M. MASSOT, J. CLOBERT, P. LORENZON and J.-M. ROSSI

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1 Ecology 02 71, Condition-dependent dispersal and ontogeny of the Blackwell Science Ltd dispersal behaviour: an experimental approach M. MASSOT, J. CLOBERT, P. LORENZON and J.-M. ROSSI Laboratoire d Ecologie, CNRS UMR 7625, Université de Paris VI, Case 237, 7 quai Saint Bernard, Paris, France Summary 1. Although little investigated, developmental processes that generate dispersal condition evolution of this behaviour. We have shown previously prenatal and postnatal influences on dispersal in the common lizard (Lacerta vivipara). The observation of these developmental processes was based on independent experiments; our primary goal in this paper is to test their interactions. Interactions could indeed be a source of inconsistencies in studies because they can mask, or even reverse, effects of factors treated additively. 2. We studied dispersal of juveniles released in natura from 416 pregnant females captured in the field. We used a factorial design to test interactions among the maternal habitat (dry vs. humid), prenatal conditions (temperature, humidity), and postnatal environments (dry vs. humid). 3. We found that juvenile dispersal was dependent on the humidity level at different developmental stages, but with varying and sometimes opposite effects. Dispersal was also influenced by the temperature during gestation and by populational differences not related to humidity (differences between replicated populations for the maternal and postnatal habitats). 4. These results confirm our previous findings that dispersal of the common lizard is condition-dependent and has multiple causation. In addition, most of the effects exhibited interactions, and the ontogeny of dispersal appeared as a sequential process where the maternal habitat conditioned prenatal influences, and the prenatal environment modulated postnatal influences. 5. The robustness of our results is supported by the finding of the same interactions in independent tests on both juvenile males and females. This militates in favour of future studies on the multiple causation of dispersal because the same dispersal status might originate from different causes, and different dispersal outcomes might be due to the same factor. Key-words: Lacerta vivipara, maternal effect, phenotypic plasticity, postnatal effects, prenatal effects. Ecology (02) 71, Ecological Society Introduction Multiple consequences of dispersal on individual fitness, such as effects on habitat selection, competitive interactions, mate choice, etc. (Clobert et al. 1994), should result in the evolution of dispersal behaviour that is sensitive to multiple factors (Massot & Clobert 00). Indeed, it has been demonstrated theoretically Correspondence: M. Massot, Laboratoire d Ecologie, CNRS UMR 7625, Université de Paris VI, Case 237, 7 quai Saint Bernard, Paris, France. mmassot@snv.jussieu.fr that dispersal might evolve in response to a variety of causes (Clobert et al. 01) so that many factors are likely to influence the current dispersal profile of a species. It has also been shown for some species that dispersal was affected by several different stimuli (MacKay & Wellington 1977; Massot & Clobert 00). In this context, we expect that some mechanisms have evolved to integrate multiple and sometimes conflicting information. One way to optimize a behaviour in a changing environment is to develop some sensitivity to cues that are related to key environmental factors, i.e. to have

2 254 M. Massot et al. a condition-dependent dispersal (Ims & Hjermann 01). While the current theoretical developments have started to study the evolution of dispersal under the influence of combined forces (Clobert et al. 01), very few of these models consider the dispersal behaviour as a condition-dependent trait (Travis & French 00; Ronce et al. 01). However, the few attempts that have been made recognized the superiority of condition-dependent dispersal strategies over condition-independent ones in the majority of cases (McPeek & Holt 1992; Doncaster et al. 1997; Lemel et al. 1997; Ronce, Clobert & Massot 1998; Travis, Murrel & Dytham 1999). One important reason for this is that dispersal is assumed to be costly, so that optimizing the cost and benefits of dispersal vs. philopatry at any point in time has some advantage. It is therefore probable that many organisms have developed condition-dependent dispersal strategies open to the influence of many environmental cues as, for example, in some insects (MacKay & Wellington 1977) and vertebrates (Lambin 1994; Massot & Clobert 00) (Ims & Hjermann 01 for a review). The question then becomes how are these cues integrated to determine the dispersal phenotype. If dispersal is condition-dependent, organisms should use cues that are good predictors of the quality of the environment they would experience had they stayed. This is particularly crucial in the case of natal dispersal where dispersal decisions by young can occur long before the quality of the environment influences their fitness. For example, in a species where dispersal takes place before sexual maturation, the potential for inbreeding has to be assessed well in advance of the individual actually facing this problem. Furthermore, this information should be gathered at the time when its content is the most reliable. There is accumulating evidence that dispersal is influenced by factors whose effects are felt at different developmental times: from just before departure time (Léna et al. 1998; Massot & Clobert 00) to during parental care (Ferrer 1993), during gestation (Massot & Clobert 1995, 00; de Fraipont et al. 00), or even earlier (grandmaternal environment, MacKay & Wellington 1977). Even in the same species, dispersal may be influenced by factors that act at several different moments throughout ontogeny (MacKay & Wellington 1977; Massot & Clobert 00). This result should not be surprising since, if dispersal is under the influence of several factors, it is not parsimonious to imagine that reliable information on each of these factors can be gathered at the same moment, or even that a single factor will transmit the same information at different times during the ontogeny (Ronce et al. 01). All the information collected during ontogeny will lead to a single behaviour, to disperse or not to disperse. Therefore, the information has to be integrated. Does this integration correspond to either an average effect or interactions among effects? To investigate this question, one needs to perform factorial experiments where several factors potentially acting on dispersal are manipulated at different ontogenic stages. To perform such an experiment, we chose the common lizard (Lacerta vivipara, Jacquin 1787) because several factors influence its dispersal behaviour (Clobert et al. 1994; Léna et al. 1998), and the dispersal phenotype is affected at different developmental stages (Massot & Clobert 00). We conducted a transplant experiment where postnatal conditions were manipulated independently from two prenatal effects and maternal habitat. We focused the study on humidity because this is one of the most important environmental factors as showed by its clear influences on the presence, abundance and life history traits of the species (Dauphin-Villemant & Xavier 1986; Lorenzon et al. 1999; Lorenzon, Clobert & Massot 01). We also manipulated temperature to contrast with prenatal conditions, temperature being another major constraint for the common lizard (van Damme et al. 1990a; van Damme, Bauwens & Verheyen 1990b; van Damme, Bauwens & Verheyen 1991). Humidity and temperature condition the abundance of food resources, and sites of thermoregulation are a key component of the local environment in reptiles. In addition, to be important components of the quality of the local environment, these two factors should mediate local competition because food and sites of thermoregulation are two main resources in our species. For these reasons, humidity and temperature are good candidates as environmental cues to influence dispersal, and we chose them to test the way used by the common lizard to integrate multiple influences on dispersal. However, no a priori hypotheses could be made for the influences of humidity and temperature because it has been shown that dispersal is enhanced by bad as well as good environmental conditions (Sorci, Massot & Clobert 1994; de Fraipont et al. 00; Massot & Clobert 00). Methods SPECIES AND STUDY SITES Lacerta vivipara is a small, live-bearing lacertid species (50 70 mm adult snout vent length) inhabiting peatbog and heathland. This species is distributed widely across Europe and Asia (from Spain to the Pacific coast of Russia, and from Scandinavia to southern Romania), and has to face a large variety of environmental situations as witnessed by the large variability of its life history traits (Bauwens, Heulin & Pilorge 1986; Sorci, Clobert & Bélichon 1996). In the study populations (Southern France), mating takes place in May (hibernation is from October April). After 2 months of gestation, parturition usually starts mid-july and last for 3 weeks. Five eggs, with a thin and transparent shell, are laid on average (range 1 13). Hatching usually occurs within 1 or 2 h after laying. Hatchlings are independent of their mother from birth (i.e. there is no parental care).

3 255 Ontogeny of dispersal 416 pregnant females captured in 4 study sites Maternal habitats Dry Humid x 2 sites x 2 sites For each site, 4 experimental groups Conditions of gestation Cold Dry Cold Humid Hot Dry Hot Humid For each litter, siblings released in 2 habitats Litters Release sites of juveniles Dry Humid x 2 sites x 2 sites Artificial litters Fig. 1. Protocol of the study on processes underlying offspring dispersal in the common lizard (Lacerta vivipara). The experiment was performed twice, in 1996 (1007 juveniles from 6 mothers) and 1997 (853 juveniles from 210 mothers). We selected four study sites on Mont Lozère (44 30 N, 3 45 E) which were contrasted by their humidity level. Two dry sites were moors, covered mainly by heath (Calluna vulgaris). The only source of water was rain and dew. Two humid sites were clearings containing small streams and covered by tufted grasses (Molinia cerulea, Nardus stricta). These sites were also largely flooded in springtime. We measured the relative humidity of the air in different microhabitats with an electric probe (pen-type thermohygrometer, Fisher Bioblock Scientific, Illkirch, France). We compared the relative humidity in July in the most used substrate as indicated by the number of captures. This was herbaceous layer for humid sites (92% of captures, n = 259) and heath in dry sites (74% of captures, n = 93). The relative humidity was significantly different between the two habitat types (F 1,29 = 16 7, P = ; mean ± SE: 63 6 ± 1 9% in humid habitats vs ± 2 7% in dry habitats). EXPERIMENTAL DESIGN We temporarily removed 416 pregnant females from the four study sites early in July 1996 and 1997 (Fig. 1): 107 and 99 females, respectively, for dry and humid sites in 1996, and 98 and 112 for dry and humid sites in Females were then kept in captivity (10 km from the study sites) until parturition. Females were housed individually in plastic terraria with about 1 cm of soil and a shelter. They were fed once a week with one larva of Pyralis farinalis (average live weight ± SD: ± g, n = 30; average dry weight ± SD: ± g, n = 30), according to standardized rearing conditions (Sorci et al. 1994; Massot & Clobert 00). They were exposed to natural daylight. We experimentally manipulated humidity and temperature during pregnancy using a factorial design (Fig. 1). For each study site, half of the females were kept in a high humidity environment and half in a low humidity environment. This was achieved by spraying water three times a day (at 8 h, 12 h and 18 h) with 10, five and five sprays for the humid group, and five, none and two sprays for the dry group. This resulted in a significant difference of the air relative humidity for the two groups (83 3% vs. 60 0%, F 1,33 = 49 1, P < ). Free-standing water was available for drinking (droplets on the wall of terraria) for more time in the humid than in the dry group. In addition, the soil was humid all day long for the humid group while it dried during the afternoon in the other group. For each treatment group and each study site, half the females were assigned to a low and high temperature group. Heat was provided by an incandescent electric bulb situated at one corner of the terrarium for 3 h a day in the low temperature group, and 6 h a day in the high temperature group. Females were assigned randomly to the four treatment groups, and the position of each treatment group was alternated systematically in the laboratory. Terraria were checked twice a day for parturition. Postpartum females were released in their site of origin at their last capture point. At birth, offspring were sexed by counting the number of ventral scales (Lecomte, Clobert & Massot 1992), measured (snout vent length and tail length) and weighed. They were marked individually by toe-clipping. Initial handling and toe-clipping have no influence on the probability of subsequent recapture and survival in the common lizard (Massot et al. 1992). In the same way, toe-clipping does not affect the maximal sprint speed in this species (G. Sorci, personal communication) as also demonstrated for two other species of lizard (Huey et al. 1990). The juveniles were then released on the study sites within 3 days after birth, as follows. Each family

4 256 M. Massot et al. was divided into two parts. One half was released into a humid site, the other half into a dry site (Fig. 1). In order to avoid juvenile dispersal being influenced by kin competition with the mother (Léna et al. 1998; Ronce et al. 1998), we systematically avoided releasing juveniles in their site of origin. This enables us to test strictly for a site effect. The experiment crossed three levels of potential environmental influences on the ontogeny of dispersal (Fig. 1): the type of maternal site, which might include prenatal effects as well as genetic differentiation, the type of treatment group during gestation which are short-term prenatal effects, and the type of release site which represent postnatal effects. We therefore had 16 groups of juveniles (two maternal habitats, four treatments during gestation, two release habitats) with a mean of 63 and 53 released juveniles per group, respectively, in 1996 and In total 1860 juveniles were released. DISPERSAL MEASURE Movement of juveniles was determined by hand recaptures in each study site. Two sessions of recapture were organized, one in September of the year of release and one in June of the following year. The first recapture session started at least 10 days after the last juvenile had been released in order to allow juveniles to disperse. Indeed, it has been demonstrated that juvenile dispersal takes place within the first 10 days of life (Massot 1992a, 1992b). Juvenile movements were then measured by comparing the coordinates of the release and last recapture point. A grid of markers spaced 5 m apart allowed location of recapture points with a 1 5-m precision. We defined as dispersers those juveniles that moved a distance greater than 30 m (upper 95% confidence limit of the home range diameter), and as philopatric those juveniles that moved less m (average of the home range diameter) (Clobert et al. 1994; Massot et al. 1994; Massot & Clobert 1995, 00). Juveniles classified as dispersers by this criterion never return to their release site (Massot & Clobert 1995). DATA ANALYSES Siblings could not be assumed a priori as independent statistical units (Massot et al. 1994; Massot & Clobert 00). Therefore, the first step in the analysis was to evaluate whether family membership affected dispersal behaviour. If a family effect is present, data for siblings must be nested within families. However, as in most studies on dispersal, the small number of recaptured juveniles in many families prevents us from using nested analyses. Moreover, half of the offspring of a single female were released in different study sites. Another way to conduct the analysis would have been to use one estimate of dispersal per family release site (mean dispersal rate or a single offspring as in Schroeder & Boag 1988), but this procedure would have wasted part of the information. To maintain independence and make full use of the data, we could have used a numerical resampling technique based on one randomly selected offspring per family release site (Massot et al. 1994). However, this method is time-consuming and difficult to apply. Instead, we used a new extension (DSCALE option) of the GENMOD procedure (SAS 1996) developed for the application of generalized linear models (McCullagh & Nelder 1989). The DSCALE option allows the calculation of an overdispersion factor of data, c (caused, for example, by a non-independence between individuals), and corrects the model selection by this factor (deviance of the model divided by its degree of freedom, see McCullagh & Nelder 1989 for more details). This procedure corrects efficiently for overdispersion due to non-independence between individuals (Lebreton et al. 1992; Anderson, Burnham & White 1994). Types of release site, maternal habitat types, humidity during gestation and temperature during gestation were considered as factor effects. The site effects corresponding to differences between replicates for release and maternal sites (two dry and two humid sites) were, respectively, nested within the types of release site and maternal habitat type. We started with the model with all these effects and their first-order interactions and gradually dropped the non-significant terms. The final model contained the terms which could not be dropped without causing a significant increase in deviance (backward selection procedure, McCullagh & Nelder 1989). We started first by examining the replicate effects and the interaction terms. When a significant interaction term was found, we left the main effect of the factors which were part of this interaction term in the final model (McCullagh & Nelder 1989). Results We tested first for the existence of a family effect on dispersal, using families for which we had the dispersal status of at least two juveniles (n = 90 juveniles from 39 families). We used a generalized linear model that included the type of release site (dry vs. humid habitats) and the sex of juveniles, two factors that could inflate the within-family variance. Juvenile dispersal was familydependent (χ 2 38 = 58 74, P = 0 017). The magnitude of the family effect was not different between sexes (χ 2 = 72, P = 0 414) or release sites (χ 2 25 = 10 23, P = 0 996). Juveniles from the same litter dispersed in the same way, either because they shared the same mother (prenatal effect), and/or because they had a common genetic background (same genetic propensity to disperse). However, as explained in the Methods section, it was impossible to fit a model with all the factors, plus a family effect. Therefore, we performed a model without this family effect, but with all the other factors, and evaluated the overdispersion induced by dropping the family effect. The overdispersion factor, c (the deviance to d.f. (degree of freedom) ratio is χ 2 distributed with d.f. as degree of freedom) was 0 82 and 0 98

5 257 Ontogeny of dispersal Table 1. The effects on juvenile dispersal of RS (type of release site: dry vs. humid sites), rrs (replicate of release site nested within RS), MS (type of maternal site: dry vs. humid sites), rms (replicate of maternal site nested within MS), Tg (temperature during gestation), Hg (humidity during gestation), and the first-order interactions between all effects (except replicate effects, which were nested) (*P < 0 05, **P < 0 01, ***P < 0 001) Effects Females in 1996 Females in 1997 Males in 1996 Males in 1997 rrs within RS χ 2 2 = 8 39 P = 0 015* χ 2 2 = 1 16 P = χ 2 2 = 0 96 P = χ 2 2 = 3 64 P = rms within MS χ 2 2 = 3 84 P = χ 2 2 = 4 48 P = χ 2 2 = 2 59 P = χ 2 2 = 9 36 P = 0 009** RS χ1 2 = P < 0 001*** χ1 2 = 5 18 P = 0 023* χ1 2 = P < 0 001*** χ1 2 = P < 0 001*** MS χ1 2 = 2 14 P = χ1 2 = 0 63 P = χ1 2 = 1 77 P = χ1 2 = 1 98 P = Tg χ1 2 = 2 57 P = χ1 2 = 0 03 P = χ1 2 = 0 09 P = χ1 2 = 0 P = Hg χ1 2 = 2 30 P = χ1 2 = 1 18 P = χ1 2 = 0 13 P = χ1 2 = 6 87 P = 0 009** RS Tg χ1 2 = 8 70 P = 0 003** χ1 2 = 1 48 P = χ1 2 = 1 76 P = χ1 2 = 5 P = 0 023* MS Hg χ1 2 = P < 0 001*** χ1 2 = 0 05 P = 0 8 χ1 2 = 1 44 P = χ1 2 = P = 0 001** Other first-order interactions (RS MS, RS Hg, MS Tg, Tg Hg) than the two reported in the table were non-significant. Sample sizes were 47 juveniles for females in 1996, 30 for females in 1997, 50 for males in 1996, and 54 for males in Percentage of dispersers (a) Males Cold Hot Cold Hot Dry release-habitat Humid release-habitat Temperature during gestation (b) Females Percentage of dispers Cold Hot Cold Hot Temperature during gestation Fig. 2. Interaction between the release habitat of offspring and the temperature during gestation on dispersal in male (a) and female (b) offspring in 1996 and Sample sizes are above bars. for juvenile males in 1996 and 1997, 0 53 and 1 35 for juvenile females in 1996 and 1997, respectively. Overdispersion occurs when the factor c is significantly higher than 1, but this did not occur significantly with females in 1997 (c = 25 69/19 = 1 35, χ 2 19 = 25 69, P = 0 139). It follows that part of the family effect that was significant in our first analysis is attributable to a maternal effect that was controlled in the analyses (maternal habitat, humidity and temperature during gestation). The remaining family effect, if present, does not cause a significant overdispersion, so we do not consider it in subsequent analyses. The initial model took into account the following factors: release site effect (dry vs. humid), replicate effect of release sites nested within release site effect, maternal habitat effect (dry vs. humid), replicate effect of maternal habitat nested within maternal habitat effect, humidity during gestation, temperature during gestation and all first-order interaction terms (except for the nested effects). All factors influenced juvenile dispersal, most often through interactions with one another (Table 1). The type of release site interacted with the temperature during gestation for females in 1996 (P = 0 003), and for males in 1997 (P = 0 023).

6 258 M. Massot et al. (a) Males Dry maternal-habitat Humid maternal-habitat Percentage of dispersers Dry Humid Dry Humid Humidity during gestation (b) Females Percentage of dispersers Dry Humid Dry Humid Humidity during gestation Fig. 3. Interaction between the maternal habitat and the humidity during gestation on dispersal in male (a) and female (b) offspring in 1996 and Sample sizes are above bars. The release site acted alone on males in 1996 (P < 0 001), and on females in 1997 (P = 0 023). Dispersal was, on the whole, more frequent in the dry release habitat than in the humid one (Fig. 2). This response was dependent on temperature during gestation, as indicated by significant interactions for males in 1997 and females in 1996: the release effect was stronger when juveniles were born from mothers at low temperature during gestation (Fig. 2). The type of maternal habitat was found to influence significantly juvenile dispersal in interaction with the humidity during gestation for females in 1996 (P < 0 001), and for males in 1997 (P = 0 001). When mothers originated from dry sites, juveniles dispersed more frequently when gestation was in more humid conditions (Fig. 3 for females in 1996 and males in 1997). Finally, replicates within the type of release sites significantly differed for females in 1996 (P = 0 015), and replicates within the type of maternal habitat differed for males in 1997 (P = 0 009). This means that some additional differences (not related to humidity) between study sites, not taken into account in this factorial experiment, also influenced dispersal of juveniles. Discussion In this study we contrasted one environmental factor, humidity, at different times during the phenotypic development. In addition, we manipulated another factor, temperature, at an intermediate stage in development. We found that dispersal behaviour was a function of the humidity level at different stages of ontogeny. Furthermore, different ontogenetic levels interacted to shape the dispersal response of a juvenile, and this was dependent on sex and year. The situation was even more complex, because the manipulation of another factor, temperature during gestation, was found to interact with the level of humidity in the release site, but not with the level of humidity in the maternal site or during gestation. Therefore, multiple causation of dispersal behaviour was found in this species, both through a single factor acting at different developmental stages and through the influence of different factors acting at a same developmental stage. Dispersal was clearly condition-dependent. SINGLE FACTOR: VARYING EFFECTS THROUGHOUT ONTOGENY Dry conditions encountered by juveniles in their release habitat (postnatal effect) enhanced dispersal in the common lizard. The humidity level encountered by the mother during gestation (prenatal effect) or in her habitat of origin (prenatal effect or genetic differentiation) also influenced offspring dispersal, but each in a different way from the postnatal effect. The humidity level of the maternal habitat interacted with the humidity level during gestation, and juvenile dispersal was enhanced by humid conditions of gestation in the 1996 females and the 1997 males that came from dry maternal habitats. Clearly, the humidity conditions experienced through different developmental phases did not produce

7 259 Ontogeny of dispersal additive effects (reinforcement) on juvenile dispersal, and even more, they produced opposite effects. Our finding of the same pattern both in juvenile males and females makes us confident that this complex response to a single factor was not obtained by chance (type I error). Although rarely tested, this is not the first example of a factor having different effects on individual behaviour at different developmental stages (de Fraipont 1992). There are several possible explanations for these varying effects of humidity during ontogeny. First, they could still reflect only a response to a single message related strictly to humidity at each stage. In this case, the humidity level at different time during ontogeny might not be correlated in the same way to the humidity level that juveniles will experience after birth, i.e. at the moment of the dispersal phase. However, we would expect, in this case, that either humidity level affects dispersal mainly at the postnatal stage (i.e. when the cue is the most reliable), or through interactions between postnatal and maternal effects. This is not what we observed. A second alternative is that females, in their natural habitat, might escape dry conditions during gestation by selecting appropriate microhabitats or adopting an appropriate behaviour (Lorenzon et al. 1999) which they cannot do in the laboratory. However, against this laboratory artefact, we have observed the same growth responses to humidity in the field and the laboratory (Lorenzon et al. 1999). In addition, we have obtained evidence of adaptive responses of juvenile body size at birth (Lorenzon et al. 01) with interactions between developmental stages similar to the interactions found for juvenile dispersal. A third possibility is that humidity carries different types of information at different stages of the phenotypic development. Indeed, differences between dry and humid sites could be due to humidity or other confounding factors such as life history traits of lizards, structure and composition of vegetation, etc. For example, since the density of conspecifics decreases with habitat humidity (Lorenzon et al. 01), an enhancement of dispersal rate with habitat humidity could be confounded with competition avoidance. The direct influence of humidity is ascertained only from the experimental prenatal effect. This prenatal effect could have been mediated by corticosterone because juvenile dispersal is influenced by the supplementation of this hormone during gestation (de Fraipont et al. 00), and corticosterone is involved in the regulation of body fluids during gestation in the common lizard (Dauphin-Villemant & Xavier 1986). However, the level of humidity during gestation can still convey information about another factor. For example, humidity might be a cue related to the mother s life expectancy as discussed in de Fraipont et al. (00), with dry conditions reducing the survival probability of the mother, and therefore decreasing the benefit of dispersal to avoid mother offspring competition. Thus, the varying effects of humidity throughout ontogeny could reflect the use of different types of information as proposed in Ronce et al. (01). INTERACTIONS BETWEEN FACTORS AND BETWEEN DEVELOPMENTAL STAGES In previous studies we have demonstrated that juvenile dispersal is dependent on multiple causes in the common lizard. Indeed, juvenile dispersal depends on maternal feeding during gestation (Massot & Clobert 1995; Massot & Clobert 00), maternal parasite load (Sorci et al. 1994), maternal age (Ronce et al. 1998), maternal stress (de Fraipont et al. 00) and postnatal conditions (Léna et al. 1998; Massot & Clobert 00). Although we were not able to control for all these effects in the present experiment, our data provide further evidence of this complexity by adding the effects of humidity at different developmental stages, the influence of temperature during gestation and replicate effects. Furthermore, although we found exactly the same interactions in males and females, they were observed at different years depending on sex. Sex-specific responses have frequently been shown in the common lizard. Juvenile males and females responded differently to maternal parasite load (Sorci et al. 1994), maternal age (Ronce et al. 1998), postnatal conditions (Massot & Clobert 00), offspring corpulence (Massot & Clobert 00) and litter sex-ratio (Massot & Clobert 00). Similarly, year-specific responses are also common in this species (Massot & Clobert 00). Indeed, we found year-specific responses of juvenile dispersal to offspring corpulence, litter sex-ratio and the level of food delivered to the mother during gestation (positive effect on offspring dispersal in 2 years, but negative effect in a third year). The opposite response to the level of maternal feeding was explained by an interaction with another factor or developmental stage (Massot & Clobert 00) as we found in this study. The effect of multiple cues on dispersal raises the problem of how disparate, and sometimes conflicting, information is integrated by organisms. Is only a small part of the information used? For example, perhaps only the last environmental cue encountered is taken into account or a single factor predominates (a main selective constraint on dispersal). However, although the postnatal influence explained an important part of the variation of dispersal rates, the maternal effects were not negligible: this is especially so since we excluded mother offspring competition, an important motivation to disperse in this species that acts mainly during prenatal stages (Léna et al. 1998; Ronce et al. 1998; de Fraipont et al. 00). Another alternative is that multiple information might be integrated through additive effects that use more information. Our results did not support this possibility, with interactions occurring between the maternal habitat and prenatal effect of humidity, and between the postnatal habitat

8 260 M. Massot et al. and prenatal effect of temperature. So, a key finding of the experiment is to extend our previous findings of multiple causation of dispersal to the combined action of several cues. These non-additive effects could be the most adaptive response because they enhance integration of diverse environmental factors. IMPORTANCE OF THE SEQUENCE OF ENVIRONMENTAL FLUCTUATIONS THROUGHOUT ONTOGENY We found interactions between different developmental stages: the maternal habitat influenced the prenatal response, and the prenatal environment modulated the response to postnatal conditions. Thus, the ontogeny of dispersal behaviour appears to be a sequential process, where earlier effects influence subsequent effects. In other words, contrasting early conditions produce distinct developmental trajectories, as suggested recently by Ronce et al. (01). Such a sequential ontogeny could be beneficial for at least three reasons. First, the redundancy of information over time could ensure information quality by reducing noise due to temporary events. Secondly, use of environmental cues at different times might provide information on temporal variability of environmental factors (i.e. dispersal behaviour could respond differently to stable and unstable conditions). Thirdly, the different stages of development could give different types of information. Indeed, the local environment at the natal site can be assessed at all stages of development, the quality of the mother can be assessed prenatally (there is no parental care in our species), and the quality of siblings can be assessed at the last developmental stages. Thus, a sequential influence of environmental cues throughout ontogeny could improve the quality, quantity and nature of available information. These potential benefits should depend on the characteristics of the organisms and the environment. With regard to the biology of species, viviparity increases the possibility of early cues being used (Massot & Clobert 00) and parental care should increase the use of late cues. To be adaptive, responses to environmental cues must have a genetic basis (to be under selection). Predictability of environmental factors must also be considered. Indeed, for the responses to be adaptive, it is also required that cues used during development provide information on conditions that offspring will face at their natal site (Bernado 1991; Massot & Clobert 00; Ronce et al. 01). It is then expected that in less predictable environments, only late cues will be used (Massot & Clobert 00; Ims & Hjermann 01). Conclusion Dispersal in the common lizard is condition-dependent and has multiple causation. Dispersal is influenced by variables that act at different stages of phenotype development, and sometimes in different ways. This suggests that the same dispersal behaviour might develop from different causes, and that different dispersal behaviours might develop from the same cause. Philopatric or dispersing individuals are therefore likely to be a mixture of individuals that have adopted the same strategy for different reasons. Searching for similarities among dispersers (or philopatric individuals) can therefore be meaningless unless the causes and mechanisms that underlie this behaviour are understood. If this is a common occurrence, then assessing proximate and ultimate causes of dispersal will be ascertained confidently only by using multifactorial approaches (Ims & Hjermann 01), by having longterm data on several populations with contrasting situations, or by manipulating individuals with known history. Acknowledgements We are grateful to A. Dufty and two reviewers who provided valuable comments on the manuscript. 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