Spatial and ecological isolation in cicadas: First data from Tibicina (Hemiptera: Cicadoidea) in France

The seven taxa of the cicada genus Tibicina (T. Corsica Corsica, T. Corsica fairmairei, T. garricola, T haematodes, T. nigronervosa, T. quadrisignata, T. tomentosa) which occur in continental France and Corsica were investigated. Extrinsic factors (geographical barriers) and factors intrinsic to the ecology of species were considered in an effort to understand the biogeography of Tibicina. Three patterns related to intrinsic factors were recognised: (1) pairs of taxa with sympatric distributions but with divergent habitat preferences; (2) pairs of taxa with sympatric distributions and similar habitat but with allochronic occurrence; (3) pairs of taxa with similar ecology but with allopatric distributions. When taxa were separated by their habitat, the height of vegetation appeared to be more important than the floristic composition of the habitat. These factors lead to the partitioning of resources in time and space. All taxa occur in secondary vegetations. Human agro-pastoral activity has probably influenced the dynamics of cicada populations and the maintenance of isolation between them.

In spite of a significant recent contribution to the knowledge of French cicadas (see Boulard & Mondon, 1996), little is still known about the distribution and ecology of the Palaearctic genus Tibicina.Some data scattered in the literature are available for one species (T.haematodes) only (Vogel, 1935;Wagner, 1939;Batiashvili & Dekanoidze, 1967;Zhigaltzeva & Tereshko, 1962;Schedl, 1973Schedl, , 1986)).The genus Tibicina occurs from North Africa to Northern India (Boulard, 1976).The genus is widespread in France including the island of Corsica, with six species and one subspecies.
This paper aims to answer the question of whether the premating isolation of Tibicina species and sub-species is maintained through spatial and/or ecological processes.To document this, we gathered data on the distribution, abundance, habitat preferences and seasonality of Tibi cina sub-species and species occurring in France.The results allowed us to investigate both the environmental parameters which hamper interspecific mating pair forma tion and the importance of human activities that play a role in the maintenance of ecological isolation between species.
Specimens of the various Tibicina taxa were collected in the south of continental France (summers 1996-2001) and in Cor sica (June 2000).Identifications were made by comparison with identified specimens in the entomological collections of the Muséum national d'Histoire naturelle (MNHN).The Tibicina material of MNHN was examined via 30 specimens of T. c. cor sica, 41 of T. c. fairmairei, 68 of T. garricola, 414 of T. haema todes, 48 of T. nigronervosa, 36 of T. quadrisignata and 21 of T. tomentosa.Distributions of species were superimposed upon the vegetation map of France (Defaut, 1996(Defaut, , 2001)).The populations of T. c. corsica and T. nigronervosa have been previously  1 for the definition of the vegetation classes.mapped by Puissant & Sueur (2001).In addition, the relative frequency of each species was estimated following Voisin (1995).The ratio f = n/N was calculated, where f is the prob ability of finding at least one specimen of one species when searching at random in a limited area during its adult phase, n is the number of sites where the species has been found and N is the total number of sites investigated in the area where a Tibicina species has been found.Because more than one species can occur at any given site, the sum of the relative frequencies is not 1.

Definition of habitats
Preliminary observations, together with some already pub lished data (Wagner, 1939;Vogel, 1938;Schedl, 1986;Pillet, 1993), clearly showed that Tibicina species do not have strict preferences in the choice of their host plants.For this reason, a classification based upon the physical structure of vegetation (height of the vegetative structures and the percentage of lig neous plants) rather than upon floristic composition has been used to define the habitat of cicadas.Eight classes have been selected (Puissant & Sueur, 2001; Table 1 and Fig. 1), which correspond to the physiognomic types of Mediterranean shrub systems as defined by Tomaselli (1981).Habitat classes differ from vegetation classes in that they do not take into account either climatic features or floristical composition.
More than one habitat can occur in one site.The probability of occupancy of each habitat by a species was estimated with the ratio: r = h/H, where r is the probability of finding at least one specimen of one species in one habitat class when searching at random in a limited area, h is the number of contacts with the species in one habitat category and H is the total number of con tacts with the species in all the habitat classes.

Seasonality
The seasonal occurrence of species was determined by field observations and by gathering the dates of capture of the speci mens in the collections of the MNHN.The data for all years have been pooled together and presented with a 2-day precision.

Distribution
The geographical distributions of the species are shown in Figs 2-4, except for T. c. corsica and T. nigronervosa which were only found in Corsica and were thus sepa rated by the Mediterranean Sea from the taxa occuring on the French mainland (i.e. T. c. fairmairei, T. garricola, T. haematodes, T. quadrisignata, T. tomentosa).In conti nental France, T. haematodes and T. quadrisignata showed allopatric and interleaved distributions with respect to each other.A disjunction related to the Rhone Valley is observed in the distributions of T. garricola, T. haematodes and T. quadrisignata.One population of T. c. fairmairei and one of T. tomentosa were found to be syntopic.
Vegetation classes used by each species are summa rised in Table 2. T. garricola, T. tomentosa in continental France, and T. c. corsica and T. nigronervosa in Corsica proved to be typical Mediterranean species whose distri butions were limited to the sub-humid temperate vegeta-  tion class (SH3).In contrast, T. c. fairmairei, T. haema todes and T. quadrisignata were found in two or more vegetation classes and their distribution appeared to be extensive.
Species frequencies are presented in Table 3.In conti nental France, T. haematodes, T. garricola and T. quad risignata were the most frequent species while T. tomentosa and T. c. fairmairei were rare.In Corsica, T. c. Corsica was more abundant than T. nigronervosa.

Habitat preferences
Habitats used by each species are summarised in Fig. 5. Differences in habitat selectivity were recognised for sympatric species: (1) for T. garricola (mainly habitat 7) and T. haematodes (mainly habitat 8), (2) for T. c. fair mairei (habitats 1, 3, 5) and T. garricola (mainly habitat  as they are associated with more than two habitat catego ries.T. c. fairmairei, T. garricola and T. tomentosa were thus limited to only one or two vegetation classes but were found in more than two habitats.This is related to the fact that one vegetation class may include several habitat classes.

Seasonality
The adult seasonal pattern of species is given in Table 4. T. haematodes exhibited the longest period of adult activity while T. tomentosa and T. quadrisignata showed the shortest.Our results clearly indicate that T. c. fair mairei populations emerge later in the year than T. tomen tosa populations.This time shift in seasonality leads to an allochrony between T. c. fairmairei and T. tomentosa in the site where the two species occur together.T. c. cor sica emerged before T. c. fairmairei.Similarly, T. garri cola emerged earlier than T. quadrisignata, a time shift particularly pronounced in the Eastern Pyrenees.The sympatric but not syntopic Corsican species T. c. corsica and T. nigronervosa showed almost the same seasonal rhythm.As shown in Table 5, taxa were therefore isolated by extrinsic factors (geographical barriers) or intrinsic fac tors.Three modalities of intrinsic factors were recognised: (1) taxa with sympatric distributions but with divergences in their habitat preferences (allotopy); (2) taxa with sympatric distributions and similar habitat but with a shift in their emergence pattern (allochrony); (3) taxa ecologically similar but with non-overlapping distri butions (allopatry).

Spatial, habitat and temporal isolation
Each of the developmental stages in cicadas (eggs, larva, adults) use vascular plants as a food resource or habitat (Myers, 1929): (1) embryonic development is achieved inside the plant (endophytous phase); (2) larval development occurs underground where larvae feed on root (endogenous phase); and (3) winged adults live for approximately two or three weeks during which they feed on the sap of vascular plants (aerial phase).Surprisingly, cicadas did not develop a strong host plant specificity.Although some host preferences have been reported (Myers, 1929;Dybas & Lloyd, 1974;Lloyd & White, 1976;Moulds, 1990;Boulard & Mondon, 1996;Cook et al., 2001), strict monophagy and strong host choice by females for oviposition is not generalized in cicadas.Our observations clearly showed that the species of Tibicina use most of the available plant species for feeding, calling and ovipositing.In spite of this absence of narrow host relationships, our results show that taxa are clearly iso lated through spatial and ecological processes.First, the taxa can be isolated by geographical barriers, which are extrinsic factors.This is the case of Corsican taxa and mainland taxa.Second, species can be isolated by intrinsic factors, with three primary patterns: (1) the taxa showed sympatric distributions with divergences in their habitat preferences (e. g.T. garricola and T. haematodes or T. c. corsica and T. nigronervosa); (2) the taxa were sympatric with similar habitat selection but were allochronic (T.garricola and T. quadrisignata; T. c. fairmairei and T. tomentosa); (3) the species presented similar ecological traits but showed allopatric distribu tions (T.haematodes and T. quadrisignata).
When taxa were separated by habitat preferences, the structure of the habitats (in particular the height of vege tation) appeared to be more important than the floristic composition.Such isolation through habitat preferences has been observed in North American species (Dybas & Lloyd, 1962, 1974;Lloyd & White, 1976;Callaham et al., 2000).The calling song produced by males was sug gested as a potential mechanism acting against dispersal (Myers, 1929) which is particularly low in cicadas (Kar ban, 1981;Lloyd et al., 1982;Taylor, 1985).Furthermore, Tibicina calls clearly have a role in Table 4. Seasonality of Tibicina taxa in France (mainland and Corsica).Data from examination of MNHN collections and per sonal observations.Limits correspond to the range of dates of collection or observation of more than two males.When taxa are not isolated by their habitat characteris tics, a shift in their emergence patterns is observed (allochrony).An example is given by the syntopic popu lations of T. c. fairmairei and T. tomentosa, the former clearly emerging after the latter.Seasonal data on T. c. fairmairei and T. tomentosa allopatric populations are unfortunately missing.Nevertheless, the emergence time pattern of T. c. fairmairei appears to be delayed in com parison to that of T. c. Corsica.This might indicate that the seasonal activity of T. c. fairmairei directly depends on the presence of T. tomentosa.This suggests that in each species the time of juvenile development is firmly fixed.
Finally, T. haematodes and T. quadrisignata show non overlapping distributions.Further studies are needed to explain this allopatry between two species that occur in similar habitats, are widely distributed along several vegetation classes, and are active throughout all summer.The isolation allows species not to compete at the same time and at the same place during their peak of emergence.This leads to a partitioning of feeding, calling and ovipositing resources.In particular, it avoids poten tial acoustic interference between the calling songs pro duced by the males of different species, as their acoustic signals exhibit roughly similar time and frequency struc ture (Boulard, 1995).

Habitat isolation and human activities
In France, all Tibicina species are distributed in secon dary vegetation formations.Thus, their distributions and their relative frequencies are closely related to human pressure on landscape structure.Open and semi-open Mediterranean habitats essentially result from an eco logical succession related to fire-setting (Trabaud, 1981) or the abandonment of cultivation (Escarré et al., 1983).Shrublands occurred throughout the last two million years in the Mediterranean Basin, but human land practices have recently considerably increased (Castri, 1981).This evolution benefited T. garricola and T. nigronervosa which predominantly live in shrublands at high densities.In contrast, T. tomentosa and T. c. fairmairei showed the lowest frequencies and presently are represented only by relict and endangered populations.These species were probably previously more abundant, at the end of the 19th century (Boulard & Mondon, 1996).They are adapted to open habitats such as fallow, grazed or temporarily aban doned fields.In southern France, a decline in cultivation and an expansion of vineyards probably dramatically decreased the size of their populations.In Corsica, where browsing and grazing by herds of domestic livestock still occurs, many open fields are still available and T. c. Cor sica remains abundant.A decline of pastoral activity in Corsica would lead T. c. Corsica to decline or to invade the habitat already occupied by T. nigronervosa.Lastly, Tibicina haematodes and T. quadrisignata are mainly found in woodlands.These euryecious species are observed along several vegetation classes and are not lim ited in their geographical extension to the Mediterranean region.A similar link between forest habitat and wide distribution has been already reported for birds (Blondel &Aronson, 1999).
To conclude, and as already reported for North American species (Callaham et al., 2000), the distribution and isolation of Tibicina species are linked to a complex association between abiotic and biotic factors, including human pressures.

Fig. 1 .
Fig. 1.Schematic representation of the eight habitat classes.See Table1for the definition of the vegetation classes.

Table 1 .
Definition of the eight habitat used based upon the height of vegetation and the percentage of ligneous plants.

Fig. 5 .
Fig. 5. Habitats used by Tibicina taxa in France (mainland and Corsica).See Table 1 and Fig. 1 for the definition and representa tion of habitat classes.

Table 2 .
Vegetation classes occupied by Tibicina taxa in France (mainland and Corsica).