Renal efficiency underlies adaptive heterothermy of heat-stressed hypohydrated goats

Abstract

We investigated the thermotolerance of the F1 progeny (Black Bedouin × Damascus crossbreed) to summer conditions alongside that of two pure breeds. Male goats (n = 7 per breed) were used to conduct a summertime 28-day trial along with hypohydration. The animals were fitted with miniscule thermologgers, intraperitoneally and subcutaneously, to measure core (Tc) and peripheral (Tp) body temperatures (BT), respectively. All goats were kept under shaded housing for a 7-day basal period before being switched to unshaded pens for the next 21 days. During the first 14 days, animals had free access to water. However, during the third 7-day period, access to water was time-restricted (4 h/day). Finally, it was restricted to 40% of the third week’s average daily intake over the last 7 days. Exposure to the unshaded conditions resulted in pronounced heat stress in all animals, as reflected by 0.42 and 1.44 °C rises for Tc and Tp, respectively. The F1 goats displayed a clear heterothermic adaptive response, especially after the water restriction bouts’ initiation. Interestingly, the F1 goats displayed higher ratios of renal relative medullary thickness (77.7, 73.3, and 72.6 ± 1.1%) along with higher circulating concentrations of antidiuretic hormone (44.6, 31.6, and 11.6 ± 3.7 ng/mL), respectively, which suggested an improved water metabolism.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Abbott, S.B.G., Machado, N.L.S., Geerling, J.C., and Saper, C.B., 2016. Reciprocal Control of Drinking Behavior by Median Preoptic Neurons in Mice, The Journal of neuroscience : the official journal of the Society for Neuroscience, 36, 8228–8237

    Article  CAS  Google Scholar 

  2. Al-Tamimi, H., 2006. Responses of core and peripheral temperatures to chronic cold stress in transiently goitrous goats, Journal of Thermal Biology, 31, 626–633

    Article  Google Scholar 

  3. Al-Tamimi, H.J., 2007a. Responses of simultaneously recorded intraperitoneal and subcutaneous temperatures of Black Bedouin goats to transient thyrosuppression during cold stress, Livestock Science, 106, 254–260

    Article  Google Scholar 

  4. Al-Tamimi, H.J., 2007b. Thermoregulatory response of goat kids subjected to heat stress, Small Ruminant Research, 71, 280–285

    Article  Google Scholar 

  5. Al-Tamimi, H.J., Obeidat, B.S., Abdullah, A.Y., and Atiyat, R.M., 2013. Disproportionate thermophysiological strain between intensively-and extensively-managed goats during summer, Small Ruminant Research, 109, 1–8

    Article  Google Scholar 

  6. Casey, T.M., Plaut, K., Kalyesubula, M., Shamay, A., Sabastian, C., Wein, Y., Bar-Shira, E., Reicher, N., and Mabjeesh, S.J., 2018. Mammary core clock gene expression is impacted by photoperiod exposure during the dry period in goats, Journal of Applied Animal Research, 46, 1214–1219

    Article  Google Scholar 

  7. Dmi'el, R., and Robertshaw, D., 1983. The Control of Panting and Sweating in the Black Bedouin Goat: A Comparison of Two Modes of Imposing a Heat Load, Physiological Zoology, 56, 404–411

    Article  Google Scholar 

  8. Donald, J., and Pannabecker, T.L., 2015. Osmoregulation in Desert-Adapted Mammals. In: K.A. Hyndman and T.L. Pannabecker (eds), Sodium and Water Homeostasis: Comparative, Evolutionary and Genetic Models, 2015, (Springer New York, New York), 191–211

    Google Scholar 

  9. Fuller, A., Moss, D.G., Skinner, J.D., Jessen, P.T., Mitchell, G., and Mitchell, D., 1999. Brain, abdominal and arterial blood temperatures of free-ranging eland in their natural habitat, Pflügers Archiv, 438, 671–680

    Article  CAS  PubMed  Google Scholar 

  10. Fuller, A., Maloney, S.K., Mitchell, G., and Mitchell, D., 2004. The eland and the oryx revisited: body and brain temperatures of free-living animals, International Congress Series, 1275, 275–282

    Article  Google Scholar 

  11. Gansloßer, U., and Jann, G., 2019. Thermoregulation in Animals: Some Fundamentals of Thermal Biology☆. In: B. Fath (ed), Encyclopedia of Ecology (Second Edition), 2019, (Elsevier, Oxford), 328–336

    Google Scholar 

  12. Gill, G.L., and Hafs, H.D., 1971. Analysis of repeated measures of animals, Journal of Animal Science, 33, 331–336

    Article  CAS  PubMed  Google Scholar 

  13. Jessen, C., 1977. Interaction of air temperature and core temperatures in thermoregulation of the goat, The Journal of Physiology, 264, 585–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kumar, D., De, K., Singh, A.K., Kumar, K., Sahoo, A., and Naqvi, S.M.K., 2016. Effect of water restriction on physiological responses and certain reproductive traits of Malpura ewes in a semiarid tropical environment, Journal of Veterinary Behavior, 12, 54–59

    Article  Google Scholar 

  15. Li, F., Yang, Y., Jenna, K., Xia, C., Lv, S., and Wei, W., 2018. Effect of heat stress on the behavioral and physiological patterns of Small-tail Han sheep housed indoors, Tropical Animal Health and Production, 50, 1893–1901

    Article  CAS  PubMed  Google Scholar 

  16. Littell, R.C., Henry, P.R., and Ammerman, C.B., 1998. Statistical analysis of repeated measures data using SAS procedures, Journal of Animal Science, 76, 1216–1231

    Article  CAS  PubMed  Google Scholar 

  17. McKinley, M., Trevaks, D., Weissenborn, F., and McAllen, R., 2017. Interaction between thermoregulation and osmoregulation in domestic animals, Brazilian Journal of Animal Science, 46, 8

    Google Scholar 

  18. Mitchell, D., Maloney, S.K., Jessen, C., Laburn, H.P., Kamerman, P.R., Mitchell, G., and Fuller, A., 2002. Adaptive heterothermy and selective brain cooling in arid-zone mammals, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 131, 571–585

    Article  Google Scholar 

  19. Moran, D.S., Pandolf, K.B., Heled, Y., and Gonzalez, R.R., 2004. Evaluation of the environmental stress index (ESI) for different terrestrial elevations below and above sea level, Journal of Thermal Biology, 29, 291–297

    Article  Google Scholar 

  20. Ribeiro, M.N., Ribeiro, N.L., Bozzi, R., and Costa, R.G., 2018. Physiological and biochemical blood variables of goats subjected to heat stress – a review, Journal of Applied Animal Research, 46, 1036–1041

    Article  CAS  Google Scholar 

  21. Romanovsky, A.A., 2014. Skin temperature: its role in thermoregulation, Acta Physiologica, 210, 498–507

    Article  CAS  PubMed  Google Scholar 

  22. Rout, P.K., Kaushik, R., and Ramachandran, N., 2016. Differential expression pattern of heat shock protein 70 gene in tissues and heat stress phenotypes in goats during peak heat stress period, Cell Stress Chaperones, 21, 645–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. SAS Institute Inc, SAS 9.1.3 Help and Documentation, Cary, NC: SAS Institute Inc., 2002–2004.

  24. Schmidt-Nielsen, K., Schmidt-Nielsen, B., Jarnum, S.A., and Houpt, T.R., 1956. Body Temperature of the Camel and Its Relation to Water Economy, American Journal of Physiology-Legacy Content, 188, 103–112

    Article  Google Scholar 

  25. Urity, V.B., Issaian, T., Braun, E.J., Dantzler, W.H., and Pannabecker, T.L., 2012. Architecture of kangaroo rat inner medulla: segmentation of descending thin limb of Henle's loop, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 302, R720-R726

    Article  CAS  PubMed  Google Scholar 

  26. Yaqub, L.S., Ayo, J.O., Kawu, M.U., and Rekwot, P.I., 2017. Diurnal thermoregulatory responses in pregnant Yankasa ewes to the dry season in a tropical Savannah, Tropical Animal Health and Production, 49, 1243–1252

    Article  PubMed  Google Scholar 

  27. Yates, D.T., Salisbury, M.W., Ross, T.T., and Anderson, H., 2010. Effects of Tasco-14 Supplementation on Growth and Fertility Traits in Young Male Boer Goats Experiencing Heat Stress, The Texas Journal of Agriculture and Natural Resources, 23, 12–18

    Google Scholar 

  28. Zimmerman, C.A., Lin, Y.C., Leib, D.E., Guo, L., Huey, E.L., Daly, G.E., Chen, Y., and Knight, Z.A., 2016. Thirst neurons anticipate the homeostatic consequences of eating and drinking, Nature, 537, 680–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Utmost gratitude is extended to the staff in the Agricultural Experimental Station, College of Agriculture at Mutah University, for the help to facilitate the experimental work.

Funding

This project was funded by the Scientific Research Fund at the Ministry of Research and Higher Education in Jordan and the Deanship of Academic Research at Mutah University, Karak-Jordan (Grant number A.V./2/25/2008).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hosam Al-Tamimi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of animal rights

All described experimental procedures were pre-approved by the Animal Care and Use Committee at Mutah University, and were in line with the regulations of all institutional and national guidelines for the care and use of research animals.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Al-Tamimi, H., Al-Atiyat, R., Al-Majali, A. et al. Renal efficiency underlies adaptive heterothermy of heat-stressed hypohydrated goats. Trop Anim Health Prod 51, 2287–2295 (2019). https://doi.org/10.1007/s11250-019-01948-5

Download citation

Keywords

  • Goat
  • Hyperthermia
  • Thermoregulation
  • Heat stress
  • Hypohydration
  • Heterothermy