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Reduced, Posterior swim bladder inflation leads to Reduced, Swimming performance
Key Event Relationship Overview
AOPs Referencing Relationship
|AOP Name||Adjacency||Weight of Evidence||Quantitative Understanding||Point of Contact||Author Status||OECD Status|
|Deiodinase 2 inhibition leading to increased mortality via reduced posterior swim bladder inflation||adjacent||Moderate||Low||Brendan Ferreri-Hanberry (send email)||Open for adoption||EAGMST Under Review|
|Deiodinase 1 inhibition leading to increased mortality via reduced posterior swim bladder inflation||adjacent||Moderate||Low||Agnes Aggy (send email)||Open for adoption||EAGMST Under Review|
|fathead minnow||Pimephales promelas||Moderate||NCBI|
|bluefin tuna||Thunnus thynnus||Moderate||NCBI|
|Dicentrarchus labrax||Dicentrarchus labrax||Moderate||NCBI|
|Perca flavescens||Perca flavescens||Moderate||NCBI|
|Salmo salar||Salmo salar||Moderate||NCBI|
Life Stage Applicability
Key Event Relationship Description
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 increased mortality.
Evidence Supporting this KER
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.
The posterior chamber of the swim bladder has a function in regulating the buoyancy of fish (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. Stoyek et al. (2011) showed that the posterior chamber volume is maintained at a stable level at varying pressures corresponding to varying depths through gas exchange with the anteror chamber.
Uncertainties and Inconsistencies
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.
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.
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
Known Feedforward/Feedback loops influencing this KER
Domain of Applicability
Taxonomic: Importance of proper functioning of the swim bladder for supporting natural swimming behaviour can be plausibly assumed to be generally applicable to fish possessing a posterior chamber. Evidence exists for a wide variety of freshwater and marine fish species.
Life stage: This KER is only applicable to early embryonic development, which is the period where the posterior swim bladder chamber inflates. To what extent fish can survive and swim with partly inflated swim bladders during later life stages is unknown.
Sex: Zebrafish are undifferentiated gonochorists since both sexes initially develop an immature ovary (Maack and Segner, 2003). Immature ovary development progresses until approximately the onset of the third week. Later, in female fish immature ovaries continue to develop further, while male fish undergo transformation of ovaries into testes. Final transformation into testes varies among male individuals, however finishes usually around 6 weeks post fertilization. Since the posterior chamber inflates around 5 days post fertilization, when sex differentiation has not started yet, sex differences are expected to play a minor role.
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.
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.
Chatain, B., 1994. Abnormal swimbladder development and lordosis in sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). Aquaculture 119:371–379.
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.
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Hagenaars, A., Stinckens, E., Vergauwen, L., Bervoets, L., Knapen, D., 2014. PFOS affects 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.
Heijlen, M., Houbrechts, A., Bagci, E., Van Herck, S., Kersseboom, S., Esguerra, C., Blust, R., Visser, T., Knapen, D., Darras, V., 2014. Knockdown of type 3 iodothyronine deiodinase severely perturbs both embryonic and early larval development in zebrafish. Endocrinology 155, 1547-1559.
Houbrechts, A.M., Delarue, J., Gabriels, I.J., Sourbron, J., Darras, V.M., 2016. Permanent Deiodinase Type 2 Deficiency Strongly Perturbs Zebrafish Development, Growth, and Fertility. Endocrinology 157, 3668-3681.
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.
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.
Maack, G., Segner, H., 2003. Morphological development of the gonads in zebrafish. Journal of Fish Biology 62, 895-906.
Massei R et al. (in preparation) Sublethal adverse effects of non-polar narcotics in the zebrafish embryo.
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.
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.
Stewart, D.B., Gee, J.H., 1981. Mechanisms of buoyancy adjustments and effects of water velocity and temperature on ability to maintain buoyancy in fathead minnows, Pimephales promelas, Rafinesque. Comparative Biochemistry and Physiology a-Physiology 68, 337-347.
Stinckens, E., Vergauwen, L., Blackwell, B.R., Anldey, G.T., Villeneuve, D.L., Knapen, D., 2020. Effect of Thyroperoxidase and Deiodinase Inhibition on Anterior Swim Bladder Inflation in the Zebrafish. Environmental Science & Technology 54, 6213-6223.
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.
Stoyek, M.R., Smith, F.M., Croll, R.P., 2011. Effects of altered ambient pressure on the volume and distribution of gas within the swimbladder of the adult zebrafish, Danio rerio. Journal of Experimental Biology 214, 2962-2972.
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.