Pan-American Journal of Aquatic Sciences

Research articles

The egg capsule of Rioraja agassizi (Müller & Henle) (Elasmobranchii, Rajidae), endemic to the SW Atlantic. ODDONE, M. C., MESA, A. & AMORIM, A. F..…………..…………………………………………43

Multivariate morphological analyses in continental and island populations of Abudefduf saxatilis (Linnaeus) (Pomacentridae, Perciformes) of Western Atlantic. MOLINA, W. F., SHIBATTA, O. A. & GALETTI-JR, P. M...... 49

Impacto potencial de invasión de Ficopomatus enigmaticus (Fauvel) (Polychaeta: Serpulidae) en la Laguna de Rocha, Uruguay. BORTHAGARAY, A. I., CLEMENTE, J. M., BOCCARDI, L., BRUGNOLI, E. & MUNIZ, P...... …………...57

Record of a pregnant bentfin devilray, Mobula thurstoni (Lloyd) (Elasmobranchii, Mobulidae) caught in Southwestern Brazil. CASAS, A. L. S., CUNHA, C. M., INTELIZANO, W. & GONZALEZ, M. M. B.....………...... 66

Intestinal bacterial diversity in live rock lobster Panulirus homarus (Linnaeus) (Decapoda, Pleocyemata, Palinuridae) during transportation process. IMMANUEL, G., RAJ, P. I., RAJ, P. E. & PALAVESAM, A...... 69

Morphological aspects and seasonal changes of some planktonic ciliates (Protozoa) from a temporary pond in Buenos Aires Province, Argentina. KÜPPERS, G. C., LOPRETTO, E. C. & CLAPS M. C…...... 74

Ocupação da praia da Boa Viagem (Recife/PE) ao longo de dois dias de verão: um estudo preliminar. SILVA, J. S., BARBOSA, S. C. T., LEAL, M. M. V., LINS, A. R. & COSTA, M. F...... 91

Report on the smallfin catshark Apristurus parvipinnis Springer & Heemstra (Chondrichthyes, Scyliorhinidae) in Western South Atlantic with notes on its taxonomy. GOMES, U. L., SIGNORI, C. N. & GADIG, O. B. F...... 99

Benthic macroinvertebrate bycatch in the snail Zidona dufresnei (Donovan) fishery from the Uruguayan continental shelf. RIESTRA, G., LOZOYA, J. P., FABIANO, G., SANTANA, O & CARRIZO, D...... 104

Feeding Ecology of Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) on Estuarine and Lagoon Environments in the Southwest Coast of Portugal. COSTA, P. F., OLIVEIRA, R. F. & FONSECA, L. C...... 114

Pan-American Journal of Aquatic Sciences (2006), 1 (1)

Original scientific photographs

Genidens genidens (Cuvier) (Pisces, Ariidae), oral incubation of eggs. GARCIA, A. M., VIEIRA, J. P. & BURNS, M. D. M...... I

Eunectes murinus (Linnaeus) (Serpentes, Boidae), preying activity. MACEDO-BERNARDE, L. C...... II

Software and Book Review

POSEIDON LINUX – Uma distribuição Linux voltada para público acadêmico e científico. FERREIRA, C. F., VELASCO, G., ALBERGONE, E. H., HELLEBRANDT, D., VAZ, B. S...... III

Pan-American Journal of Aquatic Sciences (2006), 1 (1)

The egg capsule of Rioraja agassizi (Müller & Henle) (Elasmobranchii, Rajidae), endemic to the SW Atlantic

1,3 1 2 MARÍA CRISTINA ODDONE , ALEJO MESA & ALBERTO FERREIRA DE AMORIM

1 Universidade Estadual Paulista, Departamento de Ecologia, Campus Rio Claro Av. 24-A 1515, CP 199, CEP 13506- 900, Rio Claro, SP, Brazil. 2 Instituto de Pesca, Av. Bartolomeu de Gusmão, 192, Ponta da Praia, CEP: 11030-906, Santos, SP, Brazil. 3 Correspondence to: M. C. Oddone: [email protected]

Abstract. Freshly collected egg capsules of Rioraja agassizi were light and bright brown in colour, laterally keeled and symmetrically convex with a smooth configuration of the surface. The base of the horns, the lateral margins and the ventral wall of the egg capsules were covered by sticky, shiny yellow attaching fibrils. The mean total length of the egg capsules was 47 mm and the mean width was 31 mm. Microscopically, the dorsal wall of the egg capsules was 0.21 mm thick and consisted of three layers, being the central one colourless and laminated. The ventral wall was 0.11 mm in thickness and presented the same layer’s patterns of the dorsal wall. Length of the egg capsules positively increased with female’s length.

Key words: oviparity, lateral keel, egg-bearing, microscopic structure.

Resumen. La cápsula ovígera de Rioraja agassizi (Müller & Henle, 1841) (Elasmobranchii, Rajidae), endémica del Atlántico SW. Las cápsulas ovígeras de Rioraja agassizi recientemente colectadas eran de un color marrón claro brillante, presentaban una quilla lateral, eran simétricamente convexas y poseían superficies lisas. La base de los cuernos, así como los márgenes laterales y la pared ventral estaban recubiertos por filamentos pegajosos de adhesión de color amarillo brillante. La longitud total media de las cápsulas fue 47 mm y el ancho medio 31 mm. Microscópicamente, la pared dorsal de las cápsulas ovígeras tenía un grosor de 0.21 mm y consistía en tres capas, siendo la del medio descolorida y laminada. La pared ventral tenía un grosor de 0.11 mm y presentaba el mismo patrón laminar de la fase dorsal. La longitud de las cápsulas ovígeras aumentó positivamente con la longitud total de las hembras.

Palabras clave: oviparidad, quilla lateral, ovada, estructura microscópica

Introduction relationships between genera and even between The genus Rioraja is endemic to the austral species; apart from throwing some light on adaptive region of South America (McEachran & Aschliman differentiation of various species (Ishiyama 1958). 2004) and comprises one single species, R. agassizi Apart from providing taxonomic information (Hubbs (Müller & Henle 1841), which occurs from & Ishiyama 1968), the morphology and external Argentinean waters to Rio de Janeiro in features of the skate’s egg capsules can provide data Brazil and inhabits from coastal waters to on the distribution and reproductive biology of depths of up to 130 m (Figueiredo 1977). skates (Oddone et al. 2004). Furthermore, Ishiyama In south Brazil is considered a constantly present (1958) demonstrated that the microscopic structure species being found from 15 to 60 m of depth of Japanese skates’ egg capsules is an important (Vooren 1997). source of systematic information on the different In oviparous elasmobranchs the egg is rajid species. covered with a thick leathery membrane, the egg In this work, the morphological and capsule (shell) with features that aid in their microscopical description of the egg capsule of R. identification besides establishing possible agassizi is presented.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48

44 M. C. ODDONE ET AL.

Materials and Methods microtome: a) sections were dehydrated for half an A number of 119 egg capsules of Rioraja hour in alcohol 70%, 80 %, 90 % and finally 95 %; agassizi were collected by bottom trawler b) an embedding resin was prepared and reposed for commercial vessels during March and May 2005, off 24 hours refrigerated; c) preparation protocol for Southeast Brazil. The fishing area is presented in inclusion resin consisted in mixing 15 ml of the Figure 1. Depth ranged between 13 and 52 m. Egg embedding plus 1 ml of the hardener solution, capsules were directly extracted from the females’ shaking (in the shaker) for 3 minutes and depositing uteri; fixed in 4% formalin and preserved in 70% in mould, where the egg capsules’ cuts were ethanol (Fig. 2). Terminology on the egg capsule incorporated and hold with tweezers until the resin and methods of measurements followed Hubbs & hardened to keep the vertical position to allow the Ishiyama (1968) Templeman (1982) and Gomes & transversal cut desired in the microtome; d) the Carvalho (1995). samples were kept in heater for 24 hours and immersed in silica to extract humidity; e) moulds 500 containing the sections were glued to wooden blocks 100 22° Rio de Janeiro to be cut in the microtome (LEICA RM 2145, at Histology Laboratory, Biology Department, 23° São Paulo UNESP); f) after discriminating between several 24° thickness in the microtome and observing in the microscope, the ideal thickness was found to Paraná 25° be 8 μ and this thickness was kept for all the cuts. 26° Sections were placed in the slides and deposited in the heater for 24 hours; g) sections were 27° Santa Catarina embedded in Canadian Balsam, covered with cover 28° slide, deposited in the heater for 48 hours for 100 500 fixation; h) sections were observed under 49° 48° 47° 46° 45° 44° 43° 42° 41° 40° microscope (at 100X) for black and white photographing and assessing. Internal layer refers to Figure 1. Map of the study area: Southeast Brazil, showing the trawling stations (dotted circles) from where samples of Rioraja the egg capsule’s wall layer oriented to the capsule agassizi came from. interior; external layer refers to the layer in contact to the exterior. Data recorded from each egg capsule were n.g. classified into measurable variables and features (Hubbs & Ishiyama 1968). The measurable variables were: total length; total width; total length of anterior and posterior horns, height (in the highest point) and thickness and width of the lateral keel. Features recorded were: colour; configuration of the surface or texture; basic morphology, presence of adhesion fibrils and microscopical structure of both sides of the capsule’s wall. Horns were measured on each side, according to Hubbs & Ishiyama (1968). All measurements were made with Vernier calipers with 0.1 mm precision. Differences were tested using a t-test (Sokal & Rohlf 1987) with a significance level of 0.05. The terms ‘anterior’/’posterior’ and ‘ventral/’dorsal’ refer to the position of the egg capsules in the uteri (Clark 1922, Hubbs & Ishiyama 1968).

To examine the microscopical structure of Figure 2. Complete posterior oviducts (uteri) recently extracted the egg capsules’ wall, rectangular sections (5x5 from a female of Rioraja agassizi bearing term egg capsules; mm) of the dorsal and ventral walls were carried out n.g.=nidamental glands. Black bar represents 1 cm. centrally on the egg capsules using a scalpel according to Hubbs & Ishiyama (1968). The latter A linear regression was used to analyse the were submitted to the following inclusion protocol relationship between total length of the egg capsule in historesin to be afterwards cut with the aid of a and total length of the female.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48 The egg capsule of Rioraja agassizi. 45

Results laminated, with a number of 28 superimposed In all the analysed females, only one lamina and 0.182 mm thick and an interior rather egg capsule per uterus was found. Freshly collected thin layer; dark brown and 0.007 mm thick (Fig. 4a). and fully formed egg capsules of R. agassizi The ventral wall presented the same pattern of a were typically rectangular with a horny process light, middle uncoloured layer between two darker in each corner and bright brown in colour. and rather thinner layers. In transverse section, the The base of the horns, the lateral margins and the ventral wall of the egg capsule was 0.11 mm in ventral wall of the egg capsules were covered thickness. The most external layer was dark brown by sticky, shiny yellow adhesion fibrils. and 0.022 mm thick, followed by a middle layer, To the naked eye and touch, both dorsal and colourless and laminar (consisting of about ventral walls were smooth. In lateral view, the 20 lamina) and 0.084 mm thick, and finally, an egg capsules were keeled and symmetrically interior layer, dark brown and 0.0044 mm wide (Fig. convex, with the highest point situated 4b). centrally (Fig. 3). a ext

int

b

ext

int Figure 3. The term egg capsule of Rioraja agassizi in lateral Figure 4. The microscopical structure of the dorsal (a) and view (above) and upper view (below). Black bar represents 1 ventral (b) walls of Rioraja agassizi (100X); ext.=external; cm. int.=internal.

The total length of the egg capsules of R. agassizi ranged from 41 to 56 mm Larger females were found to produce larger (mean=47.34) and the width ranged from egg capsules according to: 22 to 36 mm (mean=30.53). The descriptive ECL=0.0402*FTL+1.1632 (ECL=egg capsule statistics for all the morphological variables length; FTL=female total length). The total length of recorded are presented in Table I. The anterior the egg capsule as dependent variable had a positive horns’ length varied from 38 to 53 cm (mean=49.15) and significant (p < 0.000, R=0,61) relationship with and posterior horns’ length from 35 to 68. the female’s total length (Fig. 5). Posterior horns were significantly longer than 4.0 anterior horns (t=-15.1, P>0.000, df=95). The ratio posterior/anterior horns was 1:4. The lateral keel 3.5 was in mean 1.16 mm wide and 1.66 mm thick. The egg capsules had a mean height of 12.08 mm. In 3.0 eight egg capsules, anterior velum was absent, and was variable in length when existing, with a mean length of 3.34 mm and the posterior velum of 6.33. 2.5 Microscopically, the dorsal wall of the egg capsule of R. agassizi was 0.21 mm thick and 2.0 TOTAL LENGTH EGG CAPSULE (cm) 30 35 40 45 50 55 60 65 70 consisted of three layers: an external layer; dark TOTAL LENGTH FEMALE (cm) brown and markedly darker than the rest, 0.023 mm Figure 5. The relationship between female’s total length (cm) thick; a middle layer; colourless, luminous and and egg capsule’s length (cm) for Rioraja agassizi.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48 46 M. C. ODDONE ET AL.

Table I. Descriptive statistics for the variables measured (mm) on the egg capsules of Rioraja agassizi; number (n), mean, range, standard deviation (SD) and standard error (SE) for: total length, total width, height, width and thickness of the keel, length of anterior and posterior horns (A., P., horns), length of anterior and posterior velum (A., P., velum).

Variable n Mean Range SD SE Total length 119 47.34 41-56 3.09 0.28 Total width 118 30.53 22-36 2.32 0.21 Height 79 12.08 7-15 1.45 0.16 Keel width 110 1.16 1-2 0.33 0.03 Keel thickness 110 1.66 1-3 0.42 0.04 A. horns 112 35.93 15-53 1.06 0.45 P. horns 107 49.15 35-68 6.54 0.45 P. velum 114 6.33 3-10 1.13 0.11 A. velum 55 3.34 1-6 1.33 0.18

Discussion spp. (Oddone et al. 2004, Oddone, unpublished Single oviparity (one embryo per egg data). In Callorhynchus milii a convex surface is capsule) is the only type of reproduction in the covered with sticky fibrils that attach sand thereby family Rajidae, being one egg deposited at a time camouflaging the egg capsule, while the opposite from each oviduct usually in pairs during the side is smooth and acts as a suction cup to keep the spawning season (Musick & Ellis 2005). capsule planted in the sand (Hamlett et al. 2005) that The smooth surface of the egg capsule of likely happens in R. agassizi. The degree of R. agassizi distinguishes it from the egg capsules of development of the fibrils’ mass in some cases is a the species of genus Atlantoraja, where a marked character of value in distinguishing one species from (and macroscopical) longitudinal striation exist, with another (Ishiyama 1958). the exceptional egg capsule of A. castelnaui which Ishiyama (1958) recorded lateral keel in has a rather smooth surface that resemble the egg 20 of a total of 21 examined species. Egg capsules of capsule’s surface of R. agassizi, even in the Rioraja are typically laterally keeled as in microscopical composition of the egg capsule’s wall Atlantoraja spp., unlike in genus Symperygia (Oddone, unpublished data). In the Japanese rajids, (at least in S. acuta and S. bonapartii) where there is a notorious difference in the configuration of capsules are laterally flanged (Mabragaña et al. the surface of the main portion of the capsules 2002, Oddone et al. 2004). A striking external between the northern and the southern species; being feature of the egg capsule of R. agassizi was the the capsule somewhat roughened with minute variability of the anterior velum length that varied prickles or tubercles over the entire surface in the from absent to 6 mm, in some cases being longer northern forms, but it is, in general, very smooth in than the posterior velum. the southern ones (Ishiyama 1958). The length of the horns shows rather large Another difference with the genus intraspecific variations and as a rule, the length of Atlantoraja is the equally convex walls of the egg the posterior horns tends to appear a trifle longer capsule of R. agassizi, that are also typical of than that of the anterior ones (Ishiyama 1958). Sympterygia acuta, S. bonapartii, and Psammobatis In R. agassizi, the ratio posterior/anterior horns was spp. (Oddone & Vooren 2002, Oddone et al. 2004). 1.4. In Atlantoraja cyclophora and A. platana this The egg capsule of R. agassizi is smaller than the ratio was 2.4 and 2.7 respectively (Oddone et al. egg capsules of Atlantoraja spp. (with a mean size 2004). In S. acuta the ratio is 15.7, particularly high of ~47x30 cm against 68x39 cm in A. cyclophora, because of the presence of tendrils instead of the smallest egg capsule of the genus) and than the (posterior) horns (Oddone & Vooren 2002). egg capsules of S. bonapartii with mean dimensions As observed by Ishiyama (1958) for of 77x48 cm (Mabragaña et al. 2002), but somewhat Japanese rajid species, the main portion of the egg larger than S. acuta’s, with mean size of ~5x3 cm. capsule in R. agassizi is made of an internal, ‘pulpy’ The latter can be easily distinguished because of the layer and an external layer darker than the rest. The coloration (green olive) and the presence of tendrils author noted that, in general, the ‘pulpy’, middle instead of posterior horns as in R. agassizi (Oddone layer (forming the lining of the capsule wall) is & Vooren 2002). relatively soft and colourless, but the tissue becomes The disposition of the adhesion fibrils in R. hard and the colour changes from yellow to brown agassizi is the same than observed in Atlantoraja in the external layer which covers the surface of the

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48 The egg capsule of Rioraja agassizi. 47 capsule and that the degree of development of this Gomes, U.L. & de Carvalho, M.R. 1995. Egg ‘pulpy’ layer seemed to be correlated with the capsules of Schroederichthys tenuis and distribution of the skates. In A. cyclophora, for Scyliorhinus haeckelli (Condrichthyes, instance, the external layer corresponds with about Scyliorhinidae). Copeia, 1995 (1): 232-236. 0.33% of the egg capsule’ wall in both ventral and Hamlett, W.C, Knight, D. P., Pereira, F. T. V., dorsal walls (Oddone, 2005). In R. agassizi, this Steele, J. & Sever, M. 2005. Oviducal glands percentage is ~0.1-0.2. Ishiyama (1958) concluded in chondrichthyans. pp 301-335. In: Hamlet, that there is a close relationship between the W. C. (Ed). Reproductive biology and differentiation of the capsule and the geographical phylogeny of chondrichthyans, sharks, distribution, as well as the breeding habits of the batoids and chimaeras. Science Publishers, adult skates (though there are some examples that do Inc. Enfield, 562 p. not fit this conclusion) and the much smoother Hubbs, C.L, & Ishiyama, R. 1968. Methods for the surface of an egg capsule’s species, could have taxonomic studies and description of skates resulted from its adaptation to an environment where (Rajidae). Copeia, 1968: 483-491. the temperature is relatively high. This can be Iglesias, S.P., Du Buit, M.H. & Nakaya, K. 2002. related with the different areas inhabited by R. Egg capsules of deep-sea catsharks from agassizi and A. cyclophora; while the former prefers eastern north Atlantic, with first description of coastal, shallow waters of up to 50 m deep, the latter the capsule of Galeus mirinus and Apristurus is found at deeper shelf waters of up to 300 m deep aphyodes (Chondrichthyes: Scyliorhinidae). (Vooren 1997, Oddone 2003, Oddone 2005). Cybium, 26(1): 59-63. Positive relationships between egg capsules length Ishiyama, R. 1958. Observations on the eggs- and female’s total length have been observed for capsules of skates of the family Rajidae, several Rajidae and also Scyliorhinidae (Ishiyama found in Japan and its adjacent waters. 1958, Templeman 1982, Braccini & Chiaramonte Bulletin of the Museum of Comparative 2002, Iglesias et al. 2002). Such relationship, Zoology at Harvard College, 118(1): 1-24. however, was not observed in Atlantoraja Mabragaña, E.; Lucifora, L.O. & Massa, A.M. cyclophora (Oddone 2003). 2002. The reproductive biology and abundance of Sympterygia bonapartii Acknowledgments endemic to the south-west Atlantic. Journal We are thanked to: P. L. Mancini for collaboration of Fish Biology, 60: 951-967. in the samples’ collection and processing; skippers McEachran, J.D & Aschliman, N. 2004. Phylogeny of the CVs ‘Antares & Polares’, ‘Cigano do Mar’ I of Batoidea. p 79-113. In: Carrier, J. C., & II, ‘Dourado & Araguaia’ and ‘Jangadeiro’, G. Musick, J. A. & Heithaus, M. R. (Eds.). M. Souza for histological assistence and three Biology of sharks and their relatives. CRC referees who revised and improved the submitted Press, London, 596 p. manuscript. This study was financed by FAPESP Musick, J. A. & Ellis, J. K. 2005. Reproductive (Fundação de Amparo à Pesquisa do Estado de São evolution of chondrichthyans, pp 45-71. In: Paulo). W. C. Hamlett (ed). Reproductive biology and phylogeny of chondrichthyes, sharks, References batoids and chimaeras. Science Publishers, Braccini, J. M., & Chiaramonte, G. E. 2002. Inc. Enfield , 562 p. Reproductive biology of Psammobatis Oddone, M.C. & Vooren, C.M. 2002. Egg-cases and extenta. Journal of Fish Biology, 61: 272– size at hatching of the south-western Atlantic 288. skate Sympterygia acuta Garman, 1877 Clark, R.S. (1922) Rays and skates (Raiae) No 1. (Elasmobranchii, Rajidae). Journal of Fish Egg capsules and young. Journal of the Biology, 61: 858-861. Marine Biological Association of the United Oddone, M. C. 2003. Biologia reprodutiva de Kingdom, 12: 577-643 Atlantoraja cyclophora (Regan, 1903) no Sul Figueiredo, L.L. 1977. Manual de Peixes Marinhos do Brasil. Rio Grande, MSc. Thesis. do Sudeste do Brasil. Introdução. Caçoes, Fundação Universidade Federal do Rio raias e quimeras. Museu de Zoologia da Grande, 99 pp. Universidade de São Paulo. São Paulo, 104 Oddone, M.C, Marçal, A.S. & Vooren, C.M. 2004. pp. Egg capsules of Atlantoraja cyclophora (Regan, 1903) and A. platana (Günther,

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48 48 M. C. ODDONE ET AL.

1880) (Pisces, Elasmobranchii, Rajidae). Atlantic. Journal of Northwest Atlantic Zootaxa. 426: 1-4. Fisheries Science, 3: 47-56. Oddone, M.C. 2005. The microscopic structure of Vooren, C.M., 1997. Demersal elasmobranchs. In: the egg capsules of Atlantoraja cyclophora Seeliger, U., Odebrecht, C. & Castello, J.P. (Elasmobranchii: Rajidae: Arhynchobatinae). (Eds.). p 141-146. Subtropical convergence Biota Neotropica, 5 (2): 1-4. environment: the coast and the sea in the Sokal, R.R. & Rohlf, F.J. 1987. Introduction to Southwestern Atlantic. Berlim. Springer- Biostatistics. Second Edition. W.H. Freeman Verlag. 308 p. and Company. New York, 363 p. Templeman, W. 1982. Development, occurrence and characteristics of egg capsules of the thorny skate, Raja radiata, in the Northwest

Received May 2006 Accepted June 2006 Published online June 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 43-48

Multivariate morphological analyses in continental and island populations of Abudefduf saxatilis (Linnaeus) (Pomacentridae, Perciformes) of Western Atlantic

1 2 3 WAGNER F. MOLINA , OSCAR A. SHIBATTA & PEDRO M. GALETTI-JR.

1Departamento de Biologia Celular e Genética, Centro de Biociências, Universidade Federal do Rio Grande do Norte, CEP 59078-970 Natal, RN, Brazil. E-mail: [email protected] 2Departamento de Biologia Geral, Universidade Estadual de Londrina, CEP 86051-970 Londrina-PR, Brazil. 3Departamento de Genética e Evolução, Universidade Federal de São Carlos, Caixa Postal 676, CEP 13565-905 São Carlos-SP, Brazil. 1 Corresponding author

Abstract. The reef species Abudefduf saxatilis (Linnaeus, 1758) is usually considered as a single large Western Atlantic population distributed in reef habitats from northern United States (Rhode Island) to Uruguay. However, principal components and canonical variables analyses of samples distributed along the Brazilian coast (Rio Grande do Norte, Ceará, Bahia, Rio de Janeiro and Santa Catarina states), and oceanic islands of Atol das Rocas and St. Paul’s Rocks, showed morphological variation, which could suggest subdivisions among different populations. Clinal variations of meristic traits along the north- south direction seem to have temperature as their main causative factor. Also, there was a greater similarity among contiguous populations that become more differentiated with distance. In this context, the Brazilian Current flowing, in north-south direction, seems to play an important dispersive role. There were differences between insular and continental populations, which suggest the occurrence of self- recruitment either by a possible existence of circular currents, an active larval role and/or a possible selection for an optimal egg-laying period leading to restrictions in their dispersion. Thus, phenetic divergences seem to suggest restrictions to the genetic flow in the South Atlantic A. saxatilis population.

Key words: morphological analyses; canonical variable; population structure; geographical barriers; cline.

Resumo. Análises morfológicas multivariadas em populações continentais e insulares de Abudefduf saxatilis (Linnaeus) (Pomacentridae, Perciformes) do Atlântico Ocidental. A espécie de peixe recifal, Abudefduf saxatilis, tem sido considerada como uma única grande população Atlântica Ocidental distribuída em habitats recifais do norte dos Estados Unidos (Rhode Island) ao Uruguai. Contudo, análises por componentes principais e variáveis canônicas em amostras distribuídas ao longo da costa Brasileira (Estados do Rio Grande do Norte, Ceará, Bahia, Rio de Janeiro e Santa Catarina), e das ilhas oceânicas do Atol das Rocas e Rochedos de São Paulo, mostraram modificações morfológicas que podem sugerir subdivisões entre diferentes populações. Alguns padrões gerais podem ser observados quanto à distribuição de Abudefduf saxatilis. Variações clinais de características merísticas, na direção norte-sul, indicam a temperatura como o principal fator causal. Além disso, há uma maior similaridade entre populações contíguas que se tornam mais diferenciadas com a distância. Neste contexto, a Corrente do Brasil que flui na direção norte-sul parece desempenhar um importante papel dispersivo. Existem diferenças entre populações insulares e continentais, que sugerem a ocorrência de auto-recrutamento pela possível existência de correntes circulares, um papel ativo de larvas e/ou seleção para um período ótimo de desova levando a restrições a sua dispersão. Tais divergências fenéticas sugerem restrições ao fluxo genético entre populações de A. saxatilis.

Palavras Chave: análises morfológicas; variáveis canônicas; estrutura populacional; barreiras geográficas; clina.

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50 W. F. MOLINA ET AL.

Introduction suggesting population subdivisions. In spite of its physical continuity, the marine environment shows regional, oceanographic and Materials and Methods ecological peculiarities. Reef fish populations living Samples of different sizes (juveniles and in distinct environmental conditions across wide adults) of A. saxatilis were collected in reef and geographic areas may present subtle color rocky bottoms in the Brazilian offshore Islands - St differentiation (Planes & Doherty 1997) or Paul’s Rocks (0°55' N; 29°21' W), Atol das Rocas significant modifications in their body shape (Bell et (3o50' S; 33o49' W), respectively 960 km and 270 al. 1982). km in front to northern coast, and along Brazil coast Pomacentridae family stands out as - Natal (05°52'43" S; 35°10'23" W) (Rio Grande do important reef fishes because of its abundance in Norte state), Tinharé Island (13º28' S; 39º02' W), Western Atlantic reefs. It has great species diversity Cairu (Bahia state) and Bombinhas (27º07'54" S; but because their morphological similarities (cryptic 48º31'40" W), Penha (Santa Catarina state), and species) and pigmentation patterns that vary Fortaleza (03º41'15" S; 38º29' W) (Ceará state; only ontogenetically (Novelli et al. 2000) it is difficult to juveniles) (Fig.1). Samples were fixed in differentiate among species. They are spread over formaldehyde at 10% and stored in 70% ethyl vast areas (Allen 1975), whereas distribution of alcohol. Body measurements were taken head to tail some species is restricted to oceanic islands (Emery using a caliper precision 0.05mm using the truss 1972, Edwards & Lubbock 1983; Gasparini et al., networks method (Strauss & Bookstein 1982). The 1999). Others are found spread over vast areas samples for each geographic area are showed in the (Allen, 1975, 1991). Table I. Among widely distributed groups, the genus Abudefduf represents a good example of dispersive capacity, especially A. saxatilis. This species is distributed in reef and rocky environments from the northern USA to the border with Uruguay (Menezes & Figueiredo 1985). Disagreement about time period and number of species divergences within this genus has triggered molecular phylogenetic studies (Lessios et al. 1995, Bermingham et al. 1997). Pomacentridae shows great fidelity to their microhabitats, and can live in certain reefs for months or years (Reese 1973). This ecological characteristic indicates little or no influence of migration in their distribution, suggesting that it is conditioned basically by larval dispersion. Despite to its reduced pelagic larval stage (18-27 days), A. saxatilis shows homogeneous populations through Caribbean because its post larval, pelagic stage, may extend up to 55 days (Shulman & Bermingham 1995). It is known that modifications in body shape of populations and species usually reflect an association of environmental conditions and adaptive genetic changes (Shaklee, 1984; Lessios et Figure 1. Map of the sampling locations. (1) Ceará, (2) Rio al. 1995). Considering the current assumption of a Grande do Norte, (3) Atol das Rocas, (4) St Paul’s Rocks, (5) single large A. saxatilis population in the Atlantic Ilha de Tinhare, Bahia, (6) Bombinhas, Santa Catarina. Ocean, the present study aimed to compare geographically distant samples from the Brazilian Twenty-two quantitative traits were coast and oceanic islands. We used principal measured for each specimen. The following components and canonical variables to analyze morphological measurements of the distances of meristic and multivariate morphometry data in order landmarks (Fig. 2) in the comparative analysis of to identify possible morphological variations Abudefduf saxatilis populations were used: 1. Pre- dorsal distance, 2. Dorsal pectoral distance,

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56 Multivariate morphological analyses in Abudefduf saxatilis. 51

Table I. Variation in meristic traits among Abudefduf saxatilis populations on the coast and oceanic islands of Western Atlantic. Dorsal rays Pectoral rays Anal rays Lateral line scales Area N min/ Mode min/ min/ min/ Mean Mode Mean Mode Mean Mode Mean max max max max 14 19 13 22 Atol das Rocas 16 14-15 14.1 19 19.0 13-14 13.2 21-22 21.6 (87%) (100%) (75%) (56%) St Paul’s 13 19 13 21 11 13-14 13.4 18-19 18.7 12-14 12.8 21-22 21.4 Rocks (63%) (72%) (63%) (63%) 13 19 12 21 Ceará 09 13 13.0 18-19 18.9 11-13 12.1 21-22 21.4 (100%) (89%) (66%) (55%) R.io Grande do 13 18-19 12 21 17 13-14 13.0 17-19 18.2 12 12.0 21-22 21.4 Norte (94%) (94%) (100%) (58%) 13 19 12 21 Bahia 13 13-14 13.1 18-19 18.8 11-13 12.3 21-22 21.2 (92%) (77%) (54%) (77%) 13 17 12 21 Santa Catarina 10 12-13 12.9 16-18 17.3 12-14 12.5 21-22 21.5 (90%) (50%) (60%) (50%)

3. Pectoral ventral distance, 4. Ventral-anal distance, to upper tail base distance, 19. Distance anal fin to 5. Pectoral anal distance, 6. Diagonal between the 1st lower base of the tail, 20. Diagonal from the last ray ray on the dorsal fin and 1st ray on the anal fin, 7. of the anal fin to the upper base of the tail, 21. Diagonal between the pectoral fin and the last ray on Height of the tail peduncle, 22. Interorbital distance. the dorsal fin, 8. Diagonal of the 1st ray of the anal Body shapes were studied by morphometric fin to the start of the 3rd lateral bar, 9. Distance analysis of the canonical variables independent of between the 1st ray of the dorsal fin to the start of the size (Reis et al. 1990). This analysis allows 3rd lateral bar, 10. Length of the 1st ray of the anal visualization of morphological similarities among fin, 11. Distance between the start of the 3rd lateral individuals by projecting individual scores on bar and the last dorsal fin ray, 12. Diagonal between canonical axes of a bidimensional graph. It also st the 1 anal ray to the last dorsal ray, 13. Length from allows discrimination of traits obtained for each the base of the dorsal fin, 14. Diagonal between the group of individuals and related to collection points. st 1 ray of the dorsal fin to the last anal ray, 15. Principal components analysis (PCA) (Morrison Length of the base of the anal fin, 16. Diagonal 1976) was used to identify shape and size variation between the last ray of the dorsal fin to the last ray among A. saxatilis individuals (n=76, using the of the anal fin, 17. Diagonal from the last ray of the SAS®-PC (SAS Institute In. 1988) statistical dorsal fin to the lower base of the tail, 18. Dorsal fin program. Meristic counts of the soft ray of dorsal, pectoral and anal fins, and lateral line scales were obtained for all samples. The geographic sites and analyzed individuals per sample are showed in the Table I.

Results Meristic characters There were indications of a clinal reduction in number of segments across the north-south direction along the Brazilian coast (Table I). Atol das Rocas samples showed highest values for almost all traits analyzed, including samples from St Paul’s Rocks, located further north. Clinal values were

Figure 2. Abudefduf saxatilis (Linnaeus, 1758) specimen. more evident through analyses of structures means. Landmarks used in this study (1-11 and interorbital distance - The lowest counts were detected at Bombinhas IOD). (1) snout, (2) anterior base of dorsal fin. (3) anterior base (Santa Catarina state) in the southern portion of the of pectoral fin (leading edge). (4) anterior base of pelvic fin. (5) Brazilian coast. Number of lateral line scales hardly anterior base of anal fin. (6) length of first anal ray. (7) upper edge of third lateral strip. (8) posterior base of dorsal fin. (9) varied among samples analyzed. However, a higher posterior base of anal fin. (10) ventral base of caudal fin. (11) modal value was observed in the Atol das Rocas dorsal base of caudal fin. Scale bars = 5 cm. samples.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56 52 W. F. MOLINA ET AL.

Table II. Coefficients of variables on the first (PC1) negative values showing interaction between shape and second (PC2) principal component of traits and size. The dispersion scores graphic of canonical studied in the Abudefduf saxatilis populations. variable CV1, CV2 and CV3, plotted in bidimensional space, indicate that point distances are Character PC1 PC2 proportional to dissimilarity degree among L1 0.2002 -0.0457 populations. The most important morphometric traits L2 0.2175 0.0898 in the discrimination of each variable (p = 0.001) L3 0.2404 0.0372 were the measurements 10, 7, 3 and 21 for the L4 0.2159 -0.3635 negative side of the first axis. In contrast, variables L5 0.2313 -0.3458 that most influenced the discrimination on the L6 0.2285 0.0084 second axis were 7, 5, 14 and 11 on the positive side L7 0.2188 -0.1659 and 22, 12, 2 and 21 on the negative side. L8 0.2272 0.0380 L9 0.2259 -0.0229 L10 0.1755 0.4615 L11 0.2198 -0.2884 L12 0.2147 0.0941 L13 0.2217 -0.0466 L14 0.2210 -0.0450. L15 0.2128 0.1860 L16 0.2151 0.0039 L17 0.2007 0.0251 L18 0.1833 0.1429 L19 0.1751 -0.2299 L20 0.1973 -0.0754 L21 0.2159 0.1085 L22 0.2161 0.5212 % variation 98.78 0.2100

Principal Component Analysis (PCA) Two eigenvectors extracted from the variance-covariance matrix accounted for 98.78% and 0.21% of the observed variation, respectively (Table II). All coefficients of the first eigenvector Figure 3. Dispersion diagram of individual scores in different were positive, suggesting it may be interpreted as a Abudefduf saxatilis populations in the space defined by PC1 and multivariate measurement of size. The second PC2. (a) Rio Grande do Norte, (b) Santa Catarina, (c) St Paul’s Rocks (d) Atol das Rocas, (e) Ceará and (f) Bahia. eigenvector had positive and negative values and could be interpreted as a shape axis. Similarly to PCA, the diagram of canonical Individual scores of A. saxatilis populations variable 1 (CV1) and canonical variable 2 (CV2) plotted in PC1 and PC2 space (Fig. 3) revealed an (Fig. 4) showed that A. saxatilis from Ceará state extensive overlap among samples distributed on PC2 was different from other samples. Dispersion of axis. There were no precise differentiations among individual scores demonstrated overlapping among island and continental samples, but samples from samples of Bahia and Atol das Rocas, forming a Atol das Rocas and St Paul’s Rocks could be distinct cluster in the second canonical axis discriminated from each other. Also, samples from compared to one composed by St Paul’s Rocks, Atol das Rocas and Santa Catarina differentiated in Santa Catarina and Rio Grande do Norte samples. form. Individuals from Ceará formed a well defined This analysis showed that samples from both group by PC1, possibly reflecting the lower sizes of oceanic islands were different in shape and size. these individuals. Scores plotted in CV1 and CV3 spaces (Fig. 5) discriminated island samples from those of continent Canonical Variables Analysis (CVA) along CV3 axis. Continental samples showed greater Canonical variables 1, 2 and 3 explained overlapping, except for Ceará samples, which 51.41%, 25.43% and 11.73% of the observed formed an isolated cluster along CV1. Specimens variation, respectively. Both axes had positive and from Atol das Rocas and St Paul’s Rocks were also

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56 Multivariate morphological analyses in Abudefduf saxatilis. 53 discriminated between each other by the size Discussion component. Occurrence of physical barriers among marine fish populations is not always clear (Joyeux et al. 2001). However, geographic and/or ecological subdivisions allow the establishment of population’s traits representing suitable models for biogeographic, taxonomic, ecological and genetic studies. In such cases, morphometric analyses can produce valuable information about phenotypic plasticity of species and possible effects of genetic changes on morphological variation (Hauser et al. 1995). Abudefduf saxatilis populations along South America coast showed a clinal gradient in the north- south direction in relation to their meristic variables. Temperature may be a decisive factor explaining regional differences among these samples and it is not uncommon for meristic traits to have lower number of segments in colder waters at the southern coast, when compared to northern warmer waters. Usually, parameters delaying ontogenetic development, such as hypoxia, low temperatures, high salinity and reduced food sources, favor the development of greater number of body segments (Barlow 1961; Shaklee & Tamaru 1981). Notably, Figure 4. Dispersion of individual scores of Abudefduf saxatilis Atol das Rocas population had highest counts even populations in the space defined by CV1 and CV2. (a) Rio compared with St Paul’s Rocks located at the limit Grande do Norte, (b) Santa Catarina, (c) St Paul’s Rocks, (d) of the equatorial line. Higher mean temperatures in Atol das Rocas, (e) Ceará and (f) Bahia. shallower waters of Atol das Rocas than those of St Paul’s Rocks (environmental factor) or differences in the genetic pool of these populations (genetic factor) could account for this discrepancy. In some cases, although temperature and salinity influenced some species regarding numbers of fins’ rays, certain structures are not modified by different environmental conditions, suggesting a major genetic control in the establishment of serial elements (Barlow 1961). Among various characteristics identified in species with wide geographic distribution, size is the most frequently observed. In Pomacentridae, clinal variations in color have been shown and it is related to the great variety of pigmentation patterns in this species (Doherty et al. 1994). Genetic analyses, carried out in populations with pigment variation, have shown divergences (Amphiprion clarkii, Bell et al. 1982, Acanthochromis polyacanthus, Planes & Doherty 1997) or even the existence of cryptic species in this group (Chrysiptera cyanea, Lacson 1994, Stegastes nigricans and Chrysiptera glauca, Lacson & Clark 1995). However, the level of Figure 5. Dispersion of individual scores of Abudefduf saxatilis genetic intraspecific variability is compatible with populations in the space defined by CV1 and CV3. (a) Rio Grande do Norte, (b) Santa Catarina, (c) St Paul’s Rocks, (d) the one observed in species with no color variations Atol das Rocas, (e) Ceará and (f) Bahia. (Lacson & Clark 1995). Although data suggesting

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56 54 W. F. MOLINA ET AL. between-populations, morphological and genetic similar tendency, with both clusters being clearly differences are not necessarily correlated (Gorman & defined. This pattern could be explained by Kim 1977, Bell et al. 1982), genetic polymorphisms dispersive events caused by the Equatorial South detected by RAPD (Random Amplification of Current that comes from East Atlantic, passes by St Polymorphic DNA) markers or alozymes are Paul’s Rocks and Atol das Rocas and divides at Rio associated with pronounced among-population Grande do Norte coast, with one branch following morphometric variations in some marine species the north coast as the Guyana Current and the other (Dahle et al. 1997; Mamuris et al. 1998). Thus, flowing south as the Brazil Current. The South morphometric analyses can provide real data on Equatorial Current seems to provide a contact zone species plasticity and possible effects of genetic among oceanic populations of the Atol das Rocas, changes on morphological traits. and the populations of Ceará (north coast) and Lessios et al. (1995) identified particular Bahia. Positioned between these two resulting color patterns, in the lower suborbital margin (scale currents, Rio Grande do Norte population has lower presence or absence) and in the pre-opercule, contact with these neighboring areas. between Abudefduf concolor from eastern Pacific Abudefduf saxatilis population at St Paul’s coast and A. declivifrons from Atlantic Ocean. Body Rocks, because of its distance from the South depth, snout length and caudal peduncle depth play a American coast, seems to form an isolated and self- discriminatory role among these species. These data, maintaining population. The discontinuity caused by together with molecular differences in mtDNA and oceanic isolation was evident when canonical isoenzymes, confirmed they are distinct species. In variables 1 and 2 were analyzed. Two clusters, spite of separation estimative of ca. 14 to 15 million diverging for shape, were discriminated; one oceanic years, they still show similar phenotypic representing Atol das Rocas and St Paul’s Rocks characteristics. Long periods of time, in some cases, populations and another clustering coastal seem to be insufficient to overcome a conservative populations. situation in the morphotype of certain species. Thus, Isolated A. saxatilis populations collected on isoenzymatic markers and multivariate Ascension Island, southeast of St Paul’s Rocks in the morphometric analyses were able to discriminate mid Atlantic, showed mtDNA pattern different from two sympatric and cryptic species of the Albula those of Western Atlantic (Bermingham et al. 1997), genus in Hawaii waters. Even though they diverged also suggesting a probable genetic component around 20 to 30 million years ago, these two species associated to the morphological differences observed seem to have extremely conservative morphology in the geographical isolated St Paul’s Rocks and (Shaklee & Tamaru 1981). Atol das Rocas populations. Abudefduf saxatilis populations showed little Morphological and genetic differences in morphological discrimination when analyzed by island populations arise from the impediment to principal components analysis. This methodology is genetic flow, caused by closed circulation currents appropriated to access the morphological variability in the reproduction areas where eggs and larvae tend in shape and size in different populations. Much of to remain within their area of influence with few the variation observed could be associated to a size possibilities to disperse and to establish contact with component. However, the analysis showed good populations from other areas. Clustering of coastal discrimination for shape between Atol das Rocas populations in one group on PC1 and PC3 seems to (270 km from the coast) and St Paul’s Rocks (960 suggest an unidirectional dispersion system among km from the coast) populations. Atol das Rocas was them, capable of showing shared similarities. also divergent in size and shape from Santa Catarina However, they had sufficient peculiar characteristics coastal sample. These data agree with meristic to be distinguished by PC1 and PC2 axes. values showing that populations of these two The analyzed data indicated structuring of localities were markedly different. Ceará sample, morphologically distinct A. saxatilis populations in consisting of juvenile individuals, showed strong the Brazilian Province, whose effects were attributed discrimination in size. to dispersion by dominant currents (e.g., Briggs Canonical variable analysis showed 1974, Floeter et al. 2001). St Paul’s Rocks and Atol differentiation among populations in distinct das Rocas populations were differentiated locations. Canonical variables 1 and 2 showed morphologically in all performed analyses. greater body similarity among samples from Atol Our study provided the first investigation das Rocas, Bahia and Ceará compared to those from using methods of multivariate morphometry in St Paul’s Rocks, Rio Grande do Norte and Santa Atlantic populations of a reef fishes involving Catarina. Canonical variables 2 and 3 showed a distances over 5,000 km. Lower morphological

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56 Multivariate morphological analyses in Abudefduf saxatilis. 55 homogeneity than expected, emphasizes the Ferreira, C. E. L., Rangel, C. A. & Gasparini, importance of conservation of these populations, J. L. 2001. Geographic variation in reef-fish especially of the St Paul’s Rocks. These results, assemblages along the Brazilian coast. Global complemented by future genetic marker analyses, Ecology and Biogeography, 10: 423–431. could support effective conservation Pomacentridae Gasparini, J. L., Moura, R. L. & Sazima, I. 1999. species in South Atlantic. Stegastes trindadensis n. sp. (Pisces: Pomacentridae), a new damselfish from Acknowledgments Trindade Island, off Brazil. Boletim do The authors are grateful to P.R.A.M. Affonso for Museu Mello Leitão, 10, 3–11. sample collections of Rio de Janeiro and F. Hostim Gorman, G. C. & Kim, Y. J. 1977. Genotypic for collection of individuals in Santa Catarina coast. evolution in the face of phenotypic This research received funding from CAPES conservativeness: Abudefduf (Pomacentridae) (fellowship to WFM), CNPq and institutional from the Atlantic and Pacific sides of Panama. support from UFRN and UFSCar. Copeia, 4: 694-697. Hauser, L., Carvalho, G. R. & Pitcher, T. J. 1995. References Morphological and genetic differentiation of Allen, G. R. 1975. Damselfishes of the South Seas. the African clupeid Limnothrissa miodon 34 T.F.H. Publications. Hong Kong, 237 p. years after its introduction to Lake Kivu. Allen, G.R. 1991. Damselfishes of the world. Journal of Fish Biology, 47:127-144. Mergus Publishers, Melle, 271 p. Joyeux, J. C., Floeter, S. R., Ferreira, C. E. .L. & Barlow, G.W. 1961. Causes and significance of Gasparini, J. L. 2001. Biogeography of morphological variation in fishes. Systematic tropical reef fish: the South Atlantic puzzle. Zoology, 10: 105-117. Journal of Biogeography, 28, 831–841. Bell, L. J., Moyer, J. T. & Numachi, K. 1982. Lacson, J. M. & Clark, S. 1995. Genetic divergence Morphological and genetic variation in of Maldivian and Micronesian demes of the Japanese populations of the anemonefish damselfishes Stegastes nigricans, Chrysiptera Amphiprion clarkii. Marine Biology, 72: 99- biocellata, C. glauca and C. leucopoma 108. (Pomacentridae). Marine Biology, 121: 585- Bermingham, E., Mccafferty, S. S. & Martin, A. P. 590. 1997. Fish biogeography and molecular Lacson, J. M. 1994. Fixed allele frequency clocks: perspectives from the Panamian differences among Palauan and Okinawan Isthmus. p. 113-126. In: Kocher, T. D. & populations of the damselfishes Chrysiptera Stepien, C. A. (Eds.). Molecular Systematics cyanea and Pomacentrus coelestis. Marine of Fishes, Academic Press, New York, 314 p. Biology, 118: 359-365. Briggs, J. C. 1974. Marine Zoogeography. Lessios, H. A., Allen, G. R., Wellington G. M. & McGraw-Hill Book Co., New York, 475 p. Bermingham, E. 1995. Genetic and Dahle, G., Rahman, M. & Eriksen, A. G. 1997. morphological evidence that the eastern RAPD fingerprinting used for discriminating Pacific damselfish Abudefduf declivifrons is among three populations of Hilsa shad distinct from A. concolor (Pomacentridae). (Tenualosa ilisha). Fisheries Research, 32: Copeia, 2: 277-288. 263-269. Mamuris, Z., Apostolidis, A. P., Theodorou, A. J. & Doherty, P. J., Mather, P. & Planes, S. 1994. Triantaphyllidis, C. 1998. Application of Acanthochromis polyacanthus, a fish lacking random amplified polymorphic DNA (RAPD) larval dispersal, has genetically differenciated markers to evaluate intraspecific genetic populations at local and regional scales on the variation in red mullet (Mullus barbatus). Great Barrier Reef. Marine Biology, 121: 11- Marine Biology, 132: 171-178. 21. Menezes, N. A. & Figueiredo, J. L. 1985. Manual Edwards, A. & Lubbock, R. 1983. Marine de Peixes Marinhos do Sudeste do Brasil. Zoogeography of St Paul’s Rocks. Journal of V. Teleostei (4). São Paulo, Museu de Biogeography, 10: 65-72. Zoologia, Universidade de São Paulo. Emery, A. R. 1972. A new species of damselfish Morrison, D. F. 1976. Multivariate statistical (Pisces: Pomacentridae) from the Eastern methods. New York, McGraw Hill. Coast of South America. Copeia, 2: 330-335. Novelli, R., Nunan, G. W., Lima, N. R. W. 2000. A Floeter, S. R., Guimarães, R. Z. P., Rocha, L. A., new species of Damselfish genus Stegastes

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Jenyns, 1842 (Teleostei: Pomacentridae) from fasciolatus throughout the Hawaiian the coast of Brazil. Boletim de Museu archipelago. Copeia, 629-640. Nacional, Nova Série Zoologia, 413: 1-12. Shaklee, J. B. & Tamaru, C. S. 1981. Biochemical Planes, S. & Doherty, P. J. 1997. Genetic and color and morphological evolution of Hawaiian interactions at a contact zone of bonefishes (Albula). Systematic Zoologic, 30: Acanthochromis polyacanthus: a marine fish 125-146. lacking pelagic larvae. Evolution, 51: 1232- Shulman, M. A. & Bermingham, E. 1995. Early life 1243. histories, ocean currents, and the population Reese, E. S. 1973. Duration of residence by coral genetics of Caribbean reef fishes. Evolution, reef fishes on “home” reefs. Copeia, 1: 145- 49: 897-910. 149. Strauss, R. E. & Bookstein, F. L. 1982. The truss: Reis, S. F., Pessoa L. M. & Strauss, R. E. 1990. body form reconstructions in morphometrics. Application of size-free canonical Systematic Zoologic, 31: 113-135. discriminant analysis to studies of geographic differentiation. Revista Brasileira de Genética, 13: 509-520. SAS. 1988. Sas/Stat User’s guide, Release 6.03. SAS Institute Inc, Cary, NC. Shaklee, J.B. 1984. Genetic variation and population structure in the damselfish Stegastes

Received March 2006 Accepted June 2006 Published online June 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 49-56

Impacto potencial de invasión de Ficopomatus enigmaticus (Fauvel) (Polychaeta: Serpulidae) en la Laguna de Rocha, Uruguay

1 1 1 ANA INES BORTHAGARAY , JUAN M. CLEMENTE , LUCÍA BOCCARDI , 1 1,2 ERNESTO BRUGNOLI & PABLO MUNIZ

1 Departamento de Ecologia, Facultad de Ciencias, Iguá 4225, C.P.11.40, Montevideo, Uruguay. 2 Autor para correspondencia: Pablo Muniz. E-mail: [email protected]

Abstract. Potential impact of Ficopomatus enigmaticus (Fauvel) (Polychaeta: Serpulidae) invasion in Laguna de Rocha, Uruguay. The aim of this work is to assess the invasion risk and the potential impact of the exotic Ficopomatus enigmaticus on the benthic community structure of the northern zone of Laguna de Rocha. These evaluations were done considering the similar environmental and biological characteristics of this lagoon and other coastal systems on the Atlantic coast (Laguna Garzón and Arroyo Valizas) and the Río de la Plata (Bahia de Montevideo and Arroyo Solís Grande) that had been infected by this species. In Laguna de Mar Chiquita (Argentina), the most well studied ecosystem affected by this polychaete, the presence of F. enigmaticus has substantially modified the landscape, promoting serious ecological alterations. The environmental and benthic community characteristics of Laguna de Rocha are favourable to the settlement of the species; therefore, we can consider this lagoon as a potential reception ecosystem for the invasive pest F. enigmaticus. Because of the similarity between Rocha and Mar Chiquita lagoons, it is possible to predict the potential impact that a F. enigmaticus invasion could cause in Laguna de Rocha. Studies to achieve basic knowledge about the distribution and behaviour of this species in Laguna de Rocha are important to determine the level of biological contamination in this aquatic environment. The results of this study are required for the development of management and control strategies of the invasion process of this species and will contribute to the conservation of the aquatic biodiversity of Laguna de Rocha.

Key-word: biological contamination, invasive species, benthos, coastal lagoon.

Resumen. El objetivo de este trabajo es evaluar cualitativamente el riesgo de invasión y el impacto potencial de la especie exótica Ficopomatus enigmaticus en la estructura de la comunidad bentónica en la zona norte de la Laguna de Rocha. Esto se discute en base a la similitud de condiciones físicas y biológicas de esta laguna con otros sistemas costeros, sobre la costa atlántica (Laguna Garzón y Arroyo Valizas) y del Río de la Plata (Bahia de Montevideo, Arroyo Solís Grande) ya infectados por la especie. En la laguna costera de Mar Chiquita (Argentina) la presencia de Ficopomatus enigmaticus ha modificado notoriamente el paisaje del área, ocasionando serias alteraciones ecológicas. En un primer análisis, la Laguna de Rocha puede considerarse un ecosistema potencialmente receptor para el poliqueto invasor F. enigmaticus. Esta afirmación se sustenta en base a las condiciones físicas y biológicas que presenta este cuerpo de agua, las cuales son favorables para el asentamiento de la especie. Dada la similitud de características físicas y biológicas (comunidad bentónica) que presentan la Laguna de Rocha y la Laguna de Mar Chiquita (Argentina) se podría predecir el impacto esperado sobre la Laguna de Rocha. El desarrollo de estudios dirigidos a la generación de información básica sobre la distribución y comportamiento de esta especie en la Laguna de Rocha es importante para determinar el estado de contaminación biólogica en este sistema. Esto permitirá realizar un plan de manejo y control de este poliqueto invasor, y contribuir a la conservación de la biodiversidad acuática nativa de la Laguna de Rocha.

Palabras clave: contaminación biológica, especie invasora, bentos, laguna costera.

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 57-65

58 A. I. BORTHAGARAY ET AL

Introducción diferentes niveles de organización biológica La modificación o destrucción del hábitat a causa de (individuo, población, comunidad) (Ricciardi 2003). la introducción de especies exóticas es considerado Por lo tanto, conocida la historia de invasión de una una de los principales factores responsable de la especie y los sitios ya invadidos, sería posible pérdida de biodiversidad de los sistemas naturales identificar un patrón de impacto de la especie (Bertness 1984, Simberlof 1997). En tal sentido, el invasora y así predecir el potencial efecto de la resultado final y más dramático de la interacción invasión sobre la comunidad receptora. Sin entre una especie nativa y otra exótica (ej. embargo, se debe tener en cuenta que el competencia, depredación) es la extinción de la comportamiento de una especie en un sistema dado primera. Como consecuencia de ello, la distribución no es necesariamente el mismo que en otro sistema. y abundancia de la especie nativa así como su En Uruguay, hasta la fecha fueron composición y dinámica se ven modificadas reportadas 12 especies acuáticas exóticas (Stachowicz et al. 2002). introducidas accidentalmente (Brugnoli et al. en La gran mayoría de los ecosistemas prensa), incrementándose los reportes en los últimos terrestres, marinos y continentales han sufrido las años. En particular, varias especies bentónicas consecuencias de las invasiones biológicas introducidas accidentalmente han colonizado (Williamson 1996, Parker et al. 1999). exitosamente los ecosistemas alcanzados, Aproximadamente 102 - 104 especies exóticas han evidenciándose una rápida expansión de sus áreas sido documentadas (Ricciardi & Rasmussen 1998), de distribución (Brugnoli et al. 2005). Entre ellas, el pero este número se incrementa con el tiempo como poliqueto Ficopomatus engimaticus (Fauvel 1923) consecuencia del intenso tráfico de fauna y flora de fue citado por primera vez para Uruguay (y una región geográfica a otra. En tal sentido, el agua Atlántico Sudoccidental) en 1938 en el Arroyo Las de lastre y el transporte de sedimentos son los Brujas (San José) (Monro 1938). Si bien es aceptado principales vectores de dispersión de especies que esta especie es endémica del Hemisferio Sur exóticas acuáticas (Carlton & Geller 1993, Ruiz et (Eno et al. 1997), existe controversia respecto de su al. 2000). área de origen. Se encuentra en regiones templadas, Una vez que la especie potencialmente en cuerpos de agua salobres con salinidad variable, invasora ingresa en la nueva región (área receptora), en zonas de escasa profundidad y baja velocidad de la probabilidad de un sistema de ser infectado corriente (Obenat 2001). Este poliqueto, considerado dependerá de las condiciones locales físico-químicas exótico para nuestra región, pertenece a la familia y ecológicas, así como de las características Serpulidae y es constructor de tubos calcáreos, los biológicas de la especie invasora. La invasibilidad que conforman extensas estructuras arrecifales. de un sistema, es decir, la susceptibilidad del Hasta la fecha, este poliqueto fue observado en ambiente a ser invadido, es una propiedad emergente varios sistemas sobre la costa Atlántica y del Río de de la comunidad receptora. Diferentes hipótesis la Plata (Monro 1938, Rioja 1943, Scarabino et al. asociadas a disturbios (Crawley 1987), diversidad de 1975, Nión 1979, Muniz & Venturini 2001, especies (Elton 1958, Tilman 1997), productividad Orensanz et al. 2002). Sin embargo, el tamaño de las comunitaria (Tilman 1993) y fluctuaciones en la estructuras arrecifales observadas en Uruguay no disponibilidad de recursos (Davis et al. 2000) son parecerían ser de dimensiones tan importantes como propuestas para explicar la invasibilidad de un nuevo las encontradas en otras áreas de la región (ej. sistema (Davis & Pelsor 2001). Entre los Laguna de Mar Chiquita, Argentina; Schwindt ecosistemas acuáticos, y según su estado de impacto, 2001). Diversas explicaciones asociadas a existen diferentes grados de susceptibilidad a la condiciones físico-químicas (ej. salinidad, llegada de organismos exóticos. Los ambientes temperatura, nutrientes, velocidad de corriente) o marinos pelágicos presentan una susceptibilidad factores ecológicos (ej. competencia, depredación, menor que ambientes como ríos, lagos y zonas disponibilidad de recursos) podrían explicar la no costeras, que son especialmente vulnerables a este expansión de este poliqueto en los sistemas de fenómeno (Perrings 2002). Uruguay donde ya ha sido identificado. A pesar de El impacto provocado será función de la ello, F. enigmaticus permanece latente en estos interacción entre la especie invasora y su nuevo sitios, como especie exótica, por lo que podría ambiente (Ricciardi 2003). De este modo, la presentar una explosión poblacional. Además, las identificación de patrones de invasión a partir de áreas afectadas serían potenciales donadoras para la sitios ya infectados permitirán predecir el impacto de infección de nuevos sistemas. En la región, en una especie invasora en un nuevo sistema sobre los particular en Argentina en la Laguna de Mar Chiquita, la presencia de F. enigmaticus ha

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 57-65 Impacto potencial de invasión de Ficopomatus enigmaticus 59 modificado notoriamente el paisaje del área, nacionales (Decreto 693 de 1987) y por acuerdos ocasionando problemas ecológicos (ej. modificación internacionales (Convención de Bonn/Ley 16062 de de las interacciones intra e interespecíficas) y afecta 1989), albergan comunidades de peces y anfibios la navegación dentro de la laguna (Schwindt & endémicos de la región y una importante riqueza de Iribarne 2000, Schwindt 2001, Schwindt et al. 2001, flora. Estas lagunas fueron declaradas Áreas Luppi et al. 2002). Naturales Protegidas por decretos y leyes nacionales Recientemente, F. enigmaticus fue (Reserva de Fauna Laguna de Castillos - Decreto observado en la zona norte de la Laguna de Rocha. 266/66 y Parque Nacional Lacustre y Área de Uso En particular, se ha registrado la presencia de tubos Múltiple Lagunas de Rocha, José Ignacio y Garzón calcáreos de este poliqueto, pero no se han - Decreto 260/77) y por la suscripción de Uruguay a observado estructuras arrecifales (Clemente obs. convenciones internacionales (sitio Ramsar desde la per.). Sin embargo, dada la similitud de Laguna Merín hasta la Laguna de Castillos - Ley características físicas y biológicas (comunidad 15.337 y Reserva de Biosfera desde la Laguna de bentónica) que presenta la Laguna de Rocha y la Rocha a la Merín – MaB UNESCO) (Conde et al. Laguna de Mar Chiquita (Argentina) se podría 2003). predecir el impacto esperado sobre la Laguna de Entre estas, la Laguna de Rocha (Fig. 1) se Rocha. Por tro lado, la presencia de F. enigmaticus conecta periódicamente con el mar a través de una en la laguna representa una señal de alerta para la barra de arena y alberga una gran diversidad de conservación de la fauna de este sistema Reserva de invertebrados (Giménez et al. 2006, Pintos et al. la Biosfera, por lo cual sería de gran relevancia la 1991), peces (Pintos et al. 1988) y aves (Pintos et al. identificación de los potenciales ecosistemas 1988). Es un sitio clave para el ciclo de vida de donantes. peces costeros (Pogonias chromis, Paralichtys sp.), El objetivo del presente trabajo es evaluar crustáceos como el camarón (Farfantepenaeus cualitativamente el riesgo de invasión y el potencial paulensis) y el cangrejo azul (Callinectes sapidus). impacto de la presencia de Ficopomatus enigmaticus La laguna ha sido recientemente indicado como un en la estructura de la comunidad bentónica en la importante sitio de reproducción para la corvina zona norte de la Laguna de Rocha. Esto se discute en blanca (Micropogonias furnieri), el segundo recurso base a la similitud de condiciones físicas y pesquero del país (Conde et al. 2003). biológicas de la Laguna de Rocha con otros sistemas, potenciales zonas fuentes, ya infectados por la especie. El conocimiento del estado de infección de este ecosistema, Reserva de la Biosfera MaB UNESCO, contribuiría al desarrollo de un plan de manejo con el fin de amortiguar los efectos ya observados en otros ecosistemas.

Materiales y metodos Arroyo Valizas

Laguna Área de estudio Bahia de de Rocha Laguna Montevideo La costa atlántica uruguaya presenta una Garzon Arroyo Solis extensión de 220 km a lo largo de la cual se Grande distribuyen una serie de lagunas costeras. Las Figura 1. Costa atlántica y del Rio de la Plata de Uruguay lagunas situadas en esta zona son ecosistemas mostrando los potenciales sitios donadores para la Laguna de salobres que se continúan hacia el norte por la costa Rocha. brasilera. Son sistemas someros, ecológicamente complejos y muy productivos. Sus cuencas cumplen Riesgo de invasión e impacto ecológico potencial un importante rol hidrológico, recolectando agua en Un primer paso en la predicción de las sierras, distribuyéndola a través de un complejo invasiones biológicas es la identificación de sistema de cursos de agua y humedales, recargando potenciales regiones geográficas donadoras acuíferos, abasteciendo de agua durante sequías, (Ricciardi & Rasmussen 1998). La mayoría de las atenuando las inundaciones durante las épocas invasiones exitosas provienen de latitudes similares lluviosas y manteniendo el funcionamiento de (Carlton 1985). De este modo, la invasión podrá diversos ecosistemas (Conde & Rodríguez-Gallego iniciarse a partir de áreas donde la especie es nativa 2002). Representan áreas de cría de aves acuáticas o desde sistemas ya invadidos. residentes y migratorias protegidas por decretos La existencia de corredores de dispersión

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 57-65 60 A. I. BORTHAGARAY ET AL entre la región donadora y el área receptora podrían Tabla I. Algunas características abióticas de las aumentar la probabilidad de futuras invasiones. En potenciales zonas donadoras. S: rango de salinidad; el caso de la Laguna de Rocha, todas las áreas T: rango de temperatura; Z: profundidad media. potenciales donadoras se encuentran en el Río de la S (ups) T (°C) Z (m) Plata o el Océano Atlántico, incluida la Laguna de 1 * Mar Chiquita. En este sentido, las fluctuaciones de Bahía de Montevideo 0.5 – 25 12 – 24 3 la salinidad favorecerían la colonización, ya que esta Arroyo Solís Grande 2 2.6 – 32 18 – 23 (nd) especie está bien adaptada a la vida en aguas Laguna Garzón 3 7 - 20 23 - 28 0.5 salobres con salinidad variable aún en su fase (verano) planctónica (Obenat 2001). El vector de dispersión Arroyo Valizas 4 2.1 – 31.9 8 – 24.3 1.9 entre la Laguna de Rocha y los sistemas infectados 1 Muniz et al. 2004; 2 Muniz & Venturini 2001; 3 Conde estaría asociado principalmente al tráfico de barcos (promedio de dos veranos (2004-2005) datos no publicados); 4 deportivos, de pesca artesanal u otras estructuras Nion 1979. * Muniz com pers. nd (dato no disponible). donde F. enigmaticus podría ser transportado, o incluso a través de aves, ya que varios de los sitios Tabla II. Composición de las comunidades donadores son áreas de cría y/o alimentación de aves bentónicas en las potenciales zonas donadoras en que se desplazan localmente entre estos ambientes. relación a los principales representantes del El impacto potencial de F. enigmaticus en la macrozoobentos de la Laguna de Rocha (zona Laguna de Rocha es evaluado a través de las norte). Em: Erodona mactroides; Tp: Tagelus similitudes que ésta presenta con la Laguna de Mar plebeius; Ha: Heleobia australis; Np: Nephtys Chiquita. En tal sentido, estos sistemas presentan fluviatilis; Lc: Laeonereis culvieri; Hs: ciertas condiciones físicas y biológicas similares, lo Heteromastus similis; Cg: Chasmagnatus granulata; que permite hipotetizar comportamientos similares o Ca: Cyrtograpsus angulatus. comparables en cuanto a la respuesta del sistema Em Tp Ha Np Lc Hs Cg Ca frente a la invasión del poliqueto Ficopomatus Bahía de * * * enigmaticus. Montevideo1 Arroyo Solís 2 * * * * * * Resultados y discusión Grande Laguna * * * * * * Garzón3 Identificación de potenciales zonas donadoras de Arroyo * * * * F. enigmaticus para la Laguna de Rocha Valizas4 Carlton (1996) denomina región donadora (o Laguna * * * * * * * * fuente) a aquellos sitios donde una especie exótica Rocha5 tiene contacto con un mecanismo de transporte, 1 Venturini et al. 2004; 2 Muniz & Venturini 2001; 3 Giménez et mientras que regiones receptoras son sitios en los al. 2003; 4 Nion 1978; 5 Pintos et al. 1991. que la especie exótica es inicialmente liberada y luego se establece. Por otro lado, la similitud en Plata (isóbata de 5 m, “Barra del Indio”) (Nagy et al. condiciones físico-químicas y biológicas entre 1987). En la zona interna de la Bahía de potenciales zonas donadoras y zonas receptoras Montevideo, F. enigmaticus fue observada en las podría incrementar aun más la probabilidad de tuberías de enfriamiento de la refinería de ANCAP contagio entre ambas. En tal sentido, basado en (Boccardi & Clemente datos no publicados) y en la características físicas (Tabla I) y composición de la desembocadura del Arroyo Pantanoso (Scarabino et comunidad bentónica (Tabla II), se identificaron al. 1975). Cabe destacar que la Bahía de diferentes zonas potencialmente donadoras de F. Montevideo, y en particular su zona interna, donde enigmaticus en la costa atlántica y Río de la Plata fue encontrado F. enigmaticus, es un sitio altamente para la Laguna de Rocha: Bahía de Montevideo contaminado (Muniz et al. 2004), que lo haría más (zona interna), Arroyo Solís Grande y Laguna sensible al establecimiento de especies exóticas. Si Garzón, ubicados a 180, 105 y 30 kilómetros bien nunca fue cuantificado, probablemente las respectivamente al oeste de Laguna de Rocha, y el estructuras arrecifales observadas de ANCAP sean Arroyo Valizas, ubicado a 60 kilómetros al este de la las de mayor tamaño en Uruguay (Muniz et al. misma. 2005a). La Bahía de Montevideo se encuentra en la El Arroyo Solís Grande es un sistema zona fluvio-marina del Río de la Plata, donde se conectado con la zona fluvio-marina del Río de la ubica el frente de turbidez y salino del Río de la Plata a través de una barra arenosa que se abre periódicamente. Como consecuencia de ello, las

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 57-65 Impacto potencial de invasión de Ficopomatus enigmaticus 61 condiciones hidrodinámicas locales generan un de bivalvos. Todos los sitios potencialmente gradiente salino creciente hacia la desembocadura, donantes se comportan como sub-estuarios (Bahía que junto con las características granulométricas de Montevideo y Arroyo Solís Grande) o estuarios (sedimento areno-fangoso) determinan la (Laguna Garzón y Arroyo Valizas) (Giménez et al. composición y distribución de la comunidad 2005), son sistemas poco profundos (Tabla I) y de bentónica (Muniz & Venturini 2001) (Tabla II). En aguas salobres, conectados con el Río de la Plata u el año 1995, F. enigmaticus fue encontrado a 5 km el Océano Atlántico. En ninguna de las potenciales de la desembocadura del Arroyo Solís Grande zonas donadoras antes mencionadas se habría (Muniz & Venturini 2001). En dicha zona, los registrado la presencia de importantes estructuras sedimentos predominantes fueron arena gruesa y arrecifales como las observadas en otros sistemas fango. Además, se observó gran abundancia de costeros de la región (ej. Laguna de Mar Chiquita). valvas de moluscos, especialmente de Erodona Sin embargo cabe destacar la disponibilidad de mactroides y Tagelus plebeius. Varios trabajos valvas de Erodona mactroides y Tagelus plebeius, señalan la importancia de la disponibilidad de estas sustrato adecuado para el asentamiento de las larvas conchillas como sustrato para el asentamiento de F. de F. enigmaticus, lo que posteriormente permitiría enigmaticus y la posterior formación de sus el desarrollo de las estructuras arrecifales. Estas estructuras arrecifales (Schwindt & Iribarne 2000, valvas también son observadas en la Laguna de Obenat 2001). Sin embargo, valvas de E. mactroides Rocha, aunque su abundancia no ha sido hasta el y T. plebeius también fueron observadas en otras momento cuantificada. La composición taxonómica zonas del Arroyo Solís Grande, próximas a donde de la comunidad bentónica indica una importante fue hallado F. enigmaticus, aunque en esa zona este similitud entre los diferentes sistemas fuente y la poliqueto no fue encontrado (Muniz & Venturini Laguna de Rocha. 2001). Contrariamente a lo observado en la Laguna de Mar Chiquita, en el Arroyo Solís Grande la Impacto potencial de la expansión de F. enigmaticus comunidad bentónica asociada a la presencia de este en la Laguna de Rocha poliqueto fue sumamente pobre y poco diversa Dada la similitud entre las características (Muniz & Venturini 2001, Muniz et al. 2005b). físicas y ecológicas que presenta la Laguna de Mar Recientemente, en 2004, F. enigmaticus fue también Chiquita (37º32’S–57º19’W), Argentina, con la observado aguas arriba a 10 km de la Laguna de Rocha (Tabla III), se supone que la desembocadura sobre canto rodado en las márgenes evolución del proceso de invasión en esta laguna del arroyo (Clemente & Borthagaray obs. per.). La podría ser comparable al ocurrido en aquella. Sin intrusión del Río de la Plata en el Arroyo Solís embargo, hasta la fecha ningún estudio se ha Grande podría haber conducido un pulso de larvas realizado con el fin de confrontar ambos sistemas. aguas más arriba, ampliando su rango de En Mar Chiquita, el poliqueto invasor F. distribución dentro de este sistema. En este caso, si enigmaticus fue introducido accidentalmente antes bien no fue cuantificada su abundancia, se del año 1964 (Schwindt 2001). La cobertura de observaron las estructuras arrecifales mencionadas arrecifes aumentó 24 % desde 1975 a 1999. Hasta el por otros autores pero de tamaños menores. año 1999, estos arrecifes ocupaban 86 % de la En la Laguna Garzón y en la zona media del superficie total de la laguna, con una densidad media Arroyo Valizas, sistemas someros conectados con el de 89 arrecifes por hectárea (Schwindt 2001, Océano Atlántico a través de una barra arenosa Schwindt et al. 2004a). Estas estructuras son de también de apertura periódica, fue registrada la forma circular de hasta 7 m de diámetro y 0.5 m de presencia de F. enigmaticus (Nion 1978, Orensanz et altura. En los últimos años el incremento del tamaño al. 2002). En la zona media del Arroyo Valizas el de los arrecifes ha llevado a la fusión de varios de sustrato está compuesto por sedimento areno- ellos, constituyendo extensas plataformas calcáreas fangoso y conchillas del bivalvo E. mactroides, de varios metros de longitud (Obenat 2001). Las mientras que la comunidad bentónica de ambos larvas de F. enigmaticus necesitan de sitios de sistemas esta formada por los mismos grupos asentamiento (núcleo) para comenzar la invasión del taxonómicos que la Laguna de Rocha (Tabla II) sistema. Luego comienzan a construir los tubos (Nión 1979, Giménez et al. 2003). calcáreos y estos mismos sirven como estructura de En síntesis, las características físicas asentamiento para otras larvas, lo que en conjunto compartidas por las zonas de los sistemas donadores resulta en las estructuras arrecifales (Schwindt & infectadas con F. enigmaticus son salinidad Iribarne 2000, Obenat 2001). variable, baja o moderada velocidad de corriente y Las variables ambientales claves en el sedimentos areno-fangosos mezclado con conchillas control de la expansión de esta especie, al menos en

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 57-65 62 A. I. BORTHAGARAY ET AL

Tabla III. Comparación de las características ecológicas de la Laguna de Rocha (zona norte) y la Laguna de Mar Chiquita. Laguna de Mar Chiquita1 Laguna de Rocha Temperatura (°C) 12.6–21.5 13-25 * Salinidad (ups) 0.3–35 0-30 ** Profundidad (m) 0.2-2 0.6-1 ** Velocidad de corriente (m s-1) 0.025-0.4 (nd) Sólidos en suspensión (g l-1) 0.0086-3.68 0.030–0.040 *** pH 7.59-8.96 7.54-8.63 * Clorofila a (mg m-3) 1.52-167.32 15-30 *** Concentración de detritus (g l-1) (calculado como la diferencia de peso tras eliminación de 0.0034-2.94 (nd) la materia organica por ignición) Disponibilidad de sustrato 2 0.48 conchillas 100 m-2 (nd) 1 Schwindt et al. 2004b; * Pintos et al. 1991; ** Conde et al. 1999; *** Conde (datos no publicados) 2sustrato natural (conchillas de Pachycymbiola brasiliana) en áreas sin arrecifes. nd (dato no disponible). esta laguna, están asociadas a la salinidad, nutrientes se desconoce la disponibilidad de sustratos y velocidad de corriente (Schwindt et al. 2004b). De artificiales o naturales en la zona norte para el este modo, la baja salinidad, la alta concentración de asentamiento de F. enigmaticus. Sin embargo, nutrientes y la baja velocidad de corriente Sommaruga & Conde (1990), observaron conchillas favorecerían la reproducción y crecimiento de F. de Erodona mactroides en gran parte del fondo de la enigmaticus. Otra variable que parece ser clave para laguna, lo que podría favorcer la invasión de este la expansión de la especie en el sistema es la poliqueto. Por otro lado, es posible que en la Laguna disponibilidad de núcleos para su asentamiento y de Rocha existan otros factores estructuradores que posterior formación de los arrecifes (Schwindt & reduzcan su invasión impidiendo la formación y el Iribarne 2000). Por otro lado, cabe destacar que F. desarrollo de los sistemas arrecifales. De todos enigmaticus, al igual que otros poliquetos de la modos, la expansión de F. enigmaticus en este familia Serpulidae, puede asentarse también sobre sistema aún no ha sido observada en la magnitud sustratos artificiales como botellas, latas o restos encontrada en la Laguna de Mar Chiquita. plásticos (Schwindt et al. 2004b). Esto tiene Dada la similitud de características físicas importantes implicancias para el manejo de esta así como también de la comunidad bentónica de la especie, ya que la disponibilidad de sustratos de Laguna de Rocha y la Laguna de Mar Chiquita, origen biológico o antrópico podría asegurar el éxito frente a una expansión de F. enigmaticus sería de de colonización de la especie en un sistema. esperar cambios similares a los ocurridos en la Finalmente, existe poca evidencia de que segunda, tanto en la comunidad bentónica como en interacciones biológicas como competencia o la hidrodinámica de la laguna. La presencia de los depredación constituyan factores importantes en el arrecifes de F. enigmaticus en la Laguna de Mar control de esta especie (Schwindt 2001). Dos Chiquita ocasionó cambios ecológicos y físicos en el especies que podrían ser potenciales competidores, ambiente. Desde el punto de vista ecológico, la Balanus improvisus y Brachidontes rodriguezii, se formación de las estructuras arrecifales aumenta la encuentran en densidades muy bajas. Lo mismo heterogeneidad espacial, lo que genera nuevos sucede con el único depredador reportado para esta refugios favoreciendo así la presencia de organismos especie, el pez Gobiosoma parri (Schwindt 2003). epifaunales. Por otro lado, los arrecifes generan un Si bien la salinidad, velocidad de corriente y efecto en cascada sobre la infauna (poliquetos) al nutrientes podrían ser los factores determinantes en controlar la densidad de otros organismos la expansión de esta especie (Schwindt et al. 2004b), (cangrejos). En tal sentido, Cyrtograpsus angulatus la disponibilidad de sustratos potenciaría la invasión aumenta su densidad en áreas arrecifales (mayor de F. enigmaticus al sistema. En la Laguna de Rocha cantidad de refugios), afectando negativamente, a

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 57-65 Impacto potencial de invasión de Ficopomatus enigmaticus 63 través de su actividad excavadora, a los poliquetos el presente documento, asi como también a S. que se encuentran en las camadas sub-superficiales Obenat y otro revisor anonimo por sus valiosas del sedimento (Schwindt et al. 2001). Las correciones. estructuras arrecifales también afectan la hidrodinámica de la laguna, al interrumpir el curso Bibliografia natural del agua proveniente de arroyos y canales Bertness, M. D. 1984. Habitat and community artificiales, que debería descargarse en el mar. En modification by an introduced herbivorous consecuencia, gran parte del sedimento queda snail. Ecology, 65: 370-381. retenido en la laguna, favoreciendo la deposición de Brugnoli, E., Clemente. J., Boccardi, L., material fino en el fondo, lo que podría llevar a una Borthagaray, A. & Scarabino, F. 2005. Golden colmatación del ecosistema entero produciendo la mussel Limnoperna fortunei (Bivalvia: extinción local de todas las especies (Schwindt et al. Mytilidae) distribution in the main 2004a). hydrographical basins of Uruguay: update and predictions. Anais da Academia Brasileira Conclusiones de Ciências, 77:235-244. En un primer análisis, la Laguna de Rocha Brugnoli, E., Clemente, J., Riestra, G., Boccardi, L. puede considerarse como un ecosistema & Borthagaray, A. 2005. Especies acuáticas potencialmente receptor del poliqueto invasor F. exóticas en Uruguay: situación, problemática enigmaticus. Esta afirmación está sustentada en las y gestión. In: Menafra, R. et al. (Eds.) Bases condiciones físicas (salinidad y moderada o baja para la conservación y el manejo de la costa velocidad de corriente) y biológicas (comunidad Uruguaya. Vida Silvestre/US-Fish Wildlife bentónica) que presenta este cuerpo de agua, las Service, 1. cuales son favorables para el asentamiento de esta Carlton, J. T. & Geller, J. B. 1993. Ecological especie. La disponibilidad de sustratos naturales o roulette: the global transport of nonindigenous artificiales para el comienzo del proceso de invasión marine organisms. Science, 261:78-82. también sería otra variable a ser considerada. Si bien Carlton, J. T. 1985. Transoceanic and Interoceanic esto último no parecería ser un factor fundamental dispersal of coastal marine organism: the en el proceso de expansión de F. enigmaticus dentro biology of ballast water. Oceanography and de los sistemas, hasta el momento se desconoce la Marine Biological Review, 23: 313-317. disponibilidad de sustratos para el proceso inicial de Carlton, J. T. 1996. Pattern, process, and prediction colonización en la Laguna de Rocha. Además, varios in marine invasion ecology. Biological sitios sobre la costa atlántica y del Río de la Plata Conservation, 78:97-106. han sido identificados como potenciales zonas Conde, D., Bonilla, S., Aubriot, L., de León, R. & donadoras de este poliqueto. Pintos, W. 1999. Comparison of the areal Dado la similitud de características físicas y amount of chlorophyll a of planktonic and biológicas (comunidad bentónica) que presentan la attached microalgae in a shallow coastal Laguna de Rocha y la Laguna de Mar Chiquita se lagoon. Hydrobiologia, 408/409: 285-291. podría predecir el impacto esperado sobre la Laguna Conde, D., Rodríguez-Gallego, L. & Rodríguez- de Rocha. Para ello, es necesario desarrollar estudios Graña, L. 2003. Análisis conceptual de las dirigidos a la generación de información básica para interacciones abióticas y biológicas entre el determinar exactamente el estado de infección de océano y las lagunas de la costa Atlántica este sistema, así como su posible avance al resto de uruguaya. Informe Final PNUD/ la laguna. Esto permitiría realizar un plan de manejo GEF/RLA/99/G31 (FREPLATA), y control poblacional para este poliqueto invasor, Montevideo, Uruguay, 75 p. contribuyendo a la conservación de la biodiversidad Conde, D & Rodríguez-Gallego, L. 2002. Uso y de la Laguna de Rocha. Los estudios permitirán conservación de lagunas costeras de Uruguay. desarrollar planes de erradicación de esta especie resolución de conflictos en la Laguna de previos a su etapa de expansión en el ecosistema, Rocha. III Congreso Nacional sobre Areas cuando sus costos suelen ser menores y las Silvestres Protegidas (Vida Silvestre- posibilidades de erradicarla mayores. Uruguay) 20-22/11/02 Montevideo Crawley, M. J. 1987. What makes a community Agradecimientos invasible? In: Gray, A. J., Crawley, M. J. & Los autores agradecen a E. Schwindt y A. Carranza Edwards, P. J. (Eds.). Colonization, por sus comentarios, los cuales permitieron mejorar Succession, and Stability. London: Blackwell

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Scientifc. 103-116. Davis, M. A. & Pelsor, M. 2001. Experimental Muniz, P., Clemente, J. & Brugnoli, E. 2005a. support for a resource-base mechanistic model Benthic invasive pests in Uruguay: a new of invisibility. Ecology Letters, 4: 421-428. problem or an old one recently perceived? Davis, M., Grime, J. P. & Thompson, K. 2000. Marine Pollution Bulletin, 50: 1014-1018. Fluctuating resources in plant communities: a Muniz, P., Venturini, N., Pires-Vanin, A. M. S., general theory of invasibility. Journal of Tommasi, L. R. & Borja, A. 2005b. Testing Ecology, 88:528-534. the applicability of a Marine Biotic Index Elton, C. S. 1958. The Ecology of Invasions by (AMBI) to assessing the ecological quality of Animals and Plants. University of Chicago soft-bottom benthic communities, in the South Press. 181 p. America Atlantic region. Marine Pollution Eno, N.C., Clark R. A. & Sanderson W.G. 1997. Bulletin, 50: 624-637. Non-native marine species in British waters: a Nagy, G. J., López-Laborde, J. & Anastasia, L. review and directory. Published by JNCC, 1987. Caracterización de ambientes en el Río Peterborough. 152 p. de la Plata Exterior (salinidad y turbiedad Fauvel, P. 1923. Polychètes errantes. Faune France, óptica). Investigaciones Oceanológicas, 1: 5: 1-4. 31-56. Giménez, L., Borthagaray, A., Rodríguez, M., Nión, H. 1979. Zonación del macrobentos en un Brazeiro, A. & Dimitriadis, K. 2005. Scale- sistema lagunar litoral oceánico. Seminario dependent patterns of macrofaunal distribution sobre Ecología Bentónica y Sedimentación in soft-sediment intertidal habitats along a de la Plataforma Continental del Atlántico large-scale estuarine gradient. Helgoland Sur. (Montevideo, Uruguay), Memoria 1: Marine Research, 59: 224-236. 225-235 UNESCO. Giménez, L., Borthagaray, A. & Rodríguez, M. Obenat, S. 2001. Biología del anélido introducido 2003. Estructura de la comunidad y Ficopomatus enigmaticus (Polychaeta: distribución de las especies bentónicas en el Serpulidae) In: Iribarne, O. (Ed.). Reserva de Río de la plata y Frente Marítimo. PNUD, la Biosfera Mar Chiquita: Características Proyecto FREPLATA, 18p. físicas y ecológicas. Pp. 101-108. Editorial Giménez, L., Dimitriadis, C., Carranza, A., Martin, Mar del Plata, Argentina. Borthagaray, A. I. & Rodríguez, M. 2006. Orensanz. J. M., Schwindt, E., Pastorino, G., Unravelling the complex structure of a benthic Bortolus, A., Casas. G., Darrigran. G., Elías, community: A multiscale-multianalytical R., López-Gappa, J. J., Obenat, S., Pascual, S., approach to an estuarine sandflat. Estuarine, Penchaszadeh, P., Piriz, M. L., Scarabino, F. Coastal and Shelf Science, 68: 462-472. Spivak, E. D. & Vallarino, E. 2002. No longer Luppi, T. A., Spivak, E. D., Anger, K. & Valero, J. the pristine confines of the world ocean: a L. 2002. Patterns and processes of survey of exotic marine species in the Chasmagnathus granulate and Cyrtograpsus southwestern Atlantic. Biological Invasions, angulatus (Brachyura: Grapsidae) recruitment 4: 115-143. in Mar Chiquita Coastal Lagoon, Argentina. Parker, I. M., Simberloff, D., Lonsdale, W. M., Estuarine, Coastal and Shelf Science, 55: Goodell, K., Wonham, M., Kareiva, P. M., 287-297. Williamson, M. H., Von Holle, B., Moyle, P. Monro, C. C. A. 1938 On a small collection of B., Byers, J. E. & Goldwasser, L. 1999. Polychaeta from Uruguay. Annals and Impact: toward a framework for understanding Magazine of Nature History, 2: 311-314. the ecological effects of invaders. Biological Muniz, P. & Venturini, N. 2001. Spatial distribution Invasions, 1: 3-19. of the macrozoobenthos in the Solís Grande Perrings, C. 2002. Biological invasions in aquatic stream estuary (Canelones-Maldonado, systems: the economic problem. Bulletin of Uruguay). Brazilian Journal of Biology, 61: Marine Science, 70(2): 541-552. 409-420. Pintos, W., Conde, D., De Leon, R., Cardezo, M. J., Muniz, P., Venturini, N. & Gómez-Erache, M. 2004. Jorcin, A. & Sommaruga, R. 1991. Some Spatial distribution of chromium and lead in limnological characteristics of Laguna de the benthic environment of coastal areas of the Rocha (Uruguay). Revista Brasilera de Río de la Plata estuary (Montevideo, Biologia, 51: 79-84. Uruguay). Brazilian Journal of Biology, 64: Pintos, W., Sommaruga, R., Conde, D., de Leon, R.

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& Chalar, G. 1988. Antecedentes y nuevos effects of an invading reef-building polychaete aportes al conocimiento de la Laguna de on an Argentina estuarine environment. Rocha. Universidad de la Republica, Uruguay. Estuarine Coastal and Shelf Science, 59: Ricciardi, A. & Rasmussen, J. 1998. Predicting the 109-120. identity and impact of future biological Schwindt, E., De Francesco, C. & Iribarne, O. invaders: a priority for aquatic resources 2004b. Individual and reef growth of the management. Canadian Journal of Fish invasive reef-building polychaete Aquatic Science, 55: 1759-1765. Ficopomatus enigmaticus in a south-western Ricciardi, A. 2003. Predicting the impacts of an Atlantic coastal lagoon. Journal of the introduced species from its invasion history: Marine Association of the United Kingdom, an empirical approach applied to zebra mussel 84: 987-993. invasions. Freshwater Biology, 48: 972-981. Simberloff, D. 1997. The biology of invasions. In: Rioja, E. 1943. Estudios Anelidiológicos IX. La Simberloff, D., Schmitz, D. C. & Brown, T. C. presencia de Merecierella enigmatica Fauvel (Eds). Strangers in Paradise. Island Press, en las costas argentinas. Anales del Instituto Washington DC. de Biología (México), 14: 547-551. Stachowicz, J. J., Fried, H., Osaman, R. W. & Ruiz, G. M., Fofonoff, P. W., Carlton, J. T., Whitlatch, R. B. 2002. Biodiversity, invasion Wonham, M. J. & Hines, A. H. 2000. Invasion resistance, and marine ecosystem function: of coastal marine communities in North reconciling patterns and process. Ecology, 83: America: apparent patterns, processes, and 2575–2590. biases. Annual Review of Ecology and Sommaruga, R. & Conde, D. 1990. Distribución de Systematics, 31: 481-531. la material orgánica en los sedimentos Scarabino, V., Maytía, S. & Cachés, M. 1975. Carta recientes de la Laguna de Rocha (Rocha, Binomica litoral del departamento de Uruguay). Atlântica, 12: 35-44. Montevideo. I. Niveles superiores del Sistema Tilman, D. 1993. Species richness of experimental Litoral. Comunicaciones de la Sociedad productivity gradients: how important is Malacológica del Uruguay, 4(29): 117-129. colonization limitation? Ecology, 74: 2179- Schwindt, E. & Iribarne, O. 2000. Settlement sites, 2191. survival and effects on benthos of an Tilman, D. 1997. Community invasibility, introduced reef-building polychaete in a SW recruitment limitation, and grassland Atlantic coastal lagoon. Bulletin of Marine biodiversity. Ecology, 78: 81-92. Science, 67: 73-82. Venturini, N., Muniz, P. & Rodriguez, M. 2004 Schwindt, E. 2001. Impacto de un poliqueto exótico Macrobenthic subtidal communities in relation y formador de arrecifes. In: Iribarne, O. (Ed.), to sediment pollution: the phylum-level meta- Reserva de la Biosfera Mar Chiquita: analysis approach in a south-eastern coastal Características físicas y ecológicas. Pp. 109- region of South America. Marine Biology, 113. Editorial Martín, Mar del Plata, 144: 119-126. Argentina. Williamson, M. 1996. Biological Invasions. Schwindt, E., Bortolous, A. & Iribarne, O. 2001. London: Chapman & Hall. Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions, 3: 137-149. Schwindt, E. 2003. Arrecifes introducidos en la laguna costera Mar Chiquita, Reserva El Hombre y la Biosfera (UNESCO). Ciencia Hoy, 13: 36-41. Schwindt, E., Iribarne, O. & Isla, F. 2004a. Physical

Received April 2006 Accepted July 2006 Published online August 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 57-65

Record of a pregnant bentfin devilray, Mobula thurstoni (Lloyd) (Elasmobranchii, Mobulidae) caught in Southwestern Brazil

1 2 ANDRÉ L. S. CASAS , CARLO M. CUNHA , WAGNER 3 4 INTELIZANO & MANOEL M. B. GONZALEZ

1 Laboratório de Anatomia Veterinária, Instituto de Saúde, Universidade Paulista (UNIP-Campinas). Avenida Comendador Enzo Ferrari, 280. Swift, Campinas-SP. CEP: 13043-900. E-mail: [email protected] 2 Departamento de Cirurgia da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo. Avenida Prof. Dr. Orlando Marques de Paiva, 87, São Paulo-SP. CEP: 05508-900. E-mail: [email protected] 3 Laboratório de Anatomia Veterinária, Faculdade de Medicina Veterinária, Universidade Metropolitana de Santos. Rua da Constituição, 374, Vila Nova, Santos - São Paulo – Brasil. CEP: 11015-904. E-mail: [email protected] 4 Museu de Arqueologia e Etnologia, Universidade de São Paulo and Núcleo de Pesquisa e Estudo em Chondrichthyes, Rua Ana Pimentel, 12, Ponta da Praia, Santos - São Paulo - Brasil. CEP: 11030-050. E-mail: [email protected]

Abstract. Registro de uma fêmea grávida de raia diabo, Mobula thurstoni (Lloyd) (Elasmobranchii, Mobulidae) capturada no Sudeste do Brasil. The present paper reports the first occurrence of a 183 cm disc width pregnant female of Mobula thurstoni (Lloyd, 1908) in southwest Brazilian coast, caught by a commercial longline fishing vessel. Morphometrics and a morphological description of the male embryo are presented.

Key-word: Embryo, reproduction, mobulid, batoid, trophonemata.

Resumo. O presente trabalho reporta a primeira ocorrência de uma fêmea grávida de Mobula thurstoni (Llyod, 1908), capturada por barco de pesca de espinhel na costa sudeste do Brasil. A morfometria e a descrição morfológica do embrião macho são apresentadas.

Palavras-clave: Embrião, reprodução, mobulídeo, batóideo, trofonemata.

The family Moubulidae Rafinesque, 1810, includes (Tortonese, 1957) and in the Northern Tyrrhenian species poorly known in many biological aspects, Sea, Southeast of Gorgona Island (Notarbartolo-di- such as the reproductive pattern. Devilrays, genus Scaria & Serena, 1988). Garayzar (1991) reported Mobula, comprise nine living species, measuring the presence of embryos and gravid Mobula from 1 to about 4 m of disc width (DW) and munkiana Notarbartolo-di-Sciara, 1987 specimens in represented worldwide in warm temperate and Bahia de La Paz, Mexico and pregnant M hypostoma tropical seas (Notarbartolo-di-Scaria, 1987; Last & with term embryos were reported in south and Stevens, 1994). Five species of this genus were southwestern Brazilian coast (Kotas, et al. 2005), reported in the Western Atlantic: Mobula hypostoma however no data are available for M. thurstoni (Bancroft, 1831), Figueiredo (1977); Mobula pregnancy. An adult 1830 mm DW female specimen tarapacana (Philippi, 1893), Notarbartolo-di-Scaria was accidentally caught at about 50-80 m of depth & Hillyer (1989); Mobula rochebrunei (Vaillant, with long line and hook and landed to the fishing 1879), Mobula japanica (Müller and Henle, 1841) wharves on July, 2002 in Santos city, São Paulo and Mobula thurstoni (Lloyd, 1908), Gadig et al. State, Brazil. The specimen was donated by (2003). Occurrence of embryos and pregnant fishermen of the commercial longline fishing vessel females of Mobula mobular (Bonnaterre, 1788) have “Progressão”, (southwestern Brazil) and identified been reported in the region of Palermo, Italy as M. thurstoni following the identification key

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 66-68

Record of a pregnant bentfin devilray, Mobula thurstoni in Southwestern Brazil 67 proposed by Notarbartolo-di-Scaria (1987) and it internal organs. The left uterus presented a dilatation agrees with specimens previously studied in the and during its dissection (Figs 1-3), an embryo was same area by Gadig et al. (2003). These specimens visualized with the pectoral fins overlapping the shared the following characteristics: tail base dorsal region (Fig.1-2). The trophonemata and its dorsally depressed, prominent double curvature of secretion - the “uterine milk”, which nourishes the anterior margin of pectoral fins, a rectangular light developing embryos - were observed and gray area in the nuchal region between the origins of characterize the viviparity with matrotrophy (Fig. 2) pectoral fins and a white spot on the tip of the dorsal (Hamlett & Hysell, 1998; Hamlett, 2005). The male fin. In addition, the dorsal coloration presented a embryo was 340 mm DW and 190 mm total length grayish color and a white triangular small area (TL). The presence of uterine trophonemata and located about midway between the origin and the uterine milk in the female uterus, the incomplete apex of the dorsal fins (fig. 3). The ventral region dorsal grayish pigmentation, white marks on its presented with coloration. The material was fixed in dorsal side, the small size of the animal, and the fact 10% formalin solution, and deposited in the that this species is expected to give birth to young at ichthyological collection of the Núcleo de Pesquisa e about 850 mm DW (Notarbartolo-di-Scaria, 1987) Estudo em Chondrichthyes (NUPEC) on July, 2002. are evidences that the embryo was in mid-term stage The female was 1830 mm DW (NUPEC 1868) and of development. The presence of adult males of M. the male embryo was 340 mm DW (NUPEC1867). thurstoni, with developed claspers and pelvic fins The morphometric protocol followed (Table I) Notarbartolo-di-Scaria (1987) and the celomatic cavity was incised by the linea alba to verify the

Table I – Female and embryo measurements of Mobula thurstoni. Measurements (mm) Specimen Female Embryo Disc width 1830 340 Disc length 1030 190 Anterior projection 1 680 144 Anterior projection 2 1057 195 Predorsal lenght 840 165 Dorsal fin base length 110 15 Dorsal fin height 82 14 Precloacal distance 840 165 Tail length 1200 415 1st gill slit opening length 100 18 2nd gill slit opening length 105 18 3rd gill slit opening length 108 17 4th gill slit opening length 99 17 5th gill slit opening length 62 9 Between first gill slits 220 46 Between fifth gill slits 95 18 Rostrum to first gill slits 197 45 Rostrum to fifth gill slits 385 90 Pelvic fin length 217 37 Cephalic fin length 221 36 Cephalic fin width 71 23 Orbit height 30 10 Between antorbitals 240 67 Preoral length 75 15 Head length 232 50 Mouth width 215 45 Internarial distance 195 39 Figures 1-3. Embryo of Mobula thurstoni. 1, during the uterus Upper toothband length 195 45 dissection a fetus with the pectoral fins overlapping the dorsal region was observed. 2, the uterine trophonemata 3, embryo Lower toohband length 163 44 removed from uterus with incomplete dorsal pigmentation.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 66-68 68 A. L. S. CASAS congested and swollen may indicate mating activity Hamlett, W.C. 2005. Reproductive biology and in southwest Brazilian coast(Gadig et al. 2003). The phylogeny of Chondrichthyes: sharks, occurrence of a gravid female in the same region batoids and chimaeras. Science Publishers, corroborates the assumption that the Brazilian Enfield, 562 p. southwestern coast is an important reproductive site Kotas, J. E., Petrere, M. J., Azevedo, V. G., Santos for the species. S. 2005. A pesca de emalhe e de espinhel de superfície na Região Sudeste-Sul do Brasil. Acknowledgements Instituto Oceanográfico da USP, São Paulo, The authors wish to thank Giuseppe Notarbartolo-di- 72p. Sciara for the references provided. Last, P.R. & Stevens, J.D. 1994. Sharks and rays of Australia. CSIRO Austrália. 513p. References Notarbartolo-di-sciara, G., 1987. A revisionary Figueiredo, J. L. 1977. Manual de Peixes study of genus Mobula Rafinesque, 1810 Marinhos do Sudeste do Brasil, Parte 1. (Chondrichthyes: mobulidae) with the Introdução. Cações, raias e quimeras. description of a new species). Zoological Museu de Zoologia, Universidade de São Journal of the Linnean Society, 91:1-91. Paulo, São Paulo, 104 p. Notarbartolo di Sciara G. & Serena F., 1988. Term Gadig, O.B.F., Namora, R.C. & Motta, F.S. 2003. embryo of Mobula mobular Bonnaterre, Occurrence of the bentfin devil ray, Mobula 1788) from the Northern Tyrrhenian Sea. Atti thurstoni (Chondrichthyes: Mobulidae), in the della Società Italiana di Scienze Naturali e western Atlantic. Journal of the Marine del Museo Cívico di Storia Naturale di Biological Association of the United Milano, 129:396-400. Kingdon, 83:869-870. Notarbartolo di Sciara G. & Hillyer E.V., 1989. Garayzar, C.J.V. 1991. Observations on Mobula Mobulid rays off Eastern Venezuela. Copeia, munkiana (Chondrichthyes: Mobulidae) in the (3): 607-614. Bahia de La Paz, B.C.S. Mexico. Revista de Tortonese E., 1957. Studi sui Plagiostomi. XI. Investigação Científica de la Universidad Descrizione di un embrione di Mobula Autonoma de Baja California Sur, 2 (2): mobular. Bolletino di Zoologia, 24 (2): 45- 78-81. 47. Hamlett, W. C. & Hysell, M. 1998. Uterine specialization in Elasmobranches. Journal of Experimental Zoology, 282: 438-459.

Received May 2006 Accepted July 2006 Published online August 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (1): 66-68

Intestinal bacterial diversity in live rock lobster Panulirus homarus (Linnaeus) (Decapoda, Pleocyemata, Palinuridae) during transportation process

1, 2 1 1 GRASIAN IMMANUEL , PALANISAMY IYAPPA RAJ , PALANICHAMY ESAKKI RAJ 1 & ARUNACHALAM PALAVESAM

1 Marine Biotechnology Division, Centre for Marine Science and Technology, M. S. University, Rajakkamangalam- 629 502, Tamilnadu, India. 2 Corresponding author: Ph.: +91-4652-253078; E-mail: g [email protected]

Abstract. This study investigates the bacterial diversity in the intestine of rock lobster Panulirus homarus during live transportation process lasting for 14h. The total viable count (TVC) in the intestine of P. homarus (Linnaeus, 1758) prior to packing (control) was 130.33 x 106 cfu ml-1. In the intestine of packed lobsters (experimental), the TVC showed an increasing trend and the recorded values were between 139.0 and 150.0 x 106 cfu ml-1 respectively during 2nd and 14th h. The bacterial species composition and their percentage occurrence were also varied much between control and experimental samples (p < 0.05), but the variation in species composition between the incubation period was statistically non significant (P>0.05). Among the species identified, Pseudomonas aeruginosa (Schroeter, 1872) and Vibrio parahaemolyticus (Fujino et al., 1951) were predominantly seen and seven other less dominant species were also identified.

Key words: intestine, species composition, time intervals, TVC.

Resumo. Diversidade bacteriana intestinal em vida da Lagosta-das-rochas Panulirus homarus (Linnaeus, 1758) (Decapoda, Pleocyemata, Palinuridae) durante processo de transporte. Este estudo investigou a diversidade bacteriana em intestino da Lagosta-das-rochas Panulirus homarus (Linnaeus, 1758) durante o processo de transporte em vida passadas 14 horas. A contagem do total viável de bactérias (CVT) nos intestinos de P. homarus antes do transporte (grupo controle) foi 130,33 x 106 cfu ml-1. Nos intestinos de lagostas transportadas (grupo testado), a CVT mostrou uma tendência de aumento e os valores registrados ficaram entre 139,0 e 150,0 x 106 cfu ml-1 passados 2 e 14 horas, respectivamente. A composição de espécies de bactérias e suas percentagens de ocorrência também variaram bastante entre os grupos testados e controle apresentando médias significativamente diferentes (p < 0,05). Entre as espécies identificadas, Pseudomonas aeruginosa (Schroeter, 1872) e Vibrio parahaemolyticus (Fujino et al., 1951) foram predominantemente observadas. Outras sete espécies menos dominantes foram também identificadas.

Palavras Chave: intestino, composição de espécies, intervalos de tempo, CVT.

Introduction intestinal tract of all animal species, along with a Microbial biomass in aquatic habitat plays complex microbial community, known as intestinal an important role, besides being a subject of delicate micro flora (Tannock, 1995 & 1997). balance between the host and environment In the aquatic environment, the host relationship. When such balance is disturbed, it intestine access begins with pathogens colonize could result in disease out break, which may affect multiplication in the gills and its dissemination, adversely the host. In general, pathogenic microbes affecting in both beneficial and harmful ways usually are anaerobic forms harbored within the depending on the prevailing conditions. Separate

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 69-73 70 G. IMMANUEL ET AL

subject about fish from the previous affirmation, Materials and Methods e.g., in fishes, it has been demonstrated that, obligate Live lobsters were obtained from a local anaerobic bacteria are disseminated in the intestinal fish-landing centre at Chinnamuttam, Kanyakumari, tract of many fish species such as grass carp South India and brought to the laboratory (Ctenopharingodon idella (Valenciennes, 1844)) and and acclimatized at 28 ± 10C temperature gold fish (Carassius auratus (Linnaeus, 1758)) and a salinity of 35‰ for five days. (Trust et al., 1979). During acclimatization period, the lobsters were fed Intestinal microflora of penaeid shrimp with mussels (Perna sp. Philipsson, 1788). species was also studied. The gastrointestinal flora Afterwards, lobsters were selected considering of fresh water shrimp Palaemon paucidens de Haan, healthy, activity and weight range uniformly 1844 adapted to seawater was reported (Sujita et al., (130 ± 8.0g) for the live transportation assay based 1986a). Farfantepenaeus aztecus (Ives, 1891) from on morphological and behavioral adaptation. The sea grass meadows of Red Fish Bay near Port selected ones have been starved for 12 h before the Aransas, Texas, harbors nine bacterial genera experiment starting the procedures. including Flavobacterium, Cytophaga, Alcaligenes, For the present study, the temperature of the Pseudomonas, Xanthamonas, Alteromonas, lobster holding container (1 tone capacity) was Aeromonas, Vibrio and also Chromobacterium and brought down to 12–150C from the initial Photobacterium (Kitting et al. 1984; Dempsey & temperature of 27± 10C at the rate of 30C per hour Kitting 1987). achieving by using bags filled with ice cubes. The In crustaceans, the intestinal microbial mouth bags were sealing to avoid the melted ice colonization has great importance in healthy released into the container. Three to five ice bags condition and better growth performance. Oxley et were placed on the surface of water in the container al. (2002) reported that wild and cultured prawns and were continuously aerated to maintain a uniform (eg. Fenneropenaeus merguiensis (De Man, 1888)) temperature. harbor a diverse bacterial flora, which includes the dominant genera like Aeromonas, Plesiomonas, Photobacterium, Pseudoalteromonas, Pseudomonas and Vibrio. The similarity existing in the intestine bacterial flora of cultured prawns suggests the host specificity of intestinal microbial colonization. An understanding of the host intestinal bacterial floral interactions is of much significance for the development of a healthy cultivation environment and also to optimize the potential species growth. Despite of those reports, there are still lacks of similar information from other crustacean species. However, in recent years there has been a growing interest on the endogenous intestinal micro flora of Figure 1. Specimen of P. homarus on laboratorial conditions. commercially important finfish and shellfish species as a tool for helping fish diseases and pathological Simultaneously, sterilized dry sawdust, interpretation studies about. Information on the straw and pieces of gunny sacks were aseptically 0 micro flora of aquatic organisms is especially pre-cooled in a freezer (-20 C) along with 0.5 l available for the lobster Panulirus japonicus (Von capacity plastic bottles filled with water. Seven Siebold, 1824) (Sujita et al. 1986 b, 1987). Although thermo cool boxes (40 × 30 × 15 cm) were prepared much literature on transportation of live lobsters is with two cooled layers settled on the bottom first available (Solomon & Hawkins, 1981; Mc Larney, saw dust and the second one straw. Besides, two 1984; Homma, 1990; Sujita & Deguchi, 1990), the frozen ice bottles wrapped with filter paper were changes in the qualitative and quantitative placed at the sides of the box. Then the lobsters were composition of the intestinal microflora of live placed on the straw (10 lobsters each/box) by gently lobsters during transportation process are poorly folding the antennae and abdomen to bring them known. The present study was carried out to close to their body in order to uniformly investigate the changes in intestinal bacterial flora of accommodate. Finally the lobsters were covered lobster Panulirus homarus (Figure 1) during live with a piece of pre-cooled gunny sack and then the transportation process. box was closed with lid and sealed with adhesive tape.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 69-73 Intestinal bacterial diversity in live rock lobster Panulirus homarus 71

The intestine was sampled in the beginning obtained were statistically transformed and analyzed from unpacked lobsters (control) and then, each two by one-way ANOVA test. Significant differences hours; three lobsters were collected from different between means (p<0.05) of the TVC due to boxes, till number seven totaling 14 hours for incubation time were not detected. bioassay. The lobster intestine was collected aseptically by cutting the cuticle. The collected 16 intestinal samples were stored in a refrigerator in 14 pre-labeled containers for further bacterial 12 enumeration. All samples were analyzed about Total 10 Viable Count (TVC), bacteria diversity and number 8 using spread plate method and identified according 6 to Holt et al. (1994). The results were submitted to 4 2 parametric statistical tests, using Standard Deviation Cumulative bacterial load (%)

(SD) and Analysis of Variance (ANOVA). 0 If necessary, the data were transformed 02468101214 (log transformation) as described by Zar (1974). Time interval (h)

Figure 2. Cumulative increasing percentage of TVC in different Results and Discussion hours. Aquatic organisms often harbor a great number of bacteria into their intestinal tract, gills The bacteria qualitative and quantitative data and body surface, which they acquired from water, from all samples are presented in Table II. In the sediment and /or food. However, most of these control lobsters, 42 suspected isolates were taken bacteria are temporary residents, due to (i) from the intestinal samples. Among these, ten incompatible physical and chemical conditions, (ii) bacterial species were identified and one lethal interaction with resident bacteria and/or (iii) unidentified species was also recorded. Within these, long term immune response of the host. Qualitative Pseudomonas aeruginosa (Schroeter, 1872) strain and quantitative information concerning the micro was dominated with 21.42% occurrence. The next flora of aquatic vertebrates including fish and of dominant species was Vibrio parahaemolyticus crustaceans has been provided by Sujita et al. (Fujino et al., 1951) (14.28%) and the least (1987); Sujita & Deguchi (1988) and Cahill (1990). percentage occurrence was Alcaligenes sp. The bacterial load associated with the gill Castellani & Chalmers, 1919 (2.38%). and intestine of freshly caught Japanese spiny In experimental lobsters, the number of lobster P. japonicus ranged between 3.2 ×106 to 1.2 suspected isolates examined was 41, 39, 44, 48, 44, th × 107 cfu.g-1 (colony forming unit per g tissue) and 40 and 47 respectively during 2nd to 14 h of 9.5 × 107 to 1.3 × 109 cfu.g-1 respectively (Sujita et experimentation. Among these P. aeruginosa, V. al. 1986b, Sujita et al., 1987). The total viable count parahaemolyticus, Bacillus circulans Jordan, 1890 (TVC - cfu.ml-1) of both control (unpacked) and and Escherichia coli (Migula, 1895) were recorded experimental (packed) lobsters at different time in high numbers and the percentage occurrence intervals (2nd–14th h) after packing are given in Table ranged from 10.25 – 20.0% at different time I. The data on TVC was relatively more in the intervals. Species like Photobacterium damselae intestinal samples collected from lobsters during (Love et al., 1982) (6.25–10.25%), Flavobacterium experimentation process, when compared the value columnare (Bernardet & Grimont, 1989) (5.00 – recorded in the intestinal samples collected from the 9.09%), Micrococcus luteus (Schroeter, 1872) (5.0 – unpacked (control) lobsters. The maximum TVC 10.25%), Enterobacter aerogenes Hormaeche & value of 150.0 ± 2.51 × 106 cfu.ml-1 was noticed Edwards, 1960 (2.56 – 5.00%), Corynebacterium against the minimum value of 130.33 ± 2.51 × 106 xerosis (Lehmann & Neumann, 1896) (0 – 4.87%) cfu.ml-1 in control samples. The cumulative increase and Alcaligens (2.08 – 2.56%) were also recorded. in TVC of 14 h experimental sample was maximum Two-way ANOVA test indicated that the variation (15.09%) and it was minimum (6.23%) in 2h in bacterial species within the experimental duration experimental sample (Fig. 2). The percentage was not statistically significant (p > 0.05). increase in TVC within the experimental samples Sujita et al. (1986b, 1987) reported that, Vibrio and during 2 to 14 h was not differed much and it Pseudomonas spp were dominant in the gut and fluctuated between 0.89 to 2.08%. The TVC data gill of Scomber japonicus Houttuyn, 1782.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 69-73 72 G. IMMANUEL ET AL

Table I. Total Viable Count (TVC - cfu ml-1) of bacterial strains in the intestinal samples of live rock lobster P. homarus at different time intervals during transportation process. Time T V C (cfu ml-1) in the Increasing of TVC in different Cumulative increasing of TVC interval (h) intestinal samples hours (%) in different hours (%) 0 (Control) 130.33 ± 2.51 x 10 6 ------2 139.00 ± 1.00 x 10 6 6.23 6.23 4 140.33 ± 0.57 x 10 6 0.89 7.12 6 142.33 ± 0.57 x 10 6 2.08 9.20 8 144.00 ± 1.00 x 10 6 1.28 10.48 10 145.33 ± 0.57 x 10 6 1.02 11.50 12 147.66 ± 0.57 x 10 6 1.79 13.29 14 150.00 ± 2.00 x 10 6 1.80 15.09 Each value is a mean of three replicates (± SD) TVC was statistically non significant (P>0.05)

Table II. Species composition of micro flora (%) isolated from intestinal samples of live lobsters (P. homarus) at different time intervals (0-14h) during transportation process. Intestinal samples at different time intervals (h) Bacterial species 0 (C) 2 4 6 8 10 12 14 9 8 8 7 8 7 7 8 P. aeruginosa (21.42) (19.50) (20.51) (15.90) (16.66) (15.90) (17.5) (17.02) 6 6 5 7 7 6 6 8 V. parahaemolyticus (14.28) (14.63) (12.82) (15.90) (14.58) (13.63) (15.0) (17.02) 5 5 6 6 7 8 8 7 B. circulans (11.90) (12.19) (15.38) (13.63) (14.58) (18.18) (20.0) (14.89) 5 5 4 7 8 7 7 7 E .coli (11.90) (12.19) (10.25) (15.90) (16.66) (15.90) (17.5) (14.89) 4 4 4 3 3 4 3 4 P. damselae (9.52) (9.75) (10.25) (6.81) (6.25) (9.09) (7.50) (8.50) 4 3 3 4 4 3 2 4 F. columnare (9.52) (7.31) (7.69) (9.09) (8.33) (6.81) (5.00) (8.50) 3 3 4 3 4 3 2 4 M. luteus (7.14) (7.31) (10.25) (6.81) (8.33) (6.81) (5.00) (8.50) 2 2 1 2 2 2 2 2 E. aerogens (4.76) (4.87) (2.56) (4.54) (4.16) (4.54) (5.00) (4.25) 2 2 1 2 2 1 1 -- C. xerosis (4.76) (4.87) (2.56) (4.54) (4.16) (2.27) (2.50) -- 1 1 1 1 1 1 1 1 Alcaligenes (2.38) (2.43) (2.56) (2.27) (2.08) (2.27) (2.50) (2.12) 1 2 2 2 2 2 1 2 Unidentified (2.38) (4.87) (5.12) (4.54) (4.16) (4.54) (2.50) (4.25) Total isolates 42 41 39 44 48 44 40 47 Values in parenthesis denotes percentage of species composition Statistically significant (P<0.05) between the organisms Statistically non significant (P > 0.05) between the experimental duration

Elston (1989) reported that, out of 518 strains of recorded as the dominant species, followed by Vibrio isolated from the spiny lobster, 69 strains V. haemolyticus, B. circulans, E. coli, P. damselae, were identified as Vibrio alginolyticus (Miyamoto et F. columnare and M. luteus. It was observed Vibrio al., 1961), a causative agent of crustacean vibriosis. sp. was present in 14.28% of the control lobster. In This result suggested the prevalence of pathogenic experimental lobsters packed for live transportation, bacterial colonies even in the gills and gut of healthy the raise in TVC was 17% over the control value spiny lobsters which may cause opportunistic during 10 – 14h. This clearly indicates the processes infectious diseases under stress conditions. of bacterial proliferation during the live In the present study, P. aeruginosa was transportation.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 69-73 Intestinal bacterial diversity in live rock lobster Panulirus homarus 73

Even during processes of live lobster – A hand Book for small scale fish culture transportation by using suitable container maintained in North America. Cloudburst Press, at low temperature, the microbes colonized in gill, Vancouver, 583 p. mucus and also in intestine may proliferate and Oxley, A. P. A., Shipton, W., Owens, L. & McKay, accounts for the increase in bacterial load. This may D. 2002. Bacterial flora from the gut of the be the reason for no significant (P>0.05; One-way wild and cultured banana prawn, Penaeus ANOVA) increase of TVC value recorded during merguiensis. Applied Microbiology, 93: 214- the later hours (10 – 14 h) of experimentation 218. process in the present study. Solomon, D. I. & Hawkins, A. D. 1981. Fish capture This strongly suggests that healthy spiny and transport. p. 197 – 221. In: Hawkins, A.D. lobsters should be starved for 1-2 days before the (Ed.). Aquarium systems, Academic Press, transportation so as to minimize the nutrient New York, 452p. availability in the gut for rapid proliferation of Sujita, H., Takahshi, T., Kamemoto, F.I. & Deguchi, bacterial species. Additionally, the temperature Y. 1986a. Aerobic bacterial flora in the inside the package should be kept to a minimum digestive tract of fresh water shrimp level to reduce the rate of bacterial proliferation and Palaemon paucidens acclimated with sea also to enhance the survival to a maximum extent of water. Nippon Suisan Gakkaishi, 42: 211 – > 80%. Besides these procedures, it is recommended 215. the use of sterilized seawater and packaging Sujita, H., Veda, R. & Deguchi, Y. 1986b. An materials to avoid added microbial contamination anaerobic bacterium isolated from Japanese through the process of packing (Sujita & Deguichi, spiny lobster Panulirus japonicus. Food 1990). In the present study care was taken to Microbiology, 3: 379 - 385. sterilize and hence added bacterial proliferation was Sujita, H., Veda, R., Berger, L. R. & Deguchi, Y. avoided. The adoption of discussed precautious 1987. Microflora in the gut of Japanese measures, it might reduce the bacterial proliferation coastal crustaceans. Nippon Suisan during live lobster transportation process and Gakkaishi, 53: 1647 – 1655. prevent the spoilage by indirect mean. Sujita, H. & Deguchi, Y. 1988. Intestinal microflora in tetrodoxin bearing organisms, with special References reference to tetrodoxin producing bacteria. p. Cahill, G. F. 1990. Bacterial flora of Fishes - A 65 – 75. In: Hashimoto, K. (Ed.). Recent review. Microbial ecology, 19: 21- 41. advances in Tetrodotoxin research, Dempsey, A .C. & Kitting, C. L. 1987. Koseisha Koseidaku, Tokyo. Characteristics of bacteria isolated from Sujita, H. & Deguchi, Y. 1990. Live fish Penaeid shrimp. Crustaceana, 52: 90-94. transportation and preservation. p. 100 -108. Elston, R. 1989. Bacteriological methods for In: Hiryama, K. (Ed.). Price formation and diseased shellfish. p. 187 – 215. In: Austin, B. quality control of mariculture products, & Austin, D.A. (Eds.). Methods for Koseisha Koseidaku, Tokyo, 115 p. Microbiological Examination of fish and Tannock, G. W. 1995. Normal microflora- An shellfish, Ellis Horwood, Chichester, 317 p. introduction to microbes inhabiting the Holt, J. G., Noel, R. Kreg, Sneath, P. H. A, Stanley, human body. Chapman & Hall, London, J. T. & Williams, T. (Eds.). 1994. Bergey’s 115 p. manual of Determinative Bacteriology, Vol: Tannock, G. W. 1997. Probiotic properties of lactic 1–4, Williams & Wilkins Co., Baltimore, acid bacteria, plenty of scope for fundamental 787 p. R&D –A review. TIBTECH, 15: 270-274. Trust, T. T., Bull, L. M., Currie, B. R. & Buckley, Homma, A. 1990. An Encyclopedia on Live Fish, J.T. 1979. Journal of Fisheries Research Fugi. Technology press, Tokyo, 712 p. Board of Canada, 36: 1174 - 1179. Kitting, C. L., Fry. B. & Morgan, M. D. 1984. Zar, J. H. 1974. Bio-Statistical analysis, Prentice Detection of inconspicuous epiphytic algae Hall, New Jersey, 620 p. supporting food web in seagrass meadows. Oecologia, 62: 145-149. Mc Larney, W. 1984. The fresh water aquaculture Received June 2006 Accepted August 2006 Published online September 2006

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Morphological aspects and seasonal changes of some planktonic ciliates (Protozoa) from a temporary pond in Buenos Aires Province, Argentina

1 1 2 GABRIELA C. KÜPPERS , ESTELA C. LOPRETTO & MARÍA C. CLAPS

1 Cátedra Zoología Invertebrados I, Facultad de Ciencias Naturales y Museo (UNLP), Museo de La Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina. E-mail: [email protected]; [email protected] 2 Instituto de Limnología 'Dr. R. A. Ringuelet' (CONICET-UNLP), Avenida Calchaquí km 23.5, 1888 Florencio Varela, Argentina. E-mail: [email protected].

Abstract. The morphology of some planktonic ciliates in a temporary freshwater pond located in Buenos Aires province, Argentina, is compared and the seasonal variation in their abundances over an annual cycle is described. Samples were taken from June 2004 to June 2005. Physical and chemical characteristics of the environment were also recorded. Taxonomic identifications were made in vivo and after employing the Protargol technique. Five planktonic species were recorded for the first time in South America.

Key words: Ciliophora, plankton, freshwater pond, morphology, abundances variation.

Resumo. Aspectos morfológicos e mudanças sazonais de alguns ciliados (Protozoa, Ciliophora) planctônicos de uma poça temporária na província de Buenos Aires, Argentina. Dados morfológicos de alguns ciliados planctônicos, coletados de uma poça temporária de água doce localizada na província de Buenos Aires, Argentina, são comparados, assim como também foram descritas as variações sazonais da densidade ao longo do ciclo anual. Amostras foram obtidas desde junho de 2004 até junho de 2005 em três locais de coleta. Características físicas e químicas do ambiente foram registradas. As identificações taxonômicas foram feitas in vivo e depois da utilização da técnica de Protargol. Cinco espécies planctônicas foram registradas pela primeira vez América do Sul.

Palavras Chave: Ciliophora, plâncton, poça de água doce, morfologia, variação das abundâncias.

Introduction Vucetich & Escalante 1979, Modenutti & Taxonomic studies of freshwater ciliates have Claps 1986). At global scale, ciliates in temporary been scarcely conducted in Argentina, despite of waters are poorly known (Andrushchyshyn et al. their ubiquity in planktonic communities and 2003). These habitats, which are frequent in their important role as carbon recyclers. Buenos Aires province during humid periods, are Although ciliates taxonomy has been already populated by organisms with particular investigated employing silver staining methods and physiological and behavioral properties and function electron microscopy in other countries, mainly in as microcosms to study their ecology (Williams Europe, in South America the contribution to 2001). this field is from Paiva & da Silva-Neto The aims of this work are to compare (2003, 2004a, b, c, 2005) in Brazil and morphological aspects of planktonic ciliate species Pettigrosso et al. (1997), Pettigrosso (2001, 2003), from a temporary pond (Buenos Aires province, Barría (2002), and Pettigrosso & Barría (2004) Argentina) with earlier descriptions of in Argentina. In this country, other researchers corresponding species from other continents. We have studied the ciliate fauna of several also analyze the variability in the abundance of those temporary ponds in Buenos Aires province species along a year cycle and their relationship with by live observation (Cela 1972, Vucetich 1972, physical and chemical changes.

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Morphological aspects and seasonal changes of planktonic ciliates 75

Materials and Methods Prostomatida (one species), Choreotrichida The study was carried out in a freshwater (one species), Halteriida (one species), Strombidiida temporary pond located near the city of La Plata in (three species), and Stichotrichida (one species) Buenos Aires province, Argentina (35° 05’ S, 57° were considered. Five species were recorded 48’ W) (Fig. 1) that goes through drought for the first time in South America, another one in periods, mainly in summer and the beginning of Argentina, and additionally one in Buenos Aires autumn. During rainy periods, the pond has an province. Morphology and infraciliature approximate length of 30 m and about of Askenasia volvox, Coleps hirtus hirtus, and 1 m maximum depth. It is located beneath a Halteria grandinella, which were previously cattle field, bounded by Eucalyptus spp. (Myrtaceae) studied in vivo and by supravital staining, were and the Route 36. The water supply comes also considered. Abundances of Teuthophrys mainly from rainfall. Following the trisulca africana, Rhabdoaskenasia minima, summer drought, the macrophytes Alternanthera and Hypotrichidium conicum were not estimated philoxeroides (Amaranthaceae) and Ludwigia from field samples as these species were cultured in peploides (Onagraceae) persist in the pond for a the laboratory. short period of time and after their decomposition, the planktonic community dominates the water Order Haptorida Corliss body. Samples were taken monthly during the Teuthophrys trisulca africana (Dragesco & morning at three sampling stations, with 5 liter bottles from June 2004 to June 2005, except in Dragesco-Kernéis) Foissner, October 2004, summer 2005, and May 2005, Berger & Schaumburg when the pond was dry. Two replicates were (Table I; Figs. 2a and 3a) collected at the same time and at each sampling site, from which two 250 ml sub-samples were Sack-like body shape with three anterior, fixed using acid Lugol 2% and other live sub- spirally curved oral arms. Posterior contractile samples were cultured in wheat infusions. vacuole. Macronucleus vermiform and coiled. Temperature, pH, and conductivity were recorded Cytoplasm colorless and without endosymbiotic with a multiparameter sensor (®Horiba U21). algae. Oral arms lined by trychocysts. Somatic Dissolved oxygen was estimated by the ciliature uniform. With rod-shaped somatic Winkler method (Clesceri et al. 1998). Observations extrusomes (2.8-8 μm long) and dark granules over and measurements were performed in vivo and after the body. revealing the argentophilic structures by This species was recorded in autumn, when the Protargol technique (Wilbert 1975), at Alternanthera philoxeroides occurred, and in magnifications of 100, 400 and 1000×. Previous to cultures of mud samples taken in October 2004, the silver staining, the ciliates were fixed with where the resting cysts developed. Bouin’s solution. The drawings of impregnated cells were performed by using a tracing device and the Order Cyclotrichida Jankowski micrographs were taken with a Leica Wild MPS52. Askenasia volvox (Eichwald) Kahl Cells were counted using an inverted microscope (Table II; Figs. 2b and 3b, c) in 10 ml chambers (Utermöhl 1958), examining the entire chamber at a magnification of 150×. The Body ovoid to pyriform, widened classification proposed by Lynn & Small (2000) was posteriorly. Without endosymbiotic algae. followed. Contractile vacuole sub-equatorial and with Abbreviations used in morphometric tables another posterior floating vacuole. Macronucleus are as follow: X, arithmetic mean; Min, minimum globular to ellipsoidal, sometimes constricted. Micronucleus indented in the macronucleus. observation; Max, maximum observation; M, Somatic kineties arranged in a pre-equatorial median; SD, standard deviation; N, number of girdle, each row of them with single kinetosomes observations. with 7 groups of flame like cilia that extend anteriorly; an equatorial girdle with paired Results kinetosomes with posteriorly directed cilia; a sub- Observations on the species equatorial girdle with flexible bristles, each row with The morphology and infraciliature of 3 kinetosomes. Oral region surrounded by a ten planktonic ciliates belonging to the orders circumoral wreath of granules. Extrusomes were Haptorida (one species), Cyclotrichida (two species), faintly impregnated.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 76 G. C. KÜPPERS ET AL.

Figure 1. Location of the sampling site in Buenos Aires province, Argentina. a. Aerial view. b, c. The pond during a rainy period (b) and a dry phase (c).

This species occurred in the pond from late Order Prostomatida Schewiakoff autumn to winter and early spring. It was not Coleps hirtus hirtus (Müller) recorded at temperatures over 11 °C. The highest Foissner, Berger & Schaumburg densities occurred at the lowest conductivity values, (Table IV; Fig. 2d) alkaline pH, and over 70 % of dissolved oxygen saturation (Fig. 4). Cyclidium glaucoma Müller and Body barrel-shaped. In vivo with pretzel-like Halteria grandinella (Müller) Dujardin were cortical windows and three posterior cortical observed inside the food vacuoles of A. volvox in spines. Symbiotic algae are absent. Somatic Protargol stained preparations. kineties composed by dikinetids. With single

caudal cilium. Dorsal brush in three groups with Rhabdoaskenasia minima Krainer & Foissner two longitudinal rows of basal bodies each. (Table III; Fig. 2c) First group with four basal bodies in each row and the other groups with three basal bodies in Body pyriform, with rounded posterior end. each row. External pectinelles with two basal With a single contractile vacuole. Macronucleus bodies and internal pectinelles with four basal reniform. Oral dome surrounded by a circumoral row of dikinetids that give rise to the rhabdos. bodies. Somatic kineties, arranged in a pre-equatorial kinety Coleps hirtus hirtus was only absent in girdle with single kinetosomes in each row; an autumn. The maximum abundance of this species equatorial girdle also with single kinetosomes; a was observed under the highest temperatures, sub-equatorial girdle of bristles, with 2 kinetosomes intermediate conductivity values (183 µS cm-1), low in each row. dissolved oxygen saturation (49 %) and slightly This species occurred in late autumn. acid pH (Fig. 4).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 Morphological aspects and seasonal changes of planktonic ciliates 77

Table I. Morphometric data on Teutophrys trisulca africana. in vivo X Min Max M SD N Body, length 261.3 238 280 266 21.4 3 Body, width 126 112 140 126 14 3

After Protargol X Min Max M SD N Body, length 207.2 168 252 210 22.7 10 Body, width 98 84 112 98 8.4 8

Oral arms, length 128.7 112 154 126 10.1 13

Oral extrusomes, length 5.9 5 7 5.6 0.7 13

Somatic extrusomes, length 5.9 2.8 8 6 1.6 13 Somatic extrusomes, width 0.7 0.7 0.7 0.7 0 13

Pigmented granules, width 1.8 0.7 2.8 2.1 0.8 13

Table II. Morphometric data on Askenasia volvox. in vivo X Min Max M SD N Body, length 46.7 35 63 45.5 9.5 6 Body, width 38.5 35 42 38.5 3.8 6

Groups of anterior cilia, 7 7 7 7 0 3 number

After Protargol X Min Max M SD N Body, length 51.8 49 63 49 4.2 20 Body, width 46.5 42 56 49 4.7 20

Somatic kineties, number 49.9 46 53 50.5 2.7 20 Kinetosomes in pre- 11 8 14 10 1.9 20 equatorial girdle, number Paired kinetosomes in 9.5 9 10 9.5 0.7 2 equatorial girdle, number Kinetosomes in sub- 3 3 3 3 0 20 equatorial girdle, number

Kinetosomes per circumoral 4.5 3 5 5 0.6 20 lobe, number

Macronucleus, length 18 11.2 25.2 19.3 4.4 10 Macronucleus, width 15.1 10 26.6 14.7 5.2 10

Micronucleus, diameter 3.1 2.8 3.5 2.8 0.4 5

Five somatic kineties, three of them form a caudal Order Choreotrichida Small & Lynn spiral and the other two are shorter. Oral apparatus Strobilidium caudatum (Fromentel) Foissner composed by a closed ring of external (Table V; Figs. 2e and 3d, e) membranelles, some of which enlarge into the oral cavity, one internal membranelle, and the endoral Body pyriform, posteriorly pointed and kinety. Some specimens had irregularly spaced truncated. Horse shoe-shaped macronucleus. extrusomes and pigmented granules in the posterior Contractile vacuole at the posterior end of the body. half of the body.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 78 G. C. KÜPPERS ET AL.

Table III. Morphometric data on Rhabdoaskenasia minima. After Protargol X Min Max M SD N Body, length 52.5 42 63 52.5 14.8 2 Body, width 45.5 42 49 45.5 4.9 2

Somatic kineties, number 77.5 75 80 77.5 3.5 2 Kinetosomes in pre-equatorial 8.5 8 9 8.5 0.6 4 girdle, number Kinetosomes in sub-equatorial 2 2 2 2 0 4 girdle, number

Circumoral paired granules, 32 32 32 32 0 1 number

Macronucleus, maximum 29.4 29.4 29.4 29.4 0 1 length

Table IV. Morphometric data on Coleps hirtus hirtus. in vivo X Min Max M SD N Body, length 61.5 61.5 61.5 61.5 0 1 Body, width 24.6 24.6 24.6 24.6 0 1

After Protargol X Min Max M SD N Body, length 40 35 49 38.8 4.9 12 Body, width 17.9 11.2 28 17.8 4.2 12

Cytopharynx, length 11.4 8.4 14.7 11.2 2.1 7

Somatic kineties, number 13 11 15 13 1.2 7 Paired kinetosomes per 13 12 14 13 0.5 8 somatic kinety, number

External pectinelles, number 10 10 10 10 0 2 Kinetosomes per external 2 2 2 2 0 3 pectinelle, number Internal pectinelles, number 10 10 10 10 0 2 Kinetosomes per internal 4.4 4 5 4 0.5 5 pectinelle, number

Paired kineties in dorsal brush, 3 3 3 3 0 3 number Paired kinetosomes in dorsal 4 4 4 4 0 2 brush kinety 1, number Paired kinetosomes in dorsal 3 3 3 3 0 2 brush kinety 2, number Paired kinetosomes in dorsal 3 3 3 3 0 2 brush kinety 3, number

Macronucleus, length 10.1 7 16.8 9.1 2.8 10 Macronucleus, width 11.2 6.3 17.5 10.5 3.1 10

Micronucleus, diameter 1.4 1.4 1.4 1.4 0 2

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 Morphological aspects and seasonal changes of planktonic ciliates 79

Figure 2. Morphology of the species recorded, composite from protargol impregnation and live observation (a, b, j) and protargol impregnation only (c-i). a. Teuthophrys trisulca africana. b. Askenasia volvox. c. Rhabdoaskenasia minima, circumoral wreath of granules (left arrowhead), two sub-equatorial kinetosomes (right arrowhead). d. Coleps hirtus hirtus, cytopharynx (C), dorsal brush (DB), external pectinelles (EP), internal pectinelles (IP). e. Strobilidium caudatum, ventral view. f. Halteria grandinella, equatorial somatic kinety (arrowhead). g. Limnostrombidium pelagicum, ventral view. h. Limnostrombidium viride, ventral view, symbiont (S). i. Pelagostrombidium mirabile, ventral view. j. Hypotrichidium conicum, ventral view, contractile vacuole (arrowhead). (a) scale bar = 50 µm; (b-f, i) scale bar = 10 µm; (g, h, j) scale bar = 20 µm.

Strobilidium caudatum was only absent in oxygen concentrations. This ciliate was recorded late winter and late spring. This non under acid as well as alkaline pH values (Fig. 4). It euplanktonic species reached the maximum was also observed adhered to artificial substrates. It densities in coincidence with high conductivity, could be maintained in wheat cultures for a short low temperatures, and intermediate dissolved time.

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Figure 3. Morphology of the species recorded, after protargol impregnation. a. Teuthophrys trisulca africana, aboral view. b. Askenasia volvox. c. A. volvox, circumoral wreath of granules (left arrowhead) and three subequatorial kinetosomes (right arrowhead). d. Strobilidium caudatum, dorsal view, extrusomes (arrowhead). e. S. caudatum, oral view, caudal spiral (arrowhead). f. Limnostrombidium pelagicum, ventral view, ventral kinety (arrowhead). g. L. pelagicum, oral view. h. L. viride, symbionts near the oral region (arrowhead). i. L. viride, ventro-posterior view, clavate cilia in equatorial girdle (left arrowhead) and neoformation organelle (right arrowhead). j. Hypotrichidium conicum, ventral view, single frontal cirri (top arrowhead) and posterior rows of cirri (down arrowhead). k. H. conicum, dorsal view, posterior rows of cirri (arrowhead). (a, f, j, k) scale bar = 20 µm. (b-e, g) scale bar = 10 µm.

Order Halteriida Petz & Foissner wide range of conductivity, pH and dissolved Halteria grandinella (Müller) Dujardin oxygen concentration (Fig. 4).

(Table VI; Fig. 2f) Order Strombidiida Petz & Foissner The most important features to separate this Limnostrombidium pelagicum (Kahl) Krainer species from its congeners are the absence of (Table VII; Figs. 2g and 3f, g) symbiotic algae and the disposition of basal bodies in the equatorial somatic kineties in four groups, two Body conical-shaped, narrowed posteriorly. of them with two kinetosomes each and the other With an equatorial girdle of extrusomes, lined by a two with four kinetosomes each. ring of somatic dikinetids with clavate cilia. Ventral Halteria grandinella was recorded somatic kinety with paired kinetosomes. Oral throughout the studied period. The highest densities apparatus composed by an open ring of collar and occurred at temperatures below 11°C but under a ventral membranelles, and the endoral kinety.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 Morphological aspects and seasonal changes of planktonic ciliates 81

Without endosymbiotic algae. Macronucleus half of the body and near equatorial extrusomes. globular; micronuclei elliptical and indented in the This species was recorded from winter to late spring. posterior pole of the macronucleus. With numerous It was maintained for a few days in wheat infusion ovoid pigmented granules, mainly in the posterior cultures.

Table V. Morphometric data on Strobilidium caudatum. in vivo X Min Max M SD N Body, length 71.4 42 98 84 24.4 5 Body, width 50.1 28 68.6 56 17.7 5

After Protargol X Min Max M SD N Body, length 72.2 56 84 70 6.6 16 Body, width 59.1 49 70 56 5.1 16

Peristome, diameter 45 35 56 42 5.6 17

Apex to end of cytopharyngeal 42 33.3 50 43.3 5.2 13 fibers, distance

Macronucleus, length 7 5.6 8.4 7 1 10 Macronucleus, width 32.1 23.1 39.2 39.2 4.6 9

Micronucleus, length 2.7 2.1 3.2 2.8 0.3 6 Micronuclei, number 1 1 1 1 0 6

Somatic kineties, number 5 5 5 5 0 20

External polykineties, number 19 18 21 20 0.8 20 Enlarged external polykineties, 6 4 7 6 0.9 18 number Internal polykineties, number 1 1 1 1 0 11

Extrusomes, length 3.9 3.3 5 3.3 0.9 11 Extrusomes, width 1 0.7 1.4 1 0.3 11

Table VI. Morphometric data on Halteria grandinella. After Protargol X Min Max M SD N Body, length 24 21 28 23.8 2.8 13 Body, width 22.7 19.6 28 22.4 2 13

Equatorial somatic kineties, 7 6 7 7 0.4 16 number

Adoral polykinetids, number 16 15 17 16 0.7 15 Ventral polykinetids, number 7 6 7 7 0.5 4

Macronucleus, length 9.5 8.4 11.2 9.1 1 10 Macronucleus, width 16 9.1 21 16.4 3.3 10

Micronucleus, length 2.5 2.1 2.8 2.8 0.4 5 Micronucleus, width 2.2 2.1 2.8 2.1 0.3 5

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Table VII. Morphometric data on Limnostrombidium pelagicum. After Protargol X Min Max M SD N Body, length 61.8 48 80 60 9.2 30 Body, width 46.4 35 60 45 8.4 30

Adoral polykinetids, number 16 16 16 16 0 22 Ventral polykinetids, number 12 10 14 12 0.9 25

Ventral somatic kinety, 11 8 12 11 1 22 number of basal body pairs

Macronucleus, length 17.3 14 22 17 2.6 25 Macronucleus, width 21 14 27 21 3.2 25

Micronucleus, diameter 2.7 2.1 3.5 2.8 0.4 15 Micronucleus, number 2 1 2 2 0.3 15

Pigmented granules, diameter 2.3 2.1 2.8 2.1 0.3 25

Table VIII. Morphometric data on Limnostrombidium viride. After Protargol X Min Max M SD N Body, length 56 40 70 55 8.2 30 Body, width 42.1 30 55 40 5.9 30

Adoral polykinetids, number 16 16 16 16 0 12 Ventral polykinetids, number 13 11 15 13 0.9 18

Ventral somatic kinety, 15 13 18 15 1.2 20 number of basal body pairs

Macronucleus, length 19.9 13 25 21 3.6 10 Macronucleus, width 24.7 20 28 24 3 10

Micronucleus, diameter 2.9 2.1 3.5 2.8 0.4 9 Micronucleus, number 1.1 1 2 1 0.3 9

Pigmented granules, diameter 2.2 1.5 2.8 2.1 0.4 20

Equatorial extrusomes, number 12 10 14 12 2 3 of groups Equatorial extrusomes, 5.9 5.6 7 5.6 0.5 8 diameter of groups

Symbionts, diameter 8.9 5.6 10 9.4 1.4 8

(13-18) in ventral kinety and the number of Limnostrombidium viride (Stein) Krainer ventral membranelles (11-15) are also slightly (Table VIII; Figs. 2h and 3h, i) different. This species was recorded during This species is similar to L. pelagicum autumn and winter, coexisting with but it mainly differs in that it maintains L. pelagicum. Both species reached the functional plastids (cleptoplasts) from the algae maximum abundances at temperatures below it feeds on. The number of paired kinetosomes 8 °C (Fig. 4).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 Morphological aspects and seasonal changes of planktonic ciliates 83

Table IX. Morphometric data on Pelagostrombidium mirabile. in vivo X Min Max M SD N Body, length 40 40 40 40 0 3 Body, width 28.3 25 30 30 2.8 3

After Protargol X Min Max M SD N Body, length 42.2 30 60 40 7 24 Body, width 32.5 25 50 30 5.7 24

Adoral polykinetids, number 15 13 16 15 1 11 Ventral polykinetids, number 12 10 14 12 1.1 17

Macronucleus, length 20.2 16.8 28 19.8 2.8 12 Macronucleus, width 18.7 12.6 28 16.8 5.1 11

Micronucleus, diameter 4.8 4.2 5.6 4.9 0.5 9

Extrusomes, length 19.6 15.4 25.2 18.2 5 3

Table X. Morphometric data on Hypotrichidium conicum. in vivo X Min Max M SD N Body, length 105 98 112 105 9.8 2 Body, width 70 56 84 70 19.7 2

Buccal cavity, depth 56 56 56 56 0 2

After Protargol X Min Max M SD N Body, length 128.1 98 168 126 17.7 30 Body, width 88.2 63 112 87.5 14 30

Buccal cavity, depth 82.1 70 98 84 9.5 30

Frontal cirri, number 1 1 1 1 0 20 Frontal rows of cirri, number 4 4 4 4 0 30 Number of cirri, 1st frontal row 6 4 7 6 0.7 20 2nd frontal row 6 5 7 6 0.5 20 3rd frontal row 11 10 13 12 1.1 20 4th frontal row 14 11 16 13 1.5 20

Posterior rows of cirri, number 6 6 6 6 0 20

Rows of dorsal bristles, number 3 3 3 3 0 11

Oral polykinetids, number 41 34 49 40 3.7 20

Macronucleus, length 28.7 21 63 28 9 20 Macronucleus, width 17.8 14 21 21 3.6 20

Micronucleus, length 3.2 2.8 4.2 3.5 0.4 20 Micronucleus, width 2.7 2.1 3.5 2.8 0.3 20 Micronucleus, number 2 2 2 2 0 20

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 84 G. C. KÜPPERS ET AL.

Table XI. Compared physical and chemical variables (V) under which the species were found. T, temperature (°C); DO, dissolved oxygen (mg L-1); C, conductivity (µS cm-1).

Species V Our observations Other authors Locality Citation T 8.6 5.2 - 8.7 pH 5.4 8.4 France, Foissner et al. Teuthophrys trisulca africana DO 6.3 6.7 - 10.2 Germany (1999) C 220 ⎯

T 2.4 - 10.8 2.0 - 21.0 pH 4.5 - 8.4 5.0 - 9.5 Foissner et al. Askenasia volvox Germany DO 5.5 - 8.8 5.1 - 15.9 (1995) C 160 - 220 ⎯

T 2.39 ⎯ pH 4.97 ⎯ Rhabdoaskenasia minima ⎯ ⎯ DO 5.47 ⎯ C 220 ⎯

T 2.39-19.17 1-30 Austria, pH 4.97-8.57 4.7-9.5 Bick & Kunze Coleps hirtus hirtus Bulgaria, DO 4.53-9.65 0-38 (1971) Germany C 145-276 ⎯

T 2.4 - 20.8 5.3 - 29 Austria, pH 4.9 - 7.5 4.9 - 9.0 Foissner et al. Strobilidium caudatum Bulgaria, DO 5.5 - 8.8 4.0 - 11.0 (1991) USA C 160 - 220 ⎯

T 2.39-19.17 0.8-35 Austria, pH 4.97-8.57 4.2-9.8 Bulgaria, Foissner et al. Halteria grandinella DO 4.53-9.65 0-38 Germany, (1999) Hungary, C 145-276 ⎯ USA

T 9.4 - 24.1 10.6 - 21.4 pH 6.3 - 6.8 ⎯ Limnostrombidium pelagicum USSR Belova (1989) DO 6.3 - 7.9 ⎯ C 120 - 220 ⎯

T 2.4 - 20.8 1.4 - 21 Germany, pH 4.9 - 8.4 6.1 - 9.5 Foissner et al. L. viride Hungary, DO 5.5 - 8.8 0.2 - 15.9 (1991) USA C 145 - 220 ⎯

T 6.7 - 10.8 ⎯ pH 7.8 - 8.4 ⎯ Pelagostrombidium mirabile ⎯ ⎯ DO 6.6 - 8.0 ⎯ C 145 - 189 ⎯

T 24.7 3.0 - 27.5 pH 6.82 6.4 - 7.2 Foissner et al. Hypotrichidium conicum Slovakia DO ⎯ 1.5 - 5.8 (1999) C 190 ⎯

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 Morphological aspects and seasonal changes of planktonic ciliates 85

Pelagostrombidium mirabile (Penard) Krainer 2005. Pelagostrombidium mirabile appeared for the (Table IX; Fig. 2i) first time in July 2004 (2917 ind L-1) and was present in the pond only until September, when it -1 Body ellipsoidal, posteriorly narrower than reached the highest numbers (8066 ind L ). anteriorly, mostly covered by polygonal cortical Askenasia volvox was present from June to platelets. Cytoplasm yellowish-green due to the September 2004 and in June 2005, mostly in low numbers (less than 400 ind L-1) except during presence of cleptoplasts. Girdle of somatic -1 extrusomes lined by a non-ciliated ring of September 2004 (1233 ind L ). Strobilidium kinetosomes, continuous at the buccal vertex. Adoral caudatum was not found in the pond only in August zone of membranelles as an opened ring, composed and December 2004, and attained the highest densities during June 2004 (1000 ind L-1) and April of collar and ventral membranelles that end below -1 mid-body. Endoral kinety at the right margin of the 2005 (2283 ind L ), when it was the most abundant buccal cavity. species. Limnostrombidium spp. could not be This species was recorded in late winter and identified to species level in Lugol preserved samples and the highest number of individuals was early spring. The density peaks occurred under -1 alkaline pH, low temperature (11 °C) and low recorded during June 2004 (2783 ind L ). conductivity values, while the dissolved oxygen Limnostrombidium spp. were not recorded during concentration was high (72 % of saturation) December 2004 and June 2005. (Fig. 4). Rhabdoaskenasia minima, Teuthophrys trisulca africana, and Hypotrichidium conicum were Order Stichotrichida Fauré-Fremiet not detected in Lugol fixed samples. Hypotrichidium conicum Ilowaisky (Table X; Figs. 2j and 3j, k) Discussion Teuthophrys trisulca africana is recorded for the first time in South America. Our specimens Body pyriform, posteriorly widened and match better with the African specimens observed with a cytoplasmic process. Two macronuclear by Dragesco & Dragesco-Kernéis (1986), since it is nodules, with one indented micronucleus each. apochlorotic, although the macronucleus is not dumb Contractile vacuole on the left, lateral to the bell-shaped but vermiform and coiled. Foissner et al. peristome and in the superior third of the body. (1999) also found apochlorotic specimens from mud Single frontal cirrus in front of the paroral samples in Australia. It is considered a rare species, membrane and four rows of frontal cirri to the right which prefers the spring (Foissner et al. 1999), of the peristome. Six oblique rows of posterior cirri although we found it for the first time in autumn and and 3 dorsal rows of dikinetids. Buccal field late spring. relatively long, extending up to ¾ of body length. Askenasia volvox was previously cited in a Paroral and endoral kineties cross at the right margin water quality paper (Zaleski & Claps 2000) for a of the buccal cavity. eutrophic shallow lake from Buenos Aires province This species was recorded in spring and it but no description is available. The species was also grew from mud samples in summer. It was recorded in South America by Pinto (1925) in Brazil maintained in wheat cultures for a short time. and by Wölfl (1996) in Chile, also without Table XI shows the ranges of the physical description. The number of paired kinetosomes in and chemical variables under which this species, as the equatorial kinety girdle is lower (9-10) than that well as the other ones, were recorded. found by Packroff & Wilbert (1991) (18-20).

Rhabdoaskenasia minima is a new record Species abundances and variation along an for South America. Morphometric data are annual cycle coincident with those of Krainer & Foissner (1990), The most abundant species were Halteria although the extrusomes of our specimens were not grandinella, Coleps hirtus hirtus, and well impregnated and this is a key character Pelagostrombidium mirabile. Halteria grandinella according to Foissner et al. (1999). In this study, it was present in the pond along the whole studied was identified as R. minima due to the presence of a period, reaching the highest abundances in July 2004 very conspicuous rhabdos, single kinetosomes in the -1 (18916 ind L ). The greatest densities of C. h. hirtus equatorial kinety girdle, two basal bodies in the sub- - were recorded during December 2004 (11366 ind L equatorial kinety girdle, and a single contractile 1), being relatively scarce in the other months (less vacuole. The previously cited authors recorded this than 600 ind L-1) and was not found during June species along the whole year, peaking in autumn

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 86 G. C. KÜPPERS ET AL.

Figure 4. Ranges of species densities (ind L-1) related to conductivity and temperature (left column) and to dissolved oxygen and pH (right column).

(2670 ind L-1 and 1720 ind L-1) and feeding on authors (Foissner et al. 1994, 1999). Urotricha sp. On the contrary, we only found it once Strobilidium caudatum is a new record for in winter and coexisting with A. volvox. Argentina. It was previously observed in South Coleps hirtus hirtus was previously cited in America by Bürger (1909) in Chile, and by Guillén- Argentina and South America by other authors (de la Aguirre (2002) in Peru. Most morphometric data are Rua 1911, Cela 1972, Guillén-Aguirre 2002), coincident with those observed by other authors although it was only observed in vivo and (Foissner et al. 1991, Petz & Foissner 1992). The after supravital staining. Morphometry is number of external membranelles coincides with the coincident with the observation of other observations of Petz & Foissner (1992), although

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Foissner et al. (1991) mentioned a wider range (18- species developed from mud samples when the pond 21 vs 22-30, respectively). On the other hand, we went through a drought period, we assume it is able observed cortical extrusomes and pigmented to form resting cysts, although they were not granules in some individuals, which was not cited by observed. The contractile vacuole was located on the other authors and would need further investigation. left side, lateral to the peristome on the superior Halteria grandinella is a cosmopolitan third of the body as in H. tisiae, and not near the species, which was previously cited in Argentina cytostome, as stated in Foissner et al. (1991, 1999). and South America (de la Rua 1911, Cela 1972, It is different from the previously mentioned species Guillén-Aguirre 2002), although it was only studied by having six posterior rows of cirri, and, for this in vivo or by supravital staining. Morphometric reason, it was identified in this study as H. conicum. characters are coincident with the observations of Concerning the seasonal variation of the other authors (Fauré-Fremiet 1951, Dragesco 1970, species found, the highest density of Askenasia Foissner et al. 1999) but Song & Wilbert (1989) vovlox was recorded in early spring, while other observed a higher number of equatorial somatic authors found low numbers during the cold half of kineties (9-10 groups). the year (Wang 1928, Wilbert 1969, Foissner et al. Limnostrombidium pelagicum is a new 1999). Coleps hirtus hirtus was recorded throughout record for South America. It could have been the year, as found in previous studies, along a mistaken by other Argentinean researchers with L. maximum in spring (Foissner et al. 1999). The viride as was also pointed by Foissner et al. (1999) highest numbers of Strobilidium caudatum were for other localities. Morphometric characters observed during autumn, when macrophytes were coincide with those stated in Foissner et al. (1999), present in the pond, while Wilbert (1969) found although we observed a slightly higher number of 60000 ind L-1 during summer in a eutrophic stream basal body pairs in the ventral kinety (7-10 vs 8-12, from Germany. Halteria grandinella occurred in respectively) and numerous ovoid pigmented more than 1000 ind L-1, which indicates eutrophic or extrusomes, mainly in the posterior half of the body highly eutrophic conditions (Foissner et al. 1999). and near the equatorial extrusomes. Limnostrombidium pelagicum could not be Limnostrombidium pelagicum became very similar distinguished from L. viride in Lugol fixed samples to L. viride after a few days in culture, when it lost but, in coincidence with the findings of Krainer the plastids and presumably began to feed on (1991, 1995) in Austria, we observed higher bacteria. numbers of both species in spring and summer. Limnostrombidium viride is a new record for Limnostrombidium viride was very abundant in Buenos Aires province. It has been previously found autumn after the summer drought, while other in Argentina by Seckt (1924), in Córdoba province, authors found higher numbers in summer (Foissner who mentioned it in a checklist, without taxonomic et al. 1999) and summer and autumn (Modenutti & description, and by Modenutti & Pérez (2001), in an Pérez 2001). Mixotrophic ciliates are known to be Andean lake. Morphometric characters are dominant in oligotrophic environments due to the coincident with those described by other authors accessibility to scarce nutrients (Fenchel 1987), (Kahl 1932, Foissner et al. 1991, 1999), although in which along with the bacterivorous feeding regime the present study the specimens possessed few allow L. viride to inhabit very different habitats, symbionts and of larger size than those described in such as ultraoligotrophic lakes in Patagonia Foissner et al. (1999), which were 6 × 3.2 μm and (Modenutti & Pérez 2001) and, as in the present possibly belonging to genus Kirchneriella. study, a eutrophic shallow pond, being tolerant to a Pelagostrombidium mirabile is a new record wide range of environmental characteristics. for South America, while other authors only found it Pelagostrombidium mirabile appeared only during in Eurasia (Foissner et al. 1999). The morphometric winter and spring, while Krainer (1991) found it characters of this species match with the descriptions abundantly throughout the year in eutrophic of Penard (1922), Krainer (1991), and Foissner et al. groundwater ponds in Austria, peaking in autumn. (1999), although the range of ventral membranelles Most of the ecological characteristics in our observations is lower than that stated in recorded coincide with other findings (Table XI). In Foissner et al. (1999) (10-14 vs 12-17, respectively). addition, the physical and chemical variables under Hypotrichidium conicum is a new record for which Rhabdoaskenasia minima and the ciliate fauna from South America. This Pelagostrombidium mirabile were found, were not cosmopolitan and typical euplanktonic species has mentioned by other authors. Teuthophrys trisulca been found in other ephemeral and eutrophic africana was recorded under lower pH conditions environments (Foissner et al. 1991, 1999). As the than those stated in its ecological summary by

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90 88 G. C. KÜPPERS ET AL.

Foissner et al. (1999). microfauna de la República Argentina. The presence of the species dealt within this Protozoos. Ph.D. Thesis. Universidad study in an unpredictable environment such as this Nacional de Buenos Aires, Buenos Aires, temporary pond is related to their bacterivorous Argentina, 49 p. regime (Fenchel 1987) as a primary or secondary Dragesco, J. 1970. Ciliés libres du Cameroun. option, their tolerance to a wide range of Annales de la Faculté des Sciences (Numéro environmental conditions, when the pond was filled, hors série), Université Fédérale du Cameroun, and their ability to produce resting cysts (Foissner Yaoundé, 141 p. 1987) to survive during dry periods. Dragesco, J. & Dragesco-Kernéis, A. 1986. Ciliés libres de l’Afrique intertropicale. Introduction Acknowledgments à la connaissance et à l’étude des ciliés. Norbert Wilbert from Zoologisches Institut der Faune Tropicale, 26: 1-159. Universität Bonn, Germany, is greatly Fauré-Fremiet, E. 1951. La bipartition énantiotrope acknowledged for his unconditional help. Thanks go chez les ciliés oligotriches. Archives d' also to C. Ituarte and L. Lunaschi from the División Anatomie Microscopique et de Zoología Invertebrados, Museo de La Plata, S. Morphologie Experimental, 42: 209-225. Kleinman for improving the English, and M. Fenchel, T. 1987. Ecology of Protozoa: The Meléndez for his help with the Portuguese. Support biology of free-living phagotrophic protists. of the Consejo Nacional de Investigaciones Science Technical Publishers, Madison, 197 Científicas y Técnicas (CONICET), Argentina, to p. which the authors belong, is gratefully Foissner, W. 1987. Soil Protozoa: fundamental acknowledged. problems, ecological significance, adaptations in ciliates and testaceans, bioindicators, and References guide to the literature. Progress in Andrushchyshyn, O., Magnusson, A. K. & Williams, Protistology, 2: 69-212. D. D. 2003. Ciliate populations in temporary Foissner, W., Berger, H., Blatterer, H. & Kohmann, freshwater ponds: seasonal dynamics and F. 1995. Taxonomische und ökologische influential factors. Freshwater Biology, 48: Revision der Ciliaten des Saprobiensystems 548-564. - Band IV: Gymnostomatea Loxodes, Barría, M. S. 2002. Citología, bioecología y Suctoria. Informationsberichte des Bayer, taxonomía de Tintinnida (Ciliophora). PhD. Landesamtes für Wasserwirtschaft, München, Thesis. Universidad Nacional del Sur, Bahía Heft 1/95, 540 p. Blanca, Argentina, 213 p. Foissner, W., Berger, H. & Kohmann, F. 1994. Belova, S. L. 1989. Seasonal changes in the Taxonomische und ökologische Revision composition of the Mozhaiskreservoir der Ciliaten des Saprobiensystems - Band infusoria. Gidrobiologicheskii Zhurnal, 25: III: Hymenostomata, Prostomatida, 29-32. Nassulida. Informationsberichte des Bayer, Bick, H. & Kunze, S. 1971. Eine Zusammestellung Landesamtes für Wasserwirtschaft, München, von autökologischen und saprobiologischen Heft 1/94, 548 p. Befunden an Süßwasserciliaten. Foissner, W., Berger, H., Schaumburg, J. 1999. Internationale Revue der gesamten Identification and ecology of limnetic Hydrobiologie und Hydrographie, 56: 337- plankton ciliates. Informationsberichte des 384. Bayer, Landesamtes Wasserwirtschaft, Bürger, O. 1909. Nuevos estudios sobre protozoos München, Heft 3/99, 793 p. chilenos del agua dulce. Anales de la Foissner, W., Blatterer, H., Berger, H. & Kohmann, Universidad de Chile, 122: 137-204. F. 1991. Taxonomische und ökologische Cela, A. M. 1972. Algunos ciliados vinculados a la Revision der Ciliaten des Saprobiensystems vegetación flotante. Physis, 31 (83): 559-577. - Band I: Cyrtophorida, Oligotrichida, Clesceri, L. S., Greenberg, A. E. & Eaton, A. D. Hypotrichia, Colpodea. Informationsberichte (Eds.). 1998. Standard methods for the des Bayer, Landesamtes für Wasserwirtschaft, examination of water and wastewater. 20th München, Heft 1/91, 478 p. edition. American Public Health Association, Guillén-Aguirre, G. K. 2002. Diversidad Washington, D.C., 1325 p. protozoológica de los Pantanos de Villa, de la Rua, J. M. 1911. Contribución al estudio de la Chorrillos-Lima-Perú. PhD. Thesis.

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Universidad Nacional Mayor de San Marcos, (Ciliophora: Hypotrichea) from Brazilian Peru, 151 p. locations, including a description of Kahl, A. 1932. Urtiere oder Protozoa I: Wimpertiere Apoamphisiella foissneri sp. n. Zootaxa, 505: oder Ciliata (Infusoria) 3. Spirotricha. p. 399- 1-26. 650. In: Dahl F. (Ed.). Die Tierwelt Paiva, T. S. & Silva-Neto, I. D. da. 2004c. Ciliate Deutschlands 25. G. Fischer, Jena, 886 p. protists from Cabiúnas Lagoon (Restinga de Krainer, K. H. 1991. Contributions to the Jurubatiba, Macaé - Rio de Janeiro) with morphology, infraciliature and ecology of emphasis on water quality indicator species some planktonic ciliates Strombidium and description of Oxytricha marcili sp. n. pelagicum n. sp., Pelagostrombidium mirabile Brazilian Journal of Biology, 64: 465-478. (Penard, 1916) n. g., n. comb., and Paiva, T. S. & Silva-Neto, I. D. da. 2005. Pelagostrombidium fallax (Zacharias, 1896) Morphology, biometry and ontogenetic n. g., n. comb. (Ciliophora, Oligotrichida). aspects of Deviata estevesi sp.n. (Ciliophora: European Journal of Protistology, 27: 60- Hypotrichea), a new ciliate from a restinga 70. lagoon in Rio de Janeiro. Acta Krainer, K. H. 1995. Taxonomische Untersuchungen Protozoologica, 44: 351-362. an neuen und wenig bekannten planktischen Pettigrosso, R. E. 2001. Estudio taxonómico y Ciliaten (Protozoa, Ciliophora) aus ecológico de ciliados planctónicos Baggerseen in Österreich. Lauterbornia, 21: (Ciliophora: Choreotrichida y Strombidiida) 39-68. del estuario de Bahía Blanca, Argentina. PhD. Krainer, K. H. & Foissner, W. 1990. Revision of the Thesis. Universidad Nacional del Sur, Bahía genus Askenasia Blochmann, 1895, with Blanca, Argentina, 173 p. proposal of two new species, and description Pettigrosso, R. E. 2003. Planktonic ciliates of Rhabdoaskenasia minima n. g., n. sp. Choreotrichida and Strombidiidae from the (Ciliophora, Cyclotrichida). Journal of inner zone of Bahía Blanca estuary, Protozoology, 37: 414-427. Argentina. Iheringia, série Zoologia, 93: 117- Modenutti, B. E. & Claps, M. C. 1986. Ciliados 126. dulceacuícolas de la Argentina, III: Pettigrosso, R. E. & Barría, M. S. 2004. Ciliados Ciliophora-Peritricha. Revista de la planctónicos. p. 121-131. In: Piccolo, M. C. & Asociación de Ciencias Naturales del Hoffmeyer, M. S. (Eds.). Ecosistema del Litoral, 17 (1): 71-78. estuario de Bahía Blanca. IADO, Bahía Modenutti, B. E. & Pérez, G. L. 2001. Planktonic Blanca, Argentina, 233 p. ciliates from an oligotrophic south Andean Pettigrosso, R. E., Barría de Cao, M. S. & Popovich, lake, Morenito lake (Patagonia, Argentina). C. A. 1997. Planktonic ciliates during a Brazilian Journal of Biology, 61: 389-395. diatom bloom in Bahía Blanca Estuary, Penard, E. 1922. Études sur les infusoires d’eau Argentina. I Aloricate. Oebalia, 23: 21-31. douce. George & Cie, Genève, 331 p. Petz, W. & Foissner, W. 1992. Morphology and Packroff, G. & Wilbert, N. 1991. Taxonomischen morphogenensis of Strobilidium caudatum Studien über die Ciliatenfauna (Protozoa, (Fromentel), Meseres corlissi n. sp., Halteria Ciliophora) der Eifelmaare. Archiv für grandinella (Müller), and Strombidium Protistenkunde, 140: 121-139. rehwaldi n. sp., and a proposed phylogenetic Paiva, T. S. & Silva-Neto, I. D. da. 2003. Optical system for oligotrich ciliates (Protozoa, microscopy observations and diagnosis of Ciliophora). Journal of Protozoology, 39: Apoamphisiella jurubatiba sp. n. (Ciliophora: 159-176. Hypotrichea). Acta Microscopica, 12 Pinto, C. 1925. Protozoarios observados no Brasil. Supplement B: 287-288. Memorias do Instituto Oswaldo Cruz, 18: Paiva, T. S. & Silva-Neto, I. D. da. 2004a. 211-301. Description of Parentocirrus brasiliensis sp. Seckt, H. 1924. Estudios hidrobiológicos en la n. (Ciliophora: Spirotrichea), a new ciliate Argentina. Revista de la Universidad protist present in activated sludge. Zootaxa, Nacional de Córdoba, 11: 55-110. 504: 1-10. Song, W. & Wilbert, N. 1989. Taxonomische Paiva, T. S. & Silva-Neto, I. D. da. 2004b. Untersuchungen an Aufwuchsciliaten Comparative morphometric study of three (Protozoa, Ciliophora) im Poppelsdorfer species of Apoamphisiella Foissner, 1997 Weiher, Bonn. Lauterbornia, 3: 1-222.

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Utermöhl, H. 1958. Zur Vervollkommung der Protargolimprägnation für Ciliaten. quatitativen Phytopankton-Methodik. Mikrokosmos, 64 (6): 171-179. Mitteilungen. Internationale Vereiningung Williams, D. D. 2001. The ecology of temporary fuer Theoretische Angewandte Limnologie, waters. The Blackburn Press, Caldwell, New 9: 1-38. Jersey, 205 p. Vucetich, M. C. 1972. Presencia en la Argentina de Wölfl, S. 1996. Untersuchungen zur Ascobius lentus Henneguy (Ciliata, Zooplanktonstruktur einschließlich der Folliculinidae). Neotrópica, 18 (56): 91-93. mikrobiellen Gruppen unter besonderer Vucetich, M. C. & Escalante, A. H. 1979. Peritricos Berücksichtigung der mixotrophen Ciliaten in loricados de ambientes lénticos del área zwei südchilenischen Andenfußseen. PhD. platense (Ciliata, Peritrichida). Neotrópica, Thesis. Universität Konstanz, Germany, 25 (74): 187-194. 242 p. Wang, C. C. 1928. Ecological studies of the seasonal Zaleski, M. & Claps, M. C. 2000. Ciliados distribution of protozoa in a freshwater pond. indicadores de la calidad de agua de la laguna Journal of Morphology, 46: 431-478. San Miguel del Monte (Buenos Aires). Wilbert, N. 1969. Ökologische Untersuchung der Diversidad y Ambiente, 1: 45-51. Aufwuchs und Planktonciliaten eines eutrophen Weihers. Archiv für Hydrobiologie, Supplement 35: 411-518. Wilbert, N. 1975. Eine verbesserte Technik der

Received July 2006 Accepted August 2006 Published online September 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 74-90

Ocupação da praia da Boa Viagem (Recife/PE) ao longo de dois dias de verão: um estudo preliminar

1,2 1 JACQUELINE S. DA SILVA , SCHEYLA C. T. BARBOSA , MÔNICA M. V. LEAL, 1 ANA R. LINS & MONICA F. DA COSTA .

1 Laboratório de Ecologia e Gerenciamento de Ecossistemas Costeiros e Estuarinos (LEGECE). Departamento de Oceanografia da UFPE. Av. Arquitetura, s/n°, Cidade Universitária, Recife-PE. CEP: 50740-550. Tel/fax: (81) 2126 8225/7218. 2 E-mail: [email protected]

Abstract. Occupation of a beach in Recife (NE Brazil) during summer days: a preliminary study. The increase of local population, especially in beaches resorts, changes their carrying capacity leading to pollution, as well as an uncomfortable feeling of pressure. This work identified the carrying capacity for a beach area in Boa Viagem, Recife, Brazil. The carrying capacity was determined trough counting of beach users along crowded days. Transects had 10 m width. Paper cards were handed over to beach users when they went into the area. The beach area was divided according use, morphological and physical aspects, in three Zones: active, solarium and open sea. The carrying capacity was measured through effectively used area per person. The number of beach users varied from 0-1,590 in all Zones. The active zone was the most used. The area occupied by beach users varied from 2,9 – 40,5 m²/ person. The peak of beach users was between 10:00 to 13:00 hs. The main arrival time was from 9:00 to 10:00 h and leaving time was 15:00 h. There were significative differences (p< 0,05) for number of beach users along the day. The intense use resulted in pollution of the beach area and changed the kind of users along the time.

Key words: carrying capacity, beach users, tourist beaches, tropical beaches.

Resumo. O aumento da população local, especialmente em cidades de praia traz como conseqüência a poluição, bem como a situação de desconforto. O presente trabalho identificou a capacidade de carga para uma faixa de praia em Boa Viagem, Recife, Brasil, determinada através da contagem de usuários da praia ao longo de dias feriados. Transectos com 10m de extensão foram demarcados e cartões de papel foram entregues aos usuários quando entravam na faixa de praia estudada. A faixa de praia foi dividida de acordo com o uso, aspectos físicos e morfológicos, em três Zonas: ativa, sollarium e de mar aberto. A capacidade de carga foi medida através da área efetivamente utilizada por pessoa. O número de usuários da praia variou de 0-1590 em todas as Zonas. A zona ativa foi a mais usada. A área ocupada pelos usuários da praia variou de 2,9 - 40,5 m²/pessoa. O horário de pico de usuários ocorreu entre 10:00 e 13:00 h. O horário de chegada foi 9:00 as10:00 h, e o de saída foi ás 15:00 h. Existiram diferenças significativas (p< 0,05) no número de usuários da praia ao longo do dia. A intensidade de uso resulta na poluição da faixa de praia e mudanças no tipo de usuário ao longo do tempo.

Palavras-chave: capacidade de carga, usuários da praia, praias turísticas, praias tropicais.

Introdução exploração de ambientes litorâneos ensolarados que O turismo é atualmente um dos principais reforçam a vocação turística da costa brasileira, responsáveis pela ocupação do litoral brasileiro, com sendo a qualidade ambiental e beleza cênica fontes importante influência no processo de urbanização. A diretas de bem-estar (MMA 1998). expansão da atividade turística ocorre pela A escolha da praia visitada reflete a

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92 J. S. DA SILVA ET AL. expectativa de uma praia ideal que varia de usuário paisagístico composto de sol, areia, mar e recifes de para usuário. De Ruyk (1997) classificou os usuários arenito paralelos a linha de costa (Costa & Kahn das praias em agregacionistas e individualistas. Os 2003, Costa & Souza 2002). A orla da Boa Viagem agregacionistas vão à praia para experiência social, pode ser classificada como “exposta com preferindo praias desenvolvidas, superlotadas e com urbanização consolidada” ou “exposta com abundancia de atividades. Por outro lado, os urbanização” (PROJETO ORLA 2001). Seguindo individualistas, são aqueles que procuram uma outra classificação (Smith 1991) ela é considerada experiência de contato com a natureza, preferindo como cidade resort, ou praia altamente desenvolvida praias pouco desenvolvidas, com beleza natural e (Morgan 1999). Esta praia apresenta diferentes graus tranqüilidade (De Ruyk 1997, Morgan 1999, de conservação em relação ao ambiente praial. Os Eugenio-Martins 2004). recifes de arenito são responsáveis pela formação de A capacidade do recurso base para uso piscinas naturais durante a baixa-mar. A maioria dos recreacional pode ser analisada através da ocupação hotéis de luxo construída na orla da Boa Viagem da praia. Essa ocupação é definida através do encontram-se em frente a maior faixa de extensão número máximo de pessoas por m2, que podem usar desses recifes, explorando a beleza cênica do local. o ambiente sem declínio na qualidade da experiência Por isso, este trabalho teve como objetivo social. Estudos prévios sobre capacidade de carga definir a dinâmica de ocupação e recreação ao longo determinaram um intervalo de uso no qual o número do dia no trecho mais ocupado da praia. Um estudo de usuários compromete a experiência recreacional dessa natureza em uma praia de importância sócio- (De Ruyk 1997, Da Silva 2002a, b). É baseada no econômica e ambiental como Boa Viagem é de conceito da manutenção do nível de grande relevância. A partir dele é possível desenvolvimento e uso que não resulte na determinar os locais mais susceptíveis a impactos deterioração sócio-cultural e ambiental, ou na oferecendo base para elaboração de planos de gestão percepção da degradação do recurso pelos usuários e ordenamento da orla a fim de mitigar os efeitos (De Ruyk 1997, Papageorgiou & Brothereton 1999, negativos causados pela intensidade de uso. Morgan 1999, Eugenio-Martins 2004). O Brasil apresenta 8500 km de linha de Material e Métodos costa (Awosika & Marone 2000), o que denota uma A área de estudo, onde foi estabelecido o alta potencialidade turística, advinda das transecto, está localizada na porção central da praia características ambientais locais. Dentre estas o de Boa Viagem (Figura 1), onde ocorre a formação clima, vegetação, presença de dunas, recifes de coral das piscinas naturais na maré baixa. A escolha desta e arenito agregam valor paisagístico as praias, área foi condicionada por três variáveis: a) ser um tornando-as instrumento de apreciação dos usuários. dos pontos identificados por Silva et al. (2006) e Alguns dos principais cartões postais Leal (2006) como de maior uso da praia; b) por ter brasileiros são as praias do litoral Pernambucano. O uma qualidade ambiental considerada intermediária Estado apresenta uma linha de costa de 187 km, com (Souza 2004) e c) por ser um dos pontos de praias que são destinos turísticos em concentração de atividades econômicas. desenvolvimento e consolidados, por exemplo, Esta parte da praia apresenta Maracaípe e Boa Viagem, respectivamente. aproximadamente 50 metros de mesolitoral os quais Na década de 70, a praia da Boa Viagem foi são totalmente tomados pela água na maré alta. palco da exploração turística que acelerou seu Devido à especulação imobiliária, o supra-litoral foi processo de urbanização. Sem planejamento quase totalmente transformado na avenida beira-mar, adequado a orla da Boa Viagem passou a ser que é densamente ocupada por edifícios e hotéis explorada não só pela atividade turística, mas luxuosos. também pela atividade imobiliária, resultando na A metodologia utilizada foi baseada no perda das características ambientais. A especulação trabalho de Polette et al. (2001) e Polette & Raucci imobiliária na área acelerou a verticalização e (2003), que sugerem um zoneamento do ambiente aumentou o custo de vida da população local, sendo praial a partir das características morfológicas, o bairro da Boa Viagem um dos bairros com maior hidrodinâmicas e de uso, da seguinte maneira: custo de vida da cidade. Devido ao crescimento 1 - Zona solarium (supra e mesolitoral) – desordenado, parte da praia sofreu mudança onde são realizadas atividades como tomar banho de paisagista devido aos processos de erosão costeira sol, armar barracas e guarda-sóis, etc. (Gregório 2004, Souza 2004, Leal 2006). 2 - Zona ativa (mesolitoral) - faixa de praia A praia da Boa Viagem possui cerca de 8km junto ao mar, altamente influenciada pela oscilação de extensão os quais se apresentam em um conjunto da maré, utilizada para caminhadas e atividades

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98 Ocupação da praia de Boa Viagem 93 recreativas na areia (jogos, castelos de areia e etc.). colaborar com o experimento foram confeccionados 3 - Zona de surf (infralitoral) - faixa onde (Tabela I). Os cartões tinham diferentes cores para ocorre a quebra das ondas, e na qual são realizadas cada intervalo de hora de chegada, com a finalidade atividades recreacionais aquáticas que não de identificar a hora de chegada de cada usuário no necessitam do uso de equipamentos (nado e banho momento em que o mesmo o devolvia na saída. Os de mar). cartões devolvidos eram acondicionados em A área estudada apresenta todas as zonas envelopes com o intervalo de hora de saída supracitadas. Para visualização do ponto do identificada, a fim de calcular o tempo de experimento em cada Zona da praia, foi delimitada permanência na praia. uma faixa de 10 m de largura, que se estendia desde A equipe no local de amostragens constou o calçadão à linha d’água. Cordas laterais e de quatro pesquisadores, os quais ficaram divididos bandeiras foram utilizadas para demarcar os limites. com as seguintes funções: um para fotografar a cada A área de amostragem correspondeu a 620 m2 e 515 2 intervalo de hora, dois para realizarem a abordagem m para um feriado e domingo de verão, dos usuários e um outro para contar o número de respectivamente. usuários na zona ativa.

À medida que as pessoas entravam na área

delimitada (±100 m2), eram abordadas pelos pesquisadores, que entregavam o cartão, explanando brevemente sobre a pesquisa e como o usuário poderia colaborar com o experimento. Em seguida, era medida a área no formato de retângulo ocupada pelo grupo de usuários, o número de usuários e a atividade realizada por eles no momento da abordagem. A cada hora, das 8:00 às 18:00, foram tiradas fotografias da área delimitada da praia. As fotografias foram utilizadas para contagem de usuários na Zona de surf e de mar aberto tomando como limite as cordas estendidas na Zona do Solarium. Não foi possível utilizar as fotografias para a Zona do Solarium, visto que os guarda-sóis impossibilitavam a visualização correta do número de pessoas. Nesse mesmo intervalo de tempo, das 8:00 às 18:00, era feita a contagem do número de usuário que passavam na zona ativa, durante 15 minutos com o auxílio de um contador manual. A capacidade de carga foi calculada de acordo com Ruschman (1999) e Eugenio-Martin (2004), através da densidade de usuários na Zona do solarium: C = V/K

Onde, C é a capacidade de carga, V e área disponível para uso e K é o número de usuários. Existe uma imprecisão no experimento devido ao número de usuários que se recusaram a participar somado aos usuários que esqueceram de Figura 1. Imagem da faixa de praia estudada na Parte central da entregar o cartão. Esta recusa pode está associada a Praia da Boa Viagem, Recife/Brasil (ZS, Zona solarium; ZA, forma de abordagem que pode ter alterado o Zona ativa e ZSURF, Zona de surf). (Foto: Monica F.Costa 2002) comportamento do usuário. Esta imprecisão foi calculada pelo número de cartões que estavam Cartões de papel numerados, contendo o faltando ao final do dia somado com o número de título da pesquisa, seus objetivos e uma breve recusas recebidas. Este estudo foi realizado nos dois explicação sobre de que forma o usuário poderia dias de maior freqüência de usuário (Silva et al.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98 94 J. S. DA SILVA ET AL.

Tabela I. Modelo dos cartões bilíngües (português e inglês) que eram entregues aos usuários quando eles entravam na área de estudo. Esta é uma pesquisa sobre a capacidade de carga This is a research about Beach Carrying Capacity. Beach recreacional de uma praia. Capacidade de carga carrying capacity is the number of users that an area may recreacional é o número de visitantes que determinada receive without changing its quality. It helps planning área pode receber sem alterar sua qualidade. Isso ajuda sustainable tourism. no planejamento do turismo sustentável. Objective: To measure Boa Viagem carrying capacity in Objetivo: Determinar a capacidade de carga order to understand the beach’s dynamics and the recreacional da praia da Boa Viagem, afim de se interference of users on this environment. entender a dinâmica da praia bem como a interação dos visitantes com o meio. How can you collaborate with our experiment?

Como você pode colaborar para a nossa pesquisa? • Do not remove the flags marking the experimental area; • Não retirar as bandeiras que delimitam a área do • Allow us to take the measurements around your experimento; area and • Permita a medição da área que você está ocupando e • Hand back the card when you leave the beach. • Devolva este cartão na saída. Thank you! Obrigado!

2006) da praia de Boa Viagem: um feriado nacional dias amostrados foi em média de 1590 pessoas/dia de 8 de dezembro e o domingo subseqüente, no mês nas três Zonas da praia (Solarium, ativa e surf). A de dezembro de 2004. imprecisão foi em média de 3,7% nos dois dias Para avaliar se existe diferença significativa na amostrados, o que demonstrou uma grande aceitação quantidade de usuários nos horários amostrados uma do usuário em participar do experimento. O horário ANOVA foi realizada, utilizando o software de pico de freqüência dos mesmos esteve entre 10:00 STASTISTICA 5. Onde a ANOVA mostrou-se e 13:00 h. O horário de chegada de usuários no significativamente diferente, um teste a posteriori ponto de estudo estava entre 9:00 e 10:00 h, e o de Tukey’s foi usado para determinar quais médias saída entre 13:00 e 15:00 h (Figuras 2 e 4). Não foram significativamente diferentes (p<0,05). houve diferença significativa no comportamento da freqüência entre os dias amostrados (p > 0,05). A Resultados e Discussão análise ANOVA demonstrou existir diferenças Trabalhos de capacidade de carga significativas (p< 0,05) no número de usuários ao recreacional são amplamente utilizados para avaliar longo do dia. De acordo com os resultados, os os impactos dos usuários e a percepção destes em intervalos definidos como de pico (10:00 ás 13:00 h) relação aos problemas por eles gerados. As diferem significativamente (p<0,05) daqueles metodologias amplamente utilizadas e difundidas reconhecidos como de começo de manhã (8:00 - para o cálculo da capacidade de carga recreacional 9:00 h) e fim de tarde (15:00 - 16:00). A dinâmica são o senso visual (De Ruyk 1997, Saveriades 2000, de ocupação da praia ao longo do dia está Polette et al. 2001, Arnberger et al. 2004, diretamente associada as maiores incidências da luz Arnberg & Haider 2005, Silva et al. 2006) e solar. Diferenças de latitude proporcionam imagem aérea e digital, (Da Silva 2002a, diferenças no horário de pico e na quantidade de Arnberg et al. 2004, Arnberger & Haider 2005). horários de pico, quando comparados com outros Muitas vezes a estimativa do número de usuários estudos da mesma natureza (Deacon & Kolstad presentes está associada as entrevistas que tem 2000, Da Silva 2002b, Silva et al. 2006). Da Silva como objetivo relacionar a percepção do usuário à (2002a, b) observou que o pico de freqüência de superlotação e a possibilidade dele vir a repetir a usuários em cinco praias portuguesas estava entre visita ao local. Todos esses métodos 11:00 e 12:00 h. Deacon & Kolstad (2000) supracitados sozinhos ou em conjunto dão uma boa observaram um pico de freqüência de usuários as estimativa do número total de usuários que 13:30 h durante o final de semana nas praias de freqüentam o local, sem apresentar diferenças Newport e Huntington (Califórnia, Estados Unidos). significativas (Arnberger & Haider 2005). Para Balneário Camburiú (SC) o pico de usuários O somatório do número de usuários nos dois ocorreu às 10:00 h durante o verão, com redução

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98 Ocupação da praia de Boa Viagem 95

Figura 2. Ocupação da Zona do solarium ao longo do dia em frente ao Hotel Recife Palace Lucsim, Praia da Boa Viagem, PE. (Fotos: Jacqueline S. da Silva 2004). significativa entre 11:00 e 15:30 h (Polette et al. na praia em grupos que variaram de 2 a 4 pessoas 2001). Quando comparado com estudo anterior em (Tab. II). Leal (2006) retratou através de Boa Viagem (Silva et al. 2006), os resultados questionário estruturado o perfil do usuário da praia obtidos nestes estudos corroboram os anteriores com da Boa Viagem. De acordo com este trabalho, as relação ao horário de pico, intensidade de uso e sua pessoas que utilizam a praia permanecem área disponível. aproximadamente quatro horas e geralmente vão em A dinâmica de ocupação de uma praia é grupo de quatro pessoas, que são comumente seus refletida pela sua densidade de usuários localizados parentes. no supra e meso litoral (Zona do Solarium), onde a O número de usuários na zona ativa foi em principal atividade realizada é o banho de sol. Nas média 1391,5 pessoas/dia, com mínimo de 20 e horas de maior intensidade solar ocorreu o aumento máximo de 254 pessoas em 15 minutos (Figura 5). O de usuários, que proporcionou a diminuição da área padrão de uso desta zona foi o mesmo nos dois dias disponível para uso (Figura 3). O tamanho do grupo amostrados. A freqüência total de usuários foi quatro influenciou diretamente no valor da área ocupada vezes maior na Zona ativa do que no Solarium para (Tabela II). A área disponível para uso é todos os horários amostrados. De acordo com a inversamente proporcional ao número de usuários. A estimativa para uma hora de contagem, os horários área disponível para os usuários na faixa de praia de pico de freqüência estiveram entre 9:00 e 10:00 h, estudada variou de 2,9 a 40,5 m²/pessoa (Figura 3). o que não corresponde aos do Solarium. Ocorre uma O menor valor de área disponível ocorreu no horário diminuição do número de pessoas caminhando a de maior número de usuários (10:00-13:00 hs). De partir das 12:00 h. acordo com Leal (2006), os usuários da praia Nos últimos três anos, o turismo em habitualmente se reúnem em grupo no mesmo local, Pernambuco vem diminuindo, dando espaço a outros independente do número de visitantes. De Ruyk Estados nordestinos que têm as mesmas (1997) estabeleceu como intervalo de conforto para características de litoral ensolarado, como Ceará e os usuários 6.3-25 m²/indivíduos para praias Alagoas. Uma das razões apontadas para essa arenosas da África do Sul. Em Portugal a área diminuição é a falta de investimentos em marketing disponível para os usuários variou de 13,5 a 111,7 turístico, bem como a ocorrência de ataques de m²/pessoa (Da Silva 2002a), sendo considerada pelo tubarão na Boa Viagem. Em dez anos (1992-2002), autor como intolerável/desconfortável. foram registrados trinta e oito ataques nas quatro O tempo de permanência dos usuários variou praias metropolitanas do estado, sendo vinte e dois entre 2 a 5 horas. As pessoas que chegaram às 8:00 h em Boa Viagem (Silva 2002). Já no ano de 2006, 50 permaneceram em média 2 horas, as que chegaram ataques foram registrados na Boa Viagem. Segundo no horário de pico (11:00-13:00 h) permaneceram Leal (2006), apenas 39,6% dos freqüentadores da em média 3 horas e saíram ao final do dia (15 e 17 Boa Viagem afirma ter mudado a forma de uso da hs). Dos usuários amostrados na área 88,4% estavam praia, devido aos ataques. Entre as mudanças

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98 96 J. S. DA SILVA ET AL.

Tabela II. Comparação do tamanho médio dos em média 96,5 pessoas/dia. Os padrões entre os dois grupos de usuários localizados na zona de Solarium dias variaram bastante, provavelmente devido à da praia da Boa Viagem nos dois dias amostrados. diferença na amplitude de maré (feriado - cheia e domingo, minguante). A amplitude de maré em Total de Tamanho do grupo no Solarium (%) Recife varia aproximadamente 2,5 m. A falta de pessoas 1 2 3 ≥4 segurança no banho é um dos fatores que 204 11,6 37,8 20,5 30,1 influenciam essa evasão do uso do balneário. Na Tamanho médio da área ocupada pelos praia de Boa Viagem o usuário não entra na água grupos (m²) para tomar banho na maré alta, e quando o faz, fica 1,3 1,6 3,7 ≥ 4,6 restrito à Zona de surf, onde os recifes lhe garantem alguma proteção (Figura 2). Por essa razão o número de usuários na Zona de Surf foi baixo em relação às outras zonas. O dano ao ambiente recreacional torna-se perceptível quando a dinâmica de ocupação diminui. A faixa de areia fica repleta de resíduos sólidos, geralmente compostos por itens plásticos descartáveis, como copos, pratos, colheres e garrafas. Esses resíduos são típicos de usuários da praia (Silva et al. 2006). O declínio da qualidade Figura 3. Área utilizada na Zona de Solarium ao longo do dia. ambiental de Boa Viagem vem sendo documentado não só pela perda das características paisagísticas (Souza 2004), qualidade da água (Costa & Barleta 2004), mas também pelos impactos originados pelos seus usuários (Silva et al. 2006). A perda das características paisagísticas e a poluição da água e da areia aparentemente não cessam a visita dos usuários da praia da Boa Viagem. Ao longo dos anos esses fatores podem ter sido responsáveis pela mudança no tipo de usuário. Os usuários da praia de Boa Viagem que antes procuravam o contato com a natureza eram compostos basicamente por turistas interessados na Figura 4. Número médio de pessoas na Zona de Solarium ao exploração da beleza natural da praia. Hoje, os longo do dia. usuários da Boa Viagem são basicamente os residentes e locais que buscam a praia para experiência social (Leal 2006).

Considerações Finais A capacidade de carga recreacional é uma ferramenta que deverá ser utilizada para elaboração de planos de gestão e ordenamento da orla de modo a mitigar os efeitos negativos causados pela intensidade de uso. Cada Zona da praia apresentou uma dinâmica de uso que estava diretamente relacionada com a atividade praticada e a

Figura 5. Número de pessoas na Zona Ativa na praia ao longo intensidade solar. Os usuários da Zona Solarium, do dia. cuja principal atividade é o banho de sol, preferem horários com maior radiação solar. Já a zona ativa é apontadas por eles as principais foram: não entrar mais utilizada nos horários de baixa intensidade no mar, mergulhar em águas rasas e entrar receoso solar. A maioria dos usuários vão a praia em grupos na água (Leal 2006). Por estas razões as Zonas de compostos de 2 a 4 indivíduos. A quantidade de surf e mar aberto foram pouco freqüentadas. usuários variou significativamente ao longo do dia, O número de usuários na Zona de surf foi sendo esta variação provocada provavelmente pela

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98 Ocupação da praia de Boa Viagem 97 intensidade solar e altura da maré. A capacidade de Da Silva, C. P. 2002 a. Integração de estudos de carga recreacional para o ponto de estudo foi alta percepção da paisagem e imagens digitais na (2,9 m²/pessoa). O horário de pico ocorreu no definição da capacidade de carga de praias - O intervalo de almoço, coincidindo com a maior Troço litoral S. Torpes - Ilha do Pessegueiro. intensidade solar. Fatores como morfologia da praia, Tese de doutorado. Universidade Nova de horários de maior incidência solar e amplitude de Lisboa, Lisboa, Portugal, 327 p. maré influenciam na capacidade de carga Da Silva, C. P. 2002 b. Beach carrying capacity recreacional da praia. Devido a isso é essencial para assessment: How important is it? Journal of avaliar se a dinâmica de ocupação varia ao longo da Coastal Research, 36: 190-197 . praia amostras mais freqüentes e em outros setores De Ruyk, M.C.; Alexandre, G. S. & Mclachlan. A. da praia da Boa Viagem. 1997. Social carrying capacity as a management tool for sandy beaches. Journal Agradecimentos of Coastal Research, 13(3): 822-830. Os autores agradecem ao Hotel Recife Palace Deacon, R. T. & Kolstad, C. D., 2000. Valuing Lucsim pela autorização para fotografar em frente a beach recreation lost in environmental área de estudo. À Coordenação de Aperfeiçoamento accidents. Journal of Water Resources de Ensino Superior - CAPES, pela bolsa de Planning and Management, 126 (6): 374- Mestrado de Jacqueline Santos da Silva. 381. Eugenio-Martin, J. L. 2004. Monitoring the Referências Bibliográficas congestion level of competitive destinations Arnberg, A & Haider, W. 2005. Social effects on with mixed logic models. Dados disponíveis crowding preferences of urban visitors. on line em: http://www.nottingham.ac.uk. Urban Forestry & Urban Greening, 3: 125- (Acessado em 02 de novembro de 2006). 136. Gregório, M. N., Araújo, T. C. M. & Valença, L. M. Arnberg, A., Haider, W. & Muhar, A., 2004. Social M. 2004. Variação sedimentar das praias do Carrying Capacity of an Urban Park in Pina e da Boa Viagem, Recife (PE) Brasil. Vienna. Working Papers of the Finnish Tropical Oceanography, 31(1):39-52. Forest Research Institute, 2: 361-368. Leal, M. M. V. 2006. Percepção dos usuários quanto Awosika, L. & Marone, E. 2000. Scientific needs to à erosão costeira na praia da Boa Viagem, assess the health of the oceans in coastal Recife (PE), Brasil. Dissertação de areas: a perspective of developing countries. Mestrado. Universidade Federal de Ocean & Coastal Management, 43: 781- Pernambuco (UFPE), Pernambuco, Brasil, 791. 108p. Costa, M. & Kahn, J. R. 2003. Boa Viagem erosion Lindlberg, K., Mccool, S. & Stankey, G. 1997. prevention and beach nourishment project. Rethinking Carrying Capacity. Annals of Anais do II Congresso sobre Planejamento Tourism Research, 24: 461-465. e Gestão das Zonas Costeiras dos Países de MINISTÉRIO DO MEIO AMBIENTE. 1998. Expressão Portuguesa, IX Congresso da Roteiro de Análise econômica para o Associação Brasileira de Estudos do Programa Nacional de Gerenciamento Quaternário, II Congresso do Quaternário Costeiro. Políticas, Instrumento e Normas dos Países de Língua Ibéricas, Recife, meio Ambientais. Brasília, 67 p. magnético (CD). Morgan, R. 1999. Preferences and priorites of Costa, M. & Souza, S. T. 2002. A zona costeira recreational beach users in Wales, UK. Pernambucana e o caso especial da praia da Journal of Coastal Research, 15(3): 653- Boa Viagem: Usos e Conflitos. P. 1-16. In: 667. Construção do Saber Urbano Ambiental: A Papageorgiou, K. & Brothereton, I. 1999. A Caminho da Transdisciplinaridade. Editora management planning framework based on Humanidades, Londrina, 99 p. ecological, perceptual and economic carrying Costa, M. & Barletta, M. 2004. Beach capacity: the case study of Vikos-Aoos environmental quality - Water quality National Park, Greece. Journal of monitoring programs at recreational beaches Environmental Management, 56: 271-284. in Brazil. II International Workshop on Polette, M. & Raucci, G. 2003. Methodological Beach Eco Watch Programs. Borocay Proposal for Carrying Capacity Analysis in Island, Aisklan, The Philippines: 1-22. Sandy Beaches: A Case Study at the Central

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Beach of Balneário Camboriú - SC - Brazil. Silva, J. C. C. 2002. Ataques de tubarão em Journal of Coastal Research, 35: 94-103. Pernambuco: causas e efeitos. Monografia de Polette, M. Raucci, G. D., & Cardoso, R. C. 2001. Especialização. Universidade Federal de Proposta metodológica para análise da Pernambuco (UFPE), Pernambuco, Brasil, capacidade de carga recreacional em praias 45 p. arenosas: Estudo de caso da praia central de Silva, J. S., Leal, M. M. V., Araújo, M. C. B.; balneário Camburiú-SC (Brasil). I Congresso Tinoco, S. & Costa, M. (2006). User Sobre Planejamento e Gestão do Litoral frequency of Boa Viagem Beach, Northeast dos Paises de Expressão Portuguesa, Brazil. Journal of Coastal Research (in Açores/Lisboa, meio magnético (CD). press). PROJETO ORLA. 2001. Projeto de gestão Smith, R. A., 1991. Beach resorts: A model of integrada da orla marítima - Brasília: development evolution. Landscape and Ministério do Meio Ambiente e Ministério do Urban Planning, 21 (3): 189-210. Planejamento, Orçamento e Gestão, 80 p. Souza, S. T. 2004. A saúde das praias da Boa Ruschmann, D. 1999. Turismo e planejamento Viagem e do Pina, Recife- PE. Dissertação de sustentável: a proteção do meio ambiente. Mestrado. Universidade Federal de Campinas: Papirus, 199 p. Pernambuco (UFPE), Pernambuco, Brasil, Saveriades, A. 2000. Establishing the social tourism 99 p. carrying capacity for the tourist resorts of the coast of the Republic of Cyprus. Tourism Management, 21:147-156.

Received July 2006 Accepted October 2006 Published online November 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 91-98

Report on the smallfin catshark Apristurus parvipinnis Springer & Heemstra (Chondrichthyes, Scyliorhinidae) in Western South Atlantic with notes on its taxonomy

1 2 3* ULISSES L. GOMES , CAMILA N. SIGNORI & OTTO B. F. GADIG

1 Universidade do Estado do Rio de Janeiro, Departamento de Biologia Animal de Vegetal, Rua São Francisco Xavier 524, 20559-900, Rio de Janeiro, Brazil, [email protected], research suported by PROCIÊNCIA/UERJ/FAPERJ. 2 Universidade do Estado do Rio de Janeiro, Departamento de Oceanografia, Rua São Francisco Xavier 524, 20559- 900, Rio de Janeiro, Brazil, [email protected], research suported by IC-CNPq, process 118048/2004-0. 3 Universidade Estadual Paulista, Campus do Litoral Paulista, Praça Infante Dom Henrique s/n, 11330-900, São Vicente, SP, Brazil, e.mail: [email protected]., supported by CNPq , process 309740/2003-7; * corresponding author.

Abstract. This note presents data on the smallfin catshark Apristurus parvipinnis in the Western South Atlantic, with taxonomic comments on this species. The smallfin catshark was previously reported, usually from Western North Atlantic, but few recorded specimens are known from Brazilian Western South Atlantic. This species occurs on the upper and middle continental slopes, usually near the bottom. This report is based in one 588 mm total length mature male, collected off Rio de Janeiro between depths of 650-720 meters. Comments on its taxonomy are presented, comparing this species with other Atlantic Apristurus species.

Keywords: Elasmobranchii, Carcharhiniformes, distribution, Brazil, morphometrics.

Resumo. Registro do tubarão-gato-escuro Apristurus parvipinnis Springer & Heemstra (Chondrichthyes, Scyliorhinidae) no Atlântico Sul Ocidental, com notas sobre sua taxonomia. Este trabalho apresenta dados sobre o tubarão-gato-escuro Apristurus parvipinnis no Atlântico Sul Ocidental, com comentários taxonômicos sobre a espécie, que foi previamente registrada principalmente no Atlântico Norte Ocidental, mas poucos registros são conhecidos em águas do Brasil, no Atlântico Sul Ocidental. Esta espécie vive nos taludes superior e médio, normalmente próxima ao fundo. Os dados aqui apresentados são baseados em um exemplar macho maduro de 588 mm de comprimento total, coletado em frente ao Rio de Janeiro, entre 650 e 720 m de profundidade. São apresentados comentários sobre sua taxonomia, comparando a espécie com outros tubarões do gênero Apristurus do Atlântico.

Palavras-chave: Elasmobranchii, Carcharhiniformes, distribuição, Brasil, morfometria.

The catsharks of genus Apristurus Garman, 1913, 1992, Nakaya & Stehmann 1998, Nakaya & Sato are deepwater species from continental slopes, 1998, 1999, Nakaya et al. 1999). usually inhabiting at depths up to 2000 m (Nakaya et Apristurus parvipinnis Springer & al. 1999). The genus is characterized by a fully and Heemstra, 1979, has been reported from Gulf of mostly uniformly dark slender body with an Mexico, off Pensacola (Florida), Gulf of Campeche elongated anal fin ending in front of the beginning (Mexico), off the Caribbean coast of Panama and of the lower caudal fin, possessing a flatted and Colombia, and off French Guiana (Uyeno & Sasaki spatulated snout, and presenting upper and lower 1983, Compagno 1984). Springer (1966), studying labial furrows. The genus is comprised of thirty two the Western Atlantic scyliorhinids had erroneously recognized species and at least seven undescribed termed this species as Apristurus indicus Garman, species (Compagno 1984, Meng et al. 1985, Nakaya 1913 (recorded for the Western Indian Ocean). This 1975, 1988a, b, 1989, 1991, Nakaya & Séret 1989, species occurs near the bottom on the upper and

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 99-103 100 Apristurus parvipinnis in Western South Atlantic middle continental slopes. The holotype was bases greater than length of base of second dorsal captured in the depth of 1115 m and the twelve fin; anal fin long, its rear tip separated from origin of paratypes were collected between 676 and 1097 m. lower caudal lobe by a distance less than half the According to Springer (1979) and Compagno length of the eye. The morphometric description of (1984), it is a small shark reaching from 268 up to the Brazilian A. parvipinnis specimen is presented in 521 mm of total length (TL). Table 1 in comparison to the holotype. A few previous reports on the occurrence of According to Springer (1979) this species Apristurus parvipinnis in the Western South Atlantic presents more than 50 rows of teeth in each jaw. are presented by Gadig & Gomes (2003), for Bahia Brazilian specimen showed 89 rows of small teeth in (central Brazil) and Rincon & Vooren (2006), for the upper jaw and 90 rows in lower jaw (89/90) or Santa Catarina coast, southern Brazil. Both studies 44-45/44-46. Symphyseal and commissural teeth of do not present any aditional data on this species. upper jaw with 4 cusps, while symphyseal and The present study reports the occurrence and commissural teeth of lower jaw presented 5 and 6 or taxonomic data of the smallfin catshark, Apristurus 7 cusps, respectively. The 588 mm TL adult male parvipinnis, in the Brazilian Western South Atlantic, herein examined represents the greatest total length with taxonomic comments on this species, up to date recorded for this species. comparing it with other catsharks genus Apristurus According to Compagno (1984) a crest of from Atlantic. enlarged denticles along the dorsal margin of the The Brazilian specimen, a 588 mm TL caudal fin can be variably developed in the mature male, was caught by bottom-trawl in 2004, following species: Apristurus canutus Springer & between 650-720 meters deep off eastern Cabo Frio Heemstra, 1979, Apristurus investigatoris (Misra, (23º50' S e 41º20' W), Rio de Janeiro State. The 1962), Apristurus manis (Springer, 1979), specimen was frozen for morphometric and Apristurus microps (Gilchrist, 1922), Apristurus morphological analysis, and placed at the parvipinnis, Apristurus profundorum (Goode & Ichthyological Collection of the Universidade do Bean, 1896), Apristurus stenseni (Springer, 1979) or Estado do Rio de Janeiro - UERJ 2056. even absent in the other species of Apristurus. Morphometric and meristic data, visceral disposition Compagno (1984) affirms that A. parvipinnis pattern and cephalic sensory canal terminology presents enlarged denticles along the dorsal margin followed respectively Springer (1979), Nakaya of the caudal fin, otherwise, Uyeno & Sakaki (1983) (1991) and Nakaya & Sato (1999). report that there are no modified denticles in the The small catshark Apristurus parvipinnis caudal fin of this species. Our specimens presented (Fig. 1) was identified by the following combination not a real crest, but enlarged dermal denticles along of features: presence of a long upper labial furrows the dorsal margin of the caudal fin. reaching midway to the nostril; lengths of the upper There are 11 described Apristurus species in labial furrows are longer than the lower ones; the Atlantic Ocean (Compagno et al. 2005). distance between pectoral and pelvic fin bases long, A. parvipinnis differs from Apristurus aphyodes from 10.8 to 14.0% of the total length (14.4% in the Nakaya & Stehmann, 1998, A. manis, A. microps Brazilian specimen); anal fin base about 16.0 to and Apristurus riveri Bigelow & Schroeder, 1944 in 18,0% of the total length (17.3% in the Brazilian presenting more spiral valves counts (15-22 versus specimen); rear end of the base of second dorsal fin 8-12), head sensory canal pores discontinued and in advance of rear end of base of anal fin; distance upper labial furrow longer than lower. This species between dorsal fin bases less than distance from tip is similar to A. canutus, Apristurus laurussonii of snout to eye; origin of dorsal fin posterior to rear (Saemundsson, 1922) e Apristurus saldanha end of pelvic fin base; distance between dorsal fin (Barnard, 1925) concerning the discontinued head

Figure 1 – Apristurus parvipinnis, adult male 588 mm TL, caught off Rio de Janeiro, southern Brazil (UERJ 2056).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 99-103 ULISSES L. GOMES ET AL. 101

Table I – Morphometrics expressed as percentage of total length in Apristurus parvipinnis, comparing specimen from the present study with the holotype and range in 12 paratypes. holotype♂ paratypes UERJ 2056♂ Measurements 476 mm 268-521 mm 588 mm Tip of snout to: front of the mouth 8.8 8.6-9.2 8.2 Eye 10.1 9.6-11.2 9.2 origin pectoral fin 21.4 20.0-22.5 20.9 origin 1st dorsal fin 51.5 49.6-52.8 50.7 origin pelvic fins 42.0 39.0-43.0 42.5 origin 2nd dorsal fin 63.0 60.4-65.0 64.1 origin upper caudal lobe 72.2 69.0-73.8 74.6 Orbit: horizontal diameter 3.1 2.9-3.5 3.4 vertical diameter 1.2 0.7-1.4 1.4 Mouth: Width 7.1 7.0-9.2 9.5 Length 3.6 2.8-3.9 2.9 length upper labial furrow 2.9 2.6-3.4 3.2 length lower labial furrow 1.7 1.7-2.2 2.2 Gill slits: 1st 1.7 1.3-2.2 1.9 5th 1.5 1.0-1.7 1.4 First dorsal fin: length base 3.8 3.6-4.5 4.8 Height 3.4 1.3-3.4 1.5 length anterior margin 6.1 5.5-7.6 7.3 Second dorsal fin: length base 5.7 5.3-7.3 5.8 Heigth 2.5 2.0-3.2 2.2 length anterior margin 9.2 8.3-9.7 7.8 Pectoral fin: width base 8.0 7.1-9.8 8.2 length anterior margin 11.6 10.1-14.6 11.4 greatest width 8.2 7.2-8.5 9.2 Pelvic fin: distance origin to posterior tip 12.6 10.1-12.6 10.0 Caudal fin: upper margin 27.3 26.0-30.9 28.7 Distance between fin bases: First to second dorsals 8.0 6.7-9.4 8.8 pectoral to pelvic 13.7 11.3-13.7 14.4 sensory canal pores and size but differs in the surface area of the second dorsal fin (in A. number of counts of the intestinal spiral valves. laurussonii and A. saldanha the first dorsal fin However, such data must be carefully considered surface is a little smaller than the second dorsal fin due to the low number of specimens examined from surface area, corresponding to two thirds of the other species, as follows: A. canutus (14–17 valves, second dorsal surface area); A. parvipinnis differs 11 specimens examined), A. laurussoni (17–20, five from A. canutus in having the pectoral-pelvic specimens) and A. saldanha (16 valves, one distance more than half of the anal fin base (less specimen). than half of the anal fin base in A. canutus). In A. parvipinnis and A. canutus the first Springer (1979) and Compagno (1984) dorsal fin is much smaller than second, and the affirms that A. parvipinnis is one of the commonest surface area equal to or less than the half of the Apristurus species caught in deep trawls around Gulf

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 99-103 102 Apristurus parvipinnis in Western South Atlantic of Mexico-Caribbean area, along with Buckup, P. A., Figueiredo, J. L. & Moura, R. A. laurussonii. Previous records of this species are L. (Eds). Catálogo das Espécies de Peixes mostly from the Western North Atlantic and Marinhos do Brasil. Museu de Zoologia, Caribbean (Springer 1979, Nakaya & Stehmann Universidade de São Paulo. 197 p. 1998, Nakaya & Sato 1999). A few specimens are Meng, Q. W., Chu, Y. T. & Li, S. 1985. Description known from Western South Atlantic (Gadig & of four new species of Scyliorhinidae from Gomes 2003, Rincon & Vooren 2006), but these depths of the South China Sea. Oceanologica studies just cited A. parvipinnis in this area, with no et Limnologica Sinica, 16: 43-50. more additional taxonomic, morphological or Nakaya, K. 1975. Taxonomy, comparative anatomy biological data. The specimen herein examined and phylogeny of Japanese catsharks, represents the greatest total length up to date Scyliorhinidae. Memoirs of the Faculty of reported for this species. Fisheries of the Hokkaido University, 23: 1- Genus Apristurus’ species are known to 24. occur at deep oceanic waters and its conservative Nakaya, K. 1988a. Morphology and taxonomy of external morphology can lead, in many cases, to Apristurus longicephalus (Lamniformes, mistakes in the species identification (Nakaya & Scyliorhinidae). Japanese Journal of Sato 1999). Just one species was recorded in the Ichthyology, 34(4): 431-442. Western South Atlantic, but it is possible that more Nakaya, K. 1988b. Records of Apristurus herklotsi species do occur in Brazilian deep waters, since - (Lamniformes, Scyliorhinidae) and discussion besides the factors above mentioned - the Brazilian of its taxonomic relationships. Japanese fishery fleet usually does not operate at the deep Journal of Ichthyology, 35(2): 133-141. waters where this genus usually occurs. Oceanic Nakaya, K. 1989. Redescription of Apristurus deep sharks species comprise about 20 % of the total sibigae, and its taxonomic relationships shark species recorded in Brazilian waters, and (Lamniformes, Scyliorhinidae). Japanese Scylorhinidae represents about 31 % of these Journal of Ichthyology, 36(2): 200-207. oceanic deep species (Gadig, 2001). Rincon & Nakaya, K. 1991. A review of the long-snouted Vooren (2006) also suggest that the increasing species of Apristurus (Chondrichthyes, fishing and research efforts in such environment Scyliorhinidae). Copeia, 4: 992-1002. should provide more data on the poorly known Nakaya, K. & Sato, K. 1998. Taxonomy review of fishes. Additionally, taxonomic studies on these Apristurus laurussonii (Saemundsson, 1922) Brazilian deep sea elasmobranchs can be considered, from the eastern North Atlantic aiming for a more consistent knowledgement on the (Elasmobranchii, Scyliorhinidae). Cybium, Brazilian elasmobranch fauna. 22(2): 149-157. Nakayo, K. & Sato K., 1999. Species grouping Ackowledgements within the genus Apristurus (Elasmobranchii: To A. Tomás and B. Mourato for the Scyliorhinidae). Fifth Indo-Pacific Fish donation of the specimen; D. Pagnoncelli and Conference, Nouméa., 307-320. Á. Mendes for taking the photographs; and to Nakaya, K. & Séret, B. 1989. Scyllium K. Nakaya for sending his papers on Scyliorhinidae. spinacipellitum Vaillant, 1888, a senior synonym of Apristurus atlanticus (Koefoed, References 1927) (Chondrichthyes, Scyliorhnidae). Compagno, L. J. V. 1984. Sharks of the world. An Bulletin Muséum national d'Histoire naturelle, annotated and illustrated catalogue of shark 4(11a): 977-982. species known to date. Part 2. Nakaya, K. & Séret, B. 1992. Scylliorhinus Carcharhiniformes. FAO Fisheries Synopsis, atlanticus Koefoed, 1927 (currently 125(4): 251-655. Apristurus atlanticus: Chondrichthyes, Compagno, L. J. Dando, M. & Fowler, S. 2005. Carcharhiniformes): proposed conservation of Sharks of the world. Princeton Univeristy the specific name. Bulletin of Zoological Press, Princeton: 368 p. Nomenclature, 49(1): 49-51. Gadig, O. B, F, 2001. Tubarões da Costa Nakaya, K. & Stehmann, M. 1998. A new species of Brasileira. Tese de Doutorado, Instituto de deep-water catshark, Apristurus aphyodes Biociências, Unesp, Rio Claro: 343 p. n.sp., from the eastern North Atlantic Gadig, O. B. F. & Gomes, U. L. 2003. (Chondrichthyes: Carcharhiniformes: Scyliorhinidae. p. 19-20. In: Menezes, N. A., Scyliorhinidae). Archive Fischereiwiss,

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46(1): 77-90. Springer, S. 1966. A review of the western Atlantic Nakaya, K., Sato, K. & Stewart, A. L. 1999. A new catsharks, Scyliorhinidae, with description of species of deep-water catshark genus a new genus and five new species. Fishery Apristurus from New Zealand waters Bulletin, 65: 581-624. (Chondrichthyes, Scyliorhinidae). Journal of Springer, S. 1979. A revision of the catsharks, the Royal Society of New Zealand, 29(4): family Scyliorhinidae. NOAA Technical 325-335. Report, NMFS Circular, 422: 1-152. Rincón, G. & Vooren, C. M. 2006. Taxonomic and Uyeno, T. & Sasaki, K. 1983. Scyliorhinidae. p. 49- biological records of the South Atlantic 52. In: Uyeno, T., Matsuura, K. & Fujii (Eds.) marbled catshark, Galeus mincaronei Soto Fishes Trawled off Suriname and French (Elasmobranchii: Scyliorhinidae) off the Guiana, Tokyo: Marine Fishery Resource Southern Brazilian coast. Pan-American Research Center. 519 p. Journal of Aquatic Sciences, 1(1): 1-7.

Received October 2006 Accepted November 2006 Published online November 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 99-103

Benthic macroinvertebrate bycatch in the snail Zidona dufresnei (Donovan) fishery from the Uruguayan continental shelf

1,2 1 3 GUSTAVO RIESTRA , JUAN PABLO LOZOYA , GRACIELA FABIANO , ORLANDO 3 4 SANTANA & DANIEL CARRIZO

1 Dirección Nacional de Recursos Acuáticos, Montevideo-Uruguay. e-mail: [email protected] 2 Museo de Historia Natural “Dr. Carlos Torres de la Llosa”, Uruguay. 3 Dirección Nacional de Recursos Acuáticos, La Paloma-Uruguay. 4 Instituto de Investigaciones Químicas y Ambientales de Barcelona, Spain.

Abstract. The benthic macroinvertebrate fauna associated with the fishery of “caracol fino” Zidona dufresnei (Mollusca, Gastropoda) was analysed during three fishery cruises in the Uruguayan continental shelf. Species composition, richness, diversity and qualitative dominance were estimated from the examination of the bycatch of 172 fishing hauls using a double bottom otter trawl. In the Uruguayan Atlantic waters 55 species of macroinvertebrates were associated with Z. dufresnei, being molluscs and crustaceans the dominant taxa in species number and frequency of occurrence. Two gastropods (Adelomelon beckii and Tonna galea), two decapod crustaceans (Libinia spinosa and Propagurus gaudichaudii), one asteroid (Astropecten brasiliensis), and one Actiniaria ind. were the most representative species in the “caracol fino” bycatch. Further studies considering unexplored bathymetric gradients are strongly recommended, they will help to fill our current gap in the knowledge of the macrobenthic diversity in the Uruguayan continental shelf.

Key words: Benthic macrofauna, fauna associated, diversity, qualitative dominance, Uruguay.

Resumen. Captura incidental de macroinvertebrados bentónicos en la pesquería de caracol fino Zidona dufresnei en la plataforma continental uruguaya. La fauna de macroinvertebrados bentónicos asociada a la pesquería de “caracol fino” Zidona dufresnei (Mollusca, Gastropoda) en la plataforma continental uruguaya fue estudiada en base a tres cruceros de pesca. Se determinó la composición y riqueza específica, diversidad y dominancia cualitativa mediante el análisis de 172 lances efectuados con red de arrastre de fondo. Se registraron 55 especies de macroinvertebrados asociadas a Z. dufresnei en el Atlántico uruguayo, resultando los moluscos y los crustáceos los taxa dominantes en número y frecuencia de ocurrencia. Dos gasterópodos (Adelomelon beckii y Tonna galea), dos crustáceos decápodos (Libinia spinosa y Propagurus gaudichaudii), un asteroideo (Astropecten brasiliensis), y un Actiniaria ind. fueron las especies más representativas en el bycatch del “caracol fino”. Se recomienda considerar nuevos gradientes batimétricos a los efectos de profundizar en el conocimiento de la diversidad macrobentónica en la plataforma continental uruguaya, en futuros estudios.

Palavras Clave: Macrofauna bentónica, fauna asociada, diversidad, dominancia cualitativa, Uruguay.

Introduction started to foresee the potential effects of the Bottom trawling and the use of other active fishery generalized disturbance of the sea floor due to the techniques disrupt marine bottoms in the same way growth in number and capacity of the fleet of bottom as logging affects forest ecosystems. Although it is trawlers (Watling & Elliot 1998). easy to recognize the effects of deforestation on Unrestricted fishery has different impacts on biological diversity and economic sustainability, marine ecosystems. Fishery has direct effects on concern for the loss of marine benthic habitats as a target species, reducing populations and stocks, result of fishery is far less common. In fact, it was affecting body size composition, and in some cases not until the middle of 1980’s that marine biologists spawning biomass. Moreover, it has also indirect

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Benthic macroinvertebrate bycatch in Zidona dufresnei Uruguayan fishery. 105 effects on predator-prey interactions, modifying Materials and Methods community structure, even generating temporal Study Area alternative states. A genetic selection of certain size The study was carried out in the classes and reproductive characteristics can also be north-eastern zone of the Uruguayan continental promoted, reducing or removing local stocks. Two shelf, between 34º20' - 35º22' Lat S and additional indirect perturbations associated with the 52º47' - 54º53' Long W, which represents the fishery are the bycatch or mortality of non-target most important fishing grounds for Zidona dufresnei species, and the reduction of habitat complexity, in Uruguay (DINARA 1997). The snail’s fishing particularly by bottom trawling (Kaiser et al. 2001). area is 30 to 70 m deep (Fig. 1), with sandy, muddy, Coastal macrobenthic communities are and occasionally rocky bottoms. This zone ecologically and economically important. They is influenced by the Malvinas and Brazil currents, provide a number of ecological services to mankind, plus a significant flow of fresh water from the Río not restricted to their role in the nutrient and organic de la Plata, which results in a peculiar matter recycling and as supporting biomass for hydrographical system (Guerrero & Piola 1997, fishes (Caddy 1989). Ortega & Martínez ‘in press’). Given their relevance, identification of priority areas for marine conservation is critical, and in order to do so, basic knowledge on macrobenthic diversity is essential (Costello 1998). Exploratory studies on macrobenthic spatial patterns will contribute to a more responsible use of the marine environment (Van Hoey et al. 2004). Unfortunately, large portions of the coastal sea-bed, particularly in the Southern Hemisphere, remain poorly described, even in aspects as basic as species composition and habitat associations. The knowledge on faunal composition at the continental shelf will facilitate the prediction of potential impacts resulting from the development and growth of demersal fisheries, and will help to identify species potentially important Figure 1. Portion of the Uruguayan continental shelf where from a socio-economic point of view. fishing operations were carried out. Although several studies have described benthic communities in the South Atlantic region Sampling and laboratory methods (Buckup & Thomé 1962, Olivier et al. 1968, Escofet A total of 172 fishing hauls were undertaken et al. 1978, Roux et al. 1993, Capitoli 1996, Klein et during three commercial fishing trips (September al. 2001, Giberto et al. 2004), studies focusing on and November 2000, and May 2001), with scientific the benthic associations in the Uruguayan shelf are observers from the National Direction of Aquatic rather scarce (Juanicó & Rodríguez-Moyano 1975, Resources (DINARA) on board (Fig. 1). Milstein et al. 1976, Riestra 2000). Most of these Commercial outrigger trawlers, rigged to tow one previous studies focused on specific groups such as bottom otter trawl on each outrigger, were used in molluscs (Olivier & Scarabino 1972, Scarabino the three fishing trips where benthic 1973, Layerle & Scarabino 1984), decapod macroinvertebrate samples were taken (FAO 2005). crustaceans (Itusarry 1984), echinoderms (Barattini The trawls employed in the Z. dufresnei fishery had 1938, Bernasconi 1966, Lucchi 1985) and a 100 mm mesh size between opposed knots, a polychaetan annelids (Faget 1983). The focus of this mouth framed by a headline with floats providing a study encompasses an array of these invertebrates, maximum vertical opening of 1.5 m and a ground analyzing the benthic macroinvertebrates associated gear with chains, designed according to the bottom with the marine gastropod Zidona dufresnei condition to maximize the catches and protect the (Donovan, 1823), a volutid snail locally known as gear from damage. “caracol fino”, an important fishery resource in the Samples of the benthic macroinvertebrate Uruguayan continental shelf. bycatch were taken along each one of the three

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 106 G. RIESTRA ET AL. campaigns and from each fishing haul, labelled and Bycatch fixed in 10% formaldehyde. Afterwards, in the The macroinvertebrate bycatch associated laboratory, the organisms collected were identified with the snail Zidona dufresnei fishery in the to the lowest possible taxonomic level, in most of Uruguayan continental shelf included 55 species the cases to species level. Sampling location (GPS), (data of all trips combined). These species belong to depth, speed and tow’s duration were also registered 5 phyla (Table I and II): mollusks (45%) and for each fishing haul. The total swept area (square arthropods (36%) were the most represented, nautical miles: nm2) in each campaign was followed by echinoderms (7%), cnidarians (7%) and calculated using the vessel speed, the maximum annelids (6%). horizontal gear opening and the duration of each trawl. Species richness and diversity The total number of species (S) identified Data analyses in September 2000 (S = 33 species) was larger than Mean species richness (Sm) for each in November 2000 (S = 31 species) and May 2001 trip was obtained from the species richness of (S = 25 species). However, the total number of each haul, based on the number of benthic species, the mean species richness and the mean macroinvertebrate species obtained. Mean diversity diversity did not differ significantly among (Shannon-Weaver 1979: H’m) for each campaign campaigns (Table II). was also calculated, using the diversity of each haul. A Chi-square test (χ2) was performed to test for Qualitative dominance differences in Sm and H’m between fishing trips Based on data of the three campaigns (Zar 1999). combined, the very abundant category was The relative importance of the different composed of the exploited target species species in the three trips combined was assessed Z. dufresnei (98%), Libinia spinosa Milne-Edwards, using Qualitative dominance (Bouderesque 1971) 1834 (89%) and Adelomelon beckii (Broderip, 1836) according to the frequency of occurrence (%). (87%). Tonna galea (Linnaeus, 1758), Propagurus Five categories were defined by this author: gaudichaudii Milne-Edwards, 1836, Actiniaria ind. occasional (0-20%), scarce (21-40%), common (41- and Astropecten brasiliensis Müller & Troschel, 1842, were abundant, 4 species were common, 60%), abundant (61-80%) and very abundant (81- 7 were scarce and 37 were occasional (Table III). 100%). Other species with very low occurrence Based on the presence-absence species (scarcely present in one haul), were not considered matrix, and employing a Similarity Coefficient (Q- for this analysis: Astrangia rathbuni Vaughan, 1906, mode), the similarity between species was calculated Aequipecten tehuelchus d’Orbigny, 1842, for each trip. An Unweighted Pair Group Method for Lithophaga patagonica (d’Orbigny, 1842), Arithmetic averages (UPGMA) (Legendre & Pododesmus rudis (Broderip, 1834), Pteria Legendre 1979) was applied as a technique of hirundo (Linnaeus, 1758), Transenpitar americana average linking. (Doello-Jurado, 1951), Bostrycapulus aculeatus (Gmelin, 1791), Crepidula sp., Polystira Results formosissima (E. A. Smith, 1915), Balanidae ind., The mean duration of campaigns was Heterosquilla platensis (Berg, 1900), Corystoides 13 days, with a maximum number of fishing hauls chilensis Lucas, 1844, Leucippa pentagona in September and May (59 hauls) and a minimum in Milne-Edwards, 1833, Ovalipes trimaculatus November (54 hauls). Mean haul duration (± SE) (De Haan, 1933), Pinnotheres sp. and Portunus was shorter in May (3.14 ± 0.12 hours) than in spinicarpus (Stimpson, 1871). November (3.38 ± 0.49 hours) and September (3.45 ± 0.46 hours). The shortest (1.00 hour) and the Similarity longest (4.35 hours) hauls occurred in May. Based on the cluster analysis, the highest However, mean haul speed (± SE) was faster similarity (> 93%) was found between Z. dufresnei, in November (3.1 ± 0.13 knots) than in May L. spinosa and A. beckii for both September (Fig. 2a) (2.8 ± 0.08 knots) and September (2.8 ± 0.15 knots). and November (Fig. 2b) campaigns. However, in The bottom swept area was larger in November May 2001, the highest similarity (90%) was (6.9 nm2) than in May (5.9 nm2) and September found between the fishing target species and T. (5.8 nm2). galea (Fig. 2c). Considering a level of similarity

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 Benthic macroinvertebrate bycatch in Zidona dufresnei Uruguayan fishery. 107

Table I - Species composing of the benthic macroinvertebrate bycatch of the snail Zidona dufresnei fishery in the Uruguayan continental shelf.

Phylum Cnidaria Prunum martini (Petit, 1853) Class Anthozoa Tonna galea (Linnaeus, 1758) Alcyonaria ind. Zidona dufresnei (Donovan, 1823) Antholoba achates (Drayton, 1846) Class Cephalopoda Astrangia rathbuni Vaughan, 1906 Loligo sanpaulensis Brakoniecki, 1984 Phlyctenanthus australis Carlgren, 1950 Octopus tehuelchus d’ Orbigny, 1834

Phylum Annelida Phylum Echinodermata Class Polychaeta Class Asteroidea Aphrodita longicornis Kingberg, 1855 Asterina stelliffer (Möbius, 1859) Phyllochaetopterus socialis Claparède, 1870 Astropecten brasiliensis Müller & Troschel, 1842 Polychaeta ind. Luidia sp. Class Ophiuroidea Phylum Mollusca Ophiuroidea ind. Class Polyplacophora Chaetopleura angulata (Spengeler, 1797) Phylum Arthropoda Class Bivalvia Class Crustacea Aequipecten tehuelchus d’Orbigny, 1842 Balanidae ind. Corbula patagonica d’Orbigny, 1846 Callinectes sapidus Rathbun, 1896 Ennucula uruguayensis (E.A. Smith, 1885) Corystoides chilensis Lucas, 1844 Lithophaga patagonica (d' Orbigny, 1842) Farfantepenaeus paulensis (Pérez-Farfante, 1967) Mytilus edulis Linnaeus, 1758 Hepatus pudibundus (Herbst, 1785) Ostrea puelchana d' Orbigny, 1842 Heterosquilla platensis (Berg, 1900) Panopea abbreviata Valenciennes, 1839 Leucippa pentagona Milne-Edwards, 1833 Pitar rostratus (Koch, 1844) Leurocyclus tuberculosus Milne-Edwards & Lucas, 1842 Pododesmus rudis (Broderip, 1834) Libinia spinosa Milne-Edwards, 1834 Pteria hirundo (Linnaeus, 1758) Metanephrops rubellus (Moreira, 1905) Trachycardium muricatum (Linnaeus, 1758) Ovalipes trimaculatus (De Haan, 1933) Transenpitar americana (Doello-Jurado, 1951) Propagurus gaudichaudii Milne-Edwards, 1836 Class Gastropoda Peltarion spinosulum (White, 1843) Adelomelon beckii (Broderip, 1836) Persephona mediterranea (Herbst, 1794) Adelomelon brasiliana (Lamarck, 1811) Pinnotheres sp. Buccinanops cochlidium (Dillwyn, 1817) Platyxanthus crenulatus Milne-Edwards, 1879 Bostrycapulus aculeatus (Gmelin, 1791) Platyxanthus patagonicus Milne-Edwards, 1879 Crepidula sp. Pleoticus muelleri (Bate, 1888) Cymatium parthenopeum (von Salis, 1793) Portunus spinicarpus (Stimpson, 1871) Polystira formosissima (E.A. Smith, 1915) Scyllarides deceptor Holthuis, 1963

of 80%, the Actiniaria ind. and Buccinanops Discussion cochlidium were added to the original group, and an Some methodological constraints must be association between Octopus tehuelchus and A. considered before the discussion of the results. The brasiliensis appeared in September 2000 (Fig. 2a). objective of the fishing campaigns and mainly the Propagurus gaudichaudii, Pitar rostratus, T. galea, sampling procedure employed, which only caught Ostrea puelchana and A. brasliensis were included large macroepifauna (> 50 mm), not allow a comparison with previous studies in the region. in the initial similarity group in November 2000 The 55 species of benthic macro- (Fig. 2b), and P. gaudichaudii and L. spinosa were invertebrates that form the bycatch of the snail incorporated to the initial group in May 2001 Z. dufresnei’s fishery on the Uruguayan (Fig. 2c). Considering a 60% similarity level, continental shelf represent a lower species richness the same seven species were associated in the than for other areas of the Southeastern three campaigns: Z. dufresnei, A. beckii, T. galea, Atlantic region already described, such as the L. spinosa, P. gaudichaudii, A. brasiliensis and southern Brazilian Atlantic littoral (Klein et al. Actiniaria ind. (Figs. 2 a, b and c). 2001), the Rio de la Plata estuary and adjacent shelf

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 108 G. RIESTRA ET AL.

Table II - Mean species richness (Sm ± SE), mean diversity (H’m ± SE), associated χ2 test statistics, and phyla composition (%) of the bycatch of the three fishing campaigns.

Sep 2000 Nov 2000 May 2001 12 ± 3.6 11 ± 2.5 9 ± 2.9 Mean species richness χ2 = 1.17; P = 0.56 2.5 ± 0.3 2.3 ± 0.3 2.2 ± 0.3 Mean diversity χ2 = 0.02; P = 0.99 Mollusca 43 46 52 Arthropoda 33 32 28 Phyla Echinodermata 9 13 8 composition Annelida 9 6 8 Cnidaria 6 3 4 waters (Giberto et al. 2004), and the Mar del Plata chosen: two gastropod molluscs (A. beckii and (Argentina) region (Roux et al. 1993). It must be T. galea), two decapod crustaceans (L. spinosa and taken into account that the lack of previous studies P. gaudichaudii), one asteroid echinoderm in the region, regarding the macrobenthic bycatch in (A. brasiliensis) and one Actiniaria ind. These the Z. dufresnei’s fishery, does not results agree partially with those of Buckup & allow an adequate comparison. Nevertheless, the Thomé (1962), who considered Z. dufresnei, Shannon-Weaver diversity index obtained for the L. spinosa and Adelomelon brasiliana as very Uruguayan continental shelf was in agreement with frequent species in the Rio Grande do Sul those documented for the Argentinean zone (Roux et continental shelf (Brazil) between 20 and 50 m deep. al. 1993, Roux & Bremec 1996). In the present study, A. brasiliana did not follow The macroinvertebrate community defined that association, being classified as an occasional as the bycatch of the Z. dufresnei’s fishery showed species. faunal components of warm-temperate (e.g., Despite L. spinosa and the hermit crab H. platensis, L. pentagona and P. muelleri) and Dardanus arrosor insignis were documented as very cold-temperate regions (e.g., P. gaudichaudii and P. frequent species for that zone by Itusarry (1984), spinosulum) (Boschi et al. 1992). This could be only the first one was founded in our study. The explained by the convergence of different water unexpected absence of this hermit crab could be masses with contrasting thermohaline that partially ascribed to a potential error in the characterize the Uruguayan continental shelf identification of the hermit crabs. In the other hand, (Ortega & Martínez ‘in press’). Tropical Water the frequent occurrence of A. brasiliensis is in carried southward by the Brazil Current agreement with the results of Juanicó & Rodríguez- (Sverdrup et al. 1942), Subantarctic Water advected Moyano (1975) for the south-eastern zone of La northwards by the Malvinas Current (Bianchi et al. Paloma (Rocha, Uruguay), where it was the second 1993) and Coastal Waters mainly from the Rio de la faunal component, only preceded by Mytilus edulis, Plata estuary, result in this peculiar hydrographical between 35 and 50 m deep. This asteroid was also system (Guerrero & Piola 1997, Ortega & Martínez very well represented in the Euvola ziczac shell ‘in press’). banks at the Brazilian south coast (20 to 50 m depth) The highest qualitative dominance values (Klein et al. 2001). The very low frequency obtained corresponding to molluscs and crustaceans for Mytilus platensis, Lithophaga patagonica, are in agreement with those found for the Bostrycapulus aculeatus, and Chaetopleura isabellei Argentinean and Brazilian continental shelves could be explained by the fact that these species are (Bastida et al. 1992, Roux et al. 1993, Roux & highly associated with hard bottoms (Roux et al. Bremec 1996, Bremec & Roux 1997, Klein et al. 1993), where the Uruguayan Z. dufresnei fishery 2001), although those authors used different does not operates. sampling methods. A biological association between the snail To characterize the macrobenthic B. cochlidium and the actinian Phlyctenanthus invertebrates associated with the snail Z. dufresnei in australis, described by Pastorino (1993) for the Uruguayan continental shelf, six species with a Patagonian coastal waters (Argentina), was also coefficient of similarity higher than 60% were observed in our study. Other associations that were

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 Benthic macroinvertebrate bycatch in Zidona dufresnei Uruguayan fishery. 109

Table III - Qualitative Dominance (%) (Bouderesque, 1971) of each species and their corresponding phylum: (A) Arthropoda, (An) Annelida, (C) Cnidaria, (E) Echinodermata, (M) Mollusca.

Category Species Phylum Qualitative dominance (%) Zidona dufresnei M 98.3 Very Abundant Libinia spinosa A 89.2 Adelomelon beckii M 86.6 Tonna galea M 74.7 Abundant Propagurus gaudichaudii A 74.0 Actiniaria ind. C 71.0 Astropecten brasiliensis E 68.1 Buccinanops cochlidium M 56.3 Common Aphrodita longicornis An 55.4 Platyxanthus crenulatus A 48.8 Octopus tehuelchus M 43.1 Pitar rostratus M 39.4 Asterina stellifer E 35.8 Platyxanthus patagonicus A 33.5 Scarce Phyllochaetopterus socialis An 33.1 Leurocyclus tuberculosus A 31.5 Ostrea puelchana M 24.6 Farfantepenaus paulensis A 23.1 Loligo sanpaulensis M 17.2 Cymatium parthenopeum M 13.6 Metanephrops rubellus A 11.6 Mytilus edulis M 10.0 Peltariom spinosulum A9.6 Chaetopleura angulata M8.9 Luidia sp. E6.2 Adelomelon brasiliana M5.5 Panopea abbreviata M4.9 Trachicardium muricatum M4.0 Ophiuroidea ind. E3.1 Persephona mediterranea A2.4 Ennucula uruguayensis M1.7 Ovalipes trimaculatus A1.7 Pleoticus muelleri A1.7 Polychaeta ind. An 1.2 Alcyonaria ind. C 1.1 Astrangia rathbuni C0.6 Occasional Aequipecten tehuelchus M0.6 Balanidae ind. C 0.6 Bostrycapulus aculeatus M0.6 Callinectes sapidus A0.6 Corbula patagonica M0.6 Crepidula sp. M0.6 Corystoides chilensis C0.6 Hepatus pudibundus A0.6 Heterosquilla platensis A0.6 Leucippa pentagona C0.6 Lithophaga patagonica M0.6 Pinnotheres sp. C0.6 Pododesmus rudis M0.6 Polystira formosissima M0.6 Portunus spinicarpus C0.6 Prunum martini M0.6 Pteria hirundo M0.6 Transenpitar americana M0.6 Scyllarides deceptor A0.6

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 110 G. RIESTRA ET AL.

T.galea A .longicornis a Z.dufresnei L.spinosa A .beckii Actiniaria ind. B.cochlidium O.tehuelchus A .brasiliensis P.gaudichaudii O.puelchana P.crenulatus L.sanpaulensis L.tuberculosus F.paulensis P.socialis C.parthenopeum A .stellifer P.rostratus P.spinosulum M.rubellus M.edulis P.patagonicus P.abbreviata C.angulata P.mediterranea A .brasiliana Pinnotheres sp. S.deceptor Ophiuroidea ind. T.muricatum Alcyonaria ind. H.pudibundus 0 20 40 60 80 100

M.edulis b M.rubellus T.muricatum E.uruguayensis P.muelleri F.paulensis O.tehuelchus P.crenulatus A.magna.longicornis Z.dufresnei A.beckii L.spinosa P.gaudichaudiP.gaudichaudii P.rostratus T.galea O.puelchana A.brasiliensis P.patagonicus A.stellifer Luidia sp. C.parthenopeum CephalodiscusP.socialis sp. O.trimaculatus Alcyonaria ind. C.patagonica L.sanpaulensis C.sapidus Ophiuroidea ind. C.angulata A.brasiliana P.mediterranea 0 20 40 60 80 100

F.F.paulensis c C.C.angulata C.C.partenopheum P.P.martini P.martiniP.spinosulum M.M.edulis O.O.tehuelchus B.B.cochlidium P.P.crenulatus A.brasiliensis. A.stellifer. Z.Z.dufresnei T.T.galea P.P.gaudichaudii L.L.spinosa Actiniarianthozoa ind. A.becki. i L.L.tuberculosus A.longicornis. CephalodisP.socialis c O.O.puelchana M.M.rubellus P.P.abbreviata A.brasiliana. P.P.rostratus 0 20 40 60 80 100 Fig. 2 - Species dendrogram (UPGMA). Dotted vertical line represents the 90% of similarity between species: a) September 2000, b) November 2000 and c) May 2001.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113 Benthic macroinvertebrate bycatch in Zidona dufresnei Uruguayan fishery. 111 already observed for Argentinean waters were also E.W. Langton, A.N. Shepard & I.G. Babb. found in the Uruguayan continental shelf: 1996. The impacts of mobile fishing gear on A. brasiliana and the actinia Antholoba achates seafloor habitats in the Gulf of Maine (Luzzatto & Pastorino 2006) and Libinia spinosa (Northwest Atlantic): implications for with A. achates (Acuña et al. 2003). conservation of fish populations. Reviews in Even if in the last years the number of Fisheries Science, 4 (2): 185 - 202. vessels in the fishery of “caracol fino” has Barattini, L. 1938. Equinodermos uruguayos. substantially diminished, the fishery is still open and Boletín del Servicio Oceanográfico y de the bottom is still heavily trawled. Fishing gears Pesca, 17-29. alters seafloor habitats and understanding the extent Bastida, R., A. Roux & Martínez, D. 1992. Benthic of these impacts, and the effects on populations of communities of the Argentine continental living marine resources, is needed to properly shelf. Oceanologica Acta, 15 (6): 687 - 698. manage current and future levels of fishing effort Bernasconi, I. 1966. Los equinoideos y asteroideos (Auster et al. 1996). The knowledge of the colectados por el Buque Oceanográfico R/V macroinvertebrate diversity results essential for a “Vema”, frente a las costas argentinas, sustainable fisheries management and the uruguayas y sur de Chile. Revista del development of potentially valuable resources. Museo Argentino de Ciencias Naturales Because of the lack of pristine sites, where the use of active fishing is prohibited, no empirical studies that “Bernardino Rivadavia”, Tomo IX (7): could demonstrate population level effects of bottom 147 - 175. trawling, have been conducted so far. If marine Bianchi, A., C. Giulivi & Piola, A. 1993. Mixing fisheries management is to evolve toward an in the Brazil–Malvinas Confluence. Deep ecosystem or habitat management approach, Sea Research Part I, 40 (7): 1345 - 1358. experiments are required on the effects of habitat Boschi, E., C. Fischbach & Iorio, M. 1992. change, both anthropogenic and natural (Auster et Catálogo ilustrado de los crustáceos al. 1996). According to the current gap in the estomatópodos y decápodos marinos de knowledge of macrobenthic diversity in the Argentina. Frente Marítimo 10 (Sec. A): 7 Uruguayan continental shelf, further investigations - 94. concerning unexplored bathymetric gradients with Bouderesque, Ch. 1971. Méthodes d’étude systematic samplings and experiments are strongly qualitative et quantitative du benthos (en recommended. particulier du phytobenthos). Tethys 3 (1): 79 - 104. Acknowledgments Bremec, C. & Roux, A. 1997. Resultados del The authors wish to thank the collaboration of the análisis de una campaña de investigación fishing companies as well as to the captains and pesquera, sobre comunidades bentónicas crews of the snail vessels. We also express our asociadas a bancos de mejillón (Mytilus sincere thanks to F. Scarabino for his comments on edulis platensis D’Orb.) en costas de Buenos the determination of species and for bibliography. Aires, Argentina. Revista Investigación y We also gratefully acknowledge Dr. M. Zamponi for Desarrollo Pesquero 11: 153 - 166. his identification of the actinian. The authors want to Buckup, L. & Thomé, J. 1962. I Campanha thank Dr. E. Spivak, Dr. P. Quijón, Dr. S. Acevedo oceanográfica do Museu Rio Grandense de and Dr. McCormark for the critical revision of the Ciências Naturais – a viagem do “Pescal II” manuscript and especially to Dr. Alexandre García en julho de 1959. Iheringia 20: 1 - 42. and Dr. Gonzalo Velasco, Editorial Board of Pan- Caddy, J. 1989. Recent developments in research American Journal of Aquatic Sciences. and management for wild stocks of bivalves and gastropods. p. 665-699 In: J. Caddy (Ed), Marine Invertebrate Fishery: their References assessment and management. John Wiley Acuña, F., A. Excoffon & Scelzo, M. 2003. Sons, London. 699 p. Mutualism between the sea anemone Capitoli, R. 1996. Continental shelf benthos. Antholoba achates (Drayton, 1846) (Cnidaria: Chapter 6, p. 117-120. In: U. Seeliger, C. Actiniaria: Actinostolidae) and the spider crab Odebrecht & J.P. Castelo (Eds), Libinia spinosa Milne-Edwards, 1834 Subtropical Convergence Environments. (Crustacea: Decapoda, Majidae). Belgian Springer-Verlag, Berlín. 120p. Journal of Zoology, 133 (1): 85 - 87. Costello, M. 1998. To know, research, manage and Auster, P.J., R.J. Malatesta, R.W. Langton, L. conserve marine biodiversity. Oceanis 24: Watling, P.C. Valentine, C.L.S. Donaldson, 25 - 49.

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DINARA. 1997. Decreto 149/997.- Ajústese y Klein, J., C. Borzone & Pezzuto, P. 2001. A macro actualízase la reglamentación referente a la e megafauna béntica asociada aos bancos da explotación y dominio sobre riquezas del vieira Euvola ziczac (Mollusca: Bivalvia) no mar. Instituto Nacional de Pesca, Ministerio litoral sul do Brasil. Atlántica 23: 17 - 26. de Ganadería, Agricultura y Pesca. Layerle, C. & Scarabino, V. 1984. Moluscos del Montevideo, 16p. Frente Marítimo uruguayo entre 9 y 78 Escofet, A., J. Orensanz, S. Olivier & Scarabino, V. metros de profundidad: análisis 1978. Biocenología bentónica del Golfo San biocenológico. Contribuciones del Matías (Río Negro, Argentina): metodología, Departamento de Oceanografía (Facultad experiencias y resultados del estudio de Humanidades y Ciencias) 1 (9): 1 - 17. ecológico de un gran espacio en América Legendre, L. & Legendre, P. 1979. Ecologie Latina. Anales del Centro Ciencias del Mar numérique. Masson, Paris et les Presses de y Limnología. Universidad Nacional l’Université du Québec 2: 1 - 254. Autónoma de México 5 (1): 59 - 82. Lucchi, C. 1985. Ophiuroidea (Echinodermata) del Faget, M. 1983. Consideraciones sobre la fauna de Frente Marítimo uruguayo hasta 800 m de poliquetos de la plataforma continental profundidad, con claves para su uruguaya. Lic. Thesis. Universidad de la identificación. Contribuciones República, Facultad de Humanidades y Departamento de Oceanografía (Facultad Ciencias, Montevideo, Uruguay, 125p. de Humanidades y Ciencias) 2 (6): 165 - FAO. 2005. Fisheries Global Information System: 171. Fisheries Technologies. World Electronic Luzzatto, D. & Pastorino, G. (2006) Adelomelon Database accessible at http://www.fao. brasiliana and Antholoba achates: a org/figis/servlet/static?dom=root&xml=tech/i phoretic association between a volutid ndex.xml gastropod and a sea anemone in Argentine Giberto, D., C. Bremec, E. Acha & Mianzan, H. waters. Bulletin of Marine Science 78: 281 2004. Large-scale spatial patterns of benthic - 286. assemblages in the SW Atlantic: the Río de la Milstein, A., M. Juanicó & Olazarri, J. 1976. Plata estuary and adjacent shelf waters. Algunas asociaciones bentónicas frente a las Estuarine Coastal and Shelf Science 61: 1 - costas de Rocha, Uruguay. Resultados de la 13. Campaña del R/V “Hero”, Viaje 72-3A. Guerrero, R. & Piola, A. 1997. Masas de agua en la Comunicaciones de la Sociedad Plataforma Continental. 107-118 pp. In: E. Malacológica del Uruguay IV (30): 143 - Boschi (Ed), El mar Argentino y sus 164. recursos pesqueros. Instituto Nacional de Olivier, S. & Scarabino, V. 1972. Distribución Investigación y Desarrollo Pesquero 1, Mar ecológica de algunos moluscos recogidos del Plata, Argentina. por la expedición del “Walter Herwing” Itusarry, E. 1984. Taxonomía y distribución de los (R.E.A.) al Atlántico sudoccidental (1966). crustáceos (Decapoda) en el Frente Marítimo Revista Brasilera de Biología 32 (2): 235 - Uruguayo para los meses de febrero y marzo 247. de 1982 (Cruceros 8201-05 del B/P Lerez). Olivier, S., R. Bastida & Torti, M. 1968. Lic. Thesis. Universidad de la República, Resultados de las campañas oceanográficas Facultad de Humanidades y Ciencias, Mar del Plata I-V. Contribución al trazado Montevideo, Uruguay. 107pp. de una carta bionómica del área de Mar del Juanicó, M. & Rodríguez-Moyano, M. 1975. Plata. Las asociaciones del sistema litoral Composición faunística de la comunidad de entre 12 y 70 m de profundidad. Boletín del Mytilus edulis platensis D’Orbigny, 1846 Instituto de Biología Marina. Universidad ubicada a unas 55 millas al SE de La Paloma. Nacional de Buenos Aires (16): 1 - 85. Comunicaciones de la Sociedad Ortega, L. & Martinez, A. ‘in press’. Multiannual Malacológica del Uruguay IV (29): 113 - and seasonal variability of water masses and 116. fronts over the Uruguayan Shelf. Journal of Kaiser, M., J. Collie, S. Hall, S. Jennings & Poiner, Costal Research 22 (1) Accepted 3/6/05. I. 2001. Impacts of fishing gear on marine Pastorino, G. 1993. The association between the benthic habitats. Conference on Responsible gastropod Buccinanops cochlidium Fisheries in the Marine Ecosystem, (Dillwyn, 1817) and the sea anemone Reykjavik, Iceland. Phlyctenanthus australis Carlgren, 1949 in

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Patagonian Shallow waters. The Nautilus 106 (Sistemática, distribución). V Congreso (4): 152 - 154. Latinoamericano de Zoología, 1: 192 - Riestra, G. 2000. Análisis de la fauna acompañante 203. asociada a la pesquería de Zygochlamys Shannon, C. & Weaver, W. 1979. The patagonica en aguas uruguayas. 153-157 p. mathematical theory of communication. In: M. Rey (Ed) Recursos Pesqueros No University Illinois Press, Urbana: 117pp. Tradicionales: Moluscos Bentónicos Sverdrup, H., M. Johnson & Fleming, R. 1942. Marinos. Programa de las Naciones Unidas The Oceans. Their physics, chemistry and para el Desarrollo–Instituto Nacional de general biology. New York, Prentice Hall: Pesca, Montevideo 157pp. 1087 pp. Roux, A. & Bremec, C. 1996. Comunidades Van Hoey, G., S. Degraer & Vincx, M. 2004. bentónicas relevadas en las transecciones Macrobenthic community structure of soft- realizadas frente al Río de la Plata (35º15’S), bottom sediments at the Belgian Continental Mar del Plata (38º10’S) y Península Valdés Shelf. Estuarine Coastal and Shelf Science (42º35’S), Argentina. INIDEP Informe 59: 599 - 613. Técnico 11. Mar del Plata: 13pp. Watling, L. & Elliot, A. 1998. Disturbance of the Roux, A., R. Bastida & Bremec, C. 1993. Seabed by Mobile Fishing Gear: A Comunidades bentónicas de la plataforma Comparison to Forest Clearcutting. continental argentina. Campañas transección Conservation Biology 6 (12): 1180 - 1197. B/P “Oca Balda” 1987/88/89. Boletín Zar, J. 1999. Biostatistical analysis. Prentice-Hall, Instituto Oceanográfico San Paulo 41 (1-2): Englewood Cliffs, NJ: 717 pp. 81 - 94. Scarabino, V. 1973. Scaphopoda (Moll) del sur del Brasil, Uruguay y Argentina hasta 42ºS

Received June 2006 Accepted October 2006 Published online December 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 104-113

Feeding Ecology of Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) on Estuarine and Lagoon Environments in the Southwest Coast of Portugal

1, 2 3 2, 4 PEDRO FIDALGO E COSTA , RUI F. OLIVEIRA & LUÍS CANCELA DA FONSECA

1 Escola Superior de Educação João de Deus, Av. Alvares Cabral, 69, P - 1269-094 Lisboa, Portugal, e-mail: [email protected] 2 IMAR/Laboratório Marítimo da Guia, Estrada do Guincho, P - 2750-642 Cascais, Portugal. 3 Unidade de Investigação em Eco-Etologia, Instituto Superior de Psicologia Aplicada, R. Jardim do Tabaco 44, P - 1149-004 Lisboa, Portugal. 4 FCMA, Universidade do Algarve, Campus de Gambelas, P - 8005-139 Faro, Portugal.

Abstract. The feeding ecology of Nereis diversicolor (O. F. Müller, 1776) (Annelida: Polychaeta) was studied over 14 months at three estuarine-lagoon systems of the Southwest coast of Portugal (Odeceixe, Aljezur and Carrapateira). The analyses of digestive tract revealed that diet change according to site, period of the year and individual sizes. There are no differences in the digestive contents between sexes. In all sampling stations a total of thirty items were found, but only five shown an occurrence superior to 1%. These were: mucus (56.3%), sand (17.6%), vegetable detritus (10.7%), Nereididae (7.7%) and Corophium sp. (1.8%). N. diversicolor was detected in all sampling stations with a filter-feeding behaviour, although in Carrapateira there is evidence of slightly higher carnivore behaviour than in Odeceixe and Aljezur. Mucus (a food complex including organic matter, bacteria, fungi and phytoplankton) was the main gut content.

Key words: Seaworms, “common ragworm”, feeding behaviour, diet, brackish environments.

Resumo. Ecologia Alimentar de Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) em Ambientes Estuarino-Lagunares da Costa Sudoeste de Portugal. A ecologia alimentar de Nereis diversicolor (O.F. Müller, 1776) (Annelida: Polychaeta) foi estudada num período de 14 meses em três sistemas estuarino-lagunares da costa Sudoeste de Portugal (Odeceixe, Aljezur e Carrapateira). A análise do conteúdo digestivo revelou uma variação da dieta de acordo com os locais estudados, época do ano e com o tamanho dos indivíduos. Não houve diferenças nos conteúdos de machos e fêmeas. Foram encontrados em todas as estações amostradas um total de trinta itens, mas apenas cinco revelaram uma ocorrência superior à 1%. Estes foram: muco (56.3%), areia (17.6%), detritos vegetais (10.7%), Nereididae (7.7%) e Corophium sp. (1.8%). N. diversicolor evidenciou hábitos filtradores, em todas as estações amostradas embora na Carrapateira tenham sido detectadas percentagens de carnivoría ligeiramente superiores às encontradas em Odeceixe e Aljezur. O principal conteúdo do tracto digestivo foi o muco (complexo alimentar que aglutina matéria orgânica, bactérias, fungos e fitoplâncton).

Palavras-chave: Poliquetas, “minhocas-da-pesca”, comportamento alimentar; dieta, sistemas salobros.

Introduction and reproduce in different sediment types and in The polychaeta Nereis diversicolor (O. F. Müller, stressed environments (Bartels-Hardege & Zeeck 1776) is widely distributed in estuarine and lagoonal 1990, Cheggour et al. 1990, Miron & Kristensen habitats from North Africa to the North of Europe 1993, Zubillaga & Salinas 1997, Scaps 2002). (Mettam 1979, 1981, Gillet 1993). The species It not only adapts well to a variety of shows high physiological tolerance to extreme environments, but also its feeding habits are quite variations in environmental factors, and can grow generalist. N. diversicolor has a wide capacity

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126

Feeding Ecology of Nereis diversicolor. 115 regarding the size of food it feeds upon, which estuaries (Figure 1), with water basins of about 250, ranges from micro and macrozoobenthos, diatoms, 200 and 110 km2 respectively, which partially drain to fragmented organic matter including detritus the Western part of Southwest Portugal. According (Gorke 1971, Reise 1979, Witte & Wild 1979, Smith to Day et al. (1987), these types of brackish et al. 1996, Lucas & Bertru 1997). This species can environments, although representing a great also uses different strategies to capture its food: i) geomorphological diversity are from an ecological deposit feeding, capturing its food on the sediment point of view lagoon-estuarine ecosystems. surface and around the gallery (Esselink & Zwarts The sampling stations (two for Odeceixe, 1989, Esnault et al. 1990); ii) suspension feeding, three for Aljezur and for Carrapateira) have the releasing a web of mucus in the gallery and through highest occurrences of N. diversicolor according to dorsal-ventral movements, it generates a continuous previous studies conducted in those systems current capturing the phytoplankton in the web to be (Magalhães et al. 1987, Magalhães 1988). To ingested afterward (Harley 1950, Well & Dales facilitate the statistical work and also to keep the 1951, Riisgård 1991, Vedel 1998). It adopts this initial goal of comparing the different brackish feeding strategy when the water column presents a environments, it was decided to combine and high concentration of phytoplankton (Vedel & analyse all data per sampling site (ODX, ALZ and CAR) with no specific reference to the sampling Riisgård 1993); iii) herbivore, it is able to ingest stations, within each site. These are arranged in a parts of algae and aquatic macrophytes (Olivier et al. North-South geographic position in which ODX is 1996, Hughes et al. 2000); iv) carnivore, playing an the sampling site located further north and CAR the important role in the structure of brackish water sampling site further south. The distance between ecosystems, because it acts as a predator of different these two areas is approximately 35 km. bottom fauna species (Rönn et al. 1988). These strategies seem to be related to food availability and Field and laboratory work quality, presence or absence of predators, tidal Monthly data on rainfall, water salinity, near height and season (Esselink & Zwarts 1989, Masson sediment salinity and temperature, and sediment et al. 1995). organic matter, chlorophyll a and phaeopigments Nereis diversicolor, searched as live food or were obtained to characterize the environmental bait by aquaculture and sport fishing activities, is conditions of each site. Salinity and temperature also an important species to the structure of the food values were measured in situ at each station. Surface webs of another lagoonal environment of Portuguese and near sediment salinity values were obtained Southwest coast (Cancela da Fonseca 1989, in order to evaluate fresh water inputs. Bernardo 1990). As a part of a research project dealing with the biology and ecology of this species (Fidalgo e Costa et al. 1998, Fidalgo e Costa et al. 2002), the analysis of the monthly variation of its digestive tract contents was carried out in order to assess its feeding patterns and so, its trophic position in the wild. In addition the type of food ingested by the different size classes, as well as by different sexes, was also investigated.

Materials and Methods Study Area The studied sites are located inside a natural protected area (the Sudoeste Alentejano and Costa Vicentina Nature Park – PNSACV), in which they constitute vital habitats for many species, much of them aquatic birds. It is also one of the best preserved coastal areas in Europe with high landscape, geological and biodiversity richness (Silva e Costa et al. 1983). The sampling stations were established at the lower part of Odeceixe Figure 1 – Map of Portugal and the soutwestern coast showing (ODX), Aljezur (ALZ) and Carrapateira (CAR) the sampling sites (black dotes).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 116 P. FIDALGO E COSTA ET AL.

Rainfall values were obtained from the National binocular stereomicroscope and, when necessary, a Meteorological Institute and General Administration compound microscope. The identification of the of Natural Resources. Organic matter, chlorophyll a found food items was narrowed down to the lowest and phaeopigments of sediment were determined on possible taxonomic level. Due to the conditions of the top centimetre of sediment samples obtained in gut material, we chose to represent individual results each station with a 5 cm diameter corer and were as percentage of occurrence. For each month the frozen until laboratory analysis (Fidalgo e Costa et data were analysed as frequency of occurrence al. 2002). according to the following formula: All specimens of N. diversicolor used in this number of digestive tract with a certain item work were collected between April 1993 and May ×100 1994: i) at low tide in the sublittoral fringe (the number of digestive tract with the observed content upper subtidal layers in a tidal environment) at the lower part of ODX and ALZ; ii) in the sublittoral Sex was determined when the individuals area (the upper submerged layers in a non-tidal were opened to extract out the tract contents. environment) of CAR, in a small coastal lagoon Observation of the oocytes and the sperm plates was formed by the partial closing of a sandy barrier near performed using binocular microscopes and the total the beach. For each station, a total sampling area of sex ratio found in ODX, ALZ and CAR was always 2 female biased, being, respectively, 1:2.9, 1:3.1 and 0.1m was obtained by five sub-samples of 30 cm 2 1:4.1 (Fidalgo e Costa, 2003). depth, using a 0.02 m hand corer. The samples were From sediment samples, pigments were then sieved through a 0.5 mm square mesh and the extracted with 90 % acetone during 24 h in darkness remaining fraction was kept in 10% formalin at 4º C, and subsequently centrifuged. Chlorophyll a buffered with borax. In the laboratory, samples were (surface Chl a is generally used as an index of washed in order to extract the excess of formalin and microphytobenthos biomass) and phaeopigments sediment. The remainder was dipped into a saturated were determined spectrophotometrically by the saccharose solution, which separates the organic method of Lorenzen (1967) adapted by Plante-Cuny from the inorganic matter by flotation (Cancela da (1974) and results expressed as mg m-2. Fonseca 1989, Caron et al. 1993). All samples were The organic matter content of the superficial then kept in 70º alcohol (Möller 1985). layer of sediment was estimated through the loss on Some of the captured animals were too small ignition, a method that, according to Duck (1986), to be dissected while others had no digestive tract provides a close estimate of the total organic matter contents due to damages during sampling. Therefore expressed in g m-2. the guts of 3000 animals were observed but, from these, 907 (30%) had any content (220 in ODX, 460 Data analysis in ALZ and 227 in CAR). The proportions of different food items All individuals were measured, based on the ingested per individual were compared between the length of L3 (length of prostomium, plus sexes using T-tests and among size classes (large, peristomium and 1st chaetiger) according to Gillet medium, small) using one-way ANOVA (each food (1990, 1993). This measure presented the best item was analysed separately). In both cases the correlation with the biomass (Fidalgo e Costa et al. variables conformed to the assumptions of 1998) being a good conversion factor (dry weight parametric statistics of normality and homogeneity 3.479 2 (mg) = 1.982 (L3, mm) , N=259, r =0.914, of variances was investigated by normal probability p<0.001). All measurements were performed using a plots and Levene’s test respectively (Zar 1984, camera lucida and digitising table (Houston Underwood 1997). Instruments HiPad) linked to a PC. For the practical For the statistical analysis of seasonal effects purposes of this study, and according to the previous and due to the scarcity of gut contents in some results on cohort analysis (Fidalgo e Costa et al. months, the data from the different months were 1998), three basic sizes were established (small (S1), merged into four seasons: spring (April and May medium (S2) and large (S3)), being represented by a 1993; March, April and May 1994), summer (June, L3 measure, respectively, of [0.3, 1.5 mm [, [1.5, 3.0 July and August 1993), autumn (September, October mm [ and [3.0, 4.5 mm]. and November 1993) and winter (December 1993; The collection of digestive tract content was January and February 1994). done after opening individuals with iris scissors, Spatial (Odeceixe vs. Aljezur vs. from the first to the last chaetiger. The material was Carrapateira) and seasonal (Spring vs. Summer vs. then placed in a Petri dish and observed with a Autumn vs. Winter) effects in the proportion of food

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 Feeding Ecology of Nereis diversicolor. 117 items ingested were investigated using two-way mg.m-2, n = 24) and winter (113±17.6 mg.m-2, ANOVA after transforming the data (arc-sin of the n = 24) (post-hoc HSD test, p<0.05). square root) to match the assumptions of ANOVA The chlorophyll degradation represented (Underwood 1997), followed by planned by phaeopigment values (Figure 3B), emphasise comparisons to identify the significant differences in when (months) and where (sites) accumulation of the same site along different seasons or among the detritus of plant or microalgae cell occur. The three sites in the same season (Zar 1984, Underwood ANOVA showed only a site effect (F2,100 = 7.97, 1997). A similar analysis (i.e. two-way ANOVA p<0.001). followed by planned comparisons) was performed The sediment organic matter (Figure 3C) is for the abiotic factors measured. Of the abiotic related to grain size composition in the different factors, only salinity and temperature values were sampling sites. The ANOVA showed no significant log-transformed to meet the assumptions of ANOVA differences between sites (F2,100 = 2.19, p = 0.12) and (Underwood 1997). In order to evaluate which season of the year (F3,100 = 0.60, p = 0.62). groups differed significantly from each other post- hoc HSD tests for samples with different sizes were used with a p-level of 0.05 –. All descriptive statistics were expressed as mean ± standard error of the mean. All statistical tests were performed using software package Statistica for Windows v. 5.0, from Statsoft.

Results Abiotic factors and phytopigments Monthly water temperature values showed a variation according to the normal annual behaviour of this parameter (Figure 2). The ANOVA revealed an effect of the sampling site (F2,99 = 30.76, p<0.001) and of the season (F3,99 = 77.50, p<0.001). Significant differences on temperature stress a site effect with CAR presenting the highest value and ODX the lowest (ODX:15.6 ± 0.52 ºC, n = 42; ALZ: 17.5 ± 2.07 ºC, n = 42; CAR: 19.5 ± 0.62 ºC, n = 28) (post-hoc HSD test, p<0.05). There is also an effect caused by seasonality (Spring: 21.3 ± 2.1 ºC, n = 40; Summer; 21.6 ± 0.7 ºC, n = 24; Autumn; 15.7 ± 0.5 ºC, n = 24; Winter: 13.7 ± 0.3 ºC, n = 24 - post-hoc HSD test, p<0.05). Salinity values reflect tidal influence, rainfall and river flow, which is observed through constant stratification throughout the year (Figure 2), especially in spring and winter at sites ODX and ALZ. ANOVA undoubtedly shows an effect of the sampling site (F2,99 = 10.14, p<0.001) due to differences in bottom salinity between CAR (15.0 ± 1.2, n = 42) and the other sampling sites (ODX – 31.8 ± 0.89, n = 28; ALZ – 30.0 ± 2.8, n = 42) (post-hoc HSD test, p<0.05). Sediment chlorophyll a reveals temporal variation (F3,100= 3.46, p = 0.02), associated with the amount of fresh water brought by rain and in particular by the continental runoff that Figure 2 – Monthly rainfall on the south-western coast of penetrates the system (Figure 3A). Significant Portugal (A). Monthly values of salinity (surface and bottom) variations occurred between summer (59.8±9.90 and temperature in ODX (B), ALZ (C) and CAR (D).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 118 P. FIDALGO E COSTA ET AL.

Spatial and seasonal diet variations A total of 30 items were found in gut contents for all sampling sites (Table I). However, from this total only five showed a frequency of occurrence higher than 1%. These items were: mucus (56.3%), sand (17.6%), vegetable detritus (10.7%), Nereididae (7.7%) and Corophium sp. (1.8%). The results for feeding habits of N. diversicolor in all sampling stations clearly show the ingestion of various food items, with differences in occurrence of these items between sites and during the year (Figure 4).

Figure 4 – Different items ingested by N. diversicolor in all sampling stations clearly showing the ingestion of various food items, with differences in occurrence of these items between sites and during the year.

± 1.68 %, n = 383; summer: 59.5 ± 2.0 %, n = 205; autumn: 58.6 ± 2.84 %, n = 163) (post-hoc HSD test, p<0.05). The interaction effect was due to differences between autumn and summer in CAR, and between CAR and ALZ in winter (post-hoc HSD test, p<0.05). There were no significant differences between sampling sites concerning the amount of Figure 3 – Sediment values of chlorophyll a (A), ingested sand (F2,895 = 1.60, p = 0.20). However for phaeopigments (B) and organic matter content (C) in ODX, this variable, noteworthy differences related to ALZ and CAR during the sampling period. season (F3,895 = 5.06, p = 0.002) and interaction

(F6,895 = 4.64, p<0.001) were confirmed by ANOVA. ANOVA showed an effect of sampling In summer N. diversicolor ingested a higher site (F2,895 = 4.65, p = 0.001) and of the season percentage of sand (22.1 ± 1.79 %, n = 205) than in (F3,895 = 3.10, p = 0.03) on the percentage of mucus. spring (15.0 ± 1.18 %, n = 383) (post-hoc HSD test, There was also an effect of the interaction between p<0.05). The effect of the interaction is due to the two independent variables (F6,895 = 2.33, p = differences between ODX and ALZ in autumn (p = 0.03), showing that mucus seems to be the most 0.004), ALZ between spring and autumn (p = 0.004) important item during spring/summer periods, and ALZ between winter and autumn (p = 0.002) mainly in what concerns ODX and CAR The effect (post-hoc HSD test, p<0.05). of sampling site is due to differences between ANOVA results showed, for vegetable detritus, that there were no differences between CAR (50 ± 2.37 %, n = 227), with more lagoonal sampling sites (F2,895 = 1.95, p = 0.14), seasons characteristics, and the two remaining sampling sites (F = 0.35, p = 0.79) and also interaction between (ODX: 61.3 ± 2.17 %, n = 220; ALZ: 56.8 ± 1.54 %, 3,895 them (F6,895 = 1.23, p = 0.27). n = 460) (post-hoc HSD test, p<0.05). On the other Larvae, parapods and bristles of hand, the effect of season was determined by the N. diversicolor as well as some other Nereididae differences between winter (47.7 ± 3.01 %, n = 156) were found in the samples suggesting cannibalistic and the other three seasons of the year (spring: 58.4 behaviour. The ANOVA showed a non significant

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 Feeding Ecology of Nereis diversicolor. 119

Table I – Gut content of N. diversicolor (%) in the ALZ (0.02 ± 0.02 %, n=220; 0.8 ± 0.32 %, n = 460) whole sampling stations (main items in bold). (post-hoc HSD test, p<0.05). There was also an Gut Contents % effect of the interaction between the sampling station and season (F6,895 = 2.23, p = 0.04), due to differences between CAR and ALZ in winter. (post- mucus 56,33 hoc HSD test, p<0.05). Total Sediment 17,64 There was a clear trend for the increment of sand 17,56 the item “other” (other crustaceans, other mud 0,08 polychaetes and different animal groups found in Vegetable detritus 10,68 small quantities - cf. Table I) in the rainy seasons Total Polychaeta 7,92 (autumn, winter and spring – cf. Figure 2A), mainly Nereididae 7,68 at ALZ and CAR (Figure 4). The slight increase in this item in ODX (November and April 1994 - see Spionidae 0,07 Figure 4) was due to the presence of the ostracod Capitellidae 0,03 Cyprideis sp. and the isopod Cyathura carinata. Polychaeta (unidentified) 0,14 ALZ showed a little bit higher species richness than Total Crustacea 4,64 ODX, attributable to the presence of almost Cirripedia 0,01 completely digested and unidentifiable crustaceans. Samples from the family Anthuridae (mainly Cyprideis sp. 0,91 Cyathura carinata), Sphaeroma hookeri, and Ostracoda (unidentified) 0,19 Chironomidae larvae were also found at this site. In Copepoda 0,02 December 1993, February 1994 and April 1994 (see Cyathura carinata 0,44 Figure 4), and in comparison with other sampling Sphaeroma hookeri 0,33 sites a representative amount of unidentifiable parts of crustaceans outer Cyprideis sp., Cyathura Anthuridae 0,08 carinata and Sphaeroma hookeri, were observed in Isopoda (unidentified) 0,18 CAR. Also remarkable was the wide presence of Corophium sp. 1,76 Chironomidae larvae in this sampling site. Gammarus sp. 0,01 Figure 5 shows the contents for each site and also a graph formed by the whole of the sampling Amphipoda (unidentified) 0,29 sites. All crustaceans and polychaetes found were Crustacea (unident. remains) 0,44 grouped for all sampling sites as well as gastropods Others 2,79 and insects were also grouped for ALZ and CAR, Foraminifera 0,27 respectively, to emphasise their consumption by N. Hydrobidae 0,71 diversicolor. The analysis of this figure makes clear the main gradients found in the diet of this species Gastropoda (unidentified) 0,01 from ODX (the northern sampling site) to CAR (the Bivalvia 0,01 southern sampling site): i) sand and mucus decrease Acari 0,01 from ODX to CAR; ii) an increased predation on Chironomidae 0,78 crustaceans and polychaetes from northern to southern sampling sites; iii) gastropods and insects Insecta (unidentified) 0,10 were relevant in the diet respectively, in ALZ and unidentified 0,91 CAR. marginal effect for the sampling sites (F2,894 = 2.70, p Body size and sex effects on diet = 0.07) and a non significant effect for the season of Only mucus (F2,904 = 5.26, p = 0.005) and the year (F = 1.84, p = 0.14). Although, the same 2,894 sand (F2,904 = 6.37, p = 0.002) showed a significant analyses revealed a significant effect of the difference between the three sizes studied (S1, S2 interactions between variables (F6,894 = 2.77, p = and S3) (post-hoc HSD test, p<0.05). Smaller 0.01), due to differences between CAR in spring and individuals (S1) ingest a higher quantity of sand in winter (post-hoc HSD test, p<0.05). (S1S2=S3). The feeding strategies have changed significant effect away from the sampling sites between S1 and S2 / S3 size classes, ingesting the (F2,895 = 20.7, p<0.001) on the percentage of latter higher quantities of mucus (see Table II). Corophium sp. found in the digestive tract of N. There were no significant differences in food diversicolor. This effect is due to the fact that CAR contents between males and females (Table III, T- (5.4 ± 1.19 %, n = 227) is higher than ODX and test for each food item, p>0,05).

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 120 P. FIDALGO E COSTA ET AL.

Table II – Comparison (ANOVA) of gut contents of N. diversicolor (%) separated in different size classes: (S1) small, (S2) medium and (S3) large. S1 S2 S3 n avg. ± se. n avg. ± se. n avg. ± se. F2,904 p Mucus 344 51.9 ± 1.90 542 58.8 ± 1.40 21 66.1 ± 7.05 5.26 0.0053 Sand 21.2 ± 1.52 15.5 ± 0.98 10.7 ± 4.78 6.37 0.0017 Detritus 8.9 ± 1.02 11.1 ± 0.80 10.4 ± 2.57 1.48 0.23 Nereididae 8.15 ± 1.33 7.47 ± 0.90 5.74 ± 3.71 0.22 0.79 Corophium sp. 2.74 ± 0.75 2.17 ± 0.33 0.71 ± 0.70 2.5 0.08

Table III – Male and female N. diversicolor gut Fidalgo e Costa et al. 2002) was also another contents (%). explanation for this result. It is known that N. diversicolor acts as an active filter-feeder through ♂ (n=62) ♀ (n=159) the production of a mucus net, when there is a higher avg ± se. avg ± se. t p predation risk and/or the amount of suspended Mucus 63.0 ± 4.3 58.5 ± 2.8 0.85 0.40 particles is high (Esselink & Zwarts 1989, Vedel & Sand 11.7 ± 2.6 12.6 ± 1,7 -0.28 0.78 Riisgård 1993, Masson et al. 1995). When it is submerged, this feeding strategy may be more Detritus 9.92 ± 2.4 11.1 ± 1.6 -0.40 0.69

Nereididae 5.9 ± 2.4 7.9 ± 1.9 -0.60 0.55 Corophium sp. 1.4 ± 1.3 2.5 ± 1.1 -0.61 0.54

Discussion Nereis diversicolor worms with the digestive tract completely empty were found in the study area. Two main explanations may be used for these results: i) for southern sites, namely CAR, the increase of predatory activity showed a large number of worms with only few unidentifiable remains on the gut contents, pointing out Gaston (1987) statement that empty digestive tracts can reveal a predatory feeding strategy, in which digestion is completed more quickly, as opposed to digestion of vegetable matter rich in cellulose; and ii) the existence of a noticed continuous reproductive activity throughout the year (Fidalgo e Costa et al. 1998), in which the gut was reabsorbed and feeding ceased, as observed for this species and other Nereididae during its sexual maturity period (Golding 1987, Golding & Yuwono 1994, Last & Olive 1999). Mucus, the most frequent item found in the digestive tracts, is not by itself a food item; it is an aggregation complex of organic matter, bacteria, fungi, phytoplankton and microphytobenthos. Differences in the amount of mucus present in the contents between CAR and the remaining sample sites was certainly based on its less eutrophic state (Cancela da Fonseca et al. 2001a). The scarcity of phytoplankton in the bottom water caused by occasional stratification (Figure 2), and/or by the insufficient renewal promoted by the tidal effect, while the connection to the sea in this Figure 5 – Main gut contents of N. diversicolor (%) in the site is reduced (Cancela da Fonseca et al. 2001b, whole sampling stations and in each station separately.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 Feeding Ecology of Nereis diversicolor. 121 effective (Harley, 1950, Wells & Dales, 1951, ingested sand as it was found in CAR sampling site. Esselink & Zwarts, 1989, Vedel, 1998). In CAR, These statements were supported by the work of with its frequent lack of tidal effect, due to its several researchers that have already pointed out the lagoonal properties (except in November 1993 when effect of sediment dynamics, induced by different a rupture of the sand barrier occurred), a higher degrees of hydrodynamics and even by bioturbation, quantity of mucus was expected. But in this site N. on the superficial layers in which N. diversicolor diversicolor increases a carnivore strategy, partially feeds on (Tamaki 1987, Meadows et al. 1990, abandoning filtering through the mucus net. This Turner et al. 1995, Mclachlan 1996). fact can be explained by i) the reduced quantity of Comparisons of chlorophyll a and particulate material in the water column, or ii) a phaeopigment levels (Figure 3 A and B) with the favorable new feeding option as the capture of percentages of sand or mucus ingested (Figure 4) did crustaceans and insect larvae. not allow the establishment of a comprehensive The fact that the mucus ingestion and the pattern. This is possibly due to the fact that the aggregated food items increases at the time that the distribution and abundance of several species of ingestion of sand decreases (Table II), may be due to microalgae are controlled by a number of inter- an ontogenetic change in feeding habits. Small dependent factors (Cadée & Hegeman 1974, individuals, with small burrows, acquire Pomeroy et al. 1981, Zedler 1982). In fact values of detritivorous habits feeding more frequently on the ODX, ALZ and CAR sediment chlorophyll a (as an surface of the sediment. Possibly this strategy is due indicator of microphytobenthos biomass) strongly to the inability of obtaining enough food through correlates to rainfall, indicating a dependence of this filtration due to the reduced dimensions of its mucus environmental variable (Fidalgo e Costa et al. 2002). net or to difficulties in bringing enough water inside As it was also concluded the variation of the ratio the gallery through dorsal-ventral pumping between chlorophyll a and phaeopigments movements. On the other hand, larger individuals emphasize that the chlorophyll a increase was due to with a better physical condition are capable of an in situ production of microalgae cells (Fidalgo e building deeper galleries and pumping higher Costa et al. 2002). Nevertheless these details quantity of water (Esselink & Zwarts, 1989). reinforce the above interpretation about sand Sand was observed frequently in the ingestion because it is supposed that a peak in digestive tract contents of Nereis, which swallows chlorophyll a (related to runoff) stimulate filtration large amounts of sediment in sweep-and-plough instead of sediment ingestion behaviors. food-searching strategy. This item may also have Nevertheless it was difficult to interpret our feeding been overvalued once it was extremely persistent in results based only on a phytopigments dataset, the digestive tract, due to the fact that it is not referred only to one sampling day per month. attacked by the digestive processes like the other Detritus has an important role as a food mentioned items. Like mucus it shows microalgae source both in the freshwater and marine benthic glued to its surface (mainly diatoms), but also meio communities. It is made up of all kinds of biogenic and microfauna existing in the interstitial space materials such as bacteria, protozoa, micro and (Lucas & Bertru, 1997, Tita et al. 2000). For all macroalgae, parts of vascular plants in various sampling sites, the differences found can be degrees of decomposition, which may contain narrowed down to seasonal differences that follow energy to be used by the species consumers (Tenore, the torrential character of the southern Portuguese 1977, Hansen & Kristensen, 1998). In the study rivers in which the studied areas are included area, N. diversicolor used detritus as a food source in (Magalhães et al. 1987, Fidalgo e Costa et al. 2002) all sampling stations, especially vegetable detritus and, consequently, a greater or lower sediment such as algae, roots, and parts of the macrophyte carriage from terrestrial or marine origins. These Ruppia sp. The sampling sites revealed variations in seasonal changes are strongly evident in ODX and the percent occurrence of ingested vegetable detritus ALZ, and in CAR they present only very low which increased with precipitation (Figures 2A and amplitudes (Fidalgo e Costa et al. 2002). Frequently 4), that may be related with the detritus amount that changes include also a seasonal contribution of inside a system, with a more torrential character particulate organic matter (OM) brought by (Magalhães et al. 1987). In ODX, it was observed continental runoff (Magalhães et al. 1987). So, when that the occurrence of mucus have decreased with the OM amount is higher one may expect that N. the augmented ingestion of vegetable detritus diversicolor adopt a predominantly filter-feeding (Figure 4) contrarily to ALZ where this ingestion behaviour, reducing the amount of sand ingested. On have no influence on mucus amounts. In CAR, the the other hand a reduced organic flow may increase rise in the consumption of vegetable detritus started

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 122 P. FIDALGO E COSTA ET AL. also with rainfall rise (Figure 4). For this site, and according to Jensen & André (1993) even the November 1993 was the single month where the juvenile N. diversicolor have a negative effect on the total emptying of the lagoon occurred, remaining juvenile Corophium volutator, above all in only a few puddles. During the following period extraordinarily lentic lagoons, which is the case of filter-feeding was difficult due to the small amount this lagoon. of water available and so N. diversicolor fed on In the future, it would be interesting to remains and roots of Ruppia sp. as an alternative. verify a trade-off between food preferences and The decomposition of these macrophytes occurred as predation risk in the laboratory. It would also be a result of their emergence and exposure to the sun. interesting to determine in the field how predation The increase in the vegetable remains consumed in affects the population structure of this species. the winter and at the beginning of spring seems to be caused by their transport to the system by the Acknowledgments frequent rains during these seasons (e.g. Figure 2A). This work was supported by a grant of the The digestive contents of N. diversicolor in Portuguese National Board of Scientific Research, the present study confirm the results of previous JNICT (BD/2265/92-IG) and by the JNICT contract studies (Mcintosh 1907, Bogucki 1953), which PBIC/C/MAR/1298/92. The authors are indebted to suggest cannibalistic behavior in this species. It all the colleagues from the Guia Marine Laboratory showed continuous reproduction in the three systems who assisted in fieldwork. We are also grateful to studied, with a recruitment peak in early autumn, Dr. J.-P. Cancela da Fonseca for the revision of the reaching annual averages of 1126 ind.m-2 in ODX, manuscript and to two anonymous referees for their 957 ind.m-2 in ALZ and 337 ind.m-2 in CAR valuable criticisms and suggestions and their (Fidalgo e Costa et al. 1998). For this reason the significant contributions for its improvement. The presence of larvae and juveniles in the gut contents authors would also like to thank Dr. Elza Neto and was frequent at almost all sites (Figure 4). The Dr.Michael Heasman for improving the English. larvae, juveniles and parts of individuals found in the gut contents suggest that cannibalism follows the References life cycle of this species and showed a slightly Bartels-Hardege, H.D. & Zeeck, E. 1990. increase after the referred early autumnal peak of Reproductive behaviour of Nereis diversicolor larva with the growth of juveniles and the beginning (Annelida: Polychaeta). Marine Biology, 106: of an active free benthic life (Fidalgo e Costa et al. 409-412. 1998). Bernardo, J.M. 1990. Dinâmica de uma Lagoa Feeding on the surface of the sediment has Costeira Eutrófica (Lagoa de Santo André). been observed in wild and under laboratory PhD. Thesis, Lisbon University, Lisbon. conditions (Fidalgo e Costa et al. 2000) and it varies 322p. according to quantity of food available. This practice Bogucki, M. 1953. Rozród i rozwój wieloszczeta is considered as a complement to filter-feeding due Nereis diversicolor (O.F. Müller) w Baltyku. to the predation risks it involves (Masson et al. The reproduction and development of Nereis 1995). This feeding strategy may also be facilitated diversicolor (O.F. Müller) in the Baltic sea. by the absence of predators of N. diversicolor such Polskie Archiwum Hydrobiologii, 14: 251- as Carcinus maenas. The lack of this active predator 270. of N. diversicolor (Cancela da Fonseca, 1989) in this Cadée, G.C. & Hegeman, J. 1974. Primary lagoon was mentioned by Magalhães (1988) and confirmed during the present study. Due to the production of the benthic microflora living on apparent lack of predators, N. diversicolor could the tidal flats in the Dutch Wadden Sea. promotes prolonged feeding journeys outside of the Netherland Journal of Sea Research, 8: burrows, which together with gallery digging, favors 260-291. the sediment turnover making it easier to find prey. Cancela da Fonseca, L. 1989. Estudo da influência Corophium sp. was one of the preys frequently da "abertura ao mar" sobre um sistema observed in the intertidal environment of all lagunar costeiro: A lagoa de Santo André. sampling stations. In ODX and ALZ with abundant PhD. Thesis. Lisbon University, Lisbon. presence of C. maenas, there was no significant 355p. predation on crustaceans. However in CAR there Cancela da Fonseca, L., Duarte, P. & Pombo Gaspar, was active predation of Corophium sp. during the F. 2001a. Trophic group patterns of study period, which can be confirmed by the pieces macrobenthos in brackish coastal systems. and whole individuals found in the digestive content Boletim do Museu Municipal do Funchal, (Figure 4). In lagoonal environments such as CAR, 6: 139-165.

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126 Feeding Ecology of Nereis diversicolor. 123

Cancela da Fonseca, L., Bernardo, J.M., Costa, shallow waters environments in south-western A.M., Falcão, M. & Vale, C. 2001b. Seasonal Portugal. Boletin Instituto Español de chemical changes and eutrophication of a Oceanografia, 19 (1-4): 17-29. land-locked coastal lagoon (St. André, SW Gaston, G.R. 1987. Benthic polychaeta of the Portugal). Boletim do Museu Municipal do Middle Atlantic Bight: feeding and Funchal, 6: 167-183. distribution. Marine Ecology Progress Caron, A., Olivier, M., Desrosiers, G., Hudier, E., Series, 36: 251-262. Côté, S., Koutitonsky, V.K., Miron, G. & Gillet, P. 1990. Variation intraspécifique de Retière, C. 1993. Distribution spatiale d’une paragnathes chez Nereis diversicolor espèce benthique épitoque en zone intertidal: (Annelides, Polychetes) de l'Atlantique Nord- rôle de l’hydrodynamisme? Vie Milieu, 43: Est. Vie Millieu, 40: 297-303. 83-93. Gillet, P. 1993. Impact de l’implantation d’un Cheggour, M., Texier, H., Moguedet, G. & Elkaïm, barrage sur la dynamique des populations de B. 1990. Metal exchanges in the fauna- Nereis diversicolor (Annelide Polychete) de sediment system. The case of Nereis l’etuaire Du Bou Regreg, Maroc. Journal de diversicolor and Scrobicularia plana in the Recherche Oceanographique, 18: 15-18. Bou Regreg estuary (Morocco). Goerke, H. 1971. Die Ernährungsweise der Nereis- Hydrobiologia, 207: 209-219. Arten (Polychaeta, Nereidae) der deutschen Day, J.W. Jr., Hall, C.A.S., Kemp, W.M. & Yáñez- Küsten. Meeresforsch, 13: 1-50. Arancibia, A. 1987. Estuarine geomorphology Golding, D.W. 1987. Brain-body interaction in and physical oceanography. p. 47-78. In: John Nereis: deactivation of serebral neuro- Wiley & Sons, Inc (Eds), Estuarine Ecology, endocrine system by ganglion transplantation. 558p. International Journal of Invertebrate Duck, R.W. 1986. Bottom sediments of Loch Reproduction and Development, 12: 281- Tummel, Scotland. Sedimentary Geology, 293. 47: 293-315. Golding, D.W. & Yuwono, E. 1994. Latent Esnault, G., Retière, C. & Lambert, R. 1990. Food capacities for gametogenic cycling in the resource partitioning in a population of Nereis semelparous invertebrate Nereis. diversicolor (Annelida, Polychaeta) under Proceedings of the National Academy of experimental conditions. Proceedings of the Sciences of the United States of America, 24th European Marine Biology Symposium, 91: 11777-11781. 453-467. Hansen, K. & Kristensen, E. 1998. The impact of the Esselink, P. & Zwarts, L. 1989. Seasonal trend in polychaete Nereis diversicolor and burrow depth and tidal variation in feeding enrichment with macroalgal (Chaetomorpha activity of Nereis diversicolor. Marine linum) detritus on benthic metabolism Ecology Progress Series, 56: 243-254. and nutrient dynamics in organic-poor Fidalgo e Costa, P., Sardá, R. & Cancela da Fonseca, and organic-rich sediment. Journal of L. 1998. Life cycle, growth and production of Experimental Marine Biology and Ecology, the polychaete Nereis diversicolor O.F. 231: 201-223. Müller in three lagoonal estuarine systems of Hughes, R.G., Lloyd, D. & Emson, D. 2000. the southwestern portuguese coast (Odeceixe, The effect of the polychaete Nereis Aljezur and Carrapateira). Écologie, 29: 523- diversicolor on the distribution and 533. transplanting success of Zostera noltii. Fidalgo e Costa, P., Narciso, L. & Cancela da Helgoland Marine Research, 54:129-136. Fonseca, L. 2000. Growth, survival and fatty Harley, M.B. 1950. Occurrence of a filter-feeding acid profile of Nereis diversicolor O.F. mechanism in the polychaete Nereis Müller, 1776 fed on six different diets. diversicolor. Nature, 165: 734-735. Bulletin of Marine Science, 67: 337-343. Jensen, K.T. & André, C. 1993. Field and laboratory Fidalgo e Costa, P., Brotas, V. & Cancela da experiments on interactions among an Fonseca, L. 2002. Physical characterization infaunal polychaete, Nereis diversicolor, and and microphytobenthos biomass on estuarine two amphipods, Corophium volutator and and lagoon environments of the southwest Corophium arenarium: effects on survival, coast of Portugal. Limnetica, 21: 69-79. recruitment and migration. Journal of Fidalgo e Costa, P. 2003. The oogenic cycle of Experimental Marine Biology and Ecology, Nereis diversicolor (Annelida: Polychaeta) in 168: 259-278.

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Last, K.S. & Olive, P.J.W. 1999. Photoperiodic of adults in shallow waters of western control of growth and segment proliferation Sweden. Journal of the Marine Biological by Nereis (Neanthes) virens in relation to state Association of the United Kingdom, 65: of maturity and season. Marine Biology, 134: 603-616. 191-199. Olivier, M., Desrosiers, G., Caron, A., Retière, C. & Lorenzen, C.J. 1967. Determination of Chlorophyll Caillou, A. 1996. Juvenile growth of Nereis and Pheo-pigments: spectrophotometric diversicolor (O.F. Müller) feeding on a range equations. Limnology and Oceanography, of marine vascular and macroalgal plant 12: 343-346. sources under experimental conditions. Lucas, F. & Bertru, G. 1997. Bacteriolysis in the gut Journal of Experimental Marine Biology of Nereis diversicolor (O.F. Müller) and effect and Ecology, 208:1-12. of the diet. Journal of Experimental Marine Plante–Cuny, M. R. 1974. Evaluation par Biology and Ecology, 215: 235-245. spectrophotométrie des teneurs en Magalhães, F., Cancela da Fonseca, L., Bernardo, Chlorophylle a fonnctionelle et en J.M., Costa, A.M., Moita, I., Franco, J.E. & phéopigments de substrats meubles marines. Duarte, P. 1987. Physical characterisation of Documents Scientifiques de la Mission the Odeceixe, Aljezur and Carrapateira O.R.S.T.O.M. Nosy-Bé, 45: 1-76. lagunary systems (SW Portugal). Limnetica, Pomeroy, L.R., Darley, W.R., Dunn, E.L., 3: 211-218. Gallagher, J.L, Haines, E.B. & Whitney, D.M. Magalhães, F. 1988. Sistema lagunar da 1981. Primary production. P. 39-67. In: Bordeira/Carrapateira: Caracterização Pomeroy, L.R. & Wiegert, R.G. (Eds.). The ambiental e estudo dos povoamentos ecology of salt marsh. 271 p. macrobentónicos. Degree Thesis, Lisbon Reise, K. 1979. Moderate predation on meiofauna University, Lisbon,122 p. by the macrobenthos of the Wadden Sea. Masson, S., Desrosiers, G. & Retière, C. 1995. Helgolaender Wissenschaftliche Périodicité d’alimentation du polychète Nereis Meeresuntersuchungen, 32: 453-465. diversicolor (O.F. Müller) selon les Riisgård, H.U. 1991. Suspension feeding in the changements de la marée. Écoscience, 2: 20- polychaete Nereis diversicolor. Marine 27. Ecology Progress Series, 70: 29-37. McIntosh, W.C. 1907. On the reproduction of Nereis Rönn, C., Bonsdorf, E. & Nelson, W. 1988. diversicolor. Annals and Magazine of Predation as a mechanism of interference Natural History, 20: 176-185. within infauna in shallow brackish water soft McLachlan, A. 1996. Physical factors in benthic bottoms; experiments with an infauna ecology: effects of changing sand particle size predator, Nereis diversicolor O.F.Müller. on beach fauna. Marine Ecology Progress Journal of Experimental Marine Biology Series, 131: 205-217. and Ecology, 116: 143-157. Meadows, P.S., Tait, J. & Hussain, S.A. 1990. Scaps, P. 2002. A review of the biology, ecology Effects of estuarine infauna on sediment and potential use of the common ragworm stability and particle sedimentation. Hediste diversicolor (O.F. Müller) (Annelida: Hydrobiologia, 190: 263-266. Polychaeta). Hydrobiology, 470: 203-218. Mettam, C. 1979. Seasonal changes in populations Silva e Costa, A., Palma, L. & Cancala da Fonseca, of Nereis diversicolor O.F. Müller from L. 1983. La côte sud-ouest du Portugal. Une Severn Estuary, U.K. Proceedings of the13th valeur écologique menacée. Le Courrier de European Marine Biology Symposium, la Nature, 87: 12-17. 123-130. Smith, D., Hughes, R.G. & Cox, E.J. 1996. Mettam, C. 1981. Survival strategies in estuarine Predation of epipelic diatoms by the Nereids. 65- 77 p. In: Jones and Wolff (Eds.). amphipod Corophium volutator and the Feeding and survival strategies of estuarine polychaete Nereis diversicolor. Marine organisms. 304 p. Ecology Progress Series, 145: 53-61. Miron, G. & Kristensen, E. 1993. Factors Tamaki, A. 1987. Comparison of resistivity to influencing the distribution of nereid transport by wave action in several polychaete polychaetes: the sulfide aspect. Marine species on an intertidal sand flat. Marine Ecology Progress Series, 93: 143-153. Ecology Progress Series, 37: 181-189. Möller, P. 1985. Production and abundance of Tenore, K.R. 1977. Utilisation of aged detritus juvenile Nereis diversicolor and oogenic cycle derived from different sources by the

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polychaete Capitella capitata. Marine Wells, G.P. & Dales, R.P. 1951. Spontaneous Biology, 44: 51-55. activity patterns in animal behaviour: the Tita, G., Desrosier, G., Vincx, M. & Nozais, C. irrigation of the burrow in the polychaetes 2000. Predation and sediment disturbance Chaetopterus variopedatus Renier and Nereis effects of the intertidal polychaete Nereis diversicolor O.F. Müller. Journal of the virens (Sars) on associated meiofaunal Marine Biological Association of the United assemblages. Journal of Experimental Kingdom, 29: 661-679. Marine Biology and Ecology, 243: 261-282. Witte, F. & de Wild, P.A.W.J. 1979. On the Turner, S.J., Thrush, S.F., Pridmore, R.D., Hewiit, ecological relation between Nereis J.E., Cummings, V.J. & Maskery, M. 1995. diversicolor and juvenile Arenicola marina. Are soft-sediment communities stable? An example from a windy harbour. Marine Netherland Journal of Sea Research, 13: Ecology Progress Series, 120: 219-230. 394-405. Underwood, A.J. 1997. Experiments in Ecology: Zar, J.H. 1984. Biostatistical analysis (2nd edn.) Their Logical Design and Interpretation Prentice-Hall International, New Jersey, Using Analysis of Variance. Cambridge 718 p. University Press, Cambridge. 504p. Zedler, J.B. 1982. The ecology of southern Vedel, A. 1998. Phytoplankton depletion in the California coastal salt marshes: a benthic boundary layer caused by suspension- community profile. U.S. Fish and feeding Nereis diversicolor (Polychaeta): Wildlife Service, Biological Service Program, grazing impact and effect of temperature. Washington, D.C. FWS/OBS - 81/84, 110 p. Marine Ecology Progress Series, 163: 125- Zubillaga, G.F. & Salinas, J.I.S. 1997. Ciclo de vida 132. de Nereis diversicolor O.F. Müller (Annelida, Vedel, A. & Riisgård, H.U. 1993. Filter-feeding in Polychaeta) en dos estuarios de norte de the polychaete Nereis diversicolor: growth Espanã com diferente carga de contaminación. and bioenergetics. Marine Ecology Progress Publicaciones Especiales. Instituto Espanol Series, 100: 145-152. de Oceanografia, 23: 207-215.

Received September 2006 Accepted November 2006 Published online December 2006

Pan-American Journal of Aquatic Sciences (2006), 1 (2): 114-126

Genidens genidens (Cuvier) (Pisces, Ariidae), oral incubation of eggs

1 ALEXANDRE M. GARCIA , JOÃO P. VIEIRA & MARCELO D. M. BURNS 1 Fundação Universidade Federal de Rio Grande (FURG), Laboratório de Ictiologia, Departamento de Oceanografia, CP 474, Rio Grande, RS, Brasil. *E-mail: [email protected]

Sea catfishes represent a major resource in artisanal fisheries along the East Coast of South America, and several species, usually males, have been reported incubating eggs or young in areas of low salinity (Gomes & Araújo 2004). In fact, species of this family produce the largest eggs among teleosts (Wallace & Selman 1981). During the incubation period, males show an expansion of the hyoid region probably to increase the space available to carry eggs or young. Size of the oral cavity, therefore, can limit fecundity in this species (Chaves 1994; Gomes & Araújo 2004). The above specimen was photographed by AMG on November 15th, 2005, at São Gonçalo Channel, a natural channel connecting Mirim and Patos lagoons in the Rio Grande do Sul state, southern Brazil. The individual (ca. 202 mm) was caught by bottom trawling below the São Gonçalo’s dam. We observed only two eggs, with a diameter of approx. 15 mm each, inside the oral cavity. As previously observed by Chaves (1994), eggs and larvae could be expel out of the oral cavity due to the stress caused during the capture of the individual. He also mentioned that adults engaged in oral incubation usually show total length from 192 and 270 mm, and have eggs with maximum diameter ranging between 13.1 and 15.5 mm and weight ranging between 1.5 and 1.9 g each. Picture characteristics: Digital Machine model Fujifilm® FinePix S5100; Resolution of 4.2 megapixels (72 dpi); diaphragm aperture 5.7; time of exposition 1/480; Speed ISO-64.

References Chaves, P.T.C. 1994. A incubação de ovos e larvas em Genidens genidens (Valenciennes) (Siluriformes, Ariidae) da Baía de Guaratuba, Paraná, Brasil. Revista Brasileira de Zoologia, 11: 641-648. Wallace, R.A. & Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist, 21: 325-343. Gomes, I. D. & Araújo, G. F. 2004. Reproductive biology of two marine catfishes (Siluriformes, Ariidae) in the Sepetiba Bay, Brazil. Revista de Biologia Tropical, 52 (1): 143-156.

This picture may be used for academic or personal purposes but always accompanied by the author's information (copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire about reprints, fees, and licensing, please contact the author via e-mail. Pan-American Journal of Aquatic Sciences (2006), 1 (2): I

Eunectes murinus (Linnaeus) (Serpentes, Boidae), preying activity

LÍLIAN CRISTINA MACEDO-BERNARDE Laboratório de Ecologia Animal, Faculdade de Ciências Biomédicas de Cacoal - FACIMED, Av. Cuiabá No. 3.087, Jardim Clodoaldo, Cacoal – RO, Brasil. CEP 78.976-005. E-mail [email protected]

A B

Eunectes murinus (Linnaeus, 1758) (Figure 1 a,b) is a aquatic, nocturnal and euryphagic snake species, feeding on several vertebrates types (fishes, frogs, turtles, lizards, snakes, caimans, birds and mammals) (Strimple 1993, Martins & Oliveira 1998). On 03 May 2006 at 13:00 h it was observed a large adult specimen of E. murinus (over 4000 mm lenght) in the process of constriction killing a domestic pig (Sus scropha Linnaeus, 1758) in the edge of Mequéns river, municipality of Alto Alegre do Parecis (12º51’03 " S; 61º54’56 " W), Rondônia States, Brazil. Picture Characteristics: Digital Machine Canon PowerShot A610; Resolution of 5 megapixels (96 dpi); automatic; Speed ISO-50.

References Martins, M. & Oliveira, M. E. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History, 6:78-150. Strimple, P. 1993. Overview of the natural history of the green anaconda (Eunectes murinus). Herpetological Natural History, 1:25-35.

This picture may be used for academic or personal purposes but always accompanied by the author's information (copyright). To obtain permission for commercial use or for any other non-personal, non-academic use, or to inquire about reprints, fees, and licensing, please contact the author via e-mail. Pan-American Journal of Aquatic Sciences (2006), 1 (2): II

Software & Book Review Section

Poseidon Linux – uma distribuição Linux voltada para público acadêmico e científico

1 1,2 3 CHRISTIAN DOS S. FERREIRA , GONZALO VELASCO , BERNARDO DOS S. VAZ , 1 1,4 EDUARDO H. ALBERGONE , DENIS HELLEBRANDT

1 Fundação Universidade do Rio Grande (FURG), Rio Grande, RS, Brasil ([email protected]) 2 Universidade Estadual Paulista (UNESP), Rio Claro, SP, Brasil. 3 Universidade Federal de Pelotas (UFPEL), Pelotas, RS, Brasil. 4 School of Development Studies, University of East Anglia, Norwich, NR4 7TJ, UK.

Abstract. This paper introduces Poseidon Linux, a Linux distribution for academic and scientific use. Poseidon Linux is a remastering from Kurumin Linux, but differs from Kurumin by the addition a large number of programs applied to GIS/Maps, numerical modelling, 2D/3D/4D visualization, statistics, as well as tools for creating simple and complex graphics and programming languages. Also, it includes tools for daily use on a workstation, such as a complete office suite, internet browsers, e-mail client, instant messaging, chat, and many other tools. Poseidon Linux can run on two modes, as a live-CD or installed on the hard disk. It has support only for Brazilian Portuguese, but support for English and Spanish languages is planned.

Resumo. Este artigo introduz o Poseidon Linux, uma distribuição Linux voltada para o uso acadêmico e científico. Poseidon Linux é um remasterização do Kurumin Linux, mas difere do Kurumin por apresentar um grande número de ferramentas nas áreas de Sistemas de Informação Georeferenciadas (SIG), modelagem numérica, visualização 2D/3D/4D, estatística, ferramentas para criação de gráficos simples e/ou complexos, e linguagens de programação. Também inclui ferramentas para o uso geral em uma estação de trabalho, como um pacote de escritório completo, navegadores para internet, leitor de e- mail, mensagens instantâneas, chat, e várias outras ferramentas. O Poseidon Linux pode rodar de duas maneiras, como um “live-CD” ou instalado no disco rígido. Ele tem suporte somente para Português do Brasil, mas há planos de versões em Inglês e Espanhol.

Introdução Histórico Ao longo deste artigo iremos apresentar brevemente Desde o surgimento do sistema operacional a história do UNIX/Linux e como ela envolveu as (SO) UNIX nos anos 70, seguido por sua universidades. A partir disso, falaremos sobre o que popularização nas universidades em meados dos '70, motivou a criação do Poseidon Linux, com uma o ambiente acadêmico foi palco da criação de novas descrição das ferramentas que nele estão incluídas. ferramentas e tendências baseadas no código fonte Por último serão abordados planos para o futuro do do UNIX. Por sua portabilidade e robustez o UNIX Poseidon Linux. logo ganhou terreno em diversos centros de IV C. DOS S. FERREIRA ET AL. pesquisa, e propiciou também o surgimento da nada em seus computadores. Internet (Wirzenius 2003). Porém com o aumento da Posteriormente, o Knoppix foi usado como popularidade do UNIX nos anos 80 e devido aos base para o surgimento de diversas derivações. Entre grandes interesses econômicos, o sistema começou a elas, podemos destacar no Brasil o Kurumin Linux, se distanciar da filosofia de colaboração aberta, que incorpora diversas personalizações que buscam comum na comunidade acadêmica e científica. facilitar ainda mais a utilização do GNU/Linux por Com o objetivo de trazer novamente a usuários domésticos. abertura, Richard Stallman criou a Free Software Foundation em 1984. Stallman era um ex-aluno do Poseidon Linux Massachusetts Institute of Technology (MIT) que Usando como base o Kurumin, descontente com a filosofia do software proprietário pesquisadores da Fundação Universidade Federal do iniciou o projeto GNU (que significa “Gnu is Not Rio Grande (FURG) criaram o Poseidon Linux Unix”) (Free Software Foundation 2005). O (http://poseidon.furg.br). A finalidade desta principal objetivo do projeto era criar um UNIX distribuição é trazer para a comunidade acadêmica e aberto e gratuito. Nos anos 90, o SO GNU já estava científica diversas ferramentas fundamentais com praticamente tudo pronto, mas ainda faltava baseadas em software livre, visto que estas são uma peça fundamental, o kernel (núcleo) do sistema, gratuitas, apresentam boa estabilidade, responsável por fazer a comunicação entre o documentação, e –principalmente- tem o código hardware e o software. aberto, permitindo adaptação e personalização por Em 1993, Linus Torvalds, um estudante da parte dos usuários, se desejado (Maliszewskyj & universidade de Helsinki, Finlândia, deu o passo que Dickerson 1998, Laird 2002). faltava ao criar um kernel que, somado aos softwares A justificativa para tal deve-se a realidade do projeto de Stallman, rapidamente ganharam o atual nestes ambientes de trabalho: a presença de mundo através da Internet, dando origem ao SO sistemas e programas caros, que muitas vezes GNU/Linux (Wirzenius 2003). exigem renovação periódica das licenças, que em Com o surgimento do GNU/Linux aparece muitos casos são instáveis, ou -no pior dos casos- o um novo conceito, o das distribuições ou - nada desejado uso de cópias não autorizadas de coloquialmente- “distros” (Linux International software sem licença (pirataria). Tal cenário é 2001). Este termo vem do fato que cada grupo de incompatível com o desenvolvimento de atividades usuários ou empresas pode personalizar segundo sua de pesquisa e educação, motivo pelo qual a opção necessidade particular ou do mercado uma versão do pelo software livre torna-se tão oportuna e GNU/Linux e assim distribuí-la. Hoje em dia necessária. existem diversas distribuições de Linux, entre as Ainda, com a criação de uma plataforma mais famosas podemos destacar Debian, RedHat, como o Poseidon Linux, o conceito de colaboração e SuSE, Mandrake e Slackware. Dentre as integração em ciência pode ser trazido também para distribuições, a Debian é uma das mais importantes. o software, fazendo possível que haja uma interação É uma das maiores no mundo e conta com milhares entre diversos grupos para fomentar melhorias ou a de desenvolvedores que trabalham de forma criação de novas ferramentas o que pode se reverter voluntária (Lamerte 2002). Como resultado deste também em aprimoramentos das pesquisas modo de trabalho uma vasta gama de softwares é (Wonnacott & Dougherty 1999). mantida pela equipe. O Debian é considerado uma As ferramentas científicas incluídas no das melhores distribuições porque prima por Poseidon Linux (atualmente na versão 2.0) buscam segurança e estabilidade. Porém versões mais atuais abranger diversas áreas, tais como: Sistemas de dos programas não são incluídas até que estejam Informações Geográficas (SIG), banco de dados, totalmente testadas quanto à estabilidade, tornando-o linguagens de programação, Estatística/Matemática, um pouco menos amigável para usuários iniciantes. modelagem numérica, visualização 2D/3D/4D, Para contornar isso, Klaus Knopper criou o editoração de documentos LATEX e criação de Knoppix, uma distribuição que é executada de forma gráficos científicos. Os programas específicos direta a partir de um CD (live-CD), sem necessidade incluídos (diferenciais) são apresentados com mais de instalar o sistema no disco rígido do computador, detalhes na Tabela I. e que usa o Debian como base, incluindo também Na figura 1 mostra-se o resultado de um diversos scripts que permitem a detecção e auto- trabalho realizado totalmente no Poseidon Linux, configuração do hardware. Isso a tornou famosa já analisando milhares de dados pontuais de que permitiu que diversos usuários pudessem profundidade do oceano na costa brasileira e conhecer o GNU/Linux sem ter que instalar e alterar Poseidon Linux V

Tabela I. Lista de software específicos do Poseidon Linux (versão 2.0).

Área Softwares URL Sistema de Informações GRASS 6.0.0 http://grass.itc.it/ Geográficas e SPRING 4.1 http://www.dpi.inpe.br/spring/ Geoprocessamento Terraview 3.0+ http://www.dpi.inpe.br/terraview/ QGIS 0.6 http://qgis.sourceforge.net/ GMT 3.4.4 http://gmt.soest.hawaii.edu/ PROJ 4.4 http://proj.maptools.org/ Estatístico/Matemático R 2.0.1 http://www.r-project.org/ Scigraphica 0.8 http://scigraphica.sourceforge.net/ Modelagem numérica Octave 2.1 http://www.octave.org/ Visualização 2D/3D/4D OpenDX 4.3 http://www.opendx.org/ Vis5D 5.2 http://www.ssec.wisc.edu/~billh/vis5d.html Editor TEX Lyx 1.3.5 http://www.lyx.org/ Kile 1.7 http://kile.sourceforge.net/ Linguagens de programação C e C++ 3.3.5 http://gcc.gnu.org/ G77 3.3.5 http://www.gnu.org/software/fortran/fortran.htm Python 2.3 l http://www.python.org/ Banco de dados PostgreSQL 7.4 http://www.postgresql.org/ MySQL 4.1 http://www.mysql.com/ PostGIS 1.0.1 http://postgis.refractions.net/ Gráficos e mapas Gri 2.19 http://gri.sourceforge.net/ Editor Postscript XFig 3.2.5 http://www.xfig.org/ Editor de diagramas Dia 0.94 http://www.gnome.org/projects/dia/ CAD 2D QCAD 2.0.4 http://www.ribbonsoft.com/qcad.html integrando esses dados em uma figura tridimensional Por utilizar a tecnologia live-CD torna-se (extraído de Ferreira et al. 2005). acessível aos pesquisadores a introdução ou Além das ferramentas acadêmicas/científicas utilização plena de todas as ferramentas inclusas no estão incluídos vários programas necessários para o Poseidon Linux e o SO GNU/Linux sem a dia-a-dia, como um pacote de escritório completo necessidade de instalação. Se desejado, existe (OpenOffice.org), navegadores de internet também a opção de instalação do Poseidon Linux em (MozillaFirefox e Konqueror), leitores de correio disco rígido como sistema operacional de um eletrônico (Thunderbird), programas para mensagens computador pessoal ou portátil, inclusive para o uso instantâneas (Kopete), editores de imagens (GIMP e simultâneo de mais de um sistema no mesmo PC. Kolourpaint), e visualizadores de imagem PS e PDF, Isto é, o Poseidon Linux pode estar instalado em tudo isso num ambiente amigável e visualmente uma máquina que já possua outro(s) sistema(s) e o moderno (Fig. 2). usuário escolhe ao ligar o computador qual sistema vai usar, graças a um administrador de inicialização (LILO). O Poseidon Linux já foi apresentado em diversas palestras em universidades públicas e outras instituições do Brasil e em diversos eventos específicos, destacando-se o VI Fórum Internacional de Software Livre, realizado em Porto Alegre (RS) em 2005, onde contou com um stand de exposição especial. Já há usuários do Poseidon nas seguintes universidades brasileiras: FURG, UFPEL, UNIVALI e Instituto Oceanográfico da USP. Algumas

instituições do governo como SIVAM, EMBRAPA, Figura 1 – Mapa do relevo do fundo da plataforma continental DAER e IBAMA, já usam o Poseidon Linux ou brasileira e oceano adjacente realizada utilizando as ferramentas do Poseidon Linux e dados de pesquisa oceanográfica. estão avaliando sua utilidade. Pesquisadores de outros países da América Latina também estão VI C. DOS S. FERREIRA ET AL.

Figura 2 – Imagem da visualização do Poseidon Linux 2.0 rodando em um computador. Em detalhe o menu expandido mostrando algumas dos programas instalados. alternativa de plataforma de trabalho atraente para avaliando e/ou usando o Poseidon. Existe no site da pesquisadores, professores e alunos das internet do projeto um guia de instalação em universidades públicas e privadas, já que inclui uma espanhol, além do guia em português, o qual foi enorme gama de ferramentas estáveis e gratuitas que muito acessado desde sua publicação (Novembro de podem auxiliar-los no desenvolvimento da pesquisa 2005). e na popularização do software livre no meio acadêmico e científico. Representa um pacote Planos Futuros completo (sistema operacional base e a maioria dos A equipe Poseidon Linux já está trabalhando aplicativos utilizados no dia-a-dia, tanto em um para desenvolver versões em Espanhol e Inglês do computador pessoal como uma estação de trabalho mesmo, para atender um número maior de em uma universidade ou instituto de pesquisa). A pesquisadores fora do Brasil. Ainda, pretende-se Equipe Poseidon Linux atualiza o pacote criar uma versão específica para computação de alto periodicamente para incluir as novas versões dos desempenho (montagem de clusters). programas, quando disponíveis, e também para - eventualmente- incluir novas ferramentas científicas Conclusões que os usuários e colaboradores sugerem num fórum Esta é uma distribuição Linux totalmente aberto aos mesmos. composta por Software Livre (SL), baseado no Kurumin Linux, e inspirada pelo Quantian Linux. O Referências bibliográficas Poseidon é e sempre será livre e gratuito. Outro Ferreira, C., Albergone, E., H., Velasco, G., Vaz, B., detalhe importante é que todos os programas podem Hellebrandt, D., 2006, Poseidon Linux, uma rodar a partir do CD (“bootável”), já que o Poseidon distribuição Linux voltada para público possui tecnologias que permitem isso, sendo acadêmico e científico. Resumos do 7o possível utilizar todos os programas sem instalar Fórum Internacional do Software Livre absolutamente nada. Existe também a opção de (FISL7). Porto Alegre. instalar no computador se o pesquisador ou Free Software Foundation. 2005. The GNU estudante assim desejar. Este não é, por tanto, um Operating System. http://www.gnu.org/. produto comercial e/ou que inclui programas Acessado em abril de 2005 “piratas”. Laird, C. 2002. Open source in the lab (Python, Considera-se que o Poseidon Linux é uma Poseidon Linux VII

Perl, and open source toolkits bring Journal: Linux in a Scientific Laboratory, multiple benefits to science). IBM. http://noframes.linuxjournal.com/article/2596. http://www- Acessado em Agosto de 2005 128.ibm.com/developerworks/linux/library/l- Wirzenius, L. 2003. Linux: the big picture, oslab/. Acessado em Outubro de 2005 http://liw.iki.fi/liw/texts/linux-the-bigpicture. Lamerte, D. 2002. Debian GNU/Linux: The Past, Wonnacott, D. & Dougherty, J. 1999. Linux in the the Present and the Future, Lab http://telemetrybox.org/tokyo/. Acessado em http://www.haverford.edu/publications/summe Outubro de 2005 r99/linuxlab.htm Linux International. 2001. What is Linux. http://www.li.org/whatislinux.php Maliszewskyj, P. & Dickerson, B. 1998. Linux