API

Relationship: 1034

Title

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Reduced, Anterior swim bladder inflation leads to Reduced, Swimming performance

Upstream event

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Reduced, Anterior swim bladder inflation

Downstream event

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Reduced, Swimming performance

Key Event Relationship Overview

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AOPs Referencing Relationship

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Taxonomic Applicability

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Term Scientific Term Evidence Link
zebrafish Danio rerio NCBI
fathead minnow Pimephales promelas NCBI

Sex Applicability

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Life Stage Applicability

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How Does This Key Event Relationship Work

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Effects on swim bladder inflation can alter swimming performance and buoyancy of fish, which is essential for predator avoidance, energy sparing, migration, reproduction and feeding behaviour, resulting in lower young-of-year survival.

Weight of Evidence

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The weight of evidence supporting a direct linkage between these two KEs, i.e. reduced anterior swim bladder inflation and reduced swimming performance, is weak.

Biological Plausibility

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The anterior chamber of the swim bladder has a function in regulating the buoyancy of fish, by altering the volume of the swim bladder (Roberston et al., 2007). Fish rely on the lipid and gas content in their body to regulate their position within the water column, with the latter being more efficient at increasing body buoyancy. Therefore, fish with functional swim bladders have no problem supporting their body (Brix 2002), while it is highly likely that impaired inflation severely impacts swimming performance. Fish with no functional swim bladder can survive, but are severely disadvantaged., making the likelihood of surviving smaller.

Empirical Support for Linkage

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Buoyancy is one of the primary mechanisms of fish to regulate behaviour, swimming performance and energy expenditure. Robertson et al., (2007) suggested that the swim bladder only starts regulating buoyancy actively from 32 dpf onward in zebrafish, indicating that impaired swim bladder inflation possibly affects swimming activity during late development. The swim bladder only becomes capable of regulating buoyancy when it has fully developed into a double-chambered. However, during an MBT exposure, a TPO inhibitor, for 32 days post fertilization (dpf) in zebrafish, the swimming activity of fish was impacted starting at 26 dpf if the inflation of the anterior chamber of the swim bladder was impaired or had no normal structure/size (Stinckens et al., 2016). This effect was also observed after a 32 dpf exposure to MMI, however only for the highest tested concentration (Stinckens et al., unpublished data).

It has also been reported that larvae that fail to inflate their swim bladder use additional energy to maintain buoyancy (Lindsey et al., 2010, Goodsell et al. 1996), possibly contributing to reduced swimming activity. Furthermore, Chatain (1994) associated larvae with non-inflated swim bladders with numerous complications, such as spinal deformities and lordosis and reduced growth rates, adding to the impact on swimming behaviour.

An increasing incidence of swim bladder non-inflation has also been reported in Atlantic salmon (Poppe et al. 1997). Affected fish had severely altered balance and buoyancy, observed through a specific swimming behaviour, as the affected fish were swimming upside down in an almost vertical position (Poppe et al. 1997).

Uncertainties or Inconsistencies

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During an MMI exposure, a TPO inhibitor, for 32 dpf in zebrafish, the swimming activity of fish was impacted starting at 26 dpf if the inflation of the anterior chamber of the swim bladder was impaired (Stinckens et al., unpublished). However, this effect was only observed for the highest tested concentration. For the lowest tested concentration, during which the anterior swim bladder was severly impacted as well, no effect on swimming capacity could be observed. As Robertson et al., (2007) reported, the swim bladder only starts regulating buoyancy actively from 32 dpf onward in zebrafish, possibly explaining the lack of effect on swimming capacity for lower MMI concentrations.

The function of the posterior chamber has been clearly linked to buoyancy control and survival (Czesny et al., 2005; Woolley and Qin, 2010; Kurata et al., 2014). The link between anterior chamber inflation and impaired swimming capacity however is less clear. The most important function of the anterior chamber is producing and transducing sound through the Weberian Apparatus (Popper, 1974; Lechner and Ladich, 2008), with only a slight contribution in bouncy control. It is highly plausible that impaired inflation or size of the anterior swim bladder could lead to a reduction in young-of-year survival as hearing loss would affect their ability to respond to their surrounding environment, thus impacting ecological relevant endpoints such as predator avoidance or prey seeking (Wisenden et al., 2008; Fay2009).

Quantitative Understanding of the Linkage

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The direct evidence supporting the connection between anterior chamber impairment and swimming capacity is lacking.

Evidence Supporting Taxonomic Applicability

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Importance of swimming performance for natural behaviour is generally applicable to fish.

References

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Roberston, G.N., McGee, C.A.S., Dumbarton, T.C., Croll, R.P., Smith, F.M., 2007.Development of the swim bladder and its innervation in the zebrafish, Danio rerio. J. Morphol. 268, 967–985, http://dx.doi.org/10.1002/jmor.

Brix O (2002) The physiology of living in water. In: Hart PJ, Reynolds J (eds) Handbook of Fish Biology and Fisheries, Vol. 1, pp. 70–96. Blackwell Publishing, Malden, USA.

Stinckens, E., Vergauwen, L., Schroeder, A.L., Maho, W., Blackwell, B., Witter, H.,Blust, R., Ankley, G.T., Covaci, A., Villenueve, D.L., Knapen, D., 2016. Disruption of thyroid hormone balance after 2-mercaptobenzothiazole exposure causes swim bladder inflation impairment—part II: zebrafish. Aquat. Toxicol. 173:204-17.

Lindsey, B.W., Smith, F.M., Croll, R.P., 2010. From inflation to flotation: contributionof the swimbladder to whole-body density and swimming depth duringdevelopment of the zebrafish (Danio rerio). Zebrafish 7, 85–96, http://dx.doi.org/10.1089/zeb.2009.0616.

Goodsell, D.S., Morris, G.M., Olsen, A.J. 1996. Automated docking of fleixble ligands. Applications of Autodock. J. Mol. Recogonition, 9:1-5.

Chatain, B., 1994. Abnormal swimbladder development and lordosis in sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). Aquaculture 119:371–379.

Poppe, T.T., Hellberg, H., Griffiths, D., Mendal, H. 1977. Swim bladder abnormality in farmed Atlantic salmon, Salmo salar. Diseases of aquatic organisms 30:73-76.

Czesny, S.J., Graeb, B.D.S., Dettmersn, J.M., 2005. Ecological consequences of swimbladder noninflation for larval yellow perch. Trans. Am. Fish. Soc. 134,1011–1020, http://dx.doi.org/10.1577/T04-016.1.

Woolley, L.D., Qin, J.G., 2010. Swimbladder inflation and its implication to theculture of marine finfish larvae. Rev. Aquac. 2, 181–190, http://dx.doi.org/10.1111/j.1753-5131.2010.01035.x.

Kurata, M., Ishibashi, Y., Takii, K., Kumai, H., Miyashita, S., Sawada, Y., 2014.Influence of initial swimbladder inflation failure on survival of Pacific bluefintuna, Thuunus orientalis (Temminck and Schlegl) larvae. Aquacult. Res. 45,882–892.

Lechner, W., Ladich, F., 2008. Size matters: diversity in swimbladders andWeberian ossicles affects hearing in catfishes. J. Exp. Biol. 211, 1681–1689.

Wisenden, B.D., Pogatschnik, J., Gibson, D., Bonacci, L., Schumacher, A., Willet, A.,2008. Sound the alarm: learned association of predation risk with novelauditory stimuli by fathead minnows (Pimephales promelas) and glowlighttetras (Hemigrammus erythrozonus) after single simultaneous pairings withconspecific chemical alarm cues. Environ. Biol. Fish 81, 141–147.

Fay, R., 2009. Soundscapes and the sense of hearing of fishes. Integrative Zool. 4,26–32.