Distribution of cf. martensi (: Helicarionidae), a New Semi-Slug Pest on Hawai‘i Island, and Its Potential as a Vector for Human Angiostrongyliasis1

Robert G. Hollingsworth,2,3 Rachel Kaneta,3,4 James J. Sullivan,5,8 Henry S. Bishop,5,8 Yvonne Qvarnstrom,5,6,8 Alexandre J. da Silva,5,8 and David G. Robinson7

Abstract: The semi-slug Parmarion cf. martensi Simroth, 1893, was first discov- ered 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 Ha- wai‘i Island, reportedly displacing the Cuban slug, Veronicella cubensis (Pfeiffer, 1840), in some areas. A survey in July–August 2005 found P. cf. martensi primar- ily 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 pa- paya plantations, and survey participants reported it as a pest of and 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 angio- strongyliasis and the most common cause of human eosinophilic meningo- encephalitis. 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 transmis- sion 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 hu- man-mollusk interactions.

The semi-slug Parmarion cf. martensi Sim- Hawai‘i Island) (Arnold Hara, University of roth, 1893, is a recent introduction to the is- Hawai‘i, pers. comm., 2005). The species was land of Hawai‘i. The first record was made in recognized as being similar to, or the same as, the summer of 2004 in Paradise Park, a resi- a semi-slug species collected for the first time dential area in the district of Puna (East on the island of O‘ahu in 1996 and provision-

1 Manuscript accepted 9 January 2007. 5 Centers for Disease Control and Prevention, 4770 2 Corresponding author (phone: 808-959-4349; Buford Highway Northeast, Atlanta, Georgia 30341. e-mail: [email protected]). 6 Atlanta Research and Education Foundation in con- 3 U.S. Department of Agriculture, Agricultural Re- junction with the Atlanta Veterans Administration Medi- search Service, U.S. Pacific Basin Agricultural Research cal Center, Decatur, Georgia. Center, P.O. Box 4459, Hilo, Hawai‘i 96720. 7 U.S. Department of Agriculture, and Plant 4 Current address: 190 Southwest Brumback Street, Health Inspection Service, Plant Protection and Quaran- Linfield College, McMinnville, Oregon 97128. tine, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103. 8 The findings and conclusions in this report are those Pacific Science (2007), vol. 61, no. 4:457–467 of the authors and do not necessarily represent the views Work of the U.S. Government of the Centers for Disease Control and Prevention/the Not under copyright Agency of Toxic Substances and Disease Registry.

457 458 PACIFIC SCIENCE . October 2007 ally identified as Simroth, slug, Deroceras laeve (Mu¨ller, 1774) (Wallace 1893 (Cowie 1997). The taxon Parmarion and Rosen 1969a, Alicata 1991). martensi was originally described from Cam- Parmarion cf. martensi has the potential for bodia (Simroth 1893), but it has also been becoming an important vector of A. canton- reported from Vietnam, Malay Peninsula, Su- ensis in Hawai‘i, as happened in Okinawa matra, Java, Borneo, Japan, Taiwan, Singa- (Asato et al. 2004) after P. martensi became pore, Samoa, and American Samoa (van more prevalent there starting around the Benthem Jutting 1950, Minato 1975, Minato year 2000. Our initial survey in Koa‘e indi- and Okubo 1991, Ho 1995, Cowie 1998, cated that P. cf. martensi was extremely com- Asato et al. 2004). However, due to the diffi- mon; it was found in trash cans, in a culty of identifying Parmarion to the species composting toilet, in an outdoor shower level, the accuracy of the records listed here area, in a planting of spider lilies (Crinum asi- requires further investigation. Plate I shows aticum [Amaryllidaceae]), under plastic sheet- photos of this semi-slug collected from a site ing, and in a vegetable compost pile where in Koa‘e, East Hawai‘i Island, in December egg masses of P. cf. martensi were also found. 2004. Voucher specimens (2) collected from Specimens of P. cf. martensi collected during the site at that time were deposited in the the initial survey were sent to the Division of Academy of Natural Sciences malacological Parasitic Diseases, Centers for Disease Con- collection (Philadelphia, Pennsylvania) and trol and Prevention (CDC), Atlanta, Georgia, designated as ansp A21014. to be examined for infection. The 26 semi- In December 2004, before learning that P. slugs examined were all positive for A. canton- cf. martensi had been found on Hawai‘i Is- ensis, as determined by pepsin digestion land, R. Hollingsworth was requested by a (Graeff-Teixeira and Morera 1995). The im- local resident to investigate the presence of a portance of P. cf. martensi as a vector of this new slug species on a property in Koa‘e, near disease may be exacerbated by its high popu- the eastern tip of the island. The request was lation densities, climbing behavior, attraction prompted by the resident’s concern about to food items associated with human dwell- transmission of rat lungworm disease caused ings, and potentially high parasite load. by Angiostrongylus cantonensis (Chen, 1935), a Our objectives for this study were to: (1) rodent nematode that develops to the infec- determine the geographical distribution of tive larval stage in a slug or snail host (Mac- P. cf. martensi on Hawai‘i Island; (2) survey kerras and Sandars 1955). The disease, which homeowners to gain information about pest manifests itself in humans as eosinophilic status, feeding preferences, and foraging be- meningitis (Kliks and Palumbo 1992), can be havior; (3) compare levels of infection of A. acquired by the intentional or accidental con- cantonensis in P. cf. martensi and V. cubensis sumption of raw or undercooked slugs or collected from the same sites; and (4) com- snails or paratenic hosts (such as shrimps or pare the feeding patterns of P. cf. martensi flatworms) (i.e., capable of carrying and V. cubensis in the laboratory on selected the infective stage of the parasite but not sup- types of food. porting further development [Alicata and Jin- drak 1970, Ash 1976, Kliks and Palumbo materials and methods 1992]). The resident requesting the visit and two of her dinner guests became ill with The Parmarion survey was publicized with symptoms consistent with angiostrongyliasis advertisements in two local newspapers on 7 after consuming home-grown lettuce report- July 2005. The advertisement included a edly contaminated with immature semi-slugs. black-and-white picture of an adult P. cf. Important intermediate hosts of A. cantonensis martensi semi-slug, a caption detailing its dis- in Hawai‘i include veronicellid slugs [pri- tinguishing characteristics, and a request for marily the Cuban slug, Veronicella cubensis information from anyone who had seen this (Pfeiffer, 1840)]; the giant African snail, Acha- species on his or her property. An article tina fulica (Bowdich, 1822); and the marsh about this species and our survey that ap- PS 61-4 color plate mech 4/13/07 2:14 PM Page 1

PLATE I. Parmarion cf. martensi Simroth from East Hawai‘i Island, photographed December 2004. The distinct keel along the posterior dorsal midline helps distinguish this species from similar-looking species in Hawai‘i. A yellowish brown, flattened, fingernail-shaped shell is present on the dorsum (A), but the shell is frequently covered by mantle folds (B). Distribution of Parmarion cf. martensi on Hawai‘i Island . Hollingsworth et al. 459 peared in both newspapers on 15 July gener- positions 456 to 482 and 1,569 to 1,590 of ated an even greater response. Angiostrongylus cantonensis 18S rRNA gene; Site visits were made to follow up all GenBank entry AY295804. PCR was per- credible reports of semi-slug sightings made formed with 0.4 mM of each primer, 2 mlof within 7 weeks of the initial newspaper adver- DNA and AmpliTaq Gold PCR Master Mix tisement. Residents were asked where they (Applied Biosystems, Foster City, California) had seen this species on their property, what for a 50-ml total PCR reaction volume. PCR types of food they had observed the semi- cycling parameters were 95C 5 min, 45 slugs to eat, and whether they considered cycles of 95C 15 sec, 65C 15 sec, 72C this species a pest. At least 20 min per site 1 min, and 72C 10 min. To achieve iden- was spent collecting semi-slugs and other tification at species level, PCR amplified mollusks. The locations where P. cf. martensi products were subjected to DNA sequence were found were recorded. analysis. Specimens collected from each site during Data used to compare infection levels in P. the July survey were sorted by species and cf. martensi and V. cubensis were derived from divided into size groups (large, medium, collections of mollusks from five sites, each small, or neonate). For V. cubensis and P. cf. of which contained multiple individuals of martensi, large specimens were about 4.5–5.5 each species. The statistical model consisted cm and 3.5–4.5 cm long, respectively; me- of logistic regression implementing the gen- dium and small specimens were about one- eralized estimating equations (GEE) proce- half and one-third as long, respectively, as dure to adjust for correlation among mollusks ‘‘large’’ specimens of the same species. Neo- of the same species being collected from the nates were <0.5 cm in length. These speci- same site. Analyses were performed using mens were shipped on dry ice to the CDC, the GENMOD procedure of SAS on-line where an experimental polymerase chain re- version 9.1 (SAS Institute, Inc. 2000–2004). action (PCR) method was used to determine Alpha was set at 0.05. the percentage infected with A. cantonensis. Feeding preferences of P. cf. martensi and DNA from intact slug tissue pieces was ex- V. cubensis were compared in unreplicated tracted using one of two methods: either bioassays. The bioassay arena consisted of a using selected reagents from the FastDNA ventilated 2-liter plastic container holding kit (MP Biomedicals, Solon, Ohio) or the moist soil (about 2.5 cm deep) and three ma- DNeasy tissue kit (QIAGEN Inc., Valencia, ture semi-slugs, held for 5 days in an environ- California). The FastDNA extraction was mental chamber (27C, 80% RH, 12:12 L:D). performed as described previously (da Silva Various types of plant foods were placed on et al. 1999) with one modification: the sample the soil surface after weighing. Data collected disruption was performed for 30 sec at speed included weights of plant material and obser- 5.5 in the FastPrep 120 Disruptor (Q- vations of feeding damage. Biogene, Carlsbad, California). PCR inhibi- tors were removed from DNA extracted with results FastDNA method by further purification with the QIAquick PCR purification kit The majority of the 51 survey respondents (QIAGEN Inc., Valencia, California). DNA were from the Puna district, although calls extracted by the DNeasy tissue kit did not were also received from residents in/near need further purification. The PCR method Kailua-Kona (West Hawai‘i), Waimea amplified 1,134 base pairs from the small sub- (Northwest Hawai‘i), Honoka‘a (Northeast unit ribosomal gene in Angiostrongylus species Hawai‘i), Hilo (East Hawai‘i), and Ocean (Qvarnstrom et al. 2007). Angiostrongylus- View Estates (South Hawai‘i). Based on tele- specific primers AngioF1 (50-ATCA- phone interviews, we determined that many TAAACCTTTTTTCGAGTATCCAG-30) respondents had actually seen other types of and AngioR1 (50-TCTCGAGACAGCT- slugs. We confirmed the presence of P. cf. CAGTCCCGG-3 0) were designed based on martensi at 27 of 29 properties that in our 460 PACIFIC SCIENCE . October 2007

Figure 1. Survey locations for Parmarion cf. martensi in Hawai‘i Island (shaded circles). White circles indicate sites where P. cf. martensi was searched for but not found. A white square (in the Waimea area) indicates location of a pop- ulation detected during a 2006 survey carried out by University of Hawai‘i scientists. The large square shows Puna district. Towns are indicated by black triangles. judgment were associated with credible sight- Puna district. At least four survey participants ings of this semi-slug. The greatest concen- independently noted that populations had tration of sightings was in the Paradise Park crashed within the previous 2–3 months. We Subdivision (Figures 1 and 2). also observed such a decline on an organic At the time of our survey, populations of farm near Kapoho, near the eastern tip of P. cf. martensi were very low throughout the Hawai‘i Island, where we had regularly been Distribution of Parmarion cf. martensi on Hawai‘i Island . Hollingsworth et al. 461

Figure 2. Map inset showing the lower Puna area where Parmarion cf. martensi was generally abundant. See Figure 1 for explanation of symbols. collecting P. cf. martensi adults since January the Puna district indicated that populations 2005. In early June, we found large numbers of P. cf. martensi returned to a higher level of P. cf. martensi egg masses on the under- during the fall of 2005. sides of halved coconuts being used as mulch Thirty-seven percent of survey respon- but saw few individuals of any other life stage. dents indicated that they had first noticed Subsequent observations at various sites in this semi-slug species within the few weeks 462 PACIFIC SCIENCE . October 2007

TABLE 1 Types of Habitat Where Parmarion cf. martensi Was Observed by Survey Participants (Day and Night Observations)

Location No. of Reports

On green plants (lettuce, fennel, sweet potato, banana, passion fruit, lemongrass, Heliconia)10 On fallen fruit (avocado, guava, citrus, papaya, mango) 9 On/under plastic or plasticlike materials, including black plastic sheeting, tarps, drainpipes, 8 plant pots In compost (especially covered compost) or inside trash cans 6 In food preparation and sink areas (outdoor sinks, on dishes, grills, on toothbrush) 5 In pet food bowls or eating spilled pet food 5 On deck or stairs 5 On concrete, tile, or asphalt 5 On walls of home 4 On palm fronds or trunks or under coconut shells 4 On catchment tank (on outside, under black saran cover at top) 3 On ripe papaya fruits (on tree) 2 In plant debris other than palms 2 preceding the publicity generated by survey markets on the east side of Hawai‘i Island. announcements. However, one respondent, There were five reports of P. cf. martensi be- an organic gardener, claimed to have noticed ing attracted during daytime to food prepara- this species in lower Paradise Park in 1999. tion and sink areas. In this context, several This would be the earliest report of P. cf. respondents remarked that P. cf. martensi martensi on Hawai‘i Island, and another resi- moved more quickly than other slug species dent @3 km distant remembered seeing the they had seen around their houses, appearing semi-slug on his property in 2000 or 2001. soon after food sources first became available. Sixty-seven percent of survey participants Five people reported semi-slugs feeding on considered this species a pest because of the dog food, cat food, or parrot food that was ei- disease risk and/or fecal deposits on houses. ther spilled or left in bowls (Table 1). However, 22% did not consider it a pest, Six survey participants noted seeing the and the remaining 11% were either indiffer- semi-slugs feeding in their covered compost ent or did not provide a response. The types of habitat where semi-slugs were found as determined by survey re- TABLE 2 sponses and our observations are summarized Types of Habitat Where Parmarion cf. martensi Was in Table 1 and Table 2, respectively. Many Collected during Daytime Site Visits survey participants reported that P. cf. mar- tensi demonstrated a remarkable propensity No. of to climb objects, including drainpipes, wood Location Properties decks, the walls of homes, water tanks, and On/under plastic or plasticlike materials, 10 barbeque grills. Although this climbing be- including black plastic sheeting, havior occurred mainly at night, its extent ground tarps, drainpipes, plant pots, tires was evidenced by the large number of fecal On palm fronds (fallen or within mulch pile) 4 deposits we saw on the upper walls of houses Under rocks or tiles 3 In covered compost 2 and on water tanks. Under banana trees 2 Respondents observed semi-slugs most On drainpipe 1 commonly on green plants, fallen fruits, and In citronella grass 1 plastic surfaces (Table 1), including four re- Under woven grass mat (‘‘goza’’) 1 ports on lettuce, two of them in home gar- Palm leaves (living) 1 Coconut shell halves (overturned) 1 dens and two involving lettuce purchased at Distribution of Parmarion cf. martensi on Hawai‘i Island . Hollingsworth et al. 463 bins or in trash cans, and we collected nu- choices consumed both flower and leaf mate- merous P. cf. martensi adults and egg masses rial. A similar preference for tender plant ma- from several covered compost bins. Two sur- terial was noted in containers holding both vey participants noted that P. cf. martensi red-leaved and green-leaved varieties of ti sometimes fed on ripe papaya still attached (Cordyline sp.): P. cf. martensi fed only slightly to the tree. on the red-leaved variety, which was more In our own daylight searches, P. cf. mar- tender than the green-leaved variety, and did tensi was most often found on or under plastic not feed on the green-leaved variety held in or other objects, including tires, tarps, black the same container. Veronicella cubensis dem- plastic sheeting, and drainpipes. Eggs found onstrated a preference for the red leaves but were generally in clutches of ca. 10–30 eggs also fed on the green-leaved variety. In con- each, laid inside overturned coconut shells, tainers holding a mixture of orchid flowers, underneath plastic plant pots, or attached to orchid leaves, and pseudobulb material, both the underside of plastic sheeting that was in mollusk species fed exclusively on flowers contact with the ground or compost. In one and avoided the other plant parts. case, eggs and neonate semi-slugs were found The average level of infection by A. canton- singly within rotting leaves of Alexander ensis in P. cf. martensi and V. cubensis was palms, Archontophoenix alexandrae (F. Muell.) 77.5 and 24.3%, respectively (Table 3). This H. Wendl. & Drude (Arecaceae). Our difference was significant (P ¼ 0:0007, based searches frequently found V. cubensis under- on logistic regression using generalized esti- neath plastic objects. However, unlike V. cu- mating equations procedure). In both species, bensis, P. cf. martensi life stages (including percentage infection was highest for large in- egg masses) were seldom found in direct con- dividuals (Table 3). tact with soil. Egg masses of the two species can be easily distinguished; eggs in the egg discussion masses of the Cuban slug are larger, are chained together, and a black threadlike ma- Our survey indicated that P. cf. martensi has terial (slug feces) runs through the masses. In essentially a continuous distribution in lower egg masses of P. cf. martensi, eggs are not elevations of the Puna district. Such a wide- chained together and no black threadlike ma- spread distribution is surprising for a species terial is present. whose presence was confirmed only in 2004. Survey participants were asked if they had However, two residents of Paradise Park pro- recently noted rats or mice on their property. vided credible reports of having first seen this Rats are the usual definitive host for Angio- strongylus cantonensis, and mice are potential hosts that can be infected in the laboratory. TABLE 3 Seventy-four percent and 48% of respon- Percentage Infectiona by Angiostrongylus cantonensis in dents, respectively, indicated that they had re- Slugs Collected from Five Sites in Hawai‘i Island cently noticed rats or mice on their property. None of those surveyed considered P. cf. Slug Species Size % Infecteda nb martensi to be a serious agricultural pest, and Veronicella cubensis Small 0 9 several people volunteered that P. cf. martensi Medium 0 2 did not eat plant leaves to the same extent as Large 34.6 26 V. cubensis. These observations were sup- All sizes 24.3 37 ported by results in laboratory bioassays com- Parmarion cf. martensi Neonate 100 1 paring the feeding preferences of these two Small 25 4 Medium 76.9 13 species. Parmarion cf. martensi semi-slugs Large 86.4 22 completely consumed a large, tender hibiscus All sizes 77.5 40 flower but left hibiscus leaves present within a Infection determined by PCR and confirmed by sequencing the same container untouched. In contrast, of PCR amplicons. V. cubensis presented with the same two b Number of slugs or semi-slugs analyzed. 464 PACIFIC SCIENCE . October 2007 species on their properties in 1999 and 2001. gin’’ listed as Vietnam, Thailand, Indonesia, The rapid spread of the semi-slugs in this or Malaysia [USDA APHIS PPQ Pest Inter- area has almost certainly been aided by the ception Database (PestID), Riverdale, Mary- activities of people. There has been a con- land]. struction boom in the lower Puna area during The ecological consequences of the inva- the past 6 yr, and it is likely that semi-slugs sion of P. cf. martensi into Hawai‘i are diffi- were transported between construction sites cult to predict. Anecdotal evidence suggests on building materials, building machinery, that P. cf. martensi has displaced V. cubensis as and in potted plants. The semi-slugs found the dominant large mollusk in certain resi- in South Hilo were in trash that had been dential areas. However, during our survey we dumped in an isolated area near Stainback frequently found both species in the same Highway (Figure 2). It is possible that the property. Our survey was based on a conve- semi-slugs were derived from trash that origi- nience sample, and information provided by nated in the Puna district. As for the presence respondents on pest status may constitute a of P. cf. martensi in North Kona, the owners biased sample of surveyed areas. The dietary of the residence have a second home in the habits of P. cf. martensi have not been studied Puna district (Paradise Park Subdivision), in detail, but V. cubensis is known as a serious and it is possible that semi-slugs were acci- pest of ornamental and garden crops in dentally transported from their Puna home Hawai‘i (Furutani and Arita-Tsutsumi 1998). to their Kona residence. After our survey was Many slug species are known to feed on a completed, an additional population of P. cf. wide variety of vegetable and animal matter, martensi was found in the town of Waimea including fruits, foliage, decaying vegetable (Northwest Hawai‘i Island) (Figure 1), de- matter, dead arthropods and earthworms, tected during a statewide survey for mollusk and algae and fungi that grow on surfaces of pests carried out by University of Hawai‘i re- plants, rocks, or wood (Ebeling 2002). Her- searchers. In their 2006 survey, P. cf. martensi bivorous slugs generally prefer tender plant was also found on the island of O‘ahu, in a tissues, such as flowers, plant seedlings, or plant nursery near Kahalu‘u and in a com- mature plants that have tender leaves or mercial farming area in Waima¯nalo (Kenneth stems. Larger species (>2.5 cm) are more Hayes, University of Hawai‘i, pers. comm., likely than smaller species to feed on healthy 2006). plant tissue. In feeding tests, P. cf. martensi As previously mentioned, the taxon Par- preferred flowers over leaves of the same spe- marion martensi is apparently native to South- cies and readily fed on fruits such as papaya. east Asia. It is not known how P. cf. martensi Acceptable foliage included lettuce, cabbage, arrived in Hawai‘i or whether its presence is and hibiscus leaves. The acceptability of these the result of a single introduction. Intercep- food sources to P. cf. martensi (a relatively tion data maintained by the U.S. Department large species, with extended length sometimes of Agriculture’s Animal and Plant Health >5 cm) is not surprising. What is unusual, Inspection Service indicate that semi-slugs relative to other slug species in Hawai‘i, is in the genus Parmarion were intercepted on the propensity of P. cf. martensi to climb and Dracaena plants shipped from Malaysia to locate rich food sources, including bird food, Kailua-Kona in July 2003. On two occasions dog food, cat food, fish entrails, and (February 2001 and April 2004), Parmarion (including fruit on the tree and fruit set out has been intercepted in Honolulu during pre- on the railing of a deck high off the ground). clearance inspections on plant material being This climbing behavior, in combination with exported to the U.S. mainland. Interception an apparent attraction to rich food sources records from 1996 to 2006 document seven and a naturally high rate of infection by A. other cases in which plants destined for loca- cantonensis, increases the likelihood that peo- tions in the United States were infested with ple will come into contact with semi-slugs ‘‘Parmarion.’’ Orchids were the infested com- and the parasitic nematodes they carry. modity in five of these seven cases, with ‘‘ori- Increased contact can occur when people Distribution of Parmarion cf. martensi on Hawai‘i Island . Hollingsworth et al. 465 handle items contaminated by semi-slugs on their water tanks. However, the majority or accidentally ingest a semi-slug or part of of survey respondents using catchment water one. Current evidence suggests that the slime said they did not use this water for drinking. of mollusks (if accidentally ingested on fruits Four respondents mentioned that they drank and vegetables) may not contain sufficient their catchment water, but all said they used numbers of A. cantonensis to cause disease particle filtering systems. symptoms (Hollingsworth and Cowie 2006). The association of P. cf. martensi with Accidental ingestion of the slugs themselves plastic and other smooth surfaces may indi- on poorly washed fruits and vegetables (con- cate a feeding preference for surface-growing sumed raw) probably represents a much algae or fungi, although semi-slugs were fre- greater risk and would presumably be more quently found on plastic apparently free of likely to occur when semi-slugs are very microorganism growth. Alternatively, the as- small. Our data show that even neonate P. cf. sociation could be related to water conserva- martensi can be hosts for A. cantonensis.One tion or could represent an adaptation for survey respondent reported finding neonate avoiding disease-causing organisms. Asato semi-slugs on her garden-grown lettuce; the et al. (2004) hypothesized that P. martensi is neonates were very difficult to see because of more susceptible to infection with A. canton- their small size (about 2 mm in length). Even ensis than ‘‘Veronicella alte’’ [an apparent mis- larger specimens could be accidentally con- naming of Laevicaulis alte (Fe´russac, 1821)] sumed on lettuce or other fresh greens if because of the lower density of muscle tissue these are not thoroughly washed and checked in the former species. Artificial infection by for semi-slugs before chopping. Further re- A. cantonensis was found to increase mortality search is necessary to determine whether rates in the aquatic snail Physa elliptica (Lea, neonates and very small semi-slugs carry a 1834) relative to snails in the experimental sufficient number of nematodes to potentially control (Wallace and Rosen 1969a). How- cause disease symptoms. ever, it is not clear whether infection by A. The climbing behavior of P. cf. martensi cantonensis increases mortality of mollusks on water tanks is a potential health concern generally. because of the chance that semi-slugs might Working in Malaysia, Lim and Heyneman transmit various types of disease organisms (1965) studied Microparmarion malayanus into drinking water. Contaminated drinking (Collinge) a semi-slug species in the same water is a potential source of A. cantonensis family as P. martensi. They noted that M. ma- infection for humans (Wallace and Rosen layanus climbed trees at night, was particu- 1969b). Cheng and Alicata (1964) found that larly common under heaps of dead palm infective-stage A. cantonensis were released leaves during the day, and was an important into water from both damaged and undam- carrier of A. cantonensis. We observed these aged Achatina fulica and Subulina octona (Bru- same characteristics in P. cf. martensi in Ha- guie`re, 1792) and survived in water for up to wai‘i. In Malaysia, M. malayanus was observed 72 hr. Similar results have been found for An- to feed on rat feces, and rats were observed to giostrongylus costaricensis Morera & Cespedes, feed on M. malayanus. These aspects of the 1971, released from the freshwater snail biology of. P. cf. martensi in Hawai‘i have Biomphalaria glabrata (Say) (Ubelaker et al. not been studied. However, their elucidation 1980). None of our survey respondents re- would be an important step toward under- ported finding P. cf. martensi inside their standing the importance of P. cf. martensi for water tanks, but we received such a report the epidemiology of angiostrongyliasis in subsequently. Many Puna residents rely on Hawai‘i. water collected from roofs for household use, including more than one-half of the respon- acknowledgments dents in our survey. Several respondents ex- pressed concerns about the possible health We thank Robert Cowie and Kenneth Hayes risks associated with P. cf. martensi climbing (University of Hawai‘i at Ma¯noa, Honolulu) 466 PACIFIC SCIENCE . October 2007 for providing additional information about slug, Veronicella cubensis (Pfeiffer) on taro. the distribution of P. cf. martensi in Hawai‘i J. Hawaii. Pac. Agric. 9:1–6. and for critically reviewing early drafts of the Graeff-Teixeira, C., and P. Morera. 1995. manuscript. 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