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Post-prandial physiology and intestinal morphology of the Pacific hagfish (Eptatretus stoutii)

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Abstract

Hagfishes are unique to the vertebrate lineage in that they acquire dissolved nutrients across multiple epithelia including the intestine, gill, and skin. This feat has been attributed to their immersive feeding behavior that likely simultaneously provides benefits (nutrient rich) and potentially adverse (hypercapnia, hypoxia, high environmental ammonia) physiological effects. Examinations have been conducted of the ex vivo transport capabilities of specific nutrients as well as in vivo effects of the hypothesized feeding environments, yet the physiological effects of feeding itself have never been elucidated. We examined the post-prandial physiology of Pacific hagfish (Eptatretus stoutii), identifying changes in oxygen consumption, acid–base balance, ammonia waste excretion, and intestinal morphology following feeding in captivity. Following voluntary feeding, post-prandial oxygen consumption was significantly elevated (1868 ± 272 µmol kg−1 h−1) 8 h following feeding when compared to control resting metabolic oxygen consumption (642 ± 51 µmol kg−1 h−1) and resulted in a factorial metabolic scope of 2.92. Changes in acid–base status were not observed following feeding in either the excreted components or the caudal blood samples; however, a significant alkalosis was observed 8 h post-feeding in the major intestinal blood vein. Significant increases (16-fold) in ammonia excretion were recorded in 36 h post-fed hagfish. Finally, significant post-prandial increases in intestinal mucosal thickness and microvilli length were observed, with mucosal thickness remaining significantly increased throughout 36 h and the microvilli length returning to fasted lengths by 36 h. These results demonstrate the post-feeding physiology of the earliest diverging extant craniate and identify correlations between physiology and hindgut morphology 8 h following feeding.

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References

  • Adam H (1963) Structure and histochemistry of the alimentary canal. In: Brodal A, Fänge R (eds) The biology of myxine. Universitetsforlaget, Oslo, pp 256–288

    Google Scholar 

  • Baker DW, Sardella B, Rummer JL, Sackville M, Brauner CJ (2015) Hagfish: Champions of CO2 tolerance question the origins of vertebrate gill function. Sci Rep 5:11182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardack D (1998) Relationships of living and fossil hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The Biology of hagfishes. Chapman & Hall Ltd, London, pp 3–14

    Chapter  Google Scholar 

  • Bellamy D, Jones IC (1961) Studies on Myxine glutinosa—I. The chemical composition of the tissues. Comp Biochem Physiol 3:175–183

    Article  CAS  PubMed  Google Scholar 

  • Boutilier RG, Heming TA, and Iwama GK (1984) Appendix: physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall D (eds) Gills: anatomy, gas transfer, and acid–base regulation. Elsevier, Orlanda, pp 403–430

    Chapter  Google Scholar 

  • Bucking C (2016) A broader look at ammonia production, excretion, and transport in fish: a review of impacts of feeding and the environment. J Comp Physiol B 187:1–18

    Google Scholar 

  • Bucking C, Wood CM (2008) The alkaline tide and ammonia excretion after voluntary feeding in freshwater rainbow trout. J Exp Biol 211:2533–2541

    Article  CAS  PubMed  Google Scholar 

  • Bucking C, Fitzpatrick JL, Nadella SR, Wood CM (2009) Post-prandial metabolic alkalosis in the seawater-acclimated trout: the alkaline tide comes. J Exp Biol 212:2159–2166

    Article  CAS  PubMed  Google Scholar 

  • Bucking C, Glover CN, Wood CM (2011) Digestion under duress: nutrient acquisition and metabolism during hypoxia in the Pacific hagfish. PBZ 84(6):607–617

    CAS  PubMed  Google Scholar 

  • Christel CM, DeNardo DF, Secor SM (2007) Metabolic and digestive response to food ingestion in a binge-feeding lizard, the Gila monster (Heloderma suspectum). J Exp Biol 210:3430–3439

    Article  CAS  PubMed  Google Scholar 

  • Clifford AM, Guffey SC, Goss GG (2014) Extrabranchial mechanisms of systemic pH recovery in hagfish (Eptatretus stoutii). Comp Biochem Phys A 168:82–89

    Article  CAS  Google Scholar 

  • Clifford AM, Goss GG, Roa JN, Tresguerres M (2015a) Acid/base and ionic regulation in hagfish. In: Edwards SL, Goss GG (eds) Hagfish biology. CRC Press, Boca Raton, pp 277–297

    Chapter  Google Scholar 

  • Clifford AM, Goss GG, Wilkie MP (2015b) Adaptations of a deep sea scavenger: high ammonia tolerance and active NH4(+) excretion by the Pacific hagfish (Eptatretus stoutii). Comp Biochem Phys A 182C:64–74

    Article  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 219:2814–2818

    Article  PubMed  Google Scholar 

  • Clifford AM, Bury NR, Schultz AG, Ede JD, Goss BL, and Goss GG (2017a) Regulation of plasma glucose and sulfate excretion in Pacific hagfish, Eptatretus stoutii is not mediated by 11-deoxycortisol. GCE 247:107–115

    CAS  Google Scholar 

  • Clifford AM, Weinrauch AM, Edwards SL, Wilkie MP, Goss GG (2017b) Flexible ammonia handling strategies using both cutaneous and branchial epithelia in the highly ammonia tolerant Pacific hagfish. Am J Phys Reg Int Comp Phys. doi:10.1152/ajpregu.00351.2016

    Google Scholar 

  • Cooper CA, Wilson RA (2008) Post-prandial alkaline tide in freshwater rainbow trout: effects of meal anticipation on recovery from acid–base and ion regulatory disturbances. J Exp Biol 211:2542–2550

    Article  CAS  PubMed  Google Scholar 

  • Coulson RA, Hernandez T (1983) Alligator metabolism studies on chemical reactions in vivo. Comp Biochem Physiol B 74(1):1–182

    Article  CAS  PubMed  Google Scholar 

  • Coulson RA, Hernandez T, Dessauer HC (1950) Alkaline tide of the alligator. Proc Soc Exp Biol Med 74(4):866–869

    Article  CAS  PubMed  Google Scholar 

  • Currie S, Edwards SL (2010) The curious case of the chemical composition of hagfish tissues—50 years on. Comp Biochem Phys A 157(2):111–115

    Article  Google Scholar 

  • Day RD, Tibbetts IR, Secor SM (2014) Physiological responses to short-term fasting among herbivorous, omnivorous, and carnivorous fishes. J Comp Physiol B 184(4):497–512

    Article  PubMed  Google Scholar 

  • Drazen JC, Yeh J, Friedman J, Condon N (2011) Metabolism and enzyme activities of hagfish from shallow and deep water of the Pacific Ocean. Comp Biochem Phys A 159(2):182–187

    Article  Google Scholar 

  • Emdin SO (1982) Effects of hagfish insulin in the Atlantic hagfish, Myxine glutinosa the in vivo metabolism of [14C] glucose and [14C] leucine and studies on starvation and glucose loading. Gen Comp Endocrinol 47(4):414–425

    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 113:465–469

    CAS  PubMed  Google Scholar 

  • Evans DH, Harrie AC (2001) Vasoactivity of the ventral aorta of the American eel (Anguilla anguilla), Atlantic hagfish (Myxine glutinosa), and sea lamprey (Petromyzon marinus). J Exp Zool 289:273–284

    Article  CAS  PubMed  Google Scholar 

  • Ferry-Graham LA, Gibb AC (2009) Comparison of fasting and postfeeding metabolic rates in a sedentary shark, Cephaloscyllium ventriosum. Copeia 2001:1108–1113

    Article  Google Scholar 

  • Forster ME (1990) Confirmation of the low metabolic rate of hagfish. Comp Biochem Phys Part A 96:113–116

    Article  Google Scholar 

  • Forster ME, Russell MJ, Hambleton DC, Olson DR (2001) Blood and extracellular fluid volume in whole body and tissues of the Pacific hagfish (Eptatretus stoutii). PBZ 74(5):750–756

    CAS  PubMed  Google Scholar 

  • Foster GD, Moon TW (1986) Enzyme activities in the Atlantic hagfish Myxine glutinosa: changes with captivity and food deprivation. Can J Zool 64(5):1080–1085

    Article  CAS  Google Scholar 

  • Gillis TE, Regan MD, Cox GK, Harter TS, Brauner CJ, Richards JG, Farrell AP (2015) Characterizing the metabolic capacity of the anoxic hagfish heart. J Exp Biol 218(23):3754–3761

    Article  PubMed  Google Scholar 

  • Glass NR (1968) Effect of time of food deprivation on routine oxygen consumption of largemouth black bass (Micropterus Salmoides). Ecology 49:340–343

    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 

  • Hersey SJ, Sachs G (1995) Gastric-acid secretion. Physiol Rev 75:155–189

    Article  CAS  PubMed  Google Scholar 

  • Johansen K (1963) The cardiovascular system of Myxine glutinosa L. In: Brodal A, Fänge R (eds) The biology of Myxine. Universitetsforlaget, Oslo, pp 289–316

    Google Scholar 

  • Johnston IA, Battram J (1993) Feeding energetics and metabolism in demersal fish species from Antarctic, temperate and tropical environments. Mar Biol 115:7–14

    Article  Google Scholar 

  • Jordan AD, Steffensen JF (2007) Effects of ration size and hypoxia on specific dynamic action in the cod. PBZ 80:178–185

    PubMed  Google Scholar 

  • Kutty MN (1978) Ammonia quotient in sockeye salmon (Oncornhynchus nerka). J Fish Res Board Can 35:1003–1005

    Article  CAS  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 208:215–225

    Article  Google Scholar 

  • Li J, Das S, Herrin BR, Hirano M, Cooper MD (2013) Definition of a third VLR gene in hagfish. PNAS 110(37):15013–15018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lignot JH, Helmstetter C, Secor SM (2005) Postprandial morphological response of the intestinal epithelium of the Burmese python (Python molurus). Comp Biochem Phys A 141:280–291

    Article  Google Scholar 

  • Martini FH (1998) The ecology of hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman & Hall Ltd, London, pp 57–78

    Chapter  Google Scholar 

  • McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Phys A 144:381–394

    Article  CAS  Google Scholar 

  • Miyashita T, Diogo R (2016) Evolution of serial patterns in the vertebrate pharyngeal apparatus and paired appendages via assimilation of dissimilar units. Front Ecol E 223(4):1–25

    Google Scholar 

  • Munz FW, Morris RW (1965) Metabolic rate of the hagfish, Eptatretus Stoutii (Lockington) 1878. Comp Biochem Phys 16:1–6

    Article  CAS  Google Scholar 

  • Niv Y, Fraser GM (2002) The alkaline tide phenomenon. J Clin Gastroenterol 35:5

    Article  CAS  PubMed  Google Scholar 

  • Oisi Y, Fujimoto S, Kinya GO, Kuratani S (2015) On the peculiar morphology of the hypoglossal, glossopharyngeal and vagus nerves and hypobranchial muscles in the hagfish. Zool Lett 1(1):1–6

    Article  Google Scholar 

  • Ott BD, Secor SM (2007) Adaptive regulation of digestive performance in the genus Python. J Exp Biol 210:340–356

    Article  PubMed  Google Scholar 

  • Pancer Z, Saha NR, Kasamatsu J, Suzuki T, Amemiya CT, Kasahara M, Cooper MD (2005) Variable lymphocyte receptors in hagfish. PNAS 102(26):9224–9229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parks SK, Tresguerres M, Goss GG (2007) Blood and gill responses to HCl infusions in the Pacific hagfish (Eptatretus stoutii). Can J Zool 85:855–862

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson JD (1954) The chemical composition of the blood of some aquatic chordates, including members of the Tunicata, Cyclostomata and Osteichthyes. J Exp Biol 31:424–442

    CAS  Google Scholar 

  • Robertson RF, Meagor J, Taylor EW (2002) Specific dynamic action in the shore crab, Carcinus maenas (L.), in relation to acclimation temperature and to the onset of the emersion response. PBZ 75:350–359

    CAS  PubMed  Google Scholar 

  • Schultz AG, Guffey SC, Clifford AM, Goss GG (2014) Phosphate absorption across multiple epithelia in the Pacific hagfish (Eptatretus stoutii). Am J Physiol Reg 307(6):R643–R652

    CAS  Google Scholar 

  • Secor SM (2005) Physiological responses to feeding, fasting and estivation for anurans. J Exp Biol 208:2595–2608

    Article  PubMed  Google Scholar 

  • Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56

    Article  PubMed  Google Scholar 

  • Secor SM, Diamond J (1995) Adaptive responses to feeding in Burmese pythons: pay before pumping. J Exp Biol 198:1313–1325

    CAS  PubMed  Google Scholar 

  • Secor SM, Lignot J (2010) Morphological plasticity of vertebrate vestivation. In: Navas CA, Carvalho JE (eds) Aestivation: molecular and physiological aspects. Springer, Heidelberg, pp 183–208

    Chapter  Google Scholar 

  • Secor SM, Taylor JR, Grosell M (2012) Selected regulation of gastrointestinal acid–base secretion and tissue metabolism for the diamondback water snake and Burmese python. J Exp Biol 215(1):185–196

    Article  CAS  PubMed  Google Scholar 

  • Sidell BD, Stowe DB, Hansen CA (1984) Carbohydrate is the preferred metabolic fuel of the Hagfish (Myxine glutinosa) heart. Physiol zool 57(2):266–273

    Article  CAS  Google Scholar 

  • Sims DW, Davies SJ (1994) Does specific dynamic action (SDA) regulate return of appetite in the lesser spotted dogfish, Scyliorhinus caniculcla. J Fish Biol 45:341–348

    Google Scholar 

  • Smith HW (1935) The metabolism of the lung-fish II. Effect of feeding meat on metabolic rate. J Cell Comp Physiol 6:335–349

    Article  CAS  Google Scholar 

  • Smolka AJ, Lacy ER, Luciano L, Reale E (1994) Identification of gastric H, K-ATPase in an early vertebrate, the Atlantic stingray Dasyatis sabina. J Histochem Cytochem 42:1323–1332

    Article  CAS  PubMed  Google Scholar 

  • Somanath B, Palavesam A, Lazarus S, Ayyappan M (2000) Influence of nutrient source on specific dynamic action of Pearl spot, Etroplus suratensis (Bloch). ICLARM Q 32(2):15–17

    Google Scholar 

  • Taylor JR, Grosell M (2006) Feeding and osmoregulation: dual function of the marine teleost intestine. J Exp Biol 209:2939–2951

    Article  CAS  PubMed  Google Scholar 

  • Taylor JR, Grosell M (2009) The intestinal response to feeding in seawater gulf toadfish, Opsanus beta, includes elevated base secretion and increased epithelial oxygen consumption. J Exp Biol 212:3873–3881

    Article  CAS  PubMed  Google Scholar 

  • Taylor JR, Whittamore JM, Wilson RW, Grosell M (2007) Postprandial acid–base balance and ion regulation in freshwater and seawater-acclimated European flounder, Platichthys flesus. J Comp Physiol B 177:597–608

    Article  CAS  PubMed  Google Scholar 

  • Thwaites DT, Ford D, Glanville M, Simmons NL (1999) H+/solute-induced intracellular acidification leads to selective activation of apical Na+/H+ exchange in human intestinal epithelial cells. J Clin Invest 104(5):629–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tresguerres M, Parks SK, Goss GG (2007a) Recovery from blood alkalosis in the Pacific hagfish (Eptatretus stoutii): involvement of gill V-H+-ATPase and Na+/K+-ATPase. Comp Biochem Phys A 148:133–141

    Article  Google Scholar 

  • Tresguerres M, Parks SK, Wood CM, Goss GG (2007b) V-H+-ATPase translocation during blood alkalosis in dogfish gills: interaction with carbonic anhydrase and involvement in the postfeeding alkaline tide. Am J Physiol Reg I(292):R2012–R2019

    Google Scholar 

  • Turner JR, Black ED (2001) NHE3-dependent cytoplasmic alkalinization is triggered by Na+-glucose cotransport in intestinal epithelia. Am J Physiol Cell Physiol 281(5):C1533–C1541

    Article  CAS  PubMed  Google Scholar 

  • Verdouw H, Van Echteld CJA, Dekkers EMJ (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12:399–402

    Article  CAS  Google Scholar 

  • Wang T, Busk M, Overgaard J (2001) The respiratory consequences of feeding in amphibians and reptiles. Comp Biochem Phys A 128:533–547

    Article  Google Scholar 

  • Weinrauch A, Edwards SL, Goss GG (2015) Anatomy of the Pacific hagfish (Eptatretus stoutii). In: Edwards SL, Goss GG (eds) Hagfish biology. CRC Press, pp 1–40

  • Wilkie MP, Clifford AM, Edwards SL, Goss GG (2017) Wide scope for nitrogen catabolism and urea-N excretion in the foraging Pacific hagfish. J Mar Biol 164:126

    Article  Google Scholar 

  • Wood CM (2001) Influence of feeding, exercise, and temperature on nitrogen metabolism and excretion. In: Wright PA, Anderson P (eds) Nitrogen excretion, fish physiology. Academic Press, San Diego, pp 201–238

    Chapter  Google Scholar 

  • Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2005) Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthias). J Exp Biol 208:2693–2705

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Bucking C, Fitzpatrick J, Nadella S (2007) The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respir Physiol Neurobiol 159:163–170

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Bucking C, Grosell M (2010) Acid–base responses to feeding and intestinal Cl uptake in freshwater- and seawater-acclimated killifish, Fundulus heteroclitus, an agastric euryhaline teleost. J Exp Biol 213(15):2681–2692

    Article  CAS  PubMed  Google Scholar 

  • Zintzen V, Roberts CD, Anderson MJ, Steward AL, Struthers CD, Harvey ES (2011) Hagfish predatory behavior and slime defence mechanism. Sci Rep 1:31. doi:10.1038/srep00131

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Arlene Oatway of the University of Alberta Microscopy Sciences Department and the staff at Bamfield Marine Sciences Centre, with particular thanks to the research coordinator Dr. Eric Clelland and Janice Pierce for hagfish collection. Many thanks to anonymous reviewers for helpful comments. AMW was supported by a NSERC-PGSD, The Presidents Doctoral Prize of Distinction, Queen Elizabeth II Scholarship, Sigurd Tviet Memorial Scholarship, Dick and Leona Peter BMSC Residential bursary and the John Boom Scholarship. AMC is supported by an NSERC-PGSD, Alberta Innovates Technology Futures—Omics Scholarship, The President’s Doctoral Prize of Distinction, Donald M. Ross Memorial Scholarship, R. E. (Dick) Peter Memorial Scholarship, Andrew Stewart Memorial Prize, Western Canadian Universities Marine Sciences Society Graduate Student Award and the Dick and Leona Peter BMSC residential bursary. This research was supported by an NSERC Discovery Grant (203736) to GGG.

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Communicated by I. D. Hume.

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Weinrauch, A.M., Clifford, A.M. & Goss, G.G. Post-prandial physiology and intestinal morphology of the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 188, 101–112 (2018). https://doi.org/10.1007/s00360-017-1118-1

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