POPULATION DYNAMICS OF THE BUTTERFLY AND THE PARASITOID c. melitaearum
The spatial population dynamics of a parasitoid are constrained by the wasps’ own dispersal capacity and behaviour and by the spatial dynamics of the host. Cotesia melitaearum is a very efficient parasitoid at the local scale. The wasp has up to three generations per host generation, and it is gregarious, laying 1–30 eggs per host larva depending on their size (Lei et al. 1997; Lei & Camara 1999). The wasp thus has a very high intrinsic rate of population increase, potentially large local population size in comparison with the host population size (Table 3), and the wasp is efficient in finding the host larval groups (Stamp 1982; Lei & Hanski 1998; Lei & Camara 1999). It is therefore not surprising that the wasp may even cause the extinction of local butterfly populations (Lei & Hanski 1997; van Nouhuys & Hanski 1999). Nonetheless, at the regional scale C. melitaearum persists only at a low level within the host metapopulation in the Åland islands. This is both because it experiences an even more fragmented landscape than is experienced by the host, and because of its limited dispersal range.
Table 3. Approximate local population sizes of the host butterfly and the parasitoids and the maximum colonization distances
|M. cinxia||150 eggs/batch||100||5 km|
|H. horticola||1 egg/host|| 30||Several km (but < 8 km)|
|C. melitaearum|| || ||1·5 km|
| 1st generation (summer)||1·2 eggs/host|| 3|| |
| 2nd generation (autumn)||2·5 eggs/host||10–25|| |
| 3rd generation (spring)||18 eggs/host||20–1500|| |
In fragmented landscapes, both the host and the parasitoid are expected to be absent from those parts of the landscape in which the availability of suitable habitat patches is below a species-specific extinction threshold. In the context of classic metapopulation theory, the concept of metapopulation capacity (Hanski & Ovaskainen 2000; Ovaskainen & Hanski 2001) is helpful in allowing a quantitative assessment of the extinction threshold. Unfortunately, the quality of the data for Cotesia melitaearum does not allow us to fit the metapopulation model to the data in the manner that Hanski & Ovaskainen (2000) did for the Glanville fritillary. Here we did a more approximate analysis by comparing the metapopulation capacities of wasp-occupied and butterfly-occupied networks. The results (Fig. 3) illustrate that the metapopulation capacity of habitat patch networks that are able to support a wasp metapopulation is higher than the capacity of networks in which the butterfly may occur. In other words, the wasp is restricted to the parts of the landscape that are most favourable for occupancy by the host butterfly. Even if the parasitoid would have an equal colonization capacity to that of the host, it would nonetheless be unable to persist in a very fragmented landscape in which its host has a low incidence of patch occupancy.
In reality, the dispersal range of C. melitaearum is less than that of its host. There are very few studies of dispersal distances by free-living parasitoids (Antolin & Strong 1987; Onillon 1990; reviewed by Godfray 1994; Brodman et al. 1997), and especially few studies in which population sizes are known or have been estimated. We found that in one season and during two parasitoid generations, C. melitaearum colonized experimentally placed host populations up to 0·5 and 0·8 km from the nearest possible source population, while in a third experiment there was no colonization beyond the source population itself (Table 2). Amongst the 64 natural colonizations in our 8-year data set, the mean colonization distance from the nearest source population was 0·46 km and the most distant colonization occurred at 1·57 km from the nearest source.
More is known about dispersal of butterflies in general and the movements of the Glanville fritillary in particular (Hanski et al. 1994; Kuussaari et al. 1996; Hanski 1999). In a study of 1737 marked Glanville fritillaries (Hanski et al. 1994), most transfers took place among habitat patches located less than 0·5 km apart, but the longest observed movement distance was 3·1 km. The results of two other mark–recapture experiments produced similar results (Kuussaari et al. 1996; I. Hanski unpublished). Among the 906 colonizations observed between 1994 and 2000 in the present study, the mean distance from the nearest population was 0·6 km and the longest recorded colonization distance was 6·8 km. These results are similar to those reported for another morphologically similar butterfly species, Proclossiana eunomia, while it was spreading into a previously unoccupied fragmented landscape in Morvan, central France (Nève et al. 1996).
Based on previous mark–recapture data for the Glanville fritillary (Hanski et al. 1994, 2000; Kuussaari et al. 1996), our experimental results on the colonization of host populations by the parasitoid, and natural colonizations over 8 years, we conclude that C. melitaearum has a higher yearly colonization rate than the host in well-connected habitat patches. However, the host is able to colonize unoccupied patches over longer distances than the parasitoid (though this difference between the species may be overestimated because of a difference in sample sizes). The higher colonization rate of well-connected patches by the parasitoid (0·2–0·4 per year) than by the host (0·1–0·2 per year) is probably to a large extent because C. melitaearum has two or three generations per year while the butterfly has just one, and because many C. melitaearum can develop in each parasitized late instar host individual (Table 3).
Examining colonizations in the networks that were occupied both by the butterfly and the parasitoid produced the seemingly unexpected result that the parasitoid colonizations occurred at more isolated sites on average than the host colonizations. The explanation of this result is that sites available for colonization were more isolated for the wasp than for the host butterfly (Figs 1a and 2a), to some extent because of the higher colonization rate of the parasitoid in well-connected habitat patches. The average connectivity of empty habitat available for colonization by the butterfly in the networks occupied by the wasp was ln S= 0·39, which is only slightly smaller than the mean connectivity of colonized patches (0·52; Fig. 2a). In contrast, the mean connectivity of butterfly populations available for colonization by the wasp was ln S= −5·42, which corresponds to habitat patches much more isolated than sites ever colonized by the wasp (mean ln S of colonized patches was 0·19).
The generally small population sizes, high rate of local population extinction, and short colonization distances of C. melitaearum imply relatively high extinction risk from entire patch networks and low rate of colonization of empty networks afterwards. A case in point is the network studied by Lei & Hanski (1997, 1998). This network is made up of 45 habitat patches that were occupied by 28 well-connected host populations in 1993, some of which were very large. In this network, C. melitaearum had large populations and high colonization rate in 1993–95. Subsequently, and in part as a result of high rate of parasitism, the butterfly populations declined and many went locally extinct (Lei & Hanski 1997), causing the connectivity for the wasp to decrease. By 1997 there were 15 relatively small butterfly populations and no wasps. Since then the number of butterfly populations has increased and some of them are large, and hence the network could again support the parasitoid. However, recolonization of the network has not happened so far, and is unlikely to happen in the short term, because the nearest C. melitaearum population is 3 km away.
The interaction between the host butterfly and Cotesia melitaearum thus shows great spatial and temporal variation. If the parasitoid is present in a large butterfly metapopulation in a well-connected network, the interaction can be strong and may lead to elevated extinction rate of host populations due to parasitism (as demonstrated by Lei & Hanski 1997; see also Hanski 1999). On the other hand, a more typical situation in the Åland Islands is that C. melitaearum is completely absent from the host metapopulation, either because the regional patch network is too sparse to support a sufficiently large host metapopulation or because the host metapopulation has gone through a bottleneck in size causing a network-wide extinction of the parasitoid. The isolated C. melitaearum populations in Fig. 2 are mostly remnants of population clusters in declining host metapopulations. Additionally, factors other than host spatial dynamics and parasitoid dispersal rate and range influence the spatial population dynamics of the parasitoid. For example, the rate of colonization of host populations by C. melitaearum and their subsequent persistence depends also on the food plant species used by the host butterfly (van Nouhuys & Hanski 1999).
POPULATION DYNAMICS OF THE BUTTERFLY AND THE PARASITOID h. horticola
The presence of Hyposoter horticola in most host populations, including those that are newly established and quite isolated, suggests that it disperses at least as well as the butterfly and probably even better. Note that the parasitoid achieves the high colonization rate and long colonization distances in spite of having a smaller overall population size than the host (Table 3). It is clear that the Glanville fritillary cannot escape parasitism by dispersal, and hence H. horticola population size is regulated by local mechanisms rather than by limited access to spatially isolated local host populations. What limits H. horticola is the extremely short window of opportunity available for parasitism (S. van Nouhuys, unpublished). While H. horticola moves freely among host populations and finds most egg clusters, it is only able to parasitize a fraction of the eggs in each cluster. This is because H. horticola parasitizes fully developed larvae that are still in the eggshell. The eggs in a cluster do not mature simultaneously, and the time interval during which they are vulnerable to parasitism is extremely short (a few hours). Additionally, eggs located in the centre of the egg cluster may be physically inaccessible to the ovipositing wasp. Finally, H. horticola females appear unwilling to visit eggs in previously parasitized clusters (S. van Nouhuys, pers. obs.). The population dynamic impact of H. horticola is to make host populations uniformly smaller, which may indirectly increase the probability of their extinction.
The presence of H. horticola in both newly colonized and in relatively isolated host populations might suggest that it has alternative hosts in our study area. However, in 6 years of study we have found no evidence for H. horticola using hosts other than the Glanville fritillary in Åland. The sentinel host larval groups placed in habitat patches in Föglö and Simskäla, two large islands isolated by 8·5–11·3 km from the nearest populations of the Glanville fritillary, were not parasitized even thought the habitat patches were large, of high quality and located near to other suitable meadows with insects that typically occur with the Glanville fritillary. Hyposoter horticola has also failed to colonize very isolated Glanville fritillary populations established for other experiments (Nieminen et al. 2001), indicating that the parasitoid is not present where the butterfly is absent. Additionally, the foraging behaviour of adult H. horticola seems to be extremely specialized to gregarious hosts on specific host plants, and the wasps do not parasitize the most likely alternative host in the Åland Islands, Mellicta athalia (S. van Nouhuys, pers. obs.).
COMPETITION AMONG THE PARASITOIDS
Coexistence of competing parasitoids in a fragmented landscape does not have to be facilitated by dispersal. For example, Amarasekare (2000) describes an interaction between competing parasitoids that disperse equally well but the inferior larval competitor uses lower quality host patches. In another study, Hopper (1984) argues that colonization ability of five parasitoids is not a function of their relative dispersal capacity but of their host-finding ability once they are in a host population.
Nonetheless, if dissimilar dispersal rates were to be important for coexistence of competing parasitoids, it would seem likely to happen in a system such as the one described here. Hyposoter horticola is so well dispersed in the host metapopulations that most individuals do not occur together with C. melitaearum, whereas C. melitaearum cannot avoid direct interspecific competition with H. horticola. Hyposoter horticola has a much larger and more stable regional population size than C. melitaearum, because it is able to use virtually all host populations, and its dynamics at a large spatial scale would probably change little if C. melitaearum were absent. However, at the local scale things may be different. Lei & Hanski (1998) found that the rate of parasitism of host larval groups by H. horticola was higher in the absence of C. melitaearum, apparently because of direct competition between immature parasitoids developing in the host larvae (van Nouhuys & Tay 2001; E. Punju & S. van Nouhuys, unpublished). These results suggest that while H. horticola is the superior disperser it may be the inferior competitor at the local scale.
Our results demonstrate a striking difference in the spatial population structures and dynamics of two specialist parasitoids using the same host population in a highly fragmented landscape. The host butterfly (Melitaea cinxia) lives in networks of habitat patches as a classic metapopulation. One parasitoid (Hyposoter horticola) has such a high rate of dispersal and long colonization distances that it effectively experiences the host as a single patchily distributed population. The other parasitoid species (Cotesia melitaearum) has a high dispersal rate but such limited colonization distances that most (> 80%) local host populations are out of reach of this parasitoid at any one time. Consequently, C. melitaearum only persists in those parts of the landscape in which host populations are largest and best connected. In spite of the striking difference in their spatial population structures, the two parasitoids have a strong impact on the host metapopulation. In the case of C. melitaearum, whose density varies greatly in space and time, the parasitoid may increase the extinction rate of the host in those populations where it is present. In the case of H. horticola, whose density varies little in time or in space, the impact on host populations is more indirect, due to reduction of host population sizes by roughly 30%, which leaves the host vulnerable to other mechanisms of local extinction (Hanski 1998, 1999).
The two parasitoids interact with each other. The majority of H. horticola individuals escape direct interspecific competition because most host populations are, at any one time, too isolated to be reached by C. melitaearum. On the other hand, C. melitaearum cannot avoid competition with H. horticola. The direct interaction between the wasps in shared host populations is complex, and more research is needed to understand the actual mechanisms of their within-host competition. Nonetheless, regional coexistence of the two parasitoids may be facilitated by a trade-off between their colonization and competitive abilities.