Recent work on animal personalities has demonstrated that individuals may show consistent behaviour across situations and contexts. These studies were often carried out in one location and/or during short time intervals. Many animals, however, migrate and spend their life in several geographically distinct locations, and they may either adopt behaviours specific to the local environment or keep consistent behaviours over ecologically distinct locations. Long-distance migratory species offer excellent opportunities to test whether the animals maintain their personalities over large geographical scale, although the practical difficulties associated with these studies have hampered such tests. Here, we demonstrate for the first time consistency in disturbance tolerance behaviour in a long-distance migratory bird, using the common crane Grus grus as an ecological model species. Cranes that hatched in undisturbed habitats in Finland choose undisturbed migratory stop-over sites in Hungary, 1300–2000 km away from their breeding ground. This is remarkable, because these sites are not only separated by large distances, they also differ ecologically: the breeding sites are wooded bogs and subarctic tundra, whereas the migratory stop-over sites are temperate zone alkaline grasslands. The significance of our study goes beyond evolutionary biology and behavioural ecology: local effects on behaviour may carry over large distances, and this hitherto hidden implication of habitat selection needs to be incorporated into conservation planning.
Animals in the same population usually differ in their behaviour and underlying physiology [1,2]. Moreover, the same set of animals may show the same kind of differences in different situations (e.g. in level of predator avoidance at different foraging sites) and contexts (e.g. boldness in foraging and social interactions). For instance, great tits Parus major show consistent individual differences in exploring open field areas , and in mosquito fish, Gambusia affinis, asocial individuals show greater dispersal tendency . Although individuals may adjust their behaviour depending on situations, consistent differences between individuals usually remain. These are frequently characterized as animal personalities , temperament , behavioural syndromes or coping styles .
Many animals spend their life in several geographically distinct locations, and previous studies that investigate personality traits in a given location over short periods of time may not be able to estimate the importance of behavioural consistencies across contrasted ecological settings. Migratory insects, fishes, birds and mammals encounter wide range of habitats during their annual movements [8,9]; for instance Arctic terns Sterna paradisea fly over 70 000 km each year and cover vast range of habitats between their Arctic breeding ground and their wintering sites near Antarctica .
Animals may adopt two behavioural strategies when they encounter different ecological settings. On the one hand, they may exhibit different types of behaviour depending on local conditions during migration. On the other hand, they may show consistent behaviour even across highly contrasted environments .
Migratory species provide excellent opportunities to test these possibilities. Although the ability of migratory animals to exhibit consistent behavioural responses over large geographical areas has been suspected [12,13], no study has yet demonstrated such behaviour owing to the challenges of tracking animal behaviour over large geographical distances.
Here we investigate the behavioural consistency in a long-distance migratory bird, the common crane Grus grus, using disturbance-tolerance behaviour. Human disturbance has a large effect on the distribution, ecology and behaviour of animals [14,15], for instance, the spatial distribution of human settlements and density of roads influence avian habitat selection [16,17]. We hypothesized that the cranes' behavioural responses to human disturbance are consistent between their natal site and their migratory stop-over site that are separated by over 1000 km.
2. Material and methods
We collected data between 1995 and 2007 in Hortobágy National Park in Hungary (47°30′ N, 21°0′ E, Hortobágy henceforth), which is the largest alkaline steppe in Europe (80 200 ha), a UNESCO World Heritage Site and protected by Ramsar Convention. Hortobágy is surrounded by 18 settlements (min–max no. of inhabitants: 1950–50 000).
We use data on 273 cranes that were marked as chicks in Finland between 1985 and 2007 by individual combinations of colour rings, and resighted in Hortobágy between 1995 and 2007 (figure 1a). Locations of nest sites were collected by P.M., and resighting data were acquired from the Hungarian Bird Ringing Center (Budapest). Five proxy variables of human disturbance were estimated from 1 : 16 000 maps of the National Land Survey of Finland (http://kansalaisen.karttapaikka.fi/kartanhaku/osoitehaku.html), and the Hortobágy National Park's GIS map (Hortobágy National Park Directorate 1995–2007 unpublished data), respectively: proximity (km−1) to the nearest (i) tarmac road and (ii) human settlement, and perturbance, i.e. density (ha−1) of (iii) tarmac roads, (iv) human settlements, and (v) human population. Common crane territories are approximately 3–4 ha , and we estimated these variables within a 1 km radius around nests. On migration, the cranes move between roost sites and feeding sites, and since these are within 10 km, we estimated all five variables in a 10 km radius around roost sites .
Out of 273 cranes, 138 were observed at least twice (up to 10 times) in Hortobágy. For individuals observed several times in a year, we calculated the within-year repeatability of the disturbance variables. For those cranes that have been recorded repeatedly in different years, we calculated between-year repeatability of the disturbance variables . To investigate the consistency in behaviour between natal sites in Finland and migratory sites in Hortobágy, we fitted linear mixed-effects models (LMMs) using disturbance variables on the migratory site as response variables, and disturbance variables on the natal sites as fixed effects for all possible pairwise combinations (25 models in total ). A positive t-value, a proxy of effect size, indicates consistent result with the working hypothesis. Regions within Finland (as a control for spatial autocorrelation) and Bird ID were included in LMMs as nested random factors. We performed all statistical analyses in R .
Cranes used 10.24 ± 1.03 (mean ± s.e.) different roost sites in Hortobágy each year, and those cranes that were observed several times within a year used three (2–4.75) sites per year. Four of the five disturbance tolerance variables were significantly repeatable both within and between years for individual cranes (table 1). This indicates a high level of behavioural consistency both within a particular year and over the study period for a given individual.
Out of 25 pairwise models, 24 showed positive relationships between disturbance tolerance in the natal and migratory sites (binomial test using 0.5 expectation, p < 10−5, table 2). This was also indicated by the positive average t-values, and that their 95% confidence intervals did not include zero (figure 1b).
Common cranes show consistent disturbance tolerance behaviour between years, and between natal and migratory sites separated by over 1000 km. As far as we are aware, our study is the only one that demonstrates long-lasting individual differences in response to human disturbance using individually marked birds. Consistent disturbance tolerance behaviour may emerge in three mutually non-exclusive ways. First, young cranes may be imprinted to certain levels of human disturbance by the location of their nest, and they seek out these features during migration. Second, common cranes have extensive parental care that lasts up to 10 months after hatching . Therefore, the young crane's migratory behaviour may be influenced by their parents' behaviour . This carry-over of information may lead to cultural transmission of habitat preference in regards to disturbance . Third, habitat preference may have a genetic component so that certain genotypes tolerate more disturbance than others.
Previous studies demonstrated consistent behaviour in various contexts, including exploration, aggression, anti-predator behaviour, parental provisioning and cooperation [24–26]. Our work adds to these by showing personality-related traits in disturbance tolerance behaviour. Also, we expand the scope of personality by showing that cranes behave consistently over a long time period and between habitats with very different ecological conditions, such as northern wooded bogs, subarctic tundra and temperate zone alkaline grassland.
It would be interesting to investigate whether habitat preference correlates with other personality traits, e.g., flushing distance, exploration behaviour or physiological reactions to handling. Unfortunately, we are unable to address this proposition here because of the lack of appropriate data from individually marked cranes.
The process we demonstrate here is similar to the ecological carry-over, whereby events during one period of the annual cycle in migratory animals influence reproductive success in a subsequent season [13,27,28]. We propose that both the carry-over from one season to another and the consistent behavioural responses to disturbance we demonstrate here imply that conservation decisions for migratory species should be made at a larger geographical scale than is currently the case.
To conclude, disturbance sensitivity, a consistent personality trait, is retained in migratory species over large temporal and spatial scales as well as habitat types, and thus affecting habitat choice. These effects should be incorporated into conservation planning and policies.
Zoltán Barta was supported by TÁMOP project no. 4.2.1./B-09/1/KONV-2010-0007, which is implemented through the New Hungary Development Plan and co-financed by the European Social Fund and the European Regional Development Fund. Tamás Székely was funded by NERC (NE/C004167/1) and The Leverhulme Trust (ID200660763).
- Received March 15, 2011.
- Accepted April 13, 2011.
- This Journal is © 2011 The Royal Society