A comparison of the reproductive performance of the wild pink shrimp species Farfantepenaeus paulensis and Farfantepenaeus brasiliensis in captivity.
Article Type: Report
Subject: Shrimps (Physiological aspects)
Authors: Braga, Andre L.
Lopes, Diogo L.A.
Krummenauer, Dariano
Poersch, Luis H.
Wasielesky, Wilson, Jr.
Pub Date: 12/01/2011
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2011 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: Dec, 2011 Source Volume: 30 Source Issue: 3
Topic: Event Code: 310 Science & research
Product: Product Code: 0913080 Shrimp NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish
Geographic: Geographic Scope: Brazil Geographic Code: 3BRAZ Brazil
Accession Number: 278595641
Full Text: ABSTRACT The aim of this study was to compare the reproductive performance of the wild shrimp species Farfantepenaeus paulensis and Farfantepenaeus brasiliensis in captivity. The broodstocks were collected in offshore waters in Santa Catarina and transferred to the Marine Station of Aquaculture of the Federal University of Rio Grande. Broodstocks with a similar body weight between the two species were selected to measure reproductive performance. Females with mature ovaries were identified each day to obtain measures of reproductive performance. After spawning, fertilization rates were determined by microscopic examination. In addition, three samples of 100 eggs were collected to determine hatching rates, and three samples of 100 nauplii were collected to evaluate the rate of metamorphosis to protozoa. For males, spermatophores were manually extruded, weighed, and homogenized in 2 mL calcium-free saline solution, and 0.1 mL trypan blue was added. Sperm counts, abnormal cells (malformations of the main body or absence of the spike), and dead cells (blue coloration) were estimated with cell counts, using a hemacytometer under a light microscope. Spermatophore melanization was checked. The larval production of the two species was similar, but F. brasiliensis spawned in less time after unilateral eyestalk ablation. The spermatophore weight and sperm count were higher in the F. brasiliensis males, and none of the shrimp showed melanization.

KEY WORDS: pink shrimp, Farfantepenaeus, broodstock, sperm quality, larval production

INTRODUCTION

The shrimp Farfantepenaeus paulensis and Farfantepenaeus brasiliensis are called pink shrimp primarily because of their similar morphology. However, these species are morphologically distinguished by the short and shallow median sulcus in F. paulensis compared with the long and deep median sulcus in F. brasiliensis, and the presence of a dark spot at the third and fourth junction of the abdominal segments in F. brasiliensis (Perez-Farfante 1988).

Farfantepenaeus paulensis is distributed from Ilheus, Brazil, to Mar del Plata, Argentina (D'Incao 1991). The distribution of F. brasiliensis is wider and extends from North Carolina to Rio Grande do Sul, Brazil (Perez-Farfante & Kensley 1997). The life cycles of both species are characterized by offshore reproduction and estuarine growth (Valentini et al. 1991).

In their primary areas of distribution, both species are important resources for artisanal and commercial fisheries. For example, F. brasiliensis is the principal shrimp harvested on the Brazilian (D'Incao et al. 2002) and Mexican coasts (Perez-Castaneda & Defeo 2001), and F. paulensis is harvested more extensively in southern and southeastern Brazil (Valentini et al. 1991). The intense exploitation of these penaeids has caused declines in wild stocks. D'Incao et al. (2002) reported that the population of F. paulensis has been reduced by approximately 75% from the early 1970s to the late 1990s.

For this reason, the importance of pink shrimp culture has increased. In southern Brazil, larval F. paulensis have been produced in captivity since the 1980s (Marchiori & Boff 1983). F. paulensis culture management has been evaluated in cages (Ballester et al. 2007), pen enclosures (Wasielesky et al. 2001), and biofloc systems (Emerenciano et al. 2007). A technological package has been developed for the reproduction of this species in captivity (Peixoto et al. 2011).

Interest in F. brasiliensis culture is more recent and has been motivated by empirical observations of hardiness and resistance in broodstock capture and culture management (Lopes et al. 2011). The production of F. brasiliensis in captivity has been examined (Brito et al. 2000, Gaxiola et al. 2010). Lopes et al. (2009) compared the growth of F. paulensis and F. brasiliensis in cages in the Patos Lagoon estuary and reported that both species showed similar performance. They concluded that F. brasiliensis has the potential to be cultured. This finding may motivate the development of a technological package for the culture of this species.

However, the current knowledge of reproduction in F. brasiliensis is limited to a description of courtship (Brisson 1986) and a scale of ovarian maturation defined in terms of morphohistological traits (Quintero & Garcia 1998). Information on the reproductive performance of this species in captivity is even more limited. Therefore, this study aims to compare the reproductive performance of wild F. paulensis and F. brasiliensis in captivity, and to identify differences between the species relevant to the management of the maturation period.

MATERIALS AND METHODS

Animals and Acclimation

F. paulensis and F. brasiliensis broodstocks (n = 500) were collected in offshore waters in Santa Catarina (26054' S, 48%4' W) on November 7, 2011, and transferred to the Marine Station of Aquaculture of the Federal University of Rio Grande. The animals were stocked at 7 shrimp/[m.sup.2] (male-to-female ratio, 1:1.3) in three circular maturation tanks (3.6 m in diameter, 5,000 L) for each species and were acclimated for 1 wk. During this period, the broodstocks were fed 4 times daily with blue crab Callinectes sapidus, squid Illex argentinus, fish Macrodon ancylodon, and a commercial diet (Breed S Inve Aquaculture, Belgium) in alternation. The seawater (33 [+ or -] 1 ppt) was renewed daily at a 100% rate and maintained at a temperature of 27 [+ or -] 1[degrees]C. A 14-h/10-h light/dark artificial photoperiod was used.

Female Reproductive Performance

After acclimation, all captured females were unilaterally eyestalk ablated and maintained under the same acclimation conditions. To obtain measures of reproductive performance, females with mature ovaries were identified daily for 10 days, totaling 10 individuals for each species, which were used to measure the parameters evaluated in this study. The gonads were examined using a flashlight to illuminate the ovaries in contrast to the white bottom of the maturation tanks. The mature females were weighed and transferred to 120-L tanks. After spawning, the females were returned to their original tank, and the time in days from ablation to spawning was recorded. The number of eggs per spawning was estimated with three samples of 250 mL taken after the water mixed. The fertilization rates were determined by examining the eggs under a microscope. In addition, three samples of 100 eggs were collected to determine hatching rates, and three samples of 100 nauplii were collected to evaluate the rate of metamorphosis to protozoa. The samples of eggs and nauplii were maintained in 1-L beakers with gentle aeration and at 27 [+ or -] 1[degrees]C.

Sperm Quality

After a week of acclimation, males (n = 12 for each species) in the intermolt stage were selected and weighed. Both spermatophores of all males were extruded manually. One spermatophore was selected at random, weighed to the nearest 0,001 g, and homogenized in 2 mL calcium-free saline solution and 0.1 mL trypan blue. Sperm counts, abnormal cells (malformations of the main body or absence of the spike), and dead cells (blue coloration) were estimated with cell counts using a hemacytometer under a light microscope. Spermatophore melanization was checked by visual examination of the coxae of the 5th pereopod pair and the extruded spermatophore.

Statistical Analysis

The data on the proportions of normal and dead sperm were arcsine transformed before analysis, but only the untransformed values are presented. Previous to the analysis, the necessary statistical assumptions were evaluated. Analysis of variance (ANOVA) was used to identify significant differences in the mean values of reproductive performance among species. The statistical analyses were used at P < 0.05.

RESULTS

Female Reproductive Performance

The body weight of F. paulensis and F. brasiliensis females did not differ significantly. F. brasiliensis spawned sooner after ablation. The number of eggs and the fertilization, hatching, and metamorphosis rates did not differ significantly between the species. In addition, the total numbers of eggs, nauplii, and protozoa produced by F. brasiliensis were higher (Table 1).

The main management-related difference between the species was observed for females. It was not possible to see the gonadal maturation stage of F. brasiliensis clearly by using a flashlight to create a contrast with the white bottom of the maturation tanks.

Sperm Quality

The body weight of the males did not differ significantly between the species. The spermatophore weight and sperm count of F. brasiliensis were significantly higher. The proportions of normal and dead sperm did not differ between the species. No males of F. brasiliensis selected for analysis showed spermatophore melanization (Table 2).

DISCUSSION

Shrimp reproductive performance may be affected by different factors, including weight, which is generally correlated positively with the number of eggs and the sperm count (Racotta et al. 2003). Cavalli et al. (1997) evaluated the relation between weight and reproductive performance in F. paulensis, and suggested the use of males weighing 20 g or more and females weighing 50 g or more for reproduction in captivity. This relation is still unknown for F. brasiliensis. However, in this study, the broodstock weight was similar for the two species and approximately equal to that recommended for F. paulensis. Thus, the interspecific differences in reproductive performance observed in this study were not related to the weight of the shrimp.

The results of this study indicate that F. brasiliensis can be made to reproduce in captivity by applying the methods developed for F. paulensis. The main identified difference of management was related to the visualization of the female's maturation stages. The gonadal maturation stage of female F. paulensis can be visualized daily using a flashlight to create a contrast with the white bottom of the maturation tanks (Marchiori 1996). The carapace of F. brasiliensis is darker than that of F. paulensis. For this reason, the females of F. brasiliensis need to be removed from the tanks and examined to obtain a more reliable daily selection of mature individuals.

F. brasiliensis spawned sooner after ablation. This pattern is also evident from a comparison of different studies of the reproductive performance of these two species in captivity. Peixoto et al. (2004) reported that size and age can affect the time from ablation to spawning in female F. paulensis. For example, small females, 10 mo old, spawned in 17 days on average, whereas larger females, 16 mo old, spawned in 9 days on average. Wild F. paulensis spawned in 11 days, whereas domesticated females spawned in 9 days (Peixoto et al. 2008). Lopes et al. (2011) reported the only previous results on F. brasiliensis, which was found to spawn in 6 days on average. Thus, F. brasiliensis apparently responds more rapidly to the induction of gonadal maturation through unilateral eyestalk ablation. This more rapid response can be a consequence of the hardiness of this species, which would be more resistant to the stress of captivity and would respond more rapidly to the conditions used to produce maturation (Lopes et al. 2011).

The hardiness of F. brasiliensis did not result in better female reproductive performance. The number of eggs per spawning and the fertilization, hatching, and metamorphosis rates did not differ between the species and were similar to those previously found for F. paulensis (Peixoto et al. 2004, Nakayama et al. 2008a, Nakayama et al. 2009). Although the same weight and the same number of subjects were used for the two species, the total numbers of eggs, nauplii, and protozoa produced by F. brasiliensis was higher than those produced by F. paulensis.

However, the apparent hardiness of F. brasiliensis may have affected spermatophore quality. No males of this species showed spermatophore melanization, whereas 8.33% of the F. paulensis males had melanized spermatophores. The occurrence of melanization is associated with the physiological condition of the animal (Alfaro & Lozano 1993). Melanization is produced by the prophenoloxidase system (proPO), an inactive proenzyme present in the hemolymph. The proPO is activated to phenoloxidase (PO), the enzyme responsible by synthesis of a toxic molecule called melanin. The activation of proPO to PO may be caused by the invasion of microorganisms (male reproductive system melanization) or by atypical deposition as a result of the reduction of immunological capacity produced by captivity-related stress (male reproductive tract degenerative syndrome) (Alfaro et al. 1993, Sanchez et al. 2001, Sarathi et al. 2007). The melanization observed in this study was present only in F. paulensis apparently the specie more sensitive to captivity stress.

No information about the spermatophore and the sperm quality parameters of F. brasiliensis is currently available. The spermatophores of F. paulensis males weighing 20-27 g generally weigh 7-27 mg and contain between 1.2-6 million sperm cells (Cavalli et al. 1997, Peixoto et al. 2004, Nakayama et al. 2008b, Braga et al. 2010). In this study, the spermatophore weight and sperm count of F. brasiliensis were significantly higher than F. paulensis, but the averages for the two species were similar to those found for F. paulensis by other authors (Cavalli et al. 1997, Peixoto et al. 2004, Nakayama et al. 2008b, Braga et al. 2010).

Microscopic identification of abnormal cells by the criteria of main body malformations or the absence of a spike has been used in some penaeids (Bray & Lawrence 1998, Perez-Velazquez et al. 2001, Perez-Velazquez et al. 2002, Meunpol et al. 2005). Moreover, the percentage of dead sperm has been estimated by dyeing with trypan blue (Ceballos-Vazquez et al. 2003, Ceballos-Vazquez et al. 2004, Goimier et al. 2006). In this study, the proportions of normal and dead sperm did not differ between F. paulensis and F. brasiliensis. No previous information on the proportions of normal and dead sperm as determinate by the methods of this study is available for either species. However, the values found in this study are similar to those reported for wild Litopenaeus setiferus. This species exhibited 75-90% normal sperm at the beginning of an extreme-temperature experiment (Pascual et al. 2003), and approximately 0% dead sperm when maintained at 26[degrees]C (Pascual et al. 1998). Although these methods are frequently used, they can lack precision, primarily because the interpretation of spermatozoa malformation may vary with the observer. Thus, other methods to evaluate accurately the viability of sperm should be tested and compared with those commonly used.

Spermatophore and sperm quality parameters, mainly sperm count and sperm viability, can affect larval production through a decrease in fertilization and hatching rates (Pratoomchat et al. 1993). In this study, the higher sperm count of F. brasiliensis did not correspond to differences in fertilization rate, and larval production between the two species probably the result of the similarity in sperm viability of the species.

Commercial interest in the pink shrimp species may be justified by better prices compared with white shrimp, especially in the Asian market. F. paulensis was commercially produced in pen enclosures in the Patos Lagoon estuary (southern Brazil) during the past decade (Poersch et al. 2006). F. brasiliensis is recognized as a candidate species for aquaculture because populations remain abundant in the wild, and growth rates under culture conditions are relatively good (Gaxiola et al. 2010). Unlike of F. paulensis, this specie was not still commercially produced and more experimental studies are needed to evaluate the feasibility of its growth and, mainly, reproduction in captivity. Thus, the results obtained in this study can be useful to enable the larval production of this species in captivity using the existing methods for F. paulensis, and reinforce that F. brasiliensis is a candidate for aquaculture also because its hardiness to maturations technical and captivity conditions.

CONCLUSIONS

Reproduction in F. brasiliensis is feasible in captivity using the existing technological method for F. paulensis. However, unlike this species, F. brasiliensis females need to be removed from the tanks for accurate daily visualization of the stage of gonadal maturation. The larval production of the two species is similar, but F. brasiliensis apparently responds more rapidly to the induction of ovarian maturation through unilateral eyestalk ablation, and spawns sooner after ablation. F. brasiliensis also shows better spermatophore quality, represented by higher spermatophore weight and sperm count, and does not show melanized spermatophores.

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ANDRE L. BRAGA, (1,2) DIOGO L. A. LOPES, (2) DARIANO KRUMMENAUER, (2) LUIS H. POERSCH (2) AND WILSON WASIELESKY JR. (2) *

(1) Oceanography Institute, Federal University of Rio Grande, C.P. 474, Rio Grande (RS), 96 201-900, Brazil; [2] Marine Station of Aquaculture, Oceanography Institute, Federal University of Rio Grande, C.P. 474, Rio Grande (RS), 96 201-900, Brazi

* Corresponding author. E-mail. manow@mikrus.com.br

DOI: 10.2983/035.030.0339
TABLE 1.
Female reproductive performance in the wild pink shrimp
Farfantepenaeus paulensis and Farfantepenaeus brasiliensis.

                                               F. paulensis
Parameters                                       (n = 10)

Body weight (g)                          51.53 [+ or -] 8.62 (a)
Time from ablation to                     5.20 [+ or -] 1.61 (a)
  spawning (days)
Eggs/spawning (X[10.sup.3])                121 [+ or -] 90 (a)
Fertilization rate (%)                   75.33 [+ or -] 24.32 (a)
Hatching rate (%)                        31.50 [+ or -] 24.62 (a)
Metamorphosis rate to                    70.65 [+ or -] 26.28 (a)
  protozoa (%)
Total number of eggs (X[10.sup.3])                1,215
Total number of nauplii (X[10.sup.3])             288.30
Total number of protozoa (X[10.sup.3])            203.68

                                              F. brasiliensis
Parameters                                       (n = 10)

Body weight (g)                          51.61 [+ or -] 5.02 (a)
Time from ablation to                     3.40 [+ or -] 1.57 (b)
  spawning (days)
Eggs/spawning (X[10.sup.3])                154 [+ or -] 87 (a)
Fertilization rate (%)                   80.44 [+ or -] 26.96 (a)
Hatching rate (%)                        45.40 [+ or -] 20.42 (a)
Metamorphosis rate to                    82.45 [+ or -] 27.52 (a)
  protozoa (%)
Total number of eggs (X[10.sup.3])                1,542
Total number of nauplii (X[10.sup.3])             563.13
Total number of protozoa (X[10.sup.3])            464.30

Different superscript letters in the same row indicate
significant  differences (ANOVA, P < 0.05).

TABLE 2
Spermatophore and sperm quality of the wild pink shrimp
Farfantepenaeus paulensis and Farfantepenaeus brasiliensis.

                                   F. paulensis
Parameters                            (n = 12)

Body weight (g)              22.74 [+ or -] 4.29 (a)
Spermatophore weight (mg)       21 [+ or -] 8 (a)
Melanization (%)                     8.33
Sperm count (X[10.sup.6)      4.07 [+ or -] 1.92 (a)
Normal sperm rate (%)        74.41 [+ or -] 18.55 (a)
Dead sperm rate (%)           0.23 [+ or -] 0.38 (a)

                                 F. brasiliensis
Parameters                           (n = 12)

Body weight (g)              25.23 [+ or -] 3.13 (a)
Spermatophore weight (mg)       32 [+ or -] 6 (b)
Melanization (%)                      0
Sperm count (X[10.sup.6)      6.81 [+ or -] 2.77 (b)
Normal sperm rate (%)        70.53 [+ or -] 15.18 (a)
Dead sperm rate (%)           0.05 [+ or -] 0.09 (a)

Different superscript letters in the same row indicate
significant differences (ANOVA, P < 0.05).
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