ORIGINAL PAPER

Predator-driven biotic resistance and propagule pressureregulate the invasive apple snail Pomacea canaliculatain Japan

Yoko Yamanishi • Kazuhiro Yoshida •

Noriomi Fujimori • Yoichi Yusa

Received: 7 May 2011 / Accepted: 10 December 2011 / Published online: 20 December 2011

� Springer Science+Business Media B.V. 2011

Abstract Species richness in local communities has

been considered an important factor determining the

success of invasion by exotic species (the biotic

resistance hypothesis). However, the detailed mecha-

nisms, especially the role of predator communities, are

not well understood. We studied biotic resistance to an

invasive freshwater snail, Pomacea canaliculata, at 31

sites in an urban river basin (the Yamatogawa) in

western Japan. First, we studied the relationship

between the richness of local animal species and the

abundance of P. canaliculata, demonstrating a nega-

tive relationship, which suggests that the intensity of

biotic resistance regulates local snail populations. This

pattern was due to the richness of native predator

communities rather than that of introduced species or

non-predators (mainly competitors of the apple snail).

Local snail abundance was also affected by immigra-

tion of snails from nearby rice fields (i.e. propagule

pressure), where few predators occur. Second, we

assessed short-term predation pressure on the snail by

means of a tethering experiment. Predation pressure

was positively correlated with the number of individ-

ual predators and negatively correlated with snail

abundance. The introduced crayfish Procambarus

clarkii was responsible for the variance in predation

pressure. These results indicate that the predator

community, composed of both native and introduced

species, is responsible for resistance to a novel invader

even in a polluted urban river.

Keywords Ecological resistance � Exotic species �Freshwater � Gastropoda � Predation

Introduction

When organisms are introduced into new areas, they

are exposed to novel species interactions including

competition, predation, or parasitism. The intensity of

these interactions varies with local species richness.

Therefore, species richness has been considered an

important factor that prevents biological invasions (the

biotic resistance hypothesis; Elton 1958). Examples of

Electronic supplementary material The online version ofthis article (doi:10.1007/s10530-011-0158-9) containssupplementary material, which is available to authorized users.

Y. Yamanishi � Y. Yusa (&)

Faculty of Science, Nara Women’s University,

Kitauoya-nishi, Nara 630-8506, Japan

e-mail: yusa@cc.nara-wu.ac.jp

Present Address:Y. Yamanishi

Idea Consultants, 2-2-2 Hayabuchi, Tsuzuki, Yokohama

224-0025, Japan

K. Yoshida

National Agricultural Research Center for Kyushu-

Okinawa Region, Suya 2421, Koshi 861-1192, Japan

N. Fujimori

Toyohashi University of Technology, 1-1 Hibarigaoka,

Tempaku, Toyohashi, Aichi 441-8580, Japan

123

Biol Invasions (2012) 14:1343–1352

DOI 10.1007/s10530-011-0158-9

biotic resistance have been reported in terrestrial

(Lake and O’Dowd 1991; Parker et al. 2006), marine

(Stachowicz et al. 1999; Hunt and Yamada 2003) and

freshwater ecosystems (Harvey et al. 2004; Yonekura

et al. 2004). Most field surveys addressing biotic

resistance, however, merely report the negative asso-

ciation between species richness and a measure of

invasion success, with the mechanisms of resistance

remaining unknown in most cases (Levine and

D’Antonio 1999). When mechanisms are addressed,

the studies normally focus on the role of competition.

Some studies have reported the effect of a single

predator on an invasive species (Lake and O’Dowd

1991; Derivera et al. 2005), but the role of local

predator communities in invasion success is not

well understood (Byers 2002; Parker et al. 2006;

Carlsson et al. 2010; Dumont et al. 2011) especially in

freshwater systems (Harvey et al. 2004). This gap in

the literature is unexpected because predation is an

important factor that regulates the population dynam-

ics of species, and many exotic species become

invasive when they are free from the predators (or

parasites) in their original areas (the enemy release

hypothesis; Torchin et al. 2003).

Traditionally, local communities have been con-

sidered simply as either susceptible or resistant to

biological invasions (Elton 1958). However, biotic

resistance is not such a dichotomous characteristic of a

community (D’Antonio et al. 2001; Carlsson et al.

2010). The intensity of resistance may vary spatially or

temporally, thus influencing the probability of inva-

sion success. A further complication is that invasion

success is also influenced by other factors, such as life

history characteristics of the invader, abiotic factors of

the local ecosystems, and introduction effort (often

called propagule pressure) (Lockwood et al. 2005;

Chiron et al. 2009). Propagule pressure is a key factor

responsible for invasion success (Lockwood et al.

2005; Von Holle and Simberloff 2005; Chiron et al.

2009). Numbers of introduced individuals (propagule

size) or of introduction events (propagule number) of

an invasive species may interact with other biotic and

abiotic factors to determine its invasion success

(D’Antonio et al. 2001; Von Holle and Simberloff

2005).

Previous studies on biotic resistance often show

negative relationships, as expected, between species

richness and invasibility in small-scale experiments

(e.g., Stachowicz et al. 1999) but positive relationships

between them in large-scale field surveys (Lonsdale

1999; Levine and D’Antonio 1999; Levine 2000;

Stohlgren et al. 2006; Fridley et al. 2007; Altieri et al.

2010). In most cases, the positive relationships in

large-scale studies do not represent true causal rela-

tionships, but apparent relationships due to factors

such as spatial variation in availability of common

resources between introduced and native species, their

similar habitat use, or similar spatial patterns of seed

or larval supply (Levine and D’Antonio 1999; Levine

2000; Byers and Noonburg 2003; Jiang and Morin

2004; Fridley et al. 2007; Altieri et al. 2010). Such

confounding factors may be circumvented when biotic

resistance is studied in areas with rather uniform

climatic and physical conditions and a similar suite of

local species. Many Japanese rivers are suitable for

such studies as they show various degrees of urban-

ization in relatively small areas. Species richness and

the density of each local species vary spatially in the

urban–rural continuum (Lane and Fujioka 1998;

Urban et al. 2006; Leprieur et al. 2008), and the level

of biotic resistance would be expected to vary

correspondingly (Lake and O’Dowd 1991; Simberloff

and Von Holle 1999; D’Antonio et al. 2001).

The apple snail Pomacea canaliculata is native to

temperate and subtropical South America (Cowie

2002; Hayes et al. 2008). It has been named one of the

world’s 100 worst invasive species (Lowe et al. 2000)

because it has a large impact on local ecosystems once

introduced (Carlsson et al. 2004; Fang et al. 2010),

including an impact on aquatic crops such as rice and

lotus (Joshi and Sebastian 2006). These snails were

introduced to Japan and many other Asian countries in

the early 1980s as a food item and soon escaped and

invaded rice ecosystems (Joshi and Sebastian 2006).

In Japan, the apple snail maintains large populations in

rice fields, but populations are smaller in other

freshwater habitats such as canals, rivers and ponds

(Yusa 2006; Yusa et al. 2006). In the latter freshwater

habitats, there are many predators of this snail (Yusa

et al. 2001, 2006; Yusa 2006; Yoshie and Yusa 2008),

and one reason for its small population sizes in such

habitats may therefore be predation.

We investigated the intensity and mechanism of

biotic resistance to the apple snail at 31 study sites in

the Yamatogawa River basin in western Japan. The

Yamatogawa is a typical urban river with highly

polluted water (Ministry of Land, Infrastructure,

Transport and Tourism of Japan 2010) and relatively

1344 Y. Yamanishi et al.

123

poor fauna in terms of both species richness and

individual abundance (Osaka Museum of Natural

History 2007). Two sets of observations were made.

First, we studied the relationship between snail

abundance and animal richness, including predators

of the snail. Snail abundance was quantified both at the

study sites and upstream rice fields, to assess invasion

success and propagule pressure, respectively. If there

is biotic resistance to the apple snail, a negative

relationship between species richness and snail abun-

dance at the study sites is expected. Second, we

tethered apple snails of various sizes at each site. If

predators are important in reducing snail abundance,

mortality of the tethered snails should increase with

the number of predators.

Methods

Collection of snails and other animals

We selected 31 study sites in small rivers and

agricultural canals in the upper-middle Yamatogawa

River basin (Fig. 1). These sites were selected based

on accessibility, in areas where P. canaliculata

occurred, with environmental conditions suitable for

them (water current velocity \50 cm/s and water

depth lt;55 cm; Ichinose et al. 2000). Although the

sites were distributed over eight small river systems of

the Yamatogawa River basin (Online Resource

Table 1), there were no significant river-level differ-

ences in snail abundance (F7, 23 = 0.72, P = 0.67;

one-way ANOVA) or in the number of snails preyed

upon (F7, 23 = 1.19, P = 0.35). However, in the

model selection procedure river identity was always

included in the initial full models.

All observations were made in August and Sep-

tember 2006. At each site, we recorded: (1) environ-

mental variables, (2) number of animal species and

individuals, (3) number of P. canaliculata, and (4)

number of P. canaliculata in the nearest rice field

upstream of the study site. The environmental vari-

ables measured were water temperature, current

velocity (using Model 3631, Yokogawa Electric,

Tokyo), water depth, and dissolved oxygen (using

SWC-301DO, Sansyo, Tokyo). Current velocity,

water depth, and dissolved oxygen were measured at

least three times per site, adjacent to the locations of

the snail-baited traps (see below), and the values were

averaged to represent each site. Water temperature

was measured once per site since it varied little within

each site.

To evaluate animal richness, both catch per unit

effort and traps were used at all sites in a standardized

manner. For catch per unit effort, one of us (YYa)

collected animals using a hand net (3 mm mesh) for

10 min within an area including both riffles and

pools \30 m along the river. This procedure was

repeated by another person (KY or NF) on different

days (i.e. n = 2 samples/site). In addition, six traps

were set per site and trapped animals collected after

1 day. The 2 mm mesh traps were 25 9 25 9 40 cm

(height 9 width 9 length) in size, and they had a

round (5 cm diameter) opening on each side with a

device to prevent trapped animals escaping. Three of

the traps were set with crushed snails (mean ± SD =

20.0 ± 2.0 g in wet weight) as bait primarily to collect

potential predators of P. canaliculata, and the other

three traps were set with about 8 g of commercial

34.70N

34.50N

135.70 E 135.90E

1514

13

24

1

23

4

65

78 9 10

1112

1617

1819

202122

2328

252627

2930

31

N

10 km

Nara Pref.

Kyoto Pref.Osaka Pref.

Fig. 1 Study sites in the Yamatogawa River basin in western

Japan. Each site is represented by a circle. The numbers coincide

with the site numbers in Online Resource Tables 1 and 2

Predator-driven biotic resistance 1345

123

fish bait (4:1 mixture of ‘‘Gluten 5’’ and ‘‘Sanagi-ko’’;

Marukyu, Saitama) to collect non-predators as well as

predators. All animals 4 cm or larger in total length

collected using both methods were identified and

counted. We also collected P. canaliculata individuals

that were 5 mm or larger in shell height for 10 min at

each site using a hand net and by hand picking, and

counted them. The size threshold for animals was

chosen as most smaller predators (mainly vertebrates

and decapods in this study) do not feed on snails of this

size (Yusa et al. 2006), and some smaller predators

(mainly leeches) escape the 2 mm mesh of the trap.

To assess the effects of snail immigration from

adjacent rice fields, we collected snails from the

nearest rice field upstream of each study site. We

collected snails for 10 min from the rice fields by hand

picking and counted them (n = 28 fields; data for

three sites were not available as the fields had been

drained).

Tethering experiment

To evaluate short-term predation pressure on apple

snails, we glued 13 living snails randomly onto a

sheet (30 9 30 cm 9 3 mm thick) made of palm

fruit rinds using cyanoacrylate adhesive. The snails

were from three size classes: hatchling (shell height

2–4 mm, 5 individuals per sheet), small (4–8 mm, 5

individuals), and large (16–24 mm, 3 individuals).

Shells of small and large snails were glued directly

on the sheet, in the same posture as they crawl

(aperture down). However, shells of hatchlings were

first glued onto sponge cubes (10 mm sides) made of

melamine resin, with the aperture up, then the

sponge was glued to the sheet. This was done

because preliminary experiments showed that preda-

tors of hatchlings (mainly small fish) were ineffec-

tive at removing snails attached directly onto the

palm sheet. Two sheets were immersed on the

bottom substrate at each site and retrieved after

1 day (n = 26 snails/site). As controls, sheets with

snails were placed inside traps (without openings) at

three sites; no snails were lost after 1 day. Therefore,

we judged that natural mortality or dislodgement was

negligible, and so the lost snails in the experiment

were considered to have been preyed upon (broken

shells often remained). As the number of snails in

each size class was small, we used the sum of

missing snails on the two sheets as the index of

predation pressure at each site.

Data and statistical analyses

Animals that were previously known to prey on

P. canaliculata of any size (not eggs) in the laboratory

or field (Yusa 2006; Yusa et al. 2006) were considered

predators (Online Resource Table 2). In addition, the

fish species Carassius auratus auratus (goldfish;

treated as a distinct subspecies from Carassius auratus

langsdorfii because it is non-native), Gnathopogon

elongatus, Squalidus gracilis, Channa argus, Triden-

tiger brevispinis and Monopterus albus were tested for

the first time. For these new tests, two or three

individuals of each species and 13 P. canaliculata of

the same size classes used for the tethering experiment

were introduced into an 8-L plastic container and

maintained for 2 days at room temperature (about

25�C) with natural light conditions and aeration but

without food. Gnathopogon elongatus and Monopte-

rus albus did not consume any snails, whereas the

other fish consumed at least three individuals and

hence were treated as predators.

To identify factors affecting the number of snail

individuals at the study site (i.e. snail abundance) or

the number of snails lost in the tethering experiment

(predation pressure), a model selection procedure was

adopted. The procedure starts from the full model

including all independent variables, and, using back-

ward elimination, the model with the lowest AICc

(Akaike’s information criterion corrected for small

data size; Sugiura 1978) is selected as the best-fit

model. In the case of snail abundance, the initial

independent variables were river (one of the eight

small rivers), environmental factors (water depth,

current velocity, water temperature, and dissolved

oxygen), number of snails collected in the nearest rice

field, and animal richness and abundance (i.e. total

number of individuals of all species combined).

Animal richness and abundance were also evaluated

separately for native/introduced species and predators/

non-predators. In the case of predation pressure, the

independent variables were river, the four environ-

mental factors, snail abundance at the site, and animal

richness and abundance. The dependent variables

were transformed to natural logarithms after adding 1.

All statistical analyses were conducted with JMP

version 8 (SAS Institute 2008).

1346 Y. Yamanishi et al.

123

Results

Factors affecting snail abundance

The data for the environmental and biological vari-

ables are summarized in Online Resources Tables 1

and 2, respectively. The number of snails collected at

each site (snail abundance) ranged from 0 to 631

(mean ± SD, 62.5 ± 132.1). The number of animal

species collected (animal richness) ranged from 2 to

12 (5.29 ± 2.21). Predator species ranged from 1 to 5

(2.55 ± 1.21), and non-predator species (mainly con-

stituting competitors of P canaliculata for food as this

snail is highly omnivorous; Cowie 2002) ranged from

1 to 7 (2.74 ± 1.29). Native species ranged from 0 to 9

(3.55 ± 2.08), and introduced species from 0 to 4

(1.74 ± 1.00).

In the best-fit model (AICc = 56.83; R2 = 0.67),

only snail abundance in the rice field and animal

richness were selected as independent variables affect-

ing the snail abundance at the study site. Both effects

were significant: snail abundance in the rice field was

positively correlated with snail abundance at the study

sites (Fig. 2a; n = 28, F1, 25 = 33.88, P \ 0.001,

partial correlation) whereas animal richness was

negatively correlated (Fig. 2b; F1, 25 = 18.00, P \0.001). No environmental factors or river identity were

selected in the best-fit model. When numbers of native

and introduced species were included as explanatory

variables instead of total animal richness, native

species richness was selected as a significant indepen-

dent variable in the best-fit model (AICc = 58.82,

R2 = 0.65, F1, 25 = 15.06, P \ 0.001; Fig. 2c) in addi-

tion to snail abundance in rice fields (F1, 25 = 29.70,

P \ 0.001), whereas introduced species was not

selected (Fig. 2d). When the animals were categorized

as predators and non-predators (mainly competitors)

and included as initial independent variables, predator

richness was selected in the best-fit model (AICc =

59.40, R2 = 0.64, F1, 25 = 14.23, P \ 0.001; Fig. 2e)

in addition to snail abundance in rice fields (F1, 25 =

27.41, P \ 0.001), whereas non-predator richness was

not (Fig. 2f). When animals were categorized as native

predators, introduced predators, native non-predators,

and introduced non-predators, native predator and

introduced non-predator richness were selected in the

best-fit model (AICc = 58.90, R2 = 0.68). However,

the effect of introduced non-predator richness was

not significant (F1, 24 = 2.99, P = 0.10) whereas that

of native predators (F1, 24 = 16.96, P \ 0.001) and

that of snail abundance in rice fields were significant

(F1, 24 = 26.86, P \ 0.001).

The number of individual animals collected at

each site ranged from 2 to 153 (mean ± SD, 34.71 ±

35.11), with 1–65 predator individuals (15.94 ±

14.90) and 1–148 non-predator individuals (18.77

± 30.27). The number of individual animals was not

selected in the best-fit model to explain snail abun-

dance at the study sites (AICc = 69.16, R2 = 0.49).

In this analysis, only snail abundance in the rice field

(F1, 25 = 16.59, P \ 0.001) and water depth were

selected, though the latter was not significant

(F1, 25 = 2.69, P = 0.11). However, the crayfish,

Procambarus clarkii, accounted for 59% (=293/494)

of the total individual predators collected. When the

effects of crayfish and other individual predators were

included separately in the analysis, in the best-fit

model (AICc = 64.67, R2 = 0.61) the number of

other predators showed a nearly significant negative

correlation with snail abundance (F1, 23 = 3.39,

P = 0.08) whereas crayfish abundance (F1, 23 = 5.51,

P = 0.03) and snail abundance in rice fields

(F1, 23 = 19.97, P \0.001) had a significant positive

correlation. In this analysis, water temperature was also

selected in the best-fit model, but its effect was not

significant (F1, 23 = 3.24, P = 0.09).

Predation pressure on tethered snails

The total number of snails lost (predation pressure) in

the tethering experiment ranged from 0 to 25 of 26

individuals available at each site (mean ± SD,

8.39 ± 7.14, n = 31). The number of predator species

at each site was not selected as a significant indepen-

dent variable affecting predation pressure in the model

selection procedure (AICc = 33.36, R2 = 0.16). How-

ever, in the best-fit model (AICc = 27.48, R2 = 0.37)

the number of individual predators had a significant

positive correlation with predation pressure (F1, 27 =

8.80, P = 0.006; Fig. 3), while snail abundance at the

study site (F1, 27 = 10.96, P = 0.003; Fig. 3) and water

velocity (F1, 27 = 4.45, P = 0.04) had significantly

negative correlations with predation pressure. The

positive effect of individual predators was mainly due

to the number of crayfish rather than other preda-

tors, since in the best-fit model (AICc = 27.28,

R2 = 0.37) when these two variables were included

Predator-driven biotic resistance 1347

123

separately, only the numbers of crayfish was selected,

with a significant positive correlation (F1, 27 = 9.02,

P = 0.006), in addition to the negative correlations

with snail abundance (F1, 27 = 12.55, P = 0.002) and

water velocity (F1, 27 = 4.83, P = 0.04). The number

of other predators was not selected.

Res

idua

l no.

of P

. can

alic

ulat

a

0

1

2

3

0 100 200 300

Number of P. canaliculata in rice field

(a)

-2

-1

0

1

2

0 2 4 6 8 10 12

Number of animal species

(b)

-2

-1

0

1

2

0 1 2 3 4 5 6 7 8 9

Number of native species

(c)

-2

-1

0

1

2

0 1 2 3 4 5 6 7 8 9

Number of introduced species

(d)

-2

-1

0

1

2

0 1 2 3 4 5 6 7 8 9

Number of predator species

(e)

-2

-1

0

1

2

0 1 2 3 4 5 6 7 8 9

Number of non-predator species

(f)

ln (

Num

ber

of P

. can

alic

ulat

a +

1)

Res

idua

l no.

of P

. can

alic

ulat

a

Res

idua

l no.

of P

. can

alic

ulat

a

residual

Fig. 2 a Relationship

between the abundance of

P. canaliculata at the study

sites (ln-transformed values)

and their abundance in the

nearest rice fields. The

regression line and residual

are shown. b–f Relationship

between snail abundance

(residuals) at the study sites

and the number of:

(b) animal species,

(c) native species,

(d) introduced species,

(e) predator species, and

(f) non-predator species. In

(b)–(f), snail abundance is

expressed as the residuals of

the regression of snail

abundance at the study sites

on snail abundance in the

nearest rice field (a) for

graphical purposes

(n = 28 sites)

1348 Y. Yamanishi et al.

123

Discussion

Our result that snail abundance was negatively corre-

lated with animal richness suggests that the intensity

of biotic resistance affects the local abundance of the

highly invasive snail Pomacea canaliculata. The

Yamatogawa is a typical urban river, and the water

quality has been among the worst of Japanese rivers

for years (Ministry of Land, Infrastructure, Transport

and Tourism of Japan 2010). Although a recent survey

found several species that are relatively susceptible to

water pollution, its fauna is not rich (Osaka Museum of

Natural History 2007). It is remarkable that biotic

resistance exists at least in some part of such an urban

river. The results of this study, therefore, appear to

imply that biotic resistance to P. canaliculata may

exist in many Japanese rivers, where more animals are

expected to be present.

Another line of evidence also highlights the

importance of biological factors in affecting apple

snail populations in our study area. The number of

Pomacea canaliculata collected at the study sites was

affected by the number of snails in the nearest rice

fields. Since there are few predators of P. canaliculata,

including the crayfish Procambarus clarkii, in most

rice fields in Japan (Yusa 2006; Yusa et al. 2006),

snails can multiply there (Yoshida et al. 2009) and

many move from there into canals (Wada et al. 2009).

Our result therefore suggests that snail populations in

rivers and canals depend on immigration from rice

fields, which implies high mortality or emigration

rates in rivers and canals. Water depth, dissolved

oxygen, and temperature did not explain the variances

in snail abundance or predation pressure in the study

area. The only significant environmental factor was

water velocity, which was negatively correlated

with predation pressure. However, as there was no

significant relationship between water velocity and

snail abundance, the effect of water velocity on

predation pressure was not strong enough to affect

snail abundance. Although we only recorded environ-

mental variables in August and September, their direct

effects on apple snail abundance may be of limited

importance because P. canaliculata is tolerant of highly

variable environmental conditions including water

depth, current velocity and dissolved oxygen (Martın

et al. 2001; Kwong et al. 2008), with the exception of

low winter temperature (Yoshida et al. 2009), and

temperature in Nara is generally higher in water than on

land, seldom falling below 4�C and the water never

freezes (personal observations). Thus, apple snail

populations in rivers and canals in this part of Japan

may be regulated primarily by biological factors.

Three lines of evidence suggest that predators,

rather than non-predators (mostly competitors), regu-

late apple snail populations in our study sites. First, the

number of predator species was significantly corre-

lated with snail abundance, while that of non-predators

was not, implying that the negative relationship

between species richness and snail abundance is

mainly due to the richness of local predator commu-

nities. Among these predators, native rather than

introduced species were responsible for this pattern.

Second, although the number of individual predators

was not correlated with snail abundance, this was

probably due to opposing effects from the almost

0

1

2

3

4

0 20 40 60 80

Number of individual predators

(b)

ln (

Num

ber

of lo

st P

. can

alic

ulat

a +

1)

0

1

2

3

4

0 200 400 600 800

Number of P. canaliculata at each site

(a)Fig. 3 Relationship

between the number of

P. canaliculata lost in the

tethering experiment

(ln-transformed values) and

the number of: (a) living

P. canaliculata collected

and (b) individual predators

Predator-driven biotic resistance 1349

123

significant negative impact of overall predator num-

bers on apple snails and the positive association

between the number of crayfish and snails (see below

for further discussion). Third, the number of individual

predators was positively correlated with the number of

snails lost in the tethering experiment. However,

although the number of predator species affected snail

abundance, it did not affect predation pressure. This

inconsistency is probably related to the time span of

the study. Predation pressure, as assessed in our study,

is a measure of immediate (1-day) predation and hence

is likely to reflect the number of individual predators at

that time rather than predator species richness. How-

ever, snail abundance is affected by the cumulative

effects of long-term predation pressure, which prob-

ably reflects predator richness rather than temporal

predator abundance, which may change greatly with

time. Taken together, the three lines of evidence

indicate that predators play a key role in the mecha-

nism of biotic resistance against the apple snail.

A negative relationship between the number of

tethered snails lost and snail abundance at each site

suggests that predators did not consume tethered snails

much when there were plenty of wild snails. This result

is reasonable since the feeding potential of the predator

community is not unlimited. This is an important

applied issue, since predation pressure on an individual

snail will be weakened when snail abundance is high.

Thus, regulation by predators might be difficult, at least

in the short term, once the snail populations exceed a

critical level due to too many immigrants from rice

fields (more than several thousands from a rice field per

season; Wada et al. 2009). In our study, this might have

occurred at several sites where snail abundance was

extremely high ([100 individuals per site).

An important species responsible for the predation

pressure appears to be the crayfish Procambarus

clarkii. Crayfish accounted for 59% of all individual

predators collected, and their numbers were positively

correlated with the numbers of snails lost. The crayfish

is an important predator of thin-shelled freshwater

snail species (Correia et al. 2005) and its predation on

apple snails is intense in the laboratory (Yusa et al.

2006). However, there was a positive relationship, not

negative as expected for a predator–prey relationship,

between abundance of crayfish and apple snail abun-

dance. This suggests that the crayfish tended to co-

occur with the apple snail. Two reasons may explain

this. First, crayfish might migrate to the places where

their prey was abundant. Second, P. clarkii is also

preyed upon by many fish including the largemouth

bass (Micropterus salmoides) and the bluegill sunfish

(Lepomis macrochirus) (Maezono and Miyashita

2004), and hence crayfish might also be less abundant

at predator-rich sites. As P. clarkii is also an invasive

species, originating in North America, our results

suggest that one invasive species plays a role in biotic

resistance to new invasion by another. However, the

crayfish was not the only species responsible for the

biotic resistance to the apple snail, as the number of

native predator species had a negative relationship

with snail abundance. Although effects of native

predators on introduced prey have been little studied,

they have a great potential in regulating introduced

species (Carlsson et al. 2009).

Another important factor that affects apple snail

abundance is its propagule pressure (immigration rate)

from nearby rice fields. In fact, judging from F-values

(hence sum of squares), propagule pressure explained

the variance of local snail abundance better than

species richness. Thus, this study is in line with other

studies on various systems in that both propagule

pressure and biotic resistance regulate the success of

biological invasions (a model and review in D’Antonio

et al. 2001; plants in Von Holle and Simberloff 2005;

birds in Chiron et al. 2009). However, we stress the

importance of biotic resistance since high propagule

pressure from rice fields is ultimately due to lack of

efficient predators there (Yusa 2006; Yusa et al. 2006;

Yoshie and Yusa 2008, 2011).

In conclusion, we have demonstrated that the

intensity of biotic resistance regulates abundance of

an invasive species, Pomacea canaliculata. The biotic

resistance interacted with propagule pressure from

source populations in rice fields, where resistance is

less. The role of both native and introduced predators

is important in determining the intensity of resistance.

In other words, invasive species, once released from

their natural enemies in their original areas, may be

controlled if new enemies prey on them sufficiently in

introduced areas. To identify the environmental fac-

tors that activate predator communities is an important

next step.

Acknowledgments We thank Drs. Keiji Wada, Hiroaki Sato,

Hisao Ishii, Kenji Hamazaki, and two anonymous reviewers for

their valuable comments. We also thank members of the

Laboratory of Population and Community Ecology at Nara

Women’s University for discussion and assistance.

1350 Y. Yamanishi et al.

123

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