Do prolonged fasting periods influence the postprandial metabolic responses in turtles? What can Trachemys scripta elegans teach us about this?


Journal

Journal of experimental zoology. Part A, Ecological and integrative physiology
ISSN: 2471-5646
Titre abrégé: J Exp Zool A Ecol Integr Physiol
Pays: United States
ID NLM: 101710204

Informations de publication

Date de publication:
11 2020
Historique:
received: 16 07 2020
revised: 11 09 2020
accepted: 14 09 2020
pubmed: 1 10 2020
medline: 17 3 2021
entrez: 30 9 2020
Statut: ppublish

Résumé

The postprandial period is characterized by a modification of the gastrointestinal activity after food intake, accompanied by an increase in metabolic rate, secretion of acids, and absorption of nutrients. For ectothermic vertebrates, those changes are particularly prominent given the relatively low metabolic cost and the low frequency of food uptake. However, prolonged fasting periods decrease energy reserves and may compromise the upregulation of costly processes, such as the increase in metabolic rate after resuming the meal intake. Assuming that the main source of energy needed to support such events is provided from the animal's own body reserves, our aim with this study is to test the hypothesis that the longer the period of fasting, the smaller the metabolic rate increase during the postprandial period, since lesser energy reserves trigger these increases. For this, we measured the oxygen consumption rates (V̇O

Identifiants

pubmed: 32996720
doi: 10.1002/jez.2416
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

644-651

Informations de copyright

© 2020 Wiley Periodicals LLC.

Références

Andrade, D. V., Cruz-Neto, A. P., Abe, A. S., & Wang, T. (2005). Specific dynamic action in ectothermic vertebrates: A review of the determinants of postprandial metabolic response in fishes, amphibians, and reptiles. In J. M. Starck, & T. Wang (Eds.), Physiological and Ecological Adaptations to Feeding in Vertebrates (pp. 306-324). Science Publishers.
Angilletta, M. J. Jr. (2006). Estimating and comparing thermal performance curves. Journal of Thermal Biology, 31, 541-545. https://doi.org/10.1016/j.jtherbio.2006.06.002
Avery, H. W., Spotilat, J. R., Congdon, J. D., Fischer, R. U. J., Standora, E. A., & Ave, S. B. (1993). Roles of diet protein and temperature in the growth and nutritional energetics of juvenile slider turtles, Trachemys scripta. Physiological Zoology, 66, 902-925. http://www.jstor.org/stable/30163746?origin=JSTOR-pdf
Beaupre, S. J. (2005). Ratio representations of specific dynamic action (mass-specific SDA and SDA coefficient) do not standardize for body mass and meal size. Physiological and Biochemical Zoology, 78, 126-131. https://doi.org/10.1086/425195
Benedict, F. G. (1932). The physiology of large reptiles with special reference to the heat production of snakes, tortoises, lizards and alligators. Carnegie Institution of Washington Publication, 425, 1-539.
Bjorndal, K. A. (1991). Diet mixing: Nonadditive interactions of diet items in an omnivorous freshwater turtle. Ecology, 72, 1234-1241. https://doi.org/10.2307/1941097
Castoe, T. A., Jason de Koning, A. P., Haal, K. T., Card, D. C., Schield, D. R., Fujita, M. K., Ruggiero, R. P., Degner, J. F., Daza, J. M., Gu, W., Reyes-Velasco, J., Shaney, K. J., Castoe, J. M., Fox, S. E., Poole, A. W., Polanco, D., Dobry, J., Vandewege, M. W., Li, Q., … Pollock, D. D. (2013). The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proceedings of the National Academy of Sciences of the United States of America, 110, 20645-20650. https://doi.org/10.1073/pnas.1314475110
Churchill, T. A., & Storey, K. B. (1992). Responses to freezing exposure of hatchling turtles Trachemys scripta elegans: Factors influencing the development of freeze tolerance by reptiles. Journal of Experimental Biology, 167, 221-233.
Da Silva, R. S. M., & Migliorini, R. H. (1990). Effects of starvation and refeeding on energy- linked metabolic processes in the turtle (Phrynops hilarii). Comparative Biochemistry and Physiology A, 96, 415-419. https://doi.org/10.1016/0300-9629(90)90105-2
Dinkelacker, S. A., Costanzo, J. P., & Lee, R. E. (2005). Anoxia tolerance and freeze tolerance in hatchling turtles. Journal of Comparative Physiology B, 175, 209-217. https://doi.org/10.1007/s00360-005-0478-0
Enok, S., Simonsen, L. S., Funch, P., Kruse, A., Dahlerup, J. F., & Wang, T. (2016). Digestive physiology in reptiles with special reference to pythons. In D. V. Andrade, C. R. Bevier, & J. E. Carvalho (Eds.), Amphibian and reptile adaptations to the environment: Interplay between physiology and behavior (pp. 81-114). CRC Press Taylor & Francis Group. https://doi.org/10.1201/b20420-5
Ernst, C. H., & Barbour, R. W. (1989). Turtles of the world. Smithsonian Institution Press.
Figueiredo, A. C., Barros, F. C., & Carvalho, J. E. (2020). Effects of prolonged fasting on postprandial metabolic rates of Boa constrictor Linnaeus 1758 (Serpentes: Boidae). Herpetology Notes, 13, 621-625.
Garland, T., & Arnold, S. J. (1983). Effects of full stomach on locomotory performance of juvenile garter snakes (Thaminophis elegans). Copeia, 4, 1092-1096. www.jstor.org/stable/1445117
Gavira, R. S. B., & Andrade, D. V. (2013a). Meal size effects on the postprandial metabolic response of Bothrops alternatus (Serpentes: Viperidae). Zoologia, 30, 291-295. https://doi.org/10.1590/S1984-46702013000300005
Gavira, R. S. B., & Andrade, D. V. (2013b). Temperature and thermal regime effects on the specific dynamic action of Bothrops alternatus (Serpentes, Viperidae). Amphibia-Reptilia, 34, 483-491. https://doi.org/10.1163/15685381-00002903
Gessman, J. A., & Nagy, K. A. (1988). Energy metabolism: Errors in gas-exchange conversion factors. Physiological Zoology, 6, 507-513. www.jstor.org/stable/30156159
Greene, H. W. (1992). The ecological and behavioral context for pitviper evolution. In (Ed.) Campbell, J. A., Biology of the Pitvipers (pp. 107-117). New York: Selva Publishing.
Greene, H. W. (1997). Snakes: The evolution of mystery in nature. University of California Press. https://doi.org/10.1002/(sici)1520-6602(1998)1:2<76::aid-inbi7>3.0.co;2-h
Kleiber, M. (1961). The fire of life: An introduction to animal energetics. Wiley. https://doi.org/10.1126/science.134.3495.2033
Krivoruchko, A., & Storey, K. B. (2010). Regulation of the heat shock response under anoxia in the turtle, Trachemys scripta elegans. Journal of Comparative Physiology B, 180, 403-414. https://doi.org/10.1007/s00360-009-0414-9
Lighton, J. R. B. (2008). Measuring metabolic rates-a manual for scientists. Oxford University Press.
Lignot, J., Helmstetter, C., & Secor, S. M. (2005). Postprandial morphological response of the intestinal epithelium of the Burmese python (Python molurus). Comparative Biochemistry and Physiology A, 141, 280-291. https://doi.org/10.1016/j.cbpb.2005.05.005
Lourdais, O., Brischoux, F., DeNardo, D., & Shine, R. (2004). Protein catabolism in pregnant snakes (Epicrates cenchria maurus Boidae) compromises musculature and performance after reproduction. Journal of Comparative Physiology B, 174, 383-391. https://doi.org/10.1007/s00360-004-0424-6
McCue, M. D. (2006). Specific dynamic action: A century of investigation. Comparative Biochemistry and Physiology A, 144, 381-394. https://doi.org/10.1016/j.cbpa.2006.03.011
McCue, M. D. (2007). Western diamondback rattlesnakes demonstrate physiological and biochemical strategies for tolerating prolonged starvation. Physiological and Biochemical Zoology, 80, 25-34. https://doi.org/10.1086/509057
McCue, M. D. (2008). Fatty acid analyses may provide insight into the progression of starvation among squamate reptiles. Comparative Biochemistry and Physiology A, 151, 239-246. https://doi.org/10.1016/j.cbpa.2008.06.034
McCue, M. D. (2010). Starvation physiology: Reviewing the different strategies animals use to survive a common challenge. Comparative Biochemistry and Physiology A, 156, 1-18. https://doi.org/10.1016/j.cbpa.2010.01.002
Milton, S. L., & Prentice, H. M. (2007). Beyond anoxia: The physiology of metabolic downregulation and recovery in the anoxia-tolerant turtle. Comparative Biochemistry and Physiology A, 147, 277-290. https://doi.org/10.1016/j.cbpa.2006.08.041
Moon, D., Owens, D. W., & MacKenzie, D. S. (1999). The effects of fasting and increased feeding on plasma thyroid hormones, glucose, and total protein in sea turtles. Zoological Science, 16, 579-586. https://doi.org/10.2108/zsj.16.579
Oliveira, A. S., Candioto, C. G., Santos, D. M. S., Pereira, J. G., Sousa, A. L., & Machado, C. R. (2013). Effects of fasting and refeeding on the metabolic functions of the turtle Kinosternon scorpioides (Linnaeus, 1766) raised in captivity. Pesquisa Veterinária Brasileira, 33, 1041-1944. https://doi.org/10.1590/s0100-736x2013000800015
Ott, B. D., & Secor, S. M. (2006). The specific dynamic action in boas and pythons. In R. W. Henderson, & R. Powell (Eds.), Biology of the boas and pythons (pp. 299-311). Eagle Mountain Publishing.
Ott, B. D., & Secor, S. M. (2007). Adaptive regulation of digestive performance in the genus Python. Journal of Experimental Biology, 210, 340-356. https://doi.org/10.1242/jeb.02626
Overgaard, J., Andersen, J. B., & Wang, T. (2002). The effects of fasting duration on the metabolic response to feeding in Python molurus: An evaluation of the energetic costs associated with gastrointestinal growth and upregulation. Physiological and Biochemical Zoology, 75, 360-368. https://doi.org/10.1086/342769
Overgaard, J., Busk, M., Hicks, J. W., Jensen, F. B., & Wang, T. (1999). Respiratory consequences of feeding in the snake Python molorus. Comparative Biochemistry and Physiology Part A, 124, 359-365. https://doi.org/10.1016/s1095-6433(99)00127-0
Pan, Z. C., Xiang, J., Lu, H. L., & Ma, X. M. (2005). Metabolic response to feeding in the Chinese striped-necked turtle, Ocadia sinensis. Comparative Biochemistry and Physiology A, 141, 470-475. https://doi.org/10.1016/j.cbpb.2005.07.003
Partata, M. A., & Marques, M. (1994). Effects of fasting and seasonal variations brain glycogen disposition in the turtle (Chrysemys dorbigni). Comparative Biochemistry and Physiology A, 107, 727-730. https://doi.org/10.1016/0300-9629(94)90375-1
Polo-Cavia, N., López, P., & Martín, J. (2010). Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions, 13, 1387-1396. https://doi.org/10.1007/s10530-010-9897-2
Price, E. R. (2016). The physiology of lipid storage and use in reptiles. Biological Reviews, 92, 1406-1426. https://doi.org/10.1111/brv.12288
Riquelme, C. A., Magida, J. A., Harrison, B. C., Wall, C. E., Marr, T. G., Secor, S. M., & Leinwand, L. A. (2011). Fatty acids identified in the burmese python promote beneficial cardiac growth. Science, 334, 528-531. https://doi.org/10.1126/science.1210558
Secor, S. M. (2005). Evolutionary and cellular mechanisms regulating intestinal performance of amphibians and reptiles. Integrative and Comparative Biology, 45, 282-294. https://doi.org/10.1093/icb/45.2.282
Secor, S. M. (2009). Specific dynamic action: A review of the postprandial metabolic response. Journal of Comparative Physiology B, 179, 1-56. https://doi.org/10.1007/s00360-008-0283-7
Secor, S. M., & Carey, H. V. (2016). Integrative physiology of fasting. Comprehensive Physiology, 6, 773-825. https://doi.org/10.1002/cphy.c150013
Secor, S. M., & Diamond, J. (1995). Adaptive responses to feeding in Burmese pythons: Pay before pumping. Journal of Experimental Biology, 198, 1313-1325.
Secor, S. M., & Diamond, J. (1997). Effects of meal size on postprandial responses in juvenile Burmese pythons (Python molurus). The American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 272, 902-912. https://doi.org/10.1152/ajpregu.1997.272.3.r902
Secor, S. M., & Diamond, J. (1999). Maintenance of digestive performance in the turtles Chelydra serpentina, Sternotherus odoratus and Trachemys scripta. Copeia, 1, 75-84. https://doi.org/10.2307/1447387
Secor, S. M., & Diamond, J. (2000). Evolution of regulatory responses to feeding in snakes. Physiological and Biochemical Zoology, 7392, 123-141. https://doi.org/10.1086/316734
Secor, S. M., Fehsenfeld, D., Diamond, J., & Adrian, T. E. (2001). Responses of python gastrointestinal regulatory peptides to feeding. Proceedings of the National Academy of Sciences of the United States of America, 98, 13637-13642. https://doi.org/10.1073/pnas.241524698
Starck, J. M., Moser, P., Werner, R. A., & Linke, P. (2004). Pythons metabolize prey to fuel the response to feeding. Proceedings of the Royal Society, 27, 903-908. https://doi.org/10.1098/rspb.2004.2681
Storey, K. B. (2007). Anoxia tolerance in turtles: Metabolic regulation and gene expression. Comparative Biochemistry and Physiology A, 147, 263-276. https://doi.org/10.1016/j.cbpa.2006.03.019
Stuginski, D., Navas, C. A., Barros, F. C., Camacho, A., Bicudo, J. E. P. W., Grego, K. F., & Carvalho, J. E. (2018). Phylogenetic analysis of standard metabolic rate of snakes: a new proposal for the understanding of interspecific variation in feeding behavior. Journal of Comparative Physiology B, 188, 315-323. https://doi.org/10.1007/s00360-017-1128-z
Stuginski, D., Navas, C. A., Barros, F. C., Grego, K. F., Martins, M., & Carvalho, J. E. (2018). The role of feeding specialization on post-prandial metabolic rate in snakes of the genus Bothrops. Zoological Science, 35, 373-381. https://doi.org/10.2108/zs170058
Tattersall, G. L., Milsom, W. K., Abe, A. S., Brito, S. P., & Andrade, D. V. (2004). The thermogenesis of digestion in rattlesnakes. The Journal of Experimental Biology, 207, 579-585. https://doi.org/10.1242/jeb.00790
Toledo, L. S., Abe, A. S., & Andrade, D. V. (2003). Temperature and meal size effects on the postprandial metabolism and energetics in a boid snake. Physiological and Biochemical Zoology, 76, 240-246. https://doi.org/10.1086/374300
Waas, S., Werner, R. A., & Starck, M. (2010). Fuel switching and energy partitioning during the postprandial metabolic response in the ball python (Python regius). The Journal of Experimental Biology, 213, 1266-1271. https://doi.org/10.1242/jeb.033662
Wallace, B. P., & Jones, T. T. (2008). What makes marine turtles go: A review of metabolic rates and their consequences. Journal of Experimental Marine Biology and Ecology, 356, 8-24. https://doi.org/10.1016/j.jembe.2007.12.023
Wang, T., Hung, C. C. Y., & Randall, D. J. (2006). The comparative physiology of food deprivation: From feast to famine. Annual Review of Physiology, 68, 223-251. https://doi.org/10.1146/annurev.physiol.68.040104.105739
Wang, T., Zaarb, M., Arvedsenb, S., Vedel-Smithb, C., & Overgaard, J. (2003). Effects of temperature on the metabolic response to feeding in Python molurus. Comparative Biochemistry and Physiology, 133, 519-527. https://doi.org/10.1016/s1095-6433(02)00250-7
Zaidan, F., III, & Beaupre, S. J. (2003). Effects of body mass, meal size, fast length, and temperature on specific dynamic action in the timber rattlesnake (Crotalus horridus). Physiological and Biochemical Zoology, 76, 447-458. https://doi.org/10.1086/375661

Auteurs

Aymam C de Figueiredo (AC)

Programa de Pós-Graduação em Ecologia e Evolução, Laboratório de Ecologia, Zoologia e Fisiologia Comparada, Instituto de Ciências Ambientais, Químicas e Farmacêuticas, Universidade Federal de São Paulo, campus Diadema, Diadema, São Paulo, Brazil.

José E de Carvalho (JE)

Programa de Pós-Graduação em Ecologia e Evolução, Laboratório de Ecologia, Zoologia e Fisiologia Comparada, Instituto de Ciências Ambientais, Químicas e Farmacêuticas, Universidade Federal de São Paulo, campus Diadema, Diadema, São Paulo, Brazil.
Departamento de Ecologia e Biologia Evolutiva, Instituto de Ciências Ambientais, Químicas e Farmacêuticas, Universidade Federal de São Paulo, campus Diadema, Diadema, São Paulo, Brazil.

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