Aim Latitudinal patterns in biotic interactions, particularly in herbivory, have been widely debated. We conducted a quantitative research synthesis to test whether background losses of woody plant foliage to insects generally decrease from the equator to the poles, and whether geographical gradients in insect herbivory are stronger at higher latitudes than at lower latitudes.Location Global terrestrial ecosystems. MethodsWe used published and original data (3482 point estimates of the percentage of leaf area consumed by insects, collected from 941 species of woody plants in 836 localities world-wide) to analyse the geographical patterns in total losses of plant foliage and in losses to defoliating, leaf mining and leaf galling insects separately, and we searched for climatic factors that can explain the variation in the levels of background insect herbivory across the globe and within climate zones.Result On average, according to published data woody plants lose 7.55% of their leaf area to insects, but 4.73% according to our original data collected in a blinded way. These losses demonstrate a dome-shaped latitudinal pattern: they peak in temperate zones, slightly decrease towards the equator and strongly decrease towards the poles. This pattern is consistent between published and original data, indicating the robustness of the detected relationship between herbivory and latitude. The climatic factors explaining these latitudinal patterns in insect herbivory differ between climate zones. Main conclusionsOur study provides solid support for the hypothesis of a decrease in background herbivory with latitude, but only outside the tropics. For the first time we demonstrate that the latitudinal gradient in insect herbivory across the globe is nonlinear, i.e. its slope differs between the climate zones. In temperate and polar zones, but not in the tropics, background herbivory correlates with mean air temperatures and is therefore likely to increase with climate warming.
Despite the increasing rate of urbanization, the consequences of this process on biotic interactions remain insufficiently studied. Our aims were to identify the general pattern of urbanization impact on background insect herbivory, to explore variations in this impact related to characteristics of both urban areas and insect-plant systems, and to uncover the factors governing urbanization impacts on insect herbivory. We compared the foliar damage inflicted on the most common trees by defoliating, leafmining and gall-forming insects in rural and urban habitats associated with 16 European cities. In two of these cities, we explored quality of birch foliage for herbivorous insects, mortality of leafmining insects due to predators and parasitoids and bird predation on artificial plasticine larvae. On average, the foliage losses to insects were 16.5% lower in urban than in rural habitats. The magnitude of the overall adverse effect of urbanization on herbivory was independent of the latitude of the locality and was similar in all 11 studied tree species, but increased with an increase in the size of the urban area: it was significant in large cities (city population 1-5 million) but not significant in medium-sized and small towns. Quality of birch foliage for herbivorous insects was slightly higher in urban habitats than in rural habitats. At the same time, leafminer mortality due to ants and birds and the bird attack intensity on dummy larvae were higher in large cities than in rural habitats, which at least partially explained the decline in insect herbivory observed in response to urbanization. Our findings underscore the importance of top-down forces in mediating impacts of urbanization on plant-feeding insects: factors favouring predators may override the positive effects of temperature elevation on insects and thus reduce plant damage.
invertebrate herbivory on dwarf birch (Betula glandulosa-nana 1 complex) increases with temperature and precipitation across the tundra biome ' Polar biology, vol. 40, no. 11, pp. 2265-2278. DOI: 10.1007%2Fs00300-017-2139 Digital Object Identifier (DOI): 10.1007%2Fs00300-017-2139-7 Link: Link to publication record in Edinburgh Research Explorer Document Version: Peer reviewed version Published In: Polar biology General rightsCopyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policyThe University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact openaccess@ed.ac.uk providing details, and we will remove access to the work immediately and investigate your claim. Chronic, low intensity herbivory by invertebrates, termed background herbivory, has been understudied in tundra, 78 yet its impacts are likely to increase in a warmer Arctic. The magnitude of these changes is however hard to 79 predict as we know little about the drivers of current levels of invertebrate herbivory in tundra. We assessed the 80 intensity of invertebrate herbivory on a common tundra plant, the dwarf birch (Betula glandulosa-nana complex), 81 and investigated its relationship to latitude and climate across the tundra biome. Leaf damage by defoliating, 82 mining and gall-forming invertebrates was measured in samples collected from 192 sites at 56 locations. Our 83 results indicate that invertebrate herbivory is nearly ubiquitous across the tundra biome but occurs at low 84 intensity. On average, invertebrates damaged 11.2% of the leaves and removed 1.4% of total leaf area. The 85 damage was mainly caused by external leaf feeders, and most damaged leaves were only slightly affected (12% 86 leaf area lost). Foliar damage was consistently positively correlated with mid-summer (July) temperature and, to a 87 lesser extent, precipitation in the year of data collection, irrespective of latitude. Our models predict that, on 88 average, foliar losses to invertebrates on dwarf birch are likely to increase by 6-7% over the current levels with a 1 89 °C increase in summer temperatures. Our results show that invertebrate herbivory on dwarf birch is small in 90 magnitude but given its prevalence and dependence on climatic variables, background invertebrate herbivory 91 should be included in predictions of climate change impacts on tundra ecosystems. 92 3
The strength of biotic interactions is generally thought to increase toward the equator, but support for this hypothesis is contradictory. We explored whether predator attacks on artificial prey of eight different colors vary among climates and whether this variation affects the detection of latitudinal patterns in predation. Bird attack rates negatively correlated with model luminance in cold and temperate environments, but not in tropical environments. Bird predation on black and on white (extremes in luminance) models demonstrated different latitudinal patterns, presumably due to differences in prey conspicuousness between habitats with different light regimes. When attacks on models of all colors were combined, arthropod predation decreased, whereas bird predation increased with increasing latitude. We conclude that selection for prey coloration may vary geographically and according to predator identity, and that the importance of different predators may show contrasting patterns, thus weakening the overall latitudinal trend in top‐down control of herbivorous insects.
Latitudinal patterns in biotic interactions, including herbivory, have been widely debated during the past years. In particular, recent meta‐analysis questioned the hypothesis that herbivory increases from the poles towards the equator. Our study was designed to verify this hypothesis by exploring latitudinal patterns in abundance and diversity of birch‐feeding insect herbivores belonging to the leafminer guild in northern Europe, from 59° to 69°N. We collected branches from five mature trees of two birch species (Betula pendula and B. pubescens) at each study site (ten sites for each of five latitudinal gradients) twice per season (in early and late summer of 2008–2011) and attributed all mines found on leaves of these branches to a certain taxon of insects. Latitudinal patterns were quantified by calculating Spearman rank correlation coefficients between both abundance and diversity of leafmining taxa and latitudes of sampling sites. In general, both abundance and diversity of leafminers significantly decreased with latitude. However, we discovered pronounced variation in patterns of latitudinal changes among study years and leafminer taxa. Variation among study years was best explained by mean temperatures in July at the northern ends of our gradients. During cold years, abundance of leafminers significantly decreased with latitude, while during warm years the abundance was either independent of latitude or even increased towards the pole. In the northern boreal forests (66° to 69°N), herbivores demonstrated larger changes in densities in response to temperature variations than in the boreo‐nemoral forests (59° to 62°N). Our data suggest that climate warming will result in a stronger increase in herbivory at higher latitudes than at lower latitudes.
Modern concepts of plant tolerance to herbivory are primarily based on studies of short‐term severe damage, whereas the effects of minor chronic damage to long‐lived woody plants, corresponding to background herbivory (2–15% annual loss of foliar biomass in boreal and temperate forests), remain poorly understood. In our experiment, the annual removal of 2, 4, 8 and 16% of the leaf area from naturally growing mountain birch Betula pubescens subsp. czerepanovii saplings during a seven‐year period resulted in a pronounced reduction of plant vertical growth (–30, –34, –45 and –78%, respectively). Leaf size decreased first (already after one year of the 16% treatment), resulting in the reduction of the total leaf area. This effect was followed by a considerable decrease in the length of long shoots in all treatments. Leaf number on the plant was maintained for a longer time, being reduced by the end of the experiment in 16% treatment only; no changes in specific leaf area or chlorophyll fluorescence were observed in either of the treatments. This pattern may indicate that the plant reallocates resources from the growth of the woody parts to the maintenance of the photosynthetic area, and can be seen as a strategy of tolerance to minor herbivory, whereas compensatory responses typical of severe herbivory (increased photosynthesis rates and shoot regrowth) have not been detected. The predicted 2–5% increase in background herbivory due to climate warming can potentially produce previously unrecognised negative impacts on tree growth. We conclude that in the long term, background herbivory is likely to impose stronger effects on the growth of woody plants than short‐term devastating outbreaks of defoliators, thus contributing more to the development of plant evolutionary adaptations to herbivory than severe but episodic bouts of damage.
Knowledge of the latitudinal patterns in biotic interactions, and especially in herbivory, is crucial for understanding the mechanisms that govern ecosystem functioning and for predicting their responses to climate change. We used sap-feeding insects as a model group to test the hypotheses that the strength of plant-herbivore interactions in boreal forests decreases with latitude and that this latitudinal pattern is driven primarily by midsummer temperatures. We used a replicated sampling design and quantitatively collected and identified all sap-feeding insects from four species of forest trees along five latitudinal gradients (750-1300 km in length, ten sites in each gradient) in northern Europe (59 to 70°N and 10 to 60°E) during 2008-2011. Similar decreases in diversity of sap-feeding insects with latitude were observed in all gradients during all study years. The sap-feeder load (i.e. insect biomass per unit of foliar biomass) decreased with latitude in typical summers, but increased in an exceptionally hot summer and was independent of latitude during a warm summer. Analysis of combined data from all sites and years revealed dome-shaped relationships between the loads of sap-feeders and midsummer temperatures, peaking at 17 °C in Picea abies, at 19.5 °C in Pinus sylvestris and Betula pubescens and at 22 °C in B. pendula. From these relationships, we predict that the losses of forest trees to sap-feeders will increase by 0-45% of the current level in southern boreal forests and by 65-210% in subarctic forests with a 1 °C increase in summer temperatures. The observed relationships between temperatures and the loads of sap-feeders differ between the coniferous and deciduous tree species. We conclude that climate warming will not only increase plant losses to sap-feeding insects, especially in subarctic forests, but can also alter plant-plant interactions, thereby affecting both the productivity and the structure of future forest ecosystems.
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