Mihai Valcu

Artificial Night Lighting Affects Dawn Song, Extra-Pair Siring Success, and Lay Date in Songbirds

Associated with a continued global increase in urbanization, anthropogenic light pollution is an important problem. However, our understanding of the ecological consequences of light pollution is limited. We investigated effects of artificial night lighting on dawn song in five common forest-breeding songbirds. In four species, males near street lights started singing significantly earlier at dawn than males elsewhere in the forest, and this effect was stronger in naturally earlier-singing species. We compared reproductive behavior of blue tits breeding in edge territories with and without street lights to that of blue tits breeding in central territories over a 7 year period. Under the influence of street lights, females started egg laying on average 1.5 days earlier. Males occupying edge territories with street lights were twice as successful in obtaining extra-pair mates than their close neighbors or than males occupying central forest territories. Artificial night lighting affected both age classes but had a stronger effect on yearling males. Our findings indicate that light pollution has substantial effects on the timing of reproductive behavior and on individual mating patterns. It may have important evolutionary consequences by changing the information embedded in previously reliable quality-indicator traits.

Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds?

Among vertebrates, the sense of smell is mediated by olfactory receptors (ORs) expressed in sensory neurons within the olfactory epithelium. Comparative genomic studies suggest that the olfactory acuity of mammalian species correlates positively with both the total number and the proportion of functional OR genes encoded in their genomes. In contrast to mammals, avian olfaction is poorly understood, with birds widely regarded as relying primarily on visual and auditory inputs. Here, we show that in nine bird species from seven orders (blue tit, Cyanistes caeruleus; black coucal, Centropus grillii; brown kiwi, Apteryx australis; canary, Serinus canaria; galah, Eolophus roseicapillus; red jungle fowl, Gallus gallus; kakapo, Strigops habroptilus; mallard, Anas platyrhynchos; snow petrel, Pagodroma nivea), the majority of amplified OR sequences are predicted to be from potentially functional genes. This finding is somewhat surprising as one previous report suggested that the majority of OR genes in an avian (red jungle fowl) genomic sequence are non-functional pseudogenes. We also show that it is not the estimated proportion of potentially functional OR genes, but rather the estimated total number of OR genes that correlates positively with relative olfactory bulb size, an anatomical correlate of olfactory capability. We further demonstrate that all the nine bird genomes examined encode OR genes belonging to a large gene clade, termed γ-c, the expansion of which appears to be a shared characteristic of class Aves. In summary, our findings suggest that olfaction in birds may be a more important sense than generally believed.

Adaptive Sleep Loss in Polygynous Pectoral Sandpipers

You Snooze, You Lose Sleep serves restorative and memory functions, but it does not always operate analogously across species. Deferral of sleep may be possible when selection strongly favors the awake. Lesku et al. (p. 1654; see the Perspective by Siegel) show that sleep may be deferred without cost or impairment in pectoral sandpipers. These birds breed collectively in the high Arctic, and male competition is intense. Competing for, and displaying to, females are both physically and cognitively demanding, yet birds who slept the least showed no decrease in their ability to perform these activities. Indeed, those males who slept the least obtained the most matings and sired the most offspring. Male pectoral sandpipers go without sleep for days in order to mate as often as possible in the high Arctic. The functions of sleep remain elusive. Extensive evidence suggests that sleep performs restorative processes that sustain waking brain performance. An alternative view proposes that sleep simply enforces adaptive inactivity to conserve energy when activity is unproductive. Under this hypothesis, animals may evolve the ability to dispense with sleep when ecological demands favor wakefulness. Here, we show that male pectoral sandpipers (Calidris melanotos), a polygynous Arctic breeding shorebird, are able to maintain high neurobehavioral performance despite greatly reducing their time spent sleeping during a 3-week period of intense male-male competition for access to fertile females. Males that slept the least sired the most offspring. Our results challenge the view that decreased performance is an inescapable outcome of sleep loss.

A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

Inbreeding depression, as commonly found in natural populations, should favour the evolution of inbreeding avoidance mechanisms. If natal dispersal, the first and probably most effective mechanism, does not lead to a complete separation of males and females from a common origin, a small‐scale genetic population structure may result and other mechanisms to avoid inbreeding may exist. We studied the genetic population structure and individual mating patterns in blue tits (Parus caeruleus). The population showed a local genetic structure in two out of four years: genetic relatedness between individuals (estimated from microsatellite markers) decreased with distance. This pattern was mainly caused by immigrants to the study area; these, if paired with fellow immigrants, were more related than expected by chance. Since blue tits did not avoid inbreeding with their social partner, we examined if individuals preferred less related partners at later stages of the mate choice process. We found no evidence that females or males avoided inbreeding through extra‐pair copulations or through mate desertion and postbreeding dispersal. Although the small‐scale genetic population structure suggests that blue tits could use a simple rule of thumb to select less related mates, females did not generally prefer more distantly breeding extra‐pair partners. However, the proportion of young fathered by an extra‐pair male in mixed paternity broods depended on the genetic relatedness with the female. This suggests that there is a fertilization bias towards less related copulation partners and that blue tits are able to reduce the costs of inbreeding through a postcopulatory process.

The effects of life history and sexual selection on male and female plumage colouration

Classical sexual selection theory provides a well-supported conceptual framework for understanding the evolution and signalling function of male ornaments. It predicts that males obtain greater fitness benefits than females through multiple mating because sperm are cheaper to produce than eggs. Sexual selection should therefore lead to the evolution of male-biased secondary sexual characters. However, females of many species are also highly ornamented. The view that this is due to a correlated genetic response to selection on males was widely accepted as an explanation for female ornamentation for over 100 years and current theoretical and empirical evidence suggests that genetic constraints can limit sex-specific trait evolution. Alternatively, female ornamentation can be the outcome of direct selection for signalling needs. Since few studies have explored interspecific patterns of both male and female elaboration, our understanding of the evolution of animal ornamentation remains incomplete, especially over broad taxonomic scales. Here we use a new method to quantify plumage colour of all ~6,000 species of passerine birds to determine the main evolutionary drivers of ornamental colouration in both sexes. We found that conspecific male and female colour elaboration are strongly correlated, suggesting that evolutionary changes in one sex are constrained by changes in the other sex. Both sexes are more ornamented in larger species and in species living in tropical environments. Ornamentation in females (but not males) is increased in cooperative breeders—species in which female–female competition for reproductive opportunities and other resources related to breeding may be high. Finally, strong sexual selection on males has antagonistic effects, causing an increase in male colouration but a considerably more pronounced reduction in female ornamentation. Our results indicate that although there may be genetic constraints to sexually independent colour evolution, both female and male ornamentation are strongly and often differentially related to morphological, social and life-history variables.

When the sun never sets: diverse activity rhythms under continuous daylight in free-living arctic-breeding birds

Circadian clocks are centrally involved in the regulation of daily behavioural and physiological processes. These clocks are synchronized to the 24 h day by external cues (Zeitgeber), the most important of which is the light–dark cycle. In polar environments, however, the strength of the Zeitgeber is greatly reduced around the summer and winter solstices (continuous daylight or continuous darkness). How animals time their behaviour under such conditions has rarely been studied in the wild. Using a radio-telemetry-based system, we investigated daily activity rhythms under continuous daylight in Barrow, Alaska, throughout the breeding season in four bird species that differ in mating system and parental behaviour. We found substantial diversity in daily activity rhythms depending on species, sex and breeding stage. Individuals exhibited either robust, entrained 24 h activity cycles, were continuously active (arrhythmic) or showed ‘free-running’ activity cycles. In semipalmated sandpipers, a shorebird with biparental incubation, we show that the free-running rhythm is synchronized between pair mates. The diversity of diel time-keeping under continuous daylight emphasizes the plasticity of the circadian system, and the importance of the social and life-history context. Our results support the idea that circadian behaviour can be adaptively modified to enable species-specific time-keeping under polar conditions.

Light pollution alters the phenology of dawn and dusk singing in common European songbirds

Artificial night lighting is expanding globally, but its ecological consequences remain little understood. Animals often use changes in day length as a cue to time seasonal behaviour. Artificial night lighting may influence the perception of day length, and may thus affect both circadian and circannual rhythms. Over a 3.5 month period, from winter to breeding, we recorded daily singing activity of six common songbird species in 12 woodland sites, half of which were affected by street lighting. We previously reported on analyses suggesting that artificial night lighting affects the daily timing of singing in five species. The main aim of this study was to investigate whether the presence of artificial night lighting is also associated with the seasonal occurrence of dawn and dusk singing. We found that in four species dawn and dusk singing developed earlier in the year at sites exposed to light pollution. We also examined the effects of weather conditions and found that rain and low temperatures negatively affected the occurrence of dawn and dusk singing. Our results support the hypothesis that artificial night lighting alters natural seasonal rhythms, independently of other effects of urbanization. The fitness consequences of the observed changes in seasonal timing of behaviour remain unknown.

Causes and consequences of breeding dispersal and divorce in a blue tit, Cyanistes caeruleus, population

In socially monogamous species with a resource-based mating system, mate choice and territory choice cannot easily be separated. We studied the occurrence and consequences of postbreeding dispersal and divorce in a population of blue tits breeding in nestboxes. Dispersal was defined relative to the spatial position of territories estimated as Dirichlet tiles. Although more than 80% of males and females changed nestbox between breeding seasons, only 3% of males and 25% of females moved to a new territory. Settlement following postbreeding dispersal was driven by habitat quality: dispersing females ended up in territories with higher clutch size expectancy. Dispersed females (both widowed and divorced) reared more fledglings than resident ones, suggesting that dispersal is adaptive. Our results suggest that even at relatively small spatial scales and in continuous habitats, postbreeding dispersal may be driven by habitat quality gradients. Across all years, 53% of surviving pairs divorced. We assessed the effects of mate change independently of territory quality, by restricting analyses to resident individuals that, after divorce, shared a part of their former territory or settled in its close vicinity. Reproductive success increased for males after divorce, but decreased for females. It did not change for reunited pairs in subsequent seasons. Paternity loss or gain through extrapair copulations, and hence overall siring success, did not differ between divorced and reunited males, either before divorce or pair re-formation, or in the year after. After divorce, males but not females paired with larger, presumably higher-quality partners. The results support the better option hypothesis and suggest that males, but not females, may benefit from divorce. However, our results are also compatible with the alternative hypothesis that divorce is driven by female–female competition, whereby a dominant female evicts the former mate.

Spatial autocorrelation: an overlooked concept in behavioral ecology

Spatial autocorrelation (SAC) is the dependence of a given variable’s values on the values of the same variable recorded at neighboring locations (Cliff and Ord 1973; Fortin and Dale 2005). When high values are associated with relatively high values at neighboring locations, SAC is said to be positive and, conversely, where high values correspond to relatively low values at neighboring locations, SAC is negative. SAC can be a property of the variable itself (inherent or intrinsic SAC) or it can arise due to the dependence of the variable of interest on another spatially autocorrelated variable (induced SAC) (Legendre et al. 2002; Fortin and Dale 2005). Because it lies at the core of most spatial models, SAC is a fundamental concept of spatial analysis (Getis 2008). During the last 2 decades, mostly after Pierre Legendre published his seminal paper ‘‘Spatial autocorrelation: trouble or new paradigm’’ (Legendre 1993), SAC received considerable attention from ecologists—in particular biogeographers investigating macroecological patterns of species distributions (Kissling and Carl 2008)—and from population geneticists investigating small-scale spatial genetic structure of populations (Guillot et al. 2009). These circumstances prompted Arthur Getis, in a review on the evolution of the SAC concept, to conclude that ‘‘Nearly all the major journals that concern themselves with the ecological aspects of their subjects print articles having a spatial autocorrelation foundation’’ (Getis 2008). In stark contrast, the issue of SAC has hitherto been largely ignored in behavioral ecology, despite the fact that many studies in this field deal with a spatial component. Thus, despite its recognized importance in adjacent fields of ecological research, even very basic topics in behavioral ecology remain unexplored with respect to SAC, and we could only find a handful of studies (van der Jeugd and McCleery 2002; Laiolo and Tella 2006; Duraes et al. 2007; Aarts et al. 2008; Giesselmann et al. 2008; Holdo et al. 2009), which included SAC in their research paradigm. The general aim of this paper is to draw the attention of behavioral ecologists to the phenomenon of SAC. Specifically, we aim 1) to provide examples of spatially autocorrelated variables, indicating that SAC is widespread in variables commonly used in behavioral ecology studies, 2) to show why it is important to take SAC into account, and 3) to point to some tools to explore and model it.

Unexpected diversity in socially synchronized rhythms of shorebirds

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1–19 h, whereas period length—the time in which a parent’s probability to incubate cycles once between its highest and lowest value—varied from 6–43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light–dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.