Hemiparasites drive heterogeneity in litter arthropods: Implications for woodland insectivorous birds

Providing fruit, nectar, leaves and litter, mistletoes represent important resources for many organisms, linking above‐ground patterns with below‐ground processes. Here, we explore how mistletoe litter affects arthropod availability, especially those taxa preferentially consumed by ground‐feeding insectivorous birds, a group that has undergone widespread declines. We estimated the influence of mistletoe on arthropod occurrence by sampling arthropod communities beneath infected and uninfected trees with pit‐fall traps. Then, we experimentally isolated direct effects of mistletoe litter on arthropods with a litterbag study. Soil arthropod communities beneath infected trees had consistently greater abundance and biomass – total arthropods and the subset of arthropods preferentially consumed by ground‐foraging insectivores – compared to otherwise comparable uninfected trees. Arthropods showed a weak response to litter addition, with maximum abundances recorded from bags with low mistletoe litter, significantly lower abundances associated with higher mistletoe fractions and pure tree litter (after 5 months). Our findings confirm that mistletoe occurrence has a significant positive impact on arthropod availability, especially on those preferred by ground‐foraging bird insectivores. However, only a minor part of this impact is due to the direct, short‐term effects of mistletoe litter, which suggests that additional mistletoe‐mediated effects (e.g. local changes in structural or microclimatic factors, cumulative effects over multiple years) play significant roles. By altering arthropod assemblages within leaf litter and increasing the heterogeneity of resource availability on forest floors, mistletoe plays an important role in improving habitat quality for declining insectivores.     

Plant quality and predation risk mediated by plant ontogeny: consequences for herbivores and plants

Bottom‐up and top‐down impacts on herbivores can be influenced by plant productivity, structural complexity, vigor and size. Although these traits are likely to vary with plant development, the influence of plant ontogeny on the relative importance of plant quality (i.e. bottom‐up forces) and predation risk (i.e. top‐down forces) has been the focus of little previous investigation. We evaluated the role of plant ontogeny for the relative importance of bottom‐up and top‐down forces on insect herbivore abundance, species richness, and species diversity attacking the tropical tree Casearia nitida. We also quantified the cascading effects on herbivory, growth and reproduction of this plant species. Plant quality traits (nitrogen and phenolic compounds) were assessed in saplings and reproductive trees. Bottom‐up forces were manipulated by fertilizing plants from both ontogenetic stages. Top‐down forces were manipulated by excluding insectivorous birds from saplings and reproductive trees. Plant ontogeny influenced foliage quality in terms of total phenolics, which were in greater concentration in reproductive trees than in saplings; however, it did not influence bottom‐up forces as modified by fertilization. Bird exclusion increased herbivore density with the same magnitude on both stages. Ontogeny influenced species diversity, which was greater in reproductive trees than in saplings, and also influenced treatment impacts on species richness and diversity. Although top‐down forces increased herbivory equally on plants of each ontogenetic stage, the two stages showed different overcompensation responses to increased damage: caged saplings produced greater leaf biomass than non‐caged saplings, whereas caged trees increased in height proportionally more than non‐caged trees. In sum, plant ontogeny influenced the impact of bird predation on herbivore density, species richness, and species diversity, and the growth variables affected by increased damage in caged plants. We suggest that plant ontogeny can contribute to some extent to the influence of plant quality and the third trophic level on herbivores in this system.     

Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds

Insects and spiders were sampled on branches of spruce in a 5.5 km² area before and after each of six winters. Psocoptera, Aphidoidea and Lepidoptera larvae were the most common insects in autumn. In Feb–Mar only 1% remained, most of the decline occurring already early in the winter. Spiders were almost as common as Psocoptera in autumn but survived winter to 28–45%. Spiders therefore are potentially more important food for wintering birds than are insects. Through the first five winters there was a steady increase in density of small (but not large) spiders both in autumn (290%) and spring (390%). Spring densities of small but not large spiders were significantly correlated to autumn densities. Usually there was no added variability of spider abundance between trees and most of the variability was found within trees. In autumn spiders occurred at significantly higher densities in the lower half of the spruce trees than in the upper half. Much of the reduction of large spiders over winter is known to be caused by predation by birds. Over winter, this predation probably makes the distribution of spiders within trees more uniform. The autumn density of three tit species, the goldcrest and the treecreeper was significantly correlated with the density of large spiders at the same time, but not with small spiders (which they presumably do not eat). This might be caused by territorial behaviour being related to food density in autumn.     

Cyanogenesis in plants and arthropods

Cyanogenic glucosides are phytoanticipins known to be present in more than 2500 plant species. They are regarded as having an important role in plant defense against herbivores due to bitter taste and release of toxic hydrogen cyanide upon tissue disruption, but recent investigations demonstrate additional roles as storage compounds of reduced nitrogen and sugar that may be mobilized when demanded for use in primary metabolism. Some specialized herbivores, especially insects, preferentially feed on cyanogenic plants. Such herbivores have acquired the ability to metabolize cyanogenic glucosides or to sequester them for use in their own defense against predators. A few species of arthropods (within diplopods, chilopods and insects) are able to de novo biosynthesize cyanogenic glucosides and some are able to sequester cyanogenic glucosides from their food plant as well. This applies to larvae of Zygaena (Zygaenidae). The ratio and content of cyanogenic glucosides is tightly regulated in Zygaena filipendulae, and these compounds play several important roles in addition to defense in the life cycle of Zygaena. The transfer of a nuptial gift of cyanogenic glucosides during mating of Zygaena has been demonstrated as well as the involvement of hydrogen cyanide in male attraction and nitrogen metabolism. As more plant and arthropod species are examined, it is likely that cyanogenic glucosides are found to be more widespread than formerly thought and that cyanogenic glucosides are intricately involved in many key processes in the life cycle of plants and arthropods.     

Seed predation by birds and small mammals in semiarid Chile

We studied spatial and temporal patterns in foraging activity among diurnal birds and nocturnal mammals at a semiarid site in northern Chile using artificial foraging trays. Small mammals foraged more extensively under shrubs than in open microhabitats, but birds showed no such selection. Moreover, avian foraging was more extensive than that by small mammals in all seasons and both microhabitats. Avian foraging was highly seasonal, as many birds at our site migrate to the Andean prepuna or to Patagonia during the austral summer. Birds have tended to be overshadowed by small mammals and ants in studies of granivory, but this study suggests that their importance may be underestimated in some systems.     

Constant density and stable territoriality in some tropical insectivorous birds

Summary Four species of understory antbirds (Formicariidae: Myrmotherula fulviventris, M. axillaris, Microrhopias quixensis, and Thamnophilus punctatus) had stable populations over eight rainy seasons on Barro Colorado Island, Panama. The co-defended territories of M. fulviventris and Microrhopias quixensis, were essentially identical from year to year on our intensive study site, despite a moderate turnover of territory owners. The location of the territories of T. punctatus was also similar between years. This stability occurred in the face of considerable annual variation in the survivorship of adult M. fulviventris and T. punctatus. This variation was not significantly correlated with patterns of rainfall. Stable territoriality has rarely been reported from relatively-short-lived insectivorous birds. The annual production of young was significantly variable only in M. axillaris. Because BCI is an island comprised of one habitat (tropical forest) and so supports a closed population of antbirds, and because it is unlikely that natality equaled mortality on our study site during the entire eight years of the study, we suggest that these breeding populations are socially regulated at a constant level below the limits directly set by food supply.     

Landscape-dependent response to predation risk by forest birds

Knowing how forest loss and associated fragmentation actually impact individual birds is essential to our understanding of consequences at the population level. We conducted a landscape-level experiment to test whether deforestation affects the trade-off between foraging and antipredatory behaviour of black-capped chickadees ( Poecile atricapilla ) in 24 landscapes (range 8–88% forest cover, 500-m radius) during two winters. At a field-forest edge in the centre of each landscape, we used the maximum distance ventured into the open by flocks to get sunflower seeds placed on the snow-covered fields, as a measure of risk-taking. In the more deforested landscapes, chickadees ventured farther (up to the maximum of 40 m) into the open. Edge density and proportion of conifers in the forest had no influence on risk-taking. However, where ad libitum food was available for a few weeks prior to the experiment (in 12 of the 24 landscapes), chickadees ventured four meters or less away from the forest edge, regardless of the level of deforestation. We conclude that landscape deforestation increases energy stress, which in turn promotes risk-taking, and may therefore increase winter mortality through greater exposure to predators.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

食虫植物研究的现状和趋势

综述了食虫植物的研究概况 ,包括研究历史、食虫植物的捕虫与消化机制 ,食虫的效果以及食虫植物与环境的生态关系 ,旨在促进我国关于食虫植物的研究     

Empty seeds reduce seed predation by birds in Juniperus osteosperma

Utah juniper (Juniperus osteosperma) is one of many plant species that produce large numbers of fruits containing parthenocarpic or otherwise empty or inviable seeds. We tested the hypothesis that production of empty fruits in this species results in reduced levels of predation on fertile seeds. In a population in west-central Utah, we estimated the proportion of fruits with filled seeds in trees suffering high levels of fruit destruction by the seed-eating bird Parus inornatus and in neighbouring trees similar in crown and fruit-crop size but suffering negligible predation. We found that the heavily attacked trees had higher proportions of filled seeds. Thus, juniper may benefit from producing fruits that contain no offspring. This is the first study to demonstrate that empty seeds may reduce predation by vertebrate seed eaters and the first to demonstrate discrimination based on seed filling at the level of whole plants.     

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], beta-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.     

Frequency-dependent predation by birds at edges and interiors of woodland

Structural variations between edge and interior areas within forest fragments may bring about differences in food availability that may influence the selective behaviour of predators and prey population dynamics. The purpose of this paper was to assess patterns of artificial prey selection by wild birds (House Sparrow Passer domesticus and Rock Dove Columba livid) between edge and interior areas of woodland, taking into account differences in prey frequency (10% of one food type and 90% of the other) and density (30 baits/m^-2 and 50 baits/m-²). Experiments were conducted at 24 plots in 3 forest fragments in the city of Madrid, Spain. Selectivity did not vary among parks or between densities. However, selectivity did vary with the frequency and location of baits, showing an anti-apostatic trend (baits were preferred at low rather than at high frequencies) that was more pronounced at interiors than at edges. Two possible factors that may account for stronger anti-apostatic selection at edges are the higher densities of predators and pedestrians found there. However, there are many other possible explanations, and no specific conclusion can be supported with the current data. The results of this study also point out that site heterogeneity should be taken into account in the experimental design of future studies on frequency-dependent food selection by wild birds, particularly in fragmented landscapes.     

Tritrophic interactions: willows, herbivorous insects and insectivorous birds

Insectivorous birds can increase plant growth by consuming herbivorous insects and reducing insect damage. However, plant traits such as the level of chemical defense may affect the quantity and quality of insects, and alter the foraging behavior of birds. Therefore, I predicted that plant traits can also modify the effect of birds on leaf damage and plant growth. This study compared the effect of insectivorous birds on the herbivory and growth of two chemically different willow species, weakly defended Salix phylicifolia and strongly defended S. myrsinifolia under two fertilization levels. Half of the willows were protected from birds using a translucent gill-net, which did not limit access by insects. The effect of birds on the densities of leaf-chewing insects and leaf damage was considerable on unfertilized S. phylicifolia but less obvious on fertilized ones. The effect of bird predation was negligible on S. myrsinifolia, which had very low insect densities in all treatments. Birds increased the growth of the experimental willows, but the effect was clear only in unfertilized S. phylicifolia. I suggest that birds avoided foraging on willows with low populations of insects and little visible damage. The study shows that bird predation can alter the patterns of insect densities we see on willows, emphasizing the importance of considering multitrophic effects when studying plant-insect interactions. Received: 25 May 1999 / Accepted: 9 August 1999     

Reduced flocking by birds on islands with relaxed predation

Adaptive hypotheses for the evolution of flocking in birds have usually focused on predation avoidance or foraging enhancement. It still remains unclear to what extent each factor has contributed to the evolution of flocking. If predation avoidance were the sole factor involved, flocking should not be prevalent when predation is relaxed. I examined flocking tendencies along with mean and maximum flock size in species living on islands where predation risk is either absent or negligible and then compared these results with matched counterparts on the mainland. The dataset consisted of 46 pairs of species from 22 different islands across the world. The tendency to flock was retained on islands in most species, but in pairs with dissimilar flocking tendencies, island species were less likely to flock. Mean and maximum flock size were smaller on islands than on the mainland. Potential confounding factors such as population density, nest predation, habitat type, food type and body mass failed to account for the results. The results suggest that predation is a significant factor in the evolution of flocking in birds. Nevertheless, predation and other factors, such as foraging enhancement, probably act together to maintain the trait in most species.     

Interactions among elk, aspen, galling sawflies and insectivorous birds

Using two years of observational and experimental data, we examined the hypothesis that browsing by elk on aspen indirectly affects the distribution of a leaf-galling sawfly, which in turn affects insect diversity and foraging patterns of insectivorous birds. We found that: i) in an analyses of 33 arthropod species, the presence of sawflies significantly increased arthropod richness and abundance by 2 X and 2.5 X, respectively. ii) browsing by elk reduced sawfly gall abundance such that 90% of the galls were found on unbrowsed aspen ramets. iii) insectivorous birds attacked 60–74% of the galls on unbrowsed shoots compared to 11% on browsed shoots. When leaf-galler abundance was experimentally held constant on browsed and unbrowsed shoots, predation by insectivorous birds did not differ significantly. This result suggests that browsing affects the patterns of avian predation by altering the distribution of a galling insect. These data argue that bottom-up, top-down, and lateral factors can act in concert to affect the distribution of a galler, structure arthropod communities and affect predation by insectivorous birds.     

Dispersal limitation: Evolutionary origins and consequences in arthropods

Niche and dispersal ability are key traits for explaining the geographical structuring of species into discrete populations, and its evolutionary significance. Beyond their individual effects, the interplay between species niche and its geographic limits, together with the evolutionary lability of dispersal ability, can underpin trait diversification and speciation when exposed to gradients of selection. In this issue of Molecular Ecology, two complementary papers demonstrate how evolutionary lability for dispersal ability linked to niche shift can drive such a model in a context that includes selection. Both papers investigate the evolution of dispersal limitation in arthropods across altitudinal gradients, but using taxa with contrasting ecologies. McCulloch et al. (2019) investigate the evolution of wing loss at higher altitudes in stoneflies, a taxon inhabiting freshwater systems. Suzuki et al. (2019) report a similar phenomenon, but involving wing reduction at higher altitudes in scorpionflies, a taxon associated with moist terrestrial habitats. Here, we compare and contrast the results of both studies to explore their broader implications for understanding diversification and speciation within arthropods.