PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER

Foraging behaviour at multiple temporal scalesin a wild alpine equid

Antoine St-Louis • Steeve D. Cote

Received: 15 July 2010 / Accepted: 6 October 2011 / Published online: 28 October 2011

� Springer-Verlag 2011

Abstract Forage abundance, forage quality, and social

factors are key elements of the foraging ecology of wild

herbivores. For non-ruminant equids, forage-limited envi-

ronments are likely to impose severe constraints on their

foraging behaviour. We used a multi-scale approach to

study foraging behaviour in kiang (Equus kiang), a wild

equid inhabiting the high-altitude rangelands of the Tibetan

Plateau. Using behavioural observations and vegetation

sampling, we first assessed how patterns of plant abun-

dance and quality affected (i) the instantaneous forage

intake rate (fine scale) and (ii) the proportion of time spent

foraging (coarse scale) across seasons. We also tested

whether foraging behaviour differed among group types,

between sex in adults, and between females of different

reproductive status. At a fine scale, intake rate increased

linearly with bite size and increased following a type II

curvilinear function with biomass on feeding sites. Forage

intake rate also increased linearly with plant quality. Male

and female kiangs had similar intake rates. Likewise,

gravid and lactating females had similar intake rates as

barren and non-lactating females. At a coarse scale, kiangs

spent longer time feeding in mesic than in xeric habitats,

and spent more time feeding in early summer and fall than

in late summer. Groups of adults with foals spent less time

feeding than male groups and groups of adults without

foals. Our findings suggest that kiangs use flexible foraging

behaviours in relation to seasonal variations of vegetation

quality and abundance, a likely outcome of the extreme

seasonal conditions encountered on the Tibetan Plateau.

Keywords Foraging � Scale � Equids � Arid environment �Equus kiang

Introduction

Studying the factors driving foraging behaviour in grazing

herbivores is not trivial, as it may provide valuable insights

about mechanisms determining resource selection, and thus

further our understanding of plant-herbivore relationships

(Spalinger and Hobbs 1992; Bailey et al. 1996; Wilmshurst

et al. 1999; Owen-Smith 2002). In grassland ecosystems,

phenological stages of plant maturation are known to

influence the abundance and nutritional quality of vegeta-

tion patches, which in turn affect the foraging behaviour of

grazing herbivores (McNaughton 1985; Fryxell 1991;

Spalinger and Hobbs 1992; Wilmshurst et al. 2000). The

effect of plant abundance and quality on forage intake

depends extensively upon the digestive efficiency of her-

bivores (reviewed in Van Soest 1996), which mainly

depends on their body size and digestive anatomy (Jarman

1974; Janis 1976; Demment and Van Soest 1985). In

addition to food resources, social and demographic-related

factors such as group size (Jarman 1974; Giraldeau and

Caraco 2000), age-sex classes (Cote et al. 1997; Ruckstuhl

1998; Perez-Barberıa et al. 2008), and reproductive status

of females (Hamel and Cote 2008) are known to influence

foraging behaviour in ungulates.

Communicated by Gøran Ericsson.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s00442-011-2166-y) contains supplementarymaterial, which is available to authorized users.

A. St-Louis (&) � S. D. Cote

Departement de biologie and Centre d’etudes nordiques,

Universite Laval, Quebec, QC G1V 0A6, Canada

e-mail: antoinestlouis@yahoo.ca

S. D. Cote

e-mail: steeve.cote@bio.ulaval.ca

123

Oecologia (2012) 169:167–176

DOI 10.1007/s00442-011-2166-y

In grazing herbivores, bite size is generally positively

related to plant biomass on food patches (Illius 2006). As

bite size increases so does the time needed to handle bites

(i.e., cropping and chewing; Spalinger and Hobbs 1992).

Biting rate is thus typically negatively related to bite size,

which often leads to a type-II functional response (Spa-

linger and Hobbs 1992; Hobbs et al. 2003). Moreover,

because plant digestibility generally declines with plant

abundance in grasslands, plants on high-biomass swards

allow a fast dry matter intake but take longer to digest than

plants on low-biomass sward (Van Soest 1994; Laca et al.

2001). Grazing ruminants constrained by their digestive

capacity thus face trade-offs between short- and long-term

nutrient intake (Wilmshurst et al. 2000; Fortin et al. 2002).

Alternatively, non-ruminant equids are little constrained by

forage retention time in the digestive tract and can possibly

feed for long periods on tall swards, potentially maximiz-

ing nutrient intake at both long and short temporal scales

(Janis 1976; Duncan et al. 1990; Fortin et al. 2002).

Burchell’s zebra (Equus burchellii), an equid adapted to

temperate environments, typically feed for longer periods

and have higher forage intake rate than sympatric rumi-

nants (Okello et al. 2002; Twine 2002). On the other hand,

arid environments with limited forage like deserts or

mountains may impose severe constraints on the foraging

behaviour of wild equids, restricting their capacity to

achieve a high dry matter intake (Rubenstein 1989). Pre-

vious studies suggested that equids adapted for arid envi-

ronments make trade-offs between the nutritional quality of

plants and their abundance when selecting food resources

(Rubenstein 1989; Kaczensky et al. 2008; St-Louis 2010),

which may impose trade-offs among temporal scales of

foraging behaviour as well. How the scarcity and fluctu-

ating quality of the vegetation in forage-limited ecosystems

affect foraging behaviour and functional response in wild

equids, however, has rarely been addressed.

Equids have also evolved complex social systems,

where species in mesic environments form stable harem

groups whereas species in arid environments form only

temporary associations (Klingel 1977; Rubenstein 1986;

Sundaresan et al. 2007). Males living in these ‘‘fission–

fusion’’ society are typically territorial and associate only

temporary with female groups. Neuhaus and Ruckstuhl

(2002) observed that male and female zebras living in

stable harem groups had similar activity budget and for-

aging behaviour (but see Rubenstein 1986, 1994). In arid

environments, however, the scarcity of the food resource

may exacerbate differences in energetic requirements

between males and females, especially lactating ones,

thereby causing differences in their activity budgets and

foraging behaviour (Rubenstein 1989, 1994).

In this study, we investigated factors influencing for-

aging behaviour in an arid-adapted equid, the kiang

(Equus kiang). The kiang inhabits the high altitude steppes

of the Tibetan Plateau, a highly seasonal environment with

harsh climatic conditions and scarce vegetation (Schaller

1998). Predation risks are perceived low for kiangs (St-

Louis and Cote 2009). There are indications that kiangs

live in a fission–fusion social system (Denzau and Denzau

1999; St-Louis and Cote 2009) and that they select

resources in relation to both forage abundance and quality

(St-Louis 2010). It is not known, however, how resource

selection patterns are related to foraging behaviour, which

may provide important cues about the constraints faced by

this wild equid adapted to extreme environmental

conditions.

Our main objectives were twofold: (1) to assess the

effects of vegetation abundance and quality on foraging

behaviour in kiangs, and (2) to determine if foraging

behaviour differs among groups of different composition in

terms of age-sex classes, between males and females, and

between reproductive (gravid or lactating) and non-repro-

ductive females. We first evaluated how vegetation varied

in terms of abundance and quality across habitat types and

throughout the summer and the fall, and then assessed how

vegetation and social factors influence the foraging

behaviour of kiangs at two temporal scales: (i) the instan-

taneous intake rate of focal individuals (fine scale) and (ii)

the percentage of time spent feeding by kiang groups

during activity budgets (coarse scale). Doing so, we also

considered the potential effect of the time of the day, since

foraging behaviour may also be influenced by daily pat-

terns of temperature or daily movements (Berger 1986,

Duncan 1992). We hypothesized that (a) bite size should

increase with biomass on feeding site; (b) intake rate

should increase with bite size in a curvilinear fashion fol-

lowing a type II functional response, given that biting rate

should decline with bite size; (c) intake rate should relate

positively to vegetation biomass on food patch following a

type II functional response, given that biting rate should

also decline with biomass; (d) intake rate should be higher

on green vegetation than on dry vegetation, since green

leaves are easier to handle and chew; (e) kiangs should

spend more time feeding in morning and evening than

during the middle of the day, thereby avoiding being active

during the warmest period of the day; (f) the proportion of

time spent foraging should be negatively related to plant

biomass; (g) kiangs should spend a higher proportion of

time feeding early in the summer than later during the

summer and fall, thereby following seasonal plant growth;

(h) the proportion of time spent foraging should be nega-

tively related to plant quality; (i) females and males should

have comparable intake rates and time spent feeding

because of their similar body size; (j) similarly, gravid/

lactating females and barren/non-lactating females should

have similar intake rates, but (k) females in groups with

168 Oecologia (2012) 169:167–176

123

foals should spend more time foraging than females in

groups without foals.

Methods

Study area

We conducted this study in fall 2003 (29-Aug to 21-Nov),

summer 2004 (17-Jun to 25-Aug) and summer 2005 (26-

Jun to 20-Aug) in a 390-km2 area located in the Tso Kar

basin, Eastern Ladakh, India (32�150N, 78�000E). This area

is part of the extensive Tibetan Plateau, and represents the

westernmost and driest part of the kiang’s distribution

range, with mean annual precipitation \100 mm (Schaller

1998; St-Louis and Cote 2009). The elevation within the

Tso Kar basin ranges from 4,550 to 6,000 m, and the cli-

mate is that of high altitude/cold desert ecosystems, with

annual temperatures ranging from -40�C to 30�C. The

vegetation is typical of alpine and desert steppes (Schaller

1998), mainly composed of grasses (Poaceae), sedges

(Cyperaceae), and short dicotyledonous forbs and shrubs

(Mani 1978; Rawat and Adhikari 2005). Most common

plant genera are Stipa, Carex, Leymus, Eurotia, Artemisia,

Oxytropis, Elymus, Kobresia, Alyssum, Caragana, and

Potentilla (Rawat and Adhikari 2005). We identified three

main habitat types at Tso Kar: (a) meadows, a mesic

habitat located below 4,600 m with vegetation cover

C20%; (b) plains, a xeric habitat located \4,600 m char-

acterized by vegetation cover \20%, slope B5�; and

(c) hills, a xeric habitat located at C4,600 m with vegeta-

tion cover \20% and slope [5� (St-Louis 2010; ESM 1).

Tibetan wolves (Canis lupus chanco) occasionally prey on

kiangs, but they occur in small numbers in the Tso Kar

basin (Pfister 2004). An estimated 250 kiangs inhabit the

area on a yearly basis (Fox et al. 1991).

Observations

Focal sampling

Focal sampling (Altmann 1974) was performed on foraging

individuals to monitor fine-scale foraging behaviour. Focal

individuals were chosen randomly among adults in groups

located \500 m from the observers, and we ensured that

data were balanced across all habitat types for both sexes.

Kiangs were not marked, but we could reliably identify

individuals within groups during an observation session

with the help of natural marks and their position within the

groups, allowing us not to observe the same individuals

twice during a single day. We noted the sex of individuals

and the reproductive status of females. In summer, gravid

females are easily recognizable from barren ones because

they have a rounder and larger belly. Foals were seen

suckling as late as the end of August. From mid-July until

late-August, a female kiang accompanied by a foal was

therefore noted as lactating. For each focal animal, we

recorded during 5-min periods the number of bites and

steps taken while feeding on a hand-held tape recorder. A

step was defined as a forward movement of any of the front

legs. Interruptions in cropping sequences were noted when

kiangs raised their head above shoulder level, either for

vigilance, walking, or miscellaneous behaviour (e.g.,

grooming). The measurement of biting rates during con-

tinuous cropping sequences (expressed in number of

bites-min) led to the calculation of the forage intake rate

(see details below), which in our study corresponds to the

fine temporal scale.

Scan sampling

To monitor the proportion of time spent feeding by kiangs

during daylight, we conducted repeated scan sampling of

kiang groups (Altmann 1974), performed every 15 min

using 15–459 spotting scopes. Kiang observations spanned

the entire daylight period (0600–2000 h). Each observation

period lasted between 2 and 8 h. Kiang groups were divided

in 3 categories: (1) single male, (2) adults without foals, and

(3) adults with foals. Because it was often not possible to

discriminate males, females and yearlings during scans, the

second type encompassed bachelor groups, groups of

females and yearlings, and mixed groups with typically 1

male and several females and yearlings. Kiang behaviour

was divided into five categories: (1) feeding, (2) standing,

(3) lying, (4) walking, and (5) other (i.e. social interaction,

running). Scan observations yielded the proportion of time a

group spent feeding, which corresponds to the coarse tem-

poral scale. We followed 173 groups between 1 and 8 h, for

a total of 557 h of observation.

Habitat and feeding site surveys

The habitat type was noted visually for every group fol-

lowed during scan sampling. For focal individuals, we

surveyed feeding sites within habitat types to assess whe-

ther foraging behaviour was influenced by vegetation

attributes. Two observers were necessary to locate a

feeding site following a focal observation. One observer

moved to the site where the focal kiang had been seen

feeding and marked the centre of the site, guided through

radio contact by the other observer with a spotting scope.

The presence of grazing marks was required to confirm the

location of the feeding site. Feeding site attributes were

estimated by laying six 1-m2 plots, randomly placed within

a 10-m radius circle centered on the feeding location

(Schaefer and Messier 1995). In every plot, plant cover and

Oecologia (2012) 169:167–176 169

123

percentage of green material were estimated visually using

10% classes in four vegetation groups: grasses (mainly

family Poaceae), sedges (family Cyperaceae), forbs (all

herbaceous dicots), and shrubs (woody stemmed species).

Mean plant height was calculated by measuring five ran-

domly selected plants of each group to the nearest cm using

a ruler. To convert plant cover and height into biomass, we

clipped individual plants 1 cm above the ground in one

randomly chosen plot (out of 6) on each feeding site. Plant

samples were dried in the field in paper bags, and then oven

dried for 48 h at 60�C, and weighed using a 0.1 g precision

scale. We used linear regressions to calculate regression

coefficients for plant cover and height, and then estimated

biomass for each plant category in all plots (see Hamel and

Cote 2007 for details). The feeding site sampling design

also allowed us to estimate the mean percentage of green

vegetation in three habitat types for each field season. For

that purpose, we used only the data collected on random

feeding sites. Percentage of plant cover and height were

converted into biomass using a multiple regression analysis

(ESM 2).

Estimation of bite size

We estimated bite size by first measuring with a ruler the

grazing depth of the eight nearest grazed plants from the

centre of the feeding site, and calculated the mean grazing

depth. Within a 1-m radius circle, we then randomly located

three small square quadrats of 6 9 6 cm, corresponding to

the approximate width of a kiang’s mouth (Janis and Ehr-

hardt 1988; St-Louis and Cote 2009), and clipped plants to

the average grazing depth. Plant samples were dried in the

field in paper bags, and then oven dried for 48 h at 60�C,

and weighed using a 0.001 g precision scale.

Analyses

Fine temporal scale

Because sward biomass is known to exert a major influence

on bite size in grazing ungulates (Laca et al. 1992), we

modelled the relationship between our bite size sample

(N = 21) and the biomass on corresponding feeding sites

to extrapolate bite size measurements to all feeding sites

(N = 52). We calculated the forage intake rate achieved on

each feeding site as I = S 9 BR, where I is the intake rate

expressed in grams per minute feeding during cropping

sequences, S is the estimated bite size (in grams), and BR is

the biting rate during cropping sequences. We then asses-

sed the influence of group size on intake rate using a

general linear model (GLM). Because group size had no

statistical influence on this variable (F1,43 = 2.69, P =

0.20, N = 45), we removed it from subsequent analyses.

Secondly, we assessed the influence of bite size and forage

biomass (patch) on forage intake rate (g-min) and biting

rates (bite-min) using linear regressions and non-linear

Michaelis–Menten functions. We assumed that bites were

always visible to kiangs and that the time to reach a new

bite was not higher than the time required to crop and

swallow a bite, as commonly found for grazing ungulates.

Therefore, we used models under the process 3 of Spalin-

ger and Hobbs (1992). These models enabled us to assess

whether forage intake rate was regulated by foraging

mechanisms operating at the bite or at the patch scale. We

then analysed the influence of the greenness of plant leaves

on intake rate using a GLM.

Coarse temporal scale

The percentage of time kiang groups spent feeding was

calculated as the proportion of scans where more than 50%

of the individuals were seen feeding to the total number of

scans done on a specific group. To take into account

potential daily patterns in activity budgets, we first divided

our observations in three periods: from 0600 to 1000

(morning), 1000 to 1500 (mid-day), and 1500 to 2000

(evening). Since there was no difference in the time spent

feeding between morning and mid-day (t1,163 = 0.40, P =

0.69, N = 166) we pooled these two classes, and performed

our analyses using two daily periods: from 0600 to 1500

(daytime) and from 1500 to 2000 (evening). To take into

account the potential influence of group size on foraging

behaviour, we analysed the influence of group size on time

spent feeding using a GLM, which was not significant

(F1,164 = 1.39, P = 0.24, N = 166). Therefore, we did not

include this factor in the analyses. We used a logistic

regression to assess the influence of habitat type, date (i.e.

number of days since 1 June), period of the day and group

type on the proportion of scans where kiangs were feeding.

We tested a priori the effect of year on time spent foraging

for summers 2004 and 2005. Because there was no differ-

ence between the two summer seasons (t1,163 = -0.88,

P = 0.38, N = 166), we pooled the data for these 2 years.

Moreover, because the dates of observations in fall 2003 did

not overlap with the dates of observations during summers

2004–2005, the factor date was used as a surrogate for the

season, and the factor year was removed from the analyses.

We then built candidate models as to include combinations

of all covariates and interactions between covariates that

were biologically relevant to our initial hypotheses. Models

were ranked based on the Akaike Information Criterion,

corrected for small sample size (AICc; Burnham and

Anderson 2002). For each candidate model, we calculated

the delta AICc (Di), the Akaike weight (xi), and the evi-

dence ratio, expressed as the ratio between the Akaike

weight of the best model and the Akaike weight of model i.

170 Oecologia (2012) 169:167–176

123

This ratio indicates how the first model (i.e. with the lowest

AICc value) is likely to be the best model compared to

model i. We then calculated the percentage of variance

explained by the first model using R2 = 1-SSR/SSTO,

where SSR = R[(Yobserved-Ypredicted)2], and SSTO =

R[(Yobserved-Yobserved)2] (Xu 2003).

Statistical linear models were implemented using SAS

9.1 (SAS Institute Inc. 2003), while non-linear models of

functional response were analysed using SigmaPlot 8.0

(SPSS Inc. 2002). Means are presented ±SE. Significance

level was set at 0.05 for all statistical analyses.

Results

Vegetation parameters on feeding sites

Feeding sites in meadows were greener than those in plains

(t2,45 = 2.03, P = 0.048, N = 52) and hills (t2,45 = 5.36,

P \ 0.001, N = 52) during fall, but there was no difference

in vegetation greenness on feeding sites among the three

habitat types during summer. Meadows had higher forage

biomass than plains (t2,47 = 6.33, P \ 0.001, N = 52) and

hills (t2,47 = 8.74, P \ 0.001, N = 52) during both sea-

sons. Vegetation greenness and date were negatively rela-

ted, as leaves turned brown during the fall season, i.e. after

mid-September (R2 = 0.76, F1,50 = 163.55, P \ 0.001,

N = 52; Fig. 1).

Fine temporal scale

Bite size increased with biomass in a logarithmic fashion,

following the relationship: ln[bite size] = 4.03 ? 0.254 9

ln[biomass] (R2 = 0.29, P = 0.012, N = 21). At the bite

scale, intake rate increased linearly with bite size under the

range observed, since linear regressions and non-linear

Michaelis–Menten functions fitted the data very similarly

(R2 = 0.48, F1,50 = 45.98, P \ 0.001, N = 52; Fig. 2a).

There was no relationship between biting rate and bite size,

whether fitted by a linear (R2 \ 0.01, F1,50 = 0.01, P = 0.84,

N = 52) or a non-linear function (R2 \ 0.01, F1,50 = 0.20,

P = 0.66, N = 52). At the patch scale, forage intake rate

increased asymptotically with forage biomass, showing a type

II functional response for both feeding sites with mainly

brown and green leaves (vegetation\50% green: R2 = 0.75,

F1,11 = 33.13, P \ 0.001, N = 14; vegetation [50% green:

R2 = 0.51, F1,36 = 37.74, P \ 0.001, N = 38; Fig. 2b). The

model showed that forage intake rate started to level at a

biomass of around 20 g�m2

, and that the maximum intake

rate was 6.22 g-min (Fig. 2b). There was also no relationship

between biting rate and biomass on feeding sites (linear

regression: R2 \ 0.01, F1,50 = 0.01, P = 0.90, N = 52; non-

linear Michaelis function: R2 = 0.02, F1,50 = 2.20, P = 0.14,

N = 52). Forage intake rate increased linearly with plant

greenness (R2 = 0.20, F1,50 = 14.01, P \ 0.001, N = 52;

Fig. 3). Accordingly, intake rate decreased with date, being

larger in summer than during the fall (R2 = 0.13, F1,50 =

7.58, P = 0.008). Sex of adult kiangs had no influence on

intake rate (F1,49 = 1.17, P = 0.28, N = 52). Lactating and

non-lactating females had similar intake rates (F1,13 = 0.24,

P = 0.63, N = 15).

Coarse temporal scale

The proportion of time spent feeding during activity bud-

gets was mainly explained by the interaction of habitat type

and group type (v2 = 17.63, df = 4, P = 0.002, N = 173),

the period of the day (v2 = 36.63, df = 1, P \ 0.001,

N = 173) and the date (exponent 2) after 1 June (v2 =

49.72, df = 1, P \ 0.001, N = 173). This model had an

Akaike weight of 0.93 (see ESM 3 for the complete list of

candidate models). Kiangs generally spent 1.2 and 1.3

more time feeding in meadows than in plains and hills

(Fig. 4). Groups with foals spent generally less time

feeding than the other two group types, especially in hills

(Fig. 4). The proportion of time spent feeding by kiangs

was about 70% in early summer, declined to approximately

30% in late summer, and further increased to about 50%

very late in the summer and during autumn (Fig. 5). Kiangs

spent 1.5 more time feeding at the end of the afternoon than

during daytime (daytime: 39 ± 2%; evening: 58 ± 3%).

Discussion

In this paper, we assessed the influence of vegetation and

social factors on the foraging behaviour of a wild equid

Days since 1 June20 40 60 80 100 120 140 160

% G

reen

0

20

40

60

80

100

Jul. Aug. Sept. Oct.

Fig. 1 Percentage of vegetation greenness on kiang feeding sites in

relation to date in the Tso Kar basin, Ladakh, India, 2003–2005

Oecologia (2012) 169:167–176 171

123

adapted to a highly seasonal environment. To our knowl-

edge, this is the first study to investigate foraging behaviour

in an arid-adapted equid at several temporal scales simul-

taneously. As expected for an equid, kiangs achieved a

higher forage intake rate on habitats and patches with high

plant biomass, but the important role of vegetation quality

on fine-scale foraging processes is a novel finding. Here,

we discuss how vegetation and social factors influence

foraging behaviour in kiangs at both fine and coarse tem-

poral scales, and conclude with implications for equids

living in highly seasonal environments.

Fine scale processes

We first hypothesized that intake rate would increase with

bite size following a type II functional response. We rather

observed that intake rate increased linearly with increasing

bite sizes, without showing any deceleration. Large bites

Bite size (g)

Inta

ke r

ate

( g-m

in)

0

2

4

6

8

10

Biomass (g-m2

)

0.05 0.10 0.15 0.20 0 20 40 60 80 100 120 1400

2

4

6

8

10a b

Fig. 2 Models of functional response of kiangs foraging at Tso Kar

basin, Ladakh, India, 2003–2005. a Linear (plain line) and non-linear

Michaelis–Menten (dashed line) regressions of dry matter intake rate

in function of bite size; b non-linear regression (Michaelis–Menten)

between dry matter intake rate and vegetation biomass on feeding

sites with vegetation [50% green (empty dots with dashed line) and

feeding sites with vegetation\50% green (black dots with plain line)

Arcsine % Green0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8

Inta

ke r

ate

(g-m

in)

0

2

4

6

8

10

Fig. 3 Intake rate by kiangs in relation to plant greenness on feeding

sites (arcsine transformed) in the Tso Kar basin, Ladakh, India,

2003–2005

Days since 1 June

0 20 40 60 80 100 120 140 160 180

% T

ime

spen

t fee

ding

0

20

40

60

80

100

Fig. 5 Mean percentage of time spent feeding (±SE) by kiangs in

relation to date in the Tso Kar basin, Ladakh, India, 2003–2005

Habitat

Meadows Plains Hills

% T

ime

spen

t fee

ding

0

20

40

60

80

100Groups with foalsGroups without foalsSingle individuals

Fig. 4 Mean percentage of time spent feeding (±SE) by kiangs in

relation to group types and habitat types in the Tso Kar basin, Ladakh,

India, 2003–2005

172 Oecologia (2012) 169:167–176

123

therefore did not take more time to chew than small bites

under the range of bite sizes observed (0.07–0.22 g-bite).

This does not preclude, however, that an asymptotic rela-

tionship between bite size and intake rate exists in kiang. It

is likely that bites taken by kiangs were too small to detect

such an asymptotic relationship. For example, Gross et al.

(1993) observed that intake rate increased linearly for

several large herbivores (including domestic horses) until

bite size reached 1.5 g. The low bulk density or height of

the grass available to kiangs may thus have physically

restricted bite sizes below this minimum value. At the

patch scale, our results support the hypothesis that intake

rate increases with biomass in a curvilinear fashion fol-

lowing a type II functional response, as observed in several

studies on grazing ungulates (Gross et al. 1993; Hobbs

et al. 2003; Illius 2006). Our results show that the maxi-

mum intake rate is achieved on feeding sites that contains

more than 120 g plant per square-m. Short-term intake rate

is thus best achieved on feeding sites and habitat types

containing more food. However, this maximum point is far

from what could theoretically be achieved by a wild equid.

Gross et al. (1993) observed that the maximum intake rate

by horses was approximately 30 g-min. A likely explana-

tion is that kiangs crop plants only partially in abundant

food patches, possibly to maintain a high biting rate, and

therefore leading to an asymptotic relationship between

bite size and patch biomass. Previous authors have stressed

the importance of correctly describing the gain function,

i.e. the relationship between bite size and patch biomass as

swards are progressively depleted, in order to understand

movements between food patches and across landscapes

(Stephens and Krebs 1986; Shipley 2007). Asymptotic gain

functions are common for grazers feeding on long grass

swards, where bite size decreases consistently as patches

are depleted (Laca et al. 1994). The decelerating functional

response that we observed in kiangs on feeding sites with

both dry and green vegetation seems best explained by the

log-shaped function between feeding site biomass and bite

size rather than by the time constraint to handle large bites.

Forage palatability is known to increase daily voluntary

intake in ruminants (Van Soest 1994), and our results

indicate that a similar pattern may exist in equids as well, at

least in a forage-limited environment. Hence, the strong

relationship we found between intake rate and plant

greenness is one of the most important findings of our

study. As green leaves are easier to handle than dry leaves

(Van Soest 1994; Laca et al. 1992; Shipley 2007), plant

quality appears to play a significant role in short-term

forage intake rate in kiangs, which has rarely been dem-

onstrated in wild equids. Fleurance et al. (2009) found no

influence of increasing fibre content on forage intake rate in

horses, except for one pony. If resources are abundant,

however, high intake rate is possible on fibrous forage, as

shown in horses (Edouard et al. 2008). The strong response

of forage intake rate to the nutritional quality of plants in

kiangs is possibly a mechanism to maximize their short-

term nutrient intake in a highly seasonal and forage-limited

environment.

Intake rates did not differ between male and female

kiangs, a potential outcome of the slight dimorphism

between the two sexes (Berger 1986; St-Louis and Cote

2009). Similarly, gravid and lactating females did not

perform higher intake rates than barren and non-lactating

females. These results thus support our hypothesis that

adult kiangs of similar body sizes should have comparable

intake rates. If female of different reproductive status have

different energetic requirements, as observed in other un-

gulates (Therrien et al. 2007; Hamel and Cote 2008), our

results suggest that such difference has little implication on

fine-scale foraging processes in kiangs.

Coarse scale processes

Because instantaneous intake rate is higher in abundant

food patches than in patches with scarce plant cover, ki-

angs should be able to minimize their time spent feeding

in habitats with abundant forage (Spalinger and Hobbs

1992; Hobbs et al. 2003). We thus hypothesized that ki-

angs would need to spend less time feeding in habitats

with abundant forage (mesic) than in habitats with sparse

forage (xeric). In our study, kiangs spent a higher pro-

portion of their time feeding in mesic habitats with high

forage abundance than in xeric habitats with low forage

abundance, which contradicts our initial hypothesis. As

noted previously, the maximum intake rate achieved by

kiangs in our study is much less than the maximum rate

achieved in wild equids of comparable size. Since the

maximum intake rate occurs on habitats with standing

biomass [20 g�m2

, kiangs would benefit from eating for

extended periods on meadows with abundant forage in

order to maximize their daily dry matter intake. There-

fore, meadows appear as important feeding habitats for

kiangs in the Tso Kar basin.

Our hypothesis that time spent feeding would increase

from summer to fall season was partly supported. As leaves

become dry in fall, kiangs presumably need to feed for

extended periods to compensate for decrease intake rates in

order to meet their energetic requirements, as suggested by

our results. This suggestion, however, does not explain

why time spent feeding was higher early in the summer

than later during the season. Increased energetic require-

ments following harsh winter conditions may prompt ki-

angs to maximize their forage intake rate at both fine and

coarse temporal scales, thereby taking advantage of the

vegetation green-up by increasing their instantaneous for-

age intake rate and daily time spent feeding. In mid-

Oecologia (2012) 169:167–176 173

123

summer, which coincides with mating and birth seasons, a

reduction in feeding time is likely due to an increase in

time devoted to activities related to the reproduction period

(e.g. chases among males, tending nursery groups, milking

foals, increased vigilance of lactating females). Plant

digestibility may still be high enough so that kiangs can

maintain high short-term nutrient intake while incurring

reduced time spent feeding. Similar seasonal patterns were

observed in female mountain goats (Oreamnos americ-

anus; Hamel and Cote 2008) and Cantabrian chamois

(Rupicapra pyrenaica parva; Perez-Barberıa and Nores

1996), thereby suggesting a common behavioural pattern

among alpine ungulates.

Reproductive female ungulates generally incur higher

energetic costs than non-reproductive females, and should

thus have higher daily forage intake (Berger 1986; Therrien

et al. 2007; Hamel and Cote 2008). The observation that

adults in groups with foals spend less time feeding than

adults in groups without foals is thus a surprising result,

since we expected that lactating females would have to

spend more time feeding than non-lactating females (Ru-

benstein 1994). A possible explanation is that females in

groups with foals are more vigilant than females in groups

without foals in order to prevent harassment by males and

possible infanticide events. As in other equids, infanticide

is thought to occur in kiangs (St-Louis and Cote 2009) and

harassment of nursery groups have been observed on sev-

eral occasions in the field. Lactating females in groups

tended by a dominant stallion, however, should be able to

gain protection from intruding males and thus spend more

time feeding in order to meet their increased energetic

needs (Rubenstein 1994). Investigating the role of tending

stallions on female behaviour in kiangs would be needed to

further address this question, which has not been attempted

yet.

Implications for equids in highly seasonal environments

Plant phenology and environmental conditions strongly

influence the energetic balance and the foraging behaviour

of herbivores living in highly seasonal environments

(DelGiudice et al. 1990; Albon and Langvatn 1992; Moen

et al. 2006; Shrader et al. 2006). In arctic and alpine eco-

systems for instance, increasing forage intake following

winter is often necessary to regain body condition (Van der

Wal et al. 2000; Hamel and Cote 2008), and in tropical

grasslands to compensate for a decline in forage quality

during the dry season (Shrader et al. 2006). The observa-

tion that kiangs closely adjust their foraging behaviour to

the seasonal patterns of plant phenology suggests that plant

quality is an important driver of their foraging ecology,

possibly in response to the extreme nature of their environ-

ment. The foraging behaviour of kiangs differs somewhat

from patterns typically observed in equids (e.g. Edouard

et al. 2008), but is rather similar to ruminant ungulates

living in highly seasonal environments such as arctic and

alpine ecosystems (e.g. Cote et al. 1997; Van der Wal et al.

2000; Hamel and Cote 2008). In a forage-limited envi-

ronment, therefore, wild equids selecting food resources on

the basis of both forage abundance and nutritional quality

potentially increase their nutrient intake at several temporal

scales.

Acknowledgments Our research was funded by the Wildlife Con-

servation Society, the Natural Sciences and Engineering Research

Council of Canada and the Bureau International de l’Universite Laval,

Canada. We thank K. Gailson, S. Tsering, C. Namgyal, J. Namgyal

and the Rupshu nomadic community for their invaluable help in the

field. We also thank J.L. Fox (University of Tromsø), S. Sathyakumar

(Wildlife Institute of India), S. Ul-Haaq, J. Thakpa (Department of

Wildlife Protection of Jammu and Kashmir) and the Norwegian

Agency for Development Cooperation (WII-UiTø ICP programme)

for their logistical support. We are indebted to D.I. Rubenstein,

D. Fortin, C. Dussault, J. Pastor and an anonymous reviewer for

insightful comments on a previous version of the manuscript. Finally,

we thank J. Mainguy, S. Hamel and A. Masse for their help with

statistical analyses.

References

Albon SD, Langvatn R (1992) Plant phenology and the benefits of

migration in a temperate ungulate. Oikos 65:502–513

Altmann J (1974) Observational study of behavior: sampling

methods. Behaviour 49:227–267

Bailey DW, Gross JE, Laca EA, Rittenhouse LR, Coughenour MB,

Swift DM, Sims PL (1996) Mechanisms that result in large

herbivore grazing distribution patterns. J Range Manag 49:386–

400

Berger J (1986) Wild horses of the Great Basin: social competition

and population size. University of Chicago Press, Chicago

Burnham KP, Anderson DR (2002) Model selection and multimodel

inference: a practical information-theoretic approach. Springer-

Verlag, New York

Cote SD, Schaefer JA, Messier F (1997) Time budget and synchrony

of activities in muskoxen: the influence of sex, age, and season.

Can J Zool 75:1628–1635

DelGiudice GD, Mech LD, Seal US (1990) Effects of winter

undernutrition on body composition and physiological profiles

of white-tailed deer. J Wildl Manage 54:539–550

Demment MW, Van Soest PJ (1985) A nutritional explanation for

body-size patterns of ruminants and nonruminant herbivores. Am

Nat 125:641–672

Denzau G, Denzau H (1999) Wildesel. Thorbecke, Stuttgart

Duncan P (1992) Horses and grasses: the nutritional ecology of equids

and their impact on the Camargue. Springer, New York

Duncan P, Foose TJ, Gordon IJ, Gakahu CG, Lloyd M (1990)

Comparative nutrient extraction from forages by grazing bovids

and equids: a test of the nutritional model of equid/bovid

competition and coexistence. Oecologia 84:411–418

Edouard N, Fleurance G, Martin-Rosset W, Duncan P, Dulphy JP,

Grange S, Baumont R, Dubroeucq H, Perez-Barberıa FJ, Gordon

IJ (2008) Voluntary intake and digestibility in horses: effect of

forage quality with emphasis on individual variability. Animal

2:1526–1533. doi:10.1017/S1751731108002760

174 Oecologia (2012) 169:167–176

123

Fleurance G, Fritz H, Duncan P, Gordon IJ, Edouard N, Vial C (2009)

Instantaneous intake rate in horses of different body sizes:

influences of sward biomass and fibrousness. Appl Anim Behav

Sci 117:84–92. doi:10.1016/j.applanim.2008.11.006

Fortin D, Fryxell JM, Pilote R (2002) The temporal scale of foraging

decisions in Bison. Ecology 83:970–982

Fox JL, Nurbu C, Chundawat RS (1991) The Mountain ungulates of

Ladakh, India. Biol Conserv 58:167–190

Fryxell JM (1991) Forage quality and aggregation by large herbi-

vores. Am Nat 138:478–498

Giraldeau L-A, Caraco T (2000) Social foraging theory. Princeton

University Press, Princeton

Gross J, Shipley LA, Hobbs NT, Spalinger DE, Wunder BA (1993)

Functional response of herbivores in food-concentrated patches:

tests of a mechanistic model. Ecology 74:778–791

Hamel S, Cote SD (2007) Habitat use patterns in relation to escape

terrain: are alpine ungulate females trading off better foraging

sites for safety? Can J Zool 85:933–943

Hamel S, Cote SD (2008) Trade-offs in activity budget in an alpine

ungulate: contrasting lactating and nonlactating females. Anim

Behav 75:217–227. doi:10.1016/j.anbehav.2007.04.028

Hobbs NT, Gross JE, Shipley LA, Spalinger DE, Wunder BA (2003)

Herbivore functional response in heterogeneous environments: a

contest among models. Ecology 84:666–681

Illius AW (2006) Linking functional responses and foraging behaviour

to population dynamics. In: Danell K, Bergstrom R, Duncan P,

Pastor J (eds) Large herbivore ecology, ecosystem dynamics and

conservation. Cambridge University Press, New York, pp 71–96

Janis C (1976) The evolutionary strategy of the equidae and the

origins of rumen and caecal digestion. Evolution 30:757–774

Janis C, Ehrhardt D (1988) Correlation of relative muzzle width and

relative incisor width with dietary preference in ungulates. Zool J

Linn Soc 92:267–284

Jarman PJ (1974) The social organization of antelope in relation to

their ecology. Behaviour 48:216–267

Kaczensky P, Ganbaatar O, von Wehrden H, Walzer C (2008)

Resource selection by sympatric wild equids in the Mongolian

Gobi. J Appl Ecol 45:1762–1769. doi:10.1111/j.1365-2664.

2008.01565.x

Klingel H (1977) Observations on social organization and behaviour

of African and Asiatic Wild Asses (Equus africanus and Equushemionus). Zietschrift fur Tierpsychology 44:323–331

Laca EA, Ungar ED, Seligman N, Demment MW (1992) Effects of

sward height and bulk density on bite dimensions of cattle

grazing homogeneous swards. Grass Forage Sci 47:91–102

Laca EA, Distel RA, Griggs TC, Demment MW (1994) Effects of

canopy structure on patch depression by grazers. Ecology 75:

706–716

Laca EA, Shipley LA, Reid ED (2001) Structural anti-quality

characteristics of range and pasture plants. J Range Manage

54:413–419

Mani MS (1978) Ecology and phytogeography of high altitude plants

of the northwest Himalaya. Chapman and Hall, London

McNaughton SJ (1985) Ecology of a grazing ecosystem: the

Serengeti. Ecol Monogr 55:259–294

Moen J, Andersen R, Illius A (2006) Living in a seasonal ecosystem.

In: Danell K, Bergstrom R, Duncan P, Pastor J (eds) Large

herbivore ecology, ecosystem dynamics and conservation.

Cambridge University Press, New York, pp 50–70

Neuhaus P, Ruckstuhl KE (2002) The link between sexual dimor-

phism, activity budgets, and group cohesion: the case of the plain

zebra (Equus Burchelli). Can J Zool 80:1437–1441. doi:

10.1139/Z02-126

Okello MM, Wishitemi REL, Muhoro F (2002) Forage intake rates

and foraging efficiency of free-ranging zebra and impala. S Afr J

Wildl Res 32:93–100

Owen-Smith N (2002) Adaptive herbivore ecology. Cambridge

University Press, New York

Perez-Barberıa FJ, Nores C (1996) Grazing activity of breeding and

non-breeding female Cantabrian chamois (Rupicapra pyrenaicaparva). Ethol Ecol Evol 8:353–363

Perez-Barberıa FJ, Perez-Fernandez E, Robertson E, Alvarez-Enrı-

quez B (2008) Does the Jarman-Bell principle at intra-specific

level explain sexual segregation in polygynous ungulates? Sex

differences in forage digestibility in Soay sheep. Oecologia

157:21–30. doi:10.1007/s00442-008-1056-4

Pfister O (2004) Birds and mammals of Ladakh. Oxford University

Press, New Delhi

Rawat GS, Adhikari BS (2005) Floristics and distribution of plant

communities across moisture and topographic gradients in Tso

Kar basin, Changthang Plateau, Eastern Ladakh. Arctic Antarctic

Alpine Res 17:539–544

Rubenstein DI (1986) Ecology and sociality in horses and zebras. In:

Rubenstein DI, Wrangham RW (eds) Ecological aspects of

social evolution. Princeton University Press, Princeton,

pp 282–302

Rubenstein DI (1989) Life history and social organization in arid

adapted ungulates. J Arid Environ 17:145–156

Rubenstein DI (1994) The ecology of female social behaviour in

horses, zebras, and asses. In: Jarman P, Rossiter A (eds) Animal

societies: individuals, interactions and organisations. Kyoto

University Press, Kyoto, pp 13–28

Ruckstuhl KE (1998) Foraging behaviour and sexual segregation in

bighorn sheep. Anim Behav 56:99–106

SAS Institute Inc (2003) SAS/stat user’s guide. SAS Institute Inc,

Cary

Schaefer JA, Messier F (1995) Habitat selection as a hierarchy: the

spatial scales of winter foraging by muskoxen. Ecography

18:333–344

Schaller GB (1998) Wildlife of the Tibetan Steppe. The University of

Chicago Press, Chicago

Shipley LA (2007) The influence of bite size on foraging at larger

spatial and temporal scales by mammalian herbivores. Oikos

116:1964–1974. doi:10.1111/j.2007.0030-1299.15974.x

Shrader AM, Owen-Smith N, Ogutu JO (2006) How a mega-grazer

copes with the dry season: food and nutrient intake rates by

white rhinoceros in the wild. Funct Ecol 20:376–384

Spalinger DE, Hobbs NT (1992) Mechanisms of foraging in

mammalian herbivores: new models of functional response.

Am Nat 140:325–348

SPSS Inc (2002) SigmaPlot 8.0 user’s guide. SPSS Inc, Chicago

Stephens DW, Krebs JR (1986) Foraging theory. Princeton University

Press, Princeton

St-Louis A (2010) Ecologie du kiang au Ladakh: selection des

ressources, approvisionnement et comportement social d’un

equide meconnu du plateau tibetain. PhD dissertation, Depart-

ment of Biology, Laval University, Quebec, Quebec, Canada

St-Louis A, Cote SD (2009) Equus kiang (Perissodactyla: Equidae).

Mammalian Species 835:1–11. doi:10.1644/835.1

Sundaresan SR, Fischhoff IR, Duschhoff J, Rubenstein DI (2007)

Network metrics reveal differences in social organization between

two fission-fusion species, Grevy’s zebra and onager. Oecologia

151:140–149. doi:10.1007/s00442-006-0553-6

Therrien J-F, Cote SD, Festa-Bianchet M (2007) Conservative

maternal care in an iteroparous mammal: a resource allocation

experiment. Behav Ecol Sociobiol 62:193–199

Twine W (2002) Feeding time budgets of selected African ruminant

and non-ruminant grazers. Afr J Ecol 40:410–412

Van der Wal R, Madan N, Van Lieshout S, Dormann C, Langvatn R,

Albon SD (2000) Trading forage quality for quantity? Plant

phenology and patch choice by Svalbard reindeer. Oecologia

123:108–115

Oecologia (2012) 169:167–176 175

123

Van Soest PJ (1994) Nutritional ecology of the ruminant, vol 2nd.

Cornell University Press, Ithaca

Van Soest PJ (1996) Allometry and ecology of feeding behavior and

digestive capacity in herbivores: a review. Zoo Biol 15:455–479

Wilmshurst JF, Fryxell JM, Farm BP, Sinclair ARE, Henschel CP

(1999) Spatial distribution of Serengeti wildebeest in relation to

resources. Can J Zool 77:1223–1232

Wilmshurst JF, Fryxell JM, Bergman CM (2000) The allometry of

patch selection in ruminants. Proc Royal Soc London B 267:

345–349

Xu RH (2003) Measuring explained variation in linear mixed effects

models. Stat Med 22:3527–3541. doi:10.1002/sim.1572

176 Oecologia (2012) 169:167–176

123