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Relationship: 1028
Title
Reduced, Posterior swim bladder inflation leads to Reduced, Swimming performance
Upstream event
Downstream event
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) | Under Development: Contributions and Comments Welcome | WPHA/WNT Endorsed |
Deiodinase 1 inhibition leading to increased mortality via reduced posterior swim bladder inflation | adjacent | Moderate | Low | Agnes Aggy (send email) | Under Development: Contributions and Comments Welcome | WPHA/WNT Endorsed |
Taxonomic Applicability
Term | Scientific Term | Evidence | Link |
---|---|---|---|
zebrafish | Danio rerio | High | NCBI |
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 |
Sex Applicability
Sex | Evidence |
---|---|
Unspecific | Moderate |
Life Stage Applicability
Term | Evidence |
---|---|
Embryo | High |
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 Collection Strategy
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.
Biological Plausibility
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.
Empirical Evidence
Buoyancy is one of the primary mechanisms of fish to regulate behaviour, swimming performance and energy expenditure. There is extensive evidence of a link between reduced posterior chamber inflation and reduced swimming performance:
- Stewart and Gee (1981) showed that fathead minnows swimming from still water to a current resorbed gas to fill the swim bladder and tailor buoyancy precisely to the level were swimming is most efficient.
- Lindsey et al., 2010 reported that zebrafish 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 sea bass 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., 1977).
- Permanent DIO 2 deficiency in zebrafish was shown to result in reduced posterior chamber inflation and disturbed locomotor activity (Houbrechts et al., 2016).
- 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., 2020). 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.
- Hagenaars et al. (2014) showed that zebrafish embryos exposed to 4.28 mg/L PFOS had lower swimming speeds when the posterior chamber was not inflated. It should be noted that almost all larvae with a non-inflated swimbladder had a spinal curvature and it could therefore not statistically be determined whether the reduced swimming speed was due to a spinal curvature, a non-inflated swim bladder or the interaction of both.
- Knockdown of deiodinase 3 (expected to lead to hyperthyroidism) in zebrafish was shown to result in both impaired inflation of the posterior chamber and reduced swimming activity and escape response (Heijlen et al., 2014; Bagci et al., 2015).
- Massei et al. (in preparation) showed that impaired swim bladder inflation and reduced swimming activity of 5 day old zebrafish larvae were correlated after exposure to narcotics.
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.
Known modulating factors
Quantitative Understanding of the Linkage
The quantitative understanding of the linkage between impaired posterior chamber inflation and effect on swimming behaviour is limited.
Response-response Relationship
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
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 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: This KE/KER is plausibly applicable to both sexes. Sex differences are not often investigated in tests using early life stages of fish. In Medaka, sex can be morphologically distinguished as soon as 10 days post fertilization. Females appear more susceptible to thyroid‐induced swim bladder dysfunction compared with males (Godfrey et al., 2019). In zebrafish and fathead minnow, it is currently unclear whether sex-related differences are important in determining the magnitude of the changes in this KE/KER. 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 in zebrafish, when sex differentiation has not started yet, sex differences are expected to play a minor role. Fathead minnow gonad differentiation also occurs during larval development. Fathead minnows utilize a XY sex determination strategy and markers can be used to genotype sex in life stages where the sex is not yet clearly defined morphologically (Olmstead et al., 2011). Ovarian differentiation starts at 10 dph followed by rapid development (Van Aerle et al., 2004). At 25 dph germ cells of all stages up to the primary oocytes stage were present and at 120 dph, vitellogenic oocytes were present. The germ cells (spermatogonia) of the developing testes only entered meiosis around 90–120 dph. Mature testes with spermatozoa are present around 150 dph. Since the posterior chamber inflates around 6 days post fertilization (1 dph) in fathead minnows, sex differences are expected to play a minor role in the current AOP.
References
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.
Godfrey A, Hooser B, Abdelmoneim A, Sepulveda MS. 2019. Sex-specific endocrine-disrupting effects of three halogenated chemicals in japanese medaka. Journal of Applied Toxicology. 39(8):1215-1223.
Goodsell, D.S., Morris, G.M., Olsen, A.J. 1996. Automated docking of fleixble ligands. Applications of Autodock. J. Mol. Recogonition, 9:1-5.
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.
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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.
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