Skip to main content
SpringerLink
Log in

Evidence that elevated water temperature affects the reproductive physiology of the European bullhead Cottus gobio

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Climate change is predicted to increase the average water temperature and alter the ecology and physiology of several organisms including fish species. To examine the effects of increased water temperature on freshwater fish reproduction, adult European bullhead Cottus gobio of both genders were maintained under three temperature regimes (T1: 6–10, T2: 10–14 and T3: 14–18°C) and assessed for gonad development (gonadosomatic index—GSI and gonad histology), sex steroids (testosterone—T, 17β-estradiol—E2 and 11-ketotestosterone—11-KT) and vitellogenin (alkali-labile phosphoprotein phosphorus—ALP) dynamics in December, January, February and March. The results indicate that a 8°C rise in water temperature (T3) deeply disrupted the gonadal maturation in both genders. This observation was associated with the absence of GSI peak from January to March, and low levels of plasma sex steroids compared with T1-exposed fish. Nevertheless, exposure to an increasing temperature of 4°C (T2) appeared to accelerate oogenesis with an early peak value in GSI and level of plasma T recorded in January relative to T1-exposed females. In males, the low GSI, reduced level of plasma 11-KT and the absence of GSI increase from January to March support the deleterious effects of increasing water temperature on spermatogenesis. The findings of the present study suggest that exposure to elevated temperatures within the context of climate warming might affect the reproductive success of C. gobio. Specifically, a 4°C rise in water temperature affects gametogenesis by advancing the spawning, and a complete reproductive failure is observed at an elevated temperature of 8°C.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdoli A, Pont D, Sagnes P (2005) Influence of female age, body size and environmental conditions on annual egg production of the bullhead. J Fish Biol 67:1327–1341

    Article  Google Scholar 

  • Abdoli A, Pont D, Sagnes P (2007) Intrabasin variations in age and growth of bullhead: the effects of temperature. J Fish Biol 70:1224–1238

    Article  Google Scholar 

  • Andreasson S (1971) Feeding habits of a sculpin (Cottus gobio L. Pisces) population. Inst Freshwater Res, Drottningholm, Sweden, Rep. no. 51

  • De Silva JN (1985) Production of the common sculpin, Cottus gobio (L.) in a Belgian chalk stream, the Samson and the contribution of benthic-macroinvertebrate fauna to its diet. PhD Thesis, Namur University, Namur, Belgium

  • Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproduction performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243

    Article  Google Scholar 

  • Elliott JM, Elliott JA (1995) The critical thermal limits for the bullhead, Cottus gobio, from 3 populations in North-West England. Freshwater Biol 33:411–418

    Article  Google Scholar 

  • Fostier A, Jalabert B (1986) Steroidogenesis in rainbow trout (Salmo gairdneri) at various preovulatory stages: changes in plasma hormone levels and in vivo and in vitro responses of the ovary to salmon gonadotropin. Fish Physiol Biochem 2:87–99

    Article  CAS  Google Scholar 

  • Fox PJ (1978) Preliminary observations on different reproduction strategies in the bullhead (Cottus gobio L.) in nothern and southern England. J Fish Biol 12:5–11

    Article  Google Scholar 

  • Geraudie P, Gerbron M, Hill E, Minier C (2010) Roach (Rutilus rutilus) reproductive cycle: a study of biochemical and histological parameters in a low contaminated site. Fish Physiol Biochem 36:767–777

    Article  PubMed  CAS  Google Scholar 

  • Gillet C, Quetin P (2006) Effect of temperature changes on the reproductive cycle of roach in Lake Geneva from 1983 to 2001. J Fish Biol 69:518–534

    Article  Google Scholar 

  • Habitats Directive (2007) Appendix II. Available from http://admi.net/eur/loi/leg_euro/fr_392L0043.html

  • Hirshfield M (1980) An experimental analysis of reproductive effort and cost in the Japanese medaka Oryzias latipes. Ecology 61:282–292

    Article  Google Scholar 

  • IPCC (2007) Climate Change 2007: The physical science basis. Contribution of working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 996 pp

  • King HR, Pankhurst NW, Watts M, Pankhurst PM (2003) Effect of elevated summer temperatures on gonadal steroid production, vitellogenesis and egg quality in female Atlantic salmon. J Fish Biol 63:153–167

    Article  Google Scholar 

  • Legalle M, Santoul F, Figuerola J, Mastrorillo S, Cereghino R (2005) Factors influencing the spatial distribution patterns of the bullhead (Cottus gobio L., Teleostei Cottidae): a multi-scale study. Biodivers Conserv 14:1319–1334

    Article  Google Scholar 

  • Mandiki SN, Babiak I, Bopopi JM, Leprieur F, Kestemont P (2005) Effects of sex steroids and their inhibitors on endocrine parameters and gender growth differences in Eurasian perch (Perca fluviatilis) juveniles. Steroids 70:85–94

    Article  PubMed  CAS  Google Scholar 

  • Manning N, Kime D (1985) The effect of temperature on testicular steroid production in the rainbow trout, Salmo gairdneri, in vivo and in vitro. Gen Comp Endocrinol 57:377–382

    Article  PubMed  CAS  Google Scholar 

  • Mattheeuws A, Genin M, Detollenaere A, Micha C (1981) Etude de la reproduction du gardon (Rutilus rutilus) et des effets d’une élévation provoquée de la température en Meuse sur cette reproduction. Hydrobiologia 85:271–282

    Article  Google Scholar 

  • Milla S, Mandiki SN, Hubermont P, Rougeot C, Melard C, Kestemont P (2009) Ovarian steroidogenesis inhibition by constant photothermal conditions is caused by a lack of gonadotropin stimulation in Eurasian perch. Gen Comp Endocrinol 163:242–250

    Article  PubMed  CAS  Google Scholar 

  • Mohnen VA, Wang WC (1992) An overview of global warming. Environ Toxicol Chem 11:1051–1059

    Article  CAS  Google Scholar 

  • Morgan IJ, McDonald DG, Wood CM (2001) The cost of living for freshwater fish in a warmer, more polluted world. Global Change Biol 7:345–355

    Article  Google Scholar 

  • Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ 50(Suppl 1):S195–S219

    Article  PubMed  CAS  Google Scholar 

  • Nagahama Y, Miura T, Kobayashi T (1994) The onset of spermatogenesis in fish. Ciba Found Symp 182:255–267

    PubMed  CAS  Google Scholar 

  • Nagler JJ, Idler DR (1992) In vitro ovarian estradiol-17-beta and testosterone responses to pituitary extract and corresponding serum levels during the prespawning to vitellogenic phases of the reproductive-cycle in winter flounder (Pseudopleuronectes americanus). Comp Biochem Physiol A 101:69–75

    Article  Google Scholar 

  • Pankhurst NW, King HR (2010) Temperature and salmonid reproduction: implications for aquaculture. J Fish Biol 76:69–85

    Article  PubMed  CAS  Google Scholar 

  • Pankhurst NW, Thomas PM (1998) Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout Oncorhynchus mykiss to luteinizing hormone releasing hormone analogue. Aquaculture 166:163–177

    Article  CAS  Google Scholar 

  • Pankhurst NW, Purser GJ, Van Der Kraak G, Thomas PM, Forteath GNR (1996) Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout Oncorhynchus mykiss. Aquaculture 146:277–290

    Article  CAS  Google Scholar 

  • Rahel FJ, Keleher CJ, Anderson JL (1996) Potential habitat loss and population fragmentation for cold water fish in the north plate river drainage of the rocky mountains: response to climate warming. Limnol Oceanogr 41:1116–1123

    Article  Google Scholar 

  • Reyjol Y, Lena JP, Hervant F, Pont D (2009) Effects of temperature on biological and biochemical indicators of the life-history strategy of bullhead Cottus gobio. J Fish Biol 75:1427–1445

    Article  PubMed  CAS  Google Scholar 

  • Rinchard J, Kestemont P (1996) Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish.1. Morphological and histological features. J Fish Biol 49:883–894

    Article  Google Scholar 

  • Schulz RW, de Franca LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  PubMed  CAS  Google Scholar 

  • Smyly WJP (1957) The life history of the bullhead or Miller’s thumb (Cottus gobio L.). Proc Zool Soc Lond 128:431–453

    Google Scholar 

  • Tveiten H, Johnsen HK (1999) Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish. J Fish Biol 55:809–819

    Article  Google Scholar 

  • Tveiten H, Solevag SE, Johnsen HK (2001) Holding temperature during the breeding season influences final maturation and egg quality in common wolffish. J Fish Biol 58:374–385

    Article  Google Scholar 

  • Utzinger J, Roth C, Peter A (1998) Effects of environmental parameters on the distribution of bullhead Cottus gobio with particular consideration of the effects of obstructions. J Appl Ecol 35:882–892

    Article  Google Scholar 

  • Van Der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. Cambridge University Press, Cambridge

    Google Scholar 

  • Verslycke T, Vandenbergh GF, Versonnen B, Arijs K, Janssen CR (2002) Induction of vitellogenesis in 17alpha-ethinylestradiol-exposed rainbow trout (Oncorhynchus mykiss): a method comparison. Comp Biochem Physiol C 132:483–492

    Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  PubMed  CAS  Google Scholar 

  • Wang N, Teletchea F, Kestemont P, Milla S, Fontaine P (2010) Photothermal control of the reproductive cycle in temperate fishes. Rev Aquaculture 2:209–222

    Article  Google Scholar 

  • Watts M, Pankhurst NW, King HR (2004) Maintenance of Atlantic salmon (Salmo salar) at elevated temperature inhibits cytochrome P450 aromatase activity in isolated ovarian follicles. Gen Comp Endocrinol 135:381–390

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank A. Evrard and M.-C. Forget from URBO, and Daniel Van Vlaender from URPhym, University of Namur, Namur, Belgium, for valuable help during animal husbandry, biochemical and histological analysis, respectively. Thanks are also due to Dr Didier Pont, coordinator of the IFD (French Institute of Diversity) project. This study was supported by IFD and FNRS PhD fellowship to J. Dorts.

Author information

Authors and Affiliations

  1. Research Unit in Environmental and Evolutionary Biology (URBE), The University of Namur (FUNDP), Rue de Bruxelles 61, 5000, Namur, Belgium

    Jennifer Dorts, Jessica Douxfils, Syaghalirwa N. M. Mandiki, Sylvain Milla, Frédéric Silvestre & Patrick Kestemont

  2. Labo. Evolution et Diversité Biologique, Université Paul Sabatier, Bâtiment 4R3, 118 route de Narbonne, 31062, Toulouse Cedex 9, France

    Gaël Grenouillet

Authors
  1. Jennifer Dorts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gaël Grenouillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jessica Douxfils
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Syaghalirwa N. M. Mandiki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sylvain Milla
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frédéric Silvestre
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Patrick Kestemont
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer Dorts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dorts, J., Grenouillet, G., Douxfils, J. et al. Evidence that elevated water temperature affects the reproductive physiology of the European bullhead Cottus gobio . Fish Physiol Biochem 38, 389–399 (2012). https://doi.org/10.1007/s10695-011-9515-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-011-9515-y

Keywords

Search

Navigation