Gonadal development in male and female domesticated whiteleg shrimp, Litopenaeus vannamei, in relation to age and weight

doi:10.1016/j.aquaculture.2010.08.020

Aquaculture

Volume 308, Issues 3–4, 21 October 2010, Pages 116-123

https://doi.org/10.1016/j.aquaculture.2010.08.020 Get rights and content

Abstract

Cultivation of whiteleg shrimp (Litopenaeus vannamei) is now entirely based on closed life-cycle populations, yet few studies have analyzed gonadal development in domesticated shrimp during grow-out in ponds. To determine the effect of age and weight on morphometric, histological, and biochemical variables associated with male and female gonadal development, shrimp from the same cohort, at ages of 6, 8, 10, and 12 months were examined using body weight as a covariable in an ANCOVA design. An additional comparison between two grow-out conditions in 1-year-old shrimp was done to separate the effect of size as a result of initial stocking densities. Age-related growth of gonads was clearly dependent on somatic growth for females but not for males, although differential somatic growth produced by stocking densities explained differences in growth of gonads for both sexes. Increase in oocyte diameter and differentiation associated with age and grow-out condition were independent of body weight. Age-related female gonadal development was accompanied by increases in lipid and protein concentrations, independent of body weight. Maturation of male reproductive organs (testicle, vas deferens, terminal ampoule, and spermatophore) was sequential and depended mainly on age, although body weight could explain differences caused by different grow-out conditions. An age-related decrease in concentration of lactate occurred in all male reproductive organs and could indicate a metabolic adjustment of sperm anaerobic metabolism and lactate clearance associated with gonadal development. We highly recommend waiting for optimal reproductive potential of females at 12 months to enhance spawning frequency and larval quality. At this age, body weight seems to be of secondary importance, although optimal conditions of cultivation are necessary to have adequate growth and balanced nutrition.

Introduction

Cultivation of whiteleg shrimp (Litopenaeus vannamei) is currently based on closed life-cycle populations that offer intrinsic advantages of biosecurity (Moss and Crocos, 2001). However, few studies have analyzed gonad development in domesticated shrimp during grow-out in ponds. Under natural conditions, gonad development is regulated by environmental parameters and modified by available nutrients (Rothlisberg, 1998). Shrimp reared in ponds have reduced or altered environmental clues and may not be exposed to the diversity of nutrients that are required for gonad ripeness. Medina et al. (1996) described ovary development for pond-reared and wild caramote prawn Pemaeus kerathurus, observing that in contrast to wild shrimp, pond-reared shrimp failed to attain seasonally related ripeness (cortical-rod or mature oocytes). In addition to environmental and nutritional factors, shrimp raised in ponds are usually stocked at high densities, which can limit growth and produce stress that can affect gonadal development. For whiteleg shrimp cultivated in brackish water, Parnes et al. (2004) observed that females beyond 20 g at an age of 8.5 months developed opaque ovaries, expressed the vitellogenin gene in ovaries but not in the hepatopancreas, and had an average oocyte diameter of 48 μm, which corresponds to a development stage between previtellogenic and vitellogenic for the same species (Palacios et al., 1999, Ceballos-Vázquez et al., 2003a), although a specific gonadal development stage was not reported. For males, studies of maturation in captivity have focused on sperm characterization rather than on gonadal development. Previously, sperm quantity and quality in whiteleg shrimp were studied in relation to age, size, and grow-out conditions (Ceballos-Vázquez et al., 2003b) and a similar study was published for the giant tiger prawn Penaeus monodon (Jiang et al., 2009). Parnes et al. (2004) studied spermatophore development, characteristics and sperm count in whiteleg shrimp grown in brackish water; they found melanized spermatophores in shrimp older than 8 months.

Age is closely associated with size; for this reason, shrimp weight is among the principal criteria used for selecting broodstock. For whiteleg shrimp, weight range between 30 and 45 g is recommended for females (Aquacop, 1983, Wyban et al., 1987, Ogle, 1992). Higher weights (between 40 and 60 g) have been proposed (Otoshi et al., 2003). Size was widely used to select broodstock when the age was unknown, as in the case of wild shrimp. However, size is affected by grow-out density, feed, and environmental clues. Hence, age is a more precise criterion, particularly in closed cycles when the date of stocking is known. The age for obtaining good reproductive output in whiteleg shrimp is between 10 and 18 months (Aquacop, 1983, Ogle, 1992). However, no determination has been made whether the younger-aged shrimp could be used to obtain an acceptable/ideal reproductive output for commercial production. In addition, there is a lack of information if the youngest age is the same for males and females. Results in other species indicate that younger shrimp can be used for reproduction, with the advantage of reducing costs associated with extended cultivation to produce older shrimp. For the green tiger prawn P. semisulcatus, females as young as 6 months can be used to provide acceptable egg production and hatching rates (Coman and Crocos, 2003). The best spawning and fertilization rates in blue shrimp L. stylirostris occur at 6–9 months (Ottogalli et al., 1988). For southern white shrimp L. schmitti, 10-month-old females and 7-month-old males resulted in similar production values as was obtained with wild spawners (Pérez-Jar and Jaime-Ceballos, 1995).

No study has analyzed gonadal development in the same cohort of domesticated shrimp at different ages during grow-out, dissociating the relative influence of age and body weight. Also, it is not known if limited growth of shrimp from high stocking density, feeding conditions, or other factors has an effect on gonadal development independently of the age. This study analyzed gonad histology and biochemical development of male and female whiteleg shrimp between 6 and 12 months. Additionally, two grow-out conditions with different initial densities and natural food availability were compared in 1-year-old shrimp, with the main purpose of obtaining shrimp with marked differences in size.

Section snippets

Animals

Larvae obtained within 3 days of spawning were grown to the 20-day postlarval stage (PL20). A subset of these postlarvae was transferred to one 10,000 m² tidal pond (TP) at a density of 3 to 4 shrimp m⁻² and fed pellets containing 25% protein (PIASA, La Paz, Mexico). The ration was adjusted weekly to provide a daily supply equivalent to 5% of the shrimp biomass, but gradually adjusted downward to 2% biomass (Villalón, 1991). Another subset of the postlarvae was stocked at very high densities to

Temperature and salinity

The variation of temperature and salinity over the sampling period in the TP and LP is shown in Fig. 1.

Morphometric characteristics

The morphometric characteristics of age 6-, 8-, 10-, and 12-month females are shown in Table 1. Body weight and length increased with age. Ovary weight, GSI, and diameter of the more developed oocytes (MDO) were significantly correlated with body weight (r = 0.69, 0.66, and 0.86, respectively). Ovaries were significantly larger and GSI was significantly greater in the 12-month-old females, but

Female gonadal development

Development of the female reproductive system is characterized by growth of ovaries and parallel development and differentiation of oocytes. Stages of ovarian development are well defined for penaeid shrimp, ranging from detailed scales based on the cytological characteristics of more advanced oocytes and their diameter, such as the one used in our study (with 10 stages) as defined by Yano (1988), to more simple scales of four or five stages, based on histological appearance (Tan-Fermin and

Conclusions

As previously suggested for males, we recommended waiting until females reach 12 months to maximize reproductive potential associated with higher spawning frequency and larval quality. Once this age is attained, body weight is of secondary importance. However, it is necessary to have optimal conditions of cultivation and balanced nutrition for adequate growth.

Maturation of male reproductive organs (testicle, vas deferens, terminal ampoule, spermatophore) is sequential and depends mainly on the

Acknowledgements

We are grateful to Roberto Hernández-Herrera for technical assistance with biochemical determinations. This research was supported by SIMAC grant 00BCS7501 and SEP-CONACYT grant 101733. B.P. Ceballos-Vázquez was a recipient of doctoral fellowship from Consejo Nacional de Ciencia y Tecnología and also receives Instituto Politécnico Nacional fellowships (EDI and COOFAA).

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After 14 days of exposure, the content of BPA in the gonads of whiteleg shrimp was found to be under the detection limit for the control, solvent control (DMSO), and MPs exposure groups. Both the aquaculture industry and the recruitment of wild populations of whiteleg shrimp rely on successful gonad development, a prerequisite for the reproductive success of all sexually produced organisms (Ceballos-Vázquez et al., 2010; Fresno et al., 2021). Although gonadal development could be theoretically threatened by emergent pollutants such as MPs and BPA (Wang et al., 2019; Yan et al., 2020), to the best of our knowledge, little is known about the effects of MPs and BPA on the gonadal development of crustacean species.
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