Skip to main content

Masculinization of Convict Cichlid (Cichlasoma nigrofasciatum) by immersion in Tribulus terrestris extract

Abstract

We have examined the effects of Tribulus terrestris (TT), a non-toxic herb, on sex reversal in the Convict Cichlid Cichlasoma nigrofasciatum with the aim of introducing a new environmentally friendly method for masculinization in C. nigrofasciatum. TT is a natural plant product that elevates the testosterone levels in humans and animals. Different concentrations (0.0, 0.10, 0.20 and 0.30 g/l) of TT extract were tested for their effect on sex reversal in C. nigrofasciatum by immersing newly hatched offspring once weekly for 2 months in TT extract. Of the dosages used in the present study, 0.30 g/l TT was the most effective in terms of masculinization, resulting in a maximum male ratio of 87.23% (P < 0.001). Sex ratios of 79 and 85% at 0.10 and 0.20 g/l TT, respectively, were also significantly different from the expected 1:1 ratio (P < 0.001). Histological examinations revealed that the testes of fish treated with TT extract contained all stages of spermatogenesis, clearly demonstrating that the administration of TT extract to C. nigrofasciatum stimulated spermatogenesis. Total survival rates in all treatments and the control were uniformly high, ranging from 88.57 to 90% (P > 0.05). We concluded that TT had no negative effect on the survival rate of C. nigrofasciatum. In addition, all groups of TT-treated fish exhibited successful growth acceleration compared to the control group, but only the 0.30 g/l TT treatment significantly improved the growth rate of C. nigrofasciatum. (P < 0.01). Sex reversal in C. nigrofasciatum demonstrated that TT-treated 0-day-old larvae showed successful sex reversal, spermatogenesis and a better growth rate than untreated progenies.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Adaikan PG, Gauthaman K, Ng RNV, Prasad SC (2000) Proerectile pharmacological effects of Tribulus terrestris on the rabbit corpus cavernosum. Ann Acad Med Singapore 29(1):22–26

    PubMed  CAS  Google Scholar 

  • Adimoelja A (2000) Photochemical and the breakthrough of traditional herbs in the management of sexual dysfunctions. Int J Androl 23(2):82–84

    PubMed  Article  CAS  Google Scholar 

  • Adimoelja A, Adaikan PG (1997) Protodioscin from herbal plant Tribulus terrestris L. improves male sexual functions possibly via DHEA. Int J Impot Res 9:64

    Google Scholar 

  • Adimoelja A, Sartono S, Soedjono J (2005) Phyto-DHEA treatment, an alternative option for aging men. Int J Androl 28(Suppl 1):25

    Google Scholar 

  • Ali PK, Rao GPS (1989) Growth improvement in carp, Cyprinus carpio (Linnaeus), sterilized with 17α-methyl testosterone. Aquaculture 76:157–167

    Article  Google Scholar 

  • Aslani MR, Movassaghi AR, Mohri M, Ebrahim-pour V, Mohebi AN (2004) Experimental Tribulus terrestris poisoning in goats. Small Ruminant Res 51:261–267

    Article  Google Scholar 

  • Axelrod HR, Emmens CV, Sculthorpe D, Wingler WV, Pronek N (1971) Exotic tropical fishes. TFH Publ, Jersey City

    Google Scholar 

  • Baker IJ, Solar II, Donaldson EM (1988) Masculinization of Chinook salmon (Onchorynchus tshawtscha) by immersion treatments using 17α-methyl testosterone around the time of hatching. Aquaculture 72:359–367

    Article  CAS  Google Scholar 

  • Bromaga NR, Cumaranatunga PRT (1987) Oocyte development in the rainbow trout with special reference to vitellogenesis and atresia. In: Idler DR, Crim LW, Walsh JM (eds) Proc 3rd Int Symp Reprod Physiol Fish. St John’s, Newfoundland, p 194

  • Bucci LR (2000) Selected herbals and human exercise performance. Am J Clin Nutr 72:624–636

    Google Scholar 

  • Colgan PW, Salmon AB (1986) Breeding experience and parental behaviour in convict cichlids Cichlasoma nigrofasciatum, Behav Process 13(1–2):101–118

    Article  Google Scholar 

  • Contreras-Sanchez WM, Fitzpatrick MS, Schreck CB (2001) Fate of methyl testosterone in the pond environment: detection of Mt in pond soil from a CRSPsite. In: Gupta A, McElwee K, Burke D, Burright J, Cummings X, Egna H (eds) 18th Annu Tech Rep. PD/A CRSP (Oregon State University, Pond Dynamics/Aquaculture Collaborative Research Support Program), Corvallis, Oregon, pp 79–82

  • Çek Ş (2006) Early gonadal development and sex differentiation in rosy barb (Puntius conchonius). Anim Biol 56:335–350

    Article  Google Scholar 

  • Çek Ş, Bromage NR, Randall C, Rana K (2001) Oogenesis, hepatosomatic indexes, and sex ratio in Rosy barb (Puntius conchonius). Turk J Fish Aquat Sci 1:133–141

    Google Scholar 

  • Çek Ş, Yıldırım Y, Şereflişan H, Akyurt İ (2004) Sex control in aquaculture. In: Harmancıoğlu O, Fıstıkoğlu Y, Dalgılıç D, Gul A (eds) Water resources management; risks and challenges for the 21st century. İzmir, Turkey, pp 343–353

  • Çek Ş, Turan F, Atik E (2007) The effects of gokshura, Tribulus terrestris on sex differentiation of guppy, Poecilia reticulata. Pakistan J Biol Sci 10(5): 718–725

    Article  Google Scholar 

  • Demska-Zakes K, Zakes Z (1997) Effect of 17 α-methyl testosterone on gonadal differentiation in pikeperch, Stizostedion lucioperca L. Aquac Res 28:59–63

    Article  Google Scholar 

  • Dimitrov M, Georgiev P, Vitanov S (1987) Use of Tribestan on rams with sexual disorders. Vet Med Nauki 24(5):102–110

    PubMed  CAS  Google Scholar 

  • Fishers L (2003) Comparison of testes structure, spermatogenesis and spermatocytogenesis in young, aging and hybrid cichlid fish (Cichlidae, Teleostei). J Morphol 256(3):285–300

    Article  Google Scholar 

  • Fraser SA (1996) The influence of predators on adaptation behaviour in adult convict cichlid Cichlasoma nigrofasciatum. Can J Zool 74:1165–1173

    Google Scholar 

  • Gale WL, Fitzpatrick MS, Lucero M, Contreras-Sanchez WM, Schreck CB (1999) Masculinization of Nile tilapia (Oreochromis niloticus) by immersion in Androgens. Aquaculture 178:349–357

    Article  CAS  Google Scholar 

  • Ganzera M, Bedir E, Khan IA (2001) Determination of steroidal saponins in Tribulus terrestris by reversed-phase high-performance liquid chromatography and evaporative light scattering detection. J Pharm Sci 90:1752–1758

    PubMed  Article  CAS  Google Scholar 

  • Gauthaman K, Adaikan PG (2005) Effects of Tribulus terrestris on nicotinamide adenine dinucleotide phosphate diaphorase activity and androgen receptors in rat brain. J Ethnopharmacol 96(1–2):127–132

    PubMed  Article  CAS  Google Scholar 

  • Gauthaman K, Adaikan PG, Prasad RNV, Goh VHH, Ng SC (2000) Changes in hormonal parameters secondary to intravenous administration of Tribulus terrestris extract in primates. Int J Impot Res 12:6

    Article  Google Scholar 

  • Gauthaman K, Adaikan PG, Prasad RNV (2002) Aphrodisiac properties of Tribulus terrestris extract (Protodioscin) in normal and castrated rats. Life Sci 71(12):1385–1396

    PubMed  Article  CAS  Google Scholar 

  • George T, Pandian TJ (1996) Hormonal induction of sex reversal and progeny testing in the zebra cichlid Cichlasoma nigrofasciatum. J Exp Zool 275:374–382

    Article  CAS  Google Scholar 

  • Georgiev P, Dimitrov M, Vitanov S (1988) The effect of the preparation ‘Tribestan on the plasma concentration of testosterone and spermatogenesis of lambs and rams. Vet Sb 3:20–22

    Google Scholar 

  • Grier HJ (1981) Cellular organization of the testis and spermatogenesis in fishes. Am Zool 21:345–357

    Google Scholar 

  • Grier H (1993) Comparative organization of sertoli cells including the sertoli cell barrier. In: Rusell LD, Griswold MD (eds) The sertoli cell book. Cache River Press, St. Louis, Mo., pp 703–739

    Google Scholar 

  • Kavitha AV, Jagadessan G (2002) In vivo studies on the role of Tribulus terrestris extract on mercury intoxicated mice, Mus musculus (Linn.) large intestine – a histological survey. J Exp Zoo India 6(2):213–219

    Google Scholar 

  • Kavitha AV, Jagadessan G (2003) Histopathological alterations in small intestine of mercury intoxicated mice, Mus musculus (Linn.) in response to Tribulus terrestris (Zygophyllaceae) extract. Pollen Res 23(3):343–347

    Google Scholar 

  • Manosroi J, Petchjul K, Manosroi A (2004) Effect of fluoxymesterone fish feed granule on sex reversal of the hybrid, Thai red tilapia (Oreochromis niloticus Linn. × Oreochromis mossambicus Linn). Asian Fish Sci 17:323–331

    Google Scholar 

  • Meijide FJ, Guerrero GA (2000) Embryonic and larval development of a substrate-brooding cichlid Cichlasoma dimerus (Heckel, 1840) under laboratory conditions. J Zool 252:481–493

    Article  Google Scholar 

  • Meijide FJ, Lo Nostro FL, Guerrero GA (2005) Gonadal development and sex differentiation in the cichlid fish Cichlasoma dimerus (Teleostei, perciformes): a light and electron-microscopy study. J Morphol 264(2):191–210

    PubMed  Article  Google Scholar 

  • Nelson J (1994) Fishes of the world, 3rd edn. Wiley, New York

    Google Scholar 

  • Myers JM, Penman J, Rana KJ, Bromage NR, Powell SF, McAndrew BJ (1995) Applications of induced androgenesis with tilapia. Aquaculture 137(1–4):150

    Article  Google Scholar 

  • Nakamura Y (1975) Dosage-dependent changes in the effect of oral administration of methyl testosterone on gonadal differentiation in Tilapia mossambicus. Bull Fac Fish Hokkaido Univ 26:99–108

    Google Scholar 

  • Nicholls TJ, Graham GP (1972) The ultra structure of lobule boundary cells and leyding cell homologs in the testis of a cichlid, Cichlasoma nigrofasciatum. Gen Comp Endocrinol 19:133–146

    PubMed  Article  CAS  Google Scholar 

  • Pandian TJ, Sheela SG (1995) Hormonal induction of sex-reversal in fish. Aquaculture 138:1–22

    Article  CAS  Google Scholar 

  • Piron RD (1978) Breeding the convict cichlid (Cichlasoma nigrofasciatum) for use in laboratory fish toxicity tests. J Fish Biol 13:119–122

    Article  Google Scholar 

  • Produce M, Tsvetkov D, Nalbanski B (1983) Clinical trial of the preparation Tribestan in infertile men. Akush Ginekol 22(4):326–329

    CAS  Google Scholar 

  • Seth SD (1974) Preliminary pharmacological investigations of Tribulus terrestris. Linn (Gokhru). Indian J Med Sci 28(9):377–380

    PubMed  CAS  Google Scholar 

  • Shelton WL, Meriwether FH, Semmens KJ, Calhoun E (1983) Progeny sex ratio from intraspecific pair spawning of Tilapia aureus and Tilapia nilotica. In: Fishers L, Yaron Z (eds) International Symposium on Tilapia in Aquaculture. Tel Aviv University, Tel Aviv, pp 270–280

    Google Scholar 

  • Tapia MO, Giordano MA, Gueper HG (1994) An outbreak of hepatogenous photosensitization in sheep grazing Tribulus terrestris in Argentina. Vet Hum Toxicol 36(4):311–313

    CAS  Google Scholar 

  • Tariq Ezaz M, Mayers JM, Powell SF, McAndrew BJ, Penman DJ (2004) Sex ratio in the progeny of androgenic and gynogenetic YY male Nile tilapia, Oreochromis niloticus L. Aquaculture 232(1–4):205–214

    Article  Google Scholar 

  • Tomova M, Gjulemetova R, Zarkova S, Peeva S, Pangaroya T, Simova M (1981) Steroidal saponins from Tribulus terrestris L. with a stimulating action on the sexual functions. In: 1st Proc Int Conf Chem Biotechnol Biol Active Nat Products. Varna, pp 298–302

  • Waller GR, Yamasaki K (1996) Saponins used in food and agriculture. Advances in experimental medicine and biology. Plenum Press, New York, pp 381–382

    Google Scholar 

  • Winemiller KO, Taylor DH (1982) Inbreeding depression in the convict cichlid, Cichlasoma nigrofasciatum (Baird and Girard). J Fish Biol 21:399–402

    Article  Google Scholar 

  • Wisenden BD (1994) Factors affecting reproductive success in free ranging convict cichlids. Can J Zool 72:2177–2185

    Article  Google Scholar 

  • Zar H (1984) Biostatistical analysis. Prentice-Hall, Upper Saddle River

    Google Scholar 

Download references

Acknowledgements

The Mustafa Kemal University supported this study financially. We would like to wholeheartedly thank Dietharmonie, France for providing the TT extract that was used in this study. We also thank Dr. Haydar Fersoy and Dr. Yavuz Mazlum for reading the first draft of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Şehriban Çek.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Çek, Ş., Turan, F. & Atik, E. Masculinization of Convict Cichlid (Cichlasoma nigrofasciatum) by immersion in Tribulus terrestris extract. Aquacult Int 15, 109–119 (2007). https://doi.org/10.1007/s10499-006-9071-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-006-9071-0

Keywords

  • Cichlasoma nigrofasciatum
  • Growth
  • Histology
  • Sex reversal
  • Tribulus terrestris