Abstract
The fish gill is a multifunctional organ that is important in multiple physiological processes such as gas transfer, ionoregulation, and chemoreception. This characteristic organ of fishes has received much attention, yet an often-overlooked point is that larval fishes in most cases do not have a fully developed gill, and thus larval gills do not function identically as adult gills. In addition, large changes associated with gas exchange and ionoregulation happen in gills during the larval phase, leading to the oxygen and ionoregulatory hypotheses examining the environmental constraint that resulted in the evolution of gills. This review thus focuses exclusively on the larval fish gill of teleosts, summarizing the development of teleost larval fish gills and its function in gas transfer, ionoregulation, and chemoreception, and comparing and contrasting it to adult gills where applicable, while providing some insight into the oxygen vs ionoregulatory hypotheses debate.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
No datasets were generated or analysed during the current study.
References
Aihara Y, Yasuoka A, Yoshida Y et al (2007) Transgenic labeling of taste receptor cells in model fish under the control of the 5′-upstream region of medaka phospholipase C-beta 2 gene. Gene Expr Patterns 7:149–157. https://doi.org/10.1016/j.modgep.2006.06.004
Bartels H, Potter IC (2004) Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys: Implications for osmoregulation in fresh and seawater. J Exp Biol 207:3447–3462. https://doi.org/10.1242/jeb.01157
Beppu K, Tsutsumi R, Ansai S et al (2022) Development of a screening system for agents that modulate taste receptor expression with the CRISPR-Cas9 system in medaka. Biochem Biophys Res Commun 601:65–72. https://doi.org/10.1016/j.bbrc.2022.02.082
Blair SD, Matheson D, Goss GG (2017) Physiological and morphological investigation of Arctic grayling (Thymallus arcticus) gill filaments with high salinity exposure and recovery. Conserv Physiol 5:cox040. https://doi.org/10.1093/conphys/cox040
Bodinier C, Boulo V, Lorin-Nebel C, Charmantier G (2009) Influence of salinity on the localization and expression of the CFTR chloride channel in the ionocytes of Dicentrarchus labrax during ontogeny. J Anat 214:318–329. https://doi.org/10.1111/j.1469-7580.2009.01050.x
Brauner CJ, Rombough PJ (2012) Ontogeny and paleophysiology of the gill: new insights from larval and air-breathing fish. Respir Physiol Neurobiol 184:293–300. https://doi.org/10.1016/j.resp.2012.07.011
Burggren W (1984) Transition of respiratory processes during amphibian metamorphosis: from egg to adult. In: Seymour RS (ed) Respiration and metabolism of embryonic vertebrates. Springer, Dordrecht, pp 31–53
Burggren WW, West NH (1982) Changing respiratory importance of gills, lungs and skin during metamorphosis in the bullfrog rana catesbeiana. Respir Physiol 47:151–164. https://doi.org/10.1016/0034-5687(82)90108-6
Burleson ML, Mercer SE, Wilk-Blaszczak MA (2006) Isolation and characterization of putative O2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res 1092:100–107. https://doi.org/10.1016/j.brainres.2006.03.085
Cadiz L, Reed M, Monis S et al (2023) Identification of signalling pathways involved in gill regeneration in zebrafish. https://doi.org/10.1242/jeb.246290
Choe CP, Crump JG (2014) Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a. Development 141:3583–3593. https://doi.org/10.1242/dev.111740
Choe CP, Collazo A, Trinh LA et al (2013) Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev Cell 24:296–309. https://doi.org/10.1016/j.devcel.2012.12.003
Crump JG, Maves L, Lawson ND et al (2004) An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 131:5703–5716. https://doi.org/10.1242/dev.01444
Damas H (1944) Recherches sur le developpement de Lampetra fluviatilis L.—contribution a l’etude de la cephalogenese des vertebres. Arch Biol (paris) 55:1–289
David NB, Saint-Etienne L, Tsang M et al (2002) Requirement for endoderm and FGF3 in ventral head skeleton formation. Development 129:4457–4468. https://doi.org/10.1242/dev.129.19.4457
Dos Santos NMS, Taverne-Thiele JJ, Barnes AC et al (2001) The gill is a major organ for antibody secreting cell production following direct immersion of sea bass (Dicentrarchus labrax, L.) in a Photobacterium damselae ssp. piscicida bacterin: an ontogenetic study. Fish Shellfish Immunol 11:65–74. https://doi.org/10.1006/fsim.2000.0295
Dunaevskaya E (2010) Histological investigations of organs and tissues development of ballan wrasse larvae during ontogenesis. Master, Bodø University College
Dymowska AK, Hwang P-P, Goss GG (2012) Structure and function of ionocytes in the freshwater fish gill. Respir Physiol Neurobiol 184:282–292. https://doi.org/10.1016/j.resp.2012.08.025
El-Fiky N, Hinterleitner S, Wieser W (1987) Differentiation of swimming muscles and gills, and development of anaerobic power in the larvae of cyprinid fish (Pisces, Teleostei). Zoomorphology 107:126–132. https://doi.org/10.1007/BF00312122
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177
Finnerty SH (2019) Tracking ontogenetic changes of ionocyte distribution and morphology in larval white seabass (Atractoscion nobilis). M.S., University of California, San Diego
Foscarini R (1989) A comparative study of the skin and gill structure in oviparous and viviparous freshwater fish larvae. J Fish Biol 34:31–40. https://doi.org/10.1111/j.1095-8649.1989.tb02955.x
Fu C, Wilson JM, Rombough PJ, Brauner CJ (2010) Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss. Proc R Soc B Biol Sci 277:1553–1560. https://doi.org/10.1098/rspb.2009.1545
Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268–273. https://doi.org/10.1126/science.220.4594.268
Gao X, Hong L, Liu Z et al (2016) An integrative study of larval organogenesis of American shad Alosa sapidissima in histological aspects. Chin J Ocean Limnol 34:136–152. https://doi.org/10.1007/s00343-016-5008-2
Giacomin M, Bryant HJ, Val AL et al (2019) The osmorespiratory compromise: physiological responses and tolerance to hypoxia are affected by salinity acclimation in the euryhaline Atlantic killifish (Fundulus heteroclitus). J Exp Biol 222:jeb206599. https://doi.org/10.1242/jeb.206599
Gillis JA, Tidswell ORA (2017) The origin of vertebrate gills. Curr Biol 27:729–732. https://doi.org/10.1016/j.cub.2017.01.022
Gillis JA, Dahn RD, Shubin NH (2009a) Chondrogenesis and homology of the visceral skeleton in the little skate, Leucoraja erinacea (Chondrichthyes: Batoidea). J Morphol 270:628–643. https://doi.org/10.1002/jmor.10710
Gillis JA, Dahn RD, Shubin NH (2009b) Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc Natl Acad Sci 106:5720–5724. https://doi.org/10.1073/pnas.0810959106
Gilmour KM, Perry SF (2018) Conflict and compromise: using reversible remodeling to manage competing physiological demands at the fish gill. Physiology 33:412–422. https://doi.org/10.1152/physiol.00031.2018
Girard JP, Payan P (1980) Ion exchanges through respiratory and chloride cells in freshwater- and seawater-adapted teleosteans. Am J Physiol Regul Integr Comp Physiol 238:R260–R268. https://doi.org/10.1152/ajpregu.1980.238.3.R260
Glenn Northcutt R (2005) The new head hypothesis revisited. J Exp Zool B Mol Dev Evol 304B:274–297. https://doi.org/10.1002/jez.b.21063
González ME, Blánquez MJ, Rojo C (1996) Early gill development in the rainbow trout, Oncorhynchus mykiss. J Morphol 229:201–217. https://doi.org/10.1002/(SICI)1097-4687(199608)229:2<201::AID-JMOR5>3.0.CO;2-3
Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15. https://doi.org/10.1017/S0094837300004310
Hachero-Cruzado I, Ortiz-Delgado JB, Borrega B et al (2009) Larval organogenesis of flatfish brill Scophthalmus rhombus L: histological and histochemical aspects. Aquaculture 286:138–149. https://doi.org/10.1016/j.aquaculture.2008.09.039
Hall C, Flores MV, Murison G et al (2006) An essential role for zebrafish Fgfrl1 during gill cartilage development. Mech Dev 123:925–940. https://doi.org/10.1016/j.mod.2006.08.006
Hamada K (1968) Development of a goby, [Chaenogobius urotaenia], with special reference to the gill and the chloride cell. Bull Fac Fish Hokkaido Univ 19:185–197
Herzog W, Sonntag C, von der Hardt S et al (2004) Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis. Development 131:3681–3692. https://doi.org/10.1242/dev.01235
Hiroi J, McCormick SD (2012) New insights into gill ionocyte and ion transporter function in euryhaline and diadromous fish. Respir Physiol Neurobiol 184:257–268. https://doi.org/10.1016/j.resp.2012.07.019
Hiroi J, Kaneko T, Seikai T, Tanaka M (1998) Developmental sequence of chloride cells in the body skin and gills of Japanese flounder (Paralichthys olivaceus) larvae. jzoo 15:455–460. https://doi.org/10.2108/0289-0003(1998)15[455:DSOCCI]2.0.CO;2
Hirschberger C, Gillis JA (2022) The pseudobranch of jawed vertebrates is a mandibular arch-derived gill. Development 149:dev200184. https://doi.org/10.1242/dev.200184
Hogan BM, Hunter MP, Oates AC et al (2004) Zebrafish gcm2 is required for gill filament budding from pharyngeal ectoderm. Dev Biol 276:508–522. https://doi.org/10.1016/j.ydbio.2004.09.018
Huang C-Y, Lin C-H, Lin H-C (2015) Development of gas exchange and ion regulation in two species of air-breathing fish, Betta splendens and Macropodus opercularis. Comp Biochem Physiol a: Mol Integr Physiol 185:24–32. https://doi.org/10.1016/j.cbpa.2015.03.008
Hughes GM (1984) 1 general anatomy of the gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10, part A. Academic Press, pp 1–72
Hwang PP (1990) Salinity effects on development of chloride cells in the larvae of ayu (Plecoglossus altivelis). Mar Biol 107:1–7. https://doi.org/10.1007/BF01313236
Hwang P-P, Lee T-H, Lin L-Y (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47. https://doi.org/10.1152/ajpregu.00047.2011
Ishimaru Y, Okada S, Naito H et al (2005) Two families of candidate taste receptors in fishes. Mech Dev 122:1310–1321. https://doi.org/10.1016/j.mod.2005.07.005
Iwai T, Hughes GM (1977) Preliminary morphometric study on gill development in black sea bream (Acanthopagrus schlegeli). Nippon Suisan Gakkaishi 43:929–934. https://doi.org/10.2331/suisan.43.929
Jackman WR, Draper BW, Stock DW (2004) Fgf signaling is required for zebrafish tooth development. Dev Biol 274:139–157. https://doi.org/10.1016/j.ydbio.2004.07.003
Jin S, Jiyun O, Stellabotte F, Choe CP (2018) Foxi1 promotes late-stage pharyngeal pouch morphogenesis through ectodermal Wnt4a activation. Dev Biol 441:12–18. https://doi.org/10.1016/j.ydbio.2018.06.011
Jonz MG, Nurse CA (2005) Development of oxygen sensing in the gills of zebrafish. J Exp Biol 208:1537–1549. https://doi.org/10.1242/jeb.01564
Jonz MG, Nurse CA (2006) Epithelial mitochondria-rich cells and associated innervation in adult and developing zebrafish. J Comp Neurol 497:817–832. https://doi.org/10.1002/cne.21020
Jonz MG, Fearon IM, Nurse CA (2004) Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J Physiol 560:737–752. https://doi.org/10.1113/jphysiol.2004.069294
Kameda Y (2021) Comparative morphological and molecular studies on the oxygen-chemoreceptive cells in the carotid body and fish gills. Cell Tissue Res 384:255–273. https://doi.org/10.1007/s00441-021-03421-y
Kapsimali M, Kaushik A-L, Gibon G et al (2011) Fgf signaling controls pharyngeal taste bud formation through miR-200 and Delta-Notch activity. Development 138:3473–3484. https://doi.org/10.1242/dev.058669
Katoh F, Shimizu A, Uchida K, Kaneko T (2000) Shift of chloride cell distribution during early life stages in seawater-adapted killifish. Fundulus Heteroclitus Jzoo 17:11–18. https://doi.org/10.2108/zsj.17.11
Krogh A (1941) The comparative physiology of respiratory mechanisms. University of Pennsylvania Press, Philadelphia
Kunert E, Joyce W, Pan YK et al (2022) Role of cytosolic carbonic anhydrase Ca17a in cardiorespiratory responses to CO2 in developing zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 323:R532–R546. https://doi.org/10.1152/ajpregu.00050.2022
Kwan GT, Wexler JB, Wegner NC, Tresguerres M (2019) Ontogenetic changes in cutaneous and branchial ionocytes and morphology in yellowfin tuna (Thunnus albacares) larvae. J Comp Physiol B 189:81–95. https://doi.org/10.1007/s00360-018-1187-9
Kwong RWM, Perry SF (2015) An essential role for parathyroid hormone in gill formation and differentiation of ion-transporting cells in developing zebrafish. Endocrinology 156:2384–2394. https://doi.org/10.1210/en.2014-1968
Leerberg DM, Hopton RE, Draper BW (2019) Fibroblast growth factor receptors function redundantly during zebrafish embryonic development. Genetics 212:1301–1319. https://doi.org/10.1534/genetics.119.302345
Li J, Eygensteyn J, Lock RAC et al (1995) Branchial chloride cells in larvae and juveniles of freshwater tilapia Oreochromis mossambicus. J Exp Biol 198:2177–2184. https://doi.org/10.1242/jeb.198.10.2177
Liem KF (1981) Larvae of air-breathing fishes as countercurrent flow devices in hypoxic environments. Science 211:1177–1179. https://doi.org/10.1126/science.7466391
Liu X, Wang H, Li G et al (2013) The function of DrPax1b gene in the embryonic development of zebrafish. Genes Genet Syst 88:261–269. https://doi.org/10.1266/ggs.88.261
Liu Y-H, Lin T-C, Hwang S-PL (2020) Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development. Mech Dev 161:103598. https://doi.org/10.1016/j.mod.2020.103598
Lorin-Nebel C, Boulo V, Bodinier C, Charmantier G (2006) The Na+/K+/2Cl- cotransporter in the sea bass Dicentrarchus labrax during ontogeny: involvement in osmoregulation. J Exp Biol 209:4908–4922. https://doi.org/10.1242/jeb.02591
Mandic M, Pan YK, Gilmour KM, Perry SF (2020) Relationships between the peak hypoxic ventilatory response and critical O2 tension in larval and adult zebrafish (Danio rerio). J Exp Biol 223:jeb213942. https://doi.org/10.1242/jeb.213942
McDonald DG, McMahon BR (1977) Respiratory development in Arctic char Salvelinus alpinus under conditions of normoxia and chronic hypoxia. Can J Zool 55:1461–1467. https://doi.org/10.1139/z77-189
Melzner F, Podbielski I, Mark FC, Tresguerres M (2022) The silent loss of cell physiology hampers marine biosciences. PLoS Biol 20:e3001641. https://doi.org/10.1371/journal.pbio.3001641
Mendez-Sanchez JF, Burggren WW (2019) Hypoxia-induced developmental plasticity of larval growth, gill and labyrinth organ morphometrics in two anabantoid fish: The facultative air-breather Siamese fighting fish (Betta splendens) and the obligate air-breather the blue gourami (Trichopodus trichopterus). J Morphol 280:193–204. https://doi.org/10.1002/jmor.20931
Miller CT, Yelon D, Stainier DYR, Kimmel CB (2003) Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130:1353–1365. https://doi.org/10.1242/dev.00339
Morgan M (1974) The development of gill arches and gill blood vessels of the rainbow trout, Salmo gairdneri. J Morphol 142:351–363. https://doi.org/10.1002/jmor.1051420309
Morrison CM, Miyake T, Wright JR Jr (2001) Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J Morphol 247:172–195. https://doi.org/10.1002/1097-4687(200102)247:2%3c172::AID-JMOR1011%3e3.0.CO;2-H
Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409. https://doi.org/10.1242/jeb.000281
Nilsson GE, Dymowska A, Stecyk JAW (2012) New insights into the plasticity of gill structure. Respir Physiol Neurobiol 184:214–222. https://doi.org/10.1016/j.resp.2012.07.012
Oğuz AR (2018) Development of osmoregulatory tissues in the Lake van fish (Alburnus tarichi) during larval development. Fish Physiol Biochem 44:227–233. https://doi.org/10.1007/s10695-017-0427-3
Oikawa S, Hirata M, Kita J, Itazawa Y (1999) Ontogeny of respiratory area of a marine teleost, porgy, Pagrus major. Ichthyol Res 46:233–244. https://doi.org/10.1007/BF02678509
Oike H, Nagai T, Furuyama A et al (2007) Characterization of ligands for fish taste receptors. J Neurosci 27:5584–5592. https://doi.org/10.1523/JNEUROSCI.0651-07.2007
Okada K, Inohaya K, Mise T et al (2016) Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka. Development 143:1800–1810. https://doi.org/10.1242/dev.130039
Olson KR (1998) Hormone metabolism by the fish gill. Comp Biochem Physiol A Mol Integr Physiol 119:55–65. https://doi.org/10.1016/S1095-6433(97)00406-6
Padrós F, Villalta M, Gisbert E, Estévez A (2011) Morphological and histological study of larval development of the Senegal sole Solea senegalensis: an integrative study. J Fish Biol 79:3–32. https://doi.org/10.1111/j.1095-8649.2011.02942.x
Pan Y (2021) Oxygen chemoreception in larval zebrafish: From signal initiation to the hypoxic ventilatory response. PhD Thesis, Université d’Ottawa/University of Ottawa
Pan YK, Perry SF (2020) Neuroendocrine control of breathing in fish. Mol Cell Endocrinol 509:110800. https://doi.org/10.1016/j.mce.2020.110800
Pan YK, Perry SF (2023) The control of breathing in fishes—historical perspectives and the path ahead. J Exp Biol 226:jeb245529. https://doi.org/10.1242/jeb.245529
Pan YK, Mandic M, Zimmer AM, Perry SF (2019) Evaluating the physiological significance of hypoxic hyperventilation in larval zebrafish (Danio rerio). J Exp Biol 222:jeb204800. https://doi.org/10.1242/jeb.204800
Pan YK, Jensen G, Perry SF (2021) Disruption of tph1 genes demonstrates the importance of serotonin in regulating ventilation in larval zebrafish (Danio rerio). Respir Physiol Neurobiol 285:103594. https://doi.org/10.1016/j.resp.2020.103594
Pan YK, Julian T, Garvey K, Perry SF (2023) Catecholamines modulate the hypoxic ventilatory response of larval zebrafish (Danio rerio). J Exp Biol 226:jeb245051. https://doi.org/10.1242/jeb.245051
Pelster B, Bemis William E (1992) Structure and function of the external gill filaments of embryonic skates (Raja erinacea). Respir Physiol 89:1–13. https://doi.org/10.1016/0034-5687(92)90066-6
Perry SF, Esbaugh A, Braun M, Gilmour KM (2009) Gas transport and gill function in water-breathing fish. In: Glass ML, Wood SC (eds) Cardio-respiratory control in vertebrates: comparative and evolutionary aspects. Springer, Berlin, Heidelberg, pp 5–42
Perry SF, Pan YK, Gilmour KM (2023) Insights into the control and consequences of breathing adjustments in fishes-from larvae to adults. Front Physiol 14:1065573
Piotrowski T, Ahn D, Schilling TF et al (2003) The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130:5043–5052. https://doi.org/10.1242/dev.00704
Pisam M, Massa F, Jammet C, Prunet P (2000) Chronology of the appearance of β, A, and α mitochondria-rich cells in the gill epithelium during ontogenesis of the brown trout (Salmo trutta). Anat Rec 259:301–311. https://doi.org/10.1002/1097-0185(20000701)259:3%3c301::AID-AR70%3e3.0.CO;2-1
Pittman K, Skiftesvik AB, Berg L (1990) Morphological and behavioural development of halibut, Hippoglossus hippoglossus (L.) larvae. J Fish Biol 37:455–472. https://doi.org/10.1111/j.1095-8649.1990.tb05876.x
Porteus C, Kumai Y, Abdallah SJ et al (2021) Respiratory responses to external ammonia in zebrafish (Danio rerio). Comp Biochem Physiol A Mol Integr Physiol 251:110822. https://doi.org/10.1016/j.cbpa.2020.110822
Prescott LA, Regish AM, McMahon SJ et al (2021) Rapid embryonic development supports the early onset of gill functions in two coral reef damselfishes. J Exp Biol 224:jeb242364. https://doi.org/10.1242/jeb.242364
Qin Z, Lewis JE, Perry SF (2010) Zebrafish (Danio rerio) gill neuroepithelial cells are sensitive chemoreceptors for environmental CO2. J Physiol 588:861–872. https://doi.org/10.1113/jphysiol.2009.184739
Randall DJ, Baumgarten D, Malyusz M (1972) The relationship between gas and ion transfer across the gills of fishes. Comp Biochem Physiol A Physiol 41:629–637. https://doi.org/10.1016/0300-9629(72)90017-5
Reed M, Jonz MG (2022) Neurochemical signalling associated with gill oxygen sensing and ventilation: a receptor focused mini-review. Front Physiol 13:940020
Rombough PJ (1992) Intravascular oxygen tensions in cutaneously respiring rainbow trout (Oncorhynchus mykiss) larvae. Comp Biochem Physiol A Physiol 101:23–27. https://doi.org/10.1016/0300-9629(92)90622-W
Rombough PJ (1998) Partitioning of oxygen uptake between the gills and skin in fish larvae: a novel method for estimating cutaneous oxygen uptake. J Exp Biol 201:1763–1769. https://doi.org/10.1242/jeb.201.11.1763
Rombough PJ (1999) The gill of fish larvae. Is it primarily a respiratory or an ionoregulatory structure? J Fish Biol 55:186–204. https://doi.org/10.1111/j.1095-8649.1999.tb01055.x
Rombough P (2002) Gills are needed for ionoregulation before they are needed for O2 uptake in developing zebrafish, Danio rerio. J Exp Biol 205:1787–1794. https://doi.org/10.1242/jeb.205.12.1787
Rombough P (2007) The functional ontogeny of the teleost gill: which comes first, gas or ion exchange? Comp Biochem Physiol a: Mol Integr Physiol 148:732–742. https://doi.org/10.1016/j.cbpa.2007.03.007
Rombough PJ, Ure D (1991) Partitioning of oxygen uptake between cutaneous and branchial surfaces in larval and young juvenile chinook salmon Oncorhynchus tshawytscha. Physiol Zool 64:717–727. https://doi.org/10.1086/physzool.64.3.30158203
Rubner M (1883) Über den Einfluss der Körpergrösse auf Stoff- und Kraftwechsel. Z Biol 19:536
Sackville MA, Brauner CJ (2018) case study: gill plasticity in larval fishes. In: Burggren W, Dubansky B (eds) Development and environment. Springer, Cham, pp 377–400
Sackville MA, Cameron CB, Gillis JA, Brauner CJ (2022) Ion regulation at gills precedes gas exchange and the origin of vertebrates. Nature 610:699–703. https://doi.org/10.1038/s41586-022-05331-7
Sánchez-Amaya MI, Ortiz-Delgado JB, García-López Á et al (2007) Larval ontogeny of redbanded seabream Pagrus auriga Valenciennes, 1843 with special reference to the digestive system. A histological and histochemical approach. Aquaculture 263:259–279. https://doi.org/10.1016/j.aquaculture.2006.10.036
Santamarı́a CA, Marı́n de Mateo M, Traveset R et al (2004) Larval organogenesis in common dentex Dentex dentex L. (Sparidae): histological and histochemical aspects. Aquaculture 237:207–228. https://doi.org/10.1016/j.aquaculture.2004.03.020
Sasaki MM, Nichols JT, Kimmel CB (2013) edn1 and hand2 interact in early regulation of pharyngeal arch outgrowth during zebrafish development. PLoS ONE 8:e67522. https://doi.org/10.1371/journal.pone.0067522
Schilling TF, Piotrowski T, Grandel H et al (1996) Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 123:329–344. https://doi.org/10.1242/dev.123.1.329
Schreiber AM, Specker JL (1999) Metamorphosis in the summer flounder Paralichthys dentatus: changes in gill mitochondria-rich cells. J Exp Biol 202:2475–2484. https://doi.org/10.1242/jeb.202.18.2475
Segner H, Storch V, Reinecke M et al (1994) The development of functional digestive and metabolic organs in turbot, Scophthalmus maximus. Marine Bioliogy 119:471–486. https://doi.org/10.1007/BF00347544
Shadrin AM, Ozernyuk ND (2002) Development of the gill system in early ontogenesis of the zebrafish and ninespine stickleback. Russ J Dev Biol 33:91–96. https://doi.org/10.1023/A:1014916229219
Shen ACY, Leatherland JF (1978) Effect of ambient salinity on ionic and osmotic regulation of eggs, larvae, and alevins of rainbow trout (Salmo gairdneri). Can J Zool 56:571–577. https://doi.org/10.1139/z78-081
Shih S-W, Yan J-J, Chou M-Y, Hwang P-P (2023) Recent progress and debates in molecular physiology of Na+ uptake in teleosts. Front Mar Sci 10:1066929
Shone V, Graham A (2014) Endodermal/ectodermal interfaces during pharyngeal segmentation in vertebrates. J Anat 225:479–491. https://doi.org/10.1111/joa.12234
Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251. https://doi.org/10.1016/j.resp.2006.02.006
Soulika M, Kaushik A-L, Mathieu B et al (2016) Diversity in cell motility reveals the dynamic nature of the formation of zebrafish taste sensory organs. Development 143:2012–2024. https://doi.org/10.1242/dev.134817
Sperber SM, Saxena V, Hatch G, Ekker M (2008) Zebrafish dlx2a contributes to hindbrain neural crest survival, is necessary for differentiation of sensory ganglia and functions with dlx1a in maturation of the arch cartilage elements. Dev Biol 314:59–70. https://doi.org/10.1016/j.ydbio.2007.11.005
Stockard CR (1906) The development of the mouth and gills in Bdellostoma stouti. Am J Anat 5:481–517. https://doi.org/10.1002/aja.1000050405
Talbot JC, Johnson SL, Kimmel CB (2010) hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development 137:2507–2517. https://doi.org/10.1242/dev.049700
Tang S-L, Liang X-F, Wang Y et al (2022) Development of gill rakers may influence the prey choice in Chinese perch (Siniperca chuatsi) larvae. Aquac Res 53:1973–1980. https://doi.org/10.1111/are.15726
Thiruppathy M, Fabian P, Gillis JA, Crump JG (2022) Gill developmental program in the teleost mandibular arch. eLife 11:e78170. https://doi.org/10.7554/eLife.78170
Tresguerres M, Kwan GT, Weinrauch A (2023) Evolving views of ionic, osmotic and acid–base regulation in aquatic animals. J Exp Biol 226:jeb245747. https://doi.org/10.1242/jeb.245747
Valerio PF (1995) The development of embryos and larvae of the Atlantic cod, Gadus morhua, with particular emphasis on the ontogeny of chloride cells. Doctoral, Memorial University of Newfoundland
van Dam L (1938) On the utilization of oxygen and regulation of breathing in some aquatic animals. PhD, University of Groningen
Walker MB, Miller CT, Coffin Talbot J et al (2006) Zebrafish furin mutants reveal intricacies in regulating Endothelin1 signaling in craniofacial patterning. Dev Biol 295:194–205. https://doi.org/10.1016/j.ydbio.2006.03.028
Walshe J, Mason I (2003) Fgf signalling is required for formation of cartilage in the head. Dev Biol 264:522–536. https://doi.org/10.1016/j.ydbio.2003.08.010
Warga RM, Nüsslein-Volhard C (1999) Origin and development of the zebrafish endoderm. Development 126:827–838. https://doi.org/10.1242/dev.126.4.827
Wells PR, Pinder AW (1996a) The respiratory development of Atlantic salmon: II. Partitioning of oxygen uptake among gills, yolk sac and body surfaces. J Exp Biol 199:2737–2744. https://doi.org/10.1242/jeb.199.12.2737
Wells PR, Pinder AW (1996b) The respiratory development of Atlantic salmon: I. Morphometry of gills, yolk sac and body surface. J Exp Biol 199:2725–2736. https://doi.org/10.1242/jeb.199.12.2725
Wilson JM, Laurent P (2002) Fish gill morphology: inside out. J Exp Zool 293:192–213. https://doi.org/10.1002/jez.10124
Wood CM, Eom J (2021) The osmorespiratory compromise in the fish gill. Comp Biochem Physiol A Mol Integr Physiol 254:110895. https://doi.org/10.1016/j.cbpa.2021.110895
Yan Y-L, Bhattacharya P, He XJ et al (2012) Duplicated zebrafish co-orthologs of parathyroid hormone-related peptide (PTHrP, Pthlh) play different roles in craniofacial skeletogenesis. J Endocrinol 214:421–435. https://doi.org/10.1530/JOE-12-0110
Yoshida Y, Saitoh K, Aihara Y et al (2007) Transient receptor potential channel M5 and phospholipaseC-β2 colocalizing in zebrafish taste receptor cells. NeuroReport 18:1517. https://doi.org/10.1097/WNR.0b013e3282ec6874
Zachar PC, Jonz MG (2012a) Neuroepithelial cells of the gill and their role in oxygen sensing. Respir Physiol Neurobiol 184:301–308. https://doi.org/10.1016/j.resp.2012.06.024
Zachar PC, Jonz MG (2012b) Oxygen sensitivity of gill neuroepithelial cells in the anoxia-tolerant goldfish. In: Nurse CA, Gonzalez C, Peers C, Prabhakar N (eds) Arterial chemoreception. Springer, Dordrecht, pp 167–172
Zachar PC, Jonz MG (2012c) Confocal imaging of Merkel-like basal cells in the taste buds of zebrafish. Acta Histochem 114:101–115. https://doi.org/10.1016/j.acthis.2011.03.006
Zhang L, Nurse CA, Jonz MG, Wood CM (2011) Ammonia sensing by neuroepithelial cells and ventilatory responses to ammonia in rainbow trout. J Exp Biol 214:2678–2689. https://doi.org/10.1242/jeb.055541
Zimmer AM, Wood CM (2015) Ammonia first? The transition from cutaneous to branchial ammonia excretion in developing rainbow trout is not altered by exposure to chronically high NaCl. J Exp Biol 218:1467–1470. https://doi.org/10.1242/jeb.119362
Zimmer AM, Perry SF (2022) Physiology and aquaculture: a review of ion and acid-base regulation by the gills of fishes. Fish Fish 23:874–898. https://doi.org/10.1111/faf.12659
Zimmer AM, Wright PA, Wood CM (2014) What is the primary function of the early teleost gill? Evidence for Na+/NH+4 exchange in developing rainbow trout (Oncorhynchus mykiss). Proc R Soc B Biol Sci 281:20141422. https://doi.org/10.1098/rspb.2014.1422
Zimmer AM, Wright PA, Wood CM (2017) Ammonia and urea handling by early life stages of fishes. J Exp Biol 220:3843–3855. https://doi.org/10.1242/jeb.140210
Zimmer AM, Pan YK, Chandrapalan T et al (2019) Loss-of-function approaches in comparative physiology: is there a future for knockdown experiments in the era of genome editing? J Exp Biol 222:jeb175737. https://doi.org/10.1242/jeb.175737
Zimmer AM, Mandic M, Rourke KM, Perry SF (2020) Breathing with fins: do the pectoral fins of larval fishes play a respiratory role? Am J Physiol Regul Integr Comp Physiol 318:R89–R97. https://doi.org/10.1152/ajpregu.00265.2019
Funding
Michael Smith Health Research BC.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Steve Perry.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pan, Y.K. Structure and function of the larval teleost fish gill. J Comp Physiol B (2024). https://doi.org/10.1007/s00360-024-01550-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00360-024-01550-8