Elina Mäntylä

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.

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.

Insect herbivory may cause changes in the visual properties of leaves and affect the camouflage of herbivores to avian predators

Abstract‘Cry for help’ hypothesis predicts that attraction of predators with chemical or visual cues can decrease insect damage of plants. Visual cues involve changes in photosynthetic activity and the reflectance of leaves, and there is some evidence that birds may use these changes as foraging cues. However, changes in the visual properties of leaves have not been quantified and it is not known how birds see these changes. We also presented and tested a new ‘reduction in camouflage’ hypothesis (not mutually exclusive with cry for help) stating that herbivore-mediated changes in leaf colour can increase the conspicuousness of herbivore against leaves. To define changes in the visual properties of leaves, their detectability to birds, and whether these changes affect the conspicuousness of herbivore, we manipulated the level of herbivory in silver birch trees (Betula pendula) with autumnal moth (Epirrita autumnata) larvae, and used blue tit (Cyanistes caeruleus) vision models to images of leaves and larvae. Hue, luminance (lightness), contrast, light transmission, chlorophyll content, photosynthetic activity and water content of the leaves were compared between herbivore-damaged and control trees. The leaves of herbivore-damaged trees had a decreased chlorophyll a concentration, increased contrast and they reflected more longer wavelengths. However, these changes are likely not obvious to birds. In contrast to our expectation, there were only minor differences in conspicuousness of larvae against the leaves of damaged trees, which may be very subtle to predator vision. Nevertheless, according to visual models, larvae should be easily detectable to birds from both herbivore-damaged and control trees.Significance statementHerbivory affects photosynthetic machinery and light reflectance of leaves, and may thus provide visual foraging cues to birds, although it is not known how these changes appear to birds. We also hypothesized that the changes in leaves may reduce the camouflage of the herbivore. After applying herbivore treatment and using the avian vision models, we found that the leaves of herbivore damage may cause the leaves to appear to birds with higher contrast and greener or a more yellowish colour than control leaves. In addition, although the herbivore was visible to birds, it was slightly less conspicuous when on damaged trees, indicating that the herbivore can be adapted to changes in the food plant. Our results indicate that herbivory causes changes visual properties of leaves, but these changes are likely not obvious to birds.

Territory Choice of Pied Flycatchers is Not Based on Induced Cues of Herbivore Damaged Trees

Passerine birds use a variety of indirect cues to make territory location decisions. These birds can also distinguish herbivore-damaged plants from undamaged ones during foraging, even when they cannot see the herbivorous larvae or damaged leaves. To test the possibility that also the territory choice of passerines is affected by herbivore- induced plant cues, we established territories with and without indirect cues of herbivore presence for migratory pied flycatchers (Ficedula hypoleuca) at the time of their arrival. Half of the territories had folivorous moth larvae hidden inside mesh bags to defoliate small trees (Betula spp.) and half had only empty mesh bags on trees. Hidden herbivory on the trees did not affect the mean date of territory choice by either male or female birds. Nonetheless, there was a trend that females, but not males, chose the territories in the same order in two consecutive years. Thus, it seems that pied flycatchers do not use indirect cues of larval presence as a basis for their choice of territory, but possibly some more general environmental cues.

Ecological conditions alter cooperative behaviour and its costs in a chemically defended sawfly

The evolution of cooperation and social behaviour is often studied in isolation from the ecology of organisms. Yet, the selective environment under which individuals evolve is much more complex in nature, consisting of ecological and abiotic interactions in addition to social ones. Here, we measured the life-history costs of cooperative chemical defence in a gregarious social herbivore, Diprion pini pine sawfly larvae, and how these costs vary under different ecological conditions. We ran a rearing experiment where we manipulated diet (resin content) and attack intensity by repeatedly harassing larvae to produce a chemical defence. We show that forcing individuals to allocate more to cooperative defence (high attack intensity) incurred a clear cost by decreasing individual survival and potency of chemical defence. Cooperative behaviour and the magnitude of its costs were further shaped by host plant quality. The number of individuals participating in group defence, immune responses and female growth decreased on a high resin diet under high attack intensity. We also found some benefits of cheating: non-defending males had higher growth rates across treatments. Taken together, these results suggest that ecological interactions can shape the adaptive value of cooperative behaviour and maintain variation in the frequency of cooperation and cheating.