Effects of age and size on reproductive performance of captive ...

Aquaculture 238 (2004) 173 – 182 www.elsevier.com/locate/aqua-online

Effects of age and size on reproductive performance of captive Farfantepenaeus paulensis broodstock Silvio Peixoto *, Ronaldo O. Cavalli, Wilson Wasielesky, ˆ ngela M. Milach Fernando D’Incao, Dariano Krummenauer, A Laborato´rio de Maricultura, Departamento de Oceanografia, Fundacßaõ Universidade Federal do Rio Grande, C.P. 474, 96201-900 Rio Grande, RS, Brazil Received 10 October 2003; received in revised form 15 December 2003; accepted 12 April 2004

Abstract The performance of captivity-reared Farfantepenaeus paulensis broodstock of different ages (10 and 16 months old) and sizes were compared in two separate 30-day-long trials. For each trial, groups of 20 males and 30 unilaterally eyestalk-ablated females were stocked into two 10-m2 maturation tanks. Data on male quality (spermatophore weight and sperm count), spawning performance, hatching rates and metamorphosis to the first protozoa stage (PZI) were recorded. Histological analysis of the ovary of ready-to-spawn females was also carried out. Older males had significantly heavier spermatophores but these did not necessarily contain a higher number of sperm cells. Size rather than age appears to have a more important role in the regulation of the number of sperm cells per spermatophore. Within the same age group, larger females had a superior spawning performance than smaller ones. No significant differences in percentages of fertilization, hatching and metamorphosis to the first protozoa stage were detected. Similar to other studies with penaeids, our results suggest that female size rather than age exerts a stronger effect in determining the reproductive performance of F. paulensis. The present study also demonstrates that 10-month-old F. paulensis females reared in captivity and weighing 25 g or more may be successfully used for reproductive purposes, although significant improvements on reproductive output will be achieved if older (16-month-old) and larger ( z 45 g) females are used. D 2004 Elsevier B.V. All rights reserved. Keywords: Age; Size; Sperm quality; Spawning performance; Farfantepenaeus paulensis

* Corresponding author. E-mail address: [email protected] (S. Peixoto). 0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2004.04.024

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S. Peixoto et al. / Aquaculture 238 (2004) 173–182

1. Introduction The penaeid shrimp Farfantepenaeus paulensis is a native species in the western Atlantic Ocean from Ilheús (14j50VS), Brazil to Mar del Plata (38j30VS), Argentina (D’Incao, 1991). This species has been considered a suitable shrimp either for pond farming (Peixoto et al., 2003a) or for estuarine pen culture in southern Brazil (Wasielesky et al., 2000). Although nauplii production of F. paulensis originally relied on the use of wild breeders (Marchiori and Boff, 1983; Marchiori and Cavalli, 1993), recent studies have focused on the management and reproduction of captive broodstock due to the unpredictability and high costs associated with the capture of the wild stocks (Cavalli et al., 1997; Peixoto et al., 2003b). Several studies have been performed to close the life cycle and improve reproductive performance of different penaeid species in captivity (Ogle, 1992; Luis and Ponte, 1993; Makinouchi and Hirata, 1995; Ramos et al., 1995). It is generally accepted by hatchery managers and researchers that captive broodstock should be of an appropriate age and size for successful maturation (Browdy, 1992, 1998). Nevertheless, it is difficult to separate whether reproductive performance is age- or size-dependent as shrimps of similar size may not be of the same age and vice versa (Dall et al., 1990; Bray and Lawrence, 1992). Although fecundity in penaeids has been reported to increase with female size (Motoh, 1981; Makinouchi and Primavera, 1987; Cavalli et al., 1997; Hoang et al., 2002), results from studies examining the relationship between male size and sperm quantity have varied (Pratoomchat et al., 1993; Alfaro, 1993; Dıáz et al., 2001). The effect of age on reproductive performance has been assessed traditionally by either using know-age pond-reared broodstock (Primavera, 1978; Motoh, 1981; Makinouchi and Hirata, 1995; Ramos et al., 1995; Cavalli et al., 1997) or age estimations based on length– frequency analysis for wild-caught shrimps (Crocos and Coman, 1997; Cavalli et al., 1997; Peixoto et al., 2003b; Coman and Crocos, 2003). However, few studies have simultaneously compared the influence of age and size on the maturation of penaeid females (Hoang et al., 2002) and males (Ceballos-Va´squez et al., 2003) from the same breeding population. The aim of this study was to evaluate the influence of different ages (10 and 16 months old) and sizes on the reproduction of F. paulensis females and males reared under captive conditions. This knowledge may provide a further basis for the selection of broodstock with improved reproductive performance.

2. Material and methods 2.1. Rearing of broodstock The culture system was semi-intensive and consisted of three stages: nursery, pen culture and broodstock production. Postlarvae (PL) were produced in the Laboratory of Mariculture, University of Rio Grande, from wild broodstock captured offshore in southern Brazil (27jS) at depths of 35 – 40 m. PL10 (10-day-old) were cultured in a 10m2 nursery tank for 1 month (December, 2001) and were then transferred to a grow-out pen enclosure (3100 m2) in the Patos Lagoon estuary (Wasielesky et al., 2000). After 5


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months (January to May, 2002), shrimp were harvested and a total of 500 animals were divided in two size classes (small and large) according to a frequency distribution for body weight (BW) and carapace length (CL). These classes of shrimp juveniles were then stocked separately in 22-m2 raceway tanks enclosed in a greenhouse for broodstock production for the next 10 months (until the end of March, 2003). The rearing tank, environmental conditions and husbandry protocols were the same as described in Peixoto et al. (2003b). Animals were fed ad libitum once a day (1700 h) alternating fresh frozen crab (Callinectes sp.), squid (Illex sp.), shrimp (Artemesia longinaris), fish (several species) and a maturation diet (W/IMM crude protein 40%; Zeigler Bros.; Gardners, PA, USA). During broodstock culture, water temperature, salinity, pH and dissolved oxygen were monitored daily at 0900 and varied between 18 and 31 jC, between 33 and 35 ppt, between 7.3 and 8.9 and between 3.3 and 9.2 mg/l, respectively. 2.2. Experimental design Reproductive performance was assessed in two trials at the ages of 10 and 16 months. For each trial, two size classes were established for males and females based on the frequency distribution for body weight and carapace length. Groups of 20 males and 30 unilaterally eyestalk-ablated females were stocked into two 10-m2 maturation tanks at a stocking density of five animals/m2 and a female to male ratio of 1.5. Animals were allowed to acclimate to tank conditions for 2 days before unilateral eyestalk ablation of females was performed by cutting and cauterizing the eyestalk. Additionally, females had their uropods clipped and a color ring added to the remaining eyestalk for individual marking. Water was exchanged at a rate of 50%/day and salinity was monitored daily. Water temperature was controlled by submerged heaters and was monitored daily. Light intensity was approximately 2 AE/m2/s, with a photoperiod of 14-h light:10-h darkness. Feed was offered in four daily portions (0900, 1200, 1500 and 1800 h) of fresh frozen fish (various species), shrimp (A. longinaris), squid (Illex sp.) and crab (Callinectes sp.), respectively. All procedures adopted during the reproduction trials were standardized including broodstock selection and handling, diet and maturation protocols. The experimental period for each trial started 1 day after eyestalk ablation and lasted for 30 days. 2.3. Male quality and spawning performance Carapace length (CL, distance from the postorbital margin to the middorsal posterior edge of the carapace) and body weight (BW) were recorded for all females and males prior to each trial. Females with mature ovaries (stage III) were sourced out daily at 1800 h, according to the criteria proposed by Peixoto et al. (2003c) and then transferred into separate 90l spawning tanks. The number of eggs was estimated from three 100-ml replicate samples of the spawning tank water, collected after homogenization. Fertilization rates were determined microscopically following Primavera and Posadas (1981). Hatching rates and metamorphosis to the first protozoa stage (PZI) were obtained by placing random samples of, respectively, 100 eggs and 100 nauplii in three 1-l beakers with gentle aeration and controlled water temperature (26 F 1 jC). Additionally, reproductive performance was

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assessed in terms of the interval between eyestalk ablation and molting, the interval between eyestalk ablation and first spawn, spawning rate (number of spawns/female stocked), spawning interval (for successive spawns), number of eggs per spawning (for females that spawned at least once) and number of eggs per female (total egg production/ female stocked). At the end of the experimental period, males had their spermatophores extruded by gently pressing around the coxae of the fifth pair of pereopods (Petersen et al., 1996). Both sides of the compound spermatophore were weighed and the quantities of sperm were determined using a Neubauer hemacytometer by homogenizing each spermatophore in a calcium-free solution and by counting the sperm cells under light microscopy (LeungTrujillo and Lawrence, 1987). 2.4. Ovarian histology Histological analysis of mature ovaries was performed by selecting ready-to-spawn females 2 weeks after eyestalk ablation. In order not to compromise the data on spawning performance, the number of ovaries sampled varied from 4 to 5 per treatment, according to the availability of mature females. After the dissection of the ovary, the gonadosomatic index (GSI) was calculated as a percentage of the ovarian weight relative to the body weight. The procedures adopted for ovarian histology and the descriptions of maturation stages are detailed in previous studies (Peixoto et al., 2002a, 2003c). Digitized images from each ovary were used to record the frequency and diameter of different oocyte types according to Peixoto et al. (2003c). 2.5. Statistical analysis Based on the size and age of females and males, four treatments were established: S10 (small class, 10 months old), L10 (large class, 10 months old), S16 (small class, 16 months old) and L16 (large class, 16 months old). Initially, variation in reproductive performance was analyzed for all individuals within each size and age class using a oneway ANOVA in which individuals were treated as replicates. The results of this analysis showed that there was no significant variation ( P>0.05) between individuals within each age and size class. Subsequently, the data for all individuals within treatments were pooled and variation in reproductive performance among treatments analyzed by oneway ANOVA followed by a Tukey posthoc comparison test ( P = 0.05). Percentage data (e.g., fertilization and hatching rates, metamorphosis to PZI, GSI and frequency of oocyte type) were arcsine transformed for analysis but only original values are presented.

3. Results There were no significant differences in physicochemical parameters among the maturation tanks used in the trials. Water temperature ranged from 26 to 28 jC and salinity from 32 to 34 ppt.


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Table 1 Means ( F S.D.) of carapace length, body weight, spermatophore weight, and sperm count per spermatophore among groups of Farfantepenaeus paulensis males (n = 20) from different combinations of size (small and large) and age (10 and 16 months) classes S10 Carapace length (mm) Body weight (g) Spermatophore weight (mg) Sperm count/spermatophore ( 106)

L10 a

S16 b

24.2 F 0.3 10.3 F 0.4a 7.7 F 0.8a 1.23 F 0.17a

L16 c

27.8 F 0.3 15.1 F 0.5b 12.3 F 0.8b 0.92 F 0.19a

35.5 F 0.2d 30.2 F 0.4d 18.5 F 0.8c 2.27 F 0.19b

32.6 F 0.2 24.5 F 0.8c 16.3 F 0.8c 1.38 F 0.17a

Different superscripts within rows indicate significant differences ( P < 0.05).

3.1. Quality of males There were significant differences in initial carapace length and body weight between each of the groups of males (Table 1). Statistically significant differences were found in spermatophore weight between the 10-month-old groups. However, no significant differences were found between 16-month-old groups. Sperm counts were significantly greater in the L16 group that all other groups (Table 1). 3.2. Spawning performance Initial carapace length and body weight of females differed significantly between treatments (Table 2). Within the same age group, overall spawning performance of larger F. paulensis was superior to that of smaller individuals. Larger shrimps tended to have a longer intermolt period after eyestalk ablation but an opposite trend was observed for the time elapsed for the first spawn after ablation. Significantly higher spawning rate (2.9 spawns/female), number of eggs per spawn (147.4 103) and egg production per female (421.6 103) were obtained for the L16 females. Nevertheless, the same variables did not Table 2 Mean values ( F S.D.) of carapace length, body weight and overall spawning performance among groups of Farfantepenaeus paulensis females (n = 30) from different combinations of size (small and large) and age (10 and 16 months) classes during 30 days S10 Carapace length (mm) Body weight (g) Spawns recorded Ablation to molt (days) Ablation to first spawn (days) Spawning rate (spawns/females) Spawning interval (days) Eggs/spawning ( 103) Eggs/female ( 103) Fertilization rate (%) Hatching rate (%) Metamorphosis to the first protozoa stage (%)

L10 a

27.5 F 0.3 14.7 F 0.7a 3 9.5 F 1.2a 17.0 F 3.3a 0.2 F 0.3a 5.0 F 4.4a 35.8 F 37.7a 7.2 F 42.7a NA NA NA

S16 b

33.9 F 0.3 25.8 F 0.7b 22 11.8 F 1.2ab 11.4 F 1.3b 1.4 F 0.3b 4.9 F 1.6a 86.4 F 14.6a 123.6 F 44.1b 72.2 F 11.7a 41.5 F 9.4a 87.0 F 3.4a

L16 c

39.1 F 0.3 36.3 F 0.8c 30 14.6 F 1.7b 10.6 F 1.1b 1.8 F 0.3b 8.0 F 1.2a 101.5 F 11.9a 179.2 F 40.0b 69.7 F 6.8a 53.1 F 4.7a 97.9 F 2.1a

Different superscripts within rows indicate significant differences ( P < 0.05). NA = not available.

42.6 F 0.3d 46.7 F 0.7d 66 15.9 F 1.7b 9.2 F 0.9b 2.9 F 0.3c 6.2 F 0.7a 147.4 F 8.4b 421.6 F 34.4c 69.8 F 5.7a 64.1 F 4.9a 97.7 F 2.1a

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Table 3 Mean ( F S.D.) gonadosomatic index (GSI, %), frequency (%) and diameter (Am) of basophilic oocytes (BO), yolky oocytes (YO) and cortical oocytes (CO) in the ovarian tissue of Farfantepenaeus paulensis from different combinations of size (small and large) and age (10 and 16 months) classes L10 (4) GSI BO YO CO BO diameter YO diameter CO diameter

S16 (5) a

4.8 F 0.7 68.2 F 2.9ab 18.8 F 2.1a 13.0 F 3.3a 57.3 F 2.7a 184.6 F 1.8 226.4 F 3.3a

L16 (5) ab

6.1 F 0.6 76.4 F 1.4a 0b 23.6 F 2.7b 71.8 F 2.0b NP 234.0 F 4.9ab

7.7 F 0.6b 64.5 F 1.9b 0b 35.5 F 3.1b 69.8 F 2.2b NP 240.9 F 2.5b

Number of ovaries sampled is between parenthesis. Different superscripts within rows indicate significant differences ( P < 0.05). NP = not present.

differ significantly between S16 and L10 females. The spawning performance of S10 females was clearly inferior compared with the other groups, as indicated by the significant lower spawning rate (0.2 spawns/female) and by the absence of fertile spawns. The percentages of fertilization, hatching and metamorphosis to PZI were not significantly different among L10, S16 and L16 treatments. 3.3. Ovarian histology Ovaries from small 10-month-old females were not sampled for histology due to the limited number of mature females. Histological analysis of the ovaries revealed the presence of larger acidophilic oocytes with cortical rods (CO), clearly indicating that maturation (stage III) was attained in all treatments (Table 3). Although small basophilic oocytes (BO) were observed in all samples, L10 females showed a significantly lower frequency of CO due to the occurrence of yolky oocytes (YO) in two ovaries (stage II). The values of GSI and diameter of CO increased with female size but only differed significantly between L10 and L16.

4. Discussion Previous studies have reported that larger males of Penaeus monodon (61 –90 g) (Pratoomchat et al., 1993) produced significantly heavier spermatophores (56.6 mg) and larger numbers of sperm cells per spermatophore (2.48 106). Similarly, the spermatophore weight (19.1 –93.3 mg) and sperm count per spermatophore (1.04 – 4.57 106) were positively correlated to body weight (24.7 – 38.0 g) for Litopenaeus vannamei (CeballosVa´squez et al., 2003). In contrast, Dıáz et al. (2001) showed that spermatophore weight (51 – 96 mg) increased significantly with the size (5– 20 g) of Pleoticus muelleri but sperm count remained unchanged (2.22 – 5.62 106). These authors hypothesized that spermatophore weight is much more dependable on the structural components than on the amount of sperm cells contained therein. In accordance, the present results for F. paulensis indicate that significant differences in spermatophore weight were probably related to male size,


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especially among the S10, L10 and S16 groups but these differences do not necessarily imply differences in sperm count. Spermatophore weight increased with age, but in the 16-month-old group, the largest males had the higher sperm counts. In contrast to this, Ceballos-Va´squez et al. (2003) studied the relation of age and size on the quality of L. vannamei males and found that the influence of age was independent of body weight. Sexual maturity of wild and captive F. paulensis males is known to occur at an early stage (6 months old) of their life. Nevertheless, for commercial production, males with carapace length and body weight over 28 mm and 16 g, respectively, have been recommended (Cavalli et al., 1997). The performance of large 10-month-old males (L10) from the present study was consistent with this recommendation. Nevertheless, it is unlikely that the lack of fertile spawns for S10 females could be attributed to a lack of sperm as spermatophores were observed in the thelycum after molting and the sperm count was similar to the older and larger males (except the L16 group). Although F. paulensis males smaller than 24 mm CL and 10 g BW could be suitable as sperm donors for artificial insemination purposes (Peixoto et al., 2004), studies are necessary to evaluate the mating success and sperm quality of these males when paired with larger/older females. Sexual maturity and breeding of pond-reared females varies among species (Bray and Lawrence, 1992), with the youngest reported spawning event of a captive penaeid at 5 months old (Primavera, 1978). Hoang et al. (2002) observed that the overall performance of captive Fenneropenaeus merguiensis increased from 7 to 10 months old and declined at 13 months old. Performance of wild Penaeus semisulcatus broodstock was reported to increase from the time of first maturity until 12 months old but declined afterwards (Crocos and Coman, 1997; Coman and Crocos, 2003). Accordingly, Cavalli et al. (1997) argued that senescence was probably the reason for the inferior spawning performance of wild F. paulensis with estimated age of 16.5 months old. However, this finding is not supported in the present study as 16-month-old captive F. paulensis had an overall spawning performance higher than younger age groupings. Furthermore, 16-month-old females were well within the size range (30 to 60 g) recommended for the reproduction of F. paulensis in captivity (Bueno, 1989; Cavalli et al., 1997) and their spawning performance is consistent with previous results for wild broodstock (Marchiori and Boff, 1983; Cavalli et al., 1997, 1998; Peixoto et al., 2003b,d). The longer time elapsed for the first spawn after ablation, lower spawning rate and shorter molting interval of S10 females suggest that their energy was allocated to somatic growth rather than gonadal maturation. Although histological analysis confirmed that maturation (stage III) was attained by L10 females, the presence of yolky oocytes (stage II), lower frequency of cortical oocytes (CO), smaller diameter of CO and lower GSI value may indicate a reduced vitellogenic activity compared to 16-month-old females. Cortical rods are thought to be the precursors of the jelly layer around penaeid eggs which have an important role in their activation (Clark et al., 1990). The absence of cortical oocytes in the ovaries has usually been associated with lower hatching performance in captivity (Medina et al., 1996; Peixoto et al., 2002b). However, the lower frequency of cortical oocytes in L10 females did not appear to compromise the percentages of fertilization, hatching and metamorphosis to PZI because no significant changes for any age/size groupings were evident.

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Although it has been generally accepted that larger, presumably older, penaeid females present a superior spawning performance, the influence of age has been poorly explored (Menasveta et al., 1994; Minagawa et al., 2000). Hoang et al. (2002) reported that larger F. merguiensis females produced a superior overall spawning performance than smaller females of the same age. The effect of size rather than age on the productivity of F. paulensis was previously reported by Cavalli et al. (1997) who used one age class (8– 9 months old) for females (18 – 25 g) obtained from an extensive pond in the southern Brazil (26jS). Similarly, the current study found evidence that at the same age, the spawning performance of larger F. paulensis was superior to that of smaller individuals from the same breeding population reared in raceway tanks. Indoor facilities, such as covered ponds or raceways, have been used for successful overwintering of broodstock in temperate regions, which is crucial to close the cycle of penaeids in such areas (Browdy, 1992; Preston et al., 2004). The present study demonstrated the viability of maintaining and reproducing captive broodstock of F. paulensis in extreme southern Brazil (32jS) where low water temperatures limit broodstock culture in outdoor ponds during the winter. Similarity comparison of spawning performance between L10 and S16 animals indicates that younger females (10 months old) with carapace length and body weight over 33 mm and 25 g, respectively, could be used without significant losses in nauplii production. Nevertheless, significant improvements on reproductive output might be achieved by using older (16 months old) and larger (42 mm CL, 45 g BW) F. paulensis female. The results of this study provide a quantitative basis for optimizing reproductive performance in captive breeding programs for F. paulensis. Acknowledgements Thanks are due to Greg Coman for reviewing the manuscript and to three anonymous referees whose suggestions greatly improved the quality of this paper. Funds for this study were provided by CNPq (no. 471.056/01-4) and FAPERGS (no. 01/0684-4). R.O.C and W.W. acknowledge support as research fellows of CNPq. References Alfaro, J., 1993. Reproductive quality of male Penaeus stylirostris from a grow-out pond. J. World Aquac. Soc. 24, 6 – 11. Bray, W.A., Lawrence, A.L., 1992. Reproduction of Penaeus species in captivity. In: Fast, A.W., Lester, L.J. (Eds.), Marine Shrimp Culture: Principles and Practices. Elsevier, Amsterdam, The Netherlands, pp. 93 – 170. Browdy, C.L., 1992. A review of the reproductive biology of Penaeus species: perspectives on controlled shrimp maturation systems for high quality nauplii production. In: Wyban, J. (Ed.), Proceedings of the Special Session on Shrimp Farming, 22 – 25 May 1992, Orlando, FL, USA, World Aquaculture Society, Baton Rouge, LA, USA, pp. 22 – 51. Browdy, C.L., 1998. Recent developments in penaeid broodstock and seed production technologies: improving the outlook for superior captive stocks. Aquaculture 164, 3 – 21. Bueno, S.L.S., 1989. Tećnicas, Procedimentos e Manejos para a Produçaõ de Po´s-Larvas de Camaro˜es Peneı´deos. CIRM, Brası´lia, Brazil. Cavalli, R.O., Scardua, M.P., Wasielesky, W.J., 1997. Reproductive performance of different-sized wild and pond-reared Penaeus paulensis females. J. World Aquac. Soc. 28, 260 – 267.


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