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.     

Anti-herbivore strategies in mountain birch at the tree-line

Birch forest on the slope of the Jesnalvaara fell forms a gradient ranging from 7–8 m high trees (at 75 m a.s.l.) to birch shrubs less than 1 m high at the top of the fell (330 m a.s.l.). Upper parts of the forest (above 220 m) were defoliated by Oporinia autumnata (Lep., Geometridae) about ten years ago and, with the exception of the top, only a fraction of birches have recovered. Climatic conditions explain the limitation of the damaged area – Oporinia eggs were killed during cold winters. Predators may also limit the damage. Defensive mechanisms in the birch leaves – especially a low nitrogen content and high concentrations of phenols inhibiting trypsin – can slow down an increase in herbivore density by reducing their reproductive capacity. Birch leaves from the lower limit of the damaged area are least suitable for the growth of herbivores. They have the highest concentration of phenols, too. Birches at the foot of Jesnalvaara are able to increase leaf phenols after mechanical damage of nearby leaves. This is enough to retard the growth of several herbivore species. Ability to recover after defoliation is an important part of the anti-herbivore strategy of the birch. This ability is higher in shrub birches than in tall trees and better after a warm than a cold summer. Birch leaves in the year following defoliation are less usable for herbivores and cause increased mortality and lowered reproduction. These properties are the weakest in birches at the foot of Jesnalvaara where the probability of being defoliated is also lowest.     

Coping with fast climate change in northern ecosystems: mechanisms underlying the population‐level response of a specialist avian predator

Northern ecosystems are facing unprecedented climate modifications, which pose a major threat for arctic species, especially the specialist predator guild. However, the mechanisms underlying responses of predators to climate change remain poorly understood. Climate can influence fitness parameters of predators either through reduced reproduction or survival following adverse weather conditions, or via changes in the population dynamics of their main prey. Here, we combined three overlapping long‐term datasets on the breeding density and parameters of a rodent‐specialist predator, the rough‐legged buzzard Buteo lagopus, its main prey population dynamics and climate variables, collected in subarctic areas of Finland and Norway, to assess the impact of changing climate on the predator reproductive response. Rough‐legged buzzards responded to ongoing climate change by advancing their laying date (0.1 d yr^?1 over the 21 yr of the study period), as a consequence of earlier snowmelt. However, we documented for the same period a decrease in breeding success, which principally resulted from an indirect effect of changes in the dynamics of their main prey, i.e. grey‐sided voles Microtus oeconomus, and not from the expected negative effect of unfavorable weather conditions during the brood‐rearing period on nestling survival. Additionally, we showed the striking impact of autumn and winter weather conditions on vole population growth rates in subarctic ecosystems, with a strong positive correlation between mean snow depth in autumn and winter and both winter and summer population growth rates. Our results highlighted that, in northern ecosystems, ongoing climate change has the potential to impact specialist predator species through two mechanistic linkages, which may in the long‐run, threaten the viability of their populations, and lead to potential severe cascading trophic effects at the ecosystem level.     

Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature?

Earlier studies have suggested that insectivorous birds, similar to invertebrate predators and parasitoids, may be guided by herbivore-induced plant volatiles (HIPVs) to damaged, herbivore-rich trees. Recent studies have also shown that birds use olfaction more than previously thought, underlying the potential for HIPVs to be sensed by insectivorous birds and utilised during foraging for prey. The HIPV production in plants is mediated, at least partly, by the jasmonic acid signalling pathway, and similar HIPVs to those induced by herbivores can often be induced by exposing plants to methyl jasmonate (MeJa). We studied the effects of MeJa on volatile emission and bird attraction using mature mountain birches (Betula pubescens ssp. czerepanovii) under natural conditions in northern Finland. Experimental trees were assigned to four treatment groups: herbivore-damaged [autumnal moth (Epirrita autumnata)], higher dose of MeJa (30 mM), lower dose of MeJa (15 mM) and control. All trees had three branches covered with mesh bags, but there were larvae inside the bags only of the herbivore-damage treatment. Bird predation rate was monitored with artificial plasticine larvae which were checked daily for peck marks. Birds most often pecked the larvae in the herbivore-damaged trees, but the attractiveness of MeJa-treated trees did not differ from the control. High within-treatment variation in systemic HIPV emissions probably masked MeJa treatment effects. The bird predation rate was high in birches that emitted large amounts of α-pinene. Thus, α-pinene may be one cue used by birds to find herbivore-rich birches.     

Increasing vole numbers cause more lethal damage to saplings in tree monocultures than in mixed stands

Overall, mammalian herbivores are more harmful in mixed plantations than in monocultures, but the effect of herbivore abundance has not been experimentally tested in this context. It has been proposed that there is a critical threshold density where herbivore pressure spreads from preferred plants to everything edible, leading to non-linear density effects on low-quality plants. We experimentally investigated whether survival of an unpalatable plant is similarly related to herbivore density in both monocultures and mixed stands. This we did by establishing monocultures of unpalatable black alder (Alnus glutinosa) and mixed stands of black alder and five more palatable tree species in enclosures, where Microtus voles were introduced and their abundances monitored.The effect of stand diversity tended to depend on vole abundance. Vole damage of tree saplings did not differ between monocultures and mixed stands, but at higher vole abundances attacks had a stronger effect on sapling survival in the monocultures. Sapling survival showed a significant drop in the monocultures at peak abundance of approximately 300 voles ha^?1. In monocultures herbivores do not have alternatives and therefore are forced to become deadlier consumers.     

The difference between generalist and specialist: the effects of wide fluctuations in main food abundance on numbers and reproduction of two co-existing predators

Specialist individuals within animal populations have shown to be more efficient foragers and/or to have higher reproductive success than generalist individuals, but interspecific reproductive consequences of the degree of diet specialisation in vertebrate predators have remained unstudied. Eurasian pygmy owls (hereafter POs) have less vole-specialised diets than Tengmalm's owls (TOs), both of which mainly subsist on temporally fluctuating food resources (voles). To test whether the specialist TO is more limited by the main prey abundance than the generalist PO, we studied breeding densities and reproductive traits of co-existing POs and TOs in central-western Finland during 2002–2019. Breeding densities of POs increased with augmenting densities of voles in the previous autumn, whereas breeding densities of TOs increased with higher vole densities in both the previous autumn and the current spring. In years of vole scarcity, PO females started egg-laying earlier than TOs, whereas in years of vole abundance TO females laid eggs substantially earlier than PO females. The yearly mean clutch size and number of fledglings produced of both POs and TOs increased with abundance of voles in the current spring. POs laid large clutches and produced large broods in years of both high and low vole abundance, whereas TOs were able to do so only in years of high vole abundance. POs were able to raise on average 73% of the eggs to fledglings whereas TOs only 44%. The generalist foraging strategy of POs including flexible switching from main prey to alternative prey (small birds) appeared to be more productive than the strictly vole-specialized foraging strategy of TOs. In contrast to earlier studies at the individual-level, specialist predators at the species level (in this case TOs) appear to be less effective than generalists (POs), but diet specialisation was particularly costly under conditions when scarcity of main foods limited offspring production.     

Breeding dispersal of Eurasian kestrels Falco tinnunculus under temporally fluctuating food abundance

Costs and benefits of dispersal can vary in space and time, depending on environmental factors and individual state. Plastic, condition‐dependent dispersal strategies, in which individuals rely on external cues such as food abundance to adjust their dispersal distances, are therefore expected to evolve in temporally fluctuating environments. We examined factors affecting breeding dispersal distances in Eurasian kestrels Falco tinnunculus subsisting on multi‐annually and cyclically fluctuating voles as their main food. We attempted to avoid traditional bias in dispersal studies by having large study areas and by taking detection probabilities into account. We observed 320 dispersal events of male and 215 events of female kestrels from our study areas in western Finland during 24 yr. After correcting for distance‐specific detection probability, the estimates of mean dispersal distances increased two‐fold being still clearly higher for females than males. Vole abundance in the spring of settlement was more important in determining average dispersal distances than vole abundance in the previous autumn. At the population level (cross‐sectional model), both males and females dispersed longer distances when the spring abundance of their main food (voles) was low compared to when it was abundant, as predicted by the food depletion hypothesis. At the individual level (longitudinal model), only females responded to the food situation by dispersing more when food abundance was low in the spring of settlement. Females also dispersed longer when vole abundance in the previous autumn had been high. Individual males did not respond to vole abundance, which implies that the population level response in males might have been caused by long‐distance dispersers, which breed in the study area only in good vole years. Our results show that the dispersal distances of kestrels at northern latitudes depend both on individual properties (gender, age, and possibly individual tendency to disperse) and environmental conditions (temporal variation in main food abundance).     

Dual probe fluorescence monitoring of intracellular free calcium during ischemia in mouse heart by using continuous compensation for pH dependence of the dissociation constant of Fura-2, and the interference of myoglobin

Mitochondrial damage is the main source of cellular injury upon ischemia-reperfusion, and calcium loading has been implicated in this phenomenon. The use of optical probes for calcium monitoring of the intact heart is hampered by internal filter effects of intracellular hemoproteins, endogenous fluorescence, and their sensitivity to pH. We describe here a method for measurement of intracellular free calcium in isolated myoglobin-deficient perfused mouse hearts under conditions of large intracellular pH fluctuations by simultaneous fluorescence monitoring of the calcium-probe Fura-2 and the pH probe BCECF through dual wavelength excitation of both probes. In myoglobin-containing mouse heart endogenous chromophores interfere with Fura-2 fluorometry. It is shown that a paradoxical decrease in Fura-2 fluorescence occurs during ischemia in isolated mouse hearts. Simultaneous recording of BCECF fluorescence (calibrated against pH measurement with phosphorus NMR) and data reduction based on continual recalculation of the apparent dissociation constant of the calcium-probe complex revealed that a marked increase in intracellular free calcium occurs, and that the Fura-2 fluorescence decrease was caused by an increase in dissociation constant due to intracellular acidification. Intracellular free calcium rose almost linearly during a 20-min period of ischemia and returned to basal values rapidly upon the commencement of perfusion.