Population biology of spine shrimp Exhippolysmata oplophoroides (Holthuis) (Caridea, Hippolytidae) in a subtropical region, São Paulo, Brazil

Vivian Fransozo 1, Rogério C. Costa 2, Giovana Bertini 3 & Valter J. Cobo 4

1 Corresponding author. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista. Caixa Postal 510, 18618-000 Botucatu, São Paulo, Brasil. E-mail: [email protected] 2 Faculdade de Ciências, Universidade Estadual Paulista. 17033-360, Bauru, São Paulo, Brasil. E-mail: [email protected] 3 Universidade Estadual Paulista, Unidade de Registro. 11900-000 Registro, São Paulo, Brasil. E-mail: [email protected] 4 Departamento de Biologia, Universidade de Taubaté. 12020-270 Taubaté, São Paulo, Brasil. E-mail: [email protected]

ABSTRACT. The population biology of Exhippolysmata oplophoroides (Holthuis, 1948) was studied in Ubatuba Bay (23º26’S, 45º02’W), Ubatuba, São Paulo, Brazil, from September/1995 to August/1996. Each sampling comprised eight transects (14 000 m2 each), sampled monthly with three repetitions. The specimens were classified with respect to the presence or absence of eggs in the abdominal appendages. Spine-shrimps occurred only on six transects, being most abundant on transect II, with the highest incidence in late spring and throughout the summer months. Ovigerous and non-ovigerous shrimps were present year-round, in an approximately similar proportion (1:1). Site II in Ubatuba Bay is characterized by high salinity and oxygen values, temperature between 26 and 29ºC, low organic matter content in the sediment, and a bottom composed of very fine sand; these environment and biological features allow the establishment and maintenance of the population of E. oplophoroides. KEY WORDS. Distribution, population structure, reproduction, Southeastern Brazil, spine shrimp.

RESUMO. Biologia populacional do camarão espinho Exhippolysmata oplophoroides (Holthuis) (Carideaidea, Hippolytidae) numa região subtropicalopical, São PauloPaulo, Brasil. A biologia populacional de Exhippolysmata oplophoroides (Holthuis, 1948) foi estudada na enseada de Ubatuba (23º26’S, 45º02’W), Ubatuba, São Paulo, Brasil, de setembro de 1995 até agosto de 1996. Cada amostragem compreendeu oito transectos (14000 m2 cada), amostrados mensalmente com três repetições. Os espécimes foram classificados quanto à presença ou ausência de ovos nos apêndices abdominais. Os camarões espinhos ocorreram somente em seis transectos, sendo mais abundantes no transecto II, com a maior incidência no final da primavera e ao longo dos meses de verão. Indivíduos ovígeros e não ovígeros estiveram presentes o ano todo, numa proporção semelhante a 1:1. O transecto II é caracterizado por altos valores de salinidade e oxigênio, temperatura entre 26 e 29º C, baixo teor de matéria orgânica e sedimento composto por areia muito fina. Tais características biológicas e ambientais permitem o estabelecimen- to e a manutenção da população de E. oplophoroides na região de estudo. PALAVRAS CHAVE. Camarão espinho, distribuição, estrutura da população, sudeste do Brasil, reprodução.

Among many caridean shrimp occurring along the coast Farfantepenaeus paulensis (Pérez-Farfante, 1967), F. brasiliensis of São Paulo, the spine-shrimp Exhippolysmata oplophoroides (Latreille, 1817), Litopenaeus schmitti (Burkenroad, 1936) and (Holthuis, 1948) is the most abundant. It is a very common Xiphopenaeus kroyeri (Heller, 1862), and is consumed by the caridean in shallow marine waters along the southeastern coast local people. Despite its common occurrence in these fisheries, of Brazil. Its common name in North America is “redleg hump- the biology of the spine-shrimp is poorly known. CHACUR & back shrimp,” whereas in Brazil it is known as the “camarão- NEGREIROS-FRANSOZO (1999) reported that it reproduces continu- espinho”or “spine-shrimp;” we use the latter name herein. As ously in the Ubatuba region. In that population, CHACUR & noted by COSTA et al. (2000), the spine-shrimp is usually found NEGREIROS-FRANSOZO (1999) found no specimen with mature male together with the commercially exploited penaeid shrimps morphological features, which suggests that sexual reversion

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 Population biology of spine shrimp Exhippolysmata oplophoroides in a subtropical region... 1079 occurs in this species; sexual reversion is very common in ma- rine caridean shrimps (KAGWADE 1981, BAUER 1986, FIEDLER 1998, BAUER & HOLT 1998). NEGREIROS-FRANSOZO et al. (2002) described the first larval stage of the spine-shrimp from ovigerous fe- males, also obtained in the Ubatuba region. In biological studies on benthic organisms, the environ- mental factors usually monitored are temperature, salinity, dis- solved oxygen, texture of the sediment and organic matter. Taken together, these features can characterize peculiar envi- ronmental situations which can provide favorable conditions for the development of certain species (BUCHANAN & STONER 1988, GONZÁLEZ-GURRIARÁN et al. 1993, BERTINI & FRANSOZO 1999, COSTA & FRANSOZO 2004a, COSTA et al. 2004, 2005a, b). The aim of this study is to analyze the population biol- ogy of E. oplophoroides in Ubatuba Bay, Ubatuba, São Paulo, 23°S Brazil, with emphasis on spatial and seasonal aspects. The en- vironmental factors influencing its ecological distribution were also examined.

MATERIAL AND METHODS

Ubatuba Bay (27º26’S, 45º02’W) (Fig. 1) is located adja- 45°W cent to the Municipality of Ubatuba on the northern coast of 0 1 2 km São Paulo. The area includes five sandy beaches delimited by Figure 1. Map of ubatuba bay indicating the locations of the rocky shores. The total area of the bay is about 8 km2; its width is sampling transects. about 4.5 km at the entrance and decreases landward. Four small rivers (Indaiá, Grande, Lagoa and Acaraú) flow into this bay. Fresh water also enters from the Atlantic forest and the surrounding The specimens are deposited in the collection of the mangroves, reducing the salinity in the shallow water in the bay. Group of Studies on Biology, Ecology and Culture MANTELATTO & FRANSOZO (1999) provided a detailed characteriza- (NEBECC), Department of Zoology, Institute of Biosciences, tion of the physical and chemical parameters in Ubatuba Bay, UNESP, Botucatu, São Paulo, Brazil. during the same period as this study (Tabs I and II). The correlations between the mean numbers of spine- Shrimps were sampled monthly from September, 1995 to shrimps and environmental variables were analyzed employ- August, 1996 in Ubatuba Bay, from a fishing boat equipped with ing Pearson’s correlation coefficient (VIEIRA 1989). The median two double-rig nets (mouth 3.5 m wide, mesh size 15 mm in the sizes of the spine-shrimps were compared by the Kruskal-Wallis body and 10 mm in the cod end). Each sample series comprised analysis, complemented by Dunn’s method (SOKAL & ROHLF 1995) 8 transects (14,000 m2 each), each transect sampled repeatedly when differences were detected. The significance level adopted on three consecutive days. The specimens obtained were sorted for all tests was p < 0.05. and stored in 70% ethanol. It was not possible to sex the speci- mens by macroscopic procedures, because ovigerous shrimps RESULTS have the same external morphological features as non-oviger- ous ones. Therefore the specimens were classified based on the The total number of specimens of E. oplophoroides ob- presence or absence of eggs in the abdominal appendages. tained in this study was 9790. The number of specimens mea- All the specimens captured in each transect were counted. sured in the subsamples was 2410. Of the specimens in the When a large number of individuals were caught on a particu- subsamples, 1203 were non-ovigerous and 1207 were oviger- lar transect, subsamples of spine-shrimps were taken following ous. WENNER et al. (1991): if = 50 < n < 250 individuals were col- Size-frequency distributions were constructed separately lected, then a minimum of 50 randomly selected specimens for ovigerous shrimps and non-ovigerous shrimps, using 1.5 were measured; if > 250 < n < 500 individuals were caught, mm CL size intervals. The specimens were distributed in ten then a minimum of 20% were measured; and when n > 500 size classes, ranging from 4.0 to 19.0 mm. The smallest oviger- were caught, a minimum of 10% were measured. ous shrimp was found in the second size class (6.3 mm CL), The carapace length (CL), defined as the distance from and the largest in the 10th (17.6 mm CL). the orbital angle to the posterior margin of the carapace, was Individuals of E. oplophoroides occurred on six of the eight measured to the nearest 0.1 mm for all the individuals sorted. transects (I, II, III, IV, VI and VII). Almost all of them were

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 1080 V. Fransozo et al.

Table I. Mean values and standard deviations of the environmental factors on each transect, in Ubatuba Bay from September 1995 to August 1996 (data from MANTELATTO & FRANSOZo 1999). Transects Salinity Dissolved Oxygen (g/ml) Depth (m) Temperature (ºC) Organic Matter content (%) I 33.7 ± 1.5 4.9 ± 0.4 16.6 ± 0,9 22.5 ± 2.9 5.5 ± 5.1 II 33.3 ± 1.7 5.2 ± 0.8 11.4 ± 0.6 23.4 ± 2.7 5.3 ± 3.0 III 33.4 ± 1.7 4.6 ± 0.8 10.7 ± 0.7 23.4 ± 2.8 13.2 ± 1.5 IV 33.2 ± 1.8 5.2 ± 0.4 9.5 ± 1.0 23.7 ± 2.8 18.5 ± 9.6 V 33.1 ± 2.0 5.5 ± 0.5 7.9 ± 1.1 23.9 ± 2.6 20.3 ± 6.6 VI 33.1 ± 1.8 5.2 ± 0.6 7.6 ± 0.5 24.0 ± 2.6 14.5 ± 2.2 VII 32.9 ± 1.9 4.8 ± 0.8 7.3 ± 0.4 24.1 ± 2.8 6.1 ± 2.4 VIII 32.4 ± 2.0 5.4 ± 0.6 3.1 ± 0.3 24.9 ± 2.9 6.9 ± 1.5

Table II. Mean values and standard deviations of the environmental factors recorded monthly in Ubatuba Bay from September 1995 to August 1996 (data from MANTELATTO & FRANSOZO 1999). Months Salinity (%) Dissolved Oxygen (g/ml) Temperature (ºC) Organic matter content (%) September 31.6 ± 0.6 5.4 ± 0.7 22.4 ± 0.5 13.7 ± 8.6 October 32.7 ± 0.4 5.0 ± 0.6 22.4 ± 0.4 17.0 ± 8.4 November 29.6 ± 0.9 5.1 ± 0.9 23.5 ± 0.8 12.9 ± 10.1 December 31.5 ± 0.5 5.5 ± 0.5 22.2 ± 2.8 10.6 ± 7.6 January 35.3 ± 0.4 4.7 ± 0.7 26.6 ± 0.5 11.3 ± 8.2 February 31.8 ± 0.9 4.7 ± 0.6 27.9 ± 0.9 11.9 ± 8.3 March 34.5 ± 0.4 5.9 ± 0.7 27.4 ± 1.1 8.9 ± 6.5 April 35.2 ± 0.3 4.7 ± 0.5 26.0 ± 0.3 11.0 ± 8.4 May 32.7 ± 1.0 5.3 ± 0.5 23.5 ± 0.9 10.0 ± 6.8 June 34.4 ± 0.2 4.3 ± 0.5 23.1 ± 0.2 9.3 ± 3.3 July 34.6 ± 0.6 5.0 ± 0.4 20.2 ± 0.3 10.8 ± 5.3 August 34.2 ± 0.5 5.5 ± 0.2 19.6 ± 0.3 10.1 ± 6.7

8 The size (CL) frequency distribution of the shrimps on Ovigerous 7 each transect is presented in figure 3. On each transect, the Non ovigerous proportions of ovigerous and non-ovigerous shrimps were simi- s [Ln(x+1)] 6 lar. There was a statistically significant difference (Kruskal- 5 Wallis, p < 0.05) in the median size of shrimps from different 4 sites (Tab. III). The size (CL) frequency distributions of the shrimps in 3 each month are shown in figure 4. The proportion between 2 ovigerous and non-ovigerous shrimps was very similar through- 1 out the year. The population was unimodal. Juveniles were considered as those individuals, which were smaller than the 0

Mean number of spine-shrimp smallest ovigerous females. They were most abundant in De- I II III IV VI VII cember 1995 and in February, April and May 1996. Transect Among the environmental factors analyzed, only the Figure 2. Abundance of ovigerous and non-ovigerous spine-shrimps water temperature (Pearson’s coefficient = 0.26) and the or- E. oplophoroides at the collecting sites in Ubatuba Bay. ganic matter content of the sediment (Pearson’s coefficient = - 0.27) showed a significant correlation with the mean number caught on transect II (Fig. 2). Most of the shrimps were caught of spine-shrimps throughout the study period (Fig. 5). How- in late spring and throughout the summer, from November ever, less than 30 % of the occurrence of the spine-shrimps can 1995 to March 1996. be explained by means of these factors.

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 Population biology of spine shrimp Exhippolysmata oplophoroides in a subtropical region... 1081

70 70 70 Transect II Transect III 50 Transect I 50 50 N = 176 (166) N = 8984 (1716) N = 214 (212) 30 30 30 10 10 10 10 10 10

30 30 30 Size classes Range (mm) 50 50 50 1 4.0 -] 5.5 2 5.5 -] 7.0 70 70 70 3 7.0 -] 8.5 12345678910 12345678910 12345678910 4 8.5 -] 10.0 5 10.0 -] 11.5 70 70 6 11.5 -] 13.0 70 Transect VI Transect VII 7 13.0 -] 14.5 Transect IV 50 50 50 N = 352 (352) N = 54 (54) 8 14.5 -] 16.0 N = 10 (10) 30 30 9 16.0 -] 17.5 30 10 17.5 -] 19.0 10 10 10 10 10 10 30 30 30 Non-ovigerous 50 50 50 Ovigerous 70 70 70 12345678910 12345678910 12345678910 Figure 3. Size-frequency distribution of ovigerous and non-ovigerous spine-shrimps E. oplophoroides, at the collecting sites (transects) in Ubatuba Bay, from September 1995 to August 1996. (N) Total number, (n) subsample.

Table III. Exhippolysmata oplophoroides. Comparison of the median mass strongly influences the near-bottom sea temperature, es- size of the spine-shrimps collected. pecially on the inner shelf during the spring or summer. Season/Sites N Median Size (mm) Statistical comparison* The intrusion of SACW was detected in this study during Winter 258 11.6 a** late spring at the 17-m isobath, i.e., on transect I. Our results Autumn 470 10.5 b indicate that fluctuations in the seasonal distribution of E. Spring 833 10.4 c oplophoroides were influenced by the variation in temperature Summer 849 9.7 c levels caused by these currents. When SACW reaches the bay, II 1716 10.5 a it causes a decrease in temperature and confinement of the shrimp population in shallower areas ( < 20 m). Similar results I 166 10.3 ab were also reported for the shrimp X. kroyeri by NAKAGAKI & VI 352 10.0 bc NEGREIROS-FRANSOZO (1998) and CASTRO et al. (2005), VII 54 9.2 c constrictus (Stimpson, 1874) by COSTA & FRANSOZO (2004b), the III 212 9.1 c “Argentinean” shrimp Pleoticus muelleri Bate, 1888 by COSTA et IV 10 8.0 c al. (2004) and the rock-shrimp Sicyonia dorsalis Kingsley, 1878 ␣ * Kruskal-Wallis analysis complemented by Dunn's method; = by COSTA et al. (2005b), all in Ubatuba Bay. 0.05; ** Seasons or sites sharing at least one letter in the column The highest abundance of E. oplophoroides occurred on did not differ statistically. transects II and VI. Abundance is not determined only by a specific group of abiotic factors, but also depends on a group DISCUSSION of biotic factors. These transects contained large deposits of plant debris derived from the neighboring terrestrial vegeta- According to CASTRO-FILHO et al. (1987), the region is tion (MANTELATTO & FRANSOZO 1999). According to CASTRO et al. strongly influenced by three water masses: South Atlantic Cen- (2005), these features are essential for the establishment of ju- tral Water (SACW) with low temperature and salinity (T < 20ºC, venile shrimps of X. kroyeri. The organic material can provide a S < 36), Tropical Water (TW) with high temperature and salin- sheltered environment that allows the establishment and main- ity (T > 20ºC, S > 36), and Coastal Water (CW) with high tem- tenance of the spine-shrimp population, especially for the perature and low salinity (T > 20ºC, S < 36). These water masses ovigerous females. interact to modify the temperature, salinity and nourishment With reference to the size range of the shrimps, the single conditions during the seasons, especially during winter and possible comparison is with the data of CHACUR & NEGREIROS- late spring or summer. According to PIRES (1992), CW and SACW FRANSOZO (1999), who found a size range from 6.2 to 16.6 mm interact, forming a mixing zone that varies in time and space CL for the total population, with ovigerous shrimps varying according to the penetration intensity of the SACW. The SACW from 7.2 to 15.7 mm CL. In the present study, the specimens

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 1082 V. Fransozo et al.

40 40 40 September November 30 October 30 N = 71 (57) 30 N = 638 (232) 20 N = 192 (174) 20 20 10 10 10 0 0 0 10 10 10 20 20 20 30 30 30 40 40 40 12345678910 12345678910 12345678910

40 40 40 December January February 30 30 30 N = 2298 (427) N = 3356 (375) N = 425 (251) 20 20 20 10 10 10 0 0 0 10 10 10 20 20 20 30 30 30 40 40 40 12345678910 12345678910 12345678910

40 40 40 May March April 30 30 30 N = 431 (165) N = 1179 (223) N = 104 (104) 20 20 20 10 10 10 0 0 0 10 10 10 20 20 20 30 30 30 40 40 40 12345678910 12345678910 12345678910

40 40 40 June July August 30 30 30 N = 754 (201) N = 71 (71) N = 271 (130) 20 20 20 10 10 10 0 0 0 10 10 10 20 20 20 30 30 30 40 40 40 12345678910 12345678910 12345678910 Non-ovigerous Ovigerous Figure 4. Size-frequency distribution of ovigerous and non-ovigerous spine-shrimps E. oplophoroides, in the months of collection in Ubatuba Bay. (N) Total number, (n) subsample.

measured from 4.1 to 17.6 mm CL for the total population, ter. Similar results were found by COSTA & FRANSOZO (2004b) for and ovigerous shrimps varied from 6.3 to 17.6 mm CL. There- the peneid R. constrictus in the same region, and by GALVÃO & fore, we found a slightly wider size variation than in the previ- BUENO (1999) and MOSSOLIN & BUENO (2002) for the carideans ous study, perhaps because of a more appropriate sampling Atya scabra (Leach, 1815) and Macrobrachium olfersi (Wiegmann, design. 1836), respectively, from the Municipality of São Sebastião, According to SASTRY (1983), there is much inter- and in- which is located near Ubatuba Bay at the same latitude. The traspecific variation in spawning patterns, depending on the most frequent breeding period was late spring and summer. geographic area. Usually, populations in temperate waters Other decapod species from the same region, such as spawn over a short period of time compared to those in sub- Paguristes tortugae Schmitt, 1933, studied by NEGREIROS-FRANSOZO tropical and tropical areas. In the tropics, the great majority of & FRANSOZO (1992), show continuous reproduction throughout the species breed for a long period of time, but peaks may oc- the year. FRANSOZO & MANTELATTO (1998) observed that another cur within this period. The spine-shrimp showed continuous decapod species, Calcinus tibicen (Herbst, 1791), shows a strong reproduction in the Ubatuba region: ovigerous females were reproductive peak between September and May, with oviger- found year-round, in spite of being more frequent during win- ous females absent during the winter months. The reproduc-

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 Population biology of spine shrimp Exhippolysmata oplophoroides in a subtropical region... 1083

1000 1000 700 800 800 600 600 600 500

s 400 400 400 300 200 200 200 0 0 100 17 –] 20 20 –] 23 23 –] 26 26 –] 29 29 –] 32 28 –] 30 30 –] 32 32 –] 34 34 –] 36 0 2.0 –] 4.0 4.0 –] 6.0 6.0 –] 8.0 Temperature (ºC) Salinity (ppt) Oxygen (mg/l) 1400 1400 1200 1200 1000 1000 800 800

Mean number of600 spine-shrimp 600 400 400 200 200 0 0 1.0 –] 10.0 10.0 –] 20.0 20.0 –] 30.0 30.0 –] 40.0 0.0 –] 1.0 1.0 –] 2.0 2.0 –] 3.0 3.0 –] 4.0 4.0 –] 5.0 Organic matter (%) Mean grain diameter (mm) Figure 5. Mean number of spine-shrimps E. oplophoroides, in the entire sample taken in Ubatuba Bay, by class of environmental factor analyzed (salinity, organic matter content, oxygen, temperature and grain size).

tive cycles of decapods can vary from place to place and among Population structure of the seabob shrimp Xiphopenaeus species, suggesting that several factors can influence their re- kroyeri (Heller, 1862) (Crustacea, Penaeoidea) in the littoral productive process. Because many other aspects of the biology of São Paulo, Brazil. Scientia Marina, Barcelona, 69 (1): 105- of E. oplophoroides remain poorly known (reproduction, life 112. cycle, ecology, etc), other studies should be developed to im- CASTRO-FILHO, B.M.; L.B. MIRANDA & Y. MYAO. 1987. Condições prove our knowledge of this species and its life history. hidrográficas na plataforma continental ao largo de Ubatuba: Acknowledgments variações sazonais e em média escala. Boletim do Instituto To FAPESP for financing part of the field trips (#94/4878- Oceanográfico, São Paulo, 35 (2): 135-151. 8), and to NEBECC students Bianka Noronha and Ricardo CHACUR, M.M. & M.L. NEGREIROS-FRANSOZO. 1999. Aspectos bioló- Figueira for their help during the sampling and laboratory work. gicos do camarão-espinho Exhippolysmata oplophoroides To Dr. Janet Reid for her constructive comments on early drafts (Holthuis, 1948) (Crustacea, Caridea, Hippolytidae). Revis- of the manuscript and great help with English language. All ta Brasileira de Biologia, São Carlos, 59 (1): 173-181. sampling done in this study complies with current applicable COSTA, R.C. & A. FRANSOZO. 2004a. Abundance and ecologic state and federal laws. distribution of the shrimp Rimapenaeus constrictus (Crustacea: ) in the northern coast of São Paulo REFERENCES State, Brazil. Journal of Natural History, Oxfordshire, 38 BAUER, R.T. 1986. Sex change and life history pattern in the (7): 901-912. shrimp Thor manningi (: Caridea): a novel case of COSTA, R.C. & A. FRANSOZO. 2004b. Reproductive biology of the partial protandric hermaphroditism. Biological Bulletin, shrimp Rimapenaeus constrictus (Stimpson, 1874) (Crustacea, Woods Hole, 170: 11-31. Decapoda, Penaeidae) in Ubatuba region, SP, Brazil. Journal BAUER, R.T. & R.T. HOLT. 1998. Simultaneous hermaphroditism of Crustacean Biology, Lawrence, 24 (2): 274-281. in the marine shrimp Lysmata wurdemanni (Caridea: COSTA, R.C.; A. FRANSOZO; F.L.M. MANTELATTO & R.H. CASTRO. 2000. Hippolytidae): an undescribed sexual system in the decapod Occurrence of shrimp species (Crustacea: Decapoda: Crustacea. Marine Biology, Berlin, 132: 223-235. Natantia: Penaeidea and Caridea) in Ubatuba Bay, Ubatuba, BERTINI, G. & A. FRANSOZO. 1999. Spatial and seasonal distribution SP, Brazil. Proceedings of the Biological Society of Wa- of Petrochirus diogenes (Anomura, Diogenidae) in the Ubatuba shington, Lawrence, 113 (3): 776-781. bay, São Paulo, Brazil. Iheringia Sér. Zool., Porto Alegre, COSTA, R.C.; A. FRANSOZO & A.P. PINHEIRO. 2004. Ecological (86): 145-150. distribution of the shrimp Pleoticus muelleri (Bate, 1888) BUCHANAN, B.A. & A.W. STONER. 1988. Distributional patterns of (Decapoda: Penaeoidea) of Southeastern Brazil. blue crabs (Callinectes spp.) in a tropical estuarine lagoon. Hydrobiologia, Dordrecht, 529: 195-203. Estuaries, University, Mississippi, 11 (4): 231-239. COSTA, R.C.; A. FRANSOZO; A.L. CASTILHO & F.A.M. FREIRE. 2005a. CASTRO, R.H.; R.C. COSTA; A. FRANSOZO & F.L.M. MANTELATTO. 2005. Annual, seasonal and spatial variation of abundance of the

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005 1084 V. Fransozo et al.

shrimp Artemesia longinaris (Decapoda: Penaeoidea) in south- MOSSOLIN, E.C. & S.L.S. BUENO. 2002. Reproductive biology of eastern Brazil. Journal of the Marine Biological Association Macrobrachium olfersii (Decapoda: Palaemonidae) in São Se- of the United Kingdom, Plymouth, UK, 85: 107-112. bastião, Brazil. Journal of Crustacean Biology, Lawrence, COSTA, R.C.; A. FRANSOZO & M.L. NEGREIROS-FRANSOZO. 2005b. Ecology 22 (2): 367-376. of the rock shrimp Sicyonia dorsalis Kingsley, 1878 (Crustacea: NAKAGAKI, J.M. & M.L. NEGREIROS-FRANSOZO. 1998. Population Sicyoniidae) in a subtropical region of Brazil. Gulf and biology of Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Caribbean Research, Ocean Springs, 17 (1). Penaeidae) from Ubatuba Bay, São Paulo Brazil. Journal of FIEDLER, G.C. 1998. Functional, simultaneous hermaphroditism Shellfish Research, Hanover, 17 (4): 931-935. in female-phase Lysmata amboinensis (Decapoda: Caridea: NEGREIROS-FRANSOZO, M.L. & A. FRANSOZO. 1992. Estrutura popu- Hippolytidae). Pacific Science, Honolulu, 52 (2): 161-169. lacional e determinação do tamanho da concha em Paguristes FRANSOZO, A. & F.L.M. MANTELATTO. 1998. Population structure tortugae Schmitt, 1933 (Crustacea, Decapoda, Anomura) do and reproductive period of the tropical hermit crab Calcinus litoral paulista. Biotemas, Florianópolis, 4 (2): 135-148. tibicen (Decapoda, Diogenidae) in the Ubatuba region, São NEGREIROS-FRANSOZO, M.L.; J.I. GONZÁLEZ-GORDILLO & A. FRANSOZO. Paulo, Brazil. Journal of Crustacean Biology, Lawrence, 18: 2002. First larval stage of Exhippolysmata oplophoroides 446-452. (Holthuis, 1948) (Decapoda, Caridea, Hippolytidae) obtained GALVÃO, R. & S.L.S. BUENO. 1999. Population structure and in laboratory. Nauplius, Botucatu, 10 (1): 67-71. reproductive biology of the camacuto shrimp, Atya scabra PIRES, A.M.S. 1992. Structure and dynamics of benthic (Decapoda: Caridea. Atyidae) from São Sebastião, Brazil, p. megafauna on the continental shelf offshore of Ubatuba, 291-299. In: J.C.V. VAUPEL KLEIN & F.R. SCHRAM (Eds). The Southeastern Brazil. Marine Ecology Progress Series, Luhe, biodiversity crisis and Crustacea. Rotterdam, A.A. Balkema, Germany, 86: 63-76. Brookfield, Crustacean Issues, vol. 12, 848p. SASTRY, A.N. 1983. Ecological aspects of reproduction, p. 179- GONZÁLEZ-GURRIARÁN, E.; J. FREIRE & L. FERNÁNDEZ. 1993. Geostatisti- 270. In: F.O.J. VERNBERG & N.B. VERNBERG (Eds). Biology of cal analysis of spatial distribution of Liocarcinus depurator, Crustacea 8: environmental adaptations. New York, Macropipus tuberculatus and Polybius henslowii (Crustacea: Academic Press, 383p. Brachyura) over the Galician continental Shelf (N.W. Spain). SOKAL, R.R. & F.J. ROHLF. 1995. Biometry. New York, W.H. Free- Marine Biology, Berlin, 115: 115-461. man, 3rd ed., 887p. KAGWADE, P.V. 1981. Hermaphrodite prawn Exhippolysmata VIEIRA, S. 1989. Introdução à bioestatística. Rio de Janeiro, ensirostris Kemp. Indian Journal of Fisheries, Chennai, 28: Campus, 293p. 189-194. WENNER, E.L.; W.P. CONN III & M.H. SHEALY. 1991. A comparison MANTELATTO, F.L.M. & A. FRANSOZO. 1999. Characterization of the of species composition and abundance of decapod physical and chemical parameters of Ubatuba Bay, northern and fishes from the North and South Edisto coast of São Paulo State, Brazil. Revista Brasileira de Biolo- rivers in South Carolina. South Carolina Marine Research gia, São Carlos, 59 (1): 23-31. Center, Technical Report, Charleston, 78: 1-48.

Received in 07.III.2005; accepted in 10.XI.2005.

Revista Brasileira de Zoologia 22 (4): 1078–1084, dezembro 2005