Copper accumulation by stickleback nests containing spiggin
The three-spined stickleback is a ubiquitous fish of marine, brackish and freshwater ecosystems across the Northern hemisphere that presents intermediate sensitivity to copper. Male sticklebacks display a range of elaborate reproductive behaviours that include nest construction. To build the nests, each male binds nesting material together using an endogenous glycoprotein nesting glue, known as ‘spiggin’. Spiggin is a cysteine-rich protein and, therefore, potentially binds heavy metals present in the environment. The aim of this study was to investigate the capacity of stickleback nests to accumulate copper from environmental sources. Newly built nests, constructed by male fish from polyester threads in laboratory aquaria, were immersed in copper solutions ranging in concentration from 21.1–626.6 μg Cu L−1. Bundles of polyester threads from aquaria without male fish were also immersed in the same copper solutions. After immersion, nests presented higher amounts of copper than the thread bundles, indicating a higher capacity of nests to bind this metal. A significant, positive correlation between the concentration of copper in the exposure solution and in the exposed nests was identified, but there was no such relationship for thread bundles. Since both spiggin synthesis and male courtship behaviour are under the control of circulating androgens, we predicted that males with high courtship scores would produce and secrete high levels of the spiggin protein. In the present study, nests built by high courtship score males accumulated more copper than those built by low courtship score males. Considering the potential of spiggin to bind metals, the positive relationship between fish courtship and spiggin secretion seems to explain the higher amount of copper on the nests from the fish showing high behaviour scores. Further work is now needed to determine the consequences of the copper binding potential of spiggin in stickleback nests for the health and survival of developing embryos.
KeywordsAquatic Contamination Copper Reproductive Behaviour Spiggin Stickleback
The authors thank Ceinwen A. Tilley for her assistance during this work. Grasiela L. L. Pinho was in receipt of a postdoctoral fellowship awarded by the Brazilian CNPq (no. 245706/2012-7).
The project was conceived by GLLP and IB. The behavioural work was undertaken by GLLP with input from IB. Copper analysis was undertaken by CMGM. Data analysis was undertaken by IB and GLLP. All authors contributed to writing the manuscript and reviewed the final draft prior to submission.
- Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol 109C:219–245Google Scholar
- Clark RB (2001) Marine Pollution. Oxford University Press, New YorkGoogle Scholar
- EPS (1990) Biological test method: acute lethality test using threespine stickleback (Gasterosteus aculeatus). Environ, Prot. Serv., Environment Canada, Regulations, Codes, Protocols, OtawaGoogle Scholar
- Grosell M, Nielsen C, Bianchini A (2002) Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp Biochem Physiol 133C:287–303Google Scholar
- Kagi JHR (1993) Evolution, structure and chemical activity of class I metallothioneins overview. In: Suzuki KT, Imura N, Kimura M (eds) Metallothionein III, vol III. Birkha¨user Verlag, Basel, pp 29–55Google Scholar
- Landner L, Lindestrom L (1999) Copper in society and the environment: an account of the facts on fluxes, amounts and effects of copper in Sweden. Swedish Environmental Research Group, Stockholm, SwedenGoogle Scholar
- Sanchez W, Goin C, Brion F, Olsson PE, Goksøyr A, Porcher JM (2008) A new ELISA for the three-spined stickleback (Gasterosteus aculeatus L.) spiggin, using antibodies against synthetic peptide. Comp Biochem Physiol 147©:129–137Google Scholar
- Svecevicius G, Vosyliene MZ (1996) Acute toxicity of copper to common freshwater fishes of Lithuania. Ekologija 2:17–21Google Scholar
- USEPA (2007) Aquatic life ambient freshwater quality criteria—copper. U.S. Environmental Protection Agency, Office of Water, Office of Science and Technology, WashingtonGoogle Scholar
- Van Iersel JJA (1953) An analysis of the parental behaviour of the male three-spined stickleback (Gasterosteus aculeatus L.). Behaviour 3:1–159Google Scholar
- Wood CM, Farrell AP, Brauner CJ (2012) Fish physiology: homeostasis and toxicology of essential metals. Academic Press, New YorkGoogle Scholar
- Wootton RJ (1976) The biology of the sticklebacks. Academic Press, LondonGoogle Scholar
- Zar JH (1999) Biostatistical Analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar