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Reduced, Posterior swim bladder inflation leads to Increased Mortality
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||non-adjacent||High||Low||Dries Knapen (send email)||Under Development: Contributions and Comments Welcome||WPHA/WNT Endorsed|
|Deiodinase 1 inhibition leading to increased mortality via reduced posterior swim bladder inflation||non-adjacent||High||Low||Dries Knapen (send email)||Under Development: Contributions and Comments Welcome||WPHA/WNT Endorsed|
Life Stage Applicability
Key Event Relationship Description
Because of its roles in energy sparing and swimming performance, it is expected that failure to inflate the swim bladder would create increased oxygen and energy demands leading to decreased growth, which in turn leads to decreased probability of survival.
Evidence Collection Strategy
Evidence Supporting this KER
There is strong evidence for a link between reduced posterior chamber inflation and increased mortality across different fish species.
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. Efficient regulation of buoyancy is energy sparing and allows for fish to expend less energy in maintaining and changing positions in the water column. Because of its roles in energy sparing and swimming performance, it is expected that failure to inflate the swim bladder would create increased oxygen and energy demands leading to decreased growth, which in turn leads to decreased probability of survival. In particular, these impacts would be expected in non-laboratory environments where fish must expend energy to capture food and avoid predators and where available food is limited. Additionally, fish without a functional swim bladder are severely disadvantaged in terms of foraging and avoiding predators, making the likelihood of surviving smaller.
- Czesny et al. (2005) demonstrated that swim bladder non-inflation was associated with multiple phenotypic and behavioral outcomes that would be expected to adversely impact survival.
- Yellow perch with non-inflated swim bladders grew more slowly than those with inflated swim bladders, both in the laboratory and in the field.
- Yellow perch with non-inflated swim bladders always captured prey less efficiently than those with inflated swim bladders of the same size class.
- Yellow perch with non-inflated swim bladders suffered from increased predation risk.
- Yellow perch with non-inflated swim bladders experienced significantly increased mortality and lower time to mortality in a foodless environment compared to those with inflated swim bladders, indicating greater energy expenditure.
- Yellow perch with non-inflated swim bladders had significantly greater oxygen consumption than fish of the same size class with inflated swim bladders, again indicating greater energy expenditure.
- The authors hypothesized that failed swim bladder inflation occurs frequently in natural systems, but these individuals rarely survive in a natural environment where food resources are limited.
- Note: yellow perch are a physoclistous species in which initial inflation can only occur during a narrow window of development in which the pneumatic duct is still connected to the gut, allowing the fish to gulp air and inflate its swim bladder. Once the pneumatic duct closes, normal inflation is no longer possible.
- In aquaculture systems, failure to inflate the swim bladder has been shown to reduce growth rates and cause high mortalities in a wide range of species (reviewed by Woolley and Qin, 2010).
- Pond-cultured walleye with non-inflated swim bladders were found to be smaller (weight and length) than fish with inflated swim bladders. There was also association with deformities (e.g., lordosis) that were expected to impair survival (Kindschi and Barrows, 1993).
- Review of failed swim bladder inflation in wild perch and 26 other physoclistous species showed that fish whose swim bladders failed to inflate had higher mortality, reduced growth, and increased incidence of spinal malformations stereotypical of persistent upward swimming (Egloff, 1996).
- Chatain (1994) reported that sea bream (Sparus auratus) and sea bass (Dicentrarchus labrax) with non-inflated swim bladders were 20-30% less in weight than those with inflated swim bladders and more susceptible to stress-induced mortality (e.g., associated with handling, hypoxia, etc.). It was suggested this was due to both increased energetic demands and decreased feeding efficiency.
- Marty et al. 1995 measured increased oxygen consumption in Japanese medaka (Oryzias latipes) with non-inflated swim bladders compared to those whose swim bladders had inflated.
- In zebrafish (Danio rerio) whose smim bladder inflation was prevented by holding in a closed chamber (preventing air gulping to inflate the swim bladder), larval survival was significantly less than that of fish held in open chambers whose swim bladders could inflate. There was also increased incidence of spinal curvature in the closed chamber fish whose swim bladders were prevented from inflating (Goolish and Oukutake, 1999).
- Maternal injection of T3, resulting in increased T3 concentrations in the eggs of striped bass (Morone saxatilis) lead to significant increases in both swim bladder inflation and survival (Brown et al., 1988).
- In striped bass, (Morone saxatilis) failure to inflate the swimbladder was reported to results in dysfunctional buoyancy control, deformities, and poor larval survival and growth (Martin-Robichaud and Peterson, 2008).
- 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.
- MeHg and HgCl2 exposure in medaka caused failure to inflate the swim bladder among other malformations, and also caused increased mortality. (Dong et al., 2016)
- Medaka embryos treated either with hypoxia or with a mixture of polyaromatic hydrocarbons showed higher occurrences of swim bladder non-inflation and decreased survival. (Mu et al., 2017)
- Triphenyltin (TPT) exposure in zebrafish embryos induced a high percentage of uninflated swim bladders and all affected larvae died within 9 dph. (Horie et al., 2021)
Uncertainties and Inconsistencies
Some studies showed an absence of increased mortality after impaied posterior chamber inflation but this is probably caused by the fact that observation was limited to short term effects (e.g., Wang et al., 2020). Observations of absence of mortality often performed at 96/120 hpf in zebrafish, which is immediately after posterior chamber inflation.
Known modulating factors
Quantitative Understanding of the Linkage
Specific quantitative relationships between the lack of swim bladder inflation and the decreased probability of survival are lacking and likely to be both species and condition-specific. For example, in laboratory settings where food resources are plentiful, crowding is minimal, and predation is not an issue, impaired inflation may have relatively little or no impact on survival. In contrast, in a natural setting with limited food resources and abundant predators effects on survival may be quite profound.
Known Feedforward/Feedback loops influencing this KER
Domain of Applicability
Taxonomic: The literature provides strong support for the relevance of this KER for physoclistous fish (e.g., yellow perch, Japanese Medaka) whose inflation occurs at a critical time in development when the fish must gulp air to inflate its swim bladder before the pneumatic duct closes. The relevance to physostomes (such as zebrafish and fathead minnows) that maintain an open pneumatic duct into adulthood is less apparent. The latter likely have greater potential to inflate the swim bladder at some point in development, even if early larval inflation is impaired. However, it is plausible that structural damage that prevented inflation of the organ in a phystostome would be expected to cause similar effects.
Life stage: This KER is applicable to early embry-larval development, which is the period where the posterior swim bladder chamber inflates and larvae start to freely feed. To what extent fish can survive with partly inflated swim bladders during later life stages is unknown.
Sex: This KER is probably not sex-dependent since both females and males rely on the posterior swim bladder chamber to regulate buyoancy. Furthermore, 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.
Brown, C. L., Doroshov, S. I., Nunez, J. M., Hadley, C., Vaneenennaam, J., Nishioka, R. S. and Bern, H. A. (1988), Maternal triiodothyronine injections cause increases in swimbladder inflation and survival rates in larval striped bass, Morone saxatilis. J. Exp. Zool., 248: 168–176. doi: 10.1002/jez.1402480207
Chatain B (1994) Abnormal swimbladder development and lordosis in sea bass (Dicentrarcus-labrax) ans sea bream (Sparus-auratus). Aquaculture 119 (4): 371-9
Chatain, Beatrice. "Problems related to the lack of functional swimbladder in intensive rearing of the seabass Dicentrarchus labrax and the sea bream Sparus auratus." Advances in Tropical Aquaculture, Workshop at Tahiti, French Polynesia, 20 Feb-4 Mar 1989. 1989.
Dong W, Liu J, Wei LX, Yang JF, Chernick M, Hinton DE. 2016. Developmental toxicity from exposure to various forms of mercury compounds in medaka fish (oryzias latipes) embryos. Peerj. 4.
Egloff, M. 1996. Failure of swim bladder inflation of perch, Perca fluviatilis, L. found in natural populations. Aquat. Sci. 58(1):15-23.
Gary D. Marty , David E. Hinton & Joseph J. Cech Jr. (1995) Notes: Oxygen Consumption by Larval Japanese Medaka with Inflated or Uninflated Swim Bladders, Transactions of the American Fisheries Society, 124:4, 623-627, DOI: 10.1577/1548-8659(1995).
Goolish, E. M. and Okutake, K. (1999), Lack of gas bladder inflation by the larvae of zebrafish in the absence of an air-water interface. Journal of Fish Biology, 55: 1054–1063. doi:10.1111/j.1095-8649.1999.tb00740.x
Greg A. Kindschi & Frederic T. Barrows (1993) Survey of Swim Bladder Inflation in Walleyes Reared in Hatchery Production Ponds, The Progressive Fish-Culturist, 55:4,219-223, DOI: 10.1577/1548-8640(1993)055<0219:SOSBII>2.3.CO;2
Horie Y, Chiba T, Takahashi C, Tatarazako N, Iguchi T. 2021. Influence of triphenyltin on morphologic abnormalities and the thyroid hormone system in early-stage zebrafish (danio rerio). Comparative Biochemistry and Physiology C-Toxicology & Pharmacology. 242.
Kindschi GA, Barrows FT (1993) Survey of swim bladder inflation in walleyes reared in hatchery production ponds. Progressive Fish-Culturist 55 (4): 219-23
Martin-Robichaud, D. J. and Peterson, R. H. (1998), Effects of light intensity, tank colour and photoperiod on swimbladder inflation success in larval striped bass, Morone saxatilis (Walbaum). Aquaculture Research, 29: 539–547. doi: 10.1046/j.1365-2109.1998.00234.
Mu JL, Chernick M, Dong W, Di Giulio RT, Hinton DE. 2017. Early life co-exposures to a real-world pah mixture and hypoxia result in later life and next generation consequences in medaka (oryzias latipes). Aquatic Toxicology. 190:162-173.
Sergiusz J. Czesny, Brian D. S. Graeb & John M. Dettmers (2005): Ecological Consequences of Swim Bladder Noninflation for Larval Yellow Perch, Transactions of the American Fisheries Society, 134:4, 1011-1020. http://dx.doi.org/10.1577/T04-016.1
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.
Wang JX, Shi GH, Yao JZ, Sheng N, Cui RN, Su ZB, Guo Y, Dai JY. 2020. Perfluoropolyether carboxylic acids (novel alternatives to pfoa) impair zebrafish posterior swim bladder development via thyroid hormone disruption. Environment International. 134.
Woolley, L. D. and Qin, J. G. (2010), Swimbladder inflation and its implication to the culture of marine finfish larvae. Reviews in Aquaculture, 2: 181–190. doi: 10.1111/j.1753-5131.2010.01035.x