Journal of Thermal Biology 85 (2019) 102407 Contents lists available at ScienceDirect Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio Reproductive characteristics of bulls from two breed compositions and their correlations with infrared thermography T ∗ Vanessa Amorim Teixeiraa, Sandra Gesteira Coelhoa, Thierry Ribeiro Tomichb, , João Paulo Ρacheco Rodriguesc, Mariana Magalhães Camρosb, Fernanda Samarini Machadob, Marcos Vinícius Gualberto Barbosa da Silvab, Gabriel Augusto Monteirod, Luiz Gustavo Ribeiro Ρereirab a Department of Animal Science, Federal University of Minas Gerais, Minas Gerais, 30161-970, Brazil b Embrapa Dairy Cattle, Minas Gerais, 36038-330, Brazil c Institute of Studies of the Humid Tropic, Federal University of the South and Southeast of Pará, 68557-335, Brazil d Department of Veterinary Clinic and Surgery, Federal University of Minas Gerais, Minas Gerais, 30161-970, Brazil ARTICLE INFO ABSTRACT Keywords: The objective was to evaluate reproductive characteristics of crossbred Girolando (Gyr x Holstein) bulls from two Andrological examination breed compositions and correlate these results with infrared thermography data. Evaluations were performed Crossbreeding considering sperm motility, vigor and morphology; scrotal circumference; body morphology and temperament. Dairy cattle Infrared thermography was performed to determine surface temperatures of ocular and scrotal areas. Girolando Thermoregulation capacity was assessed by differences between air and rectal temperatures, air and maximum Reproduction temperatures in ocular and scrotal areas, and dorsal and ventral lines of the scrotum. Data analysis was per- Semen fi ff ff Thermoregulation formed using a linear mixed model (breed composition as xed e ect and year of evaluation as random e ect). Spearman correlation coefficient was used to associate thermography and reproductive data. Girolando 3/4 Holstein bulls had higher (P ≤ 0.001) scrotal circumference and higher average body morphology and tem- perament, whereas 5/8 Holstein bulls had a higher (P < 0.001) percentage of major-type and total sperm defects. Girolando 3/4 Holstein bulls had scrotal temperatures 0.8 °C higher (P < 0.001) and 5/8 Holstein bulls had 9.8% and 10.6% higher differences on “rectal – scrotal area” and “ocular area – scrotal area” temperatures, respectively. Ocular area temperatures had negative correlations (P ≤ 0.1) with sperm motility and vigor, and positive correlations (P < 0.001) with minor-type and total sperm defects. Ventral line scrotal temperatures had positive correlations (P < 0.001) with minor-type and total sperm defects. Girolando 3/4 Holstein bulls were found to be superior to 5/8 Holstein bulls for reproductive characteristics. Under non-stressing climatic con- ditions, semen characteristics of Girolando bulls were more influenced by breed composition than by the ca- pacity for scrotal thermoregulation. Correlations between semen quality and scrotal temperatures can aid in the identification of bulls for breeding, particularly when a large number of animals are in the tests. 1. Introduction between Holstein and Gyr cattle, called Girolando, contributes to 80% of the milk produced in Brazil (FAO, 2017), with an estimated popu- Various breed compositions encompass the dairy production sys- lation close to 10 million Girolando animals (Oliveira Júnior et al., tems in Brazil, which is the world's fifth largest producer and consumer 2017). of bovine milk and its derivatives (USDA-NASS, 2017). The use of an- Girolando breeding program has adopted progeny tests and en- imals adapted to the tropical environment increases farmers' yields couraged the commercialization of semen. In 2015, 641,360 semen (Paranhos da Costa et al., 2015) and, because of their greater adapt- doses from Girolando bulls were sold, a value 70% higher than that of ability to the tropics and productive potential, the crossbreeding 2013. Mating with 3/4 Holstein and 5/8 Holstein bulls is important for ∗ Corresponding author. E-mail addresses: [email protected] (V.A. Teixeira), [email protected] (S.G. Coelho), [email protected] (T.R. Tomich), [email protected] (J.P. Ρacheco Rodrigues), [email protected] (M.M. Camρos), [email protected] (F.S. Machado), [email protected] (M.V. Gualberto Barbosa da Silva), [email protected] (G.A. Monteiro), [email protected] (L.G. Ribeiro Ρereira). https://doi.org/10.1016/j.jtherbio.2019.102407 Received 26 April 2018; Received in revised form 15 August 2019; Accepted 25 August 2019 Available online 26 August 2019 0306-4565/ © 2019 Elsevier Ltd. All rights reserved. V.A. Teixeira, et al. Journal of Thermal Biology 85 (2019) 102407 obtaining the main breed compositions of Girolando (Silva et al., 2016). 2.3. Data collection The proportion of taurine genes in breed compositions of Girolando (75% or 62.5% of Holstein genes for Girolando 3/4 and 5/8, respec- 2.3.1. Reproductive parameters tively) may represent one of the factors responsible for reproductive Scrotal circumference (SC) was evaluated according to Kastelic and (Godfrey et al., 1990) and productive (Silva et al., 2016)differences in Thundathil (2008), three times during each year. Two consecutive progenies of bulls. measurements were performed using a specific tape for measuring The fact that a single bull reproduces with several cows denotes the scrotal perimeter with a millimeter scale (Walmur Instrumentos Ve- greater importance of bulls to imprint genetic traits of interest in herds terinários Ltda., Porto Alegre, RS, Brazil). (Franco et al., 2006). In order to increase reproductive capacity, bulls Semen analyses were performed according to procedures described must produce morphologically normal and large numbers of sperm. For by the Brazilian College of Animal Reproduction (CBRA, 2013). Sam- effective spermatogenesis, testes temperature must be between 2 and ples were obtained by electrical stimulation using the Autojac-Neovet 6 °C below body temperature (Kastelic, 2014a). According to Brito et al. device (Autojac®, Neovet, Campinas, SP, Brazil). Monthly collections (2004),effects of testicular temperature elevation have direct reflexes were carried out during the three-month test period of each year. Im- in the decrease of sperm production and semen quality, as well as in mediately after each collection, microscopic analysis of the semen was bull fertility, resulting in economic loss that implies a lower pregnancy performed. Sperm individual motility (MOT) was examined with a rate. bright-field microscope (LEICA Microsystems, Buffalo, NY, USA) at Infrared thermography is an indirect non-invasive method that can 400× magnification using ~10 μL aliquot of semen placed on a heated aid in the measurement of scrotal surface temperature in bulls (Brito glass slide (37 °C) and covered with a coverslip. The MOT index was et al., 2002). It is a promising alternative method to evaluate the ca- evaluated as the percentage of motile sperm (0–100%) at intervals of pacity for testicular thermoregulation in bulls raised under high en- 5%. Sperm vigor (VIG) was evaluated using a 0 to 5 scale based on vironmental temperatures and, consequently, can be used to identify progressive sperm movement, where 0 = none, 1 = very weak, animals adapted for breeding. However, there is still a lack of precise 2 = weak, 3 = intermediate, 4 = strong and 5 = very strong. These information to associate thermography with physiological or patholo- evaluations were done by visualizing at least three fields and the result gical phenomena in animal reproduction. expressed by the average of its results. An aliquot of semen was also Based on the hypotheses: i) breed composition of Girolando bulls diluted in buffered saline-formaldehyde solution (1:10) for evaluation influences reproductive characteristics and ii) it is possible to use in- of sperm morphology. These analyzes were performed under magnifi- frared thermography as a fast-track non-invasive auxiliary method of cation 1,000× using a phase-contrast microscope (Meiji Techno, Chi- assessing the reproductive performance of bulls, the objective of this kumazawa, Japan). A wet chamber was prepared for reading (aliquot of study was to evaluate the influence of breed composition of Girolando 10 μL of semen between glass slide and coverslip), counting 200 cells bulls on andrological and semen characteristics and to correlate these per sample. Major-type sperm defects (MAJD) were considered as: ac- with infrared thermography data. rosomal defect, abnormal head, folded head, dorsal cytoplasmic dro- plet, midpiece defect, accessory tail, and folded tail. Minor-type sperm 2. Material and methods defects (MIND) included ventral cytoplasmic droplet, abaxial insertion, folded tail, and large heads. Total defects (TOTD) were considered in 2.1. Experimental area 200 spermatozoa of each animal and sperm classification was based on the criteria adopted by Barth (2007). The study was conducted between February and April 2016 and 2017, involving animals of the Girolando testing program at the Federal 2.3.2. Body morphology Institute of Education, Science and Technology of Triângulo Mineiro Body morphology (MORP) test evaluated: body conformation and (19°39′17.9″S 47°57′41.9″W), in Uberaba, MG, Brazil. All procedures capacity (20%) - considering body depth, masculinity, body length, a involving animals were approved by the Embrapa Dairy Cattle Ethics strong back/loin, height at rump and breeding characteristics; dairy