Abstract
Monosex male culture of C. quadricarinatus is proposed for increasing yields because males reach a larger size at harvest than females. An experiment was done to evaluate the effects of androgenic gland extract and temperature on sex reversal and somatic growth in early juvenile females. Females were exposed to the following experimental conditions: C: control food and temperature maintained at 26 ± 1°C; HT (high temperature): control food and temperature maintained at 28.5 ± 1°C; VHT (very high temperature): control food and temperature maintained at 31 ± 1°C; AG: food with enriched with androgenic gland (1/10 dose for each juvenile per day) and temperature maintained at (26 ± 1)°C. The juveniles were weighed, sexed, and growth increment (GI) and growth rate (GR) were calculated twice a month. The HT and AG groups differed from the C group in GI and GR indicating a greater somatic growth. At the end of the experiment, the HT and AG groups had similar weight but only the HT group had enhanced oocyte diameter, with some vitellogenic oocytes compared to the C group. In the HT group, there was significant sex reversal, as indicated by development of male and intersex male characteristics in different individuals. Both temperature and AG diet have a high potential for culture of this species because of their enhancement of somatic growth; higher temperature increases the proportion of males, a desirable characteristic of cultured populations.
Similar content being viewed by others
References
Abdu U, Yehezkel G, Sagi A (2000) Oocyte development and polypeptide dynamics during ovarian maturation in the red-claw crayfish Cherax quadricarinatus. Invertebr Reprod Dev 37:75–83
Aflalo ED, Hoang TT, Nguyen VH, Lam Q, Nguyen DM, Trinh QS, Raviv S, Sagi A (2006) A new two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 256:468–478. doi:10.1016/j.aquaculture.2006.01.035
Azuma T, Takeda K, Doi T, Muto K, Akutsu M, Sawada M, Sagi A (2004) The influence of temperature on sex determination in sockeye salmon Oncorhynchus nerka. Aquaculture 234:461–473. doi:10.1016/j.aquaculture.2003.11.023
Barki A, Karplus I, Khalaila I, Manor R, Sagi A (2003) Male-like behavioral patterns and physiological alterations induced by androgenic gland implantation in female crayfish. J Exp Biol 206:1791–1797. doi:10.1242/jeb.00335
Bauer RT (2002) Tests of hypotheses on the adaptive value of an extended male phase in the hermaphroditic shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Biol Bull 203:347–357. doi:10.2307/1543577
Brian LV, Leonard WA, Kildea DG (2001) A method for testing the effectiveness of artificial incubation of eggs vs. maternal brooding in the freshwater crayfish Cherax destructor (Decapoda: Parastacidae). Aquaculture 195:299–309. doi:10.1016/S0044-8486(00)00561-5
Calado R, Dinis MT (2007) Minimization of precocious sexual phase change during culture of juvenile ornamental shrimps Lysmata seticaudata (Decapoda: Hippolytidae). Aquaculture 269:299–305. doi:10.1016/j.aquaculture.2007.04.063
Carmona-Osalde C, Rodríguez-Serna M, Olvera-Novoa MA, Gutiérrez-Yurrita PJ (2004) Gonadal development, spawning, growth and survival of the crayfish Procambarus llamasi at three different water temperatures. Aquaculture 232:305–316. doi:10.1016/S0044-8486(03)00527-1
Charniaux-Cotton H, Payen G (1988) Crustacean reproduction. In: Laufer H, Downer RG (eds) Endocrinology of selected invertebrate type. Liss, New York, pp 279–303
Cimino EJ, Owens L, Bromage E, Anderson TA (2002) A newly developed ELISA showing the effect of environmental stress on levels of hsp86 in Cherax quadricarinatus and Penaeus monodon. Comp Biochem Physiol Part A 132:591–598. doi:10.1016/S1095-6433(02)00101-0
Cui Z, Liu H, Lo TS, Chu KH (2005) Inhibitory effects of the androgenic gland on ovarian development in the mud crab Scylla paramamosain. Comp Biochem Physiol Part A 140:343–348. doi:10.1016/j.cbpb.2005.01.017
Curtis MC, Jones CM (1995) Observations on monosex culture of redclaw crayfish Cherax quadricarinatus Von Martens (Decapoda: Parastacidae) in earthern ponds. J Word aquac Soc 26:154–158. doi:10.1111/j.1749-7345.1995.tb00238.x
Edgerton B (2005) Freshwater crayfish production for poverty alleviation. World Aquac 36:48–64
Fielder GC (2002) The influence of social environment on sex determination in harlequin shrimp (Hymenocera picta: Decapoda, Gnathophyllidae). J Crustac Biol 22:750–761. doi:10.1651/0278-0372(2002)022[0750:TIOSES]2.0.CO;2
Fotedar R (2004) Effect of dietary protein and lipid source on the growth, survival, condition indices, and body composition of marron, Cherax tenuimanus (Smith). Aquaculture 230:439–455. doi:10.1016/S0044-8486(03)00418-6
Fowler RS, Leonard BV (1999) The structure and function of the androgenic gland in Cherax destructor (Decapoda: Parastacidae). Aquaculture 171:135–148. doi:10.1016/S0044-8486(98)00416-5
García-Guerrero M, Villarreal H, Racotta IS (2003) Effect of temperatura on lipids, proteins, and carbohydrates levels during development from egg extrusion to juvenile stage of Cherax quadricarinatus (Decapoda: Parastacidae). Comp Biochem Physiol Part A 138:147–154. doi:10.1016/S1095-6433(02)00354-9
Ginsburger-Vogel T, Charniaux-Cotton H (1982) Sex determination. In: Abele LG (ed) The biology of Crustacea, embryology morphology and genetics, vol 2. Academic Press, New York, pp 257–281
Hasegawa Y, Hirose E, Katakura Y (1993) Hormonal control of sexual differentiation and reproduction in crustacea. Am Zool 33:403–411
Jones CM (1995a) Production of juvenile redclaw crayfish, Cherax quadricarinatus (von Martens) (Decapoda, Parastacidae) I. Development of hatchery and nursery procedures. Aquaculture 138:221–238. doi:10.1016/0044-8486(95)00068-2
Jones CM (1995b) Production of juvenile redclaw crayfish, Cherax quadricarinatus (von Martens) (Decapoda, Parastacidae) II Juvenile nutrition and habitat. Aquaculture 138:239–245. doi:10.1016/0044-8486(95)00069-0
Jones CM (1997) The biology and aquaculture potencial of the tropical freshwater crayfish Cherax quadricarinatus. Department of Primary Industries Queensland, Queensland Government, Information Series Q
Karplus I, Hulata G, Barki A (2003) Shifting the natural spring–summer breeding season of the Australian freshwater crayfish Cherax quadricarinatus into the winter by environmental manipulations. Aquaculture 220:277–286. doi:10.1016/S0044-8486(02)00225-9
Khalaila I, Weil S, Sagi A (1999) Endocrine balance between male and female components of the reproductive system in intersex Cherax quadricarinatus (Decapoda: Parastacidae). J Exp Zool 283:286–294. doi:10.1002/(SICI)1097-010X(19990215)283:3<286::AID-JEZ6>3.0.CO;2-R
Khalaila I, Katz T, Abdu U, Yehezkel G, Sagi A (2001) Effects of implantation of hypertrophied androgenic glands on sexual characters and physiology of the reproductive system in the female red claw crayfish, Cherax quadricarinatus. Gen Comp Endocrinol 121:242–249. doi:10.1006/gcen.2001.7607
King CR (1994) Growth and survival of red claw crayfish hatchlings (Cherax quadricarinatus von Martens) in relation to temperature, with comments on the relative suitability of Cherax quadricarinatus and Cherax destructor for culture in Queensland. Aquaculture 122:75–80. doi:10.1016/0044-8486(94)90335-2
Lawrence C, Jones C (2002) Cherax. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell, Oxford, pp 635–669
Lawrence C, Morrisy N (1997) Enhancement of yabbie production from WA farm dams. Freshwat Farmer 4:6–7
Levi T, Barki A, Hulata G, Karplus I (1999) Mother–offspring relationships in the redclaw crayfish Cherax quadricarinatus. J Crustac Biol 19:477–484. doi:10.2307/1549256
López Greco LS, Stella VS, Rodríguez E (1997) Size at the onset of the sexual maturity in Chasmagnathus granulata (Decapoda, Brachyura). Nauplius 5:65–75
López Greco LS, Vazquez FJ, Rodríguez E (2007) Sperm production and spermatophore formation in the freshwater “red claw” crayfish Cherax quadricarinatus (Von Martens, 1898) (Decapoda, Parastacidae). Acta Zool 88:223–229. doi:10.1111/j.1463-6395.2007.00269.x
Manor R, Seguev R, Leibovitz M, Aflalo ED, Sagi A (2002) Intensification of redclaw crayfish Cherax quadricarinatus culture II Growth out in a separate system. Aquacult Eng 26:263–276. doi:10.1016/S0144-8609(02)00035-3
Manor R, Aflalo ED, Segall C, Weil S, Azulay D, Ventura T, Sagi A (2004) Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr Reprod Dev 45:151–159
Manor R, Weil S, Oren S, Glazer L, Aflalo E, Ventura T, Chalifa-Caspi V, Sagi A (2007) Insulin and gender: an insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. Gen Comp Endocrinol 150:326–336. doi:10.1016/j.ygcen.2006.09.006
Masser MP, Rouse DB (1997) Australian red claw crayfish. SRAC Publication No.244. Southern Regional Aquaculture Center, Auburn University, United States
McCabe J, Dunn AM (1997) Adaptive significance of environmental sex determination in Gammarus duebeni. J Evol Biol 10:515–527. doi:10.1007/s000360050039
Medley P, Rouse DB (1993) Intersex Australian red claw crayfish (Cherax quadricarinatus). J Shellfish Res 12:93–94
Medley PB, Jones CM, Avault JW Jr (1994) A global perspective on the culture of Australian redclaw crayfish, Cherax quadricarinatus: production, economics and marketing. World Aquac 25:6–13
Parnes S, Khalaila I, Hulata G, Sagi A (2003) Sex determination in crayfish: are intersex Cherax quadricarinatus (Decapoda, Crustacea) genetically females? Genet Res 82:107–116. doi:10.1017/S0016672303006372
Pavasovic A, Anderson AJ, Mather PB, Richardson NA (2007) Effects of a variety of animal, plant and single cell-based feed ingredients on diet digestibility and digestive enzyme activity in redclaw crayfish, Cherax quadricarinatus (Von Martens 1868). Aquaculture 272:564–572. doi:10.1016/j.aquaculture.2007.08.027
Payen GG (1990) Roles of androgenic gland hormone in determining the sexual characters in crustacea. In: Gupta AP (ed) Morphogenetic hormones of Arthropods. Roles in histogenesis, organogenesis and morphogenesis. Rutgers University Press, New Brunswick, pp 431–452
Portelance B, Dube P (1990) Temperature and photoperiod effects on ovarian maturation, ovarian growth and egg-laying of crayfish Orconectes viridis. Freshwat Crayfish 8:321–330
Rodgers LJ, Saoud PI, Rouse DB (2006) The effects of monosex culture and stocking density on survival, growth and yield of redclaw crayfish (Cherax quadricarinatus) in earthern ponds. Aquaculture 259:164–168. doi:10.1016/j.aquaculture.2005.11.056
Romero XM (1997) Redclaw crayfish aquaculture in Ecuador: the new boom. ICLARM Quarterly 20:18–21
Sagi A (1988) The androgenic gland in crustacean—with emphasis on the cultured freshwater prawn Macrobrachium rosenbergii - a review. Isr J Aquac- Bamidgeh 40:9–16
Sagi A, Aflalo ED (2005) The androgenic gland and monosex culture of freshwater prawn Macrobrachium rosenbergii (De Man): a biotechnological perspective. Aquacult Res 36:231–237. doi:10.1111/j.1365-2109.2005.01238.x
Sagi A, Khalaila I (2001) The crustacean androgen: a hormone in an isopod and androgenic activity in decapods. Am Zool 41:477–484. doi:10.1668/0003-1569(2001)041[0477:TCAAHI]2.0.CO;2
Sagi A, Ra’Anan Z, Cohen D, Wax I (1986) Production of Macrobrachium rosenbergii in monosex populations: yield characteristics under intensive monoculture conditions in cages. Aquaculture 51:265–275. doi:10.1016/0044-8486(86)90318-2
Sagi A, Khalaila I, Barki A, Hulata G, Karplus I (1996) Intersex red claw crayfish Cherax quadricarinatus (von Martens): functional males with pre-vitellogenic ovaries. Biol Bull 190:16–23. doi:10.2307/1542672
Sagi A, Snir E, Khalaila I (1997) Sexual differentiation in decapod crustaceans: role of the androgenic gland. Invertebr Reprod Dev 31:55–61
Sagi A, Khalaila I, Adbu U, Shoukrun R, Weil S (1999) A newly established ELISA showing the effect of the androgenic gland on secondary-vitellogenic-specific protein in the hemolymph of the crayfish Cherax quadricarinatus. Gen Comp Endocrinol 115:37–45. doi:10.1006/gcen.1999.7277
Sagi A, Manor R, Segall C, Davis C, Khalaila I (2002) On intersexuality in the crayfish Cherax quadricarinatus: an inducible sexual plasticity model. Invertebr Reprod Dev 41:27–33
Suzuki S, Yamasaki K (1998) Sex reversal by implantation of ethanol-treated androgenic glands of female isopods, Armadillidium vulgare (Malacostraca, Crustacea). Gen Comp Endocrinol 111:367–375. doi:10.1006/gcen.1998.7121
Van Den Hurk R, van Oordt PG (1985) Effects of natural androgens and corticosteroids on gonad differentiation in the rainbow trout, Salmo gairdneri. Gen Comp Endocrinol 57:216–222. doi:10.1016/0016-6480(85)90266-7
Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med NY 34:428–432
Vazquez FJ, López Greco LS (2007a) Intersex females in the red claw freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Rev Biol Trop 55:25–32
Vazquez FJ, López Greco LS (2007b) Differentiation of the male reproductive system and onset of maturity in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Proceedings of the mid-year meeting of the Crustacean Society, Coquimbo, Chile, p 151
Vazquez FJ, Chaulet A, Bugnot A, López Greco LS (2004) Effect of temperature on sexual differentiation in juveniles of the freshwater crayfish, Cherax quadricarinatus (Astacida, Parastacidae). Proceedings of the III Congreso Iberoamericano Virtual de Acuicultura, pp 255–259
Vazquez FJ, Tropea C, López Greco LS (2008) Differentiation of the female reproductive system and the onset of maturity in the freshwater crayfish “red claw” Cherax quadricarinatus (Von Martens 1898) (Decapoda, Parastacidae) through a macroscopic and microscopic approach. Inv Biol 127:433–443
Yeh H, Rouse D (1995) Effects of water temperature, density, and sex ratio on the spawning rate of red claw crayfish Cherax quadricarinatus (Von Martens). J World Aquacult Soc 26:160–164. doi:10.1111/j.1749-7345.1995.tb00239.x
Zapata V, López Greco LS, Medesani D, Rodríguez E (2003) Ovarian growth in the crab Chasmagnathus granulata, induced by hormones and neuroregulators throughout the year in vivo and in vitro studies. Aquaculture 224:339–352. doi:10.1016/S0044-8486(03)00226-6
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood Cliffs
Zhao Y, Meng F, Chen L, Gu Z, Xu G, Liu Q (2000) Effects of different gradient temperatures on embryonic development of the Cherax quadricarinatus (Crustacea, Decapoda). J Lake Sci 12:59–62
Acknowledgments
We wish to thank Dr. Amir Sagi (Ben-Gurion University of the Negev, Israel) for reviewing the manuscript and his comments and Dr. Christopher Tudge (Department of Biology, American University, Washington) and Dr. Raymond Bauer (Dept. of Biology, University of Louisiana, Lafayette) for their suggestions and great help with the English version. We also wish to thank Lic. Fernanda Vazquez (University of Buenos Aires) for her help with the slides. This work is part of an undergraduate scholarship by MSDB (University of Buenos Aires). This research was funded by Agencia Nacional de Promoción Científica y Tecnológica (PICT 2004, project 953), UBACYT (projects X143 and X 458) and Antorchas Foundation (project 4248-138). We are grateful to anonymous reviewers for their critical comments to improve this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
De Bock, M.S., López Greco, L.S. Sex reversal and growth performance in juvenile females of the freshwater crayfish Cherax quadricarinatus (Parastacidae): effect of increasing temperature and androgenic gland extract in the diet. Aquacult Int 18, 231–243 (2010). https://doi.org/10.1007/s10499-008-9239-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-008-9239-x