1

1Vegetation recovery in response to the exclusion of grazing by sika deer

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(Cervus nippon) in seminatural grassland on Mt. Kushigata, Japan

3
4

Takuo Nagaike (Yamanashi Forest Research Institute, Japan)

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Eiji Ohkubo (Yamanashi Gakuin Junior College, Japan)

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Kazuhiro Hirose (Minami-Alps City Office, Japan)

78Corresponding author: Takuo Nagaike

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Yamanashi Forest Research Institute, Japan

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Saisyoji 2290-1, Fujikawa, Yamanashi 400-0502, Japan11

Tel +81 556 22 8001

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Fax +81 556 22 8002

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nagaike-zty@pref.yamanashi.lg.jp

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ABSTRACT

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We examined the recovery of vegetation in seminatural grassland in central Japan after

17

eliminating grazing by sika deer (Cervus nippon) by fencing. By 2012 after 5 years

18

fencing for exclusion of sika deer, the species composition of quadrats within the19

enclosure reverted to the original species composition in 1981, not browsed by sika deer.

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Conversely, that outside the fence was different from the baseline quadrats in 1981. Iris

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sanguinea, a prominent flower in the area, recovered within the enclosure, while it

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continued to decrease with grazing outside the fence. Nevertheless, the I. sanguinea

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cover had not recovered to 1981 levels in the enclosure. Fencing can effectively restore

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vegetation as the species composition within the enclosure gradually reverts to the225

original vegetation. Preventing grazing in intensively grazed seminatural grassland

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might lead to different successional pathways. Since I. sanguinea did not recover fully

27

within the enclosure and the species composition differed slightly from the original

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vegetation, this suggests that the vegetation within the enclosure will change to an

29

alternative state. Therefore, different management is needed to promote the correct

30

succession pathways for ecological restoration, perhaps by enhancing the colonization

31

of target species, to prevent restored sites from giving rise to alternative states.

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INTRODUCTION

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Traditionally, seminatural grasslands in Japan have been managed for grazing cattle and35

harvesting agricultural materials [e.g., fertilizer; 1]. However, most of these have been

36

abandoned with changes in lifestyle and farming methods [2], as in other countries [e.g.,373]. In Japan, forests cover 78% of the land area [4] and the mild, humid climate

38

promotes the growth of forests [5]. Consequently, abandoned grasslands are invaded by39

trees, and important for especially early successional species and species favoring open

40

habitats [e.g., 6]. So, such seminatural grassland has high priority to conserve biological41

diversity.

42

Recently, the population of sika deer (Cervus nippon) in Japan has increased

43

sharply [7, 8]. The effects of deer on natural grassland vegetation have been reported

44

worldwide [e.g., 9]. In Japan, deer have had serious effects in natural forest [10, 11],45

plantations [12, 13], and grasslands [14; 15]. Since sika deer prefer open habitat as46

foraging sites [16], patchy grasslands surrounded by forests are used heavily by sika

47

deer. Consequently, the plant species composition in the grasslands has been altered48

markedly by grazing sika deer.

349

On Mt. Kushigata (2053 m a.s.l. at the summit) in central Japan, seminatural

50

grasslands are distributed patchily with plantations and fragmented natural forests [17].

51

In the grassland, the flowers of Iris sanguinea and other meadow species (e.g.,

52

Veronicastrum japonicum) had been renowned. However, those flowers have been53

decreasing since 2000 because of grazing by sika deer. As countermeasures for the54

grazing, fences were set in the grassland in 2007. Fencing is effective for recovering

55

from herbivore grazing [18, 19] and promotes tree regeneration [20, 21]. The effects of56

grazing exclusion from seminatural grasslands on species richness [22] and spatial

57

patterns [23] have been studied. However, undesirable results, in which attempted at58

ecological restoration might lead to alternative states [24], can occasionally occur when

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fencing is used as a tool for conservation in overgrazed environments [25]. Therefore,

60

restoration efforts should be checked by comparing the results with the restoration target

61[3, 4].

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This paper presents the vegetation recovery pattern in seminatural grassland, in63

central Japan, after preventing grazing with fencing, addressing the questions can I.

64

sanguinea and a vegetation community recover to the original situation and community

65

before those were affected by sika deer?

66
67

METHODS

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Study site

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The study was conducted on Mt. Kushigata (2053 m a.s.l. at the summit), Yamanashi

70

Prefecture, in the cool–temperate zone of central Japan (35°35'N, 138°22'E). The mean

71

annual precipitation and temperature at the nearest meteorological station (Oizumi, 867

72

m a.s.l.) are approximately 1140 mm and 10.7°C, respectively. The estimated mean

473

annual temperature at the summit of Mt. Kushigata is about 3.5°C. Snow cover is74

usually less than 1 m.

75

On Mt. Kushigata, seminatural grasslands are distributed patchily with plantations

76

and fragmented natural forests [17]. The origin of the grassland is not clear, but

77

elevations in this region around 2000 m are typically dominated by subalpine coniferous

78

forests composed of Abies and Tsuga species. The grassland was probably the result of

79

human activity, such as mowing or burning. We studied the Hadakayama area of Mt.

80

Kushigata. Hadakayama means “naked mountain,” which indicates that this area has not

81

been covered by forest for a long time. The grasslands in the Hadakayama area are82

renown for the flowers of I. sanguinea. Over a 10-year period, however, the number of I.

83

sanguinea flowers has decreased, possibly as a result of natural succession from84

grassland to the typical subalpine coniferous forest. Grazing by sika deer was another85

potential reason. Therefore, fences to exclude sika deer were erected to prevent grazing86

in 2007.

87
88

Field study89

In July 1981, the science club of Koma High School studied the vegetation in the

90

Hadakayama area [6]. They set 32 1 × 1-m quadrats in the Hadakayama area typically91

dominated by I. sanguinea and applied the standard Braun–Blanquet scale: +, sparse92

cover; 1, cover <5%; 2, cover 5–25%; 3, cover 25–50%; 4, cover 50–75%; 5, cover93

75–100%. The species composition in 1981 is considered the original vegetation not

94

affected by grazing by sika deer.

95

In October 2007, we established a 20 × 20-m plot and fenced half of it (10 × 20

96m) to protect it from deer grazing. The quadrats set by Koma High School were 20 m

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from the plot. In June 2008, we established 20 1 × 1-m quadrats, 10 inside and 10

98

outside the fence, and conducted annual surveys from 2008 to 2012 using the99

Braun–Blanquet method. We counted the number of individuals of I. sanguinea in each100

quadrat every year.

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102

Analysis

103

Koma High School [6] did not list all rare species (i.e., species with low coverage in the104

quadrats studied). Therefore, we analyzed the species with coverage with a score >1 on

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the Braun–Blanquet scale.

106

We used nonmetric multidimensional scaling [NMS; 26] to provide an107

ecologically interpretable quantification of the compositional differences among

108

original vegetation (1981) and quadrats inside and outside the fence (2008-2012). NMS

109

applied Sørensen’s similarity index to calculate a distance matrix. We used the species

110

cover in each quadrat for NMS, after transforming the Braun–Blanquet scale

111

quantitatively. The data transformed to cover values (the midpoints of the cover112

intervals for each score) were used, i.e., scores of 1 to 5 were converted to the values

113

2.5%, 12.5%, 37.5%, 62.5%, and 87.5%, respectively [27]. NMS was performed using

114

PC-ORD [26].

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116

To show the recovery of I. sanguinea, we compared the number of individuals
and cover.

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RESULTS119

The recovery of I. sanguinea inside the fence was good, while outside the fence, it

120

decreased continuously with grazing (Fig. 1). The number of flowering I. sanguinea

6

121

also increased inside the fence to 25 in 2010, 198 in 2011, and 307 in 2012, while no122

flowers occurred outside the fence (unpublished data, Committee of Conservation of I.

123sanguinea at Mt. Kushigata). Nevertheless, the I. sanguinea cover had not recovered

124

fully compared to 1981 (Fig. 2).

125

The changes in the number of species inside and outside the fence showed126

contrasting trends (Fig. 3). The number of species increased inside the fence, but not127

outside it. The species composition differed markedly inside and outside the fence (Fig.

128

4). In 2008, most of the quadrats were located in the upper left position in the NMS

129

diagram. Then, the species composition of the quadrats within the fence shifted to the130

upper right position in the diagram, where the species composition in 1981 was located131(i.e., not browsed by sika deer). Conversely, the species composition of the quadrats

132

outside the fence was shifted to the lower right. Species that occurred in more quadrats

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inside the fence were Dianthus superbus var. longicalycinus, Phedimus aizoon var.

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floribundus, Serratula coronata, and Chamerion angustifolium as well as I. sanguinea

135(Table 1). Angelia pubescens, Veronicastrum japonicum, and I. sanguinea, which were136

categorized by tall herbs, were only dominated inside the fence. Brachypodium

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sylvaticum and Raunculus japonicas were less dominated before grazing, but were138

domnated after exclusion of sika deer. Outside the fence, Artemisia princeps initially139

dominated, and subsequently the graminoids Stipa pekinensis and B. sylvaticum, which

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appeared to be unpalatable, dominated.

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DISSCUSION

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Exclusion of sika deer by fencing were successfully recovering the cover and144

number of individuals of I. sanguinea because those outside the fence were

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continuously low. Thus, effects of grazing by sika deer were continuously severe. In

146seminatural grassland of northern Japan, Iris setosa dominated the most at sites grazed

147

by horses, which improved the surface soil characteristics [28]. In our study, sika deer148

grazed on I. sanguinea directly, causing serious damage. Thus, to conserve I. sanguinea,

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fencing seems necessary under the present circumstances. Since Tamura [29] showed

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that vegetation recovery, particularly tall herb species, was poor when fencing was151

delayed, it will be impossible for I. sanguinea to recover fully even if fences are erected

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now. However I. sanguinea would not recover fully compared to situation before

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grazing despite the fence.

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Fencing appeared to be effective at restoring the vegetation as the species

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composition in the fence gradually reverted to the original vegetation. Herbivores often,156

but not always, increase plant diversity in grasslands [30]. Outside the fence, however,157

since the species composition was altered and the number of species was low, intense158

grazing pressure by sika deer likely existed.

159

Rooney and Dress [31] showed that species with relatively lower abundance160

were more likely to be missing due to browsing than more abundant species. Actually,161

species with lower abundance in 1981 (e.g., Polygonatum odoratum, Ixeridium

162

dentatum, Hakomechlon macra) were not recover even after fencing. By grazing,163

tall-growing herb were reduced and lower-growing species were increased [32] and164

grazing-resisted species were shorter in height than grazing-susceptible species [33].

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Thus, tall herb species were easy to grazing and hard to recover after grazing.

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CONCLUSIONS

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Preventing grazing after intensive grazing of seminatural grassland might result in

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different successional pathways being followed and the species composition is slightly170

different from the original vegetation, this suggests that the vegetation inside the fence

171

will change to an alternative state [24]. Galvánek and Lepš [3] showed that the species

172

composition of the restored plots after the reintroduction of mowing was still far from173

the target composition. Therefore, different management methods are needed to ensure

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the correct succession pathways are followed for ecological restoration and to enhance

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colonization of the target species [34], rather than the restored site resulting in an

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alternative state [24]. Thus, other methods to restore the vegetation (e.g., remowing of

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unpalatable recalcitrant species, [35]) inside of the fence would be necessary. Moreover,178

as Wright et al. [36] suggested that complete removal of ungulates may be required for179

recovery in heavily browsed forest understory vegetation in New Zealand, control of180sika deer population should be required.

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ACKNOWLEDGEMENTS183

We thank members of committee of conservation of I. sanguinea on Mt. Kushigata, and184

Dr. Masako Kubo (Shimane University) and Dr. Hayato Iijima (Yamanashi Forest

185

Research Institute) for helping with the field study and Ms. Atsuko Hayashi (Forest and186

Forest Products Research Institute) for finding the references.

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Figure caption

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Fig. 1 Changes of mean number of individual of Iris sanguinea in each quadrat.

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Fig. 2 Changes of mean cover of Iris sanguinea in each quadrat.

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Fig. 3 Changes of mean number of species occurred in each quadrat.

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Fig. 4 Results of nonmetric multidimensional scaling (NMS) for species occurred in

193

each quadrat.

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200
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Fig.1

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*

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203
204
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Fig.2

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*

206
207
208
209

Fig.3

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＊1981
▲2008 inside△2008 outside▼2009 inside▽2009 outside●2010 inside○2010 outside◆2011 inside◇2011 outside■2012 inside□2012 outside

210
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Fig.4

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Table 1. Number of quadrats in species occurred. Total number of quadrats are 36 in "Before grazing", 10 in "Inside the fence" and 10
in"Outside the fence", respectively.
Species

Adenophora remotiflora
Adenophora triphylla
Agrostis clavata
Anaphalis margaritacea
Angelica pubescens
Aquilegia buergeriana
Arabis hirsuta
Arenaria serpyllifolia
Artemisia princeps
Astilbe microphylla
Brachypodium sylvaticum
Campanula punctata
Chamerion angustifolium
Cirsium gratiosum
Clinopodium chinense subsp. grandiflorum
Dianthus superbus var. longicalycinus
Dryopteris expansa
Filipendula multijuga
Fragaria nipponica
Geranium onoei
Gymnadenia conopsea
Hakonechloa macra
Iris sanguinea
Ixeridium dentatum
Jacobaea cannabifolia
Ligularia dentata
Malus toringo
Moehringia lateriflora
Oxalis corniculata
Phedimus aizoon var. floribundus
Picris hieracioides
Polygonatum odoratum
Polygonum cuspidatum
Potentilla freyniana
Ranunculus japonicus
Scabiosa japonica
Serratula coronata
Solidago virgaurea
Stipa pekinensis
Tephroseris flammea
Veronicastrum japonicum
Viola acuminata

212

Before grazing
1981
1
3

2008

Inside the fence
2009 2010 2011

2012

2008

Outside the fence
2009 2010 2011

2012

1
2
2

4
1
1

3
1

2

3

5
1

10

10

8

7

8

9

9

3

2

4

4

3

5

7
1

8

10

10

1

1

1

1

3

1

2

2

1

1

2

2

3

3

1

1

1
1

2
6
2
6

1
5

2
1

3

2

4
1

1
2
2
1

3
5

1
4
9

6

9

10

10

2

4

4

4

4
4
14
2
23
1
4
1
3

1

1
2
1
1

2

1
1

1
1
3
1
1
8
19
4

1

4
10

5
8
1

1
1
8
2

1

1
2

2

1

3
2
8
1
2

8
2
2

1

1
3
12

7

8

10

1
9
2

10
3

2

5

2

4

3

4

8
2
1

10
6

10
4

10
3