Published online: 27 April 2018

Records of the Hawaii Biological Survey for 2017. Edited by Neal L.
Evenhuis. Bishop Museum Occasional Papers 123: 19–24 (2018)ISSN (online): 2376-3191

Rat Lungworm (Angiostrongylus cantonensis) in Hawai‘i:
Updated Host Gastropod Records and Distributions on Maui1NORINE W. YEUNG2,3, JAYNEE R. KIM & KENNEtH A. HAYES2,3Hawaii Biological Survey, Bishop Museum, 1525 Bernice Street, Honolulu, Hawai‘i 96817, USA;
Emails: norine@bishopmuseum.org. kenneth.hayes@bishopmuseum.org, jaynee@hawaii.edu

INTRODUCTION
Rat lungworm (RLW), Angiostrongylus cantonensis, is an emerging infectious disease
that causes eosinophilic meningitis. the first reported case of angiostrongyliasis inHawai‘i was in 1961 (Horio & Alicata 1961) and between 2001 and 2016, 85 cases of thisdisease were reported (Cowie 2017), three of which were fatal. this is nearly four and ahalf times as many cases (19) as reported from 1959 to 2000 (Cowie 2017). Kim et al.
(2014) in their state-wide assessment of intermediate hosts (gastropods) for RLW foundthat 16 of the 37 species tested carried the parasite, including two native species.
the report of recent cases of eosinophilic meningitis from Maui (Cowie 2017)
prompted increased interest in identifying the potential host gastropods and developing abetter understanding of the distribution of RLW hosts across the island. As such, surveys
for gastropods were conducted December 2016–August 2017, and resulted in the collection of 205 non-native land snails representing 21 species from 13 sites across Maui (Fig.
1), all of which were screened for rat lungworm using the non-quantitative PCR approachfrom Kim et al. (2014).
Nine species from these recent collections tested positive for RLW. Of these, twowere new island records as hosts for the parasite, and one is a new state record, never having been reported as a carrier of RLW in Hawai‘i. In total, this brings the number of gastropod hosts for RLW in Hawai‘i to 21. Knowing which snails serve as vectors for theRLW and their distributions on each island is critical to developing effective management
and educational outreach strategies to protect the public and natural ecosystems.
Collections were made by Norine W. Yeung (NWY), Jaynee R. Kim (JRK), Keahi
M. Bustamente (KMB) and Kenneth A. Hayes (KAH). All collected material are deposited in the Bishop Museum (BPBM) Malacology collection. Catalog numbers are BPBM
Malacology collection numbers. Latitude and longitude coordinates were recorded by
GPS. Many areas are owned privately, therefore, exact locations are kept in the State ofHawai‘i Invasive Species Council and Bishop Museum Malacology databases.

1. Contribution No. 2018-004 the Hawaii Biological Survey.
2. Research Affiliate, Pacific Biosciences Research Center, University of Hawai‘i, 3050 Maile Way, Gilmore 408,Honolulu, Hawai‘i 96822, USA
3. Research Collaborator, Smithsonian Institution, National Museum of Natural History, PO Box 37012, MRC 163,Washington, DC, 20013, USA

20BISHOP MUSEUM OCCASIONAL PAPERS: No. 123, 2018

Figure 1. Sites surveyed on Maui as part of this study. Red circles are sites with non-native landsnails that were positive for RLW. Yellow circles sites with non-native snails that tested negative forRLW. Map created in QGIS v. 2.18.

Achatinidae
Lissachatina fulica (Bowdich, 1822)(Fig. 2A)
this species, also known as the giant African snail, was first recorded in Hawai‘i in 1936
and is present on all main Hawaiian Islands (Cowie 1997). Wallace & Rosen (1969) firstreported this species on O‘ahu as a RLW host, and 11.3% (7/62) of the individuals tested
were positive in Kim et al. (2014), while only 10% (1/10; BPBM 284201) were positive
among the 15 collected (BPBM 284187, 284201, 284211, 284219, 284247).

Agriolimacidae
Deroceras laeve (Müller, 1774)
New Island Record for Gastropod Host(Fig. 2B)
this Western European snail (Kerney & Cameron 1979) was first recorded in Hawai‘i in1897 and considered wide spread on all the main Hawaiian Islands (Cowie 1997). thisFigure 2 (opposite page). A) Lissachatina fulica (shell length = 10 cm); B) Deroceras laeve (length= 1.5 cm); C) Deroceras reticulatum (length = 2.0 cm); D) Parmarion martensi (length = 4.0 cm); E)
Bradybaena similaris (shell diameter = 1.0 cm); F) Cornu aspersum (shell diameter = 3.0 cm); G)
Euglandina rosea (shell length = 5.0 cm); H) Laevicaulis alte (length = 7.0 cm); I) Veronicellacubensis (length = 7.0 cm).

HBS Records for 20172122BISHOP MUSEUM OCCASIONAL PAPERS: No. 123, 2018

species was first reported as a carrier of RLW on O‘ahu by Wallace & Rosen (1969), but
none of the individuals tested by Kim et al. (2014) were positive. In this study, ~56%
(10/18) of individuals tested were positive (BPBM 284177, 284191, 284194, 284228,284234, 284239) from a total sample of 21 individuals collected (BPBM 284177, 284191,284194, 284228, 284234, 284239, 284252).

Deroceras reticulatum (Müller, 1774)(Fig. 2C)
this Western European species (Kerney & Cameron 1979) was first recorded in Hawai‘iin 1963 and is found on all main Hawaiian Islands (Cowie 1997, Hayes et al. 2012). Kimet al. (2014) first reported this species in Hawai‘i as a RLW carrier. Nine individuals werecollected (BPBM 284178, 284195) and three out of six (50%) individuals tested positivein this study (BPBM 284178, 284195).

Ariophantidae
Parmarion martensi Simroth, 1893
(Fig. 2D)First recorded from the islands in 1996 on O‘ahu, then on Hawai‘i Island, and more
recently spread to Maui (Cowie 1997; Cowie et al. 2008, 2018), but went unnoticed until
2017 when it became anecdotally associated with multiple cases of angiostrongyliasis on
Maui (Howe & Jarvi 2017). Hollingsworth et al. (2007) first reported this species onHawai‘i Island as a RLW carrier with 77.5% of specimens screened testing positive. Kimet al. (2014) found a similar rate of infection, with 70% of specimens tested being carriers.
Fifty-three individuals were collected (BPBM 284202, 284212, 284220) for this study,
but only five out of 16 (31%) individuals screened tested positive (BPBM 284202,284220), a considerably lower rate of infection than found in Hawai‘i Island populations.

Bradybaenidae
Bradybaena similaris (Férussac, 1821)
New Island Record for Gastropod Host(Fig. 2E)
Commonly known as the Asian tramp snail, this species was first recorded in Hawai‘i in1893 and is considered established throughout the main Hawaiian Islands (Cowie 1997).
Similar to the Deroceras laeve account, Wallace & Rosen (1969) first reported this specieson O‘ahu as a RLW carrier, but none of the individuals tested by Kim et al. (2014) werepositive. However, twenty-eight individuals were collected (BPBM 284181, 284192,284235, 284240) for this study, and one of the fourteen (7%) individuals screened waspositive (BPBM 284240). It is possible that this species may be less susceptible to A. cantonensis infection in general, or just here in the islands, when compared to other species(Kim et al. 2014).

Helicidae
Cornu aspersum (Müller, 1774)
New State Record for Gastropod Host(Fig. 2F)
the brown garden snail is native throughout the Mediterranean and Western Europe(Kerney & Cameron 1979, Cowie 1997). It was first recorded in Hawai‘i in 1952 onO‘ahu, and subsequently on Kaua‘i, Maui and Hawai‘i Island, but and is currently considered established only on Maui and Hawai‘i (Cowie 1997). twelve individuals were

HBS Records for 201723

collected (BPBM 284179, 284188, 284193, 284196, 284237) for this study, and of these,
20% (2/10; BPBM 284196) were positive. this is the first record of Cornu aspersum as acarrier of RLW in the islands.

Spiraxidae
Euglandina rosea (Férussac, 1821)(Fig. 2G)
this predatory snail species was first introduced to Hawai‘i in 1955 as a biological control
agent for the giant African snail Lissachatina fulica (Cowie 1997). During this introduction, two species were inadvertently introduced, and it is likely that neither is the true
Euglandina rosea (Meyer et al. 2017). However, here, we refer it to E. rosea until this isresolved. It has been reported from all the main Hawaiian Islands, but only as shells onLāna‘i (Hayes et al. 2007; Meyer et al. 2017). Wallace & Rosen (1969) first reported thisspecies on O‘ahu as a RLW carrier and eight of the thirty-nine individuals tested positivein Kim et al. (2014). three individuals were collected (BPBM 284230, 284241, 284256),
but only one (33%) of these was positive in this study (BPBM 284230).

Veronicellidae
Laevicaulis alte (Férussac, 1822)(Fig. 2H)
the tropical leatherleaf was first recorded from Hawai‘i Island in 1900 (Cowie 1997), but
is currently found on all main Hawaiian Islands and Midway Atoll (Hayes et al. 2007,Cowie et al. 2008). Wallace & Rosen (1969) first reported this species from O‘ahu as aRLW carrier, and 13 of the 44 individuals tested positive by Kim et al. (2014) were positive. Notably, one of these individuals had the highest parasite load in that study. twelve(BPBM 284185, 284209, 284217, 284244) individuals were collected for this study, andtwo (BPBM 284209) of nine (22%) were positive for RLW.

Veronicella cubensis (Pfeiffer, 1840)(Fig. 2I)
this species, known as the Cuban slug, was first recorded in Hawai‘i in 1985 (Cowie1997) and is currently found on all main Hawaiian Islands (Hayes et al. 2007, Cowie etal. 2008). Qvarnstrom et al. (2007) first reported this species from Hawai‘i as a RLW carrier, and only 2.5% (4/159) of individuals screened by Kim et al. (2014) were positive.
However, this study found double that rate (5%). Only two (5%) out of 39 individuals tested positive in this study (BPBM 284233, 284259) from 122 individuals collected (BPBM284186, 284190, 284210, 284218, 284226, 284233, 284245, 284250, 284259).

ACKNOWLEDGMENTS
this study was supported in part by grants from the Hawai‘i Community Foundation (viaAdam Radford, Maui Invasive Species Council), U.S. Department of Agriculture,
Cooperative Agricultural Pest Survey program to NWY and KAH, National Science
Foundation grants to NWY, KAH, John Slapcinsky (DEB-1656254, 1656231) and to
NWY, KAH (DBI-1561774). We thank Caroline Owens, Amma Boateng, Uduak Udoh,
and Megan Paustian (Howard University) for assistance with specimen processing.

24BISHOP MUSEUM OCCASIONAL PAPERS: No. 123, 2018

LITERATURE CITED
Cowie, R.H. 2017. Angiostrongylus cantonensis: agent of a sometimes fatal globallyemerging infectious disease (rat lungworm disease). ACS Chemical Neuroscience 8:2102–2104.
Cowie, R.H. 2018. Parmarion martensi Simroth, 1893 (Gastropoda: Ariophantidae), anintermediate host of Angiostrongylus cantonensis (rat lungworm), on Maui. Bishop
Museum Occasional Papers 123: 7–10.
Cowie, R.H., Hayes, K.A., Tran, C.T. & Meyer, W.M., III. 2008. the horticulturalindustry as a vector of alien snails and slugs: widespread invasions in Hawaii.
International Journal of Pest Management 54: 267–276.
Hayes, K.A., Tran, C.T. & Cowie, R.H. 2007. New records of alien Mollusca in theHawaiian Islands: nonmarine snails and slugs (Gastropoda) associated with the horticultural trade. Bishop Museum Occasional Papers 96: 54–63.
Hayes, K.A., Yeung, N.W., Kim, J.R. & Cowie, R.H. 2012. New records of alien
Gastropoda in the Hawaiian Islands: 1996–2010. Bishop Museum Occasional Papers
112: 21–28.
Hollingsworth, R.G., Kaneta, R., Sullivan, J.J., Bishop, H.S., Qvarnstrom, Y., Silva,
A.J. da & Robinson, D.G. 2007. 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. Pacific Science 61: 457–467.
Horio, S.R. & Alicata, J.E. 1961. Parasitic meningo-encephalitis in Hawai‘i. A new parasitic disease of man. Hawaii Medical Journal 21: 139–140.
Howe, K. & Jarvi, S.I. 2017. Angiostrongyliasis (rat lungworm disease): viewpoints
from Hawai‘i Island. ACS Chemical Neuroscience 8: 1820–1822.
Kerney, M.P. & Cameron, R.A.D. 1979. A field guide to the land snails of Britain andNorthwest Europe. Harper Collins Publishers, London. 288 pp.
Kim, J.R., Hayes, K.H, Yeung, N.W. & Cowie, R.H. 2014. Diverse gastropod hosts ofAngiostrongylus cantonensis, the rat lungworm, globally and with a focus on theHawaiian Islands. PLoS One 9: e94969.
Meyer, W.M., III, Yeung, N.W., Slapcinsky, J. & Hayes, K.A. 2017. two for one: inadvertent introduction of Euglandina species during failed bio-control efforts inHawaii. Biological Invasions 19: 1399–1405.
Qvarnstrom, Y., Sullivan, J.J., Bishop, H.S., Hollingsworth, R. & Silva, A.J. da 2007.
PCR-based detection of Angiostrongylus cantonensis in tissue and mucus secretions
from molluscan hosts. Applied and Environmental Microbiology 73: 1415–1419.
Wallace, G.D. & Rosen, L. 1969. Studies on eosinophilic meningitis. V. Molluscan hostsof Angiostrongylus cantonensis on Pacific islands. American Journal of TropicalMedicine and Hygiene 18: 206–216.