Journal of Asia-Pacific Entomology 16 (2013) 415–419

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Journal of Asia-Pacific Entomology

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Short Communication

Occurrence and distribution of the grape rust mite Calepitrimerus vitis(Nalepa, 1905) in Korea

Myoung Rae Cho a, Jong-Ho Lee b, Sung-Wook Jeon a, Taek Jun Kang a, Hyeong Hwan Kim a,Chang Yeol Yang a, Seung-Joon Ahn a,⁎a National Institute of Horticultural & Herbal Science, RDA, Suwon 441-440, Republic of Koreab Department of Plant Quarantine, Animal, Plant and Fisheries Quarantine and Inspection Agency, Anyang 430-016, Republic of Korea

⁎ Corresponding author. Tel.: +82 31 290 6229; fax:E-mail addresses: massai94@hanmail.net, massai@ko

1226-8615/$ – see front matter © 2013 Korean SocietyAll rights reserved.http://dx.doi.org/10.1016/j.aspen.2013.05.005

a b s t r a c t

a r t i c l e i n f o

Article history:Received 12 February 2013Revised 16 April 2013Accepted 21 May 2013

Keywords:Grape rust miteCalepitrimerus vitisTaxonomyOverwinterDistribution

The grape rust mite, Calepitrimerus vitis, was identified from grapevines firstly in Korea. In the spring of 2011,symptoms characterized by the retarded growth of young shoots and flower buds in the grapevine werereported by local farmers in Hwaseong, Gyeonggi province of Korea. A large number of the small, white,and longitudinal mites were observed both on the twig surfaces and the overwintering buds. The mite wasidentified as Calepitrimerus vitis (Nalepa) (Acari: Eriophyidae) by morphological observations under both amicroscope and scanning electron microscope (SEM). Nationwide surveys in 2011–2012 were conductedto figure out the distribution of the mite, revealing that the mite was widely distributed in the grape pro-duction area in Korea both in greenhouse and in open field vineyards. Interestingly, the mite density wasmuch higher in Hwaseong, a middle-west coast of Korea, with several hundred mites per overwinteringbud. However, no significant damage was observed from the sprouting season to the harvest time, exceptfor the retarded growth of shoot and flower buds in the early season. The morphological characteristics ofC. vitiswith SEMmicrographs and the survey results in major grape production areas in Korea are reportedherein.© 2013 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection

Society. Published by Elsevier B.V. All rights reserved.

Introduction

The grape rust mite, Calepitrimerus vitis (Nalepa), is known as one ofthe major pests of grapevine in the world including Germany, France,Spain, Switzerland, Italy, Brazil, Australia, and the USA (Bernard et al.,2005; Prischmann and James, 2005; Walton et al., 2007; Duso et al.,2010). This mite has been recognized as an obligate pest of Vitis plantsincluding V. vinifera L., V. riparia Michx, and Vitis sp.

The grape rust mite is known to be associated with typical symp-toms in grapevine: the restricted spring growth (RSG) syndrome in-cludes leaf and shoot distortions and retarded shoot growth in earlyspring (Bernard et al., 2005) and the short shoot syndrome (SSS)causes bunch necrosis, malformed leaves, short and angled shoots inspring leading to scarred tissue and bronzed leaves in summer(Walton et al., 2007). Both of the symptoms ultimately cause signifi-cant yield losses at harvest, therefore the mite is regarded as an eco-nomically important pest. In addition, eriophyid mites where thegrape rust mite belongs to can cause serious implications for cropproduction, therefore being considered as a quarantine pest in manycountries (Lindquist et al., 1996).

+82 31 290 6256.rea.kr (S.-J. Ahn).

of Applied Entomology, Taiwan Ent

There was no report on eriophyid mites occurring in grapevines inKorea. In 2011, however, damage symptoms probably caused by themite were observed at a greenhouse-grown grapevine in Hwaseong,Gyeonggi province. Here, we report the occurrence of the mite atvineyards in Korea for the first time, with descriptions on the mor-phological characteristics together with electron microscopy, damagesymptoms, and nationwide surveys on its distribution in Korea.

Materials and methods

Observation of the damage symptoms by the grape rust mite

The mite damage symptoms were observed at a greenhouse-growngrapevine in Hwaseong, Gyeonggi province, in April 2011. Damagesymptoms by the putative mite infestation were carefully investigatedon-site and photographs were taken of the shoots and flower buds inthe mite-infested grapevine. Damaged twigs were brought to the labo-ratory, examined under stereomicroscope (SteREO Discovery. V8, CarlZeiss, Germany) with 20× magnifications to identify the presenceof the mite, and photographed with a CCD camera (DP450, DeltaPix,Denmark) connected to the stereomicroscope. Additional visits to thefarm were done in August and October for further observations of thedamage symptoms.

omological Society and Malaysian Plant Protection Society. Published by Elsevier B.V.

416 M.R. Cho et al. / Journal of Asia-Pacific Entomology 16 (2013) 415–419

Morphological characteristics and scanning electron microscopy of thegrape rust mite

The mite was collected from the infested grapevine, and processedfor slide preparation according to the Keifer's method (Keifer, 1952a).The morphometric characteristics were examined under differentialinterference contrast microscope (Nikon Optiphot-2, Japan). Draw-ings were done using a drawing tube. The number was expressed inpositive numbers and the value was expressed in micrometers. Thetaxonomic characters were recorded based on the specimens previ-ously collected from other grape production areas in Korea (Gwangju,Jeollanam-do and Yeongdong, Chungcheongbuk-do; 1999 to 2001).The mites were dehydrated and processed by a critical point dryerfor scanning electron microscopic observation. Morphological char-acters were observed and photographed using a scanning electronmicroscope (Hitachi S-2460N, Japan).

Surveys on the distribution of the grape rust mite in Korea

Field surveys were conducted for two years (2011 and 2012) on thedistribution of the grape rust mite at major grape production areas inKorea. The nationwide surveys included 106 vineyards from 28 differ-ent locations distributed in 5 provinces. Ten twigs were randomly

Fig. 1. Damage symptoms infested by the grape rust mite. Infested (A) and normal (B) flowedormant bud (E) and the scanning electron micrograph (F) of the grape rust mite.

selected from each vineyard and were brought to the laboratory. Eachtwig was carefully examined under stereomicroscope (SteREO Discov-ery. V8, Carl Zeiss, Germany) by observing the stem surface anddissecting dormant buds to check the presence of the mite. Whendetected, the number ofmiteswas counted from the 3–4 buds per twig.

Results

Damage symptoms of the grape rust mite

When compared to healthy ones, the damaged grapevines hadshorter shoots and smaller flower stalks (Fig. 1A and B). No visiblecolor difference, however, was observed on shoots or buds. So, itseemed too difficult for unexperienced farmers to distinguish themfrom undamaged ones. A bunch of white-colored mites were ob-served at the damaged shoots and flower buds under the stereomi-croscope (Fig. 1C). It was finally identified as the grape rust mite,Calepitrimerus vitis (See below). As the grapevine grew, the visiblesymptom was no longer observed and the mite was not detected onthe mature leaves or stems of the infested grapevines. However, thegrape rust mite was identified again on the surface or inside of thedormant buds in the twigs sampled from the farm after the harvest

r bud stalks; the grape rust mite on the stem surface (C) and on the bud surface (D); the

417M.R. Cho et al. / Journal of Asia-Pacific Entomology 16 (2013) 415–419

season (Fig. 1D, and E). Sometimes, hundreds of mites were observedinside the buds.

Morphological characteristics and scanning electron microscopy of thegrape rust mite

The morphological characteristics of the grape rust mite,Calepitrimerus vitis (Nalepa) are as follows.

Calepitrimerus vitis (Nalepa, 1905) (Korean name: podo-nok-eung-ae)(Fig. 2)

Phyllocoptes vitis Nalepa, 1905a, Anz. Kais. Akad. Wiss. Math.-NaturKl. Wien. 42(16): 268 (TL: Austria; TH: Vitis vinifera L.).Epitrimerus vitis Nalepa, 1905b, Anz. Kais. Akad. Wiss. Math.-NaturKl. Wien. 42(25): 445.Calepitrimerus vitis (Nalepa): Keifer, 1952b, Bull. Calif. Insect Survey2(1): 57.

DiagnosisThis species differs from others by bilobed frontal lobe, upward

scapular setae, relatively shorter middorsal ridge than lateral ridges,and 4-rayed empodia.

Female (Protogyne)Body fusiform, 170–190 long, 50–52 wide. Gnathosoma directed

down, 20–25 long. Prodorsal shield broadly triangular, 33–36 long,38–43 wide; frontal lobe overhanging gnathosoma, bilobed; prodorsal

Fig. 2. Calepitrimerus vitis (Nalepa). CG: coxigenital region; D: dorsal mite; EM:empodia; IG: female internal genitalia; LM: lateral mite; LO: lateral opisthosoma, L1:leg I; L2: leg II; MG: male genitalia.

shield with median and admedian lines and granular lateral lines;dorsal tubercles ahead of rear margin; setae directed up and centrad.Dorsal annuli 67–72, slightly less than ventral annuli, 70–74, terminalannuli 5; three-fourths of dorsal annuli with middorsal ridge; dorsalannuli lobed dorsally and with faint, elongate, rounded micro-tubercles touching rear annular margins laterally. Ventral annuliwith small rounded microtubercles touching rear annular margins.Setae h1 present, 5 long. Coverflap with 2–3 transverse granularlines basally, 10–12 longitudinal ridges, setae 13–14 long. Coxaewith granulation, sternal line simple and faint. Empodia 4-rayed;tarsal solenidia knobbed.

Female (Deutogyne)Present, slight smaller than protogyne, 150–170 long, 55 wide;

opisthosoma without dorsal ridge; dorsal annuli smooth withoutmicrotubercles; ventral annuli with microtubercles in the middlearea, but faint and few.

MalePresent, smaller than female, 146–158 long, 45–50 wide.

Materials examined5♀, 9♂ (Coll.#990805-1), Gwangju, Jeollanam-do (JN),

5.vii.1999, Jong-Ho Lee, on Vitis vinifera L.; 9♀[2 deutogyne], 2♂(Coll.#0100928-1), ditto, 28.ix.2001, Jeong-Woo Seo, on V.vinifera L.; 16♀[15 deutogyne], 1♂ (Coll.#010924-1), Yeongdong,Chungcheongbuk-do (CB), 24.ix.2001, Dong-Soon Kim, on V. viniferaL.; 20♀ (Coll. #110429-1), Jebu, Hwaseong, Gyeonggi-do (GG), 29.iv.2011, Myoung-Rae Cho, on V. vinifera L.

Host plantsVitis riparia Michx., V. vinifera L., and Vitis sp. (Vitaceae).

Damage symptomVagrant on lower leaf surface, sometimes making shorter shoots

and flower stalks. It was also known to cause leaf rust (Keifer, 1952a).

DistributionKorea (GG, CB, JN); Japan; Austria, Czechoslovakia, France, Germany,

Greece, Hungary, Italy, Moldova, Portugal, Rumania, Slovenia, Spain,Switzerland, Yugoslavia, USSR; Canada, USA; Brazil; Australia, NewZealand.

Scanning electron microscopic observation on the grape rust miterevealed the characteristic shapes of annuli and prodorsal shield(Fig. 1F). The dorsal annuli had faint and round microtubercles. Theprodorsal shield was broadly triangular, and the frontal lobe wasoverhanging gnathosoma. The prodorsal shield had median andadmedian lines and granular lateral lines.

Distribution of the grape rust mite in Korea

The grape rust mite was widely distributed in Korea, includingHwaseong, Anseong, Cheonan, Okcheon, Yeongdong, Gimcheon,which are major areas of grape production in Korea (Table 1 andJ.-H. Lee's collections). Among them, an unusually high occurrenceof the grape rust mite was observed in Hwaseong, Gyeonggi province.On the other hand, no mite was observed at several regions, includingGimpo, Suwon, Boeun, and a couple of survey locations in Anseong,Cheonan, and Sangju.

Discussions

We report the first identification of the grape rust mite,Calepitrimerus vitis (Nalepa), in Korea, with a description of its dam-ages to shoots and flower buds of the grapevine resulting in the re-tarded growth in spring. Calepitrimerus vitis is one of the important

Table 1Survey on the occurrence of the grape rust mite, Calepitrimerus vitis (Nalepa), in themajor grape production areas in Korea. Ten twigs from each farm were randomly col-lected and brought to the laboratory. The number of mites was counted from individualbuds at each twig from 10 randomly-collected twigs from each farm.

Province Region Location Year No.farmsa

Densityb

Gyeonggi-do Pocheon Soheul-eup 2012 4/5 ++Gapyeong Sang-myeon 2011 1/1 +Gimpo Tongjin-eup 2012 0/5 −Hwaseong1 Gwangpyung-ri 2011 8/8 ++++Hwaseong2 Sangan-ri 2011 3/5 +++Hwaseong3 Jangoe-ri 2011 3/5 +++Hwaseong4 Maehwa-ri 2011 5/5 ++++Hwaseong5 Jeongok-ri 2011 3/6 +++Ansan Daebu-do 2012 3/5 +Suwon1 Top-dong 2011 0/1 −Suwon2 Imok-dong 2011 0/2 −Anseong1 Gongdo-eup 2011 2/5 +Anseong1 Gongdo-eup 2012 0/1 −Anseong2 Seoun-myeon 2012 1/3 +

Chungcheongnam-do Cheonan1 Seonggeo-eup 2011 1/5 +Cheonan1 Seonggeo-eup 2012 0/3 −Cheonan2 Ipjang-myeon 2012 0/5 −

Chungcheongbuk-do Boeun1 Maro-myeon 2012 0/1 −Boeun2 Tanbu-myeon 2012 0/1 −Okcheon Dongi-myeon 2011 3/5 ++

Jeollabuk-do Jeonju Deokjin-dong 2011 2/5 +Gimjae Baekgu-myeon 2011 1/5 +

Gyeongsangbuk-do Gimcheon Bongsan-myeon 2011 3/5 +Sangju1 Hwadong-myeon 2012 4/4 +Sangju2 Hwaseo-myeon 2012 0/4 −Sangju3 Hwanam-myeon 2012 0/3 −Sangju4 Moseo-myeon 2012 1/1 +Sangju5 Modong-myeon 2012 2/2 +

a a/b, Number of farms where the grape rust mite observed (a) per surveyed (b).b Average density (mites/bud) of the grape rust mite at each location surveyed (3–4

buds, 10 twigs per farm). Density index: +, 1–50 mites; ++, 50–100 mites; +++,100–200 mites; ++++, 200–500 mites.

418 M.R. Cho et al. / Journal of Asia-Pacific Entomology 16 (2013) 415–419

grapevine pests all over the world including the USA (Prischmannand James, 2005), South America (Reis et al., 1998), Europe (Dusoand de Lillo, 1996), South Africa (Dennill, 1986), Iran (Xue et al.,2009) and Australia (Bernard et al., 2005). In Asia, the mite wasrecorded only in Japan (Ehara, 1995), but not in other countries. Itwas revealed that the grape rust mite presents in Korea, throughoutall the provinces where the host plant, grapevine, is grown as one ofthe major fruit trees. Among 106 vineyards located in 28 grape pro-duction locations surveyed for two years, the mite occurred at atotal of 50 vineyards (47.2%) in 18 locations (64.3%), indicating thatthe mite has already been spread throughout Korea and settleddown in the major grape production areas (Table 1). The grape rustmite-infested grapevines showed a retarded shoot and flower devel-opment (Fig. 1), which is similar to the symptom known as ‘Restrict-ed Spring Growth (RSG)’ detected in a number of Australianvineyards. RSG is associated with leaf and shoot distortions and re-tarded shoot growth in early spring caused by the grape rust mitefeeding (Bernard et al., 2005). Similarly, ‘Short Shoot Syndrome(SSS)’ was reported in the Pacific Northwest of the United States asa cause of malformed leaves, and short and angled shoots in spring,and wounded tissues and bronzed leaves in summer resulting in se-vere crop losses due to high population densities of the grape rustmite (Walton et al., 2007; Petanović and Kielkiewicz, 2010). Howev-er, no visible symptom or no mites were observed when the infestedvineyards in Hwaseong were revisited in summer. According to thelocal farmer, acaricides had been applied twice in April and Mayafter the first observation of the symptom in April. Not only thespraying, but conventional branch-pruning could also reduce themite population. However, further studies are required to investigatethe progress of the symptom in detail as the grapevine grows.

However, it was obvious that the mite occurred in high density atall of the five vineyards inspected in Hwaseong compared to the otherlocations surveyed (Table 1). It was reported that such an abundantpopulation of the mite could be established by high summer temper-atures (Kast et al., 2004), pesticide use (Van Leeuwen et al., 2010), orunusual climatic changes (Varner et al., 2006). The increase in sum-mer temperatures has been positively correlated with the mite infes-tations occurring in the subsequent year in Germany (Kast et al.,2004). Resistance to acaricides and/or pesticide misusage affectingnatural enemies can cause the unexpected increase of the mite popu-lation, but this has not been examined in depth (Van Leeuwen et al.,2010). Unusual climate conditions can also impact on the balance be-tween predatory mites and the grape rust mite, according to a studywith a predatory mite, Typhlodromus pyri, in different rearing condi-tions (Sengonca et al., 2003). Although the conventionally conductedpesticide-spraying and branch-pruning must have reduced the popu-lation density during the growing season in Hwaseong, it is unknownhow such a large stock of overwintering mites was produced. Thegeographic location of the five vineyards inspected, which is along-side the west coast, might need to be considered as well for furtherstudies. Extending the survey area to neighboring locations couldgive a clue for how far the ‘hot spot’ of the mite has been spread.

A congeneric species, Colomerus vitis (Pagenstecher), which hadonce been recorded as a cause of ‘felt disease on grapevine leaves’in Korea (Anonymous, 1928), and has never been reported again inKorea thereafter, was not found in this survey. Although this studyon a nationwide scale supports the absence of the mite in Korea, thepresence of Colomerus vitis in Korea is still controversial (J.-H. Lee,Personal Communication).

Acknowledgments

Authors thank the anonymous reviewers for the valuable com-ments. This work was carried out with the support of “Research Pro-gram for Agriculture Science & Technology Development (Project No.PJ009462)”, Rural Development Administration, Republic of Korea.

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