Skip to main content
Log in

Evidence of endoplasmic reticulum stress and liver inflammation in the American mink Neovison vison with benign hepatic steatosis

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

Abstract

We investigated the presence of inflammatory signs in the progression of fatty liver disease induced by fasting. Sixty standard black American mink (Neovison vison) were fasted for 0, 1, 3, 5, or 7 days and one group for 7 days followed by re-feeding for 28 days. Liver sections were evaluated histologically and liver mRNA levels indicating endoplasmic reticulum (ER) stress, adipogenic transformation, and inflammation were assessed by quantitative real-time PCR. After 3 days of fasting, the mink had developed moderate liver steatosis. Increased hyaluronan reactivity in lymphocytic foci but no Mallory–Denk bodies were seen in livers of the mink fasted for 5–7 days. Up-regulation of glucose-regulated protein, 78 kDa was observed on day 7 indicating ER stress, especially in the females. Liver lipoprotein lipase and monocyte chemoattractant protein 1 mRNA levels increased in response to 5–7 days of food deprivation, while tumor necrosis factor α (TNF-α) was the highest in the mink fasted for 5 days. The expression of the genes of interest, except for TNF-α, correlated with each other and with the liver fat content. The mRNA levels were found to change more rapidly below n-3/n-6 polyunsaturated fatty acid ratio threshold of 0.15. Following re-feeding, hepatocyte morphology and mRNA abundance returned to pre-fasting levels. Within the studied timeframe, evidence for ER stress, adipogenic transformation, and liver inflammation suggested incipient transition from steatosis to steatohepatitis with potential for development of more severe liver disease. This may present a possibility to influence disease progression before histologically observable steatohepatitis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ER:

Endoplasmic reticulum

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

GRP78:

Glucose-regulated protein, 78 kDa

HA:

Hyaluronan

LPL:

Lipoprotein lipase

MCP-1:

Monocyte chemoattractant protein 1

MDB:

Mallory–Denk body

MUFA:

Monounsaturated fatty acid

NAFLD:

Non-alcoholic fatty liver disease

NAI:

Non-alcoholic steatohepatitis activity index

NASH:

Non-alcoholic steatohepatitis

NEFA:

Non-esterified fatty acid

PUFA:

Polyunsaturated fatty acid

qPCR:

Quantitative real-time polymerase chain reaction

TAG:

Triacylglycerols

TNF-α:

Tumor necrosis factor α

References

  • Anderson RA (1998) Chromium, glucose intolerance and diabetes. J Am Coll Nutr 17:548–555

    Article  PubMed  CAS  Google Scholar 

  • Anstee QM, Targher G, Day CP (2013) Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 10:330–344

    Article  PubMed  CAS  Google Scholar 

  • Antuna-Puente B, Feve B, Fellahi S et al (2008) Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab 34:2–11

    Article  PubMed  CAS  Google Scholar 

  • Armstrong J, Blanchard G (2009) Hepatic lipidosis in cats. Vet Clin North Am Small Anim Pract 39:599–616

    Article  PubMed  Google Scholar 

  • Bates DM, Watts DG (2007) Nonlinear regression and its applications. Wiley, New York

    Google Scholar 

  • Bertola A, Bonnafous S, Anty R et al (2010) Hepatic expression patterns of inflammatory and immune response genes associated with obesity and NASH in morbidly obese patients. PLoS ONE 5:e13577

    Article  PubMed  PubMed Central  Google Scholar 

  • Bjornvad C, Elnif J, Sangild P (2004) Short-term fasting induces intrahepatic lipid accumulation and decreases intestinal mass without reduced brush-border enzyme activity in mink (Mustela vison) small intestine. J Comp Physiol B 174:625–632

    Article  PubMed  CAS  Google Scholar 

  • Boudreau L, Benkel B, Astatkie T et al (2014) Ideal body condition improves reproductive performance and influences genetic health in female mink. Anim Reprod Sci 145:86–98

    Article  PubMed  Google Scholar 

  • Brunt E, Janney C, Di Bisceglie A et al (1999) Non-alcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 94:2467–2474

    Article  PubMed  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA et al (2009) The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  PubMed  CAS  Google Scholar 

  • Canadian Council on Animal Care (CCAC) (1993) In: Olfert ED, Cross BM, McWilliam AA (eds) Guide to the care and use of experimental animals, vol 1. CCAC, Ottawa

  • Cayón A, Crespo J, Guerra AR et al (2008) Gene expression in obese patients with non-alcoholic steatohepatitis. Rev Esp Enferm Dig 100:212–218

    Article  PubMed  Google Scholar 

  • Chalasani N, Wilson L, Kleiner DE et al (2008) Relationship of steatosis grade and zonal location to histological features of steatohepatitis in adult patients with non-alcoholic fatty liver disease. J Hepatol 48:829–834

    Article  PubMed  PubMed Central  Google Scholar 

  • Clausen TN, Olesen CR, Hansen O et al (1992) Nursing sickness in lactating mink (Mustela vison) I. Epidemiological and pathological observations. Can J Vet Res 56:89–94

    PubMed  CAS  PubMed Central  Google Scholar 

  • Crespo J, Cayón A, Fernández-Gil P et al (2001) Gene expression of tumor necrosis factor α and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology 34:1158–1163

    Article  PubMed  CAS  Google Scholar 

  • Day CP (2002) Pathogenesis of steatohepatitis. Best Pract Res Clin Gastroenterol 16:663–678

    Article  PubMed  CAS  Google Scholar 

  • Dick MF, Hurford J, Lei S et al (2014) High feeding intensity increases the severity of fatty liver in the American mink (Neovison vison) with potential ameliorating role for long-chain n-3 polyunsaturated fatty acids. Acta Vet Scand 56:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Dimski D, Taboada J (1995) Feline idiopathic hepatic lipidosis. Vet Clin North Am Small Anim Pract 25:357–373

    PubMed  CAS  Google Scholar 

  • Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nature Rev Immunol 11:98–107

    Article  CAS  Google Scholar 

  • Dowman JK, Tomlinson JW, Newsome PN (2010) Pathogenesis of non-alcoholic fatty liver disease. Q J Med 103:71–83

    Article  CAS  Google Scholar 

  • Dunstone N (1993) The mink. T & AD Poyser Ltd, London

    Google Scholar 

  • Eisert R (2011) Hypercarnivory and the brain: protein requirements of cat reconsidered. J Comp Physiol B 181:1–17

    Article  PubMed  CAS  Google Scholar 

  • El-Badry A, Grad R, Clavien P-A (2007) Omega 3–Omega 6: what is right for the liver? J Hepatol 47:718–725

    Article  PubMed  CAS  Google Scholar 

  • El Midaoui A, Wu R, de Champlain J (2002) Prevention of hypertension, hyperglycemia and vascular oxidative stress by aspirin treatment in chronically glucose-fed rats. J Hypertens 20:1407–1412

    Article  PubMed  Google Scholar 

  • Endo M, Masaki T, Seike M et al (2007) TNF-alpha induces hepatic steatosis in mice by enhancing gene expression of sterol regulatory element binding protein-1c (SREBP-1c). Exp Biol Med 232:614–621

    CAS  Google Scholar 

  • Farrell GC, Larter CZ (2006) Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43:S99–S112

    Article  PubMed  CAS  Google Scholar 

  • Gabay C (2006) Interleukin-6 and chronic inflammation. Arthritis Res Ther 8:S3

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerdin B, Hällgren R (1997) Dynamic role of hyaluronan (HYA) in connective tissue activation and inflammation. J Intern Med 242:49–55

    Article  PubMed  CAS  Google Scholar 

  • Greco D, Kotronen A, Westerbacka J et al (2008) Gene expression in human NAFLD. Am J Physiol Gastrointest Liver Physiol 294:G1281–G1287

    Article  PubMed  CAS  Google Scholar 

  • Guerra Ruiz A, Casafont F, Crespo J et al (2007) Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients: evidence for the potential role of endotoxin in the pathogenesis of non-alcoholic steatohepatitis. Obes Surg 17:1374–1380

    Article  Google Scholar 

  • Hanada S, Haralda M, Kumemura H et al (2007) Oxidative stress induces the endoplasmic reticulum stress and facilitates inclusion formation in cultured cells. J Hepatol 47:93–102

    Article  PubMed  CAS  Google Scholar 

  • Haukeland JW, Damås JK, Konopski Z et al (2006) Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J Hepatol 44:1167–1174

    Article  PubMed  CAS  Google Scholar 

  • Heinrich PC, Castell JV, Andus T (1990) Interleukin-6 and the acute phase response. Biochem J 265:621–636

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hodson L, Frayn KN (2011) Hepatic fatty acid partitioning. Curr Opin Lipidol 2:216–224

    Article  Google Scholar 

  • Hotamisligil GS, Arner P, Caro JF et al (1995) Increased adipose tissue expression of tumor necrosis factor-α in human obesity and insulin resistance. J Clin Invest 95:2409–2415

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hunter B, Barker IK (1996) Digestive system of mink. In: Hunter B, Lemieux N (eds) Mink… biology, health and disease. University of Guelph Graphic and Print Service, Guelph, pp 14:1–20

  • Hynes AMJ, Rouvinen-Watt K (2007a) Monitoring blood glucose levels in female mink during the reproductive cycle: 1. Prevention of hyperglycemia during the nursing period. Can J Vet Res 71:241–248

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hynes AMJ, Rouvinen-Watt K (2007b) Monitoring blood glucose levels in female mink during the reproductive cycle: 2. Effects of short-term fish oil, chromium picolinate, and acetylsalicylic acid supplementation during late lactation. Can J Vet Res 71:249–255

    PubMed  CAS  PubMed Central  Google Scholar 

  • Iredale J (2007) Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J Clin Invest 117:539–548

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jump DB (2011) Fatty acid regulation of hepatic lipid metabolism. Curr Opin Clin Nutr Metab Care 14:115–120

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim JK, Fillmore JJ, Chen Y et al (2001) Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance. Proc Natl Acad Sci 98:7522–7527

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kleiner D, Brunt E, Van Natta M et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321

    Article  PubMed  Google Scholar 

  • Kratky D, Zimmermann R, Wagner EM et al (2005) Endothelial lipase provides an alternative pathway for FFA uptake in lipoprotein lipase-deficient mouse adipose tissue. J Clin Invest 115:161–167

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lassén TM, Tauson A-H, Ahlstrøm Ø et al (2012) Energy and main nutrients in feed for mink and foxes, 2nd edn. In: Skrede A (ed) Nordic association of agricultural scientists, subsection for fur animals. Nutrition and Feeding Committee, Report No. 63

  • Lee A (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373–381

    Article  PubMed  CAS  Google Scholar 

  • Li L, Renier G (2007) Adipocyte-derived lipoprotein lipase induces macrophage activation and monocyte adhesion: role of fatty acids. Obesity 15:2595–2604

    Article  PubMed  CAS  Google Scholar 

  • Lindberg A, Nordstoga K, Christopherson B et al (1998) A mutation in the lipoprotein lipase gene associated with hyperlipoproteinemia type I in mink: studies on lipid and lipase levels in heterozygotes. Int J Mol Med 1:529–538

    PubMed  CAS  Google Scholar 

  • Luna L (1968) Manual of histologic staining methods of the Armed Forces Institute of Pathology, 3rd edn. Blakison Division, McGraw-Hill Book Co, New York

  • Malínská H, Oliyarnyk O, Hubová M et al (2010) Increased liver oxidative stress and altered PUFA metabolism precede development of non-alcoholic steatohepatitis in SREBP-1a transgenic spontaneously hypertensive rats with genetic predisposition to hepatic steatosis. Mol Cell Biochem 335:119–125

    Article  PubMed  Google Scholar 

  • Mantena S, King A, Andringa K et al (2008) Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol and obesity-induced fatty liver diseases. Free Radic Biol Med 44:1259–1272

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marceau P, Biron S, Hould FS et al (1999) Liver pathology and the metabolic syndrome X in severe obesity. J Clin Endocrinol Metab 84:1513–1517

    Article  PubMed  CAS  Google Scholar 

  • Marra F, DeFranco R, Grappone C et al (1998) Increased expression of monocyte chemotactic protein-1 during active hepatic fibrogenesis: correlation with monocyte infiltration. Am J Pathol 152:423–430

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80:753–769

    Article  PubMed  CAS  Google Scholar 

  • Merat S, Khadem-Sameni F, Nouraie M et al (2010) A modification of the Brunt system for scoring liver histology of patients with non-alcoholic fatty liver disease. Arch Iran Med 13:38–44

    PubMed  Google Scholar 

  • Mitchell J, Rouvinen-Watt K (2008) Body condition, liver fat and liver glycogen content of wild American mink (Neovison vison) in Nova Scotia, Canada. Scientifur 32:217–218

    Google Scholar 

  • Montgomery DC (2013) Design and analysis of experiments, 8th edn. Wiley, New York

    Google Scholar 

  • Mustonen A-M, Pyykönen T, Paakkonen T et al (2005) Adaptations to fasting in the American mink (Mustela vison): carbohydrate and lipid metabolism. Comp Biochem Physiol A 140:195–202

    Article  Google Scholar 

  • Mustonen A-M, Puukka M, Saarela S et al (2006) Adaptations to fasting in a terrestrial mustelid, the sable (Martes zibellina). Comp Biochem Physiol A 144:444–450

    Article  Google Scholar 

  • Mustonen A-M, Puukka M, Rouvinen-Watt K et al (2009) Response to fasting in an unnaturally obese carnivore, the captive European polecat Mustela putorius. Exp Biol Med 234:1287–1295

    Article  CAS  Google Scholar 

  • Mustonen A-M, Kärjä V, Kilpiö M et al (2013) Manifestations of fasting-induced fatty liver and rapid recovery from steatosis in voles fed lard or flaxseed oil lipids. Nutrients 5:4211–4230

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nguyen P, Leray V, Diez M et al (2008) Liver lipid metabolism. J Anim Physiol Anim Nutr 92:272–283

    Article  CAS  Google Scholar 

  • Nieminen P, Mustonen A-M, Kärjä V et al (2009) Fatty acid composition and development of hepatic lipidosis during food deprivation—mustelids as a potential animal model for liver steatosis. Exp Biol Med 234:278–286

    Article  CAS  Google Scholar 

  • Obstfeld AE, Sugaru E, Thearle M et al (2010) C-C chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis. Diabetes 59:916–925

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Oikari S, Jokela TA, Tammi RH et al (2012) Multiple roles of hyaluronan as a target and modifier of the inflammatory response. In: Karamanos NK (ed) Extracellular matrix: pathobiology and signaling. Walter de Gruyter, Berlin, pp 39–65

    Google Scholar 

  • Özcan U, Cao Q, Yilmaz E et al (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457–461

    Article  PubMed  Google Scholar 

  • Pardina E, Baena-Fustegueres JA, Llamas R et al (2009) Lipoprotein lipase expression in livers of morbidly obese patients could be responsible for liver steatosis. Obes Surg 19:608–616

    Article  PubMed  Google Scholar 

  • Park EJ, Lee JH, Yu G-Y et al (2010) Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 140:197–208

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Popa C, Netea MG, van Riel PLCM et al (2007) The role of TNF-α in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J Lipid Res 48:751–762

    Article  PubMed  CAS  Google Scholar 

  • Rouvinen-Watt K (2003) Nursing sickness in the mink—a metabolic mystery or a familiar foe? Can J Vet Res 67:161–168

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rouvinen-Watt K, White MB, Campbell R (2005) Mink feeds and feeding. Ontario Ministry of Agriculture and Food, Ottawa, Nova Scotia Agricultural College, Truro

  • Rouvinen-Watt K, Mustonen A-M, Conway R et al (2010) Rapid development of fasting-induced hepatic lipidosis in the American mink (Neovison vison): effects of food deprivation and re-alimentation on body fat depots, tissue fatty acid profiles, hematology and endocrinology. Lipids 45:111–128

    Article  PubMed  CAS  Google Scholar 

  • Rouvinen-Watt K, Harris L, Dick M et al (2012) Role of hepatic de novo lipogenesis in the development of fasting-induced fatty liver in the American mink (Neovison vison). Br J Nutr 108:1360–1370

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • SAS Institute Inc (2010) SAS/STAT® 9.3 User’s Guide. SAS Institute Inc, Cary. http://support.sas.com/documentation/cdl/en/statug/63962/HTML/default/viewer.htm#titlepage.htm

  • Sriburi R, Jackowski S, Mori K et al (2004) XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol 167:35–41

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stanton MC, Chen SC, Jackson JV et al (2011) Inflammatory signals shift from adipose to liver during high fat feeding and influence the development of steatohepatitis in mice. J Inflamm 8:8

    Article  CAS  Google Scholar 

  • Tammi R, Pasonen-Seppänen S, Kolehmainen E et al (2005) Hyaluronan synthase induction and hyaluronan accumulation in mouse epidermis following skin injury. J Invest Dermatol 124:898–905

    Article  PubMed  CAS  Google Scholar 

  • Tannapfel A, Denk H, Dienes H-P et al (2011) Histopathological diagnosis of non-alcoholic and alcoholic fatty liver disease. Virchows Arch 458:511–523

    Article  PubMed  CAS  Google Scholar 

  • Toshimitsu K, Matsuura B, Ohkubo I et al (2007) Dietary habits and nutrient intake in non-alcoholic steatohepatitis. Nutrition 23:46–52

    Article  PubMed  Google Scholar 

  • Verbrugghe A, Bacovic M (2013) Peculiarities of one-carbon metabolism in the strict carnivorous cat and the role in feline hepatic lipidosis. Nutrients 5:2811–2835

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Verbrugghe A, Hesta M, Daminet S et al (2012) Nutritional modulation of insulin resistance in the true carnivorous cat: a review. Crit Rev Food Sci Nutr 52:172–182

    Article  PubMed  CAS  Google Scholar 

  • Videla L, Rodrigo R, Araya J et al (2004) Oxidative stress and depletion of hepatic long-chain polyunsaturated fatty acids may contribute to nonalcoholic fatty liver disease. Free Radic Biol Med 37:1499–1507

    Article  PubMed  CAS  Google Scholar 

  • Westerbacka J, Kolak M, Kiviluoto T et al (2007) Genes involved in fatty acid partitioning and binding, lipolysis, monocyte/macrophage recruitment, and inflammation are overexpressed in the human fatty liver of insulin-resistant subjects. Diabetes 56:2759–2765

    Article  PubMed  CAS  Google Scholar 

  • Westphal S (2008) Obesity, abdominal obesity, and insulin resistance. Clin Cornerstone 9:23–31

    Article  PubMed  Google Scholar 

  • Xu L, Ma X, Cui B et al (2011) Selection of reference genes for qRT-PCR in high fat diet-induced hepatic steatosis mice model. Mol Biotechnol 48:255–262

    Article  PubMed  CAS  Google Scholar 

  • York LW, Puthalapattu S, Wu G (2009) Nonalcoholic fatty liver disease and low-carbohydrate diets. Annu Rev Nutr 29:365–379

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Takamura N, Shuto T et al (2010) The citrus flavonoid hesperetin and naringenin block the lipolytic actions of TNF-α in mouse adipocytes. Biochem Biophys Res Commun 394:728–732

    Article  PubMed  CAS  Google Scholar 

  • Yuan M, Konstantopoulos N, Lee J et al (2001) Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkβ. Science 293:1673–1677

    Article  PubMed  CAS  Google Scholar 

  • Zechner R, Strauss J, Frank S et al (2000) The role of lipoprotein lipase in adipose tissue development and metabolism. Int J Obes 24:S53–S56

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Canadian Centre for Fur Animal Research for their skillful technical assistance during the mink experiment. This study was supported by the Natural Sciences and Engineering Research Council of Canada (Discovery Grant to K. Rouvinen-Watt, Undergraduate Student Research Award to C. Pal and D. Kryzskaya), the Nova Scotia Department of Agriculture Technology Development Program (DEV26-001), the Canada Mink Breeders’ Association, and the Graduate Research Training Initiative (C. Pal). The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kirsti Rouvinen-Watt.

Additional information

Communicated by H.V. Carey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 55 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rouvinen-Watt, K., Pal, C., Martin, T. et al. Evidence of endoplasmic reticulum stress and liver inflammation in the American mink Neovison vison with benign hepatic steatosis. J Comp Physiol B 184, 913–927 (2014). https://doi.org/10.1007/s00360-014-0845-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-014-0845-9

Keywords

Navigation