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FORUM is intended for new ideas or new ways of interpreting existing information. It provides a chance for suggesting hypotheses and for challenging current thinking on ecological issues. A lighter prose, designed to attract readers, will be permitted. Formal research reports, albeit short, will not be accepted, and all contributions should be concise with a relatively short list of references. A summary is not required.
When range expansion rate is faster in marginal habitats Reidar Andersen, Ivar Herfindal and Bernt-Erik Sæther, Dept. of Biology, Norwegian Univ. of Science and Technology, NO-7491 Trondheim, Norway (
[email protected]). / John D. C. Linnell and John Odden, Norwegian Institute for Nature Research, NO-7485 Trondheim, Norway. / Olof Liberg, Grimso¨ Research Station, SE-730 91 Riddarhyttan, Sweden.
Knowledge about the potential spatial dynamics of species is important. Already in 1922, the American ornithologist Joseph Grinnell (Grinnell 1922) noted that in order to understand the population consequences of dispersal, its role in the stochastic nature of rare longdistance movements and the interplay between innate and environmental factors in triggering dispersal, have to be known. Furthermore, Grinnell claimed, we need knowledge of the role of dispersal in the colonisation (or re-colonisation) of unoccupied areas of suitable habitats. Although many animals are regarded as relatively sedentary and specialised in marginal parts of their geographical distribution (Thomas et al. 2001), several species (Spivak et al. 1991, Hill et al. 1999) develop more dispersive forms at range fronts, which increases rates of range expansion. Such physiologically plastic responses to new environments are unlikely to occur in larger species (Weisser 2001). Here we report that a medium-sized cervid / the roe deer (Capreolus capreolus ) increases its expansion rate 3- to 20-fold in marginal habitats by performing a conditional dispersal strategy in accordance with the balanced-exchange dispersal model (Doncaster et al. 1997). A bi-sexual dispersal behaviour (Wahlstro¨m and Liberg 1995a, Linnell et al. 1998) and an inverse relationship between local patch quality and local dispersal probability are shown to have profound implications for expansion rates, by decreasing the rate of local extinction (i.e. the rescue effect, sensu Brown and Kodric-Brown 1977) and increasing the rate of colonisation (i.e. the establishment effect, sensu Lande et al. 1998).
The roe deer in the Scandinavian peninsula The Scandinavian peninsula includes Norway and Sweden, and ranges from about 558 10? N to 718 10? N, and 48 30? E to 308 0? E. The southern region is dominated by 210
boreal forests, agricultural areas and broad-leaf vegetation, while a fragmented forest landscape dominated by coniferous forest and birch (Betula pubescens ) prevails in the north. Roe deer have been present in the area since the late Preboreal period 9500 b.p. (Lepiskaar 1986). After periods with population fluctuations throughout the Holocene, roe deer went nearly extinct in the seventeenth century, and only less than 100 individuals survived in the southernmost part of Sweden (Ekman 1919). From this restricted area roe deer started their expansion in 1850.
Measures of expansion rate In the 19th century Sweden and Norway were divided in more than 450 municipalities in each country (at present 289 and 434 municipalities, respectively). Based on annual published records from more than 900 municipality-organised wildlife boards, on the time for establishment of a stationary roe deer population in each area, summarised by Ekman (1919) and later von Essen (1958) and Cederlund and Liberg (1995), we constructed an isocline map where each line represented the roe deer invasion front in one specific year (Fig. 1). Although we can question the accuracy of timing of the establishment of stationary populations, we expect that the occurrence of a ‘‘new species’’ in the municipality would attract attention, and be noted by the wildlife boards. Previous methods for estimating expansion rate assume a circular expansion or constant expansion rate (Hengeveld 1989). In most studies of dispersal and invasion, these assumptions are not true. In order to evaluate expansion rate for roe deer in our study, a 10 km regular point coverage was established covering all areas invaded by roe deer from 1850 to 1980. The distance from each 10 km regular point to its nearest previous invasion front was calculated. Distance of dispersal was calculated only in areas where roe deer OIKOS 107:1 (2004)
actually could move (i.e. ocean and high mountain areas were treated as barriers). In order to obtain a measure of expansion rate for each point, the distance from each point was divided with the time difference between its two neighbouring isoclines. From satellite images one can derive several measurements of vegetation, where the normalised difference vegetation index (NDVI), calculated as (near IR-band/ red band)/(near IR-band/red band), is the most used (Myneni et al. 1995). NDVI has been recognised to correlate with several important vegetation parameters, like greenness, amount of photosynthetical active radiation absorbed by the photosynthesising tissue (fPAR), leaf area index (LAI), and others (Veroustraete et al. 1996). More important, annual NDVI has a strong
correlation with net primary production (Schloss et al. 1999), which has great influence on higher trophic levels (McNaughton et al. 1989). Like most vegetation indexes, NDVI is expected to be highly correlated with latitude (Schloss et al. 1999). However, even though they well may reflect the same processes affecting roe deer habitat quality, latitude can expect to be a proxy variable for factors that are important for roe deer not represented by the NDVI indexes. Using both will give a stronger indication on the effect of habitat on expansion rate of roe deer. From south to north the length of snow cover period increases, whereas the length of plant growth season decreases (Moen 1999), clearly reflected by the annual mean NDVI values, which decrease substantially with
Fig. 1. Mean annual NDVI-values of the vegetation classes in SLCRimages. More blue is higher NDVI, more red is lower NDVI.
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latitude (Fig. 1). Due to its small size, 20 /30 kg, roe deer needs forage with high digestibility (Demment and Van Soest 1985). A short growing season, and early snow accumulation will exclude the animal from high quality ground vegetation like billberry (Vaccinium myrtillus ), and force them to utilise lower quality browsing species (Holand 1993). As roe deer both in absolute and relative terms accumulates less fat reserves than other cervids (Holand 1992), they suffer high mortality rates when facing harsh conditions during winter (Holand 1990). Thus we will argue that there is a south /north continuum of optimal to marginal habitats for roe deer on the Scandinavian peninsula. A SLCR version 2.0 satellite derived image covering the study area was downloaded from the WebPages of the EROS Data Centre, Distributed Active Archive Centre (http://edcdaac.usgs.gov/main.html). These images are 1 km resolution multi-spectral AVHRR-images reclassified into 255 global vegetation classes, of which 96 were represented in our study area. An annual mean NDVI is calculated for each class (Fig. 1). The NDVIvalues were assigned to the roe deer expansion points by interpolating values from the 4 NDVI-image pixels closest to each point. Latitude was measured as decimal degrees for each point. Since the observation unit is not given in this study, we used bootstrap resample techniques to estimate the slope and 95% confidence interval of the slope in a linear regression between expansion rate latitude, and expansion rate and NDVI-values.
Expansion rates is faster in marginal habitats After being reduced to a small population in the southernmost tip of the Scandinavian peninsula, roe deer started their expansion northward in 1850. After 75 years roe deer were established in central Norway, 880 km further north; an expansion rate of 11.7 km per year.
Heading further northwards in Norway they expanded more than 500 km in 50 years (10.4 km per year). The expansion rate in the northernmost parts of Sweden was also high. These expansion rates averaged 36 km and 31.7 km per year in areas south and north of the Arctic circle, respectively. In contrast to these high expansion rates in the marginal habitats in the north, a much lower expansion rate was found in the optimal habitats along the southern coast of the Scandinavian peninsula. From its source area in Sweden roe deer used 20 years to reach 120 km to the north-west (6 km per year), decreasing to 4 km per year andB/2 km per year in the next two decades, respectively. The expansion rates were even lower in the high quality habitats along the southern coast of Norway. In the first four decades of the 20th century, expansion rates were less than 1 km per year. The expansion rate in kilometres per year decreased with increasing NDVI-values (Beta / /0.103, 95% CI: [ /0.127; /0.080], Fig. 2) and increased with increasing latitude (Beta /0.469, 95% CI: [0.405: 0.537] Fig. 2), i.e. increased expansion rates with decreasing habitat quality. Although the expansion rates should not be interpreted as constants for roe deer in general but as approximate rates of spread over a specific period in specific areas, they should allow comparisons among species and between marginal and optimal habitats. Among the highest recorded expansion rates is an example with feral horses (Darwin 1845, Caughley 1963). After being liberated in Buenos Aires in 1537 a group of feral horses founded a population at the Straits of Magellan in 1580; an expansion rate of 48 km per year. In the northernmost areas in Scandinavia, roe deer perform expansion rates comparable with these figures. Contrasting expansion rates for roe deer with other ungulates, demonstrates that the European roe deer have some of the highest expansion rates ever recorded for cervids and bovids (Caughley 1963), that the expansion
Fig. 2. Relationship between expansion rate of roe deer, and latitude and NDVI-values. Grey lines show each bootstrap resample while black dashed line are based on mean intercept and beta from all bootstraps.
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rate is highest in marginal habitats, and that roe deer are able to establish bridgeheads far ahead of the wave front.
Example of a conditional dispersal strategy? There are at least two factors responsible for the observed expansion behaviour; a bi-sexual dispersal behaviour and a density-independent pre-saturation dispersal. First, in most cervids and bovids males are the first to colonise areas surrounding the breeding range as a consequence of searching movements (Caughley 1970, Clarke 1971). Females generally demonstrate less marked exploratory dispersal, and when they enter an area, their reproduction could be affected by the Allee effect (Veit and Lewis 1996). In contrast, both male and female roe deer perform a bi-sexual dispersal behavior (Wahlstro¨m and Liberg 1995a, Linnell et al. 1998). Thus, the occurrence of both sexes in newly colonised areas, facilitates a high potential population growth rate, and a rapid establishment of a breeding population. Secondly, there is strong evidence that roe deer demonstrate presaturation dispersal (Linnell et al. 1998), i.e. a large proportion of young animals leaving their natal areas during the increase phase of population growth. Because the individuals leave the population before it reaches its carrying capacity and before the resources are depleted, dispersers are in good condition (Wahlstro¨m and Liberg 1995a), thus increasing their chances of survival and their probability of colonising a new area (Lidicker 1975). The findings are in accordance with earlier studies in Sweden. By contrasting dispersal patterns in two Swedish roe deer populations occupying a southern optimal habitat and a northern marginal habitat, Wahlstro¨m and Liberg (1995b) showed that average dispersal distance increased from 4 km in the south to 120 km in the north. Furthermore, nearly all animals left their natal areas in the northern area, whereas less than half of the animals showed the same behaviour in the southern population. Although the underlying causes of dispersal may differ between the sexes, e.g. females optimise access to resources, whereas males optimise access to mates (Wolff 1993), they have one thing in common; they need to find an individual of the opposite sex to mate with in order to maximise fitness. This means that they have to move until they find conspecifics. In roe deer, the initial dispersal out of their natal area takes place in spring or early summer when animals approach their first birthday (both sexes) or in either of the two subsequent springs (males only; Linnell et al. 1998). This means that dispersal takes place in a period with bare ground, which makes it difficult to judge the quality of the area as winter habitat. We suggest that in order to minimise the disadvantages of moving in unfamiliar terrain (Nelson and Mech 1991), dispersing roe deer use conspecifics as OIKOS 107:1 (2004)
cues of local habitat quality. The fact that there are few, and scattered suitable habitats in the northern parts of the Scandinavian peninsula, explains why we find the highest expansion rates in these marginal areas, which leads to the establishment of bridgeheads far ahead of the wave front. Several aspects of the roe deer dispersal pattern are in accordance with the balanced exchange model by McPeek and Holt (1992); a bi-sexual dispersal behaviour (Wahlstro¨m and Liberg 1995a, Linnell et al. 1998), and an inverse relation between local population size and local dispersal probability (Wahlstro¨m and Liberg 1995b). We will argue that roe deer have a conditional dispersal strategy, i.e. conform to a highly flexible dispersal rule, which is sensitive to habitat type, local population size and other cues of local habitat quality. A highly flexible dispersal rule also explains why the findings are in accordance with outputs from an extended invasion model developed by Hengeveld and Van der Bosch (1997), were spatially heterogeneous conditions gives a non-linearity in invasion rate. Acknowledgements / We thank the thousands of local wildlife managers that every year sent their status reports to official country offices. This work was funded by the Norwegian Research Council and the Directorate for Nature Management.
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