THE SIZE AT MATURITY OF THE BROWN CRAB CALLINECTES BELLICOSUS (DECAPODA, PORTUNIDAE) IN THE GULF OF CALIFORNIA

Crustaceana 85 (12-13) 1513-1523 THE SIZE AT MATURITY OF THE BROWN CRAB CALLINECTES BELLICOSUS (DECAPODA, PORTUNIDAE) IN THE GULF OF CALIFORNIA BY GUILLERMO RODRÍGUEZ-DOMÍNGUEZ 1,2 ), SERGIO G. CASTILLO-VARGASMACHUCA 1 ), RAÚL PÉREZ-GONZÁLEZ 2 ) and E. ALBERTO ARAGÓN-NORIEGA 3,4 ) 1 ) Posgrado en Ciencias Biológico Agropecuarias, Universidad Autónoma de Nayarit, Carretera Tepic-Compostela Km 9 Xalisco, Nayarit 63780, Mexico 2 ) Laboratorio Manejo de Zona Costera, Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Paseo Claussen S/N, Mazatlán, Sinaloa 82000, Mexico 3 ) Unidad Sonora del Centro de Investigaciones Biológicas del Noroeste, Km 2.35 Camino al Tular, Estero de Bacochibampo, Guaymas, Sonora 85454, Mexico ABSTRACT This study describes the size (carapace width, CW) at maturity of Callinectes bellicosus (Stimpson, 1859) based on samples from a coastal lagoon in the southern Gulf of California. The study was conducted since knowledge of the species in particular and the genus in general on the Pacific coast is scarce or non-existent and size at maturity is a key biological parameter for fisheries management. The collection of statistics on the crab fishery began in 1982, but landings of crab from the fishery increased exponentially until 2003. Samples were collected at the mouth of the lagoon and in the inside lagoon. A total of 651 brown crabs, including 255 females and 396 males, were processed from both sites. The crabs from the coastal lagoon showed a marked segregation of the sexes. In all, 73% of the crabs from the inside lagoon were males, and 71% of the crabs from the mouth of the lagoon were females. Immature females were predominant (78% of all females) in the inside lagoon, whereas mature females were predominant (81% of all females) at the mouth of the lagoon. Segregation according to the size at maturity was observed. The size at maturity was greater in the inside lagoon (114.08 mm CW) than at the mouth of the lagoon (103.73 mm CW). The pooled size at maturity was 107.78 mm CW. This report presents the first information onsegregationbysexandmaturitystageinanycallinectes species from the Mexican Pacific coast. These findings are important not only for fisheries management but also for the general biological knowledge of Callinectes species. We concluded that this study offers an improved approach for evaluating fisheries management, at least for the species studied here. 4 ) Corresponding author; Fax: (52-622) 221-2238; e-mail: aaragon04@cibnor.mx Koninklijke Brill NV, Leiden, 2012 DOI:10.1163/156854012X651600

1514 GUILLERMO RODRÍGUEZ-DOMÍNGUEZ ET AL. RESUMEN El estudio describe la talla (longitud del caparazón, LC) de primera madurez de Callinectes bellicosus (Stimpson, 1859) de muestras tomadas en una laguna costera de la región sur del Golfo de California. El estudio fue motivado ya que el conocimiento es muy escaso sobre la especie en particular, y en general para el género en toda la costa del Pacífico. La talla de primera madurez, en particular, es un factor clave para el manejo de pesquerías. El registro de las estadísticas pesqueras inició desde 1982, pero fue hasta 2003 cuando la producción tuvo un incremento exponencial. Se recolectaron muestras en dos sitios ; al interior y en la boca de la laguna. Se capturaron un total de 625 jaibas de las cuales 255 fueron hembras y 396 machos. Se observó una marcada segregación entre sexos ; en el interior de la laguna el 73% del total fueron machos y 71% hembras del total en la boca de la laguna. Del total de hembras se encontró que las del interior de la laguna el 78% estaban inmaduras, mientras que en la boca de la laguna el 81% estaban maduras. También se observó segregación en cuanto a tallas, la talla de primera madurez en el interior de la laguna fue de 114,08 mm LC, mientras que en la boca de la laguna fue de 103,73 mm LC. Combinando los datos de ambos sitios se encontró una talla de primera madurez de 107,78 mm LC. Los resultados de este estudio son importantes tanto para el manejo pesquero como para en conocimiento de la biología general de las especies del género Callinectes. La conclusión de este estudio es que se ofrece una oportunidad de mejora para evaluar el manejo pesquero actual de esta especie. INTRODUCTION The population biology of eastern Pacific swimming crabs (Brachyura, Portunidae) belonging to the genus Callinectes is poorly documented. This lack of knowledge has important practical implications, because since 1982 Callinectes bellicosus (Stimpson, 1959) has become the focus of an important commercial fishery in Mexico, especially in the eastern Gulf of California, where a small-scale fishery for these crabs has been established. The coastal lagoon of Santa María La Reforma is included in this area. The brown crab C. bellicosus has different local common names that include jaiba café, jaiba verde and jaiba guerrera ; the approximate translation into English is brown crab (as we use in this study), green crab and warrior crab, respectively. Most of the studies have been conducted on Atlantic coastal species (Williams, 1974). This knowledge has been adapted to develop several strategies to manage the Pacific crab fishery (e.g., first size at capture for fishery crabs species in Mexican Pacific coast to assure enough broodstock in the wild population). Our search of the existing literature primarily found government reports and located only three formal papers that focused on C. bellicosus.all of these papers reported research conducted in estuarine lagoons along the Pacific coast (Paul, 1982; Arreola-Lizárraga et al., 2003; Hernández & Arreola-Lizárraga, 2007). Crabs of the genus Callinectes are found in estuaries and coastal lagoons on the Pacific coast of the Americas from Los Angeles, California to south Peru (Williams, 1974). This exploited population might be expected to receive significant attention as an object of marine biological research, but this is not the

MATURITY OF CALLINECTES BELLICOSUS IN THE GULF OF CALIFORNIA 1515 case. Fisheries management demands knowledge of many aspects of population biology. These aspects include the reproductive characteristics of the population. Spawning is the basic renewal mechanism for a fishery resource and the basis for the conservation of the stock. Studies of the reproduction of exploited crab populations are critical for developing management strategies. The core tactic is to protect the reproductive season and the reproductive areas and to allow females to reproduce at least once before being caught. To allow the individual to reproduce at least once before entering the fishery, knowledge of the size at maturity is essential because data on the size at maturity can be used to establish the minimum legal size of the crab to be fished. If catches target individuals of sizes smaller than the size at first maturity and, in case of intense fishing, recruitment overfishing will result. If recruitment overfishing occurs, it is probable that the recovery of the population will encounter serious problems. Cushing (1988) documents several fish pelagic stocks which collapsed because catches of immature fish played an important part in generating recruitment overfishing, like herring fisheries in North Sea, the Norwegian Sea and Northwest Atlantic Sea. The purpose of this investigation is to determine the size at maturity of the brown crab C. bellicosus in a coastal lagoon in the Gulf of California. MATERIAL AND METHODS Study area The Santa María la Reforma lagoon-estuarine system is located on the continental shelf of the central Mexican Pacific. It is a type IIIA, inside-shelf coastal lagoon (Lankford, 1977) with mangrove vegetation. Water temperature in the lagoon reaches its maximum in August (31.0 C) and minimum in December (20.1 C) but can be as low as 17.5 C as in year 2008 (Flores-Cárdenas, 2011). During our study we recorded temperatures of 25.7 C and 26.2 C in May and June, respectively. During our study the salinity ranged from 25.1 to 38.6. The maximum depth of the lagoon is 24 m, and the mean depth is 7 m. The lagoon connects with the Pacific Ocean through two 5-km wide channels with depths of 12-17 m (fig. 1). Biological sampling Crabs were collected with ring nets by small commercial fishing vessels. A technician was always present on these small vessels to ensure that the data for this study were collected. The collection period was May and June, the middle of the reproductive season. Ramírez-Felix (2003) mentioned that reproductive period of Callinectes bellicosus off Sinaloa is from April to August, so we decided to

1516 GUILLERMO RODRÍGUEZ-DOMÍNGUEZ ET AL. Fig. 1. Study area. Santa María La Reforma Coastal Lagoon, Sinaloa, Mexico. sample only those two months because the objective of the study was only to determine the size at maturity. Samples were collected at two different locations: the inside lagoon and the mouth of the lagoon of the Bahía Santa María la Reforma (fig. 1). The sex, gonad maturity and carapace width (CW), measured as the distance between the tips of the longest lateral spines, were registered for each specimen. The degree of gonad maturity was classified according to six phases (phase I, immature juvenile; phase II, fecund adults without external eggs; phase III, yellow external eggs; phase IV, orange external eggs; phase V, brownish-grey or black external eggs; and phase VI, vestiges of eggs in black filaments). For this study, we grouped the organisms into immature (phase I) and mature (phases II, III, IV, V and VI) groups. Data analysis The maturity rates were adjusted with a logistic model as follows: ( ) 1 MR j = 1 + e (CW j CW 50% )/φ where MR j is the maturity rate in CW interval j,cw j is the mean carapace width in interval j, CW 50% is the carapace width at maturity and φ is a parameter of the model.

MATURITY OF CALLINECTES BELLICOSUS IN THE GULF OF CALIFORNIA 1517 Nonlinear estimates of CW 50% and φ were calculated with an iterative procedure in which the Newton algorithm was used to maximize the sum of the binomial distribution: k (( ) ) nj ln MR mf j mf j (1 MR j ) n j mf j j j=1 where n j is the total number of females in the j-th CW interval and mf j the number of mature females in th j-th CW interval. The likelihood profile was used to estimate the confidence interval for the size at maturity (Venzon & Moolgavkar, 1988). The confidence interval for the θ parameter was estimated based on the chi-squared distribution. The confidence interval was defined as all values of θ that satisfy the inequality 2(L(Y/θ) L(Y/θ best )) < χ 2 1,1 α where L(Y/θ best ) is the negative log-likelihood of the most likely value of θ and χ 2 1,1 α are the values of χ 2 with 1 degree of freedom at a confidence level of 1 α. Thus, the 95% confidence interval for θ encompasses all values of θ that are twice the difference between the negative log-likelihood and the overall negative loglikelihood of the best estimate of θ that is less than 3.84 for the parameter (Haddon, 2001). The likelihood profile shape was estimated for the θ i that generates a negative log-likelihood equal to the maximum negative log-likelihood L(Y/θ best ) minus half the required χ 2 value (3.84/2). The estimator is: L(Y/θ) = L(Y/θ best ) χ2 1,1 α 2 RESULTS A total of 651 brown crabs sampled in two zones: inside the lagoon and at the mouth of the lagoon, were processed in this study. This total included 255 females and 396 males. The crabs from the coastal lagoon showed a marked segregation of the sexes: 73% were males (fig. 2A), whereas 71% of the crabs from the mouth of the lagoon were females (fig. 2B). Immature females were predominant in the lagoon (78% of total females, fig. 2A), while mature females were predominant at the mouth of the lagoon (81% of total females, fig. 2B). The carapace-width (CW) frequency distributions of females from both sampling zones are shown in fig. 2A-C. Mature female frequency showed a peak at 115 mm CW in both zones, but the CW range was wider at the mouth of the lagoon than in the inside lagoon (fig. 2A-B). The segregation by sex observed in the lagoon was similar to the segregation by size shown by the females. The immature

1518 GUILLERMO RODRÍGUEZ-DOMÍNGUEZ ET AL. Fig. 2. CW structure of crab females of Callinectes bellicosus (Stimpson, 1859) collected at the inside area (A) and the mouth (B) of Santa Maria lagoon, and pooled samples (C). In the circular plot: proportions of the sexes and maturity stages of females. females showed a peak frequency at 105 mm CW inside the lagoon and 95 mm CW at the mouth of the lagoon. Another form of segregation was shown by the size at maturity (measured as carapace width). The size at maturity was larger in the inside lagoon (114.08 mm) than at the mouth of the lagoon (103.73 mm). Table I shows the size at maturity at TABLE I Estimated size at maturity (carapace width) and confidence interval for Callinectes bellicosus (Stimpson, 1859) in a coastal lagoon in the Gulf of California Source Size at maturity (CW) LL 95% UL 95% Inside lagoon 114.08 112.3 115.9 Mouth of lagoon 103.73 102.9 104.4 Pooled sample 107.78 106.5 109.1

MATURITY OF CALLINECTES BELLICOSUS IN THE GULF OF CALIFORNIA 1519 Fig. 3. Size at first maturity (carapace width) of brown crab females Callinectes bellicosus (Stimpson, 1859) collected at the inside area and the mouth of Santa Maria coastal lagoon in the Gulf of California. both sites and the upper and lower limits of the 95% confidence interval. Table I also shows that the size at maturity for the pooled samples was 107.78 mm. Fig. 3 shows the curves for the maturity rates for both sites and the pooled samples. Fig. 3 highlights the size at which 50% of the females are mature. The likelihood profiles and χ 2 probabilities are shown in fig. 4. DISCUSSION The knowledge of the size of crabs at first maturity is very important in fisheries management. The average or expected size at first maturity is usually estimated fitting a logistic model to the proportion of mature females by size interval. The Fig. 4. Likelihood profiles for size at maturity (carapace width) of brown crab females Callinectes bellicosus (Stimpson, 1859) collected at inside area and mouth of Santa Maria coastal lagoon in the Gulf of California. The solid line represents the negative log-likelihood profiles and the dashed line the chi-squared probability.

1520 GUILLERMO RODRÍGUEZ-DOMÍNGUEZ ET AL. fitted logistic regression can then be assumed to represent a cumulative distribution function, and the expected size at first maturity corresponds to 50% probability. Studies for other economically important species, such as shrimp (Aragón- Noriega & Alcántara-Razo, 2005) have yielded abundant biological information. Surprisingly, published biological information is scarce for crabs, although the commercial catch has increased to 16 000 metric tons in the Gulf of California alone. Callinectes bellicosus represents 13 680 metric tons of this total. No peerreviewed papers have previously addressed the size at first maturity in this species. Certain information about size at maturity in the congener Callinectes arcuatus (Ordway, 1863) is available. Fisher & Wolff (2006) found that the size at maturity of the males of this species was 94.3 mm. However, they found it difficult to obtain data on females from commercial sources of data on this crab. This problem with data sources was cited by Hernández & Arreola-Lizárraga (2007), who found a value of 75 mm for the mean size at maturity of females. This value was not in agreement with the value of 59.4 mm for the size at first maturity reported by Nevarez-Martínez et al. (2003). This discrepancy was explained by the difference in data sources. Hernández & Arreola-Lizárraga (2007) used a trawling net in non-commercial areas, whereas Nevarez-Martínez et al. (2003) used only data from the commercial fleet on crabs caught in traps. We emphasize this point because we decided to sample at the mouth of the lagoon, where no commercial activities occur, and in the inside lagoon, where commercial activities are conducted. We found segregation by sex in the lagoon. The inside lagoon was dominated by males, a result similar to that reported by Fisher & Wolff (2006) for the congener Callinectes arcuatus in Costa Rica. Those studies that relied on traps and commercial sites may obtain size-frequency distributions that include a bias. In summary, we advise caution regarding the type of collection and the site of the collection for a study of this topic. For this study, the collections were concentrated in the middle period of the reproductive season, which corresponded to the maximum percentage of mature females. The samples included a site different from that at which the commercial fishery operated, and different sampling gear was used. Previous non-peer-reviewed documents (Ayala-Cota & Espinoza-Cruz, 2001; Ramírez-Félix et al., 2003) reported a value of 115 mm CW for the size at first maturity of C. bellicosus in a coastal lagoon of the Gulf of California. This value is similar to that found in the inside lagoon in this study. We captured mature females at the mouth of the lagoon and in the inside lagoon. Our data from the inside lagoon are consistent with the value of 115 mm CW for the size at first maturity of C. bellicosus reported by previous studies. To our knowledge, our report is the first to present data on segregation by sex and stage of maturity in any Callinectes species from the Mexican Pacific coast. These findings are important not only for fisheries management but also for the general biological knowledge of Callinectes species. Callinectes bellicosus matures at a larger size than its

MATURITY OF CALLINECTES BELLICOSUS IN THE GULF OF CALIFORNIA 1521 most commercially important congener, C. arcuatus, which matures at 95 mm CW (Fisher & Wolff, 2006). This variability in size at maturity is a direct reflection of the differences in the growth rates of the species. Ramírez-Félix et al. (2003) reported the growth parameters of both species for the entire Mexican Pacific coast. These authors used the Von Bertalanffy growth model (VBGM) for their analyses. The smallest k and L parameters of the VBGM for C. bellicosus (3.5 and 149, respectively) exceed the largest k and L parameters of the VBGM for C. arcuatus (2.5 and 142, respectively). Growth rates can also vary due to differences in the water temperature among regions. However, the differences in the growth rates and the size at maturity between C. bellicosus and C. arcuatus cannot be easily explained by temperature differences because these two species share the same range along the Mexican Pacific coast. The limited knowledge of the biology of crab species from this region makes comparisons more complicated. Comparisons of the size at maturity of shrimp of the Gulf of California region (Aragón-Noriega & Alcántara-Razo, 2005) showed the effect of the sea surface temperature (SST) on the maturity period and the size at maturity. This finding is relevant to the current study because Aragón-Noriega & Alcántara-Razo (2005) found that higher latitudes and a lower average annual SST corresponded to a shorter maturity period and a larger size at maturity. However, the only report of the size at maturity of C. bellicosus found at higher latitudes and lower average annual SST (Nevarez-Martínez et al., 2003) presents a contradictory result. Nevarez-Martínez et al. (2003) reported a size at first maturity of 59.4 mm CW. This value differs substantially from our results, as we found a size at first maturity of 115 mm CW for the inside lagoon and a value of 103.7 mm CW for the mouth of the lagoon. We interpret this discrepancy as a reflection of a methodological bias, but other factors, such as temperature, might also influence results; in addition, size at first maturity might be a variable parameter, as in other marine organisms. We do not suppose that Callinectes spp. represent the only group of marine animals that fail to follow the paradigm outlined by Kinne (1970): Thermal requirements for reproduction often are restricted to a narrow temperature window separating growth from the reproductive temperature range. It is important for fisheries management to recognize the findings of this study and to consider a value of 107.78 mm CW as the size at first maturity of C. bellicosus from the lagoon investigated by this research. Of course, it is also necessary to review previous reports (e.g., Nevarez-Martínez et al., 2003), in which a value of 59.4 mm CW is reported for the size at first maturity. Other reports must be reviewed to evaluate the methods used to collect the raw data. It is most important to complete the knowledge of Callinectes spp. on the Pacific coast to contribute to the general knowledge of crustaceans and to fisheries management, thereby enhancing the sustainability of fisheries worldwide. We concluded that the

1522 GUILLERMO RODRÍGUEZ-DOMÍNGUEZ ET AL. information on segregation by size at maturity and by sex found by this study can be used to facilitate an improved approach to evaluate the management of fisheries, at least for the species studied here. ACKNOWLEDGEMENTS G.R.D. thanks the Universidad Autónoma de Sinaloa for financial support (PROFAPI 2011) and the fishermen from La Reforma for logistic support and administrative data. E.A.A.N. received financial aid from CIBNOR s fisheries ecology programme EP0.1. REFERENCES ARAGÓN-NORIEGA, E. A.& E. ALCÁNTARA-RAZO, 2005. Influence of sea surface temperature on reproductive period and size at maturity of the brown shrimp (Farfantepenaeus californiensis) in the Gulf of California. Marine Biology, 146(2): 373-379. ARREOLA-LIZÁRRAGA, J.A.,L.G.HERNÁNDEZ-MORENO, S.HERNÁNDEZ-VÁZQUEZ, F.J. FLORES-VERDUGO, C. LECHUGA-DEVEZÉ & A. ORTEGA-RUBIO, 2003. Ecology of Callinectes arcuatus and C. bellicosus (Decapoda: Portunidae) in a coastal lagoon of northwest Mexico. Crustaceana, 76: 651-664. AYALA-COTA, F. J.& L. J. ESPINOZA-CRUZ, 2001. Parámetros poblacionales de la jaiba café Callinectes bellicosus (Stimpson, 1859) en la Bahía Santa María de la Reforma: 1-35. (B.Sc. Thesis, Universidad Autónoma de Sinaloa, Mazatlán, Mexico). CUSHING, D., 1988. The provident sea: 1-329. (Cambridge University Press, Cambridge). FISCHER, S. & M. WOLFF, 2006. Fisheries assessment of Callinectes arcuatus (Brachyura, Portunidae) in the Gulf of Nicoya, Costa Rica. Fisheries Research, 77: 301-311. FLORES-CÁRDENAS, F., 2011. Vulnerabilidad del Sistema Lagunar Santa María-La Reforma (Sinaloa) asociada a las dimensiones humanas y variabilidad climática: 1-66. (M.Sc. Thesis, Universidad Autónoma de Sinaloa, Mazatlán, Mexico). HADDON, M., 2001. Modelling and quantitative methods in fisheries: 1-406. (Chapman & Hall/CRC, Boca Raton, FL). HERNÁNDEZ, L.& J. A. ARREOLA-LIZÁRRAGA, 2007. Estructura de tallas y crecimiento de los cangrejos Callinectes arcuatus and C. bellicosus (Decapoda: Portunidae) en la laguna costera Las Guásimas, México. Revista de Biología Tropical, 55(1): 225-233. KINNE, O., 1970. Marine ecology-a comprehensive, integrated treatise on life in the oceans and coastal waters, 1: Environmental factors: 1-1774. (John Wiley & Sons, New York, NY). LANKFORD, R. R., 1977. Coastal lagoons of Mexico: their origin and classification. In: M. WILEY (ed.), Estuarine processes, circulation, sediments and transfer of materials in the estuary: 182-215. (Academic Press, New York, NY). NEVÁREZ-MARTÍNEZ, M. O., J. LÓPEZ-MARTÍNEZ, C. CERVANTES-VALLE, E. MIRANDA- MIER, R.MORALES-AZPEITIA &M.L.ANGUIANO-CARRASCO, 2003. Evaluación biológica y pesquera de las jaibas Callinectes bellicosus y Callinectes arcuatus (Brachyura: Decapoda: Portunidae) en las bahías de Guásimas y Lobos, Sonora, México. In: M. E. HEN- DRICKX (ed.), Contributions to the study of East Pacific crustaceans, 2: 125-138. (Instituto de Ciencias del Mar y Limnología, UNAM, Mazatlán, Mexico).

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