Appl. Entomol. Zool. 37 (4): 589 593 (2002) A mango pest, Procontarinia mangicola (Shi) comb. nov. (Diptera: Cecidomyiidae), recently found in Okinawa, Japan 1 Nami Uechi,* Futoshi Kawamura, 2 Makoto Tokuda and Junichi Yukawa 3 Entomological Laboratory, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka 812 8581, Japan 2 Okinawa Prefectural Agricultural Experiment Station, Naha, Okinawa 903 0814, Japan 3 Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka 812 8581, Japan (Received 17 June 2002; Accepted 22 July 2002) Abstract A gall midge species producing circular blisters on mango leaves was found in 2000 at Tamagusuku Village on Okinawa Island, Japan. This gall midge is identified as Procontarinia mangicola (Shi), and was originally placed in the genus Erosomyia. Another species, Procontarinia schreineri Harris, described from Guam is newly synonymized with P. mangicola. By 2001, this gall midge was found on eight islands in Okinawa Prefecture. Heavily galled leaves fell to the ground much earlier than usual and mango trees with galled leaves had almost no inflorescences, resulting in low yields of mango fruit. We consider that the gall midge adults might be dispersed by wind or that the larvae could be transported with soil or other substrates covering the roots of mango plants in nurseries. We also provide some comments on control measures that may be used against this gall midge. Key words: Cecidomyiidae, Procontarinia mangicola, mango, Mangifera indica, gall midge INTRODUCTION At least 16 nominal species of gall midges (Diptera: Cecidomyiidae) are known to attack mango, Mangifera indica L. (Anacardiaceae) in Asia where this plant is indigenous. One of those species, Erosomyia mangiferae (Felt), has also been accidentally introduced into the Caribbean and Brazil with its host (Harris and Schreiner, 1992). Until now, no mango gall midges have been recorded in Japan (Yukawa and Masuda, 1996), probably because mango does not grow naturally even in Okinawa Prefecture, situated between 24 and 27 north latitude. Mango was first introduced to Okinawa Prefecture, Japan as a yard tree shortly before 1897 (Igei, 1994; Yasutomi, 1994). Commercial cultivation of mango started in the 1950s, using a cultivar, Irwin, introduced from Hawaii. Later, the cultivation of mango under a roof or in a greenhouse improved the survival rate of inflorescences and brought a large yield of fruit to growers (Igei, 1994; Yasutomi, 1994). In addition, two species of fruit fly, Bactrocera dorsalis (Hendel) and B. cucurbitae (Coquillett) (Diptera: Tephritidae) were eradicated from Okinawa Prefecture by 1986 and 1993, respectively (e.g., Itô and Kakinohana, 1998). This allowed growers to ship fresh mango fruit from Okinawa Prefecture to consumers in other parts of Japan and further promoted the mango industry. Because mango can be cultivated only in the southern parts of Japan, it has become an important cash fruit in various prefectures such as Okinawa, Kagoshima, Miyazaki, Fukuoka, and Wakayama. In November 2000, a gall midge producing circular blister galls on mango leaves was first found in a mango greenhouse at Tamagusuku Village on Okinawa Island (Fig. 1). By 2001, this gall midge was found at various localities on six islands in Okinawa Prefecture. Since galled leaves remaining on trees are known to provide reservoirs of anthracnose inoculum (Harris and Schreiner, 1992), it is feared that heavily infested mango trees may put out few inflorescences, resulting in reduced yields of mango fruits. Thus an identification of the mango gall midge in Okinawa is an urgent necessity as the first step toward the establishment of control measures. In 1 Contribution from the Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka (Ser. 5, No. 85). * To whom correspondence should be addressed at: E-mail: uechi@agr.kyushu-u.ac.jp 589
590 N. Uechi et al. this paper we identify the gall midge and report the details of field surveys in Okinawa Prefecture. We also provide distributional information and comment on pest status, possible range expansion and control measures. MATERIALS AND METHODS Identification of the mango gall midge in Okinawa. Adults and larvae of the gall midge were collected in 2000 by FK from a mango greenhouse in Horikawa, Tamagusuku Village, Okinawa Island. The specimens were preserved in 75% ethanol for morphological comparison and in 99.5% acetone for future DNA analysis. Some of the ethanol-preserved specimens were mounted on slides in Canada balsam using the techniques outlined in Gagné (1989) to compare the mango gall midge in Okinawa with those in other areas. Some of the specimens were sent to Dr. R. J. Gagné (Systematic Entomology Laboratory, PSI, Agricultural Research Service, USDA, USA) and Dr. K. M. Harris (Former Director of the International Institute of Entomology, UK) for confirmation of our identification. Fig. 1. Map of islands in Okinawa Prefecture. Circles indicate cities, towns, and villages where the infestation of Procontarinia mangicola was found by 2002. Arrow points toward Tamagusuku Village where the gall midge was first found. Most specimens examined in this study are kept in the collection of the Entomological Laboratory, Faculty of Agriculture, Kyushu University and some are in the U. S. National Museum, Washington, D.C., USA. Immediately after the discovery of the mango gall midge in November 2000, we surveyed almost all mango cultivation areas on Okinawa Island. By January 2002, our surveys extended over 44 cities, towns, and villages on eight islands in Okinawa Prefecture. The islands, from north to south, are: Okinawa, Henza, Kume, Miyako, Kurima, Ishigaki, Iriomote, and Yonaguni. In February 2001, we examined scars of midge galls on old mango leaves on the islands of Okinawa, Ishigaki, and Iriomote. The old midge gall scars tell us the approximate time of invasion by the gall midge because some ungalled or lightly galled leaves survive for at least five years. From February 26 to March 3, 2001, FK visited several mango orchards in Tainan, the southern part of Taiwan, to see if the mango gall midge occurs there. RESULTS AND DISCUSSION Identification of the mango gall midge in Okinawa At first we applied the name Procontarinia schreineri Harris to the gall midge on mango in Okinawa, based on the description by Harris and Schreiner (1992) for the mango gall midge in Guam. However, an older possible name, Erosomyia mangicola Shi, 1980, for the mango midge was noticed by Dr. R. J. Gagné (2001, personal communication) in the course of his work on a world catalog of gall midges. Dr. K. M. Harris, who had described P. schreineri, was immediately notified and consulted as to his opinion of this species. Dr. Harris stated that there was no doubt that the two names were synonymous (2001, personal communication). We also observed similarities between E. mangicola and P. schreineri, particularly in the male genitalia that are provided with a curved aedeagus with distal triangular lateral extensions (see Harris and Schreiner, 1992 for detailed illustrations of the male genitalia, ovipositor, larval sternal spatula, etc.). One reason why the earlier name, E. mangicola, was unnoticed until recently is that Shi (1980) had placed his species in
A Mango Pest, Procontarinia mangicola in Okinawa 591 the genus Erosomyia. In this paper, JY and NU place this species in Procontarinia as a new combination, Procontarinia mangicola (Shi), and synonymize P. schreineri with P. mangicola, following the advice of Dr. R. J. Gagné and Dr. K. M. Harris. We now use the name P. mangicola for the mango gall midge in Okinawa and propose a new combination and a new synonymy as follows: Procontarinia mangicola (Shi, 1980) New combination: Yukawa and Uechi (Fig. 2). Erosomyia mangicola Shi, 1980; Entomotaxonomia 2: 131. Fig. 2. Procontarinia mangicola. A: Mature larvae in the galls; B: Pupa; C: Male adult. Fig. 3. A: A mango leaf with circular blisters produced by Procontarinia mangicola; B: Symptoms caused by an anthracnose, Colletotrichum gloeosporioides.
592 N. Uechi et al. Procontarinia schreineri Harris, 1992 (in Harris and Schreiner, 1992). Bull. Entomol. Res. 82: 42. New synonymy: Yukawa and Uechi. Biology and survey details In Guam, P. mangicola attacks fresh mango leaves and produces circular blister galls, causing the leaves to crinkle (Harris and Schreiner, 1992). Development of eggs and the larval feeding period are completed within five days and mature larvae then leave the gall, dropping to the ground to pupate. Adults emerge six days later. Old galls on damaged leaves provide reservoirs of anthracnose inoculum. On November 9, 2000, a gall midge species producing circular blister galls on mango leaves was first found in a mango greenhouse at Horikawa, Tamagusuku Village on Okinawa Island (Fig. 1). On the next day, we confirmed that this gall midge had already been attacking mango (cultivars: Irwin and Keitt) widely in southern parts of Okinawa Island. By February 2001, P. mangicola was found in northern parts of Okinawa Island and at various localities on five other islands in Okinawa Prefecture (Fig. 1). Additional findings of this gall midge were reported from two more islands during the period between February 2001 and January 2002. As a result, we found this gall midge in 28 out of 44 cities, towns, and villages surveyed on eight islands in Okinawa Prefecture. According to the Okinawa General Bureau (2001), about 78% (158 ha) of mango growing areas (202 ha) in Okinawa were infested by the gall midge. Thus P. mangicola is now a common and important pest of mango in Okinawa Prefecture. However, it has not yet been found in Kagoshima and Miyazaki Prefectures, north of Okinawa. In February 2001, we found midge gall scars on one- to five-year old leaves on Ishigaki and Iriomote Islands. This means that P. mangicola became established in or before 1997 on these two islands. On Okinawa Island, there were midge gall scars on the 2000 year-class leaves but not on older leaves, indicating that P. mangicola probably arrived on Okinawa Island in 2000. Distributional information and possible expansion P. mangicola has been recorded from Guangxi Zhuang Autonomous Region, China (Shi, 1980) and Guam (Harris and Schreiner, 1992), while it has never been found in the Philippines and Taiwan, where mango gall midges were not intensively surveyed until 2000. However, in 2001, FK found anthracnose disease symptoms on old blister midge galls in Tainan, Taiwan. This indicates a possible occurrence of one or more Procontarinia species in Tainan. We do not know at the moment how and from where P. mangicola came to Okinawa, but we assume that the gall midge larvae could be transported with soil or other substrates covering the roots of mango plants in nurseries. Therefore we have to be aware of the possibility that the range of this gall midge could extend to Kagoshima and Miyazaki Prefectures in this way. In addition, wind could disperse the adults from island to island, as has been noted in Yukawa and Partomihardjo (1997) for gall midges that colonized the Krakatau Islands, Indonesia, which are about 40 and 35 km distant from Java and Sumatra, respectively. Pest status In most mango orchards surveyed, heavily galled leaves fell to the ground much earlier than usual and most galled leaves remaining on trees suffered from anthracnose inoculum. Satoshi Taba (unpublished data) detected an anthracnose, Colletotrichum gloeosporioides (Penzig) Penzig and Saccardo from most of the young galled mango leaves on Okinawa Island. Shoots of heavily infested mango trees had almost no inflorescences, resulting in low yields of mango fruit (Fig. 3). Such damage was frequently observed in relatively high humidity mango orchards where the undergrowth was very thick and mango trees were not pruned adequately. As has been noted in Harris and Schreiner (1992), high humidity improves larval and pupal survival and more galls appear. Comments on control measures Up to the present, no effective insecticide has been screened for this pest in Japan, although Okinawa Prefectural Agricultural Experiment Station is now testing some sorts of insecticides against the gall midge. Some parasitoid wasps are known to attack Procontarinia spp. in India (Srivastava, 1997). However, we have not found any wasps parasitizing P. mangicola in Okinawa. This may be because P.
A Mango Pest, Procontarinia mangicola in Okinawa 593 mangicola came to Okinawa recently unaccompanied by parasitoid wasps. The introduction of parasitoids to Okinawa from other regions might be one effective method to control P. mangicola. In order to reduce the infestation of P. mangicola, we recommend growers to keep mango orchards relatively dry by pruning away offshoots and clearing away the undergrowth. ACKNOWLEDGEMENTS We would like to express our thanks to Dr. R. J. Gagné (Systematic Entomology Laboratory, PSI, Agricultural Research Service, USDA, USA) and Dr. K. M. Harris (Former Director of the International Institute of Entomology, UK) for their help in confirming our identification and reading an early draft. Our thanks are due to Messrs. K. Yasuda, M. Taniguchi, T. Ohishi (Okinawa Prefectural Agricultural Experiment Station), D. Haraguchi, and Ms. A. Maehira (Okinawa Prefectural Plant Disease and Insect Control Station) for their assistance in the field surveys. We are also indebted to Mr. Satoshi Taba (Okinawa Prefectural Agricultural Experiment Station) who identified an anthracnose fungus. Nami Uechi and Makoto Tokuda thank Dr. O. Tadauchi, Dr. S. Kamitani, and Mr. D. Yamaguchi (Entomological Laboratory, Kyushu University) for their support and encouragement. REFERENCES Gagné, R. J. (1989) The Plant-Feeding Gall Midges of North America. Cornell University Press, Ithaca, pp. 99 100. Harris, K. M. and I. H. Schreiner (1992) A new species of gall midge (Diptera: Cecidomyiidae) attacking mango foliage in Guam, with observations on its pest status and biology. Bull. Entomol. Res. 82: 41 48. Igei, Y. (1994) Mango culture and its problems in Okinawa. J. Okinawa Agric. 29: 16 25 (in Japanese). Itô, Y. and H. Kakinohana (1998) [A Battle against an Insect Pest without Using Insecticide]. Iwanami Junior Shinsho, Tokyo, pp. 13 14, 169 191 (in Japanese). Okinawa General Bureau (2001) [Statistical Information on Horticultural and Industrial Crop Production by City, Town, and Village for the 2000 Fiscal Year]. Agriculture, Forestry and Fishery Department, Okinawa General Bureau, Naha, pp. 42 43 (in Japanese). Shi, D. S. (1980) A new species of gall midges affecting young leaf of mango (Diptera: Cecidomyiidae). Entomotaxonomia 2: 131 134. Srivastava, R. P. (1997) Mango Insect Pest Management. International Book Distributing Co., New Delhi, pp. 61 74. Yasutomi, T. (1994) General remarks on mango culture in Okinawa. J. Okinawa Agric. 29: 26 35 (in Japanese). Yukawa, J. and H. Masuda (1996) Insect and Mite Galls of Japan in Colors. Zenkoku Nôson Kyôiku Kyôkai, Tokyo, pp. 657 682 (in Japanese with English explanations for color plates). Yukawa, J. and T. Partomihardjo (1997) Insect and mite galls collected from Peucang, Panaitan, and the Krakatau Islands, Indonesia. Tropics 7: 141 152.