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FEEDING PREFERENCES OF TWO PREDATORY SNAILS INTRODUCED
TO HAWAII AND THEIR CONSERVATION IMPLICATIONS
Wallace M. Meyer III1, 2* & Robert H. Cowie1
ABSTRACT
Two introduced predatory land snails, Euglandina rosea and Oxychilus alliarius, have been
LPSOLFDWHGLQWKHGHFOLQHRIQDWLYH+DZDLLDQDQG3DFL¿FLVODQGODQGVQDLOV:HH[DPLQHGWKH
feeding ecology of E. rosea and O. alliariusIRFXVLQJ¿UVWRQSUH\VL]HDQGVSHFLHVSUHIHUHQFHV
and second on quantifying consumption rates, which is necessary to address the possible
OHYHOVRILPSDFWRQQDWXUDOSRSXODWLRQV,QSUH\VL]HSUHIHUHQFHH[SHULPHQWVE. rosea always
FRQVXPHGPRUHVQDLOVLQWKHVPDOOHUVL]HFODVV,QSUH\VSHFLHVSUHIHUHQFHH[SHULPHQWVE.
roseaSUHIHUUHGVQDLOVWRVOXJVEXWVKRZHGQRSUHIHUHQFHDPRQJVQDLOVSHFLHV6L]HSUHIHUHQFHH[SHULPHQWVLQGLFDWHGWKDWO. alliarius will only consume prey less than 3 mm in shell
OHQJWK,QSUH\VSHFLHVSUHIHUHQFHH[SHULPHQWVO. alliarius consumed every snail species
offered but did not consume either of the slug species. Consumption rates were positively
UHODWHGWRWKHVL]HRIWKHSUHGDWRUZLWKWKHODUJHUSUHGDWRUE. rosea, having a much higher
consumption rate than O. alliarius, and with larger E. rosea consuming more than smaller E.
rosea7KHVHUHVXOWVKDYHXQIRUWXQDWHFRQVHUYDWLRQUDPL¿FDWLRQVEHFDXVHVLQFHWKH\LQGLFDWH
that both E. rosea and O. alliarius are generalist snail predators feeding preferentially on the
VPDOOHVWVQDLOVDOWKRXJKWKH\UDUHO\HDWVOXJV6LQFHPDQ\H[WDQW+DZDLLDQDQG3DFL¿FLVODQG
snail species are small, they are at risk of predation by these two introduced predators, while
invasive slugs – there are no native slugs in Hawaii – may not be impacted by them.
Key words: consumption rate, Euglandina rosea, Gastropoda, Oxychilus alliarius, slug.
INTRODUCTION
/DQGVQDLOIDXQDVZRUOGZLGHDUHXQGHUH[treme threat, and have the dubious honor of
KDYLQJWKHKLJKHVWQXPEHURIGRFXPHQWHGH[WLQFWLRQVRIDQ\PDMRUWD[RQRPLFJURXS&RZLH
2004; Nash, 2004; Lydeard et al., 2004). The
2008 IUCN Red List of Threatened Species
,8&1LQFOXGHGJDVWURSRGVVQDLOV
DQGVOXJVRIZKLFKZHUHOLVWHGDVH[WLQFW
1DWLYH3DFL¿FLVODQGODQGVQDLOVLQSDUWLFXODU
DUH UHFRJQL]HG IRU WKHLU GLYHUVLW\ KLJK OHYHOV
of endemism and the fact that they are under
H[WUHPHWKUHDWZLWKSHUKDSVDVPDQ\DV
RI WKH VSHFLHV KDYLQJ GLVDSSHDUHG /\GHDUG
HW DO )RU H[DPSOH H[WLQFWLRQ RI WKH
WUHHVQDLO VSHFLHV $FKDWLQHOOLQDH LQ +DZDLL
DQG 3DUWXOLGDH RQ RWKHU 3DFL¿F LVODQGV KDV
EHHQFDWDVWURSKLF&ODUNHHWDO+DG¿HOG
0XUUD\HWDO&RZLH+DG¿HOGHWDO&RRWH/RqYH
In Hawaii, the situation may be especially
critical. The native Hawaiian land-snail fauna
XVHGWREHH[WUHPHO\GLYHUVHRYHUVSHFLHVDQGH[KLELWHGH[WUHPHO\KLJKHQGHPLVP
RYHU&RZLHHWDOEXWHVWLPDWHV
RIH[WLQFWLRQRIWKHVHXQLTXHVSHFLHVUDQJHIURP
±6ROHPWR&RZLH
/\GHDUGHWDO)RUH[DPSOHWKH$PDVWULdae, an endemic Hawaiian family of more than
VSHFLHV&RZLHHWDOPD\QRZEH
UHGXFHGWRDVIHZDVWHQRUVRVSHFLHVH[LVWLQJ
LQWLQ\KLJKO\ORFDOL]HGUHPQDQWSRSXODWLRQV
The Endodontidae in Hawaii and throughout
WKH3DFL¿FDSSHDUUHGXFHGWRVSDUVHSRSXODtions on those islands they formerly inhabited
/\GHDUGHWDO0H\HU
Two introduced predatory land snails, Euglandina rosea and Oxychilus alliarius, have been
implicated in the decline of the native land-snail
faunas. Euglandina rosea was purposely introGXFHGWR+DZDLLLQWRFRQWUROSRSXODWLRQV
1&HQWHUIRU&RQVHUYDWLRQ5HVHDUFKDQG7UDLQLQJ3DFL¿F%LRVFLHQFHV5HVHDUFK&HQWHU8QLYHUVLW\RI+DZDLLDW0DQRD
0DLOH:D\*LOPRUH+RQROXOX+DZDLL86$
2'HSDUWPHQWRI=RRORJ\8QLYHUVLW\RI+DZDLLDW0DQRD0F&DUWK\0DOO(GPRQVRQ+RQROXOX+DZDLL86$
*Corresponding author: [email protected]
135
MEYER & COWIE
of another introduced snail, Achatina fulica,
WKHJLDQW$IULFDQVQDLO'DYLV%XWOHU
6LPEHUORII&LYH\UHO6LPEHUORII
Cowie, 2001). Subsequently, it was introduced
HOVHZKHUH 0HDG DQG LV QRZ ZLGHO\
GLVWULEXWHG WKURXJKRXW WKH 3DFLILF &RZLH
2001; Cowie et al., 2008). Unfortunately, the
introduction of E. rosea has not reduced A.
fulicaSRSXODWLRQV&LYH\UHO6LPEHUORII
Cowie, 2001), but has been associated with
the decline of many of the tree-snail species,
QRWRQO\LQ+DZDLLEXWHOVHZKHUHLQWKH3DFL¿F
&ODUNHHWDO+DG¿HOG+DG¿HOGHW
DO0XUUD\*HUODFK&RRWH
/RqYHDQGPD\KDYHFDXVHGWKHH[WLQFWLRQRIRWKHUQDWLYHODQGVQDLOVSHFLHV&RZLH
1DWLYHWR(XURSHO. alliarius was
¿UVWUHFRUGHGLQWKH+DZDLLDQ,VODQGVLQ
&RZLH,JQRUHGXQWLOPRUHUHFHQWO\O.
alliarius KDV EHFRPH H[WUHPHO\ DEXQGDQW RQ
WKHLVODQGVRI0DXL6HYHUQVDQG+DZDLL
0H\HU &RZLH LQ SUHVV DQG QRZ RFFXUV
DOVRRQ0RORNDLDQG.DXDL&RZLHDQG
RQ 2DKX : 0 0 SHUVRQDO REVHUYDWLRQ
Oxychilus alliarius is omnivorous, but is known
as a snail predator; it may have played a role
in the decline of the native Hawaiian land snail
fauna, as it is thought to have done in New
=HDODQG%DUNHU(IIRUGDQGLWFRXOG
EH D WKUHDW WR WKH UHPDLQLQJ H[WDQW VSHFLHV
6HYHUQV
Certain aspects of the feeding ecology of E.
rosea have been studied, including feeding
EHKDYLRUDQGSUH\WUDLOIROORZLQJ&RRND
E*HUODFKSUH\VL]HSUHIHUHQFHV&KLX
&KRX'DYLV%XWOHU1LVKLGD
1DSRPSHWK&RRNDE*HUODFK
DQGSUH\VSHFLHVVHOHFWLRQLQWKHZLOG
*ULI¿WKVHWDO+RZHYHUH[WUDSRODWLQJ
from these results to determine the effect E.
rosea is having on land snail faunas as a whole
LV GLI¿FXOW HVSHFLDOO\ EHFDXVH FRQVXPSWLRQ
rates and the reasons for prey preferences
have not been adequately addressed. For
LQVWDQFHH[SHULPHQWVWKDWDGGUHVVHGVSHFLHV
SUHIHUHQFHVGLGQRWFRQWUROIRUSUH\VL]HDPRQJ
SUH\VSHFLHVRIIHUHG&RRNDE,QVWHDG
WRWDOZHLJKWRIHDFKVSHFLHVZDVVWDQGDUGL]HG
+RZHYHULISUH\VL]HLVDVLPSRUWDQWDVVXJJHVWHG &KLX &KRX 'DYLV %XWOHU
1LVKLGD 1DSRPSHWK &RRN
DEWKHIDFWWKDWWKHVPDOOHUVSHFLHVZHUH
SUHIHUUHG LQ FKRLFH H[SHULPHQWV WHOOV XV OLWWOH
DERXW SUHIHUHQFHV IRU VSHFL¿F VSHFLHV$OVR
WKH PLFURFRVPV XVHG LQ WKHVH H[SHULPHQWV
FOHDUJODVVGLVKHVGLGQRWSURYLGHFRQGLWLRQV
permitting all possible predator avoidance
behaviors. We know of no reports of feeding
SUHIHUHQFHH[SHULPHQWVRQO. alliarius.
Despite the two predators’ reputations,
relatively little attention has been paid to the
ELRORJ\RIHLWKHU2XUREMHFWLYHZDVWRH[DPLQH
the feeding ecology of E. rosea and O. alliarius,
IRFXVLQJ¿UVWRQSUH\VL]HDQGVSHFLHVSUHIHUences, and second on quantifying consumption
rates in order to address the possible levels of
impact on natural populations.
METHODS
$OOH[SHULPHQWVZHUHFRQGXFWHGZLWKVQDLOV
collected from the wild less than one month
previously. They were allowed to acclimate to
laboratory conditions for at least three days
SULRUWRDQ\H[SHULPHQWV%RWKSUHGDWRUVSHcies were fed a diet of Bradybaena similaris, a
common invasive snail in Hawaii. Bradybaena
similaris was not used as a prey species in
WKHVXEVHTXHQWH[SHULPHQWV$OODQLPDOVZHUH
maintained in the same kind of containers as
WKRVHXVHGLQWKHH[SHULPHQWV[[
cm for E. rosea[[FPIRUO. alliarius.
/DERUDWRU\WHPSHUDWXUHVZHUH±ƒ&GXULQJ
WKHH[SHULPHQWV
Different methods were used to assess
the feeding behavior of each predator, since
E. rosea has a much higher consumption
rate than O. alliarius. The primary difference
EHWZHHQWKHPHWKRGVZHUHWKDWH[SHULPHQWV
H[DPLQLQJ E. rosea SUHIHUHQFHV SUH\ VL]H
DQG VSHFLHV ZHUH FKRLFH H[SHULPHQWV ZLWK
individual predators given a choice between
two prey options, while O. alliariusH[SHULPHQWV
were no-choice, as each predator was only offered one prey option. A different individual was
used as a predator for every replicate across
DOOH[SHULPHQWV)RUWKHE. roseaH[SHULPHQWV
because hundreds of prey individuals were
required, we used only non-native species,
IURP ¿YH GLVWLQFW IDPLOLHV WZR VOXJ VSHFLHV
Veronicella cubensis, Deroceras laeve) and
WKUHHVQDLOVSHFLHVAchatina fulica, Paropeas
achatinaceum, Succinea tenella). These species are phylogenetically diverse, such that the
results should be generalisable. Inclusion of a
species of non-native Succineidae, a family
WKDW KDV SURSRUWLRQDWHO\ PRUH H[WDQW QDWLYH
VSHFLHVLQ+DZDLLWKDQDQ\RWKHUIDPLO\5XQGHOOHWDODOVRSURYLGHVPRUHVSHFL¿F
relevance to the local fauna. Given the much
lower consumption rates of O. alliarius, it was
PREDATORY SNAILS IN HAWAII
reasonable to include native species as prey
Succinea spp., Philonesia sp., Tornatellides
spp.) in addition to common invasive species
Arion intermedius, Deroceras laeve, Paropeas
achatinaceum), all of which occur in areas in
Hawaii with abundant O. alliarius.
137
We have only seen O. alliarius feed via the
aperture, as opposed to consuming the entire
prey snail including its shell. Differences in
PRUWDOLW\ EHWZHHQ FRQWURO DQG H[SHULPHQWDO
WUHDWPHQWV IRU HDFK VL]H FODVV ZHUH WHVWHG
using the log odds ratio, l(o)6RNDO5RKOI
DVIROORZV
3UH\6L]H3UHIHUHQFH
Euglandina rosea
Seventeen adult E. rosea±PPVKHOO
OHQJWKZHUHVWDUYHGIRUWZRGD\VSULRUWRH[SHULPHQWDWLRQWRVWDQGDUGL]HKXQJHUOHYHOV(DFK
H[SHULPHQWDOFRQWDLQHUZDV¿OOHGZLWKFPRI
VRLODFDOFLXPVRXUFHFXWWOHERQHDQGVRPH
lettuce OHDYHVDVIRRGIRUWKHSUH\7KHSUH\A.
fulicaZHUHGLYLGHGLQWRIRXUVL]HFODVVHV±
1–2, 2–3, and 3–4 cm shell length). Ten snails
IURPWZRRIWKHIRXUVL]HFODVVHVZHUHRIIHUHG
to one E. rosea after the prey had been allowed
to acclimate to the container for one day. Euglandina rosea consumes small snails whole
as well as eating larger snails via the shell
aperture. Every 12 h consumed individuals
were replaced with new individuals of the same
VL]HFODVV1RPRUHWKDQIRXUVQDLOVRIRQHVL]H
class were replaced at one interval, so a choice
RI SUH\ ZDV DOZD\V DYDLODEOH ([SHULPHQWV
were run for four to ten days depending on
consumption rates and prey availability. At the
HQGRIWKHH[SHULPHQWVWKHQXPEHUVRIVPDOO
prey and large prey consumed were added up
for each container. Differences in preference
between small and large prey were assessed
by comparing the number of containers with
more small prey consumed to containers with
more large prey consumed using a sign test
6RNDO5RKOI
Oxychilus alliarius
Adult O. alliarius±PPVKHOOZLGWKZHUH
RIIHUHGSUH\QDWLYHSuccinea spp. from areas
where O. alliarius is abundant) of various
VL]HV2QHSUH\LWHPZDVSODFHGLQDFRQWDLQHU
with 2 cm of soil and one leaf of Broussaisia
arguta to provide it with habitat and food. Prey
ZHUHGLYLGHGLQWRVL[VL]HFODVVHV±±
±±±DQG±PPVKHOOOHQJWK
6HYHQW\IRXU H[SHULPHQWDO UHSOLFDWHV HDFK
contained one adult O. alliarius in addition
to the prey snail, while 48 control replicates
each contained only the prey snail. Each
trial was run for seven days at the end of
which prey were recorded as alive or dead.
which is useful because it permits standard
errors, sl(o), to be calculated from binary data,
as follows:
where N 11 LV WKH QXPEHU RI H[SHULPHQWDO
replicates in which the prey survived; N12 is
the number of control replicates in which the
species survived; N21LVWKHQXPEHURIH[SHULmental replicates in which the prey died; N22
is the number of control replicates in which
the prey died.
,IPRUWDOLW\LVHTXDOLQFRQWURODQGH[SHULPHQWDOWUHDWPHQWVWKHORJRGGVUDWLRLV]HUR6LJQL¿cant differences in mortality were determined
ZKHQDORJRGGVUDWLRZDVIXUWKHUWKDQ
VWDQGDUGHUURUVDZD\IURP]HURSDQG
IXUWKHUWKDQVWDQGDUGHUURUVDZD\IURP
]HURS
Prey-Species Preference
Euglandina rosea
Prey-species preference of E. rosea was assessed by offering a choice between two of the
¿YHSUH\VSHFLHVOLVWHGDERYH3UH\ZHUH±
PPLQH[WHQGHGIRRWOHQJWK7KHVL]HGLVWULEXtion, that is, the numbers of snails/slugs of variRXVVL]HVLQHDFKWULDOZDVPDWFKHGEHWZHHQ
WKHWZRSUH\VSHFLHVLQRUGHUWRPLQLPL]HDQ\
HIIHFWRIVL]HLQGHWHUPLQLQJVSHFLHVSUHIHUHQFH
8VLQJWKHOHQJWKRIWKHH[WHQGHGIRRWUDWKHU
WKDQDVKHOOVL]HPHDVXUHZDVQHFHVVDU\VLQFH
VRPHRIWKHSUH\FKRLFHVZHUHVOXJVV. cubensis and D. laeve). Of the ten possible pair-wise
FRPELQDWLRQVHLJKWZHUHWHVWHGD. laeve vs.
S. tenella and D. laeve vs. A. fulicaZHUHH[cluded because of lack of adequate numbers
of D. laeve). There were ten replicates for each
pair-wise combination. A different E. rosea and
SUH\WHQLQGLYLGXDOVRIWZRVSHFLHVZHUH
used in each replicate. The number of each
W\SHRISUH\FRQVXPHGQRUHSODFHPHQWRYHU
a 24 h period was recorded.
138
MEYER & COWIE
$SUHIHUHQFHLQGH[ZDVFDOFXODWHGIRUHDFK
predator in each replicate/container using a
YHUVLRQ RI 0DQO\¶V Į LQGH[ WKDW DFFRXQWV IRU
variable prey populations, that is where prey
DUHQRWUHSODFHG.UHEVDVIROORZV
ZKHUHĮiLV0DQO\¶VĮSUHIHUHQFHLQGH[IRUSUH\
type i; pi, and pj are the proportions of prey i
RUMUHPDLQLQJDWWKHHQGRIWKHH[SHULPHQWL «PM «PWKDWLVHi/ni in
which ei is the number of prey type i remaining
XQHDWHQDWWKHHQGRIWKHH[SHULPHQWQi is the
LQLWLDOQXPEHURISUH\W\SHLLQWKHH[SHULPHQW
DQGPLVWKHQXPEHURISUH\W\SHVVLPLODUO\IRU
ej/nj9DOXHVIRUWKLVLQGH[UDQJHEHWZHHQDQG
1; values > 0.5 indicate preference and values
DYRLGDQFH 6LJQL¿FDQFH RI GLYHUJHQFH
IURP QR SUHIHUHQFH ZDV DVVHVVHG ZLWK
single sample t-tests.
LQWKHVL]HUDQJH±PPDQGLQWKHUDQJH
5–12 mm shell length) were then offered to an
individual E. rosea for a period of 24 h. Each
prey snail was weighed to the nearest 0.0001
JDQGLQGLYLGXDOO\PDUNHG$WWKHHQGRIWKHH[periment, the number of snails remaining alive
was counted, and any shells remaining from
consumed snails were weighed to the nearest
0.0001 g, these weights being subtracted from
the weights of those snails at the beginning of
WKH H[SHULPHQW WR JLYH D YDOXH RI WKH ZHLJKW
consumed. Adding this amount to the known
weight of snails consumed whole provided a
value for the total weight consumed. Growth
RISUH\VQDLOVRYHUWKHKRIWKHH[SHULPHQW
was assumed to be negligible. Wet weight consumed was regressed on E. roseaVL]H0DQO\¶V
ĮLQGH[GHVFULEHGDERYHZDVXVHGWRGH¿QH
preference, followed by a Mann-Whitney U-test
WRWHVWIRUVLJQL¿FDQWGLIIHUHQFHVLQSUHIHUHQFH
IRUVPDOOSUH\±PPYVODUJHSUH\±
mm) between adult and juvenile E. rosea.
Oxychilus alliarius
Prey-species preference of O. alliarius
ZDV DVVHVVHG E\ RIIHULQJ DGXOWV ± PP
PD[LPXPVKHOOZLGWKDVLQJOHSUH\LQGLYLGXDO
RI YDULRXV VSHFLHV PP PD[LPXP VKHOO
GLPHQVLRQIRUVQDLOVDQGVLPLODUO\VL]HGVOXJV
GHWHUPLQHG E\ PDWFKLQJ IRRW VL]H EHWZHHQ
slugs and snails) following the same procedure
and analyses as in the O. alliariusSUH\VL]HH[periments. Prey species used were: the native
snail species Succinea VSSH[SHULPHQWDO
trials, 18 controls), TornatellidesVSS
and PhilonesiaVSWKHLQYDVLYHVQDLO
species P. achatinaceumDQGWKHLQYDsive slug species A. intermediusDQG
D. leave
Consumption Rate
TABLE 1. Number of Achatina fulica eaten by
Euglandina rosea when given a choice between
WZRVL]HFODVVHV(DFKH[SHULPHQWXVHGDGLIIHUHQW
E. rosea individual.
Number Eaten
6L]H&ODVVHV 'XUDWLRQGD\V Smaller Larger
0–1 vs. 1–2 cm
0–1 vs. 2–3 cm
0–1 vs. 3–4 cm
1–2 vs. 2–3 cm
Euglandina rosea
Twelve E. rosea were used in consumption
UDWH H[SHULPHQWV VHYHQ DGXOWV ± PP
VKHOO OHQJWK ¿YH MXYHQLOHV ± PP VKHOO
OHQJWK)RUDZHHNSULRUWRWKHH[SHULPHQWV
they ZHUHSURYLGHGZLWKSUH\VQDLOVA.fulica,
P. achatinaceum, B. similarisRIYDULRXVVL]HV
ad libitum. Snails were not starved, so that the
consumption rate measured would be a more
QDWXUDO UDWKHU WKDQ D PD[LPXP UDWH 7KLUW\
SUH\ VQDLOV QRQQDWLYH Succinea tenella, 15
1–2 vs. 3–4 cm
2–3 vs. 3–4 cm
Total
4
4
4
4
5
5
5
5
5
5
5
4
4
10
10
10
10
10
13
2
11
4
10
4
4
3
0
3
1
0
2
1
0
77
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
PREDATORY SNAILS IN HAWAII
TABLE 2. Predation of Oxychilus alliarius on native SuccineaVSSRIGLIIHUHQWVL]HFODVVHVVKHOOOHQJWK
P-Value based on log odds ratio tests. NS indicates P-Values > 0.05.
Control
([SHULPHQWDO
6L]H&ODVV
No. Survived
No. Died
0–3 mm
±PP
±PP
!PP
20
17
12
0
0
0
1
No. Survived
No. Died
P-value
33
0
0
0
NS
NS
NS
3
17
12
RESULTS
Oxychilus alliarius
Twelve O. alliarius were used in consumptionUDWHH[SHULPHQWV7KH\ZHUHFROOHFWHGIURPWKH
¿HOGDQGSODFHGGLUHFWO\LQWRLQGLYLGXDOFRQWDLQHUVHDFKZLWK¿YHSUH\VQDLOV Succinea spp.,
1–3 mm shell length) for seven days. Each prey
item was weighed to the nearest 0.0001 g and
was individually marked prior to being placed
LQWKHFRQWDLQHU$WWKHHQGRIWKHH[SHULPHQW
the snails remaining alive were counted and
any shells remaining from consumed snails
were weighed to the nearest 0.0001 g, these
weights being subtracted from the weights of
WKRVHVQDLOVDWWKHEHJLQQLQJRIWKHH[SHULPHQW
to give a value of the weight consumed.
3UH\6L]H3UHIHUHQFH
Regardless of which snail combination E.
rosea ZDV RIIHUHG 7DEOH LQ DOO FDVHV LQ
ZKLFKDWOHDVWRQHSUH\ZDVFRQVXPHGRI
17) more of the smaller snails were consumed
VLJQ WHVW 3 (YHQ EHLQJ H[WUHPHO\
conservative and considering the three instances in which no prey were eaten and the
one in which two of the larger prey were eaten
LQWKH±YV±FPWULDOVDVVXSSRUWLQJWKH
null hypothesis of no preference, gives a twoVLGHG39DOXHRI3RROLQJWKHGDWD
VQDLOVLQWKHVPDOOHUVL]HFODVVZHUHFRQVXPHG
7$%/(5HVXOWVRISDLUZLVHFRPSDULVRQRISUHIHUHQFHV0DQO\¶VĮRIE. roseaDPRQJ¿YHSUH\VSHFLHV
Vc Veronicella cubensis, Dl Deroceras laeveWKHWZRVOXJVSHFLHVPa Paropeas achatinaceum,
Af Achatina fulica, St Succinea tenella9DOXHVRIĮ!LQGLFDWHSUHIHUHQFH9DOXHVLQGLFDWH
DYRLGDQFH$VLQJOHVDPSOHWWHVWZDVXVHGWRWHVWLIWKHSUHIHUHQFHLQGLFHVGLIIHUHGVLJQL¿FDQWO\IURP
6WDWLVWLFDOO\VLJQL¿FDQWGLIIHUHQFHVDUHLQGLFDWHGE\DVWHULVNV3YDOXHVDUHLQDOOFDVHV
Treatment
0DQO\¶VĮ3UHIHUHQFH,QGH[6(
Snails vs. Snails
Pa vs. St
Pa vs. Af
Af vs. St
Pa Pa Af S Af S Slugs vs. Snails
Vc vs. Pa
Vc vs. St
Vc vs. Af
Dl vs. Pa
Vc
Vc
Vc
Dl
Pa S Af Pa Slugs vs. Slugs
Dl vs. Vc
Dl Vc 140
MEYER & COWIE
),*&RQVXPSWLRQUDWHZHWZHLJKWFRQVXPHGGXULQJDKSHULRGYVZHLJKW
of Euglandina rosea.
),*0DQO\¶VĮLQGLFHVIRUDGXOWDQGMXYHQLOHE. rosea preference for smaller prey
PPVKHOOOHQJWKRUODUJHUSUH\12 mm shell length). Error bars represent
± 1 standard error.
PREDATORY SNAILS IN HAWAII
141
TABLE 4. Predation of Oxychilus alliarius RQQDWLYHDQGLQWURGXFHGVQDLOVSuccinea spp., Tornatellides
spp., Philonesia sp., P. achatinaceumDQGVOXJVD. laeve and A. intermedius). P-Value based on log
odds ratio tests. NS indicates P-values > 0.05. *Native species.
Control
([SHULPHQWDO
No. Survived
No. Died
No. Survived
No. Died
P-value
Snails
Succinea spp.*
Tornatellides spp.*
Philonesia sp.*
P. achatinaceum
18
14
12
8
0
1
0
0
1
4
1
25
12
8
Slugs
D. laeve
A. intermedius
10
0
1
10
17
1
0
NS
NS
7D[D
FRPSDUHGWRRQO\WZRIURPWKHODUJHUVL]HFODVV
Euglandina rosea thus prefers smaller snails
when given a choice.
In the O. alliarius H[SHULPHQWV QR VQDLO
above 3 mm in shell length was preyed upon
FRPSDUHGWRRIWKHWKDWZHUH
mm in shell length or less; hence, there was
QRVLJQL¿FDQWGLIIHUHQFHEHWZHHQFRQWURODQG
H[SHULPHQWDOWUHDWPHQWVH[FHSWLQWKH±PP
SUH\VL]HFDWHJRU\7DEOH
Prey-Species Preference
Euglandina rosea always preferred the snail
over the slug species but showed no preferHQFHDPRQJWKHWKUHHVQDLOVSHFLHV7DEOH
Veronicella cubensis was the least preferred
prey, and D. laeve seemed to be preferred
over V. cubensis but was less attractive than
P. achatinaceum and therefore probably also
OHVVDWWUDFWLYHWKDQWKHRWKHUVQDLOVSHFLHVS.
tenella and A. fulica).
Oxychilus alliarius readily consumed all snail
species offered, as indicated by the much
KLJKHUPRUWDOLW\LQWKHH[SHULPHQWDOWUHDWPHQWV
but there was no difference in mortality between
FRQWURODQGH[SHULPHQWDOWUHDWPHQWVIRUWKHWZR
VOXJVSHFLHV7DEOH
Consumption Rate
Wet weight consumed increased as E. rosea
ZHLJKW LQFUHDVHG )LJ 7KH KLJK U2 value
)LJVXJJHVWVWKDWWKLVPDWKHPDWLFDOPRGHO
describes the relationship well. The regression
line was not forced to go through the origin but
the y-intercept was nevertheless close to it.
Adult E. rosea preferred smaller snails to larger
VQDLOVĮ 6( 7 GI 3EXWMXYHQLOHE. rosea showed no
SUHIHUHQFHĮ 6( 7 GI 3 7KHGLIIHUHQFHLQSUHIHUHQFH
ZDVVLJQL¿FDQW8 3 )LJ
The consumption rate for O. alliarius was
“ 6( J RI ZHW ZHLJKW SHU
GD\ZKLFKHTXDWHVWRDERXWRQHVQDLO±PP
PD[LPXPVKHOOGLPHQVLRQFRQVXPHGE\HDFK
LQGLYLGXDOGXULQJWKHH[SHULPHQWGD\V
DISCUSSION
Small snails were more vulnerable to predation by both E. rosea and O. alliarius. While
O. alliarius can only consume small snails
OHVV WKDQ PP PD[LPXP VKHOO GLPHQVLRQ
E. rosea can consume larger prey. However,
ZKHQ JLYHQ D FKRLFH RI SUH\ VL]HV E. rosea
ZLOO HDW VLJQL¿FDQWO\ PRUH VPDOO VQDLOV WKDQ
ODUJHVQDLOV7DEOH)LJ7KHVHUHVXOWVDUH
FRQVLVWHQWZLWKRWKHUVWXGLHVRISUH\VL]HSUHIerence in E. rosea&KLX&KRX'DYLV
%XWOHU1LVKLGD1DSRPSHWK
&RRNDE*ULI¿WKVHWDO*HUODFK
+RZHYHURXUUHVXOWVLQGLFDWHWKDWWKLV
VL]HSUHIHUHQFHLVUHODWLYHQRWDEVROXWHWKDWLV
PLGVL]HGSUH\±RU±FPLQVKHOOOHQJWK
are not eaten if presented along with smaller
prey, but are eaten if presented with larger
SUH\7DEOH,WLVQRWVLPSO\WKDWODUJHUSUH\
FDQQRWEHHDWHQ7KLVEHKDYLRUDOÀH[LELOLW\LV
interesting, and perhaps important for the dy-
142
MEYER & COWIE
namics of the interaction, although the data are
too few to evaluate further. Nonetheless, our
results and those of other studies indicate that
GLIIHUHQFHVLQVL]HDPRQJSUH\FDQLQÀXHQFH
the predatory behavior of E. rosea, and thus
confound conclusions of prey species preferHQFHLISUH\VL]HLVQRWDSSURSULDWHO\FRQWUROOHG
LQH[SHULPHQWV
7KH VL]H RI E. rosea is also important in
XQGHUVWDQGLQJSUH\VL]HSUHIHUHQFH$OWKRXJK
counter-intuitive, larger E. rosea had a stronJHUSUHIHUHQFHIRUVPDOOHUSUH\)LJ7KLV
may be because large E. rosea have a greater
ability to consume snails whole. Thus, the
impact of large E. rosea on small snails may
EHHYHQJUHDWHU,QWKH¿HOGDODUJHPDMRULW\
of the species consumed by E. rosea were
VZDOORZHGZKROH*ULI¿WKVHWDO2QH
reason usually proposed for E. rosea’s preference for smaller snails is calcium intake.
&RRNDVXJJHVWHGWKDWWKHUHPD\EHD
compromise between the input of important
nutrients, primarily calcium, when the prey is
FRQVXPHGZKROHVKHOOLQFOXGHGDQGWKHFDloric intake that comes from the consumption
of just body tissue.
%RWKSUHGDWRUVH[KLELWHGDFOHDUSUHIHUHQFH
for the snail species over the slug species in all
WHVWV7DEOHV,QDOOH[SHULPHQWVH[DPLQing E. rosea’s preference between snails and
slugs, it preferred the snails, while showing no
preference among snail species in snail vs.
VQDLOH[SHULPHQWV7DEOH+RZHYHUEHWZHHQ
the slugs, E. rosea did prefer D. laeve over V.
cubensis7DEOHOxychillus alliarius showed
similar preferences, consuming all snail speFLHVRIIHUHGEXWQRVOXJV7DEOH7KHUHDUH
no native slugs in Hawaii, but non-native slugs
DUH DEXQGDQW DQG ZLGHVSUHDG &RZLH HW DO
2008; Meyer & Cowie, in press) and negatively
LQÀXHQFH +DZDLLDQ HFRV\VWHPV E\ UHGXFLQJ
VXUYLYRUVKLS RI \RXQJ QDWLYH SODQWV -RH Daehler, 2008). Thus, predation on slugs could
a priori be seen as a positive counter balance
to the introduction of these predatory snails,
but unfortunately, our results show that both
O. alliarius and E. rosea prefer snails to slugs,
DQGPDQ\RIWKHVOXJVUHDFKVL]HVZHOODERYH
WKH SUHIHUUHG VL]H UDQJH RI ERWK O. alliarius
and E. rosea.
Consumption rate was related to predator
VL]H7KDWRIO. alliarus was much lower than
that of E. rosea UHÀHFWLQJ WKH PXFK VPDOOHU
VL]H RI O. alliarius; and within E. rosea conVXPSWLRQ UDWH LQFUHDVHG ZLWK SUHGDWRU VL]H
)LJ+RZHYHUWKHLPSDFWRIO. alliarius on
native snails may still be considerable because
of the high densities this species can reach,
notably at higher elevations on the islands of
Maui and Hawaii.
0DQ\RIWKHH[WDQWQDWLYH3DFL¿F,VODQGVQDLOV
DUH VPDOO HJ QXPHURXV HQGRGRQWLGV KHOLFLQLGVYHUWLJLQLGVDQGDFKDWLQHOOLGVH[FOXGLQJ
$FKDWLQHOOLQDHDUHPPLQPD[LPXPVKHOO
dimension for their entire life) compared to
some of the abundant introduced snails/slugs
WKDWKDYHEHFRPHHVWDEOLVKHGHJAchatina
fulica, Cornu aspersum, Limax maximus, Veronicella cubensis, and Meghimatium striatum)
&RZLHHWDO-RH'DHKOHU0H\HU
& Cowie, in press). Most survive only in sparse
SRSXODWLRQV /\GHDUG HW DO 0H\HU
7KHUHVXOWVLQGLFDWHWKDWO. alliarius and
E. rosea would readily consume these native
snails. Some native succineid species are also
relatively small during the early stages of their
life history, being less than 1 mm in shell length
DWKDWFKLQJDQGUDUHO\H[FHHGLQJPPLQVKHOO
OHQJWK%URZQHWDO5XQGHOO&RZLH
2003; W. M. M., personal observations), making
them vulnerable to O. alliariusIRUWKH¿UVWIHZ
months of their lives and to E. rosea for their
entire lives. Achatinellids are more diverse in
VL]H)RULQVWDQFHPDQ\$FKDWLQHOOLGDHZLWK
WKHH[FHSWLRQRI$FKDWLQHOOLQDHDUHZLGHO\EXW
SDWFKLO\GLVWULEXWHGDQGH[WUHPHO\VPDOOPDQ\
PPLQVKHOOOHQJWKDQGDUHWKXVYXOQHUDEOH
to predation by both predators. Conversely,
Achatinellinae, the Hawaiian tree snails, are
larger. For instance, Achatinella mustelina are
!PPDWELUWKDQGUHDFKVL]HVJUHDWHUWKDQ
PP LQ VKHOO OHQJWK +DG¿HOG 0RXQWDLQ
+DG¿HOGHWDO7KXVZKLOHWKH\
are not likely to be consumed by O. alliarius,
their populations have declined following the
introduction of E. rosea+DG¿HOG0RXQWDLQ
+DG¿HOG+DG¿HOGHWDODV
KDYHVLPLODUVL]HG3DUWXOLGDH3DFL¿FLVODQGWUHH
snails) following the introduction of E. rosea
HOVHZKHUH&ODUNHHWDO0XUUD\HWDO
0XUUD\*HUODFK&RRWH
/RqYH
Although consumption rates of O. alliarius
are much lower than those of E. rosea, O. alliarius may be having a large impact on native
land snails. Populations of O. alliarius are more
dense than those of E. rosea in native rain forests, notably on the islands of Hawaii and Maui,
and are becoming more prevalent on other
islands at higher elevations where most of the
H[WDQWQDWLYHVQDLOVDUHIRXQG6HYHUQV
Meyer & Cowie, in press). Endangered Hawaiian tree snails are probably not impacted by
O. alliarius, as they are too large even at birth,
PREDATORY SNAILS IN HAWAII
but much of the remaining Hawaiian land snail
diversity may well be affected. Nevertheless,
to ascertain the real individual and combined
impacts of these predators on the land snail
community as a whole and on populations of
species of particular interest will require data
RQWKHSRSXODWLRQGHQVLWLHVDQGVL]HGLVWULEXtions of these predators as well as on the lifehistories of the prey species. Unfortunately,
data on population densities and life-histories
for both prey and predators are few. However,
investigations of these aspects of their ecology,
combined with the preference and consumption
rate data presented here, would permit models
to be developed describing the dynamics of this
system, which could help biodiversity managers protect native populations and control alien
species.
$OWKRXJK PDQ\ 3DFL¿F ODQGVQDLO VSHFLHV
DUHH[WLQFWPDQ\XQLTXHVSHFLHVUHPDLQUHSresenting all of the native families. Knowledge
of the feeding ecology of these predators is
therefore essential if natural resources managers are to design better conservation strategies
targeting these remaining native species. The
results of this study are relevant beyond Hawaii
as both predatory snails and the introduced
VSHFLHVXVHGDVSUH\VSHFLHVLQWKHVHH[SHULments have been widely distributed by human
DFWLYLWLHV 6ROHP &RZLH &RRWH
/RqYH%DUNHU(IIRUG&iGL]
& Gallardo, 2007). This may be especially
pertinent for understanding the threat of these
SUHGDWRU\ VQDLO VSHFLHV LQ WKH 3DFL¿F VLQFH
PDQ\ QDWLYH 3DFL¿F LVODQG VQDLO IDXQDV DUH
composed of species belonging to many of
WKHVDPHIDPLOLHV&RZLHHWDO&RZLH
:HVWLOOKDYHWKHRSSRUWXQLW\WRSURWHFW
WKHVHXQLTXHOLQHDJHVIURPH[WLQFWLRQEXWWKLV
is dependent on monitoring the presence of
these predators and evaluating their impacts.
ACKNOWLEDGEMENTS
We thank the following for funding and support: U.S. Army Environmental, Oahu, the
University of Hawaii Ecology, Evolution and
&RQVHUYDWLRQ %LRORJ\ SURJUDP 16) JUDQW
DGE05-38550 to K. Y. Kaneshiro). We thank Alvin Yoshinaga and staff at Lyon Arboretum, and
the U.S. Army Environmental staff, especially
9LQFH&RVWHOORDQG6WHSKDQLH-RHIRUDFFHVV
and help in collecting snails and slugs. We
also thank Brian Bowen, Tad Fukami, Rebecca
Ostertag and especially Andy Taylor for their
helpful comments on a draft of this paper.
143
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