active and passive dispersal of invasive snail in south france

7/27/2019 Active and Passive Dispersal of Invasive Snail in South France

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Journal of Animal

Ecology 200675, 802813

2006 The Authors.Journal compilation 2006 BritishEcological Society

Blackwell Publishing Ltd

Active and passive dispersal of an invading land snail in

Mediterranean France

SBAS TIEN AUBRY, CORINNE L ABAUNE, FRD RIC M AGNIN,PHILI P ROCHE and LAURENC E KIS SInstitut 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 ofthe French Mediterranean region by Xeropicta derbentina

(Krynicki 1836), as well asthe 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 stratified 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 field, the capturemarkrecapture method recorded a maximum distance covered of 42 m in 6 monthswithin a radius of 38 m from the original release point.

5.

Temperature and humidity, and therefore the time of year, influence the main type ofdispersal. Dispersal is active during wet periods and essentially passive in dry and hotmonths.

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 foundmore 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 asuccessful invasive species and explains the rapid spread and current distribution of thisspecies.

Key-words

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

Xeropicta derbentina

(Krynicki).

Journal of Animal Ecology

(2006) 75

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

Introduction

Dispersal is an important, but little understood, featureof ecology (Wiens 2001). In the case of alien species, anunderstanding 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 froman initial colony (Shigesada & Kawasaki 1997). Thisrange expansion can result from a simple diffusionprocess based on random movement into adjacentareas. However, it can also result from the combinationof several dispersal modes (i.e. long range and shortrange). Xeropicta derbentina

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

Correspondence: Sbastien Aubry, Institut MditerranendEcologie 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: [email protected]


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region in 1949 (van regteren Altena 1960). Since the1960s it has rapidly invaded most open environmentsin Provence (Fig. 1), and a number of isolated andephemeral populations have been reported hundredsof kilometres away from its current main French range(Labaune & Magnin 1999). This wide geographicalrange extension in a short time, coinciding with largelocal 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 dispersalabilities of such successful invasive species. A diffusionprocess based on random walk seems insufficient toexplain the current distribution of that species. Instead,the distribution map suggests an invasion by stratifieddiffusion where long- and medium-range dispersal eventsoccur together with short-range dispersal (Hengeveld1989; Shigesada & Kawasaki 1997).

Active dispersal of gastropods (snails and slugs) isinfluenced by many factors, including population density,habitat complexity, climatic conditions and individual

characteristics such as body size or behaviours such ashoming tendency (Cowie 1980; Baker 1988a,b; Baur& Baur 1990, 1991; Baur 1991). However, land snailmobility is generally considered fairly poor and the roleof active dispersal in the rapid spread of invasive landsnails is thus considered negligible. For instance, large-sized snail species, such asArianta arbustorum

, have beenshown to move between 2 and 5 m on average, with amaximal distance recorded of 14 m, during a 3-month

activity period (Baur & Baur 1990), whereas Trochoideageyeri

, smaller thanX. derbentina,

moves 3 m on averageduring its entire annual life cycle (Pfenninger, Bahl &Streit 1996). Theba pisana

and Cernuella virgata

, twoland snail species with body size and ecological andbiological features similar to X. derbentina

, seem tohave greater dispersal ability with movement of severaltens of metres recorded in 1 month (Baker 1986, 1988afor T. pisana

, but see Cowie 1980, 1984; Baker 1988bfor C. virgata

). However, the poor natural mobility ofland snails can be compensated for by a great potentialfor passive dispersal by humans or animals (Kew 1893;

Fig. 1. (a) Distribution of the genusXeropictaand the subspecies X. derbentina homoleuca(Brusina, 1870). Dashed line indicatesthe limit of the Mediterranean climate. (b) Distribution of X. derbentinain south-eastern France: A, first 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.


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Locard & Germain 1903; Schlesch 1928; Welter-Schultes1998; Cowie & Robinson 2003) and long-distance dis-persals have been demonstrated (Schlesch 1928; Evans1969; Cook, Goodfriend & Cameron 1993; Goodfriend,Cameron & Cook 1994; Robinson 1999; Preece 2001).

Preliminary field observations identified a potentialmechanism 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; Cowie1985). This behaviour during dry summer periodsleads to the formation of large clusters of individualsrendering the invasion more visible. During thisaestivation period, an individual X. derbentina

fallingon hot ground (e.g. dislodged by a vehicle, a walker,an animal) becomes active and climbs up the nearestresting site, which can be a vehicle or an object able totransport it long distances and even overseas. Thisbehaviour, called the climbing reflex, is thereforeassumed to be one of the main and most efficient features

in the process of passive dispersal. If this behaviour isthe main mechanism in X. derbentina

dispersal it maycertainly influence its distribution over the landscape,i.e. distribution should be related to the location ofcorridors that favour dispersal via human activity.

The aim of this paper was to study the active and passivedispersal modes of X. derbentina

by (i) measuring themonthly distances moved by individual snails, (ii) analysingthe aestivation behaviour, more particularly the climbingreflex and its supposed role in passive dispersal, and

(iii) analysing the distribution of X. derbentina

at thelandscape scale

.

Materials and methods

:

Active dispersal rates were measured in the field, in aheterogeneous open environment composed of shrubs

within a matrix of grassland, thyme, lavender and baresoil with rocks, delimited by stone walls, trees anddense shrubs (Fig. 2). Within this 60

60 m field, 100snails were measured and located with coordinates in ahomogeneous 25 m

2

quadrat and identified with anumber using an indelible marker, a marking techniquethat does not impede the dispersal rate (Baker 1988a,b).Each individual was then released where it had beenfound. Each month, for a period of 6 months, the markedsnails, which had dispersed quickly out of the initial25 m

2

quadrat, were searched for carefully by examiningthe quadrat and its surroundings in a concentric

manner. The whole 60

60 m field as well as the sur-rounding fields not shown on Fig. 2 were explored ateach time. The coordinates of each recaptured snailwere recorded, individuals were measured and markedagain in order to prevent the obliteration of the markby mucus or shell growth. Only individuals found 2 monthsrunning were taken into account to calculate the averagemonthly distances moved. These monthly distanceswere compared by a one-way analysis of variance (

)using the software package

for Windows version

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


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50 (StatSoft France 1997). The temperature and relativehumidity at ground level were recorded using tinytalkII Data Loggers.

Aestivating X. derbentina

can form as many as threeepiphragms. We tested the reaction of snails taken fromtheir natural support, tearing off only their first epiphragm.

Individuals which had formed only one and whichbody was therefore visible after dislodgement werediscarded from the experiment. In total, 390 individu-als were placed immediately beside an artificial support(diameter = 1 cm; height = 55 cm). In order to limitthe manipulation time, this was conducted in the field.The time required by each individual to become activeand climb on the support, as well as the height at whichit stopped, were recorded. These experiments were runwith groups of five individuals and five artificial supports.Because of the time needed to test so many individualreactions, 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 differenttimes 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, field observationswere performed at the end of the drought period inAugust. Cars were searched visually (wheels and body)for individual snails. In order to search a large numberof vehicles, this was carried out in the parking areas ofseven supermarkets within the X. derbentina

Frenchdistribution range. A total of 1247 cars were searched.

X

.

DERBENTINA

In order to confirm the role of passive dispersal byhuman activities on the distribution of X. derbentina

,the spatial relationship between its abundance andvarious communication routes and human activitieswas tested. The study site was located at the easternlimit of the Luberon Mountain in Provence, 80 kmfrom the Mediterranean Sea. It is a 400 ha limestoneplateau with maximum elevation at 603 m, coveredmainly by grasslands or Genista

and Juniperus

shrub-

lands. These open habitats result from ancient intensepastoral activity. However, because this area is unsuit-able for mechanical agriculture the cover of woodyplants has increased rapidly during the last decades.Consequently, in order to preserve this remarkablybiologically rich open environment, the Luberon RegionalNatural Park, in collaboration with shepherds, hasestablished a pastoral management programme on thissite.

A total of 140 sites distributed along nine transectswere sampled (Fig. 3). Each site was examined for30 min to collect all living or freshly dead snail species

visible to the naked eye (D > 5 mm). Individuals werethen identified and counted in the laboratory.

A standard site description procedure was used,based on Godron et al

. (1968). Fourteen environmentalvariables describing habitat structure at the soil surfaceand grazing pressure were noted for each site duringthe fieldwork. The different types of habitat colonizedby X. derbentina

within the study area were definedusing a cluster analysis (Euclidean distance) performedon the environmental variable-samples matrix. Five

main habitat types were defined: (1) ruderal land, (2)grasslands with high grazing pressure, (3) abandonedland and grassland with weak grazing pressure, (4)cultivated land (truffle oaks and lavender) and (5) shrub-land. A principa l component analysis was performedon the environmental data of the 140 sites in order toprovide a quantitative and brief description of each sitethat can be used in further analyses (principal compo-nents: PC). Only the first four principal components(PcC1, PcC2, PcC3 and PcC4), explaining 578% ofthe total variation of the data, were kept for the nextanalyses.

The distances between sampling sites and landscapecomponents able to serve as corridors for passive dispersalof X. derbentina

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

X. derbentina

as a function of the distance from thesethree kinds of corridors was compared using KolmogorovSmirnov tests.

Correlation coefficients and simple regressions werecalculated using

for Windows version 50.Four variables of distances [distances to the roads(Dr), the tracks (Dt), the grazing route (Dg) and to anycommunication route (Drtg)] and the coordinates ofeach sample on the first four axes of the PCA (PcC1, PcC2,PcC3 and PcC4) were used as explanatory variables inGLM analyses performed on the 139 samples (one missingvalue) using the software

version 8.

Results

X

.

DERBENTINA

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 recoveryrate stabilized at around 30%. This relatively poorrecovery rate is due to the difficulty of finding thesmaller marked snails (26%), i.e. less than 10 mm indiameter (Table 2). The strong decrease in recapture inOctober (12%) led to closure of the experiment.

In 6 months, the maximum distance covered by anindividualX. derbentina

(corresponding to the sum of itsmonthly displacements) was 42 m and the mean distancemoved (corresponding to the sum of average monthly


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Fig. 3. Location of the 140 samples collected at St-Michel-lObservatoire (Alpes-de-Hautes-Provence, France) and abundance ofX. derbentina.

Table 1. Recovery rates, maximal and average distances covered by X. derbentina

MonthsNumber of days AprilMay29 days MayJune27 days JuneJuly31 days JulyAug26 days AugSept28 days SeptOct34 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 42Cumulated average covered distances (m) 57 22 92 43 128 53 155 64 178 77 272 10


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

s show that there is a significant differencebetween 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 differencebetween the distances moved in May, June, Augustand September, with a global average of 51 m, butthat there is a significant decrease (mean = 28 m) ofdisplacements in July and a significant increase

(mean = 95 m) in October in comparison to these 4months.

Individual movements are shortest in July during thedry season when X. derbentina

aestivates (Fig. 4). InAugust, recaptures took place after a few rainy daysthat allowed snail activity. This explains the increase ofsnail displacements observed although this was, onaverage, a dry month. With the onset of autumn weather,distances moved by individuals increased dramaticallyin October (maximal distance moved of 216 m). Thisincrease may explain the decrease of recovery rates(12%), as some individuals might have moved further,making them difficult to find.

Climbing reflex

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

C, and relativehumidity (RH) between 23 and 46%. For each of thesemicroclimatic conditions, the mean times required bysnails to become active (reaction time), climb onto thesupport (climbing time) and the mean height at whichthey came to rest are summarized in Table 3. Of the 390individuals tested, only nine did not react.

There was no significant difference [non-parametricFriedman

for multiple dependent samples,

2

(

n

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

< 0219] among the relativehumidities recorded near the ground and at heights upto 48 cm above the ground (Fig. 5a). On the otherhand, temperatures recorded near the ground and atdifferent heights were significantly different (Friedmans

, 2 (n = 23, d.f. = 5) = 102277, P < 0001)(Fig. 5b). There was a significant decrease of tempera-ture between ground level and 6 cm above the ground:the mean decrease of temperature was 82 C betweenthe 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 6Once 1 1 0 0 3 20 22 9 6Twice 0 0 0 0 3 16 17 7 3

Fig. 4. Mean and maximal distances moved by individual X. derbentinaand daily temperature and relative humidity during the6-month survey.


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12 and 48 cm above ground there was no significantvariation in temperature.

Individual snails required between 26 s and 3 min38 s to become active and between 3 min and 8 min 17 sto climb and come to rest upon the support. The rela-tionships between reaction time, climbing time and thetwo microclimatic variables recorded near the groundwere studied using multiple regression: reaction time =2255T+ 21 RH (r2= 038; P< 001); climbingtime = 62388T+ 12 RH (r2= 012; P< 001).

The time required by an individual to become activeand climb onto the support decreases significantly withincreasing temperature (r =058, P< 001) and decreasingrelative humidity (r =052, P< 001). This behavioursuggests that the water loss caused by becoming activeis less important than the potential danger of remaininginactive in the high temperature conditions on the ground.

There is no strong relationship between microcli-matic conditions near the ground and snail fixationheight. Nevertheless, the mean resting height of the 381individuals was 69 cm, which is just above the level ofsignificant temperature decrease. This confirms that this

behaviour is a way to escape high temperatures near theground. Furthermore, when levels of relative humidityare sufficiently high, individuals remain active forlonger periods of time and climb to slightly higher levels.When the ground temperature is above 39 C, restingheight is also negatively correlated with humidity (r =025, P< 001). This corresponds to a situation inwhich individuals need to climb higher to escape harsherhot and dry conditions.

Number of X. derbentinafound on cars

X. derbentinawas found on 088% of the searched vehiclesfor a total of 21 individuals on 11 cars (Table 4).

X. DERBENTINA

The distances of samples, with and withoutX. derbentina,to the nearest roads, tracks or grazing routes of sheep(Figs 3 and 6) were compared. The distance to a trackof the 62 samples with X. derbentinawas significantlydifferent from that of the 78 samples without X. derbentina(KolmogorovSmirnov test, Dobs= 026, P< 005);

Fig. 5. (a) Temperature, (b) relative humidity recorded 23times at six heights during the experiment (means, standard

errors and 95% confidence intervals are given).

Fig. 6. Number of samples with (black) and without (grey) X.derbentinaat varying distances from (a) roads, (b) tracks, (c)grazing route.


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this difference was highly significant when the dis-tances to the roads (Dobs= 036, P< 001) and grazingroutes (Dobs= 048, P < 001) were considered.

Distances to the tracks, roads and grazing routes cantherefore explain the presence of X. derbentina. Indeed,75% of the samples containing X. derbentinawere lessthan 100 m from a track, 200 m from a road and 250 mfrom grazing routes.

In order to confirm the unique distribution of X.derbentinaa comparison was made to that of two otherland snail species: Candidula unifasciata(Poiret 1801)(36 59 mm) and Jaminia quadridens(Mller 1774)(712 35 4 mm). C. unifasciata, with 4968 individualscollected in 131 samples, was the most abundant speciesin the study area after X. derbentinaand J. quadridens

was, like X. derbentina, present in 62 samples. Theproportion 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) wascalculated (Fig. 7). Unlike X. derbentina (%Xde =60602 distRCP; r2= 074; P< 001), there is nolinear relationship between the presence of either of thetwo other species in a sample and its distance from acommunication route (%Cun: r2= 0027, P= 06;%Jqu: r2= 016, P= 019).

A first series of GLMs, using a quasi-Poisson distri-bution fitted to the data, was performed in order to findthe best subset of variables explaining the abundance ofX. derbentina.Three variables, Drtg, PcC1 and PcC2,were significant when tested separately and explained,

Table 3. Mean time required by individuals to become active (reaction time), climb on the support (climbing time) and meanheight at which they came to rest for the 23 different conditions of temperature and humidity above ground

Series (no. ofindividuals)

Groundtemperature(C)

Ground relativehumidity (%) 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 14S2 (10) 36 41 1 min 40 s 1 min 5 min 11 s 1 min 45 s 6 4S3 (10) 36 40 3 min 11 s 1 min 43 s 7 min 22 s 2 min 15 s 5 5S4 (9) 36 39 2 min 04 s 44 s 7 min 00 s 5 min 05 s 10 10S5 (15) 37 36 1 min 39 s 32 s 5 min 15 s 2 min 24 s 9 11S6 (10) 38 33 2 min 20 s 44 s 2 min 58 s 3 min 16 s 1 1S7 (10) 39 43 1 min 35 s 32 s 7 min 27 s 4 min 01 s 8 6S8 (8) 39 40 2 min 29 s 39 s 6 min 49 s 2 min 12 s 10 11S9 (15) 39 35 1 min 58 s 45 s 5 min 25 s 3 min 21 s 5 9S10 (18) 39 30 1min 18 s 31 s 2 min 54 s 2 min 16 s 3 5S11 (10) 39 27 1 min 11 s 32 s 5 min 13 s 1 min 54 s 16 16S12 (20) 39 26 53 s 24 s 4 min 08 s 2 min 02 s 9 8S13 (15) 40 40 2 min 08 s 1 min 13 s 6 min 49 s 3 min 21 s 5 7S14 (29) 41 41 1 min 42 s 56 s 3 min 31s 1 min 55 s 4 3S15 (30) 43 43 1 min 05 s 28 s 2 min 37 s 1 min 18 s 3 2S16 (15) 43 40 1 min 47 s 39 s 3 min 46 s 2 min 19 s 4 5S17 (18) 43 28 1 min 25 s 39 2 min 46 s 1 min 41 s 1 1S18 (20) 45 27 55 s 33 s 3 min 37 s 52 s 2 2S19 (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 14S21 (15) 49 23 35 s 12 s 3 min 30 s 1 min 22 s 9 8S22 (25) 50 26 26 s 12 s 3 min 04 s 2 min 17 s 9 12S23 (35) 52 26 31 s 10 s 4 min 44 s 2 min 59 s 12 14

Correlation coefficients T 058; P< 001 034; P< 001 009; NSHR 052; P< 001 026; P< 001 013; NS

Table 4. Number of X. derbentinafound on cars at seven carparks in Provence

SitesNo. ofcars

No. ofinfestedcars

% infestedcars

No. ofindividuals

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 1Total 1247 11 088 21

Fig. 7. Proportion of samples containing X. derbentina, C.unifasciataor J. quadridensat varying distances (every 25 m)from a road, a track or the grazing route.


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respectively, 225%; 136% and 04% of the total deviance(Table 5). The first two principal components, PcC1and PcC2, describe the habitat structure of the samples.PcC1 distinguishes woodlands and grasslands whilePcC2 distinguishes shrublands from the others. Thesetwo variables are significant because no X. derbentina

individual was found in woodlands in the study area.The three variables were incorporated into a secondGLM. Together, these variables explain 29% of thetotal deviance (Table 5). The distance to any com-munication routes is the most important term of themodel; however, the structure of habitat still explains6539% of the deviance. The current distribution andabundance of X. derbentinaat the landscape level istherefore dependent on two main features: commun-ication routes and suitable habitats. No interactionbetween these terms was found to be significant.

Discussion

X. DERBENTINA

This paper provides evidence that the active dispersalabilities of X. derbentinaare not as limited as thoughtpreviously. Similar to many other land snail species, thedistances covered by individuals of X. derbentinavaryaccording to weather conditions, in particular withsnails being least active during dry seasons (Cowie1980; Baur & Baur 1990; Baker 1992). The distancescovered increase during the period of activity, which

corresponds in general with the reproductive season(Baur & Baur 1993).

X. derbentinaconfirms this general model. Its dispersalwas lowest in July, the driest month (mean 28 m, max-imum 104 m). Conversely, in October at the beginningof the reproductive season, the most humid month ofthe study, the longest distances moved were recorded(mean 95 m, maximum 216 m).

In autumn, the rate of recaptures strongly decreasedand no dead marked snails were found. Two hypothesesmight explain this lack of recapture: either dilution ofmarked snails is too important within the total area

prospected or individuals have dispersed outside thatarea. While the latter hypothesis would suggest that thedata underestimates the real distances covered by indi-vidual X. derbentina, the fact that larger snails wererecaptured more often suggests that the drop in recap-ture rates results from the low probability of findingsnails in an heterogeneous habitat. This probabilitydecreased with time, as dispersal implies an increasedarea to be prospected. Indeed, at the end of the experi-ment the total area that was prospected (60 60 m field

and surrounding fields) makes individual snails unlikelyto be found.

These results can be compared to those obtained onthe active dispersal of two biologically and ecologicallycomparable species: T. pisana (Humphreys 1976;Johnson 1981; Baker 1986) and C. virgata (Pomeroy1969; Baker 1986, 1988a,b, 1992; Cowie 1980).

In Australia, Baker (1988a,b) found that C. virgataand T. pisanacould disperse actively as far as 25 and55 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 lowand high shrubs. Johnson (1981) recorded shortermovements for T. pisanabut considered that the dataunderestimated 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 influence was small, popu-lations of T. pisanaexpanded approximately 20 m peryear. The recorded values for X. derbentinamovement(within a radius of 38 m during the 6-month studyperiod) suggest that greater population expansion couldbe achieved by this species.

These results, however, need to be considered withcaution as a range of outcomes may result from variouscontexts (habitats, climate, study period). Indeed, ratesof 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 isclear in the case of X. derbentinathat these are non-negligible and X. derbentinadispersed preferentially inopen land. Also, these results are sensitive to a potentialsource of error: local dispersal of the snails by animalssuch as birds. In the present case, although the figuresare concordant with personal observations, this alterna-tive cannot be rejected.

X. DERBENTINA

The results show the importance of climatic conditionsin the climbing behaviour of X. derbentina. During theday, temperatures decrease steeply with increasing heightabove 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 thenearest support they can find. This behaviour occurs

Table 5. Results of GLM using a quasi-Poisson distributionfitted to the data. Dependent variable is abundance ofXeropicta derbentina. Only three significant explanatoryvariables are kept in the general model. No interactionbetween variables was found to be significant. Individualpercentage of deviance were obtained from former GLMsfitted for each variable separately

Variables d.f. Deviance F pr.Accumulated% deviance

Individual% deviance

Drtg 1 45206 < 0001 22497 22497PcC1 1 9380 0003 4668 13607PcC2 1 3759 0059 1871 0400Residual 135 139186Total 138 200944


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especially in xerophilous species and characterizesHelicidae, living in environments where no shade ispresent, which cannot burrow into the ground (Sacchi1971; Jaremovic & Rollo 1979). The behaviour reportedhere highlights the 6 cm above-ground threshold up towhich temperatures decrease steeply. This threshold isan important one in stress conditions. However, snailscan often be found several metres above ground duringwet periods.

The fact that individuals fallen from their support do

not wait for better climatic conditions (night) to becomeactive but try almost instantly to reach a safer environ-ment is a crucial behaviour in the passive dispersal ofthis species. In summer this event is not rare. Indeed, awalker, an animal or a car, stopping in environmentswhere clusters of snails occur, almost always dislodge afew individuals. The speed with which they react allowsthe snails to climb onto the vehicle or object that disturbedthem and to be transported kilometres away. The rela-tively high percentage of cars carrying X. derbentinaand the fact that X. derbentinawas the only speciesfound reinforce this hypothesis. Furthermore, as only

the body and wheels of the vehicles were inspected,these observations are certainly an underestimation ofthe actual importance of passive dispersal by vehicles.That the countryside in Provence is heavily populatedin summer possibly influences the efficiency of thispassive dispersal mechanism. Indeed, the colonizationof tourist areas in Provence seems to confirm thishypothesis, because X. derbentina populations arefrequently found restricted to car parks when thesurrounding habitat is unsuitable (e.g. forests, mountaingrassland) or when colonization is recent.

X. DERBENTINA

The present study shows that passive dispersal is afrequent and efficient means of dispersal that has allowedX. derbentinato colonize a large area in a short time.The study also demonstrates that the distribution ofX. derbentinawithin the landscape is strongly depend-ent on the distribution of communication routes. Indeed,although X. derbentinadistribution is dependent onthe habitat structure, with populations occurring onlyin open habitat in the study area (Aubry et al. 2005), it

is the proximity to a communication route that explainsmost of its abundance. In 1992 it was present in thestudy area at only one site, situated near the sampleE10 of the present study (Bigot & Favet 1994). Its rapidspread cannot be explained by active dispersal aloneand the relationship between the presence of corridorsand the occurrence of X. derbentinahighlights the impor-tance of human dispersal. The national road (N100),which traverses the study area, but also the tracks wherecars have access as well as the opening of habitats alongthem, 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. derbentinaand thegrazing routes seems to indicate a passive dispersal ofthat species by sheep. Although no experimental work hasbeen conducted on this species, studies analysing dis-persal by sheep have shown that is possible for otherland snail species (Fischer, Poschold & Beinlich 1996)and it is one of the possible causes of the currentdistribution of C. unifasciataon a larger scale (Pfenninger

& Posada 2002).

-

In view of the normal active speed of movement of landsnail, long-distance dispersal is one of their mostimpressive features. Kew (1893), analysing the distri-bution of land Mollusca, accumulated examples of suchlong-distance dispersal and reported many possiblemechanisms allowing passive dispersal. Human activ-ities have long been recognized as the main factor influ-encing long-distance dispersal of land snails (Schlesch

1928). The present study reports the mechanisms thathave allowed X. derbentinato rapidly colonize the southof France. In fact, this apparent rapid colonization canalso be the result of multiple introductions of snailsfrom Eastern Europe. Unfortunately, the study of threemitochondrial DNA markers on individuals fromseveral population in Provence and Croatia did not provideany significant result, and this alternative hypothesiscannot be ruled out. However, the present study showsthat multiple introductions were not necessary to explainthe current range of X. derbentina.

The rate of spread, as well as the vector of dispersal,of

X. derbentinaare comparable to those of

Helix aspersaor T. pisana. Indeed, since the 19th century the formerhas become the most widespread Mediterranean landsnail world-wide. Originating from North Africa, itapparently colonized Europe instantaneously duringthe Roman period (Evans 1972). It reached America,Australia and various other countries later, with thegrowth of human transportation. Similarly, T. pisanacolonized Europe from North Africa during the IronAge and extended its range dramatically with the increaseof human transportation. However, it must be notedthat Helix aspersa(an edible snail) was transported notonly accidentally but also intentionally by Romans and

others who were breeding this species. As a result,H. aspersa has successfully colonized the majority ofregions where it had been transported whereas T. pisana,because of its narrower ecological requirements, isoften restricted to the littoral of the regions it reached.This present study shows that transport by vehiclesmay explain the occurrence of restricted, and prob-ably ephemeral, populations of X. derbentinain non-Mediterranean regions (e.g. Alsace, A. Bertrand, personalcommunication). This study also explains its overseasdispersal and how X. derbentinacan be one of the 20snail species most commonly intercepted on retrograde


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military cargos (interception records 197487 APHIS-USDA).

Acknowledgements

This work was supported by Agence Rgionale pourlEnvironnement (Conseil Rgional Provence-Alpes-Cte-dAzur) and Ministre de lAmnagement duTerritoire et de lEnvironnement (Programme Inva-sions Biologiques). The authors thank Adam P. Coutts

and three anonymous referees for their comments on aprevious version of the manuscript.

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Received 13 November 2005; accepted 22 February 2006


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