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Energy turnover in European hares is centrally limited during early, but not during peak lactation

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Abstract

We investigated metabolizable energy intake (MEI) and milk energy output in European hares throughout gestation and lactation in females raising three young, i.e., close to maximum litter size in this precocial species. We hypothesized that herbivorous hares may face a central limitation of energy turnover during lactation, imposed by maximum capacity of the gastrointestinal tract. Females were provided with low-energy or high-energy diets, either continually, or during lactation only. Unexpectedly, females on either diet reached identical peak MEIs (>6 times BMR) during late lactation, with females on low-energy diet increasing food intake proportionally. Thus, we reject our hypothesis that in lactating hares, peak MEI is centrally limited. During early lactation, MEI and milk transfer was, however, significantly impaired in females on the low-energy diet, indicating a temporal central limitation due to a time-lag caused by the readjustment of energy intake capacity. Importantly, irrespective of the diet, females significantly increased peak MEI late in the breeding season. Consequently, earlier in the season, when energy reserves are still high, energy throughput was not limited by physiological constraints at all. We conclude that extreme MEI may have fitness costs, and that females maximize lifetime reproductive success by actively down-regulating MEI whenever possible.

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Abbreviations

AE:

Assimilation efficiency

ADF:

Acid detergent fibre

BMR:

Basal metabolic rate

GEI:

Gross energy intake

LM:

Linear models

LME:

Linear mixed effects models

MEI:

Metabolizable energy intake

NFE:

Nitrogen free extracts

NIRS:

Near infrared spectroscopy

SusEI:

Sustained energy intake

SusMR:

Sustained metabolic rate

References

  • Bacigalupe LD, Bozinovic F (2002) Design, limitations and sustained metabolic rate: lessons from small mammals. J Exp Biol 205:2963–2970

    PubMed  Google Scholar 

  • Broekhuizen S, Maaskamp F (1980) Behavior of does and leverets of the European hare (Lepus europaeus) whilst nursing. J Zool (Lond) 191:487–501

    Article  Google Scholar 

  • Brüll U (1976) Nahrungsbiologische Studien am Feldhasen in Schleswig- Holstein: ein Beitrag zur Äsungsverbesserung. In: Pielowski Z, Pucek Z (eds) Ecology and management of the European hare populations. Polish Hunting Association, Warszawa, pp 93–99

    Google Scholar 

  • Butler WR, Smith RD (1989) Interrelationships between energy balance and postpartum reproductive function in dairy cattle. J Dairy Sci 72:767–783

    PubMed  CAS  Google Scholar 

  • Dekinga A, Dietz MW, Koolhaas A, Piersma T (2001) Time course and reversibility of changes in the gizzards of red knots alternately eating hard and soft food. J Exp Biol 204:2167–2173

    PubMed  CAS  Google Scholar 

  • Devitt Mc, Speakman JR (1994) Central limits to sustainable metabolic rate have no role in cold acclimation of the short -tailed field vole (Microtus agrestis). Physiol Zool 67:1117–1139

    Google Scholar 

  • DeWitt T, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. TREE 13:77–81

    Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Forbes JM (1970) Voluntary food intake of pregnant ewes. J Anim Sci 31:1222–1227

    Google Scholar 

  • Forbes JM (2007) Reproduction and lactation. In: Forbes JM (ed) Voluntary food intake and diet selection in farm animals, 2nd edn. Cab International, London, pp 341–364

    Google Scholar 

  • Garland T (1983) The relation between maximal running speed and body mass in terrestrial mammals. J Zool (Lond) 199:157–170

    Article  Google Scholar 

  • Gilbert AN (1986) Mammary number and litter size in rodentia: the “one-half rule”. Proc Natl Acad Sci USA 83:4828–4830

    Article  PubMed  CAS  Google Scholar 

  • Gross JE, Wang Z, Wunder B (1985) Effects of food quality and energy needs: changes in gut morphology and capacity of Microtus ochrogaster. J Mammal 66:661–667

    Article  Google Scholar 

  • Hackländer K, Tataruch F, Ruf T (2002a) The effect of dietary fat content on lactation energetics in the European hare (Lepus europaeus). PBZ 75:19–28. doi:10.1086/324770

    PubMed  Google Scholar 

  • Hackländer K, Arnold W, Ruf T (2002b) Postnatal development and thermoregulation in the precocial European hare (Lepus europaeus). J Comp Biochem Physiol B 172:183–190. doi:10.1007/s00360-001-0243-y

    Article  Google Scholar 

  • Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462. doi:10.1038/386457a0

    Article  PubMed  CAS  Google Scholar 

  • Hammond KA, Kristan D (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). PBZ 73:547–556

    PubMed  CAS  Google Scholar 

  • Hammond KA, Wunder B (1991) The role of diet quality and energy need in the nutritional ecology of a small herbivore, Microtus ochrogaster. Physiol Zool 64:541–567

    Google Scholar 

  • Hammond KA, Konarzewski M, Torres R, Diamond J (1994) Metabolic ceilings under a combination of peak energy demands. Physiol Zool 67:1479–1506

    Google Scholar 

  • Hammond KA, Lloyd K, Diamond J (1996) Is mammary output capacity limiting to lactational performance in mice? J Exp Biol 199:337–349

    PubMed  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. doi:10.1002/bimj.200810425

    Article  PubMed  Google Scholar 

  • Ingvartsen KL, Andersen JB (2000) Integration of metabolism and intake regulation: a review focusing on periparturient animals. J Dairy Sci 83:1573–1597

    PubMed  CAS  Google Scholar 

  • Johnson MS, Speakman JR (2001) Limits to sustained energy intake: V. Effect of cold- exposure during lactation in Mus musculus. J Exp Biol 204:1967–1977

    PubMed  CAS  Google Scholar 

  • Johnson MS, Thomson SC, Speakman JR (2001a) Limits to sustained energy intake: I. Lactation in the laboratory mouse, Mus musculus. J Exp Biol 204:1925–1935

    PubMed  CAS  Google Scholar 

  • Johnson MS, Thomson SC, Speakman JR (2001b) Limits to sustained energy intake: II. Inter-relationships between resting metabolic rate, life-history traits and morphology in Mus musculus. J Exp Biol 204:1937–1946

    PubMed  CAS  Google Scholar 

  • Johnson MS, Thomson SC, Speakman JR (2001c) Limits to sustained energy intake: III. Effects of concurrent pregnancy and lactation in Mus musculus. J Exp Biol 204:1947–1956

    PubMed  CAS  Google Scholar 

  • Koteja P (1996) Limits to the energy budget in a rodent, Peromyscus maniculatus: the central limitation hypothesis. Physiol Zool 69:981–993

    Google Scholar 

  • Krol E, Murphy M, Speakman JR (2007) Limits to sustained energy intake X. Effects of fur removal on reproductive performance in laboratory mice. J Exp Biol 210:4233–4243

    Article  PubMed  Google Scholar 

  • Künkele J (2000) Energetics of gestation relative to lactation in a precocial rodent, the guinea pig (Cavia porcellus). J Zool (Lond) 250:533–539

    Google Scholar 

  • Livesey G (1984) The energy equivalents of ATP and the energy values of food proteins and fats. Brit J Nutr 51:15–28

    Article  PubMed  CAS  Google Scholar 

  • Livesey G, Marinos E (1988) Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. Am J Clin Nutr 47:608–628

    PubMed  CAS  Google Scholar 

  • Marboutin E, Aebischer NJ (1996) Does harvesting arable crops influence the behaviour of the European hare, Lepus europaeus ? Wildl Biol 2:83–91

    Google Scholar 

  • Mitchell-Jones AJ, Amori G, Bogdanowicz W, Krystufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralik V, Zima J (1999) Atlas of European mammals. Academic Press, London

    Google Scholar 

  • Naya DE, Ebensperger LA, Sabat P, Bozinovic F (2008) Digestive and metabolic flexibility allows female degus to cope with lactation costs. PBZ 81:186–194

    PubMed  Google Scholar 

  • Nehring K (1960) Agrikulturchemische Untersuchungsmethoden für Dünge- und Futtermittel. Böden und Milch, Parey, Hamburg

    Google Scholar 

  • Onderscheka K, Tataruch F (1982) Ein Versuch zur Erstellung von Normalwerten wildlebender Tiere und die Anwendung dieser Daten in der Wildbiologie. Wien Tierärztl Monschr 69:274–279

    CAS  Google Scholar 

  • Otzelberger K (1983) Österreichisches Methodenbuch für die Untersuchung von Futtermitteln, Futterzusatzstoffen und Schadstoffen. Arbeitsgemeinschaft der Landwirtschaftlichen Versuchsanstalten in Österreich, Wien

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. TREE 18:228–233

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core team (2008) nlme: linear and nonlinear mixed effects models. R package version 3.1-88

  • Reichlin T, Klansek E, Hackländer K (2006) Diet selection by hares (Lepus europaeus) in arable land and its implications for habitat management. Eur J Wildl Res 51:137–295

    Google Scholar 

  • Speakman JR (2008) The physiological costs of reproduction in small mammals. Phil Trans R Soc B 363:375–398. doi:10.1098/rstb.2007.2145

    Article  PubMed  Google Scholar 

  • Speakman JR, Krol E (2005) Limits to sustained energy intake IX: a review of hypotheses. J Comp Physiol B 175:375–394. doi:10.1007/s00360-005-0013-3

    Article  PubMed  Google Scholar 

  • Speakman JR, McQueenie J (1996) Limits to sustained metabolic rate: the link between food intake, basal metabolic rate, and morphology in reproducing mice, Mus musculus. Physiol Zool 69:746–769

    Google Scholar 

  • Speakman JR, Gidney A, Bett J, Mitchell IP, Johnson MS (2001) Limits to sustained energy intake: IV. Effect of variation in food quality on lactating mice, Mus musculus. J Exp Biol 204:1957–1965

    PubMed  CAS  Google Scholar 

  • Starck JM (1999) Phenotypic flexibility of the avian gizzard: rapid, reversible and repeated changes of organ size in response to changes in dietary fibre content. J Exp Biol 202:3171–3179

    PubMed  Google Scholar 

  • Stubbs RJ, Prentice AM, James WPT (1997) Carbohydrates and energy balance. Ann N Y Acad Sci 819:44–69

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org

  • Thompson SD (1992) Gestation and lactation in small mammals: basal metabolic rate and the limits of energy use. In: Tomasi TE, Horton TH (eds) Mammalian energetics. Interdisciplinary views of metabolism and reproduction. Comstock, Ithaca, pp 213–259

    Google Scholar 

  • Valencak TG, Tataruch F, Ruf T (2009) Peak energy turnover in lactating European hares: the role of fat reserves. J Exp Biol 212:231–237. doi:10.1242/jeb.022640

    Article  PubMed  CAS  Google Scholar 

  • Vande Haar MJ (1999) Nutritional factors and lactation. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction, vol III. Academic Press, San Diego, pp 422–432

    Google Scholar 

  • Veloso C, Bozinovic F (2000) Effect of food quality on the energetics of reproduction in a precocial rodent, Octodon degus. J Mammal 81:971–978

    Article  Google Scholar 

  • Villa-Godoy A, Hughes TL, Emery RS, Chapin LT, Fogwell RL (1988) Association between energy balance and luteal function in lactating dairy cows. J Dairy Sci 71:1063–1072

    Article  PubMed  CAS  Google Scholar 

  • Weiner J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. TREE 7:384–388. doi:10.1016/0169-5347(92)90009-Z

    Google Scholar 

  • Weldon WC, Lewis AJ, Louis GF, Kovar JL, Giesemann MA, Miller PS (1994) Postpartum hypophagia in primiparous sows: I. Effects of gestation feeding level on feed intake, feeding behavior, and plasma metabolite concentrations during lactation. J Anim Sci 72:387–394

    PubMed  CAS  Google Scholar 

  • Zörner E (1996) Der Feldhase Spektrum Akademischer. Verlag, Heidelberg

    Google Scholar 

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Acknowledgments

This work was funded by grant P17794-B06 from the Austrian Science Fund, and by the province of Lower Austria. We are grateful to the animal house facility staff (Michaela Salaba, Peter Steiger) and to numerous students who helped with hare welfare and data sampling. We would like to thank Eva Steiger and Le Minh Hien who performed all chemical analyses under direction of Frieda Tataruch. All experiments described here comply with the current laws in Austria, where the experiments were performed.

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Correspondence to Thomas Ruf.

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Communicated by G. Heldmaier.

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Valencak, T.G., Ruf, T. Energy turnover in European hares is centrally limited during early, but not during peak lactation. J Comp Physiol B 179, 933–943 (2009). https://doi.org/10.1007/s00360-009-0376-y

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