Prieto, O. Delgado and E. Ballesteros, 1994. Seasonal variation in the productivity of Caulerpa prolifera in relation to light and temperature: Preliminary results. Proceedings of the 1st International Workshop on C. prolifera, GIS Posidonie, (GISP'94), Marseille, pp: 309-313.
Gianotti, A., E. Ghelardi and S. Senesi, 1994. Characterization of seawater bacterial green seaweed C. prolifera. Proceedings of the 1st International Workshop on C. prolifera. GIS Posidonie, (GISP'94), Marseille, pp: 197-201.
Guerriero, A., A. Meines, M. D'amberosio and F. Pietra 1992. Isolation of toxic and potentially toxic sesqui-and monoterpenes from tropical green seaweed Caulerpa prolifera which has invaded the region of Cap Martin and Monaco. Helv. Chem. Acta, 75: 689-695.
Direct Link |
Guerriero, A., F. Marchetti, M. D'amberosio, S. Senesi, F. Dini and F. Pietra, 1993. New ectoxicologically and biogenetically relevant terpens of the tropical green seaweed Caulerpa prolifera which is invading the Mediterranean. Helv. Chem. Acta, 76: 855-864.
Direct Link |
Harmelin-Vivien, M., J.C. Harmelin and P. Francour, 1994. Influencede quelques facteurs du milieu sur le peuplement de poisons des prairies a C. prolifera a Monaco. Proceedings of the 1st International Workshop on C. prolifera, GIS Posidonie, (GISP'94), Marseille, pp: 155-159.
Kershaw, K.A., 1980. Quantitative and Dynamic Plant Ecology. Edward Arnold, London.
Komatsu, T., A. Meinesz and D. Buckles, 1994. Donnees preliminaries surl-l'influence de la temperature et de la lumiere sur le development et la croissance de Caulerpa prolifera en culture. Proceedings of the 1st International Workshop on C. prolifera. GIS Posidonie, (GISP'94), Marseille, pp: 279-283.
Lemee, R., D. Pesando, M. Durand-Clement, A. Dubreuil, A. Meinesz, A. Gueffiero and F. Pietra, 1993. Preliminary survey on the toxicity of the green alga Caulerpa prolifera introduced into the Western Mediterranean Sea. J. Applied Phycol., 5: 485-493.
Direct Link |
Lipkin, Y., 1972. Marine algal and seagrass flora of Suez Canal (the significance of this flora to the understanding of the recent migration through the canal). Israel J. Zool., 2193: 405-446.
Meinesz, A. and B. Hesse, 1991. Introduction et invasion de I'algue tropicale Caulerpa prolifera en Mediterranee Occidentale. Oceanol. Acta, 14: 414-426.
Meinesz, A., 1992. Modes de dissemination de I'algue Caulerpa prolifera en Mediterranee. Comm. Int. Exp. Sci. Med., Rapp. Comm. Int. Mer Medit., pp: 33-44.
Meinesz, A., J. De-Vaugelas and B. Hesse, 1993. Spread of the introduced tropical green alga C. taxifolia in northern Mediterranean waters. J. Applied Phycol., 5: 141-147.
Direct Link |
Meinesz, A., J. De-Vaugelas, L. Benichou, G. Caye and J.M. Cottalorda et al., 1993. Suivi de l'invasion de I'algue tropicale Caulerpa prolifera en Mediterranee. Situation au 31 Decembre 1992. Lab. Env. Mar. Litt. Univ. Nice, Gis Posidonic, Marseille. pp: 80.
Merino, V., E. Clavero and M. Hernadez-Marine, 1994. The effect of Caulerpa prolifera Agardh on the growth of marine microalgae. Proceedings of the 1st International Workshop on Caulepa prolifera, GIS Posidonie, (GISP'94), Marseille, pp: 213-217.
Pergent, G., J. Romero, C. Pergent-Martini, M.A. Mateo and C.F. Boudouresque, 1994. Primary production, stocks and fluxes in the Mediterranean Seagrass Posidonia oceanica. Mar. Ecol. Progr. Ser., 106: 139-146.
Direct Link |
Pesandro, D., R. Lemde, M. Durand-Clement, A. Dubreuil and P. Amade et al., 1994. Resques lies a la toxicite de C. prolifera. Agardh. Proceedings of the 1st International Workshop on C. prolifera, GIS Posidonie, (GISP'94), Marseille, pp: 265-269.
Por, F.D., 1978. Ecological Studies 23. Lessepsian Migration. Springer Verlag, Berlin Heidelberg.
Romero, J., G. Pergent, C. Pergent-Martini, M.A. Mateo and C. Regnier, 1992. The detritic compartment in a Posidonia oceanica meadow: Litter features, decomposition rates and mineral stocks. Mar. Ecol., 13: 69-83.
Direct Link |
Sanchez-Moyano, J.M., F.J. Estacio, E.M. Garcia-Adiego and J.C.Garcia-Gomez, 2001. Effect of the vegetative cycle of Caulerpa prolifera on the spatio-temporal variation of invertebrate macrofauna. Aquat. Bot., 70: 163-174.
Direct Link |
Sanchiz, C., A.M. Garcia-Carrascosa and A. Pastor, 2001. Relationships between sediment physico-chemical characteristics and Heavy metal bioaccumulation in Mediterranean soft-bottom macrophytes. Aquat. Bot., 69: 63-73.
Direct Link |
Talpin, K.A., E.A. Irlandi and R. Raves, 2005. Interference between the macroalga Caulerpa prolifera and seagrass Halodule wrightii. Aquat. Bot., 83: 175-186.
Direct Link |
Vaugelas, J.D.E., J. Blachier, J.M. Cottalorda, T. Komatsu and R. Lemee et al., 1994. Premiers resultates de la campagne de sensibilisation europeenne sur l'invasion de Caulerpa prolifera sur les cotes francaises de la Mediterranee a la fin de 1993. Proceedings of the 1st International Workshop on C. prolifera. GIS Posidonie, (GISP'94), Marseille, pp: 265-269.
Walker, D.I. and A.J. McComb, 1992. Seagrasses degradation in Australian coastal waters. Mar. Pollut. Bull., 25: 191-195.
Direct Link |