Are behaviour and stress-related phenotypes in urban birds adaptive?

Urbanisation is a world-wide phenomenon converting natural habitats into new artificial ones. Environmental conditions associated with urbanisation represent great challenges for wildlife. Behaviour and stress tolerance are considered of major importance in the adaptation to novel urban habitats and numerous studies already reported behavioural and stress response phenotypes associated with urbanisation, often suggesting they represented adaptations, while rarely demonstrating it. The main goal of this study was to test the adaptive nature of urban shifts in behavioural and stress-related traits, and by adaptive we mean phenotypic change favouring traits in the same direction as selection. Using 7 years of monitoring of urban and forest great tits, we first tested for differences in exploratory behaviour, aggressiveness and breath rate, between both habitats. Second, we performed habitat-specific analyses of selection on the three former traits using (a) reproductive success and (b) survival estimated via capture-mark-recapture models, as fitness estimates, to determine whether shifts in these behavioural and stress-related traits were aligned with patterns of ongoing selection. We found that urban birds displayed higher exploratory behaviour and aggressiveness, and higher breath rate, compared to forest birds. Selection analyses overall revealed that these shifts were not adaptive and could even be maladaptive. In particular, higher handling aggression and higher breath rate in urban birds was associated with lower fitness. Higher exploration scores were correlated with lower survival in both habitats, but higher reproductive success only in forest males. Overall, differences in patterns of selection between habitats were not consistent with the phenotypic divergence observed. Taken together, these results highlight that phenotypic shifts observed in cities do not necessarily result from new selection pressures and could be maladaptive. We hypothesise that divergences in behavioural traits for urban birds could result from the filtering of individuals settling in cities. We thus encourage urban evolutionary scientists to further explore the adaptive potential of behavioural traits measured in urban habitats (a) by replicating this type of study in multiple cities and species, (b) by implementing studies focusing on immigrant phenotypes and (c) by measuring selection at multiple life stages.

Caizergues AE ，Grégoire A ，Choquet R ，Perret S ，Charmantier A ... -  《-》

Urban versus forest ecotypes are not explained by divergent reproductive selection.

Increasing urbanization offers a unique opportunity to study adaptive responses to rapid environmental change. Numerous studies have demonstrated phenotypic divergence between urban and rural organisms. However, comparing the direction and magnitude of natural selection between these environments has rarely been attempted. Using seven years of monitoring of great tits (Parus major) breeding in nest-boxes across the city of Montpellier and in a nearby oak forest, we find phenotypic divergence in four morphological and two life-history traits between urban and forest birds. We then measure reproductive selection on these traits, and compare selection between the habitats. Urban birds had significantly smaller morphological features than their rural counterparts, with a shorter tarsus, lower body mass, and smaller wing and tail lengths relative to their overall body size. While urban female tarsus length was under stabilizing selection, and forest males show positive selection for tarsus length and negative selection for body mass, selection gradients were significantly divergent between habitats only for body mass. Urban great tits also had earlier laying dates and smaller clutches. Surprisingly, we found selection for earlier laying date in the forest but not in the city. Conversely, we detected no linear selection on clutch size in the forest, but positive selection on clutch size in the urban habitat. Overall, these results do not support the hypothesis that contemporary reproductive selection explains differences in morphology and life history between urban- and forest-breeding great tits. We discuss how further experimental approaches will help confirm whether the observed divergence is maladaptive while identifying the environmental drivers behind it.

Caizergues AE ，Grégoire A ，Charmantier A 《-》

Urbanisation-associated shifts in the avian metabolome within the annual cycle.

While organisms have evolved to cope with predictable changes in the environment, the rapid rate of current global change presents numerous novel and unpredictable stressors to which organisms have had less time to adapt. To persist in the urban environment, organisms must modify their physiology, morphology and behaviour accordingly. Metabolomics offers great potential for characterising organismal responses to natural and anthropogenic stressors at the systems level and can be applied to any species, even without genomic knowledge. Using metabolomic profiling of blood, we investigated how two closely related species of passerine bird respond to the urban environment. Great tits Parus major and blue tits Cyanistes caeruleus residing in urban and forest habitats were sampled during the breeding (spring) and non-breeding (winter) seasons across replicated sites in southern Sweden. During breeding, differences in the plasma metabolome between urban and forest birds were characterised by higher levels of amino acids in urban-dwelling tits and higher levels of fatty acyls in forest-dwelling tits. The suggested higher rates of fatty acid oxidation in forest tits could be driven by habitat-associated differences in diet and could explain the higher reproductive investment and success of forest tits. High levels of amino acids in breeding urban tits could reflect the lack of lipid-rich caterpillars in the urban environment and a dietary switch to protein-rich spiders, which could be of benefit for tackling inflammation and oxidative stress associated with pollution. In winter, metabolomic profiles indicated lower overall levels of amino acids and fatty acyls in urban tits, which could reflect relaxed energetic demands in the urban environment. Our metabolomic profiling of two urban-adapted species suggests that their metabolism is modified by urban living, though whether these changes represent adaptative or non-adaptive mechanisms to cope with anthropogenic challenges remains to be determined.

Watson H ，Nilsson JÅ ，Smith E ，Ottosson F ，Melander O ，Hegemann A ，Urhan U ，Isaksson C ... -  《-》

Great tits feed their nestlings with more but smaller prey items and fewer caterpillars in cities than in forests.

Rapidly increasing urbanisation is one of the most significant anthropogenic environmental changes which can affect demographic traits of animal populations, for example resulting in reduced reproductive success. The food limitation hypothesis suggests that the shortage of high-quality nestling food in cities is a major factor responsible for the reduced reproductive performance in insectivorous birds. To study this explanation, we collected data on the parental provisioning behaviour of urban and forest great tits (Parus major) in three years that varied both in caterpillar availability (the main food of great tit nestlings) and in reproductive success of the birds. In all years, urban parents provisioned caterpillars in a smaller proportion to their nestlings, but the total amount of food per nestling (estimated by the volumes of all prey items) did not differ between habitats. In the two years with much lower reproductive success in urban than forest habitats, urban parents had higher provisioning rates, but provided more non-arthropod food and brought smaller prey items than forest parents. In the year with reduced habitat difference in reproductive success, urban parents were able to compensate for the scarcity of caterpillars by provisioning other arthropods rather than non-arthropod food, and by delivering larger preys than in the other years. Specifically, in this latter year, caterpillars provisioned by urban pairs were cc. twice as large as in the other two years, and were similar in size to caterpillars provisioned in the forest broods. These results show that although urban great tit parents can provide the same quantity of food per nestling as forest parents by reducing their brood size and increasing the per capita feeding rates for nestlings, they cannot compensate fully for the scarcity of high-quality preys (caterpillars) in poor years. In some years, however, favourable conditions for urban caterpillar development can greatly reduce food limitation in cities, allowing urban birds to achieve higher reproductive success. We suggest that urban green areas designed and managed in a way to facilitate conditions for phytophagous arthropods could improve habitat quality for urban birds.

Sinkovics C ，Seress G ，Pipoly I ，Vincze E ，Liker A ... -  《Scientific Reports》

Repeatability and degree of territorial aggression differs among urban and rural great tits (Parus major).

Hardman SI ，Dalesman S 《-》