Skip to main content
SpringerLink
Log in

The origins of gas exchange and ion regulation in fish gills: evidence from structure and function

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Gill function in gas exchange and ion regulation has played key roles in the evolution of fishes. In this review, we summarize data from the fields of palaeontology, developmental biology and comparative physiology for when and how the gills first acquired these functions. Data from across disciplines strongly supports a stem vertebrate origin for gas exchange structures and function at the gills with the emergence of larger, more active fishes. However, the recent discovery of putative ionocytes in extant cephalochordates and hemichordates suggests that ion regulation at gills might have originated much earlier than gas exchange, perhaps in the ciliated pharyngeal arches in the last common ancestor of deuterostomes. We hypothesize that the ancestral form of ion regulation served a filter-feeding function in the ciliated pharyngeal arches, and was later coopted in vertebrates to regulate extracellular ion and acid–base balance. We propose that future research should explore ionocyte homology and function across extant deuterostomes to test this hypothesis and others in order to determine the ancestral origins of ion regulation in fish gills.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ambort D, Johansson ME, Gustafsson JK, Nilsson HE, Ermund A, Johansson BR, Koeck PJ, Hebert H, Hansson GC (2012) Calcium and pH-dependent packing and release of the gel-forming MUC2 mucin. Proc Natl Acad Sci 109(15):5645–5650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrington EJ (1965) The biology of hemichordata and protochordata. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Bettex-Galland M, Hughes GM (1973) Contractile filamentous material in the pillar cells of fish gills. J Cell Sci 13(2):359–370

    Article  CAS  PubMed  Google Scholar 

  • Birchenough GM, Johansson ME, Gustafsson JK, Bergström JH, Hansson G (2015) New developments in goblet cell mucus secretion and function. Mucosal Immunol 8(4):712–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blewett TA, Goss GG (2017) A novel pathway of nutrient absorption in crustaceans: branchial amino acid uptake in the green shore crab (Carcinus maenas). Proc R Soc B 284(1868):20171298

    Article  PubMed  PubMed Central  Google Scholar 

  • Boot MJ, Gittenberger-De Groot AC, Van Iperen L, Hierck BP, Poelmann RE (2003) Spatiotemporally separated cardiac neural crest subpopulations that target the outflow tract septum and pharyngeal arch arteries. Anat Rec 275A:1009–1018

    Article  Google Scholar 

  • Booth JH (1978) The distribution of blood flow in the gills of fish: Application of a new technique to rainbow trout (Salmo Gairdneri). J Exp Biol 73:119

    Article  Google Scholar 

  • Bronner ME, LeDouarin NM (2012) Development and evolution of the neural crest: an overview. Dev Biol 366(1):2–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cameron JN (1989) The respiratory physiology of animals. Oxford University Press, New York

    Google Scholar 

  • Cameron CB (2005) A phylogeny of the hemichordates based on morphological characters. Can J Zool 83:196–215

    Article  Google Scholar 

  • Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci 97:4469–4474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caron J-B, Morris SC, Cameron CB (2013) Tubicolous enteropneusts from the Cambrian period. Nature 495:503–506

    Article  CAS  PubMed  Google Scholar 

  • Cavanaugh AM, Huang J, Chen JN (2015) Two developmentally distinct populations of neural crest cells contribute to the zebrafish heart. Dev Biol 404(2):103–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clifford AM, Goss GG, Roa JN, Tresguerres M (2015) Acid/base and ionic regulation in hagfish. In: Edwards SL, Goss GG (eds) Hagfish biology. CRC Press, Hoboken, pp 277–298

    Google Scholar 

  • Clifford AM, Zimmer AM, Wood CM, Goss GG (2016) It’s all in the gills: evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin. J Exp Biol 219(18):2814–2818

    PubMed  Google Scholar 

  • Collard M, Laitat K, Moulin L, Catarino AI, Grosjean P, Dubois P (2013) Buffer capacity of the coelomic fluid in echinoderms. Comp Biochem Physiol A Mol Integr Physiol 166:199–206

    Article  CAS  PubMed  Google Scholar 

  • Collard M, De Ridder C, David B, Dehairs F, Dubois P (2015) Could the acid-base status of Antarctic sea urchins indicate a better-than-expected resilience to near-future ocean acidification? Glob Change Biol 21:605–617

    Article  Google Scholar 

  • Damas H (1944) Recherches sur le développement de Lampetra fluviatilis L.-contribution à l’étude de la cephalogénèse des vertébrès. Arch Biol Paris 55:1–289

    Google Scholar 

  • Dohrn A (1884) Studien zur Urgeschichte des Wirbelthierkorpers. IV. Die Entwicklung und Differenzirung der Kiemenbogen der Selachier. V. Zur Entstehung und Differenzirung der Visceralbogen bei Petromyzon planeri. Mitt Zool Stat Neapel 5:102–161

    Google Scholar 

  • Dymowska AK, Hwang P-P, Goss GG (2012) Structure and function of ionocytes in the freshwater fish gill. Respir Physiol Neurobiol 184:282–292

    Article  CAS  PubMed  Google Scholar 

  • Edwards SL, Marshall WS (2012) Principles and patterns of osmoregulation and euryhalinity in fishes. In: McCormick SD, Farrell AP, Brauner CJ (eds) Euryhaline fishes. Academic Press, Hoboken, pp 1–44

    Google Scholar 

  • Esaki M, Hoshijima K, Kobayashi S, Fukuda H, Kawakami K, Hirose S (2007) Visualization in zebrafish larvae of Na+ uptake in mitochondria-rich cells whose differentiation is dependent on foxi3a. Am J Physiol Regul Integr Comp Physiol 292:R470–R480

    Article  CAS  PubMed  Google Scholar 

  • Espinosa M (2002) Acidic pH and increasing [Ca2+] reduce the swelling of mucins in primary cultures of human cervical cells. Hum Reprod 17:1964–1972

    Article  CAS  PubMed  Google Scholar 

  • Evans D (1984) Gill Na+/H+ and Cl-/HCO3- exchange systems evolved before the vertebrates entered fresh water. J Exp Biol 113:465

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Formery L, Peluso P, Kohnle I, Malnick J, Thompson JR, Pitel M, Uhlinger KR, Rokshar DS, Rank DR, Lowe CJ (2023) Molecular evidence of anteroposterior patterning in adult echinoderms. Nature 623:555–561

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268

    Article  CAS  PubMed  Google Scholar 

  • Gillis JA, Tidswell ORA (2017) The origin of vertebrate gills. Curr Biol 27:729–732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillis JA, Fritzenwanker JH, Lowe CJ (2012) A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc R Soc B Biol Sci 279:237–246

    Article  Google Scholar 

  • Glover CN, Bucking C, Wood CM (2011) Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrate. Proc R Soc B Biol Sci 278:3096–3101

    Article  Google Scholar 

  • Glover CN, Bucking C, Wood CM (2013) The skin of fish as a transport epithelium: a review. J Comp Physiol B 183:877–891

    Article  CAS  PubMed  Google Scholar 

  • Goette A (1901) Über die Kiemen der Fische. Z Wiss Zool 69:533–577

    Google Scholar 

  • Gomme J (2001) Transport of exogenous organic substances by invertebrate integuments: the field revisited. J Exp Zool 289:254–265

    Article  CAS  PubMed  Google Scholar 

  • Greco AM, Gilmour KM, Fenwick JC, Perry SF (1995) The effects of softwater acclimation on respiratory gas transfer in the rainbow trout Oncorhynchus mykiss. J Exp Biol 198:2557

    Article  Google Scholar 

  • Greco AM, Fenwick JC, Perry SF (1996) The effects of soft-water acclimation on gill structure in the rainbow trout Oncorhynchus mykiss. Cell Tissue Res 285:75–82

    Article  CAS  PubMed  Google Scholar 

  • Green SA, Simoes-Costa M, Bronner ME (2015) Evolution of vertebrates as viewed from the crest. Nature 520:474–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustafsson JK, Ermund A, Ambort D, Johansson MEV, Nilsson HE, Thorell K, Hebert H, Sjövall H, Hansson GC (2012) Bicarbonate and functional CFTR channel are required for proper mucin secretion and link cystic fibrosis with its mucus phenotype. J Exp Med 209:1263–1272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland LZ (2016) Tunicates. Curr Biol 26:R146–R152

    Article  CAS  PubMed  Google Scholar 

  • Holland ND, Holland LZ, Holland PWH (2015) Scenarios for the making of vertebrates. Nature 520:450–455

    Article  CAS  PubMed  Google Scholar 

  • Hsia CC, Schmitz A, Lambertz M, Perry SF, Maina JN (2013) Evolution of air breathing: oxygen homeostasis and the transitions from water to land and sky. Compr Physiol 3(2):849–915

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsiao C-D, You M-S, Guh Y-J, Ma M, Jiang Y-J, Hwang P-P (2007) A positive regulatory loop between foxi3a and foxi3b is essential for specification and differentiation of zebrafish epidermal ionocytes. PLoS ONE 2:e302

    Article  PubMed  PubMed Central  Google Scholar 

  • Hughes GM, Morgan M (1973) The structure of fish gills in relation to their respiratory function. Biol Rev 48:419–475

    Article  Google Scholar 

  • Hwang PP, Lin LY (2013) Gill ionic transport, acid-base regulation, and nitrogen excretion. In: Evans DH, Claiborne JB, Currie S (eds) The physiology of fishes. CRC Press, Balkema, pp 205–234

    Google Scholar 

  • Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: Recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47

    Article  CAS  PubMed  Google Scholar 

  • Janvier P (2007) Living primitive fishes and fishes from deep time. In: Brauner CJ, Farrell AP, McKenzie DJ (eds) Primitive fishes, fish physiology, vol 26. Academic Press, Hoboken, pp 1–51

    Chapter  Google Scholar 

  • Janvier P (2008) Early jawless vertebrates and cyclostome origins. Zoolog Sci 25:1045–1056

    Article  PubMed  Google Scholar 

  • Janvier P, Pradel A (2015) Elasmobranchs and their extinct relatives: Diversity, relatives and adaptations through time. In: Shadwick R, Brauner CJ, Farrell AP (eds) Physiology of elasmobranch fishes, fish physiology, vol 34A. Academic Press, Hoboken, pp 1–17

    Google Scholar 

  • Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, Fisher S (2012) Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE 7(11):e47394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirsch R, Nonnotte G (1977) Cutaneous respiration in three freshwater teleosts. Resp Physiol 29(3):339–354

    Article  CAS  Google Scholar 

  • Langille RM, Hall BK (1986) Evidence of cranial neural crest contribution to the skeleton of the sea lamprey Petromyzon marinus. In: Slavkin H (ed) Progress in developmental biology. Alan Riss Inc, New York, pp 263–266

    Google Scholar 

  • Langille RM, Hall BK (1988) Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, Petromyzon marinus (L.). Development 102(2):301–310

    Article  Google Scholar 

  • Lesser MP, Martini FH, Heiser JB (1997) Ecology of the hagfish, Myxine glutinosa L. in the Gulf of Maine I. Metabolic rates and energetics. J Exp Mar Biol Ecol 208(1–2):215–225

    Article  Google Scholar 

  • Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J (2015) The deuterostome context of chordate origins. Nature 520:456–465

    Article  CAS  PubMed  Google Scholar 

  • McCauley DW, Bronner-Fraser M (2003) Neural crest contributions to the lamprey head. Development 130(11):2317–2327

    Article  CAS  PubMed  Google Scholar 

  • McDonald DG, Cavdek V, Calvert L, Milligan CL (1991) Acid-base regulation in the Atlantic hagfish Myxine glutinosa. J Exp Biol 161(1):201–215

    Article  Google Scholar 

  • Milsom WK, Kinkead R, Hedrick MS, Gilmour K, Perry S, Gargaglioni L, Wang T (2022) Evolution of vertebrate respiratory central rhythm generators. Resp Physiol Neurobiol 295:103781

    Article  CAS  Google Scholar 

  • Mongera A, Singh AP, Levesque MP, Chen Y-Y, Konstantinidis P, Nusslein- Volhard C (2013) Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140:916–925

    Article  CAS  PubMed  Google Scholar 

  • Montoro DT, Haber AL, Biton M, Vinarsky V, Lin B, Birket SE, Yuan F, Chen S, Leung HM, Villoria J et al (2018) A revised airway epithelial hierarchy includes CFTR-expressing ionocytes. Nature 560:319–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris SC, Caron J-B (2012) Pikaia gracilens Walcott, a stem-group chordate from the Middle Cambrian of British Columbia. Biol Rev 87:480–512

    Article  PubMed  Google Scholar 

  • Morris SC, Caron J-B (2014) A primitive fish from the Cambrian of North America. Nature 512:419–422

    Article  CAS  PubMed  Google Scholar 

  • Nanglu K, Caron J-B, Cameron CB (2015) Using experimental decay of modern forms to reconstruct the early evolution and morphology of fossil enteropneusts. Paleobiology 41:460–478

    Article  Google Scholar 

  • Nanglu K, Caron J-B, Cameron CB (2020) Cambrian tentaculate worms and the origin of the hemichordate body plan. Curr Biol 30(21):4238–4244

    Article  CAS  PubMed  Google Scholar 

  • Newstead JD (1967) Fine structure of the respiratory lamellae of teleostean gills. Z Für Zellforsch Mikrosk Anat 79:396–428

    Article  CAS  Google Scholar 

  • Newth DR (1951) Experiments on the neural crest of the lamprey embryo. J Exp Biol 28:247–260

    Article  Google Scholar 

  • Newth DR (1956) On the neural crest of lamprey embryos. J Embryol Exp Morph 4:358–375

    Google Scholar 

  • Nonnotte G (1981) Cutaneous respiration in six freshwater teleosts. Comp Biochem Physiol A 70(4):541–543

    Article  Google Scholar 

  • Nonnotte G, Kirsch R (1978) Cutaneous respiration in seven sea-water teleosts. Resp Physiol 35(2):111–118

    Article  CAS  Google Scholar 

  • Northcutt GR (2005) The new head hypothesis revisited. J Exp Zoolog B Mol Dev Evol 304B:274–297

    Article  Google Scholar 

  • Pan W, Godoy RS, Cook DP, Scott AL, Nurse CA, Jonz MG (2022) Single-cell transcriptomic analysis of neuroepithelial cells and other cell types of the gills of zebrafish (Danio rerio) exposed to hypoxia. Sci Rep 12(1):10144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quigley IK, Stubbs JL, Kintner C (2011) Specification of ion transport cells in the Xenopus larval skin. Development 138:705–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinton PM (2008) Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis. The Lancet 372:415–417

    Article  CAS  Google Scholar 

  • Quinton PM (2010) Role of epithelial HCO3- transport in mucin secretion: lessons from cystic fibrosis. Am J Physiol Cell Physiol 299(6):C1222–C1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randall DJ (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100(1):275–288

    Article  Google Scholar 

  • Reis-Santos P, McCormick SD, Wilson JM (2008) Ionoregulatory changes during metamorphosis and salinity exposure of juvenile sea lamprey (Petromyzon marinus L.). J Exp Biol 211(6):978–988

    Article  CAS  PubMed  Google Scholar 

  • Rombough PJ, Ure D (1991) Partitioning of oxygen uptake between cutaneous and branchial surfaces in larval and juvenile Chinook salmon Oncorhynchus tshawytscha. Physiol Zool 64:717–727

    Article  Google Scholar 

  • Sackville MA, Cameron CB, Gillis JA, Brauner CJ (2022) Ion regulation at gills precedes gas exchange and the origin of vertebrates. Nature 610(7933):699–703

    Article  CAS  PubMed  Google Scholar 

  • Sackville MA, Cameron CB, Brauner CJ (2023) Gills are not used for gas exchange in the suspension-feeding hemichordate Protoglossus graveolens. BioRxiv 2023:553704

    Google Scholar 

  • Saunders RL (1962) The irrigation of the gills in fishes: II. Efficiency of oxygen uptake in relation to respiratory flow activity and concentrations of oxygen and carbon dioxide. Can J Zool 40:817–862

    Article  CAS  Google Scholar 

  • Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120:483–494

    Article  CAS  PubMed  Google Scholar 

  • Schmitz A, Gemmel M, Perry SF (2000) Morphometric partitioning of respiratory surfaces in amphioxus (Branchiostoma lanceolatum Pallas). J Exp Biol 203:3381

    Article  CAS  PubMed  Google Scholar 

  • Schultze H-P (2009) Interpretation of marine and freshwater paleoenvironments in Permo- Carboniferous deposits. Palaeogeogr Palaeoclimatol 281:126–136

    Article  Google Scholar 

  • Shaughnessy CA, McCormick SD (2020) Functional characterization and osmoregulatory role of the Na+-K+-2Cl− cotransporter in the gill of sea lamprey (Petromyzon marinus), a basal vertebrate. Am J Physiol Reg Int Comp Physiol 318(1):R17–R29

    Article  CAS  Google Scholar 

  • Shu D-G, Luo H-L, Conway Morris S, Zhang X-L, Hu S-X, Chen L, Han J, Zhu M, Li Y, Chen L-Z (1999) Lower Cambrian vertebrates from south China. Nature 402:42–46

    Article  CAS  Google Scholar 

  • Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F et al (2015) Hemichordate genomes and deuterostome origins. Nature 527:459–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith AB (2008) Deuterostomes in a twist: the origins of a radical new body plan. Evol Dev 10:493–503

    Article  PubMed  Google Scholar 

  • Steffensen JF, Lomholt JP, Johansen K (1981) The relative importance of skin oxygen uptake in the naturally buried plaice, Pleuronectes platessa, exposed to graded hypoxia. Respir Physiol 44(3):269–275

    Article  CAS  PubMed  Google Scholar 

  • Steffensen JF, Johansen K, Sindberg CD, Sørensen JH, Møller JL (1984) Ventilation and oxygen consumption in the hagfish, Myxine glutinosa L. J Exp Mar Biol Ecol 84(2):173–178

    Article  Google Scholar 

  • Stenslokken KO, Sundin L, Nilsson GE (1999) Cardiovascular and gill microcirculatory effects of endothelin-1 in Atlantic cod: evidence for pillar cell contraction. J Exp Biol 202:1151

    Article  CAS  PubMed  Google Scholar 

  • Stockard CR (1906) The development of the mouth and gills in Bdellostoma stouti. Am J Anat 5:481–517

    Article  Google Scholar 

  • Stumpp M, Hu MY (2017) pH regulation and excretion in echinoderms. In: Weihrauch D, O’Donnell M (eds) Acid-base balance and nitrogen excretion in invertebrates. Springer, Berlin, pp 261–273

    Chapter  Google Scholar 

  • Stumpp M, Trübenbach K, Brennecke D, Hu MY, Melzner F (2012) Resource allocation and extracellular acid–base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat Toxicol 110(111):194–207

    Article  PubMed  Google Scholar 

  • Sumrall CD, Wray GA (2007) Ontogeny in the fossil record: diversification of body plans and the evolution of “aberrant” symmetry in Paleozoic echinoderms. Paleobiology 33:149–163

    Article  Google Scholar 

  • Sundin L, Nilsson GE (1998) Endothelin redistributes blood flow through the lamellae of rainbow trout gills. J Comp Physiol B 168:619–623

    Article  CAS  Google Scholar 

  • Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc B Biol Sci 363:1557–1568

    Article  Google Scholar 

  • Tang W, Martik ML, Li Y, Bronner ME (2019) Cardiac neural crest contributes to cardiomyocytes in amniotes and heart regeneration in zebrafish. Elife 8:e47929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toulmond A, Dejours P, Truchot JP (1982) Cutaneous O2 and CO2 exchanges in the dogfish, Scyliorhinus canicula. Respir Physiol 48(2):169–181

    Article  CAS  PubMed  Google Scholar 

  • Tresguerres M, Katoh F, Fenton H, Jasinska E, Goss GG (2005) Regulation of branchial V-H+-ATPase, Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J Exp Biol 208:345–354

    Article  CAS  PubMed  Google Scholar 

  • Tresguerres M, Parks SK, Goss GG (2006) V-H+-ATPase, Na+/K+-ATPase and NHE2 immunoreactivity in the gill epithelium of the Pacific hagfish (Epatretus stoutii). Comp Biochem Physiol A 145:312–321

    Article  Google Scholar 

  • van der Meer DLM, van den Thillart E, Witte F, de Bakker M, Besser J, Richardson MK, Spaink HP, Leito J, Bagowski CP (2005) Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am J Regul Integr Comp Physiol 289:R1512–R1519

    Article  Google Scholar 

  • Vo M, Mehrabian S, Étienne S, Pelletier D, Cameron CB (2019) The hemichordate pharynx and gill pores impose functional constraints at small and large body sizes. Biol J Linn Soc 127:75–87

    Article  Google Scholar 

  • Warga RM, Nüsslein-Volhard C (1999) Origin and development of the zebrafish endoderm. Development 126:827–838

    Article  CAS  PubMed  Google Scholar 

  • Wegner NC (2015) Elasmobranch gill structure. In: Shadwick R, Brauner CJ, Farrell AP (eds) Physiology of elasmobranch fishes, fish physiology, vol 34A. Academic Press, Hoboken, pp 101–151

    Google Scholar 

  • Wells P, Pinder A (1996a) The respiratory development of Atlantic salmon. I. Morphometry of gills, yolk sac and body surface. J Exp Biol 199:2725

    Article  CAS  PubMed  Google Scholar 

  • Wells P, Pinder A (1996b) The respiratory development of Atlantic salmon. II. Partitioning of oxygen uptake among gills, yolk sac and body surfaces. J Exp Biol 199:2737

    Article  CAS  PubMed  Google Scholar 

  • Wilson JM, Laurent P (2002) Fish gill morphology: inside out. J Exp Zool 293(3):192–213

    Article  PubMed  Google Scholar 

  • Wright PA, Wood CM (2012) Seven things fish know about ammonia and we don’t. Resp Physiol Neurobi 184(3):231–240

    Article  CAS  Google Scholar 

  • Xian-guang H, Aldridge RJ, Siveter DJ, Siveter DJ, Xiang-hong F (2002) New evidence on the anatomy and phylogeny of the earliest vertebrates. Proc R Soc Lond B Biol Sci 269:1865–1869

    Article  Google Scholar 

Download references

Acknowledgements

We thank B. Pelster and S.F. Perry for their kind invitation to contribute to this special issue on fish gill physiology. J.A. Gillis was supported by MBL institutional funds.

Author information

Authors and Affiliations

  1. Bay Paul Centre, Marine Biological Laboratory, Woods Hole, MA, USA

    Michael A. Sackville & J. Andrew Gillis

  2. Department of Zoology, University of British Columbia, Vancouver, BC, Canada

    Colin J. Brauner

Authors
  1. Michael A. Sackville
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Andrew Gillis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Colin J. Brauner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael A. Sackville.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Communicated by Bernd Pelster.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sackville, M.A., Gillis, J.A. & Brauner, C.J. The origins of gas exchange and ion regulation in fish gills: evidence from structure and function. J Comp Physiol B (2024). https://doi.org/10.1007/s00360-024-01545-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00360-024-01545-5

Keywords

Search

Navigation