Thermal biology in river buffalo in the humid tropics: neurophysiological and behavioral responses assessed by infrared thermography
Daniel Mota-Rojas, Fabio Napolitano, Ada Braghieri, Isabel Guerrero-Legarreta, Aldo Bertoni, Julio Martínez-Burnes, Rosy Cruz-Monterrosa, Jocelyn Gómez, Efren Ramírez-Bribiesca, Hugo Barrios-García, Nancy José, Adolfo Álvarez, Patricia Mora-Medina, Agustín Orihuela
Abstract
The present review aims to analyze the effect of extremely hot climates on the neurophysiological responses of thermal control and behavior in the river buffalo. Understanding thermal neuromodulation and its effects on the buffalo’s behavior is of central importance, for this will allow us to make better decisions in terms of improving the level of welfare of buffaloes living in environments characterized by extreme heat, such as the humid tropics. The thermoregulation process involves a complex mechanism that begins with the integration of peripheral signals that are sent to the lateral parabrachial nucleus of the brainstem and then to the preoptic nucleus of the hypothalamus to generate physiological variations such as vasodilatation to dissipate heat under conditions of thermal stress, or vasoconstriction to conserve heat upon the perception of cold stimuli. The thermal biology of the river buffalo is based on several different adaptation mechanisms. The infrared thermography (IRT) technique will be of great help in this area because it permits the detection of vascular microcirculation changes in different thermal windows under adverse climatic conditions. Although buffaloes are classified as rustic animals, it is important to take into account their morpho-physiology and thermoregulation mechanisms to prevent thermal stress and the resulting poor welfare and reduced productivity. However, if appropriate thermoregulation facilities are provided (i.e., ponds, pools, potholes, or swampy areas), buffaloes can properly thermoregulate and tolerate high ambient temperatures. Therefore, they may represent a good option and an appropriate animal-based enterprise under climate change and global warming conditions.
Keywords
References
Ablas DDS, Titto EAL, Pereira AMF, Titto CG, da Cunha Leme T (2007) Comportamento de Bubalinos a pasto frente a disponibilidade de sombra e água para imersão. Ciência Animal Brasileira 8:167-175.
Aggarwal A, Upadhyay R (2013) Stress, heat productivity, animal. In: Stress, heat productivity, animal. Springer-Verlag, pp 1-25.
Barros DV, Silva LKX, Kahwage PR, Laurenco Junior JB, Dousa JS, Franco IM, Martorano LG, Garcia AR (2016) Assessment of surface temperatures of buffalo bulls (Bubalus bubalis) raised under tropical conditions using infrared thermography. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 68:422-430.
Batchelder P, Kinney RO, Demlow L, Lynch CB (1983) Effects of temperature and social interactions on huddling behavior in Mus musculus. Physiology and Behaviour 31:97-102.
Berdugo-Gutiérrez J., Napolitano F., Mota-Rojas (2018) El Búfalo de Agua y el Estrés Calórico - BM Editores. In: Spec. Sect. Let’s Learn Anim. Welf. together. BM Ed. Press. Mex. City. Mex. https://bmeditores.mx/secciones-especiales/el-bufalo-de-agua-y-el-estres-calorico-1877/. Accessed 13 Aug 2019.
Bertoni A, Álvarez-Macias A, Mota-Rojas D (2019) Productive performance of buffaloes and their development options in tropical regions. Sociedades Rurales Producción y Medio Ambiente 19:59-80.
Bertoni A, Napolitano F, Mota-Rojas D, Sabia E, Alvarez A, Mora P, Morales A, Berdugo J, Guerrero-Legarretra I (2020a) Similarities and differences between river buffaloes and cattle: health, physiological, behavioural and productivity aspects. Journal of Buffalo Science 9:92-109.
Bertoni A, Mota-Rojas D, Álvarez-Macias A, Mora-Medina P, Guerrero-Legarreta I, Morales-Canela A, Gómez-Prado J, José-Pérez N, Martínez-Burnes J (2020b) Scientific findings related to changes in vascular microcirculation using infrared thermography in the river buffalo. Journal of Animal Behaviour and Biometeorology 8:288-297.
Bradley G. (2013) Cunningham’s Textbook of Veterinary Physiology, Fifth ed. Elsevier, Spain.
Casas-Alvarado A, Mota-Rojas D, Hernández-Ávalos I, Mora P, Olmos HÁ, Verduzco A, Reyes B, Martínez-Burnes J (2020) Advances in infrared thermography: Surgical aspects, vascular changes, and pain monitoring in veterinary medicine. Journal of Thermal Biology 92:102664.
Castro AC, Lourenço Júnior J de B, Santos N de FA dos (2008) Sistema silvipastoril na Amazônia: ferramenta para elevar o desempenho produtivo de búfalos. Ciência Rural 38:2395-2402.
Church JS, Hegadoren PR, Paetkau MJ, Miller CC, Regev-Shoshani G, Schaefer AL, Schwartzkopf-Genswein KS (2014) Influence of environmental factors on infrared eye temperature measurements in cattle. Research in Veterinary Science 96:220-226.
Cravello B, Ferri A (2008) Relationships between skin properties and environmental parameters. Skin Research and Technology 14:180-186.
Cruz-Monterrosa RG, Mota-Rojas D, Ramírez-Bibriesca E, Mora-Medina P, Guerrero-Legarreta I (2020) Scientific findings on the quality of river buffalo meat and it's prospects for future studies. Journal of Buffalo Science 9:170-180.
Das KS, Singh G, Paul SS, Malik R, Oberoi P, Deb S (2011) Physiological responses and performance of Nili-Ravi buffalo calves under different washing frequency during hot summer months in tropics. Tropical Animal Health and Production 43:35-39.
Das S., Upadhyay R., Madan M. (1999) Heat stress in Murrah buffalo calves. Livest Prod Sci 61:71-78.
De Rosa G, Grasso F, Braghieri A, Bilancione A, Di Francia A, Napolitano F (2009) Behavior and milk production of buffalo cows as affected by housing system. Journal of Dairy Science 92:907-912.
De Rosa G, Napolitano F, Grasso F, Pacelli C, Borde A (2005) On the development of a monitoring scheme of buffalo welfare at farm level. Italian Journal of Animal Science 4:115-125.
Dimri U, Ranjan R, Sharma MC, Varshney VP (2010) Effect of vitamin E and selenium supplementation on oxidative stress indices and cortisol level in blood in water buffaloes during pregnancy and early postpartum period. Tropical Animal Health and Production 42:405-410.
Gu Z, Yang S, Leng J (2016) Impacts of shade on physiological and behavioural pattern of Dehong buffalo calves under high temperature. Applied Animal Behaviour Science 177:1-5.
Guerrero-Legarreta I, Napolitano F, Mota-Rojas D (2019) El búfalo de agua, versatil y rústico como productor de carne. Agro Meat. Buenos Aires, Argentina 2019; Febrero: 1-10.
Guerrero-Legarreta I, Napolitano F, Cruz-Monterrosa R, Mota-Rojas D, Mora P, Ramírez-Bribiesca E, Bertoni A, Berdugo J, Braghieri A (2020) A River buffalo meat production and quality: sustainability, productivity, chemical composition and sensory properties. Journal of Buffalo Science 9:159-169.
Hafez E, Badreldin A, Shafie M (1995) Skin structure of Egyptian buffalo and cattle with particular reference to sweat glands. Journal Agriculture Science 46:19-30.
Hooda OK, Singh G (2010) Effect of Thermal Stress on Feed Intake, Plasma Enzymes and Blood Biochemicals in Buffalo Heifers. Indian Journal of Animal Nutrition 27:122-127.
Kamal R, Dutt T, Patel M (2016) Behavioural, biochemical and hormonal responses of heat-stressed crossbred calves to different shade materials. Applied Animal Behaviour Science 44:347-354.
Kanosue K, Crawshaw LI, Nagashima K, Yoda T (2010) Concepts to utilize in describing thermoregulation and neurophysiological evidence for how the system works. European Journal Applied Physiology 109:5-11.
Khongdee T, Sripoon S, Vajrabukka C (2011) The effects of high temperature and wallow on physiological responses of swamp buffaloes (Bubalus bubalis) during winter season in Thailand. Journal of Thermal Biology 36:417-421.
Khongdee T, Sripoon S, Vajrabukka C (2013) The effects of high temperature and roof modification on physiological responses of swamp buffalo (Bubalus bubalis) in the tropics. International Journal of Biometeorology 57:349-354.
Koga A, Chikamune T, Kanai Y (1991) Effects of High Environmental Temperatures on Some Physicochemical Parameters of Blood and Heat Production in Swamp Buffaloes and Holstein Cattle. Animal Science and Technology 62:1022-1028.
Koga A, Kurata K, Ohata K, M. Nakajima, Hirose H, Furukawa R, Kanai Y, Chikamune T (1999) Internal changes of blood compartment and heat distribution in swamp buffaloes under hot conditions: comparative study of thermo-regulation in buffaloes and friesian cows. Asian-Australasian Journal of Animal Sciences 12:886-890.
Llamas Luceño N, de Souza Ramos Angrimani D, de Cássia Bicudo L (2020) Exposing dairy bulls to high temperature-humidity index during spermatogenesis compromises subsequent embryo development in vitro. Theriogenology 141:16-25.
Madden CJ, Morrison SF (2019) Central nervous system circuits that control body temperature. Neuroscience Letter 696:225-232.
Marai IFM, Haeeb AAM (2010) Buffalo’s biological functions as affected by heat stress — A review. Livestock Science 127:89-109.
Mitat-Valdés A (2011) Antecedentes y perspectivas de la actividad bufalina en el trópico. Revista de Tecnología en Marcha 24: 121.
Mohankumar SMJ, Balasubramanian P, Dharmaraj M, Mohankumar PS (2012) Neuroendocrine regulation of adaptive mechanisms in livestock. In: Environmental Stress and Amelioration in Livestock Production. Springer-Verlag Berlin Heidelberg, pp 263-298.
Montanholi YR, Odongo NE, Swanson KC, Schenkel F, McBride B, Miller S, (2008) Application of infrared thermography as an indicator of heat and methane production and its use in the study of skin temperature in response to physiological events in dairy cattle (Bos taurus). Journal of Thermal Biology 33:468-475.
Mora-Medina P, Berdugo-Gutiérrez JA, Mota-Rojas D, Ruiz J, Nava J, Guerrero-Legarreta I (2018a) Behaviour and welfare of dairy buffaloes: pasture or confinement? Journal of Buffalo Science 7:43-48.
Mora-Medina P, Napolitano F, Mota-Rojas D, Berdugo J, Ruiz J, Guerrero-Legarreta I (2018b) Imprinting, Sucking and Allosucking Behaviors in Buffalo Calves. Journal of Buffalo Science 7:49-57.
Morrison SF (2011) 2010 Carl Ludwig Distinguished Lectureship of the APS Neural Control and Autonomic Regulation Section: Central neural pathways for thermoregulatory cold defense. Journal of Applied Physiology 110:1137-1149.
Morrison SF (2016) Central neural control of thermoregulation and brown adipose tissue. Auton Neuroscience 196:14-24.
Morrison SF, Nakamura K (2019) Central Mechanisms for Thermoregulation. Annual Review Physiology 81:285-308.
Mota-Rojas D, Velarde A, Maris-Huertas S, Cajiao-Pachón M. (2016) Animal welfare, a global vision in Ibero-America. [Bienestar Animal una visión global en Iberoamérica]. 3rd edn. Elsevier, Barcelona, Spain.
Mota-Rojas D, De Rosa G, Mora-Medina P, Braghieri A, Guerrero-Legarreta I, Napolitano F (2019) Invited review: Dairy buffalo behaviour and welfare from calving to milking. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 1-9. doi: 10.1079/PAVSNNR201914035
Mota-Rojas D, Martínez-Burnes J, Napolitano F, et al (2020a) Invited Review: Dystocia: factors affecting parturition in domestic animals. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 15:1-16.
Mota-Rojas D, Olmos-Hernández A, Verduzco-Mendoza A, Lecona-Butrón H, Martínez-Burnes J, Mora-Medina P, Gómez-Prado PJ, Orihuela A (2020b) Infrared thermal imaging associated with pain in laboratory animals. Experimental Animals doi: 10.1538/expanim.20-0052
Mota-Rojas D, Broom DM, Orihuela A, Velarde A, Napolitano N, Alonso-Spilsbury M (2020c) Effects of human-animal relationship on animal productivity and welfare. Journal of Animal Behaviour and Biometeorology 8:196-205.
Nakamura K (2011) Central circuitries for body temperature regulation and fever. American Journal of Physiology Integrative Comparative Physiolology 301:R1207-R1228.
Napolitano F, Arney D, Mota-Rojas D, De Rosa G (2020) Chapter 17. Reproductive technologies and animal welfare. In: Presicce G (ed) Reproductive technologies in animals., 1st edn. S&T Sciences/Elsevier Press, Italy, p 266
Napolitano F, Pacelli C, Grasso F, Braghieri A, De Rosa G (2013) The behaviour and welfare of buffaloes (Bubalus bubalis ) in modern dairy enterprises. Animal 7:1704-1713.
Oliveira JPF, Rangel AHN, Barreto MLJ, Araujo V, Lima Junior D, Novaes LP, Oliveira JPF, Rangel AHN, Barreto MLJ, Araújo VM, Lima Júnior DM, Novaes LP, Aureliano IPL (2013) Temperamento de búfalas em sala de ordenha sobre índices produtivos e adaptabilidade ao ambiente: uma revisão. Journal of Animal Behaviour and Biometeorology 1:21-30.
Ootsuka Y, McAllen RM (2005) Interactive drives from two brain stem premotor nuclei are essential to support rat tail sympathetic activity. American Journal of Physiology Integrative Comparative Physiolology 289:R1107-R1115.
Ootsuka Y, Tanaka M (2015) Control of cutaneous blood flow by central nervous system. Temperature 2:392-405.
Paciullo DSC, de Castro CRT, Gomide CA de M, Mauricio RM, Avila Pires MF, Dias Muller M (2011) Performance of dairy heifers in a silvopastoral system. Livestock Science 141:166-172.
Peng D, Chen S, Li G, Cheng J, Wang J, Gu X (2019) Infrared thermography measured body surface temperature and its relationship with rectal temperature in dairy cows under different temperature-humidity indexes. International Journal of Biometeorology 63:327-336.
Rance NE, Dacks PA, Mittelman-Smith MA, Romanovsky AA, Krajewski-Hall SJ (2013) Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: A novel hypothesis on the mechanism of hot flushes. Frontiers in Neuroendocrinology 34:211-227.
Risk LM, Centre VA (2012) The impact of climate change on livestock production amongst the resource-poor farmers of third world countries: A Review. Asian Journal Agriculture Rural Development 2:621-631.
Rojas-Downing MM, Nejadhashemi AP, Harrigan T, Woznicki SA (2017) Climate change and livestock: impacts, adaptation, and mitigation. Climate Risk Management 16:145-163.
Sessler DI (2016) Perioperative thermoregulation and heat balance. Lancet 387:2655-2664.
Sevegnani KB, Fernandes DPB, Silva SHM-G da (2016) Evaluation of thermorregulatory capacity of dairy buffaloes using infrared thermography. Engenharia Agrícola 36:1-12.
Silva LKX, Sousa JS, Silva AOA (2018) Testicular thermoregulation, scrotal surface temperature patterns and semen quality of water buffalo bulls reared in a tropical climate. Andrologia 50:e12836.
Smith CJ, Johnson JM (2016) Responses to hyperthermia. Optimizing heat dissipation by convection and evaporation: Neural control of skin blood flow and sweating in humans. Auton Neuroscience 196:25-36.
Soroko M, Howell K, Zwyrzykowska A, Dudek K, Zielińska P, Kupczyński R (2016) Maximum Eye Temperature in the Assessment of Training in Racehorses: Correlations With Salivary Cortisol Concentration, Rectal Temperature, and Heart Rate. Journal of Equine Veterinary Science 45:39-45.
Tan CL, Knight ZA (2018) Regulation of Body Temperature by the Nervous System. Neuron 98:31-48.
Tattersall GJ (2016) Infrared thermography: A non-invasive window into thermal physiology. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 202:78-98.
Terrien J, Perret M, Aujard F (2011) Behavioral thermoregulation in mammals: a review. Frontiers in Bioscience 16:1428.
Thornton PK, van de Steeg J, Notenbaert A, Herrero M (2009) The impacts of climate change on livestock and livestock systems in developing countries: A review of what we know and what we need to know. Agriculture System 101:113-127.
Villanueva-García D, Mota-Rojas D, Martínez-Burnes J, Mora MP, Salmeron C, Gómez J, Boscato L, Gutiérrez O, Reyes, B, González-Lozano M (2021) Hypothermia in newly born piglets: Mechanisms of thermoregulation and pathophysiology of death. Journal of Animal Behaviour and Biometeorology 9:2101.
Weindl I, Lotze-Campen H, Popp A, Müller C, Havlík P, HerreroM, Schmitz C, Rolinski S (2015) Livestock in a changing climate: production system transitions as an adaptation strategy for agriculture. Environmental Research Letters 10:094021.
Zicarelli L (2016) Estacionalidad Reproductiva en Búfalas. In: Crudeli G (ed) Reproducción en Búfalas. Ediciones. Moglia, Argentina.
Submitted date:
08/14/2020
Accepted date:
09/09/2020
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email