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Effects of Androgenic Gland Ablation on Growth, Sexual Characters and Spermatogenesis of the White Shrimp, Litopenaeus Vannamei (Decapoda: Penaeidae) Males

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Effects of Androgenic Gland Ablation on Growth, Sexual Characters and Spermatogenesis of the White Shrimp, Litopenaeus Vannamei (Decapoda: Penaeidae) Males Aquaculture Research, 2015, 1–10 doi:10.1111/are.12727 Effects of androgenic gland ablation on growth, sexual characters and spermatogenesis of the white shrimp, Litopenaeus vannamei (Decapoda: Penaeidae) males Jorge Alfaro-Montoya1,Luıs Hernandez-Noguera 1,Luıs Vega-Alpızar1 & Rodolfo Umana-Castro~ 2 1Estacion de Biologıa Marina: Lic. Juan Bertoglia Richards, Escuela de Ciencias Biologicas, Universidad Nacional, Puntarenas, Costa Rica 2Laboratorio de Analisis Genomico, Escuela de Ciencias Biologicas, Universidad Nacional, Heredia, Costa Rica Correspondence: J Alfaro-Montoya, Estacion de Biologıa Marina: Lic. Juan Bertoglia Richards, Escuela de Ciencias Biologicas, Universidad Nacional, Puntarenas, Costa Rica. E-mail: [email protected] has been identified in many crustaceans including Abstract amphipods, isopods and decapods (Ventura, Rosen This research was implemented to study the effects & Sagi 2011). In decapods, the insulin-like andro- of androgenic gland ablation in the white shrimp genic hormone (IAG) was found to regulate the Litopenaeus vannamei to explore sex reversal poten- masculinization of primary and secondary sexual tial as an alternative technology for monosex characters (Ventura & Sagi 2012). female mariculture based on the sex dimorphic In the family Penaeidae, the complete cDNA of growth of this species. The surgical procedure was IAGs, of the giant tiger prawn Penaeus monodon, applied to male postlarvae (PL) at different ages, the kuruma prawn Marsupenaeus japonicus and the after external sex differentiation, as well as in sex Chinese shrimp Fenneropenaeus chinensis (Li, Li, undifferentiated PL. Andrectomized males regener- Sun & Xiang 2012) have been reported. The defin- ated normal appendices including pereiopods and itive demonstration of the AG structure and loca- pleopods; however, body growth and relative size tion by molecular probes has been done in of regenerated petasmas and appendices masculi- P. monodon and F. chinensis (Banzai, Ishizaka, As- nae were statistically inferior (P ˂ 0.05) to control ahina, Suitoh, Izumi & Ohira 2011; Mareddy, males. Spermatogenesis in andrectomized males Rosen, Thaggard, Manor, Kuballa, Aflalo, Sagi, was active, but a phenomenon of degradation of Paterson & Elizur 2011; Li et al. 2012). spermatids and reproductive tissues was detected. In the most economically important penaeid No sex reversal was accomplished regardless of PL species: the white shrimp Litopenaeus vannamei, the age from sex undifferentiated stages (PL38) to complete sequence of the IAG gene was recently sex differentiated stages (˃PL55). The complete reported (Vazquez-Islas, Garza-Torres, Guerrero- regeneration of sexual characters in andrectomized Tortolero & Campos-Ramos 2014). The histology L. vannamei (Dendrobranchiata) is different from of the presumptive AG of Litopenaeus, including previous reports from Decapoda. the southern shrimp Litopenaeus setiferus, the white shrimp Litopenaeus occidentalis, the blue shrimp Li- Keywords: Penaeidae, androgenic gland, Litope- topenaeus stylirostris and L. vannamei has been par- naeus vannamei, sex reversal, shrimp tially described (Campos-Ramos, Garza-Torres, Guerrero-Tortolero, Maeda-Martınez & Obregon- Barboza 2006; Garza-Torres, Campos-Ramos & Introduction Maeda-Martınez 2009; Alfaro-Montoya & Hernan- Malacostracan crustaceans control sex differentia- dez 2012; Vazquez-Islas et al. 2014). These find- tion by the androgenic gland (AG) that releases ings indicate that the AG in Litopenaeus is the androgenic hormone. This insulin-like peptide associated to the terminal ampoule and stretched © 2015 John Wiley & Sons Ltd 1 Androgenic gland ablation in Litopenaeus vannamei J Alfaro-Montoya et al. Aquaculture Research, 2015, 1–10 along the distal region of the descending vas defer- Regeneration of pereiopods and male sexual ens. The aim of this study is to evaluate the effects characters of the ablation of the presumptive AG (andrecto- my) associated with the terminal ampoules of Litopenaeus vannamei postlarvae were collected L. vannamei on growth, male sexual characters from commercial farms after 15 days of culture and spermatogenesis. (PL 25-35), and transported to EBM for further culture in laboratory tanks (volume = 330 L) until reaching the following PL stages. Three Materials and methods groups of males (MA: n = 25, PL180, MB: n = 74, PL70 and MC: n = 60, PL55 to 107, See Evaluation of L. vannamei dimorphic growth Table 1) were andrectomized and monitored for under pond and tank culture regeneration of pereiopods, petasmas and appendi- The growth of 358 organisms cultured in a com- ces masculinae. Animals were mounted dorsally mercial semi-intensive earthen pond in Golfo de Ni- on Velcro straps or moulding clay under a dis- coya, Costa Rica, was recorded monthly as body secting stereo microscope. Petasma identification weight (BW) from postlarvae stage 12 (PL12) to was done by removing the left first pleopod. Iden- PL108. Conventional aquaculture systems for tified males were andrectomized. The coxas of the L. vannamei harvest 3-month old animals; therefore, fifth walking legs were removed, as well as the to evaluate dimorphic growth after harvesting age, terminal ampoules, the adjacent AGs, and vasa a complementary tank culture experiment was deferentia using fine tweezers. The appendix mas- implemented. Three groups of 160 animals each culina associated with the left second pleopod were harvested from commercial ponds at 21, 20 was removed leaving the right pleopod intact as and 16 g BW for groups A: rainy season culture, B: control. The regeneration of the ablated pleopod rainy-dry season culture and C: dry-rainy season served as an additional tool to monitor the effects culture respectively. Each group was grown in a of AG ablation. separated shaded external tank (18 m2; 20 MT; 9 shrimp per m2) at different periods of the year, Andrectomy of sex differentiated individuals allowing to compare performance under dry and rainy seasons. Culture time was different for each Litopenaeus vannamei postlarvae from group B (pre- group depending on actual growth rate and it lasted vious experiment: PL70, BW = 4.36 Æ 1.44 g) until reaching at least 30 g for females at Estacion were further evaluated against a control group for de Biologıa Marina (EBM) in a flow-through system, body growth and re-development of sexual charac- using new water pretreated by high-pressure silica ters based on the following treatments: sand filtration and sedimentation. Animals were fed Andrectomy (AN): As described above. First and at 3% BW of a dry commercial feed (Nicovita©, 30% second left pleopods were removed (n = 34). protein, Callao, Peru) supplemented with fresh fro- Control (CO): removal of fifth walking legs dam- zen sardines (Opistonema sp.). Sex and BW was aging neither the coxa nor the ampoule-vas defer- monitored monthly in the three groups by popula- ens. First and second left pleopods were also tion samples of n = 20 animals. removed (n = 28). Males from both treatments were maintained in the same tank (water volume = 330 L) under Identification of the AG a flow-through system, using new water pre- Bilaterally eyestalk ablated L. vannamei males treated by high-pressure silica sand filtration and (n = 3, 30 g BW), were anaesthetized in cold sedimentation. Salinity was 32 ppt, temperature water (20°C) 8 days post eyestalk ablation, and was maintained at 28°C, and the photoperiod andrectomized by removing the coxas of their fifth was 13:11 (L:D). Animals were fed daily ad libi- pereiopods and the associated terminal ampoules. tum with Nicovita© feed (30% protein). After Samples of ampoules were fixed in Davidson’s 4 months of culture, males from both treatments solution for 24 h, dehydrated in ethyl alcohol, were inspected for the presence of ampoules/ paraffin embedded and serially sectioned in cross- spermatophores (CO) or absence of ampoules/ orientation. Sections were stained in Hematoxylin spermatophores (AN), and measured in terms of and Eosin. BW (g), total length (TL, mm; measured from 2 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 1–10 Aquaculture Research, 2015, 1–10 Androgenic gland ablation in Litopenaeus vannamei J Alfaro-Montoya et al. Table 1 Evaluation of microsurger- ies of fifth pereiopods on Litopenaeus Experimental groups vannamei males Parameter MA MB MC Number of microsurgeries 25 74 60 Culture time (months) 8 4 3 Initial PL stage 180 70 55–107 Initial size (mm) 97.8 Æ 6.4 69.1 Æ 7.8 36.6 Æ 3.6 Initial weight (g) – 4.36 Æ 1.44 0.50 Æ 0.23 Surgery mortality (%) 24 16 23 Number of final survivors 14 47 12 Survival (%) 74 76 26 Final size (mm) 117.9 Æ 7.7 110.5 Æ 7.3 54.4 Æ 12.3 Final weight (g) 22.46 Æ 4.79 18.19 Æ 3.52 — Regeneration of fifth pereiopods (%) 100 100 100 Regeneration of left petasma (%) 100 100 100 Regeneration of left appendix – 100 100 masculine (%) the eyestalk base to the tip of telson), regener- previously, paraffin embedded, sectioned and ated petasma length (PEL) and petasma width stained in Hematoxylin and Eosin. (PEW, mm) and regenerated appendix masculina length (APL) and appendix masculina width Statistics (APW, mm). Body weights and lengths were analysed using t- test for independent samples, at P < 0.05 (Ott Ablation of sex undifferentiated postlarvae 1984), using the program GNU PSPP version Litopenaeus vannamei postlarvae at PL30 were col- 0.8.1 (Boston, MA, USA). Male petasma and lected from a commercial farm, transported to appendix masculina measurements were normal- EBM for further culture in laboratory tanks. Sex ized as follows: relative petasma length, undifferentiated PL38 (BW = 0.052 Æ 0.015 g) RPEL = PEL/TL; relative petasma width, were selected for the following treatments: RPEW = PEW/TL; relative appendix masculina Ablation (ABL): removal of fifth walking legs at length, RAPL = APL/TL; relative appendix mascu- PL38 as described above (n = 60). lina width, RAPW = APW/TL. Normalized data Control (CO): Non treated group of PL38 were analysed by linear regression and t-test for (n = 92). independent samples, at P < 0.05 (Ott 1984). Both groups were cultured in separated tanks The Levene statistic was applied to test for homo- (330 L), since gross external signs of andrectom- geneity of variance.
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