Journal of Animal

Ecology

2006

75

, 802813

2006 The Authors.
Journal compilation
2006 British
Ecological Society

Blackwell Publishing Ltd

Active and passive dispersal of an invading land snail in
Mediterranean France

SBASTIEN AUBRY, CORINNE LABAUNE, FRDRIC MAGNIN,
PHILIP ROCHE and LAURENCE KISS

Institut Mditerranen dEcologie et de Palocologie, IMEP-CNRS UMR 6116, Universit Paul Czanne
Aix-Marseille III, Btiment Villemin, Europle mditerranen de lArbois, BP80, 13545 Aix-en-Provence cedex 04,
France

Summary
1.

Land snail dispersal abilities are considered poor; however, the current invasion of
the French Mediterranean region by

Xeropicta derbentina

(Krynicki 1836), as well as
the past invasions of this region by several other species, seems to contradict this view.

2.

Using a multilevel approach, from individual experimentation to landscape analysis,
the dispersal abilities and mechanisms allowing the passive dispersal of

X. derbentina

are studied.

3.

The colonization of Provence occurred by stratied diffusion, where short-range
active dispersal occurs side by side with long-range passive dispersal.

4.

Active dispersal is not as limited as previously thought. In the eld, the capture
markrecapture method recorded a maximum distance covered of 42 m in 6 months
within a radius of 38 m from the original release point.

5.

Temperature and humidity, and therefore the time of year, inuence the main type of
dispersal. Dispersal is active during wet periods and essentially passive in dry and hot
months.

6.

Heat avoidance behaviour is one of the mechanisms allowing passive dispersal.

7.

Passive dispersal via human activities is the main determinant of

X. derbentina

distribution within the landscape. In comparison to other species,

X. derbentina

is found
more often in the vicinity of a communication route.

8.

These results show that land snails can cover large distances in a lifetime. The potential
for active and passive dispersal described in this paper enables

X. derbentina

to be a
successful invasive species and explains the rapid spread and current distribution of this
species.

Key-words

: behaviour, dispersal abilities, human impact, spatial distribution,

Xeropicta derbentina

(Krynicki).

Journal of Animal Ecology

(2006)

75

, 802813
doi: 10.1111/j.1365-2656.2006.01100.x

Introduction

Dispersal is an important, but little understood, feature
of ecology (Wiens 2001). In the case of alien species, an
understanding of this process is critical (Elton 1958;
Dieckman 1999; Holway & Suarez 1999; Ferriere

et al

.
2000). The dynamic of an invasion depends on the
mode of dispersal in use, and different types of models
have been developed to explain range expansion from
an initial colony (Shigesada & Kawasaki 1997). This
range expansion can result from a simple diffusion
process based on random movement into adjacent
areas. However, it can also result from the combination
of several dispersal modes (i.e. long range and short
range).

Xeropicta derbentina

(Krynicki 1836) is a land
snail in the family Helicidae, native to the eastern Medi-
terranean region including Croatia, Northern Greece,
Bulgaria, Romania, the Caucasus and Turkey. This
open-ground land snail, introduced to the south of
France in the 1940s, was recorded initially in that

Correspondence: Sbastien Aubry, Institut Mditerranen
dEcologie et de Palocologie, IMEP-CNRS UMR 6116,
Universit Paul Czanne Aix-Marseille III, Btiment Villemin,
Europle mditerranen de lArbois, BP80, 13545 Aix-
en-Provence cedex 04, France. E-mail: sa257@cam.ac.uk
803

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invasive land snail

2006 The Authors.
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Ecological Society,

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,

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region in 1949 (van regteren Altena 1960). Since the
1960s it has rapidly invaded most open environments
in Provence (Fig. 1), and a number of isolated and
ephemeral populations have been reported hundreds
of kilometres away from its current main French range
(Labaune & Magnin 1999). This wide geographical
range extension in a short time, coinciding with large
local productivity (with populations of

X. derbentina

often very dense, up to 10 350 snails m

2

), contradicts
the classical view of the slow dispersal of land gastro-
pods and highlights the need for studying the dispersal
abilities of such successful invasive species. A diffusion
process based on random walk seems insufcient to
explain the current distribution of that species. Instead,
the distribution map suggests an invasion by stratied
diffusion where long- and medium-range dispersal events
occur together with short-range dispersal (Hengeveld
1989; Shigesada & Kawasaki 1997).
Active dispersal of gastropods (snails and slugs) is
inuenced by many factors, including population density,
habitat complexity, climatic conditions and individual
characteristics such as body size or behaviours such as
homing tendency (Cowie 1980; Baker 1988a,b; Baur
& Baur 1990, 1991; Baur 1991). However, land snail
mobility is generally considered fairly poor and the role
of active dispersal in the rapid spread of invasive land
snails is thus considered negligible. For instance, large-
sized snail species, such as

Arianta arbustorum

, have been
shown to move between 2 and 5 m on average, with a
maximal distance recorded of 14 m, during a 3-month
activity period (Baur & Baur 1990), whereas

Trochoidea
geyeri

, smaller than

X. derbentina,

moves 3 m on average
during its entire annual life cycle (Pfenninger, Bahl &
Streit 1996).

Theba pisana

and

Cernuella virgata

, two
land snail species with body size and ecological and
biological features similar to

X. derbentina

, seem to
have greater dispersal ability with movement of several
tens of metres recorded in 1 month (Baker 1986, 1988a
for

T. pisana

, but see Cowie 1980, 1984; Baker 1988b
for

C. virgata

). However, the poor natural mobility of
land snails can be compensated for by a great potential
for passive dispersal by humans or animals (Kew 1893;
Fig. 1. (a) Distribution of the genus Xeropicta and the subspecies X. derbentina homoleuca (Brusina, 1870). Dashed line indicates
the limit of the Mediterranean climate. (b) Distribution of X. derbentina in south-eastern France: A, rst records of occurrence
(van regteren Altena 1960) 1 Tholonet 1949, 2 Rousset 1958, 3 Le Luc 1958; B, current continuous geographical range; C,
isolated populations; D, study site of Saint Michel-lObservatoire.
804

S. Aubry

et al.

2006 The Authors.
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Ecological Society,

Journal of Animal
Ecology

,

75

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802813

Locard & Germain 1903; Schlesch 1928; Welter-Schultes
1998; Cowie & Robinson 2003) and long-distance dis-
persals have been demonstrated (Schlesch 1928; Evans
1969; Cook, Goodfriend & Cameron 1993; Goodfriend,
Cameron & Cook 1994; Robinson 1999; Preece 2001).
Preliminary eld observations identied a potential
mechanism that may facilitate passive dispersal by

X. derbentina

. Like many xerophilous snail species,

X. derbentina

aestivates on vegetation or other above-
ground resting sites to escape ground heat (Bigot 1967;
Machin 1967; Sacchi 1971; Newel & Machin 1976;
Jaremovic & Rollo 1979; Newel & Appleton 1979; Cowie
1985). This behaviour during dry summer periods
leads to the formation of large clusters of individuals
rendering the invasion more visible. During this
aestivation period, an individual

X. derbentina

falling
on hot ground (e.g. dislodged by a vehicle, a walker,
an animal) becomes active and climbs up the nearest
resting site, which can be a vehicle or an object able to
transport it long distances and even overseas. This
behaviour, called the climbing reex, is therefore
assumed to be one of the main and most efcient features
in the process of passive dispersal. If this behaviour is
the main mechanism in

X. derbentina

dispersal it may
certainly inuence its distribution over the landscape,
i.e. distribution should be related to the location of
corridors that favour dispersal via human activity.
The aim of this paper was to study the active and passive
dispersal modes of

X. derbentina

by (i) measuring the
monthly distances moved by individual snails, (ii) analysing
the aestivation behaviour, more particularly the climbing
reex and its supposed role in passive dispersal, and
(iii) analysing the distribution of

X. derbentina

at the
landscape scale

.

Materials and methods

:c1i vr ni sirs:i xr:sirxrN1:
x:xrir:srrc:i1ir xr1non

Active dispersal rates were measured in the eld, in a
heterogeneous open environment composed of shrubs
within a matrix of grassland, thyme, lavender and bare
soil with rocks, delimited by stone walls, trees and
dense shrubs (Fig. 2). Within this 60

60 m eld, 100
snails were measured and located with coordinates in a
homogeneous 25 m

2

quadrat and identied with a
number using an indelible marker, a marking technique
that does not impede the dispersal rate (Baker 1988a,b).
Each individual was then released where it had been
found. Each month, for a period of 6 months, the marked
snails, which had dispersed quickly out of the initial
25 m

2

quadrat, were searched for carefully by examining
the quadrat and its surroundings in a concentric
manner. The whole 60

60 m eld as well as the sur-
rounding elds not shown on Fig. 2 were explored at
each time. The coordinates of each recaptured snail
were recorded, individuals were measured and marked
again in order to prevent the obliteration of the mark
by mucus or shell growth. Only individuals found 2 months
running were taken into account to calculate the average
monthly distances moved. These monthly distances
were compared by a one-way analysis of variance (

:Nov:

)
using the software package

s1:1is1ic:

for Windows version
Fig. 2. Schematic view of the study site where the capturemarkrecapture experiment was performed. A hundred individuals
were released in the grey square. The entire area, as well as the eld situated beyond the stone wall on the left of the gure, were
searched for marked snail every month. Dotted lines show the recorded displacement of six of the 12 individuals recaptured ve
consecutive times. Habitat types are: A, dense shrubland; B, grass and thyme; C, low grassland; D, marles; E, marles with thyme.
805

Dispersal of an
invasive land snail

2006 The Authors.
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Ecological Society,

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,

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50 (StatSoft France 1997). The temperature and relative
humidity at ground level were recorded using tinytalk
II Data Loggers.

cii xni Nc rrirx :s : iocrss or
ni sirs:i

Aestivating

X. derbentina

can form as many as three
epiphragms. We tested the reaction of snails taken from
their natural support, tearing off only their rst epiphragm.
Individuals which had formed only one and which
body was therefore visible after dislodgement were
discarded from the experiment. In total, 390 individu-
als were placed immediately beside an articial support
(diameter = 1 cm; height = 55 cm). In order to limit
the manipulation time, this was conducted in the eld.
The time required by each individual to become active
and climb on the support, as well as the height at which
it stopped, were recorded. These experiments were run
with groups of ve individuals and ve articial supports.
Because of the time needed to test so many individual
reactions, different microclimatic conditions occurred
during this experiment. In order to quantify the impor-
tance of these climatic conditions, 23 series of temper-
ature and relative humidity were recorded at different
times of the day above ground at 2 cm, 6 cm, 12 cm,
24 cm and 48 cm using a thermo-hygrometer.
In addition to this experiment, eld observations
were performed at the end of the drought period in
August. Cars were searched visually (wheels and body)
for individual snails. In order to search a large number
of vehicles, this was carried out in the parking areas of
seven supermarkets within the

X. derbentina

French
distribution range. A total of 1247 cars were searched.

ni s1i ni1i oN or

X

.



DERBENTI NA

vi 1ni N
1nr i:Nnsc:ir

In order to conrm the role of passive dispersal by
human activities on the distribution of

X. derbentina

,
the spatial relationship between its abundance and
various communication routes and human activities
was tested. The study site was located at the eastern
limit of the Luberon Mountain in Provence, 80 km
from the Mediterranean Sea. It is a 400 ha limestone
plateau with maximum elevation at 603 m, covered
mainly by grasslands or

Genista

and

Juniperus

shrub-
lands. These open habitats result from ancient intense
pastoral activity. However, because this area is unsuit-
able for mechanical agriculture the cover of woody
plants has increased rapidly during the last decades.
Consequently, in order to preserve this remarkably
biologically rich open environment, the Luberon Regional
Natural Park, in collaboration with shepherds, has
established a pastoral management programme on this
site.
A total of 140 sites distributed along nine transects
were sampled (Fig. 3). Each site was examined for
30 min to collect all living or freshly dead snail species
visible to the naked eye (D > 5 mm). Individuals were
then identied and counted in the laboratory.
A standard site description procedure was used,
based on Godron

et al

. (1968). Fourteen environmental
variables describing habitat structure at the soil surface
and grazing pressure were noted for each site during
the eldwork. The different types of habitat colonized
by

X. derbentina

within the study area were dened
using a cluster analysis (Euclidean distance) performed
on the environmental variable-samples matrix. Five
main habitat types were dened: (1) ruderal land, (2)
grasslands with high grazing pressure, (3) abandoned
land and grassland with weak grazing pressure, (4)
cultivated land (trufe oaks and lavender) and (5) shrub-
land. A principal component analysis was performed
on the environmental data of the 140 sites in order to
provide a quantitative and brief description of each site
that can be used in further analyses (principal compo-
nents: PC). Only the rst four principal components
(PcC1, PcC2, PcC3 and PcC4), explaining 578% of
the total variation of the data, were kept for the next
analyses.
The distances between sampling sites and landscape
components able to serve as corridors for passive dispersal
of

X. derbentina

, i.e. roads, tracks and grazing routes of
the sheep ock, were measured using a geographical
information system (GIS) (TNTmips 60 software).
The distribution of sampling sites with and without

X. derbentina

as a function of the distance from these
three kinds of corridors was compared using Kolmogorov
Smirnov tests.
Correlation coefcients and simple regressions were
calculated using

s1:1is1ic:

for Windows version 50.
Four variables of distances [distances to the roads
(Dr), the tracks (Dt), the grazing route (Dg) and to any
communication route (Drtg)] and the coordinates of
each sample on the rst four axes of the PCA (PcC1, PcC2,
PcC3 and PcC4) were used as explanatory variables in
GLM analyses performed on the 139 samples (one missing
value) using the software

crNs1:1

version 8.

Results

xoN1nix ni sii:crxrN1s or

X

.



DERBENTI NA

The recapture rates and distances covered in 1 month
by individual snails are shown in Table 1. After 1 month,
only about half of the marked snails were recovered
(54%), and during the following months the recovery
rate stabilized at around 30%. This relatively poor
recovery rate is due to the difculty of nding the
smaller marked snails (26%), i.e. less than 10 mm in
diameter (Table 2). The strong decrease in recapture in
October (12%) led to closure of the experiment.
In 6 months, the maximum distance covered by an
individual

X. derbentina

(corresponding to the sum of its
monthly displacements) was 42 m and the mean distance
moved (corresponding to the sum of average monthly
806

S. Aubry

et al.

2006 The Authors.
Journal compilation
2006 British
Ecological Society,

Journal of Animal
Ecology

,

75

,
802813
Fig. 3. Location of the 140 samples collected at St-Michel-lObservatoire (Alpes-de-Hautes-Provence, France) and abundance of
X. derbentina.
Table 1. Recovery rates, maximal and average distances covered by X. derbentina


Months
Number of days
AprilMay
29 days
MayJune
27 days
JuneJuly
31 days
JulyAug
26 days
AugSept
28 days
SeptOct
34 days
Recovery rates 54% 36% 33% 34% 29% 12%
Rates of consecutive recovery 31% 23% 20% 18% 9%
Maximum distance covered per month (m) 94 115 104 12 166 216
(03 m/days) (04 m/days) (03 m/days) (046 m/days) (06 m/days) (06 m/days)
Averages of distances covered per month (m) 57 22 5 35 28 28 58 33 5 38 95 67
(019 m/days) (018 m/days) (009 m/days) (022 m/days) (018 m/days) (028 m/days)
Covered maximal distances cumulated (m) 94 18 217 268 304 42
Cumulated average covered distances (m) 57 22 92 43 128 53 155 64 178 77 272 10
807

Dispersal of an
invasive land snail

2006 The Authors.
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,

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distances) was 272 m. Only 12 marked snails were
recovered for 5 consecutive months. These individuals
were found between 8 and 38 m of their initial position
(Fig. 2).

:Nov:

s show that there is a signicant difference
between the monthly distances moved by an individual
(

F

5,119

= 4708,

P

< 0001). Fishers least-squares differ-
ence (LSD)

post hoc

tests show that there is no difference
between the distances moved in May, June, August
and September, with a global average of 51 m, but
that there is a signicant decrease (mean = 28 m) of
displacements in July and a signicant increase
(mean = 95 m) in October in comparison to these 4
months.
Individual movements are shortest in July during the
dry season when

X. derbentina

aestivates (Fig. 4). In
August, recaptures took place after a few rainy days
that allowed snail activity. This explains the increase of
snail displacements observed although this was, on
average, a dry month. With the onset of autumn weather,
distances moved by individuals increased dramatically
in October (maximal distance moved of 216 m). This
increase may explain the decrease of recovery rates
(12%), as some individuals might have moved further,
making them difcult to nd.

nrn:vi oi :Nn i:ssi vr ni sirs:i

Climbing reex

Snail reactions were studied at several ground temper-
ature and relative humidity conditions (Fig. 5). Ground
temperature (T) varied between 33 and 52

C, and relative
humidity (RH) between 23 and 46%. For each of these
microclimatic conditions, the mean times required by
snails to become active (reaction time), climb onto the
support (climbing time) and the mean height at which
they came to rest are summarized in Table 3. Of the 390
individuals tested, only nine did not react.
There was no signicant difference [non-parametric
Friedman

:Nov:

for multiple dependent samples,

2

(

n

= 23, d.f. = 5) = 7018,

P

< 0219] among the relative
humidities recorded near the ground and at heights up
to 48 cm above the ground (Fig. 5a). On the other
hand, temperatures recorded near the ground and at
different heights were signicantly different (Friedmans

:Nov:

,

2

(

n

= 23, d.f. = 5) = 102277,

P

< 0001)
(Fig. 5b). There was a signicant decrease of tempera-
ture between ground level and 6 cm above the ground:
the mean decrease of temperature was 82

C between
the ground and 2 cm above the ground and 98

C
between the ground and 6 cm above the ground. Between
Table 2. Shell diameters of marked individual and number of individuals recaptured at least once or twice for each size class


Diameter 6 mm 7 mm 8 mm 9 mm 10 mm 11 mm 12 mm 13 mm 14 mm
(26 individuals) (74 individuals)
Marked 5 9 6 6 4 28 24 12 6
Once 1 1 0 0 3 20 22 9 6
Twice 0 0 0 0 3 16 17 7 3
Fig. 4. Mean and maximal distances moved by individual X. derbentina and daily temperature and relative humidity during the
6-month survey.
808
S. Aubry et al.
2006 The Authors.
Journal compilation
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Ecological Society,
Journal of Animal
Ecology, 75,
802813
12 and 48 cm above ground there was no signicant
variation in temperature.
Individual snails required between 26 s and 3 min
38 s to become active and between 3 min and 8 min 17 s
to climb and come to rest upon the support. The rela-
tionships between reaction time, climbing time and the
two microclimatic variables recorded near the ground
were studied using multiple regression: reaction time =
2255T + 21 RH (r
2
= 038; P < 001); climbing
time = 62388T + 12 RH (r
2
= 012; P < 001).
The time required by an individual to become active
and climb onto the support decreases signicantly with
increasing temperature (r
=
058, P < 001) and decreasing
relative humidity (r = 052, P < 001). This behaviour
suggests that the water loss caused by becoming active
is less important than the potential danger of remaining
inactive in the high temperature conditions on the ground.
There is no strong relationship between microcli-
matic conditions near the ground and snail xation
height. Nevertheless, the mean resting height of the 381
individuals was 69 cm, which is just above the level of
signicant temperature decrease. This conrms that this
behaviour is a way to escape high temperatures near the
ground. Furthermore, when levels of relative humidity
are sufciently high, individuals remain active for
longer periods of time and climb to slightly higher levels.
When the ground temperature is above 39 C, resting
height is also negatively correlated with humidity (r =
025, P < 001). This corresponds to a situation in
which individuals need to climb higher to escape harsher
hot and dry conditions.
Number of X. derbentina found on cars
X. derbentina was found on 088% of the searched vehicles
for a total of 21 individuals on 11 cars ( Table 4).
1nr ni s1i ni1i oN or X. DERBENTI NA :1
1nr i:Nnsc:ir sc:ir
The distances of samples, with and without X. derbentina,
to the nearest roads, tracks or grazing routes of sheep
(Figs 3 and 6) were compared. The distance to a track
of the 62 samples with X. derbentina was signicantly
different from that of the 78 samples without X. derbentina
(KolmogorovSmirnov test, D
obs
= 026, P < 005);
Fig. 5. (a) Temperature, (b) relative humidity recorded 23
times at six heights during the experiment (means, standard
errors and 95% condence intervals are given).
Fig. 6. Number of samples with (black) and without (grey) X.
derbentina at varying distances from (a) roads, (b) tracks, (c)
grazing route.
809
Dispersal of an
invasive land snail
2006 The Authors.
Journal compilation
2006 British
Ecological Society,
Journal of Animal
Ecology, 75,
802813
this difference was highly signicant when the dis-
tances to the roads (D
obs
= 036, P < 001) and grazing
routes (D
obs
= 048, P < 001) were considered.
Distances to the tracks, roads and grazing routes can
therefore explain the presence of X. derbentina. Indeed,
75% of the samples containing X. derbentina were less
than 100 m from a track, 200 m from a road and 250 m
from grazing routes.
In order to conrm the unique distribution of X.
derbentina a comparison was made to that of two other
land snail species: Candidula unifasciata (Poiret 1801)
(36 59 mm) and Jaminia quadridens (Mller 1774)
(712 354 mm). C. unifasciata, with 4968 individuals
collected in 131 samples, was the most abundant species
in the study area after X. derbentina and J. quadridens
was, like X. derbentina, present in 62 samples. The
proportion of samples containing any of these species
(%Xde, %Cun and %Jqu) in each 25-m class of distance
from a road, a track or grazing routes (distRCP) was
calculated (Fig. 7). Unlike X. derbentina (%Xde =
60602 distRCP; r
2
= 074; P < 001), there is no
linear relationship between the presence of either of the
two other species in a sample and its distance from a
communication route (%Cun: r
2
= 0027, P = 06;
%Jqu: r
2
= 016, P = 019).
A rst series of GLMs, using a quasi-Poisson distri-
bution tted to the data, was performed in order to nd
the best subset of variables explaining the abundance of
X. derbentina. Three variables, Drtg, PcC1 and PcC2,
were signicant when tested separately and explained,
Table 3. Mean time required by individuals to become active (reaction time), climb on the support (climbing time) and mean
height at which they came to rest for the 23 different conditions of temperature and humidity above ground


Series (no. of
individuals)
Ground
temperature
(C)
Ground relative
humidity (%) Reaction time Climbing time
Resting height
(cm)
S1 (9) 33 46 3 min 38 s 1 min 17 s 8 min 17 s 1 min 45 s 17 14
S2 (10) 36 41 1 min 40 s 1 min 5 min 11 s 1 min 45 s 6 4
S3 (10) 36 40 3 min 11 s 1 min 43 s 7 min 22 s 2 min 15 s 5 5
S4 (9) 36 39 2 min 04 s 44 s 7 min 00 s 5 min 05 s 10 10
S5 (15) 37 36 1 min 39 s 32 s 5 min 15 s 2 min 24 s 9 11
S6 (10) 38 33 2 min 20 s 44 s 2 min 58 s 3 min 16 s 1 1
S7 (10) 39 43 1 min 35 s 32 s 7 min 27 s 4 min 01 s 8 6
S8 (8) 39 40 2 min 29 s 39 s 6 min 49 s 2 min 12 s 10 11
S9 (15) 39 35 1 min 58 s 45 s 5 min 25 s 3 min 21 s 5 9
S10 (18) 39 30 1min 18 s 31 s 2 min 54 s 2 min 16 s 3 5
S11 (10) 39 27 1 min 11 s 32 s 5 min 13 s 1 min 54 s 16 16
S12 (20) 39 26 53 s 24 s 4 min 08 s 2 min 02 s 9 8
S13 (15) 40 40 2 min 08 s 1 min 13 s 6 min 49 s 3 min 21 s 5 7
S14 (29) 41 41 1 min 42 s 56 s 3 min 31s 1 min 55 s 4 3
S15 (30) 43 43 1 min 05 s 28 s 2 min 37 s 1 min 18 s 3 2
S16 (15) 43 40 1 min 47 s 39 s 3 min 46 s 2 min 19 s 4 5
S17 (18) 43 28 1 min 25 s 39 2 min 46 s 1 min 41 s 1 1
S18 (20) 45 27 55 s 33 s 3 min 37 s 52 s 2 2
S19 (20) 47 27 31 s 13 s 3 min 08 s 1 min 33 s 13 12
S20 (15) 48 25 44 s 16 s 4 min 02 s 1 min 25 s 9 14
S21 (15) 49 23 35 s 12 s 3 min 30 s 1 min 22 s 9 8
S22 (25) 50 26 26 s 12 s 3 min 04 s 2 min 17 s 9 12
S23 (35) 52 26 31 s 10 s 4 min 44 s 2 min 59 s 12 14
Correlation coefcients
T 058; P < 001 034; P < 001 009; NS
HR 052; P < 001 026; P < 001 013; NS
Table 4. Number of X. derbentina found on cars at seven car
parks in Provence


Sites
No. of
cars
No. of
infested
cars
% infested
cars
No. of
individuals
Lourmarin 240 3 125 7 (3, 3, 1)
Cucuron 168 2 120 4 (3, 1)
Pertuis north 261 3 115 5 (2, 2, 1)
Pertuis south 274 2 073 4 (2, 2)
Aubagne 130
Pont de lEtoile 23
La Destrousse 151 1 066 1
Total 1247 11 088 21
Fig. 7. Proportion of samples containing X. derbentina, C.
unifasciata or J. quadridens at varying distances (every 25 m)
from a road, a track or the grazing route.
810
S. Aubry et al.
2006 The Authors.
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respectively, 225%; 136% and 04% of the total deviance
(Table 5). The rst two principal components, PcC1
and PcC2, describe the habitat structure of the samples.
PcC1 distinguishes woodlands and grasslands while
PcC2 distinguishes shrublands from the others. These
two variables are signicant because no X. derbentina
individual was found in woodlands in the study area.
The three variables were incorporated into a second
GLM. Together, these variables explain 29% of the
total deviance (Table 5). The distance to any com-
munication routes is the most important term of the
model; however, the structure of habitat still explains
6539% of the deviance. The current distribution and
abundance of X. derbentina at the landscape level is
therefore dependent on two main features: commun-
ication routes and suitable habitats. No interaction
between these terms was found to be signicant.
Discussion
X. DERBENTI NA n:s coon :c1i vr
ni sirs:i :ni ii 1i rs
This paper provides evidence that the active dispersal
abilities of X. derbentina are not as limited as thought
previously. Similar to many other land snail species, the
distances covered by individuals of X. derbentina vary
according to weather conditions, in particular with
snails being least active during dry seasons (Cowie
1980; Baur & Baur 1990; Baker 1992). The distances
covered increase during the period of activity, which
corresponds in general with the reproductive season
(Baur & Baur 1993).
X. derbentina conrms this general model. Its dispersal
was lowest in July, the driest month (mean 28 m, max-
imum 104 m). Conversely, in October at the beginning
of the reproductive season, the most humid month of
the study, the longest distances moved were recorded
(mean 95 m, maximum 216 m).
In autumn, the rate of recaptures strongly decreased
and no dead marked snails were found. Two hypotheses
might explain this lack of recapture: either dilution of
marked snails is too important within the total area
prospected or individuals have dispersed outside that
area. While the latter hypothesis would suggest that the
data underestimates the real distances covered by indi-
vidual X. derbentina, the fact that larger snails were
recaptured more often suggests that the drop in recap-
ture rates results from the low probability of nding
snails in an heterogeneous habitat. This probability
decreased with time, as dispersal implies an increased
area to be prospected. Indeed, at the end of the experi-
ment the total area that was prospected (60 60 m eld
and surrounding elds) makes individual snails unlikely
to be found.
These results can be compared to those obtained on
the active dispersal of two biologically and ecologically
comparable species: T. pisana (Humphreys 1976;
Johnson 1981; Baker 1986) and C. virgata (Pomeroy
1969; Baker 1986, 1988a,b, 1992; Cowie 1980).
In Australia, Baker (1988a,b) found that C. virgata
and T. pisana could disperse actively as far as 25 and
55 m, respectively, in 1 month during their active period.
However, these distances were recorded in a homogene-
ous and heavily grazed low grassland, whereas the present
study site is a heterogeneous mosaic of grass and low
and high shrubs. Johnson (1981) recorded shorter
movements for T. pisana but considered that the data
underestimated the real values. On Rottnest Island
(Australia) Johnson & Black 1979, cited by Baker (1986),
considered that where dispersal seemed unimpeded, i.e.
where physical and human inuence was small, popu-
lations of T. pisana expanded approximately 20 m per
year. The recorded values for X. derbentina movement
(within a radius of 38 m during the 6-month study
period) suggest that greater population expansion could
be achieved by this species.
These results, however, need to be considered with
caution as a range of outcomes may result from various
contexts (habitats, climate, study period). Indeed, rates
of dispersal vary greatly with the structure of the habitat
(Cowie 1980; Wiens 2001) as well as with climate, micro-
climate and population density Baker (1988a). It is
clear in the case of X. derbentina that these are non-
negligible and X. derbentina dispersed preferentially in
open land. Also, these results are sensitive to a potential
source of error: local dispersal of the snails by animals
such as birds. In the present case, although the gures
are concordant with personal observations, this alterna-
tive cannot be rejected.
cii xni Nc rrirx i s : cici :i nrn:vi oi
i N 1nr iocrss or i:ssi vr ni sirs:i or
X. DERBENTI NA
The results show the importance of climatic conditions
in the climbing behaviour of X. derbentina. During the
day, temperatures decrease steeply with increasing height
above ground. In order to escape the hot and dry con-
ditions near the ground and the consequent desiccation
(Machin 1967; Cameron 1970), snails climb onto the
nearest support they can nd. This behaviour occurs
Table 5. Results of GLM using a quasi-Poisson distribution
tted to the data. Dependent variable is abundance of
Xeropicta derbentina. Only three signicant explanatory
variables are kept in the general model. No interaction
between variables was found to be signicant. Individual
percentage of deviance were obtained from former GLMs
tted for each variable separately


Variables d.f. Deviance F pr.
Accumulated
% deviance
Individual
% deviance
Drtg 1 45206 < 0001 22497 22497
PcC1 1 9380 0003 4668 13607
PcC2 1 3759 0059 1871 0400
Residual 135 139186
Total 138 200944
811
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2006 The Authors.
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2006 British
Ecological Society,
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Ecology, 75,
802813
especially in xerophilous species and characterizes
Helicidae, living in environments where no shade is
present, which cannot burrow into the ground (Sacchi
1971; Jaremovic & Rollo 1979). The behaviour reported
here highlights the 6 cm above-ground threshold up to
which temperatures decrease steeply. This threshold is
an important one in stress conditions. However, snails
can often be found several metres above ground during
wet periods.
The fact that individuals fallen from their support do
not wait for better climatic conditions (night) to become
active but try almost instantly to reach a safer environ-
ment is a crucial behaviour in the passive dispersal of
this species. In summer this event is not rare. Indeed, a
walker, an animal or a car, stopping in environments
where clusters of snails occur, almost always dislodge a
few individuals. The speed with which they react allows
the snails to climb onto the vehicle or object that disturbed
them and to be transported kilometres away. The rela-
tively high percentage of cars carrying X. derbentina
and the fact that X. derbentina was the only species
found reinforce this hypothesis. Furthermore, as only
the body and wheels of the vehicles were inspected,
these observations are certainly an underestimation of
the actual importance of passive dispersal by vehicles.
That the countryside in Provence is heavily populated
in summer possibly inuences the efciency of this
passive dispersal mechanism. Indeed, the colonization
of tourist areas in Provence seems to conrm this
hypothesis, because X. derbentina populations are
frequently found restricted to car parks when the
surrounding habitat is unsuitable (e.g. forests, mountain
grassland) or when colonization is recent.
i:Nnsc:ir ni s1i ni1i oN or
X. DERBENTI NA coNroxs 1o 1nr i:ssi vr
ni sirs:i xonri
The present study shows that passive dispersal is a
frequent and efcient means of dispersal that has allowed
X. derbentina to colonize a large area in a short time.
The study also demonstrates that the distribution of
X. derbentina within the landscape is strongly depend-
ent on the distribution of communication routes. Indeed,
although X. derbentina distribution is dependent on
the habitat structure, with populations occurring only
in open habitat in the study area (Aubry et al. 2005), it
is the proximity to a communication route that explains
most of its abundance. In 1992 it was present in the
study area at only one site, situated near the sample
E10 of the present study (Bigot & Favet 1994). Its rapid
spread cannot be explained by active dispersal alone
and the relationship between the presence of corridors
and the occurrence of X. derbentina highlights the impor-
tance of human dispersal. The national road (N100),
which traverses the study area, but also the tracks where
cars have access as well as the opening of habitats along
them, has promoted this invasion. Indeed, it is the con-
cordance between a suitable habitat and the proximity
to a communication route that determines the abund-
ance of this species at any particular site. The relation-
ship between the occurrence of X. derbentina and the
grazing routes seems to indicate a passive dispersal of
that species by sheep. Although no experimental work has
been conducted on this species, studies analysing dis-
persal by sheep have shown that is possible for other
land snail species (Fischer, Poschold & Beinlich 1996)
and it is one of the possible causes of the current
distribution of C. unifasciata on a larger scale (Pfenninger
& Posada 2002).
ioNc-ni s1:Ncr ni sirs:i
In view of the normal active speed of movement of land
snail, long-distance dispersal is one of their most
impressive features. Kew (1893), analysing the distri-
bution of land Mollusca, accumulated examples of such
long-distance dispersal and reported many possible
mechanisms allowing passive dispersal. Human activ-
ities have long been recognized as the main factor inu-
encing long-distance dispersal of land snails (Schlesch
1928). The present study reports the mechanisms that
have allowed X. derbentina to rapidly colonize the south
of France. In fact, this apparent rapid colonization can
also be the result of multiple introductions of snails
from Eastern Europe. Unfortunately, the study of three
mitochondrial DNA markers on individuals from
several population in Provence and Croatia did not provide
any signicant result, and this alternative hypothesis
cannot be ruled out. However, the present study shows
that multiple introductions were not necessary to explain
the current range of X. derbentina.
The rate of spread, as well as the vector of dispersal,
of X. derbentina are comparable to those of Helix aspersa
or T. pisana. Indeed, since the 19th century the former
has become the most widespread Mediterranean land
snail world-wide. Originating from North Africa, it
apparently colonized Europe instantaneously during
the Roman period (Evans 1972). It reached America,
Australia and various other countries later, with the
growth of human transportation. Similarly, T. pisana
colonized Europe from North Africa during the Iron
Age and extended its range dramatically with the increase
of human transportation. However, it must be noted
that Helix aspersa (an edible snail) was transported not
only accidentally but also intentionally by Romans and
others who were breeding this species. As a result,
H. aspersa has successfully colonized the majority of
regions where it had been transported whereas T. pisana,
because of its narrower ecological requirements, is
often restricted to the littoral of the regions it reached.
This present study shows that transport by vehicles
may explain the occurrence of restricted, and prob-
ably ephemeral, populations of X. derbentina in non-
Mediterranean regions (e.g. Alsace, A. Bertrand, personal
communication). This study also explains its overseas
dispersal and how X. derbentina can be one of the 20
snail species most commonly intercepted on retrograde
812
S. Aubry et al.
2006 The Authors.
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2006 British
Ecological Society,
Journal of Animal
Ecology, 75,
802813
military cargos (interception records 197487 APHIS-
USDA).
Acknowledgements
This work was supported by Agence Rgionale pour
lEnvironnement (Conseil Rgional Provence-Alpes-
Cte-dAzur) and Ministre de lAmnagement du
Territoire et de lEnvironnement (Programme Inva-
sions Biologiques). The authors thank Adam P. Coutts
and three anonymous referees for their comments on a
previous version of the manuscript.
References
Aubry, S., Labaune, C., Magnin, F. & Kiss, L. (2005) Habitat
and integration within indigenous communities of Xeropicta
derbentina (Gastropoda: hygromiidae), a recently introduced
land snail in South-Eastern France. Diversity and Distribu-
tions, 11, 539547.
Baker, G.H. (1986) The biology and control of white snails
(Mollusca: Helicidae), introduced pests in Australia. CSIRO
Australian Division of Entomology Technical Paper, 25, 131.
Baker, G.H. (1988a) Dispersal of Theba pisana (Mollusca:
Helicidae). Journal of Applied Ecology, 25, 889900.
Baker, G.H. (1988b) The dispersal of Cernuella virgata
(Mollusca: Helicidae). Australian Journal of Zoology, 36,
513520.
Baker, G.H. (1992) Movement of introduced white snails
between pasture and cereal crops in south Australia. Pest of
Pastures: Weed, Invertebrate and Diseases Pests of Australian
Sheep Pastures (ed. E.S. Delfosse), pp. 115120. Common-
wealth Scientic and Industrial Research Organization (CSIRO)
Information Services, Melbourne.
Baur, A. (1991) Effects of competitive interactions and habitat
structure on life-history traits and dispersal in land snails.
Comprehensive Summaries of Uppsala Dissertations from
the Faculty of Science, 325, 32 pp. Uppsala University,
Uppsala.
Baur, A. & Baur, B. (1990) Are roads barriers to dispersal in the
land snail Arianta arbustorum? Canadian Journal of Zoology,
68, 613617.
Baur, A. & Baur, B. (1991) Effect of habitat form on dispersal
in the land snail Arianta arbustorum. Effects of competitive
interactions and habitat structure on life-history traits and
dispersal in the land snails. Appendix VI. PhD Thesis,
Uppsala University, Uppsala.
Baur, B. & Baur, A. (1993) Climatic warming due to thermal
radiation from an urban area as possible cause for local extinc-
tion of a land snail. Journal of Applied Ecology, 30, 333340.
Bigot, L. (1967) Recherches sur les groupements de gastro-
podes terrestres: la constitution des grappes. Vie et Milieu,
18, 127.
Bigot, L. & Favet, C. (1994) Craux de St Michel lObservatoire:
Inventaire Des Invertbrs, 35 pp. Parc Naturel Rgionale
du Luberon, Apt.
Cameron, R.A.D. (1970) The effect of temperature on the
activity of three species of helicid snail (Mollusca: Gastro-
poda). Journal of Zoology (London), 162, 303315.
Cook, L.M., Goodfriend, G.A. & Cameron, R.A.D. (1993)
Changes in the land snail fauna of eastern Madeira during
the Quaternary. Philosophical Transactions of the Royal
Society of London, 339, 83103.
Cowie, R.H. (1980) Observations on the dispersal of two
species of British land snail. Journal of Conchology, 30,
201208.
Cowie, R.H. (1984) Density, dispersal and neighbourhood
size in the land snail Theba pisana. Heredity, 52, 391401.
Cowie, R.H. (1985) Microhabitat choice and high temper-
ature tolerance in the land snail Theba pisana (Mollusca:
Gastropoda). Journal of Zoology, London A, 207, 201
211.
Cowie, R.H. & Robinson, D.G. (2003) Pathways of introduc-
tion of nonindegenous land and freshwater snails and slugs.
Invasive Species: Vector and Management Strategies (eds
G. M. Ruiz & J. T. Carlton), pp. 93122. Island Press, London.
Dieckman, U. (1999) The evolutionary ecology of dispersal.
Trends in Ecology and Evolution, 14, 8890.
Elton, C.S. (1958) The Ecology of Invasions by Animals and
Plants. Methuen, London.
Evans, J.G. (1969) Land and freshwater Mollusca in archae-
ology: chronological aspects. World Archaeology, 2, 170
185.
Evans, J.G. (1972) Land Snails in Archaeology. Seminar Press,
London & New York.
Ferriere, R., Belthoff, J.R., Olivieri, I. & Krackow, S. (2000)
Evolving dispersal: where to go next? Trends in Ecology and
Evolution, 15, 57.
Fischer, S., Poschold, P. & Beinlich, B. (1996) Experimental
studies on the dispersal of plants and animals on sheep in
calcareous grasslands. Journal of Applied Ecology, 33,
12061222.
Godron, M., Daget, P., Long, G., Sauvage, C., Emberger, L.,
Le Floch, E., Wacquant, J.P. & Poissonnet, J. (1968) Code
Pour le Relev Mthodique de la Vgtation et Du Milieu.
Centre National de la Recherche Scientique (CNRS) edn.
CNRS, Paris.
Goodfriend, G.A., Cameron, R.A.D. & Cook, L.M. (1994)
Fossil evidence of recent human impact on the land
snail fauna of Madeira. Journal of Biogeography, 21, 309
321.
Hengeveld, R. (1989) Dynamics of Biological Invasions.
Chapman & Hall, London.
Holway, D.A. & Suarez, A.V. (1999) Animal behaviour: an
essential component of invasion biology. Trends in Ecology
and Evolution, 14, 328330.
Humphreys, J. (1976) Field observations on Theba pisana
(Mller) (Gastropoda: Helicidae) at St. Ives, Cornwall.
Journal of Conchology, 29, 93106.
Jaremovic, R. & Rollo, D. (1979) Tree climbing by the snail
Cepaea nemoralis (L.): a possible method for regulating
temperature and hydratation. Canadian Journal of Zoology,
57, 10101014.
Johnson, M.S. (1981) Effects of migration and habitat choice
on shell banding frequencies in Theba pisana at a habitat
boundary. Heredity, 47, 121134.
Kew, H.W. (1893) The Dispersal of Shells. Kegan Paul, Trench,
Trbner & Co., London.
Labaune, C. & Magnin, F. (1999) Un escargot nouveau venu
dans le Luberon et en Provence: Xeropicta derbentina
(Krinicki, 1836). Courrier Scientique Du Parc Naturel
Rgional de Luberon, 3, 102110.
Locard, A. & Germain, L. (1903) Sur lintroduction despces
mridionales dans la faune malacologique des environs de
Paris. Mmoires de Lacadmie des Sciences, Belles Lettres
et Arts de Lyon, 3
e
Srie, VIII, 57126.
Machin, J. (1967) Structural adaptations for reducing water-
loss in three species of terrestrial snail. Journal of Zoology,
152, 5565.
Newel, P.F. & Machin, J. (1976) Water regulation in aestivat-
ing snails. Ultrastructural and analytical evidence for an
unusual cellular phenomenon. Cell and Tissue Research,
173, 417421.
Newell, P.F. & Appleton, T.C. (1979) Aestivating snails the
physiology of water regulation in the mantle of the ter-
restrial pulmonate Otala lactea. Malacologia, 18, 575
581.
Pfenninger, M., Bahl, A. & Streit, B. (1996) Isolation by
distance in a population of a small land snail Trochoidea
813
Dispersal of an
invasive land snail
2006 The Authors.
Journal compilation
2006 British
Ecological Society,
Journal of Animal
Ecology, 75,
802813
geyeri: evidence from direct and indirect methods. Pro-
ceedings of the Royal Society of London, 263, 12111217.
Pfenninger, M. & Posada, D. (2002) Phylogeographic history
of the land snail Candidula unifasciata (Helicellinae,
Stylomatophora): fragmentation, corridor, migration,
and secondary contact. Evolution, 56, 17761778.
Pomeroy, D.E. (1969) Some aspects of the ecology of the land
snail, Helicella virgata in South Australia. Australian Jour-
nal of Zoology, 17, 495514.
Preece, R.C. (2001) Introduced land molluscs on the islands
of the Tristan da CunhaGough group (South Atlantic).
Journal of Conchology, 37, 253259.
Regteren Altena, C.O. van (1960) On the occurrence of a
species of Xeropicta in France. Basteria, 24, 2126.
Robinson, D.G. (1999) Alien invasions: the effects of the
global economy on non-marine gastropod introductions
into the United States. Malacologia, 41, 413438.
Sacchi, C.F. (1971) Ecologie compare des Gastropodes
Pulmons des dunes mditerranennes et atlantiques. Natura,
62, 277358.
Schlesch, H. (1928) La dispersion des mollusques. Actes de la
Socit Linnenne de Bordeaux, LXXX, 119146.
Shigesada. N. & Kawasaki, K. (1997) Biological Invasions:
Theory and Practice. Oxford University Press, Oxford.
StatSoft France (1997) STATISTICA Pour Windows. StatSoft
France, Charenton-le-Pont.
Welter-Schultes, F.W. (1998) Human-dispersed land snails in
Crete, with special reference to Albinaria (Gastropoda:
Clausiliidae). Biologia Gallo-Hellenica, 24, 83106.
Wiens, J.A. (2001) The landscape context of dispersal. Dispersal
(eds J. Clobert, E. Danchin, A.A. Dhont & J.D. Nichols),
pp. 96109. Oxford University Press, Oxford.
Received 13 November 2005; accepted 22 February 2006