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Journal of Thermal Biology 77 (2018) 24–37

Contents lists available at ScienceDirect

Journal of Thermal Biology


journal homepage: www.elsevier.com/locate/jtherbio

A review and quantitative assessment of cattle-related thermal indices T


a,b c d e a,⁎
Xiaoshuai Wang , Bjarne Schmidt Bjerg , Christopher Y. Choi , Chao Zong , Guoqiang Zhang
a
Department of Engineering, Aarhus University, Blichers Allé 20, P.O. Box 50, 8830 Tjele, Denmark
b
College of Biosystems Engineering and Food Science, Zhejiang University, No. 866 Yuhangtang Road, 310058, Hangzhou, China
c
Department of Large Animal Sciences, University of Copenhagen, Grønnegårdsvej 2, 1870 Frederiksberg C, Denmark
d
Department of Biological Systems Engineering, University of Wisconsin-Madison, 460H Mall, Madison 53706, WI, United States
e
College of Water Resources and Civil Engineering, China Agricultural University, Beijing 100083, China

A R T I C LE I N FO A B S T R A C T

Keywords: Many thermal indices have been developed to assess the levels of heat stress imposed on cattle during hot
Cattle weather. In this paper, the 16 cattle-related thermal indices are critically reviewed. The primary emphasis is to
Heat stress evaluate each index's coherence to the typical heat transfer characteristics of a cow. Other perspectives including
Thermal index incorporated environmental parameters in the equation(s), experimental data, correlated physiological re-
Heat transfer mechanism
sponses, heat-stress thresholds, scope of application, specific cattle breed involved, and experiment location(s)
Equivalent temperature
are also well categorised and discussed. The coherence evaluation indicates that the main effects of environ-
Review
mental parameters on heat stress have been properly reflected, while some interactions between the parameters
have been treated differently. Given the variety of the equations used to define the 16 indices and the wide range
of information used to develop each index, we conclude that each thermal index is distinct to an extent that it
should be selected and employed carefully.

Greek letters TI Thermal index

εbg Emissivity of the black-globe, equals to 1 1. Introduction


σ The Stefan-Boltzmann constant, equals to 5.67 × 10−8
Heat stress is an aggregate of two sets of factors: 1) animal's meta-
bolization and physical activities that generate heat load, and 2) spe-
cific environmental factors (e.g., air temperature, relative humidity,
wind speed, and solar radiation) that affect the dissipation of the heat
Acronyms (Mader et al., 2006). As a constantly troubling issue in the tropics,
subtropics, and temperate regions during summertime (Hill and Wall,
BGHI Black global temperature humidity index 2014), heat stress occurs when an animal has troubles in getting rid of
CCI Comprehensive climate index its surplus body heat and maintaining a constant body temperature.
ERHL Effective radiation heat load Heat stress adversely affects dairy producers both economically and
ESI Environmental Stress Index ethically by reducing milk production and fertility rates and by im-
ET Effective temperature pairing animal welfare (de Andrade Ferrazza et al., 2017), and it has
ETI Equivalent temperature index traditionally incurred tremendous economic losses ($2 billion annually
HLI Heat load index in the US) to the livestock industry (St-Pierre et al., 2003). In recent
ITSC Index of thermal stress for cow years, the problems associated with heat stress often exacerbate as the
Nu Nusselt number density of the animals increases, particularly in large-scale indoor dairy
Re Reynolds number operations.
RRI Respiration rate index The effect of heat stress on cattle has been intensively studied for
Sh Sherwood number several decades because of its importance to the success of cattle hus-
THI Temperature humidity index bandry. Due to the increasing concerns about climate change and


Corresponding author.
E-mail address: guoqiang.zhang@eng.au.dk (G. Zhang).

https://doi.org/10.1016/j.jtherbio.2018.08.005
Received 5 March 2018; Received in revised form 4 August 2018; Accepted 7 August 2018
Available online 09 August 2018
0306-4565/ © 2018 Elsevier Ltd. All rights reserved.
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

Nomenclatures sr Solar Radiation, W m-2


Sp Solar irradiance obtained directly by means of a pyr-
DSRadj Direct solar radiation correction factor, °C anometer, W m-2
SRadj Surface temperature correction factor, °C RADadj Radiation correction factor, °C
hbg the convective heat transfer coefficient of the black-globe, Ta Air temperature, °C
W m-2 °C-1 Tbg Black-globe temperature, °C
Hc Rate of convective heat dissipation, W Tdp Dew point temperature, °C
Hcd Rate of conductive heat dissipation, W Tequ Equivalent air temperature change, °C
Hsk Rate of heat dissipation by sweating, W Tgs Ground surface temperature, °C
Hr Rate of heat dissipation by respiration, W Trm Mean radiant temperature of the environment, K
Hrad Rate of radiative heat flow, W Ts-ave The average afternoon hair coat surface temperature, °C
Hs Rate of heat stored in animal body, W Tsk Skin temperature of cow, °C
M Metabolic heat generation rate, W Twb Wet bulb temperature, °C
Pva Air partial vapour pressure, kPa v Air velocity, m s-1
RHadj Relative humidity correction factor, °C Vadj Air velocity correction factor, °C
rh Relative humidity, %

wellbeing of animal, as well as the increasing scale of today's farming 2. Heat balance of cattle
operations, more and more researchers and farmers have expressed
interest in heat stress abatement approaches. Currently, cooling heat- Cattle dissipate heat by means of conduction, convection, radiation,
stressed animals is one of the most commonly applied approaches and evaporation (Maia and Loureiro, 2005). Fig. 1 illustrated the heat
(West, 2003). To properly implement a cooling strategy involves first balance between a housed standing dairy cow and the ambient en-
making a fast and accurate evaluation of the heat stress imposed on the vironment.
animals. To quantitatively assess the heat stress imposed on cattle, According to the heat transfer mechanism, the heat balance of a cow
many cattle-related thermal indices have been developed, and all have can be expressed as Eq. (1) (Baeta et al., 1987; da Silva et al., 2015):
proved able to acceptably assess the heat stress levels. However, dif-
M = Hcd + Hc + Hrad + Hr + Hsk + Hs (1)
ferences in breed, modelling methods, and investigation emphases (not
to mention climate type and other factors) will often result in differing where, M represents metabolic heat generation rate (W); Hcd, Hc, Hrad
results, depending on which particular index is applied. Accordingly, it represents the heat dissipation via conduction, convection and radia-
is reasonable to conclude that a thermal index may produce significant tion, respectively (W); Hr and Hsk represents the evaporative heat dis-
inaccuracies if it is applied without considering its specific assumptions, sipation form respiration and skin, respectively (W); Hs represents the
the type of thermal environment it typically assesses and the methods heat storage in animal body (W).
that were used to derive the index. To avoid potential misapplication of Note that a negative value of Hcd, Hc, or Hrad means the animal is
a thermal index, a comprehensive understanding of all the indices is gaining heat from the ambient environment via the specific transport
essential. Most certainly, any effort to achieve such an understanding mechanism. A positive value of Hs means that extra heat is accumu-
could be facilitated by a comprehensive review of the existing cattle- lating in the animal's body and will lead to changes in physiological
related thermal indices and the crucial information relating to index responses, such as an increase in respiration rate and sweating rate.
development. Our survey of the literature associated with heat-stress
evaluation uncovered no such review; therefore, we have reviewed
3. Evaluation method used in this work
sixteen thermal indices that were judged worthy of consideration.
In this review, we first provide a brief description of the heat ex-
3.1. Definition of equivalent air temperature change
change process that occurs between a dairy cow and its environment.
Then we present systematic reviews of the sixteen cattle-related
To evaluate the performance of each thermal index in assessing
thermal indices, including the information related to the development
thermal effects of environmental parameters, we used a measure, re-
of each index and its relevance to the heat transfer characteristics of the
ferred to as equivalent air temperature change (Tequ), which was de-
breed being analyzed. Finally, in a summary, we explain why we be-
fined as a change in air temperature (e.g., from Ta1 to Ta2) such that the
lieve that new cattle-related thermal indices should be developed.
variation of thermal index caused by a change in another

Fig. 1. Illustration of the mechanisms related to the heat exchange of a housed cow.

25
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

environmental parameter (e.g., relative humidity from rh1 to rh2, air cases because domestic animals are mostly confined in barns where air
velocity from v1 to v2, or solar radiation from sr1 to sr2, at air tem- movement is low and solar radiation is effectively blocked (Li et al.,
perature of Ta1) is equal to a variation of the same thermal index caused 2009).
by the change in air temperature (from Ta1 to Ta2) but keeping the other Four different formulae for calculating the THI are usually be ap-
environmental parameters unchanged. Eqs. (2) and (3) were listed to plied to evaluate the heat stress level imposed on cattle, as expressed in
further explain the calculations of equivalent air temperature change Eqs. (4)–(7). Note that, the “Ta × 1.8 + 32” is a term that converts air
(Tequ). temperature from Celsius to Fahrenheit. The reason for doing the
conversion is that most previous such indices were calculated using the
TITa1, rh2, v1, sr 1 = TITa2, rh1 v1, sr 1 (for a change from rh1 to rh2)
Fahrenheit scale (Bernabucci et al., 2014).
TITa1, rh1, v 2, sr 1 = TITa2, rh1, v1, sr 1 (for a change from v1 to v2)
TITa1, = TITa2, (for a change from sr1 to sr2) THI 1 = (0.35×Ta+0.65 ×Twb) × 1.8 + 32 (4)
rh1, v1, sr 2 rh1, v1, sr 1 (2)

Tequ = Ta1 − Ta2 THI 2 = (1.8×Ta + 32)−[(0.55 − 0.0055×rh) × (1.8×Ta − 26)] (5)
(3)

where TITa1, rh2, v1, rad1 represents the value of a thermal index when the THI 3 = (0.55×Ta+0.2 ×Tdp)×1.8 + 32 + 17.5 = Ta+0.36 ×Tdp + 49.5
air temperature is Ta1, relative humidity is rh2, air velocity is v1 and (6)
solar radiation is sr1.
A positive value of Tequ indicates that the thermal effect associated THI 4 = Ta+0.36 ×Tdp + 41.5 (7)
with a variation in the investigated parameter of the corresponding where, Tdb, Tdp, Twb are ambient dry bulb temperature, dew point
thermal index was treated as a heating effect on heat stress, whereas a temperature and wet bulb temperature, respectively (°C); rh is relative
negative value indicates a chilling effect. Additionally, a larger absolute humidity (%).
value of Tequ implies a stronger chilling/heating effect in the corre- In a study by Bianca (1962), aimed at developing THI1, the re-
sponding index. spective weighting of air temperature and humidity (in the forms of dry
bulb and wet bulb temperature, respectively) in terms of their influence
3.2. Spans of environmental parameters in the evaluation in causing heat stress was evaluated. Four 9-month-old Ayrshire bull
calves were confined in a climatic room and exposed to nine different
In our evaluations, four levels of air temperature, 25, 30, 35 and environmental conditions. Nine tests with different air temperature
40 oC, were selected because cattle normally experience heat stress in (from 30 to 50 °C) or/and dew point temperature (from 8.3 to 30.6 °C)
this range (West, 2003). Three levels of relative humidity were used, were conducted. The rectal temperatures were measured as physiolo-
which are determined according to the respective application range of gical heat stress indicator. Bianca (1962) found that the regression
relative humidity. The evaluation aims to include all climate regions of coefficients of 0.35 and 0.65 for dry-bulb and wet-bulb temperatures
the world where heat stress among cattle may be a significant issue, and closely corresponded to the rectal temperature responses, and THI1 was
to respect the validity of the index concerned, including whether it is proposed based on this finding.
meant for indoor cattle, outdoor cattle or both. THI2 and THI3 appeared in “A Guide to Environmental Research on
For the sake of consistency, all the air-velocity increments used in Animals” (NRC,1971). However, the information concerning the de-
each evaluation were assumed to increase from 1 to 2 m s-1, and all the velopment of THI2 and THI3 in this book proved to be insufficient.
solar radiation increments were assumed to increase from 400 to There are some comments relating to THI2 found in literature: 1)
500 W m-2. The change from 1 to 2 m s-1 and from 400 to 500 W m-2 are Bohmanova et al. (2007) pointed out that THI2 was designed to reveal
both chosen to represent an increase in the middle of the range for these the heat stress level of cattle outdoors, and 2) Hahn et al. (2003) found
parameters in indices where they are included. that THI2, at the time the study was conducted, has been intensively
used with respect to different environments. Besides, given condition
4. Cattle-related thermal indices with saturated air (rh = 100% and Ta = Twb), both THI1 and THI2 are
equal to the dry-bulb temperature, which indicates that the evaluations
The index reviews in this section are presented in chronological of the humidity effect used to define both THI1 and THI2 were based on
order in which these indices were first developed. Each sub-section a saturation point, and any decline in air humidity (from that a sa-
reviews one index (or in some cases several similar thermal indices), turation point) will be interpreted as a decrease in the index.
beginning with an overview of the respective thermal index/indices and THI4 was first described in “A Stress Physiology in Livestock” by
ending with an assessment of the index's coherence to the heat transfer Yousef (1985). While the authors did note that THI4 was developed to
characteristics of cattle and the environment. A summary of the as- specifically assess heat stress in Holsteins, they provided little in-
sessments on all the reviewed thermal indices is provided in the final formation related to how the index was developed.
sub-section.
4.1.2. Assessment of the THIs
4.1. Temperature humidity index Using the equivalent temperature method, a study comparing the
four THIs was conducted. Fig. 2 shows the variations in equivalent
4.1.1. Overview temperature associated with a relative humidity increment of from 50%
The temperature-humidity index (THI) was developed as a means of to 60% in each THI as air temperature rose from 25 to 40 °C. Note that,
quantifying the level of discomfort experienced by a human during the because the weights of the dry-bulb temperatures and dew-point tem-
summer season. It was therefore originally referred to as “discomfort peratures of THI3 and THI4 were the same, they were plotted on the
index” by Thom (1959) after concluding that the evaluation of heat same curve.
stress using air temperature alone would tend to fail as a measure of As can be seen, the Tequ of a relative humidity increase of from 50%
discomfort. Bianca (1962) and Berry et al. (1964) extended this concept to 60% at 25 °C was approximately 0.8 °C for THI2, THI3, and THI4,
to estimate heat stress imposed on cattle. while the Tequ for THI1 at 25 °C was about 1.1 °C. As the air temperature
The THI is one of the most widely used thermal indices (Mader rose from 25 to 40 °C, the Tequ increased from 1.1 to 1.5 °C for THI1,
et al., 2006) because 1) it is simple to apply, as both involved compo- from 0.8 to 1.9 °C for THI2, and from 0.8 to 0.9 oC for THI3 and THI4.
nents (air temperature and humidity) are easy to measure; 2) the THI The increment rate of Tequ associated with THI2 was the largest, fol-
can predict the thermal environment accurately and quickly in many lowed by that associated with THI1.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

expressed in Eq. (8):

BGHI = Tbg +0.36×Tdp + 41.5 (8)

where, Tbg is the black globe temperature (°C).


Black-globe temperature is a comprehensive temperature that
combines the integrated effects of air velocity and solar radiation
(Dimiceli et al., 2013; Gaughan et al., 2008). The black-globe tem-
perature used in the development of BGHI was obtained by measuring
the surface temperature of a 15-cm-diameter black copper sphere fixed
at a height of 2.1 m above ground. The environmental data were listed
in Table 1. A comparison of the BGHI and THI4 showed that the BGHI
had a better correlation with milk yield (r2 = 0.355) than did THI4 (r2
= 0.263) when the cows were exposed to solar radiation (Buffington
et al., 1981). No obvious difference between THI4 (r2 = 0.244) and
BGHI (r2 = 0.228) for shaded cows has been found.
Fig. 2. The equivalent air temperature changes (Tequ) associated with a relative
humidity increase of from 50% to 60% in each THI as air temperature rises from
25 to 40 °C.
4.2.2. Assessment of the BGHI
Due to the lack of Tbg data, a quantitative assessment of the co-
4.2. The black-globe temperature humidity index herence to heat transfer characteristics has been omitted. It seems ap-
propriate to use black-globe temperature in an evaluation of the heat
4.2.1. Overview stress imposed on cows, particularly with respect to cows exposed to
Buffington et al. (1981) developed a black-globe temperature-hu- solar radiation, because black-globe temperature integrates the thermal
midity index (BGHI) based on THI4 by replacing the dry-bulb tem- effects of air temperature, air velocity, and solar radiation.
perature with a field-measured black-globe temperature (Tbg), as

Table 1
The application range and information on environmental parameters of thermal indices.
Thermal index Application ranges Information on environmental parameters in experiment

THI1 Not stated Ta: 30–50 °C;


Twb: 20.4–32.5 °C
THI2, THI3, and THI4 Not stated Not stated
BGHI Not stated Shade: No shade:
Ta: 27.52 ± 3.35 °C Ta: 27.88 ± 3.72 °C
Tbg: 28.43 ± 3.10 °C Tbg: 36.74 ± 7.30 °C
Tdp: 23.70 ± 1.51 °C Tdp: 23.70 ± 1.51 °C
v: 2.10 ± 1.10 m s−1 v: 2.00 ± 1.05 m s−1
sr: 0 W m−2 sr: 432.5 ± 237.38 W m−2
ETI Ta: 16–41 °C; Ta: 15.9–41.0 °C;
rh: 40–90%; rh: 39.8–90.2%;
v: 0.5–6.5 m s−1 v: 0.5–6.5 m s−1
ET1 Ta: 4–30 °C; Ta: 3.9–30.5 °C;
v: 0–2.25 m s−1 v: 0.27–1.92 m s−1
ET2 Not stated Summer: Autumn:
Ta: 26.5–32.8 °C Ta: 16.2–19.9 °C
Tbg: 36.4–46.2 °C Tbg: 29.5–37.4 °C
RRI1 Ta: > 25 °C; Period YtDa, days Ta, °C rh, % v, m s−1 sr, W m−2
1 162–167 23.52 ± 0.13 66.70 ± 0.41 4.53 ± 0.04 340.20 ± 8.58
2 176–180 25.61 ± 0.11 63.73 ± 0.33 4.77 ± 0.04 320.12 ± 9.01
3 187–191 27.55 ± 0.11 70.53 ± 0.42 3.16 ± 0.03 327.67 ± 9.20
4 197–206 27.97 ± 0.08 72.46 ± 0.28 2.70 ± 0.02 295.88 ± 5.81
5 215–220 28.65 ± 0.11 65.58 ± 0.50 2.17 ± 0.03 273.18 ± 7.11
6 225–229 22.53 ± 0.11 79.87 ± 0.49 2.27 ± 0.03 266.23 ± 8.04
7 239–243 23.87 ± 0.14 76.50 ± 0.58 1.88 ± 0.03 248.52 ± 8.15
8 262–264 17.94 ± 0.20 81.85 ± 0.71 2.68 ± 0.05 236.15 ± 10.78
RRI2 and RRI3 Not stated Not stated
adjusted-THI Ta: 15–40 °C; Hourly (14:00–17:00) Daily
rh: 35–90%; Ta: 17.2–36.0 °C; Ta: 15.6–29.4 °C;
rh: 37.5–98.5%; rh: 62.5–92.7%;
v: 1.0–8.4 m s−1 v: 1.2–6.3 m s−1
sr: 17.6–971.7 W m−2 sr: 56.7–361.5 W m−2
HLI Not stated Not stated
CCI Not stated Summer conditionb
Ta: 19.22–36.36 °C;
rh: 34.36–96.60%;
v: 0.45–7.30 m s−1
sr: 0–1115.32 W m−2
ITSC Not stated Not stated

a
Year to date.
b
CCI contains summer condition and winter condition, but herein only summer condition was shown.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

4.3. The equivalent temperature index increment lasted 30 min, and a 15-min time interval was set with no air
movement.
4.3.1. Overview The authors concluded that the weighting ratio of air temperature
Baeta et al. (1987) proposed an equivalent temperature index (ETI) (Ta) and the square root of air movement (v0.5) varied from 1:–9.2 to
for evaluating the heat stress conditions of housed cattle (Eq. (9)). The 1:–10.5 with respect to the variations in respiration rate and the cows’
ETI is based on laboratory experiments that involved five high-produ- mean skin temperature. Accordingly, an effective temperature index
cing Holstein dairy cows in a controllable climatic chamber. (marked as ET1), as expressed in Eq. (10), was developed:

ETI = 27.88 − 0.456×Ta+0.010754×Ta2−0.4905×rh+0.00088×rh2+1.15×v ET 1 = Ta−10(v 0.5) (10)


−0.12644×v 2+0.019876×Ta × rh−0.046313×Ta × v (9) Afterwards, Yamamoto et al. (1994) developed a second effective
where, v is the air velocity (m s-1). temperature index (marked as ET2) that could be used to evaluate the
During testing, cows were exposed to twenty-one environmental effect of solar radiation on the thermoregulatory physiological re-
scenarios, as listed in Table 2. Every scenario lasted three days and was sponses of young cattle. The black-globe temperature was used as a
followed by a 1- to 7-day recovery period spent in a comfortable en- measure of solar radiation. The meteorological data and physiological
vironment (that is, 18 °C in Ta, 50% in rh, and 0.5 m s-1 in v) to let the response data were measured and averaged every half hour from
cows return to their normal milk-production levels. During the entire 13:00–16:00 in summer and from 12:30–15:30 in autumn. With respect
experimental period, physiological responses, including milk produc- to respiration rate and mean body temperature, the weighting ratio of
tion, rectal temperature, and hair coat temperature, were recorded. air temperature (Ta) to the temperature difference between black-globe
The ETI is designed as the equivalent air temperature under con- temperature and dry bulb temperature (Tbg – Ta) was determined as
dition of 40% relative humidity and 0.5 m s-1 air velocity. Any changes 1:0.76. Thus, the second effective temperature (ET2) was
in relative humidity and air velocity will thus be translated to equiva- ET 2 = 0.24Ta+0.76Tbg (11)
lent temperatures with respect to milk production and heat loss rate.
The ETI developers noted that the ETI should only be used when the
ambient temperature ranges from 16 to 41 °C, relative humidity ranges 4.4.2. Assessment of the ETs
from 40% to 90%, and air velocity ranges from 0.5 to 6.5 m s-1. With respect to ET1, the effect of air movement on the rate at which
heat is lost from a cow is adjusted to a temperature scale in an ex-
4.3.2. Assessment of the ETI ponential relationship. The exponent of 0.5 in ET1 is very close to the
Fig. 3 shows the equivalent air temperature change (Tequ) as air exponent of 0.53 that was obtained from a laboratory experiment in-
velocity increased from 1 to 2 m s-1 with the air temperature rising from volving a six-cylinder artificial cow model (Wiersma and Nelson, 1967).
25 to 40 °C at three different relative humidity levels (40%, 65%, and This power function, which is related to air velocity, demonstrates the
90%). The relative humidity levels were determined based on the ap- relationship that the chilling effect decreases at an incremental rate as
plication range of ETI (Baeta et al., 1987). air velocity increases. However, as an index capable of revealing the
According to Fig. 3, we can find that: 1) all the values of Tequ were thermal effect of air velocity on heat stress, ET1 fails to consider the
negative, indicating that the ETI assumes that any increase in air ve- interaction occurring between air temperature and air velocity.
locity will have a chilling effect; 2) for all of the three relative humidity Due to the incorporation of black-globe temperature, ET2 could be a
levels, the value of Tequ decreased as the air temperature rose, which good heat-stress indicator for cattle subjected to solar radiation because
implies that the ETI assumes the chilling effect associated with in- it can reflect the main effect of solar radiation. However, ET2 should
creasing air velocity will increase as air temperature rises; 3) the value not be regarded as a good indicator of heat stress in housed/shaded
of Tequ at a fixed air temperature increases as relative humidity in- cattle because it cannot provide much more than the indoor air tem-
creases, indicating that ETI assumes the chilling effect associated with perature.
an increasing air velocity decreases as relative humidity rises at a fixed Also, due to the specific objectives of both effective temperature
air temperature in the ETI. studies, the thermal effect of relative humidity on the heat stress im-
Besides, a review of the literature indicates that the ETI has not been posed on cattle was neglected in both indices. For this reason, both
widely accepted or applied. Perhaps this is because, as Hahn et al. effective temperature indices may be problematic under humid condi-
(2009) pointed out, the ETI was derived from observations of the test tions.
animals’ milk production over a period of only 3 days and therefore the
results might not reflect longer-term effects. 4.5. The respiration rate indices

4.4. The effective-temperature index 4.5.1. Overview


Since the significant correlation between respiration rate and the
ET was used as the abbreviation of the effective-temperature index heat-stress level was first established, three indices related to respira-
in this study, in order to distinguish it from the equivalent temperature tion rate (all specific to unshaded cattle) have been developed as
index – ETI in Section 4.3.
Table 2
4.4.1. Overview Combinations of environmental scenarios, cited from (Baeta et al., 1987).
To determine the effects of air temperature and air speed on ther- Scenario # Ta, °C rh, % v, m s-1 Scenario # Ta, °C rh, % v, m s-1
moregulatory physiological responses (i.e., rectal temperature, mean
20 20 50 1.7 17 15.9 65 3.5
skin surface temperature, respiration rate, and heart rate), Yamamoto
12 32 50 1.7 9 36.1 65 3.5
et al. (1989) conducted an experiment with four lactating Holstein cows 8 20 80 1.7 5 26 39.8 3.5
in an environmental chamber. Six levels of air temperature (i.e., 4, 8, 18 32 80 1.7 7 26 90.2 3.5
12, 18, 24, and 30 °C) coupled with four levels of air velocity (i.e., 0.60, 16 20 50 5.3 6 26 65 0.5
1.00, 1.60, and 2.25 m s-1) were continuously tested in 6 days with one 14 32 50 5.3 2 26 65 6.5
10 20 80 5.3 1,3,4,13, 15, and 26 65 3.5
temperature setting per day from 11:00–16:00. During the experimental
19
period, the air velocity measurements began at 0.6 m s-1 and continued 11 32 80 5.3 Extra 41 39.8 0.5
as the velocity gradually increased to 2.25 m s-1. Each air velocity

28
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

quadratic effects (i.e., Tdp2, Ta2, v2, Tdp*Ta, and Ta*v). In order to take
the effect of cattle breed into the estimation of respiration rate, the
average afternoon temperature of the hair-coat surface (Ts-ave) was
linearly incorporated in both RRI2 and RRI3, which was 42.7 °C for
Angus, 42.1 °C for MARC III, 40.8 °C for Gelbvieh, and 38.4 °C for
Charolais (Brown-Brandl et al., 2003).

4.5.2. Assessment of the RRIs


According to the equations used by the RRIs, an increase of 1 m s-1
in air velocity will result in a decrease of 1.7 and 1.53 breaths min-1 in
RRI1 and RRI2, respectively, whereas an increase of 100 W m-2 in solar
irradiance will contribute an increase of 3.9, 3, and 3 breaths min-1 in
RRI1, RRI2, and RRI3, respectively.
Fig. 4 shows the variation in respiration rate predicted by RRI1,
RRI2, and RRI3 as air temperature rises from 25 to 40 °C under 3 levels
Fig. 3. Equivalent air temperature changing (Tequ) of air velocity increase from of relative humidity (65%, 72.5%, and 80%). In this calculation, the air
1 to 2 m s-1 as air temperature rises from 25 to 40 °C at three relative humidity velocity and solar radiation were fixed at 1 m s-1 and 100 W m-2, re-
levels (40%, 65%, and 90%). spectively. Additionally, RRI2 and RRI3 also assume a skin temperature
of 40.8 °C.
measures of heat stress, as expressed in Eqs. (12)–(14): As Fig. 4 shows, the predicted respiration rate associated with RRI1
increased as both air temperature and relative humidity rose, whereas
RRI 1 = −105.7 + 5.1×Ta+0.58×rh − 1.7×v+0.039×sr (12)
the respiration rate associated with RRI2 increased as air temperature
RRI 2 = −183.6 + 4.22×Ts − ave+3.89×Ta−0.07×Tdp−1.53×v+0.03×sr rose, but it did so independently of changes in relative humidity. In
addition, the respiration rate predicted by RRI3 (which is associated
(13)
with an RH of 80%) does not increase as air temperature increases.
RRI 3 = −223.7 + 4.23×Ts − ave−4.10×Ta−12.42×Tdp+3.50×v+0.03×sr Fig. 5 shows that the equivalent air temperature change (Tequ) as air
velocity increased from 1 to 2 m s-1 and air temperature rose from 25 to
+0.12 ×Ta2−0.50 × Tdp
2
+0.3×v 2+0.22 ×Ta × Tdp−0.21×Ta × v 40 °C at a relative humidity of 50%.
(14) The values of Tequ for all three RRIs were negative, indicating that
-2 all the RRIs treat the thermal effect that an air velocity increase has on
where, sr is the solar irradiance (W m ); Ts-ave is average afternoon hair
heat stress as a chilling effect. The Tequ associated with both RRI1 and
coat surface temperature (°C).
RRI2 was not affected by rises in air temperature, whereas the Tequ
RRI1 was developed by Eigenberg et al. (2005) based on field
associated with RRI3 decreased as the air temperature increased. Such a
measurements with eight crossbred steers (1/4 Angus, 1/4 Hereford, 1/
decline in Tequ indicates that, with regard to RRI3, the chilling effect
4 Pinzgauer, 1/4 Red Poll). There were eight experimental periods
produced by any increase in air velocity increases as the air tempera-
within a 4-month time span, and each experimental period lasted, on
ture rises.
average, 4.5 days. Information related to environmental parameters can
Besides, both RRI2 and RRI3 incorporate breed effect into their
be found in Table 1. Linear regression analysis was employed to de-
predictions of respiration rate by adding the term Ts-ave. However,
velop the RRI1. Note that RRI1 can only be used to estimate respiration
making a prediction that takes into account this physiological para-
rates when the air temperature exceeds 25 °C under no-shade conditions
meter also depends greatly on the level of solar radiation; in other
(Eigenberg et al., 2005).
words, applying either RRI2 or RRI3 requires additional measurements
RRI2 and RRI3 were both developed by Brown-Brandl et al. (2005).
of skin surface temperature.
Five different modelling methods (two regression methods, a data-de-
pendent fuzzy inference system, a data-free fuzzy inference system, and
a neural-network model) were used to establish the relationship be- 4.6. The adjusted THIs
tween respiration rate and the environmental parameters (i.e., Ta, Tdp,
v, and sr). RRI2 is a linear regression model considering the linear ef- 4.6.1. Overview
fects of four environmental parameters (i.e., Ta, Tdp, v, and sr) and RRI3 Mader et al. (2006) improved the predictive ability of THI2 by
is a quadratic model that considers not only the five linear effects adding the linear effects of wind speed and solar radiation. The data
considered by RRI2, but also five additional significant interaction and used (except for solar radiation data) were all collected continuously

Fig. 4. Respiration rates predicted by RRI1, RRI2, and RRI3 as air temperature increases at 3 different relative humidity levels − 65% (a), 72.5% (b), and 80% (c),
when air velocity is 1 m s-1, and solar radiation is 100 W m-2.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

an air-velocity increase as a chilling effect; 2) no variation of the Tequ in


either adjusted THIs has observed as air temperature increases, in-
dicating that both adjusted THIs assume that air temperature rise has no
effect on the chilling effect of a certain air velocity increment; 3) the
values of Tequ in both indices decrease as the relative humidity in-
creases, which indicates that both indices assume that the chilling effect
of a certain air velocity increment decreases as relative humidity in-
crease.

4.7. The heat load index

4.7.1. Overview
Gaughan et al. (2008) proposed a heat load index (HLI) that in-
corporated black-globe temperature, relative humidity, and wind speed
to predict heat-stress levels and thereby aided the heat-stress abatement
strategies inside cattle barns during hot weather. Data from 13 feedlots
(ten of them located in Australia, and the rest located in the United
Fig. 5. Equivalent air temperature change (Tequ) as air velocity increases from 1
to 2 m s-1 for RRI1, RRI2, and RRI3 as air temperature rises at a relative hu- States) were used to develop and evaluate the HLI. All the environ-
midity of 50% (Ts-ave = 40.8 °C). mental data were recorded at 10-min intervals by automated weather
stations located in each feedlot. The panting scores of 2490 unshaded
Angus steers were compiled from visually recorded data and used to not
and compiled hourly by a weather station located in the centre of the
only develop the index but also classify the heat-stress thresholds. Based
feedlot facility. The solar radiation data were obtained from a nearby
on an analysis of panting-score data, a black-globe temperature
weather station (High Plains Climate Centre). The data ranges can be
threshold of 25 °C was identified, above which the panting score of
found in Table 1. Panting rates, via direct visual observation, was used
more than 20% of the cattle increased from 0 to 1. Thus, it was decided
as a heat-stress physiological indicator. Linear regression was used to
that the black-globe temperature of 25 °C would serve as a “knee point”
reveal the relationship between environmental parameters and panting
separating the HLI into two parts, as expressed in Eq. (17). To predict
score. As hourly data (collected from 14:00–17:00) and daily data were
black-globe temperature, a formula (Eq. (18)), initially developed by
used separately in the index-development phase, two different adjusted
Gaughan et al. (2002), was adopted:
THI models (THIadj-h and THIadj-d, respectively) were developed, as
expressed in Eqs. (15) and (16), respectively: HLITbg < 25 = 10.66 + 0.28×rh+1.3×Tbg − v

THIadj − h = THI 2 − 1.992×v +0.0068×sr + 4.51 (15) HLITbg > 25 = 8.62 + 0.38×rh+1.55×Tbg −0.5×v + e 2.14 − v (17)

THIadj − d = THI 2 − 3.075×v +0.0114×sr + 6.80 (16) Tbg = 1.33Ta−2.65Ta 0.5+3.21log (sr +1)+3.5 (18)

where, THI2 denotes the temperature humidity index expressed in Eq. It should be noted that accurately predicting black-globe tempera-
(5). ture requires a consideration of air temperature, air velocity, and solar
As was stated, the hourly-adjusted THI can reveal a “real-time” heat- radiation (direct and indirect) (Dimiceli et al., 2013). However, the
stress situation and serve as a basis for modifying a cooling strategy predicted black-globe temperature (Eq. (18)) does not incorporate air
according to cloud cover and wind speed, and the daily-adjusted THI velocity and the zenith angle of the sun. Therefore, it can be reasonably
could be a better choice for the prediction of heat-stress levels related to concluded that using the (Eq. (18)) or a direct measurement to predict
changing climatic conditions. black-globe temperature could result in a discrepancy.

4.7.2. Assessment of the HLI


4.6.2. Assessment of the adjusted THIs
In accordance with Eq. (17), the thermal effect of a 10% increase in
According to the Eqs. (15) and (16), the thermal effect of an increase
relative humidity will be linearly adjusted to 0.28 and 0.38 (HLI unit)
of 1 m s-1 in air velocity will be linearly adjusted to − 1.992 and
for any Tbg above or below 25 °C, respectively, which means that the
− 3.075 (THI unit) in THIadj-h and THIadj-d, respectively, indicating that
HLI treats any increase in relative humidity as a heating effect. Also, the
both indices treat the increase in air velocity as a chilling effect. The
different coefficients indicate that the HLI gives less weight to relative
coefficient of − 1.992 in THIadj-h is greater than the one in THIadj-d,
implying that THIadj-d treats the chilling effect produced by an increase
in air velocity as a stronger chilling effect comparing with THIadj-h.
Likewise, the thermal effect of an increase in solar radiation of
100 W m-2 will be adjusted to 0.68 and 1.14 (THI units) in THIadj-h and
THIadj-d, respectively, meaning that both adjusted THIs will treat the
increase of solar radiation as a heating effect. The coefficient of 0.0068
in THIadj-h is smaller than the one (0.0114) in THIadj-d, implying that
THIadj-d treats the heating effect produced by an increase in solar ra-
diation as more stronger heating effect comparing with THIadj-h.
The equivalent air temperature changes (Tequ) that occurred as the
air velocity increased from 1 to 2 m s-1 at three relative humidity levels
(35%, 50%, and 80% with respect to the application range—see
Table 1) and as air temperature rose from 25 to 40 °C were plotted to
examine the interactions that would occur between air temperature,
relative humidity, and air velocity (Fig. 6). Fig. 6. Equivalent air temperature changing (Tequ) of air velocity increases from
According to Fig. 6, we can find that: 1) the values of Tequ were all 1 to 2 m s-1 at three RH levels (35%, 50%, and 80%) as air temperature rises
negative, indicating that both adjusted THIs treat the thermal effect of from 25 to 40 °C.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

humidity when the Tbg is above 25 °C. Likewise, the fact that the −6.56
Vadj = −0.00566×v 2+3.33
thermal effect of an increase of 1 m s-1 in air velocity will be linearly exp ⎧
1 ⎫
−6 2.5 −2
adjusted to − 1 (HLI unit) when the Tbg is below 25 °C implies that any ⎨
⎩ (2.26 × v +0.23)0.45 × [2.9 + 1.14 × 10 × v − log0.3 (2.26 × v +0.33) ] ⎬

increase of air velocity will be treated as a chilling effect when the Tbg is (21)
below 25 °C. When the Tbg is above 25 °C, the adjustment made to ac-
count for an increasing air velocity will not be linear. where, RHadj, Vadj, and RADadj are the correlation factors of relative
The equivalent air temperature changes that occur when the air humidity, air velocity, and solar radiation, respectively (°C).
velocity increases from 1 to 2 m s-1 (marked as Tequ1) and solar irra- In Eq. (20), an exponential regression was performed to evaluate the
diance increases from 400 to 500 W m-2 (marked as Tequ2) at three re- thermal effect of relative humidity. The relative humidity of 30% was
lative humidity levels (20%, 50%, and 80%) and four air temperature chosen as the baseline, with the air temperature of the CCI being ad-
levels (25, 30, 35, and 40 °C) were listed in order to examine the in- justed up or down according to whether the relative humidity value was
teractions that will occur between air temperature, relative humidity, above or below the baseline. The thermal effect of wind speed was
and air velocity (Table 3). To calculate Tequ1, solar radiation was fixed determined to be a logarithmic adjustment (Eq. (21)). Compared with
at 500 W m-2, and to calculate Tequ2, the air velocity was fixed at 1 m s-1. the linear adjustment of wind speed that was made in the adjusted THI,
According to Table 3, we can find that: 1) all the values of Tequ1 were this adjustment of wind speed in the CCI was reported to be more ac-
negative, indicating that any increase of air velocity will be treated as a curate because it will reflect the greater chilling effect that occurs with
chilling effect when Tbg is above 25 °C; 2) Tequ1 did not change as the a certain increase in wind speed when the wind speed is low rather than
relative humidity increased from 20% to 50% and to 80%, meaning that high (Mader et al., 2010).
the HLI assumes that the increase of relative humidity has no effect on The adjustment in total radiation (RADadj, Eq. (25)) was separated
the change of the chilling effect of an air velocity increment; 3) the into two shares: an adjustment in direct solar radiation (DSRadj, Eq.
limited increase in Tequ1 as air temperature rose, which can be ne- (22)) and an adjustment in surface radiation (SRadj, Eq. (24)). The effect
glected, indicating that HLI assumes that the increase of air temperature of irradiated ground-surface radiation matters because the amount of
has no effect on the change of the chilling effect of an air velocity in- water a cow drinks appears to be highly dependent on irradiated
crement; 4) all the values of Tequ2 were positive, indicating that the HLI ground-surface temperature (r2 = 0.70–0.86) (Arias and Mader, 2009).
will treat any increase of solar radiation as a heating effect. To predict the irradiated ground-surface temperature, Mader et al.
(2010) proposed a linear regression model (Eq. (23)):

DSRadj = 0.0057sr −0.00002sr × Ta+0.00005Ta2 × sr (22)


4.8. The comprehensive climate index

4.8.1. Overview Tgs = Ta+0.019sr (23)


Mader et al. (2010) proposed a comprehensive climate index (CCI,
Eq. (19)) to evaluate not only heat stress but also cold stress. Reported
SRadj = 0.1×Tgs−2 (24)
data from two previous thermal indices (i.e., the adjusted THIs (Mader
et al., 2006) and the HLI (Gaughan et al., 2008)) were used to de-
termine the relationship between physiological response (panting RADadj = DSRadj + SRadj = 0.0076×sr −0.00002×sr × Ta+0.00005×Ta2
score) and the relevant environmental parameters (air temperature,
relative humidity, wind speed, and solar radiation) for warm condition × sr +0.1×Ta−2 (25)
(Ta > 5 °C). For air temperatures below 5 °C, the relationship of dry
where, DSRadj, and SRadj are the correlation factors of direct solar ra-
matter intake (DMI) to environmental parameters was defined based on
diation and surface temperature, respectively, (°C); Tgs is the ground
data reported in published works (i.e., (Birkelo and Lounsbery, 1992),
surface temperature (°C).
(Stanton et al., 1994), (Anderson and Schoonmaker, 2005), (Anderson
et al., 2006), (Mader and Colgan, 2007)). Once the general relation-
ships for hot and cold environmental conditions were defined, gen-
4.8.2. Correction of the Vadj in CCI
eralized exponential and logarithmic algorithms (and data from 7 heat-
There is a calculation example provided by the authors (Mader
stress events and 2 winter conditions, see Table 1) were used to develop
et al., 2010), as stated: “An example CCI calculation for environmental
a final model for assessing a full range of environmental conditions.
conditions, represented by Ta, RH, WS, and RAD of 30 °C, 50%, 1.0 m s− 1,
In developing the CCI, the thermal effects of relative humidity, wind
and 500 W/m2, respectively, would be as follows: 30 °C + 1.8 (RH ad-
speed, and solar radiation were all adjusted to conform to dry bulb
justment from Eq. [1] (Eq. 20 in this review)) + 0.6 (WS adjustment from
temperature (Eqs. 20, 21, and 25, respectively).
Eq. [2] (Eq. 21 in this review)) + 5.5 (RAD adjustment from Eq. [3] (Eq.
CCI = Ta + RHadj + Vadj + RADadj (19) 25 in this review)) = 37.9”. However, an examination of the corre-
sponding equations shows that the values of RHadj, WSadj (Vadj in the
present study) and RADadj are 1.8 °C, − 0.3 °C, and 5.5 °C, respectively,
RHadj = exp (0.00182×rh+1.8×10−5 × Tdb × rh) and the CCI under the given environmental condition equals to 37.0 °C,
×(0.000054×Ta2+0.00192×Ta−0.0246) × (rh−30) (20) which means that the Eq. (21) might be incorrectly edited.
After a communication with the corresponding author of that paper
(Mader et al., 2010), we got the corrected version of the Vadj (Eq. (26))

Table 3
The equivalent air temperature changing of an air velocity increase from 1 to 2 m s-1 (Tequ1) and a solar irradiance increase from 400 to 500 W m-2 (Tequ2) at three
relative humidity levels (20%, 50%, and 80%) and four air temperatures (25, 30, 35, and 40 °C).
Ta, °C Tequ1 (sr = 500 W m-2) Tequ2 (v = 1 m s-1)

25 30 35 40 25 30 35 40

rh: 20%, 50%, and 80% − 1.096 − 1.073 − 1.056 − 1.043 0.292 0.285 0.281 0.277

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

⎧ ⎫ radiative-heated ground surface and surrounding objects. The ERHL


⎪ −6.56 ⎪
Vadj = and Trm can be determined by the following Eqs. (28 and 29):

⎪ exp

{ 1
(2.26 × v +0.23)0.45
× [2.9 + 1.14×10−6 × v 2.5 − log0.3 (2.26×v +0.33)−2] } ⎬

⎭ ITSC = 77.1747 + 4.8327×Tdb−34.8189×v +1.111v 2+118.6981×Pva
−0.00566×v 2+3.33 (26) 2
−14.7956×Pva −0.1059×ERHL (27)
Therefore, the following assessment of the CCI was derived based on
the Eq. (26). ERHL = 0.5Sp + σTrm 4 (28)

4.8.3. Assessment of the CCI Trm = [εbg −1hbg (Tbg − Ta) + σ (Tbg +273.15) 4]0.25 (29)
Fig. 7 shows the equivalent change in air temperature that occurred where, εbg = 1 represents the emissivity of the black globe; hbg is the
(Tequ) when relative humidity increased from 50% to 60% and the air convective heat transfer coefficient of the black-globe (W m-2 °C-1); Tbg
temperature rose from 25 to 40 °C. All the values of Tequ were positive, is the measured black-globe temperature (°C); σ = 5.67 × 10−8 is the
indicating that the CCI treats an increase in relative humidity during Stefan-Boltzmann constant; Sp is the solar irradiance obtained directly
warm weather (25–40 °C) as a heating effect. The fact that Tequ gra- by means of a pyranometer (W m-2).
dually increased implies that the heating effect that occurs as relative
humidity rises gains in strength as air temperature rises.
4.9.2. Assessment of the ITSC
The equivalent air temperature changes (Tequ) that occurred as the
According to Eq. (27), the ERHL is the sole term for evaluating the
air velocity increased from 1 to 2 m s-1 and the solar radiation incre-
effect of solar radiation on heat stress. Theoretically, the thermal effect
ment rose from 400 to 500 W m-2 at three relative humidity levels
that an increasing solar radiation has on heat stress should be a heating
(20%, 50%, and 80%) as air temperature rose from 25 to 40 °C are
effect, which means that the ITSC should increase as the ERHL in-
displayed in Fig. 8a and b, respectively.
creases. However, the ITSC decreases as the ERHL value increases be-
According to the Fig. 8a, we can find that: 1) the values of Tequ were
cause the coefficient of the ERHL used in the ITSC was negative
all negative, which indicates that the CCI treats the thermal effect
(−0.1059). Because some of the variables (Sp, hbg, and Tbg) cannot be
produced when air velocity increases as a chilling effect; 2) the Tequ
determined based on the information provided in the published paper, a
associated with the air velocity increment from 1 to 2 m s-1 increases as
further analysis of the ITSC was not conducted.
the air temperature rises from 25 to 40 oC, which indicates that the CCI
assumes the chilling effect of air velocity increase becomes weak as the
4.10. Summary of the reviewed thermal indices with respect to their ability
air temperature rises; 3) the Tequ associated with the air velocity in-
to reflect the heat transfer mechanism
crement from 1 to 2 m s-1 increases as relative humidity increase at a
fixed air temperature, indicating that CCI assumes the chilling effect of
This summary is intended to make clear the various attributes and
air velocity increase decreases as the relative humidity increases.
drawbacks of the thermal indices we reviewed. All the cattle-related
From Fig. 8b, we found that 1) all the values of Tequ were positive,
thermal indices were checked to make sure that the heat transfer
indicating that the CCI treats the thermal effect produced by an increase
characteristics listed in Table 4 were reasonably reflected.
in solar irradiance as a heating effect; 2) the Tequ decreased as the re-
As can be seen, the development of thermal indices trends toward
lative humidity increased at a fixed air temperature, which indicates
incorporating more environmental parameters, most likely because, as
that, the CCI treats the heating effect produced by an increase in a given
many studies have shown, the more environmental parameters in-
solar irradiance decreases as relative humidity increases. Besides, note
cluded, the better the index's ability to predict heat stress (Hill and
that the values of Tequ in Fig. 8b associated with a relative humidity of
Wall, 2017).
20% and a relative humidity of 50% increased gradually as air tem-
All of the thermal indices treat increases in air temperature and
perature increased, whereas the values of Tequ at a relative humidity of
humidity (if incorporates) as heating effects and as the primary en-
80% remain steadily at 0.55 °C.
vironmental parameters driving heat stress. All the thermal indices
(except the CCI) that incorporate air velocity treat the thermal effect of
4.9. The index of thermal stress for cows
an air-velocity increase as a chilling effect. However, only the ET1 and
CCI consider the fact that the incremental rate of the chilling effect
4.9.1. Overview
associated with air velocity increasing decreases as the air velocity in-
da Silva et al. (2015) developed an index for measuring the thermal
creases. Besides, all the thermal indices (except the ITSC) that in-
stress suffered by cows (ITSC, Eq. (27)) with special emphasis placed on
corporate the solar radiation component treat the thermal effect of a
the effect of solar radiation in tropical environments. Only Holstein
solar radiation increase as a heating effect.
lactating cows were considered in the study. The cows were exposed to
solar radiation after milking, a period beginning at 07:00 and lasting
until about 16:30. Meteorological data such as the direct and diffused
solar radiations, air temperature, wind speed, and air partial vapour
pressure were measured. Six physiological traits, i.e., rectal tempera-
ture, respiratory rate, convective heat loss, skin surface evaporation,
respiratory evaporation, and radiation heat gain were used to develop
the ITSC. It should also be noted that the amount of convective heat
loss, respiratory evaporation, and radiation heat gain were calculated
based on heat transfer theory. The details of calculations pertaining to
these three physiological traits can be found in (da Silva et al., 2015).
In the ITSC, both direct and diffused solar radiations are considered,
while reflected solar radiation is neglected because it reportedly ac-
counts for only a very small portion (13.2%) of the total short-wave
radiation (da Silva et al., 2010). In the course of the work, two new
metrics for quantifying the mean radiant temperature of the environ-
ment (Trm) and the effective radiation heat load (ERHL) were developed Fig. 7. Equivalent air temperature change (Tequ) of relative humidity increase
and used to estimate the amount of thermal energy emanating from the from 50% to 60% as air temperature rises from 25 to 40 °C.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

Fig. 8. Equivalent air temperature changes (Tequ) that occur when (a) air velocity increases from 1 to 2 m s-1, and (b) solar radiation increases from 400 to 500 W m-2
at three relative humidity levels (20%, 50%, and 80%) as air temperature rises from 25 to 40 °C.

5. Application ranges of thermal indices animal in question. This section contains three sub-sections, one that
describes the THI threshold, one describing the HLI threshold, and one
To avoid misapplication, an application range should be considered describing the threshold used by all the other thermal indices.
as an important component of any thermal index. Theoretically (due to
the regression method used to develop an index), the application range
6.1. Thresholds of THI
of a thermal index should match the range of the field measurement
data. Table 1 lists the application ranges and information pertaining to
Traditionally, the THI recognizes four threshold levels, i.e., normal,
the environmental parameters. Some thermal indices provide an ap-
THI ≤ 74; alert, 74 < THI < 79; danger, 79 ≤ THI < 84; emergency,
plication range in accordance with the relevant range of environmental
THI ≥ 84 (LCI, 1970). However, in the literature, these levels are cir-
parameters, while others do not. Consequently, it is recommended that
cumscribed differently to account for the differing heat tolerances of
future thermal-index development provide a suggested application
various breeds. Table 5 lists the published THI “thresholds of alert” for
range together with relevant statistical information pertaining to the
cows.
environmental parameters.
All of the THI thresholds for alert reviewed here were identified
based on THI2, which in many related studies has become the de facto
6. Thresholds of thermal indices standard for evaluating heat stress (Hahn et al., 2003). The THI value of
72 is frequently deemed the threshold at which dairy cattle become
The term “threshold” refers to the level at which heat stress will heat-stressed. As can be seen, the highest threshold, 78.2 for Holstein
begin to occur, and as such, it should be regarded as a key component of cattle in Florida, US, was reported by Dikmen and Hansen (2009),
any thermal index. Understandably, the different heat-stress levels are whereas the lowest threshold, 60 for Holsteins in Germany, was re-
typically defined according to the physiological performance of the ported by Brügemann et al. (2012). Milk yield has been used frequently

Table 4
Summary of cattle-related thermal indices in reflecting heat transfer characteristics.
Thermal Environmental Heat transfer characteristic if the index can reflect (Ta ranges from 25 to 40°C)
index parameters included
Heating effect Heating effect Chilling effect Heating effect Increment rate of eChilling ffect of v Chilling effect of v
of Ta increase? of rh increase? of v increase? of sr increase? chilling effect increasing decreases increasing decreases
decreases as v as Ta increases? as rh increases?
increases?

THI1 T, h y y nn nn nn nn nn
THI2 T, h y y nn nn nn nn nn
THI3 T, h y y nn nn nn nn nn
THI4 T, h y y nn nn nn nn nn
BGHIa T, h, r y y nn y n n n
ETI T, h, v y y y nn n n y
ET1 T, v y nn y nn y n nn
ET2 T, r y nn nn y nn nn nn
RRI1 T, h, v, r y y y y n n n
RRI2 T, h, v, r y y y y n n n
RRI3 T, h, v, r y y y y n n n
THIadj-d T, h, v, r y y y y n n n
HLI T, h, v, r y y y y n n n
CCI T, h, v, r y y n y n n n
ITSC T, h, v, r y y y n n n n

T = air temperature component; h = air humidity component; v = air velocity component; r = solar radiation component.
y = the index can reflect the heat transfer characteristic.
nn = the index cannot reflect the heat transfer characteristic, due to a lack of the relating environmental parameter.
n = the index cannot reflect the heat transfer characteristic, although it involves the relating environmental parameter.
a
Black-globe temperature was considered only as a metric of solar radiation, as HLI did.

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X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

to identify thresholds; however, other parameters, such as protein yield, For these reasons, the location of the experimental barn in which an
fat yield, protein percentage, and rectal temperature, have also been index was developed matters.
used. Table 8 lists pertinent information related to index development,
It should be noted that the Holstein breed has received more at- such as cattle breed, physiological response, experimental location, and
tention than other breeds, most likely because it is the most common, whether the animals were shaded or unshaded during testing. Also,
and all of the reviewed studies were conducted in either the US or whether the thermal index was published in a peer-reviewed journal or
Europe. Apparently, while the THI thresholds will differ according to elsewhere is noted in Table 8. As can be seen, several cattle breeds have
climate, our literature review uncovered no published study to establish been used in the development of thermal indices. Among them, Hol-
THI thresholds in other regions. stein cattle received the most intensive investigations. Of the many
physiological responses that have been considered during index de-
6.2. Thresholds of HLI velopment, respiration rate might be the most common, most likely
because respiration rate is a physiological heat-stress indicator that has
A comprehensive classification of the heat-stress threshold alerts less thermal lag (Eigenberg et al., 2005).
was proposed by Gaughan et al. (2008). This classification took into Besides, most of the indices were developed based on field experi-
account not only cattle breed but also coat colour, health status, ac- mental data collected in the US (RRI1, RRI2, RRI3, adjusted THI in
climatization, access to shade, manure management, and the tem- Nebraska, and BGHI in Florida), except for the ET2 in Japan, the HLI in
perature of the available drinking water. The HLI value of 86 was Australia, and the ITSC in Brazil. Note that THI1, THI4, ETI, and ET1
deemed the base threshold of alert for unshaded Angus steers. Adjust- were developed based on data collected inside environmental control
ments were proposed according to genotype, coat colour, health status, chambers.
acclimatization, shade, drinking water temperature, and manure man-
agement (as listed in Table 6). For dairy cattle in tropical regions, da
8. Overview of comparisons of indices found in the literature
Silva et al. (2007) proposed a classification system based on the HLI,
which deemed < 89 to be “safe”, 89–92 to be “caution”, 92–95 “ex-
To date, four comparisons that used field measurement data have
treme caution”, and > 95 to be “danger”.
been reported in the literature.
da Silva et al. (2007) has evaluated five cattle related thermal in-
6.3. Thresholds of the remaining thermal indices dices (i.e., THI4, BGHI, ETI, HLI, and RRI1) and also the ESI (En-
vironmental Stress Index) for Holstein and Jersey cows located in a
Table 7 lists the thresholds that pertain to the remaining thermal tropical region (northeast region of Brazil). Note that the ESI was a
indices. As can be seen, the RRIs, the adjusted-THI, the CCI, and the human-based thermal index (Moran et al., 2001). In all these evalua-
ITSC are all treated as the same, while no classification of thresholds tions, the indices were correlated with the rectal temperatures and re-
that pertains to the BGHI, the ETI, the ET1, or the ET2 can be found in spiration rates of the test animals. Both THI4 and the BGHI did not
the corresponding publications. As the BGHI was developed on the basis correlate with the animals’ actual rectal temperatures and the respira-
of the THI4, the BGHI might use the same thresholds as the THI. da tion rates. The HLI correlated most closely (r = 0.542) with the re-
Silva et al. (2007) provided a classification of heat stress specifically for spiration rates, followed by the ETI (r = 0.520). The ETI correlated
use with the ETI in tropical regions. most closely (r = 0.293) with rectal temperatures, followed by the HLI
(r = 0.286). According to these results, the HLI and the ETI are re-
7. Summary of other information commended for evaluating thermal stress in cattle in tropical environ-
ments.
Since heat tolerance is breed-specific (Gaughan et al., 2010), under Li et al. (2009) evaluated eight thermal indices (i.e., THI4, THIadj-d,
identical thermal environments different cattle breeds may react dif- BGHI, ETI, HLI, RRI1), as well as the predicted black-globe temperature
ferently in their physiological, behavioural and production responses to (Eq. (18)) and the ESI for cattle in the US, using data pertaining to four
heat stress (Stone et al., 2017). Consequently, a thermal index devel- physiological responses (i.e., skin temperature, rectal temperature,
oped based on one particular breed could over- or under-estimate the sweating rate, and respiration rate). Two datasets were used in this
heat-stress level imposed on another breed, even when the environ- evaluation. The data pertaining to the four physiological responses in
mental conditions are exactly the same in both instances. Besides, da the first dataset were collected at five different sites (i.e., Ona, Florida;
Silva and Maia (2012) found that even individual cows of the same Oahu, Hawaii; Starkville, Mississippi; Clay Centre, Nebraska; Tucson,
breed but living in different climates could perform differently under Arizona) from three breeds of dairy cow (Holsteins; Gir-Holstein cross;
identical environmental conditions on account of climate adaptability. Jersey) and six breeds of feedlot heifer (Augus White, Augus Brookville,

Table 5
Published THI thresholds of alert for cows (listed chronologically).
Study THI No. Threshold Physiological responses used for identification Cattle breed Location

(Igono et al., 1992) THI2 72 milk yield Holstein cattle Arizona, US


(Ravagnolo et al., 2000) THI2 72 milk and protein yield Holstein cattle Georgia, US
(Ravagnolo and Misztal, 2002) THI2 72 milk yield Holstein cattle Northern US
76 Southern US
(Bohmanova et al., 2007) THI2 72 milk yield US Holstein cattle Georgia, US
(Bohmanova et al., 2007) THI2 74 milk yield US Holstein cattle Arizona, US
(Broucek et al., 2007) THI2 72 milk yield Slovakian Pied cattle and Holstein cattle Southern Slovakia
(Dikmen and Hansen, 2009) THI2 78.2 rectal temperature Holstein cattle Florida, US
(Zimbelman et al., 2009) THI2 68 milk yield Holstein cattle Arizona, US
(Brügemann et al., 2012) THI2 60 milk yield Holstein cattle Germany
(Hammami et al., 2013) THI2 62 milk, fat, and protein yield Holstein cattle Luxembourg
(Bernabucci et al., 2014) THI2 73–76 milk yield Italian Holstein cattle Cremona, Italy
65–71 protein percentage
72–73 protein yield

34
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

Table 6 Table 7
Animal (genotype, coat colour, health status, acclimatization) and management Thresholds of reviewed thermal indices (except THI and HLI).
(access to shade, days on feed, manure management, and drinking water tem-
Thermal index Thresholds
perature) adjustments (+ and −) to the heat load index (HLI) threshold of the
reference steera (Adopted from (Gaughan et al., 2008)). BGHI –
ETIa Safe, < 30;
Item Relative effect on upper HLI threshold
Caution, 30 – 34;
of the reference steer (HLI = 86)
Extreme caution, 34–38;
Genotype Danger, > 38
Bos taurus (British) 0b ET1 and ET2 –
B. taurus (European) + 3 (i.e., 86 + 3) RRI1, RRI2, and RRI3 Normal, ≤ 90;
Waygu +4 Alert, 90–110;
Bos indicus (25%) +4 Danger, 110–130;
B. indicus (50%) +7 Emergency, ≥ 130b
B. indicus (75%) +8 adjusted THI Normal: ≤ 74.0;
B. indicus (100%) + 10 Alert: 74 – 79;
Coat colour Danger 79 – 84;
Black 0 Emergency: ≥ 84
Red +1 CCI No stress, ≤ 25 °C;
White +3 Mild, 25–30 °C;
Health status Moderate, 30–35 °C;
Healthy 0 Severe, 35–40 °C;
Showing clinical signs of disease or −5 Extreme, 40–45 °C;
recovering Extreme danger, ≥ 45 °C.
Acclimatization ITSC Comfort, ≤ 150;
Acclimated 0 Mild discomfort, 151–200;
Not acclimated −5 Discomfort, 201–250;
Shadec Stress, 251–350;
No shade 0 Warning, ≥ 350.
Shade, m2/animal a
> 1.5–2 +3 suggested by da Silva et al. (2007) for using ETI in tropical regions.
b
2.0–3 +5 developed with respect to the corresponding categories in THI2
3.0 +7 (Normal: ≤ 74.0; Alert: 74 – 79; Danger 79 – 84; Emergency: ≥84) under
Days on feedd solar radiation and wind speed of 800 W m-2 and 0 m s-1, respectively.
0–80 +2
80–130 0
somatic cell count. The authors reported that the heat-stress thresholds
130 + −3
Manure managemente, maximum depth of all the thermal indices investigated under the continental temperate
of manure pack, mm climate conditions were lower than those obtained under tropical,
50 0 subtropical and Mediterranean climate conditions. The authors specu-
100 −4
lated that this decline in thresholds might be the result of a reduced
200 −8
Drinking water temperaturef, °C adaptability to heat stress under temperate conditions. The THIadj-d was
15–20 +1 recommended for preliminary heat-stress prediction and herd man-
21–30 0 agement under temperate climate conditions.
31–35 −1 da Silva et al. (2015) compared the prediction performances of four
> 35 −2
indices (CCI, HLI, BGHI, and ITSC) based on six physiological traits
a
A healthy, unshaded Angus at 100 d on feed. (i.e., rectal temperature, respiratory rate, convective heat loss, skin
b
The values for the reference steer are presented as 0 (i.e., no change from surface evaporation, respiratory evaporation, radiation heat gain) ex-
the threshold of 86). hibited by Holstein cows kept in a tropical environment. The analysis
c
For shade that provides 70% blockout (includes shade cloth and also steel showed that the CCI correlated most closely with actual rectal tem-
structures with gaps in the roof). Unshaded B. indicus cattle > 25% were not perature (r = 0.374), respiration rate (r = 0.365), and respiratory
included. evaporation (r = 0.408), and the ITSC correlated most closely with
d
Not all cattle were assessed for this trait. Waygu cattle were excluded from convective heat loss (r = −0.493), skin surface evaporation
130 + d. (r = −0.647), and radiation heat gain (r = −0.818).
e
Mean depth over 54d.
f Table 9 lists the correlation coefficients between thermal indices
Only unshaded Angus cattle were assessed for this trait.
and physiological responses (respiration rate, rectal temperature, and
skin temperature) of cattle in the four comparisons. The highest cor-
Augus Kansas, Charolais, MARC I, MARC III). The second dataset was
relation coefficient in each dataset was marked in bold. As can be seen,
obtained from a four-day measurement cycle performed on twelve
the indices performed differently from dataset to dataset. THI4, RRI1
lactating Holsteins confined in controllable environmental chambers at
and ITSC did not result in the best correlation with any of the 8 in-
the University of Arizona Research Complex during August 2008. The
vestigated datasets. Both THIadj-d and HLI resulted in the best correla-
environmental parameters (air temperature, relative humidity, air ve-
tion with one of the datasets, while BGHI, ETI and CCI resulted in the
locity, and solar radiation) were controlled in the experiment, and data
best correlation with two datasets. However, the coefficient of ETI in
pertaining to all four physiological responses were recorded. Li et al.
one dataset was negative. Besides, RRI1 was evaluated by six datasets,
(2009) concluded that skin temperature responded most sensitively to
and four of the six correlation coefficients were relatively high. Like-
environmental conditions, and the THIadj-d, the BGHI, and the RRI1
wise, the THIadj-d was evaluated by four datasets and three of the
correlated most closely to skin temperature. Sweating rate was noted as
coefficients were high. Accordingly, it is quite difficult to determine
the poorest physiological indicator.
which is the best. Generally, however, BGHI, RR1, THIadj-d and CCI
Hammami et al. (2013) assessed six thermal indices (THI2, THIadj-d,
performed better in most datasets.
HLI, ETI, ESI, and CCI) using Holstein cows kept under continental
temperate climate conditions in Luxembourg. The six thermal indices
were evaluated on the basis of milk yields, fat yields, protein yields, and

35
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

Table 8
Overview of cattle-related thermal indices that considered cattle breed, physiological responses used for index development (PR), experimental location, testing with
or without direct solar radiation, and place published.
Thermal index CB PRa Location of experiment With or without direct solar Published placeb
radiation

THI1 9-month-old Ayrshire bull calve RT Ayr, UK (climatic room) Shaded PRJP
THI2 & THI3 N/A N/A N/A N/A Book
THI4 Holstein cattle N/A N/A N/A Book
BGHI Mostly Lactating Holstein cows MY Florida, US Both shaded and unshaded PRJP
ETI Lactating Holstein cows MY, HLR Missouri, US (environmental Shaded CP
chamber)
ET1 Lactating Holstein cows RT, MST, RR Hiroshima, Japan (environmental Shaded PRJP
chamber)
ET2 Young Holstein heifers RT, MST, RR Hiroshima, Japan Unshaded PRJP
RRI1 Crossbred steers (1/4 Angus, 1/4 Hereford, 1/4 RR Nebraska, US Feedlot (access to shade) PRJP
Pinzgauer, 1/4 Red Poll)
RRI2 & RRI3 Crossbred steers (1/4 Angus, 1/4 Hereford, 1/4 RR Nebraska, US Feedlot (access to shade) PRJP
Pinzgauer, 1/4 Red Poll)
Adjusted THI Angus and Angus crossbred steers PS Nebraska, US Feedlot (access to shade) PRJP
HLI Bos taurus steers, B. Taurus crossbred steers, B. PS Queensland, Australia and Feedlot (access to shade) PRJP
taurus × Bos indicus steers, indicus steers Nebraska, US
CCI One-year-old steer PS, DMIc Nebraska, US Feedlot (access to shade) PRJP
ITSC Lactating Holstein cows RT, RR, MST, CHL, The northeastern region of Brazil Unshadedd PRJP
SE, RE, RHG

N/A = not available.


a
the physiological responses including: RT = Rectal temperature; MY = Milk yield; HLR = Heat loss rate; MST = mean skin temperature; RR = respiration rate;
PS = Panting score; DMI = Dry matter intake; CHL = Convective heat loss; SE = skin surface evaporation; RE = Respiratory evaporation; RHG = Radiation heat
gain.
b
the published place including: PRJP = peer reviewed journal paper; CP = conference paper.
c
Panting score for hot condition, dry matter intake for cold condition.
d
Cows were driven to a barnyard without shade after milking at 07:00, and continuously exposed to sun until about 16:30.

9. Conclusions and suggestion based on THI2. Different breeds, management styles (e.g., the pos-
sibility of access to shade, the cooling method applied inside the
The sixteen cattle-related thermal indices have been reviewed and barn, the temperature of drinking water, manure management, etc.),
evaluated in this study. Based on the results of our evaluations, we can and the location of the barn where the experiments took place can
draw the following conclusions: all affect the threshold-identification outcomes.
4. Application range, another important component, helps index users
1. Research aimed at evaluating the various indices has trended to- to employ an index accurately. The application range of an index is
wards incorporating more environmental parameters under the as- similar to the range of environmental data that was used for index
sumption that doing so will enable the index to predict heat stress development.
more accurately. 5. The thermal indices reviewed herein are distinct in many ways, such
2. The main effects that environmental parameters impose on heat as in cattle breed tested, physiological responses included, the lo-
stress can be correctly interpreted as either heating effects (in- cation where experiments took place, and type of management style,
creasing of air temperature, relative humidity, and solar radiation) to name a few. Significant differences could occur among the
or chilling effects (increasing of air velocity), as long as the corre- thermal indices even when applied under similar environmental
sponding parameter is incorporated. The interaction effects between conditions.
environmental parameters are either omitted or treated differently. 6. We summarized the results of the four comparisons of indices found
3. The concept of the heat-stress threshold is an important component in the extant literature. Indices performed differently from dataset
of any thermal index. Most such “thresholds of alert” are identified to dataset. Generally, BGHI, RRI1, THIadj-d and CCI performed better

Table 9
Correlation coefficients between thermal indices and physiological responses of cattle in reviewed caparisons. The coefficients were marked bold if the coefficients
were the highest one in the investigated dataset.
Respiration rate Rectal temperature Skin temperature

TI (da Silva et al., (Li et al., 2009) (Li et al., 2009) (da Silva et al., (da Silva et al., (da Silva et al., (Li et al., 2009) (Li et al., 2009)
2007) dataset 1 dataset 2 2015) 2007) 2015) dataset1 dataset2

THI4 – 0.16 + + 0.39 + – – – 0.40 + + 0.10 ns


BGHI 0.054 ns 0.02 ns 0.73 + 0.198 * * 0.155 * * 0.219 * * 0.42 + + 0.56 + +
ETI 0.293 * * 0.34 + 0.23 + – 0.520 * * – 0.30 + + − 0.29 + +
RRI1 0.114 * * 0.10 ns 0.68 + – 0.344 * * – 0.48 + + 0.54 + +
THIadj-d – 0.19 + + 0.65 + – – – 0.52 + + 0.49 + +
HLI 0.286 * * 0.22 + + 0.68 + 0.123 * * 0.542 * * 0.219 * * 0.36 + + 0.31 + +
CCI – – – 0.365 * * – 0.374 * * – –
ITSC – – – 0.255 * * – 0.275 * * – –

ns = non-significant, * * p-value < 0.01.


+ p-value ≤ 0.0001, + + 0.0001 < p-value < 0.05.

36
X. Wang et al. Journal of Thermal Biology 77 (2018) 24–37

in the most studies. for dairy cows in tropical regions. Rev. Bras. Zootec. 36, 1192–1198.
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animal-specific barn climatization facing temperature rise and in- Hahn, G.L., Mader, T.L., Eigenberg, R.A., 2003. Perspective on development of thermal indices
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number: 201406320185) and the S.C. Van Fonden (Grant number:
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