- Email: [email protected]
Growth and reproduction of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) from the southeastern coast of Brazil
Regional Studies in Marine Science 6 (2016) 1–9
Contents lists available at ScienceDirect
Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma
Growth and reproduction of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) from the southeastern coast of Brazil Joyce Rocha Garcia a , Milena Regina Wolf a , Rogerio Caetano da Costa b , Antonio Leão Castilho a,∗ a
Study Group on Crustacean Biology, Ecology and Culture (NEBECC) – Zoology Department, Bioscience Institute, UNESP, 18618-000, Botucatu, Brazil
b
Laboratory of the Biology of Marine and Freshwater Shrimps (LABCAM) – Biological Sciences Department, Faculty of Sciences, UNESP, 17033-360, Bauru, Brazil
highlights • • • •
Non-selective trawls collect high diversity of shrimps as Rimapenaeus constrictus. Food availability for larval stages seems to be important for reproductive success. This species is in accordance with latitudinal pattern of reproduction. Growth rate and longevity are closely related.
article
info
Article history: Received 3 November 2015 Received in revised form 23 February 2016 Accepted 23 February 2016 Available online 2 March 2016 Keywords: Seasonality Subtropical region Roughneck-shrimp Match–mismatch theory
abstract Few studies have been performed on the shrimp Rimapenaeus constrictus, despite its wide geographic distribution in the western Atlantic Ocean. The population dynamics of R. constrictus were evaluated, focusing on sex ratios, growth, longevity, and reproduction, in the Cananeia region, along the southern coast of São Paulo state, Brazil. Monthly trawls were conducted from July 2012 through May 2014 using a shrimp boat outfitted with double-rig nets. The shrimp were identified according to their sex and reproductive condition, and carapace length (CL) was measured. A total of 1702 individuals were collected, and females were found to reach sexual maturity at a greater CL (9 mm) than males (7 mm). Based on the estimated growth curve parameters, males exhibit shorter longevity (0.73 years) than females (1.14 years). In terms of the sex ratio, there was a statistically significant bias toward females observed over the months, beginning at a CL of 9 mm (binomial test, p < 0.05). The seasonal reproductive pattern recorded during the spring and summer coincided with higher temperatures and chlorophyll concentrations (plankton production), which suggests that food availability for protozoeal and mysis larvae may be an important selective factor in the reproductive success of R. constrictus. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Penaeidae shrimps are of great economic importance in the Brazilian fishing industry; more than 53 thousand tons of crustaceans were caught in the country during 2005, more than 30 thousand tons of which consisted only of shrimps (SEAP and IBAMA, 2006). The majority of the shrimp catch in Brazil is obtained using non-selective trawls as fishing gear, resulting in the accidental extraction of bycatch fauna with a high biodiversity, as observed for the species Rimapenaeus constrictus (Stimpson, 1874)
∗
Corresponding author. Tel.: +55 14 38800645. E-mail address: [email protected] (A.L. Castilho).
http://dx.doi.org/10.1016/j.rsma.2016.02.006 2352-4855/© 2016 Elsevier B.V. All rights reserved.
in the Brazilian fauna (Neto, 2011; Costa and Fransozo, 2004a,b; Castilho et al., 2015). Fishing activity is considered to represent a complex situation because of the involvement of many sectors of interest, including the social, economic and environmental sectors. Therefore, the conception and implementation of an effective management plan in Brazil is difficult for both shrimps of economic importance to the industry and bycatch species. Thus, national organizations recognize the importance of understanding the life history of shrimps as an important tool for contributing to conservation planning in the future (Neto, 2011). However, studies on the reproductive biology of R. constrictus are scarce, with the available reports consisting of work by Costa and Fransozo (2004a), who clarified the temporal variation of the
2
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 1. Cananeia region, showing sampling stations in the adjacent oceanic area (I, II, III and IV) and estuarine area (Mar Pequeno—V, VI and VII).
spawning intensity and the recruitment of juveniles in the tropical region of Ubatuba in Brazil, and by Bauer and Lin (1994), who contributed information about the seasonal pattern of breeding in R. constrictus and Rimapenaeus similis (Smith, 1885) in a subtropical region in the United States. Other studies found in the literature that specifically address R. constrictus focused on its ecological distribution (Costa and Fransozo, 2004b; Hiroki et al., 2011). There are no studies on the growth and longevity of R. constrictus reported in the literature. Thus, the present study represents pioneering work on this subject. Such studies are important for the development of management plans for these shrimps, where the biological parameters obtained from the Von Bertalanffy (1938) growth model, associating individual size and age, provide estimates of mortality rates and longevity. The formulation of a mathematical model for age determination in crustaceans is of great importance, as crustaceans do not exhibit permanent bony structures; instead, the crustacean exoskeleton is periodically replaced in a process termed ecdysis, making evaluations based on periodic markings on their body surface impossible (Hartnoll, 2001; Keunecke et al., 2011; Castilho et al., 2015). This study aimed to investigate the reproductive biology, growth and longevity of the population of R. constrictus from Cananeia, along the southern coast of São Paulo state, Brazil. The reproductive aspects of the investigation included assessment of the sex ratio, the temporal variation of reproduction (continuous or seasonal) and juvenile recruitment, in comparison with the existing literature, as well as evaluation of the influence of several environmental factors (temperature, salinity and chlorophyll a concentration) on reproductive events.
oceanic area, using a shrimp boat equipped with double-rig nets to obtain biological material (Fig. 1). Samples were collected monthly from July 2012 through May 2014. A total of seven stations were previously selected to cover estuarine and oceanic areas of Cananeia, on the southern coast of São Paulo state. Depths were verified according to the bathymetric stratification described in nautical charts. During sampling, depth was monitored with a Eureka multiparameter probe. Four sampling stations were located in the oceanic area adjacent to the Cananeia region: stations I, II and III were positioned along the 10–15 m isobath and IV in the 5–10 m isobath. The other three sampling stations, V, VI and VII (5–10 m isobath), were located in the Mar Pequeno estuarine area, between Cananeia and Comprida Islands, which is influenced by fresh water from the complex estuarine–lagoon system of Cananeia-Iguape (Besnard, 1950).
2. Materials and methods
2.3. Reproduction
2.1. Sampling
Individuals were subjected to measurement of carapace length (CL: from the orbital angle to the posterior margin of the carapace) with a caliper and were classified by sex, according to the presence of a petasma, in males, or a thelycum, in females (Costa et al., 2003).
Trawls lasting 30 min were performed in the complex estuarine–lagoon system of Cananeia-Iguape and the adjacent
2.2. Bottom environmental parameters Environmental parameters, including temperature (°C), salinity and chlorophyll concentrations (µg/l), were measured with a Eureka multiparameter probe (Manta model 2-4.0) at each of the seven sampling stations. Temperature and salinity were registered from July 2012 through May 2014, whereas chlorophyll concentrations were measured from January through December 2013. Due to adverse environmental conditions in March 2013, samples were only collected at sampling stations V, VI and VII.
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
The stages of reproductive development were determined through macroscopic analysis of the male and female reproductive apparatuses. Female reproductive condition was assessed via macroscopic observation of the degree of ovarian development (according to color and the volume occupied by the gonads). Ovaries were categorized as immature (IM) if they varied from thin, transparent strands to thicker strands; as spent (SP) if they were white and much larger and thicker than those of immature females; as developed (DE) if they were light green; or as mature (MA) if they were green to dark green, occupying the entire dorsal portion of the abdomen as well as part of the carapace (more details in Costa and Fransozo, 2004a). In females, the presence of a sperm plug attached to the thelycum (inseminated females) was also observed macroscopically. Females with gonads in the SP, DE and MA stages were defined as adults, while those with gonads in the DE and MA stages were considered reproductive females, and those with gonads in the IM stage were defined as recruits. The reproductive period was determined based on the presence of reproductive females over the studied months (Castilho et al., 2008). Sexual maturity of male penaeids is usually indicated by fusion of the petasmal lobes (gonadal endopods), whereas immature males (IM) exhibit separated petasmal lobes (Boschi, 1989). The maturity of adult males was classified according to the development of spermatophores in the terminal ampoule (ejaculatory duct), which is convenient because spermatophores are visible through the exoskeleton (Chu, 1995). When spermatophores were not visible through macroscopic observation in an adult male, the individual was classified as lacking spermatophores (LS). If spermatophores were visible and occupied a portion of or all terminal ampoules, males were classified as spermatophore-bearing males (MA) (Castilho et al., 2012, 2015). Males with gonads in the LS and MA stages were defined as adults, while those with gonads in the MA stage were considered reproductive males, and those with gonads in the IM stage were defined as recruits. Size at sexual maturity was determined for males and females using the proportion of juvenile and adult individuals in 0.5 mmCL size classes. The procedure employed here to estimate sexual maturity was based on fitting a sigmoid logistic curve (Somerton, 1980). We used the equation y = 1/(1 + e(−r (CL − CL50 ))), where y is the estimated proportion of adult shrimps, CL50 is the carapace measurement at the onset of sexual maturity, and r is the coefficient for the slope of the logistic curve. The logistic curve was fitted via the least squares method to the previously indicated proportions for each size class of all individuals and samples using maximum-likelihood iterations. After adjusting the regression model, sexual maturity (CL50 ) was estimated as the size at which 50% of males and females reached maturity. All analyses of CL50 values were conducted in Microsoft Office Excel 2010. Juvenile recruitment was temporally characterized based on the frequency of immature individuals of both sexes in the population, whereas the beginning of sexual maturity was determined based on the length of the smallest adult individuals (Bauer, 1989). Due to the absence of reproductive individuals and inseminated females at sampling stations VI and VII, the statistical analyses were based only on the biological and environmental parameters recorded monthly at sampling stations I through V. For the statistical analysis, the assumption of normality was verified via the Shapiro–Wilk test. When the data were not distributed according to a Gaussian curve, they were logarithmically transformed (Log x + 1). All tests were performed with a significance level of 5% (Zar, 1999). The binomial test was used to estimate the sex ratios per month and per size class, and crosscorrelations were employed to evaluate the possible correlation of spermatophore-bearing males
3
with spent, inseminated or reproductive females. Crosscorrelations were also used to evaluate the correlation of the monthly abundance of reproductive females with recruits and with the mean values of temperature, salinity and chlorophyll concentrations by month. In crosscorrelations, two series of data are compared as a function of the time lag (n), using the Pearson correlation coefficient to measure relationships between values of the first data series and values of the second series from either earlier (in negative lags) or later months (in positive lags). Correlation coefficient values at lag 0 are equivalent to the standard Pearson correlation (STATSOFT, 2011). 2.4. Growth and longevity The population growth analyses for crustaceans were adapted from previous studies on fish and were based on mathematical models developed by Von Bertalanffy (1938), assuming that body length is a function of the age of individuals (Sparre and Venema, 1997). For the analysis of population growth, individuals were distributed into 0.5 mm-CL size classes in the analyzed time period, which allowed the identification of modes in the PeakFit 4.0 program (Automatic Peak Fitting Detection and Fitting, Method I—Residual, no Data Smoothing) (Fonseca and D’Incao, 2003). The obtained modes were plotted against time in a dispersion graph, from which it was possible to identify growth cohorts for males and females (Castilho et al., 2015). Posteriorly, three growth parameters were estimated with the Solver tool of Microsoft Office Excel for each identified cohort. The obtained parameters were based on the Von Bertalanffy growth model (VBGM) (1938): CLt = CLinf [1 − e − k(t −t0) ] and were as follows: (1) asymptotic length (CLinf ), which corresponds to the size reached by an individual if it grows indefinitely; (2) the growth coefficient (k), which is the rate at which the asymptotic length is reached; and (3) an adjusted parameter (t0 ), which corresponds to the theoretical age that the individual would exhibit at size zero. The seed values used to determine the parameters were the largest values of CL observed in this study for males (13.6 mm) and females (17.2 mm). Subsequently, the ages (in days) were corrected according to the time interval between the samples and the value obtained for t0 . From this, mean curves were constructed for males and females, which were compared by an F test (p = 0.05) (Cerrato, 1990). Longevity was estimated by the inverted VBGM with an adaptation suggested by D’Incao and Fonseca (1999): t max = (0 −(1 − k) ln(1 − CLt /CLinf )). The time that individuals take to reach sexual maturity and the minimal sizes of the recruitment cohorts were calculated according to the equation proposed by King (1995): t = t0 − (1/k) ln[1 − CL(m, s) /CLinf ], where k is the growth coefficient, CL is the size at sexual maturity (CLm ) or the size of the smaller individual (CLs ) and CLinf is the asymptotic length. 3. Results 3.1. Sex ratio A total of 1702 individuals were collected during the sampling period, among which 1276 were females, and 426 were males. At most time points, a bias toward females was observed, with females always showing a greater abundance than males (binomial test, p < 0.05) (Fig. 2). However, there was a trend toward sex ratios close to 50% up to a size of 8.5 mm; after this size, the sex ratio was biased in favor of females (Fig. 3).
4
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 2. Rimapenaeus constrictus. Monthly variation of the sex ratio (number of males /total number) from July 2012 through May 2014 in the Cananeia region. According to the binomial test, points below the 0.50 line represent significant deviation of the sex ratio in favor of females, and the points above this line represent significant deviation in favor of males.
Fig. 4. Rimapenaeus constrictus. Distribution of demographic categories of males and females among size classes from July 2012 through May 2014 in the Cananeia region (the categories are as follows: MA = mature males and females, SP = spent females, LS = spermatophore-lacking males, IM = immature males and females).
Fig. 3. Rimapenaeus constrictus. Variation of the sex ratio (number of males/total number) in relation to size classes from July 2012 through May 2014 in the Cananeia region. According to the binomial test, points below the 0.50 line represent significant deviation of the sex ratio in favor of females, and points above this line represent significant deviation in favor of males.
3.2. Reproduction and recruitment Males and females displayed different distributions in terms of size classes; most of the females were in the spent stage (10–10.5 mm), while most of the males were in the reproductive stage (8–8.5 mm) (Fig. 4). The largest size registered for females was 17.2 mm, whereas for males, it was 13.6 mm. The size at sexual maturity (CL50 ) was estimated at 8.2 mm for males and 10.5 mm for females (Fig. 4). Only the significant results from the crosscorrelation analysis are described: the number of spermatophore-bearing males was positively correlated with spent (R = 0.69; p = 0.0003) and inseminated (R = 0.51, p = 0.0135) females, with no time lag (lag = 0). Reproductive females were recorded in the spring, and their numbers peaked in October 2012 and in the summer, especially in February 2013 and January 2014, with lower abundance or a complete absence being observed in the colder months (autumn and winter). Immature individuals were distributed sparsely throughout the months of collection, especially in January 2013 and May 2014. In spite of the absence of a significant relationship between reproductive females and immature individuals (crosscorrelation, p > 0.05), the two highest peaks for immature individuals were found in January 2013 and May 2014, following the two highest peaks for reproductive females, in October 2012 and January 2014 (Fig. 5).
Fig. 5. Rimapenaeus constrictus. Monthly distribution of reproductive females and immature individuals from July 2012 through May 2014 in the Cananeia region.
No significant relationship was found between reproductive females and the chlorophyll concentration. However, reproductive peaks were observed in February, June and September, prior to periods with higher phytoplankton productivity in March, July and October–November (Fig. 6). 3.3. Growth and longevity Based on the growth analysis, 14 cohorts were identified for females and seven for males (Figs. 7 and 8). The calculated parameters revealed a CL∞ of 16.40 mm, k of 0.011 and t0 of −0.16 days for females and a CL∞ of 11.74 mm, k of 0.017 and t0 of −0.36 days for males. Females showed greater longevity than males, at 415 days (1.14 years) versus 267 days (0.73 years). The growth curves for males and females were significantly different (F critical = 2.70 < F calculated = 13.57; p = 2.09.10−7 ).
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 6. Rimapenaeus constrictus. Abundance of reproductive and inseminated females according to the chlorophyll concentration (µg/l) from July 2012 through May 2014.
Cohorts of small individuals (juvenile recruitment) were identified in January and April 2013 and May 2014 (Figs. 7 and 8). The minimal sizes of the recruitment cohorts were 4.97 mm (females— January 2013) and 5.82 mm (males—November 2012), corresponding to ages of 33 and 40 days, respectively. The proposed sizes at sexual maturity of 8.2 mm and 10.5 mm for males and females correspond to ages of 71 and 93 days, respectively. 4. Discussion In this study, it was observed that females reached larger sizes than males. According to Boschi (1989), this pattern is a general rule for penaeids and constitutes an important sexual dimorphism in these species. A larger size of females is an adaptation to increase egg production (Gab-Alla et al., 1990). Studies on R. constrictus and other penaeids have corroborated this dimorphism (Castilho et al., 2012, 2015; Costa and Fransozo, 2004a; Semensato and Di Beneditto, 2008; Simões et al., 2013). Thus, females reach sexual maturity later than males, which was confirmed in this species in a previous study in Ubatuba (Costa and Fransozo, 2004a) as well as among other species of penaeids (Castilho et al., 2012, 2015; Heckler et al., 2013; Semensato and Di Beneditto, 2008). The reproductive period of a marine species usually follows a latitudinal pattern, in which seasonal reproduction occurs in subtropical regions, and reproduction tends to be continuous in the tropics (Bauer, 1992); this pattern was also observed in the present study and has been previously described in the literature for R. constrictus. In the current study in Cananeia (a subtropical region), seasonal reproduction was observed, as reported by Bauer and Lin (1994) in the northern hemisphere (a subtropical region). In contrast, continuous reproduction was recorded in this species in a study performed on the northern coast of São Paulo state (latitude 23 ° S) (Costa and Fransozo, 2004a). Temperature is considered to be important factor in the maintenance of gametogenesis, which defines the reproductive period of a species (Bauer, 1992). In the present study, it was possible observe a significant relationship between an increased abundance of reproductive females and the hotter periods registered during the sampling periods (spring and summer). This means that temperature acts as an important factor in ovarian stimulation, as observed by Bauer and Lin (1994), Castilho et al. (2007, 2012, 2015) and Williams (1984), among others. The months with the greatest number of reproductive females preceded periods with the highest chlorophyll concentrations in the water column, suggesting that offspring in the larval stage (protozoeal and mysis larvae) will exhibit greater developmental success due to increased food availability (phytoplankton productivity), in accord with the match/mismatch theory proposed by Cushing (1975).
5
The positive correlation found between spermatophore-bearing males and spent and inseminated females corroborates the reproductive pattern described for species with a closed thelycum. According to Dall et al. (1990), insemination in closed thelycum species occurs immediately after ecdysis (i.e., in spent females). Therefore, it is expected that males ready for reproduction (spermatophore-bearing) and females ready for copulation (spent females) or inseminated females (suggesting that copulation has just occurred) will be observed at the same time. Juvenile recruitment of R. constrictus was discontinuous along the months, without significant relationship with reproductive females. Thus, recruitment could be considered as episodic, indicating a complex stock—recruitment relationship, as observed by Bauer and Lin (1994) and Costa and Fransozo (2004a) for the same species and by Castilho et al. (2007) for Artemesia longinaris Spence Bate, 1888. Several conditions can generate episodic recruitment, such as high variation in the mortality of planktonic larvae and early juvenile stages (Bauer, 1989), due to fluctuations in phytoplankton production (providing food for protozoeal and mysis larvae). In addition, the physical conditions of each region and the presence of predators might also satisfactorily explain episodic recruitment (Castilho et al., 2007). The longevity of shrimps observed in nature may be similar or different in the two sexes. For example, males and females of the species Pleoticus muelleri (Spence Bate, 1888) live for approximately two years, although females live slightly longer than males (Castilho et al., 2012). In contrast, in the case of Macrobrachium hainanense (Parisi, 1919), females live for 29 months, whereas males live for 48 months (Mantel and Dudgeon, 2005). Although the cited examples indicate that longevity in nature is variable in relation to the sex, it is very common in growth studies in penaeids to find that females present greater longevity than males (Campos et al., 2011; Castilho et al., 2012, 2015; Heckler et al., 2013), as observed in the present study. The discrepancy between sexes in terms of longevity could have many causes, such as differences in hormones and the cost of reproduction (Vogt, 2012). The mechanism underlying these differences is not well understood, but it is known that there is a huge advantage in the fitness of species when females live for longer periods, as a single female is capable of producing many eggs (Chacur and NegreirosFransozo, 1998), thus guaranteeing more efficient replacement of the population in association with greater longevity. Among penaeids, it is common for males to exhibit a higher growth rate (k) and a lower asymptotic length than females (Gulland and Rothschild, 1981; Petriella and Boschi, 1997); this difference was also observed in the present study. Since the early twentieth century, researchers have believed that high metabolic rates lead to cellular aging and, thus, decreased longevity (Pearl, 1928). It is thought that a greater growth investment in males (greater k than females) leads to higher metabolic rates, which culminate in decreased longevity and lower asymptotic lengths. The monthly sex ratio was skewed toward females, demonstrating that R. constrictus provides another exception to the rule proposed by Fisher (1930). A deviation in the sex ratio may be associated with the influence of factors such as migration and a differential mortality rate between sexes (Wenner, 1972). According to Gab-Alla et al. (1990), males tend to present a higher mortality rate than females, which contributes to the deviation of the sex ratio usually observed in marine crustaceans. Recent studies have demonstrated that the sex ratio is a function of individual size (Castilho et al., 2012; Heckler et al., 2013; Semensato and Di Beneditto, 2008; Simões et al., 2013), as observed in the present study. Males displayed a higher growth rate and lower asymptotic length than females, which contributed to the observed skewed sex ratio because the chance of finding a
6
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 7. Rimapenaeus constrictus. Frequency distribution of the carapace length (CL) of females from July 2012 through May 2014 in the Cananeia region. The lines represent the cohorts identified during the sampling months (Cont. = Continuation).
male of a certain size was lower. The lower longevity of males is expected to be another factor related to the deviation of the sex ratio in the largest size classes.
Research conducted by Bauer (1992) could provide a hint about the latitudinal variation of the longevity of R. constrictus. This author proposed that growth and longevity in marine crustaceans
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
7
Fig. 8. Rimapenaeus constrictus. Frequency distribution of the carapace length (CL) of males from July 2012 through May 2014 in the Cananeia region. The lines represent the cohorts identified during the sampling months (Cont. = Continuation).
8
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
follow a latitudinal pattern, based on the observation that shrimp species belonging to Sicyoniidae present greater longevity in subtropical and cold temperate regions compared with species in tropical regions. Cananeia is located in a subtropical region, and it is therefore possible to suggest that in future studies on R. constrictus from tropical regions, individuals will exhibit lower longevity in relation to that observed in the present research. Crustacean growth is generally strongly influenced by temperature. In ectothermic species (such as crustaceans), metabolic processes tend to increase with increasing temperature, speeding up the molting process, which culminates in an increase in growth rates (k) (Hartnoll, 2001). It is proposed here that the high average temperatures observed in the summers of 2013 and 2014 in the present study (over 25 °C) influenced the observed k for both males and females. Thus, R. constrictus presented a seasonal reproductive pattern and complex recruitment characteristics. It is believed that longevity and growth rates are closely related. However, further studies on the growth and longevity of this species in different locations are necessary for comparison and to achieve a better understanding of its population dynamics on a larger geographic scale. The influence of the chlorophyll concentration also requires further investigation, possibly involving larval stage collections. Moreover, temperature can be regarded as the most important factor in the reproduction and growth of this species. Acknowledgments The authors are indebted to the ‘‘Fundação de Amparo à Pesquisa do Estado de São Paulo’’ (FAPESP) for providing financial support for field collections, visiting activities and scholarships (2007/56733-5, 2010/50188-8, 2013/14174-0), CAPES CIMAR (N° 23038.004310/2014-85) and to CNPq (Research Scholarships PQ 305919/2014-8 and PQ 308653/2014-9). The authors thank many colleagues from the NEBECC group who helped with sampling and laboratory analyses and the ‘‘Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis’’ (IBAMA) for granting permission to collect the shrimp. References Bauer, R.T., 1989. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. J. Exp. Mar. Ecol. 127, 175–187. http://dx.doi.org/10.1016/0022-0981(89)90183-4. Bauer, R.T., 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. J. Invertebr. Reprod. Dev. 22, 193–202. http://dx.doi.org/10.1080/07924259.1992.9672272. Bauer, R.T., Lin, J., 1994. Temporal patterns of reproduction and recruitment in populations of the penaeid shrimps Trachypenaeus similis (Smith) and T. constrictus (Stimpson) (Crustacea: Decapoda) from the Northcentral Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 185, 205–222. http://dx.doi.org/10.1016/00220981(94)90052-3. Besnard, W., 1950. Considerações gerais em torno da região lagunar de CananéiaIguape I. Bol. Inst. Paul. Oceanogr. 1, 9–26. http://dx.doi.org/10.1590/S010042391950000200001. Boschi, E.E., 1989. Biología pesquera del langostino del litoral patagonico de Argentina. Inst. Nac. Desarro. Pesq. (INIDEP). Campos, B.R., Branco, J.O., D’Incao, F., 2011. Crescimento do camarão-sete-barbas (Xiphopenaeus kroyeri (Heller 1862)), na baía de Tijucas, Tijucas, SC (Brasil). Atlântica 33, 201–208. Castilho, A.L., Bauer, R.T., Freire, F.A.M., Fransozo, V., Costa, R.C., Grabowski, R.C., Fransozo, A., 2015. Lifespan and reproductive dynamics of the commercially important sea bob shrimp Xiphopenaeus kroyeri (Penaeoidea): synthesis of a 5-year study. J. Crustac. Biol. 35, 30–40. http://dx.doi.org/10.1163/1937240X00002300. Castilho, A.L., Costa, R.C., Fransozo, A., Boschi, E.E., 2007. Reproductive pattern of the South American endemic shrimp Artemesia longinaris (Decapoda, Penaeidae), off the coast of São Paulo state, Brazil. Rev. Biol. Trop. 55, 39–48. http://dx.doi.org/10.15517/rbt.v55i0.5804. Castilho, A.L., Costa, R.C., Fransozo, A., Negreiros-Fransozo, M.L., 2008. Reproduction and recruitment of the South American red shrimp, Pleoticus muelleri (Crustacea: Solenoceridae), from the southeastern coast of Brazil. Mar. Biol. Res. 4, 361–368. http://dx.doi.org/10.1080/17451000802029536.
Castilho, A.L., Wolf, M.R., Simões, S.M., Bochini, G.L., Fransozo, V., Costa, R.C., 2012. Growth and reproductive dynamics of the South American red shrimp, Pleoticus muelleri (Decapoda: Solenoceridae), from the Southeastern coast of Brazil. J. Mar. Syst. 105, 135–144. http://dx.doi.org/10.1016/j.jmarsys.2012.07.004. Cerrato, R.M., 1990. Interpretable statistical tests for growth comparisons using parameters in the von Bertalanffy equation. Can. J. Fish. Aquat. Sci. 47, 1416–1426. http://dx.doi.org/10.1139/f90-160. Chacur, M.M., Negreiros-Fransozo, M.L., 1998. Aspectos biológicos do camarãoespinho Exhippolysmata oplophoroides (Holthuis, 1948) (Crustacea, Caridea, Hippolytidae). Rev. Bras. Biol. 59, 173–181. http://dx.doi.org/10.1590/S003471081999000100022. Chu, K.H., 1995. Aspects of reproductive biology of the shrimp Metapenaeus joyneri from the Zhujiang Estuary, China. J. Crustac. Biol. 15, 214–219. http://dx.doi.org/10.1163/193724095X00226. Costa, R.C., Fransozo, A., 2004a. Reproductive biology of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) in the Ubatuba region of Brazil. J. Crustac. Biol. 24, 274–281. http://dx.doi.org/10.1651/C-2437. Costa, R.C., Fransozo, A., 2004b. Abundance and ecologic distribution of the shrimp Rimapenaeus constrictus (Crustacea: Penaeidae) on the Northern coast of São Paulo State, Brazil. J. Nat. Hist. 38, 901–912. http://dx.doi.org/10.1080/0022293021000046441. Costa, R.C., Fransozo, A., Melo, G.A.S., Freire, F.A.M., 2003. Chave ilustrada para identificação dos camarões dendrobranchiata do litoral norte do estado de São Paulo, Brasil. Biota Neotrop. 3, 1–12. http://dx.doi.org/10.1590/S1676-06032003000100011. Cushing, D.H., 1975. Marine Ecology and Fisheries. Cambridge University Press, Great Britain, p. 278. Dall, W., Hill, B.J., Rothlisberg, P.C., Staples, D.J., 1990. The biology of the Penaeidae. In: Blaxter, J.H.S., Southward, A.J. (Eds.), Advances in Marine Biology, Vol. 27. Academic Press, San Diego, p. 489. D’Incao, F., Fonseca, D.B., 1999. Performance of the von Bertalanffy growth curve in penaeid shrimps: a critical approach. In: Proceedings of the Fourth International Crustacean Congress. Amsterdam, Netherlands, pp. 733–737. Fisher, R.A., 1930. The Genetical Theory of Natural Selection. New York Dover Publications, New York, p. 318. Fonseca, D.B., D’Incao, F., 2003. Growth and reproductive parameters of Kalliapseudes schubartii in the estuarine region of the Lagoa dos Patos (southern Brazil). J. Mar. Biol. Assoc. UK 83, 931–935. Gab-Alla, A.A.F.A., Hartnoll, R.G., Ghobashy, A.F., Mohammed, S.Z., 1990. Biology of penaeid prawns in the Suez Canal Lakes. Mar. Biol. 107, 417–426. http://dx.doi.org/10.1007/BF01313423. Gulland, J.A., Rothschild, B.J., 1981. Penaeid Shrimps: Their Biology and Management. Fishing News Books, Farnham, p. 312. Hartnoll, R.G., 2001. Growth in Crustacea—Twenty years on. Hydrobiologia 449, 111–122. http://dx.doi.org/10.1023/A:1017597104367. Heckler, G.S., Simões, S.M., Santos, A.P.F., Fransozo, A., Costa, R.C., 2013. Population dynamics of the seabob shrimp Xiphopenaeus kroyeri (Dendrobranchiata, Penaeidae) in south-eastern Brazil. Afr. J. Mar. Sci. 35, 17–24. http://dx.doi.org/10.2989/1814232X.2013.769901. Hiroki, K.A.N., Fransozo, A., Costa, R.C., Castilho, A.L., Shimizu, R.M., Almeida, A.C., Furlan, M., 2011. Bathymetric distribution of the shrimp Rimapenaeus constrictus (Stimpson, 1874) (Decapoda, Penaeidae) in two locations off the southeastern Brazilian coast. Mar. Biol. Res. 7, 176–185. http://dx.doi.org/10.1080/17451000.2010.489614. King, M., 1995. Fisheries Biology, Assessment and Management. Fishing News Books, Cambridge, p. 341. Keunecke, K.A., D’Incao, F., Moreira, F.N., Silva Jr, D.R., Verani, J.R., 2008. Idade e crescimento de Callinectes danae e C. ornatus (Crustacea, Decapoda) na Baía de Guanabara, Rio de Janeiro, Brasil. Iheringia, Sér. Zool 98, 231–235. Mantel, K.S., Dudgeon, D., 2005. Reproduction and sexual dimorphism of the palaemonid shrimp Macrobrachium hainanense in Hong Kong streams. J. Crustac. Biol. 25, 450–459. http://dx.doi.org/10.1651/C-2541. Neto, J.D., 2011. Proposta de plano nacional de gestão para o uso sustentável de camarões marinhos do Brasil. Brasília: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis e Ministério do Meio Ambiente. Pearl, R., 1928. The Rate of Living. Knopf, New York, p. 167. Petriella, A.M., Boschi, E.E., 1997. Crecimiento en crustáceos decápodos: resultados de investigaciones realizadas en Argentina. Rev. Investig. Mar. 25, 135–157. http://dx.doi.org/10.4067/S0717-71781997002500010. SEAP (Secretaria Especial de Pesca e Aquicultura da Presidência da República), IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis), 2006. Relatório final do projeto de monitoramento da atividade pesqueira no litoral do Brasil—Projeto STATPESCA. Brasília, p. 328. Semensato, X.E.G., Di Beneditto, A.P.M., 2008. Population dynamic and reproduction of Artemesia longinaris (Decapoda: Penaeidae) in Rio de Janeiro State, South-Eastern Brazil. Bol. Inst. Pesca 34, 89–98. Simões, S.M., D’Incao, F., Fransozo, A., Castilho, A.L., Costa, R.C., 2013. Sex ratio, growth and recruitment of the pelagic shrimp Acetes americanus on the southeastern coast of Brazil. J. Crustac. Biol. 33, 1–9. http://dx.doi.org/10.1163/1937240X-00002108. Somerton, D.A., 1980. A computer technique for estimating the size of sexual maturity in crabs. Can. J. Fish. Aquat. Sci. 37, 1488–1494. Sparre, P., Venema, S., 1997. Introdução à avaliação de mananciais de peixes tropicais. Doc. Technol. Pesca 306, 418. STATSOFT, 2011. Statistica: Data Analysis Software System, version 10.0. StatSoft, Tulsa, OK.
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9 Vogt, G., 2012. Ageing and longevity in the Decapoda (Crustacea): A review. Zool. Anz. 251, 1–25. http://dx.doi.org/10.1016/j.jcz.2011.05.003. Von Bertalanffy, L., 1938. A quantitative theory of organic growth (Inquities on growth laws II). Hum. Biol. 10, 181–213. Wenner, A.M., 1972. Sex ratio as a function of size in marine crustacean. Am. Nat. 383, 317–353.
9
Williams, A.B., 1984. Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, p. 550. Zar, J.H., 1999. Biostatistical Analysis. Pratice-Hall, Upper Saddle River, p. 929.
Contents lists available at ScienceDirect
Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma
Growth and reproduction of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) from the southeastern coast of Brazil Joyce Rocha Garcia a , Milena Regina Wolf a , Rogerio Caetano da Costa b , Antonio Leão Castilho a,∗ a
Study Group on Crustacean Biology, Ecology and Culture (NEBECC) – Zoology Department, Bioscience Institute, UNESP, 18618-000, Botucatu, Brazil
b
Laboratory of the Biology of Marine and Freshwater Shrimps (LABCAM) – Biological Sciences Department, Faculty of Sciences, UNESP, 17033-360, Bauru, Brazil
highlights • • • •
Non-selective trawls collect high diversity of shrimps as Rimapenaeus constrictus. Food availability for larval stages seems to be important for reproductive success. This species is in accordance with latitudinal pattern of reproduction. Growth rate and longevity are closely related.
article
info
Article history: Received 3 November 2015 Received in revised form 23 February 2016 Accepted 23 February 2016 Available online 2 March 2016 Keywords: Seasonality Subtropical region Roughneck-shrimp Match–mismatch theory
abstract Few studies have been performed on the shrimp Rimapenaeus constrictus, despite its wide geographic distribution in the western Atlantic Ocean. The population dynamics of R. constrictus were evaluated, focusing on sex ratios, growth, longevity, and reproduction, in the Cananeia region, along the southern coast of São Paulo state, Brazil. Monthly trawls were conducted from July 2012 through May 2014 using a shrimp boat outfitted with double-rig nets. The shrimp were identified according to their sex and reproductive condition, and carapace length (CL) was measured. A total of 1702 individuals were collected, and females were found to reach sexual maturity at a greater CL (9 mm) than males (7 mm). Based on the estimated growth curve parameters, males exhibit shorter longevity (0.73 years) than females (1.14 years). In terms of the sex ratio, there was a statistically significant bias toward females observed over the months, beginning at a CL of 9 mm (binomial test, p < 0.05). The seasonal reproductive pattern recorded during the spring and summer coincided with higher temperatures and chlorophyll concentrations (plankton production), which suggests that food availability for protozoeal and mysis larvae may be an important selective factor in the reproductive success of R. constrictus. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Penaeidae shrimps are of great economic importance in the Brazilian fishing industry; more than 53 thousand tons of crustaceans were caught in the country during 2005, more than 30 thousand tons of which consisted only of shrimps (SEAP and IBAMA, 2006). The majority of the shrimp catch in Brazil is obtained using non-selective trawls as fishing gear, resulting in the accidental extraction of bycatch fauna with a high biodiversity, as observed for the species Rimapenaeus constrictus (Stimpson, 1874)
∗
Corresponding author. Tel.: +55 14 38800645. E-mail address: [email protected] (A.L. Castilho).
http://dx.doi.org/10.1016/j.rsma.2016.02.006 2352-4855/© 2016 Elsevier B.V. All rights reserved.
in the Brazilian fauna (Neto, 2011; Costa and Fransozo, 2004a,b; Castilho et al., 2015). Fishing activity is considered to represent a complex situation because of the involvement of many sectors of interest, including the social, economic and environmental sectors. Therefore, the conception and implementation of an effective management plan in Brazil is difficult for both shrimps of economic importance to the industry and bycatch species. Thus, national organizations recognize the importance of understanding the life history of shrimps as an important tool for contributing to conservation planning in the future (Neto, 2011). However, studies on the reproductive biology of R. constrictus are scarce, with the available reports consisting of work by Costa and Fransozo (2004a), who clarified the temporal variation of the
2
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 1. Cananeia region, showing sampling stations in the adjacent oceanic area (I, II, III and IV) and estuarine area (Mar Pequeno—V, VI and VII).
spawning intensity and the recruitment of juveniles in the tropical region of Ubatuba in Brazil, and by Bauer and Lin (1994), who contributed information about the seasonal pattern of breeding in R. constrictus and Rimapenaeus similis (Smith, 1885) in a subtropical region in the United States. Other studies found in the literature that specifically address R. constrictus focused on its ecological distribution (Costa and Fransozo, 2004b; Hiroki et al., 2011). There are no studies on the growth and longevity of R. constrictus reported in the literature. Thus, the present study represents pioneering work on this subject. Such studies are important for the development of management plans for these shrimps, where the biological parameters obtained from the Von Bertalanffy (1938) growth model, associating individual size and age, provide estimates of mortality rates and longevity. The formulation of a mathematical model for age determination in crustaceans is of great importance, as crustaceans do not exhibit permanent bony structures; instead, the crustacean exoskeleton is periodically replaced in a process termed ecdysis, making evaluations based on periodic markings on their body surface impossible (Hartnoll, 2001; Keunecke et al., 2011; Castilho et al., 2015). This study aimed to investigate the reproductive biology, growth and longevity of the population of R. constrictus from Cananeia, along the southern coast of São Paulo state, Brazil. The reproductive aspects of the investigation included assessment of the sex ratio, the temporal variation of reproduction (continuous or seasonal) and juvenile recruitment, in comparison with the existing literature, as well as evaluation of the influence of several environmental factors (temperature, salinity and chlorophyll a concentration) on reproductive events.
oceanic area, using a shrimp boat equipped with double-rig nets to obtain biological material (Fig. 1). Samples were collected monthly from July 2012 through May 2014. A total of seven stations were previously selected to cover estuarine and oceanic areas of Cananeia, on the southern coast of São Paulo state. Depths were verified according to the bathymetric stratification described in nautical charts. During sampling, depth was monitored with a Eureka multiparameter probe. Four sampling stations were located in the oceanic area adjacent to the Cananeia region: stations I, II and III were positioned along the 10–15 m isobath and IV in the 5–10 m isobath. The other three sampling stations, V, VI and VII (5–10 m isobath), were located in the Mar Pequeno estuarine area, between Cananeia and Comprida Islands, which is influenced by fresh water from the complex estuarine–lagoon system of Cananeia-Iguape (Besnard, 1950).
2. Materials and methods
2.3. Reproduction
2.1. Sampling
Individuals were subjected to measurement of carapace length (CL: from the orbital angle to the posterior margin of the carapace) with a caliper and were classified by sex, according to the presence of a petasma, in males, or a thelycum, in females (Costa et al., 2003).
Trawls lasting 30 min were performed in the complex estuarine–lagoon system of Cananeia-Iguape and the adjacent
2.2. Bottom environmental parameters Environmental parameters, including temperature (°C), salinity and chlorophyll concentrations (µg/l), were measured with a Eureka multiparameter probe (Manta model 2-4.0) at each of the seven sampling stations. Temperature and salinity were registered from July 2012 through May 2014, whereas chlorophyll concentrations were measured from January through December 2013. Due to adverse environmental conditions in March 2013, samples were only collected at sampling stations V, VI and VII.
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
The stages of reproductive development were determined through macroscopic analysis of the male and female reproductive apparatuses. Female reproductive condition was assessed via macroscopic observation of the degree of ovarian development (according to color and the volume occupied by the gonads). Ovaries were categorized as immature (IM) if they varied from thin, transparent strands to thicker strands; as spent (SP) if they were white and much larger and thicker than those of immature females; as developed (DE) if they were light green; or as mature (MA) if they were green to dark green, occupying the entire dorsal portion of the abdomen as well as part of the carapace (more details in Costa and Fransozo, 2004a). In females, the presence of a sperm plug attached to the thelycum (inseminated females) was also observed macroscopically. Females with gonads in the SP, DE and MA stages were defined as adults, while those with gonads in the DE and MA stages were considered reproductive females, and those with gonads in the IM stage were defined as recruits. The reproductive period was determined based on the presence of reproductive females over the studied months (Castilho et al., 2008). Sexual maturity of male penaeids is usually indicated by fusion of the petasmal lobes (gonadal endopods), whereas immature males (IM) exhibit separated petasmal lobes (Boschi, 1989). The maturity of adult males was classified according to the development of spermatophores in the terminal ampoule (ejaculatory duct), which is convenient because spermatophores are visible through the exoskeleton (Chu, 1995). When spermatophores were not visible through macroscopic observation in an adult male, the individual was classified as lacking spermatophores (LS). If spermatophores were visible and occupied a portion of or all terminal ampoules, males were classified as spermatophore-bearing males (MA) (Castilho et al., 2012, 2015). Males with gonads in the LS and MA stages were defined as adults, while those with gonads in the MA stage were considered reproductive males, and those with gonads in the IM stage were defined as recruits. Size at sexual maturity was determined for males and females using the proportion of juvenile and adult individuals in 0.5 mmCL size classes. The procedure employed here to estimate sexual maturity was based on fitting a sigmoid logistic curve (Somerton, 1980). We used the equation y = 1/(1 + e(−r (CL − CL50 ))), where y is the estimated proportion of adult shrimps, CL50 is the carapace measurement at the onset of sexual maturity, and r is the coefficient for the slope of the logistic curve. The logistic curve was fitted via the least squares method to the previously indicated proportions for each size class of all individuals and samples using maximum-likelihood iterations. After adjusting the regression model, sexual maturity (CL50 ) was estimated as the size at which 50% of males and females reached maturity. All analyses of CL50 values were conducted in Microsoft Office Excel 2010. Juvenile recruitment was temporally characterized based on the frequency of immature individuals of both sexes in the population, whereas the beginning of sexual maturity was determined based on the length of the smallest adult individuals (Bauer, 1989). Due to the absence of reproductive individuals and inseminated females at sampling stations VI and VII, the statistical analyses were based only on the biological and environmental parameters recorded monthly at sampling stations I through V. For the statistical analysis, the assumption of normality was verified via the Shapiro–Wilk test. When the data were not distributed according to a Gaussian curve, they were logarithmically transformed (Log x + 1). All tests were performed with a significance level of 5% (Zar, 1999). The binomial test was used to estimate the sex ratios per month and per size class, and crosscorrelations were employed to evaluate the possible correlation of spermatophore-bearing males
3
with spent, inseminated or reproductive females. Crosscorrelations were also used to evaluate the correlation of the monthly abundance of reproductive females with recruits and with the mean values of temperature, salinity and chlorophyll concentrations by month. In crosscorrelations, two series of data are compared as a function of the time lag (n), using the Pearson correlation coefficient to measure relationships between values of the first data series and values of the second series from either earlier (in negative lags) or later months (in positive lags). Correlation coefficient values at lag 0 are equivalent to the standard Pearson correlation (STATSOFT, 2011). 2.4. Growth and longevity The population growth analyses for crustaceans were adapted from previous studies on fish and were based on mathematical models developed by Von Bertalanffy (1938), assuming that body length is a function of the age of individuals (Sparre and Venema, 1997). For the analysis of population growth, individuals were distributed into 0.5 mm-CL size classes in the analyzed time period, which allowed the identification of modes in the PeakFit 4.0 program (Automatic Peak Fitting Detection and Fitting, Method I—Residual, no Data Smoothing) (Fonseca and D’Incao, 2003). The obtained modes were plotted against time in a dispersion graph, from which it was possible to identify growth cohorts for males and females (Castilho et al., 2015). Posteriorly, three growth parameters were estimated with the Solver tool of Microsoft Office Excel for each identified cohort. The obtained parameters were based on the Von Bertalanffy growth model (VBGM) (1938): CLt = CLinf [1 − e − k(t −t0) ] and were as follows: (1) asymptotic length (CLinf ), which corresponds to the size reached by an individual if it grows indefinitely; (2) the growth coefficient (k), which is the rate at which the asymptotic length is reached; and (3) an adjusted parameter (t0 ), which corresponds to the theoretical age that the individual would exhibit at size zero. The seed values used to determine the parameters were the largest values of CL observed in this study for males (13.6 mm) and females (17.2 mm). Subsequently, the ages (in days) were corrected according to the time interval between the samples and the value obtained for t0 . From this, mean curves were constructed for males and females, which were compared by an F test (p = 0.05) (Cerrato, 1990). Longevity was estimated by the inverted VBGM with an adaptation suggested by D’Incao and Fonseca (1999): t max = (0 −(1 − k) ln(1 − CLt /CLinf )). The time that individuals take to reach sexual maturity and the minimal sizes of the recruitment cohorts were calculated according to the equation proposed by King (1995): t = t0 − (1/k) ln[1 − CL(m, s) /CLinf ], where k is the growth coefficient, CL is the size at sexual maturity (CLm ) or the size of the smaller individual (CLs ) and CLinf is the asymptotic length. 3. Results 3.1. Sex ratio A total of 1702 individuals were collected during the sampling period, among which 1276 were females, and 426 were males. At most time points, a bias toward females was observed, with females always showing a greater abundance than males (binomial test, p < 0.05) (Fig. 2). However, there was a trend toward sex ratios close to 50% up to a size of 8.5 mm; after this size, the sex ratio was biased in favor of females (Fig. 3).
4
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 2. Rimapenaeus constrictus. Monthly variation of the sex ratio (number of males /total number) from July 2012 through May 2014 in the Cananeia region. According to the binomial test, points below the 0.50 line represent significant deviation of the sex ratio in favor of females, and the points above this line represent significant deviation in favor of males.
Fig. 4. Rimapenaeus constrictus. Distribution of demographic categories of males and females among size classes from July 2012 through May 2014 in the Cananeia region (the categories are as follows: MA = mature males and females, SP = spent females, LS = spermatophore-lacking males, IM = immature males and females).
Fig. 3. Rimapenaeus constrictus. Variation of the sex ratio (number of males/total number) in relation to size classes from July 2012 through May 2014 in the Cananeia region. According to the binomial test, points below the 0.50 line represent significant deviation of the sex ratio in favor of females, and points above this line represent significant deviation in favor of males.
3.2. Reproduction and recruitment Males and females displayed different distributions in terms of size classes; most of the females were in the spent stage (10–10.5 mm), while most of the males were in the reproductive stage (8–8.5 mm) (Fig. 4). The largest size registered for females was 17.2 mm, whereas for males, it was 13.6 mm. The size at sexual maturity (CL50 ) was estimated at 8.2 mm for males and 10.5 mm for females (Fig. 4). Only the significant results from the crosscorrelation analysis are described: the number of spermatophore-bearing males was positively correlated with spent (R = 0.69; p = 0.0003) and inseminated (R = 0.51, p = 0.0135) females, with no time lag (lag = 0). Reproductive females were recorded in the spring, and their numbers peaked in October 2012 and in the summer, especially in February 2013 and January 2014, with lower abundance or a complete absence being observed in the colder months (autumn and winter). Immature individuals were distributed sparsely throughout the months of collection, especially in January 2013 and May 2014. In spite of the absence of a significant relationship between reproductive females and immature individuals (crosscorrelation, p > 0.05), the two highest peaks for immature individuals were found in January 2013 and May 2014, following the two highest peaks for reproductive females, in October 2012 and January 2014 (Fig. 5).
Fig. 5. Rimapenaeus constrictus. Monthly distribution of reproductive females and immature individuals from July 2012 through May 2014 in the Cananeia region.
No significant relationship was found between reproductive females and the chlorophyll concentration. However, reproductive peaks were observed in February, June and September, prior to periods with higher phytoplankton productivity in March, July and October–November (Fig. 6). 3.3. Growth and longevity Based on the growth analysis, 14 cohorts were identified for females and seven for males (Figs. 7 and 8). The calculated parameters revealed a CL∞ of 16.40 mm, k of 0.011 and t0 of −0.16 days for females and a CL∞ of 11.74 mm, k of 0.017 and t0 of −0.36 days for males. Females showed greater longevity than males, at 415 days (1.14 years) versus 267 days (0.73 years). The growth curves for males and females were significantly different (F critical = 2.70 < F calculated = 13.57; p = 2.09.10−7 ).
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 6. Rimapenaeus constrictus. Abundance of reproductive and inseminated females according to the chlorophyll concentration (µg/l) from July 2012 through May 2014.
Cohorts of small individuals (juvenile recruitment) were identified in January and April 2013 and May 2014 (Figs. 7 and 8). The minimal sizes of the recruitment cohorts were 4.97 mm (females— January 2013) and 5.82 mm (males—November 2012), corresponding to ages of 33 and 40 days, respectively. The proposed sizes at sexual maturity of 8.2 mm and 10.5 mm for males and females correspond to ages of 71 and 93 days, respectively. 4. Discussion In this study, it was observed that females reached larger sizes than males. According to Boschi (1989), this pattern is a general rule for penaeids and constitutes an important sexual dimorphism in these species. A larger size of females is an adaptation to increase egg production (Gab-Alla et al., 1990). Studies on R. constrictus and other penaeids have corroborated this dimorphism (Castilho et al., 2012, 2015; Costa and Fransozo, 2004a; Semensato and Di Beneditto, 2008; Simões et al., 2013). Thus, females reach sexual maturity later than males, which was confirmed in this species in a previous study in Ubatuba (Costa and Fransozo, 2004a) as well as among other species of penaeids (Castilho et al., 2012, 2015; Heckler et al., 2013; Semensato and Di Beneditto, 2008). The reproductive period of a marine species usually follows a latitudinal pattern, in which seasonal reproduction occurs in subtropical regions, and reproduction tends to be continuous in the tropics (Bauer, 1992); this pattern was also observed in the present study and has been previously described in the literature for R. constrictus. In the current study in Cananeia (a subtropical region), seasonal reproduction was observed, as reported by Bauer and Lin (1994) in the northern hemisphere (a subtropical region). In contrast, continuous reproduction was recorded in this species in a study performed on the northern coast of São Paulo state (latitude 23 ° S) (Costa and Fransozo, 2004a). Temperature is considered to be important factor in the maintenance of gametogenesis, which defines the reproductive period of a species (Bauer, 1992). In the present study, it was possible observe a significant relationship between an increased abundance of reproductive females and the hotter periods registered during the sampling periods (spring and summer). This means that temperature acts as an important factor in ovarian stimulation, as observed by Bauer and Lin (1994), Castilho et al. (2007, 2012, 2015) and Williams (1984), among others. The months with the greatest number of reproductive females preceded periods with the highest chlorophyll concentrations in the water column, suggesting that offspring in the larval stage (protozoeal and mysis larvae) will exhibit greater developmental success due to increased food availability (phytoplankton productivity), in accord with the match/mismatch theory proposed by Cushing (1975).
5
The positive correlation found between spermatophore-bearing males and spent and inseminated females corroborates the reproductive pattern described for species with a closed thelycum. According to Dall et al. (1990), insemination in closed thelycum species occurs immediately after ecdysis (i.e., in spent females). Therefore, it is expected that males ready for reproduction (spermatophore-bearing) and females ready for copulation (spent females) or inseminated females (suggesting that copulation has just occurred) will be observed at the same time. Juvenile recruitment of R. constrictus was discontinuous along the months, without significant relationship with reproductive females. Thus, recruitment could be considered as episodic, indicating a complex stock—recruitment relationship, as observed by Bauer and Lin (1994) and Costa and Fransozo (2004a) for the same species and by Castilho et al. (2007) for Artemesia longinaris Spence Bate, 1888. Several conditions can generate episodic recruitment, such as high variation in the mortality of planktonic larvae and early juvenile stages (Bauer, 1989), due to fluctuations in phytoplankton production (providing food for protozoeal and mysis larvae). In addition, the physical conditions of each region and the presence of predators might also satisfactorily explain episodic recruitment (Castilho et al., 2007). The longevity of shrimps observed in nature may be similar or different in the two sexes. For example, males and females of the species Pleoticus muelleri (Spence Bate, 1888) live for approximately two years, although females live slightly longer than males (Castilho et al., 2012). In contrast, in the case of Macrobrachium hainanense (Parisi, 1919), females live for 29 months, whereas males live for 48 months (Mantel and Dudgeon, 2005). Although the cited examples indicate that longevity in nature is variable in relation to the sex, it is very common in growth studies in penaeids to find that females present greater longevity than males (Campos et al., 2011; Castilho et al., 2012, 2015; Heckler et al., 2013), as observed in the present study. The discrepancy between sexes in terms of longevity could have many causes, such as differences in hormones and the cost of reproduction (Vogt, 2012). The mechanism underlying these differences is not well understood, but it is known that there is a huge advantage in the fitness of species when females live for longer periods, as a single female is capable of producing many eggs (Chacur and NegreirosFransozo, 1998), thus guaranteeing more efficient replacement of the population in association with greater longevity. Among penaeids, it is common for males to exhibit a higher growth rate (k) and a lower asymptotic length than females (Gulland and Rothschild, 1981; Petriella and Boschi, 1997); this difference was also observed in the present study. Since the early twentieth century, researchers have believed that high metabolic rates lead to cellular aging and, thus, decreased longevity (Pearl, 1928). It is thought that a greater growth investment in males (greater k than females) leads to higher metabolic rates, which culminate in decreased longevity and lower asymptotic lengths. The monthly sex ratio was skewed toward females, demonstrating that R. constrictus provides another exception to the rule proposed by Fisher (1930). A deviation in the sex ratio may be associated with the influence of factors such as migration and a differential mortality rate between sexes (Wenner, 1972). According to Gab-Alla et al. (1990), males tend to present a higher mortality rate than females, which contributes to the deviation of the sex ratio usually observed in marine crustaceans. Recent studies have demonstrated that the sex ratio is a function of individual size (Castilho et al., 2012; Heckler et al., 2013; Semensato and Di Beneditto, 2008; Simões et al., 2013), as observed in the present study. Males displayed a higher growth rate and lower asymptotic length than females, which contributed to the observed skewed sex ratio because the chance of finding a
6
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
Fig. 7. Rimapenaeus constrictus. Frequency distribution of the carapace length (CL) of females from July 2012 through May 2014 in the Cananeia region. The lines represent the cohorts identified during the sampling months (Cont. = Continuation).
male of a certain size was lower. The lower longevity of males is expected to be another factor related to the deviation of the sex ratio in the largest size classes.
Research conducted by Bauer (1992) could provide a hint about the latitudinal variation of the longevity of R. constrictus. This author proposed that growth and longevity in marine crustaceans
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
7
Fig. 8. Rimapenaeus constrictus. Frequency distribution of the carapace length (CL) of males from July 2012 through May 2014 in the Cananeia region. The lines represent the cohorts identified during the sampling months (Cont. = Continuation).
8
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9
follow a latitudinal pattern, based on the observation that shrimp species belonging to Sicyoniidae present greater longevity in subtropical and cold temperate regions compared with species in tropical regions. Cananeia is located in a subtropical region, and it is therefore possible to suggest that in future studies on R. constrictus from tropical regions, individuals will exhibit lower longevity in relation to that observed in the present research. Crustacean growth is generally strongly influenced by temperature. In ectothermic species (such as crustaceans), metabolic processes tend to increase with increasing temperature, speeding up the molting process, which culminates in an increase in growth rates (k) (Hartnoll, 2001). It is proposed here that the high average temperatures observed in the summers of 2013 and 2014 in the present study (over 25 °C) influenced the observed k for both males and females. Thus, R. constrictus presented a seasonal reproductive pattern and complex recruitment characteristics. It is believed that longevity and growth rates are closely related. However, further studies on the growth and longevity of this species in different locations are necessary for comparison and to achieve a better understanding of its population dynamics on a larger geographic scale. The influence of the chlorophyll concentration also requires further investigation, possibly involving larval stage collections. Moreover, temperature can be regarded as the most important factor in the reproduction and growth of this species. Acknowledgments The authors are indebted to the ‘‘Fundação de Amparo à Pesquisa do Estado de São Paulo’’ (FAPESP) for providing financial support for field collections, visiting activities and scholarships (2007/56733-5, 2010/50188-8, 2013/14174-0), CAPES CIMAR (N° 23038.004310/2014-85) and to CNPq (Research Scholarships PQ 305919/2014-8 and PQ 308653/2014-9). The authors thank many colleagues from the NEBECC group who helped with sampling and laboratory analyses and the ‘‘Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis’’ (IBAMA) for granting permission to collect the shrimp. References Bauer, R.T., 1989. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. J. Exp. Mar. Ecol. 127, 175–187. http://dx.doi.org/10.1016/0022-0981(89)90183-4. Bauer, R.T., 1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. J. Invertebr. Reprod. Dev. 22, 193–202. http://dx.doi.org/10.1080/07924259.1992.9672272. Bauer, R.T., Lin, J., 1994. Temporal patterns of reproduction and recruitment in populations of the penaeid shrimps Trachypenaeus similis (Smith) and T. constrictus (Stimpson) (Crustacea: Decapoda) from the Northcentral Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 185, 205–222. http://dx.doi.org/10.1016/00220981(94)90052-3. Besnard, W., 1950. Considerações gerais em torno da região lagunar de CananéiaIguape I. Bol. Inst. Paul. Oceanogr. 1, 9–26. http://dx.doi.org/10.1590/S010042391950000200001. Boschi, E.E., 1989. Biología pesquera del langostino del litoral patagonico de Argentina. Inst. Nac. Desarro. Pesq. (INIDEP). Campos, B.R., Branco, J.O., D’Incao, F., 2011. Crescimento do camarão-sete-barbas (Xiphopenaeus kroyeri (Heller 1862)), na baía de Tijucas, Tijucas, SC (Brasil). Atlântica 33, 201–208. Castilho, A.L., Bauer, R.T., Freire, F.A.M., Fransozo, V., Costa, R.C., Grabowski, R.C., Fransozo, A., 2015. Lifespan and reproductive dynamics of the commercially important sea bob shrimp Xiphopenaeus kroyeri (Penaeoidea): synthesis of a 5-year study. J. Crustac. Biol. 35, 30–40. http://dx.doi.org/10.1163/1937240X00002300. Castilho, A.L., Costa, R.C., Fransozo, A., Boschi, E.E., 2007. Reproductive pattern of the South American endemic shrimp Artemesia longinaris (Decapoda, Penaeidae), off the coast of São Paulo state, Brazil. Rev. Biol. Trop. 55, 39–48. http://dx.doi.org/10.15517/rbt.v55i0.5804. Castilho, A.L., Costa, R.C., Fransozo, A., Negreiros-Fransozo, M.L., 2008. Reproduction and recruitment of the South American red shrimp, Pleoticus muelleri (Crustacea: Solenoceridae), from the southeastern coast of Brazil. Mar. Biol. Res. 4, 361–368. http://dx.doi.org/10.1080/17451000802029536.
Castilho, A.L., Wolf, M.R., Simões, S.M., Bochini, G.L., Fransozo, V., Costa, R.C., 2012. Growth and reproductive dynamics of the South American red shrimp, Pleoticus muelleri (Decapoda: Solenoceridae), from the Southeastern coast of Brazil. J. Mar. Syst. 105, 135–144. http://dx.doi.org/10.1016/j.jmarsys.2012.07.004. Cerrato, R.M., 1990. Interpretable statistical tests for growth comparisons using parameters in the von Bertalanffy equation. Can. J. Fish. Aquat. Sci. 47, 1416–1426. http://dx.doi.org/10.1139/f90-160. Chacur, M.M., Negreiros-Fransozo, M.L., 1998. Aspectos biológicos do camarãoespinho Exhippolysmata oplophoroides (Holthuis, 1948) (Crustacea, Caridea, Hippolytidae). Rev. Bras. Biol. 59, 173–181. http://dx.doi.org/10.1590/S003471081999000100022. Chu, K.H., 1995. Aspects of reproductive biology of the shrimp Metapenaeus joyneri from the Zhujiang Estuary, China. J. Crustac. Biol. 15, 214–219. http://dx.doi.org/10.1163/193724095X00226. Costa, R.C., Fransozo, A., 2004a. Reproductive biology of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) in the Ubatuba region of Brazil. J. Crustac. Biol. 24, 274–281. http://dx.doi.org/10.1651/C-2437. Costa, R.C., Fransozo, A., 2004b. Abundance and ecologic distribution of the shrimp Rimapenaeus constrictus (Crustacea: Penaeidae) on the Northern coast of São Paulo State, Brazil. J. Nat. Hist. 38, 901–912. http://dx.doi.org/10.1080/0022293021000046441. Costa, R.C., Fransozo, A., Melo, G.A.S., Freire, F.A.M., 2003. Chave ilustrada para identificação dos camarões dendrobranchiata do litoral norte do estado de São Paulo, Brasil. Biota Neotrop. 3, 1–12. http://dx.doi.org/10.1590/S1676-06032003000100011. Cushing, D.H., 1975. Marine Ecology and Fisheries. Cambridge University Press, Great Britain, p. 278. Dall, W., Hill, B.J., Rothlisberg, P.C., Staples, D.J., 1990. The biology of the Penaeidae. In: Blaxter, J.H.S., Southward, A.J. (Eds.), Advances in Marine Biology, Vol. 27. Academic Press, San Diego, p. 489. D’Incao, F., Fonseca, D.B., 1999. Performance of the von Bertalanffy growth curve in penaeid shrimps: a critical approach. In: Proceedings of the Fourth International Crustacean Congress. Amsterdam, Netherlands, pp. 733–737. Fisher, R.A., 1930. The Genetical Theory of Natural Selection. New York Dover Publications, New York, p. 318. Fonseca, D.B., D’Incao, F., 2003. Growth and reproductive parameters of Kalliapseudes schubartii in the estuarine region of the Lagoa dos Patos (southern Brazil). J. Mar. Biol. Assoc. UK 83, 931–935. Gab-Alla, A.A.F.A., Hartnoll, R.G., Ghobashy, A.F., Mohammed, S.Z., 1990. Biology of penaeid prawns in the Suez Canal Lakes. Mar. Biol. 107, 417–426. http://dx.doi.org/10.1007/BF01313423. Gulland, J.A., Rothschild, B.J., 1981. Penaeid Shrimps: Their Biology and Management. Fishing News Books, Farnham, p. 312. Hartnoll, R.G., 2001. Growth in Crustacea—Twenty years on. Hydrobiologia 449, 111–122. http://dx.doi.org/10.1023/A:1017597104367. Heckler, G.S., Simões, S.M., Santos, A.P.F., Fransozo, A., Costa, R.C., 2013. Population dynamics of the seabob shrimp Xiphopenaeus kroyeri (Dendrobranchiata, Penaeidae) in south-eastern Brazil. Afr. J. Mar. Sci. 35, 17–24. http://dx.doi.org/10.2989/1814232X.2013.769901. Hiroki, K.A.N., Fransozo, A., Costa, R.C., Castilho, A.L., Shimizu, R.M., Almeida, A.C., Furlan, M., 2011. Bathymetric distribution of the shrimp Rimapenaeus constrictus (Stimpson, 1874) (Decapoda, Penaeidae) in two locations off the southeastern Brazilian coast. Mar. Biol. Res. 7, 176–185. http://dx.doi.org/10.1080/17451000.2010.489614. King, M., 1995. Fisheries Biology, Assessment and Management. Fishing News Books, Cambridge, p. 341. Keunecke, K.A., D’Incao, F., Moreira, F.N., Silva Jr, D.R., Verani, J.R., 2008. Idade e crescimento de Callinectes danae e C. ornatus (Crustacea, Decapoda) na Baía de Guanabara, Rio de Janeiro, Brasil. Iheringia, Sér. Zool 98, 231–235. Mantel, K.S., Dudgeon, D., 2005. Reproduction and sexual dimorphism of the palaemonid shrimp Macrobrachium hainanense in Hong Kong streams. J. Crustac. Biol. 25, 450–459. http://dx.doi.org/10.1651/C-2541. Neto, J.D., 2011. Proposta de plano nacional de gestão para o uso sustentável de camarões marinhos do Brasil. Brasília: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis e Ministério do Meio Ambiente. Pearl, R., 1928. The Rate of Living. Knopf, New York, p. 167. Petriella, A.M., Boschi, E.E., 1997. Crecimiento en crustáceos decápodos: resultados de investigaciones realizadas en Argentina. Rev. Investig. Mar. 25, 135–157. http://dx.doi.org/10.4067/S0717-71781997002500010. SEAP (Secretaria Especial de Pesca e Aquicultura da Presidência da República), IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis), 2006. Relatório final do projeto de monitoramento da atividade pesqueira no litoral do Brasil—Projeto STATPESCA. Brasília, p. 328. Semensato, X.E.G., Di Beneditto, A.P.M., 2008. Population dynamic and reproduction of Artemesia longinaris (Decapoda: Penaeidae) in Rio de Janeiro State, South-Eastern Brazil. Bol. Inst. Pesca 34, 89–98. Simões, S.M., D’Incao, F., Fransozo, A., Castilho, A.L., Costa, R.C., 2013. Sex ratio, growth and recruitment of the pelagic shrimp Acetes americanus on the southeastern coast of Brazil. J. Crustac. Biol. 33, 1–9. http://dx.doi.org/10.1163/1937240X-00002108. Somerton, D.A., 1980. A computer technique for estimating the size of sexual maturity in crabs. Can. J. Fish. Aquat. Sci. 37, 1488–1494. Sparre, P., Venema, S., 1997. Introdução à avaliação de mananciais de peixes tropicais. Doc. Technol. Pesca 306, 418. STATSOFT, 2011. Statistica: Data Analysis Software System, version 10.0. StatSoft, Tulsa, OK.
J.R. Garcia et al. / Regional Studies in Marine Science 6 (2016) 1–9 Vogt, G., 2012. Ageing and longevity in the Decapoda (Crustacea): A review. Zool. Anz. 251, 1–25. http://dx.doi.org/10.1016/j.jcz.2011.05.003. Von Bertalanffy, L., 1938. A quantitative theory of organic growth (Inquities on growth laws II). Hum. Biol. 10, 181–213. Wenner, A.M., 1972. Sex ratio as a function of size in marine crustacean. Am. Nat. 383, 317–353.
9
Williams, A.B., 1984. Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, p. 550. Zar, J.H., 1999. Biostatistical Analysis. Pratice-Hall, Upper Saddle River, p. 929.