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- Materials and methods
Dispersal, that is the movements of organisms between suitable habitat patches, is a key process in population biology, shaping the characteristic texture of populations, communities and ecosystems in space and time (Wiens 2001). Two complementary, but still rarely overlapping approaches consider dispersal as a major explanatory factor of population persistence within landscapes. In landscape ecology, ‘the degree to which the landscape facilitates or impedes movement among resource patches’ (i.e. landscape connectivity: Taylor et al. 1993) depends on how organisms perceive and move through the different portions of their habitat; this determines how individuals distribute in the landscape (e.g. Wiens, Stenseth & Ims 1993; Wiens 1997, 2001), which in turn influences population dynamics and generates distribution patterns. In metapopulation biology, the intensity of dispersal affects the relative importance of local processes (birth and death rates) vs. regional processes (immigration and emigration rates) to metapopulation dynamics (Hanski 1991, 1999; Thomas & Kunin 1999). Although with both the landscape ecology and the metapopulation approaches the starting point of dispersal through the matrix is individual behaviour at habitat patch boundaries (Haddad 1999; Jonsen & Taylor 2000; Matthysen 2002), this particular point has rarely been studied directly. The effect of landscape structure on behaviour at habitat patch boundaries is even more poorly known.
Butterflies are excellent model organisms for the study of dispersal, and a great deal of information has been gathered on dispersal patterns (i.e. between–patch exchanges) in butterfly metapopulations (e.g. Harrison, Murphy & Ehrlich 1988; Hanski & Kuussaari 1995; Petit et al. 2001; Wahlberg et al. 2002). Moreover, several empirical studies document how dispersing individuals behave in the matrix and locate suitable habitat patches (Conradt et al. 2000; Conradt, Roper & Thomas 2001). Theoretical models of metapopulation dynamics generally assume that the emigration rate is higher out of smaller habitat patches, because encounters with patch boundaries are more frequent, and indeed some empirical butterfly studies support this hypothesis (Hill, Thomas & Lewis 1996; Kuussaari, Nieminen & Hanski 1996; Thomas & Hanski 1997; Baguette, Petit & Queva 2000; Petit et al. 2001; Wahlberg et al. 2002). However, we have shown previously that the emigration rate was dependent on the fragmentation level of the landscape (Baguette et al. in press; Mennechez, Schtickzelle & Baguette in press). Indeed, in the bog fritillary butterfly Proclossiana eunomia Esper, the comparison of dispersal patterns between a highly fragmented and a more continuous landscape using capture–mark–recapture revealed a significant drop of dispersal in relation to fragmentation. Moreover, dispersal in both landscapes was affected by patch area effects on emigration rates in the highly fragmented landscape only. In light of previous observations of butterflies performing exploratory movements out of the departure patch, followed by returns at irregular intervals after a flight over unsuitable habitats (Baguette et al. 1998), we suggested that in fragmented landscapes butterflies are more reluctant to leave a patch − where they may find mates, oviposition sites and food supply − to fly through the ‘hostile’ matrix (Mennechez et al. in press). Habitat fragmentation is therefore associated with a cost of dispersal through the matrix, due to predation risk and the uncertainty of reaching another suitable habitat patch (e.g. Olivieri & Gouyon 1997; Andreassen & Ims 1998; Heino & Hanski 2001). Therefore, in opposition to a simple diffusion process, we hypothesize that dispersal out of a suitable habitat patch is an individual decision dependent on the perception of boundaries and resulting in habitat patch boundary crossings. Our decision hypothesis is supported by recent experimental evidence indicating that butterflies use visual cues to locate landscape elements (Dover & Fry 2001). Compared to fragmented landscapes, the cost of dispersal should be much lower in more continuous landscapes due to the very close proximity of suitable habitat patches. Therefore, we hypothesize that in more continuous landscapes, where butterflies cross patch boundaries more freely, dispersal will correspond much more to a diffusion process. The effect of patch area on emigration rates in the highly fragmented landscape was interpreted in the light of the cost of dispersal hypothesis (Mennechez et al. in press). In large patches, individuals will be reluctant to leave because of resource abundance, while in smaller patches resources may be limited, triggering dispersal of butterflies in spite of its cost. Consequently, the number of resident butterflies will be very low in such small patches.
In this paper, we investigate whether or not behavioural processes determine emigration out of a suitable habitat patch (the starting point of dispersal within the matrix). To do this we (i) tracked individuals and investigated whether movement paths differed between two isolated patch networks of contrasting fragmentation levels, and (ii) investigated differences in dispersal rates between the two networks using capture–mark–recapture methods. In the highly fragmented network, we expect that (i) spatial patterns of movement paths, reflecting behavioural decisions, differ at patch boundaries, and (ii) emigration rates should be lower. In the more continuous network we expect that (i) no differences exist between the spatial patterns of paths close or far from the patch boundary, and (ii) emigration rates should be higher. It is worth noting that the habitat fragmentation process is associated with extensive modifications in the matrix quality: in the highly fragmented network, both suitable habitat and the original, natural matrix are destroyed and replaced by large tracts of forests or intensively managed agricultural fields or pastures; on the contrary, habitat patches and the matrix are nearly undisturbed in the continuous network.
Then we turn to the cost of dispersal hypothesis: applying the Virtual Migration (VM) model (Hanski et al. 2000) to capture–mark–recapture data, we search for differences in mortality during dispersal between the two networks. Under this hypothesis we expect significantly higher dispersal mortality in the highly fragmented network. Finally, we develop a simulation model to explore how behaviour at habitat patch boundary affects emigration rates and their relationship with patch area. By modifying boundary permeability, i.e. the probability that a potential emigrant crosses the patch boundary (e.g. Stamps, Buechner & Krishnan 1987), we investigate how contrasting relationships between emigration rate and patch area may occur.
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- Materials and methods
We compared here two networks of habitat patches differing in fragmentation level and matrix quality, but situated within the same landscape. This location was chosen to guarantee that environmental and historical factors affecting both P. eunomia metapopulations are comparable. Genetic tests using RAPDs indicate that the metapopulations are isolated from each other (Vandewoestijne & Baguette, unpublished data).
Although the paths were recorded during different years in the two networks, the observed differences can really be attributed to the effect of landscape structure and not to a temporal effect. Indeed, (i) all the paths were recorded under similar, favourable climatic conditions as it is well known that sunny and warm weather increases butterfly activity (e.g. Shreeve 1992); (ii) no behavioural differences were observed during the 11 years of capture–mark–recapture data collection in FRAG; and (ii) some paths were also recorded in the AGGREG network in the same year as in the FRAG network (1994) and they show the same characteristics as the AGGREG 2002 data set and the same differences from the FRAG 1994 data set. However these were not numerous enough to allow proper statistical comparison with the FRAG data set, which is the reason for the recording of new paths in AGGREG in 2002.
Our results clearly show that butterfly behaviour at patch boundaries was modified by habitat fragmentation. Analyses of track recordings using various complementary tests unanimously indicated that in the highly fragmented network (FRAG) butterflies approaching patch boundaries engaged in U-turns significantly more often than in the more aggregated one (AGGREG). Therefore, boundary perception by flying butterflies is evident here, as already reported by Schultz & Crone (2001) for another butterfly species. Additionally, we show here that boundary perception has different consequences depending on the fragmentation of the networks: while boundary crossing avoidance was the rule in the highly fragmented network, boundary crossings occurred quite frequently in the more aggregated network. This difference in behaviour corresponds to the biological process determining contrasting levels of boundary permeability (e.g. Stamps et al. 1987), because these behavioural differences directly affect the number of patch-boundary crossings leading to emigration. Except for the behaviour at patch boundaries, no difference between networks is seen in movement patterns (move length and turning angle distributions) – even when separately estimated, values are very similar, thus allowing us to exclude the possibility of too small sample sizes preventing us from detecting significant differences. All subsequent analyses of dispersal using capture–mark–recapture data at the network level revealed emigration rates lower in the highly fragmented network, which is in agreement with a limitation of dispersal with habitat fragmentation.
This general pattern of decreasing dispersal with increasing fragmentation level corresponds to the general predictions of theoretical models of the evolution of dispersal (Olivieri & Gouyon 1997; Heino & Hanski 2001). We go further here, by testing for the cost of dispersal hypothesis, which is the key parameter of such models (e.g. Wahlberg et al. 2002). Using the Virtual Migration model, we detected a significantly higher mortality during dispersal in the highly fragmented network than in the more aggregated one. This result is not surprising as it corresponds to selection pressures that shape the evolution of behavioural responses to habitat patch boundaries, which are themselves the processes leading to the decrease in dispersal rates within fragmented landscapes. To our knowledge, this is the first time that such a cost of dispersal associated with fragmentation has been empirically demonstrated.
This difference in dispersal mortality has to be related to the fact that, for dispersing butterflies, the matrix matters (Ricketts 2001). As we pointed out earlier, there was a striking difference in the quality of the matrix between the two networks, in term of naturalness: the matrix of the more aggregated AGGREG network (peat bog) was much more natural than in the other network (areas of afforestation or artificial pastures). The landing of dispersing butterflies in the more natural matrix of the AGGREG network was recorded several times during individual tracks, while this was never the case in the matrix of the highly fragmented FRAG network. Therefore, we propose that, besides the classical risks associated with dispersal in the matrix (predation or uncertainty of reaching suitable habitats), whether or not the matrix offers the possibility for interruption of interpatch travel may be an important factor for dispersal survival.
The relationship between emigration rate and patch area was found to be different according to the fragmentation level of the landscape: the widely accepted pattern of decreasing emigration with increasing patch area, generally observed in fragmented landscapes (e.g. Hill et al. 1996; Kuussaari et al. 1996; Thomas & Hanski 1997; Kindvall 1999; Baguette et al. 2000; Petit et al. 2001; Wahlberg et al. 2002) with consequences for metapopulation persistence (Kindvall & Petersson 2000), was challenged by the comparison of bog fritillary butterfly dispersal between a continuous and a highly fragmented landscape (Mennechez et al. in press). In this latter study, no relationship was detected between patch area and emigration rate in the continuous landscape, while emigration rate out of small patches was significantly higher than out of larger patches in the highly fragmented landscape. Our simulation model of butterfly movements in patches with different permeability provides predictions in good qualitative agreement with these empirical results. The decreasing effect of patch area on emigration rate when the habitat patch boundary permeability increases can be explained as follows. When the permeability is low, potential emigrants have to reach the patch boundary several times before crossing over it, because they return frequently into the patch. The number of boundary hits rapidly decreases as the patch becomes larger, leading to a lower emigration rate. However when the permeability is high, only a few hits are needed to trigger boundary crossing and so lead to emigration. Thus, with high permeability, even in a large patch potential emigrants encounter the boundary at a high enough frequency to allow emigration, leading to a reduced effect of patch area. These predictions correspond to empirical data obtained in the present study: we showed that boundary permeability in the FRAG network can be considered as low (butterflies engaged in U-turns when they reached a patch boundary), and indeed we report a high effect of patch area on emigration rate. On the other hand, in the AGGREG network patch permeability may be considered higher (butterflies cross over patch boundaries in more than 40% of patch boundary encounters), and the effect of patch area on emigration rate is limited.
Our results indicate that a metapopulation model assuming that emigration rate decreases with increasing patch area is not always realistic, and is justified only when boundary permeability is low. Specifically, the use of such a function parameterized with data from one landscape to predict emigration rate in another landscape is not appropriate, unless the boundary permeability can be assumed to be roughly the same, that is if the quality of the matrices is similar. Our results offer a clear warning against using unconsidered generalizations in population viability analysis and conservation biology.
In conclusion, our study provides a coherent picture of the effect of fragmentation on dispersal. We suggest that the lower survival of dispersing individuals in the fragmented habitat patch network that we document here is the key biological process at the basis of the evolution of behavioural avoidance of patch boundaries. According to this hypothesis, this behaviour will in turn induce the difference in dispersal rate patterns observed in the comparison between fragmented and continuous patch networks. It is worth noting that habitat fragmentation occurred over a maximum of 30 butterfly generations in the FRAG network (Baguette et al., in press). An example of such an evolution of dispersal ability related to habitat fragmentation has been shown to occur in Plebejus argus L. (Thomas, Hill & Lewis 1998). An alternative hypothesis is that butterflies respond to subtle differences in the properties of habitat patch boundaries between the two networks, because matrix quality was very different in the two environments. According to this hypothesis, Kuussaari et al. (1996) showed that the quality of patch boundary influences movement rates in the butterfly Melitaea cinxia L. Experimental releases in the same patches of butterflies collected from the two networks, and subsequent comparative analyses of their movement paths, will help to rigorously solve this critical issue.