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Application of an egg production index to determine reproductive period of the brown shrimp Farfantepenaeus californiensis near Agiabampo, Sonora-Sinaloa, Mexico.

ABSTRACT Using the percentage of mature females as an index, the reproductive period of the brown shrimp, Farfantepenaeus californiensis, off the coast of Sonora in Mexico, has been shown to occur throughout the year with two peaks of mass spawning. The objective of this study is to determine if a similar reproductive period occurred off Agiabampo, at the Sonora-Sinaloa border. By combining 3 indices of mature females: size structure, abundance and fecundity at size, a single egg production index (EPI) was calculated. Monthly samples from January through December 2002 were collected during 5 continuous days around the full moon (full moon [+ or -] 2 days). Trawl net tows were used at depths from 1-9 m, 2 km north and south of the mouth of a coastal lagoon. Using the EPI, a single reproductive peak, May to August, was found, with May as the most important egg production mouth. On the other hand, the percentage of mature females showed a two peak reproductive period, one more intensive from May to August and the second one less intensive in November. We concluded that the best determination of the reproductive period of the brown shrimp required the use of three indices. Particularly off Agiabampo, this species has a well-defined reproductive period with just one massive spawning peak.

KEY WORDS: reproductive cycle, egg production index, shrimp, Farfantepenaeus californiensis, Gulf of California, Agiabampo

INTRODUCTION

Most studies about reproductive patterns in shrimp are based on the percentage of mature females (Mathews 1981, Lopez-Martinez et al. 1999, Lopez-Martinez et al. 2005, Leal-Gaxiola et al. 2001). This is a biased index of population reproduction and must be combined with an index of mature female abundance and fecundity-at-size data (Garcia 1985). If one wants to find the most important period for population renewal, the studies of the reproductive biology of shrimp must take into account more than just reproductive percentage of mature females. Among others indices that have been considered for this target, we found a gonadal index, egg production for the population (Oh & Hartnoll 1999).

Reproductive studies of brown shrimp Farfantepenaeus californiensis (Holmes, 1900) are few (Olguin-Palacios 1968, Edwards 1978, Mathews 1981, Barreiro-Guemez 1986, Mendez-Tenorio 1986, Garduno-Argueta & Calderon-Perez 1994, Leal-Gaxiola et al. 2001, Aragon Noriega & Alcantara Razo 2005). Using only the percentage of mature females, the reproductive period of brown shrimp was determined as continuous throughout the year with two peaks of massive spawning. In these reproductive studies, 2 main sources of data have been used: daily packing-plant sampling from commercial catches (September to May) off Sonora, (Leal-Gaxiola et al. 2001) and data from research cruises that evaluated shrimp populations off Sinaloa (Barreiro-Guemez 1986, Garduno-Argueta & Calderon-Perez 1994). Sinaloa and Sonora comprise the eastern coast of the Gulf of California (Fig. 1).

[FIGURE 1 OMITTED]

The daily packing-plant data did not include all months of the year, but comprised a long data series (Leal-Gaxiola et al. 2001), and for this reason many reproductive studies were based on these data. A disadvantage of this data is that abundance could not be evaluated but only percentage of mature females. On board sampling commercial trawl vessel are scarce, and temporally sporadic (Aragon Noriega & Alcantara Razo 2005). The advantage of onboard sampling is that an evaluation of abundance of mature female shrimp can be made.

Fecundity of brown shrimp has been described with a power equation with a value around 3 (F = 0.0962 [L.sup.2.9642], Mathews 1981). The quantity of eggs spawned by ripe females increased because of the increasing size of mature females (Mathews 1981).

Although the fecundity and reproductive pattern of brown shrimp off Sinaloa and Sonora have been determined, fecundity-at-size, abundance and size structure of mature females have not been combined in previous studies. The application of egg production index (EPI) in penaeid shrimp was proposed by Courtney & Masel (1997). They found that this index is a more quantitative measure of egg production in a population at a particular sampling station or sampling time. Aragon-Noriega (2005) used an EPI calculated from size structure, fecundity-at-size, and abundance of mature females to determine the maturity period of blue shrimp Litopenaeus stylirostris (Stimpson, 1874) in central Gulf of California.

Studies on reproduction of exploited species are critical not only for fisheries managers, but they also have a general scientific interest because spawning is the basis of population renewal and conservation of the stocks. With this in mind, we should look for more precise methods that can help to determine the maturity period of species with economical or ecological importance.

The objective of this study is to determine the reproductive period of brown shrimp off Agiabampo, at the Sonora-Sinaloa state border, by combining the fecundity-at-size, abundance and size structure of mature females indices into a single index, EPI.

MATERIAL AND METHODS

Study Area

The Estero de Agiabampo (26.3[degrees]N, 109.3[degrees]W, Fig. 1) is a relatively long and narrow barrier lagoon created by sediment deposition of longshore currents. The broad region has a subtropical desert (BWh) climate (Garci 1988) and the sea surface temperature averages 30.4[degrees]C in July and 19.5[degrees]C in January.

Sampling

From January to December 2002, shrimp samples were taken each month for five continuous days (full moon [+ or -]2 days). Collection was done with small boats, about 7 m long. We used trawl nets with a 15-m mouth and 32-mm mesh. Tows were made every 1.5 h at flood and ebb tides. This was done at depths from 1-9 m at locations ranging up to 2 km north and south of the mouth of the coastal lagoon (Fig. 1).

Sex, gonad maturity, total length (tip of the rostrum to tip of the telson) [+ or -]1 mm and abdominal length of the samples was determined. Degree of gonad maturity was determined with the morphochromatic scale, comprising four stages (Leal-Gaxiola et al. 2001). For this study the specimens were grouped into immature (Stages I and II) and mature (Stages III and IV) categories.

Abundance of mature females was determined as specimens per hectare. This was done using a sweeping area described in Sparre & Venema (1995). Satellite geo-positioning devices locate the beginning and ending position of each trawl. The total of mature females was divided by the calculated area (in hectares). Fecundity-at-size was determined by the equations mentioned in Mathews (1981).

Egg production index (EPI), similar to one proposed by Aragon-Noriega (2005) was determined by combining size structure, fecundity-at-size and abundance of mature females. The EPI is formed as follows:

EPI = [n.summation overi=1] F(P[L.sub.ci]a)

where: EPI is the egg production index, i is the ith size class, F is fecundity at size, [L.sub.ci] is the mean value of length of class i, P is proportion of class i in a particular month, and a is the abundance of mature female in particular month.

RESULTS

A total of 5,780 specimens of all stages were collected (3,723 females and 2,057 males), yielding a female:male ratio of close to 2:1. However, for mature specimens, the ratio was 3:4, female: male ratio.

Period of Sexual Maturity

The percentage of mature males was more than 50% during the complete sampling period (Fig. 2). We found one period (May to August) in which the percentage of mature females was near or greater than 40% (Fig. 2). The other months in which mature females appeared were November (17%), April (10%) and February (1%).

[FIGURE 2 OMITTED]

Abundance

Monthly abundance of mature females determined by the sweeping area method were as follows: April, 29 females [ha.sup.-1]; May, 176 females [ha.sup.-1]; June, 97 females, [ha.sup.-1]; July, 82 females [ha.sup.-1]; August, 58 females [ha.sup.-1] and November, 5 females [ha.sup.-1] (Fig. 3). These results show that spring and summer is the most important reproductive period for brown shrimp, using abundance and percentage of mature females.

[FIGURE 3 OMITTED]

Frequency of Sizes

Total length of mature males ranged from 90-160 mm, averaging 123 [+ or -] 1 mm and a 10% coefficient of variation. Total length of mature females for the entire study period was 110-190 mm, averaging 151 [+ or -] 1 mm with an 8% coefficient of variation. Male and female sizes were significantly different ([F.sub.(1,3100)] : 3255, P < 0.05). Frequency of total length groups for May to August is shown in Figure 4. The modal size group was 44% greater than 165 mm in May. For June, July and August the percentage of specimens in the modal size group was 24%, 12% and 15%, respectively. Average total length of mature females was significantly greater in May ([F.sub.(3, 1428)] = 47.96, P < 0.05). No significant differences were found in June, July and August (Fig. 5).

[FIGURES 4-5 OMITTED]

Eggs Production

The EPI in eggs x [ha.sup.-1] did not match with months of higher percentage of mature females. EPI indicates that May is the most important month of potential egg production, followed by a clear negative tendency of EPI (Fig. 6). In May more than 60 million eggs x [ha.sup.-1] was the potential production on average. From June to August the average of potential eggs x [ha.sup.-1] were not more than 30 million. These results highlight the importance of using more than a single index to determine reproductive period for brown shrimp.

[FIGURE 6 OMITTED]

DISCUSSION

The reproductive period of brown shrimp F. californiensis off the coast of the Estero de Agiabampo is well defined as late spring to early summer, as quantified by using EPI. Leal-Gaxiola et al. (2001) found the reproductive period off southern Sonora as continuous during the year with two peaks of massive reproduction. However, those authors did not include data from June to September. For this reason their results are not adequate to determine the reproductive season for brown shrimp in that zone. The study of Leal-Gaxiola et al. (2001) could be easily combined with those of Mendez-Tenorio (1986) because this author sampled from June to January in the same zone and in the same years. Data from that study show an increasing percentage of mature females from June to August and decreasing percentage of mature females from August to January. The combination of data from the two studies yield a result similar to our findings. Leal-Gaxiola et al. (2001) found the times when the percentage of mature females was increasing and decreasing, but they erroneously concluded there were two periods of mass reproduction.

We found a single period of high rates of reproduction by using the percentage of mature females, similar to results found off Guaymas by Mathews (1981). He found mature females from February to November but a higher percentage from May to August. The reproduction period of brown shrimp reported off Mazatl fin, Sinaloa is either continuous, with two periods of higher intensity (Garduno-Argueta & Calderon-Perez 1994) or bimodal with a greater peak reproductive activity from March to May and a lower peak in October and November (Barreiro-Guemez 1986). Garcia (1985) reviewed various types of spawning seasonal patterns of many shrimp species from around the world. He concluded that in spite of the shortcomings of the method (percentage of mature female) used for quantifying spawning activity, it seems that a bimodal pattern is most frequent. The main shortcoming of the percentage of mature female method is that overall population abundance of mature female is not taken into account but only a relative percentage of an unknown number per area (e.g., [km.sup.-2], ha or other measurement).

Garcia (1985) also concluded that reproductive behavior of shrimp species respond to transition periods of temperature. In the Gulf of California well-defined periods of transition in temperature occurs from spring to summer and from fall to winter (Aragon-Noriega & Alcantara-Razo 2005). So, conclusion that brown shrimp display a double peaked spawning pattern where accepted mentioned that the reproductive period (determined by the percentage of mature brown shrimp females) in the Gulf of California depends on the SST.

Because the percentage of mature females is a biased index of population reproduction (Garcia 1985), we combined 3 indices: abundance, fecundity and size structure of the mature female brown shrimp, representing the first published index for this species. The only other study of EPI application was conducted on L. stylirostris (Aragon-Noriega 2005). In May we found 44% of the mature females over 161 mm TL. From the fecundity-at-size pro posed by Barreiro-Guemez (1986), 44% of the females could be spawning 800,000 or more eggs. Though the higher percentage of mature females was collected in July, we propose that May is the most important month for the reproductive period of brown shrimp off Agiabampo, because the highest EPI was found this month.

The percentage of mature females in November suggests a second, less intensive spawning period, but EPI showed that only a 1-million eggs x [ha.sup.-1] was the potential production, on average, in that month.

To determine the actual maturity period of any species we should take into account all shortcomings of the available methods. A problem for an exploited species is the specimens that remain unaccounted for after the fishery season. For the case of the brown shrimp near Agiabampo we surmise that if the reproductive behavior of this species responds to transition periods of temperature (Garcia 1985) the abundance of mature female remaining after the trawl fishery is too low to be considered as a two-peaked pattern species. The use of EPI could help to redefine the actual maturity period for those two groups of penaeid shrimp, even if the second period of spawning for browns has been greatly diminished by fisheries activities.

This study clearly shows that results from one area cannot be extrapolated to other areas of the Gulf of California. Also, we found that current commercial catch data are not adequate for determining the reproductive pattern of brown shrimp. We agree with the proposal of Garcia (1985) to use at least two other indices, and not just the percentage of the mature females in samples. We conclude that the appropriate combination of indices include size structure of mature females, abundance of mature females and fecundity-at-size to determine the reproductive period of brown shrimp. Specifically, those three indices for the brown shrimp off Agiabampo show a single maturation period from May to August.

ACKNOWLEDGMENTS

This study was supported by contract 908-1G of the National Fisheries Institute (INP) and CIBNOR. The National Council of Science and Technology of Mexico granted a fellowship to the first author (CONACYT 111763) and IPN "DICTAMEN 209."

LITERATURE CITED

Aragon-Noriega, E. A. 2005. Reproductive output of the blue shrimp, Litopenaeus stylirostris (Decapoda: Penaeidae) in the Gulf of California coast at Agiabampo, Sonora-Sinaloa, Mdxico. J. Shellfish Res. 24(2):597-601.

Aragon-Noriega, E. A. & E. Alcantara-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. Mar. Biol. 146(2):373-379.

Barreiro-Guemez, M. T. 1986. Estudio sobre la madurez y desove de Penaeus californiensis y Penaeus vannamei (Crustacea Decapoda, Penaidae) en la costa sur de Sinaloa. Memorias del Primer Intercambio academico sobre investigaciones del Mar de Cortes. Hermosillo, Sonora, Mexico, pp. 1-30.

Courtney, A. J. & J. M. Masel. 1997. Spawning stock dynamics of two penaeid prawns, Metapenaeus bennettae and Penaeus esculentus, in Moreton Bay, Queensland, Australia. Mar. Ecol. Prog. Ser. 148:37-47.

Edwards, R. R. C. 1978. The fishery and fisheries biology of the penaeid shrimp on the Pacific Coast of Mexico. Oeanogr. Mar. Biol. Ann. Rev. 16:145-180.

Garcia, E. 1988. Modificacion al sistema de clasificacion climatica de Koppen para adaptarlo a las condiciones de la Republica Mexicana. Offset Larios. Mexico, 222 pp.

Garcia, S. 1985. Reproduction, stock assessment models and population parameters in exploited Penaeid shrimp populations. In: P. C. B. Rothlisberg, J. Hill & D. J. Staples, editors. Second Australian National Prawn Seminar, NOS2. Cleveland, Australia. pp 139-158.

Garduno-Argueta, H. & J. A. Calderon-Perez. 1994. Abundancia y maduracion sexual de hembras de camaron (Penaeus spp) en la costa sur de Sinaloa, Mexico. Rev. Inv. Cient. Universidad Autonoma de Baja California Sur. Serie Ciencias Marinas 1:27 34.

Leal-Gaxiola, A., J. Lopez-Martinez, E. A. Chavez, S. Hernandez-Vazquez & F. Mendez-Tenorio. 2001. Interannual variability of reproductive period of the brown shrimp, Farfantepenaeus californiensis (Holmes, 1900) (Decapoda, Natantia). Crustaceana 74(9):839-851.

Lopez-Martinez, J., F. Garcia-Dominguez, E. Alcantara-Razo & E. A. Chavez. 1999. Periodo reproductivo y talla de madurez masiva del camaron de roca Sicyonia penicillata (Decapada: Sicyoniidae) en Bahia Kino, Sonora, Mexico. Rev. Biol. Trop. 47(1-2):109-117.

Lopez-Martinez, J., C. Rabago-Quiroz, M. O. Nevarez-Martinez, A. R. Garcia-Juarez, G. Rivera Parra & J. Chavez Villalba. 2005. Growth, reproduction and size at first maturity of blue shrimp Litopenaeus stylirostris (Stimpson, 1874) along the east coast of the Gulf of California, Mexico. Fish. Res. 71:93-102.

Mathews, C. P. 1981. A review of the North American penaeid fisheries, with particular reference to Mexico. Kuwait Bull. Mar. Sci. 2:325-409.

Mendez-Tenorio, F. J. 1986. Aspectos relativos a la madurez gonadica en camaron de altamar en las costas de Sonora y Baja California. Memorias del Primer Intercambio academico sobre investigaciones del Mar de Cortes. Hermosillo, Sonora, Mexico, pp. 230-244.

Oh, C. W. & R. G. Hartnoll. 1999. Size at sexual maturity, reproductive output, and seasonal reproduction of Philocheras trispinosus (Decapoda) in Port Erin Bay. Isle of Man. J. Crustacean Biol. 19(2):252-259.

Olguin-Palacios, M. 1968. Estudio de la biologia del camaron cafe Penaeus californiensis Holmes. FAO Fish. Rep. 57(2):331-356.

Sparre, P. & S. C. Venema. 1995. Introduccion a la evaluacion de recursos pesqueros tropicales. Parte 1. Manual. FAO Documento Tecnico de Pesca No. 306. 1st. Rev. 440 pp.

WENCESLAO VALENZUELA-QUINONEZ, (1,2) * EUGENIO ALBERTO ARAGON-NORIEGA (1), DULCE PATRICIA ALVARADO-ROMERO, (1) CESAR AUGUSTO SALINAS-ZAVALA (3) AND ALMA ROSA GARCIA-JUAREZ (1,4)

(1) Centro de Investigaciones Biologicas del Noroeste (CIBNOR), Unidad Sonora, Apdo. Postal 349, Guaymas, Sonora 85400 Mexico; (2) Centro Interdisciplinario de Investigacion para el Desarrollo Integral Regional-IPN, Guasave, Sinaloa Km 1.0 Carretera a Las Glorias, Mexico 81101; (3) Centro de Investigaciones Biologicas del Noroeste (CIBNOR), Unidad La Paz, Mar Bermejo No. 195 Colonia Playa Palo de Santa Rita, La Paz, B.C.S. 23090 Mexico; (4) Centro Regional de Investigacion Pesquera de Guaymas, Instituto Nacional de Pesca (INP), Calle 20 No. 605 Sur, Col. Cantera, Guaymas, Sonora 85400, Mexico

* Corresponding author. E-mail: wvalenzuela@cibnor.mx
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Author:Garcia-Juarez, Alma Rosa
Publication:Journal of Shellfish Research
Geographic Code:1MEX
Date:Apr 1, 2006
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