Occurrence of Cicadulina Bipunctata (Hemiptera: Cicadellidae) In

Appl Entomol Zool (2014) 49:325–330 DOI 10.1007/s13355-014-0253-3 ORIGINAL RESEARCH PAPER Occurrence of Cicadulina bipunctata (Hemiptera: Cicadellidae) in southwestern Shikoku, Japan and comparisons of gall-inducing ability between Kyushu and Shikoku populations Shun Kumashiro • Keiichiro Matsukura • Ryo Ogawa • Masaya Matsumura • Makoto Tokuda Received: 2 July 2013 / Accepted: 19 February 2014 / Published online: 8 March 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com Abstract The maize orange leafhopper Cicadulina bi- bipunctata had a gall inducing ability similar to the punctata (Melichar) is an insect pest of cereal crops in Kumamoto population. More attention should be paid to tropical and subtropical regions of the Old World. This assessing the risk of further expansion of C. bipunctata leafhopper induces gall symptoms characterized by stunted populations in Shikoku. growth and swollen leaf veins on various Poaceae. Damage by C. bipunctata has been reported from Australia, the Keywords Distribution Á Maize orange leafhopper Á Philippines, China, Taiwan, and Japan. In Japan, C. bi- Maize wallaby ear symptom Á Poaceae punctata occurs in the central and southern parts of Kyu- shu. Because the leafhopper is a potential pest of various cereal crops, we conducted field surveys in Shikoku and the Introduction southern part of the Kii Peninsula (a part of Honshu), where the climate seems to be suitable for the establish- Maize orange leafhopper, Cicadulina bipunctata (Meli- ment of C. bipunctata. As a result, we found C. bipunctata char), is distributed in tropical and subtropical regions of at some localities in Ehime and Kochi Prefectures. This is the Old World (Webb 1987; Matsukura et al. 2009a). In the first record of this leafhopper from Shikoku. Our lab- Japan, this species is known to occur in the Bonin Islands oratory experiment revealed that a Kochi population of C. (Matsumura 1914), the Ryukyu Islands (Hayashi 2002), and Kyushu (Matsumura et al. 2006; Matsukura et al. 2009a; Kumashiro et al. 2012). The leafhopper feeds on Electronic supplementary material The online version of this various Poaceae including important crops, such as maize, article (doi:10.1007/s13355-014-0253-3) contains supplementary rice and wheat (Maramorosch et al. 1961; Catindig et al. material, which is available to authorized users. 1996; Kumashiro et al. 2011). Cicadulina bipunctata is a S. Kumashiro (&) serious pest of maize because feeding by the leafhopper The United Graduate School of Agricultural Sciences, induces gall symptoms characterized by stunted growth Kagoshima University, Korimoto, Kagoshima 890-0065, Japan and swollen leaf veins, which is referred to as the maize e-mail: [email protected] wallaby ear symptom (Grylls 1975; Ohata 1993). The K. Matsukura Á M. Matsumura symptoms have been reported from Australia (Grylls Agro-Environment Research Division, NARO Kyushu Okinawa 1975), the Philippines (Agati and Calica 1949; Mara- Agricultural Research Center, Koshi, Kumamoto 861-1192, morosch et al. 1961), China (Li and Liu 2004; Li et al. Japan 2004), Taiwan (Chen 1991), and Japan (Ohata 1993; R. Ogawa Matsumura et al. 2005, 2006). Entomological Laboratory, Faculty of Agriculture Ehime Although previous studies attributed the symptoms to a University, Tarumi, Matsuyama, Ehime 790-8566, Japan leafhopper-transmitted virus (Agati and Calica 1949; Maramorosch et al. 1961; Grylls 1975; Reddy et al. 1976; M. Tokuda Laboratory of Systems Ecology, Faculty of Agriculture, Saga Boccardo et al. 1980), recent studies have recognized that University, Honjo, Saga 840-8502, Japan some chemicals injected by C. bipunctata during feeding 123 326 Appl Entomol Zool (2014) 49:325–330 are responsible for gall induction (Ofori and Francki 1983; Agency 2011). This implies that the climate in these areas Ohata 1993; Kawano 1994; Matsukura et al. 2012a). Galls would permit the survival of C. bipunctata. are induced only on leaves which are newly expanding To assess the potential risk of agricultural damage by C. during leafhopper feeding, but not on leaves already bipunctata, information about the detailed distribution of developed or those which expand after the removal of C. bipunctata and its gall-inducing ability in local popu- leafhoppers (Ofori and Francki 1983; Ohata 1993; Mat- lations will be very important. In this study, we surveyed sukura et al. 2009b). The degree of gall induction depends the distribution of C. bipunctata in the southwestern and on the density and duration of feeding by C. bipunctata eastern parts of Shikoku and the southwestern part of the (Matsukura et al. 2009a; Matsukura and Matsumura 2010; Kii Peninsula, and we compared the gall inducing ability of Tokuda et al. 2013). C. bipunctata between Kyushu and Shikoku populations. In Japan, the gall symptom was first reported in Kumamoto and Okinawa Prefectures in the late 1980s (Ohata 1993; Kawano 1994). Heavy damage occurred on Materials and methods the second planting of forage maize, especially in Kuma- moto Prefecture (Ohata 1993). According to Matsumura Field survey et al. (2005), the total area of forage maize fields damaged by C. bipunctata has expanded gradually since 2001 in Field investigations were conducted in 17 localities in Kumamoto Prefecture, and outbreaks of the leafhopper Ehime Prefecture and in 16 localities in Kochi Prefecture, were reported in 2004. Thereafter, a resistant maize variety southwestern Shikoku, Japan in November 2011. Addi- was developed to reduce the damage caused by C. bi- tional investigations were performed in 8 localities in punctata (Tokuda and Matsumura 2005). Kagawa Prefecture, 11 localities in Tokushima Prefecture, Because C. bipunctata has a certain degree of tolerance eastern Shikoku and 18 localities in Wakayama Prefecture, to high temperatures, such as 31 and 34 °C (Tokuda and southwestern Kii Peninsula in October 2012 (Table 1 and Matsumura 2005), the expansion of distribution range fol- Supplementary Table 1). In each locality, the grasslands lowing global warming is of concern for this species where host grassy weeds of C. bipunctata such as Eleusine (Matsumura et al. 2005; Matsukura et al. 2009a, 2012b). indica (L.), Digitaria ciliaris (Retz.), and Setaria viridis Cicadulina bipunctata occurs in the southern parts and (L.) grew were selected for the census sites and 30 or 25 middle-western parts of Kyushu (Webb 1987; Matsukura sweeps using a sweeping net with a diameter of 42 cm et al. 2009a), and our most recent study revealed that the were performed at each census site. The census sites were leafhopper is also distributed in the middle-eastern parts, separated from each other by at least 2 km. Collected but not in the northern parts, of Kyushu (Kumashiro et al. leafhoppers were kept in glass tubes filled with 99.5 % 2012). Until now, C. bipunctata had not been reported from ethanol, but approximately 40 adults collected from a Shikoku or the Kii Peninsula, Honshu, even though the census site in Kochi (Ohtsu, see Fig. 1; Table 1) were annual mean temperatures of these areas are rather higher transferred alive to Kyushu Okinawa Agricultural Research than in the middle parts of Kyushu (Japan Meteorological Center in Kumamoto and reared on rice seedlings at 25 °C Table 1 Collection sites and No. Census site Longitude Latitude (E) Male Female Total numbers of C. bipunctata (N) captured in Ehime Prefecture 1 Shimodomari, Mikame Town, Seiyo City, 33°20005.7 132°22041.2 19 7 26 Ehime 2 Karihama, Akehama Town, Seiyo City, Ehime 33°18036.9 132°26046.9 0 2 2 3 Sunokawa, Ainan Town, Ehime 33°01048.0 132°28056.1 1 2 3 4 Ohtsu, Tosashimizu City, Kochi 32°45003.9 132°47001.0 31 32 63 5 Tsumajiro, Tosashimizu City, Kochi 32°47016.1 132°52013.5 1 0 1 6 Nakanohama, Tosashimizu City, Kochi 32°46022.9 132°57052.4 1 3 4 7 Ashizurimisaki, Tosashimizu City, Kochi 32°43017.4 133°00039.9 1 2 3 8 Kubotsu, Tosashimizu City, Kochi 32°46057.2 132°59036.6 3 7 10 9 Ukibuchi, Kuroshio Town, Kochi 32°59033.4 133°00025.6 1 0 1 Sites where C. bipunctata was 10 Shirahama, Kuroshio Town, Kochi 33°02026.3 133°05048.2 18 24 42 not found are shown in 11 Okitsu, Shimanto Town, Kochi 33°09045.9 133°12024.3 60 74 134 Supplementary Table 1 123 Appl Entomol Zool (2014) 49:325–330 327 Fig. 1 Census sites for C. bipunctata in Shikoku and the Kii Peninsula. Sites where C. 0 100 bipunctata was found are km marked by solid circles with site Kagawa numbers shown in Table 1 and those where it was not found are shown with open circles or Tokushima squares Wakayama Ehime Kochi 1 2 11 0 500 km 10 3 9 8 4 5 6 7 Kumamoto C. bipunctata found (in November 2011) Honshu Not found (in November 2011) Shikoku Not found (in October 2012) Kyushu under a 16L: 8D photoperiod, as in Matsumura and Tokuda Prior to the release of males, all plants were covered (2004). individually with an acrylic cylinder (4.5 cm diameter and 24.5 cm high) with nylon cloth on the top for ventilation. Gall-inducing ability Seven days after the release, all males were removed from the plants and the number of surviving individuals was In order to compare the gall-inducing ability of C. bipunctata counted. between Kyushu and Shikoku populations, the following two As mentioned earlier, galls of C. bipunctata are induced stock cultures, Kumamoto and Kochi populations, of C. bi- on leaves newly expanding during leafhopper feeding. punctata were used in this study. The Kumamoto population Thus, the length of the third (var. 3470) or fourth (var. was established from approximately 70 adults collected from 30D44) leaf was measured from the base of plant to the tip Shisui, Kumamoto, Kyushu in December 2012 and the Kochi of plant (an equivalent measurement to leaf length often Population was established from ca.

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