CHAPTER 5

SEASONAL HABITAT USE OF PERSIAN GAZELLES (Gazella

subgutturosa subgutturosa) BASED ON VEGETATION PARAMETERS AT

GOLESTAN NATIONAL PARK, IRAN

4.0 INTRODUCTION

The Persian gazelle (Gazella subgutturosa subgutturosa)

(Güldenstaedt 1780) is a sub-species of the Goitered

gazelle (G. subgutturosa) in the genus Gazelle, family Bovidae

and order Artiodactyla. This sub-species is distributed

from eastern Turkey to Iran, Pakistan, Turkmenistan and

Central Asia (Kingswood & Blank 1996). It is currently

categorized as Vulnerable (VU) and if conservation

efforts are not implemented for this species in the near

future, this could change to the Extinction (EX) category

(IUCN Red List 2013). One of the most important

ecological concepts in wildlife management is habitat

use, i.e., the interaction of animals with biotic and

abiotic parameters in their habitat. Theories or models

of habitat use strive to capture the essentials of

resource allocation by an organism and its implications

for fitness (Lawes & Nanni 1993). 1

The distribution and abundance of ungulate

populations are affected by the availability of food,

cover, and freestanding water (Dasmann 1971), as well as

high primary production and high biodiversity (Penka et

al. 1985) because these resources provide the basic

physiological and biological requirements of the ungulate

in the habitat. Also, the agricultural fields situated

near the habitat offer very specific conditions, which

can significantly influence the habitat use of animal

species living there (Prokesova et al. 2006; Kaplan

1994). Ward and Saltz (1994) concluded that feeding

behaviour of some species of gazelle can be changed

according to

2

environmental conditions during different seasons and

years; Junsheng et al (1999) reported that the food

availability of the Mongolian gazelle showed seasonal

changes; the plant biomass was higher in spring and

summer than that in autumn and winter. Food availability

and food choice are closely related to the feeding

strategy of forage plants; together they influence the

feeding behaviour, feeding type, and even social

organization of the ruminants (Geist 1974; Jarman 1974).

Radio telemetry, track count and direct observation

are methods commonly used to measure habitat use by large

ungulates. Radio telemetry can be expensive and needs

advanced transmitters and other equipment (Weckerly &

Ricca 2000). Track counts are not useful during the fall

and winter when the weather is unstable, rain and snow

are common, and lower temperatures tend to decrease the

activity of ungulates (Mooty et al. 1984). Direct

observation is time consuming and the results are rarely

accurate (Harkonen & Heikkila 1999). Pellet-group

counting is a more effective and less expensive method of

assessing habitat use (e.g., Sutherland 1996) as it does

not rely on technology and investment to capture, radio

track, or “camera trap” animals. However, pellet group

count has some disadvantages. The identification of each

species’ track and pellet is sometimes not reliable, and

the quantification of signs may be affected by the

species, sign features, substrate quality, weather, and

3

other factors influenced by habitat conditions and

seasonality (Rabinowitz 1993).

In other studies by Collins and Urness (1981), and

Andersen et al (1992) they reported that as the

defecation rates of animals varied due to different food

sources and activities throughout the year, pellet group

count cannot be a strong model to determine habitat use.

In spite of these impediments, pellet group count has

been a common method for assessing population trends and

habitat use of wild ruminants since the 1940s (Neff 1968;

Weckerly & Ricca 2000; Palmer & Truscott 2003). With this

method, the overall animal and pellet abundance are

monitored over several months with a concentrated

recording effort (Marques et al. 2001), and habitat

attributes, such as vegetation parameters are registered

simultaneously on the same spatial scale. The habitat

utilization data can be used in the management of

ungulate populations and their habitat essentials (Hemami

et al. 2004).

The pellet group count method has been widely used

to collect data on the habitat use of large herbivores

like elk, deer and moose throughout the whole world

(Guillet et al. 1995; Härkönen & Heikkilä 1999; Palmer &

Truscott 2003). However, only a few investigations have

been conducted on gazelles (Nowzari et al. 2007; Hazeri

et al. 2009). Thus, this study attempts to identify

habitat use by the Persian gazelle, using clearance

4

transect pellet group counts to identify the quantity and

quality factors of habitats in relation to habitat use

during seasons.

4.1 MATERIALS AND METHODS

4.1.1 Study Area

The Golestan National Park (GNP), covering an area of

91859 hectares, is located to the south-east of the

Caspian Sea (55° 43' to 56° 17' E, 37° 16' to 37° 31' N).

This park has been protected since 1957 because of its

valuable natural assets, such as a verdant and virgin

forest and diverse species of flora and fauna. Due to the

geographic location of the GNP, plant coverage can be

divided into two zones: the Hirkani forest in east

Alborz, and Iran-Toorani growth. The park includes

mountainous areas in the northern and western parts, and

undulating fields and plains in the eastern part. The

maximum and minimum elevations are approximately 2411 m

and 450 m respectively.

Persian gazelles live in the steppe habitats of the

GNP, scattered throughout the northern, southern and

eastern parts of the region (Figure 4.1). The main plant

cover includes thick shrubs, evergreens and annual

5

vegetation, which mostly belong to the Iran-Toorani

elements. Artemisia spp is the main endemic species of the

local vegetation. Parts of the GNP that feature this kind

of habitat have warm, dry summers and cold winters. The

average annual precipitation is 400 mm and the average

annual temperature varies between 11.5 ° to 17.5°° C. The

absolute minimum temperature is -25 °° C and the reported

maximum is 45 °°C.

6

Figure 4.1 Location of three gazelle habitats(Mirzabylou plain, Solegerd and Lohondur areas)at Golestan National Park. The green squares arevillages and farmlands around park

The density of shrub growth forms range from sparse

to dense thickets from Mirzabailo and its surrounding

area, to the southern part of the park, to the Dasht and

Almeh valleys, to the Sulgerd Mountains and to the

northern part of the park up to Lohondor. In some cases

these growths are associated with barberry shrubs, Rosa

sp. and Tamarix. Around the Almeh valley, the density and

7

variation of vegetation are higher. Artemisia spp annual

species and steppe communities provide good cover in the

hills and valleys, giving an expanded scrubland landscape

that is a suitable habitat for the wildlife species of

the park, such as gazelle, wild sheep and goats.

Among the three gazelle habitats at the GNP, the

Mirzabailo plain was selected as the main habitat because

it had a variety of vegetation types. This allowed the

determination of gazelle habitat use through vegetation

parameters (Table 4.1 and Figure 4.1). The map of

vegetation types was established during several field

visits to the habitat, using the topographic position,

vegetation structure, and direct (Figure 4.2). All

vegetation types were located in the plain areas that

have gentle topographic variation, mostly between 1000 m

and 1300 m elevation. The area covers a minor portion of

the park, has low soil erosion, so the soils are deep to

very deep and have good development. The soils of this

area include less than 15% of gravel. The best type of

texture is loam and its derivatives like clay loam or

sandy loam that can be found in this group of soils.

In order to assess the composition of each vegetation

type, in May 2009 plant surveys by random sampling of 1 m2

plots were used based on the Daubenmire (1959) method. A

general description of the vegetation in each sampling

plot was complied by using 4 plant growth forms; shrub,

8

annual grasses, perennial grasses and annual forbs. Each

vegetation type was defined based on at least two

dominant plant species which were identified using a

field guide and Flora of Golestan National Park (Akhani

et al.1999). Based on the description of the vegetation

in each plot, the study area was classified into 5 types

(Table 4.1). All the vegetation types were dominated by

shrub species mostly Artemisia herba-alba.

9

Table 4.1 Total number of transects and area of eachvegetation type of gazelle habitat in the study site inGolestan National Park

Gazellehabitat Vegetation type Area

(ha)

Numberof

Transects

I. Artemisia herba-alba / Eremopyrun bonaipartis /Anabasis aphylla/ Aellenia sp.

678.68 4

II. Artemisia herba-alba / Salsola rigida

968.63 5

Mirzabailo III. Artemisia herba-alba / Salsola vermiculata / Stipa barbata / Poa bulbosa

205.00

2

3

IV. Artemisia herba-alba / Eurotia ceratoides / Stipa barbata / Poa bulbosa

865.11 4

V. Artemisia herba-alba/ Aellenia sp. / Annual forb

847.70

0

4

Sulgerd IV. Artemisia herba-alba / Eurotia ceratoides / Stipa barbata / Poa bulbosa

759.00

2

-

Lohondor IV. Artemisia herba-alba / Eurotia ceratoides / Stipa barbata / Poa bulbosa

572.96 -

10

11

Figure 4.2 Map of the Mirzabailo plain, which is themain gazelle habitat at Golestan National Park.Monitoring transects were distributedproportional to the extent of the vegetationtypes. The blue symbols show the artificial watersources.

Vegetation types III and IV in the hilly terrain at

1300 m elevation were dominated by shrubs and perennial

grasses with 48% and 39% vegetation cover, respectively.

The dominant shrub species included Artemisia herba-alba, Salsola

vermiculata and Eurotia ceratoides. Of the grasses the main

species were Stipa barbata and Poa bulbosa.

12

Vegetation types II and V were located in the middle

of the habitat between 1100 m and 1200 m elevation. Type

II was dominated by the shrubs Artemisia herba-alba and Salsola

rigida and had 29% vegetation cover, while type V was

dominated by shrubs and annual forbs with 25% total

vegetation cover. Its dominant shrub species were Artemisia

herba-alba and Aellenia sp., while the main annual forbs are

Alyssum strigosum, Astragalus spp, Tragopogon longirostris, Trigonella

arcouta and Ziziphora tenuior (for more details see Appendix 1).

Vegetation type I in the low steppe area of the

habitat was located at less than 1100 m elevation near

the intercity road from Gorgan to Mashhad, which crosses

the reserve from east to west (Figure 4.2). It generally

had no more than 17% total vegetation cover, and most of

this part of the habitat had bare ground with salty,

white soil. Shrub species such as Artemisia herba-alba, Anabasis

aphylla and Aellenia sp were dominant here, while Eremopyrun

bonaipartis was the most dominant species of grass.

4.1.2 Gazelle Pellet-Group Survey

A total of 20 transects, each 3 m x 210 m were

established between 28th - 30th May 2010 on the Mirzabilo

plain and at the same time all the accumulated pellet

groups were removed from the transects. The size of the

transects was decided based on methods successfully used

in other gazelle habitats (Nowzari et al. 2007; Hazeri et

al. 2009) and the number of transects was proportional to

13

the area of the vegetation types (Table 4.1 and Figure

4.2). Transects were distributed by stratified random

sampling. The beginning and end of each transect was

marked using the Global Positioning System (GPS). In

order to achieve greater accuracy, each transect was sub-

divided using numbered wooden pegs into of 1.5 m x 30 m

segments (Nowzari et al. 2007; Hazeri et al. 2009).

Pellet-groups were counted in each segments and were then

removed.

In spring, gazelle pellets were separated into two

age groups, adults: male-female (1-1+ years old) and

fawns: male-female (0-1 year old). The size and shape of

the pellets for each age group were categorized by local

hunters assisting us based on diagnostic features. Feld

researchers had also received training at the Zoo and in

the field. We only recorded pellet groups with more than

five individual pellets, and any pellet-group at the edge

would be counted if more than half of it lay inside the

transect (Hemami et al. 2004; Nowzari et al. 2007).

Pellet group counts and clearance were completed at

two-monthly intervals due to the low decomposition rate

of the pellet groups in arid areas (Nowzari et al. 2007).

All signs of gazelles were removed from a transect at

each site visit. Accumulated pellet-groups within

transects were counted and removed between 29th - 31st

July, 29th September - 1st October, 28th - 30th November, 28th

14

February - 1st March, 27th - 29th April . In the winter,

because of harsh weather conditions, data collection had

to be postponed by one month.

4.1.3 Vegetation Parameters

Canopy cover, density, diversity, forage production and

forage quality (crude protein) comprised the vegetation

parameters, which were significant elements of habitat

quality (Mysterud et al. 1999). These were surveyed

simultaneously and on the same spatial scale as gazelle

signs in each transect (Table 4.1).

In each 1.5m x 30m transect segment, the percentage

cover of all plant species (perennial and annual) was

visually surveyed based on Daubenmire (1959) cover

classes. The species percentage cover data was used to

calculate the diversity within the vegetation types.

At each 3 m x 30 m transect area, a 1 m2 plot was

randomly sited behind the right shoulder of the observer

to measure the species density and forage production.

This sample size is deemed adequate for sampling shrubs

and grass in the study site and in other arid and semi-

arid environments. Species density was estimated by

counting individual plants in each plot. To determine

forage production, the edible parts of the plants, around

2.5 cm above ground were harvested by manual clipping.

15

This height represents a typical standing crop that has

been grazed by the gazelle during feeding (Nowzari et al.

2007). Clipped plants were weighed (wet weight) before

drying in an oven at 70° C for at most 48 hours and then

reweighed (dry weight). The dry matter of all plant

species was determined at different seasons. The total

number of pellet-groups and the mean vegetation

parameters were then calculated for each transect.

To consider of forage quality, plant samples were

collected at different seasons from the edible part of

shrubs, grasses and forbs. The samples selected as their

presence was dominant (i.e., they were the most common

species in the gazelle habitat based on Table 4.1) and

they were the most consumed food by gazelles (based on

personal direct observation and literature review).

Sighting records of the gazelle foods along

transects were made with the aid of a telescope at

bimonthly intervals. As a gazelle’s upper jaw does not

have any incisor or canine teeth as it separates the

leaves from the stems of plants, some skin will remain on

the intact parts, so plants eaten by the gazelle can be

recognized (Nowzari et al. 2007). Thus, direct

observations in the morning and at mid-day were used as a

secondary method besides the pellet-group count method

(Holechek et al. 1982; Rominger et al. 1988; Saltz & Ward

2000; Nowzari et al. 2007).

16

Besides primary field data, information from local

guides and the results of other studies of gazelles in

other regions were also utilized to compile a list of the

gazelle food plants and their seasonal availability in

the study area. A study of the food preferences in the

Khosh Yeilagh Wildlife Refuge by Mowlavi (1978) showed

that shrubs comprised 86% of their diet, followed by

grasses (11%), and forbs 3%. Analysis of the rumen

content of a female gazelle in the Ghamishloo Wildlife

Refuge in 1992 indicated that Salsola sp. was the most

common component of the diet, followed by grasses. In

southern Iran, they feed on shrubs, grasses, and forbs in

the winter and early spring, but browsing diversifies

during the rest of the year.

A variety of shrubs and grasses were selected in the

study area; Artemisia herba-alba, Salsola rigida, Salsola vermiculata,

Erotia ceratoidea, Anabasis aphylla, Stipa barbata, Poa bulbosa, Eremopyrun

bonaris and Allysum strigosum. Plant species for chemical

analysis were selected from different parts of the

habitat with three replicates at each phenological stage.

Plant samples were washed thoroughly dried for 72 hours

at 60°° C and ground using a 1 mm screen in a Wiley mill.

Crude protein was selected as an important indicator of

forage quality and was measured using the Kjeldahl method

(AOAC 2000).

17

4.1.4 Statistical Analyses

A normality test was done on data for frequency

distribution and homogeneity of variance. For statistical

analysis, Log10 was used to transform pellet group density

and a number of vegetation variables (production and

density) and square root transformation was used for

vegetation canopy cover.

Differences in the pellet group density and the

vegetation parameters (based on variables in Tables 4.3

and 4.4; Figures 4.3, 4.4 and 4.5) between vegetation

types and seasons were analyzed using one-way analysis of

variance [ANOVA]. Species diversity between vegetation

types was estimated with the Shannon-Wiener formula

(Krebs 1989). The difference between forage quality and

quantity in each season was analysed by one-way ANOVA and

the Kruskal Wallis test, respectively (Table 4.5 and

4.6).

The matrix data of pellet groups (as dependent

variable) and the canopy cover of all plant species (as

independent variable) were set at different seasons. The

stepwise regression model (forward selection) was then

used to determine which one of the plant species was

18

significantly associated with the density of gazelle

pellet groups in each season.

4.2 RESULTS

4.2.1 Pellet Group Analysis

The mean density of pellet groups in the 630 m2 transects

was compared between the five vegetation types using one-

way ANOVA. It was found that signs of gazelle presence

were not homogeneously distributed among the five

vegetation types (P<0.05) (Figure 4.3). In spring,

vegetation type I was highly used by adult gazelles (P =

0.004, F = 6.30) and vegetation type V was highly used by

fawns (P = 0.030, F = 3.60), while vegetation types III

and IV were used less by both age groups. In mid-summer

(P=1.11, F=0.39) and the end of summer (P = 1.51, F =

0.24) no significant difference was detected in the use

pattern of all vegetation types. In fall, both vegetation

types I and II were more preferred than vegetation type

III (P = 0.005, F = 5.73). In winter vegetation type II

was consumed more than vegetation types III, IV and V (P

= 0.011, F = 4.82). The overall values of the pellet

group accumulation indicated that gazelles ranged rather

uniformly over all the vegetation types within the

habitat (Figure 4.3). But, the field results showed that

the gazelles had a higher intensity of use of vegetation

19

types I and II followed by type V (P = 0, F = 9.97).

Moreover, although we identified a significant seasonal

difference in pellet group accumulation (P = 0.04, F =

2.51), but the high pellet density in all seasons showed

that gazelles use the steppe area of the GNP throughout

the year (Figure 4.4).

20

21

Figure 4.3 Mean ± s.d of Log transformed pellet group density accumulated in differentvegetation types and seasons by pellet-group clearance transects in the gazellehabitats of Golestan National Park. (A, B, C indicate difference or similarity of theparameter across vegetation types and seasons by Tukey Test).

22

Figure 4.4 Mean ± s.d of Log transformed pellet groupdensity accumulated at different seasons.

A significant relationship between the pellet-group

density and the square root transformed vegetation canopy

cover was recognized by stepwise regression (Table 4.2).

In spring, there were significant positive relationships

among Aellenia sp, Eremopyrun bonaris, and annual forbs with

the adult and fawn pellet group density. Significant

negative relationships were found between Stipa barbata and

adult pellet groups (P= 0, R2= 73.3%). These results

indicated a higher utilization of vegetation types I and

V. Conversely, lower use of vegetation types III and IV

were shown during the spring (Figure 4.3). In mid-summer

the gazelle pellet density had a positive significant

relationship with Aellenia sp and a negative significant

relationship with Salsola rigida and annual forbs (P= 0.034,

R2= 41%). At the end of the summer, there was a

significant negative relationship between Poa bulbosa, Stipa

23

barbata and pellet group density (P = 0.004, R2 = 47.8%),

that justified the lower usage of vegetation types III

and IV. In the fall and winter a significant positive

relationship was detected between Salsola rigida and pellet

group density, while a significant negative relationship

between pellet groups and Stipa barbata and Poa bulbosa was

found (in fall P= 0.035, R2=32.7%; in winter P=0.086,

R2=33%). This verified the higher use of vegetation type

II and lower use of vegetation types III and IV in cold

seasons. Despite the fact that Artemisia herba-alba was a

dominant species throughout the area, there was no

significant relationship between pellet group density and

canopy cover of this species during the various seasons.

24

Table 4.2 Step-wise forward multiple regressions between log transformed pellet-group densityand square root canopy cover for each season

Seasons Regression equationP R2

Spring Adult Y = 0.190 + 0.224 ER BO *+ 0.0778 AE SP - 0.0468 ST BA0.000 73.3%

Fawn Y = 0.145 + 0.0687 ER BO + 0.0715 AE SP + 0.128 AN FO0.002 60.5%

Mid-summerY = 1.24 + 0.0867 AE SP - 0.0393 SA RI - 0.0967 AN FO

0.034 41%

Late-summer

Y = 1.32 - 0.0554 PO BU - 0.168 ST BA0.004 47.8%

25

Fall Y = 1.17 - 0.169 PO BU + 0.0401 SA RI0.035 32.7%

WinterY= 1.34 - 0.0665 PO BU + 0.0363 SA RI - 0.166 ST BA

0.086 33.0%ER BO (Eremopyrun bonaipartis), AE SP (Aellenia sp), ST BA (Stipa barbata), AN FO (Annual forb), SA RI (Salsola rigida), PO BU

(Poa bulbosa).

26

4.2.2 Vegetation Parameter Evaluation

Canopy cover, diversity, density and forage production

are vegetation parameters which demonstrate significant

differences among seasons and vegetation communities

(P<0.05). As expected, the values of all vegetation

parameters were higher in the spring and mid-summer than

in other seasons (P<0.05; Table 4.3). Total forage

production, canopy cover and density were greater in

vegetation types IV, III and II than in the other

vegetation types, respectively. Moreover, a calculation

of Shannon’s diversity (H’) indicated that species

diversity was greatest (P<0.05) in vegetation type II

than in the other vegetation types (Table 4.4). Figure 6

shows the relative canopy cover of the main forage

species in each vegetation type (habitat) throughout one

year.

27

Table 4.3. Vegetation parameters (Mean ± [s.d.]) in five vegetation types during differentseasons. Log transformed vegetation variables were compared with One-way ANOVA (a, b, c,indicate difference or similarity of the parameter across vegetation types and seasons by TukeyTest)

Vegetationparameter

Spring Mid-Summer Late-Summer Fall Winter

Canopy cover, %(F=6.43, P=0.000,DF=4)

1.4576±[0.2415] A

1.1718±[0.2309] B

1.2571±[0.2599] AB

1.2600±[0.2801] AB

1.0314±[0.3409] B

Density(F= 16.76, P=0.000,

0.9181±[0.1416] AB

1.0276±[0.2007] A

0.7689±[0.1851] BC

0.6968±[0.1995] CD

0.5980±[0.2044] D

28

DF=4)

Production, gr/m2

(F= 31.67, P=0.000, DF=4 )

1.4057±[0.2638] A

1.1173±[0.1564] B

0.8290±[0.2292] CD

0.8594±[0.2876] C

0.6201±[0.2638] D

Table 4.4 ) The comparison of vegetation parameters (Mean ± [s.d.]) in five vegetationtypes/habitats. Log transformed vegetation variables were compared with One-way ANOVA (a, b, c,indicate difference or similarity of the parameter across vegetation types and seasons by TukeyTest).

Vegetationparameter

Vegetationtype IN= 40

Vegetationtype II N= 25

Vegetationtype IIIN=15

Vegetationtype IVN=20

Vegetationtype VN=35

0.9251±

29

Canopy cover, %(F=15.51, P=0.000,DF=4)

[0.3279]C 1.2661±[0.2718]AB

1.4598±[0.1403]A

1.4247±[0.1478]A

1.1507±[0.2242]B

Density(F=2.24, P=0.071,DF=4)

0.6703±[0.3398]B

0.8522±[.2211]A

0.7986±[0.0877]AB

0.8656±[0.1679]A

0.8092±[0.2523]AB

Production, gr/m2

(F=7.72, P=0.000,DF=4)

0.6757±[0.3218]C

1.0472±[0.3153]AB

1.1019±[0.3602]AB

1.1634±[0.2566]A

0.8570±[0.3437]BC

Diversity(P=0, DF=4 )

1.27C 1.15A 1.21B 1.6D 1.77E

30

31

Figure 4.5 Means ± s.d of relative canopy cover of each forage species at differentvegetation types in Golestan National Park (A, B, C indicate difference or similarityof the parameter across vegetation types and seasons by Tukey Test).

32

There were significant differences (P<0.05) in the

quantity and quality among species, season and the

species-season interaction. The results of Tables 4.5 and

4.6 show there were significant differences in the

quantity and quality among the dominant and edible plant

species in each season (P=0.00), which probably accounted

for the different use of vegetation communities by the

gazelles. In comparison to the other shrub species,

Artemisia herba-alba had a much higher production and less

crude protein while Anabasis aphylla had higher crude protein

and less production.

In spring, A. herba-alba, Salsola vermiculata and Eurotia

ceratoides have the most production while the level of crude

protein was higher in the shrubs as Anabasis aphylla and

Aellenia sp. In midsummer, S. rigida, A. herba-alba and Aellenia sp have

higher production but crude protein concentration is more

in A. aphylla and Aellenia sp. In endsummer, A. herba-alba, S. rigida and

Eurotia ceratoides have higher production amount while the

highest percentage of crude protein was accumulated in A.

aphylla and E. ceratoides. During fall and winter, A. herba-alba, S.

rigida, A. aphylla and E.ceratoides have high production rate but

crude protein was more concentrated in A. aphylla and S. rigida

(Table 4.5 and 4.6).

33

34

Table 4.5. Forage quantity [Average Rank] at differentseasons. Species forage productions in each season were

compared with Kruskal Wallis analysis.

Species Spring(P=0,DF= 10)

Mid-summer(P=0,

DF= 10)

Late-summer( P=0,DF=9)

Fall( P=0,DF=7)

Winter( P=0,DF=7)

ShrubsArtemisia.herba-alba

1 2 1 1 1

Salsola rigida 4 1 2 2 2Anabasisaphylla

9 4 6 3 4

Aellenia spp 6 3 7 7 7Eurotiaceratoides

3 10 3 4 3

Salsolavermiculata

2 5 9 8 8

GrassesPoa bulbosa 11 8 5 5 5Stipa barbata 5 7 4 6 6Eremopyrunbonaipartis

7 6 10 - -

ForbsAlyssumstrigosum

10 9 11 - -

Otherannualforbs

8 11 8 - -

---1 to 11 related to rank of speciesproduction from high to low, respectively.

35

Table 4.6 Forage crude protein (Mean ± [s.d.]) at different seasons. Percent of Crude proteinwas compared with One-way ANOVA (a, b, c, indicate difference or similarity of the proteinacross plant species by Tukey Test).

Species Spring(F= 79, P=0,

DF= 9)

Mid-summer(F=223.19, P=0,DF=

10)

Late-summer(F=43.94, P=0,

DF=9)

Fall(F=34.46, P=0,

DF=7)

Winter(F=34.46,P=0,DF=7)

Shrubs

Artemisia. herba-alba 15.98±1.40C 15.98±1.40C 12.55±0.74CD 8±0.57C 8±0.57C

Salsola rigida 17.80±0.48BC 17.80±0.48BC 14.06±0.60BC 11±0.015B 11±0.015B

Anabasis aphylla 28.60±0.13A 28.65±0.13A 22.04±2.36A 15.98±0.53A 15.98±0.53A

Aellenia spp 20.77±0. 47B 20.77±0.78B 14.34±0.08BC 8.92±0.35BC 8.92±0.35BC

Eurotia ceratoides 15.96±0.56C 15.96±0.56C 16.31±1.70B 7.83±0.17C 7.83±0.17C

Salsola vermiculata 11.89±1.48D 10.43±0.62D 7.48±0.61E 7.48±0.61C 7.48±0.61C

GrassesPoa bulbosa 17.36±0.39BC 5.77±0.61E 6.95±2.23E 6.33±2.23C 6.33±2.23C

Stipa barbata 18.33±1.27BC 9.49±1.01D 8±0.22E 8±0.22C 7.66±0.22C

Eremopyrun 11.28±1.48D 10.09±1.01D 9.44±0.17DE * *

36

bonaipartisForbsAlyssum strigosum 10.38±1.25D 9.70±0.61D 9.18±0.87DE * *other annualforbs ** 8.85±0.54D

** * *** no data available; *These species were absent during these seasons

37

4.3 DISCUSSION

4.3.1 Pellet Groups Analysis

Pellet group count was employed to consider the habitat

use of the Persian gazelle based on the vegetation

structure and nutritional content of dominant forages in

the steppe vegetation of the GNP. Nutrient content and

availability of forages have been identified as the main

parameters to determine the food selection and habitat

use patterns of ungulates . In the present study, food

quantity and quality have seasonal changes. The highest

nutritional content and forage availability were detected

in spring and the lowest levels identified during the

fall and winter. During cold seasons, nutrients and fiber

content are not as necessary for gazelles as in the

spring and summer (Sinclair 1975; Fryxell 1987). Thus,

the lack of sufficient food of high quality and quantity

would be the determinant factor in gazelle survival or

death during the cold seasons (Junsheng et al. 1999).

Gazelles are known to eat a variety of grasses,

forbs and shrubs during the different seasons (Olson et

al. 2010; Xu et al. 2012). During the calving period in

the spring, Persian gazelles feed mostly on

Chenopodiaceae, Gramineae and forbs, which comprised

38.8% to 85.1% of their diet (Karami et al. 2002;

Wenxuan et al. 2008). Moreover, in a previous study by

Vallentine (2000) as well as in this study a positive

38

relationship between the presence of these plant families

and gazelle densities was observed. In our study, annual

forbs and grasses generally had their highest production

and protein content in the spring, while their quantity

and quality factors decreased rapidly by the end of the

year and were below gazelle‘s requirements. Hence, it

seems the annual species should be selected by the

gazelle before they declined in nutrient content.

Therefore, habitat types I and V with higher abundance of

nutritional species like Aellenia sp, Eremopyrun bonaris and

annual forbs are the most suitable food sources for adult

and fawn gazelles in the spring. The presence of Annual

forbs and grasses was verified in the diet of the

goitered gazelle during spring, although they are

ubiquitous but not dominant in the gazelle habitat at the

GNP.

Summer is the driest season in the study area and

water sources and water stress condition are considered

to be a very important factor in the gazelle survey.

Despite the water sources being located in the upland

hilly terrain (type IV), even in the hot summer there was

no significant difference in the aggregation of pellet

groups in the upland areas compared to other parts of the

habitat. In another study on predicting habitat

suitability (Bagherirad et al. in press) we found that

gazelles were distributed more homogenously 10 km around

the water sources, which seemed a long distance for a

39

water-dependent species, such as the gazelle. Moreover,

in the current study, the results of step-wise forward

multiple regressions indicated significant positive

relationship between the pellet group density and the

cover of Aellenia sp, a species that was scattered but not

dominant in the study area. Therefore, a hypothesis can

be generated that in the summer there is no significant

difference in the pellet group densities among the

vegetation types due to the fact that the gazelles

searche all areas to find Aellenia sp. Our study results

indicate that Aellenia sp is the only green and hydrous

plant with 60% water content, which also has a high

production rate and protein content compared to the other

species. Moreover, in several direct observations of the

grazed plants, we found that mostly succulent species

like Aellenia sp were consumed by the gazelles during the

summer time. In agreement with these results, Williamson

and Delima (1991); Wenxuan et al (2008); Farhadinia et al

(2009) and Xu et al (2012) also reported that the

gazelles tended to obtain a considerable portion of their

water needs through the consumption of plants with high

water content. The importance of utilising succulent

plants during the dry season by gazelles has been

reported in some other studies throughout the world. For

instance, although the content of crude protein in Acacia

tortilis was low (4-5%), but the high water content (48-63%)

in this shrub species during the dry days of summer make

it the most selected by the dorcas gazelle (Grettenberger

40

1987), dama gazelle in Niger (Grettenberger & Newby

1986), and by dorcas gazelle in Israel (Baharav 1982).

Moreover, Baharav & Rosenzweig (1985) found that for

their survival during summer the dorca gazelles made more

attempt to optimize water intake rather than energy and

protein intake, which is probably similar for the

goitered gazelle in the GNP during the challenging season

by making use of succulent shrubs such as Aellenia spp.

Gazelles are territorial animals and this behaviour

is partly related to their reproductive activity. The

mating behaviour of the Persian gazelle takes place from

September through November in the study area. During the

mating season the pellet group density is similar in all

the habitat types, which is probably because the male

gazelles become more territorial and keep other males out

of their territory. Gazelles defend their territory by

leaving pellets and urine in parts of their habitat. As a

result, each area is occupied by the territorial male and

their females.

during the fall and winter generally the nutritional

quality and quantity of the forage species decreased and

were below the gazelle’s nutritional need for herbaceous

plants. In addition, annual herbaceous plants were

removed from the habitat by intensive grazing and only

the permanent species remained. During the fall the

percentage of protein in grasses was 4-5%, which is too

41

low for nutritional maintenance (the lowest acceptable

level is 7%). In shrubs the preference level drops to

only 8% in winter, thus bushes sustain more nutrition

than grasses (Kaplan 1995; Beck & Peek 2005). The

deficiency in nutritional quality is simultaneous with

mating and pregnancy in the fall, when more food with

high levels of protein and energy are needed. Thus, the

positive relationship between canopy cover of Salsola rigida

and pellet group density in the cold seasons is

significant because of the higher production and protein

content in shrubs compared to grass species such as Stipa

barbata and Poa bulbosa. Similar to livestock, the gazelle

might avoid grazing grass species because of the hard

awns and silvery silky plumes of Stipa barbata in the

seeding season, as reported by Moghaddam (1998).

It is interesting to note that, there was not any

significant relationship between the pellet group density

and canopy cover of shrubs such as Artemisia herba-alba and

Anabasis aphylla, although these browse are dominant species

with high nutritional quality rather than the herbaceous

types. Although habitat type I was used by the gazelles

during the fall and winter, there was no significant

relationship between the pellet groups and the associated

plant species by stepwise forward multiple regressions,

even with dominant species such as Artemisia herba alba and

Anabasis aphylla. However, in other studies, it has been

documented that Artemisia herba-alba is a dominant species in

42

gazelle habitats (Mowlavi, 1978; Mallon & Kingswood,

2001; Olson et al. 2010; Xu et al. 2012) and more was

consumed during the fall and winter after rain, when its

toxic components had been washed off (Olson et al. 2010).

Most of the shrub species such as Anabasis aphylla have

secondary plant components that are seldom consumed by

gazelles during the growing season as they contain high

levels of toxic substances such as antimicrobial and

antioxidant phenolic compounds, terpenoids, saponins, and

alkaloids (Jia, 1987; Shakeri, 2012). However, it is the

most preferred plant food in the winter, with consumption

more that six times than in the fall (Xu et al. 2012).

Hence, the hypothesis can be suggested that the high

density of gazelles in type I during the fall and winter

might be related to a high density of shrub species such

as Artemisia herba-alba and Anabasis aphylla or the proximity of

farmlands to the south of their habitat. The cultivated

lands with a plentiful supply of palatable and green

crops that are very rare in the wild habitat during the

cold season, seem to be a good choice and reliable food

source for the free ranging wildlife. In earlier studies,

Kaplan (1995) reported that the analysis of stomach

contents of Mongolian gazelles showed they preferred more

bushes and shrubs in the autumn season, while Baharav &

Rozenzweig (1985) also reported a significant

relationship between shrub density and the presence of

Dorcas gazelles in winter.

43

The current results of habitat use surveyed over one

year indicated that although the Persian gazelles used

all vegetation types, habitats I and II were the most

favoured and habitats III and IV were the least favoured.

Types I and II were the most suitable habitats because of

the higher density of annual forbs and grasses like

Asteragalus sp, Bromus tectorum, Trigonella arcouta, and Eremopyrun

bonaipartis; and shrub species such as Artemisia herba-alba,

Anabasis aphylla, Salsola rigida Aellenia sp, as they are high

quantity and quality food sources. Additionally, the

proximity of habitat type I to agricultural activity that

apparently offered food sources with high protein content

and artificial water sources would also attract gazelles

throughout the year. Based on interviews with several

farm owners and villagers, they complained that the

gazelles encroach into farmland from fall through spring

due to the existence of palatable and green crops such as

wheat and wild alfalfa.

The lower use of habitat types III and IV might be

explained by less density of main food sources such as

annual forbs, Eremopyrun bonaipartis, Aellenia sp, Anabasis aphylla

and Salsola rigida; and the higher density of low nutritional

quality forages such as Stipa barbata and Poa bulbosa. The

protein content of Poa bulbosa falls below the minimum

maintenance requirement (7%); and the protein content of

Salsola vermiculata, the dominant species in habitat III, falls

below the minimum requirement (14%) for fawn survival, as

reported by Murphy & Coates (1966). As previously

44

discussed, the main limiting factors for the low presence

of gazelles in the upland areas were the absence of their

main food resources and the deficiency in the quality of

indicator plant species. Notably, other limiting factors

might be the uneven rocky grounds of vegetation types III

and IV and the presence of wild carnivores such as

leopards and wolves.

The habitats of gazelles at the GNP are composed of

various plant species and families. As a result of these

high resource levels small herbivores like the gazelle

would be more selective (Westoby 1974; Belovsky 1978).

Since the gazelles are small ruminant ungulates with a

relatively low daily forage consumption of around 1

kg/day (Karami et al. 2002), they may be forced to

fulfill their need for protein and energy from a low

volume of forages. Furthermore, they are also endothermic

animals with a smaller body size that requires more

metabolic energy . As their energy requirements are

relatively high and they have a low rumen volume , the

Persian gazelle has to be selective in both the quantity

and quality of its food resources. There are two theories

on food choice of ruminants. The first is by Bell (1971)

who worked with large ungulates in Africa and found that

the body weight of ruminants is an important factor in

their food habits. As opposed to large ungulates, small

ruminants are more selective and choose highly

nutritional plants. In other words, low rumen content in

45

small ruminants is an important factor for selecting

digestive plants with low fibre content such as forbs and

shrubs (Hanley 1982). The second theory was established

by Jarman (1974) whose focus was on the availability and

distribution of forages as important variables in the

feeding behaviour of ungulates. The results of our study

showed that more annual forbs and grasses were consumed

by gazelles in the spring when the former were both

abundant and nutritious. Shrub species were preferred as

the main and dominant food source in the study area

throughout the year, especially in the fall and winter,

when the annual herbaceous plants were not available.

Therefore, the findings of this study are in line with

points of view suggested by Bell and Jarman, indicating

that both availability and quality of food resources are

important in the habitat selection of small ungulates

such as the gazelle.

the high density of gazelle pellet groups

accumulated at different seasons indicated that the

steppe areas of the GNP are suitable habitats for the

Persian gazelle throughout the year. The accumulation of

different amounts of pellets during each time period

surveyed could be related to patterns of gazelle habitat

use in the study area (which cannot be determined by this

method) or a to variation in the gazelle defecation rate

or level of activity in different periods of the year. As

indicated by Nowzari et al (2007) the lowest pellet

46

densities in the gazelle habitat were recorded during the

mating season, when the male gazelles feed less but spent

more time defending their females.

Comparative results between seasons also showed that

the values of vegetation parameters were low in the

winter, but the high pellet group density during this

season was a good indication that the plains of the GNP

are a particularly suitable habitat for the gazelles

during the fall and winter seasons.

4.4 CONCLUSION

Many types of habitat may occur within a home range of an

animal, but gazelles may utilize only a few of these

available patches. Preference for certain habitat types

can be due to food preferences, diversity, presence of

toxic plants, high safety factors, water sources, cover,

or other factors. However, during the one year study of

the gazelle’s habitat parameters, it was found that they

are selective ungulates with seasonal changes in their

habitat use patterns. Overall, several direct

observations besides pellet group counts confirmed that

the gazelles focus more on habitat type II, which was

characterized by the highest species diversity, density

and canopy cover with high nutritional forage quantity

and quality. Moreover, this habitat type was located in

47

the middle of their habitat, and a safe distance from the

hilly terrain and villages. With respect to the low

population of leopards and cheetahs in the steppe

vegetation area of the GNP, it seems the gazelles are

most at risk by poachers in the adjacent villages,

especially when the gazelles graze cultivated farms from

the fall to spring. Therefore, less use of upland areas

(habitat types III and IV) seemed more related to

insufficient forage quality, which in some dominant

forage species was measured and found to be less than the

minimum requirement for the gazelles.

The importance of food diversity, nutrient quality

and quantity in habitat use by small ungulates may be

related to a response to the requirement for a wide

variety of food in order to enhance foraging performance

in small ruminants. Thus, the prominent presence of

gazelles in those habitats with higher plant quality and

greater diversity can be attributed to the quality of

feeding sites, and indicate that as selective ungulates

they have more chance to select better food in their

natural habitats. In the open plains, because of high

visibility, the risk of poaching is minimized and there

is a strong increase in the forage efficiency of

gazelles. Due to the fact there is no conflict between

feeding efficiency and the risk of poaching, the safest

places could also increase the feeding efficiency of this

48

ungulate. As a result, the gazelles only select safe

places and there is no tradeoff between these factors.

Appendix I. List of plant species in steppe habitats of

Golestan National Park, under gazelle grazing

Species Family Duration*

Growthform

Life form**

Palatability***

Aellenia sp Salsolaceae

P shrub CH III

Alyssum strigosum Brassicaceae

A Forb TH III

Anabasis aphylla Salsolaceae

P Shrub CH III

Arabis nova Brassicaceae

A Forb TH III

Artemisia sieberi Asteraceae P Shrub CH II

49

Astragalus tribuloides Fabaceae A Forb TH IIIAstragalus brividens Fabaceae A Forb TH IBromus tectorum Poaceae A Grass TH IICapsella bursa-pastoris Brassicace

aeA Forb TH III

Carex stenophylla Cyperaceae P Forb HE IIIConsolida orientalis Ranunculac

eaceA Forb TH III

Delphinium biternatum Ranunculaceace

A Forb TH III

Cousinia bakhtiarica Asteraceae P Forb HE IIIEremopyrun bonaipartis Poaceae A Grass TH IIIEromostachys boissieriana Lamiaceae P Forb HE IIIEuphorbia characias wulfenii

Euphorbiaceae

A Forb TH III

Eurotia ceratoides Salsolaceae

P Shrub CH II

Gagea reticulata Liliaceae P Forb GEO IIIJeraenium eriantum Geranniace

aA Forb TH II

Lathyrus latifolius Fabaceae A Forb TH IIIorobanche gracilis Orbancheac

eA Forb EPY III

Papaver pavonicum Papaveracea

A Forb TH III

Roemeria hybrida Papaveracea

A Forb TH III

Peganum harmala Zygophillaceae

P Forb HE III

Poa bulbosa Poaceae P Grass GEO IIRapistrum rugosum Brassicace

aeA Forb TH II

Salsola kali Salsolaceae

A Forb TH III

Salsola rigida Salsolaceae

P Shrub CH I

Salsola vermiculata Salsolaceae

P Shrub CH III

Salvia nemorosa Lamiaceae P Forb HE IIISenecio vulgaris Asteraceae A Forb TH IIStachys inflata Lamiaceae P Forb HE IIIStipa barbata Poaceae P Grass HE IITragopogon longirostris Asteraceae P Forb HE ITrigonella arcouta Fabaceae A Forb TH ITulipa wilsoniana Liliaceae P Forb GEO IIIVeronica persicum plantagina

ceaeA Forb TH III

Ziziphora tenuior Lamiaceae A Forb TH III

50

Zosimia absinthifolia Apiaceae P Forb HE IIIZygophyllum atriplicaides Zygophilla

ceaeP Bush PH III

* A: annual plant P: perennial plant

**Plant species were split into seven groups based on morphology(life form) and life span. The groups included: Phanerophyte (thesurviving buds or shoot apices are borne on shoots, which projectedinto the air), Chamaephyte (a perennial plant that sets its dormantvegetative buds just at or above the surface of the ground), Hemi-cryptophyte, Cryotophyte, Geophytes (a perennial plant that propagates byunderground bulbs or tubers or corms), Therophyte (plants completedtheir life cycle from seed to seed and died), Epiphyte (Kreps, 2001).*** Palatability class: I = high palatable; II = medium palatable;III = low-unpalatable (Bagherirad et al., 2012).

51