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Animal Science Journal (2014) 85, 915–918
doi: 10.1111/asj.12226
ORIGINAL ARTICLE Relationship of climatic conditions to fecal corticosterone levels of captive cheetahs reared in Japan Katsuji UETAKE,1 Yumi UNE,1 Shu ITO,2 Marino YAMABE,1 Hideto TOYODA1* and Toshio TANAKA1 1
School of Veterinary Medicine, Azabu University, Sagamihara and 2Wakayama Adventure World, Wakayama, Japan
ABSTRACT To assess the stress level of cheetahs reared in Japan and to identify the prime components of the climatic conditions that affect their thermal stress, fecal corticosterone was monitored for 8 months from May to the following January. A total of 203 fecal samples were gathered in the morning from seven adult cheetahs that were kept at a zoological garden in Wakayama, Japan. Cheetahs were on exhibit singly or together with a harmonious conspecific during the day, but housed singly at night. Although the monthly fluctuation in corticosterone concentrations was not significant, the concentrations were relatively low during the summer season. Individual differences among cheetahs and the interaction effect between individual and month on the corticosterone concentrations were significant. Whereas the corticosterone concentrations negatively correlated with air temperature, they were positively correlated with the amount of rainfall. The highest air temperature and the amount of rainfall were extracted as the prime factors affecting corticosterone concentrations. These results suggest that cheetahs reared in Japan are somewhat subjected to thermal stress, particularly on cooler and/or rainy days.
Key words: cheetah, climatic condition, fecal corticosterone, stress.
INTRODUCTION Livestock science has been contributing to the improvement of the breeding management technique of zoo animals. For instance, the knowledge of environmental physiology provides practical methods to improve their reproductive success through stress management (Terio et al. 2003). In order to assess thermal stress, the concept of temperature humidity index (THI) in farm animals (e.g. Berman 2005) is applied to zoo animals as well. The cheetah (Acinonyx jubatus) is an endangered species whose adult population is estimated to be only 7500 worldwide and has decreased 30% over the last 18 years (African Wildlife Foundation 2013). Most wild cheetahs are found in eastern and southwestern Africa, and they are under pressure as the wide-open grasslands they favor are disappearing at the hands of human settlers (National Geographic Society 2013). To ensure cheetahs’ future existence, some international protection projects have been conducted in their habitats. In addition, breeding programs, including artificial fertilization, have been tried in zoos around the world (Gugliotta 2008). © 2014 Japanese Society of Animal Science
In spite of various measures, the captive population of cheetahs has not been self-sustaining because of their poor reproductive performance and an increased prevalence of a certain kind of disease not commonly observed in wild cheetahs (Terio et al. 1999). Some of these problems may be caused by stress and result from maladaptation of cheetahs to present management conditions (Wielebnowski et al. 2002; Terio et al. 2004). Chronic stress of cheetahs has been demonstrated in a captive environment in comparison with a near-natural environment (Terio et al. 2004). This may be particularly true in climatic regions different from their original habitats. There are big climatic differences between Japan and the cheetah’s original habitats in eastern and
Correspondence: Katsuji Uetake, School of Veterinary Medicine, Azabu University, Chuo, Sagamihara, Kanagawa 2525201, Japan. (Email:[email protected]) *Present address: Saitama Children’s Zoo, Higashimatsuyama, Japan. Received 1 August 2013; accepted for publication 4 February 2014.
916 K. UETAKE et al.
southwestern Africa. Thus, the objectives of this study were to: (i) assess stress levels of cheetahs that are reared in Japan by monitoring fecal corticosterone concentrations; and (ii) determine the relationships between components of the climatic environment and the corticosterone response of cheetahs.
MATERIALS AND METHODS Fresh fecal samples were collected in the morning (09.00– 10.00 hours) at the animal house for 8 months (May 10, 2012–January 11, 2013) from seven adult cheetahs (two males and five females). The total number of samples was 203. The cheetahs were between four and nine years old, and weighed between 27 and 44 kg. All individuals had been kept at the Wakayama Adventure World (Shirahama, Wakayama, Japan) at least 4 months before the study. One female cheetah was born in South Africa and the others were born in Japan. The cheetahs were on exhibit from 09.45 to 16.40 hours during the summer season (May–September) and from 10.15 to 16.40 hours during the winter season (October–April). In addition, they were kept on exhibit until 20.30 hours in the mid-summer (July 28–September 1). Each cheetah was on exhibit alone or together with a harmonious conspecific, but housed singly at night. The areas of the animal house and the exhibit space were 3.8–5.3 m2 and 7500 m2, respectively. The animal house was concrete and the interior floor was waterproofed. The cheetahs were exposed to natural climatic conditions in the daytime and fed a beef-, horse- and/or cat food-based diet. Water was available ad libitum. Individual fecal samples were stored in a polypropylene bag and frozen at −80°C until drying. The fecal samples were dried with a drying oven (SDN27; Sansyo Co., Ltd, Tokyo, Japan) at 100°C for more than 16 h and then dried samples were powdered with a mill (IFM-800DG; Iwatani Corporation, Osaka, Japan). Powdered feces were extracted using a vortexing method modified from Wasser et al. (2000). Briefly, 0.1 g of dried sample was placed in a capped 2 mL microtube with 1 mL of 95.5% ethanol, vortexed (5 min) using the vortex mixer (Vortex-Genie2; M&S Instruments Inc., Osaka, Japan), and then centrifuged (CN-820; AS ONE Corporation, Osaka, Japan) for 5 min at 1050 × g. The supernatant was used to determine the fecal corticosterone concentrations with an enzyme immunoassay kit (ADV900-097; Cosmo Bio Co. Ltd, Tokyo, Japan). The extraction efficiency of exogenous corticosterone was 65.1% using this extraction method. All fecal concentration data were expressed as nanograms per gram of dry feces.
Seven components that comprise the climatic conditions were downloaded from the data provided by the Automated Meteorological Data Acquisition System (AMeDAS) of the Japan Meteorological Agency (JMA): the lowest, highest and mean air temperature (°C), lowest and average relative humidity (%), sunlight hours (h) and the amount of rainfall (mm). Data measured at Shionomisaki, which is nearest to Wakayama Adventure World, were used (Japan Meteorological Agency 2012–2013). A previous study reported that an elevation in blood cortisol concentration is followed 1–2 days later by a substantial increase in fecal corticoid excretion in cats (Graham & Brown 1996). Thus, the climatic data of the previous day were matched with the fecal corticosterone data for statistical analysis. Statistics describing the climatic conditions used in the analyses are shown in Table 1. An unbalanced mixed model analysis of variance was performed (SAS version 9.3; SAS Institute Inc., Cary, NC, USA). Eight months, considered as a fixed effect, and seven cheetahs, considered as a random effect, were analyzed. The month × cheetah interaction was declared as a random effect. Pearson’s correlations were performed to determine the relationships between components of the climatic conditions and fecal corticosterone concentrations of cheetahs. Then stepwise regression analyses were performed to identify the prime factors affecting a cheetah’s thermal stress. The forward model-selection method and the criteria of an F-value larger than 2 were applied. These two kinds of analyses were carried out with the statistical software program Statcel3 (version 3, 2011; OMS Publishing Inc., Tokyo, Japan).
RESULTS AND DISCUSSION Figure 1 shows the day-to-day variation in fecal corticosterone concentrations of subject cheetahs (lower) with the highest air temperature and the amount of rainfall (upper) during the experimental period. Although a significant monthly fluctuation in fecal corticosterone concentrations was not confirmed (F8, 52.0 = 1.24, P = 0.298), only 8% (5/62) of samples showed a concentration higher than 500 ng/g dry feces, which reflect stress response (Terio et al. 1999), during the summer season from July to September. On the other hand, that rate was 19% (27/141) in the months excluding the summer season. Individual differences among cheetahs (F6, 55.9 = 7.37, P < 0.001) and
Table 1 Climatic conditions analyzed in this study
Variable Air temperature (°C) Lowest Highest Mean Relative humidity (%) Lowest Mean Sunlight hours (h) Amount of rainfall (mm)
Mean
SD
Maximum
Minimum
16.3 21.9 19.0
7.4 6.8 7.1
26.3 30.4 27.7
1.3 7.6 3.8
56.3 72.1 6.6 6.2
15.6 13.9 3.6 16.6
87.0 95.0 12.7 85.5
28.0 46.0 0.0 0.0
n = 203.
© 2014 Japanese Society of Animal Science
Animal Science Journal (2014) 85, 915–918
CLIMATIC STRESS IN CHEETAHS
90
35
70 25 60 20
50
15
40 30
䕔 Amount of rainfall 䠄mm䠅
80
30
䕺 Highest air temperature䠄℃䠅
917
10 20 5
10 0 1/9
1/2
12/26
12/19
12/5
12/12
11/28
11/21
11/7
11/14
10/31
10/17
10/24
10/3
10/10
9/26
9/19
9/5
9/12
8/29
8/22
8/8
8/15
8/1
7/25
7/18
7/4
7/11
6/27
6/20
6/6
6/13
5/30
5/23
5/9
5/16
0
14,000
Fecal corƟcosterone concentraƟon 䠄ng/g dry feces䠅
#1 #2
12,000
#3 #4
10,000
#5 #6 #7
8,000
6,000
4,000
2,000
1/10
1/3
12/27
12/20
12/13
12/6
11/29
11/15
11/22
11/8
11/1
10/25
10/18
10/11
10/4
9/27
9/20
9/13
9/6
8/30
8/23
8/16
8/9
8/2
7/26
7/19
7/12
7/5
6/28
6/21
6/14
6/7
5/31
5/24
5/17
5/10
0
Figure 1 The day-to-day variation of fecal corticosterone concentrations of subject cheetahs (lower) and the highest air temperature and the amount of rainfall (upper) during the experimental period.
the interaction effect between individual and month (F48, 140 = 1.51, P < 0.05) were both significant. Table 2 shows correlation coefficients between components of the climatic conditions and fecal corticosterone concentrations of cheetahs (n = 203). The lowest (r = −0.151, P < 0.05), highest (r = −0.161, P < 0.05) and mean (r = −0.155, P < 0.05) air temperature had negative correlations, and the amount of rainfall (r = 0.166, P < 0.05) had a positive correlation with fecal corticosterone concentrations. Neither the lowest or average relative humidity had significant correlations. In stepwise multiple regression analyses, the highest air temperature and the amount of rainfall indepenAnimal Science Journal (2014) 85, 915–918
Table 2 Correlation coefficients between components of climatic conditions and fecal corticosterone concentrations of cheetahs
Variable
Fecal corticosterone concentration
Lowest air temperature Highest air temperature Mean air temperature Lowest relative humidity Average relative humidity Sunlight hours Amount of rainfall
−0.151* −0.161* −0.155* −0.055 −0.070 −0.110 0.166*
Pearson’s correlation coefficient; n = 203, *P < 0.05.
© 2014 Japanese Society of Animal Science
918 K. UETAKE et al.
dently correlated with fecal corticosterone concentrations of cheetahs (R2 = 0.058, F2, 200 = 6.13, P < 0.01). The contributions to R2 were 0.030 and 0.028, respectively. The regression coefficients were −44.08 for the highest air temperature (F1, 200 = 6.40, P < 0.05) and 18.53 for the amount of rainfall (F1, 200 = 6.78, P < 0.01). Fecal corticosterone concentrations of cheetahs were relatively low during the summer season from July to September. The highest air temperature, which was identified as one of the prime factors affecting their thermal stress, was more than 25°C throughout the summer season. On the other hand, some individuals occasionally showed high fecal corticosterone concentrations on the day after a day when air temperature decreased during the spring and autumn seasons. This sensitiveness to cold temperature appears not only in the significant interaction effect between individual and month, but also in the significant negative correlations between all three variables concerning air temperature and fecal corticosterone concentrations. Wild cheetahs are mainly found in eastern and southwestern Africa (National Geographic Society 2013) where the air temperature is stable at around 20–25°C through the year (Japan Meteorological Agency 2013). In addition to this low temperature fluctuation, those regions have a small amount of rainfall from June to September (Japan Meteorological Agency 2013). In contrast, the neighborhood of the Wakayama Adventure World has the highest rainfall during these months (Japan Meteorological Agency 2012–2013). Thus, these climatic differences between Japan and their native habitat, particularly in summer, would result in thermal stress in cheetahs. Although significant statistically, the contributions of climatic components (highest air temperature and amount of rainfall) to considerable variations in fecal corticosterone concentrations were not more than 10%. Thus investigation is necessary about a complex index like the THI in livestock. In addition, at the individual level, some specific cheetahs showed a high corticosterone concentration. Therefore, attention is of course needed on other management-related and/or animal-related (social) factors (Terio et al. 1999; Wielebnowski et al. 2002; Wells et al. 2004) in order to reduce stress in captive cheetahs (Terio et al. 2004). It will be needed to consider these factors in future.
REFERENCES African Wildlife Foundation (AWF). 2013. The cheetah’s habitat is now only 25% of its former size. [homepage on the internet]. AWF, Karen; [cited 18 April 2013]. Available from URL: http://www.awf.org/wildlife -conservation/cheetah Berman A. 2005. Estimates of heat stress relief need for Holstein dairy cows. Journal of Animal Science 83, 1377– 1384. Graham L, Brown J. 1996. Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered fields. Zoo Biology 15, 71–82. Gugliotta G. 2008. Rare breed – can Laurie Marker help the world’s fastest mammal outrun its fate? [homepage on the internet]. Smithsonian Magazine, Washington, DC; [cited 26 June 2013]. Available from URL: http:// www.smithsonianmag.com/science-nature/rarebreed.html Japan Meteorological Agency (JMA). 2012–2013. Past weather data search. (In Japanese) [homepage on the internet]. JMA, Tokyo; [cited 9 April 2013]. Available from URL: http://www.data.jma.go.jp/obd/stats/etrn/ Japan Meteorological Agency (JMA). 2013. World weather chart. (In Japanese) [homepage on the internet]. JMA, Tokyo; [cited 2 July 2013]. Available from URL: http:// www.data.jma.go.jp/gmd/cpd/db/monitor/ ?tm=normal&el=rn National Geographic Society (NGS). 2013. Cheetah. [homepage on the internet]. NGS, Washington, DC; [cited 18 April 2013]. Available from URL: http://animals .nationalgeographic.com/animals/mammals/cheetah/ Terio KA, Citino SB, Brown JL. 1999. Fecal cortisol metabolite analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). Journal of Zoo and Wildlife Medicine 30, 484–491. Terio KA, Marker L, Munson L. 2004. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. Journal of Wildlife Diseases 40, 259–266. Terio KA, Marker L, Overstrom EW, Brown JL. 2003. Analysis of ovarian and adrenal activity in Namibian cheetahs. South African Journal of Wildlife Research 33, 71–76. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett M, Bechert U, et al. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General and Comparative Endocrinology 120, 260–275. Wells A, Terio KA, Ziccardi MH, Munson L. 2004. The stress response to environmental change in captive cheetahs (Acinonyx jubatus). Journal of Zoo and Wildlife Medicine 35, 8–14. Wielebnowski NC, Ziegler K, Wildt DE, Lukas J, Brown JL. 2002. Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus). Animal Conservation 5, 291–301.
ACKNOWLEDGMENTS We thank Ms. Ayaka Mutoh and other staff members in charge of rearing cheetahs at the Wakayama Adventure World for their contribution to fecal sampling.
© 2014 Japanese Society of Animal Science
Animal Science Journal (2014) 85, 915–918
Animal Science Journal (2014) 85, 915–918
doi: 10.1111/asj.12226
ORIGINAL ARTICLE Relationship of climatic conditions to fecal corticosterone levels of captive cheetahs reared in Japan Katsuji UETAKE,1 Yumi UNE,1 Shu ITO,2 Marino YAMABE,1 Hideto TOYODA1* and Toshio TANAKA1 1
School of Veterinary Medicine, Azabu University, Sagamihara and 2Wakayama Adventure World, Wakayama, Japan
ABSTRACT To assess the stress level of cheetahs reared in Japan and to identify the prime components of the climatic conditions that affect their thermal stress, fecal corticosterone was monitored for 8 months from May to the following January. A total of 203 fecal samples were gathered in the morning from seven adult cheetahs that were kept at a zoological garden in Wakayama, Japan. Cheetahs were on exhibit singly or together with a harmonious conspecific during the day, but housed singly at night. Although the monthly fluctuation in corticosterone concentrations was not significant, the concentrations were relatively low during the summer season. Individual differences among cheetahs and the interaction effect between individual and month on the corticosterone concentrations were significant. Whereas the corticosterone concentrations negatively correlated with air temperature, they were positively correlated with the amount of rainfall. The highest air temperature and the amount of rainfall were extracted as the prime factors affecting corticosterone concentrations. These results suggest that cheetahs reared in Japan are somewhat subjected to thermal stress, particularly on cooler and/or rainy days.
Key words: cheetah, climatic condition, fecal corticosterone, stress.
INTRODUCTION Livestock science has been contributing to the improvement of the breeding management technique of zoo animals. For instance, the knowledge of environmental physiology provides practical methods to improve their reproductive success through stress management (Terio et al. 2003). In order to assess thermal stress, the concept of temperature humidity index (THI) in farm animals (e.g. Berman 2005) is applied to zoo animals as well. The cheetah (Acinonyx jubatus) is an endangered species whose adult population is estimated to be only 7500 worldwide and has decreased 30% over the last 18 years (African Wildlife Foundation 2013). Most wild cheetahs are found in eastern and southwestern Africa, and they are under pressure as the wide-open grasslands they favor are disappearing at the hands of human settlers (National Geographic Society 2013). To ensure cheetahs’ future existence, some international protection projects have been conducted in their habitats. In addition, breeding programs, including artificial fertilization, have been tried in zoos around the world (Gugliotta 2008). © 2014 Japanese Society of Animal Science
In spite of various measures, the captive population of cheetahs has not been self-sustaining because of their poor reproductive performance and an increased prevalence of a certain kind of disease not commonly observed in wild cheetahs (Terio et al. 1999). Some of these problems may be caused by stress and result from maladaptation of cheetahs to present management conditions (Wielebnowski et al. 2002; Terio et al. 2004). Chronic stress of cheetahs has been demonstrated in a captive environment in comparison with a near-natural environment (Terio et al. 2004). This may be particularly true in climatic regions different from their original habitats. There are big climatic differences between Japan and the cheetah’s original habitats in eastern and
Correspondence: Katsuji Uetake, School of Veterinary Medicine, Azabu University, Chuo, Sagamihara, Kanagawa 2525201, Japan. (Email:[email protected]) *Present address: Saitama Children’s Zoo, Higashimatsuyama, Japan. Received 1 August 2013; accepted for publication 4 February 2014.
916 K. UETAKE et al.
southwestern Africa. Thus, the objectives of this study were to: (i) assess stress levels of cheetahs that are reared in Japan by monitoring fecal corticosterone concentrations; and (ii) determine the relationships between components of the climatic environment and the corticosterone response of cheetahs.
MATERIALS AND METHODS Fresh fecal samples were collected in the morning (09.00– 10.00 hours) at the animal house for 8 months (May 10, 2012–January 11, 2013) from seven adult cheetahs (two males and five females). The total number of samples was 203. The cheetahs were between four and nine years old, and weighed between 27 and 44 kg. All individuals had been kept at the Wakayama Adventure World (Shirahama, Wakayama, Japan) at least 4 months before the study. One female cheetah was born in South Africa and the others were born in Japan. The cheetahs were on exhibit from 09.45 to 16.40 hours during the summer season (May–September) and from 10.15 to 16.40 hours during the winter season (October–April). In addition, they were kept on exhibit until 20.30 hours in the mid-summer (July 28–September 1). Each cheetah was on exhibit alone or together with a harmonious conspecific, but housed singly at night. The areas of the animal house and the exhibit space were 3.8–5.3 m2 and 7500 m2, respectively. The animal house was concrete and the interior floor was waterproofed. The cheetahs were exposed to natural climatic conditions in the daytime and fed a beef-, horse- and/or cat food-based diet. Water was available ad libitum. Individual fecal samples were stored in a polypropylene bag and frozen at −80°C until drying. The fecal samples were dried with a drying oven (SDN27; Sansyo Co., Ltd, Tokyo, Japan) at 100°C for more than 16 h and then dried samples were powdered with a mill (IFM-800DG; Iwatani Corporation, Osaka, Japan). Powdered feces were extracted using a vortexing method modified from Wasser et al. (2000). Briefly, 0.1 g of dried sample was placed in a capped 2 mL microtube with 1 mL of 95.5% ethanol, vortexed (5 min) using the vortex mixer (Vortex-Genie2; M&S Instruments Inc., Osaka, Japan), and then centrifuged (CN-820; AS ONE Corporation, Osaka, Japan) for 5 min at 1050 × g. The supernatant was used to determine the fecal corticosterone concentrations with an enzyme immunoassay kit (ADV900-097; Cosmo Bio Co. Ltd, Tokyo, Japan). The extraction efficiency of exogenous corticosterone was 65.1% using this extraction method. All fecal concentration data were expressed as nanograms per gram of dry feces.
Seven components that comprise the climatic conditions were downloaded from the data provided by the Automated Meteorological Data Acquisition System (AMeDAS) of the Japan Meteorological Agency (JMA): the lowest, highest and mean air temperature (°C), lowest and average relative humidity (%), sunlight hours (h) and the amount of rainfall (mm). Data measured at Shionomisaki, which is nearest to Wakayama Adventure World, were used (Japan Meteorological Agency 2012–2013). A previous study reported that an elevation in blood cortisol concentration is followed 1–2 days later by a substantial increase in fecal corticoid excretion in cats (Graham & Brown 1996). Thus, the climatic data of the previous day were matched with the fecal corticosterone data for statistical analysis. Statistics describing the climatic conditions used in the analyses are shown in Table 1. An unbalanced mixed model analysis of variance was performed (SAS version 9.3; SAS Institute Inc., Cary, NC, USA). Eight months, considered as a fixed effect, and seven cheetahs, considered as a random effect, were analyzed. The month × cheetah interaction was declared as a random effect. Pearson’s correlations were performed to determine the relationships between components of the climatic conditions and fecal corticosterone concentrations of cheetahs. Then stepwise regression analyses were performed to identify the prime factors affecting a cheetah’s thermal stress. The forward model-selection method and the criteria of an F-value larger than 2 were applied. These two kinds of analyses were carried out with the statistical software program Statcel3 (version 3, 2011; OMS Publishing Inc., Tokyo, Japan).
RESULTS AND DISCUSSION Figure 1 shows the day-to-day variation in fecal corticosterone concentrations of subject cheetahs (lower) with the highest air temperature and the amount of rainfall (upper) during the experimental period. Although a significant monthly fluctuation in fecal corticosterone concentrations was not confirmed (F8, 52.0 = 1.24, P = 0.298), only 8% (5/62) of samples showed a concentration higher than 500 ng/g dry feces, which reflect stress response (Terio et al. 1999), during the summer season from July to September. On the other hand, that rate was 19% (27/141) in the months excluding the summer season. Individual differences among cheetahs (F6, 55.9 = 7.37, P < 0.001) and
Table 1 Climatic conditions analyzed in this study
Variable Air temperature (°C) Lowest Highest Mean Relative humidity (%) Lowest Mean Sunlight hours (h) Amount of rainfall (mm)
Mean
SD
Maximum
Minimum
16.3 21.9 19.0
7.4 6.8 7.1
26.3 30.4 27.7
1.3 7.6 3.8
56.3 72.1 6.6 6.2
15.6 13.9 3.6 16.6
87.0 95.0 12.7 85.5
28.0 46.0 0.0 0.0
n = 203.
© 2014 Japanese Society of Animal Science
Animal Science Journal (2014) 85, 915–918
CLIMATIC STRESS IN CHEETAHS
90
35
70 25 60 20
50
15
40 30
䕔 Amount of rainfall 䠄mm䠅
80
30
䕺 Highest air temperature䠄℃䠅
917
10 20 5
10 0 1/9
1/2
12/26
12/19
12/5
12/12
11/28
11/21
11/7
11/14
10/31
10/17
10/24
10/3
10/10
9/26
9/19
9/5
9/12
8/29
8/22
8/8
8/15
8/1
7/25
7/18
7/4
7/11
6/27
6/20
6/6
6/13
5/30
5/23
5/9
5/16
0
14,000
Fecal corƟcosterone concentraƟon 䠄ng/g dry feces䠅
#1 #2
12,000
#3 #4
10,000
#5 #6 #7
8,000
6,000
4,000
2,000
1/10
1/3
12/27
12/20
12/13
12/6
11/29
11/15
11/22
11/8
11/1
10/25
10/18
10/11
10/4
9/27
9/20
9/13
9/6
8/30
8/23
8/16
8/9
8/2
7/26
7/19
7/12
7/5
6/28
6/21
6/14
6/7
5/31
5/24
5/17
5/10
0
Figure 1 The day-to-day variation of fecal corticosterone concentrations of subject cheetahs (lower) and the highest air temperature and the amount of rainfall (upper) during the experimental period.
the interaction effect between individual and month (F48, 140 = 1.51, P < 0.05) were both significant. Table 2 shows correlation coefficients between components of the climatic conditions and fecal corticosterone concentrations of cheetahs (n = 203). The lowest (r = −0.151, P < 0.05), highest (r = −0.161, P < 0.05) and mean (r = −0.155, P < 0.05) air temperature had negative correlations, and the amount of rainfall (r = 0.166, P < 0.05) had a positive correlation with fecal corticosterone concentrations. Neither the lowest or average relative humidity had significant correlations. In stepwise multiple regression analyses, the highest air temperature and the amount of rainfall indepenAnimal Science Journal (2014) 85, 915–918
Table 2 Correlation coefficients between components of climatic conditions and fecal corticosterone concentrations of cheetahs
Variable
Fecal corticosterone concentration
Lowest air temperature Highest air temperature Mean air temperature Lowest relative humidity Average relative humidity Sunlight hours Amount of rainfall
−0.151* −0.161* −0.155* −0.055 −0.070 −0.110 0.166*
Pearson’s correlation coefficient; n = 203, *P < 0.05.
© 2014 Japanese Society of Animal Science
918 K. UETAKE et al.
dently correlated with fecal corticosterone concentrations of cheetahs (R2 = 0.058, F2, 200 = 6.13, P < 0.01). The contributions to R2 were 0.030 and 0.028, respectively. The regression coefficients were −44.08 for the highest air temperature (F1, 200 = 6.40, P < 0.05) and 18.53 for the amount of rainfall (F1, 200 = 6.78, P < 0.01). Fecal corticosterone concentrations of cheetahs were relatively low during the summer season from July to September. The highest air temperature, which was identified as one of the prime factors affecting their thermal stress, was more than 25°C throughout the summer season. On the other hand, some individuals occasionally showed high fecal corticosterone concentrations on the day after a day when air temperature decreased during the spring and autumn seasons. This sensitiveness to cold temperature appears not only in the significant interaction effect between individual and month, but also in the significant negative correlations between all three variables concerning air temperature and fecal corticosterone concentrations. Wild cheetahs are mainly found in eastern and southwestern Africa (National Geographic Society 2013) where the air temperature is stable at around 20–25°C through the year (Japan Meteorological Agency 2013). In addition to this low temperature fluctuation, those regions have a small amount of rainfall from June to September (Japan Meteorological Agency 2013). In contrast, the neighborhood of the Wakayama Adventure World has the highest rainfall during these months (Japan Meteorological Agency 2012–2013). Thus, these climatic differences between Japan and their native habitat, particularly in summer, would result in thermal stress in cheetahs. Although significant statistically, the contributions of climatic components (highest air temperature and amount of rainfall) to considerable variations in fecal corticosterone concentrations were not more than 10%. Thus investigation is necessary about a complex index like the THI in livestock. In addition, at the individual level, some specific cheetahs showed a high corticosterone concentration. Therefore, attention is of course needed on other management-related and/or animal-related (social) factors (Terio et al. 1999; Wielebnowski et al. 2002; Wells et al. 2004) in order to reduce stress in captive cheetahs (Terio et al. 2004). It will be needed to consider these factors in future.
REFERENCES African Wildlife Foundation (AWF). 2013. The cheetah’s habitat is now only 25% of its former size. [homepage on the internet]. AWF, Karen; [cited 18 April 2013]. Available from URL: http://www.awf.org/wildlife -conservation/cheetah Berman A. 2005. Estimates of heat stress relief need for Holstein dairy cows. Journal of Animal Science 83, 1377– 1384. Graham L, Brown J. 1996. Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered fields. Zoo Biology 15, 71–82. Gugliotta G. 2008. Rare breed – can Laurie Marker help the world’s fastest mammal outrun its fate? [homepage on the internet]. Smithsonian Magazine, Washington, DC; [cited 26 June 2013]. Available from URL: http:// www.smithsonianmag.com/science-nature/rarebreed.html Japan Meteorological Agency (JMA). 2012–2013. Past weather data search. (In Japanese) [homepage on the internet]. JMA, Tokyo; [cited 9 April 2013]. Available from URL: http://www.data.jma.go.jp/obd/stats/etrn/ Japan Meteorological Agency (JMA). 2013. World weather chart. (In Japanese) [homepage on the internet]. JMA, Tokyo; [cited 2 July 2013]. Available from URL: http:// www.data.jma.go.jp/gmd/cpd/db/monitor/ ?tm=normal&el=rn National Geographic Society (NGS). 2013. Cheetah. [homepage on the internet]. NGS, Washington, DC; [cited 18 April 2013]. Available from URL: http://animals .nationalgeographic.com/animals/mammals/cheetah/ Terio KA, Citino SB, Brown JL. 1999. Fecal cortisol metabolite analysis for noninvasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). Journal of Zoo and Wildlife Medicine 30, 484–491. Terio KA, Marker L, Munson L. 2004. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. Journal of Wildlife Diseases 40, 259–266. Terio KA, Marker L, Overstrom EW, Brown JL. 2003. Analysis of ovarian and adrenal activity in Namibian cheetahs. South African Journal of Wildlife Research 33, 71–76. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett M, Bechert U, et al. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General and Comparative Endocrinology 120, 260–275. Wells A, Terio KA, Ziccardi MH, Munson L. 2004. The stress response to environmental change in captive cheetahs (Acinonyx jubatus). Journal of Zoo and Wildlife Medicine 35, 8–14. Wielebnowski NC, Ziegler K, Wildt DE, Lukas J, Brown JL. 2002. Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus). Animal Conservation 5, 291–301.
ACKNOWLEDGMENTS We thank Ms. Ayaka Mutoh and other staff members in charge of rearing cheetahs at the Wakayama Adventure World for their contribution to fecal sampling.
© 2014 Japanese Society of Animal Science
Animal Science Journal (2014) 85, 915–918
