An Occasional Journal of the Nodai Ent. Lab.

Nodai Entomology (3): 1-7 (2022)

N ODAI E NTOMOLOGYISSN 2435-3965 (Online)© Nodai Entomological Laboratory
https://www.nodai.ac.jp/agri/original/konken/shigen/publication/publication.html

Butterfly diversity in a vineyard developed from abandoned orchards
Koichi TANAKA 1) & Yoshinobu KUSUMOTO 2)
1) Laboratory of Entomology, Tokyo University of Agriculture, 1737 Funako, Atsugi, Kanagawa, 243-0034 Japan

E-mail: kt206540@nodai.ac.jp
2) Division of Hilly and Semi-Mountainous Area Farming Research, Western Region Agricultural Research Center, NARO,

2575 Ikano-cho, Zentsuji, Kagawa, 765-8508 Japan

Abstract A vineyard was developed from abandoned orchards in Koshu-shi, Yamanashi Prefecture,
Central Japan, in 2017. To investigate the effect of development of abandoned farmland on biodiversity
and evaluate the biodiversity in Japanese vineyards, we surveyed butterflies in this vineyard from 2016
to 2022. The species richness and diversity index of butterflies were low in 2016, before the vineyard
was developed. After 2018, the butterfly diversity increased as vineyard vegetation became richer andmore abundant. Argyronome laodice japonica, a vulnerable species, was observed in 2021 and 2022. This
study was the first to evaluate the biodiversity in a Japanese vineyard; it revealed that the developmentof vineyards from abandoned orchards is effective for the conservation of butterflies.
Biodiversity loss continues despite substantial ongoing efforts for biodiversity conservation andsustainable use (Secretariat of the Convention on Biological Diversity, 2020) and an average ofapproximately 25% of species in assessed animal and plant groups are threatened (IPBES, 2019). In
Japan, biodiversity loss has recently been remarkable in agroecosystems (Hidaka, 1998; Katoh et al.,2009). The traditional agroecosystem "satoyama", commonly known as SEPLS (socio-ecologicalproduction landscapes and seascapes), conserves biodiversity while providing various resources
including food, fuel, and building materials (The International Partnership for the Statoyama Initiative,2022). However, abandonment of farmland has threatened to cause biodiversity loss of various taxa inagroecosystems in Japan as well as worldwide (Koshida & Katayama, 2018), and as a result, a numberof species inhabiting satoyama are now endangered (Hidaka, 1998; Katoh et al., 2009; Ministry ofEnvironment, 2020). Restoration of abandoned farmlands is expected to recover biodiversity.
Many studies have evaluated the biodiversity of plants and arthropods in vineyards in Europe,
the United States of America, and the Republic of South Africa (e.g., Nicholls et al., 2001; Kehinde &Samways, 2014; Cohen et al., 2015; Burgio et al., 2016). In contrast, no study has investigated vineyard
biodiversity in Japan.
Yamanashi Prefecture ranks first in grape production in Japan (Ministry of Agriculture, Forestry
and Fisheries, 2022). In particular, Koshu-shi is well known for producing wine-brewing and tablegrapes.
Mercian Corporation (a wine maker), Kirin Holdings, developed a vineyard from abandoned
orchards in Koshu-shi, in 2017. An investigation of changes in biodiversity caused by vineyard
development could elucidate the effect of abandoned farmland development on biodiversity andevaluate the biodiversity status in Japanese vineyards. To address these objectives, we started surveyof plants and insects in this field in 2016, just before the vineyard was developed. We chose butterflies
as an indicator insect taxon for the following reasons. Butterflies depend on plants; the larvae of mostbutterfly species feed on specific species or groups of plants and the adult butterflies suck flower nectar
or tree sap. Thus, butterflies are suitable indicators of vegetation types and quality. In addition, it iseasy to identify butterfly species. This paper shows and discusses the changes in butterfly diversity
after the vineyard development.
Accepted 22 November 2022; published 9 December 2022
Licensed under a Creative Commons Attribution License CCBY 4.0

2

Nodai Entomology, (3): 1-7

Materials and Methods
Study area
The vineyard, named "Tenguzawa vineyard",
was developed from abandoned orchards at anelevation of 820–860 m in Kamiodawara, Koshushi, Yamanashi Prefecture, Central Japan, in 2017.
These orchards mainly included peach and plumtrees and were abandoned sometime around 1990.
In 2016 before the vineyard development, grasses
dominated in this area, and trees including
chestnut (Castanea crenata Siebold et Zucc.), oak(Quercus acutissima Carruth.), and pine (Pinus
densiflora Siebold et Zucc.) grew sparsely (Fig. 1).
In a wide region of Yamanashi Prefecture
including the study area, the sika deer Cervus
nippon Temminck, 1838 has caused serious
damage to vegetation (Iijima et al., 2013; Iijima &Nagaike, 2015). Consequently, dominant weeds
were unpalatable plants for sika deer, i.e.,
Pennisetum alopecuroides (L.) Spreng., Miscanthus
sinensis Andersson (Hashimoto & Fujiki, 2014),
and Cirsium vulgare (Savi) Ten. (Tazaki et al., 2014).
In addition, heavy grazing and stamping of sika
deer resulted in patches of bare ground where
Oxalis corniculata L. and O. dillenii Jacq. invaded.
The Tenguzawa vineyard covers an area ofapproximately 50,000 m2, consisting of several
terraced fields because it is located on a slope. To
protect grapevines from sika deer, the vineyard
was enclosed with 2.3 m-high wire-mesh fencing.
The grapevines were cultivated using a training
system of vertical shoot positioning on a verticaltrellis. In each terraced field, a margin of 4 –8 msurrounded the vine rows to allow farmmachinery to pass. The white clover (Trifolium
repens L.) and pasture grasses (Festuca arundinacea
Schreb., Poa pratensis L., and Lolium perenne L.)
were planted on the field margins and between thevine rows as ground cover plants, whereas herbs
and grasses were planted on the slopes between
fields. These plants were sparse in 2018 and grewdenser annually (Fig. 2).

Fig. 1. Study area of abandoned orchards in2016 before the Tenguzawa vineyard wasdeveloped.

2018

2022
Fig. 2. Study area of the Tenguzawa vineyardin 2018 and 2022.

Survey methods
Butterflies were censused in July 2016 (before the vineyard development) and May, June, July, andSeptember as a rule from 2018 to 2022 (after the vineyard development). However, in 2020, no surveys
were carried out in May and June because the national government declared a state of emergency for
the Kanto district including Kanagawa Prefecture owing to pandemic of the COVID-19 (coronavirus

TANAKA & KUSUMOTO (2022) —Butterfly diversity in a vineyard

3

disease 2019). The survey dates were July 25, 2016; May 19, June 23, and July 29, 2018; May 11, June 16,
and September 20, 2019; July 22 and September 24, 2020; May 14, June 21, July 12, and September 14,
2021; and May 12, June 27, July 18, and September 21, 2022. The censuses were conducted between 9:00
to 16:00 on fine days by Tanaka alone. It took 2.5–3.0 h to census the entire vineyard. Butterflies wereidentified and counted by direct observation, observation through field glasses, or by capture with an
insect net on the field margins and the slopes between the fields. To evaluate the butterfly diversity,
species richness and the Shannon-Wiener diversity index (H') were calculated.
Results
A total of 35 species of butterflies were observed for six years (Table 1). In 2021 and 2022,
Argyronome laodice japonica (tribe Argynnini), a vulnerable species in the Japanese Red List 2020
(Ministry of the Environment, 2020) was identified. The species richness (number of species) andnumber of individuals of butterflies observed by each census are shown in Table 2 and 3, respectively.
Table 1. Butterfly species observed in the Tenguzawa vineyard in 2016–2022
FamilySpecies

Japanese name2016 2018 2019 2020 2021 2022

Hesperiidae
Erynnis montana montana (Bremer, 1861)
Isoteinon lamprospilus lamprospilus C. Felder et R. Felder, 1862
Ochlodes venatus venatus (Bremer et Grey, 1852)
Pelopidas mathias (Fabricius, 1798)
Parnara guttata guttata (Bremer et Grey, 1852)
Papilionidae

ミヤマセセリ

Papilio xuthus Linnaeus, 1767
Papilio dehaanii dehaanii C. Felder et R. Felder, 1864
Pieridaeアゲハ
カラスアゲハ●Eurema mandarina mandarina (de l'Orza, 1869)
Colias erate poliographa Motschulsky, [1861]
Pieris rapae crucivora Boisduval, 1836
Pieris melete Ménétriès, 1857
Pieris nesis japonica Shirôzu, 1952
Lycaenidae

キタキチョウ●●●Curetis acuta paracuta de Niceville, 1902
Arhopala japonica (Murray, 1875)
Japonica saepestriata saepestriata (Hewitson, [1865])
Antigius attilia attilia (Bremer, 1861)
Lycaena phlaeas chinensis (C. Felder, 1862)
Lampides boeticus (Linnaeus, 1767)
Zizeeria maha argia (Menetries, 1857)
Everes argiades argiades (Pallas, 1771)
Celastrina argiolus ladonides (de l'Orza, 1869)
Nymphalidae

ウラギンシジミ

Libythea lepita celtoides Fruhstorfer, [1909]
Argyronome laodice japonica (Ménétriès, 1857)
Argynnis paphia tsushimana Fruhstorfer, 1906
Nephargynnis anadyomene ella (Bremer, [1865])
Fabriciana adippe pallescens (Butler, 1873)
Argyreus hyperbius hyperbius (Linnaeus, 1763)
Limenitis camilla japonica Menetries, 1857
Neptis sappho intermedia W. B. Pryer, 1877
Polygonia c-aureum c-aureum (Linnaeus, 1758)
Kaniska canace nojaponicum (von Siebold, 1824)
Inachis io geisha (Stichel, 1908)
Vanessa cardui (Linnaeus, 1758)
Ypthima argus argus Butler, 1866
Minois dryas bipunctata (Motschulsky, [1861])

テングチョウNo. of species●●●

ホソバセセリコキマダラセセリ●

チャバネセセリ
イチモンジセセリ

モンキチョウ
モンシロチョウ

●●●スジグロシロチョウ

●
●
●
●

●
●
●

●

●
●
●

●

●
●

●
●

●
●
●
●

●
●
●
●

●
●
●
●
●

●

●
●
●

●
●
●
●
●

●
●
●
●
●
●
●
●
●
●
●

ヤマトスジグロシロチョウ

ムラサキシジミ
ウラナミアカシジミ
ミズイロオナガシジミ

●
●

●
●

ベニシジミ
ウラナミシジミ●

ヤマトシジミツバメシジミ

●
●

●
●
●
●

●
●
●
●

ルリシジミ

●

●
●

●

●
●

●
●

●
●
●
●
●
●
●
●
●

●
●
●
●
18

●
●
●
19

●
●
●
●
28

ウラギンスジヒョウモン●

ミドリヒョウモン
クモガタヒョウモン
ウラギンヒョウモン
ツマグロヒョウモン

●
●

●
●

イチモンジチョウ
コミスジ
キタテハ

●

●
●

●

ルリタテハ
クジャクチョウ
ヒメアカタテハ
ヒメウラナミジャノメ
ジャノメチョウ

35

●
●
13

●
●
●
●
13

●
●
●
30

4

Nodai Entomology, (3): 1-7

The species richness in July was low in 2018, a year
Table 2. Butterfly species richness (number
after the vineyard establishment; however, itof species) in the Tenguzawa vineyard
subsequently increased and was higher in 2020–
Year May June July Sep. Total
2022 than it was before the vineyard was
2016
––
––
13
––
13
established. In May, June, and September, the
2018
6
6
7
––
13
species richness of butterflies tended to increase
2019
3
10
––
12
18
2020
––
––
16
13
19
annually. On the other hand, the number of
2021
10
14
15
16
28
butterfly individuals did not consistently increase
2022
9
13
18
18
30
nor decrease although it fluctuated annually––:
Surveyswerenotcarriedout.
(Table 3).
The Shannon-Wiener diversity indices (H') of butterflies are shown in Table 4. Because the species
richness was low in May (Table 2), the index was not calculated for this month. The lowest H' wasobserved in July 2016 and the H' became higher annually as well as the species richness. The H' in July
2016 was lower than that in June and July 2018 although the species richness in July 2016 was higher
than that in June and July 2018. In July 2016, two dominant species, i.e., Zizeeria maha argia (109individuals) and Minois dryas bipunctata (85 individuals) accounted for 89% of a total of 218 butterfly
individuals observed (Table 3). After 2018, in addition to these two species, two pierid species, i.e., Colias
erate poliographa and Eurema mandarina mandarina, became dominant (Table 3).
Table 3. Number of butterfly individuals
observed in the Tenguzawa vineyard

Table 4. Butterfly diversity index (ShannonWiener H’) in the Tenguzawa vineyard

Year May June
July
Sep.
2016
––
––
––
218 (109, 85, 1, 9)1)
2018
19
50
95 (35, 7, 3, 25）
––
2019
23
98
––
136
2020
––
––
194 (27, 44, 31, 33)
245
2021
58
64
89 (30, 9, 18, 5)
249
2022
59
129
122 (15, 13, 31, 17)210––: Surveys were not carried out.
1) The figures in the parenthesis (Z, M, C, E)
indicate the numbers of individuals of Zizeeria
maha argia (Z), Minois dryas bipunctata (M), Colias
erate poliographa (C), and Eurema mandarina
mandarina (E).

Year
June
July
2016
––
1.182
2018
1.469
1.488
2019
1.822
––
2020
––
1.979
2021
1.958
2.115
2022
1.874
2.315
––: Surveys were not carried out.

Sep.
––
––
1.851
1.702
1.944
2.120

Discussion
This study was the first to evaluate the biodiversity of the Japanese vineyard by surveying
butterflies. In the abandoned orchards surveyed in 2016, prior to vineyard development, the species
richness of butterflies was low, and especially the diversity index (the Shannon-Wiener H') was low.
The observed low diversity index was due to dominance of two species, Z. maha argia and M. dryas
bipunctata. Heavy grazing by sika deer caused poor vegetation in the abandoned orchards where
unpalatable plants for sika deer (i.e., P. alopecuroides, M. sinensis, and C. vulgare) were dominant, andOxalis plants were abundant in patches of bare ground. Oxalis and M. sinensis are the host plants of Z.
maha argia and M. dryas bipunctata, respectively. Thus, the dominance of a few plant species due to thesika deer grazing resulted in the dominance of two butterfly species and low butterfly diversity.
In 2018, a year after the vineyard development, vegetation was poor in the vineyard, and thereafter
became richer annually. As vegetation became richer, the species richness and diversity index ofbutterflies increased. In addition, a vulnerable species, Argyronome laodice japonica, was identified in

TANAKA & KUSUMOTO (2022) —Butterfly diversity in a vineyard

52021 and 2022. The tribe Argynnini, which includes this species, is representative taxon of grasslands,
and its host plants are members of a genus Viola, such as V. grypoceras A. Gray and V. verecunda A. Gray.
Although five Argynnini species (Argyronome laodice japonica, Argynnis paphia tsushimana, Nephargynnis
anadyomene ella, Fabriciana adippe pallescens, and Argyreus hyperbius hyperbius) were observed in thevineyard, they were not abundant. Surveys in the area surrounding the vineyard showed that the Viola
plants were not abundant there. This low abundance of Viola plants was certainly ascribed to grazing
by sika deer, which may have caused low populations of the Arginnini butterflies. In the vineyard, Viola
plants were not seen until 2020 but were observed in 2021 and increased in 2022. In addition, a final
instar larva of Argyreus hyperbius hyperbius was found within the vineyard on September 21, 2022.
Argyreus hyperbius hyperbius has rather different biology from other Arginnini species; its habitat
includes residential areas and the larvae feed on decorated Viola cultivars (pansies) as well as wild Violaspecies unlike other Arginnini species depending on wild Viola species. However, the finding of the
Arginnini larva which has grown in the vineyard suggests that Arginnini butterflies including A. laodica
japonica will inhabit the vineyard when Viola plants become more abundant. Arginnini butterflies
visited the flowers of Taraxacum officinale Weber et F. H. Wigg., Erigeron annuus (L.) Pers., and Erigeron
philadelphicus L. in the vineyard. These plants were scarce outside the vineyard, while their abundancein the vineyard increased during the study period. This observation indicates that the vineyard
provides nectar resources for butterflies. In addition, many bees, such as Apis mellifera Linnaeus, 1758,
visited flowers of T. repens. Kratschmer et al. (2019) demonstrated that increasing floral resources andreducing vegetation management promoted wild bee diversity and abundance in the European
vineyards. These observations suggest that the vineyard also had an important function of providing
nectar and pollen resources for pollinators.
This study revealed that the Tenguzawa vineyard provides habitats for insects, as observed inplants and arthropods in vineyards of Europe, the United States of America, and the Republic of South
Africa (e.g., Nicholls et al., 2001; Kehinde & Samways, 2014; Cohen et al., 2015; Burgio et al., 2016). This
result indicates that developing vineyards from abandoned orchards is effective for conservation
butterflies, particularly grassland butterflies. Grasslands, especially semi-natural grasslands, havedrastically decreased in Japan (Ogura, 2010); consequently, many species of plants and animals
inhabiting grasslands are endangered (Nakamura, 2011; Ministry of Environment, 2020). Thus,
farmlands such as the vineyards developed from abandoned orchards are certainly important toconserve the grassland-dwelling species. However, research evaluating the vineyard biodiversity inJapan is lacking. Therefore, further studies are needed to investigate vineyard biodiversity in otherregions and taxa.
要 約
田中幸一・楠本良延：耕作放棄果樹園から造成したワイン用ブドウ園におけるチョウ類の多様性．———— 2017 年に山梨県甲州市において，耕作放棄された果樹園からワイン用ブドウ園が造成された．
耕作放棄地を農地に造成することが生物多様性に及ぼす影響を調査すること，また日本のブドウ園における生物多様性を評価することを目的として，造成されたブドウ園において，2016 年から 2022 年までチョウ類の調査を行った．造成前の 2016 年には，チョウ類の種数および多様度指数は低かった．
2018 年以降は，ブドウ園の植生が豊かになるにつれて，チョウ類の多様性が増加した．2021，2022 年には，絶滅危惧種であるウラギンスジヒョウモンが確認された．本研究は，日本のブドウ園における生物多様性を評価した最初のものであり，耕作放棄果樹園をブドウ園に造成することが，チョウ類の保全に有効であることを示した．
Acknowledgments
We thank T. Tamura, Y. Yoshida, and Y. Sonoda of Château Mercian; K. Fujiwara, Y. Okamoto, Y.
Okonogi and C. Okimura of Kirin Holdings for allowing us to conduct field surveys and providing

6

Nodai Entomology, (3): 1-7

information of vine culture. This study was financially supported by Kirin Holdings.
References
Burgio, G., E. Marchesini, N. Reggiani, G. Montepaone, P. Schiatti & D. Sommaggio, 2016. Habitat
management of organic vineyard in Northern Italy: The role of cover plants management onarthropod functional biodiversity. Bulletin of Entomological Research, 106: 759-768.
Cohen, M., C. Bilodeaub, F. Alexandrec, M. Godronb, J. Andrieud, E. Grésillonb, F. Garlattib & A.
Morgantib, 2015. What is the plant biodiversity in a cultural landscape? A comparative, multi-scale
and interdisciplinary study in olive groves and vineyards (Mediterranean France). Agriculture,
Ecosystems and Environment, 212: 175-186.
Hashimoto, Y. & D. Fujiki, 2014. List of food plants and unpalatable plants of sika deer (Cervus nippon)in Japan. Humans and Nature, 25: 133-160. (In Japanese.)
Hidaka, K., 1998. Biodiversity conservation and environmentally regenerated farming system in paddy
fields. Japanese Journal of Ecology, 48:167-178. (In Japanese.)
Iijima, H. & T. Nagaike, 2015. Appropriate vegetation indices for measuring the impacts of deer onforest ecosystems. Ecological Indicators, 48: 457-463.
Iijima, H., T. Nagaike & T. Honda, 2013. Estimation of deer population dynamics using a Bayesian statespace model with multiple abundance indices. The Journal of Wildlife Management, 77: 1038-1047.
IPBES, 2019. Global Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity andEcosystem Services, Brondízio, E. S., J. Settele, S. Díaz & H.T. Ngo (eds). 1144 pp. IPBES Secretariat,
Bonn.
Katoh, K., S. Sakai & T. Takahashi, 2009. Factors maintaining species diversity in satoyama, a traditional
agricultural landscape of Japan. Biological Conservation, 142: 1930-1936.
Kehinde, T. & M.J. Samways, 2014. Effects of vineyard management on biotic homogenization of insect–
flower interaction networks in the Cape Floristic Region biodiversity hotspot. Journal of Insect
Conservation, 18: 469-477.
Koshida, C. & N. Katayama, 2018. Meta-analysis of the effects of rice-field abandonment on biodiversity
in Japan. Conservation Biology, 32: 1392-1402.
Kratschmer, S., B. Pachinger, M. Schwantzer, D. Paredes, G. Guzmán, J.A. Goméz, J.A. Entrenas, M.
Guernion, F. Burel, A. Nicolai, A. Fertil, D. Popescu, L. Macavei, A. Hoble, C. Bunea, M.
Kriechbaum, J.G. Zaller & S. Winter, 2019. Response of wild bee diversity, abundance, andfunctional traits to vineyard inter-row management intensity and landscape diversity acrossEurope. Ecology and Evolution, 9: 4103-4115.
Ministry of Agriculture, Forestry and Fisheries, 2022. https://www.maff.go.jp/j/tokei/kekka_gaiyou/sakumotu/sakkyou_kajyu/nasi_budou/r3/index.html. (Published 15 February 2022. Last cited
29 September 2022.)
Ministry of Environment, 2020. The Japanese Red List 2020. https://ikilog.biodic.go.jp/Rdb/booklist.
(Last cited 29 September 2022.)
Nakamura, Y., 2011. Conservation of butterflies in Japan: status, actions and strategy. Journal of Insect
Conservation, 15: 5-22.
Nicholls, C.I., M. Parrella & M.A. Altieri, 2001. The effects of a vegetational corridor on the abundanceand dispersal of insect biodiversity within a northern California organic vineyard. LandscapeEcology, 16: 133-146.
Ogura, J., 2010. Historical studies of grasslands in Japan. Japanese Journal of Grassland Science, 56: 216219. (In Japanese.)
Secretariat of the Convention on Biological Diversity, 2020. Global Biodiversity Outlook 5. 208 pp.
Secretariat of the Convention on Biological Diversity, Montreal.
Tazaki, F., M. Miyaki, H. Toda & Y. Miyake, 2014. Vegetation response and development of theTANAKA & KUSUMOTO (2022) —Butterfly diversity in a vineyard

7vegetation index on grassland by experimental density manipulations for sika deer (Cervus nippon
yesoensis H.) at Cape Shiretoko. Journal of the Japanese Society of Revegetation Technology, 39: 503-511.
(In Japanese with English abstract.)
The International Partnership for the Statoyama Initiative, 2022. https://satoyama-initiative.org/. (Lastcited 29 September 2022.)