Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil

v ELSEVIER

Aquatic Botany 52 (1996) 283-299

Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil Mariana Alves de Guimaraens a, *, Ricardo Coutinho b a Rosenstiel School o f Marine and Atmospheric Science, Division of Marine Biology and Fisheries, 4600 Rickenbacker Causeway, Miami, FL 33149, USA b lnstituto de Estudos do Mar Alte, Paulo Moreira, IEAPM - - Arraial do Cabo-RJ, Brazil

Accepted 20 September 1995

Abstract The Cabo Frio (23°01'S, 42°00'W) upwelling region has been recognized as a biogeographic barrier to the macroalgal flora of the Brazilian coast. Five sites in this area were studied to evaluate the regional variation (along an upwelling gradien0 and local variation of the flora (under similar upwelling influence); collections were also made in different seasons of the year from November 1988 to April 1990 to document temporal variation. Some variables (temperature, salinity, total inorganic nitlogen and total phosphate) were analyzed to determine the oceanographic characteristics influencing the studied sites. Hierarchical Cluster Analysis and Ordination Factorial Analysis of Correspondence (FAC) were used to determine the structure of the macroalgae community in this area. The sites influenced by the upwelling waters showed lower water temperature values and higher nutrient concentrations in the spring-summer upweUing period. The benthic flora survey recorded elements with warm temperate affinities (i.e. Ceramium diaphanum (Lightfoot) Roth, Polysiphonia decussata Hollenberg and Endarachne binghamiae J. Agardh) and algae with tropical affmities (i.e. Gelidiopsis gracilis (Kiitzing) Vickers, Dictyota cervicornis Kiitzing and Caulerpa racemosa (Forssk~l) J. Agardh). In general the local flora showed a peak in reproduction during the spring-summer period. The multivariate analysis distinguished the sites influenced by upwelling waters, and some samples taken in the same inlet suggested that further differences in the floral composition were due to wave exposure. Keywords: Benthic algae; Spatial distribution; Upwelling; Brazil

* Corresponding author. Fax: (305) 361-4077; e-mail: [email protected]. 0304-3770/96/$15.00 © 1996 Elsevier Science B.V. SSDI 0304-3770(95)005 11-0

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M.A.d. Guimaraens, R. Coutinho/ Aquatic Botany 52 (1996)283-299

1. Introduction

According to Liining (1990) the Western Atlantic Tropical Region ranges from southem Florida to Cabo Frio in Brazil. The Brazil current enables tropical organisms to survive to the Cabo Frio region. Consequently, this area has been recognized as a biogeographic barrier to the macroalgal flora of the Brazilian coast (Yoneshigue, 1985). In addition, coastal upwelling in the region provides favorable conditions for the occurrence of species with temperate affinities. Among the physical factors potentially limiting regional seaweed distributions temperature is the variable that concerns phytogeographers the most. Factors such as salinity and wave exposure have localized effects. Indirect evidence of the importance of temperature to seaweed floras can be drawn from the effects of ocean currents and upwelling phenomena (Lobban et al., 1985), that cause changes in seaweed floras without much latitudinal changes. The work by Murray and Littler (1981) shows a remarkable difference in the seaweed flora of the California coast, with a cold temperate flora in the central part slightly overlapping the flora of southern California, bathed more regularly by warm waters, illustrating the effect of temperature anomalies on seaweed distributions. The purpose of this research was to evaluate the influence of the local temperature anomaly on the species distribution and phenology of benthic marine algae in the Cabo Frio upwelling. To evaluate the extension of upwelling on the flora we considered sites in a range of 150 km which showed a gradient in upwelling intensity.

2. Materials and methods A coastal upwelling of surface water has been identified in the Cabo Frio region (23°01'S, 42°00'W) (Valentin, 1984), being associated with the local wind regime and bathymetry. The process occurs southwest of Cabo Frio Island (Fig. 1) mainly between the months of October and April (approximately south hemisphere spring and summer). During the non upwelling period the coastal surface waters are characterized by temperatures above 21°C, salinity between 35 and 36%0 and low nutrient concentrations (nitrates and phosphates less then 1 ixg 1-1). The upwelling conditions are well characterized by the low temperature values, below 18°C, reaching as low as 13°C, and high nitrate concentrations, around 10 p~g l-1. Variations in salinity and phosphates are less evident (Valentin, 1984). To evaluate the effects of the upwelling gradient over the benthic flora, five stations were selected for the present study (Fig. 1). Sonar, at Arraial do Cabo to the southwest of Cabo Frio Island is located in the main upwelling area. Jacon6, situated 50 km west of Cabo Frio Island is supposed to be influenced by the upwelling to a lesser extent. Rasa Shore, at Bdzios, north of Cabo Frio island, is not under the influence of upwelling waters. Fortaleza and Forno, at Fomo Inlet, are influenced by sporadic penetration of upwelling waters. Two sites were selected inside Forno Inlet to evaluate possible effects of wave exposure (Forno is a sheltered area while Fortaleza is exposed to waves). Note that the five stations are separated by only a few kilometers.

M.A.d. Guimaraens, R. Coutinho / Aquatic Botany 52 (1996) 283-299

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The collections of benthic algae were made in the period between November 1988 and April 1990, during different seasons of the year. Samples were taken in the intertidal zone by scraping at least three quadrats in each level, along the rocky coasts. The levels were defined by dominant organisms in different heights on the coast. The quadrats were used to obtain biomass data on the dominant species. The quadrat size to sample the upper levels of the coast (dominated by Porphyra, Chthamalus and Brachidontes) was 10 cm X 10 cm; for samples taken at lower levels (dominated by Tetraclita, Ulva/Perna and Megabalanus) the quadrat size used was 20 cm × 20 cm. This method was used to make sure that the samples were taken from the upper to the lower intertidal zone. The sampled material was preserved in 4% formalin. An optical microscope was used for species identification and to determine their reproductive state. The algae were classified according to Wynne (1986) and Silva et al. (1987).

286

M.4.d. Guimaraens, R. Coutinho /Aquatic Botany 52 (1996)283-299

Surface water samples were collected fortnightly at each site (Rasa Shore, Forno Inlet, Sonar and Jacon~) during the study period for determination of chemical and physical variables (total phosphate, total inorganic nitrogen, temperature and salinity). Samples taken for nutrient analyses remained unfiltered. Total phosphate and total inorganic nitrogen were measured according to the methodology described by Strickland and Parsons (1972). Multivariate statistical analysis was used to provide simultaneous analysis of variation of a large number of species, in several samples. Hierarchical Cluster Analysis and Ordination Factorial Analysis of Correspondence (FAC) were made based on binary data (presence or absence of species in each sample) summarized in a 115 species per 24 samples matrix. Sample similarity was assessed by Sorensen's coefficient. The use of factorial analysis of correspondence permitted the ordination of the species and the studied sites simultaneously according to a gradient of environmental conditions (Legendre and Legendre, 1983).

3. Results

The temporal series evidenced the upwelling process occurring southwest of Cabo Frio Island (Figs. 2-5). Rasa Shore and Forno Inlet, to the north, present temperature values above 20°C with maxima in summer and minima in the winter. Jacon~ and Sonar upwelling is characterized by low temperature values, below 18°C, during spring and

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summer periods, inverting the normal seasonal variability. W e believe that Jacon~ and Sonar are influenced in a similar way by upwelling waters. The values o f total nitrogen show a similar behavior as the temperature (Figs. 2 and 4). Higher values o f phosphate are also observed during the upwelling period in Jacon~

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M.A.d. Guimaraens, R. Coutinho/ Aquatic Botany 52 (1996) 283-299

288

and Sonar (Fig. 5). The variations observed in phosphate and total nitrogen in Rasa Shore, that is not under the upwelling influence, can possibly be attributed to river discharge, which is significantly higher close to this area than to the other sites. The freshwater influence is also apparent in salinity variations (Fig. 3). The survey of benthic algae recorded elements with temperate affinities (i.e. Por-

phyra acanthophora, Ceramium diaphanum, Polysiphonia decussata, Endarachne binghamiae), occurring in the sites directly influenced by upwelling waters (Tables 1 and 2). Algae with tropical affinities (i.e. Gelidiopsis gracilis, Vidalia obtusiloba, Dictyota cervicornis, Caulerpa racemosa) occurred at sites not influenced by upwelling waters (Tables 1-3). Analysis of reproductive structures of the local flora indicates that the majority of the species underwent seasonal changes. A few species (e.g. Polysiphonia howei and Polysiphonia scopulorum) were fertile during two periods: during the summer at sites not influenced by the upwelling, and during winter at sites influenced by upwelling. Species with temperate affinities (e.g. Porphyra pujalsii, Ceramium diaphanum, Petalonia fascia and Polysiphonia decussata), were fertile in spring and summer, when the cold water upwelled. Nevertheless, some species were reproductive during the whole year (i.e. Callithamnion felliponei, Jania rubens, Levringia brasiliensis, Hincksia mitchelliae, Feldmannia irregularis), appearing to be aseasonal annuals. Taking into account the occurrence and phenology of the benthic algae in the Cabo Frio upwelling region, we recorded a peak of species occurrence and development of reproductive structures in the spring-summer period (Tables 1-3).

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M.A.d. Guimaraens, R. Coutinho / Aquatic Botany 52 (1996)283-299

Table 1 Distribution, seasonal occurrence and phenology of chlorophyta in the Cabo Frio upweUing region Species

Rasa Shore

Sonar

Forno

Fortaleza

Jacon6

Sp Sm A W Sp Sm A W Sp Sm A W Sp Sm A SP Sm A Enteromorpha compressa (L.) X

X X

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X

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Kiitzing Cladophora oagabunda (L.)

X X

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van den Hoek Cladophora rupestris (L.)

X

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(Roth) Kiitzing ex Harvey 8ryopsis corymbosa J. Agardh Bryopsis pennata Lamouroux Bryopsis plumosa (Hudson) C. Agardh Derbesia marina (Lyngbye) Kjellman Codium intertextum

X

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Vickers Caulerpa fastigiata

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Montagne Caulerpa racemosa Forssk~tl

J. Agardh x, occurrence; Sp, spring; Sm, summer; A, autumn; W, winter.

Using the hierarchical cluster analysis, we established four distinctive groups at 0.5 similarity level at five sites: group I, Rasa Shore; group II, Fortaleza; group III, Sonar and Jacon6; group IV, Forno (Fig. 6). The same four groups were obtained using FAC. In factorial plane 1 - 2 (with 26% o f the variance explained), groups I, II, and III were ordinate along axis I, which explained 15% o f the total variance. Axis I represents the temperature gradient caused b y the local upwelling. Group IV is formed by the samples taken from the only sheltered area studied. It is separated from group II by axis II

290

M.A.d. Guimaraens, R. Coutinho / Aquatic Botany 52 (1996)283-299

Table 2 Distribution, seasonal occurrence and phenology of the pheophyta at Cabo Frio upwelling region Species

Rasa Shore

Sonar

Fomo

Fortaleza

Jacond

Sp Sm A W Sp Sm A W Sp Sm A W Sp Sm A Sp Sm A Bachelotia antillarum

P

(Gnmow) Gerloff Hincksia breviarticulata

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(Kiitzing) Hamel Proteocarpus speciosus

P

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X

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(Hering) Papenfuss Colpomenia sinuosa

X

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J. Agardh Sphacelaria brachygonia

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Lamouroux Dictyota ceroicornis

K~tzing Dictyota ciliolata

X

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X

(Hudson) Lamouroux Dictyota pardalis

X

X

X

X

Kiitzing Lobophora variegata

(Lamouroux) Womersley

X

X

X

X

291

M.A.d. Guimaraens, R. Coutinho /Aquatic Botany 52 (1996) 283-299

Table 2 (continued)

Species

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Fomo

Fortaleza

Jacon6

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(explaining 11.3% of the total variance), that represents different exposure conditions (Fig. 7).

4. D i s c u s s i o n

The periodic occurrence of the upwelling phenomenon is a preponderant influence on the variability of the macroalgal populations of Cabo Frio upwelling region (Yoneshigue and Valentin, 1992). Differences in oceanographic conditions lead to great variability in the composition of the flora, distribution, and reproductive seasonality in this restricted geographic area. The dual nature of the local flora is evidenced by the occurrence of algae with warm temperate affinities (i.e. Porphyra leucosticta, Polysiphonia decussata,

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Ceramium diaphanum, Endarachne binghamiae) in sites directly influenced by upwelling waters, and the occurrence of another group with affinities to warm water (i.e.

Gelidiella acerosa, Gelidiopsis gracilis, Gracilaria cervicornis, Dictyota pardalis, Caulerpa fastigiata, Caulerpa racemosa), at Rasa Shore, that is influenced the whole year by tropical coastal waters. At the sites located at Forno Inlet, species with warm temperate affinities (i.e. Petaloniafascia, Porphyra pujalsii) and elements with tropical affinities (i.e. Gelidium pusillum) were recorded, which characterizes a mixed flora. The Feldmann (1938) index, that is, the ratio of rhodophyta to pheophyta (R/P), for the local flora was 3.3. The Cheney (1977) index, the ratio of rhodophyta species plus chlorophyta species to pheophyta (R + C/P) was 4.2. Both characterize a mixed flora and were calculated using Tables 1-3. The most sensitive stages in the life cycle of individuals can only survive under limited environmental conditions (Golikov et al., 1990). Sporophytic dominance over the gametophytic phase typically occurs when species are at the extreme limit of their range of geographical distribution (L'tining, 1990). As the structures more commonly found in the rhodophyta are the tetraspores we suggest that Cabo Frio may be a boundary, with one phase of the life cycle reduced near their distribution limits. Spermatangia were rarely observed, probably owing to their short life-span compared with those of cystocarps and tetrasporophytes (Coutinho and Seeliger, 1986) (Table 3). In the FAC the sampling sites and species were ordinate along axis I, according to a gradient in upwelling intensity. In the factorial plan 1-2 (Fig. 8, Table 4) we noticed at

296

M.A.d. Guimaraens, R. Coutinho/Aquatic Botany 52 (1996) 283-299

Table 4 Main absolute contributions (%) from species to the axis I-II formation in the Cabo Frio upwelling region Species % Species % Factorial axis I Ceramium diaphanum Arthrocardia gardneri Arthrocardia stephensonii Chaetomorpha antennina Polysiphonia decussata Bryopsis pennata Ophidocladus simpliciusculus Laurencia obtusa Laurencia flagellifera Corallina officinalis Dictyopteris delicatula Caulerpa fastigiata Bryopsis plumosa Dasya brasiliensis Gelidiopsis gracilis Acanthophora spicifera Champia feldmannii Cheilosporum sagittatum Sargassumfurcatum Dictyota cervicornis Enteromorpha flexuosa Porphyra acanthophora Jania rubens Hypnea cervicornis Gymnogongrus griffithsiae Padina gymnospora

2.1 2.1 2.1 1.9

Cladophora vagabunda Dasya corymbifera Centroceras clavulatum Ectocarpus breviarticulatus Caulerpa racemosa Enteromorpha lingulata Dictyota pardalis Callithanmion felliponei Chnoospora minima Wrangelia argus Spyridia hypnoides Gastroclonium parvum Sphacelaria tribuloides

1.9

Factorial axis II

1.9 1.8 1.7

Cladophoropsis membranacea Ulva lactuca Gelidium puMllum Ralfsia e~ansa Bachelotia antillarum Enteromorpha compressa Petalonia fascia Ceramium brasiliense Ceramiumflaccidum Cladophora vagabunda Polysiphonia ferulacea Bostrychia radicans Centroceras clavulatum

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1.3 i.3

one extreme the formation of a group of algae (group I) with marked warm affinities and high values of absolute contributions to the axis formation (i.e. Laurencia spp. 4.3%, Gelidiopais gracilis 1.8%, Sargassum furcatum 1.6%). At the other extreme another group (group III) was established, gathering algae with warm temperate affinities, that also showed a main contribution to the axis formation (i.e. Ceramium diaphanum 4.5%, Polysiphonia decussata 3.0%). The sites located at F o m o Inlet, which are sporadically influenced by the upwelling, showed a mixed flora and are gathered in relation to axis I. Forno species are split from Fortaleza ones by axis II which determines the ordination of samples from the only sheltered site surveyed (Fig. 8). The characteristic algal species from places with low exposure were important to axis II formation (i.e. Cladophoropsis membranacea 16.0%, Bachelotia antillarum 8.5%), contrasting with the contribution of characteristic algae of the highly exposed places, that contribute to axis I formation (i.e. Chaetomorpha

Fig. 8. Factorial correspondence analysis (FAC) showing the species ordination along the factorial plan 1-2 at Cabo Frio upwelling region.

M.A.d. Guimaraens, R. Coutinho /Aquatic Botany 52 (1996) 283-299

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M.A.d. Guimaraens, R. Coutinho/Aquatic Botany 52 (1996) 283-299

antennina 3.3%) (Table 4). With the multivariate analysis we found a correlative

relationship between temperature and species distribution; in this regard we want to emphasize the lack of work with the benthic algae at Cabo Frio region demonstrating the direct effect of temperature on their distribution ranges. In conclusion, our data on distribution and reproduction of species show that the temperature anomaly affects the benthic algal flora enabling warm temperate species to survive under otherwise tropical conditions at the Cabo Frio upwelling region. The ordination of species and sites shows a correlation between the gradient in upwelling intensity and the flora distribution. We consider the exposure to waves to affect the local distribution of algae.

Acknowledgements Thanks to the Instituto de Estudos do Mar Almirante Paulo Moreira (IEAPM) team for helping in the field trips and to Dr. Jean Valentin for his useful comments on the data treatment. Also to A.M. Paiva for critically reviewing the manuscript. This work was supported in part by Funda~o de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), Grant no. E-29/150.096/89. The first author is presently supported by a scholarship from Conselho Nacional de Desenvolvimento Cienfffico e Technol6gico (CNPq) grant no. 201839/93-8.

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Yoneshigue, Y., 1985. Taxonomie et 6cologie des aigues marines darts la region de Cabo Frio-Rio de Janeiro, Br6sil. Ph.D. Thesis, Universit6 d' Aix Marseille II Facuit6 de Sciences de Luminy, 466 pp. Yoneshigue, Y. and Valentin, J., 1992. The macroalgae in the Cabo Frio (Brazil) upwelling region. Ordination of Plant Communities. In: U. Seeliger (Editor), Coastal Plants of Latin America. Academic Press, San Diego, CA, pp. 31-49.