API

Relationship: 1028

Title

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

Upstream event

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Reduced, Posterior 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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Sex Evidence
Unspecific

Life Stage Applicability

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Term Evidence
All life stages

Key Event Relationship Description

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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.

Evidence Supporting this KER

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

Biological Plausibility

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The posterior 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, as has been suggested previously (Bagci et al., 2015; Hagenaars et al., 2014). Fish without a functional swim bladder are severely disadvantaged, making the likelihood of surviving smaller.

Empirical Evidence

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Buoyancy is one of the primary mechanisms of fish to regulate behaviour, swimming performance and energy expenditure.

Lindsey et al., 2010 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, they reported that the range of swimming depth varies with stages of swim bladder development.

Czesny et al., 2005 reported that yellow perch larvae without inflated swim bladders capture free-swimming prey poorly and expend more energy on feeding and maintaining their position within the water column, due to impacted swimming behaviour.

Kurata et al., 2014 observed that Bluefin tuna larvae present at the bottom of a tank, incapable of swimming upwards, had significantly lower swim bladder inflation.

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. 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).

Michiels et al. (2017) showed that both for controls and zebrafish embryos exposed to an environmental sample, the swimming distance was significantly lower in larvae that failed to inflate the posterior chamber compared to larvae from the same treatment that had inflated posterior chambers.

Exposure of zebrafish embryos to thyroid disrupting compounds resulted in an effect on posterior chamber inflation as well as on the swimming distance in the larval stage (Stinckens et al., unpublished).

All zebrafish larvae that failed to inflate the posterior chamber after exposure to 2 mg/L iopanoic acid (IOP), died by the age of 9 dpf (Stinckens et al., unpublished). Since larvae from the same group that were able to inflate the posterior chamber survived, it is plausible to assume that uninflated posterior chambers limited the ability to swim and find food.

 

Uncertainties and Inconsistencies

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Robertson et al., (2007) reported that the swim bladder only becomes functional as a buoyancy regulator when it is fully developed into a double-chambered swim bladder. This implies that effects on posterior chamber inflation would not directly result in effects on swimming capacity. However, it was also reported that gas in the swim bladder increases the buoyancy of zebrafish larvae already just after initial inflation, while it would be actively controlled only after 28–30 d post hatch. Therefore, an effect on swimming capacity is still likely.

Exposure of zebrafish embryos to 6-propylthiouracil (PTU) resulted in an effect on posterior chamber inflation, but did not result in a direct effect on the swimming distance in the larval stage (Stinckens et al., unpublished). Vergauwen et al. (2015) reported decreased swimming activity as well as impaired posterior chamber inflation after exposure to phenanthrene, a non-polar narcotic, but there was no significant difference between swimming activity of larvae with our without inflated posterior chamber within the same treatment. Possibly, the impact of baseline toxicity on respiration and energy metabolism was more important in decreasing swimming activity compared to impaired inflation of the posterior chamber.

It has been difficult to unambiguously attribute reduced swimming activity to impaired inflation of the posterior chamber, since swimming activity can be altered via different modes of action including altered energy metabolism, altered brain development and thus swimming behaviour. For example, the swimming activity of zebrafish larvae was reduced after 5 days of exposure to 2-mercaptobenzothiazole (MBT), while they had inflated posterior chambers.

Quantitative Understanding of the Linkage

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The quantitative understanding of the linkage between impaired posterior chamber inflation and effect on swimming behaviour is limited.

Response-response Relationship

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Relations between reduced swim bladder inflation and reduced swimming performance are currently based on a binary observation of swim bladder inflation. Several studies have shown that larvae with inflated swim bladders have higher swiming activity compared to larvae that failed to inflate the swim bladder. No direct relationship between swim bladder surface (quantitative measure of swim bladder inflation) and swimming performance has been reported yet.

Time-scale

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The data of Michiels et al. (2017) and Stinckens et al. (unpublished) on swim bladder inflation and swimming activity have been collected on the same day. The process of posterior chamber inflation normally occurs during a specific developmental time frame, resulting in limited flexibility to explore temporal concordance. Based on the biologically plausible direct importance of swim bladder functionality to swimming performance, no lag is expected.

Known modulating factors

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Known Feedforward/Feedback loops influencing this KER

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Domain of Applicability

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Importance of proper functioning of the swim bladder for supporting natural swimming behaviour is generally applicable to fish across sexes and lifestages.

 

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.

Bagci, E., Heijlen, M., Vergauwen, L., Hagenaars, A., Houbrechts, A.M., Esguerra, C.V.,Blust, R., Darras, V.M., Knapen, D., 2015. Deiodinase knockdown during earlyzebrafish development affects growth, development, energy metabolism,motility and phototransduction. PLoS One 10, e0123285, http://dx.doi.org/10.1371/journal.pone.0123285.

Hagenaars, A., Stinckens, E., Vergauwen, L., Bervoets, L., Knapen, D., 2014. PFOSaffects posterior swim bladder chamber inflation and swimming performanceof zebrafish larvae. Aquat. Toxicol. 157, 225–235, http://dx.doi.org/10.1016/j.aquatox.2014.10.017.

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.

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.

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.

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

Michiels, E.D.G., Vergauwen, L., Hagenaars, A., Fransen, E., Van Dongen, S., Van Cruchten, S.J., Bervoets, L., Knapen, D., 2017. Evaluating Complex Mixtures in the Zebrafish Embryo by Reconstituting Field Water Samples: A Metal Pollution Case Study. International Journal of Molecular Sciences 18, 539.

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.

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.

Vergauwen, L., Schmidt, S.N., Stinckens, E., Maho, W., Blust, R., Mayer, P., Covaci, A., Knapen, D., 2015. A high throughput passive dosing format for the Fish Embryo Acute Toxicity test. Chemosphere 139, 9-17.