Body temperatures of Manis pentadactyla and Manis javanica.

Body temperature is an important parameter for assessing animal health and physiological function. An iButton thermometer was used to measure the body temperatures of three Chinese pangolins (Manis pentadacyla) and three Sunda pangolins (M. javanica). The body temperature of Chinese pangolins was 33.2 ± 0.95°C (30.6-34.2°C, n = 3) and that of Sunda pangolins was 32.8 ± 0.48°C (31.7-34.2°C, n = 3). The daily variation in body temperature was 1.0-2.9°C in three Chinese pangolins and 1.2-1.9°C in three Sunda pangolins. The body temperature of Sunda pangolins tended to rise at night, with the highest body temperatures occurring mostly at night. This study provides valuable body temperature data for Chinese and Sunda pangolins and lays the foundation for future research on their mechanisms of body temperature regulation.

INTRODUCTION

Mammals are advance endothermal animals that able to maintain stable body temperatures within certain ambient temperature ranges (Yang, 2015). Mammals able to maintain is temperature as it has a high degree of metabolic heat production and various mechanisms to control body‐surface heat dissipation (Li & Zheng, 2009). In addition, mammals are able to maintain homeostasis when faced with changes in environmental factors (Sun, 2001; Liu & Zheng, 2009). Approximately 95% of mammals belong to Eutheria, a group of higher mammals with good thermoregulatory abilities (Liu & Zheng, 2009). Refinetti (2010) summarised the body temperatures of more than 60 mammalian species and found that most species had body temperatures of 36.0–40.4°C, with significant differences in the body temperatures of different types of animals.

Body temperature is the average heat energy generated by the internal metabolism of animals (Yang, 2015). Stable body temperature is an important prerequisite for maintaining normal metabolism and life activities in animals (Chen, 2019). The body temperature of mammals remain relatively constant to certain ambient temperatures. However, when ambient temperatures are too high or low, the body temperatures will fluctuate significantly (Fuller et al., 1978; Refinetti, 1996, 1997). A number of factors such as age, food availability, reproductive status and activity level can affect physiological function of animal body temperature (Refinetti & Menaker, 1992; Refinetti, 2010).

Pangolins belong to the order Pholidota that lacks dense hair and its body covered with scales (Corbet & Hill, 1992; Gaubert & Antunes, 2005; Gaudin et al., 2020). Pangolins are unable to adapt to environmental temperature fluctuation and pangolins kept in captivity are susceptible to pneumonia due to sudden temperature flunctuation (Wang 2012). Data on the body temperatures of healthy Chinese and Sunda pangolins have not been established. Heath and Hammel (1986) measured the body temperatures of four Chinese pangolins (two males and two females) and found that their body temperatures were maintained within a range of 33–35°C. McNab (1984) found the body temperatures of a juvenile male and an adult female Sunda pangolin to be 31.7°C and 32.3°C, respectively. Heath (1987) collected continuous body temperature data on four Chinese pangolins and the results show an obvious body temperature fluctuation rhythms. Body temperatures were lower during the day than at night, with the highest temperature around midnight and the lowest around noon. However, previous studies have not consistently measured body temperature or daily fluctuations in body temperature.

The purpose of this study is to understand body temperature characteristics and fluctuation patterns in Chinese and Sunda pangolins and to increase our knowledge of basic physiological data of pangolins.

MATERIALS AND METHODS

Study animals

A total of three Chinese pangolins and three Sunda pangolins were used in this study. The Chinese pangolin numbered HS09 and the three Sunda pangolins numbered FS06, FS15 and FS18 were from the Pangolin Research Base for Artificial Rescue and Conservation Breeding of South China Normal University, Guangdong, China. Pangolins were kept in separate enclosures with artificial food and drinking water were provided daily (Zhang et al., 2015, 2017). The two Chinese pangolins numbered GX01 and GX02 were kept at the Terrestrial Wildlife Rescue Center of the Guangxi Zhuang Autonomous Region, Guangxi, China. These two pangolins were kept at a different location and provided a different diet. All pangolins were in good health during the study with normal levels of activity, eating and defecating. When body temperatures were measured, all pangolins appeared in good physical and mental condition with normal levels of activity, eating and defecating.

Measuring body temperature

Body temperatures of the pangolins were measured using the DS1922L temperature recorder (Wodisen Electronic Technology Company, Shanghai, China). The device measured temperature every 10 min, and the data were stored in the instrument. Data were transferred by ElitechLog V3.0.0. to Microsoft Excel 2010 for analysis. The temperature measurements stopped when the thermometer dropped from the animal's rectum.

The DS1922L temperature recorder was wrapped with rubber film and a length of string (0.3 m) was attached before the study. The film was used to protect the instrument from short circuits and the string was used to retrieve the button thermometer from the animal's rectum at the end of the study. After preparations were complete, the tail of the pangolin were lifted so that its body was perpendicular to the ground with the anus exposed and let the pangolin's forelimbs and head dangle close to the ground to prevent it from curling. Blunt long tweezers were used to clamp the end of the temperature recorder and applied lubricant to the film covering the recorder. When the pangolin was in a relaxed state, the temperature recorder were placed approximately 3 cm into the rectum to measure the animal's rectal temperature. Finally, after situating the temperature recorder, the handler gently put the pangolin down and observed it for 15 min to ensure that the animal showed no abnormal behaviour and that the thermometer did not fall from the anus.

Measuring ambient temperature

The DS1922L temperature recorder was placed approximately 30 cm from the ground to measure the ambient temperature of the enclosure.

Data collation and analysis

The data were sorted and analysed using Microsoft Excel 2010 and IBM SSPS 19.0 and are expressed as the mean ± SD. SigmaPlot 12.5 was used to draw a timing sequence diagram for body temperature.

RESULTS

Pangolin body temperature

The body temperatures of the six pangolins are shown in Table 1. The mean body temperature of the three Chinese pangolins was 33.2 ± 0.95°C (30.6–34.2°C) and the three Sunda pangolins was 32.8 ± 0.48°C (31.7–34.2°C).

TABLE 1

Body temperatures of pangolins

Species	No.	Sex	Body weight (kg)	Body temperature (°C, mean ± SD)
Manis pentadactyla	HS09	♀	4.93	31.7 ± 0.79 (30.6–33.5, n = 124)
	GX01	♂	5.50	33.6 ± 0.23 (33.2–34.2, n = 99)
	GX02	♀	7.50	33.7 ± 0.28 (32.8–34.2, n = 269)
Manis javanica	FS06	♀	3.75	32.8 ± 0.47 (31.8–34.1, n = 1424)
	FS15	♂	3.90	32.9 ± 0.56 (31.7–34.0, n = 216)
	FS18	♂	4.07	33.0 ± 0.37 (32.4–34.2, n = 144)

Fluctuations in body temperature

Fluctuations in the body temperatures of four pangolins are shown in Table 2. The body temperature fluctuations of pangolins FS15 and FS18 were not recorded as the iButton dropped from these individuals during the study. The body temperatures of the Chinese pangolins fluctuated from 1.0°C to 2.9°C (HS09, GX01 and GX02) and the body temperature of the Sunda pangolin (FS06) fluctuated from 1.2°C to 1.9°C. Continuous recording of body temperature for 9 consecutive days was obtained for only one Sunda pangolin (FS06). Figure 1 shows that body temperatures exhibited an upward trend at night. The highest body temperature (+1.9°C) of the animals occurred mostly at night (Table 3). The accumulated daytime body temperature of FS06 was 21001.4°C which was lower than the accumulated nighttime body temperature (21518.1°C).

TABLE 2

Body temperature fluctuations in pangolins

Species	No.	Time	Duration (h)	Lowest (°C)	Highest (°C)	Range (°C)
Manis pentadactyla	HS09	2018/5/11 23:30–5/13 00:30	25	30.6	33.5	2.9
	GX01	2019/6/23 11:30–23:50	12	33.2	34.2	1.0
	GX02	2019/6/23 23:20–6/25 9:00	33.5	32.9	34.2	1.3
Manis javanica	FS06	2018/12/28 0:00–24:00	24	32.7	33.9	1.2
		2018/12/29 0:00–24:00	24	32.2	33.6	1.4
		2018/12/30 0:00–24:00	24	32.2	34.1	1.9
		2018/12/31 0:00–24:00	24	32.2	33.5	1.3
		2019/1/1 0:00–24:00	24	31.9	33.3	1.4
		2019/1/2 0:00–24:00	24	31.9	33.6	1.7
		2019/1/3 0:00–24:00	24	32.2	33.5	1.3
		2019/1/4 0:00–24:00	24	31.8	33.2	1.4
		2019/1/5 0:00–24:00	24	31.9	33.3	1.4
		2019/1/6 0:00–21:20	21.5	31.5	33.1	1.6

The body temperature of HS09 was measured at ambient temperatures of 22.7–30.5°C. The body temperatures of GX01 and GX02 were measured at ambient temperatures of 27.4–29.6°C. The body temperatures of FS06, FS15 and FS18 were measured at ambient temperatures of 25.8–28.5°C.

FIGURE 1

Variations in Sunda pangolin FS06 body temperature (mean)

TABLE 3

Extreme temperatures of Sunda pangolin FS06

Date	Body temperature (Max/Min,°C)		Time	Day/night
2018.12.28	Max	33.9	20:20	N
	Min	32.7	14:10	D
2018.12.29	Max	33.6	20:30	N
	Min	32.2	13:00	D
2018.12.30	Max	34.1	08:20	D
	Min	32.2	23:50	N
2018.12.31	Max	33.5	20:00	N
	Min	32.2	03:50	N
2019.01.01	Max	33.3	23:50	N
	Min	31.9	15:20	D
2019.01.02	Max	33.6	21:40	N
	Min	31.9	12:50	D
2019.01.03	Max	33.5	23:40	N
	Min	32.2	12:50	D
2019.01.04	Max	33.2	23:40	N
	Min	31.8	20:30	N
2019.01.05	Max	33.3	23:40	N
	Min	31.9	03:40	N

Day 06:00–18:00, Night 18:00–06:00.

DISCUSSION

The body temperature of Chinese pangolins in this study was 33.20 ± 0.95°C and that of Sunda pangolins was 32.80 ± 0.48°C. The body temperature for both species were lower than the body temperature of Eutheria (35.0–39.0°C). The findings are similar to those reported previously in other pangolins (Table 4).

TABLE 4

Published data on pangolin body temperature

Species	Sex	Mass (kg)	Body temperature (°C)	Source
Manis pentadactyla	2♀2♂	2.3–5.2	33–35	Heath and Hammel, 1986
	2♀1♂	4.93–7.50	30.60–34.20	This study
Manis javanica	1♀1♂	2.11–4.22	31.7, 32.3	McNab, 1984
	1♀2♂	3.75–4.07	31.70–34.20	This study
Manis crassicaudata	—	15.91	31.7	McNab, 1984
Phataginus tricuspis	1♀2♂	—	28.8–33.3	Jones, 1973
	—	2.73	30.0–36.0	Hildwein, 1974
	—	—	32.2–35.2	Eisentraut, 1956
Smutsia gigantea	1♀1♂	—	32.0–34.5	Jones, 1973
Phataginus tetradactyla	—	—	30.0–36.0	Hildwein, 1974

The body temperature of an animal is closely related to its basal metabolic rate (Chen, 2019). The basal metabolic rate of animals is affected by many factors including body weight, phylogeny, diet, climate, season, habits, and reproduction (Song & Wang, 2002). The low body temperatures in pangolins are possibly due to the low metabolic rates of species. Kleiber (1932) suggested that the low body temperature are related to the diet of pangolins as diets of Chinese and Sunda pangolin consist primarily of ants and termites. These food items have high fractions of non‐digestible chitinous exoskeleton (Heath & Hammel, 1986; Wu et al., 2005). Pangolin will ingest both the prey and non‐digestible debris of its prey (McNab, 1984). The ingestion of non‐digestible debris will reduce the nutritional and caloric density of the food (McNab, 1984). Additionally, these low caloric dense foods are not abundant enough to permit their predators to maintain constant or periodic high rates of energy expenditure (McNab, 1984).

The body temperature fluctuations of the Chinese pangolins measured in this study were as high as 2.9°C, that was greater than 48 species of Eutheria recorded by Refinetti (2010) that recorded fluctuation of 2.5°C of its body temperature. Previous studies on two African pangolins, Phataginus tricuspis and P. tetradactyla also recorded temperature fluctuations of 2.5°C and 4.5°C, respectively (Jones, 1973). Pangolins have poor temperature regulation due to the lack of heat‐insulating fur and their hair erector muscles are underdeveloped (Heath & Hammel, 1986). This hinders the prevention of heat loss and leads to fluctuations of its body temperature (Heath & Hammel, 1986).

Authors found that the highest body temperatures of Sunda pangolin FS06 occurred mostly at night. The higher body temperature at night than during the day may be related to its activity levels. Sunda pangolins are nocturnal mammals, and their activity level is highest at night. Sunda pangolin FS06 was observed to emerge mainly after 20:00 and was provided with artificial food from 23:00 to 00:00 every day. This increase of activity level leads to increased metabolic rate and body temperature. A similar finding was recorded in three Chinese pangolins when their body temperature changes were recorded in day time and night time (Heath, 1987). The daily fluctuation in body temperatures was 0.5–1.9°C with the highest body temperature occurred at night and the lowest during the day. Pangolin body temperature increased significantly after pangolin increase its activity at night.

This study provides baseline data on the body temperatures of pangolins that provide for the management of captive pangolins. These baseline data on the body temperature ranges of Chinese and Sunda pangolins enable researchers to monitor pangolin health status and detect physiological abnormalities that may affect pangolin health.

AUTHOR CONTRIBUTIONS

Yishuang Yu: Investigation, methodology and writing‐original draft. Shibao Wu: Conceptualisation, data curation, project administration and supervision. Fuhua Zhang: Investigation and supervision. Amna Mahmood: Writing‐review and editing. Wenhua Wang: Investigation.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.611