Magnus L Aaskov, Atsushi Ishimatsu, Jens R Nyengaard, Hans Malte, Henrik Lauridsen, Nguyen Thi Kim Ha, Do Thi Thanh Huong, Mark Bayley
{"title":"Modulation of gill surface area does not correlate with oxygen loss in <i>Chitala ornata</i>.","authors":"Magnus L Aaskov, Atsushi Ishimatsu, Jens R Nyengaard, Hans Malte, Henrik Lauridsen, Nguyen Thi Kim Ha, Do Thi Thanh Huong, Mark Bayley","doi":"10.1098/rspb.2024.1884","DOIUrl":null,"url":null,"abstract":"<p><p>Air-breathing fish risk losing aerially sourced oxygen to ambient hypoxic water since oxygenated blood from the air-breathing organ returns through the heart to the branchial basket before distribution. This loss is thought to help drive the evolutionary reduction in gill size with the advent of air-breathing. In many teleost fish, gill size is known to be highly plastic by modulation of their anatomic diffusion factor (ADF) with inter-lamellar cell mass (ILCM). In the anoxia-tolerant crucian carp, ILCM recedes with hypoxia but regrows in anoxia. The air-breathing teleost <i>Chitala ornata</i> has been shown to increase gill ADF from normoxic to mildly hypoxic water by reducing ILCM. Here, we test the hypothesis that ADF is modulated to minimize oxygen loss in severe aquatic hypoxia by measuring ADF, gas-exchange, and by using computed tomography scans to reveal possible trans-branchial shunt vessels. Contrary to our hypothesis, ADF does not modulate to prevent oxygen loss and despite no evident trans-branchial shunting, <i>C. ornata</i> loses only 3% of its aerially sourced O<sub>2</sub> while still excreting 79% of its CO<sub>2</sub> production to the severely hypoxic water. We propose this is achieved by ventilatory control and by compensating the minor oxygen loss by extra aerial O<sub>2</sub> uptake.</p>","PeriodicalId":20589,"journal":{"name":"Proceedings of the Royal Society B: Biological Sciences","volume":"291 2033","pages":"20241884"},"PeriodicalIF":3.8000,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521143/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the Royal Society B: Biological Sciences","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1098/rspb.2024.1884","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/16 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Air-breathing fish risk losing aerially sourced oxygen to ambient hypoxic water since oxygenated blood from the air-breathing organ returns through the heart to the branchial basket before distribution. This loss is thought to help drive the evolutionary reduction in gill size with the advent of air-breathing. In many teleost fish, gill size is known to be highly plastic by modulation of their anatomic diffusion factor (ADF) with inter-lamellar cell mass (ILCM). In the anoxia-tolerant crucian carp, ILCM recedes with hypoxia but regrows in anoxia. The air-breathing teleost Chitala ornata has been shown to increase gill ADF from normoxic to mildly hypoxic water by reducing ILCM. Here, we test the hypothesis that ADF is modulated to minimize oxygen loss in severe aquatic hypoxia by measuring ADF, gas-exchange, and by using computed tomography scans to reveal possible trans-branchial shunt vessels. Contrary to our hypothesis, ADF does not modulate to prevent oxygen loss and despite no evident trans-branchial shunting, C. ornata loses only 3% of its aerially sourced O2 while still excreting 79% of its CO2 production to the severely hypoxic water. We propose this is achieved by ventilatory control and by compensating the minor oxygen loss by extra aerial O2 uptake.
期刊介绍:
Proceedings B is the Royal Society’s flagship biological research journal, accepting original articles and reviews of outstanding scientific importance and broad general interest. The main criteria for acceptance are that a study is novel, and has general significance to biologists. Articles published cover a wide range of areas within the biological sciences, many have relevance to organisms and the environments in which they live. The scope includes, but is not limited to, ecology, evolution, behavior, health and disease epidemiology, neuroscience and cognition, behavioral genetics, development, biomechanics, paleontology, comparative biology, molecular ecology and evolution, and global change biology.