The effect of habitat corridors on rates of transfer and interbreeding between vole demes.
Habitat fragmentation has been recognized as the main threat to many wildlife populations (Soule 1986, Lande 1988, Robinson et al. 1995, Leach and Givnish 1996). Among several fragmentation-induced phenomena contributing to reduced population viability, low genetic variation at the level of individual organisms (i.e., decreased heterozygosity) has been of considerable concern (Soule and Simberloff 1986, Boyce 1992, Caughley 1994, Frankham 1995, Young et al. 1996). A critical determinant of heterozygosity is the amount of gene flow between spatially segregated demes (Hansson et al. 1995). Gene flow in fragmented animal populations results from two processes. Transfer denotes the process by which an individual emigrates from its natal patch or deme, disperses through uninhabitable areas, and finally settles permanently in another patch or deme (Ims and Yoccoz 1997). Gamete dispersal results from short-term mating excursions by which the individual returns to the home patch or deme (Waser and Elliot 1991, Koenig et al. 1996). As restricted mobility of the individuals is often the most immediate consequence of habitat fragmentation (Ims 1995), both modes of gene flow may be affected enough to cause isolation, and therefore cause decreased levels of heterozygosity.
For more than two decades, ecologists have argued that habitat corridors (i.e., narrow strips of habitat connecting otherwise isolated habitat fragments) may enhance the transfer of individuals and genes in fragmented landscapes (Fahrig and Merriam 1985, Forman and Godron 1986, Saunders and Hobbs 1991, Hobbs 1992, Dawson 1994, Forman 1995). Habitat corridors are currently implemented as an expensive conservation strategy world wide (Mann and Plummer 1993). However, empirical evidence for the assumed enhancement of successful transfer is scant (Noss 1987, Simberloff and Cox 1987, Simberloff et al. 1992, Mann and Plummer 1993). In particular, no studies have tested experimentally whether corridors enhance interbreeding between demes so as to maintain high levels of heterozygosity in fragmented populations. The paucity of empirical studies has sparked controversies among ecologists (Hobbs 1992), and the urgent need for experimental studies has been generally recognized (Dawson 1994, Mann and Plummer 1995).
Employing experimental designs to untangle the effects of habitat corridors on natural populations has proved to be particularly difficult (Inglis and Underwood 1992, Andreassen et al. 1996a). In ecology, experimental model systems may aid in uncovering presumed mechanisms that have proved difficult to explore in unreplicated, nonmanipulative studies of natural populations (Ires and Stenseth 1989, Kareiva 1989, Robinson et al. 1992, Wiens et al. 1993, Lawton 1995). We have adopted this approach to test the effect of habitat corridors on rates of transfer and interbreeding between spatially segregated demes in experimentally fragmented populations of the root vole Microtus oeconomus. Specifically, we employed a combination of demographic and genetic techniques to disentangle the relative importance of transfer and gamete dispersal in replicate populations with and without a corridor connecting two spatially segregated demes.
The root vole is a small (40-80 g), herbivorous rodent threatened by habitat fragmentation some places in Europe (Bergers et al. 1994). Boreal and subarctic root vole populations are typically restricted to small meadows and sedge bogs that are very patchily distributed in the landscape (Lambin et al. 1992, Viitala 1994, Tast 1966). Reproductive females colonize habitat patches at the onset of the breeding season in the early summer (Tast 1966), and local demes typically consist of matrilineally related individuals (Lambin et al. 1992). The root vole has proved to be especially amenable for small-scale model experiments of individual and population-level effects of habitat fragmentation due to its short generation time and small space requirements (Ims et al. 1993, Wiens et al. 1993, Johannesen and Ims 1996).
We caught root voles in Valdres, in southeast Norway (60 [degrees] 45[minutes] N, 9 [degrees] 25[minutes] E), in the fall of 1993 and 1994. Here root voles inhabit highly patchy habitats (small sedge bogs and creek banks) and deme sizes may vary from [less than] 10 to [greater than] 100 individuals. The wild-caught individuals were brought to the laboratory and bred for one to three generations to give rise to two genetic strains homozygous with respect to alleles (a and b) of the locus coding for the enzyme Mannose 6-phospho-Isomerase (MPI). Allozymic forms were assumed to be selectively neutral, and thereby to function only as genetic markers in this study. This assumption was supported by the Hardy-Weinberg proportions of the three allelic combinations in the sample of 107 wild-caught animals (aa: bb:ab = 45:16:46, [X.sup.2] = 0.56, df = 1, P = 0.454). To reduce probability of breeding between kin in the laboratory, animals from the field were never allowed to breed with animals trapped at the same locality. In subsequent generations, new pairs were never formed from lines known to be genetically related.
Within each of the two homozygous strains (aa or bb) obtained in the laboratory, six experimental founder demes to be used in the field experiment the following spring (1994 or 1995) were established. Each founder deme consisted of three mothers and their unweaned litters. The litters were synchronously born around 14 June ([+ or -] 1.8 d [SD]). To induce sociality within demes, which depends on familiarity in Microtus (Ferkin et al. 1992, Lambin and Mathers 1997), the three families forming a founder deme were kept close together (visual and olfactory contact, but in separate wire-mesh cages) in the laboratory [approximately] 10 d after parturition and until weaning, when we initiated the field part of the experiment. On average, the demes consisted of 7.8 [+ or -] 1.3 males (mean [+ or -] 1 SD) and 11.6 [+ or -] 1.8 females at the onset of the field experiment.
The field part of the experiment was conducted during two summer seasons (1994 and 1995) at Evenstad Research Station, in southeast Norway (61 [degrees] 12[minutes] N, 11 [degrees] 06[minutes] E). At the onset of each season (2 July in both years), six experimental populations, each consisting of two laboratory-raised founder demes, were established in six 50 x 100 m enclosed meadow patch systems. Each of the two founder demes, being homozygous for different alleles (aa or bb), colonized one of the two 750-[m.sup.2] habitat patches per system [ILLUSTRATION FOR FIGURE 1 OMITTED]. The patch size is similar to those that can be found in natural populations (Viitala 1994, Tast 1966). The habitat patches consisted of dense grass and herb vegetation of a type inhabited by native root voles in the surroundings of the experimental plots at Evenstad. The patches were imbedded in a matrix area devegetated by herbicides and generally avoided by voles (Ims et al. 1993). The interpatch distance was 50 m. This distance is approximately twice the length of male and female root vole home range diameters (Fauske et al. 1997, Gliwicz 1997). According to the classification scheme by Noss (1991), the systems should be at the landscape mosaic scale. Distances equivalent to the interpatch distances employed in our experiment have proved to be sufficient to cause substantial genetic differentiation among conspecific Microtus demes even in continuous habitats (Bowen 1982, Lidicker and Patton 1987).
The experimental factor, presence or absence of a 0.5-m wide habitat corridor between habitat patches, was applied in a balanced and spatially interspersed design over two seasons, yielding six population and 12 deme replicates per treatment [ILLUSTRATION FOR FIGURE 1 OMITTED]. The width of the corridors (0.5 m) has previously been shown to induce exploratory movements in root voles, but without allowing for permanent settlement of breeding individuals (Andreassen et al. 1996a, b). The two study seasons were terminated due to snowfall at the onset of the winter and encompassed 16 wk (1994: termination 20 October) and 21 wk (1995: termination 25 November), with up to three vole generations. These periods are equivalent to the length of the breeding season in natural arctic and subarctic populations (Tast 1966, Lambin et al. 1992, Krebs et al. 1995).
The study populations were monitored by capture-recapture trapping. Trapping grids consisted of three trapping lines 10 m apart in the habitat patches. These lines had one Ugglan multiple live trap every 5 m and one pitfall trap every 10 m, giving a total of 24 Ugglan traps and 12 pitfall traps in each patch. The combination of pitfalls and ordinary live traps ensured a high trappability of individuals in all age classes (Boonstra and Krebs 1978). Trapping was conducted at 15-d intervals (six periods in 1994 and eight periods in 1995). Each trapping period lasted for 3 d and included six checks. Each day the traps were set at 2400 and checked at 0600 and 1300. Thereafter they were set open. This trapping protocol ensured a very high trappability. Minimum trappability estimates (Krebs and Boonstra 1984) averaged 99.5% (range: 96.9-100%) over trapping periods for the founder generation and 97.2% (range: 93.9-100%) for the subsequent generations combined.
In addition to this period trapping schedule, six "fence traps" per plot were activated each night throughout the study seasons. These traps were placed in the barren nonhabitat beside the fences and captured animals that presumably were prone to emigrate from the plots. Animals were removed from the plots if caught at least five times during a period of 8 d or less and when these captures involved two different traps separated by more than 50 m (Aars et al. 1995). We regarded this rule to be a reasonable compromise between the errors of removing animals making occasional excursions to the fences and retaining animals attempting to emigrate. These animals were removed to prevent "fence effect" and abnormal densities (Ostfeld 1994). The individuals removed, of the total number marked per population, averaged 10.4% (range: 5.7-18.8%).
New recruits were marked individually and genotyped upon first capture. Toe clippings were used for individual marking and genotyping. Location of capture, individual identity, mass, and reproductive status were recorded at each capture. Males were deemed reproductive when scrotal, and females when pregnant (indicated by abdominal swelling) or lactating.
Capture/recapture-based population sizes were very similar for populations with and without habitat corridors [ILLUSTRATION FOR FIGURE 2 OMITTED]. However, the populations generally grew to much larger sizes in 1994 than in 1995. For both years combined there were 22 912 captures among 2540 individuals. Among these were 2076 field-born recruits.
Transfer occurred predominantly among founder generation animals early in the season [ILLUSTRATION FOR FIGURE 3 OMITTED]. Transfer in the subsequent (field-born) generations was much lower (0.5% in males and 1.0% in females). The transfer rate was strikingly sex biased: generally 77% of the founder generation males changed fragment or deme, compared to [less than] 12% for females [ILLUSTRATION FOR FIGURE 3 OMITTED]. We tested for effects of habitat corridors on transfer rates by applying sex-specific logistic-binomial models. The dependent variable was the patch-specific proportion of animals that emigrated from their patch or deme of origin to the opposite patch or deme in the period between two trapping periods. The binomial denominator was the number of individuals of each sex still present in their origin patch of the preceding trapping period (i.e., animals at "risk" in a given period; Hosmer and Lemeshow 1989). The proportions were not correlated among patches within the plots (logistic regressions; all P [greater than] 0.10), justifying analysis at the deme level, which assumes that demes were statistically independent. In addition to the treatment factor (presence or absence of corridors), period and year were included in the model.
Although the transfer rate was generally low in females, corridors nevertheless enhanced it ([X.sup.2] = 6.02, df = 1, P = 0.014). On the contrary, male transfer appeared to be equally high in populations with and without corridors ([X.sup.2] = 0.11, df = 1, P = 0.750). Although period was significant for both females ([X.sup.2] = 44.18, df = 5, P = 0.000) and males ([X.sup.2] = 18.83, df = 5, P = 0.002), neither year nor any of the interaction terms had effects on the sex-specific transfer rates (all P [greater than] 0.10). The time period in which transfer occurred appeared to be terminated earlier among females than among males [ILLUSTRATION FOR FIGURE 3 OMITTED]. While female transfer took place before 22 July, male transfer was not completed before one month later [ILLUSTRATION FOR FIGURE 3 OMITTED].
Although some of the initially transferred animals returned to their patch of origin later in the season, most of the recorded movements between demes led to permanent settlements in the foreign deme. Of the total number of males (N = 57) and females (N = 18) ever trapped in a foreign deme during a trapping period, 10.0% of the males and 22.2% of the females later returned to their deme of origin. These return rates were significantly enhanced by the presence of corridors ([X.sup.2] = 7.47, df = 1, P = 0.006), as six of 30 males and four of 12 females returned in the corridor populations, compared to zero of 27 males and one of six females in populations without corridors. These proportions include only animals that were alive at least one trapping period after the dispersal event.
The expected frequency of heterozygosity among offspring recruited in a habitat patch during a trapping period was compared with the observed frequency. The expected frequencies were calculated based on actual composition of breeding animals resulting from the transfer of individuals between the habitat patches. The calculations were done assuming random mating and equal contributions to the gene pool by reproductive animals residing in a given patch two trapping periods before. Two trapping periods ([approximately]35 d) correspond to the time span between conception and weaning in root voles (Ims 1997). Under these assumptions, the expected deme-specific proportion of recruits becoming heterozygous ([p.sub.ab]) is given by
[Mathematical Expression Omitted]
where f and m denote female and male proportions of the different genotypes present two trapping periods before.
The highly sex-biased transfer of founder genotypes gave rise to very high levels of expected offspring heterozygosity [ILLUSTRATION FOR FIGURE 4A OMITTED]. The expected values increased in parallel to the transfer trajectories [ILLUSTRATION FOR FIGURE 3 OMITTED] and exceeded the expectation from population-level random mating (i.e., 50% heterozygosity, assuming equal success of the two founder demes). The expected heterozygosity did not differ between demes that were connected by corridors and those that were not [ILLUSTRATION FOR FIGURE 4A OMITTED].
Empirical estimates based on the observed proportions of heterozygosity were obtained from a logistic-binomial model with habitat patch and period specific proportion of heterozygous offspring recruited as the response variable. Treatment (presence or absence of corridor), year, period, and the expected frequency of heterozygous offspring were included as predictor variables. Of the total number of recruits, the observed proportions of heterozygous recruits were not correlated among patches within the plots ([X.sup.3] = 0.07, df = 1, P = 0.789), justifying patch-specific proportions as units in the analysis. Only the predictor variables, treatment, and expected frequency of heterozygosity accounted for a significant portions of the total variability in the data (Model [X.sup.2] = 322.3, df = 2, P = 0.000). However, the residual error in this model was overdispersed (Residual [X.sup.2]/df = 3.57). A model taking into account this overdispersion by the use of quasi-likelihood techniques (Collett 1991) gave significant partial effects of treatment ([X.sup.2] = 6.32, df = 1, P = 0.012) and expected heterozygosity ([X.sup.2] = 61.5, df = 1, P = 0.000). Estimates obtained from the quasi-likelihood model showed that the observed frequency of heterozygous offspring became significantly higher in corridor-connected demes than in isolated demes [ILLUSTRATION FOR FIGURE 4B OMITTED]. In particular, the observed heterozygosity in corridor-connected demes significantly exceeded the expected heterozygosity derived from the transfer pattern.
Our assumption that the two alleles were selectively neutral could not be rejected by our experimental data. The estimated allelic frequencies at the termination of the experimental periods were approximately even (weighted mean frequency of the a allele based on population specific estimates: 0.540, 95% confidence interval: 0.444-0.637).
When evaluating results from experimental model systems like ours, one has to be aware that artifacts may intrude on the results. However, considering the focal response in our study, the rate of transfer (dispersal), it appeared to posses all the main characteristics of other microtine populations (Boonstra et al. 1987, Cockburn 1988, Ims 1989, Johnson and Gaines 1990, Stenseth and Lidicker 1992, Bollinger et al. 1993, Lambin 1994): it occurred predominantly in the spring-born cohort, females dispersed somewhat earlier than males, and it was male biased. Once transferred, most breeding individuals appeared to have settled, as few individuals returned to their patch of origin. Breeding dispersal appears to be an uncommon phenomenon in Microtus populations (Lambin 1997)
The male-biased transfer and its effect on the degree of interbreeding between the demes was extreme in our experiment, albeit not unique. Male-biased dispersal predominates in mammals and is most often thought to stem from inbreeding avoidance (Pusey 1987, Cockburn 1988, Pusey and Wolf 1996). This interpretation seems also to be adequate for our study, as inbreeding depression is prevalent in this particular geographic race of the root vole (Santos et al. 1995).
The predominance of male natal dispersal or transfer in microtines seems to be a rigid phenomenon that is little affected by the prevailing circumstances, whereas the less frequent transfer of females may be more determined by the prevailing conditions (Ims 1989). This finding is corroborated by theoretical studies (Chesser and Ryman 1986). The fact that only females responded to the presence of corridors in this experiment demonstrates another, but previously not demonstrated, ecological condition toward which the sexes responded differently.
The most intriguing result of the present experiment was that the observed frequency of heterozygosity in corridor-connected demes exceeded the expected frequency based on the transfer pattern. Earlier, excess heterozygosity within breeding groups (Chesser 1991) has also been observed in natural, spatially subdivided populations of small mammals (Schwartz and Armitage 1980, Foltz and Hoogland 1983). It has been proposed that this sort of mismatch (the so-called Wahlund effect; Wahlund 1928) between demography and genetics of local demes may be due to gamete dispersal (Waser and Elliot 1991, Koenig et al. 1996). Circumstantial evidence suggests that the subtle process of gamete dispersal, which is hardly detectable by standard demographic methods, was operating among the corridor-connected demes in our experiment: in reproductive animals 14% of the females and 32% of the males were observed to make excursions to traps in the corridors within trapping periods. Corridors may have facilitated short-term excursions and thereby functioned as a contiguous contact zone between the demes. In other words, corridors apparently increased the outbreeding potential for post-transfer animals by extending their "social neighborhood" into the corridors. Gliwicz (1997), in a recent radiotelemetric study on a natural root vole population, has suggested that females may seek mating beyond their normal home range. It is noteworthy that both the transfer pattern and the genetic development of the populations were consistent among the two years with very different population densities, which suggests that these phenomena are not very density dependent.
Our experiment provided two novel results, contributing to the knowledge about habitat corridors at a spatial scale where transfer and, most likely, gamete dispersal was operating.
First, the conduit function of corridors with respect to transfer of root vole individuals was sex specific, as only transfer of females was enhanced. Thus, habitat corridors may allow reproductive females to become transferred and thereby rescue (sensu Brown and Kodric-Brown 1977) small extinction-prone demes in fragmented populations (Fahrig and Merriam 1985, Saunders and Hobbs 1991, Forman 1995).
Second, it was not possible based on the transfer pattern and the actual composition of breeding animals at the deme level, to predict the genetic structuring of new generations in the population with corridors, probably because the subtle process of gamete dispersal was involved. The functioning of habitat corridors, and the relative importance of transfer and gamete dispersal for the genetic structuring of fragmented populations (e.g., the degree of heterozygosity) will be dependent on spatial scale (Merriam 1991, Noss 1991, Soule and Gilpin 1991, Tischendorf and Vissel 1997). Specifically, short-term mating excursions leading to gamete dispersal must be expected to be a more small-scale phenomenon than permanent transfer of individuals (Ims and Yoccoz 1997). Apparently, at the spatial scale of our experiment both these modes of gene flow were operating, but gamete dispersal only when corridors were present. Future studies of the ecology and genetics of fragmented populations need to consider that, depending on the degree of habitat connectivity, spatial scale, and sex-specific behavior, different processes may come into play determining the future of the population.
This work was supported by the Research Council of Norway. The following people provided indispensable help in the laboratory and the field: Harry Andreassen, Rine Carlsen, Gry Gundersen, Hege Gundersen, Eva Irgens, Edda Johannesen, Jannecke Moe, and Anders Nielsen. We thank Ottar Bjornstad, Per Erik Jorde, Edda Johannesen, Xavier Lambin, and Nigel G. Yoccoz for comments on the manuscript.
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|Author:||Aars, Jon; Ims, Rolf A.|
|Date:||Jul 1, 1999|
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