Meat Science 181 (2021) 108581 Contents lists available at ScienceDirect Meat Science journal homepage: www.elsevier.com/locate/meatsci Impact of heat stress on the growth performance and retail meat quality of 2nd cross (Poll Dorset × (Border Leicester × Merino)) and Dorper lambs Minghao Zhang a, Robyn D. Warner a, Frank R. Dunshea a,b, Kristy DiGiacomo a, Aleena Joy a, Archana Abhijith a, Richard Osei-Amponsah a,c, David L. Hopkins d, Minh Ha a, Surinder S. Chauhan a,* a School of Agriculture and Food, The University of Melbourne, Parkville, VIC 3010, Australia b Faculty of Biological Sciences, The University of Leeds, Leeds LS2 9JT, United Kingdom c Department of Animal Science, University of Ghana, Legon, Ghana d Centre for Red Meat and Sheep Development, NSW Department of Primary Industries, Cowra, NSW 2794, Australia A R T I C L E I N F O A B S T R A C T Keywords: The present study investigated the impact of heat stress and genetics on lamb growth performance and meat Growth performance quality. Forty-eight Dorper and 2nd cross [Poll Dorset × (Border Leicester × Merino)] lambs (38-–42 kg; 4–5 Heat stress months old) were allocated to either thermoneutral [TN; 18–21 ◦C, 45–55% relative humidity (RH)], or heat Lamb meat stress (HS; 28 ◦C–38 ◦C, 40–60% RH) conditions in a 2 × 2 factorial design for 2 weeks. Compared with 2nd Retail display cross, Dorper lambs had a lower respiration rate (RR) and rectal temperature (RT), and exhibited less decline in body weight under HS. 2nd cross lambs showed a higher body weight gain than Dorpers under TN conditions. HS increased a* and chroma of the Longissimus thoracis et lumborum (LTL) from 2nd cross lambs over 10 days of display, but had no impact on Dorper LTL. In conclusion, Dorpers showed higher heat tolerance compared with 2nd cross lambs during the 2 weeks HS. 1. Introduction 1.67 ◦C and 48.8 ± 7.57% RH, 6 m) had a negative effect on fresh colour, tenderness and water holding capacity (WHC) of sheep and goat meat. Heat stress (HS) is one of the greatest challenges facing the global Conversely, albeit at a much lower ambient temperature, Saha et al. livestock industry. An increase in global temperature and relative hu- (2013) and Rana et al. (2014) reported that 4 and 8 h (27.8 ◦C, 81.9% midity (RH) is likely to compromise animal welfare and production RH; 45 d) heat exposure had no effect on goat slaughter weight and drip during hot summer months, especially in the warmer parts of the world. loss of the meat. Recently, Archana et al. (2018) showed that seasonal HS occurs when an animal is unable to maintain normal core body HS significantly increased Longissimus thoracis et lumborum (LTL) pH24, temperature due to increased ambient temperature which compromises and shear force of meat from Osmanabadi and Salem Black goats, but the animal’s ability to lose heat from the body. HS is not only detri- had no influence on colour and WHC. The majority of researchers agree mental for animal welfare and production, but has been implicated in that high summer temperatures would have negative impact on animal higher incidence of dark cutting or pale soft and exudative (PSE) meat welfare and meat quality (Gregory, 2010; Zhang et al., 2020). However, (Gonzalez et al., 2020; Gregory, 2010; Zhang et al., 2020). the extent to which it is affected may vary depending upon the severity Stress is well known to deplete muscle glycogen stores and lead to of HS which in turn depends upon the daily ambient temperature, RH, lower acidification of postmortem muscle and consequently a higher and exposure duration (Tang, Yu, Zhang, & Bao, 2013; Zhang et al., ultimate pH (pHu) (Scanga, Belk, Tatum, Grandin, & Smith, 1998) and 2018a, b) as animals may have variable responses to short-term and dark cutting. However, the studies reporting the impact of HS on chronic HS. Ponnampalam et al. (2016) reported that one-week of HS different meat quality traits of ruminants are equivocal, and most of (28–40 ◦C, 30–40% RH) had no effect on lamb growth performance these focused on effects of long-term (≥ 1 month) HS. For example, (slaughter weight, carcass weight and fat depth) or meat quality (pHu Kadim, Mahgoub, and Khalaf (2014) reported that seasonal HS (34.3 ± and lipid oxidation). Thus, there is a need for further research to * Corresponding author. E-mail address: ss.chauhan@unimelb.edu.au (S.S. Chauhan). https://doi.org/10.1016/j.meatsci.2021.108581 Received 17 November 2020; Received in revised form 26 March 2021; Accepted 24 May 2021 Available online 29 May 2021 0309-1740/© 2021 Elsevier Ltd. All rights reserved. M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 45 40 35 30 25 HS TN 20 15 10 Time Fig. 1. Average daily Temperature Humidity Index (THI) recorded in the heat stress (HS) and thermoneutral (TN) treatments during the experimental period. The average THI of HS was 34.1 (stander error = 0.34) and the THI of TN conditions was 20.1 (standard error = 0.41). THI < 22.2 = no stress, 22.2 to 23.3 = moderate heat stress, 23.3 to 25.6 = serve heat stress, >25.6 = extreme severe heat stress (Marai et al., 2007). elucidate the impacts of HS exposure on growth performance and meat 1 week before being relocated to metabolism cages (1.0 × 0.5 m with quality of small ruminants. polypropylene slat flooring that has a stable grip preventing sheep from Hair and wool traits are known to affect heat tolerance in sheep slipping). Lambs were individually fed a mixed ration consisting of oaten (McManus et al., 2011). Hair sheep breeds such as Pelibuey, Dorper, (25%) and lucerne (25%) chaff and standard lamb finisher pellets (50%; Katahdin, and their crossbreds have better adaptability to high envi- 14% protein, 8% crude fibre, 2% added salt, 1% added urea) formulated ronmental temperatures which is attributed to improved physiological as per NRC, 2007. Lambs were fed ad libitum and offered at 2 times and metabolic responses (lower thyroid hormone levels and metabolic maintenance requirements, and water was always available. Daily feed heat production, and deeper breathing compared with wool sheep requirements of the animals were calculated using the equation; feed (kg breeds (Correa et al., 2012; Romero, Pardo, Montaldo, Rodriguez, & DM/day) = W0.75 × 450/1000/ME, where ME is maintenance energy. Ceron, 2013; Ross, Goode, & Linnerud, 1985). In Australia, higher After acclimatization, animals were exposed to thermo-neutral (TN; carcass yield was reported for Dorper and Damara (African hair sheep) 18–21 ◦C, 45–55% RH, n = 6 for each replication) or cyclic HS; 38 ◦C compared to Merino sheep (Almeida et al., 2013). However, it is un- (between 0800 and 1600 h) and 28 ◦C (between 1600 and 0800 h) known whether heat tolerance would have any implications for meat 40–60% RH, n = 6 for each replication) for 2 weeks while housed in quality attributes and growth performance, when heat exposure shorter metabolism cages in purpose-built climatic chambers. Briefly, heat was than 1 month and breeds are compared. The objective of this study was turned on at 8 a.m. (allowing the temperature to rise to the peak at 38 ◦C therefore to compare the growth performance and meat quality attri- in 4–6 h and then maintained between 36 and 38 ◦C till 4 p.m.) and butes of hair-type sheep breeds (Dorper) and wool-type sheep breeds turned off at 4 p.m. (allowing the temperature to drop to 28 ◦C by 6 p.m. [2nd cross; Poll Dorset × (Border Leicester × Merino)] exposed to two and then maintained between 26 and 28 ◦C overnight until the next weeks of HS during the finishing phase. The choice of breeds for ex- morning at 8 a.m.) to simulate hot summer conditions (hot day followed amination was based on the hypothesis that, under HS conditions, by warm night). Room temperature and RH were recorded every 30 Dorper lambs (hair breed) would exhibit a higher degree of thermotol- mins by temperature-humidity data loggers and the temper- erance, better growth rates and meat quality attributes compared to 2nd ature–humidity index (THI) was calculated by the following equation: cross lambs (wool breed). THI = db ◦C-((0.31–0.31 RH) (db ◦C- 14.4) (Marai, El-Darawany, Fadiel, & Abdel-Hafez, 2007 and is presented in Fig. 1 for the two treatments. 2. Materials and methods 2.2. Growth performance and physiological parameters 2.1. Animals and experimental conditions At the beginning of the experimental period, and then on a weekly The experiment was approved by the University of Melbourne Fac- basis, lamb body weights were recorded (after overnight fasting) using ulty of Veterinary and Animal Sciences Animal Ethics Committee (AEC walkover scales in the morning (before feeding) to calculate the average ID 1714357.1) and the protocols used for the live animal part of this daily body weight gain (ADG). Physiological parameters, respiration study have been reported elsewhere (Joy et al., 2020). Briefly, forty- rate (RR) and rectal temperature (RT) were measured at 0800, 1200, and eight lambs [Poll Dorset × (Border Leicester × Merino) (n = 24) and 1600 h daily, as reported previously (Joy, Dunshea, Leury, DuGuacomo, Dorper (n = 24)] aged 4–5 months (body weight range: 38–42 kg) were et al., 2020). The RR was determined by counting the flank movements purchased from 5 different breeders across North-East Victoria. All for 20 s and was converted to breaths per minute. A digital thermometer lambs were purchased following thorough examination for general (DT-01; Tollot Pty. Ltd., Blacktown, AU) was used to measure RT. Daily health and were vaccinated and dewormed as per standard practices on feed intake was recorded by weighing the refusals before the morning farm. Using a randomized 2 × 2 factorial design with 4 consecutive feeding at 10:00 am. experimental runs (n = 12), lambs from each breed (n = 3) were randomly allocated to either HS (28 ◦C–38 ◦C, 40–60% RH) or TN (18–21 ◦C, 45–55% RH) conditions, following 2 weeks acclimatization 2.3. Slaughter and carcass quality (13.9–29.1 ◦C) to indoor experimental facilities. The lambs were accli- matized for 1 week in group pens and then housed in individual pens for At the end of each replication, animals were transported to a com- mercial abattoir with 1 h transportation and kept in lairage for 12 h. All 2 THI 00:00 01:00 02:00 03:00 04:00 05:00 06:00 07:00 08:00 09:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 19:00 20:00 21:00 22:00 23:00 M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 Table 1 The effect of temperature (thermoneutal, TN vs heat stress HS) and breed (Dorper vs 2nd cross, Poll Dorset × (Merino × Border Leicester)) on growth performance and carcass characteristics of finishing lambs (n = 48). Dorper 2nd cross P-value TN HS TN HS SED5 Breed Temp.1 Breed×Temp. Daily feed intake, kg / d 1.29 1.29 1.39 1.22 0.05 0.612 0.029 0.039 ADG3, g / d 5.95 − 50.6 101 − 92.3 52.6 0.475 0.002 0.073 Hot Carcass weight, kg 21.6 21.5 23.3 22.7 0.71 0.006 0.448 0.679 GR4 depth, mm 16.3 15.8 14.2 14.2 1.50 0.076 0.841 0.841 Loin eye area, cm2 14.0 13.5 13.3 14.6 0.89 0.711 0.579 0.163 pHu2 5.54 5.60 5.60 5.63 0.03 0.008 0.018 0.365 1 Temp. = Temperature. 2 pHu = ultimate pH at 24 h after slaughter. 3 ADG = Average daily body weight gain. 4 GR = total tissue thickness at the twelfth rib, 110 mm from the midline. 5 SED = Standard error of the difference of means. slaughter procedures were followed as per standard commercial oper- Denmark), as specified by Otto, Roehe, Looft, Thoelking, and Kalm ations including stunning and electrical stimulation. After slaughter, (2004). Samples (17 cm thickness, 10 g) were excised using a circular carcasses were weighed for hot carcass weight (HCW) before moving knife, then weighed (W1) and placed in EZ-drip loss tube container at into the chiller set at 0–4 ◦C and the GR tissue depth was measured with 4–6 ◦C. After 48 h, samples were weighed again (W2), and the drip loss a GR knife at 24 h postmortem (total tissue thickness at the 12th rib, 110 was calculated as: Drip loss (%) = {(W1-W2)/W1} × 100. mm from the midline) (Hopkins, Anderson, Morgan, & Hall, 1995). The Longissimus thoracis et lumborum (LTL) was removed from both sides of 2.5.2. Water holding capacity the carcasses and the cross-sectional area of LTL was measured at the Water holding capacity (WHC) was determined by measuring drip 12th rib by taking the length and width of the muscle and multiplying loss, cooking loss and purge loss of the samples. Meat samples were used this value by 0.8. Ultimate pH (pHu) was measured at lumbar/sacral for purge loss and cooking loss after colour measurements. Muscle junction of the LTL at 24 h postmortem using a combined pH and tem- samples (90 g) were weighed (W1) and packaged in trays. After 5 d to 10 perature meter (WP-80M, TPS, Brendale, Australia) with a spear-head d retail display, the samples were weighed (W2) and cooked in plastic IJ44C pH probe (TPS, Brendale, Australia). The pH probe was cali- bags using a temperature-equilibrated water bath (F38-ME, Julabo, brated using 7.0 and 4.0 buffers at regular intervals before use. 77960 Seelbach/Germany) until a core temperature of 71 ◦C was reached, as measured with a Grant thermometer equipped with T-type 2.4. Packaging and retail display conditions thermocouples during cooking. After cooking, samples were chilled at 0–4 ◦C for 16 h and reweighed (W3) (Hopkins, Ponnampalam, van de After 48 h postmortem, each LTL was cut into 6 pieces (90 g) and Ven, & Warner, 2014). Purge and cooking loss were calculated as: Purge randomly allocated to a display time after packaging in modified at- loss (%) = {(W1-W2)/W1} × 100/Cooking loss (%) = {(W2-W3)/W2} × mosphere packaging (80% O2, 20% CO2). The high oxygen (HiOx) 100. modified atmosphere packaging (MAP) was conducted with a Multivac T200 (Sepp Haggenmüller GmbH & Co., Wolferschwenden, Germany) 2.5.3. Texture measurements connected to a gas mixer to achieve a final O2: CO ratio of 80%: 20%. After cooking loss measurements, the cooked samples (from cooking 2 LTL chops (90 g) were placed on a cello pad positioned in Cryovac black loss measurements) were subjected to Warner-Bratzler peak shear force trays (170 mm × 223 mm, Sealed Air, Australia). The trays were sealed (WBSF) and texture profile analysis (TPA, hardness, adhesiveness, with a biaxially Oriented PolyAmide/Polyethylene/Ethylene vinyl springiness, chewiness) by the texture analyzer (TA-1, Lloyd In- alcohol-based film (LID-1050, OTR 10 cm3/m2/24). Trays were subse- struments, AMETEK, USA), which was conducted as per the previously quently stored at 4–6 ◦C in display cabinets with high-impact LED in- established protocols outlined by Ha, Dunshea, and Warner (2017). ternal lighting on each side (maximum 18 W) (GM1000LWCAS, Bromic Each sample was cut into 6 cuboid (1 cm × 1 cm × 4 cm) for WBSF and a Pty Limited). for 0 d, 2.5 d, 5 d, 7.5 d and 10 d retail display. Meat separate 1 cm thickness sample was used for TPA (Hardness, Adhe- colour, cooking loss, purge loss, Warner-Bratzler peak shear force siveness, Springiness and Chewiness) with 6 readings (each reading (WBSF) and texture profile analysis were measured at each display time point located at the centre of 2 cm × 2 cm square pieces) and all samples point as described below. were cut parallel to the direction of muscle fibers. WBSF was measured by a shear blade (V-shaped) with a 500 N load cell, and the shearing speed was set at 300 mm/min. The TPA was performed using a 0.63 cm 2.5. Meat quality measurements diameter flat-ended probe with 1.5 cm height, 50 mm/min speed and 80% penetration for a 1 cm thick sample. A total of 2 penetrations were 2.5.1. Surface colour applied to meat cut parallel to the direction of muscle fibers and the Meat colour (lightness, redness/greenness and yellowness/blueness force work was recoded. A total of 6 measurements were taken for each (L*, a*, b*) of the LTL surface was measured using a Minolta colorimeter sample and presented as means. (CR-400, Konica Minolta, Japan; 10◦ observer angle and D65 illumina- tion) at 0 d, 2,5 d, 5 d, 7.5 d and 10 d, and the average of three readings were recorded. The chroma and hue angle were calculated as (a*2 + 2.6. Statistical analysis b*2)1/2 and tan− 1 (b*/a*) respectively. Muscle drip loss was measured at 0 d retail display day by EZ-drip loss equipment (Danish meat, Statistical analysis was performed using liner mixed model 3 M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 procedures in GenStat 16th edition. Breed and temperature were fitted as fixed factors for the lamb growth performance (RT, RR, feed intake, ADG) and carcass parameters (carcass weight, GR, loin eye area and pHu), whereas replication and sheep/carcass ID were kept as random terms. For the analysis of retail meat quality parameters (colour, WHC and texture), fixed factors were breed, temperature and retail display time, and replications and sheep ID were included as random terms in the model. Means were considered to differ statistically when P ≤ 0.05 based on 2 times the standard error of the difference (SED). 3. Results and discussion 3.1. THI and growth performance Temperature–humidity index (THI) is commonly used to measure heat stress which is calculated based on the ambient temperature and relative humidity. An ambient environment with a THI lower than 22.2 is classified as the absence of a heat stress condition. From 22.2 to 23.3 is recognized as moderate heat stress. When THI ranges from 23.3 to 25.6, it is referred to as a severe heat stress condition, and extreme severe heat stress condition when the THI exceeds 25.6 (Marai et al., 2007; St Pierre, 2003). In this study, the average THI in the HS room was 34.1. Hence in this study, the recorded THI clearly showed that the lambs exposed to high temperature in the climatic chambers were exposed to severe extreme heat stress conditions (Fig. 1). HS led to a significant (P < 0.05) decline in feed intake of the 2nd cross lambs while had no influence on Dorper lambs. Both Dorper and 2nd cross lambs lost body weight during the HS period (P < 0.05), and the decline in weight of the 2nd crosses was higher than in the Dorpers. However, for lambs under the TN con- ditions, 2nd cross lambs had higher (P < 0.01) average daily gain (ADG) and feed intake (Table 1). In this study, HS reduced lambs’ feed intake (P < 0.05) and ADG (P Fig. 2. The mean effect of heat stress (HS) or thermoneutral (TN) treatments, < 0.01), which has been reported previously (Marai et al., 2007).There breed (2nd cross, Poll Dorset × (Merino × Border Leicester)); Dorper) and time was an effect (P 0.01) of breed on carcass weight such that the 2nd (08:00, 12:00 and 16:00 h) on (a) respiration rate and (b) rectal temperature in < cross (both HS and TN) groups had higher carcass weights compared finishing lambs (n = 48) (Joy, Dunshea, Leury, DuGuacomo, et al., 2020). (a) Respiration rate; temperature, breed, time, temperature × breed, treatment with Dorpers (P < 0.01), but there was no effect of temperature (P > × time, breed × time, all P < 0.001. 0.05) nor was there an interaction between temperature and breed. Both (b) Rectal temperature; temperature, breed, time, temperature × breed, treat- temperature and breed had no influence (P > 0.05) on GR or loin eye ment × time, all P < 0.01. breed×time, P < 0.05. area. In contrast to growth results, HS had a very limited effect on the Least squares mean are shown and error bars are the pooled SED for the two breeds in terms of carcass quality parameters. interaction of temperature × time × breed. The lack of reduction in feed intake and lower decline in body weight of Dorper lambs as compared to the 2nd cross lambs, suggests that the by higher ambient temperatures due to insufficient heat loss (Franz- Dorper breed is better adapted to higher environmental temperatures mann, 1971). and thus may exhibit better growth performance than the high pro- In this study, significant breed differences were observed for lamb RR ducing breed, which has been reported previously (Archana et al., 2018; and RT as reported before (Joy, Dunshea, Leury, DuGuacomo, et al., Srikandakumar, Johnson, & Mahgoub, 2003). Under the TN conditions, 2020). HS increased RR and RT (P < 0.01) of both Dorper (RR 163.8/ 2nd cross lambs had better growth performance than Dorpers, which min, RT 40.2 ◦C) and 2nd cross (RR 185.2/min, RT 40.5 ◦C) lambs included a higher daily feed intake, ADG and hot carcass weight (P < (Fig. 2; P < 0.05), which confirms the lambs were under HS conditions 0.05 for all). These variations of growth performance with Dorper and and agreed with previous studies (Chauhan, Celi, Leury, Clarke, & 2nd cross under TN conditions agreed with the results of previous Dunshea, 2015; Marai et al., 2007). Based on the classification of RR by studies which reported that Dorpers had lower carcass weights, ADG and Silanikove (2000), 40–60/min is classified as low stress, 60–80 is higher fat thickness compared to Suffolks (Burke & Apple, 2007; medium-high stress, 80–120/min-high stress and > 200 is a severe stress Schoeman, 2000; Snowder & Duckett, 2003). However, Almeida et al. condition. A comparison of 2nd cross lambs with the Dorpers showed (2013) pointed out that Dorper and Damara (hair sheep) had higher feed lower RR and RT in the latter (P < 0.05), under both temperature con- intakes and carcass weights compared with Merino (wool-type sheep) ditions throughout the day (0800, 1200 and 1600 h). This showed that lambs. Dorpers had a higher ability to regulate body heat during the heat exposure period (Horton, 1990; Srikandakumar et al., 2003). As re- 3.2. Respiration rate and rectal temperature ported by Macias-Cruz et al. (2016), hair sheep breeds appear to produce low concentrations of thyroid hormones, hence they tend to reduce their Respiration rate and rectal temperature are some of the most metabolic heat production, and their breathing is slower and deeper commonly used indicators of physiological responses to HS in sheep and than wool breeds which helps them to lose more body heat. Compared cattle (Marai et al., 2007). Under high ambient temperature and hu- with wool breeds, hair sheep with lower coat thickness, shorter and midity, respiratory heat loss contributes about 60% of the total heat loss lower density of hair, and higher sweat glands are adapted to HS, and a to maintain thermal balance in sheep (Wojtas, Cwynar, & Kołacz, 2014). lower density of hair increases the penetration of air in the sheep fleece Similar to other homeothermic animals, sheep body temperatures are to improve heat transfer (McManus et al., 2011). maintained within a very narrow range (38.3–39.9 ◦C) and are affected 4 M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 Table 2 The effect of temperature (thermoneutal, TN vs heat stress HS) and breed (Dorper vs 2nd cross, Poll Dorset × (Merino × Border Leicester)) on colour of Longissimus thoracis et lumborum during 10 d high oxygen package retail display of finishing lamb meat (n = 48). Dorper 2nd cross P-values Day TN HS TN HS SED2 Breed Temp.1 Time Breed×Temp. CIE-L* value 0 34.1 34. 4 33.4 33.5 0.97 0.082 0.665 <0.001 0.832 2.5 36.4 36.6 35.2 36.6 5 39.1 38.3 37.9 37.4 7.5 38.3 37.7 37.7 36.1 10 39.1 39.4 38.8 38.1 CIE-a* value 0 16.3 16.4 16.3 16.6 0.81 0.219 0.006 <0.001 0.120 2.5 16.8 17.3 16.4 17.8 5 12.5 13.9 12.2 15.1 7.5 10.3 11.2 10.7 12.7 10 9.54 9.29 9.05 11.5 CIE-b* value 0 7.17 7.38 7.19 7.69 0.37 0.492 0.033 <0.001 0.914 2.5 8.99 9.55 8.98 9.86 5 8.16 9.01 8.37 8.81 7.5 8.43 8.40 8.50 8.19 10 9.15 9.29 9.38 9.44 Chroma 0 17.9 18.0 17.8 18.3 0.62 0.203 <0.001 <0.001 0.019 2.5 19.1 19.7 18.7 20.4 5 14.9 16.7 14.9 17.5 7.5 13.6 14.2 13.8 15.1 10 13.5 13.5 13.1 15.0 Hue angle 0 23.7 24.2 23.7 24.7 2.76 0.307. 0.226 <0.001 0.178 2.5 27.9 29.0 28.6 28.6 5 33.6 33.6 35.0 30.1 7.5 40.7 38.8 39.5 32.8 10 45.0 46.3 46.2 39.7 1 Temp. = Temperature. 2 SED=Standard error of the difference of means. 3.3. Retail meat quality exposure duration might exist between 2 weeks to 1 month, as a dif- ference in pHu was reported with longer HS duration, as shown by 3.3.1. Meat colour and pHu Archana et al. (2018) (28 and 40 ◦C and 29–58% RH, 1 month), Macías Overall, 2nd cross lambs had higher pHu compared with Dorpers (P Cruz (2020) (28.4 ◦C, 55.2%; 1 month) and Kadim et al. (2007) (35 ◦C < 0.01), and HS had an impact on the pHu of the LTL (P < 0.05). As and 47% RH; 6 months). As such, the influence of HS on muscle loin pH shown in Table 1, the pHu of Dorper HS (5.60) was higher than Dorper might be greater with the increased duration of HS exposure. TN group (5.54) but, there was no difference between 2nd cross HS For meat colour during display, HS increased LTL muscle a* (P < (5.63) and 2nd cross TN (5.60; P > 0.05). 0.01), b* (P < 0.05), and chroma (P < 0.01) values of both breeds, but Compared with TN, the overall increase in pHu of meat under the HS had no effect on L* (P > 0.05) (Table 2). Across both TN and HS, Dorpers condition (P < 0.05) was consistent with previous HS studies of rumi- had higher L* values than 2nd cross lambs, but the difference was not nants. Kadim et al. (2008) reported that seasonal HS (35 ◦C, 47% RH) significant. There was an interaction between breed and temperature for significantly increased the pHu in the Psoas major and minor of Omani chroma value such that HS increased the chroma of 2nd cross over the Somali goats and Somali Merino sheep compared with cool season 10 d of retail display (P < 0.05) while had no effect on Dorpers (P > (21 ◦C, 59% RH). Compared to each treatment group, the pHu of the 2nd 0.05). After 10 d retail display, 2 weeks HS significantly reduced meat cross HS was greater than that of the Dorper TN (P < 0.05). Using 5.7 as hue and increased chroma value of 2nd cross breed but had no impact on the threshold for dark-cutting high pHu meat (McGilchrist, Alston, Dorpers. Gardner, Thomson, & Pethick, 2012), HS did not result in dark cutting During the display period, samples from 2nd cross HS animals had meat for either Dorper or 2nd cross in the present experiment. The in- better colour performance as indicated by the highest a* and chroma crease of pHu of HS lambs in this study is in accordance with previous values and lowest hue values. A previous study showed that HiOx MAP studies of sheep and goats, although the magnitude of the difference in increased the redness a* values of beef steaks with higher pH values pHu between HS and TN was much lower compared with previous (>5.80) after 4 d of chilled storage and HiOx MAP had no effect on the studies (Archana et al., 2018; Kadim et al., 2007, 2008). The different redness a* level of meat with normal pH < 5.8 (Zhang et al., 2018a, b). exposure times could be a reasonable explanation as a previous study by Neethling, Hoffman, Sigge, and Suman (2019) also reported that a Lowe, Gregory, Fisher, and Payne (2002) that exposed sheep to 33 ◦C, higher pH of LTL had a positive correlation with springbok muscle 85–100% RH for 12 h, and a recent study (Chauhan, Dunshea, Plozza, colour stability and metmyoglobin reducing activity during 8 d of Hopkins, & Ponnampalam, 2020) that exposed lambs to 28–40 ◦C, overwrapped storage. Similar to lamb physiological parameters, Dorper 30–40% RH for 1 week, showed that the short term HS had no influence lamb pHu was not influenced by the HS condition again indicating that on muscle pHu. The critical time point of the negative impact of HS Dorper (a hair breed) had better heat tolerance when compared with 5 M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 Table 3 The effect of temperature (thermoneutal, TN vs heat stress HS) and breed (Dorper vs 2nd cross, Poll Dorset × (Merino × Border Leicester)) on drip, purge and cooking loss of Longissimus thoracis et lumborum during 10 d high oxygen package retail display. Dorper 2nd cross P-values Day TN HS TN HS SED2 Breed Temp.1 Time Breed×Temp. Drip loss (%) 0 1.94 2.36 2.23 1.80 0.35 0.652 0.980 – 0.093 Purge loss (%) 5 6.21 7.21 6.74 6.77 0.44 0.457 0.127 <0.001 0.117 10 8.00 8.64 8.61 8.52 Cooking loss (%) 0 19.4 21.9 22.1 21.3 1.39 0.041 0.206 <0.001 0.101 5 19.5 20.9 21.1 20.6 10 17.5 18.2 18.8 19.6 1 Temp. = Temperature. 2 SED=Standard error of the difference of means. high production 2nd cross lambs (wool breed). This also supports the Chauhan et al. (2020) (28–40 ◦C, 30–40% RH, 1 week), and Lowe et al. previous observations that the impact of HS is variable and depends on (2002) (33 ◦C, 85–100% RH, 12 h). Combined with the results of this animal breed, and the extent of increases in environment temperature, experiment, it appears that the impact of HS on meat colour is quite humidity and solar radiation (Aggarwal & Upadhyay, 2013; Silanikove, limited when the heat exposure time is shorter than 1 month. 2000). Many HS studies have pointed out that the seasonal HS could lead to increased incidence of dark cutting meat. For example, Kadim et al. 3.3.2. Water holding capacity and texture (2008) reported 6 months high temperature (35 ◦C and 47% RH) Overall, there was no main effect of breed and temperature on meat significantly increased the muscle psoas major and minor a* and drip loss or purge loss (Table 3) and neither were there any interactions decreased L* and b* values of sheep and goats. Gregory (2010) also between breed and temperature (P > 0.05 for all traits covered here). pointed out a higher frequency of dark cutting beef during summer However, there was an effect of breed on cooking loss such that 2nd months. However, for a shorter duration of heat exposure, the relevant cross lamb meat had higher cooking loss (P < 0.05) as compared to studies are very limited and the negative impact of HS on meat colour is Dorpers. The purge loss increased (P < 0.01) from 5 d to 10 d display. weak. For example, Macías Cruz (2020) reported that 1 month of sum- The retail display time also had a significant impact on cooking loss such mer feeding (28.4 ◦C, 55.2% RH) had no detrimental changes in hair that cooking loss of both Dorper and 2nd cross lambs exposed to TN breed sheep (Dorper × Katahdin) meat colour compared with the winter conditions was decreased from 0 d to 10 d display (P < 0.05), but not in (19.2 ◦C, 41.7% RH), which was in accordance with the results reported 2nd cross (P > 0.05) lambs exposed to HS conditions. The decrease in by Archana et al. (2018) (28 and 40 ◦C and 29–58% RH, 1 month), cooking loss in MAP could have resulted from the increased content of Table 4 The effect of temperature (thermoneutal, TN vs heat stress HS) and breed (Dorper vs 2nd cross, Poll Dorset × (Merino × Border Leicester)) on WBSF and texture profile analysis (TPA) of Longissimus thoracis et lumborum during 10 d high oxygen package retail display. Dorper 2nd cross P-values TN HS TN HS SED2 Breed Temp.1 Time Breed×Temp. WBSF (N) 0 d 46.3 47.2 50.9 48.6 4.00 0.482 0.897 <0.001 0.639 5 d 31.9 29.5 33.7 31. 7 10 d 26.1 30.0 27.7 27.7 Hardness (N) 0 d 38.4 39.1 37.1 38.0 2.14 0.051 0.435 <0.001 0.725 5 d 38.7 38.3 36.4 37.0 10 d 34.9 35.8 32.1 33.7 Adhesiveness (Nmm) 0 d 4.64 4.55 4.45 4.49 0.75 0.154 0.983 <0.001 0.363 5 d 4.34 4.28 3.97 4.50 10 d 3.30 2.65 1.50 1.95 Springiness (mm) 0 d − 1.64 − 1.68 − 1.70 − 1.55 0.09 0.831 0.207 0.059 0.872 5 d − 1.56 − 1.55 − 1.53 − 1.62 10 d − 1.73 − 1.60 − 1.69 − 1.64 Chewiness (N) 0 d 13.3 13.5 12.8 13.5 1.10 0.155 0.150 0.073 0.637 5 d 13.6 14.2 13.0 13.3 10 d 11.9 13.6 11.5 12.0 1 Temp. = Temperature. 2 SED=Standard error of the difference of means. 6 M. Zhang et al. M e a t S c i e n c e 181 (2021) 108581 exogenous enzymes (Marcinkowska-Lesiak et al., 2016), as the colla- Almeida, A. M., Kilminster, T., Scanlon, T., Araujo, S. S., Milton, J., Oldham, C., & genase enzymes disintegrate the myofibrillar proteins and connective Greeff, J. C. (2013). Assessing carcass and meat characteristics of Damara, Dorper and Australian merino lambs under restricted feeding. Tropical Animal Health and tissue thereby improving water holding capacity of proteins (Jama et al., Production, 45(6), 1305–1311. 2008). Generally, cooking loss has a negative correlation with sheep Archana, P. R., Sejian, V., Ruban, W., Bagath, M., Krishnan, G., Aleena, J., … Bhatta, R. meat pHu in the region of 5.5–5.8 (Adzitey, 2011; Bouton, Harris, & (2018). Comparative assessment of heat stress induced changes in carcass traits, plasma leptin profile and skeletal muscle myostatin and HSP70 gene expression Shorthose, 1971). However, there are limited reports on the cooking loss patterns between indigenous Osmanabadi and Salem Black goat breeds. Meat of sheep meat from animals exposed to HS conditions and most of them Science, 141, 66–80. investigated only fresh meat quality (within 48 h. postmortem) which Bouton, P. E., Harris, P. V., & Shorthose, W. R. (1971). Effect of ultimate ph upon the did not include further ageing or display periods. Present studies of fresh water-holding capacity and tenderness of mutton. Journal of Food Science, 36(3), 435–439. meat reported that a high temperature environment (35 ◦C, 47% RH; 4 Burke, J. M., & Apple, J. K. (2007). Growth performance and carcass traits of forage-fed months) had a negative impact on expressed juice of psoas major and hair sheep wethers. Small Ruminant Research, 67(2–3), 264–270. minor muscle of Merino sheep with higher pHu (5.77) compared with a Chauhan, S. S., Celi, P., Leury, B. J., Clarke, I. J., & Dunshea, F. R. (2015). Errata. Journal of Animal Science, 93(3), 1418. cool season (21 ◦C, 59% RH; pHu 5.64) (Kadim et al., 2008). Archana Chauhan, S. S., Dunshea, F. R., Plozza, T., Hopkins, D. L., & Ponnampalam, E. N. (2020). et al. (2018) showed that HS had a negative effect on cooking loss of The impact of antioxidant supplementation and heat stress on carcass characteristics, Salem Black goat meat while there was no effect on Osmanabadi goat muscle nutritional profile and functionality of lamb meat. Animals, 10(8), 1286. Correa, M. P. C., Cardoso, M. T., Castanheira, M., Landim, A. V., Dallago, B. S. L., meat. Louvandini, H., & McManus, C. (2012). Heat tolerance in three genetic groups of For texture results, HS, breed and their interaction had no effect on lambs in central Brazil. Small Ruminant Research, 104(1–3), 70–77. the WBSF and TPA (P > 0.05) (Table 4). Our results for texture were in Franzmann, A. W. (1971). Variation of rectal temperature in bighorn sheep. The Journal of Wildlife Management, 488. contrast to previous findings which showed HS increased meat WBSF, Gonzalez, R., Gonzalez Rivas, P., Chauhan, S. S., Ha, M., Fegan, N., Dunshea, F. R., & hence increased toughness (Archana et al., 2018; Saha et al., 2013). Warner, R. D. (2020). Effects of heat stress on animal physiology, metabolism, and Kadim et al. (2007) reported HS decreased the myofibril fragmentation meat quality: a review. Meat Science, 162. Article 108025. Gregory, N. G. (2010). How climatic changes could affect meat quality. Food Research index, which indicates reduced proteolysis and reduced tenderness, for International, 43(7), 1866–1873. meat from Merino sheep, but they showed no effect in Somali sheep. It is Ha, M., Dunshea, F. R., & Warner, R. D. (2017). Investigation of tenderness and water worth mentioning that the various results of water holding capacity and holding capacity of aged pork loins in two packaging systems. Final report. Parkville: Co- texture were conducted under different heat exposure times, breeds, operative Research Center for High Integrity Australian Pork, University of Melbourne. slaughter and chilling ways as mentioned previously (Archana et al., Hopkins, D. L., Anderson, M. A., Morgan, J. E., & Hall, D. G. (1995). A probe to measure 2018; Saha et al., 2013;), and the magnitude of the increase in pHu with GR in lamb carcasses at chain speed. Meat Science, 39(2), 159–165. HS was also variable in these studies. Hopkins, D. L., Ponnampalam, E. N., van de Ven, R. J., & Warner, R. D. (2014). The effect of pH decline rate on the meat and eating quality of beef carcasses. Animal Production Science, 54(4), 407–413. 4. Conclusion Horton, G. M. J. (1990). Effect of confinement on performance and physiological indicators of stress in lambs. Journal of Animal Science, 68, 260. Jama, N., Muchenje, V., Chimonyo, M., Strydom, P. E., Dzama, K., & Raats, J. G. (2008). Two weeks cyclic HS had significant negative effect on both Dorper Cooking loss components of beef from nguni, bonsmara and angus steers. African and 2nd cross lambs’ physiological responses and growth performance. Journal of Agricultural Research, 3(6), 416–420. When exposed to 2 weeks cyclic HS, Dorpers showed higher heat Joy, A., Dunshea, F. R., Leury, B. J., DuGuacomo, K., Clarke, I. J., Zhang, M., … Chauhan, S. S. (2020). Comparative assessment of thermotolerance in Dorper and tolerance (less decline of feed intake and body weight and lower RR and second-cross (Poll Dorset/Merino× Border Leicester) lambs. Animals, 10(12), 2441. RT) than 2nd cross lambs. However, 2nd cross lamb’s had higher growth Kadim, I. T., Mahgoub, O., Alkindi, A. Y., Al-Marzooqi, W., Al-Saqri, N. M., Almaney, M., performance compared with Dorpers under the TN conditions. Two & Mahmoud, I. Y. (2007). Effect of transportation at high ambient temperatures on physiological responses, carcass and meat quality characteristics in two age groups weeks of heat exposure caused a small increase in muscle pHu of the two of Omani sheep. Asian-Australasian Journal of Animal Sciences, 20(3), 424–431. breeds. In terms of retail meat quality, meat from 2nd cross HS animals Kadim, I. T., Mahgoub, O., Al-Marzooqi, W., Al-Ajmi, D. S., Al-Maqbali, R. S., & Al- had higher redness a* during 10 d of retail display. Except for colour, HS Lawati, S. M. (2008). The influence of seasonal temperatures on meat quality characteristics of hot-boned, m. psoas major and minor, from goats and sheep. Meat had no impact on drip loss, purge loss, cooking loss and texture in both Science, 80(2), 210–215. 2nd cross and Dorper lambs. It is suggested that high meat production Kadim, I. T., Mahgoub, O., & Khalaf, S. (2014). Effects of the transportation during hot breeds are more likely to exhibit adverse effects of HS due to lower heat season and electrical stimulation on meat quality characteristics of goat Longissimus dorsi muscle. Small Ruminant Research, 121(1), 120–124. adaption capacity as compared to hardy breeds that are more adapted to Lowe, T. E., Gregory, N. G., Fisher, A. D., & Payne, S. R. (2002). The effects of heat. While the negative impacts of HS on sheep growth performance are temperature elevation and water deprivation on lamb physiology, welfare, and meat quite evident, the impact of short-term (2 weeks) HS on meat quality are quality. Australian Journal of Agricultural Research, 53(6), 707–714. not as evident and might be variable depending upon the duration of Macías Cruz, U. (2020). Feedlot growth, carcass characteristics and meat quality of hair breed male lambs exposed to seasonal heat stress (winter vs. summer) in an arid heat exposure. Hence, further research is still warranted to evaluate the climate. Meat Science, 169. effect of HS on meat quality under different durations of temperature Macias-Cruz, U., Lopez-Baca, M. A., Vicente, R., Mejia, A., Alvarez, F. D., Correa- exposure, as there are significant variations in animal responses to acute Calderon, A.-R., & L.. (2016). Effects of seasonal ambient heat stress (spring vs. summer) on physiological and metabolic variables in hair sheep located in an arid and chronic heat exposure. region. International Journal of Biometeorology, 60(8), 1279–1286. Marai, I. F. M., El-Darawany, A. A., Fadiel, A., & Abdel-Hafez, M. A. M. (2007). Acknowledgements Physiological traits as affected by heat stress in sheep—A review. Small Ruminant Research, 71(1–3), 1–12. Marcinkowska-Lesiak, M., Zdanowska-Sąsiadek, Ż., Stelmasiak, A., Damaziak, K., Authors would like to acknowledge Faculty of Veterinary and Agri- Michalczuk, M., Polawska, E., … Wierzbicka, A. (2016). 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