Gábor Markó

The geography of fear: a latitudinal gradient in anti-predator escape distances of birds across Europe

All animals flee from potential predators, and the distance at which this happens is optimized so the benefits from staying are balanced against the costs of flight. Because predator diversity and abundance decreases with increasing latitude, and differs between rural and urban areas, we should expect escape distance when a predator approached the individual to decrease with latitude and depend on urbanization. We measured the distance at which individual birds fled (flight initiation distance, FID, which represents a reliable and previously validated surrogate measure of response to predation risk) following a standardized protocol in nine pairs of rural and urban sites along a ca. 3000 km gradient from Southern Spain to Northern Finland during the breeding seasons 2009–2010. Raptor abundance was estimated by means of standard point counts at the same sites where FID information was recorded. Data on body mass and phylogenetic relationships among bird species sampled were extracted from the literature. An analysis of 12,495 flight distances of 714 populations of 159 species showed that mean FID decreased with increasing latitude after accounting for body size and phylogenetic effects. This decrease was paralleled by a similar cline in an index of the abundance of raptors. Urban populations had consistently shorter FIDs, supporting previous findings. The difference between rural and urban habitats decreased with increasing latitude, also paralleling raptor abundance trends. Overall, the latitudinal gradient in bird fear was explained by raptor abundance gradients, with additional small effects of latitude and intermediate effects of habitat. This study provides the first empirical documentation of a latitudinal trend in anti-predator behavior, which correlated positively with a similar trend in the abundance of predators.

Oxidative damage and plasma antioxidant capacity in relation to body size, age, male sexual traits and female reproductive performance in the collared flycatcher (Ficedula albicollis)

The study of oxidative stress is a potential tool for studying the functional interactions among life history traits, sexual traits and physiological status in animals. In this study, we investigated relationships between measures of plasma oxidative status and male sexual traits, female reproductive investment and three other life history traits, in a wild population of collared flycatchers (Ficedula albicollis). Flycatcher males with a larger white forehead patch had higher level of plasma antioxidant capacity. For females, clutch size was not associated with plasma oxidative status, but egg size was positively correlated with antioxidant capacity. The relationship between age and levels of plasma oxidative damage remains controversial in this species: young female flycatchers showed higher levels of hydroperoxides compared to antioxidants, whereas age did not predict oxidative status of males. Males had higher levels of oxidative damage than females, although the concentration of antioxidant compounds was similar between the sexes. Females that mated with more ornamented males had higher plasma antioxidant capacity. Our results suggest that, for males and females, greater investment in sexual signal and reproduction, respectively, does not reduce the capacity for self-maintenance or avoidance of oxidative stress. Finally, our data support indirectly the occurrence of assortative mating in our species, since females with higher plasma antioxidant capacity mated with more ornamented males.

Urbanized birds have superior establishment success in novel environments

Many animals have adapted to the proximity of humans and thereby gained an advantage in a world increasingly affected by human activity. Numerous organisms have invaded novel areas and thereby increased their range. Here, we hypothesize that an ability to thrive in urban habitats is a key innovation that facilitates successful establishment and invasion. We test this hypothesis by relating the probability of establishment by birds on oceanic islands to the difference in breeding population density between urban and nearby rural habitats as a measure of urbanization in the ancestral range. This measure was the single-most important predictor of establishment success and the only statistically significant one, with additional effects of sexual dichromatism, number of releases and release effort, showing that the ability to cope with human proximity is a central component of successful establishment. Because most invasions occur as a consequence of human-assisted establishment, the ability to cope with human proximity will often be of central importance for successful establishment.

Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population

When mean behaviors correlate among individuals, they form behavioral syndromes. One way to understand the evolution of such a group-level phenomenon is to compare horizontally patterns of correlations among populations (or species) or follow longitudinally the same population over years in the light of parallel differences in the environment. We applied the longitudinal approach to 8-year field data and analyzed phenotypic correlations, and their within- and between-individual components, among three behaviors (novelty avoidance, aggression, and risk-taking) in male collared flycatchers, Ficedula albicollis, in a meta-analytic framework. The phenotypic correlation between novelty avoidance and aggression varied heterogeneously (it was positive in some years, while it was negative in other years), while the other pair-wise correlations were consistently positive over the study period. We investigated four potential socio-ecological factors, and found evidence that the among-year alterations in the demographic structure of the population (density, age composition) can be responsible for the heterogeneous effect sizes. Comparing within- and between-individual correlations across pairs of traits, we found that the correlation between aggression and risk-taking at the among-individual level was the strongest suggesting that this relationship has the highest potential to form a behavioral syndrome. Within-year repeatabilities varied among traits, but were systematically higher than between-year repeatabilities. Our study highlights on an empirical basis that there can be several biological and statistical reasons behind detecting a phenotypic correlation in a study, but only few of these imply that fixed behavioral syndromes are maintained in a natural population. In fact, some correlations seem to be shaped by environmental fluctuations.

Essential oil yield and composition reflect browsing damage of junipers

The impact of browsing on vegetation depends on the relative density and species composition of browsers. Herbivore density and plant damage can be either site-specific or change seasonally and spatially. For juniper (Juniperus communis) forests of a sand dune region in Hungary, it has been assumed that plant damage investigated at different temporal and spatial scales would reflect selective herbivory. The level of juniper damage was tested for a possible correlation with the concentration of plant secondary metabolites (PSMs) in plants and seasonal changes in browsing pressure. Heavily browsed and nonbrowsed junipers were also assumed to differ in their chemical composition, and the spatial distribution of browsing damage within each forest was analyzed to reveal the main browser. Long-term differences in local browsing pressure were also expected and would be reflected in site-specific age distributions of distant juniper populations. The concentrations of PSMs (essential oils) varied significantly among junipers and seasons. Heavily browsed shrubs contained the lowest oil yield; essential oils were highest in shrubs bearing no damage, indicating that PSMs might contribute to reduce browsing in undamaged shrubs. There was a seasonal fluctuation in the yield of essential oil that was lower in the summer period than in other seasons. Gas chromatography (GC) revealed differences in some essential oil components, suggesting that certain chemicals could have contributed to reduced consumption. The consequential long-term changes were reflected in differences in age distribution between distant juniper forests. These results confirm that both the concentration of PSMs and specific compounds of the essential oil may play a role in selective browsing damage by local herbivores.

The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher

There is increasing evidence that the genetic architecture of exploration behavior includes the dopamine receptor D4 gene (DRD4). Such a link implies that the within-individual consistency in the same behavior has a genetic basis. Behavioral consistency is also prevalent in the form of between-individual correlation of functionally different behaviors; thus, the relationship between DRD4 polymorphism and exploration may also be manifested for other behaviors. Here, in a Hungarian population of the collared flycatcher, Ficedula albicollis, we investigate how males with distinct DRD4 genotypes differ in the consistent elements of their behavioral displays during the courtship period. In completely natural conditions, we assayed novelty avoidance, aggression and risk-taking, traits that were previously shown repeatable over time and correlate with each other, suggesting that they could have a common mechanistic basis. We identified two single-nucleotide polymorphisms (SNP554 and SNP764) in the exon 3 of the DRD4 gene by sequencing a subsample, then we screened 202 individuals of both sexes for these SNPs. Focusing on the genotypic variation in courting males, we found that “AC” heterozygote individuals at the SNP764 take lower risk than the most common “AA” homozygotes (the “CC” homozygotes were not represented in our subsample of males). We also found a considerable effect size for the relationship between SNP554 polymorphism and novelty avoidance. Therefore, in addition to exploration, DRD4 polymorphisms may also be associated with the regulation of behaviors that may incur fear or stress. Moreover, polymorphisms at the two SNPs were not independent indicating a potential role for genetic constraints or another functional link, which may partially explain behavioral correlations.

Nest material selection affects nest insulation quality for the European ground squirrel (Spermophilus citellus)

Abstract Natural nests of the European ground squirrel (Spermophilus citellus) are constructed almost exclusively of fresh fescue (Festuca pseudovina: Poaceae). We performed laboratory experiments to understand the functional significance of preference of wild squirrels for nest material. We examined the factors contributing to nest quality by monitoring the construction and analyzing the composition of squirrel nests. As in the wild, squirrels showed strong preference for fescue during the laboratory tests and preferred fresh material to dry material. Because preference for fresh material was not expected, because high water content reduces insulation, we manipulated the moisture content of nests made from either fresh or dry fescue to determine how nest quality and moisture level contribute to insulation. We found that the insulation property of fresh grass nests was superior to nests constructed from dry grass only. Intracellular water in the nest material did not affect thermal conductance and insulation significantly. We concluded that fresh fescue provided a more flexible material that allows squirrels to construct nests with better insulation under both field and laboratory conditions.

Morphology and function of communal mounds of overwintering mound-building mice (Mus spicilegus)

Mound-building mice (Mus spicilegus) construct large mounds of soil and plant material in autumn, where juvenile animals overwinter in groups without reproducing. The mounds have several functions, including food storage, thermoregulation, and protection from predators. We examined whether these mounds have food storage or thermoregulatory function. Mice used mainly seeds and ears of certain plants (Echinochloa sp., Chenopodium spp., and Setaria spp., depending on availability) as building materials, but microhistological analysis of mice feces revealed that the cached plants are not represented in their actual diet. By comparing the features of soil under the mound to neighboring random points we found that the mounds have water-insulating and thermoregulatory properties. We also found a positive correlation between the size of the mound, its vegetal content, and its effectiveness to lessen the impact of the harsh conditions of the outside environment. Mound size was dependent on the number of inhabitants, indicating that larger mounds are constructed by and shelter bigger groups. The existence of communal mound building thus can contribute greatly to successful overwintering and the relatively low fluctuation in population size in this species.

Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher

The possible integration of different sexual ornaments into a composite system, and especially the information content of such ornament complexes, is poorly investigated. Many bird species display complex plumage coloration, but whether this represents one integrated or several independent sexual traits can be unclear. Collared flycatchers (Ficedula albicollis) display melanised and depigmented plumage areas, and the spectral features (brightness and UV chroma) of these are correlated with each other across the plumage. In a 5-year dataset of male and female plumage reflectance, we examined some of the potential information content of integrated, plumage-level colour attributes by estimating their relationships to previous and current year body condition, laying date and clutch size. Females were in better condition the year before they became darker pigmented, and males in better current year condition were also darker pigmented. Female pigment-based brightness was positively, while male structurally based brightness was negatively related to current laying date. Finally, the overall UV chroma of white plumage areas in males was positively associated with current clutch size. Our results show that higher degree of pigmentation is related to better condition, while the structural colour component is associated with some aspects of reproductive investment. These results highlight the possibility that correlated aspects of a multiple plumage ornamentation system may reflect together some aspects of individual quality, thereby functioning as a composite signal.

Rural-Urban Differences in Escape Behavior of European Birds across a Latitudinal Gradient

Behavioral adjustment is a key factor that facilitates species’ coexistence with humans in a rapidly urbanizing world. Because urban animals often experience reduced predation risk compared to their rural counterparts, and because escape behaviour is energetically costly, we expect that urban environments will select for increased tolerance to humans. Many studies have supported this expectation by demonstrating that urban birds have reduced flight initiation distance (FID = predator-prey distance when escape by the prey begins) than rural birds. Here we advanced this approach and, for the first time, assessed how 32 species of birds, found in 92 paired urban-rural populations, along a 3,900 km latitudinal gradient across Europe, changed their predation risk assessment and escape strategy as a function of living in urban areas. We found that urban birds took longer than rural birds to be alerted to human approaches, and urban birds tolerated closer human approach than rural birds. While both rural and urban populations take longer to be aware of an approaching human as latitude increased, this behavioral change with latitude is more intense in urban birds (for a given unit of latitude, urban birds increased their distance more than rural birds). We also found that as mean alert distance was shorter, urban birds escaped more quickly from approaching humans, but there was no such a relationship in rural populations. Although both rural and urban populations tended to escape more quickly as latitude increased, urban birds delayed their escape more at low latitudes when compared with rural birds. These results suggest that urban birds in Europe live under lower predation risk than their rural counterparts. Furthermore, the patterns found in our study indicate that birds prioritize the reduction of on-going monitoring costs when predation risk is low. We conclude that splitting escape variables into constituent components may provide additional and complementary information on the underlying causes of escape. This new approach is essential for understanding, predicting, and managing wildlife in a rapidly urbanizing world.