Short term effects of restricted food availability and peripheral leptin injections in redheaded bunting, Emberiza bruniceps
Article Main
Abstract
Migratory birds need continued food supply and efficient metabolic machinery to meet high energy demands of the magnanimous feat of flight. Two questions are important i.e. as to 1) how a bird adapts to a temporary food constrain on a daily basis, and 2) how peripheral leptin, an anorectic hormone, impacted feeding and migratory behaviour in buntings? The aim of this study was to induce a non-photoperiodic tweak in the physiology of redheaded buntings through exogenous leptin administration and study its effect on their food intake and migratory behaviour. Groups of male redheaded buntings, Emberiza bruniceps (n=17) were transferred from short (8L: 16D) to long (16L: 8D) days and presented with food only either for first (morning food presence, MFP) or second (evening food presence, EFP) half of the 16h lighted phase, while control group received food ad libitum. Total daily food intake (FI) did not differ significantly between the MFP, EFP and controls, but hourly FI in MFP and EFP indicated increased activity differences based on time of food availability and bird’s tendency to cache food/ recompense for food scarcity during migration. In another experiment, a chemical tweak in bird’s FI was induced by peripheral administration of leptin, to add to current understanding of transition in buntings’ metabolic efficiency during high energy demanding migratory journey. Exogenous leptin appeared to safeguard cadaveric effect of exogenous injection in migrating buntings through promoting blood cholesterol and reduced liver fibrosis. Food restriction in the morning was better responded by buntings than that in evening. Therefore, migratory buntings exhibited diurnal variation in response to food scarcity.
Article Details
Article Details
Keywords
Activity, Food, Leptin, Migration, Restriction
References
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Boswell, T. & Dunn, I. C. (2015). Regulation of the avian central melanocortin system and the role of leptin. General and Comparative Endocrinology, 221, 278–283. doi.org/10.1016/j.ygcen.2014.12.009
Budki, P., Rani, S. & Kumar, V. (2009). Food deprivation during photosensitive and photorefractory life-history stages affects the reproductive cycle in the migratory Red-headed Bunting (Emberiza bruniceps). The Journal of Experimental Biology, 212(2), 225–230. doi.org/10.1242/jeb.024190
Cerasale, D. J., Zajac, D. M. & Guglielmo, C. G. (2011). Behavioral and physiological effects of photoperiod-induced migratory state and leptin on a migratory bird, Zonotrichia albicollis: I. Anorectic effects of leptin administration. General and Comparative Endocrinology, 174(3), 276–286. doi.org/10.1016/j.ygcen.2011.08.025
Das, S. & Gupta, N. J. (2016). Seasonal modulation of diurnal food consumption in Indian songbirds. Biological Rhythm Research, 47(4), 621-629. doi.org/10.10 80/09291016.2016.1178415
Ferretti, A., Maggini, I., Lupi, S., Cardinale, M. & Fusani, L. (2019). The amount of available food affects diurnal locomotor activity in migratory songbirds during stopover. Scientific Reports, 9(1), 19027. doi.org/10.1038/s41598-019-55404-3
Friedman-Einat, M. & Seroussi, E. (2019). Avian Leptin: Bird's-Eye View of the Evolution of Vertebrate Energy-Balance Control. Trends in Endocrinology and Metabolism: TEM, 30(11), 819–832. doi.org/10.1016/j.t em.2019.07.007
Fusani, L., Coccon, F., Rojas Mora, A. & Goymann, W. (2013). Melatonin reduces migratory restlessness in Sylvia warblers during autumnal migration. Frontiers in Zoology, 10(1), 79. doi.org/10.1186/1742-9994-10-79
Gill, S. & Panda, S. (2011). Feeding mistiming decreases reproductive fitness in flies. Cell Metabolism, 13(6), 613–614. doi.org/10.1016/j.cmet.2011.05.003
Goymann, W., Lupi, S., Kaiya, H., Cardinale, M. & Fusani, L. (2017). Ghrelin affects stopover decisions and food intake in a long-distance migrant. Proceedings of the National Academy of Sciences of the United States of America, 114(8), 1946–1951. doi.org/10.1073/pnas.1619565114
Gupta, N. J. & Kumar, V. (2013). Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting. Animal Biology, 63, 321-329.
Gupta, N. J., Nanda, R. K., Das, S., Das, M. K. & Arya, R. (2020). Night migratory songbirds exhibit metabolic ability to support high aerobic capacity during migration. ACS Omega, 5(43), 28088–28095. doi.org/10.1021/acsomega.0c03691
Hen, G., Yosefi, S., Ronin, A., Einat, P., Rosenblum, C. I., Denver, R. J. & Friedman-Einat, M. (2008). Monitoring leptin activity using the chicken leptin receptor. The Journal of Endocrinology, 197(2), 325–333. doi.org/10.1677/JOE-08-0065
Henderson, L. J., Cockcroft, R. C., Kaiya, H., Boswell, T. & Smulders, T. V. (2018). Peripherally injected ghrelin and leptin reduce food hoarding and mass gain in the coal tit (Periparus ater). Proceedings. Biological Sciences, 285(1879), 20180417. doi.org/10.1098/rspb.2018.0417
Jain, N. & Kumar, V. (1995). Changes in food intake, body weight, gonads and plasma concentrations of thyroxine, luteinizing hormone and testosterone in captive buntings exposed to natural day lengths at 29◦ N. Journal of Biosciences, 20, 417-426.
Kaiya, H., Furuse, M., Miyazato, M. & Kangawa, K. (2009). Current knowledge of the roles of ghrelin in regulating food intake and energy balance in birds. General and Comparative Endocrinology, 163(1-2), 33–38. doi.org/10.1016/j.ygcen.2008.11.008
Klaassen M. (1996). Metabolic constraints on long-distance migration in birds. The Journal of Experimental Biology, 199 (1), 57-64.
Kochan, Z., Karbowska, J. & Meissner, W. (2006). Leptin is synthesized in the liver and adipose tissue of the dunlin (Calidris alpina). General and Comparative Endocrinology, 148(3), 336–339. doi.org/10.1016/j.ygcen.2006.04.004
Krause, J. S., Pérez, J. H., Meddle, S. L. & Wingfield, J. C. (2017). Effects of short-term fasting on stress physiology, body condition, and locomotor activity in wintering male white-crowned sparrows. Physiology & Behavior, 177, 282–290. doi.org/10.1016/j.physbeh.2017.04.026
Kumar, V., Singh, S., Misra, M. & Malik, S. (2001). Effects of duration and time of food availability on photoperiodic responses in the migratory male blackheaded bunting (Emberiza melanocephala). The Journal of Experimental Biology, 204(16), 2843–2848.
Kurokawa, T. & Ohkohchi, N. (2017). Platelets in liver disease, cancer and regeneration. World Journal of Gastroenterology, 23(18), 3228–3239. doi.org/10.3748/wjg.v23.i18.3228
Landys, M. M., Piersma, T., Guglielmo, C. G., Jukema, J., Ramenofsky, M. & Wingfield, J. C. (2005). Metabolic profile of long-distance migratory flight and stopover in a shorebird. Proceedings. Biological Sciences, 272(1560), 295–302. doi.org/10.1098/rspb.2004.2952
Lõhmus, M. & Björklund, M. (2009). Leptin affects life history decisions in a passerine bird: a field experiment. PLOS One, 4(2), e4602. doi.org/10.1371/journal.po ne.0004602
Lõhmus, M., Sandberg, R., Holberton, R. L. & Moore, F. R. (2003). Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus). Behavioral Ecology and Sociobiology, 54, 233–239. doi.org/10.1007/s00265-003-0618-z
Lynn, S. E., Breuner, C. W. & Wingfield, J. C. (2003). Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Hormones and Behavior, 43(1), 150–157. doi.org/10.1016/s0018-506x(02)00023-5
Malik, S., Rani, S. & Kumar, V. (2004). Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting (Emberiza melanocephala). Chronobiology International, 21(3), 367–384. doi.org/10.1081/cbi-120038742
McWilliams, S. R., Guglielmo, C., Pierce, B. & Klaassen, M. (2004). Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. Journal of Avian Biology, 35(5), 377-393. doi.org/10.1111/j.0908-8857.2004.03378.x
Misra, I. (2016). Mechanism of adaptation for breeding in opportunistic, atypical photosensitive and photoperiodic songbirds. PhD Thesis submitted to Delhi University, India.
Morton, M. L. (1967). Diurnal Feeding Patterns in White-crowned Sparrows, Zonotrichia leucophrys gambelii. Condor, 69(5), 491-512.
Myers, S., Bowden, R., Tumian, A., Bontrop, R. E., Freeman, C., MacFie, T. S., McVean, G. & Donnelly, P. (2010). Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science, 327(5967), 876–879. doi.org/10.1126/science.1182363
Perfito, N., Kwong, J. M., Bentley, G. E. & Hau, M. (2008). Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)?. Hormones and Behavior, 53(4), 567–572. doi.org/10.1016/j.yhbeh.2008.01.002
Prabhat, A., Batra, T. & Kumar, V. (2020). Effects of timed food availability on reproduction and metabolism in zebra finches: Molecular insights into homeostatic adaptation to food-restriction in diurnal vertebrates. Hormones and Behavior, 125, 104820. doi.org/10.1016/j.yhbeh.20 20.10 4820
Rees, E. C. (1982). The effect of photoperiod on the timing of spring migration in the Bewick’s Swan. Wildfowl, 33, 119-132.
Seroussi, E., Knytl, M., Pitel, F., Elleder, D., Krylov, V., Leroux, S., Morisson, M., Yosefi, S., Miyara, S., Ganesan, S., Ruzal, M., Andersson, L. & Friedman-Einat, M. (2019). Avian Expression Patterns and Genomic Mapping Implicate Leptin in Digestion and TNF in Immunity, Suggesting That Their Interacting Adipokine Role Has Been Acquired Only in Mammals. International Journal of Molecular Sciences, 20(18), 4489. doi.org/10.3390/ijms20184489
William, W. N., Jr, Ceddia, R. B. & Curi, R. (2002). Leptin controls the fate of fatty acids in isolated rat white adipocytes. The Journal of Endocrinology, 175(3), 735–744. doi.org/10.1677/joe.0.1750735
Yosefi, S., Hen, G., Rosenblum, C. I., Cerasale, D. J., Beaulieu, M., Criscuolo, F. & Friedman-Einat, M. (2010). Lack of leptin activity in blood samples of Adélie penguin and bar-tailed godwit. The Journal of Endocrinology, 207(1), 113–122. doi.org/10.1677/JOE-10-0177
Bhardwaj, S. K. & Anushi (2004). The effect of duration and time of food availability on the photoperiodic response in the male house sparrow, Passer domesticus. Reproduction, Nutrition, Development, 44(1), 29–35. doi.org/10.1051/rnd:2004014
Boswell, T. & Dunn, I. C. (2015). Regulation of the avian central melanocortin system and the role of leptin. General and Comparative Endocrinology, 221, 278–283. doi.org/10.1016/j.ygcen.2014.12.009
Budki, P., Rani, S. & Kumar, V. (2009). Food deprivation during photosensitive and photorefractory life-history stages affects the reproductive cycle in the migratory Red-headed Bunting (Emberiza bruniceps). The Journal of Experimental Biology, 212(2), 225–230. doi.org/10.1242/jeb.024190
Cerasale, D. J., Zajac, D. M. & Guglielmo, C. G. (2011). Behavioral and physiological effects of photoperiod-induced migratory state and leptin on a migratory bird, Zonotrichia albicollis: I. Anorectic effects of leptin administration. General and Comparative Endocrinology, 174(3), 276–286. doi.org/10.1016/j.ygcen.2011.08.025
Das, S. & Gupta, N. J. (2016). Seasonal modulation of diurnal food consumption in Indian songbirds. Biological Rhythm Research, 47(4), 621-629. doi.org/10.10 80/09291016.2016.1178415
Ferretti, A., Maggini, I., Lupi, S., Cardinale, M. & Fusani, L. (2019). The amount of available food affects diurnal locomotor activity in migratory songbirds during stopover. Scientific Reports, 9(1), 19027. doi.org/10.1038/s41598-019-55404-3
Friedman-Einat, M. & Seroussi, E. (2019). Avian Leptin: Bird's-Eye View of the Evolution of Vertebrate Energy-Balance Control. Trends in Endocrinology and Metabolism: TEM, 30(11), 819–832. doi.org/10.1016/j.t em.2019.07.007
Fusani, L., Coccon, F., Rojas Mora, A. & Goymann, W. (2013). Melatonin reduces migratory restlessness in Sylvia warblers during autumnal migration. Frontiers in Zoology, 10(1), 79. doi.org/10.1186/1742-9994-10-79
Gill, S. & Panda, S. (2011). Feeding mistiming decreases reproductive fitness in flies. Cell Metabolism, 13(6), 613–614. doi.org/10.1016/j.cmet.2011.05.003
Goymann, W., Lupi, S., Kaiya, H., Cardinale, M. & Fusani, L. (2017). Ghrelin affects stopover decisions and food intake in a long-distance migrant. Proceedings of the National Academy of Sciences of the United States of America, 114(8), 1946–1951. doi.org/10.1073/pnas.1619565114
Gupta, N. J. & Kumar, V. (2013). Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting. Animal Biology, 63, 321-329.
Gupta, N. J., Nanda, R. K., Das, S., Das, M. K. & Arya, R. (2020). Night migratory songbirds exhibit metabolic ability to support high aerobic capacity during migration. ACS Omega, 5(43), 28088–28095. doi.org/10.1021/acsomega.0c03691
Hen, G., Yosefi, S., Ronin, A., Einat, P., Rosenblum, C. I., Denver, R. J. & Friedman-Einat, M. (2008). Monitoring leptin activity using the chicken leptin receptor. The Journal of Endocrinology, 197(2), 325–333. doi.org/10.1677/JOE-08-0065
Henderson, L. J., Cockcroft, R. C., Kaiya, H., Boswell, T. & Smulders, T. V. (2018). Peripherally injected ghrelin and leptin reduce food hoarding and mass gain in the coal tit (Periparus ater). Proceedings. Biological Sciences, 285(1879), 20180417. doi.org/10.1098/rspb.2018.0417
Jain, N. & Kumar, V. (1995). Changes in food intake, body weight, gonads and plasma concentrations of thyroxine, luteinizing hormone and testosterone in captive buntings exposed to natural day lengths at 29◦ N. Journal of Biosciences, 20, 417-426.
Kaiya, H., Furuse, M., Miyazato, M. & Kangawa, K. (2009). Current knowledge of the roles of ghrelin in regulating food intake and energy balance in birds. General and Comparative Endocrinology, 163(1-2), 33–38. doi.org/10.1016/j.ygcen.2008.11.008
Klaassen M. (1996). Metabolic constraints on long-distance migration in birds. The Journal of Experimental Biology, 199 (1), 57-64.
Kochan, Z., Karbowska, J. & Meissner, W. (2006). Leptin is synthesized in the liver and adipose tissue of the dunlin (Calidris alpina). General and Comparative Endocrinology, 148(3), 336–339. doi.org/10.1016/j.ygcen.2006.04.004
Krause, J. S., Pérez, J. H., Meddle, S. L. & Wingfield, J. C. (2017). Effects of short-term fasting on stress physiology, body condition, and locomotor activity in wintering male white-crowned sparrows. Physiology & Behavior, 177, 282–290. doi.org/10.1016/j.physbeh.2017.04.026
Kumar, V., Singh, S., Misra, M. & Malik, S. (2001). Effects of duration and time of food availability on photoperiodic responses in the migratory male blackheaded bunting (Emberiza melanocephala). The Journal of Experimental Biology, 204(16), 2843–2848.
Kurokawa, T. & Ohkohchi, N. (2017). Platelets in liver disease, cancer and regeneration. World Journal of Gastroenterology, 23(18), 3228–3239. doi.org/10.3748/wjg.v23.i18.3228
Landys, M. M., Piersma, T., Guglielmo, C. G., Jukema, J., Ramenofsky, M. & Wingfield, J. C. (2005). Metabolic profile of long-distance migratory flight and stopover in a shorebird. Proceedings. Biological Sciences, 272(1560), 295–302. doi.org/10.1098/rspb.2004.2952
Lõhmus, M. & Björklund, M. (2009). Leptin affects life history decisions in a passerine bird: a field experiment. PLOS One, 4(2), e4602. doi.org/10.1371/journal.po ne.0004602
Lõhmus, M., Sandberg, R., Holberton, R. L. & Moore, F. R. (2003). Corticosterone levels in relation to migratory readiness in red-eyed vireos (Vireo olivaceus). Behavioral Ecology and Sociobiology, 54, 233–239. doi.org/10.1007/s00265-003-0618-z
Lynn, S. E., Breuner, C. W. & Wingfield, J. C. (2003). Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Hormones and Behavior, 43(1), 150–157. doi.org/10.1016/s0018-506x(02)00023-5
Malik, S., Rani, S. & Kumar, V. (2004). Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting (Emberiza melanocephala). Chronobiology International, 21(3), 367–384. doi.org/10.1081/cbi-120038742
McWilliams, S. R., Guglielmo, C., Pierce, B. & Klaassen, M. (2004). Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. Journal of Avian Biology, 35(5), 377-393. doi.org/10.1111/j.0908-8857.2004.03378.x
Misra, I. (2016). Mechanism of adaptation for breeding in opportunistic, atypical photosensitive and photoperiodic songbirds. PhD Thesis submitted to Delhi University, India.
Morton, M. L. (1967). Diurnal Feeding Patterns in White-crowned Sparrows, Zonotrichia leucophrys gambelii. Condor, 69(5), 491-512.
Myers, S., Bowden, R., Tumian, A., Bontrop, R. E., Freeman, C., MacFie, T. S., McVean, G. & Donnelly, P. (2010). Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science, 327(5967), 876–879. doi.org/10.1126/science.1182363
Perfito, N., Kwong, J. M., Bentley, G. E. & Hau, M. (2008). Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)?. Hormones and Behavior, 53(4), 567–572. doi.org/10.1016/j.yhbeh.2008.01.002
Prabhat, A., Batra, T. & Kumar, V. (2020). Effects of timed food availability on reproduction and metabolism in zebra finches: Molecular insights into homeostatic adaptation to food-restriction in diurnal vertebrates. Hormones and Behavior, 125, 104820. doi.org/10.1016/j.yhbeh.20 20.10 4820
Rees, E. C. (1982). The effect of photoperiod on the timing of spring migration in the Bewick’s Swan. Wildfowl, 33, 119-132.
Seroussi, E., Knytl, M., Pitel, F., Elleder, D., Krylov, V., Leroux, S., Morisson, M., Yosefi, S., Miyara, S., Ganesan, S., Ruzal, M., Andersson, L. & Friedman-Einat, M. (2019). Avian Expression Patterns and Genomic Mapping Implicate Leptin in Digestion and TNF in Immunity, Suggesting That Their Interacting Adipokine Role Has Been Acquired Only in Mammals. International Journal of Molecular Sciences, 20(18), 4489. doi.org/10.3390/ijms20184489
William, W. N., Jr, Ceddia, R. B. & Curi, R. (2002). Leptin controls the fate of fatty acids in isolated rat white adipocytes. The Journal of Endocrinology, 175(3), 735–744. doi.org/10.1677/joe.0.1750735
Yosefi, S., Hen, G., Rosenblum, C. I., Cerasale, D. J., Beaulieu, M., Criscuolo, F. & Friedman-Einat, M. (2010). Lack of leptin activity in blood samples of Adélie penguin and bar-tailed godwit. The Journal of Endocrinology, 207(1), 113–122. doi.org/10.1677/JOE-10-0177
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Short term effects of restricted food availability and peripheral leptin injections in redheaded bunting, Emberiza bruniceps. (2021). Journal of Applied and Natural Science, 13(4), 1430-1436. https://doi.org/10.31018/jans.v13i4.3139
