Tolerance of Human Disturbance by Urban Magpie-Larks

1 AUSTRALIAN Field Ornithology 2010, 27, 1–9 Tolerance of Human Disturbance by Urban Magpie-larks

KIM KITCHEN, ALAN LILL1 and MEGAN PRICE2 Wildlife Ecology Research Group, School of Biological Sciences, Monash University, Clayton Campus, Victoria 3800 1Corresponding author: [email protected] 2Present address: Kalahari Meerkat Project, Kuruman River Reserve, P.O. Box 64, Van Zylsrus, Northern Cape 8467, Republic of South Africa

Summary To successfully colonise cities, birds must be highly tolerant of human traffic. We examined this tolerance in a native urban coloniser, the Magpie-lark Grallina cyanoleuca, in suburban Melbourne, Victoria. We compared flushing behaviour and the Flight Initiation Distance (FID) of urban and rural individuals, and of urban individuals encountered near to and farther away from roads and pathways carrying vehicular and pedestrian traffic. Mean FID to a researcher was 12 ± 1 m in Melbourne, compared with 35 ± 3 m in rural Victoria. Rural birds also flushed more by flying (100% versus 57.6%) and fled farther than urban individuals. Mean FID to a researcher was 1.9 times larger farther from (13 ± 2 m) than near to (7 ± 0.6 m) urban roads, but time allocations to vigilance (24.1%) and foraging (65.5–69.4%) and the percentage of birds that flushed (86% and 75%) were similar in the two locations. People caused more of the flushing of Magpie-larks near to (55%) than farther from (20%) urban roads and pedestrian pathways. We speculate that the disparities in flushing behaviour (urban/rural and near to/farther from urban roads) probably resulted mainly from habituation, a learning process that could be critical in facilitating urban colonisation and use of habitat near busy urban traffic corridors by members of temperamentally inherently ‘bold’ species.

Introduction In birds, high volumes of human traffic can reduce the species richness and alter the composition of communities (van der Zande & Vos 1984; Fernández-Juricic 2002), depress population density (Reijnen et al. 1997), alter spatial dispersion (Fernández-Juricic & Tellería 2000), disrupt vital behaviour (Steidl & Anthony 2000), stimulate intraspecific aggression (Burger 1981), reduce fecundity (Medeiros et al. 2007) and cause stress and mortality (Anderson & Keith 1980; Ellenberg et al. 2007). These effects probably occur mainly because many birds treat humans as potential predators, even when they are harmless, and consequently try to avoid them or become stressed when evasion is difficult or uneconomical (Frid & Dill 2002). Many native birds cannot make the transition to urban life, but the ecology and behaviour of some species, termed ‘urban adapters’ (Blair 2001), apparently ‘pre-adapts’ them to city life. One aspect of this pre-adaptation is likely to be possession of a temperament that permits rapid habituation to the heavy human traffic typical of cities (McDougall et al. 2006). Many northern-hemisphere urban birds have indeed been shown to be more tolerant of human proximity than rural conspecifics are (Cooke 1980; Møller 2008). Urban adapters often occur at higher population densities in urban than non-urban environments (Gliwicz et al. 1994). Conceivably, one factor permitting this is their ability to habituate so well to human traffic that they can permanently inhabit, or at least regularly exploit, ecologically suitable habitat adjoining busy urban traffic corridors, with perhaps reduced competition from less adaptable competitors. Much research has been AUSTRALIAN 2 KITCHEN, LILL & PRICE Field Ornithology conducted on urban colonisation by native Australian birds (e.g. Catterall 2004; French et al. 2008; Lill 2009), but their tolerance of vehicular and pedestrian traffic is poorly documented and understood. The natural habitat of the Magpie-lark Grallina cyanoleuca is open and savanna woodlands and native grasslands, but this species is also widespread in anthropogenically modified habitats (e.g. farmland) and is one of Australia’s most successful native, avian urban adapters. Adult pairs are territorial year-round and commonly forage terrestrially for insects in urban parkland and streetscapes (Higgins et al. 2006). We examined the species’ tolerance of human proximity and traffic by measuring two behaviour variables commonly employed for this purpose: (1) the Flight Initiation Distance (FID)—the distance between a bird and an approaching human at which the bird flees (Blumstein 2003), and (2) the time-activity budget (TAB)—human proximity may be insufficient to stimulate fleeing, but can nevertheless negatively influence a bird’s time allocations to vital maintenance (of self and progeny) and predator-monitoring (vigilance) behaviour. The TAB allows any such effects to be quantified, and is commonly used to evaluate the effects of human traffic and proximity (Burger & Gochfeld 1998; Fernández- Juricic & Schroeder 2003). We specifically examined (a) whether FID in response to a researcher approaching on foot differed between urban and rural Magpie- larks, and (b) whether the stimuli eliciting natural fleeing behaviour, the fleeing mode, FID to an approaching researcher, and time allocations to foraging and vigilance differed in urban Magpie-larks encountered near to and farther away from pathways and roads carrying substantial pedestrian and vehicular traffic.

Methods

Study area and sites The first (Study 1: April–August 2003) of two studies conducted 2 years apart compared the tolerance of urban and rural Magpie-larks to human approach. The 16 urban study sites were public parks and streetscapes in suburban Melbourne in an area bounded by Wheelers Hill (37°54′S, 145°12′E), Bundoora (37°47′S, 145°03′E), Parkville (37°47′S, 144°56′E) and Braeside (38°00′S, 145°07′E). The 24 rural Victorian sites included roadside vegetation corridors, agricultural land and lawns and gardens, and were 36–314 km from Melbourne in an area bounded by Wannon (37°40′S, 141°50′E), Mansfield (37°03′S, 146°05′E), Leongatha (38°28′S, 145°56′E) and Werribee (37°54′S, 144°39′E). The second investigation (Study 2: October 2005–January 2006) was conducted in 92 public parks, reserves, gardens and streetscapes in Melbourne in an area bounded by Wheelers Hill, Parkville, Williamstown (37°51′S, 144°53′E) and Dingley (37°57′S, 145°07′E). Most parks and reserves had open turfed areas, trees, garden-beds and pedestrian footpaths, and many had roads carrying vehicular traffic. Streetscapes contained a road and usually pedestrian footpaths and grass verges. Mean monthly maximum and minimum temperatures in Melbourne averaged 17 and 9°C, respectively, during Study 1 and 25.3 and 14.4°C, respectively, during Study 2. Melbourne’s monthly rainfall averaged 50 and 58.8 mm during the 2003 and 2005–06 investigations, respectively.

Measurement of behaviour We minimised resampling of individuals, and hence increased statistical independence of the data, by using (a) many dispersed study sites only once or twice each, and (b) spatially well-separated locations within a site. The strong territoriality and distinct male and female plumage patterns of breeding adults facilitated this strategy. Sampling was restricted to fine weather. The observers wore the same-coloured clothing for all observation sessions. To achieve measurement consistency, a single researcher made all FID determinations within a study. Observations were made with binoculars, and distances were measured (± 1 m) by calibrated pacing (Study 1) or with a Bushnell® Yardage Pro Sport 450 laser rangefinder (Study 2). VOL. 27 (1) march 2010 Tolerance of Humans by Magpie-lark 3

In Study 2, the natural flushing behaviour (i.e. retreat from a ‘threatening’ stimulus by flying, running or walking) of urban Magpie-larks was recorded in five large parks in January. A focal bird was observed for ≤10 minutes from ≥20 m. We recorded whether it flushed, the stimulus responsible (people and dogs; birds; vehicles and loud noises), flushing latency (time elapsed in minutes from observation onset to flushing) and the bird’s proximity (≤10 m or >10 m) to a road carrying vehicular traffic or a pathway for pedestrians and cyclists. The causes of flushing of focal birds were pedestrians, cyclists, dogs (usually accompanying pedestrians) and other birds, including both con- and heterospecifics. FID was measured by a researcher approaching a Magpie-lark in a direct line at a constant walking speed (2.5–3.5 km h-1) until it fled. In Study 2 we measured the Starting Distance (STD, distance between observer and target bird when approach commenced), FID, mode of flushing (flying, running or walking) and location (≤20 m or ≥50 m from a road carrying substantial vehicular traffic) in approaches made to focal birds at 60 sites. STD influences FID in some species and circumstances (Blumstein 2003). Additional covariates coded as indicator variables (Quinn & Keough 2002) were the sex and age (adult or juvenile) of the approached bird, and the presence of conspecifics within 10 m or humans and/or dogs within 20 m of the focal bird. Only 3.7% of FIDs were obtained from juveniles. At the 40 sites used in Study 1 we did not measure these covariates or the proximity to a road, but recorded whether a bird fled less or more than 15 m radially from the point of flushing by the researcher within 30 seconds of being flushed. In Study 2, the proportions of time allocated to vigilance (‘head up’ visual surveillance for predators) (Sadedin & Elgar 1998) and foraging (‘head down’ searching for and consuming food items) were measured for Magpie-larks in 55 sites over 3 months. Time allocation was determined by instantaneous sampling (Martin & Bateson 2007) of focal birds at 15-second intervals for 2–10 minutes. As for FID determination, the focal bird’s proximity (≤20 m or ≥50 m) to a road carrying vehicular traffic, its sex and age, and the presence of conspecifics and humans and dogs were recorded. Only 6% of TAB data was obtained from juveniles.

Data analysis Statistical analyses were conducted with Systat v. 10 software. Differences between the proportions of urban Magpie-larks that flushed and the stimuli that elicited flushing close to and farther from roads and pathways in Study 2 (2005–2006) were examined with chi-squared (χ2) contingency analyses. This approach was also used in examining urban–rural differences in flushing mode and distance in Study 1 (2003). Analysis of Covariance (ANCOVA) was employed to determine whether urban Magpie-larks’ FIDs and relative time allocations to foraging and vigilance in Study 1 differed near to and farther from roads. As proportional times spent foraging and being vigilant were not independent, the critical probability level was adjusted to 0.025 for these analyses, according to the Bonferroni procedure (Quinn & Keough 2002). When comparing variables between locations in both studies, logarithmic or arcsine transformation of data was used to help meet assumptions of normality and homoscedasticity or, where this did not help, we employed a non-parametric test (Quinn & Keough 2002). Results are reported as means ± standard error.

Results

Urban–rural differences in tolerance of human approach In autumn and winter 2003 (Study 1), mean FID of rural Magpie-larks to a human researcher was nearly three times that of urban individuals (rural 35 ± 3 m, urban 12 ± 1 m; independent t (53) = 8.214, P <0.001). Rural birds avoided the researcher exclusively by flying away, whereas urban Magpie-larks flew away 2 on only 57.6% of occasions, running or walking nearly as often (χ (1) = 10.384, P = 0.001, n = 55). Rural Magpie-larks fled >15 m from the location from which they were flushed by the approaching observer on 95.5% of occasions, whereas 2 only 45.5% of urban birds fled >15 m (χ (1) = 12.467, P <0.001, n = 55). AUSTRALIAN 4 KITCHEN, LILL & PRICE Field Ornithology

Natural flushing behaviour in the urban environment In 2005–06 (Study 2), 81% of focal Magpie-larks flushed during observation periods that had a 10–minute maximum duration. There was no significant difference in the percentage of birds that flushed ≤10 m (86%) and >10 m (75%) 2 from roads and pathways (χ (1) =1.548, P = 0.213, n = 117), nor in the mean latency to flush (3.3 ± 0.3 versus 3.1 ± 0.4 min.) in the two locations (Mann-Whitney U = 1032.5, P = 0.611, n = 95). However, there was a significant difference in the stimuli that elicited flushing near to and farther from roads and pathways. Near to roads and pathways, people and dogs stimulated 55% of flushing, birds 27.5%, and vehicles and loud sounds 17.5%; the corresponding percentages >10 m 2 from roads and pathways were 20%, 70% and 10% (χ (2) = 11.26, P = 0.01, n = 60). Analysis of χ2 residuals suggested that ‘birds’ were probably particularly responsible for this disparity (z = 0.018). Other Magpie-larks caused 48% of the flushing responses stimulated by birds, and most of the other bird-induced flushing was stimulated by Australian Magpies Cracticus tibicen.

Tolerance of human approach near to and farther away from urban roads In 2005–06 (Study 2), mean FID of urban Magpie-larks to a researcher was very similar to that recorded in 2003 (Study 1), averaging 10 ± 1 m (n = 109). It was significantly larger (by a factor of ~1.9) farther from (>50 m) than close to (≤20 m) roads (13 ± 2 m, n = 53, versus 7 ± 0.6 m, n = 56) (Table 1). Mean STD of the observer was 47 ± 3 m, males comprised 68% of the adult birds approached, conspecifics were present during 31% of researcher approaches, and other humans and/or dogs on 6% of occasions. However, no significant F-ratios were obtained in the analysis examining the effect of proximity to roads on FID for any of the covariates. The mode of fleeing from the approaching experimenter was similar near to and farther from roads: flying comprised 57%, running 20% and walking 23% of flushing responses near to roads, the corresponding percentages farther 2 from roads being 50%, 29% and 21%, respectively (χ (2) = 1.26, P = 0.534, n = 108).

Time-activity budgets (TABs) near to and farther away from urban roads In Study 2 (2005–06), vigilance comprised 24.1 ± 2.2 % and foraging 67.6 ± 2.7% of the TAB of Magpie-larks away from the nest (n = 115). Proximity to roads had no significant effect on the proportional time allocations to these two activities (Table 2). Vigilance accounted for ~24% of the TAB away from the nest both near to and farther from roads; comparable values for foraging were 65.5% and 69.4%, respectively. Conspecifics were present on 57% and other humans and/or dogs on 45% of occasions. The effect of proximity to roads on the TAB was influenced by the covariables ‘presence of conspecifics’ and ‘focal bird’s sex’ (Table 2). Magpie- larks were more vigilant (1.5×) and foraged less (0.8×) when conspecifics were present, and males (which comprised 67% of the adults sampled) were more vigilant (1.7×) and foraged less (0.8×) than females.

Discussion

Urban–rural disparity in flushing behaviour There was a robust difference in the response of urban and rural Magpie- larks to a researcher’s approach: urban birds had a smaller FID, flushed less VOL. 27 (1) march 2010 Tolerance of Humans by Magpie-lark 5

Table 1 Outcome of Analysis of Covariance (ANCOVA) examining the effect of proximity to roads on the Flight Initiation Distance (FID) of Magpie-larks (Study 2). Degrees of freedom = 1 for all sources of variation. Significant probability is shown in bold. Source of variation Sum of squares F- ratio Probability

Proximity to roads 0.936 6.791 0.011 Sex 0.034 0.248 0.619 Presence of conspecifics 0.014 0.098 0.755 Presence of humans and/or dogs 0.242 1.757 0.188 Observer Starting Distance (STD) 0.244 1.772 0.186

Table 2 Outcome of ANCOVAs examining the effect of proximity to roads on the percentage of time allocated to vigilance and foraging by Magpie-larks (Study 2). V = vigilance, F = foraging. Degrees of freedom = 1 for all sources of variation. P (critical) = 0.025 after Bonferroni adjustment (see text). Significant probabilities are shown in bold. Source of variation Behaviour Sum of squares F-ratio Probability

Proximity to roads V 0.002 0.026 0.873 F 0.087 0.632 0.428 Sex V 0.435 5.381 0.022 F 1.107 8.066 0.005 Time of day V 0.288 3.554 0.062 F 0.347 2.525 0.115 Presence of conspecifics V 1.289 15.937 <0.001 F 1.995 14.537 <0.001 Presence of humans and/or dogs V 0.092 1.138 0.289 F 0.076 0.554 0.458 often by flying, and retreated a shorter distance than rural conspecifics (Study 1). As even rural birds did not retreat very far from the researcher, it is unlikely that the urban–rural disparity was simply a product of a smaller territory size of urban pairs (Higgins et al. 2006; Møller 2008). Rollinson (2003) reported very similar findings for the Australian Magpie, another native urban adapter: when approached by a researcher, individuals in rural and semi-natural areas had a FID 6–7 times greater, fled 3.7–7.7 times farther, retreated 50% more often by flying rather than running or walking, and took much longer to resume their previous behaviour than Magpies in suburban Brisbane, Qld. Cooke (1980) and Møller (2008) have also demonstrated similarly greater tolerance in urban populations of some common European birds. Two aspects of Magpie-larks’ behaviour may underpin their capacity to tolerate human traffic in cities. Firstly, they appear inherently to have a ‘bold’ temperament, as suggested by their tendency to attack and threaten actual and potential predators and non-predatory birds (Higgins et al. 2006), as well as their own mirror image and models of predators (A. Lill unpubl. obs.). Secondly, they apparently have sufficient behavioural plasticity to habituate to some threatening stimuli that their experience indicates are mostly AUSTRALIAN 6 KITCHEN, LILL & PRICE Field Ornithology harmless. The latter facility would have been important in their initial capacity to colonise cities, but the ability to successfully inhabit suburbia long-term may be enhanced in urban adapters by gradual evolutionary adaptation. Møller (2008) presented indirect support for genetic adaptation by showing for some European birds (a) that interspecific variation in FID of urban relative to rural populations was predicted by the estimated number of generations since urban colonisation, and (b) that in species with relatively larger urban than rural populations, implying gradual local urban adaptation, relative FID was shorter. Few studies have examined the genetic distinctness of urban and rural populations of any bird species, but Partecke et al. (2006) demonstrated that Common Blackbird Turdus merula populations in Munich, Germany, and in a rural forest ~50 km away from there were not genetically differentiated, despite some functional genetic adaptation of urban individuals. There are no obvious barriers to gene flow between the Magpie-lark population in Melbourne and those of much of nearby rural Victoria. The urban–rural disparity demonstrated in the present study needs to be examined for other Australian cities inhabited by Magpie-larks to establish if it is widespread.

Stimuli eliciting natural flushing behaviour in urban Melbourne People commonly stimulate flushing in urban birds (Fernández-Juricic & Tellería 2000). The greater role of people and dogs in flushing urban Magpie-larks near to than farther away from roads and paths in Study 2 was predictable, because pedestrian traffic predominantly used the paths. Nearly 50% of the flushing of urban Magpie-larks between October and January that was stimulated by birds was attributable to conspecifics, which probably reflected this species’ strong breeding territoriality (Neill & Lill 1998). The importance of Australian Magpies in stimulating Magpie-lark flushing was not surprising, given their abundance in Melbourne’s parks, tendency to forage in similar sites (i.e. on the ground in open areas), and much larger size (1.5-fold). The small contribution of vehicles to inducing flushing partly reflected the relatively small proportion of observations conducted near roads carrying vehicular, as opposed to pedestrian, traffic in this set of observations, but also probably the fact that people appear to be perceived by wildlife as less threatening when in vehicles than on foot (Rodgers & Smith 1995). Moreover, most vehicular approach was tangential, which is usually less threatening than direct approach, although there are exceptions (Fernández-Juricic et al. 2005). Flight was used exclusively in fleeing by rural, and commonly by urban, Magpie-larks. Despite the high metabolic cost of short flights (Nudds & Bryant 2000), the benefit is rapid escape from a perceived strong threat.

Proximity to urban roads, tolerance of approach and the time-activity budget Urban Magpie-larks near roads carrying vehicular traffic had a shorter FID to an approaching ambulatory researcher than individuals farther away from roads (Study 2). Conceivably, roadsides were occupied by individuals inherently more tolerant of human proximity, although it seems more plausible that all urban Magpie-larks are capable of habituating to human proximity if given sufficient exposure. If habituation were involved, it is interesting that the roadside birds would probably have had more exposure to vehicular than to pedestrian traffic. To properly evaluate why the more tolerant birds near roads exhibited the same vigilance effort as individuals farther away from roads would require documentation of the relative frequencies of all threatening stimuli in the two VOL. 27 (1) march 2010 Tolerance of Humans by Magpie-lark 7 locations. Natural (i.e. non-experimental) flushing probabilities to threatening stimuli were similar in the two locations, although a different spatial criterion was used in Study 2. Vigilance was presumably broadly ‘tuned’ to all threatening stimuli, not just to people. It is worth noting too that in Magpie-larks some low- quality visual surveillance may be possible during ‘head-down’ foraging (Lima & Bednekoff 1999). The greater vigilance observed in the presence of conspecifics was contrary to the common finding that individual vigilance is reduced, but predator detection enhanced, in groups (Roberts 1996). However, adult males were more vigilant than females, so the enhanced vigilance in the presence of conspecifics may have reflected the fact that our observations were made when breeding-season intraspecific territoriality was strong, and conspecifics stimulated nearly half of the many flushing responses caused by birds. Neill & Lill (1998) reported that males featured in most conspecific territorial intrusions, 83% of which elicited aggression in the resident male. Some other authors have reported similar greater tolerance of human proximity by birds in areas with high, rather than low, volumes of pedestrian traffic, although not particularly in association with trails or roads (van Heezik & Seddon 1990; Sutherland et al. 2006; Walker et al. 2006). In contrast, some authors have demonstrated reduced tolerance of human proximity by birds and large mammals near pedestrian trails or roads (Miller et al. 2000; Burger & Gochfeld 2001; Taylor & Knight 2003). However, these studies were mostly in rural locations. More directly relevant is the argument that the greater volume of vehicular and pedestrian traffic observed at the edges than in the interior of wooded urban parks in Madrid, Spain, led to lower breeding densities in bird species less accustomed to urban traffic (Fernández-Juricic 2001). Fernández-Juricic and Tellería (2000) also found that Common Blackbirds in these parks exhibited increased vigilance and reduced feeding in the presence of humans, and avoided close proximity to pathways as pedestrian traffic on them increased. An intriguing, and as yet largely unanswered, question about urban adapters such as the Magpie-lark concerns the features of their natural habitat that have exerted selection for a bold temperament and behavioural plasticity. These traits apparently allow them to tolerate high volumes of human traffic, which is so crucial to successful, high-density colonisation of the urban environment.

Acknowledgements We thank Helen Crisp, Kylie Eklom, Evelyn Nicholson, Alistair Stewart, Ian Stewart and Nathan Walker for various kinds of assistance with the project.

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Received 9 July 2009 