High Resilience of Mediterranean Land Snail Communities to Wildfires

Biodiversity and Conservation (2006) 15:2925–2944 Springer 2006 DOI 10.1007/s10531-005-3430-4

-1 High resilience of Mediterranean land snail communities to wildﬁres

LAURENCE KISS* and FRE´ DE´ RIC MAGNIN Institut Me´diterraneén d’Ecologie et de Paleóećologie, U.M.R. 6116 du C.N.R.S., Baˆtiment Villemin, Domaine du Petit Arbois, Avenue Louis Philibert, BP 80, Cerege 13545, Aix-en-Provence Cedex 04; *Author for correspondence(e-mail: [email protected]; phone: (+0)-33-04-42-90-84-42; fax: (+0)-33-04-42-90-84-48)

Received 6 May 2004; accepted in revised form 28 February 2005

Key words: Biodiversity, Land snails, Mediterranean ecosystems, Resilience, Wildﬁres

Abstract. In the Mediterranean region, wildfires have devastating effects on animals with limited mobility. With their poor dispersal abilities, their habitats on vegetation and in litter, and their sensitivity to humidity and shade, we expected land snails to be an interesting model to assess short, medium and long-term impact of fires on fauna biodiversity and their resilience. Stratified sampling was carried out on 12 sampling sites in garrigues and forests of Provence (southeastern France), according to fire regime (number of fires, fire intervals and age of the last fire) over the past 30 years. Data were investigated using diversity indexes, Kruskal–Wallis test, dendrogram of affinities and Correspondence Analysis (CA). We found, however, that Mediterranean land snail communities are particularly resilient to fires. Although abundance is drastically reduced in the short-term, species richness and community diversity are preserved provided that the time lapse between two successive fires is longer than the time required for recovery (i.e. around 5 years). This high community resilience in the short-term may be partly due to ecological and ethological aptitudes of land snails. However, these astonishing results, which have implications for conservation biology, are mainly due to the presence, within burned areas, of cryptic refuges that allow initial land snail survival, malacofauna persistence after successive fires and consistent biogeographical patterns in the long-term.

Introduction

Wildfires are major disturbances within the Mediterranean basin, particularly within ecosystems of Provence (southeastern France) owing to climatic conditions (drought during summer and a strong wind called Mistral) and flammability of vegetation (Sousa 1984; Le Houe´ rou 1987; Trabaud 1987; Whelan 1995). Over recent decades, wildfires have been reinforced by build-up of fuel due to increasing garrigue (calcareous mattoral) and forest subsequent to land-abandonment since the beginning of the 20th century (Barbero et al. 1987; Le Houe´ rou 1987). Over the last decades, consequences of wildfires on Mediterranean fauna have been broadly studied (Athias-Binche et al. 1987; Hetier 1993; Whelan 1995; Hailey 2000; Haim 2002; Santalla et al. 2002). Both direct and short-term impacts of fire generally have devastating effects on fauna with an immediate reduction in abundance (Athias-Binche 2926 et al. 1987; Arnold et al. 1993; Hetier 1993; Whelan 1995; Lyon et al. 2000). Animals, with limited mobility living above ground on vegetation or in litter, which are not able to escape approaching front flame, are most vulnerable to fire-caused mortality and injury (Hetier 1993; Whelan 1995; Hailey 2000; Lyon et al. 2000; Vernes 2000; Tooker and Hanks 2003). In addition, the resulting habitat loss influences communities much more dra- matically than does smoke, heat or flames (Whelan 1995; Hailey 2000; Lyon et al. 2000). Burned areas are more open, illuminated and desiccated than pre-fire areas, and generally favour a more xerophilous fauna (Athias-Binche et al. 1987; Arnold et al. 1993; Fons et al. 1993; Whelan 1995; Santalla et al. 2002; Kiss and Magnin 2003). Habitat structure, vegetation stands and fauna generally respond to disturbance by secondary successions, i.e. post-fire changes (Sousa 1984; Athias-Binche et al. 1987; Fons et al. 1993; Haim 1993). During the one or two decades following fire, ecosystems reach more or less rapidly a stable state comparable to the pre-fire state (Trabaud and Lepart 1980): initially dominant herbaceous layers decrease, while shrub and tree layers become dominant over time (Barbero et al. 1987; Trabaud 1987). Species with high dispersal ability, which are able to use post-fire resources under rough habitat conditions, are favoured during the first post-fire years and replace pre-fire species (Sousa 1984; Athias-Binche et al. 1987; Blondel 1995; Whelan 1995). However, when frequent fires occur with fire interval of under 10 years, vegetation structure tends to be very simple, with only low shrubs and grass, (Barbero et al. 1987) and fire regime may also induce change in fauna biodiversity (Gill and McCarthy 1998). Although numerous studies treat the effects of fire on fauna and on their patterns of post-fire recovery, our studies (Kiss 1999, 2002; Kiss and Magnin 2002, 2003; Kiss et al. 2004) are among the few which have dealt with the impact of wildfire on Mediterranean land snail communities and with their habitat destruction. Land snails live for the most part on vegetation and in litter (Kerney et al. 1999; Heller 2001), and they have little or no ability to escape and poor active dispersal aptitudes (Cameron et al. 1980; Baur and Baur 1990; Pfenninger 2002). Moreover, gastropods are very sensitive to desiccation (Bonavita 1961; Lazaridou-Dimitriadou and Daguzan 1978; Godan 1983) and they probably do not survive the high temperatures reached during a fire. In consequence, they are highly vulnerable to fire and then to destruction of their habitats. In addition, land snails are particularly sensitive to the structure, humidity and shade of their micro-habitats (Boycott 1934; Cameron and Redfern 1976; Bishop 1977; Kerney et al. 1999). Thus, malacofaunas are expected to have low ability to respond to disturbances. They would appear to be an interesting model to reliably assess the short, medium and long-term impact of wildfires on fauna biodiversity, and to analyse their patterns of recovery and their resilience after one or successive fires. Understanding such patterns may be important in conservation. 2927

Figure 1. Location map of study area and of sampling sites. The 12 sampling sites are named after the dates of the various wildﬁres over the sampling period (i.e. 1973–2001).

Materials and methods

Study area

The study area is located in the ‘‘de´ partement des Bouches-du-Rhoˆ ne’’ (Provence, southeastern France) (Figure 1; Table 1) where ﬁre is a frequent disturbance, with an average of 26 wildﬁres of over 100 ha per year between 1973 and 2001 (Centre informatique de la Pre´ fecture des Bouches-du-Rhoˆ ne 2002). A true Mediterranean climate (three dry summer months and two cold winter months) characterises the study area with annual rain averaging between 543 and 680 mm and annual temperatures averaging between 14 and 11 C (C.N.R.S. 1975). Sampling sites, with calcareous substrates, range from 140 to 660 m in altitude and are composed of grassland, of garrigue (calcareous mattoral), and of pine and oak woods (Molinier 1974).

Sampling strategy

Stratified sampling, based on synchronic study, was carried out according to number of fires, fire intervals and age of the last fire over the past 30 years, i.e. fire regime (Sousa 1984; Whelan 1995; Lloret and Marı´ 2001). Twelve sites of various fire regimes were selected. Six sites which have burned once over the period studied (i.e. 1973–2001) were sampled during Spring 2000. Five sites 2928

Table 1. Sampling sites.

Fire dates Name of mountainous areas

1998 Regagnas 1997 Chaıˆ ne de l’Etoile 1979–1997 Chaıˆ ne de l’Etoile 1973–1979–1997 Chaıˆ ne de l’Etoile 1979–1989–1997 Chaıˆ ne de l’Etoile 1995 Chaıˆ ne des Coˆ tes 1989–1995 Chaıˆ ne des Coˆ tes 1993 Sainte Baume 1991 Chaıˆ ne des Coˆ tes 1989 Regagnas 1979–1989 Chaıˆ ne des Coˆ tes 1971 Chaıˆ ne des Coˆ tes Each sampling site is named after the dates of the various wildfires over the sampling period (i.e. 1973–2001). The mountainous areas for each sampling site are also indicated. which have burned twice or three times and one last burned in 1971 were sampled during Spring 2001. This latter site was chosen to act as a reference site since post-fire recovery of forest in the French Mediterranean region is around 30 years (Barbero et al. 1987; Hetier 1993). For each site, 10 sampling points were plotted in various post-fire vegetation stands: grassland (Brachypodium retusum Beauvais), garrigue (Quercus coccifera Linnaeus, Quercus ilex Linnaeus, Ulex parviflorus Pourret, Rosmarinus officinalis Linnaeus and Cistus albidus Linnaeus), oak stand (Quercus pubescens Willdenow) and pine stand (Pinus halepensis Miller). For the sites which have burned more than once, sampling was performed at the intersection of the burned areas. A total of 120 sampling points were performed in order to ensure a proper representation of land snail communities from various post-fire vegetation stands within each sampling site. Floristic variables, environmental variables (Godron et al. 1968) and malacofauna were recorded at each sampling point consisting of a square of 5 · 5m.

Sampling of land snails

At each sampling point, two different samples of land snails were taken (Kiss et al. 2004). All land snails over 5 mm in diameter were collected during a standard interval of 30 min within the square of 5 · 5 m. Minute species (i.e. under 5 mm in diameter) were collected in four squares of 25 · 25 cm including litter and the five upper centimetres of soil. Soil sample treatment (sieved on series of meshes graded from 5 to 0.5 mm), snail count and snail identification were performed in the laboratory. Only fresh shells (i.e. with intact periostracum) and living individuals were taken into account because they are representative of current communities. The list of species sampled follows the nomenclature of Kerney et al. (1999) (see Appendix 1). 2929

Data analyses

The impact of fire regime on biodiversity of gastropod communities was assessed using the Shannon diversity index and equitability (Legendre and Legendre 1998). Species richness, diversity of communities and land snail abundance were compared at the twelve sampling sites using the Kruskal– Wallis test (nonparametric statistical test, significance threshold at p = 0.05) because of heterogeneity of variance (homogeneity of variance test, significant threshold at p = 0.01). Changes in land snail communities exposed to various fire regimes were assessed using Correspondence Analysis (CA). Xeropicta derbentina was considered as supplementary variable, because it strongly contributed to the first two axes and because it affected readability of scatter plots (variables and sampling points) of a preliminary CA. Thus, the final CA was performed on a land snail data matrix composed of 45 species collected within 120 sampling points (SLP Statistique Jambu 1994). The consequences of various fire regimes on species composition of communities were also analysed. Similarities between community composition at each sampling site were estimated using Sørensen index (Legendre and Legendre 1998). A Sørensen matrix was compiled using Sørensen indices cal- culated between sampling sites taken two at a time. The Sørensen matrix was then subjected to a Principal coordinate analysis (PcoA). Coordinates obtained on all axes of the PcoA were used to elaborate a dendrogram of affinities between the malacofauna at each sampling site, according to the Ward’s minimum variance methods (i.e. hierarchical agglomerative clustering method) (Ward 1963; Legendre and Legendre 1998).

Results

Short-term impact of ﬁres

The short-term impact of fires was studied on sampling sites burned in 1998 and in 1997 whatever the fire regime (Figures 2–4). Sampling was carried out respectively 18 months, 3 and 4 years after the last fire. Abundance is drastically reduced after fire (Figures 2 and 3). For all species, only 30 living individuals remained 18 months later out of 1269 individuals/250 m2 collected (Figures 2 and 3). However, abundance in living individuals varies widely between the second and the third year after a single fire: it increases from 30 to 310 living individuals (Figure 2). Moreover, abundance reaches 591 living individuals on average four years after fire at the three other sites with last fire in 1997 (i.e. 1973–1979–1997, 1979–1989– 1997 and 1979–1997), i.e. whatever the number of fires and the fire intervals (Figure 2). 2930

Figure 2. Abundance of living individuals within the 12 sampling sites. Sampling sites are ordered on the axis according to the last ﬁre date and the number of ﬁres.

Figure 3. Species richness (in black) and abundance of living individuals and fresh shells (in grey) of communities within the 12 sampling sites. Sampling sites are ordered on the axis according to the last ﬁre date and the number of ﬁres.

Fires seem to have limited short-term impact on composition of land snail communities (i.e. fresh shells and living individuals), whatever the fire regime, i.e. number of fires, fire intervals and age of the last fire. Eighteen months after fire, although communities are not very abundant, they are greatly diversified, with open-habitat species, saxicolous species, shrubland species, and even Mediterranean shade-loving species (Figure 4). One to two years after the last fire, mesophilous and forest species are present in post-fire communities, whatever the number of fires and the fire intervals. Moreover, litter species and minute species living in the upper centimetres of soil are also predominant, even on the sampling site recently burned (Figure 4b). Some of the most common species in Provence, i.e. Papillifera solida, Solatopupa similis, Candidula gigaxii, Candidula unifasciata, Granaria variabilis, Microxeromagna armillata, Pomatias elegans, Oxychilus draparnaudi, 2931

Figure 4. Abundance of fresh shells and living individuals of species sampled within sampling sites recently burned. (a) Land snails over 5 mm in diameter, (b) species under 5 mm in diameter. All species collected are classified in four groups according to their habitat requirements, i.e. saxicolous, xerophilous, shade-tolerant and shade-loving species. Sampling sites are ordered on the axis according to the last fire date and the number of fires. 1998 – Sampling site burned 18 months ago; 1997 – Sampling site burned 3 years ago; 1979–1997, 1973–1979–1997 and 1979–1989–1997 – Sampling sites burned 4 years ago. See Appendix 1 for species codes.

Granopupa granum and Truncatellina callicratis are relatively abundant on all the sampling sites.

Impact of various ﬁre regimes on species richness, abundance and diversity

Successive fires do not seem to induce a decrease in abundance of communities (Figures 2 and 3). However, abundance varies among sampling sites, with an average of 528±303 living individuals/250 m2 and 2484±1190 individuals/ 250 m2 (i.e., fresh shells and living individuals) (Figures 2 and 3). Indeed, significant differences in abundance are revealed by the Kruskal–Wallis tests performed at sampling sites not only on living individuals (i.e. X2 = 28.37, p = 0.003, df = 11) but also on fresh shells and living individuals (i.e. X2 = 27.2, p = 0.004, df = 11). Abundances are low during the first four post-fire years, i.e. under 600 living individuals/250 m2 and 2000 individuals/ 250 m2 (Figures 2 and 3). However, communities seem to reach an equilibrium a few years after fire because abundance generally increases with the age of the last fire, with the exception of three sampling sites, i.e. two sampling sites burned once in 1991 and in 1989 and the sampling site with regular fire frequency (i.e. 1979–1989– 1997). In this latter, the high abundances observed are due to the presence of 2932 numerous individuals of two minute species, i.e. Vallonia costata with 1217 individuals/250 m2 and G. granum with 1669 individuals/250 m2 (Figure 4b). At both former sampling sites, these results may be due to dense vegetation cover of garrigue, composed of Q. coccifera and U. parviflorus, which favours increase in shelter and in litter cover. This in turn makes it more difficult to sample large land snails (i.e. over 5 mm in diameter). The various fire regimes do not seem to affect either species richness (i.e., living individuals and fresh shells per sampling site) or diversity (Figure 3; Table 2). Indeed, species richness is comparable among sampling sites with an average of 24.5±3.5 species and the Kruskal–Wallis test does not demonstrate significant differences in species richness among sampling sites (i.e. X2 = 13.40, p = 0.27, df = 11). However, the least species richness is not observed at the site recently burned (i.e. 1998 with 25 species) but at the sampling sites burned twice with short and moderate fire interval (i.e. 1989–1995 and 1979–1989), where there are only 20 species (Figure 3). Moreover, the greatest species richness is not observed at the reference site burned once in 1971 (23 species) but at the sampling sites burned once in 1991 (31 species) and twice with a long fire interval (i.e. 1979–1989; 30 species). Diversity indexes are also comparable among sampling sites, with Shannon index, Is = 3.43±0.37 and equitability, E = 0.75±0.06 on average (Table 2). No significant differences in Shannon indexes among sampling sites are revealed by the Kruskal–Wallis test (i.e. X2 = 12, p = 0.36, df = 11). How- ever, the sampling sites which have burned twice with short or moderate fire interval or three times with moderate fire intervals (i.e. 1989–1995, 1979–1989 and 1979–1989–1997) have the lowest diversity indexes, respectively Is = 2.85 and E = 0.66, Is = 2.84 and E = 0.66 and Is = 3.22 and E = 0.68.

Changes in land snail communities exposed to various ﬁre regimes

The CA was performed to assess changes in malacofaunas and structure of land snail communities after various ﬁre regimes (Figure 5). Axis 1 (10.78% of total inertia) is a habitat closing gradient which places human-modiﬁed

Table 2. Shannon diversity index and equitability of sampling sites ordered according to the last ﬁre date and the number of ﬁres.

1998 1997 1979 1973 1979 1995 1989 1993 1991 1989 1979 1971

1997 1979 1989 1995 1989

1997 1997

Shannon index 3.93 3.85 3.75 3.47 3.22 3.40 2.85 3.12 3.70 3.74 2.84 3.31 Equitability 0.85 0.81 0.76 0.77 0.68 0.75 0.66 0.68 0.75 0.84 0.66 0.73 2933

Figure 5. Axes 1–2 of the CA performed on the land snail data matrix (45 species–120 sampling points). (a) Ordination diagram of species; (b) ordination diagram of sampling points. Stars – southern sampling sites located in ‘‘la Chaıˆ ne de l’Etoile’’; squares – southern sampling sites located in ‘‘le Regagnas’’ and ‘‘la Sainte Baume’’; triangles – northern sampling sites located in ‘‘la Chaıˆ ne des Coˆ tes’’. See Appendix 1 for species codes. habitats, grassland, and fallow land on the positive end and garrigue, pine stand and oak stand on the negative end. It places open habitat species (C. gigaxii and G. granum) on the positive end, and litter and forest species (Punctum pygmaeum, Vitrea contracta, Acanthinula aculeata, V. costata, T. callicratis and P. elegans) on the negative end (Figure 5a; Table 3). Axis 1 2934

Table 3. Signiﬁcant species variables on axes 1 and 2 of the CA (45 species–120 sampling points).a

Positive end Negative end

Axis 1 Granopupa granum (Ctr. = 0.16) Punctum pygmaeum (Ctr. = 0.26) Candidula gigaxii (Ctr. = 0.04) Vitrea contracta (Ctr. = 0.11) Acanthinula aculeata (Ctr. = 0.06) Vallonia costata (Ctr. = 0.05) Truncatellina callicratis (Ctr. = 0.05) Pomatias elegans (Ctr. = 0.03) Axis 2 Punctum pygmaeum (Ctr. = 0.06) Vallonia costata (Ctr. = 0.64) Candidula unifasciata (Ctr. = 0.04) Lauria cylindracea (Ctr. = 0.05) Xerosecta cespitum (Ctr. = 0.04) Monacha cantiana (Ctr. = 0.03) Solatopupa similis (Ctr. = 0.02) aCtr. – Contribution. clearly places sampling points of both sites burned once in 1971 and in 1998 on the negative end, and the sampling points of the sites located in ‘‘la Chaıˆ ne de l’Etoile’’ burned once or thrice respectively in 1997 and in 1979– 1989–1997 on the positive end (Figure 5b; Table 4). All the sampling points of the site burned at short ﬁre interval (i.e. 1989–1995) are clustered on the positive end together with open and dry habitat species (Sphincterochila candidissima, Trochoidea pyramidata, S. similis, C. unifasciata, C. gigaxii) (Figures 5a and b). Axis 2 (9.25% of total inertia) places fallow land (Monacha cantiana, Xerosecta cespitum) and garrigue (P. pygmaeum, C. unifasciata and S. similis) species on the positive end, and pine stand species (V. costata and Lauria cylindracea) on the negative end (Figure 5a; Table 3). Axis 2 seems to be not only a habitat structure gradient but also a site location gradient because it discriminates between sampling points of southern sites (i.e. 1989, 1979–1997

Table 4. Signiﬁcant sampling point variables on axes 1 and 2 of the CA (45 species–120 sampling points).a

Positive end Negative end

Axis 1 1997sn09 (Ctr. = 0.03) 1971sn03 (Ctr. = 0.10) 1979–1989–1997sn06 (Ctr. = 0.02) 1991sn01 (Ctr. = 0.05) 1971sn07 (Ctr. = 0.05) 1998sn10 (Ctr. = 0.03) 1971sn09 (Ctr. = 0.03) 1998sn03 (Ctr. = 0.03) Axis 2 1971sn09 (Ctr. = 0.02) 1979–1989–1997sn09 (Ctr. = 0.32) 1995sn01 (Ctr. = 0.02) 1979–1989–1997sn08 (Ctr. = 0.15) 1979–1989–1997sn07 (Ctr. = 0.08) 1989sn08 (Ctr. = 0.04) 1979–1997sn02 (Ctr. = 0.03) aCtr. – Contribution; sn – sampling point number from 01 to 10. 2935 and 1979–1989–1997) on the negative end and sampling points of northern sites (1971 and 1995) on the positive end (Figure 5b; Table 4). In the CA, communities are not organised according to the various fire regime, i.e. age of the last fire, fire intervals and number of fires; except for short fire interval which seems to induce a change in composition and in structure of land snail malacofaunas. Mediterranean mesophilous and forest species are present in several sites, whatever the fire regime. However, communities seem to be sensitive to post-fire habitat structure and to site location since sampling points are organised in the CA according to their post-fire habitat structure (i.e. grassland, garrigue or woods composed of living or dead trees) and according to the mountainous area sampled.

Comparison of composition of land snail communities exposed to various ﬁre regimes

The dendrogram of affinities roughly splits the sampling sites into two groups according to their location in the study area, whatever the fire regime (Figure 6). First, it discriminates between northern sampling sites (i.e. 1971, 1995 and 1979–1989) and southern sampling sites. Second, it splits southern sites into two sub-groups according to the mountainous area where they are located. The sites located in ‘‘le Regagnas’’ are grouped (i.e. 1989 and 1998) and separated from the sites located in ‘‘la Chaıˆ ne de l’Etoile’’ (i.e. 1997, 1973– 1979–1997 and 1979–1997) and in ‘‘la Sainte Baume’’ (i.e. 1993). However, three sampling sites with various fire regimes (1991, 1989–1995 and 1979–1989– 1997) and located in two different areas seem to be grouped according to their pre-fire habitat, i.e. mainly composed of garrigue. Thus, no conspicuous change in composition of land snail communities is revealed by this analysis and, with the exception of some sites, malacofaunas seem to persist after fires and to be organised according to a geographical gradient.

Discussion

Malacofaunas were initially expected to be highly sensitive to wildfires and to be drastically affected by these disturbances. However, the present study revealed high resilience of land snail communities to wildfires in the short, medium and long-term. Biodiversity and species richness are high whatever the number of fires, the fire intervals and the age of the last fire, even on sites recently burned. Land snail communities are not greatly damaged by fires in the short-term. Although abundance is drastically affected, with less than 3% of land snails alive 18 months after fire, all species from various habitats (i.e. grassland, garrigue and woods) and even Mediterranean forest species are represented whatever the fire regime. Litter dwellers (i.e. micro-mammals, arthropods and 2936

Figure 6. Dendrogram of affinities between the malacofaunas at each sampling site. Stars – southern sampling sites located in ‘‘la Chaıˆ ne de l’Etoile’’; squares – southern sampling sites located in ‘‘le Regagnas’’ and ‘‘la Sainte Baume’’; triangles – northern sampling sites located in ‘‘la Chaıˆ ne des Coˆ tes’’. micro-arthropods) with limited mobility are usually the most vulnerable to fire and to the subsequent shelter loss (Athias-Binche et al. 1987; Gillon et al. 1987; Tooker and Hanks 2003) and recovery of litter cover determines their ability to re-invade burned areas (Athias-Binche et al. 1987; Whelan 1995). This result expected was not observed for malacofaunas since minute species living in litter and in topsoil are well represented in areas recently burned. However, although communities are diversified as early as the first post-fire year, few living individuals of mesophilous, forest and litter species remained alive. Habitat conditions are greatly affected one year after fire: available food and shelters (Athias-Binche 1987; Whelan 1995), and humidity greatly decrease and temperature increases by 17 C at soil surface in the Mediterranean region (Gillon et al. 1987). Hence, while some mesophilous land snails can survive fire, and can recolonise burned areas, not many individuals can be maintained throughout the first post-fire year, owing to unfavourable habitats. Recovery speeds of communities are high because land snail abundance greatly increases in only one year, between the second and the third years, after one single fire. Moreover, this increase in abundance is observed whatever the fire regime. Several hypotheses, both ecological and ethological, may explain 2937 the high recovery speeds observed from the third post-fire year. First, numerous gastropod species have biological aptitudes, i.e. quiescence or dia- pause, that allow land snails to survive when conditions of humidity and temperature become unfavourable (Bonavita 1965; Sacchi and Testard 1971; Godan 1983; Kerney et al. 1999; Cook 2001). Therefore, a few individuals may remain inactive (i.e. in rest period) within burned areas during the first post-fire months. Second, most Mediterranean species in Provence have an annual or a biennial life cycle. Egg-laying season is at the end of spring for annual species and, in autumn for biennial species (Berner 1941; Bonavita 1965). Some invasive species (e.g., Theba pisana or X. derbentina) have high phenotypic plasticity and juveniles can have interrupted growth when climatic conditions are unfavourable and little food is available (Cowie 1984; Baker and Vogelzang 1988). These species can switch from an annual life cycle to a biennial cycle, with individuals maturing by the second autumn. Hence, abundance only increases from the third year. Thirdly, although a varying number of eggs is laid per species over their life span (Berner 1941; Heller 2001), a ordinary behaviour of gastropods and of a few Mediterranean species is to mate and to lay a large number of eggs at several times and several interval days apart (Madec 1989; Labaune 2001; Kiss et al. 2005). Therefore, land snail abundance can increase rapidly. Finally, although this is rare for terrestrial land snails, even among Helicidae, some species have self-fertilisation ability (Heller 2001), which could allow perpetuation of species when populations are greatly reduced during the first post-fire years. To summarise, some species are expected to have one or more of these behaviours within burned areas, which may induce a demographic explosion from the third post-fire year, when habitat conditions become more favourable for land snails. Malacofaunas are highly resilient in the medium-term since land snail abundance steadily increases during the first post-fire years and communities seem to reach equilibrium with their habitats in 5 years, not only after one fire (Kiss and Magnin 2002, 2003) but also after successive fires. However, no patterns of post-fire succession are revealed after one single fire. Mala- cofaunas are greatly diversified and no significant difference is demonstrated in species richness and in community diversity whatever the age of the last fire, in the medium-term. They are not organised according to post-fire patterns of succession whatever the age of the last fire (CA). Unlike other fauna groups (Athias-Binche et al. 1987; Fons et al. 1993; Haim 1993), pre- fire communities are not replaced by xerophilous and open habitat communities whatever the age of the last fire. Although recovery speeds of around five post-fire years are comparable to other invertebrates (micro- arthropods and arthropods) and vertebrates (micro-mammals) (Athias- Binche et al. 1987), communities include shade-loving and shade-tolerant species from the first post-fire year. Hence, land snail communities are more resilient to fire than other fauna groups studied in the Mediterranean region. 2938

Mediterranean malacofaunas have a high resilience to fire disturbance in the long-term because they are greatly diversified whatever the fire regime, and even whatever the number of fires. However, the time lapse between successive fires seems to influence malacofauna composition (Kiss and Magnin in preparation). Indeed, communities from the sites burned with fire intervals of 10 years or less have the least species richness and the lowest diversity indexes (i.e. 1989–1995; 1979–1989 and 1979–1989–1997). In addition, closed and successive fires induce change in community composition (CA and dendrogram), which includes more species living in open, sunny and dry habitats, i.e. stony areas, grassland and garrigue. To conclude, Mediterranean land snail communities are greatly resilient to fire provided that the time elapsed between fires is over 5 years, i.e. the time needed for malacofaunas to recover equilibrium with their habitat. Moreover, communities seem to persist whatever the fire regime, according to the results of our previous study on the role of landscape history and persistent biogeographical patterns in shaping the responses of malacofaunas to recent fires (Kiss et al. 2004). Sampling sites are mainly grouped in the analyses (CA and dendrogram) according to their geographical location in the study area, i.e. according to the mountainous areas. Northern sampling sites are clearly distinguished from southern sites. The possibility of fire is the same throughout the ‘‘de´ partement des Bouches-du-Rhoˆ ne’’ (Centre Informatique de la Pre´ fecture des Bouches-du-Rhoˆ ne 2002). Thus, the persistence of malacofaunas within each mountainous area and whatever the fire regime suggests a geographical gradient, especially a biogeographical gradient, in composition of communities (Kiss et al. 2004). Composition of post-fire communities also depends on pre-fire vegetation structure and on recent vegetation cover history (Kiss et al. 2004). Although both southern sites, burned in 1998 and in 1989, and the northern site burned in 1971 are from two different geographical locations (i.e. respectively, ‘‘le Regagnas’’ and ‘‘la Chaıˆ ne des Coˆ tes’’), the composition of their communities is comparable (CA) since they have similar vegetation cover history and pre-fire vegetation composed of woods (Kiss et al. 2004). Sampling sites mainly composed of pre-fire vegetation of garrigue (i.e. 1991, 1993, 1989–1995 and all the sites with last fire in 1997) are similarly clustered in analyses (CA and dendrogram). Adaptation to wildfires could explain the high resilience of malacofaunas and their persistence observed. Indeed, since wildfires are considered a natural part of Mediterranean ecosystems (Sousa 1984; Whelan 1995; Carcaillet 1998), we could expect that they play a role in community composition perhaps by excluding species that cannot cope with arid conditions and the fire regime, or by speciation processes. However, although one case of ecological speciation in Provence due to the settlement of Mediterranean climate over the Pleistocene (Dubar and Magnin 1992) has been described for Candidula rugosiuscula (Michaud, 1831) (Pfenninger et al. 2003), which frequently occurs on burned areas, it remains difficult to estimate the role of wildfires in such remote events. Rather the malacofauna resilience observed 2939 appears due to population survival of species with various habitat requirements within burned areas than to an adaptation to wildfires. Indeed, the persistence of malacofaunas and their resilience to fire seem to be mainly explained by cryptic refuges within burned areas (Kiss and Magnin 2002, 2003). Communities are composed of large and minute land snails from forest and litter even a few months after fire. Although the immediate mortality rate was not estimated in the present study, previous experiments have revealed that some individuals are able to survive prescribed burning, i.e. fire of low intensity and of high speed, consuming only the grass layer. Survival rate reaches 20% for the species located on trunks, under rocks or within unburned litter which were relatively abundant before burning (Kiss 2002). Moreover, species living in the upper centimetres of soil are represented in areas recently burned. Sterilisation by fire affects only the first centimetres of the soil (Whelan 1995), and heating of soil varies within burned areas, depending on slope, wind, water content of humus, vegetation, thickness of litter, among others (Sousa 1984; Whelan 1995; Rigolot 1998; Tooker and Hanks 2003). Conse- quently, land snails buried to some extent in the soil can survive fire, especially as they aestivate during summer, when fires usually occur (Kiss and Magnin 2002, 2003). In conclusion, spatial variability in fire severity and land snail location at the time of fire probably induce numerous scattered cryptic refuges within burned areas (Kiss 2002, in prep; Kiss and Magnin 2003; Kiss et al. 2004). Moreover, an analysis of the patterns of post-fire recolonisation at sites burned once has shown that land snail abundance does not decrease with distance from potential sources, i.e. either burned/unburned boundaries, vegetation refuges spared by the fire and stony areas (Kiss and Magnin 2002, 2003; Kiss in preparation). In the present study, since potential sources have a low influence on recolonisation patterns, the sampling was carried out far from these sources. Indeed, the recolonisation patterns observed were mainly related to cryptic refuges, difficult to locate a priori (Kiss 2002, in preparation; Kiss and Magnin 2002, 2003). Thus, malacofaunas do not respond to fire by patterns of post-fire succession and they seem to persist after successive fires on condition that time lapse between fire is long. To summarise, these refuges allow, first, initial survival of land snails, even among minute species and Mediterranean forest species. Second, they also allow the persistence of malacofaunas not only over the first post-fire years but also after and between successive fires (Kiss et al. 2004; Kiss and Magnin in preparation).

Conclusion

Wildfires were initially expected to be a great threat to gastropods and to malacofauna biodiversity. However, this study clearly indicates a high resilience of Mediterranean land snail communities to fire disturbances. Although abundance is drastically reduced after fire, species richness and diversity of 2940 communities are preserved, whatever the fire regime, since the time lapse between two successive fires is longer than the time required for malacofauna recovery (i.e. around 5 years). Indeed, successive fires with short fire intervals tend to favour gastropod communities of garrigue and grassland (Kiss and Magnin in prep). The high resilience of land snail communities in the short-term may be partly due to ecological and ethological aptitudes of gastropods. However, this resilience observed mainly involves cryptic refuges located in burned areas that allow, first, initial land snail survival, secondly, malacofauna persistence after successive fires, and third, consistent biogeographical patterns over a long period (Kiss et al. 2004). These astonishing results, which demonstrate the limited effects of fires on land snails, may be of importance for conservation biology in the Mediterranean basin.

Acknowledgements

This study was carried out under the framework of the GIS ‘‘Impacts e´ cologique et paysager des incendies sur les garrigues et les foreˆ ts pe´ ri-marseill- aises’’ (IMEP-CNRS/CEMAGREF) and was supported by funds provided by the Conseil Ge´ ne´ ral des Bouches-du-Rhoˆ ne and by Unitas Malacologica. We wish to thank Franck Torre for his help in preparing the dendrogram of aﬃnities. We would like to thank Isabelle Girard, Cinderella Grout, Virginie Libois and Sylvie Marguerier for assistance in the ﬁeldwork. We are indebted to Marjorie Sweetko for her careful rereading and her help with English and to an anonymous referee for his judicious advice on the manuscript.

Appendix 1. Land snail species are listed, accompanied by author’s names and ﬁgure codes, at each of the 12 sampling sites.

Species Codes

Abida polyodon (Draparnaud 1801) APO Acanthinula aculeata (O.F. Mu¨ ller 1774) AAC Candidula gigaxii (L. Pfeiﬀer 1850) CGI Candidula unifasciata (Poiret 1801) CUN Cecilioides acicula (O.F. Mu¨ ller 1774) CAC Cepaea nemoralis (Linnaeus 1758) CNE Cernuella virgata (da Costa 1778) CVI Chondrina avenacea (Bruguie` re 1972) CAV Clausilia rugosa (A. Fe´ russac 1807) CRU Cochlostoma patulum (Draparnaud 1801) CPA Cryptomphalus aspersus (O.F. Mu¨ ller 1774) CAS Eobania vermiculata (O.F. Mu¨ ller 1774) EVE Euconulus fulvus (O.F. Mu¨ ller 1774) EFU Granaria variabilis (Draparnaud 1801) GVA 2941

Appendix 1. Continued.

Granopupa granum (Draparnaud 1801) GGR Helicigona lapicida (Linnaeus 1758) HLA Hypnophila boissiy (Dupuy 1850) HBO Jaminia quadridens (O.F. Mu¨ ller 1774) JQA Lauria cylindracea (da Costa 1778) LCY Merdigera obscura (O.F. Mu¨ ller 1774) MOB Microxeromagna armillata (Lowe 1852) MAR Monacha cantiana (Montagu 1803) MCA Monacha cartusiana (O.F. Mu¨ ller 1774) MCR Oxychilus alliarius (Miller 1822) OAL Oxychilus draparnaudi (Beck 1837) ODR Oxychilus hydatinus (Rossma¨ ssler 1838) OHY Papillifera solida (Draparnaud 1805) PSO Phenacolimax major (A. Fe´ russac 1807) PMA Pomatias elegans (O.F. Mu¨ ller 1774) PEL Pseudotachea splendida (Draparnaud 1801) PSP Punctum pygmaeum (Draparnaud 1801) PPY Solatopupa similis (Bruguie` re 1792) SSI Sphincterochila candidissima (Draparnaud 1801) SCA Trochoidea elegans (Gmelin 1791) TEL Trochoidea pyramidata (Draparnaud 1805) TPY Trochoidea trochoides (Poiret 1789) TTR Truncatellina callicratis (Scacchi 1833) TCA Vallonia costata (O.F. Mu¨ ller 1774) VCS Vitrea contracta (Westerlund 1871) VCO Vitrea crystallina (O.F. Mu¨ ller 1774) VCY Vitrea narbonensis (Clessin 1877) VNA Xeropicta derbentina (Krynicki 1836) XDE Xerosecta cespitum (Draparnaud 1801) XCE Xerotricha conspurcata (Draparnaud 1801) XCO Zonites algirus (Linnaeus 1758) ZAL

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