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Phaeophyta) by Caulerpa Scalpelliformis (Chlorophyta Botanica Marina 48 (2005): 208–217 ᮊ 2005 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2005.033 Changes in shallow phytobenthic assemblages in southeastern Brazil, following the replacement of Sargassum vulgare (Phaeophyta) by Caulerpa scalpelliformis (Chlorophyta) Cristina Falca˜o1,* and Maria Teresa Menezes tered and unpolluted sites are dominated by Sargassum de Sze´ chy2 species (Phaeophyta, Sargassaceae), forming dense and extensive beds (Oliveira Filho and Paula 1979, Sze´ chy 1 Bioconsult Ambiental Ltda, Rua Maria Ama´ lia 658/101, and Paula 2000a, Amado Filho et al. 2003). Sargassum Tijuca, Rio de Janeiro, RJ, Brazil CEP 20511-270, vulgare C. Agardh and S. filipendula C. Agardh are com- e-mail: [email protected] monly encountered in the rocky phytobenthic communi- 2 Universidade Federal do Rio de Janeiro, Centro de ties of Ilha Grande Bay, on the southern coast of the state Cieˆ ncias da Sau´ de, Instituto de Biologia, Rua Conde de of Rio de Janeiro (Falca˜ o et al. 1992, Sze´ chy and Paula Bonfim 74/601, Tijuca, Rio de Janeiro, RJ, Brazil CEP 2000b). 20520-053 Sargassum species are strong competitors for space *Corresponding author and light in rocky shore communities, as in the case of S. muticum (Yendo) Fensholt (Critchley et al. 1990). Paula and Eston (1987) suggested that some Brazilian species, such as S. stenophyllum Mart., possess the same inva- Abstract sive potential as S. muticum, when comparing their adaptive strategies. Later, the competitive superiority of The structure of shallow sublittoral phytobenthic assem- S. stenophyllum in a shallow rocky sublittoral community blages from Ilha Grande Bay, Rio de Janeiro, southeast- from the state of Sa˜ o Paulo was demonstrated by Eston ern Brazil, was described to evaluate the effect of the and Bussab (1990). presence of Caulerpa scalpelliformis on the dominant The state of Rio de Janeiro is situated on the south- species, Sargassum vulgare. The canopy cover of mac- eastern coast of Brazil, which is defined as a warm tem- roscopic organisms was analyzed monthly or less fre- perate region (Horta et al. 2001). Compared to the quently on rocky substrata from Baleia Beach (impact tropical Brazilian northeastern coast, this region has a location, where C. scalpelliformis appeared) and from two low number of species of Caulerpa, including Caulerpa reference locations (without C. scalpelliformis), during the fastigiata Montagne, C. mexicana Sonder ex Ku¨ tzing, C. periods September 1993 to May 1995 and October 2001 racemosa (Forsska˚ l) J. Agardh, C. sertularioides (S.G. to September 2003, using the point sampling method Gmelin) M. Howe and C. verticillata J. Agardh (Oliveira (ns5 random quadrats). At the impact location, S. vul- Filho 1977, Mitchell et al. 1979, Falca˜ o et al. 1992, Pedri- gare was dominant from September 1993 to September ni et al. 1994, Guimaraens and Coutinho 1996, Sze´ chy 2001, when C. scalpelliformis appeared on the rocky and Paula 2000b, Amado Filho et al. 2003). Among these substratum beneath S. vulgare. In a few months, the cov- species, C. racemosa is recognized as an invasive spe- er of S. vulgare declined dramatically and C. scalpellifor- cies in the Mediterranean Sea (Modena et al. 2000, Piazzi mis became dominant on the rocky and sandy substrata et al. 2001, Ceccherelli et al. 2002, Verlaque et al. 2003). until the end of the study. Over the same period, S. vul- Sparse occurrence of Caulerpa scalpelliformis (R. gare was dominant at the reference locations. Multiva- Brown ex Turner) C. Agardh has been reported along the riate community analysis revealed significant changes in tropical region of the Brazilian coast (Joly et al. 1965, the macroalgal community structure following the Pinheiro-Vieira and Ferreira 1968, Ferreira-Correia and appearance of C. scalpelliformis. The replacement of S. Pinheiro-Vieira 1969, Nunes 1998), where this species vulgare by C. scalpelliformis suggests the competitive does not show invasive behavior. Previous to the present superiority of C. scalpelliformis under sheltered condi- study, the southern limit of distribution for this species tions. This is the first record of this pantropical macroalga on the Brazilian coast was established as the state of in the warm temperate region of the Brazilian coast. Espı´rito Santo (Mitchell et al. 1990) (Figure 1), a transition region between the Brazilian tropical and warm temper- Keywords: abundance; benthic communities; Brazil; ate regions (Horta et al. 2001). Caulerpa; invasive species; Sargassum. This study aimed at chronicling the changes occurring in a phytobenthic assemblage of the shallow sublittoral zone of Ilha Grande Bay, dominated by the brown alga Introduction Sargassum vulgare, following the appearance of the green alga Caulerpa scalpelliformis. We contrast an Along the southeastern Brazilian coast, phytobenthic invaded site at Baleia Beach with two nearby uninvaded assemblages of the shallow sublittoral zone from shel- reference locations. C. Falca˜ o and M.T.M. de Sze´ chy: Replacement of Sargassum by Caulerpa 209 Figure 1 Distribution of Caulerpa scalpelliformis along the Brazilian coast, with the corresponding references. sprevious records; wspresent record. 1sJoly et al. (1965); 2sPinheiro-Vieira and Ferreira (1968); 3sFerreira-Correia and Pinheiro- Vieira (1969); 4sMitchell et al. (1990); 5sNunes (1998). ESsEspirito Santo state; MGsMinas Gerais state; SPsSa˜ o Paulo state. Materials and methods tions of these lines provided 81 points. For each sam- pling, five quadrats were analyzed, following the recommendation of other Sargassum studies (Critchley Two sites in Jacuacanga Cove, Ilha Grande Bay, were et al. 1990, Largo et al. 1994). The quadrats were ran- surveyed by diving: Baleia Beach and Gordas Beach domly positioned along a horizontal extension of approx- (Figure 2). At Baleia Beach, two rocky shores were mon- imately 20 m of the rocky substratum, around the initial itored: one, where C. scalpelliformis appeared (impacted point where Caulerpa scalpelliformis was found later. location) and the other, where C. scalpelliformis did not From October 2001 to September 2003, canopy cover occur (reference location 1). The rocky shore at Gordas at the impact location was quantified bimonthly or slightly Beach was taken as reference location 2. less frequently, on rocky substrata (ns5), as well as on Baleia Beach is relatively protected from exposure to adjacent sandy substrata (ns5), approximately 2 m deep, wave action; there the impact location is more protected using the same point quadrat sampling method. than reference location 1. Reference location 2 was mod- To evaluate whether the temporal changes in the rocky erately exposed to wave action. Baleia Beach is situated assemblage of the impact location are related to the in the inner part of Jacuacanga Cove, near Verolme ship- presence of Caulerpa scalpelliformis, the canopy cover yard and Monsuaba village, where non-treated waste- of the organisms on rocky substrata of both reference water is discharged directly into the sea. In addition, locations was analyzed monthly, from June 2002 to Feb- there are many points along the coast of Jacuacanga ruary 2003, using the point quadrat sampling method, Cove where the discharge of non-treated wastewater can with 50=50 cm quadrats (ns5), randomly placed along be found (personal observations). At the three locations, a horizontal extension of 20 m. boulders of different sizes covered the bottom from the Possible relationships between mean percentage cov- fringe of the sublittoral zone to approximately 2 m depth. er of Sargassum vulgare and Caulerpa scalpelliformis At the beginning of the study period, Sargassum vulgare were tested by the Spearman’s rank correlation coeffi- formed a continuous and conspicuous bed on these cient (Zar 1984). rocky substrata. The software package Primer 5 (Plymouth Routines in At the impact location, temporal variation in the canopy Multivariate Ecological Research, from Plymouth Marine cover of algae and sessile invertebrates on rocky sub- Laboratory, UK) was used for multivariate statistical anal- strata in the shallow sublittoral zone (1.0–1.5 m deep in yses to describe differences in the community structure relation to mean low water) was monitored from Septem- at the different locations and times. Data were double ber 1993 to May 1995. Non-destructive samples were square root transformed. Bray-Curtis similarity matrix taken monthly. Only macroscopic organisms that could was calculated and used to generate a two-dimensional be readily identified in the field with the unaided eye were plot with the non-metric multidimensional scaling (nMDS) included. The percentage cover was estimated using the technique (Clarke and Warwick 1994). One-way analysis point quadrat sampling method (Foster et al. 1991). The of similarity (ANOSIM) was used to test whether the com- quadrat was a 20=20 cm aluminium frame, divided by munity structure at the impact location differed signifi- perpendicular nylon lines strung inside it; the intersec- cantly from that at reference locations. 210 C. Falca˜ o and M.T.M. de Sze´ chy: Replacement of Sargassum by Caulerpa Figure 2 Study area at Jacuacanga Cove, Ilha Grande Bay, Rio de Janeiro state, showing the two sites studied: Baleia Beach (1) and Gordas Beach (2). Note ‘‘Verolme’’ shipyard and oil terminal ‘‘Ilha Grande Bay’’. Material deposited in herbarium: Caulerpa scalpellifor- Figure 3 Caulerpa scalpelliformis from Jacuacanga Cove, Ilha mis f. denticulata – Brazil, state of
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