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Review
The Impact of Heat Load on Cattle
Angela M. Lees 1, 2, * , Veerasamy Sejian 3, Andrea L. Wallage 1, Cameron C. Steel 2,
Terry L. Mader 4,5, Jarrod C. Lees 2and John B. Gaughan 1, *
1School of Agriculture and Food Sciences, The University of Queensland; Gatton, QLD 4343, Australia;
a.wallage@uq.edu.au
2School of Environmental and Rural Science, University of New England, Armidale, NSW 2350, Australia;
csteel5@une.edu.au (C.C.S.); Jarrod.Lees@une.edu.au (J.C.L.)
3Indian Council of Agricultural Research (ICAR)-National Institute of Animal Nutrition and Physiology,
Adugodi, Bangalore 560030, India; drsejian@gmail.com
4Department of Animal Science, University of Nebraska, Lincoln, NE 68588, USA; tmader12@msn.com
5Mader Consulting, Gretna, NE 68028, USA
*Correspondence: angela.lees@une.edu.au (A.M.L.); j.gaughan@uq.edu.au (J.B.G.);
Tel.: +617-5460-1036 (J.B.G.)
Received: 17 April 2019; Accepted: 31 May 2019; Published: 6 June 2019
Simple Summary:
It is well known that the thermal environment has an integral role in maintaining
the health and productivity of cattle. Although cold stress has been identified to negatively influence
cattle comfort and productivity, the predominant focus herein has been describing the influence of
heat stress on bovines. The impact of heat stress is particularly important due to the changing global
environment. Global warming is likely to occur, however, the nature and magnitude of environmental
changes, both climatic and non-climatic, are difficult to elucidate. Therefore a predominant focus
on the impact of hot environments on cattle is warranted. This review provides an overview of the
dynamic relationship that exists between the thermal environment and bovines.
Abstract:
Heat stress and cold stress have a negative influence on cattle welfare and productivity.
There have been some studies investigating the influence of cold stress on cattle, however the
emphasis within this review is the influence of heat stress on cattle. The impact of hot weather on
cattle is of increasing importance due to the changing global environment. Heat stress is a worldwide
phenomenon that is associated with reduced animal productivity and welfare, particularly during
the summer months. Animal responses to their thermal environment are extremely varied, however,
it is clear that the thermal environment influences the health, productivity, and welfare of cattle.
Whilst knowledge continues to be developed, managing livestock to reduce the negative impact of
hot climatic conditions remains somewhat challenging. This review provides an overview of the
impact of heat stress on production and reproduction in bovines.
Keywords:
cattle welfare; climate change; heat load; heat stress; mitigation techniques; multiple
stressors; production; reproduction; thermotolerance
1. Introduction
The thermal environment can have a negative influence on cattle welfare. Historically, Ames [1]
defined the thermoneutral zone as the thermal environment where an animal experiences optimum
health and maximum productivity. Whilst cattle comfort and productivity may be compromised
during exposure to cold, wet and/or windy conditions [
2
,
3
], there has been a predominant focus on
the influence of hot weather on cattle, and other species. The impact of hot weather on cattle is of
increasing importance, particularly in conjunction with the changing global environment.
Animals 2019,9, 322; doi:10.3390/ani9060322 www.mdpi.com/journal/animals
Animals 2019,9, 322 2 of 20
Beyond the direct impact that heat stress has on the health and productivity of animals, the economic
impact on livestock producers also needs to be considered. In 2003, St-Pierre et al. [
4
] estimated that
heat stress had an annual economic burden of between $1.69 and $2.36 billion (USD) on the US animal
agriculture industries. Within this estimate, economic losses of $897 to $1500 million (USD) were
attributed to the dairy industry and $370 million (USD) for the beef industry [
4
]. Sackett et al. [
5
]
estimated the economic costs of heat stress to Australian feedlots at approximately 16.5 million (AUD).
Given that these analyses were conducted over a decade ago, these estimates may not reflect the current
economic impact of heat stress. Furthermore, in conjunction with climate change, it is probable that
these estimates are underestimating the economic impact of heat stress on cattle production systems.
For livestock production enterprises, climate change has the potential to alter the thermal
environment, which may result in the climate having an increasingly negative impact on the welfare
and productivity of cattle. Periods of hot weather are already associated with reduced animal
health, reduced reproductive efficiency in both males and females, and decreased feed conversion
efficiency [
4
,
6
]. Therefore, it is likely that climate change will have a considerable impact on the
economic viability of animal agriculture worldwide.
In spite of this, all animals possess the capacity to adapt to their thermal environment.
Animals are capable of modifying their behavioral, physiological, and morphological characteristics,
or a combination of these, in response to the thermal environment [
7
]. This review has attempted to
provide a rounded overview of the impact that heat stress has on bovines.
2. Climate Change
The effect of climate change is highly variable globally and is largely influenced by geographical
location. Cattle and livestock enterprises have the ability to adapt to an increasing mean global
temperature, the primary concern, however, is the ability of livestock to cope with climatic extremes,
e.g., heat waves [
8
]. Climate change has the potential to present as (i) rapid changes in climate
over a couple of years or (ii) as more subtle changes over decades [
8
]. However, irrespective of
the manifestation of climate change, global warming is likely to have a significant impact on the
stability and sustainability of livestock production worldwide. Globally, various climate change
models are predicting a 1.1
◦
C to 6.4
◦
C increase in temperature by the end of this century [
9
].
Furthermore, in southern Australia, the average number of consecutive days of heat-stress has
increased from two days per heat stress event from 1960 to 1999, to four days from 2000 to 2008 [10].
Numerous species are likely to be negatively impacted by the changing global environment [
11
],
due to changes in ecosystem microclimates. Many species have adaptations to cope with short-term
climate variability, i.e., seasonal changes. However, these adaptations may not be successful for species
survival with the predicted climate change [
11
]. Predicting the effect of climate change on livestock is
somewhat challenging due to the interrelationships that exist between the animal and its surrounding
environment, and the impact of human activity on these relationships [
8
]. It is also important to
consider the indirect effects of climate change on soil fertility and degradation, water availability, grain
yield, quality and availability, and spread of diseases/pathogens that may potentially impact the cattle
producers and their ability to manage periods of hot weather [9,12].
Irrespective of livestock productions contribution to climate change, animal production needs to
increase to satisfy consumer demand. A challenge regarding the effects of climate change on livestock
enterprises is how dependent the enterprise is on the thermal environment and what can be implemented
to offset the impacts of increasing temperatures [
9
]. The current effect of the thermal environment is
estimated by the impact of climatic conditions on animal performance, health, and welfare [9].
3. Heat Wave Events
Heat waves are defined as a number of successive days, typically three to five, where maximum
ambient conditions are above a specific threshold [
13
,
14
]. One predicted consequence of climate change
is the increased prevalence and intensity of heat waves [
15
]. Climatic trends of heat waves differ from
Animals 2019,9, 322 3 of 20
summer to summer, and future predictions suggest that the climatic behavior of heat wave events
over the years will continue to be varied [
16
,
17
]. Gaughan and Cawdell-Smith [
8
] suggested that
there is little doubt that there has been an increase in heat waves since the 1990’s. Although, over the
last 50 years there has been a significant advancement in the ability to predict and forecast climatic
events [
16
]. This ability to forecast heat wave events has enabled livestock producers to implement
mitigation strategies to prepare for forthcoming adverse climatic events.
The effects of heat waves on individual cattle are influenced by the intensity and duration of
the heat wave. It is well documented that feedlot cattle can be particularly susceptible to changes
in climatic conditions [
18
–
20
]. The susceptibility of feedlot cattle to heat load has been emphasized
during prolonged heat wave events and where conditions manifest with limited nighttime relief [
18
,
20
].
Numerous authors have reported heat wave conditions where cattle, particularly feedlot cattle, have
succumbed to heat load, for example:
•
February 1991–4000 deaths were recorded in Queensland (Australia) [
21
], with one feedlot
reporting 2680 deaths [
22
] during a heat wave event with high relative humidity and limited
air movement
•
July 1995–3750 deaths were estimated in Western Iowa, [
23
], and total deaths for the mid-central US
were over 4000 cattle [
24
]. This particular heat wave was associated with an estimated economic
loss of approximately $28 million contributed from production losses [20]
•
Hahn [
20
] reported the loss of 100 feedlot cattle in central Nebraska over a heat wave that had three
spikes in thermal loads. Deaths occurred during the third spike where it was hypothesized that ad
libitum feed intake resulted in large metabolic heat load and in conjunction with environmental
heat load, surpassed the animals’ ability to maintain thermal balance [20]
•
1999–over 5000 feedlot cattle died during an extreme heat wave in north-eastern Nebraska [
25
,
26
]
•
February 2000–1255 cattle died in southwestern New South Wales with deaths occurring after
a rainfall event where climatic conditions presented high relative humidity and high overnight
ambient temperature [22]
•
June 2017–4000 to 6000 dairy cows died in Fresno, Kings and Tulare counties USA [
27
] during a
heat wave
4. Defining Heat Load
Traditionally, the impact of hot weather has been referred to as heat stress. Buffington et al. [
28
]
suggested that heat stress is caused by a combination of environmental conditions that result in the
effective temperature of the environment to be greater than the temperature range of the thermoneutral
zone. This is somewhat misleading as the term heat stress by definition refers to the combination of
environmental conditions alone without consideration of animal factors [
21
,
28
]. However, factors, such
as genotype, coat type and coat color, diet type and diet composition, body condition, i.e., fat coverage
and deposition, performance, i.e., growth and lactation, health status, and degree of adaptation,
are known to influence thermal balance. Thus, throughout this review, the term heat load will be used
rather than heat stress, as the term heat load incorporates the cumulative effects of animal factors and
environmental conditions on the thermal comfort of animals [
21
] and, therefore, becomes a better
descriptor of an animal’s thermal balance.
Multiple Stressors
Animals that are adapted to a hot climate generally exhibit reduced growth and reproductive
efficiency [
29
], which is associated with the adaptive mechanisms that ensure survival [
30
]. In extensive
grazing systems, it has been identified that climatic constraints are not the only factor that negatively
influences livestock production. The indirect effects of climate change will also influence pasture
resources [
31
], potentially depriving grazing animals of nutrient requirements. Similarly, the changing
climate may also result in droughts, ultimately resulting in feed and water scarcity for grazing animals.
Animals 2019,9, 322 4 of 20
These situations can be associated with a decrease in growth and reproductive efficiency in livestock [
32
].
Furthermore, these animals may also be required to walk long distances under high solar loads to
find feed and water, imposing locomotor stress on grazing animals [
33
]. Therefore, it is important to
consider the impact of multiple stressors on livestock, this is particularly important to consider in
conjunction with climate change, as it is unlikely that animals will be exposed to a single stressor.
Numerous sheep and goat studies have evaluated the impact of multiple environmental stressors
(heat, nutritional, and walking) on production, reproduction, and ability to cope with stressful
conditions [
32
,
34
–
37
]. These studies have identified that when these species are exposed to a single
stressor, they are able to effectively cope without altering normal body functions [
38
]. However, when
these animals are exposed to two or more stressors simultaneously, the combined stress has a negative
influence on growth [
37
,
38
] and reproduction [
34
,
36
]. This is associated with the animal’s inability to
cope with cumulative effects of multiple stressors. In these instances, the animal’s body reserves are
not sufficient to effectively counter exposure to these stressors. As a result, the adaptive capability of
the animals is reduced, and there is an inability to maintain normal homeothermy [32,35].
Although the concept of multiple stressors is becoming a focal research topic in small ruminants,
the impact of multiples stressors has not been adequately researched, and as such, there is no information
on large ruminants. Therefore, it is essential to explore the impact of multiple stressors on both dairy
and beef cattle, particularly in conjunction with the changing global environment. Figure 1depicts the
proposed hypothetical model describing the concept of multiple stressors in cattle. The generation of
baseline information is vital as this will allow for the development of appropriate amelioration and
adaptive strategies to support livestock production systems.
Animals 2019, 9, x 4 of 21
efficiency in livestock [32]. Furthermore, these animals may also be required to walk long distances
under high solar loads to find feed and water, imposing locomotor stress on grazing animals [33].
Therefore, it is important to consider the impact of multiple stressors on livestock, this is particularly
important to consider in conjunction with climate change, as it is unlikely that animals will be
exposed to a single stressor.
Numerous sheep and goat studies have evaluated the impact of multiple environmental
stressors (heat, nutritional, and walking) on production, reproduction, and ability to cope with
stressful conditions [32,34–37]. These studies have identified that when these species are exposed to
a single stressor, they are able to effectively cope without altering normal body functions [38].
However, when these animals are exposed to two or more stressors simultaneously, the combined
stress has a negative influence on growth [37,38] and reproduction [34,36]. This is associated with the
animal’s inability to cope with cumulative effects of multiple stressors. In these instances, the animal’s
body reserves are not sufficient to effectively counter exposure to these stressors. As a result, the
adaptive capability of the animals is reduced, and there is an inability to maintain normal
homeothermy [32,35].
Although the concept of multiple stressors is becoming a focal research topic in small ruminants,
the impact of multiples stressors has not been adequately researched, and as such, there is no
information on large ruminants. Therefore, it is essential to explore the impact of multiple stressors
on both dairy and beef cattle, particularly in conjunction with the changing global environment.
Figure 1 depicts the proposed hypothetical model describing the concept of multiple stressors in
cattle. The generation of baseline information is vital as this will allow for the development of
appropriate amelioration and adaptive strategies to support livestock production systems.
Figure 1. Schematic highlighting the concept of multiple stressors on cattle (adopted and modified
from Sejian et al. [30]).
5. Implications of Hot Environmental Conditions
Animal responses to environmental stressors have been investigated for some time, and
although knowledge continues to be developed, managing livestock to reduce the negative impact of
hot weather remains challenging [18,20]. Reductions in dry matter intake (DMI), growth, feed
conversion efficiency [25,39,40], reproduction [41], milk production and milk quality [42,43], are
commonly observed when cattle are exposed to thermal stress. Quantifiable measures, such as
physiological, behavioral, and biological responses to heat load have been identified as indicators of
heat load. Physiological responses to heat load include increased sweating rate [14], respiration rate,
breaths per minute [44], panting score [45], and body temperature [46]. Behavioral responses include
alterations to posture, including increasing the proportion of time standing, increased duration in
shaded areas or increased shade seeking, including shade provided from other animals, and body
splashing at water troughs [47]. Biological markers in the blood are also indicators in determining
the level of stress an animal is under [48]. Cattle also use adaptive behaviors to reduce heat load,
primarily consisting of shade seeking, under shade structures or other animals, and the alignment of
Figure 1.
Schematic highlighting the concept of multiple stressors on cattle (adopted and modified
from Sejian et al. [30]).
5. Implications of Hot Environmental Conditions
Animal responses to environmental stressors have been investigated for some time, and although
knowledge continues to be developed, managing livestock to reduce the negative impact of hot
weather remains challenging [
18
,
20
]. Reductions in dry matter intake (DMI), growth, feed conversion
efficiency [
25
,
39
,
40
], reproduction [
41
], milk production and milk quality [
42
,
43
], are commonly
observed when cattle are exposed to thermal stress. Quantifiable measures, such as physiological,
behavioral, and biological responses to heat load have been identified as indicators of heat load.
Physiological responses to heat load include increased sweating rate [
14
], respiration rate, breaths per
minute [
44
], panting score [
45
], and body temperature [
46
]. Behavioral responses include alterations to
posture, including increasing the proportion of time standing, increased duration in shaded areas or
increased shade seeking, including shade provided from other animals, and body splashing at water
troughs [
47
]. Biological markers in the blood are also indicators in determining the level of stress an
animal is under [
48
]. Cattle also use adaptive behaviors to reduce heat load, primarily consisting of
Animals 2019,9, 322 5 of 20
shade seeking, under shade structures or other animals, and the alignment of the body in accordance
with solar radiation (W/m2) to reduce whole-body exposure to direct sunlight [49].
5.1. Nutrition and Eating Behavior
Heat production has a positive relationship with feed intake in ruminants, and it has been
shown that heat production is closely associated with feeding time [
50
]. Metabolic heat produced
during microbial fermentation [
51
], accounts for 3 to 8% of the total heat production by cattle [
52
].
As ambient heat load increases and DMI decreases there is a reduction in metabolic heat production [
50
].
During hot weather, cattle compensate for the hotter conditions by consuming smaller meals, more
frequently, and shifting feed intake to cooler parts of the day [
40
,
53
,
54
]. Voluntary feed intake has been
reported to commence declining when ambient temperature reaches approximately 25
◦
C to 27
◦
C [
55
].
However, the ambient temperature at which DMI begins to decline is influenced by diet type and
composition specifically diets with a greater proportion of roughage exhibit more rapid reductions in
DMI [
55
]. Variations in DMI are also influenced by breed (genotype), production status, health status,
body condition, and days on feed.
5.2. Water Intake
Water is available to animals in three forms, free drinking water, water in feed, and water
produced via oxidation of organic compounds or metabolic water [
56
]. Water requirements of cattle are
influenced by ambient conditions, diet type, breed (genotype), weight, and physiological functions [
57
].
Daily water intake is also influenced by a number of body functions, including the regulation of
core body temperature, growth and development, lactation and reproductive functions, digestion
and metabolism, and hydrolysis of proteins, fats and carbohydrates [
58
]. Water intake is linked to
DMI, with both feed intake and feed type influencing water intake [
59
]. Furthermore, water intake is
influenced by the amount of water gained from drinking, eating, via metabolic water, and the amount
of water lost per unit time through respiration, sweating, faces, urine, and lactation [
60
]. Arias and
Mader [
57
] reported that feedlot cattle finished in the summer consumed 87.3% more (p<0.01) water
compared to cattle finished during winter (32.4 L/d versus 17.3 L/d). Increased water consumption
during summer can be attributed to increases in urine volume (25%), respiratory tract evaporation
(54%), and evaporative heat loss, mainly due to sweating (177%) [
59
]. However, an increase in water
intake may also be a reflection of ruminants attempting to compensate for heat loads, particularly in
un-shaded grazing systems [61].
5.3. Metabolic Dysfunction
Digestion and absorption processes carried out by the animal are affected by the thermal
environment. Primarily, during heat load, absorbable nutrients are diverted from growth and
development and directed to maintaining homeostasis [
62
]. High heat load conditions are also
associated with a reduction in gut motility and rumination [
55
]. When cattle start to accumulate body
heat, i.e., core body temperature is increasing, there is a redistribution of blood flow from the internal
organs to the extremities [
63
], thus away from the gastrointestinal tract, or more specifically reduced
blood flow to the mucosa of the dorsal rumen (32%) and reticulum (31%) [
64
]. Given that there is
a reduction in DMI and blood flow to the gastrointestinal tract during heat load, the concentration
of absorbable nutrients per unit of blood volume must increase if the animal is to satisfy daily
requirements [55] and maintain normal bodily functions.
Additionally, heat load has been associated with a 7% to 25% increase in maintenance energy
requirements [
65
], which is associated with energy costs required to dissipate accumulated heat
load [
63
], e.g., via increased respiration rate. However, the increase in maintenance energy requirements
does not adequately describe the total increase in energy requirements as it does not include the
energy costs associated with protein synthesis or hematological responses that occur outside normal
homeostasis [
66
,
67
]. Therefore, a voluntary reduction in DMI is not beneficial to animal performance
Animals 2019,9, 322 6 of 20
and wellbeing. However, the reduction in DMI is an important contributing factor to the maintenance
of core body temperature. Additionally, the effect of heat load on digestion and nutrient partitioning
cannot be completely explained by the reduction in DMI [
43
,
68
]. Therefore, these metabolic changes
can potentially become classified as a part of the acclimation and adaptation to hot environments,
where many of the changes in metabolic pathways are not yet defined and/or understood.
5.4. Body Temperature
During periods of hot weather, an increase in core body temperature becomes a function of
heat accumulated and dissipated between the animal and the environment [
69
]. Therefore changes
in body temperature can be considered to be a reliable indicator of heat storage and disrupted
homeostasis [
70
,
71
]. However, it is important to consider that body temperature is not static and
exhibits a circadian rhythm [72,73], although is generally regulated within a ±1◦C gradient [46].
Under thermoneutral conditions, the core body temperature of cattle is between 38
◦
C to 38.5
◦
C [
74
]
and a rectal temperature greater than 42
◦
C is considered to be lethal [
75
]. Verwoerd et al. [
76
] concluded
that cattle were able to isolate their body temperature from the thermal environment during moderate
temperatures, however, when conditions become hot cattle are no longer able to cope with increasing
ambient conditions. Furthermore, Spiers et al. [
77
] indicated that rectal temperature of cattle increased
within 24 h after the onset of acute heat stress.
Under moderate conditions (18
±
7
◦
C) the diurnal rhythm of body temperature has been suggested
to lag ambient conditions by 8 to 10 h, i.e., body temperature will peak 8 to 10 h after the ambient
temperature has peaked [
24
]. However, during heat wave events (32
±
7
◦
C), the lag between body
temperature and ambient temperature decreases to 3 to 5 h [
24
]. This suggests that hot conditions
impede an animal’s capacity to remain in thermal equilibrium with its environment. This emphasizes
that when conditions exceed the thermoneutral zone there is a breakdown in the biological mechanisms
that regulate body temperature in bovines. Mehla et al., [
78
] indicated that as body temperature
increases towards 42
◦
C there are numerous effects on bodily functions: (i) direct damage to cells where
there is an increase in membrane fluidity and permeability, (ii) an increase in the animal’s metabolic
rate, and (iii) a reduction in blood flow around the body [
78
]. Above 42
◦
C homeostatic systems within
the body reach their upper critical limits for normal function [78], likely resulting in death.
5.5. Reproduction
Heat load has also been associated with impaired reproductive success in cattle. Some of the
negative impacts on reproduction can be associated with the increase in body temperature that occurs
during heat load. Declines in reproductive success are not isolated specifically to males or females
during periods of heat load. This is reflected by the numerous studies that have been conducted on the
impact of heat load on male and female reproduction in bovines and in other species, particularly sheep.
5.5.1. Impact on Males
Over the years, there has been an emphasis on the influence of heat load on male fertility and
the role that the scrotum plays in thermoregulation of the testicles. One consistent finding across
studies is that heat load, either via through scrotal insulation or whole body exposure, adversely
affects spermatogenesis and/or the viability of stored spermatozoa [
79
–
86
]. Furthermore, recovery
time from a single heat-related insult can be as long as eight weeks [
85
], however, recovery is likely
to encompass a full spermatogenesis cycle [
87
]. There have been no studies that have reported a
positive relationship between heat load and spermatogenesis. With the consequences of climate change
including predictions of more extreme weather events including heat waves as well as longer and
hotter summers, there is going to be the potential for increased incidences of heat load, thus thermal
insults on the scrotum. What has not yet been well defined is the ability of the scrotum to maintain
the optimal temperature for spermatogenesis during periods of heat load. Recently, studies have
evaluated scrotal temperature, and body temperature of Wagyu bulls, where scrotal temperatures were
Animals 2019,9, 322 7 of 20
remotely monitored whilst bulls were placed through a series of heat load regimes [
88
,
89
]. The findings
from these studies highlight that the mechanisms thought to maintain scrotal temperature start to
breakdown during periods of heat load [88,89].
5.5.2. Impact on Females
Heat load impairs numerous functions associated with establishing and maintaining pregnancy,
including altered follicular development and dominance patterns [
90
–
92
], corpus luteum regression [
90
],
impaired ovarian function [
93
], impaired oocyte quality and competence [
94
–
96
], embryonic
development [
97
,
98
], increased embryonic mortality and early fetal loss [
99
,
100
], endometrial
function [
101
], reduced uterine blood flow [
102
], and reduced expression of estrus and estrus behaviors,
i.e., mounting [
91
,
95
,
103
]. The impact of heat load on female reproduction may be more pronounced
in Bos taurus cows, however, this does not mean that there are no negative implications for Bos indicus
cows [95].
As heat load intensity increases there is a continuous decline in conception rates in lactating
cows [
91
,
104
]. Conception rates can be influenced by a heat load event during the month preceding
breeding to two weeks following breeding [
105
]. Heat load is also associated with smaller conceptus
size, which may influence maternal recognition of pregnancy and maintenance of corpus lutea
function [
99
]. Furthermore, heat load has been associated with compromising gestation during the
peri-implantation period, where there is an increased risk in early fetal loss between days 21 to 30 of
gestation [
94
]. This may be further confounded by a reduction in uterine blood flow, which may
also influence the availability of nutrients and hormones to the uterus [
102
]. However, as embryonic
development progresses, there is an increase in embryonic thermotolerance [97]. In conjunction with
climate change, it is probable that the impact of hot weather on reproduction may become more
pronounced. It has been suggested that some of the negative effects of heat load may be negated via
the use of mitigation techniques [
106
], however, Al-Katanani et al. [
96
] suggest that cooling cows for
42 days did not alleviate the impact of heat load on oocyte competence.
5.6. Health
Hot weather has a negative influence on animal bioenergetics, and as such has a negative influence
on animal performance, health, and well-being [
40
,
107
]. Heat load has been associated with an
increased incidence of nutrient deficiencies, respiratory alkalosis, ketosis, and ruminal acidosis [
108
].
Furthermore, in lactating dairy cows, heat load has been associated with an increased frequency and
incidence of clinical mastitis [
109
,
110
]. The health status of an animal is also likely to have a significant
influence on the animal’s ability to cope with heat load conditions. A study by Brown-Brandl et al. [
26
]
reported that animals with previous treatment history for pneumonia, anytime from birth to slaughter,
had respiration rates that were on average 10.5% higher compared to those never diagnosed or treated.
Similarly, previous and active health ailments have been reported to decrease average daily gains in
feedlot cattle [
26
,
111
]. The net effect of illness related fever and exposure to heat load conditions could
potentially result in an increased risk of mortality [
112
]. Animal health is also likely to be impacted
by disease-causing agents, including vectors and parasites that flourish during summer when the
conditions are hot and humid [108].
5.7. Productivity
During periods of high heat load, absorbable nutrients are diverted from growth and development
and directed towards maintaining body temperature [62,113].
5.7.1. Growth
Periods of heat stress are associated with reductions in growth, i.e., live weight gains [
114
] and
DMI [
40
,
55
]. As ambient heat load increases, cattle divert energy that is typically partitioned for
growth towards maintaining homeostasis [
71
,
108
], resulting in a reduction in growth and growth
Animals 2019,9, 322 8 of 20
efficiency. For feedlot cattle, this diversion of energy is associated with depressed growth rates,
whereby heat-related decreases in weight gain are approximately 10 kg, which coincides with a
seven-day increase in days on feed [
62
]. There is considerable variability in average daily gains and
feed conversion across feedlot studies [
31
,
115
–
121
]. However, it is probable that these are reflective of
weather conditions and cattle management throughout these studies. Overall reduced growth rate
increases days on feed, thereby increasing the cost of production.
5.7.2. Milk Production and Composition
It is widely accepted that milk yields decline during hot weather [
108
,
122
–
125
].
Ambient temperatures of 29
◦
C have been reported to reduce milk yield of dairy cows by 23% [
77
].
Additionally, it has been estimated that the energy requirement of the cow is 20% greater at 35
◦
C when
compared with the energy requirements at 20
◦
C [
126
]. Reductions in milk yield during heat load are
predominantly associated with reduced DMI [
127
]. However, only 35% to 50% of the reduction in
milk yield can be accounted for via the decrease in DMI [
43
,
68
]. Heat load is considered to have a
greater impact on high production cows [
42
,
126
]. This is not unexpected given the positive correlation
between increased milk yield, feed intake and metabolic heat production [
108
]. Purwanto et al. [
128
]
concluded that cows with milk yields of 18.5 kg/d and 31.6 kg/d had 27.3% and 48.5% greater metabolic
heat production (kJ/kgW
0.75
per h) when compared to dry cows. Another important consideration
is that the impact of heat stress conditions may have prolonged effects. A reduced milk yield may
be seen well after the heat load period has abated. Milk production may not return to pre-exposure
production levels as the energy deficit experienced combined with a decline in body condition score
cannot be compensated for, particularly in the high producing cow, resulting in a permanent reduction
in milk production for the remainder of that lactation [
127
]. This reduction in milk yield is directly
proportional to the length and severity of the heat load experienced and how adversely individual
cows were impacted by the heat load [127].
Heat load also has a negative association with milk fat and protein composition [
129
].
Climatic conditions appear to have the most influence on milk composition during the first 60 days of
lactation [
123
,
130
]. Furthermore, the stage of lactation, diet type and composition, health status of the
cow, cow genetics, and climatic conditions are all drivers of variation in milk protein [
129
,
131
].
Protein composition is further influenced by the protein secretion of the individual cow [
132
].
However, numerous authors have reported a negative relationship between heat load and milk
fat [
125
,
129
,
130
,
133
–
139
] and protein composition [
125
,
129
,
135
,
136
,
138
–
140
]. Garner et al. [
139
] found
that cows exposed to heat produced milk with a lactose and protein composition 49% lower than
thermoneutral control cows. These findings suggest that milk fat and protein composition is variable,
a portion of this variability can be contributed to climatic conditions. However, it is important to
consider that variations in milk composition are also related to genetic and nutritional factors [
141
,
142
].
5.7.3. Dark Cutting Beef
To date, there have been limited studies investigating the influence of hot and cold conditions on
carcass characteristics, meat quality or consumer acceptance. Anecdotally, Australian feedlots have
reported an increased incidence of “dark cutting” during the summer months, attributing this increased
incidence to heat load. Dark cutting, is a complex multifactorial problem that is influenced by numerous
pre-slaughter stress factors. Dark cutting is generally attributed to low muscle glycogen stores at
slaughter, which is predominantly a function of glycogenesis [
143
]. Muscle glycogen depletion has
been associated with numerous factors including, but not limited, to nutritional status, particularly in
grazing systems [
144
,
145
], water supply and quality [
143
], animal temperament [
145
,
146
], sex [
145
,
146
],
climatic conditions and climatic variability [
147
], and hormone growth promotants, however, this may
be confounded by sex [
148
]. Furthermore, periods of heat load are associated with a decrease in feed
intake [
40
,
50
,
55
,
149
]. This reduction in feed intake and whole-body exposure to stressors which may
result in lower muscle glycogen. Managing muscle glycogen is crucial to minimizing the incidence of
Animals 2019,9, 322 9 of 20
dark cutting beef. Further studies are required to examine the relationship between carcass attributes
and climatic conditions in cattle. Furthermore, the influence of environmental conditions and/or time
of exposure to these conditions on the incidence of dark cutting is yet to be established.
6. Mitigation Opportunities
The provision of alleviation strategies is paramount in supporting the animals to achieve comfort
and production goals. Heat load alleviation strategies are focused on reducing the impact of the thermal
environment and facilitate the ability to maintain normal body temperature [
150
] and ultimately
homeostasis. The use of cooling mechanisms is encouraged and reduces the impact of environmental
conditions on productive performance [
122
]. Heat loss is achieved through conduction, convection,
and radiation. However, all of these mechanisms are dependent on a thermal gradient [
42
]. As ambient
temperature increases there is a shift in the cooling mechanisms utilized by animals, i.e., transitioning
from non-evaporative cooling to evaporative heat loss [42].
Traditionally, strategies for mitigating of heat load have involved environmental modification
where the focus has been on (i) reducing solar radiation and (ii) increasing air movement [
39
].
However, there have also been studies investigating wetting cattle [
151
]. A study by Gaughan et al. [
152
]
investigated the influence of day and night cooling, through the use of water application and air
movement, on managing heat load as determined by changes in rectal temperature, respiration
rate, and DMI. Gaughan et al. [
152
] concluded that actively cooling cattle after maximum ambient
temperature occurred, was more effective at cooling cattle when compared to animals that were cooled
when ambient temperature was at its peak. Cattle that were cooled during peak ambient temperature
have been suddenly exposed to hot conditions, resulting in a rapid accumulation of body heat as these
cattle had not been required to initiate normal physiological responses to cope with heat load whilst
being actively cooled [151].
Whilst not covered in substantial detail here, the implementation of mitigation strategies will
become increasingly important in livestock production systems. There are numerous mitigation
opportunities available to producers, however, here an emphasis has been placed on (i) shade
structures, (ii) nutritional management, and (iii) genetics and genomic selection. Shade structures
are predominantly implemented in commercial industries globally, as they are cost effective and
relatively simplistic to implement. Nutritional strategies are becoming more prominent in research,
particularly in light of antibiotic resistance. Whilst it is well understood that genetics has an integral
role in thermotolerance, the genomic selection of livestock for heat tolerance is an emerging field of
study. Mitigation opportunities need to be evaluated for individual livestock systems to ensure that
the alleviation strategies implemented become an effective management tool for reducing the impact
of heat load in that particular enterprise.
6.1. Shade Structures
It has been well established that the provision of shade is an advantageous heat load alleviation
tool for lactating dairy cows [
28
,
114
,
151
,
153
–
160
]. The provision of shade structures reduces exposure
to direct solar radiation. However, shade structures do not alter ambient temperature or relative
humidity [
28
,
159
,
161
]. Shaded areas can reduce the radiant heat load of an animal by 30%, by simply
blocking out the sun [
162
]. Roman-Ponce et al. [
163
] showed that providing shade reduced black
globe temperature by approximately 8
◦
C. Therefore, providing shade for cattle presents a cooler
microclimate that cattle can utilize to seek relief from hot weather [
114
]. However, the beneficial aspects
of shade structures, i.e., reduced exposure to solar radiation, may be offset by a lack of air movement
under the structure itself [161].
The benefits associated with the use of shade structures during hot ambient conditions have been
of interest for many years [
40
]. The advantage of shade structures is that the application is passive,
where animals are able to utilize shaded areas voluntarily [
39
]. Schütz et al. [
153
] suggested that cows
preferred shade on days where ambient temperatures were
≥
30
◦
C. The authors also noted that shade
Animals 2019,9, 322 10 of 20
utilization was reduced when relative humidity was
≥
55% [
153
]. Furthermore, Schütz et al. [
155
]
reported that cows preferred shade that blocked out a higher proportion of solar radiation.
What remains clear is that as heat load increases, shade seeking behaviors also increase [
155
].
Entwistle et al. [
22
] reported that during a heat wave shade reduced the impact of severe conditions on
excessive heat load related deaths, whereas unshaded pens had a higher, 5.8%, mortality rate compared
with shaded pens, 0.2%. Schütz et al. [
156
] described that as heat stress conditions intensify there is an
increase in competition for shade between cows. However, there is also some conjecture regarding the
amount of shade, m2/animal, required to offset the impact of heat load.
6.2. Nutrition
Nutritional management strategies for cattle during hot conditions are focused on using (i) high
energy diets [
152
,
164
], (ii) feed additives such as betaine
[165–167]
, probiotic yeast supplements
[168–171]
,
and antioxidants [
172
], (iii) managing the proportion of roughage in the diet [
173
] and (iv) altering feeding
time to reduce metabolic heat loads during the hottest hours of the day [
174
]. However, there is considerable
variability in the success of these techniques during heat load. Further studies are required to ensure the
appropriateness of nutritional supplements as a heat load mitigation tool.
6.3. Genetics
An animal’s genotype is a major factor contributing to its susceptibility or tolerance to heat load.
It is widely acknowledged that Bos indicus breeds have greater heat tolerance compared to Bos taurus
breeds. Gaughan et al. [
29
] indicated that the identification of heat tolerant cattle is not a new concept,
as many breeds are already known for their thermal tolerance, i.e., Brahman and other Bos indicus
breeds [
25
]. Additionally, there are Bos taurus genotypes that are considered tropically adapted and
able to cope with hot weather. However, it is important to consider that the ability of heat tolerant Bos
taurus genotypes to cope with hot weather does not compare to animals of Bos indicus heritage [175].
Further consideration needs to be extended to the selection of breeding animals. Performance-based
selection of livestock has been used for numerous decades, i.e., selection of breeding stock based on
the phenotypic performance of economically important traits such as high growth rates. In future
years, producers will continue to select replacement breeding stock based on individual performances
for traits that are deemed economically important. Rhoades et al. [
176
] suggested that whilst genetic
improvement programs continue to place emphasis on these economically important traits, there is the
potential that this will decrease thermotolerance due to the relationship that is observed between animal
productivity and increasing metabolic heat production. This increase in metabolic heat production
typically reduces the thermoneutral zone of these animals, and in conjunction with climate change
may present some difficulty in managing cattle during hot weather.
6.4. Genomic Selection for Heat Tolerance
Recently, there have been studies investigating the potential for genomic selection for heat tolerance
in dairy cattle [
177
–
180
]. Genomic selection for heat tolerance has the potential to have cumulative and
permanent effects [
178
], on heat tolerance in production species. Whilst research in this area continues
to develop, the commercial viability of selection for heat tolerance needs to be evaluated. It is also
important to consider that the selection for one trait may have negative consequences for another trait.
It is generally accepted that improved heat tolerance comes at the cost of growth and reproduction [
29
].
However, there remains some conjecture regarding this, S
á
nchez et al. [
181
] suggested that cows
with higher heat tolerance would have a lower rate of decline in production, although cows that are
considered as ‘low production’ cows do not exhibit as severe declines in production [
182
], therefore
may be classified as thermotolerant. However, it is more likely that this thermotolerance is related to
the proportion of heat dissipation required by high production cows. It is known that high production
cows produce a greater proportion of metabolic heat. Cows with milk yields of 18.5 kg/d and 31.6 kg/d
had 27.3% and 48.5% greater metabolic heat production (kJ/kgW
0.75
per h) when compared to dry
Animals 2019,9, 322 11 of 20
cows [
128
]. Thus, high producing cows may be more susceptible to hot weather, regardless of genomic
selection. Furthermore, it is unclear if declines in milk production provide the ‘best’ evaluation of
heat tolerance in dairy cows. Other measures such as evaluation of body temperature may be a
more reliable estimate of heat tolerance. Some consideration must also be extended to the impact of
epigenetic mechanisms that regulate thermotolerance as well as understanding of transgenerational
effects [
183
,
184
]. Recently, there have been studies attempting to quantify epigenetic change in cattle
populations [184–188].
7. Adaptation and Acclimation
It is important to consider that all animals possess the capacity to adapt to their thermal
environment. Animals are capable of modifying their behavioral, physiological, and morphological,
or a combination of these, characteristics in response to the thermal environment [
7
]. Thus all animals
have developed survival techniques that minimize the effect that heat load has on the body as a whole.
The coping mechanisms developed by animals can be summarized into adaptation and acclimation.
Adaptation and acclimation have different meanings, however, they are often interchanged [21].
7.1. Acclimation
Acclimation is a homeostatic process that is driven by the endocrine system, resulting in cellular,
metabolic, and systemic changes, enabling animals to respond and cope with thermal stressors.
Acclimation can be separated into (i) developmental and (ii) reversible [
7
]. Developmental acclimation
refers to irreversible changes, and reversible acclimation refers to regulated animal responses, i.e., changes
in response to the changing seasons [
7
], such as changing coat characteristics. Therefore, acclimation can
be considered as a within a lifetime process whereby continuous exposure to a particular stressor, i.e.,
hot weather, results in biological adjustments thereby increasing the fitness of that individual animal to
survive in those conditions [
189
]. Horowitz [
189
] also indicated that a part of the acclimation response is a
widening in the dynamic range of body temperature, resulting in greater shifts in upper and lower critical
temperature. Hahn and Mader [
24
] reported that cattle appear to be acclimating when post heat wave
body temperature transitioned and stabilized around a new elevated temperature. Changing the dynamic
range in body temperature will have a positive influence on the regulation of body temperature through
adjustments to heat accumulation and dissipation from the body.
7.2. Adaptation
Adaptation refers to the biological change in successive generations by favoring genetic selection
within a population due to continuous stressor exposure that supports species survival [
190
]. Bos indicus
cattle evolved in tropical regions, with high ambient temperature and relative humidity and as a result,
these breeds of cattle have a number of genetic differences that support thermotolerance [
190
,
191
].
Therefore, the survivability of Bos indicus breeds in tropical environments arises from the adaptations
developed throughout successive generations. In grazing breeding herds there is the potential that
climate change will be a driver for the ‘natural’ selection for heat tolerant cattle, regardless of selection
pressures placed on the population. The adaptation of successive generations has the potential to
enhance the progeny’s ability to cope with hot conditions, although this is somewhat difficult to define
in bovines due to long generation intervals. When acclimation and adaptation occur, they provide a
level of resilience within cattle populations. Furthermore, in conjunction with the use of mitigation
opportunities, acclimation and adaptation have the potential to enhance cattle welfare and productivity
during periods of heat load.
8. Conclusions
Climatic conditions are an important regulator in agricultural production systems worldwide.
For livestock production, climate change has the potential to alter the thermal environment, which may
have a negative impact on welfare and productivity. It is clearly evident that the thermal environment
Animals 2019,9, 322 12 of 20
has an influence on the wellbeing and productivity of bovines. Regardless of climate change and the
predicted changes to the thermal environment, hot weather will continue to incite heat load responses
in cattle worldwide. Therefore, it is imperative that livestock production systems identify and utilize
mitigation strategies that are efficient and effective at reducing heat load. In future years, an integrated
approach to the adoption and management of mitigation opportunities will become increasingly
important to support the sustainability of livestock production systems.
In anticipation of climate change and climate variability, there is a need to develop a greater
understanding of the impact global warming is likely to have on biological parameters in cattle [
12
].
However, this may be somewhat misleading as there is a level of uncertainty in the climate change
predictions and what effect the changes will have on livestock in the coming decades. A more achievable
objective may be to identify and establish effective management strategies for livestock under suboptimal
conditions, rather than selection for maximum productivity and/or adaptability [
8
]. Furthermore, there
is a need to accurately quantify the indirect effects of climate change on livestock enterprises, such as
changing soil quality, water availability, grain, and pasture resources, and the changing distribution of
diseases and pathogens [
9
,
12
]. Developing a comprehensive understanding of the factors that influence
heat load, including climatic, environmental, and animal, will allow for innovative mitigation strategies to
be established. Enhancing mitigation strategies provides an opportunity for the continual improvement of
animal welfare and productivity during periods of heat load.
Author Contributions:
This review was conceptualized by J.B.G. and A.M.L., V.S., J.C.L., A.L.W., C.C.S., and T.L.M.
wrote sections of the review, contributing to the original draft. All authors contributed to reviewing of the final
draft, however, J.B.G., J.C.L., and A.M.L. conducted the final review and edited the manuscript prior to submission.
Funding: No external funding was received to prepare this review.
Conflicts of Interest: The authors declare no conflict of interest.
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