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On the use of body mass measures in severity assessment in laboratory passerine birds

Published online by Cambridge University Press:  01 January 2023

CP Andrews
CP Andrews*
Affiliation:
University of Stirling, Division of Psychology, Faculty of Natural Sciences, Stirling FK9 4LA, UK Newcastle University, Population Health Sciences Institute, Henry Wellcome Building, Framlington Place, Newcastle-upon-Tyne NE2 4HH, UK
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Abstract

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Criteria for assessing the severity of scientific procedures in laboratory rodents include the loss of body mass. However, guidance is limited for passerine birds and application of criteria developed for mammals risks poor welfare decisions. Here, I ask whether, and how, body mass criteria could be incorporated into laboratory welfare assessment of passerines. Passerine birds strategically adjust their body mass to minimise combined mortality risk from starvation and predation. A systematic literature review found that strategic mass changes can be sizeable (sometimes > 10%) even over short timescales. Many aspects of a bird's current or past environment, including husbandry and experimental procedures, may alter perceived starvation or predation risks and thus drive strategic mass change via evolved mechanisms. Therefore, body mass criteria used for rodents may be too stringent for passerines, potentially leading to over-estimated severity. Strategic mass changes might obscure those stemming from experimental interventions yet could also offer insights into whether birds perceive an intervention or altered husbandry as a threat. Mass criteria for severity assessment should be species- and context-specific in order to balance needs for refinement and reduction. To guide the development of appropriate criteria, a future research priority is for greater data collection and sharing based on standardised routine monitoring of mass variation under a representative range of husbandry conditions and procedures.

Keywords

animal welfareavian modelbody massmass regulationpasserineseverity
Type
Research Article
Information
Animal Welfare , Volume 31 , Issue 3 , August 2022 , pp. 387 - 401
Copyright
© 2022 Universities Federation for Animal Welfare

References

Abbey-Lee, RN, Mathot, KJ and Dingemanse, NJ 2016 Behavioral and morphological responses to perceived predation risk: A field experiment in passerines. Behavioral Ecology 27: 857–864. https://doi.org/10.1093/beheco/arv228CrossRefGoogle Scholar
Acquarone, C, Cucco, M, Cauli, SL and Malacarne, G 2002 Effects of food abundance and predictability on body condition and health parameters: experimental tests with the Hooded Crow. Ibis 144: E155–E163. https://doi.org/10.1046/j.1474-919X.2002.t01-2-00094_1.xCrossRefGoogle Scholar
Adriaensen, F, Dhondt, A, Dongen, SV, Lens, L and Matthysen, E 1998 Stabilizing selection on blue tit fledgling mass in the pres-ence of sparrowhawks. Proceedings of the Royal Society B: Biological Sciences 265: 1011–1016. https://doi.org/10.1098/rspb.1998.0392CrossRefGoogle Scholar
Alonso-Alvarez, C and Tella, JL 2001 Effects of experimental food restriction and body-mass changes on the avian T-cell-medi-ated immune response. Canadian Journal of Zoology 79: 101–105. https://doi.org/10.1139/z00-190CrossRefGoogle Scholar
Andrews, C, Viviani, J, Egan, E, Bedford, T, Brilot, B, Nettle, D and Bateson, M 2015 Early life adversity increases foraging and information gathering in European starlings. Animal Behaviour 109: 123–132. https://doi.org/10.1016/j.anbehav.2015.08.009CrossRefGoogle ScholarPubMed
Barluenga, M, Barbosa, A and Moreno, E 2001 Differences in daily mass gain between subordinate species are explained by dif-ferences in ecological plasticity. Écoscience 8: 437–440. https://doi.org/10.1080/11956860.2001.11682672CrossRefGoogle Scholar
Bateson, M, Andrews, C, Dunn, J, Egger, CBCM, Gray, F, McHugh, M and Nettle, D 2021 Food insecurity increases ener-getic efficiency, not food consumption: an exploratory study in European starlings. PeerJ 9: e11541. https://doi.org/10.7717/peerj.11541CrossRefGoogle Scholar
Bateson, M and Feenders, G 2010 The use of passerine bird species in laboratory research: implications of basic biology for husbandry and welfare. ILAR Journal/National Research Council, Institute of Laboratory Animal Resources 51: 394–408. https://doi.org/10.1093/ilar.51.4.394CrossRefGoogle ScholarPubMed
Bateson, M and Nolan, R 2022 A refined method for studying foraging behaviour and body mass in group-housed European star-lings. Animals 12: 1159. https://doi.org/10.3390/ani12091159CrossRefGoogle Scholar
Bauchinger, U, Wohlmann, A and Biebach, H 2005 Flexible remodeling of organ size during spring migration of the garden warbler Sylvia borin. Zoology 108: 97–106. https://doi.org/10.1016/j.zool.2005.03.003CrossRefGoogle ScholarPubMed
Bauer, CM, Glassman, LW, Cyr, NE and Romero, LM 2011 Effects of predictable and unpredictable food restriction on the stress response in molting and non-molting European starlings (Sturnus vulgaris). Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 160: 390–399. https://doi.org/10.1016/j.cbpa.2011.07.009CrossRefGoogle ScholarPubMed
Bautista, LM, Tinbergen, J, Wiersma, P and Kacelnik, A 1998 Optimal foraging and beyond: How starlings cope with changes in food availability. The American Naturalist 152: 543–561. https://doi.org/10.1086/286189CrossRefGoogle ScholarPubMed
Bednekoff, PA, Biebach, H and Krebs, J 1994 Great tit fat reserves under unpredictable temperatures. Journal of Avian Biology 25: 156–160. https://doi.org/10.2307/3677035CrossRefGoogle Scholar
Bednekoff, PA and Houston, AI 1994a Optimising fat reserves over the entire winter: A dynamic model. Oikos 71: 408–415. https://doi.org/10.2307/3545828CrossRefGoogle Scholar
Bednekoff, PA and Houston, AI 1994b Avian daily foraging pat-terns: Effects of digestive constraints and variability. Evolutionary Ecology 8: 36–52. https://doi.org/10.1007/BF01237664CrossRefGoogle Scholar
Bednekoff, PA and Krebs, JR 1995 Great tit fat reserves: Effects of changing and unpredictable feeding day length. Functional Ecology 9: 457–462. https://doi.org/10.2307/2390009CrossRefGoogle Scholar
Ben-Hamo, M, Burns, DJ, Bauchinger, U, Mukherjee, S, Embar, K and Pinshow, B 2016 Behavioural responses during feather replacement in house sparrows. Journal of Avian Biology 47: 103–108. https://doi.org/10.1111/jav.00651CrossRefGoogle Scholar
Blem, CR 1976 Patterns of lipid storage and utilization in birds. American Zoologist 16: 671–684. https://doi.org/10.1093/icb/16.4.671CrossRefGoogle Scholar
Bonneaud, C, Mazuc, J, Gonzalez, G, Haussy, C, Chastel, O, Faivre, B and Sorci, G 2003 Assessing the cost of mounting an immune response. The American Naturalist 161: 367–379. https://doi.org/10.1086/346134CrossRefGoogle ScholarPubMed
Brandt, MJ and Cresswell, W 2009 Diurnal foraging routines in a tropical bird, the rock finch Lagonosticta sanguinodorsalis: How important is predation risk? Journal of Avian Biology 40: 90–94. https://doi.org/10.1111/j.1600-048X.2008.04389.xCrossRefGoogle Scholar
Braun, EJ and Sweazea, KL 2008 Glucose regulation in birds. Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology 151: 1–9. https://doi.org/10.1016/j.cbpb.2008.05.007CrossRefGoogle ScholarPubMed
Breuner, C, Sprague, R, Patterson, S and Woods, H 2013 Environment, behavior and physiology: do birds use barometric pressure to predict storms? Journal of Experimental Biology 216: 1982–1990. https://doi.org/10.1242/jeb.081067CrossRefGoogle ScholarPubMed
Bridge, ES, Schoech, SJ, Bowman, R and Wingfield, JC 2009 Temporal predictability in food availability: Effects upon the repro-ductive axis in Scrub-Jays. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 311: 35–44. https://doi.org/10.1002/jez.493CrossRefGoogle Scholar
Brilot, BO and Bateson, M 2012 Water bathing alters threat perception in starlings. Biology Letters 8: 379–381. https://doi.org/10.1098/rsbl.2011.1200CrossRefGoogle ScholarPubMed
Brodin, A 2000 Why do hoarding birds gain fat in winter in the wrong way? Suggestions from a dynamic model. Behavioral Ecology 11: 27–39. https://doi.org/10.1093/beheco/11.1.27CrossRefGoogle Scholar
Brodin, A 2001 Mass-dependent predation and metabolic expen-diture in wintering birds: is there a trade-off between different forms of predation? Animal Behaviour 62: 993–999. https://doi.org/10.1006/anbe.2001.1844CrossRefGoogle Scholar
Brodin, A 2007 Theoretical models of adaptive energy manage-ment in small wintering birds. Philosophical Transactions of the Royal Society B: Biological Sciences 362: 1857–1871. https://doi.org/10.1098/rstb.2006.1812CrossRefGoogle Scholar
Broggi, J, Koivula, K, Lahti, K and Orell, M 2003 Seasonality in daily body mass variation in a hoarding boreal passerine. Oecologia 137: 627–633. https://doi.org/10.1007/s00442-003-1355-8CrossRefGoogle Scholar
Brown, JS and Kotler, BP 2004 Hazardous duty pay and the for-aging cost of predation. Ecology Letters 7: 999–1014. https://doi.org/10.1111/j.1461-0248.2004.00661.xCrossRefGoogle Scholar
Brown, ME 1996 Assessing body condition in birds. In: Nolan, V and Ketterson, ED (eds) Current Ornithology, Volume 13 pp 67–135. Springer: Boston MA, USA. https://doi.org/10.1007/978-1-4615-5881-1_3CrossRefGoogle Scholar
Burns, JG and Ydenberg, RC 2002 The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behavioral Ecology and Sociobiology 52: 128–136. https://doi.org/10.1007/s00265-002-0494-yCrossRefGoogle Scholar
Butler, PJ and Bishop, CM 2000 Flight. In: Whittow, G (ed) Sturkie's Avian Physiology, Fifth Edition pp 391–435. Elsevier Science: London, UK. https://doi.org/10.1016/B978-012747605-6/50016-XCrossRefGoogle Scholar
Carrascal, LM and Polo, V 1999 Coal tits, Parus ater, lose weight in response to chases by predators. Animal Behaviour 58: 281–285. https://doi.org/10.1006/anbe.1999.1142CrossRefGoogle ScholarPubMed
Carrascal, LM and Polo, V 2006 Effects of wing area reduction on winter body mass and foraging behaviour in coal tits: field and aviary experiments. Animal Behaviour 72: 663–672. https://doi.org/10.1016/j.anbehav.2005.11.027CrossRefGoogle Scholar
Carrete, M and Tella, JL 2015 Rapid loss of antipredatory behaviour in captive-bred birds is linked to current avian invasions. Scientific Reports 5: 1–8. https://doi.org/10.1038/srep18274CrossRefGoogle ScholarPubMed
Clark, A 1979 Bodyweights of birds - a review. Condor 81: 193–202. https://doi.org/10.2307/1367288CrossRefGoogle Scholar
Clark, CW and Ekman, J 1995 Dominant and subordinate fat-tening strategies: A dynamic game. Oikos 72: 205–212. https://doi.org/10.2307/3546222CrossRefGoogle Scholar
Clayton, NS and Emery, NJ 2015 Avian models for human cog-nitive neuroscience: A proposal. Neuron 86: 1330–1342. https://doi.org/10.1016/j.neuron.2015.04.024CrossRefGoogle Scholar
Clinchy, M, Sheriff, MJ and Zanette, LY 2013 Predator-induced stress and the ecology of fear. Functional Ecology 27: 56–65. https://doi.org/10.1111/1365-2435.12007CrossRefGoogle Scholar
Clinchy, M, Zanette, L, Boonstra, R, Wingfield, JC and Smith, JNM 2004 Balancing food and predator pressure induces chronic stress in songbirds. Proceedings of the Royal Society B: Biological Sciences 271: 2473–2479. https://doi.org/10.1098/rspb.2004.2913CrossRefGoogle ScholarPubMed
Clinchy, M, Zanette, L, Charlier, TD, Newman, AEM, Schmidt, KL, Boonstra, R and Soma, KK 2011 Multiple mea-sures elucidate glucocorticoid responses to environmental variation in predation threat. Oecologia 166: 607–614. https://doi.org/10.1007/s00442-011-1915-2CrossRefGoogle Scholar
Cooper, SJ 2007 Daily and seasonal variation in body mass and vis-ible fat in mountain chickadees and juniper titmice. The Wilson Journal of Ornithology 119: 720–724. https://doi.org/10.1676/06-183.1CrossRefGoogle Scholar
Cornelius, EA, Vézina, F, Regimbald, L, Hallot, F, Petit, M, Love, OP and Karasov, WH 2017 Chickadees faced with unpre-dictable food increase fat reserves but certain components of their immune function decline. Physiological and Biochemical Zoology 90: 190–200. https://doi.org/10.1086/689913CrossRefGoogle ScholarPubMed
Cox, DTC, Brandt, MJ, McGregor, R, Ottosson, U, Stevens, MC and Cresswell, W 2011 Patterns of seasonal and yearly mass variation in West African tropical savannah birds. Ibis 153: 672–683. https://doi.org/10.1111/j.1474-919X.2011.01150.xCrossRefGoogle Scholar
Cresswell, W 1998 Diurnal and seasonal mass variation in black-birds Turdus merula: consequences for mass-dependent prdation risk. Journal of Animal Ecology 67: 78–90. https://doi.org/10.1046/j.1365-2656.1998.00174.xCrossRefGoogle Scholar
Cucco, M, Ottonelli, R, Raviola, M and Malacarne, G 2002 Variations of body mass and immune function in response to food unpredictability in magpies. Acta Oecologica 23: 271–276. https://doi.org/10.1016/S1146-609X(02)01154-2CrossRefGoogle Scholar
Cuthill, IC, Hunt, S, Cleary, C and Clark, C 1997 Colour bands, dominance, and body mass regulation in male zebra finches (Taeniopygia guttata). Proceedings: Biological Sciences 264: 1093–1099. https://doi.org/10.1098/rspb.1997.0151Google Scholar
Cuthill, IC, Maddocks, SA, Weall, CV and Jones, EKM 2000 Body mass regulation in response to changes in feeding pre-dictability and overnight energy expenditure. Behavioral Ecology 11: 189–195. https://doi.org/10.1093/beheco/11.2.189CrossRefGoogle Scholar
Cyr, NE, Earle, K, Tam, C and Romero, LM 2007 The effect of chronic psychological stress on corticosterone, plasma metabo-lites, and immune responsiveness in European starlings. General and Comparative Endocrinology 154: 59–66. https://doi.org/10.1016/j.ygcen.2007.06.016CrossRefGoogle Scholar
Dall, SRX and Witter, MS 1998 Feeding interruptions, diurnal mass changes and daily routines of behaviour in the zebra finch. Animal Behaviour 55: 715–725. https://doi.org/10.1006/anbe.1997.0749CrossRefGoogle ScholarPubMed
D’Eath, RB, Tolkamp, BJ, Kyriazakis, I and Lawrence, AB 2009 ‘Freedom from hunger’ and preventing obesity: the animal welfare implications of reducing food quantity or quality. Animal Behaviour 77: 275–288. https://doi.org/10.1016/j.anbehav.2008.10.028CrossRefGoogle Scholar
Dickens, MJ, Earle, KA and Romero, LM 2009 Initial transfer-ence of wild birds to captivity alters stress physiology. General and Comparative Endocrinology 160: 76–83. https://doi.org/10.1016/j.ygcen.2008.10.023CrossRefGoogle ScholarPubMed
Dunn, IC, Wilson, PW, Smulders, TV, Sandilands, V, D’Eath, RB and Boswell, T 2015 Hypothalamic agouti-related protein expression is affected by both acute and chronic experience of food restriction and re-feeding in chickens. Journal of Neuroendocrinology 25: 920–928. https://doi.org/10.1111/jne.12088CrossRefGoogle Scholar
Dunn, J, Andrews, C, Nettle, D and Bateson, M 2018 Early-life begging effort reduces adult body mass but strengthens behavioural defence of the rate of energy intake in European star-lings. Royal Society Open Science 5: 171918. https://doi.org/10.1098/rsos.171918CrossRefGoogle Scholar
Ekman, J 2004 Mass-dependence in the predation risk of unequal competitors; some models. Oikos 105: 109–116. https://doi.org/10.1111/j.0030-1299.2004.10804.xCrossRefGoogle Scholar
Ekman, JB and Hake, MK 1990 Monitoring starvation risk: adjustment of body reserves in greenfinches (Carduleis chloris L) during periods of unpredictable foraging success. Behavioral Ecology 1: 62–67. https://doi.org/10.1093/beheco/1.1.62CrossRefGoogle Scholar
Ekman, JB and Lilliendahl, K 1993 Using priority to food access - fattening stretegies in dominance structured willow tits (Parus montanus) flocks. Behavioural Ecology 4: 232–238. https://doi.org/10.1093/beheco/4.3.232CrossRefGoogle Scholar
European Comission 2012 Caring for animals aiming for better science. Directive 2010/63/EU on protection of animals used for scien-tific purposes. EC: Brussels, BelgiumGoogle Scholar
European Commission 2013 Examples to illustrate the process of severity classification, day-to-day assessment and actual severity assess-ment. EC: Brussels, BelgiumGoogle Scholar
Feare, C 1984 The Starling. Oxford University Press: Oxford, UKGoogle Scholar
Feenders, G and Bateson, M 2011 Hand-rearing reduces fear of humans in European starlings, Sturnus vulgaris. PLOS ONE 6: e17466. https://doi.org/10.1371/journal.pone.0017466CrossRefGoogle ScholarPubMed
Feenders, G, Klaus, K and Bateson, M 2011 Fear and explo-ration in European starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught birds. PLOS ONE 6: e19074. https://doi.org/10.1371/journal.pone.0019074CrossRefGoogle ScholarPubMed
Fischer, CP, Wright-Lichter, J and Romero, LM 2018 Chronic stress and the introduction to captivity: How wild house sparrows (Passer domesticus) adjust to laboratory conditions. General and Comparative Endocrinology 259: 85–92. https://doi.org/10.1016/j.ygcen.2017.11.007CrossRefGoogle ScholarPubMed
Flores-Santin, J and Burggren, WW 2021 Beyond the chicken: Alternative avian models for developmental physiological research. Frontiers in Physiology 12: 712633. https://doi.org/10.3389/fphys.2021.712633CrossRefGoogle ScholarPubMed
Fokidis, HB, des Roziers, MB, Sparr, R, Rogowski, C, Sweazea, K and Deviche, P 2012 Unpredictable food availability induces metabolic and hormonal changes independent of food intake in a sedentary songbird. Journal of Experimental Biology 215: 2920–2930. https://doi.org/10.1242/jeb.071043CrossRefGoogle Scholar
Fransson, T and Weber, TP 1997 Migratory fuelling in blackcaps (Sylvia atricapilla) under perceived risk of predation. Behavioral Ecology and Sociobiology 41: 75–80. https://doi.org/10.1007/s002650050366CrossRefGoogle Scholar
Gallagher, AJ, Creel, S, Wilson, RP and Cooke, SJ 2017 Energy landscapes and the landscape of fear. Trends in Ecology and Evolution 32: 88–96. https://doi.org/10.1016/j.tree.2016.10.010CrossRefGoogle ScholarPubMed
Garamszegi, LZ, Møller, AP, Török, J, Michl, G, Péczely, P and Richard, M 2004 Immune challenge mediates vocal communication in a passerine bird: An experiment. Behavioral Ecology 15: 148–157. https://doi.org/10.1093/beheco/arg108CrossRefGoogle Scholar
Gentle, LK and Gosler, AG 2001 Fat reserves and perceived predation risk in the great tit, Parus major. Proceedings: Biological Sciences 268: 487–491. https://doi.org/10.1098/rspb.2000.1405Google ScholarPubMed
Gómez, C, Bayly, NJ, Norris, DR, Mackenzie, SA, Rosenberg, KV, Taylor, PD, Hobson, KA and Cadena, C 2017 Fuel loads acquired at a stopover site influence the pace of intercontinental migration in a boreal songbird. Scientific Reports 7: 1–11. https://doi.org/10.1038/s41598-017-03503-4CrossRefGoogle Scholar
Gosler, A 2001 The effects of trapping on the perception, and trade-off, of risks in the great tit Parus major. Ardea 89: 75–84Google Scholar
Gosler, AG 1996 Environmental and social determinants of win-ter fat storage in the great tit (Parus major). Journal of Animal Ecology 65: 1–17. https://doi.org/10.2307/5695CrossRefGoogle Scholar
Gosler, AG 2002 Strategy and constraint in the winter fattening response to temperature in the great tit Parus major. Journal of Animal Ecology 71: 771–779. https://doi.org/10.1046/j.1365-2656.2002.00642.xCrossRefGoogle Scholar
Gosler, AG, Greenwood, JJD and Perrins, C 1995 Predation risk and the cost of being fat. Nature 377: 621–623. https://doi.org/10.1038/377621a0CrossRefGoogle Scholar
Goymann, W, Trappschuh, M, Jensen, W and Schwabl, I 2006 Low ambient temperature increases food intake and dropping production, leading to incorrect estimates of hormone metabolite concentrations in European stonechats. Hormones and Behavior 49: 644–653. https://doi.org/10.1016/j.yhbeh.2005.12.006CrossRefGoogle ScholarPubMed
Guglielmo, CG 2018 Obese super athletes: fat-fueled migration in birds and bats. The Journal of Experimental Biology 221: jeb165753. https://doi.org/10.1242/jeb.165753CrossRefGoogle ScholarPubMed
Haftorn, S 1989 Seasonal and diurnal body weight variations in titmice, based on analyses of individual birds. The Wilson Bulletin 101: 217–235Google Scholar
Haftorn, S 1992 The diurnal body weight cycle in titmice Parus spp. Ornis Scandinavica 23: 435–443. https://doi.org/10.2307/3676674CrossRefGoogle Scholar
Haftorn, S 2000 Rank-dependent winter fattening in the willow tit Parus montanus. Ornis Fennica 77: 49–56Google Scholar
Hake, MK 1996 Fattening strategies in dominance-structured greenfinch (Carduelis chloris) flocks in winter. Behavioral Ecology and Sociobiology 39: 71–76. https://doi.org/10.1007/s002650050268CrossRefGoogle Scholar
Harris, BN and Carr, JA 2016 The role of the hypothalamus-pituitary-adrenal/interrenal axis in mediating predator-avoidance trade-offs. General and Comparative Endocrinology 231: 110–142. https://doi.org/10.1016/j.ygcen.2016.04.006CrossRefGoogle Scholar
Hau, M, Haussmann, MF, Greives, TJ, Matlack, C, Costantini, D, Quetting, M, Adelman, JS, Miranda, A and Partecke, J 2015 Repeated stressors in adulthood increase the rate of biological ageing. Frontiers in Zoology 12: 4. https://doi.org/10.1186/s12983-015-0095-zCrossRefGoogle ScholarPubMed
Hawkins, P, Morton, DB, Cameron, D, Cuthill, I, Francis, R, Freire, R, Gosler, A, Healy, S, Hudson, A, Inglis, I, Jones, A, Kirkwood, J, Lawton, M, Monaghan, P, Sherwin, C and Townsend, P 2001 Laboratory birds: refinements in husbandry and procedures. Laboratory Animals 35(S1): 1–163. https://doi.org/10.1258/0023677011911967CrossRefGoogle Scholar
Hiebert, SM, Salvante, KG, Ramenofsky, M and Wingfield, JC 2000 Corticosterone and nocturnal torpor in the rufous hum-mingbird (Selasphorus rufus). General and Comparative Endocrinology 120: 220–234. https://doi.org/10.1006/gcen.2000.7555CrossRefGoogle Scholar
Higginson, AD, McNamara, JM and Houston, AI 2012 The starvation-predation trade-off predicts trends in body size, muscu-larity, and adiposity between and within taxa. The American Naturalist 179: 338–350. https://doi.org/10.1086/664457CrossRefGoogle ScholarPubMed
Home Office 2014 Guidance on the operation of the Animals (Scientific Procedures) Act 1986. https://www.gov.uk/guidance/guidance-on-the-operation-of-the-animals-scientific-procedures-act-1986Google Scholar
Houston, AI and McNamara, JM 1993 A theoretical investigation of the fat reserves and mortality levels of small birds in winter. Ornis Scandinavica 24: 205–219. https://doi.org/10.2307/3676736CrossRefGoogle Scholar
Houston, AI, McNamara, JM and Hutchinson, JMC 1993 General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society B: Biological Sciences 341: 375–397. https://doi.org/10.1098/rstb.1993.0123Google Scholar
Houston, AI, Welton, NJ and McNamara, JM 1997 Acquisition and maintenance costs in the long-term regulation of avian fat reserves. Oikos 78: 331–340. https://doi.org/10.2307/3546301CrossRefGoogle Scholar
Hudin, NS, Strubbe, D, Teyssier, A, De Neve, L, White, J, Janssens, GPJ and Lens, L 2016 Predictable food supplies induce plastic shifts in avian scaled body mass. Behavioral Ecology 27: 1833–1840Google Scholar
Hurly, TA 1992 Energetic reserves of marsh tits (Parus palustris): Food and fat storage in response to variable food supply. Behavioral Ecology 3: 181–188. https://doi.org/10.1093/beheco/3.2.181CrossRefGoogle Scholar
Johnstone, AM, Murison, SD, Duncan, JS, Rance, KA and Speakman, JR 2005 Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. American Journal of Clinical Nutrition 82: 941–948. https://doi.org/10.1093/ajcn/82.5.941CrossRefGoogle ScholarPubMed
Jones, HRP, Oates, J and Trussell, BA 1996 An applied approach to the assessment of severity. In: Hendriksen, CFM and Morton, DB (eds) Humane Endpoints in Animal Experiments for Biomedical Research. Proceedings of the International Conference pp 40–47. 22-25 November 1998, Zeist, The Netherlands. Royal Society for Medicine Press Ltd: London, UKGoogle Scholar
Katti, M and Price, T 1999 Annual variation in fat storage by a migrant warbler overwintering in the Indian tropics. Journal of Animal Ecology 68: 815–823. https://doi.org/10.1046/j.1365-2656.1999.00331.xCrossRefGoogle Scholar
Kelly, JP, Warnock, N, Page, GW and Weathers, WW 2002 Effects of weather on daily body mass regulation in wintering dun-lin. Journal of Experimental Biology 205: 109–120. https://doi.org/10.1242/jeb.205.1.109CrossRefGoogle Scholar
Knight, K 2018 The biology of fat. The Journal of Experimental Biology 221: jeb178020. https://doi.org/10.1242/jeb.178020CrossRefGoogle Scholar
Kobiela, ME, Cristol, DA and Swaddle, JP 2015 Risk-taking behaviours in zebra finches affected by mercury exposure. Animal Behaviour 103: 153–160. https://doi.org/10.1016/j.anbehav.2015.02.024CrossRefGoogle Scholar
Koivula, K, Orell, M and Lahti, K 2002 Plastic daily fattening routines in willow tits. Journal of Animal Ecology 71: 816–823. https://doi.org/10.1046/j.1365-2656.2002.00646.xCrossRefGoogle Scholar
Koivula, K, Orell, M, Rytkönen, S, Lahti, K, Koivula, K, Orell, M, Rytkonen, S and Lahti, K 1995 Fatness, sex and dominance; seasonal and daily body mass changes in willow tits. Journal of Avian Biology 26: 209–216. https://doi.org/10.2307/3677321CrossRefGoogle Scholar
Krams, I 2000 Length of feeding day and body weight of great tits in a single- and a two-predator environment. Behavioral Ecology and Sociobiology 48: 147–153. https://doi.org/10.1007/s002650000214CrossRefGoogle Scholar
Krams, I 2002 Mass-dependent take-off ability in wintering great tits (Parus major): Comparison of top-ranked adult males and sub-ordinate juvenile females. Behavioral Ecology and Sociobiology 51: 345–349. https://doi.org/10.1007/s00265-002-0452-8CrossRefGoogle Scholar
Krams, I, Cirule, D, Suraka, V, Krama, T, Rantala, MJ and Ramey, G 2010 Fattening strategies of wintering great tits sup-port the optimal body mass hypothesis under conditions of extremely low ambient temperature. Functional Ecology 24: 172–177. https://doi.org/10.1111/j.1365-2435.2009.01628.xCrossRefGoogle Scholar
Krams, I, Vrublevska, J, Nord, A, Krama, T, Cirule, D and Rantala, MJ 2012 Nocturnal loss of body reserves reveals high survival risk for subordinate great tits wintering at extremely low ambient temperatures. Oecologia 172: 339–346. https://doi.org/10.1007/s00442-012-2505-7CrossRefGoogle ScholarPubMed
Krause, ET and Ruploh, T 2016 Captive domesticated zebra finch-es (Taeniopygia guttata) have increased plasma corticosterone con-centrations in the absence of bathing water. Applied Animal Behaviour Science 182: 80–85. https://doi.org/10.1016/j.applanim.2016.06.003CrossRefGoogle Scholar
Krause, J and Ruxton, GD 2002 Living in Groups. Oxford University Press: Oxford, UKGoogle Scholar
Kullberg, C 1998 Does diurnal variation in body mass affect take-off ability in wintering willow tits? Animal Behaviour 56: 227–233. https://doi.org/10.1006/anbe.1998.0765CrossRefGoogle ScholarPubMed
Kullberg, C, Fransson, T and Jakobsson, S 1996 Impaired preda-tor evasion in fat blackcaps. Proceedings of the Royal Society B: Biological Sciences 263: 1671–1675. https://doi.org/10.1098/rspb.1996.0244Google Scholar
Kullberg, C, Jakobsson, S and Fransson, T 1998 Predator-induced take-off strategy in great tits (Parus major). Proceedings of the Royal Society B: Biological Sciences 265: 1659–1664. https://doi.org/10.1098/rspb.1998.0485CrossRefGoogle Scholar
Kullberg, C, Jakobsson, S and Fransson, T 2000 High migratory fuel loads impair predator evasion in sedge warblers. The Auk 117: 1034–1038. https://doi.org/10.1093/auk/117.4.1034CrossRefGoogle Scholar
Kullberg, C, Metcalfe, NB and Houston, DC 2002 Impaired flight ability during incubation in the pied flycatcher. Journal of Avian Biology 33: 179–183. https://doi.org/10.1034/j.1600-048X.2002.330209.xCrossRefGoogle Scholar
Lange, H and Leimar, O 2004 Social stability and daily body mass gain in great tits. Behavioral Ecology 15: 549–554. https://doi.org/10.1093/beheco/arh044CrossRefGoogle Scholar
LASA/APC 2008 Final report of a LASA/APC Working Group to examine the feasibility of reporting data on the severity of scientific pro-cedures on animals. https://assets.publishing.service.gov.uk/govern-ment/uploads/system/uploads/attachment_data/file/118989/sever-ity-scientific-procedures.pdfGoogle Scholar
Lasiewski, RC and Dawson, WR 1967 A re-examination of the relation between standard metabolic rate and bodyweight in birds. The Condor 69: 13–23. https://doi.org/10.2307/1366368CrossRefGoogle Scholar
Lehikoinen, E 1987 Seasonality of the daily weight cycle in win-tering passerines and its consequences. Ornis Scandinavica 18: 216–226. https://doi.org/10.2307/3676769CrossRefGoogle Scholar
Lilliendahl, K 1997 The effect of predator presence on body mass in captive greenfinches. Animal Behaviour 53: 75–81. https://doi.org/10.1006/anbe.1996.0279CrossRefGoogle Scholar
Lilliendahl, K 1998 Yellowhammers get fatter in the presence of a predator. Animal Behaviour 55: 1335–1340. https://doi.org/10.1006/anbe.1997.0706CrossRefGoogle ScholarPubMed
Lilliendahl, K 2000 Daily accumulation of body reserves under increased predation risk in captive Greenfinches Carduelis chloris. Ibis 142: 587–595. https://doi.org/10.1111/j.1474-919X.2000.tb04458.xCrossRefGoogle Scholar
Lilliendahl, K 2002 Daily patterns of body mass gain in four species of small wintering birds. Journal of Avian Biology 3: 212–218. https://doi.org/10.1034/j.1600-048X.2002.330302.xCrossRefGoogle Scholar
Lilliendahl, K, Carlson, A, Welander, J, Ekman, JB and Jonas, W 2011 Behavioural control of daily fattening in great tits (Parus major). Canadian Journal of Zoology 74: 1612–1616. https://doi.org/10.1139/z96-178CrossRefGoogle Scholar
Lima, SLSL 1986 Predation risk and unpredictable feeding con-ditions: Determinants of body mass in birds. Ecology 67: 377–385. https://doi.org/10.2307/1938580CrossRefGoogle Scholar
Love, A, Lovern, M and DuRant, S 2017 Captivity influences immune responses, stress endocrinology, and organ size in house sparrows (Passer domesticus). General and Comparative Endocrinology 252: 18–26. https://doi.org/10.1016/j.ygcen.2017.07.014CrossRefGoogle ScholarPubMed
Macleod, R, Barnett, P, Clark, JA and Cresswell, W 2005a Body mass change strategies in blackbirds Turdus merula: The star-vation-predation risk trade-off. Journal of Animal Ecology 74: 292–302. https://doi.org/10.1111/j.1365-2656.2005.00923.xCrossRefGoogle Scholar
Macleod, R, Clark, J and Cresswell, W 2008 The starvation-pre-dation risk trade-off, body mass and population status in the com-mon starling Sturnus vulgaris. Ibis 150: 199–208. https://doi.org/10.1111/j.1474-919X.2008.00820.xCrossRefGoogle Scholar
Macleod, R and Gosler, AG 2006 Capture and mass change: per-ceived predation risk or interrupted foraging? Animal Behaviour 71: 1081–1087. https://doi.org/10.1016/j.anbehav.2005.07.022CrossRefGoogle Scholar
Macleod, R, Gosler, AG and Cresswell, W 2005b Diurnal mass gain strategies and perceived predation risk in the great tit Parus major. Journal of Animal Ecology 74: 956–964. https://doi.org/10.1111/j.1365-2656.2005.00993.xCrossRefGoogle Scholar
MacLeod, R, Lind, J, Clark, J and Cresswell, W 2007 Mass reg-ulation in response to predation risk can indicate population declines. Ecology Letters 10: 945–955. https://doi.org/10.1111/j.1461-0248.2007.01088.xCrossRefGoogle Scholar
Marasco, V, Boner, W, Heidinger, B, Griffiths, K and Monaghan, P 2015 Repeated exposure to stressful conditions can have beneficial effects on survival. Experimental Gerontology 69: 170–175. https://doi.org/10.1016/j.exger.2015.06.011CrossRefGoogle ScholarPubMed
Mathot, KJ, Abbey-Lee, RN, Kempenaers, B and Dingemanse, NJ 2016 Do great tits (Parus major) suppress basal metabolic rate in response to increased perceived predation dan-ger? A field experiment. Physiology and Behavior 164: 400–406. https://doi.org/10.1016/j.physbeh.2016.06.029CrossRefGoogle ScholarPubMed
McMillan, FD 2013 Stress-induced and emotional eating in animals: A review of the experimental evidence and implications for compan-ion animal obesity. Journal of Veterinary Behavior: Clinical Applications and Research 8: 376–385. https://doi.org/10.1016/j.jveb.2012.11.001CrossRefGoogle Scholar
McNamara, JM and Houston, AI 1990 The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheoretica 38: 37–61. https://doi.org/10.1007/BF00047272CrossRefGoogle ScholarPubMed
McNamara, JM, Houston, AI, Lima, SL, Mcnamara, JM, Houston, AI and Lima, SL 1994 Foraging routines of small birds in winter: A theoretical investigation. Journal of Avian Biology 25: 287–302. https://doi.org/10.2307/3677276CrossRefGoogle Scholar
McWilliams, SR and Karasov, WH 2005 Migration takes guts: Digestive physiology of migratory birds and its ecological significance. In: Greenberg, R and Marra, PP (eds) Birds of Two Worlds: The Ecology and Evolution of Migration pp 67–78. JHU Press: Baltimore, MD, USAGoogle Scholar
Meijer, T, Möhring, FJ and Trillmich, F 1994 Annual and daily variation in body mass and fat of starlings Sturnus vulgaris. Journal of Avian Biology 25: 98–104. https://doi.org/10.2307/3677026CrossRefGoogle Scholar
Meijer, T, Rozman, J, Schulte, M and StachDreesmann, C 1996 New findings in body mass regulation in zebra finches (Taeniopygia guttata) in response to photoperiod and temperature. Journal of Zoology 240: 717–734. https://doi.org/10.1111/j.1469-7998.1996.tb05317.xCrossRefGoogle Scholar
Mello, CV 2014 The zebra finch (Taeniopygia guttata). An avian model for investigating the neurobiological basis of vocal learning. Cold Spring Harbor Protocols 12: 1237–1242. https://doi.org/10.1101/pdb.emo084574Google Scholar
Metcalfe, J, Schmidt, KL, Bezner, W, Guglielmo, CG and MacDougall-Shackleton, SA 2013 White-throated sparrows adjust behaviour in response to manipulations of barometric pres-sure and temperature. Animal Behaviour 86: 1285–1290. https://doi.org/10.1016/j.anbehav.2013.09.033CrossRefGoogle Scholar
Metcalfe, NB and Ure, SE 1995 Diurnal variation in flight perfor-mance and hence potential predation risk in small birds. Proceedings: Biological Sciences 261: 395–400. https://doi.org/10.1098/rspb.1995.0165Google Scholar
Middleton, A 1982 Response by American goldfinches, Carduelis tristis, to a severe winter storm. Canadian Field-Naturalist 96: 202–204Google Scholar
Moiron, M, Mathot, KJ and Dingemanse, NJ 2018 To eat and not be eaten: Diurnal mass gain and foraging strategies in wintering great tits. Proceedings of the Royal Society B: Biological Sciences 285: 20172868. https://doi.org/10.1098/rspb.2017.2868CrossRefGoogle Scholar
Mori, C and Wada, K 2015 Songbird: a unique animal model for studying the molecular basis of disorders of vocal development and communication. Experimental Animals 64(3): 221–230. https://doi.org/10.1538/expanim.15-0008CrossRefGoogle ScholarPubMed
Morosinotto, C, Villers, A, Varjonen, R and Korpimäki, E 2017 Food supplementation and predation risk in harsh climate: inter-active effects on abundance and body condition of tit species. Oikos 126: 863–873. https://doi.org/10.1111/oik.03476CrossRefGoogle Scholar
Mueller, HC and Berger, DD 1966 Analyses of weight and fat variations in transient Swainson's thrushes. Bird-Banding 37: 83–112. https://doi.org/10.2307/4511260CrossRefGoogle Scholar
Nettle, D, Andrews, C and Bateson, M 2017 Food insecurity as a driver of obesity in humans: The insurance hypothesis. Behavioral and Brain Sciences 40: e105. https://doi.org/10.1017/S0140525X16000947CrossRefGoogle ScholarPubMed
Nettle, D and Bateson, M 2015 Adaptive developmental plastic-ity: what is it, how can we recognize it and when can it evolve? Proceedings of the Royal Society B282: 20151005. https://doi.org/10.1098/rspb.2015.1005CrossRefGoogle Scholar
Norberg, RA 1981 Temporary weight decrease in breeding birds may result in more fledged young. The American Naturalist 118: 838–850. https://doi.org/10.1086/283874CrossRefGoogle Scholar
Nord A, Sköld-Chiriac S, Hasselquist D and Nilsson JÅ 2014 A tradeoff between perceived predation risk and energy conservation revealed by an immune challenge experiment. Oikos 123: 1091–1100. https://doi.org/10.1111/oik.01221CrossRefGoogle Scholar
Nwaogu, CJ, Dietz, MW, Tieleman, BI and Cresswell, W 2017 Breeding limits foraging time: evidence of interrupted foraging response from body mass variation in a tropical environment. Journal of Avian Biology 48: 563–569. https://doi.org/10.1111/jav.01132CrossRefGoogle Scholar
O’Hagan, D, Andrews, CP, Bedford, T, Bateson, M and Nettle, D 2015 Early life disadvantage strengthens flight performance trade-offs in European starlings, Sturnus vulgaris. Animal Behaviour 102: 141–148. https://doi.org/10.1016/j.anbehav.2015.01.016CrossRefGoogle ScholarPubMed
Pennycuick, CJ 1990 Bird Flight Performance: A Practical Calculation Manual. Oxford University Press: Oxford, UKGoogle Scholar
Piersma T and Lindström Å 1997 Rapid reversible changes in organ size as a component of adaptive behaviour. Trends in Ecology and Evolution 12: 134–138. https://doi.org/10.1016/S0169-5347(97)01003-3CrossRefGoogle Scholar
Polo, V and Bautista, LM 2002 Daily body mass regulation in dominance- structured coal tit (Parus ater) flocks in response to variable food access: a laboratory study. Behavioral Ecology 13: 696–704. https://doi.org/10.1093/beheco/13.5.696CrossRefGoogle Scholar
Polo, V and Bautista, LM 2006a Daily routines of body mass gain in birds: 1. An exponential model. Animal Behaviour 72: 503–516. https://doi.org/10.1016/j.anbehav.2005.09.024CrossRefGoogle Scholar
Polo, V and Bautista, LM 2006b Daily routines of body mass gain in birds: 2. An experiment with reduced food availability. Animal Behaviour 72: 517–522. https://doi.org/10.1016/j.anbehav.2005.09.025CrossRefGoogle Scholar
Polo, V, Carrascal, LM and Metcalfe, NB 2007 The effects of latitude and day length on fattening strategies of wintering coal tits Periparus ater (L): A field study and aviary experiment. Journal of Animal Ecology 76: 866–872. https://doi.org/10.1111/j.1365-2656.2007.01270.xCrossRefGoogle Scholar
Pravosudov, VV and Grubb, TC 1997 Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply. Behavioral Ecology 8: 332–339. https://doi.org/10.1093/beheco/8.3.332CrossRefGoogle Scholar
Pravosudov, VV and Grubb, TC 1998b Management of fat reserves in tufted titmice Baelophus bicolor in relation to risk of predation. Animal Behaviour 56: 49–54. https://doi.org/10.1006/anbe.1998.0739CrossRefGoogle ScholarPubMed
Pravosudov, VV and Grubb, TCJ 1998a Management of fat reserves in tufted titmice (Parus bicolor): Evidence against a trade-off with food hoards. Behavioral Ecology and Sociobiology 42: 57–62. https://doi.org/10.1007/s002650050411CrossRefGoogle Scholar
Pravosudov, VV, Grubb, TC Jr, Doherty, PF Jr, Pravosudova, EV and Dolby, AS 1999 Social dominance and energy reserves in wintering woodland birds. The Condor 101: 880–884. https://doi.org/10.2307/1370081CrossRefGoogle Scholar
Pravosudov, VV, Kitaysky, AS, Wingfield, JC and Clayton, NS 2001 Long-term unpredictable foraging conditions and physiolog-ical stress response in mountain chickadees (Poecile gambeli). General and Comparative Endocrinology 123: 324–331. https://doi.org/10.1006/gcen.2001.7684CrossRefGoogle ScholarPubMed
Pravosudov, VV and Lucas, JR 2000 The effect of social domi-nance on fattening and food-caching behaviour in Carolina chick-adees, Poecile carolinensis. Animal Behaviour 60: 483–493. https://doi.org/10.1006/anbe.2000.1506CrossRefGoogle Scholar
Rands, SA and Cuthill, IC 2001 Separating the effects of predation risk and interrupted foraging upon mass changes in the blue tit Parus caeruleus. Proceedings of the Royal Society B: Biological Sciences 268: 1783–1790. https://doi.org/10.1098/rspb.2001.1653CrossRefGoogle ScholarPubMed
Remage-Healey, L and Romero, LM 2001 Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. American Journal of Physiology - Regulatory Integrative and Comparative Physiology 281: 994–1003. https://doi.org/10.1152/ajpregu.2001.281.3.R994CrossRefGoogle ScholarPubMed
Rich, EL and Romero, LM 2005 Exposure to chronic stress down-regulates corticosterone responses to acute stressors. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 288: R1628–R1636. https://doi.org/10.1152/ajpregu.00484.2004CrossRefGoogle Scholar
Ricklefs, RE, Konarzewski, M and Daan, S 2018 The relation-ship between basal metabolic rate and daily energy expenditure in birds and mammals. The American Naturalist 147: 1047–1071. https://doi.org/10.1086/285892CrossRefGoogle Scholar
Rintamäki, PT, Stone, JR and Lundberg, A 2003 Seasonal and diurnal body mass fluctuations for two nonhoarding species of parus in Sweden modeled using path analysis. The Auk 120: 658–668. https://doi.org/10.1093/auk/120.3.658CrossRefGoogle Scholar
Rogers, CM 1987 Predation risk and fasting capacity: Do wintering birds maintain optimal body mass? Ecology 68: 1051–1061. https://doi.org/10.2307/1938377CrossRefGoogle Scholar
Rogers, CM 1995 Experimental evidence for temperature-depen-dent winter lipid storage in the dark-eyed junco (Junco hyemalis ore-ganus) and song sparrow (Melospiza melodia morphna). Physiological Zoology 68: 277–289. https://doi.org/10.1086/physzool.68.2.30166504CrossRefGoogle Scholar
Rogers, CM 2015 Testing optimal body mass theory: Evidence for cost of fat in wintering birds. Ecosphere 6: 1–12. https://doi.org/10.1890/ES14-00317.1CrossRefGoogle Scholar
Rogers, CM, Nolan, V Jr and Ketterson, ED 1994 Winter fat-tening in the dark-eyed junco: plasticity and possible interaction with migration trade-offs. Oecologia 97: 526–532. https://doi.org/10.1007/BF00325892CrossRefGoogle ScholarPubMed
Rogers, CM and Reed, AK 2003 Does avian winter fat storage integrate temperature and resource conditions? A long-term study. Journal of Avian Biology 34: 112–118. https://doi.org/10.1034/j.1600-048X.2003.02984.xCrossRefGoogle Scholar
Rogers, CM and Smith, JN 1993 Life-history theory in the non-breeding period: Trade-offs in avian fat reserves. Ecology 74: 419–426. https://doi.org/10.2307/1939303CrossRefGoogle Scholar
Rozman, J, Runciman, D and Zann, RA 2003 Seasonal variation in body mass and fat of Zebra Finches in south-eastern Australia. Emu 103: 11–19. https://doi.org/10.1071/MU02003CrossRefGoogle Scholar
Ruuskanen, S, Morosinotto, C, Thomson, RL, Ratnayake, CP and Korpimäki, E 2017 Food supplementation, but not predation risk, alters female antioxidant status during breeding. Behavioral Ecology and Sociobiology 71: 69. https://doi.org/10.1007/s00265-017-2299-zCrossRefGoogle Scholar
Sapolsky, RM, Romero, LM and Munck, AU 2000 How do glu-cocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21: 55–89. https://doi.org/10.1210/edrv.21.1.0389Google ScholarPubMed
Scheuerlein, A and Ricklefs, RE 2004 Prevalence of blood par-asites in European passeriform birds. Proceedings of the Royal Society B: Biological Sciences 271: 1363–1370. https://doi.org/10.1098/rspb.2004.2726CrossRefGoogle ScholarPubMed
Schmidt, MF 2010a Contributions of bird studies to behavioral and neurobiological research. ILAR Journal 51: 305–309. https://doi.org/10.1093/ilar.51.4.305CrossRefGoogle ScholarPubMed
Schmidt, MF 2010b An IACUC perspective on songbirds and their use in neurobiological research. ILAR Journal 51: 424–430. https://doi.org/10.1093/ilar.51.4.424CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K 1997 Animal Physiology: Adaptation & Environment, Fifth Edition. Cambridge University Press: Cambridge, UK. https://doi.org/10.1017/9780511801822CrossRefGoogle Scholar
Schultner, J, Kitaysky, AS, Welcker, J and Hatch, S 2013 Fat or lean: Adjustment of endogenous energy stores to predictable and unpredictable changes in allostatic load. Functional Ecology 27: 45–55. https://doi.org/10.1111/j.1365-2435.2012.02058.xCrossRefGoogle Scholar
Scott, BB, Velho, TA, Sim, S and Lois, C 2010 Applications of avian transgenesis. ILAR Journal 51: 353–361. https://doi.org/10.1093/ilar.51.4.353CrossRefGoogle ScholarPubMed
Scott, I, Mitchell, PI and Evans, PR 1994 Seasonal changes in body mass, body composition and food requirements in wild migratory birds. Proceedings of the Nutrition Society 53: 521–531. https://doi.org/10.1079/PNS19940062CrossRefGoogle ScholarPubMed
Senar, JC 2002 Great tits (Parus major) reduce body mass in response to wing area reduction: a field experiment. Behavioral Ecology 13: 725–727. https://doi.org/10.1093/beheco/13.6.725CrossRefGoogle Scholar
Smith, RD and Metcalfe, NB 1997 Diurnal, seasonal and altitudinal variation in energy reserves of wintering snow buntings. Journal of Avian Biology 28: 216–222. https://doi.org/10.2307/3676972CrossRefGoogle Scholar
Speakman, JR 2018 The evolution of body fatness: trading off dis-ease and predation risk. The Journal of Experimental Biology 221: jeb167254. https://doi.org/10.1242/jeb.167254CrossRefGoogle Scholar
Thomas, RJ and Cuthill, IC 2002 Body mass regulation and the daily singing routines of European robins. Animal Behaviour 63: 285–295. https://doi.org/10.1006/anbe.2001.1926CrossRefGoogle Scholar
Travers, M, Zanette, LY, Williams, TD, Clinchy, M and Hobson, KA 2013 Food use is affected by the experience of nest predation: implications for indirect predator effects on clutch size. Oecologia 172: 1031–1039. https://doi.org/10.1007/s00442-012-2570-yGoogle Scholar
Ullman-Culleré, MH and Foltz, CJ 1999 Body condition scoring: a rapid and accurate method for assessing health status in mice. Laboratory Animal Science 49: 319–323Google ScholarPubMed
Van Den Hout, PJ, Mathot, KJ, Maas, LRM and Piersma, T 2010 Predator escape tactics in birds: Linking ecology and aerodynamics. Behavioral Ecology 21: 16–25. https://doi.org/10.1093/beheco/arp146CrossRefGoogle Scholar
Van Den Hout, PJ, Piersma, T, Dekinga, A, Lubbe, SK and Henk Visser, G 2006 Ruddy turnstones Arenaria interpres rapidly build pectoral muscle after raptor scares. Journal of Avian Biology 37: 425–430. https://doi.org/10.1111/j.0908-8857.2006.03887.xCrossRefGoogle Scholar
van der Veen, IT 1999 Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella). Behavioral Ecology 10: 545–551. https://doi.org/10.1093/beheco/10.5.545CrossRefGoogle Scholar
van der Veen, ITT and Sivars, LEE 2000 Causes and conse-quences of mass loss upon predator encounter: feeding interruption, stress or fit-for-flight. Functional Ecology 14: 638–664. https://doi.org/10.1046/j.1365-2435.2000.t01-1-00465.xCrossRefGoogle Scholar
Verhulst, S and Hogstad, O 1996 Social dominance and energy reserves in flocks of willow tits. Journal of Avian Biology 27: 203–208. https://doi.org/10.2307/3677223CrossRefGoogle Scholar
Vézina, F, Charlebois, D and Thomas, DW 2009 An automated system for the measurement of mass and identification of birds at perches. Journal of Field Ornithology 72: 211–220. https://doi.org/10.1648/0273-8570-72.2.211CrossRefGoogle Scholar
Wallace, J, Sanford, DJ, Smith, MW and Spencer, KV 1990 The assessment and control of the severity of scientific procedures on laboratory animals. Laboratory Animals 24: 97–130. https://doi.org/10.1258/002367790780890185Google Scholar
Walters, BT, Cheng, TNN, Doyle, J, Guglielmo, CG, Clinchy, M and Zanette, LY 2017 Too important to tamper with: predation risk affects body mass and escape behaviour but not escape ability. Functional Ecology 31: 1405–1417. https://doi.org/10.1111/1365-2435.12851CrossRefGoogle Scholar
Ward, S, Möller, U, Rayner, JMV, Jackson, DM, Nachtigall, W and Speakman, JR 2004 Metabolic power of European starlings Sturnus vulgaris during flight in a wind tunnel, estimated from heat transfer modelling, doubly labelled water and mask respirometry. The Journal of Experimental Biology 207: 4291–4298. https://doi.org/10.1242/jeb.01281CrossRefGoogle Scholar
Wingfield, JC, Maney, DL, Breuner, CW, Jacobs, JD, Lynn, S, Ramenofsky, M and Richardson, RD 1998 Ecological bases of hormone-behavior interactions: The ‘emergency life history stage’. American Zoologist 38: 191–206. https://doi.org/10.1093/icb/38.1.191CrossRefGoogle Scholar
Witter, M, Swaddle, JP and Cuthill, IC 1995 Periodic food availability and strategic regulation of body mass in the European Starling, Sturnus vulgaris. Functional Ecology 9: 568–574. https://doi.org/10.2307/2390146CrossRefGoogle Scholar
Witter, MS and Cuthill, IC 1993 The ecological costs of avian fat storage. Philosophical Transactions of the Royal Society B: Biological Sciences 340: 73–92. https://doi.org/10.1098/rstb.1993.0050Google ScholarPubMed
Witter, MS, Cuthill, IC and Bonser, RHC 1994 Experimental investigations of mass-dependent predation risk in the European starling, Sturnus vulgaris. Animal Behaviour 48: 201–222. https://doi.org/10.1006/anbe.1994.1227CrossRefGoogle Scholar
Witter, MS and Goldsmith, AR 1997 Social stimulation and regulation of body mass in female starlings. Animal Behaviour 54: 279–287. https://doi.org/10.1006/anbe.1996.0443CrossRefGoogle ScholarPubMed
Witter, MS and Swaddle, JP 1995 Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris. Behavioral Ecology 6: 343–348. https://doi.org/10.1093/beheco/6.3.343CrossRefGoogle Scholar
Witter, MS and Swaddle, JP 1997 Mass regulation in juvenile starlings: response to change in food availability depends on initial body mass. Functional Ecology 11: 11–15. https://doi.org/10.1046/j.1365-2435.1997.00041.xCrossRefGoogle Scholar
Yamahachi, H, Zai, AT, Tachibana, RO, Stepien, AE, Rodrigues, DI, Cavé-Lopez, S, Narula, G, Lee, J, Huang, Z, Hörster, H, Düring, D and Hahnloser, RHR 2017 Welfare of zebra finches used in research. bioRxiv: 154567. https://doi.org/10.1101/154567CrossRefGoogle Scholar
Yau, YHC and Potenza, MN 2013 Stress and eating behaviors. Minerva Endocrinologica 38: 255–267Google ScholarPubMed
Zimmer, C, Boos, M, Petit, O and Robin, JP 2010 Body mass variations in disturbed mallards Anas platyrhynchos fit to the mass-dependent starvation-predation risk trade-off. Journal of Avian Biology 41: 637–644. https://doi.org/10.1111/j.1600-048X.2010.05110.xCrossRefGoogle Scholar
Zimmer, C, Boos, M, Poulin, N, Gosler, A, Petit, O and Robin, JP 2011 Evidence of the trade-off between starvation and predation risks in ducks. PLoS ONE 6: e22352. https://doi.org/10.1371/journal.pone.0022352CrossRefGoogle ScholarPubMed
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