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Habitat utilization by the reproductive stock of the brown shrimp Farfantepenaeus californiensis in the central Gulf of California.

ABSTRACT To fully understand the reproductive habitat of brown shrimp, Farfantepenaeus californiensis, this study analyzed reproductive dynamics of the stock in a semiarid coastal region of the Gulf of California. Monthly biological samplings were conducted simultaneously in a coastal lagoon and in adjacent marine waters from January through December 2002, during 5-d periods centered on full moon (full moon [+ or -] 2 d). An Egg Production Index EPI was used to determine the reproductive period. The main reproductive period was from April to August in coastal waters and June to July inside the lagoon. The EPI was 10 times greater in coastal waters than inside the lagoon. We conclude that, contrary to what is generally believed, brown shrimp can mature and possibly reproduce inside the coastal lagoon, although the most important spawning habitat is coastal waters.

KEY WORDS: reproduction, habitat, shrimp, Farfantepenaeus californiensis, Gulf of California

INTRODUCTION

All the known members of the family Penaeidae have a similar life cycle: planktonic larval stages; including nauplius, protozoea, mysis, and postlarva; followed by juvenile and adult stages (Dall et al. 1990). The great difference among genera lies in the habitat preferred by the postlarvae, juveniles and adults, be it estuaries or coastal lagoons, continental or oceanic shelf.

Dall et al. (1990) mention that the basis for classifying the life cycle of penaeids is the environment in which adults spawn and postlarvae settle. They distinguish four types of life cycles, but clarify that overlap may occur among them. In the type 3 life cycle, the adult and reproductive stages occur in oceanic conditions (between the open sea and the continental shelf). Eggs are released by females into the marine environment where they go through the four larval stages. Postlarvae and juveniles inhabit coastal, but not estuarine, environments. In type 1, species need to be extremely euryhaline, because their entire life occurs in estuarine habitat.

For penaeid shrimp inhabiting the Gulf of California it was established that all species depend on estuarine systems to complete their life cycle, with slight variations for each species (Edwards 1978). This life cycle is applicable to estuarine systems with an ephemeral connection to the sea and positive circulation, such as those described by Kjerfve (1986) in the classification of coastal lagoons. In coastal lagoons of arid regions with permanent connection to the sea and negative estuarine circulation, penaeid shrimp develop a particular life cycle that differs from that accepted for the general shrimp ecology.

Farfantepenaeus californiensis or brown shrimp (Holmes 1900), a stenohaline species with a salinity tolerance from 3038 psu, has been regarded as preferring marine habitats, based on low dependence upon coastal lagoons for postlarval growth (Garcia & Le Reste 1981). Porchas et al. (2000) found larval development in F. californiensis restricted to 33-38 psu.

The eastern coast of the Gulf of California, north of the Tropic of Cancer is characterized by a series of wide outlet coastal lagoons opening to the sea (Arreola-Lizarraga 2003). Brown shrimp in these lagoons have been found in Estero del Soldado (Loesch 1980), Laguna de la Cruz (Grijalva-Chon & Barraza-Guardado 1992), and Las Guasimas (Arreola-Lizarraga 2003). Furthermore, at Laguna Agiabampo, straddling the Sonora-Sinaloa border, Romero-Sedano et al. (2004) found female brown shrimp maturing inside this coastal lagoon.

Brown shrimp sustain an important fishery in the Gulf of California. Fishing takes place in coastal lagoons and in adjacent coastal waters. The harvest season is from September to March Fishing in the remaining months is prohibited for the purposes of maintaining spawning stocks/preventing recruitment overfishing (INP 2001).

This study attempts to provide a spatial analysis of egg production and spawning in the population of brown shrimp F. californiensis in the Gulf of California. We present results from samplings outside and inside the Agibampo coastal lagoon, in the east side of the Gulf of California in northwestern Mexico. This lagoon received no river discharge for about 50 y (Bandas 1997), establishing hypersaline conditions over most of the year. Because of environmental conditions prevailing in the lagoon, brown shrimp appear to have modified its ecological requirements.

MATERIAL AN D METHODS

Study Area

The Agiabampo Lagoon (26[degrees]05' to 26[degrees]30'N and 109[degrees]05' to 109[degrees]20'W) covers 184 [km.sup.2], has an average depth of 2 m and communicates with the Gulf of California through a 1.5-km wide inlet (Fig. 1). The 20-m deep inlet channel has currents reaching 3 m [s.sup.-1]. According to Kjerfve's (1986) classification system of lagoons (choked, restricted, and leaky), the lagoon is "restricted" because it: (1) has a permanent wide mouth open to the sea; (2) has a well-defined tidal circulation; (3) is strongly influenced by winds; and (4) is vertically well-mixed. Evaporation rate is about 300 cm [year.sup.-1] and greatly exceeds rainfall (about 30 cm [year.sup.-1]). The offshore front of the lagoon (26[degrees]00' to 26[degrees]30' N and 109[degrees]15' to 109[degrees]25'W) has irregular depth and is dominated by several shallow zones and channels oblique to the coast.

Sampling

From January to December 2002, shrimp samples were taken each month for five consecutive days (full moon [+ or -] 2 d). Collection was done on small fishing boats, about 7 m long using trawl nets with a 15-m mouth and 32-ram 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, for the coastal sampling. A total of 24 georeferenced stations was sampled within the lagoon (Fig. 1).

Sex, gonadal maturity, total length (tip of the rostrum to tip of the telson) [+ or -] 1 mm, and abdominal length of individuals of the samples were recorded. Females were considered mature if gonads were ripe, regardless of size. The degree of gonadal maturity was determined with the four phases of the morphochromatic scale (Leal-Gaxiola et al. 2001). For this study, specimens were grouped into immature (Stages I and II) and mature (Stages III and IV) categories.

[FIGURE 1 OMITTED]

Data Analysis

The percent distribution of mature females each month t ([PMF.sub.t]) over the sampling period was determined as:

[PMF.sub.t] = [[FM.sub.t]/[FT.sub.t]] 100

where [FM.sub.t] is the number of mature females in month t and [FT.sub.t] the total females in month t.

Relative abundance of mature females was determined as total number per hectare. This was done using swept area described in Sparre & Venema (1995). Satellite geo-positioning devices were used to locate the starting and ending position of each trawl; this allowed determination of distance towed, which multiplied by width of the sampling net yielded area swept. The number of mature females per sample was divided by the calculated area swept (in hectares). Fecundity-at-size was determined using the equations described by Mathews (1981). Total length (TL) of mature females was grouped in 5-mm intervals.

An egg production index (EPI) was proposed by Aragon-Noriega (2005) and Valenzuela-Quinonez et al. (2006) to determine reproductive output in shrimp populations. The EPI was determined by combining size structure, fecundity-at-size, and abundance of mature females. The EPI is formulated as follows:

[EPI.sub.t] = [n.summation over (i=I)] [F.sub.i] ([P.sub.i][LC.sub.i][a.sub.t])

where [F.sub.i] is fecundity at size class i, [LC.sub.i] is the mean length of size class i, [P.sub.t] is relative abundance of mature females of class i in month t, and [a.sub.t] is the relative abundance of mature females in month t. This formula allows for a standardized comparison between EPI inside the lagoon and in coastal waters.

The relationship of length at maturity can be modeled as:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

(King 1995) which can be expressed in linear form to yield:

ln(1 - P/p) = [rL.sub.m] - [rL.sub.i]

where P is the proportion of mature females at length [L.sub.i], r is the slope of the curve, [L.sub.m] is length at first maturity or length corresponding to 50% of ovigerous females.

We then plotted:

ln(1 - P/P)

against [L.sub.i] and used stepwise linear regression to solve for r.

RESULTS

A total of 33,474 specimens were collected (5,780 in coastal waters and 27,694 inside the lagoon). The female:male ratio varied between habitat: 3,723 females and 2,057 males in coastal waters; 12,297 females and 15,397 males in the lagoon.

Period of Sexual Maturity

Relative abundance of mature males of brown shrimp, Farfantepenaeus californiensis, inside the lagoon habitat exceeded 60% of total males throughout the sampling period, except from August to October (Fig. 2) when it was less than 30%. In the coastal habitat, mature males exceeded 50% during the sampling period with highest percents from April to August. The presence of mature females in coastal waters extended for a longer period than in the lagoon habitat. Percentage of mature females in coastal waters was close to or greater than 40% from May to August (Fig. 2). In the lagoon habitat, mature females were restricted to June, July and November, but were always less than 10%.

Relative Abundance

Relative abundance of mature females varied monthly in the lagoon and coastal habitats. Mature females were much more abundant and frequent in coastal waters than in the lagoon. In coastal waters the index peaked at 175 females [ha.sup.-1] in May, then declined steadily (Fig. 3). In the lagoon habitat the index of mature female was 20 in June, 13 in July, and two females [ha.sup.-1] in November.

Size Frequencies

Total length of mature females during the study period ranged from 90-195 mm (Fig. 4); average length was 151 [+ or -] 1 mm in coastal waters and 134 [+ or -] 2 mm in the lagoon (Fig. 5). Average total length of mature females was significantly greater in coastal waters ([F.sub.(1, 1556)] = 350.19, P < 0.05) than in the lagoon.

Egg Production

The EPI indicated that May was a very important month in terms of potential egg production in coastal waters, with 60 x [10.sup.6] eggs [ha.sup.-1] (Fig. 6) followed by a clear declining trend. The trend in EPI was similar for the two habitats only in June and July; however, it is one order of magnitude greater in coastal waters.

[FIGURE 2 OMITTED]

Size at Maturity

Size at maturity or size at massive maturation was calculated to be 155 mm total length for coastal waters and 146 mm in the lagoon (Fig. 7).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

DISCUSSION

Studies of brown shrimp reproduction have been conducted mostly in marine habitats (Olguin-Palacios 1968, Edwards 1978, Mathews 1981, Aragon-Noriega & Alcantara-Razo 2005) but only one in a coastal lagoon habitat (Romero-Sedano et al. 2004). There is a gap of knowledge regarding biological aspects of brown shrimp in coastal lagoons of the Gulf of California. Closing this gap is paramount for fisheries conservation and management decisions.

Spawning is an important biological process as it is basic for renewal of stocks and conservation of the species. Understanding this site and species process also has implications in economics of fisheries as it is critical to protecting reproductive areas. For the Gulf of California, where shrimp stocks have been declared at their maximum sustainable yield (SAGARPA, 2004), this is particularly true.

Farfantepenaeus californiensis has been classified as an oceanic species (Garcia & Le Reste 1981). Mathews (1981) thought it enters shallow inner waters during the first postlarval stages and leaves this habitat when it has attained a mean total length of 35 mm, because this species has never been officially recorded in coastal lagoon catches (Mathews 1981, Del Valle & Martin 1995). In the Gulf of California, it is possible that mature brown shrimp do not occupy lagoons south of 23[degrees]N (southern Sinaloa) where most studies of shrimp biology have been conducted. This may be related to differences in the local hydrology (Poli & Calderon-Perez 1987). In southern Sinaloa during dry periods, estuarine systems are separated from the sea by sandbars. Our study site, Agiabampo lagoon, has a permanent connection to the sea offering species a structurally complex habitat within the beds of submerged macrophytes where they can find protection from predators (Arreola-Lizarraga 2003). In these conditions brown shrimp may remain in the lagoon or move in and out during the adult phase.

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

Other studies have documented the presence of brown shrimp in coastal lagoons of the Gulf of California in arid regions, north of 26[degrees]N, such as Estero del Soldado (Loesch 1980), Laguna de La Cruz (Grijalva-Chon & Barraza-Guardado 1992), and Laguna de Las Guasimas (Arreola-Lizarraga 2003). However, those studies did not report mature brown shrimp inside the coastal lagoons.

Romero-Sedano et al. (2004) previously highlighted the importance of describing coastal lagoons as habitat for reproductive stocks of the brown shrimp. Our objective in the present study was to compare stock indices (abundance, size, EPI and PMF) of brown shrimp to determine habitat preferences for reproduction. Agiabampo is the only coastal lagoon where brown shrimp have been sampled in spawning condition among three other coastal lagoons where its presence has been reported. The main difference we found within and outside the lagoon was the size at maturity. Mature female brown shrimp were larger in size in coastal waters than inside the lagoon. Although more specimens were collected inside the lagoon, the percentage of mature female was smaller there than in coastal waters. This contrasts with abundance data of mature female, which were higher in coastal waters than inside the lagoon, resulting in a greater EPI outside the lagoon.

In the present study of brown shrimp in Agiabampo, we found that this species has the facultative characteristic to develop its full life cycle in the lagoon system. Our results point to the hypothesis of a metapopulation structure between coastal waters and lagoon stocks in this region. The conclusion is that reproductive behavior of brown shrimp is different from what occurs in other coastal lagoons in northwestern Mexico. Brown shrimp appear capable of maturing and possibly spawning in the lagoon, although most egg production occurs in coastal waters further offshore. For fisheries management purposes, this finding is important because closing the fishery for brown shrimp during spawning season inside the lagoon could be a conservative measure to help protect the fishery. Additional studies could further support this hypothesis.

[FIGURE 7 OMITTED]

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 WVQ and ARGJ. The "Sylvia Ramirez" Fisheries Cooperative Society provided logistic support for field sampling.

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, Mexico. J. Shellfish Res. 24:597-601.

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. 146:373-379.

Arreola-Lizarraga, J. A. 2003. Bases de manejo costero: Patrones ecologicos en la laguna costera Las Guasimas, Territorio Yaqui, Mexico. Doctoral Thesis, La Paz, Mexico. Centro de Investigaciones Biologicas del Noroeste. 60 pp.

BANDAS (Banco Nacional de Datos de Aguas Superficiales). 1997 Instituto Mexicano de Tecnologia del Agua, Periodo 1921-1994. CD-rom data base, Morelos, Mexico.

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Kjerfve, B. 1986. Comparative oceanography of coastal lagoons. In: D. A. Wolfe editor. Estuarine variability. San Diego, CA: Academic Press. pp 1-81.

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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 74:839-851.

Loesch, H. 1980. Some ecological observations on slow-swimming nekton with emphasis on Penaeidae shrimp in a small Mexican west coast estuary. Ann. hist. Cienc. Mar y Limnol. UNAM 7:1526.

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

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

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Porchas. M. A., L. R. Martinez, J. Naranjo, F. Magallon, G. Portillo & M. Unzueta. 2000. Efecto de la salinidad en la larvicultura del camaron cafe Farfantepenaeus californiensis (Holmes, 1900) a bajas temperaturas. Cienc. Mar. 26:503-510.

Romero-Sedano, C., E. A. Aragon-Noriega, M. M. Manzano-Sarabia, C. A. Salinas-Zavala & A. R. Garcia-Juarez. 2004. Reproductive period of brown shrimp Farfantepenaeus californiensis (Holmes 1900) in the Agiabampo coastal lagoon System, Sonora/Sinaloa, Mexico. Cienc. Mar. 30:465-475.

SAGARPA. 2004. Carta Nacional Pesquera. Mexico. Diario oficial de la federacion 15 de marzo de 2004. http://www.inp.sagarpa.gob.mx/CNP/index.htm

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.

Valenzuela-Quinonez, W., E. A. Aragon-Noriega, D. P. Alvarado Romero, C. A. Salinas-Zavala & A. R. Garcia Juarez. 2006. Application of an egg production index to determine reproductive period of the brown shrimp Farfantepenaeus californiensis near Agiabampo, Sonora-Sinaloa. Mexico. J. Shellfish Res. 25:123-127.

EUGENIO ALBERTO ARAGON-NORIEGA, (1) * MIGUEL ANGEL CISNEROS-MATA, (2) EDGAR ALCANTARA-RAZO, (1) WENCESLAO VALENZUELA-QUINONEZ (1,4) AND ALMA ROSA GARCIA-JUAREZ (1,3)

(1) Centro de Investigaciones Biologicas del Noroeste, S.C. (CIBNOR), Unidad Sonora. Km 2.35 Camino al Tular, Estero de Bacochibampo, Guaymas, Sonora. 85454. Mexico; (2) Instituto Nacional de la Pesca (INP), Pitagoras 1320-8vo. piso. Col. Santa Cruz Atoyac. Mexico, D.F. 03310. Mexico; (3) Centro Regional de Investigacion Pesquera de Guaymas, Instituto Nacional de Pesca. Calle 20 No. 605 Sur, Col. Cantera, Guaymas, Sonora. 85400. Mexico; (4) Centro Interdisciplinario de Investigacion para el Desarrollo Integral Regional-IPN, Unidad Sinaloa. Km. 1.0 Carretera a Las Glorias, Guasave, Sinaloa 81101 Mexico

* Corresponding author. E-mail: aaragon04@cibnor.mx
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Author:Aragon-Noriega, Eugenio Alberto; Cisneros-Mata, Miguel Angel; Alcantara-Razo, Edgar; Valenzuela-Quin
Publication:Journal of Shellfish Research
Geographic Code:1MEX
Date:Aug 1, 2007
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