Distribution of Parmarion martensi and its potential as a vector for human Angiostrongyliasis

457

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

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. Robinson

Abstract: The semi-slug Parmarion cf. martensi Simroth, 1893, was ?rst 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 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 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.

T h e s e m i - s l u g

Parmarion cf. martensi Sim-

roth, 1893, is a recent introduction to the is-
land of Hawai?i. The ?rst record was made in
the summer of 2004 in Paradise Park, a resi-
dential 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 ?rst time
on the island of O?ahu in 1996 and provision-

Paci?c Science (2007), vol. 61, no. 4:457?467
Work of the U.S. Government
Not under copyright

Manuscript accepted 9 January 2007.

Corresponding

author

(phone:

808-959-4349;

e-mail: rholling@pbarc.ars.usda.gov).

U.S. Department of Agriculture, Agricultural Re-

search Service, U.S. Paci?c Basin Agricultural Research
Center, P.O. Box 4459, Hilo, Hawai?i 96720.

Current address: 190 Southwest Brumback Street,

Lin?eld College, McMinnville, Oregon 97128.

Centers for Disease Control and Prevention, 4770

Buford Highway Northeast, Atlanta, Georgia 30341.

Atlanta Research and Education Foundation in con-

junction with the Atlanta Veterans Administration Medi-
cal Center, Decatur, Georgia.

U.S. Department of Agriculture, Animal and Plant

Health Inspection Service, Plant Protection and Quaran-
tine, Academy of Natural Sciences, 1900 Benjamin
Franklin Parkway, Philadelphia, Pennsylvania 19103.

The ?ndings 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 identi?ed as Parmarion martensi Simroth,
1893 (Cowie 1997). The taxon Parmarion
martensi was originally described from Cam-
bodia (Simroth 1893), but it has also been
reported from Vietnam, Malay Peninsula, Su-
matra, Java, Borneo, Japan, Taiwan, Singa-
pore, 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 dif?-
culty 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 Is-
land, 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 infec-
tive larval stage in a slug or snail host (Mac-
kerras 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 con-
sumption of raw or undercooked slugs or
snails or paratenic hosts (such as shrimps or
?atworms) (i.e., animals capable of carrying
the infective stage of the parasite but not sup-
porting further development [Alicata and Jin-
drak 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 report-
edly contaminated with immature semi-slugs.
Important intermediate hosts of A. cantonensis
in Hawai?i include veronicellid slugs [pri-
marily the Cuban slug, Veronicella cubensis
(Pfeiffer, 1840)]; the giant African snail, Acha-
tina fulica (Bowdich, 1822); and the marsh

slug, Deroceras laeve (Mu?ller, 1774) (Wallace
and Rosen 1969a, Alicata 1991).

Parmarion cf. martensi has the potential for

becoming an important vector of A. canton-
ensis 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 indi-
cated that P. cf. martensi was extremely com-
mon; it was found in trash cans, in a
composting toilet, in an outdoor shower
area, in a planting of spider lilies (Crinum asi-
aticum [Amaryllidaceae]), under plastic sheet-
ing, 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 Con-
trol and Prevention (CDC), Atlanta, Georgia,
to be examined for infection. The 26 semi-
slugs examined were all positive for A. canton-
ensis, as determined by pepsin digestion
(Graeff-Teixeira and Morera 1995). The im-
portance of P. cf. martensi as a vector of this
disease may be exacerbated by its high popu-
lation densities, climbing behavior, attraction
to food items associated with human dwell-
ings, 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 be-
havior; (3) compare levels of infection of A.
cantonensis in P. cf. martensi and V. cubensis
collected from the same sites; and (4) com-
pare the feeding patterns of P. cf. martensi
and V. cubensis in the laboratory on selected
types of food.

m a t e r i a l s a n d m e t h o d s

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 dis-
tinguishing 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 ap-

458

PACIFIC SCIENCE

October 2007

peared in both newspapers on 15 July gener-
ated an even greater response.

Site visits were made to follow up all

credible reports of semi-slug sightings made
within 7 weeks of the initial newspaper adver-
tisement. Residents were asked where they
had seen this species on their property, what
types of food they had observed the semi-
slugs to eat, and whether they considered
this species a pest. At least 20 min per site
was spent collecting semi-slugs and other
mollusks. The locations where P. cf. martensi
were found were recorded.

Specimens collected from each site during

the July survey were sorted by species and
divided into size groups (large, medium,
small, or neonate). For V. cubensis and P. cf.
martensi, large specimens were about 4.5?5.5
cm and 3.5?4.5 cm long, respectively; me-
dium and small specimens were about one-
half and one-third as long, respectively, as
??large?? specimens of the same species. Neo-
nates were <0.5 cm in length. These speci-
mens were shipped on dry ice to the CDC,
where an experimental polymerase chain re-
action (PCR) method was used to determine
the percentage infected with A. cantonensis.
DNA from intact slug tissue pieces was ex-
tracted using one of two methods: either
using selected reagents from the FastDNA
kit (MP Biomedicals, Solon, Ohio) or the
DNeasy tissue kit (QIAGEN Inc., Valencia,
California). The FastDNA extraction was
performed as described previously (da Silva
et al. 1999) with one modi?cation: the sample
disruption was performed for 30 sec at speed
5.5 in the FastPrep 120 Disruptor (Q-
Biogene, Carlsbad, California). PCR inhibi-
tors were removed from DNA extracted with
FastDNA method by further puri?cation
with the QIAquick PCR puri?cation kit
(QIAGEN Inc., Valencia, California). DNA
extracted by the DNeasy tissue kit did not
need further puri?cation. The PCR method
ampli?ed 1,134 base pairs from the small sub-
unit ribosomal gene in Angiostrongylus species
(Qvarnstrom et al. 2007). Angiostrongylus-
speci?c

primers

AngioF1

-ATCA-

TAAACCTTTTTTCGAGTATCCAG-3

)

and

AngioR1

-TCTCGAGACAGCT-

CAGTCCCGG-3

) were designed based on

positions 456 to 482 and 1,569 to 1,590 of
Angiostrongylus cantonensis 18S rRNA gene;
GenBank entry AY295804. PCR was per-
formed with 0.4 mM of each primer, 2 ml of
DNA and AmpliTaq Gold PCR Master Mix
(Applied Biosystems, Foster City, California)
for a 50-ml total PCR reaction volume. PCR
cycling parameters were 95 C 5 min, 45
cycles of 95 C 15 sec, 65 C 15 sec, 72 C
1 min, and 72 C 10 min. To achieve iden-
ti?cation at species level, PCR ampli?ed
products were subjected to DNA sequence
analysis.

Data used to compare infection levels in P.

cf. martensi and V. cubensis were derived from
collections of mollusks from ?ve sites, each
of which contained multiple individuals of
each species. The statistical model consisted
of logistic regression implementing the gen-
eralized estimating equations (GEE) proce-
dure to adjust for correlation among mollusks
of the same species being collected from the
same site. Analyses were performed using
the GENMOD procedure of SAS on-line
version 9.1 (SAS Institute, Inc. 2000?2004).
Alpha was set at 0.05.

Feeding preferences of P. cf. martensi and

V. cubensis were compared in unreplicated
bioassays. The bioassay arena consisted of a
ventilated 2-liter plastic container holding
moist soil (about 2.5 cm deep) and three ma-
ture semi-slugs, held for 5 days in an environ-
mental chamber (27 C, 80% RH, 12:12 L:D).
Various types of plant foods were placed on
the soil surface after weighing. Data collected
included weights of plant material and obser-
vations of feeding damage.

r e s u l t s

The majority of the 51 survey respondents
were from the Puna district, although calls
were also received from residents in/near
Kailua-Kona

(West

Hawai?i),

Waimea

(Northwest Hawai?i), Honoka?a (Northeast
Hawai?i), Hilo (East Hawai?i), and Ocean
View Estates (South Hawai?i). Based on tele-
phone interviews, we determined that many
respondents had actually seen other types of
slugs. We con?rmed the presence of P. cf.
martensi at 27 of 29 properties that in our

Distribution of Parmarion cf. martensi on Hawai?i Island

Hollingsworth et al.

459

judgment were associated with credible sight-
ings of this semi-slug. The greatest concen-
tration of sightings was in the Paradise Park
Subdivision (Figures 1 and 2).

At the time of our survey, populations of

P. cf. martensi were very low throughout the

Puna district. At least four survey participants
independently noted that populations had
crashed within the previous 2?3 months. We
also observed such a decline on an organic
farm near Kapoho, near the eastern tip of
Hawai?i Island, where we had regularly been

F i g u r e

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.

460

PACIFIC SCIENCE

October 2007

preceding the publicity generated by survey
announcements. However, one respondent,
an organic gardener, claimed to have noticed
this species in lower Paradise Park in 1999.
This would be the earliest report of P. cf.
martensi on Hawai?i Island, and another resi-
dent @3 km distant remembered seeing the
semi-slug on his property in 2000 or 2001.
Sixty-seven percent of survey participants
considered this species a pest because of the
disease risk and/or fecal deposits on houses.
However, 22% did not consider it a pest,
and the remaining 11% were either indiffer-
ent or did not provide a response.

The types of habitat where semi-slugs

were found as determined by survey re-
sponses and our observations are summarized
in Table 1 and Table 2, respectively. Many
survey participants reported that P. cf. mar-
tensi demonstrated a remarkable propensity
to climb objects, including drainpipes, wood
decks, the walls of homes, water tanks, and
barbeque grills. Although this climbing be-
havior occurred mainly at night, its extent
was evidenced by the large number of fecal
deposits we saw on the upper walls of houses
and on water tanks.

Respondents observed semi-slugs most

commonly on green plants, fallen fruits, and
plastic surfaces (Table 1), including four re-
ports on lettuce, two of them in home gar-
dens and two involving lettuce purchased at

markets on the east side of Hawai?i Island.
There were ?ve reports of P. cf. martensi be-
ing attracted during daytime to food prepara-
tion and sink areas. In this context, several
respondents remarked that P. cf. martensi
moved more quickly than other slug species
they had seen around their houses, appearing
soon after food sources ?rst became available.
Five people reported semi-slugs feeding on
dog food, cat food, or parrot food that was ei-
ther spilled or left in bowls (Table 1).

Six survey participants noted seeing the

semi-slugs feeding in their covered compost

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)

On fallen fruit (avocado, guava, citrus, papaya, mango)

On/under plastic or plasticlike materials, including black plastic sheeting, tarps, drainpipes,

plant pots

In compost (especially covered compost) or inside trash cans

In food preparation and sink areas (outdoor sinks, on dishes, grills, on toothbrush)

In pet food bowls or eating spilled pet food

On deck or stairs

On concrete, tile, or asphalt

On walls of home

On palm fronds or trunks or under coconut shells

On catchment tank (on outside, under black saran cover at top)

On ripe papaya fruits (on tree)

In plant debris other than palms

TABLE 2

Types of Habitat Where Parmarion cf. martensi Was

Collected during Daytime Site Visits

Location

No. of

Properties

On/under plastic or plasticlike materials,

including black plastic sheeting,
ground tarps, drainpipes, plant pots, tires

On palm fronds (fallen or within mulch pile)

Under rocks or tiles

In covered compost

Under banana trees

On drainpipe

In citronella grass

Under woven grass mat (??goza??)

Palm leaves (living)

Coconut shell halves (overturned)

462

PACIFIC SCIENCE

October 2007

bins or in trash cans, and we collected nu-
merous P. cf. martensi adults and egg masses
from several covered compost bins. Two sur-
vey participants noted that P. cf. martensi
sometimes fed on ripe papaya still attached
to the tree.

In our own daylight searches, P. cf. mar-

tensi was most often found on or under plastic
or other objects, including tires, tarps, black
plastic sheeting, and drainpipes. Eggs found
were generally in clutches of ca. 10?30 eggs
each, laid inside overturned coconut shells,
underneath plastic plant pots, or attached to
the underside of plastic sheeting that was in
contact with the ground or compost. In one
case, eggs and neonate semi-slugs were found
singly within rotting leaves of Alexander
palms, Archontophoenix alexandrae (F. Muell.)
H. Wendl. & Drude (Arecaceae). Our
searches frequently found V. cubensis under-
neath plastic objects. However, unlike V. cu-
bensis, P. cf. martensi life stages (including
egg masses) were seldom found in direct con-
tact with soil. Egg masses of the two species
can be easily distinguished; eggs in the egg
masses of the Cuban slug are larger, are
chained together, and a black threadlike ma-
terial (slug feces) runs through the masses. In
egg masses of P. cf. martensi, eggs are not
chained together and no black threadlike ma-
terial is present.

Survey participants were asked if they had

recently noted rats or mice on their property.
Rats are the usual de?nitive host for Angio-
strongylus cantonensis, and mice are potential
hosts that can be infected in the laboratory.
Seventy-four percent and 48% of respon-
dents, respectively, indicated that they had re-
cently noticed rats or mice on their property.

None of those surveyed considered P. cf.

martensi to be a serious agricultural pest, and
several people volunteered that P. cf. martensi
did not eat plant leaves to the same extent as
V. cubensis. These observations were sup-
ported by results in laboratory bioassays com-
paring the feeding preferences of these two
species. Parmarion cf. martensi semi-slugs
completely consumed a large, tender hibiscus
?ower but left hibiscus leaves present within
the same container untouched. In contrast,
V. cubensis presented with the same two

choices consumed both ?ower and leaf mate-
rial. A similar preference for tender plant ma-
terial was noted in containers holding both
red-leaved and green-leaved varieties of ti
(Cordyline sp.): P. cf. martensi fed only slightly
on the red-leaved variety, which was more
tender than the green-leaved variety, and did
not feed on the green-leaved variety held in
the same container. Veronicella cubensis dem-
onstrated a preference for the red leaves but
also fed on the green-leaved variety. In con-
tainers holding a mixture of orchid ?owers,
orchid leaves, and pseudobulb material, both
mollusk species fed exclusively on ?owers
and avoided the other plant parts.

The average level of infection by A. canton-

ensis in P. cf. martensi and V. cubensis was
77.5 and 24.3%, respectively (Table 3). This
difference was signi?cant (P ? 0:0007, based
on logistic regression using generalized esti-
mating equations procedure). In both species,
percentage infection was highest for large in-
dividuals (Table 3).

d i s c u s s i o n

Our survey indicated that P. cf. martensi has
essentially a continuous distribution in lower
elevations of the Puna district. Such a wide-
spread distribution is surprising for a species
whose presence was con?rmed only in 2004.
However, two residents of Paradise Park pro-
vided credible reports of having ?rst seen this

TABLE 3

Percentage Infection

by Angiostrongylus cantonensis in

Slugs Collected from Five Sites in Hawai?i Island

Slug Species

Size

% Infected

Veronicella cubensis

Small

Medium

Large

34.6

All sizes

24.3

Parmarion cf. martensi

Neonate

100

Small

Medium

76.9

Large

86.4

All sizes

77.5

Infection determined by PCR and con?rmed by sequencing

of PCR amplicons.

Number of slugs or semi-slugs analyzed.

Distribution of Parmarion cf. martensi on Hawai?i Island

Hollingsworth et al.

463

species on their properties in 1999 and 2001.
The rapid spread of the semi-slugs in this
area has almost certainly been aided by the
activities of people. There has been a con-
struction boom in the lower Puna area during
the past 6 yr, and it is likely that semi-slugs
were transported between construction sites
on building materials, building machinery,
and in potted plants. The semi-slugs found
in South Hilo were in trash that had been
dumped in an isolated area near Stainback
Highway (Figure 2). It is possible that the
semi-slugs were derived from trash that origi-
nated in the Puna district. As for the presence
of P. cf. martensi in North Kona, the owners
of the residence have a second home in the
Puna district (Paradise Park Subdivision),
and it is possible that semi-slugs were acci-
dentally transported from their Puna home
to their Kona residence. After our survey was
completed, an additional population of P. cf.
martensi was found in the town of Waimea
(Northwest Hawai?i Island) (Figure 1), de-
tected during a statewide survey for mollusk
pests carried out by University of Hawai?i re-
searchers. In their 2006 survey, P. cf. martensi
was also found on the island of O?ahu, in a
plant nursery near Kahalu?u and in a com-
mercial farming area in Waima�nalo (Kenneth
Hayes, University of Hawai?i, pers. comm.,
2006).

As previously mentioned, the taxon Par-

marion martensi is apparently native to South-
east Asia. It is not known how P. cf. martensi
arrived in Hawai?i or whether its presence is
the result of a single introduction. Intercep-
tion data maintained by the U.S. Department
of Agriculture?s Animal and Plant Health
Inspection Service indicate that semi-slugs
in the genus Parmarion were intercepted on
Dracaena plants shipped from Malaysia to
Kailua-Kona in July 2003. On two occasions
(February 2001 and April 2004), Parmarion
has been intercepted in Honolulu during pre-
clearance inspections on plant material being
exported to the U.S. mainland. Interception
records from 1996 to 2006 document seven
other cases in which plants destined for loca-
tions in the United States were infested with
??Parmarion.?? Orchids were the infested com-
modity in ?ve of these seven cases, with ??ori-

gin?? listed as Vietnam, Thailand, Indonesia,
or Malaysia [USDA APHIS PPQ Pest Inter-
ception Database (PestID), Riverdale, Mary-
land].

The ecological consequences of the inva-

sion of P. cf. martensi into Hawai?i are dif?-
cult to predict. Anecdotal evidence suggests
that P. cf. martensi has displaced V. cubensis as
the dominant large mollusk in certain resi-
dential areas. However, during our survey we
frequently found both species in the same
property. Our survey was based on a conve-
nience sample, and information provided by
respondents on pest status may constitute a
biased sample of surveyed areas. The dietary
habits of P. cf. martensi have not been studied
in detail, but V. cubensis is known as a serious
pest of ornamental and garden crops in
Hawai?i (Furutani and Arita-Tsutsumi 1998).
Many slug species are known to feed on a
wide variety of vegetable and animal matter,
including fruits, foliage, decaying vegetable
matter, dead arthropods and earthworms,
and algae and fungi that grow on surfaces of
plants, rocks, or wood (Ebeling 2002). Her-
bivorous slugs generally prefer tender plant
tissues, such as ?owers, plant seedlings, or
mature plants that have tender leaves or
stems. Larger species (>2.5 cm) are more
likely than smaller species to feed on healthy
plant tissue. In feeding tests, P. cf. martensi
preferred ?owers over leaves of the same spe-
cies and readily fed on fruits such as papaya.
Acceptable foliage included lettuce, cabbage,
and hibiscus leaves. The acceptability of these
food sources to P. cf. martensi (a relatively
large species, with extended length sometimes
>

5 cm) is not surprising. What is unusual,

relative to other slug species in Hawai?i, is
the propensity of P. cf. martensi to climb and
locate rich food sources, including bird food,
dog food, cat food, ?sh entrails, and papayas
(including fruit on the tree and fruit set out
on the railing of a deck high off the ground).
This climbing behavior, in combination with
an apparent attraction to rich food sources
and a naturally high rate of infection by A.
cantonensis, increases the likelihood that peo-
ple will come into contact with semi-slugs
and the parasitic nematodes they carry.
Increased contact can occur when people

464

PACIFIC SCIENCE

October 2007

handle items contaminated by semi-slugs
or accidentally ingest a semi-slug or part of
one. Current evidence suggests that the slime
of mollusks (if accidentally ingested on fruits
and vegetables) may not contain suf?cient
numbers of A. cantonensis to cause disease
symptoms (Hollingsworth and Cowie 2006).
Accidental ingestion of the slugs themselves
on poorly washed fruits and vegetables (con-
sumed raw) probably represents a much
greater risk and would presumably be more
likely to occur when semi-slugs are very
small. Our data show that even neonate P. cf.
martensi can be hosts for A. cantonensis. One
survey respondent reported ?nding neonate
semi-slugs on her garden-grown lettuce; the
neonates were very dif?cult to see because of
their small size (about 2 mm in length). Even
larger specimens could be accidentally con-
sumed on lettuce or other fresh greens if
these are not thoroughly washed and checked
for semi-slugs before chopping. Further re-
search is necessary to determine whether
neonates and very small semi-slugs carry a
suf?cient number of nematodes to potentially
cause disease symptoms.

The climbing behavior of P. cf. martensi

on water tanks is a potential health concern
because of the chance that semi-slugs might
transmit various types of disease organisms
into drinking water. Contaminated drinking
water is a potential source of A. cantonensis
infection for humans (Wallace and Rosen
1969b). Cheng and Alicata (1964) found that
infective-stage A. cantonensis were released
into water from both damaged and undam-
aged Achatina fulica and Subulina octona (Bru-
guie`re, 1792) and survived in water for up to
72 hr. Similar results have been found for An-
giostrongylus costaricensis Morera & Cespedes,
1971, released from the freshwater snail
Biomphalaria glabrata (Say) (Ubelaker et al.
1980). None of our survey respondents re-
ported ?nding P. cf. martensi inside their
water tanks, but we received such a report
subsequently. Many Puna residents rely on
water collected from roofs for household use,
including more than one-half of the respon-
dents in our survey. Several respondents ex-
pressed concerns about the possible health
risks associated with P. cf. martensi climbing

on their water tanks. However, the majority
of survey respondents using catchment water
said they did not use this water for drinking.
Four respondents mentioned that they drank
their catchment water, but all said they used
particle ?ltering systems.

The association of P. cf. martensi with

plastic and other smooth surfaces may indi-
cate a feeding preference for surface-growing
algae or fungi, although semi-slugs were fre-
quently found on plastic apparently free of
microorganism growth. Alternatively, the as-
sociation could be related to water conserva-
tion or could represent an adaptation for
avoiding disease-causing organisms. Asato
et al. (2004) hypothesized that P. martensi is
more susceptible to infection with A. canton-
ensis than ??Veronicella alte?? [an apparent mis-
naming of Laevicaulis alte (Fe?russac, 1821)]
because of the lower density of muscle tissue
in the former species. Arti?cial infection by
A. cantonensis was found to increase mortality
rates in the aquatic snail Physa elliptica (Lea,
1834) relative to snails in the experimental
control (Wallace and Rosen 1969a). How-
ever, it is not clear whether infection by A.
cantonensis increases mortality of mollusks
generally.

Working in Malaysia, Lim and Heyneman

(1965) studied Microparmarion malayanus
(Collinge) a semi-slug species in the same
family as P. martensi. They noted that M. ma-
layanus climbed trees at night, was particu-
larly common under heaps of dead palm
leaves during the day, and was an important
carrier of A. cantonensis. We observed these
same characteristics in P. cf. martensi in Ha-
wai?i. In Malaysia, M. malayanus was observed
to feed on rat feces, and rats were observed to
feed on M. malayanus. These aspects of the
biology of. P. cf. martensi in Hawai?i have
not been studied. However, their elucidation
would be an important step toward under-
standing the importance of P. cf. martensi for
the epidemiology of angiostrongyliasis in
Hawai?i.

a c k n o w l e d g m e n t s

We thank Robert Cowie and Kenneth Hayes
(University of Hawai?i at Ma�noa, Honolulu)

Distribution of Parmarion cf. martensi on Hawai?i Island

Hollingsworth et al.

465

for providing additional information about
the distribution of P. cf. martensi in Hawai?i
and for critically reviewing early drafts of the
manuscript.

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467