Toni Laaksonen

From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory

Background An understanding of the evolution of potential signals from plants to the predators of their herbivores may provide exciting examples of co-evolution among multiple trophic levels. Understanding the mechanism behind the attraction of predators to plants is crucial to conclusions about co-evolution. For example, insectivorous birds are attracted to herbivore-damaged trees without seeing the herbivores or the defoliated parts, but it is not known whether birds use cues from herbivore-damaged plants with a specific adaptation of plants for this purpose. Methodology We examined whether signals from damaged trees attract avian predators in the wild and whether birds could use volatile organic compound (VOC) emissions or net photosynthesis of leaves as cues to detect herbivore-rich trees. We conducted a field experiment with mountain birches (Betula pubescens ssp. czerepanovii), their main herbivore (Epirrita autumnata) and insectivorous birds. Half of the trees had herbivore larvae defoliating trees hidden inside branch bags and half had empty bags as controls. We measured predation rate of birds towards artificial larvae on tree branches, and VOC emissions and net photosynthesis of leaves. Principal Findings and Significance The predation rate was higher in the herbivore trees than in the control trees. This confirms that birds use cues from trees to locate insect-rich trees in the wild. The herbivore trees had decreased photosynthesis and elevated emissions of many VOCs, which suggests that birds could use either one, or both, as cues. There was, however, large variation in how the VOC emission correlated with predation rate. Emissions of (E)-DMNT [(E)-4,8-dimethyl-1,3,7-nonatriene], β-ocimene and linalool were positively correlated with predation rate, while those of highly inducible green leaf volatiles were not. These three VOCs are also involved in the attraction of insect parasitoids and predatory mites to herbivore-damaged plants, which suggests that plants may not have specific adaptations to signal only to birds.

Geographic patterns of genetic differentiation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca)

The pied flycatcher is one of the most phenotypically variable bird species in Europe. The geographic variation in phenotypes has often been attributed to spatial variation in selection regimes that is associated with the presence or absence of the congeneric collared flycatcher. Spatial variation in phenotypes could however also be generated by spatially restricted gene flow and genetic drift. We examined the genetic population structure of pied flycatchers across the breeding range and applied the phenotypic QST (PST)–FST approach to detect indirect signals of divergent selection on dorsal plumage colouration in pied flycatcher males. Allelic frequencies at neutral markers were found to significantly differ among populations breeding in central and southern Europe whereas northerly breeding pied flycatchers were found to be one apparently panmictic group of individuals. Pairwise differences between phenotypic (PST) and neutral genetic distances (FST) were positively correlated after removing the most differentiated Spanish and Swiss populations from the analysis, suggesting that genetic drift may have contributed to the observed phenotypic differentiation in some parts of the pied flycatcher breeding range. Differentiation in dorsal plumage colouration however greatly exceeded that observed at neutral genetic markers, which indicates that the observed pattern of phenotypic differentiation is unlikely to be solely maintained by restricted gene flow and genetic drift.

A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels

Melanin pigments are responsible for most non-structural brown, black and grey colouration in animals. The extent to which melanin-based colouration in birds is genetically or environmentally determined has been subject to controversy. One reason for this it is paucity of empirical data on the role of key environmental factors, such as food availability, on the development of melanin-based traits. We analysed whether brown and grey colouration in rumps of Eurasian kestrels Falco tinnunculus is based on melanin and examined the relationships between high inter-annual variation in main food supply, parental condition and the expression of grey colouration in male nestlings. We also performed a partial cross-fostering experiment to allocate randomly nestlings among environments. The proportion of male nestlings with predominantly grey colouration was higher in years with abundant prey (voles). The only variable associated with intra-annual variation of grey colouration in male nestlings was body mass of the female rearing them. The colouration of nestlings in the cross-foster experiment was correlated with the body mass of their foster mother, but not with that of their genetic mother. Melanin colouration did not correlate with T-cell mediated immune response. These results indicate that this melanin-based trait reflects the environmental conditions in which the nestlings grew up.

Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators

The tritrophic interactions between plants, herbivores and avian predators are complex and prone to trophic cascades. We conducted a meta-analysis of original articles that have studied birds as predators of invertebrate herbivores, to compare top-down trophic cascades with different plant responses from different environments and climatic areas. Our search found 29 suitable articles, with a total of 81 separate experimental study set-ups. The meta-analysis revealed that plants benefited from the presence of birds. A significant reduction was observed in the level of leaf damage and plant mortality. The presence of birds also positively affected the amount of plant biomass, whereas effects on plant growth were negligible. There were no differences in the effects between agricultural and natural environments. Similarly, plants performed better in all climatic areas (tropical, temperate and boreal) when birds were present. Moreover, both mature plants and saplings gained benefits from the presence of birds. Our results show that birds cause top-down trophic cascades and thus they play an integral role in ecosystems.

Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca).

The hormonal environment during early development, such as maternally derived androgens in bird eggs, shapes the development and phenotype of the offspring in ways that may have important long-term consequences for behaviour. We studied the effects of yolk androgens on multiple behavioural traits in female and male pied flycatchers (Ficedula hypoleuca) by experimentally elevating androgen levels (testosterone and androstenedione) in the eggs. The birds were housed in a common-garden environment in captivity until full independence, after which their behaviour was tested. We found that androgen-treated males were more likely than control males to explore a novel environment and showed higher activity in the presence of a novel object. In response to a simulated predator attack, androgen-treated males mainly showed freezing behaviour, while control males showed escape behaviour. Females from the androgen treatment and control group showed no differences in these behaviours. Androgen treatment did not affect neophobia (latency to approach the novel object) or dominance behaviour in either sex. Behaviour in the novel environment and towards a novel object was repeatable, but behaviours in the different experiments were mostly not inter-correlated. These results indicate that yolk androgens have various long-lasting effects on behaviour, especially in males, but that they do not induce a distinct behavioural syndrome. As behaviour is strongly linked with fitness, our results suggest that yolk androgens may play a role in determining fitness, and thus play a potentially adaptive role.

Geographical variation in egg mass and egg content in a passerine bird.

Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

Female field voles with high testosterone and glucose levels produce male-biased litters

The proximate physiological mechanisms producing the parental ability to vary offspring sex ratio in many vertebrates remain elusive. Recently, high concentrations of maternal testosterone and glucose and low concentrations of maternal corticosterone have been suggested to explain male bias in offspring sex ratio. We examined how these factors affect secondary offspring sex ratio in nondomesticated field voles, Microtus agrestis, while controlling for maternal age, testosterone level of the male and body condition of both the female and the male. We found that females with high preconception serum testosterone and glucose levels produced a male-biased litter, whereas there was no association between maternal corticosterone level and litter sex ratio. Older females produced a bias towards sons, but neither their body condition nor paternal testosterone level correlated with litter sex ratio. Finally, females mated with a high body-condition male tended to deliver a male-biased litter. Our results suggest that several physiological traits of the mother may simultaneously be related to offspring sex ratio in mammals.

Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher

To understand how sexual selection works, it is important to distinguish between the mechanisms underlying mating success. One of the basic questions is to differentiate between the importance of territory-related resources (gained through male–male competition) and male quality in female choice. Few studies, however, have tried to separate these two often intercorrelated variables. We randomized territory quality among male pied flycatchers, Ficedula hypoleuca , and studied which male traits were associated with their success in female mate choice. Females appeared to choose multiple male traits in the wild when the males were not allowed to choose territories before female choice for males. Males with a long tarsus, large white wing patch and versatile song were favoured by females. In addition, the contrast of ultraviolet (UV) reflectance in the white wing patch relative to its background, that is, the dorsal brown-black coloration of the males, appeared to be an important mate choice cue. The UV reflectance had a stronger effect on pairing success in dark males than in brown ones. An experimental manipulation of the UV reflectance revealed that the UV coloration of the males appeared to be used in female choice early but not late in the pairing season, which suggests time-dependent plasticity in female choice. Our study thus exemplifies the complexity of mate choice; it is both temporally constrained and dependent on multiple ornaments.

Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca

Extrapair paternity may create marked variation in the reproductive success of males and thus contribute to the evolution of sexually selected traits in socially monogamous mating systems. We examined the distribution of extrapair paternity in a passerine bird, the pied flycatcher, in relation to plumage coloration and male age. The frequency of extrapair paternity was found to be low in our study population in Southwest Finland (38 of 857 (4.4%) offspring in 25 of 191 (13%) broods). We were able to identify the sire for 53% of the extrapair young and in each case the extrapair sire was at least 2 years old. The probability of siring extrapair young was not associated with pigment-based brown-black dorsal plumage coloration, structural ultraviolet (UV) coloration or forehead patch size. The probability of being cuckolded, however, increased with decreasing UV chroma of the white wing patch. Our results thus indicate that there are multiple factors influencing when and with whom females engage in extrapair copulations. They also indicate that the male traits influencing the decision to cuckold the social mate are different from those used for choosing an extrapair mate.