The influence of social behaviour, dispersal and landscape fragmentation on population structure in a sedentary bird

Biological Conservation 109 (2003) 237–248 www.elsevier.com/locate/biocon

The influence of social behaviour, dispersal and landscape fragmentation on population structure in a sedentary bird Peter G. Cale* Zoology Department, University of New England, Armidale, NSW 2351, Australia Received 7 February 2002; received in revised form 8 March 2002; accepted 10 March 2002 This paper is dedicated to the late Dr. James F. Lynch whose work and encouragement led me to study the White-browed Babbler

Abstract White-browed Babblers Pomatostomus superciliosus lived in groups of up to 13 birds in the highly fragmented landscape of the WA wheatbelt. Contacts between these groups and sexual differences in dispersal behaviour interacted with the landscape mosaic at a number of spatial scales to produce a hierarchically structured population with four levels of organization: (1) groups, which were the basic breeding unit; (2) social neighbourhoods, where group interactions were frequent, and male dispersal and female postnatal and breeding dispersal occurred; (3) local population neighbourhoods, which contained social neighbourhoods between which female natal dispersal was frequent; and (4) metapopulations, which contained local population neighbourhoods between which dispersal was infrequent. The boundaries of these structural units, with the exception of the group, were not discrete and were influenced by the structure of the landscape they occupied. Interactions between groups occupying different patches were rare, and the frequency of group interactions was lower in small patches. Male dispersal was restricted to groups within the same patch or in patches less than 1 km apart. Therefore, decreasing patch size and increasing patch isolation resulted in smaller social neighbourhoods. Males generally dispersed to smaller groups and these dispersals may have enhanced the productivity of these groups by increasing their size. Therefore, habitat loss and fragmentation are likely to disrupt social neighbourhoods resulting in lower levels of social interaction and reduced productivity. The size and configuration of local populations were dependent on female natal dispersal, which in turn depended on landscape connectivity. White-browed Babblers used remnant vegetation in preference to other landscape elements when dispersing, but were not dependent solely on corridors. The permeability to dispersal of the boundaries between remnants and agricultural vegetation was dependent on patch configuration. Changes in boundary permeability were found to alter connectivity between habitat patches in a complex and asymmetric manner. Therefore, it is essential to consider landscape connectivity in a spatially explicit context for species that use some elements of the landscape mosaic in preference to others when dispersing. Habitat loss and fragmentation impose a complex set of changes, at a number of different scales, to processes that affect aspects of a species’ life history. In order to manage species in fragmented agricultural landscapes it is necessary to understand the hierarchical structure of their populations, and how processes affect the different organizational levels within this structure. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Metapopulation; Fragmentation; Dispersal; Scale; Connectivity

1. Introduction In landscapes modified by humans for extensive agriculture, native species often face habitat loss and fragmentation. These changes include a decline in the size of habitat patches and an increase in their spatial isolation * Present address: Rivercare Ecologist, Dept. Primary Industries, Water & Environment, GPO Box 44, Hobart Tasmania 7001, Australia. E-mail address: [email protected] (P.G. Cale).

(Saunders et al., 1991). It has generally been assumed that these changes lead to a reduction in the exchange of individuals between patches (Simberloff, 1988; Opdam, 1990; Saunders et al., 1991); although some have stressed that the response will be species specific (Saunders et al. 1991). This view of the effect of habitat loss and fragmentation on population dynamics developed from the Theory of Island Biogeography, but has been criticized as being too simplistic (Wiens, 1994). A new view of landscapes is developing that acknowledges their complexity; and argues that population processes are

0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(02)00152-0

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affected not only by the shape and spatial distribution of a species’ habitat, but also by the structure of the landscape mosaic in which these patches occur (Dunning et al., 1992; Taylor et al., 1993; Wiens, 1997). Dispersal patterns are pivotal to the population structure of a species. Ims et al. (1993) suggested that a species’ dispersal pattern might have one of two responses to fragmentation; a fusion response where increased fragmentation results in reduced dispersal, or a fission response where the frequency and/or the distance of inter-patch dispersals increases with increasing fragmentation. Empirical studies have shown that this is a valuable model, but that species’ responses are sometimes more complex (Wiggett and Boag 1989; Matthysen et al., 1995; Bjornstad et al., 1998). Using a spatially explicit dispersal model, Brooker et al. (1999) showed that dispersal by two bird species in the wheatbelt of Western Australia was probably dependent on the distribution of remnant vegetation. Although dispersals were likely to be made through remnant vegetation, both species were capable of crossing gaps in this vegetation (Brooker et al., 1999). Therefore, the connectivity of the landscape for these species was not dependent solely on corridors of remnant vegetation, but also on the spatial pattern of the landscape mosaic. The interaction between the dispersal capabilities of a species and the landscape mosaic is only one factor determining population structure. Behavioural ecologists have long acknowledged the existence of social structure within populations (Alexander, 1974; Brown, 1978). More recently, geneticists have shown that social structure has important implications for population genetics (Chesser, 1991; Cabarrero and Hill, 1992). This has led to some arguing strongly for the inclusion of social structure into models of population dynamics (Sugg et al., 1996; Vucetich et al., 1997). This paper uses data collected on the White-browed Babbler Pomatostomus superciliosus to investigate the effects of three factors; social structure, dispersal capabilities, and the landscape mosaic on population structure in fragmented landscapes. Specifically, it seeks to determine if interactions between these factors produce structure within populations, and if the concept of a metapopulation is an appropriate model for such populations. It then investigates the effects of landscape modification on these processes.

2. Methods 2.1. Study area This study was carried out within a 1680 km2 area just north of Kellerberrin, which is approximately 200 km east of Perth, Western Australia. This area is part of the Western Australian wheatbelt, which has undergone

extensive clearing for the purposes of agriculture. The Kellerberrin area was settled by Europeans in the early 1860s and most clearing occurred before 1960 (Arnold and Weeldenburg, 1991). By 1984, when clearing had virtually ceased, 93% of the area had been cleared for agriculture. Of the remaining 7% of the original vegetation, 77% occurs in remnants that are less than 20 ha, and only 4% occurs in remnants larger than 100 ha (Arnold and Weeldenburg, 1991). Road verges now represent an important source of original vegetation in the district. There are approximately 600 km of road verges, varying in width from 20 to 100 m, many of which still contain the area’s original vegetation. The vegetation is typical of the district, but generally suffers a greater degree of disturbance compared to other remnant vegetation (Cale and Hobbs, 1991). Two sites, each approximately 3750 ha, were used in this study. Both sites were dominated by agricultural land use, but Site A had slightly more remnant vegetation than Site B (17 and 12%, respectively). Approximately the same proportion of remnant vegetation in these two sites was considered suitable habitat for White-browed Babblers (27 and 31%, respectively). This vegetation was contained in a total of 24 patches (11 patches in Site A, 13 in Site B). White-browed Babblers occupying 20 of these patches, varying in size from 2 to 70 ha, were monitored. The number of groups occupying the monitored patches varied from 34 to 39 during the study period 1994–1996. 2.2. The White-browed Babbler White-browed Babblers are medium-sized (37–50 g), predominantly insectivorous birds. The adults forage on the ground or under the bark of shrubs (Cale, 1994, 1999). They feed their young a wide range of invertebrates and occasionally small skinks (Cale, 1999). There are no discernible differences in the plumage of male and female White-browed Babblers. However, the sexes do differ in size and can be reliably distinguished using the head-bill measurement (Rogers et al., 1986; Cale, 1999). The native vegetation within the Kellerberrin area is a diverse mosaic of communities including, heaths, shrublands, mallee and woodlands (McArthur, 1993). White-browed Babblers occupy the tall shrubland communities in this mosaic and are dependent on remnant vegetation for both foraging and breeding (Cale, 1994, 1999). However, unlike many remnant-dependent bird species, they used remnant patches and remnant vegetation along road verges with equal frequency (Lynch and Saunders, 1991). White-browed Babblers rarely use agricultural land (i.e. pasture and crops), except within 20 m of remnant edges where they sometimes foraged (Cale, 1994; Lynch et al., 1995). White-browed Babblers are cooperative breeders (Chandler, 1920; Cale, 1999). In the Kellerberrin area

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they generally lived in groups consisting of a single breeding pair and from one to 11 helpers (Cale, 1999). These groups held breeding territories, but had overlapping home ranges during the non-breeding season (Cale, in press). During the latter period there was a high level of social interaction between nearby groups and individual birds visited nearby groups throughout the year (Cale, 1999). The dispersal and social behaviour of White-browed Babblers is consistent with the Queuing model for cooperative breeders (Wiley and Rabenold, 1984). Male babblers generally become helpers and wait to inherit their natal territory (Cale, 1999). However, males also interact with nearby groups and assess them for enhanced opportunities to gain a breeding position (assessment sphere sensu Zack and Stutchbury, 1992). These dispersing males generally join groups which contain fewer males, because in these smaller groups they are likely to gain a breeding position sooner than in their natal group (Cale, 1999). Females generally disperse from their natal territory (Cale, 1999). There are three types of dispersal found in Whitebrowed Babblers. Birds dispersed from their natal territories to breed elsewhere (natal dispersal sensu Greenwood and Harvey, 1982). This was found in both male and female White-browed Babblers (Cale, 1999). Female babblers were also found to disperse from groups in which they had previously nested (breeding dispersal sensu Greenwood and Harvey, 1982). It was not known if breeding dispersal occurred in males, because the breeding male in a group could not be determined with certainty. The third type of dispersal was found in both sexes and involved dispersal between groups by birds that had already dispersed from their natal territory, but had not yet bred. These dispersals are called post-natal dispersal in the current paper. Such dispersals would generally be considered part of natal dispersal (Greenwood and Harvey, 1982). However, they have been distinguished from natal dispersal, because for females the spatial scale of post-natal and breeding dispersal was smaller than for natal dispersal (Cale, 1999). It was not always possible to determine if a dispersal event was natal or post-natal dispersal, because the origin of some individuals was not known. Therefore, only known post-natal dispersals were distinguished when considering issues of spatial scale. All others were considered natal dispersal. 2.3. Group composition I caught and colour-banded 357 White-browed Babblers in the two study sites. Most were caught using mist nets, but I also banded nestlings before they fledged and occasionally caught newly fledged young by hand. I visited most habitat patches in the two sites regularly (1–4 times per month) throughout the breeding

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seasons (July–October) of 1994–1996. Visits during the non-breeding season were less frequent, but most habitat patches were visited at least four times during this period of each year. In addition to the regular searches of the study sites, I searched (at least once each year) remnant vegetation around the edges of these sites in an attempt to find dispersing birds. During each visit to a habitat patch I attempted to locate all groups of babblers occupying that patch. I considered a group to be present in a patch for a given year if it occupied that patch throughout the breeding season. Group members for a given year were those individuals that remained in the group throughout the breeding season. 2.4. Habitat patch scale For all babbler groups found in the study sites I defined a habitat patch based on the distribution of vegetation considered suitable for the permanent occupation of a group. The boundaries of these habitat patches were determined from a 1994 Landsat image that was enhanced to maximize the differences between major vegetation types. Boundaries were then verified on the ground. Areas of suitable vegetation were considered to be discrete habitat patches if separated by more than 100 m of unsuitable vegetation. Different types of interactions occurred between babbler groups, resulting in social contact between members of these groups (Cale, in press). An index was calculated to describe differences in the frequency of interactions in habitat patches that contained different numbers of groups. Habitat patches were visited at different frequencies, so this index standardised the observed frequency of interaction for differences in the frequency of visits. The Interaction Rate (IR) was calculated using the formula: X  IR ¼ Ia =ðN  V10  TÞ where Ia is the sum of the interactions for each group within a habitat patch, N is the number of groups within the habitat patch, V10 is the number of visits I made to the habitat patch to monitor groups (V was measured in groups of 10 visits to prevent very small values of IR), and T is the number of years over which these interactions occurred. The inclusion of N and V10 in the index standardised the number of interactions in patches for differences in the number of groups present and the frequency with which these groups were monitored. Each habitat patch was placed into one of four group size classes: those containing only one group, 2–3 groups, 4–5 groups, and those containing 6–7 groups. The number of dispersals originating from a habitat patch of a certain size class was averaged for the number

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of years that habitat patch was monitored. In some cases the number of groups within a habitat patch varied from one year to the next. If these changes shifted a habitat patch from one size class to another it was treated as a different patch for each year. 2.5. Local population neighbourhoods White-browed Babblers were not evenly distributed across the survey area (Cale, 1999). Groups aggregated within habitat patches and at larger scales these habitat patches were spatially aggregated across the landscape (i.e. patch clusters). This patchy distribution suggests that the population structure of this species might fit the concept of a Metapopulation (Hanski and Simberloff, 1997). The local populations within a Metapopulation can occur in a range of configurations (Harrison and Taylor, 1997). For example, local populations can be contained within habitat patches (Moilanen et al., 1998), or closely associated habitat patches may represent patchy local populations (Hill et al., 1996). The appropriate spatial structure depends on the relative rates of dispersal between landscape elements. This is the concept of an Ecological Neighbourhood (Addicott et al., 1987). I defined a Local Population Neighbourhood (LPN) as that region of the landscape in which dispersal between elements within the neighbourhood was equally likely, but dispersal between neighbourhoods was less frequent. Given the distribution of White-browed Babbler groups in the study area, I proposed a simple conceptual model of the possible scales at which interactions between these groups might occur (Fig. 1). The purpose of this model was to provide a framework for determining local population neighbourhoods. Dispersals can occur between groups occupying the same habitat patch (Dw), between groups occupying different habitat patches in the same patch cluster (Db), or between groups occupying habitat patches in different patch clusters (DPC). If a change in the rate of dispersal occurred at one of these scales this would define the local population neighbourhood. For example, if Dw > DbDPC then habitat patches would represent local population neighbourhoods, while, if DwDb > DPC then patch clusters would represent local population neighbourhoods. The spatial scale associated with Dw is determined by the distribution of the vegetation in the landscape, but patch clusters, which define Db and DPC, can be defined at any spatial scale. Therefore, some means of determining a biologically meaningful scale is required. This was done using a spatially explicit dispersal simulation model (Brooker et al., 1999). 2.6. Simulation model The dispersal simulation model was run separately for all White-browed Babbler groups in the two study sites.

Fig.1. A conceptual model of the scales which might be important in determining the population structure of White-browed Babblers in the Kellerberrin landscape. There are three scales at which interactions (dispersals) might change: Dw between groups (solid circles) within habitat patches (fine ellipses), Db between habitat patches within patch clusters defined at some spatial scale (thick ellipses), and DPC between patch clusters.

Previous modelling and the observed dispersals had shown that the two sites were not connected to each other by dispersing individuals (Cale, 1999). In the dispersal simulation the animal moved randomly through remnant vegetation from a designated origin group until it reached the designated target group, or the time limit of 10 000 steps (one step equals 30 m) had expired. This model has one user-defined parameter, gap tolerance, which sets the rules for the movement of the simulated animals across agricultural landscape elements. This parameter was set at the values determined for the White-browed Babbler in the Kellerberrin landscape by Brooker et al. (1999). Each run of the simulation model consisted of 100 iterations of the dispersal of a simulated animal. One of the outputs from this model was the number of times the simulated animal found the designated target group (e.g. 50 hits from 100 iterations). This value was used as a measure of the relative association between pairs of babbler groups. Local population neighbourhoods were then defined as those groups that were associated at a pre-defined level (e.g. 550 hits from 100 iterations or 50%). Neighbourhood models were the local population neighbourhoods generated at one of three pre-defined levels of association, 25, 50, or 75%. The level of association between pairs of groups was not symmetrical. Unidirectional associations between local population neighbourhoods occurred when the association between

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groups in one direction met the criterion for inclusion in the same local population neighbourhood, but did not meet this criterion in the opposite direction.

3. Results 3.1. Habitat patches There was a significant positive relationship between the area of a habitat patch and the average number of groups that occupied that habitat patch (Adj. R2=0.74, F(1, 10)=32.40, P=0.0002; Fig. 2). One patch, in site B, was excluded as an outlier from this model as it was burnt in 1991, and therefore, it was likely that some of its habitat was not suitable for babbler groups at the time of the study. This patch supported fewer groups than would be expected given its area. The regression model was Number of Groups=0.005+0.16 (Habitat Patch Area). This model predicts that the number of groups in a habitat patch will increase by one with an increase of 6.2 ha in the area of the habitat patch. There was a significant positive relationship between the Interaction Rate and the number of groups within a habitat patch (Adj. R2=0.96, F(1, 11)=288.23, P=0.0001; Fig. 3). Forty-two dispersals were observed during this study, and 22 (52%) of these were between groups in different habitat patches. A significantly higher proportion of female natal dispersal (93%) involved movement

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between habitat patches than did male natal dispersal (42%) (w2(1)=5.73, P=0.017; Table 1). There was no significant difference in the frequency of male natal and post-natal dispersal between habitat patches (w2(1)=0.09, P=0.768; Table 1). Female natal dispersals between habitat patches were significantly more common than post-natal and breeding dispersals between patches (w2(1)=8.26, P=0.004). There was a significant increase in the number of dispersals per patch as the number of groups in patches increased (F(3, 16)=3.88, P=0.029; Table 2). However, when standardized for the number of groups per patch the dispersal rate was not significantly different (F(3, 16)=0.17, P=0.910). The percentage of dispersals that resulted in emigration from the habitat patch declined as the number of groups in the habitat patch increased (Table 2). The proportion of male dispersals resulting in patch emigration declined rapidly as the number of groups/ patch increased, but for females this proportion never dropped below 50% (Fig. 4). Males emigrating from their natal patch never dispersed further than 1 km to their new patch, while females emigrating from their natal patch dispersed to patches up to 4 km away (Fig. 5). 3.2. Local population neighbourhoods In the simulation model the level of association between groups within the same habitat patch was generally

Fig. 2. The relationship between the area of habitat patches and the average number of groups occupying that habitat patch from 1994 to 1996. *This value was excluded from the regression model as an outlier (see text).

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P.G. Cale / Biological Conservation 109 (2003) 237–248 Table 2 The variation in the rate of dispersal and the frequency of patch emigration from habitat patches occupied by different numbers of groups Number of groups per habitat patch

Number of dispersals/ patch/year Number of dispersals/ group/year % Of dispersals between patchesa

1

2–3

4–5

6–7

0.70.2

1.40.4

2.11.1

5.03.0

0.70.2

0.60.2

0.50.3

0.70.4

100

75

42

10

a The percentage of dispersals between patches represents that proportion of all dispersals that resulted in movement between habitat patches (patch emigration). Values for the number of dispersals are meansS.E.

Fig. 3. The relationship between the number of groups in a habitat patch and the frequency of interactions between those groups. Interaction Rate equals the number of interactions/group/10 observations/ year. 2 and 3 indicate points which represent two or three patches, respectively. Table 1 The frequency of dispersals within and between habitat patches for male and female White-browed Babblers Number of dispersals Within patches

Between patches

Males Likely natal Known post-natal

7 4

5 1

Females Likely natal Known post-natal Known breeding

1 2 3

13 1 0

17

20

Total

Likely natal dispersals may include post-natal dispersals, because the natal group was not known for all individuals. For known post-natal and breeding dispersals the origin of the individual was known. Breeding dispersals for males could not be determined, because the breeding male in each group was unknown. Five dispersing birds were excluded, because their sex was unknown

575 hits in 100 iterations (75%) and never fell below 65%. Those group pairs with levels of association below 75% were always in habitat patches containing more than two groups and always had levels of association 575% in common with other groups in the patch. In Site A all habitat patches were included in the same local population neighbourhood at the lowest level of association (25% neighbourhood model; Fig. 6a). This local population neighbourhood was divided into three in the 50% neighbourhood model. However, there were unidirectional associations between some population neighbourhoods that were just below the model’s criterion for inclusion as a single neighbourhood. Eight

local population neighbourhoods occurred in the 75% neighbourhood model, but there was a unidirectional association between some of these local population neighbourhoods. The 25% neighbourhood model for Site B had only one local population neighbourhood (Fig. 6b). The 50% neighbourhood model had four local population neighbourhoods. In this model there were unidirectional associations between several neighbourhoods, but the level of association between these neighbourhoods in the opposite direction was low. The 75% neighbourhood model had seven local population neighbourhoods, with unidirectional associations between three of these that were just below this model’s criterion. I calculated the number of dispersals that occurred within and between both habitat patches and the local population neighbourhoods defined by each neighbourhood model shown in Fig. 6. Since both 25% neighbourhood models had only one local population neighbourhood all observed dispersals were within the local population neighbourhoods. For Site A half of the observed dispersals occurred between groups in different habitat patches (Table 3). Approximately one in every four dispersing birds moved between local population neighbourhoods defined by the 75% neighbourhood model, which was more than twice as high as for those local population neighbourhoods defined by the 50% neighbourhood model. The number of dispersals observed in Site B was low (12 dispersals), but more than half of these dispersals were between groups in different habitat patches (Table 3). One in three dispersing birds moved between the local population neighbourhoods defined by the 75% neighbourhood model. No dispersals were observed between groups occupying the different local population neighbourhoods defined by the 50% neighbourhood model. Using the 50% neighbourhood model, the total number of dispersals within habitat patches (Dw) was similar to the total number of dispersals between habitat patches

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Fig. 4. Sexual differences in the relationship between the percentage of dispersals between habitat patches (patch emigration) and the number of groups in habitat patches. (Male n=17; female n=20).

Fig. 6. The local population neighbourhoods for (a) Site A and (b) Site B, defined by three neighbourhood models; 25%—light grey shaded area, 50%—moderate grey, and 75%—dark grey. The black dots represent babbler groups, white areas with solid lines represent habitat patches. The arrows represent unidirectional associations within the prescribed neighbourhood model.

Fig. 5. Sexual differences in the distribution of dispersal distances for individuals that dispersed between habitat patches. Dispersal distances were measured between the edges of habitat patches. The maximum value for each distance class is represented.

in the same local population neighbourhood (Db), for both study sites (Table 4). Dw and Db were higher than DLPN (dispersals between groups occupying habitat patches in different local population neighbourhoods) in both study sites. The relative frequency of dispersals at the three scales varied greatly for each local population neighbourhood, but generally neighbourhoods where few dispersals were observed had low values of DLPN (Table 4).

4. Discussion For a species dependent on remnant vegetation, such as the White-browed Babbler, one of the major

consequences of habitat loss and fragmentation is a reduction in the size of habitat patches. This results in fewer groups occupying each habitat patch. Since the relative frequency of social interactions between babbler groups declined as the number of groups in a patch declined, declining patch size corresponds to a depression in social interaction. Social interaction is important to dispersal in cooperatively breeding birds (Zack and Rabenold, 1989; Cale, 1999). Consequently, changes in patch size are likely to have a negative effect on not only social interactions, but also on dispersal behaviour. Change in dispersal behaviour resulting from declining patch size was reflected in an increase in the proportion of dispersals that resulted in patch emigration as the number of groups in a patch declined (Table 2). This was despite the number of dispersals/group remaining constant. The change in the frequency of patch emigration differed for males and females (Fig. 4), which can be explained by sexual differences in dispersal behaviour resulting from the social structure of White-browed Babblers. Male helpers monitor groups near their current territory seeking better opportunities to obtain a

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Table 3 The number of observed dispersals that occurred within and between the local population neighbourhoods (LPN) defined by the three neighbourhood models and using habitat patches as local population neighbourhoods Model

Dispersals Within LPN

Between LPNs

% Between LPNs

Site A 25% Neighbourhood model 50% Neighbourhood model 75% Neighbourhood model Habitat patch model

30 26 22 15

NAa 4 8 15

NA 13 27 50

Site B 25% Neighbourhood model 50% Neighbourhood model 75% Neighbourhood model Habitat patch model

12 12 8 5

NA 0 4 7

NA 0 33 58

a

NA indicates situations where all dispersals were within LPNs, because only one LPN was defined.

breeding position (assessment sphere). In habitat patches with many groups a male’s assessment sphere is encompassed by the patch, but in small patches it must extend beyond the patch or the male must accept fewer opportunities to disperse. An increase in patch emigration with decreasing patch size was also found in Nuthatches Sitta europaea by Matthysen et al. (1995). They described this phenomenon as a dilution effect of fragmentation and found that it also increased the distances dispersed by individuals (Matthysen et al., 1995). In the White-browed Babbler, however, patch emigration by males was limited to patches with inter-patch distances of no more than 1 km (Fig. 5). Therefore, if fragmentation increased inter-patch distances beyond this threshold the frequency of dispersal by males would decline. Female natal dispersals were substantially larger than the spatial scale of habitat patches (Cale, 1999). This explains the greater frequency of patch emigration by females even in the largest habitat patches (50%, Fig. 4). If females made only natal dispersals then there should be no relationship between patch size and the proportion of dispersals resulting in patch emigration, which was not the case. Females also made post-natal and breeding dispersals that appeared to be confined to the same spatial scale as male dispersals (Table 1), because, like males, these females assessed neighbouring groups for breeding opportunities (Cale, 1999). A reduction in the spatial scale of female breeding dispersal compared to natal dispersal has also been found in other bird species (Matthysen et al., 1995; Brooker and Brooker, 1997). Male dispersal and female post-natal and breeding dispersal were restricted to groups with a high level of

social contact. These dispersals did not define population boundaries, because female natal dispersal occurred at a much larger spatial scale and consequently connected a greater number of habitat patches. Therefore, these smaller scale dispersals created structure within populations. This is similar to the behaviourally structured population model of Sugg et al. (1996), in which populations are made up of groups that prevent complete random mating across the population. This social structure within populations has been found to play an important role in population demographics (Vucetich et al. 1997), and in maintaining genetic variation (Sugg et al., 1996). I call this level of association within a population a social neighbourhood. 4.1. Population structure The high level of patch emigration in White-browed Babblers does not mean that the metapopulation concept is inappropriate for this species. Habitat patches are not evenly distributed within the landscape and the landscape mosaic associated with these patches varies. This results in differences in landscape connectivity and means that the level of association between different habitat patches with respect to dispersal may differ. In the conceptual model (Fig. 1) I proposed that the population structure of babblers could be considered a metapopulation if there was a significant difference in the level of dispersal among groups within and between local population neighbourhoods defined at some spatial scale. The 50 and 75% neighbourhood models met this criterion (Table 3). Which of these models best represents the real local population boundaries in this landscape is dependent on the relative rates of dispersal between the defined populations. The rate of dispersal between the local population neighbourhoods defined by the different models showed an even decline with increasing spatial scale (Table 3). Therefore, there was no discrete local population structure defined by the configuration of these landscapes. In this situation the functional boundaries of local population neighbourhoods would depend on the production of potential dispersers in each habitat patch and the vagaries of dispersal by these dispersers. Estimating such boundaries is beyond the capabilities of the data presented here. I chose the 50% neighbourhood model as that which might best represent real local population boundaries, because it showed low but significant levels of dispersal between the defined local population neighbourhoods. The local populations generated by this model differed in structure, with most containing a number of habitat patches while others contained only one patch. This is similar to the mixed metapopulation structure defined by Harrison and Taylor (1997), and found in an empirical study of the Silver-spotted Skipper butterfly Hesperia comma (Hill et al., 1996).

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Table 4 The number of observed dispersals within and between the local population neighbourhoods (LPN) defined by the 50% neighbourhood modela Dispersals within LPNs Dw

Db

Emigration from LPNs

% Db

DLPN

%DLPN

Site A LPN 1 LPN 2 LPN 3

12 3 0

5 5 1

29 62 100

3 0 1

15 0 50

Total

15

11

42

4

13

Site B LPN 1 LPN 2 LPN 4

2 2 0

NA 5 2

NA 71 100

0 0 0

0 0 0

Total

4

7

64

0

0

a %Db is the percentage of dispersals within a local population neighbourhood that occurred between different habitat patches, while % DLPN is the percentage of all dispersals that resulted in emigration from the local population neighbourhood. LPN 3 from Site B was excluded because only two groups in one habitat patch had banded birds. There was one dispersal observed within this habitat patch. NA: LPN 1 in Site B had only one habitat patch, so Db was not applicable.

Therefore, the population of White-browed Babblers in the Kellerberrin landscape can be considered to represent a metapopulation, but it has a hierarchical structure (Fig. 7). The basic unit of this structure is the group, which represents a single breeding unit. Babbler groups interact with nearby groups facilitating male dispersal and female post-natal and breeding dispersal. This level of association represents the second level of organization, the social neighbourhood. Social neighbourhoods are connected by female natal dispersal to form local population neighbourhoods. Local population neighbourhoods form a metapopulation, because there is a low level of dispersal between them that influences their dynamics, but is unlikely to be frequent enough to prevent them from changing independently of each other (Cale, 1999). Although this population structure fits the broad definition of a metapopulation (Hanski and Simberloff, 1997), as with many empirical studies, it does not reflect the definition of a metapopulation that has been used to generate most of Metapopulation Theory (Harrison and Taylor, 1997). Habitat patches used by White-browed Babblers were discrete units, but because dispersal between many habitat patches was high they represented social structuring within local populations not local populations themselves. Andre´n (1994) has argued that many bird and mammal studies that have used the concept of a metapopulation have done so with habitat patches that are too small to support local populations.

Fig. 7. A Hierarchically Structured Population Model. There are four levels in the hierarchy. Breeding units (solid black circles) in Whitebrowed Babblers are represented by groups. Social neighbourhoods are defined by high levels of social interaction between groups. Local population neighbourhoods are clusters of social neighbourhoods associated by high levels of dispersal. The metapopulation is a cluster of local population neighbourhoods which have independent dynamics, but are connected by a low level of dispersal.

This presents a problem, since the processes that are causing extinction and recolonisation in these patches may be related more to the dynamics of individuals than populations (Haila, 1990; Andre´n, 1994). 4.2. The effect of landscape change on dispersal The response of White-browed Babblers to the dilution effect of fragmentation is complex, because of the sexual differences in dispersal behaviour. Both sexes increased the frequency of dispersals between habitat patches as patch size decreased, but most of this dispersal was related to social neighbourhoods not populations. Female natal dispersal, which defined local population neighbourhoods, occurred at a spatial scale larger than that of habitat patches and did not appear to be affected by changing patch size. Therefore, the fission response proposed by Ims et al. (1993) was observed in White-browed Babblers at the scale of the social neighbourhood, but not at the population scale.

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This indicates that a more complex model that included social aspects of a species would better describe their response to landscape change (see Lima and Zollner, 1996). These dispersal patterns are influenced by the permeability to dispersal of habitat patch boundaries, but this permeability was dependent on the level of organization being considered. The edges of habitat patches appeared to be relatively impermeable boundaries to the social dynamics of babbler groups (social neighbourhood). However, the degree of permeability of these boundaries was dependent on patch size and the context of the patch. When patches and inter-patch distances were small, patch edges appeared to be more permeable to social interactions. At the local population scale the permeability of habitat patch boundaries was dependent on the landscape mosaic associated with the patch. White-browed Babblers were able to traverse areas of agricultural land if patches of native vegetation occurred in a configuration that allowed them to be used as ‘stepping stones’. Consequently, the permeability to dispersal of the boundaries between habitat patches and agricultural vegetation was dependent on the unique configuration of the different landscape elements around each habitat patch. This resulted in the frequency of dispersal between some patches being asymmetrical. This characteristic was also found for the European Badger Meles meles, using a very different type of dispersal simulation (Schippers et al., 1996), and has been predicted by theoretical models (Taylor et al., 1993; Gustafson and Gardner, 1996; Wiens, 1997). The consequences of asymmetrical dispersal rates between patches is that it is essential to consider landscape connectivity in a spatially explicit context, at least for species that use some elements of the landscape mosaic in preference to others when dispersing. Fahrig (1998) argued that spatially explicit modelling to investigate the effects of fragmentation was only necessary under a very narrow set of conditions. However, Fahrig’s modelling was done using two underlying assumptions that are not appropriate for the Whitebrowed Babbler and for many other cases of landscape fragmentation. The first of these assumptions is that all of the landscape could be occupied by individuals. Many species in landscapes fragmented by agriculture never occupy (except possibly during the short period of dispersal) that portion of the matrix containing agricultural vegetation types. Secondly, Fahrig (1998) limited her modelling to a landscape with a homogeneous matrix that is unlikely to be common in real landscapes (Wiens, 1994, 1997). Even in the simple model used in the current study, which contained three landscape elements (suitable habitat, other remnant vegetation and agricultural vegetation), the spatial pattern of these elements strongly influenced dispersal patterns (Brooker et

al., 1999). Species living in landscapes that fail to meet these two assumptions are likely to be affected by spatially explicit fragmentation effects, such as those described for White-browed Babblers. 4.3. The effect of demography on population structure As argued earlier, the number of potential dispersers produced in each habitat patch will determine the functional boundaries of local population neighbourhoods. The reproductive quality of White-browed Babbler habitat patches was found to be dependent on patch shape (linear patches, such as road verges, were of lower reproductive quality than more circular patches) and the structure of the vegetation (denser vegetation was of higher reproductive quality; Cale, 1999). However, reproductive success was also enhanced by increases in group size. Males tended to disperse from large to small groups, which may have maintained a larger median group size in habitat of lower reproductive quality, and so increased reproductive success (Cale, 1999). This influence of male dispersal on reproductive success means that the reproductive quality of habitat patches is context dependent. Habitat patches that have similar physical characteristics may differ in reproductive quality, because the frequency of male dispersal differs depending on the landscape configuration at the scale of the social neighbourhood. Therefore, since increasing fragmentation and isolation of habitat patches reduces male dispersal, the average reproductive success of social neighbourhoods may decline. As a consequence, the boundaries of local population neighbourhoods may shrink due to the decline in the number of potential dispersers. Fragmentation and habitat loss are also likely to affect the dynamics of local population neighbourhoods directly. The levels of dispersal within and between the defined local population neighbourhoods showed considerable variation (Table 4). In part, this was because habitat patches differed in size, but the spatial isolation of patches and the overall size of the local population also appeared to have an effect. Hill et al. (1996) found that the per capita emigration rate of the Silver-spotted Skipper was higher in small local populations compared to larger ones. Although the sample size of dispersals for the White-browed Babbler is small, it does show similarities to this relationship. The smallest local population in Site A (LPN 3, Table 4) produced 25% of the observed emigrations despite producing only 7% of all dispersals in this landscape (Table 4). The problem of higher emigration from small local populations can be exacerbated by the observed asymmetric dispersal patterns between patches. This dispersal pattern means that some local populations may face a high rate of emigration that is not compensated for by a corresponding rate of immigration.

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5. Conclusions The complex population structure of the Whitebrowed Babbler in the fragmented landscape of Kellerberrin is the consequence of demographic processes being influenced at a number of spatial scales. The consequence of this is that it is essential to consider which organisational level a process is operating at before assessing how the patchiness of the landscape relevant to that process is structured. The Hierarchical Model of Heterogeneity proposed by Kotliar and Wiens (1990) outlines an approach to dealing with this complexity. Modelling approaches are a major step forward in dealing with the problem of the complexity of interactions between processes at multiple scales (With, 1997; With and King, 1999). However, modelling is only as good as the quality of the empirical data upon which models operate. These empirical data need to address the validity of the assumptions used in models, but equally modelling research must seek to investigate the influence different sets of assumptions have on model outcomes (e.g. the effect of multiple spatial scales or the inclusion of social dynamics). Without an effort to improve the empirical base upon which modelling is done, such as including differences in a hierarchy of spatial scales and aspects of social behaviour, the generalisations about how landscape fragmentation affects the persistence of species will continue to elude us.

Acknowledgements I am grateful to Belinda Cale and Hugh Ford for commenting on earlier versions of this manuscript. This manuscript represents part of a PhD at the University of New England, and was funded by the University of New England and CSIRO Wildlife and Ecology.

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