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Diurnal Time Budgets and Behavioral Rhythms of White-Lipped Deer Cervus albirostris in the Qilian Mountains of Qinghai China.

Byline: Bang Li Gonghua Lin Xianxian Zhao Jianping Su and Tongzuo Zhang

Abstract White-lipped deer (Cervus albirostris) is very important in the natural ecosystem of the Qinghai- Tibet Plateau China. However data on the diurnal time budgets of these Vulnerable" animals' in the wild are still limited. Here we used a focal sampling method to investigate the diurnal time budgets of the white-lipped deer in Qinghai China during a one year period from June 2012 to April 2013. Results revealed that both males and females spend the majority of their time either feeding or resting throughout the year. The duration of both feeding (Z= 3.128 p= 0.002) and resting (Z= -2.426 p= 0.015) over the seasons were significantly different for females while the duration of resting (Z= -2.062 p= 0.039) and vigilance (Z= 2.897 p= 0.002) were significant for males. Moreover white-lipped deer showed a trimodal distribution of feeding activity during the warm season and a bimodal distribution in the cold season.

Moreover during the cold season gestating females devoted much more time to feeding likely due to the increased energy demands of pregnancy and the reduced nutritional value of their forage. This data will help with future range-management of white-lipped deer on the Qinghai-Tibet Plateau and its seasonal- dependent cohabitation with local livestock.

Key words: Diurnal time budgets; white-lipped deer; Cervus albirostris; behavior rhythm.

INTRODUCTION

White-lipped deer (Cervus albirostris Przewalski 1883) is endemic to China and is a critical ungulate in the ecosystem of the Qinghai Tibet Plateau. It previously ranged across much of the plateau (Ohtaishi and Gao 1990; Cai 1988) but presently only occurs in small fragmented populations in northwestern and southwestern Gansu eastern central and southern Qinghai eastern Tibet western Sichuan and northwestern Yunnan (Ohtaishi and Gao 1990; Yu et al. 1990; Kaji et al. 1989 1993; Schaller 1998; Wu and Wang 1999). The white-lipped deer is classified as " Vulnerable " (IUCN) and is currently listed as a Class I protected species under Chinese law. In the past this species was extensively hunted for its meat antlers and other organs which were used in traditional Chinese medicine (Koizumi et al. 1993). Currently competition with livestock is the white- lipped deer's largest threat due to the destruction of a large part of its natural habitat

which in turn has caused both decreased and fragmented populations of the wild ungulate throughout the plateau (Koizumi et al. 1993; Ohtaishi and Gao 1990; Harris 2007).

Diurnal time budgets are specific to each species and are uniquely modulated by both external and internal factors (Moncorps et al. 1997). The effects of internal (physiological state behavioral ontogeny and body mass) and external (group size natural cycle of day and night and environmental conditions) factors have been described in detail for many ungulate species (Duncan 1980; Maher 1991; Owen-Smith 1998; Schaller 1998; Xia et al. 2011). Diurnal behavioral time budgets play a major role in determining an animal's ability to adapt to seasonal and diurnal variations in environmental factors and have been instrumental in our understanding of the social organization foraging ecology and evolutionary relationships of many species of animals (Geist 1974; Jarman 1974; Schaller 1977; Fox 1992).

Data on white-lipped deer activity is limited but includes studies on social organization and mating behaviour parturition and neonatal care (Yu et al. 1993) and behavior patterns (He et al. 2001). However these reports do not reflect the time budgets of the white-lipped deer living on the Qinghai-Tibet Plateau. In this paper we attempt to describe the diurnal time budgets of the white- lipped deer living on the Qinghai-Tibet Plateau and the influence of sex season and the time of day on their activities.

MATERIALS AND METHODS

Study area

We conducted our study in Yanglong Village Qilian County Qinghai Province China (3839.034' to ~3840.338'N; 9832.506' to ~9833.586'E) located in the west of Qilian Mountains (Fig. 1) anywhere between 3821 to 5287 meters above sea level with an average elevation of 4000 meters. Four seasons are not distinct in the study area and the local climate can be divided into two seasons: a long winter and a short summer. The mean annual temperature is -3.08C and the extreme recorded low temperature is -36.3C. Annual precipitation varied from 218.9 to 359.1 mm where the majority of rain occurs from June through September. Alpine meadows were the primary feeding area for the white-lipped deer. of June 2012 through May 2013 from 07:00-18:00 in December January March and April (cold season) and 06:00-20:00 in June July and August (warm season). Observations were made via the focal-animal sampling method as described by Altmann (1974).

The total number of deer observed was 52 29 males (6 deer: 11 to 4 years old; 18 deer 4 to 10 years old; 5 deer: 1 to 3 years old) and 23 females (19 deer: 4 to 10 years old; 4 deer: 1 to 3 years old). Infant deer (1 to 3 years old) were excluded from the adult animal groupings. For each survey we randomly selected an individual (focal) animal with binoculars and then used a telescope to observe its behavior. We noted the following parameters: date time weather. The behaviors of the focal animals were also recorded by Samsung voice recorders. We defined five behavioral categories: foraging vigilance resting moving and other activities (e.g. drinking excreting jumping grooming and playing). White-lipped deer were categorized as foraging when standing with their head below shoulder level biting or chewing vegetation or when they were walking with their muzzles close to the ground. Vigilant was defined as watching with the head at or above the shoulder level while standing.

Moving was defined as walking or running with their head at or above the shoulder level. Resting was recorded if the animal was lying down. Each observation bout lasted 10 minutes.

Statistical analyses

Behavioral data were not normally distributed (KolmogorovSmirnov tests for normality Pless than 0.001 and Bartlett-Box F tests for homoscedasticity Pless than 0.05). We therefore used the mean and Bootstrap Confidence Interval throughout the paper; bootstrap sample size was 10000 and the confidence interval was set as 95%. Kruskal-Wallis tests were used to test for the differences of time budgets between the seasons for each activity and daytime period. The Mann-Whitney U-test was used to compare the different behavior categories during each season and for daytime budgets of both females and males. The level of significance was set at Pless than 0.05. All statistical analyses were performed using the SPSS21.0 statistical package.

RESULTS

Diurnal time budgets

The five behavioral categories were significantly different from each other during each season for both females and males (Kruskal-Wallis test warm-season females: 2= 145.51 df= 4 Pless than 0.001; males: 2= 136.12 df= 4 Pless than 0.001; cold- season females: 2=129.72 df= 4 Pless than 0.001; males: 2= 104.05 df= 4 Pless than 0.001).

There were no significant differences in feeding moving resting and other" activities between males and females during each of the seasons except that males were significantly more vigilant than females (Mann-Whitney U-test: Z= - 2.210 P=0.027) (Table I).

Table I.- Diurnal activity budgets of female and male white-lipped deer.

Behavioral###Warm seasons###Cold seasons

categories###Male###Female###Male###Female

Feeding###43.45%###40.97%###53.54%###55.14%

###(35.70-###(34.25-###(47.29-###(48.62-

###51.33)a###47.63)a###59.94)a###61.43)a

Moving###2.84%###1.86%###2.37%###1.64%

###(1.37-###(1.26-###(1.50-###(1.04

###4.72)a###2.57)a###3.46)a###2.36)a

Resting###51.09%###53.27%###39.07%###40.29%

###(42.57-###(45.91-###(32.20-###(33.46

###59.55)a###60.62)a###45.81)a###46.98)a

Vigilance###2.01%###3.22%###3.99%###2.54%

###(1.17-###(2.21-###(2.79-###(1.81-

###2.98)a###4.37)a###5.40)a###3.42)b

Others###0.61%###0.74%###1.03%###0.46%

###(0.35-###(0.45-###(0.43-###(0.28

###0.93)a###1.09)a###1.82)a###0.69)a

Seasonal variations in activity

There were significant difference in the duration of feeding (Z= 3.128 P= 0.002) and resting (Z= -2.426 P= 0.015) between the seasons for females while no significant differences were found in moving (Z= -0.105 P= 0.908) vigilance (Z= - 0.102 P= 0.919) and other" activities (Z= -0.41 P= 0.682). For males significant differences were observed between the seasons for the duration of resting (Z= -2.062 P= 0.039) and vigilance

Daily variations of activity

During the warm season both female and male white-lipped deer had three feeding and one or two resting peaks. The feeding peaks usually occurred in early morning early afternoon and evening (18:0020:00). During the cold season males showed only a morning (07:0009:00) and an evening (17:0018:00) feeding peak (Fig. 2) while resting was at its highest level during the middle of the day (10:0013:00). Similarly females also had two feeding peaks and one resting peak during the cold season (Fig. 3).

DISCUSSION

According to our data feeding was the primary activity and resting was the second most important activity during both the warm and cold seasons. Moving vigilance and other" activities comprised only a small part of the daytime activity budgets. Similar results have been noted for many other ungulate species such as red deer (Cervus elaphus) (PACopyrightpin et al. 2006) Przewalski's gazelle (Procapra przewalskii) (Chen et al. 1997) Tibetan antelope (Panthalops hodgsoni) (Lian et al. 2007) goitred gazelles (Gazella subgutturosa) (Xia et al. 2011) and Asiatic wild ass (Equus hemionus) (Xia et al. 2013). We did not find a statistical difference in any of the monitored activities between the genders during the warm season.

Alternatively during the cold season males spent more time moving standing at vigilance and doing other" activities as compare to females although only vigilance was significantly different. Previous studies have found that male Przewalski's gazelle (Chen et al. 1997) and Tibetan antelope (Lian et al. 2007) were more vigilant than females during the rutting period because of an increase in aggression and sparring activities. Similarly with the rutting season for the white-lipped deer between September and November (the cold season) (Zheng et al. 1989; Sheng and Ohtaishi 1993) the higher vigilance rates of the males observed here may reflect intraspecific competition where territorial males are watching for other males and for receptive females (Hart et al. 1992).

In this study we observed considerable differences in the time budgets of the deer between the two seasons. Where June to mid-September is the plant-growing season late September to May is the plant-withering season. The pasture has much more biomass in the warm season and a decreased biomass in the cold season. In order to satisfy their energy and nutrient requirements the deer have to increase their intake of food and thus spend more time feeding during the cold season. Similar results have been found in other ungulates living in the plateau such as the Przewalski's gazelle (Chen et al. 1997) and Tibetan antelope (Lian et al. 2007).

Our data also showed that the white-lipped deer spends the majority of their time resting during the warm season and less time resting during the cold season (Table I). Resting generally leads to a lower basic metabolic rate which is a natural response to extremely high ambient temperatures (Arnold et al. 2004; Maloney et al. 2005). However the mean annual temperature was -3.08C in our study area and there was no extremely high temperature measured during the warm season. In contrast the cold season was severely cold resulting in a large decrease in vegetation biomass. Hence feeding became almost continuous during the daytime during the cold season. We suggest that this increased duration of feeding ultimately caused the decreased duration of resting in the cold season.

Both male and female deer showed a trimodal feeding pattern during the warm season but a bimodal feeding pattern during the cold season. Some studies have reported that bigger ruminants have an increased number of feeding peaks during the summer such as: red deer (Georgii 1981) European bison (Bison banasus) (Cabon-raczynska et al. 1987) and Apennine chamois (Rupicapra pyrenaica) (Bruno and Lovari 1989). White-lipped deer generally weigh 130-200kg and hence can be viewed as a large ungulate (Ohtaishi et al. 1993). The increased feeding peaks of the deer during the warm season also support the hypothesis that larger- bodied ruminants are less sensitive to temperature and can be much more active during the heat of the day (Du Toit and Yetman 2005). We will not discuss the rest behaviors because no special features were found between the deer and other ungulates.

It should be also mentioned that the effects of human activities on the behavior of deer should not be overlooked. With the rapid growth of human populations and an improvement in their living standards the number of livestock stock grazing on meadow and steppes on the Qinghai-Tibet Plateau have increased in turn (Zhao and Zhou 1999). Livestock often undergo competition with wild ungulates for food (Campos-Arceiz et al. 2004). In our study area the local herdsmen practice a pastoral grazing system. As such domestic animals graze these ranges from October-June (the cold season). Furthermore Gramineae (Kobresia pygmaea Kobresia humilis Kobresia capillifolia) and Cyperaceae (Sitipa purpurea Elymus nutans Poa. spp.) are the primary food source of the white- lipped deer (Cai 1988; Zheng et al. 1989). Incidentally they are also the main food of Tibetan domestic sheep (Li et al. 2008) and domestic yak (Dong et al. 2004).

Although speculative this data suggests that a dietary overlap between livestock and white-lipped deer likely exists during the cold season. Although speculative this data suggests that a dietary overlap between livestock and white- lipped deer likely exists during the cold season. Consequently feeding conditions would become particularly difficult for the white-lipped deer during this time which might also contribute to the increased feeding and decreased resting durations in the cold season.

Taken together we conclude that the best way to protect this Vulnerable" animal would be for the local government to limit the grazing of livestock in the white-lipped deer's habitats especially during the cold season. By reducing the competition for food and habitat we can better manage the declining populations of white-lipped deer.

ACKNOWLEDGEMENTS

This study was funded by the Wildlife and Nature Reserve Administration of Qinghai Province to Tongzuo Zhang. We would like to thank Benjia Yang and his family from the Yanglong village for their help.

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