Revista de Biología Tropical ISSN: 0034-7744 [email protected] Universidad de Costa Rica Costa Rica de Lima Bueno, Maristela; Garcia Tavares, Yara Aparecida; Di Domenico, Maikon; Borges, Michela Gametogenesis and weight change of body organs of the sea cucumber Holothuria (Halodeima) grisea (Aspidochirotida: Holothuriidae) in Southern Brazil Revista de Biología Tropical, vol. 63, núm. 2, junio, 2015, pp. 285-296 Universidad de Costa Rica San Pedro de Montes de Oca, Costa Rica Available in: http://www.redalyc.org/articulo.oa?id=44943929024 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Gametogenesis and weight change of body organs of the sea cucumber Holothuria (Halodeima) grisea (Aspidochirotida: Holothuriidae) in Southern Brazil Maristela de Lima Bueno1,2,3, Yara Aparecida Garcia Tavares3, Maikon Di Domenico1 & Michela Borges1 1. Zoological Museum “Prof. Dr. Adão José Cardoso”, Institute of Biology, University of Campinas; Campinas, São Paulo, Brazil; [email protected], [email protected] 2. Postgraduate degree in Animal Biology, Institute of Biology, University of Campinas; Campinas, São Paulo, Brazil; [email protected] 3. University of Paraná, campus Paranaguá, Department of Biological Sciences; Paranaguá, Paraná, Brazil; [email protected] Received 30-VI-2014. Corrected 10-X-2014. Accepted 10-XI-2014. Abstract: The sea cucumber Holothuria (Halodeima) grisea is a widely distributed and economically important species that has been harvested in Brazil for several years, where there are no studies on its reproduction. We studied a population near Guaratuba Bay in Southern Brazil. Four sampling campaigns were made, in February, April, June and October 2008. We examined the macroscopic and microscopic features of the gonads to describe the gametogenesis. In addition, we analyzed the weight change of body organs. A total of 94 individuals were examined and no evidence of external sexual dimorphism was found. In April there were more males than females. Biometrically the body wall and gonads are the most important organs. The body wall increases in the June and the gonads during October and February; there might be an exchange of energy between these organs. Mature gonads are elongated and thick (red in females, cream in males). There were mature individuals year round, with an increase of sexual activity in February when oocyte mature diameter ranges from 70 to 160 µm. Spawning was in winter (June). Maturation period and body component variations were similar between sexes. Rev. Biol. Trop. 63 (Suppl. 2): 285-296. Epub 2015 June 01. Key words: reproduction, sea cucumber, gonad index, histology, spawning, rocky shore. Holothuroidea is a diverse class of worm- Most holothurians are large organisms, like and usually soft-bodied echinoderms. They free-living, iteroparous and dioecious. They are commonly found in tropical shallow waters typically reproduce once a year by spawning from the intertidal zone to the deep ocean their gametes into the sea where fertiliza- (Hadel, Monteiro, Ditadi, Tiago & Tommasi, tion occurs (Hyman, 1955; Smiley, McEuen, 1999; Pawson, 2007) which can comprise up Chaffee & Krishnan, 1991). The reproductive to 90 % of the total biomass of these environ- cycle in sea cucumbers is often very complex. ments (Pawson, 1966; Hendler, Miller, Paw- Gametogenesis and spawning usually follow a son & Kier, 1995). In Brazilian coast, these distinct seasonal pattern, varying in relation to organisms are found rather commonly grouped species and geographic locations (Drumm & under rocky outcrops (Mendes, Marenzi & Di Loneragan, 2005). Some abiotic factors such as Domenico, 2006), usually in contact with the seawater temperature and photoperiod (Smiley sandy floor, from which they feed during peri- et al., 1991; Ramofafia, Byrne & Battaglene, ods of immersion (Tommasi, 1969). 2000), lunar rhythms (Battaglene, Seymour, Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 63 (Suppl. 2): 285-296, June 2015 285 Ramofafia & Lane, 2002; Mercier, Sun, Bail- period in early winter (Lana, Marone, Lopes lon & Hamel, 2011) and biotic factors such as & Machado, 2001). The tides are characterized food availability (Drumm & Loneragan, 2005) by diurnal inequality and attain to maximum have been suggested as exogenous cues affect- and minimum amplitudes of approximately 2 ing the reproduction of the species. and 0.5 m respectively (Knoppers, Brandini & Holothuria (Halodeima) grisea has been Thamm, 1987). harvested in some areas of southeastern-south In the sampling campaigns the water tem- Brazilian coast (Hadel et al., 1999; A. Marenzi, perature varied from 26 ºC (February) to 19 personal communication, February 19, 2010) ºC (April and June) in the studied period. The several years ago. A sustainable exploita- seawater salinity remained relatively constant, tion of this resource necessarily requires a approximately 30. description of the reproduction cycle of this potentially exploitable species to implement Field sampling and lab routines: Holo- a harvest season and a closure during the thuria (Halodeima) grisea specimens were spawning (Guzmán, Guevara & Hernandez, sampled in February, April, June and October 2003; Abdel-Razek, Abdel-Rahman, El-Shimy 2008. About twenty to twenty-five specimens & Omar, 2005). larger than 10 cm were randomly collected by Though Holothuria (Halodeima) grisea hand in each month. Surface seawater tem- represents a very common sea cucumber along perature and salinity were recorded in situ. All the Brazilian coast, its spatial and temporal individuals were transferred to the laboratory, distribution, beyond ecological aspects of this relaxed and dissected. The total body drained species are still poorly understood. In this weight following the opening of the body investigation, the reproductive aspects of a and the removal of coelomic fluid, the body population of Holothuria (Halodeima) grisea wall, respiratory tree, haemal system, empty was evaluated by macroscopic and histologi- digestive tract and gonads were recorded with cal characteristics of gonads, as well as the an electronic precision scale (0.0001 g). The participation of the body components in the removed gonads were macroscopically and gametogenesis process. microscopic examined in order to determinate sex and maturity stage and then fixed in 9 % MATERIALS AND METHODS formaldehyde (Despalatovic, Grubelic, Simu- novic, Antolic & Zuljevic, 2004). Study site: Specimens were collected The gonadal macroscopic features (gonad from a rocky shore located nearby the mouth color, opacity and consistency of the tubules) zone of Guaratuba Bay in the State of Paraná, were presented on a scale adapted from Abdel- Southern Brazil (25° 53’ 22.73” S and 48° 33’ Razek et al. (2005) and Ghobadyan, Morov- 37.81” W) .The climate is classified as meso- vati, Ghazvineh and Tavassolpour (2012). For thermic subtropical with a mean annual rainfall the histological examinations, small sections of of 2.500 mm (maximum of 5.300 mm), an the gonad tubules were dehydrated, embedded average annual temperature of 22 °C with a hot in paraffin wax, sectioned (7 μm-thick) and rainy summer season and mean air humidity stained with haemotoxylin and eosin (H / E). around 85 % (Marone et al., 2004). The stages of gametogenesis were based on The main atmospheric disturbances are those used in previous studies of sea cucumber cold fronts from the SW-NE direction that gonads (Purwati & Luong-Van, 2003; Drumm originate in Southern America. A typical rainy & Lonergan, 2005; Rasolofonirina, Vaitilingon, season initiates in late spring and lasts dur- Eeckhaut & Jangoux, 2005; Shiell & Uthicke, ing most of the summer while the dry season 2006). The mature oocytes were measured by lasts from late autumn to late winter, but is the median diameter axis [(length + width) x usually interrupted by a short and weak rainy 0.5] with an ocular micrometer. 286 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 63 (Suppl. 2): 285-296, June 2015 Data Analysis: Frequency distribution of test and the significance was tested at the 95 % the maturity scale in both sexes (growing, confidence level. mature or post-spawning) was calculated at each month. Sex ratio was estimated consider- RESULTS ing the total sample over the study period and between months. Statistically significant differ- Macroscopic features in gametogenesis ence from the expected 1:1 sex ratio was tested stages (Fig. 1 a - d): Gonads are a single using c2 (Chi-square test) (Zar, 1996). structure, consisting of numerous filamentous The relationship between total wet weight tubules basically gathered into one tuft attached and organs (body wall, respiratory tree, haemal to the left side of the dorsal mesentery. The system, digestive tract, gonadal) is described macroscopic appearance in relation to color, by the linear function (y = a + bx). To evaluate if the relationship between total wet weight and opacity and texture of the gonads between the individual’s organ weight among the months, months showed noticeable differences to the we use analysis of covariance (ANCOVA) naked eye. However, during growth and deplet- after logarithmic transformation of all the ed, no macroscopic morphological differences variables (Ebert, Hernandez & Russell, 2011). were observed between sexes.