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Energy metabolism and thermoregulation in pygmy lorises (Nycticebus pygmaeus) from Yunnan Daweishan Nature Reserve
Acta Ecologica Sinica 30 (2010) 129–134
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Energy metabolism and thermoregulation in pygmy lorises (Nycticebus pygmaeus) from Yunnan Daweishan Nature Reserve Xiao CaiHong a,b,c, Wang ZhengKun a,b,c,*, Zhu WanLong a,b,c, Chu YongXing d, Liu ChunYan a,b,c, Jia Ting a,b,c, Meng LiHua a,b,c, Cai JinHong a,b,c a
School of Life Sciences, Yunnan Normal University, Kunming 650092, China Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming 650092, China The Key Laboratory of Biomass Energy and Environmental Biotechnology in Yunnan Province, Kunming 650092, China d Yunnan Daweishan National Nature Reserve, Yunnan Pingbian County 661200, China b c
a r t i c l e
i n f o
Keywords: Pygmy loris (Nycticebus pygmaeus) Energy budget RMR Body temperature Thermal conductance
a b s t r a c t The pygmy loris (Nycticebus pygmaeus) is a small prosimian living in Vietnam, Laos, eastern Cambodia and the south part of China. In China it is only found in Pingbian, Hekou, Jinping, Luchun of Yunnan. As N. pygmaeus is seriously threatened by hunting, trade and habitat destruction, it is listed in Appendix II of CITES, and in 2006 the IUCN classified it as ‘‘vulnerable”. In order to understand the characteristics of energy metabolism and thermoregulation of N. pygmaeus, the resting metabolic rate (RMR) and body temperature (Tb) at different ambient temperature (Ta) of pygmy lorises, as well as body mass, energy intake, digestable energy intake, digestability and the thermal conductance were measured in captivity. The results obtained mainly are as follows: (1) Pygmy loris feed dry food averaged 12.90 ± 1.02 g/d. They could gain 214.87 ± 16.65 kJ/d from food intake, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability. (2) The Tb at room temperatures was a little low (35.23 ± 0.16 °C) and varied with Ta from 25 °C to 35 °C. There was a positive relationship between Tb and Ta, which was described as: Tb = 27.22 + 0.34Ta (r = 0.880). (3) The resting metabolic rate (RMR) of the pygmy loris was 0.3844 ± 0.0162 mlO2/g/h, which was 51.91 ± 1.90% of the previous predicted rate by Kleiber (1961) [21]. (4) The average thermal conductance of the pygmy loris (N. pygmaeus) was 0.0449 ± 0.0031 mlO2/g/h/°C. These characteristics of energy metabolism and thermoregulation of N. pygmaeus in Yunnan Daweishan Nature Reserve might be considered as the adaptive characteristics to their environment in tropical semi-evergreen forests and secondary forests. Ó 2010 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction Genus Nycticebus belongs to Mammalia; Eutheria; Primates; Suborder Prosimii; and Family Loridae. It is generally believed that the slow lorises (Nycticebus coucang and Nycticebus bengalensis) and pygmy lorises (Nycticebus pygmaeus) are two species that belong to Nycticebus. But N. pygmaeus has a much more limited distribution range than the slow lorises [1], scantly covering Vietnam, eastern Cambodia, Lao PDR and Yunnan Province in Southern China. In China it is only found in Pingbian, Hekou, Jinping and Luchun of Yunnan from the year of 1986 [2–4]. N. pygmaeus is a nocturnal and almost entirely arboreal primate species. It typically lives in semi-evergreen and secondary forests [1,5,6]. Due to their nocturnal, arboreal lifestyle and their latent habit, pygmy lorises have been widely ignored in by field studies and * Corresponding author at: School of Life Sciences, Yunnan Normal University, Kunming 650092, China. E-mail address: [email protected] (Z.K. Wang).
well-based data are lacking. In physiological ecology field, only temperature regulation and cellular respiration of the pygmy lorises were reported as yet [7,8]. N. pygmaeus is one of the least studied species of all prosimians [9]. It is listed in Appendix II of CITES. In its latest assessment in 2006 the IUCN (The World Conservation Union) classified the pygmy lorises as ‘‘vulnerable” [10]. It is also listed as one of the first protected animals in China. The energy metabolic level always decided species’ distribution, diversity, breed and fitness. Thermal features and temperature regulation of the animals are usually related to their energy use, distribution, life histories and evolution, reflecting their adaptation mode and physiological capability [11–13]. The use of BMR as an important index of energy expenditure from intraspecies to interspecies has received a great deal of attention from ecophysiologists and comparative physiologists for several decade years [14]. The factors influencing the level of BMR in mammals have been examined several times so far. One of the first was by Hayssen and Lacy, who argued that body mass was the single most important factor influencing the BMR of 248 species [15]. Soon thereafter an analysis
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of data from 321 species of mammals demonstrated that BMR correlated with body mass, food habits, and taxonomy [16]. Recently, the factors that influence the level and scaling of BMR in mammals are justified because almost twice as many species have had adequate estimates of their basal rates of metabolism reported. Data on body mass and BMR were presented on 639 species of mammals along with information on the ecological and behavioral characteristics of these species, including food habits, climate, habitat, substrate used, their exclusive occurrence on mountains or islands, and their use of torpor. It is suggested that individuals from only one population can properly represent a species because individuals living in different environments often have different basal rates [14]. Presumably, the level of energy metabolism in mammals that live in the areas of origin may also be different from living in the laboratory. But most studies of animal’s energy metabolism were conducted in laboratory on captive animal before, while scarcely in their country of origin. In this study we measured the digestible energy of N. pygmaeus in Yunnan Daweishan Nature Reserve, as well as the resting metabolic rate (RMR) and the body temperature (Tb) at different ambient temperature (Ta), and hoped to offer some basic materials to the conservation of N. pygmaeus in situ. 2. Materials and methods 2.1. Samples National Nature Reserve of Dawei Mountain lies to the south of the North-Tropic of Cancer, east longitudes 103°200 –104°030 , north latitudes 22°350 –23°070 , with a total territory of 153.7 km2. The Dawei Mountain where the reserve is located, is situated to the southeast part of China, Red River state, including the county of Pingbian, Hekou, Gejiu and Mengzi. The highest peak, Dajian Peak has an elevation of 2365 m, the second highest mountain, Dawei Mountain, 2345 m, and the lowest, 225 m in the area. Because of the barrier of the surrounding high mountains with only the narrow Red River valley mouth (76.4 m elevation) in its southeast leading to the north bay of Vietnam, this area becomes the only place that is affected most profoundly by the southeast tropical monsoon with warm and humid currents in the whole Yunnan Province. It has ample rainfall and heat, hot and rainy in summer, warm, humid, and foggy in winter with an average annual temperature of 22.6 °C. N. pygmaeus generally lives in the semi-evergreen and secondary forests of Daweishan Nature Reserve. A total of 6 N. pygmaeus (male 4, average body mass is 429.56 ± 14.01 g, n = 60 and female 2, average body mass is 538.81 ± 6.17 g, n = 30), all healthy adults, were bred in Yunnan Daweishan Nature Reserve. They were placed in cage (400 mm 200 mm 200 mm), one in a cage, and were provided with natural illumination. Average room temperature was 25.97 °C (23.4– 28.7 °C), and average relative humidity was 140.22% (105.3– 162.6%). Their average body temperature is 35.23 °C, varying from 32.3 °C to 36.9 °C. They were feeding honey, apple, banana, ripe egg white and vitelline in fix quantity and timing everyday, in addition to 50 ml water. In experimental period, they lived healthily. 2.2. Measurement of energy budget Energy expenditure was measured in the pygmy loris according to energy balance [17]. Before the test, animals were breeding in cage a week. We measured animal’s body mass, feed them in a certain ration, and sampled food to dry for finding their water content between 14:30 and 15:00 one day before. At the time of test, we diurnally repeated to measure animal’s body mass, gather food residue and feces, then feed them in the same proportion, and sampled food to dry for finding their water content between 14:30 and 15:00 from
the first day to the eight day. Food and feces was dried using vacuum drying chamber, and measured energy contained by use of fullautomatic calorimeter (YX-ZR/Q, U-THERM, Changsha China). We calculated energy intake, feces energy, digestable energy intake and digestability according to the following equations [17,18]: Energy intake ðkJ=dÞ ¼ Dry mass of food intake ðg=dÞFood caloric ðkJ=gÞ Feces energy ðkJ=dÞ ¼ Dry mass of feces ðg=dÞFeces caloric ðkJ=gÞ Digestable energy intake ðkJ=dÞ ¼ Energy intake ðkJ=dÞFeces energy ðkJ=dÞ Digestability ð%Þ ¼ Digestable energy intake ðkJ=dÞ=Energy intake ðkJ=dÞ100%
2.3. Measurement of metabolic rates Metabolic rates of N. pygmaeus were measured using the closed-circuit respirometer at 25 °C, 27.5 °C, 30 °C, 32.5 °C and 35 °C according to Gorecki [19]. Briefly, the temperature of metabolic chamber was controlled within ±0.5 °C by water bath. Carbon dioxide and water in the metabolic chamber were absorbed with KOH and silica gel. At the time of measurement, animals were fasted 5 h prior to being put into the metabolic chamber. After 60 min stabilization in the chamber, metabolic measurement was conducted for 60 min. Oxygen consumption was recorded at 5-min intervals. Three continuous stable minimum recordings were taken to calculate RMR. Before and after each test, the animal’s body mass was measured. Metabolic rates were expressed as mlO2/g/h and corrected to standard temperature and air pressure (STP) conditions. Body temperature was measured by a digital thermometer after each experiment. Considering the influence of the day and night rhythm, all measurement was made between 18:00 and 24:00. 2.4. Thermal conductance (C) If corresponded with Newton’s law of cooling, thermal conductance was evaluated as C = RMR/(Tb Ta), where RMR is the basal metabolic rate (BMR) (mlO2/g/h), Tb is the body temperature (°C), and Ta is the ambient temperature (°C) [20]. But if not, we must correct it according to the equation: Cm = Cf(1 + 0.06DTb), where Cm is the minimum thermal conductance, Cf is the gradient of the regression both RMR and Ta, and the DTb is the balance between actual body temperature and theoretic body temperature. 2.5. Statistical analyses Statistical analyses were performed using SPSS for Windows 16.0 software package. Food intake, feces discharged, energy intake, digestable energy intake and digestability of the pygmy lorises were analysed using independence sample T-test and repeat metrical regression. In order to remove the effect of body mass, analysis of covariance (ANCOVA) was used to analyse the data, using body mass as the covariate. Differences among groups were determined by one-way ANOVA, and linear regression analysis was used to analyse the relationship between body temperature (Tb), metabolic rates, thermal conductance (C) and ambient temperature (Ta). Least significant difference (LSD) was used for statistical analysis of different groups. All data in this paper were reported as mean ± standard deviation and P < 0.05 was taken to be statistically significant. 3. Results 3.1. Energy budget There are five kind of food, including honey, apple, banana, egg white and vitelline. Their water content and energy contained are shown in Table 1.
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C.H. Xiao et al. / Acta Ecologica Sinica 30 (2010) 129–134 Table 1 The water content and energy contained per gram of food. Food
Water content (%)
Energy contained per gram (kJ/g)
Honey Apple Banana Egg White Vitelline
20.39 ± 0.07 83.64 ± 0.05 78.65 ± 0.46 85.45 ± 0.19 49.59 ± 0.03
14.79 ± 0.21 16.11 ± 0.16 15.38 ± 0.15 20.64 ± 0.76 31.47 ± 0.18
(7) (7) (7) (7) (7)
(7) (7) (7) (7) (7)
Note: The number of the bracket denotes the times of testing in each food.
The average body mass of N. pygmaeus was 465.98 ± 12.12 g (n = 48), and changed indistinctively in experimental period (F(1,8) = 0.026, P > 0.05). The pygmy loris feed dry food averaged 12.90 ± 1.02 g/d which was about 2.67% ± 0.20% of body weight. They could gain 214.87 ± 16.65 kJ/d from food intake, while lost 14.72 ± 1.04 kJ/d through feces, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability (Table 2). The result showed that the effect of body mass was not statistically significant to the food intake (F = 1.097, P > 0.05), energy intake (F = 1.128, P > 0.05), digestable energy intake (F = 1.042, P > 0.05) and digestability (F = 3.717, P > 0.05) through the analysis of covariance. By using analysis of repeat metrical regression, Food intake (F(1,6) = 1.765, P > 0.05), feces discharged (F(1,6) = 0.192, P > 0.05), energy intake (F(1,6) = 1.422, P > 0.05), feces energy (F(1,6) = 0.324, P > 0.05), digestable energy intake (F(1,6) = 1.496, P > 0.05) and digestability (F(1,6) = 1.257, P > 0.05) of the pygmy lorises were taken to be statistically insignificant in the eight continuously experimental days. 3.2. Body temperature (Tb) The Tb of N. pygmaeus at room temperatures was a little low (35.23 ± 0.16 °C, n = 48) and varied with Ta from 25 °C to 35 °C. There was a positive relationship between Tb and Ta, which was represented by the following equation: Tb = 27.22 + 0.34Ta (r = 0.880) (Fig. 1, **P < 0.01). 3.3. Metabolic rates Using analysis of repeat metrical regression, when Ta is between 27.5 and 35 °C, oxygen consumption in pygmy loris did not show significant correlation (P > 0.05) (Fig. 2). Hence the thermal neutral zone (TNZ) of N. pygmaeus was 27.5–35 °C. In the TNZ, BMR of N. pygmaeus was 0.3844 ± 0.0162 mlO2/g/h, and Kleiber’s [21] body mass predicted value was 51.91% ± 1.90%, While Haysseen and Lacy’s [15], McNab’s [16] and McNab’s [14], respectively, were 57.78% ± 2.06%, 64.12% ± 2.31% and 67.77% ± 2.42%.
Fig. 1. The relationship between body temperatures and ambient temperatures in pygmy loris.
3.4. Thermal conductance There are two conditions in calculating thermal conductance using Newton’s law of cooling. On the one hand, there is a linear correlation between oxygen consumption and ambient temperature. On the other hand, the intersection of regression line between RMR and Ta in X axis equal to the body temperature, when RMR is zero. From the result of this study, there was a relation of correlation and regression between RMR and Ta, which was represented by the following equation: RMR(mlO2/g/h) = 1.041 0.02Ta (N = 30, P < 0.001). But when RMR reached up to zero, the point of the regression line in X axis (52.0 °C) was bigger than actual body temperature (31.25 °C). For this reason, we corrected it according to the equation: Cm = Cf(1 + 0.06DTb) [20], calculated that the thermal conductance (Cm) of N. pygmaeus was 0.0449 ± 0.0031 mlO2/g/h/°C, and McNab’s predicted value (C = 1.02W0.51) was 99.12 ± 6.33% [22].
4. Discussions 4.1. Energy budget All energy required in animals comes from food. The abundance, quality, and the assimilation of food have an important effect on the level of energy metabolism, which plays an important
Table 2 The energy budget of Nycticebus pygmaeus in Yunnan Daweishan Nature Reserve (n = 6). Energy budget
EI (kJ/d)
EI/BW (kJ/d/g)
FE (kJ/d)
FE/BW (kJ/d/g)
DEI (kJ/d)
DEI/BW (kJ/d/g)
1 day 2 day 3 day 4 day 5 day 6 day 7 day 8 day
250.31 ± 45.04 232.71 ± 33.82 256.07 ± 41.17 217.89 ± 34.26 248.76 ± 63.67 205.93 ± 47.17 160.53 ± 53.08 146.76 ± 56.45
0.54 ± 0.12 0.48 ± 0.07 0.54 ± 0.10 0.46 ± 0.08 0.51 ± 0.12 0.43 ± 0.10 0.33 ± 0.09 0.30 ± 0.09
15.45 ± 3.15 16.42 ± 3.19 13.40 ± 1.55 14.62 ± 3.76 13.47 ± 2.78 16.83 ± 2.22 11.99 ± 2.91 15.55 ± 4.25
0.0321 ± 0.0059 0.0342 ± 0.0075 0.0273 ± 0.0020 0.0321 ± 0.0097 0.0272 ± 0.0043 0.0352 ± 0.0047 0.0267 ± 0.0070 0.0304 ± 0.0115
234.87 ± 43.92 216.29 ± 33.12 242.67 ± 40.83 203.27 ± 35.31 235.29 ± 61.85 189.10 ± 45.41 148.54 ± 52.57 131.21 ± 54.91
0.51 ± 0.12 0.45 ± 0.07 0.52 ± 0.10 0.43 ± 0.08 0.48 ± 0.11 0.39 ± 0.09 0.30 ± 0.08 0.26 ± 0.09
EI: energy intake; BM: body mass; EI/BM: energy intake/body mass; FE: feces energy; FE/BM: feces energy/body mass; DEI: digestable energy intake; and DEI/BM: digestable energy intake/body mass.
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Fig. 2. The relationship between metabolic rates and ambient temperatures in pygmy loris.
role in their fitness, reproduction and evolution [8]. We can reckon their energy expenditure by means of energy balance [23]. This method has been widely applied in ecological risk assessment [24]. In this study, energy intake (EI) and digestable energy intake (DEI) of N. pygmaeus in Daweishan Nature Reserve are significantly higher than in Kunming Zoo reported by Xiao et al. [25]. But their energy intake per body mass (EI/BM) and digestable energy intake per body mass (DEI/BM) have no significant differences (P > 0.05). So their energy budgets are nonsignificantly, and both lower. It is confirmed that small nocturnal prosimians living in the torrid zone, have a adaptive lower energy expenditure [26,27]. Compared with Anthropoidea, a slow pace of life in Prosimii is characterized by low activity rates, low daily energy expenditure and low basal metabolic rates (BMRs) [28–30]. A slow lifestyle in Loridae has been interpreted as a mechanism for dealing with a diet that either is low in energy content, unpredictably periodically scarce, or contains high concentrations of toxic compounds or digestion inhibitors [31,32]. 4.2. BMR and adaptive significance The energy metabolic characters are the result of integrated function both the behavioral and physiological fitness, reflecting their adaptation mode and evolution [33,34]. BMR, as an important index of the level of energy metabolism, is related to their life history traits, their ecological and behavioral characteristics. Many factors influence the level of BMR in animals, including body mass, food habits, climate, habitat, a distribution restricted to islands or mountains, use of torpor, and the type of reproduction [14,35]. Since Kleiber had reported [36], the one factor that has the greatest impact on energy expenditure is body size [37], usually measured as body mass. Most (96.8%) of the variation in BMR is accounted for by body mass [14]. The result in the test showed that BMR of N. pygmaeus was 0.3844 ± 0.0162 mlO2/g/h, and Kleiber’s (BMR = 3.4W0.25) [21] body mass predicted value was 51.91% ± 1.90%, While Hayssen and Lacy’s (BMR = 4.325W0.307) [15] and McNab’s (BMR = 3.45W0.287) [16], respectively, were 57.78% ± 2.06% and 64.12% ± 2.31%. It is reported that all lorisines examined have BMRs lower than 60% of the predicted value [28–30,36,38]. A correlation of BMR in prosimian with body mass appears obvious: small species
should be expected to have higher basal metabolic rates than larger species. In terms of Nycticebus, BMR in N. pygmaeus is much higher than in N. coucang [38] (Table 3). McNab argued that food habits were an important factor being associated with the level of BMR in nearly all species [39]. Müller reported that Colobus guereza and Cercopithecus mitis living in the same habitat and having the same life history traits, but had different BMR because of their different food habits [40]. Pygmy lorises eat primarily fruit, and supplement their diet with invertebrates (including ants), vertebrates, leaf parts, and possibly plant gums, nectar, and bark [41,42]. By contrast with Kleiber’s body mass predicted value, it generally considered that the bigger phytophagous animals and predator in primate have higher metabolic rate than folivorous, insectivorous and frugivorous animals [39]. Veloso also conformed that individuals eating the food of high cellulose contained had much lower BMR than eating the food of low cellulose contained. It may be one aspect’s reason that the level of BMR in N. pygmaeus was much lower, and in Lemur fulvus (0.14 mlO2/h/ g) was far lower than other kind of Prosimii [43]. BMR of mammals is also associated with selective factors, such as climate and habitat. Generally speaking, BMR of mammals in the torrid zone is lower than that in the temperate zone, and BMR of mammals in the temperate zone is lower than that in the frigid zone. N. pygmaeus is a nocturnal and arboreal primate species. It typically lives in tropical semi-evergreen and secondary forests. Recently, an analysis of data from 639 species of mammals demonstrated the relationship of BMR with six kind of ecological factors [14]. This analysis gives rise to the equation: BMR (kJ/ d) = 0.064(M I S T C H E F)g0.694, where non-dimensional coefficients describe the response of BMR to various conditions, including M for mountains or lowlands; I for islands or continents; S for substrate; T for torpor; C for climate; H for habitat; E for infraclasses; and F for food habits. According to the equation, the mean ± SE measured BMR in N. pygmaeus is 67.77 ± 2.42% of the calculated BMR, i.e., far lower than expected. It is reported that small prosimians living in the torrid zone, have a adaptive relatively lower BMR [26,27,38]. Furthermore, the resting metabolic rate (RMR) of N. pygmaeus measured in this study (0.3844 ± 0.0162 mlO2/g/h) is much lower than reported in an earlier study reported by Wang et al. (0.498 ± 0.0396 mlO2/g/h) [7]. It may be because his study was conducted in the laboratory of Kunming, where the average room temperature (22.5 °C, 18.5–24.5 °C) was much lower than in Yunnan Daweishan Nature Reserve (25.97 °C, 23.4–28.7 °C), and the average relative humidity (72–93%) was also much lower than the Nature Reserve (105.3–162.6%). Therefore, the pygmy lorises seem like progressing a low cold acclimation, which is an energy strategy for them to cope with the environmental conditions in torrid zone. Individuals from a same species living in different environments often have different basal rates [44,45], which may have adaptive significance for them to survive in a particular environmental condition [46]. This situation was also seen in Tupaia belangeri [47,48]. 4.3. Thermal conductance and thermoregulation The body temperature of N. pygmaeus at room temperatures (23.4–28.7 °C) was a little low (35.23 ± 0.16 °C, n = 48) and changed from 32.3 °C to 36.9 °C. It was much higher than the value measured by Wang et al. [7] and Müller [38], while the variation range was identical with theirs. But the Tb of N. pygmaeus was a litter lower than N. coucang (35.3 °C) [30], similar to Hapalemur griseus (32–36 °C), and the variation range was much smaller than Microcebus murinus (21.7–38.2 °C) [28]. The lower body temperature in Prosimii is a typical characteristic of original homoiothermy [38]. Wang indicated that the thermoregulation index of
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C.H. Xiao et al. / Acta Ecologica Sinica 30 (2010) 129–134 Table 3 Basal rate of metabolism and ecological characteristics of mammals.
a b c
Species
Body weight (g)
Body temperature (°C)
Experimental temperature (°C)
TNZ (°C)
BMR (mlO2/h/g)
C (mlO2/h/g/°C)
Climatea
Habitatb
Foodc
Reference
Tupaia belangeri Tupaia belangeri Lemur fulvus Nycticebus coucang Perodicticus potto Aotus trivirgatus Cebuella pygmaea Nycticebus pygmaeus Nycticebus pygmaeus
108–131 123 2330 1300 1090 1020 153 310 466
37.6–38.7 – 38.2 ± 0.07 – – 38 ± 0.5 34.9–35.5 33.8 ± 0.18 35.2 ± 0.16
5–37.5 – 2 to 40 5–37 – 1–39 20–35 10–37.5 25–35
27.5–35 30–37 30–40 25–33 25–29 28–30 27–34 30 27.5–35
1.56–1.94 0.76 0.14 0.25 0.37 0.45 0.64 0.50 0.38
0.1449–0.1860 – 0.00370 – 0.0288 – 0.0846 0.0804 0.0449
TR TR TR TR TR TR TR TR TR
D, D, D, N, N, N, N, N, N,
IN, FR IN, FR FO IN FR O O – –
[47] [48] [43] [38] [49] [50] [51] [7] This study
B B A A A A A A A
Climate: TR, tropical. Habitat: D, diurnal; N, nocturnal; B, burrow; and A, arboreal. Food: IN, insectivorous; FO, folivorous; FR, frugivorous; and O, omnivorous.
N. pygmaeus was 0.535 (Ta, 10–30 °C) or 0.5997 (Ta, 15–30 °C), and suggested that the ability of thermoregulation in N. pygmaeus is a little lower [7]. In addition, the relatively low body temperature of N. pygmaeus may be an adaptation characteristic for a paticular environment. N. pygmaeus is a nocturnal and arboreal primate species. It typically lives in tropical semi-evergreen and secondary forests. Lowing body temperature can reduce the difference in temperature in tropical region, save energy consumption, and avoid the force from the high temperature during the day. When the ambient temperature (Ta) reached up to 27.5 °C, the body temperature (Tb) of N. pygmaeus rised rapidly. The Tb was 38.87 °C at the time of Ta arriving at 35 °C. Because of the small body mass and the big body surface area in N. pygmaeus, their lower body temperature can effectively avoid the force from the high temperature. Thermal conductance of N. pygmaeus was 0.0449 ± 0.0031 mlO2/ g/h/°C, lower than Wang’s measured (0.0804 mlO2/g/h/°C) [7], but higher than L. fulvus (0.037 mlO2/g/h/°C) [43]. McNab’s predicted value (C = 1.02W0.51) was 99.12 ± 6.33% [22]. Low metabolic rates and high thermal insulation are characteristics of mammals living in the torrid zone [22]. In the experiment, we found that the pygmy lorises smeared themselves saliva. The higher ambient temperature, the bigger area they smeared, which was reported by Wang et al. [7]. The response pattern was also found in many other mammals, such as N. coucang [38] and Perodicticus potto [29]. This shows that high thermal conductance and salivation may be considered as alternative adaptation to the tropical environment. In conclusion, the results may reflect features of energy metabolism in small tropical prosimians: the pygmy lorises in the Yunnan Daweishan Nature Reserve had low levels of energy intake and body temperature and BMR, as well as high levels of thermal conductance. Compared with the values measured in the laboratory of Kunming, they are characterized by a lower BMR, while their body temperatures are relatively higher. All these characteristics have important adaptive significance for them to cope with the environmental conditions in tropical semi-evergreen forests and secondary forests. Acknowledgement The project was financially supported by Basic Project in Application of Yunnan Province (No. 2007C043M) and Basilic Project of Yunnan Province (No. 2007C000Z1). References [1] J.H. Wolfhein, Primates of the World: Distribution, Abundance and Conservation, University of Washington Press, Seattle and London, 1983. pp. 37–57.
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Energy metabolism and thermoregulation in pygmy lorises (Nycticebus pygmaeus) from Yunnan Daweishan Nature Reserve Xiao CaiHong a,b,c, Wang ZhengKun a,b,c,*, Zhu WanLong a,b,c, Chu YongXing d, Liu ChunYan a,b,c, Jia Ting a,b,c, Meng LiHua a,b,c, Cai JinHong a,b,c a
School of Life Sciences, Yunnan Normal University, Kunming 650092, China Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming 650092, China The Key Laboratory of Biomass Energy and Environmental Biotechnology in Yunnan Province, Kunming 650092, China d Yunnan Daweishan National Nature Reserve, Yunnan Pingbian County 661200, China b c
a r t i c l e
i n f o
Keywords: Pygmy loris (Nycticebus pygmaeus) Energy budget RMR Body temperature Thermal conductance
a b s t r a c t The pygmy loris (Nycticebus pygmaeus) is a small prosimian living in Vietnam, Laos, eastern Cambodia and the south part of China. In China it is only found in Pingbian, Hekou, Jinping, Luchun of Yunnan. As N. pygmaeus is seriously threatened by hunting, trade and habitat destruction, it is listed in Appendix II of CITES, and in 2006 the IUCN classified it as ‘‘vulnerable”. In order to understand the characteristics of energy metabolism and thermoregulation of N. pygmaeus, the resting metabolic rate (RMR) and body temperature (Tb) at different ambient temperature (Ta) of pygmy lorises, as well as body mass, energy intake, digestable energy intake, digestability and the thermal conductance were measured in captivity. The results obtained mainly are as follows: (1) Pygmy loris feed dry food averaged 12.90 ± 1.02 g/d. They could gain 214.87 ± 16.65 kJ/d from food intake, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability. (2) The Tb at room temperatures was a little low (35.23 ± 0.16 °C) and varied with Ta from 25 °C to 35 °C. There was a positive relationship between Tb and Ta, which was described as: Tb = 27.22 + 0.34Ta (r = 0.880). (3) The resting metabolic rate (RMR) of the pygmy loris was 0.3844 ± 0.0162 mlO2/g/h, which was 51.91 ± 1.90% of the previous predicted rate by Kleiber (1961) [21]. (4) The average thermal conductance of the pygmy loris (N. pygmaeus) was 0.0449 ± 0.0031 mlO2/g/h/°C. These characteristics of energy metabolism and thermoregulation of N. pygmaeus in Yunnan Daweishan Nature Reserve might be considered as the adaptive characteristics to their environment in tropical semi-evergreen forests and secondary forests. Ó 2010 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction Genus Nycticebus belongs to Mammalia; Eutheria; Primates; Suborder Prosimii; and Family Loridae. It is generally believed that the slow lorises (Nycticebus coucang and Nycticebus bengalensis) and pygmy lorises (Nycticebus pygmaeus) are two species that belong to Nycticebus. But N. pygmaeus has a much more limited distribution range than the slow lorises [1], scantly covering Vietnam, eastern Cambodia, Lao PDR and Yunnan Province in Southern China. In China it is only found in Pingbian, Hekou, Jinping and Luchun of Yunnan from the year of 1986 [2–4]. N. pygmaeus is a nocturnal and almost entirely arboreal primate species. It typically lives in semi-evergreen and secondary forests [1,5,6]. Due to their nocturnal, arboreal lifestyle and their latent habit, pygmy lorises have been widely ignored in by field studies and * Corresponding author at: School of Life Sciences, Yunnan Normal University, Kunming 650092, China. E-mail address: [email protected] (Z.K. Wang).
well-based data are lacking. In physiological ecology field, only temperature regulation and cellular respiration of the pygmy lorises were reported as yet [7,8]. N. pygmaeus is one of the least studied species of all prosimians [9]. It is listed in Appendix II of CITES. In its latest assessment in 2006 the IUCN (The World Conservation Union) classified the pygmy lorises as ‘‘vulnerable” [10]. It is also listed as one of the first protected animals in China. The energy metabolic level always decided species’ distribution, diversity, breed and fitness. Thermal features and temperature regulation of the animals are usually related to their energy use, distribution, life histories and evolution, reflecting their adaptation mode and physiological capability [11–13]. The use of BMR as an important index of energy expenditure from intraspecies to interspecies has received a great deal of attention from ecophysiologists and comparative physiologists for several decade years [14]. The factors influencing the level of BMR in mammals have been examined several times so far. One of the first was by Hayssen and Lacy, who argued that body mass was the single most important factor influencing the BMR of 248 species [15]. Soon thereafter an analysis
1872-2032/$ - see front matter Ó 2010 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2010.04.002
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of data from 321 species of mammals demonstrated that BMR correlated with body mass, food habits, and taxonomy [16]. Recently, the factors that influence the level and scaling of BMR in mammals are justified because almost twice as many species have had adequate estimates of their basal rates of metabolism reported. Data on body mass and BMR were presented on 639 species of mammals along with information on the ecological and behavioral characteristics of these species, including food habits, climate, habitat, substrate used, their exclusive occurrence on mountains or islands, and their use of torpor. It is suggested that individuals from only one population can properly represent a species because individuals living in different environments often have different basal rates [14]. Presumably, the level of energy metabolism in mammals that live in the areas of origin may also be different from living in the laboratory. But most studies of animal’s energy metabolism were conducted in laboratory on captive animal before, while scarcely in their country of origin. In this study we measured the digestible energy of N. pygmaeus in Yunnan Daweishan Nature Reserve, as well as the resting metabolic rate (RMR) and the body temperature (Tb) at different ambient temperature (Ta), and hoped to offer some basic materials to the conservation of N. pygmaeus in situ. 2. Materials and methods 2.1. Samples National Nature Reserve of Dawei Mountain lies to the south of the North-Tropic of Cancer, east longitudes 103°200 –104°030 , north latitudes 22°350 –23°070 , with a total territory of 153.7 km2. The Dawei Mountain where the reserve is located, is situated to the southeast part of China, Red River state, including the county of Pingbian, Hekou, Gejiu and Mengzi. The highest peak, Dajian Peak has an elevation of 2365 m, the second highest mountain, Dawei Mountain, 2345 m, and the lowest, 225 m in the area. Because of the barrier of the surrounding high mountains with only the narrow Red River valley mouth (76.4 m elevation) in its southeast leading to the north bay of Vietnam, this area becomes the only place that is affected most profoundly by the southeast tropical monsoon with warm and humid currents in the whole Yunnan Province. It has ample rainfall and heat, hot and rainy in summer, warm, humid, and foggy in winter with an average annual temperature of 22.6 °C. N. pygmaeus generally lives in the semi-evergreen and secondary forests of Daweishan Nature Reserve. A total of 6 N. pygmaeus (male 4, average body mass is 429.56 ± 14.01 g, n = 60 and female 2, average body mass is 538.81 ± 6.17 g, n = 30), all healthy adults, were bred in Yunnan Daweishan Nature Reserve. They were placed in cage (400 mm 200 mm 200 mm), one in a cage, and were provided with natural illumination. Average room temperature was 25.97 °C (23.4– 28.7 °C), and average relative humidity was 140.22% (105.3– 162.6%). Their average body temperature is 35.23 °C, varying from 32.3 °C to 36.9 °C. They were feeding honey, apple, banana, ripe egg white and vitelline in fix quantity and timing everyday, in addition to 50 ml water. In experimental period, they lived healthily. 2.2. Measurement of energy budget Energy expenditure was measured in the pygmy loris according to energy balance [17]. Before the test, animals were breeding in cage a week. We measured animal’s body mass, feed them in a certain ration, and sampled food to dry for finding their water content between 14:30 and 15:00 one day before. At the time of test, we diurnally repeated to measure animal’s body mass, gather food residue and feces, then feed them in the same proportion, and sampled food to dry for finding their water content between 14:30 and 15:00 from
the first day to the eight day. Food and feces was dried using vacuum drying chamber, and measured energy contained by use of fullautomatic calorimeter (YX-ZR/Q, U-THERM, Changsha China). We calculated energy intake, feces energy, digestable energy intake and digestability according to the following equations [17,18]: Energy intake ðkJ=dÞ ¼ Dry mass of food intake ðg=dÞFood caloric ðkJ=gÞ Feces energy ðkJ=dÞ ¼ Dry mass of feces ðg=dÞFeces caloric ðkJ=gÞ Digestable energy intake ðkJ=dÞ ¼ Energy intake ðkJ=dÞFeces energy ðkJ=dÞ Digestability ð%Þ ¼ Digestable energy intake ðkJ=dÞ=Energy intake ðkJ=dÞ100%
2.3. Measurement of metabolic rates Metabolic rates of N. pygmaeus were measured using the closed-circuit respirometer at 25 °C, 27.5 °C, 30 °C, 32.5 °C and 35 °C according to Gorecki [19]. Briefly, the temperature of metabolic chamber was controlled within ±0.5 °C by water bath. Carbon dioxide and water in the metabolic chamber were absorbed with KOH and silica gel. At the time of measurement, animals were fasted 5 h prior to being put into the metabolic chamber. After 60 min stabilization in the chamber, metabolic measurement was conducted for 60 min. Oxygen consumption was recorded at 5-min intervals. Three continuous stable minimum recordings were taken to calculate RMR. Before and after each test, the animal’s body mass was measured. Metabolic rates were expressed as mlO2/g/h and corrected to standard temperature and air pressure (STP) conditions. Body temperature was measured by a digital thermometer after each experiment. Considering the influence of the day and night rhythm, all measurement was made between 18:00 and 24:00. 2.4. Thermal conductance (C) If corresponded with Newton’s law of cooling, thermal conductance was evaluated as C = RMR/(Tb Ta), where RMR is the basal metabolic rate (BMR) (mlO2/g/h), Tb is the body temperature (°C), and Ta is the ambient temperature (°C) [20]. But if not, we must correct it according to the equation: Cm = Cf(1 + 0.06DTb), where Cm is the minimum thermal conductance, Cf is the gradient of the regression both RMR and Ta, and the DTb is the balance between actual body temperature and theoretic body temperature. 2.5. Statistical analyses Statistical analyses were performed using SPSS for Windows 16.0 software package. Food intake, feces discharged, energy intake, digestable energy intake and digestability of the pygmy lorises were analysed using independence sample T-test and repeat metrical regression. In order to remove the effect of body mass, analysis of covariance (ANCOVA) was used to analyse the data, using body mass as the covariate. Differences among groups were determined by one-way ANOVA, and linear regression analysis was used to analyse the relationship between body temperature (Tb), metabolic rates, thermal conductance (C) and ambient temperature (Ta). Least significant difference (LSD) was used for statistical analysis of different groups. All data in this paper were reported as mean ± standard deviation and P < 0.05 was taken to be statistically significant. 3. Results 3.1. Energy budget There are five kind of food, including honey, apple, banana, egg white and vitelline. Their water content and energy contained are shown in Table 1.
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C.H. Xiao et al. / Acta Ecologica Sinica 30 (2010) 129–134 Table 1 The water content and energy contained per gram of food. Food
Water content (%)
Energy contained per gram (kJ/g)
Honey Apple Banana Egg White Vitelline
20.39 ± 0.07 83.64 ± 0.05 78.65 ± 0.46 85.45 ± 0.19 49.59 ± 0.03
14.79 ± 0.21 16.11 ± 0.16 15.38 ± 0.15 20.64 ± 0.76 31.47 ± 0.18
(7) (7) (7) (7) (7)
(7) (7) (7) (7) (7)
Note: The number of the bracket denotes the times of testing in each food.
The average body mass of N. pygmaeus was 465.98 ± 12.12 g (n = 48), and changed indistinctively in experimental period (F(1,8) = 0.026, P > 0.05). The pygmy loris feed dry food averaged 12.90 ± 1.02 g/d which was about 2.67% ± 0.20% of body weight. They could gain 214.87 ± 16.65 kJ/d from food intake, while lost 14.72 ± 1.04 kJ/d through feces, and earned 200.15 ± 16.36 kJ digestable energy intake per day with 90.13 ± 1.34% of the digestability (Table 2). The result showed that the effect of body mass was not statistically significant to the food intake (F = 1.097, P > 0.05), energy intake (F = 1.128, P > 0.05), digestable energy intake (F = 1.042, P > 0.05) and digestability (F = 3.717, P > 0.05) through the analysis of covariance. By using analysis of repeat metrical regression, Food intake (F(1,6) = 1.765, P > 0.05), feces discharged (F(1,6) = 0.192, P > 0.05), energy intake (F(1,6) = 1.422, P > 0.05), feces energy (F(1,6) = 0.324, P > 0.05), digestable energy intake (F(1,6) = 1.496, P > 0.05) and digestability (F(1,6) = 1.257, P > 0.05) of the pygmy lorises were taken to be statistically insignificant in the eight continuously experimental days. 3.2. Body temperature (Tb) The Tb of N. pygmaeus at room temperatures was a little low (35.23 ± 0.16 °C, n = 48) and varied with Ta from 25 °C to 35 °C. There was a positive relationship between Tb and Ta, which was represented by the following equation: Tb = 27.22 + 0.34Ta (r = 0.880) (Fig. 1, **P < 0.01). 3.3. Metabolic rates Using analysis of repeat metrical regression, when Ta is between 27.5 and 35 °C, oxygen consumption in pygmy loris did not show significant correlation (P > 0.05) (Fig. 2). Hence the thermal neutral zone (TNZ) of N. pygmaeus was 27.5–35 °C. In the TNZ, BMR of N. pygmaeus was 0.3844 ± 0.0162 mlO2/g/h, and Kleiber’s [21] body mass predicted value was 51.91% ± 1.90%, While Haysseen and Lacy’s [15], McNab’s [16] and McNab’s [14], respectively, were 57.78% ± 2.06%, 64.12% ± 2.31% and 67.77% ± 2.42%.
Fig. 1. The relationship between body temperatures and ambient temperatures in pygmy loris.
3.4. Thermal conductance There are two conditions in calculating thermal conductance using Newton’s law of cooling. On the one hand, there is a linear correlation between oxygen consumption and ambient temperature. On the other hand, the intersection of regression line between RMR and Ta in X axis equal to the body temperature, when RMR is zero. From the result of this study, there was a relation of correlation and regression between RMR and Ta, which was represented by the following equation: RMR(mlO2/g/h) = 1.041 0.02Ta (N = 30, P < 0.001). But when RMR reached up to zero, the point of the regression line in X axis (52.0 °C) was bigger than actual body temperature (31.25 °C). For this reason, we corrected it according to the equation: Cm = Cf(1 + 0.06DTb) [20], calculated that the thermal conductance (Cm) of N. pygmaeus was 0.0449 ± 0.0031 mlO2/g/h/°C, and McNab’s predicted value (C = 1.02W0.51) was 99.12 ± 6.33% [22].
4. Discussions 4.1. Energy budget All energy required in animals comes from food. The abundance, quality, and the assimilation of food have an important effect on the level of energy metabolism, which plays an important
Table 2 The energy budget of Nycticebus pygmaeus in Yunnan Daweishan Nature Reserve (n = 6). Energy budget
EI (kJ/d)
EI/BW (kJ/d/g)
FE (kJ/d)
FE/BW (kJ/d/g)
DEI (kJ/d)
DEI/BW (kJ/d/g)
1 day 2 day 3 day 4 day 5 day 6 day 7 day 8 day
250.31 ± 45.04 232.71 ± 33.82 256.07 ± 41.17 217.89 ± 34.26 248.76 ± 63.67 205.93 ± 47.17 160.53 ± 53.08 146.76 ± 56.45
0.54 ± 0.12 0.48 ± 0.07 0.54 ± 0.10 0.46 ± 0.08 0.51 ± 0.12 0.43 ± 0.10 0.33 ± 0.09 0.30 ± 0.09
15.45 ± 3.15 16.42 ± 3.19 13.40 ± 1.55 14.62 ± 3.76 13.47 ± 2.78 16.83 ± 2.22 11.99 ± 2.91 15.55 ± 4.25
0.0321 ± 0.0059 0.0342 ± 0.0075 0.0273 ± 0.0020 0.0321 ± 0.0097 0.0272 ± 0.0043 0.0352 ± 0.0047 0.0267 ± 0.0070 0.0304 ± 0.0115
234.87 ± 43.92 216.29 ± 33.12 242.67 ± 40.83 203.27 ± 35.31 235.29 ± 61.85 189.10 ± 45.41 148.54 ± 52.57 131.21 ± 54.91
0.51 ± 0.12 0.45 ± 0.07 0.52 ± 0.10 0.43 ± 0.08 0.48 ± 0.11 0.39 ± 0.09 0.30 ± 0.08 0.26 ± 0.09
EI: energy intake; BM: body mass; EI/BM: energy intake/body mass; FE: feces energy; FE/BM: feces energy/body mass; DEI: digestable energy intake; and DEI/BM: digestable energy intake/body mass.
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C.H. Xiao et al. / Acta Ecologica Sinica 30 (2010) 129–134
Fig. 2. The relationship between metabolic rates and ambient temperatures in pygmy loris.
role in their fitness, reproduction and evolution [8]. We can reckon their energy expenditure by means of energy balance [23]. This method has been widely applied in ecological risk assessment [24]. In this study, energy intake (EI) and digestable energy intake (DEI) of N. pygmaeus in Daweishan Nature Reserve are significantly higher than in Kunming Zoo reported by Xiao et al. [25]. But their energy intake per body mass (EI/BM) and digestable energy intake per body mass (DEI/BM) have no significant differences (P > 0.05). So their energy budgets are nonsignificantly, and both lower. It is confirmed that small nocturnal prosimians living in the torrid zone, have a adaptive lower energy expenditure [26,27]. Compared with Anthropoidea, a slow pace of life in Prosimii is characterized by low activity rates, low daily energy expenditure and low basal metabolic rates (BMRs) [28–30]. A slow lifestyle in Loridae has been interpreted as a mechanism for dealing with a diet that either is low in energy content, unpredictably periodically scarce, or contains high concentrations of toxic compounds or digestion inhibitors [31,32]. 4.2. BMR and adaptive significance The energy metabolic characters are the result of integrated function both the behavioral and physiological fitness, reflecting their adaptation mode and evolution [33,34]. BMR, as an important index of the level of energy metabolism, is related to their life history traits, their ecological and behavioral characteristics. Many factors influence the level of BMR in animals, including body mass, food habits, climate, habitat, a distribution restricted to islands or mountains, use of torpor, and the type of reproduction [14,35]. Since Kleiber had reported [36], the one factor that has the greatest impact on energy expenditure is body size [37], usually measured as body mass. Most (96.8%) of the variation in BMR is accounted for by body mass [14]. The result in the test showed that BMR of N. pygmaeus was 0.3844 ± 0.0162 mlO2/g/h, and Kleiber’s (BMR = 3.4W0.25) [21] body mass predicted value was 51.91% ± 1.90%, While Hayssen and Lacy’s (BMR = 4.325W0.307) [15] and McNab’s (BMR = 3.45W0.287) [16], respectively, were 57.78% ± 2.06% and 64.12% ± 2.31%. It is reported that all lorisines examined have BMRs lower than 60% of the predicted value [28–30,36,38]. A correlation of BMR in prosimian with body mass appears obvious: small species
should be expected to have higher basal metabolic rates than larger species. In terms of Nycticebus, BMR in N. pygmaeus is much higher than in N. coucang [38] (Table 3). McNab argued that food habits were an important factor being associated with the level of BMR in nearly all species [39]. Müller reported that Colobus guereza and Cercopithecus mitis living in the same habitat and having the same life history traits, but had different BMR because of their different food habits [40]. Pygmy lorises eat primarily fruit, and supplement their diet with invertebrates (including ants), vertebrates, leaf parts, and possibly plant gums, nectar, and bark [41,42]. By contrast with Kleiber’s body mass predicted value, it generally considered that the bigger phytophagous animals and predator in primate have higher metabolic rate than folivorous, insectivorous and frugivorous animals [39]. Veloso also conformed that individuals eating the food of high cellulose contained had much lower BMR than eating the food of low cellulose contained. It may be one aspect’s reason that the level of BMR in N. pygmaeus was much lower, and in Lemur fulvus (0.14 mlO2/h/ g) was far lower than other kind of Prosimii [43]. BMR of mammals is also associated with selective factors, such as climate and habitat. Generally speaking, BMR of mammals in the torrid zone is lower than that in the temperate zone, and BMR of mammals in the temperate zone is lower than that in the frigid zone. N. pygmaeus is a nocturnal and arboreal primate species. It typically lives in tropical semi-evergreen and secondary forests. Recently, an analysis of data from 639 species of mammals demonstrated the relationship of BMR with six kind of ecological factors [14]. This analysis gives rise to the equation: BMR (kJ/ d) = 0.064(M I S T C H E F)g0.694, where non-dimensional coefficients describe the response of BMR to various conditions, including M for mountains or lowlands; I for islands or continents; S for substrate; T for torpor; C for climate; H for habitat; E for infraclasses; and F for food habits. According to the equation, the mean ± SE measured BMR in N. pygmaeus is 67.77 ± 2.42% of the calculated BMR, i.e., far lower than expected. It is reported that small prosimians living in the torrid zone, have a adaptive relatively lower BMR [26,27,38]. Furthermore, the resting metabolic rate (RMR) of N. pygmaeus measured in this study (0.3844 ± 0.0162 mlO2/g/h) is much lower than reported in an earlier study reported by Wang et al. (0.498 ± 0.0396 mlO2/g/h) [7]. It may be because his study was conducted in the laboratory of Kunming, where the average room temperature (22.5 °C, 18.5–24.5 °C) was much lower than in Yunnan Daweishan Nature Reserve (25.97 °C, 23.4–28.7 °C), and the average relative humidity (72–93%) was also much lower than the Nature Reserve (105.3–162.6%). Therefore, the pygmy lorises seem like progressing a low cold acclimation, which is an energy strategy for them to cope with the environmental conditions in torrid zone. Individuals from a same species living in different environments often have different basal rates [44,45], which may have adaptive significance for them to survive in a particular environmental condition [46]. This situation was also seen in Tupaia belangeri [47,48]. 4.3. Thermal conductance and thermoregulation The body temperature of N. pygmaeus at room temperatures (23.4–28.7 °C) was a little low (35.23 ± 0.16 °C, n = 48) and changed from 32.3 °C to 36.9 °C. It was much higher than the value measured by Wang et al. [7] and Müller [38], while the variation range was identical with theirs. But the Tb of N. pygmaeus was a litter lower than N. coucang (35.3 °C) [30], similar to Hapalemur griseus (32–36 °C), and the variation range was much smaller than Microcebus murinus (21.7–38.2 °C) [28]. The lower body temperature in Prosimii is a typical characteristic of original homoiothermy [38]. Wang indicated that the thermoregulation index of
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C.H. Xiao et al. / Acta Ecologica Sinica 30 (2010) 129–134 Table 3 Basal rate of metabolism and ecological characteristics of mammals.
a b c
Species
Body weight (g)
Body temperature (°C)
Experimental temperature (°C)
TNZ (°C)
BMR (mlO2/h/g)
C (mlO2/h/g/°C)
Climatea
Habitatb
Foodc
Reference
Tupaia belangeri Tupaia belangeri Lemur fulvus Nycticebus coucang Perodicticus potto Aotus trivirgatus Cebuella pygmaea Nycticebus pygmaeus Nycticebus pygmaeus
108–131 123 2330 1300 1090 1020 153 310 466
37.6–38.7 – 38.2 ± 0.07 – – 38 ± 0.5 34.9–35.5 33.8 ± 0.18 35.2 ± 0.16
5–37.5 – 2 to 40 5–37 – 1–39 20–35 10–37.5 25–35
27.5–35 30–37 30–40 25–33 25–29 28–30 27–34 30 27.5–35
1.56–1.94 0.76 0.14 0.25 0.37 0.45 0.64 0.50 0.38
0.1449–0.1860 – 0.00370 – 0.0288 – 0.0846 0.0804 0.0449
TR TR TR TR TR TR TR TR TR
D, D, D, N, N, N, N, N, N,
IN, FR IN, FR FO IN FR O O – –
[47] [48] [43] [38] [49] [50] [51] [7] This study
B B A A A A A A A
Climate: TR, tropical. Habitat: D, diurnal; N, nocturnal; B, burrow; and A, arboreal. Food: IN, insectivorous; FO, folivorous; FR, frugivorous; and O, omnivorous.
N. pygmaeus was 0.535 (Ta, 10–30 °C) or 0.5997 (Ta, 15–30 °C), and suggested that the ability of thermoregulation in N. pygmaeus is a little lower [7]. In addition, the relatively low body temperature of N. pygmaeus may be an adaptation characteristic for a paticular environment. N. pygmaeus is a nocturnal and arboreal primate species. It typically lives in tropical semi-evergreen and secondary forests. Lowing body temperature can reduce the difference in temperature in tropical region, save energy consumption, and avoid the force from the high temperature during the day. When the ambient temperature (Ta) reached up to 27.5 °C, the body temperature (Tb) of N. pygmaeus rised rapidly. The Tb was 38.87 °C at the time of Ta arriving at 35 °C. Because of the small body mass and the big body surface area in N. pygmaeus, their lower body temperature can effectively avoid the force from the high temperature. Thermal conductance of N. pygmaeus was 0.0449 ± 0.0031 mlO2/ g/h/°C, lower than Wang’s measured (0.0804 mlO2/g/h/°C) [7], but higher than L. fulvus (0.037 mlO2/g/h/°C) [43]. McNab’s predicted value (C = 1.02W0.51) was 99.12 ± 6.33% [22]. Low metabolic rates and high thermal insulation are characteristics of mammals living in the torrid zone [22]. In the experiment, we found that the pygmy lorises smeared themselves saliva. The higher ambient temperature, the bigger area they smeared, which was reported by Wang et al. [7]. The response pattern was also found in many other mammals, such as N. coucang [38] and Perodicticus potto [29]. This shows that high thermal conductance and salivation may be considered as alternative adaptation to the tropical environment. In conclusion, the results may reflect features of energy metabolism in small tropical prosimians: the pygmy lorises in the Yunnan Daweishan Nature Reserve had low levels of energy intake and body temperature and BMR, as well as high levels of thermal conductance. Compared with the values measured in the laboratory of Kunming, they are characterized by a lower BMR, while their body temperatures are relatively higher. All these characteristics have important adaptive significance for them to cope with the environmental conditions in tropical semi-evergreen forests and secondary forests. Acknowledgement The project was financially supported by Basic Project in Application of Yunnan Province (No. 2007C043M) and Basilic Project of Yunnan Province (No. 2007C000Z1). References [1] J.H. Wolfhein, Primates of the World: Distribution, Abundance and Conservation, University of Washington Press, Seattle and London, 1983. pp. 37–57.
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