Distribution of Parmarion cf. martensi (Pulmonata: Helicarionidae), a New Semi-Slug Pest on Hawai‘i Island, and Its Potential as a Vector for Human Angiostrongyliasis

The semi-slug Parmarion cf. martensi Simroth, 1893, was first discovered on O‘ahu, Hawai‘i, in 1996 and then on the island of Hawai‘i in 2004. This species, which is probably native to Southeast Asia, is abundant in eastern Hawai‘i Island, reportedly displacing the Cuban slug, Veronicella cubensis (Pfeiffer, 1840), in some areas. A survey in July–August 2005 found P. cf. martensi primarily in the lower Puna area of Hawai‘i Island, with an isolated population in Kailua-Kona (western Hawai‘i Island). It is now established in commercial papaya plantations, and survey participants reported it as a pest of lettuce and papaya in home gardens. Survey respondents considered P. cf. martensi a pest also because of its tendency to climb on structures where it deposits its feces and because of its potential to transmit disease. Individuals of this species were found to carry large numbers of infective third-stage larvae of the nematode Angiostrongylus cantonensis (Chen, 1935), the causative agent of human angiostrongyliasis and the most common cause of human eosinophilic meningoencephalitis. Using a newly developed polymerase chain reaction test, 77.5% of P. cf. martensi collected at survey sites were found infected with A. cantonensis, compared with 24.3% of V. cubensis sampled from the same areas. The transmission potential of this species may be higher than that for other slugs and snails in Hawai‘i because of the high prevalence of infection, worm burdens, and its greater association with human habitations, increasing the possibility of human-mollusk interactions. The semi-slug Parmarion cf. martensi Simroth, 1893, is a recent introduction to the island of Hawai‘i. The first record was made in the summer of 2004 in Paradise Park, a residential area in the district of Puna (East Hawai‘i Island) (Arnold Hara, University of Hawai‘i, pers. comm., 2005). The species was recognized as being similar to, or the same as, a semi-slug species collected for the first time on the island of O‘ahu in 1996 and provisionPacific Science (2007), vol. 61, no. 4:457–467 Work of the U.S. Government Not under copyright 1 Manuscript accepted 9 January 2007. 2 Corresponding author (phone: 808-959-4349; e-mail: [email protected]). 3 U.S. Department of Agriculture, Agricultural Research Service, U.S. Pacific Basin Agricultural Research Center, P.O. Box 4459, Hilo, Hawai‘i 96720. 4 Current address: 190 Southwest Brumback Street, Linfield College, McMinnville, Oregon 97128. 5 Centers for Disease Control and Prevention, 4770 Buford Highway Northeast, Atlanta, Georgia 30341. 6 Atlanta Research and Education Foundation in conjunction with the Atlanta Veterans Administration Medical Center, Decatur, Georgia. 7 U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103. 8 The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention/the Agency of Toxic Substances and Disease Registry. ally identified as Parmarion martensi Simroth, 1893 (Cowie 1997). The taxon Parmarion martensi was originally described from Cambodia (Simroth 1893), but it has also been reported from Vietnam, Malay Peninsula, Sumatra, Java, Borneo, Japan, Taiwan, Singapore, Samoa, and American Samoa (van Benthem Jutting 1950, Minato 1975, Minato and Okubo 1991, Ho 1995, Cowie 1998, Asato et al. 2004). However, due to the difficulty of identifying Parmarion to the species level, the accuracy of the records listed here requires further investigation. Plate I shows photos of this semi-slug collected from a site in Koa‘e, East Hawai‘i Island, in December 2004. Voucher specimens (2) collected from the site at that time were deposited in the Academy of Natural Sciences malacological collection (Philadelphia, Pennsylvania) and designated as ansp A21014. In December 2004, before learning that P. cf. martensi had been found on Hawai‘i Island, R. Hollingsworth was requested by a local resident to investigate the presence of a new slug species on a property in Koa‘e, near the eastern tip of the island. The request was prompted by the resident’s concern about transmission of rat lungworm disease caused by Angiostrongylus cantonensis (Chen, 1935), a rodent nematode that develops to the infective larval stage in a slug or snail host (Mackerras and Sandars 1955). The disease, which manifests itself in humans as eosinophilic meningitis (Kliks and Palumbo 1992), can be acquired by the intentional or accidental consumption of raw or undercooked slugs or snails or paratenic hosts (such as shrimps or flatworms) (i.e., animals capable of carrying the infective stage of the parasite but not supporting further development [Alicata and Jindrak 1970, Ash 1976, Kliks and Palumbo 1992]). The resident requesting the visit and two of her dinner guests became ill with symptoms consistent with angiostrongyliasis after consuming home-grown lettuce reportedly contaminated with immature semi-slugs. Important intermediate hosts of A. cantonensis in Hawai‘i include veronicellid slugs [primarily the Cuban slug, Veronicella cubensis (Pfeiffer, 1840)]; the giant African snail, Achatina fulica (Bowdich, 1822); and the marsh slug, Deroceras laeve (Müller, 1774) (Wallace and Rosen 1969a, Alicata 1991). Parmarion cf. martensi has the potential for becoming an important vector of A. cantonensis in Hawai‘i, as happened in Okinawa (Asato et al. 2004) after P. martensi became more prevalent there starting around the year 2000. Our initial survey in Koa‘e indicated that P. cf. martensi was extremely common; it was found in trash cans, in a composting toilet, in an outdoor shower area, in a planting of spider lilies (Crinum asiaticum [Amaryllidaceae]), under plastic sheeting, and in a vegetable compost pile where egg masses of P. cf. martensi were also found. Specimens of P. cf. martensi collected during the initial survey were sent to the Division of Parasitic Diseases, Centers for Disease Control and Prevention (CDC), Atlanta, Georgia, to be examined for infection. The 26 semislugs examined were all positive for A. cantonensis, as determined by pepsin digestion (Graeff-Teixeira and Morera 1995). The importance of P. cf. martensi as a vector of this disease may be exacerbated by its high population densities, climbing behavior, attraction to food items associated with human dwellings, and potentially high parasite load. Our objectives for this study were to: (1) determine the geographical distribution of P. cf. martensi on Hawai‘i Island; (2) survey homeowners to gain information about pest status, feeding preferences, and foraging behavior; (3) compare levels of infection of A. cantonensis in P. cf. martensi and V. cubensis collected from the same sites; and (4) compare the feeding patterns of P. cf. martensi and V. cubensis in the laboratory on selected types of food. materials and methods The Parmarion survey was publicized with advertisements in two local newspapers on 7 July 2005. The advertisement included a black-and-white picture of an adult P. cf. martensi semi-slug, a caption detailing its distinguishing characteristics, and a request for information from anyone who had seen this species on his or her property. An article about this species and our survey that ap458 PACIFIC SCIENCE . October 2007