Impacts of urbanization on insect herbivory and plant defences in oak trees

Systematic comparisons of species interactions in urban versus rural environments can improve our understanding of shifts in ecological processes due to urbanization. However, such studies are relatively uncommon and the mechanisms driving urbanization effects on species interactions (e.g. between plants and insect herbivores) remain elusive. Here we investigated the effects of urbanization on leaf herbivory by insect chewers and miners associated with the English oak Quercus robur by sampling trees in rural and urban areas throughout most of the latitudinal distribution of this species. In performing these comparisons, we also controlled for the size of the urban areas (18 cities) and gathered data on CO₂ emissions. In addition, we assessed whether urbanization affected leaf chemical defences (phenolic compounds) and nutritional traits (phosphorus and nitrogen), and whether such changes correlated with herbivory levels. Urbanization significantly reduced leaf chewer damage but did not affect leaf miners. In addition, we found that leaves from urban locations had lower levels of chemical defences (condensed and hydrolysable tannins) and higher levels of nutrients (nitrogen and phosphorus) compared to leaves in rural locations. The magnitude of urbanization effects on herbivory and leaf defences was not contingent upon city size. Importantly, while the effects of urbanization on chemical defences were associated with CO₂ emissions, changes in leaf chewer damage were not associated with either leaf traits or CO₂ levels. These results suggest that effects of urbanization on herbivory occur through mechanisms other than changes in the plant traits measured here. Overall, our simultaneous assessment of insect herbivory, plant traits and abiotic correlates advances our understanding of the main drivers of urbanization effects on plant–herbivore interactions.     

Insect herbivory in an intact forest understory under experimental CO2 enrichment

Human-induced increases in atmospheric CO₂ concentration have the potential to alter the chemical composition of plant tissue, and thereby affect the amount of tissue consumed by herbivorous arthropods. At the Duke Forest free-air concentration enrichment (FACE) facility in North Carolina (FACTS–1 research facility), we measured the amount of leaf tissue damaged by insects and other herbivorous arthropods during two growing seasons in a deciduous forest understory continuously exposed to ambient (360 l l^–1) and elevated (~560 µl l^–1) CO₂ conditions. In 1999, there was a significant interaction between CO₂ and species such that winged elm (Ulmus alata) showed lower herbivory in elevated CO₂ plots, whereas red maple (Acer rubra) and sweetgum (Liquidambar styraciflua) did not. In 2000, our results did not achieve statistical significance but the magnitude of the result was consistent with the 1999 results. In 1999 and 2000, we found a decline (10–46%) in community-level herbivory in elevated CO₂ plots driven primarily by reductions in herbivory on elm. The major contribution to total leaf damage was from missing tissue (66% of the damaged tissue), with galls, skeletonized, and discolored tissue making smaller contributions. It is unclear whether the decline in leaf damage is a result of altered insect populations, altered feeding, or a combination. We were not able to quantify insect populations, and our measurements did not resolve an effect of elevated CO₂ on leaf chemical composition (total nitrogen, carbon, C/N, sugars, phenolics, starch). Despite predictions from a large number of single-species studies that herbivory may increase under elevated CO₂, we have found a decrease in herbivory in a naturally established forest understory exposed to a full suite of insect herbivores and their predators.     

Effects of scale insect herbivory and shading on net gas exchange and growth of a subtropical tree species (Guaiacum sanctum L.)

Summary The scale insect, Toumeyella sp., feeds exclusively on the subtropical hammock tree lignum vitae (Guaiacum sanctum L.). The combined effects of scale herbivory and shading on leaf gas exchange characteristics and growth of lignum vitae trees were studied using a factorial design. Trees grown in full sun or in 75% shade were manually infested with scale or left noninfested. Beginning 4 weeks after infestation, net CO₂ assimilation, stomatal conductance, transpiration, internal partial pressure of CO₂, and water-use efficiency were determined on single-leaves at 4-week intervals for trees in each treatment. At the end of the experiment, net CO₂ assimilation was determined for whole plants. Total leaf area, leaf, stem, and root dry weights, and leaf chlorophyll and nitrogen concentrations were also determined. Scale infested trees generally had lower net CO₂ assimilation, stomatal conductance, and transpiration rates as well as less leaf area, and root, stem, and leaf dry weights than noninfested trees. Twenty four weeks after the shade treatment was imposed, sun-grown trees had approximately twice the leaf area of shade-grown trees. Shade-grown trees compensated for the reduced leaf area by increasing their photosynthetic efficiency. This resulted in no difference in light saturated net CO₂ assimilation on a whole plant basis between sun-grown and shade-grown trees. Chlorophyll and nitrogen concentrations per unit leaf area were greater in leaves of shade-grown trees than in leaves of sun-grown trees. Shading and herbivory by Toumeyella sp. each resulted in decreased growth of Guaiacum sanctum. Scale insect herbivory did not result in greater detrimental effects on leaf gas exchange characteristics for shade-grown than for sun-grown trees. Herbivory by Toumeyella resulted in a greater decrease in tree growth for sun-grown than for shade-grown trees.     

Effects of elevated CO2 and O3 on leaf damage and insect abundance in a soybean agroecosystem

By altering myriad aspects of leaf chemistry, increasing concentrations of CO₂ and O₃ in the atmosphere derived from human activities may fundamentally alter the relationships between insect herbivores and plants. Because exposure to elevated CO₂ can alter the nutritional value of leaves, some herbivores may increase consumption rates to compensate. The effects of O₃ on leaf nutritional quality are less clear; however, increased senescence may also reduce leaf quality for insect herbivores. Additionally, changes in secondary chemistry and the microclimate of leaves may render plants more susceptible to herbivory in elevated CO₂ and O₃. Damage to soybean (Glycine max L.) leaves and the size and composition of the insect community in the plant canopy were examined in large intact plots exposed to elevated CO₂ (~550 μmol mol⁻¹) and elevated O₃ (1.2*ambient) in a fully factorial design with a Soybean Free Air Concentration Enrichment system (SoyFACE). Leaf area removed by folivorous insects was estimated by digital photography and insect surveys were conducted during two consecutive growing seasons, 2003 and 2004. Elevated CO₂ alone and in combination with O₃ increased the number of insects and the amount of leaf area removed by insect herbivores across feeding guilds. Exposure to elevated CO₂ significantly increased the number of western corn rootworm (Diabrotica virgifera) adults (foliage chewer) and soybean aphids (Aphis glycines; phloem feeder). No consistent effect of elevated O₃ on herbivory or insect population size was detected. Increased loss of leaf area to herbivores was associated with increased carbon-to-nitrogen ratio and leaf surface temperature. Soybean aphids are invasive pests in North America and new to this ecosystem. Higher concentrations of CO₂ in the atmosphere may increase herbivory in the soybean agroecosystem, particularly by recently introduced insect herbivores. Handling editor: Gary Felton.     

Seeing the forest for the trees: long-term exposure to elevated CO2 increases some herbivore densities

The effects of elevated CO₂ on plant growth and insect herbivory have been frequently investigated over the past 20 years. Most studies have shown an increase in plant growth, a decrease in plant nitrogen concentration, an increase in plant secondary metabolites and a decrease in herbivory. However, such studies have generally overlooked the fact that increases in plant production could cause increases of herbivores per unit area of habitat. Our study investigated leaf production, herbivory levels and herbivore abundance per unit area of leaf litter in a scrub‐oak system at Kennedy Space Center, Florida, under conditions of ambient and elevated CO₂, over an 11‐year period, from 1996 to 2007. In every year, herbivory, that is leafminer and leaftier abundance per 200 leaves, was lower under elevated CO₂ than ambient CO₂ for each of three species of oaks, Quercus myrtifolia, Quercus chapmanii and Quercus geminata. However, leaf litter production per 0.1143 m² was greater under elevated CO₂ than ambient CO₂ for Q. myrtifolia and Q. chapmanii, and this difference increased over the 11 years of the study. Leaf production of Q. geminata under elevated CO₂ did not increase. Leafminer densities per 0.1143 m² of litterfall for Q. myrtifolia and Q. chapmanii were initially lower under elevated CO₂. However, shortly after canopy closure in 2001, leafminer densities per 0.1143 m² of litter fall became higher under elevated CO₂ and remained higher for the remainder of the experiment. Leaftier densities per 0.1143 m² were also higher under elevated CO₂ for Q. myrtifolia and Q. chapmanii over the last 6 years of the experiment. There were no differences in leafminer or leaftier densities per 0.1143 m² of litter for Q. geminata. These results show three phenomena. First, they show that elevated CO₂ decreases herbivory on all oak species in the Florida scrub‐oak system. Second, despite lower numbers of herbivores per 200 leaves in elevated CO₂, increased leaf production resulted in higher herbivore densities per unit area of leaf litter for two oak species. Third, they corroborate other studies which suggest that the effects of elevated CO₂ on herbivores are species specific, meaning they depend on the particular plant species involved. Two oak species showed increases in leaf production and herbivore densities per 0.1143 m² in elevated CO₂ over time while another oak species did not. Our results point to a future world of elevated CO₂ where, despite lower plant herbivory, some insect herbivores may become more common.     

Will chemical defenses become more effective against specialist herbivores under elevated CO2?

Elevated atmospheric CO₂ is known to affect plant–insect herbivore interactions. Elevated CO₂ causes leaf nitrogen to decrease, the ostensible cause of herbivore compensatory feeding. CO₂ may also affect herbivore consumption by altering chemical defenses via changes in plant hormones. We considered the effects of elevated CO₂, in conjunction with soil fertility and damage (simulated herbivory), on glucosinolate concentrations of mustard (Brassica nigra) and collard (B. oleracea var. acephala) and the effects of leaf nitrogen and glucosinolate groups on specialist Pieris rapae consumption. Elevated CO₂ affected B. oleracea but not B. nigra glucosinolates; responses to soil fertility and damage were also species‐specific. Soil fertility and damage also affected B. oleracea glucosinolates differently under elevated CO₂. Glucosinolates did not affect P. rapae consumption at either CO₂ concentration in B. nigra, but had CO₂‐specific effects on consumption in B. oleracea. At ambient CO₂, leaf nitrogen had strong effects on glucosinolate concentrations and P. rapae consumption but only gluconasturtiin was a feeding stimulant. At elevated CO₂, direct effects of leaf nitrogen were weaker, but glucosinolates had stronger effects on consumption. Gluconasturtiin and aliphatic glucosinolates were feeding stimulants and indole glucosinolates were feeding deterrents. These results do not support the compensatory feeding hypothesis as the sole driver of changes in P. rapae consumption under elevated CO₂. Support for hormone‐mediated CO₂ response (HMCR) was mixed; it explained few treatment effects on constitutive or induced glucosinolates, but did explain patterns in SEMs. Further, the novel feeding deterrent effect of indole glucosinolates under elevated CO₂ in B. oleracae underscores the importance of defensive chemistry in CO₂ response. We speculate that P. rapae indole glucosinolate detoxification mechanisms may have been overwhelmed under elevated CO₂ forcing slowed consumption. Specialists may have to contend with hosts with poorer nutritional quality and more effective chemical defenses under elevated CO₂.     

Leaf quality and insect herbivory in model tropical plant communities after long-term exposure to elevated atmospheric CO2

Results from laboratory feeding experiments have shown that elevated atmospheric carbon dioxide can affect interactions between plants and insect herbivores, primarily through changes in leaf nutritional quality occurring at elevated CO₂. Very few data are available on insect herbivory in plant communities where insects can choose among species and positions in the canopy in which to feed. Our objectives were to determine the extent to which CO₂-induced changes in plant communities and leaf nutritional quality may affect herbivory at the level of the entire canopy. We introduced equivalent populations of fourth instar Spodoptera eridania, a lepidopteran generalist, to complex model ecosystems containing seven species of moist tropical plants maintained under low mineral nutrient supply. Larvae were allowed to feed freely for 14 days, by which time they had reached the seventh instar. Prior to larval introductions, plant communities had been continuously exposed to either 340 l CO₂ l^–1 or to 610 l CO₂ l^–1 for 1.5 years. No major shifts in leaf nutritional quality [concentrations of N, total non-structural carbohydrates (TNC), sugar, and starch; ratios of: C/N, TNC/N, sugar/N, starch/N; leaf toughness] were observed between CO₂ treatments for any of the species. Furthermore, no correlations were observed between these measures of leaf quality and leaf biomass consumption. Total leaf area and biomass of all plant communities were similar when caterpillars were introduced. However, leaf biomass of some species was slightly greater-and for other species slightly less (e.g. Cecropia peltata)-in communities exposed to elevated CO₂. Larvae showed the strongest preference for C. peltata leaves, the plant species that was least abundant in all communites, and fed relatively little on plants species which were more abundant. Thus, our results indicate that leaf tissue quality, as described by these parameters, is not necessarily affected by elevated CO₂ under relatively low nutrient conditions. Hence, the potential importance of CO₂-induced shifts in leaf nutritional quality, as determinants of herbivory, may be overestimated for many plant communities growing on nutrient-poor sites if estimates are based on traditional laboratory feeding studies. Finally, slight shifts in the abundance of leaf tissue of various species occurring under elevated CO₂ will probably not significantly affect herbivory by generalist insects. However, generalist insect herbivores appear to become more dependent on less-preferred plant species in cases where elevated CO₂ results in reduced availability of leaves of a favoured plant species, and this greater dependency may eventually affect insect populations adversely.     

Effect of elevated CO2 on interactions betwe en the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) and the common milkweed, Asclepias syriaca

We measured the effect of elevated CO₂ on populations of the western flower thrips, Frankliniella occidentalis and on the amount of leaf damage inflicted by the thrips to one of its host plants, the common milkweed, Asclepias syriaca. Plants grown at elevated CO₂ had significantly greater aboveground biomass and C:N ratios, and significantly reduced percentage nitrogen. The number of thrips per plant was not affected by CO₂ treatment, but the density of thrips (numbers per gram aboveground biomass), was significantly reduced at high CO₂. Consumption by thrips, expressed as the amount of damaged leaf area per capita, was significantly greater at high CO₂, and the amount of leaf area damaged by thrips was increased by 33%. However overall leaf area at elevated CO₂ increased by 62%, more than compensating for the increase in thrips consumption. The net outcome was that plants at elevated CO₂ had 3.6 times more undamaged leaf area available for photosynthesis than plants at ambient CO₂, even though they had only 1.6 times the overall amount of leaf area. This study highlights the need for measuring the effects of herbivory at the whole-plant level and also the importance of taking herbivory into account when predicting plant responses to elevated CO₂. Received: 9 January 1996 /Accepted: 30 July 1996     

Long‐term evolutionary and ecological responses of calcifying phytoplankton to changes in atmospheric CO2

Calcifying phytoplankton play an important role in marine ecosystems and global biogeochemical cycles, affecting the transfer of both organic and inorganic carbon from the surface to the deep ocean. Coccolithophores are the most prominent members of this group, being well adapted to low‐nutrients environments (e.g., subtropical gyres). Despite urgent concerns, their response to rising atmospheric carbon dioxide levels (pCO₂) and ocean acidification is still poorly understood, and short‐term experiments may not extrapolate into longer‐term climatic adaptation. Current atmospheric pCO₂ (~390 ppmv) is unprecedented since at least 3 million years ago (Ma), and levels projected for the next century were last seen more than 34 Ma. Hence, a deep‐time perspective is needed to understand the long‐term effects of high pCO₂ on the biosphere. Here we combine a comprehensive fossil data set on coccolithophore cell size with a novel measure of ecological prominence: Summed Common Species Occurrence Rate (SCOR). The SCOR is decoupled from species richness, and captures changes in the extent to which coccolithophores were common and widespread, based on global occurrences in deep‐sea sediments. The size and SCOR records are compared to state‐of‐the‐art data on climatic and environmental changes from 50 to 5 Ma. We advance beyond simple correlations and trends to quantify the relative strength and directionality of information transfer among these records. Coccolithophores were globally more common and widespread, larger, and more heavily calcified in the pre‐34 Ma greenhouse world, and declined along with pCO₂ during the Oligocene (34–23 Ma). Our results suggest that atmospheric pCO₂ has exerted an important long‐term control on coccolithophores, directly through its availability for photosynthesis or indirectly via weathering supply of resources for growth and calcification.     

Invasive plant removal increases insect herbivory pressure on a native tree due to an increase in resource quality

Insect predator densities and plant nutritional status can affect insect herbivore densities, but these effects have not yet been assessed in the context of an invasive species management. This study investigated the influence of (i) altered predatory arthropod abundance and community composition (top-down-effects); and (ii) altered leaf nitrogen and phosphorus levels (bottom-up-effects) as possible causes of fluctuations in herbivore abundance and herbivory on the native tree Brabejum stellatifolium in riparian sites that differ in invasion status (near pristine, heavily invaded by Acacia mearnsii, and restored). Species richness, abundance and composition of herbivorous and predatory arthropods were compared between categories. Herbivore and predator abundance, species richness and assemblage composition were significantly influenced by invasion status. As expected, herbivore abundance was significantly and positively correlated to levels of leaf damage. Leaf nitrogen levels were the highest at restored sites where herbivorous arthropods were also most abundant and the abundance of predators was intermediate. These results suggest that altered leaf nitrogen content is likely a key influence for the increased herbivore pressure on B. stellatifolium at sites under pressure from invasive A. mearnsii and its status. Bottom-up influences therefore may be more important than top-down effects on controlling herbivore abundances in these altered riparian environments.

     

Seasonality of insect herbivory on the leaves of Neoboutonia macrocalyx in the Kibale National Park, Uganda

The seasonality of herbivory on the leaves of Neoboutonia macrocalyx Pax. in Kibale Forest National Park, Uganda, was studied. A total of 2929 fallen leaves was collected during 15 months under randomly-selected trees in three different habitats; natural forest and two selectively cut forest sites. The percentage of leaf area eaten and leaf size were estimated. Leaf herbivory was highly seasonal and correlated with rainfall in the previous 2 months, but less than 100 mm monthly rainfall had no effect. There was no correlation between leaf size and rainfall. Although Kibale Forest has two wet seasons, insect feeding on leaves had only one peak during the major rainy season from September to December. Three to four months after peak herbivory, leaves had very low rates of insect damage. Habitat had only a small effect on the amount of insect feeding. The sampling time accounted for 71% of variation in leaf herbivory. New leaves were formed continuously year-round. The constant leaf production by Neoboutonia trees may be an adaptation to escape generalist herbivorous insects which might be synchronized with the major wet season when the leaf flush of the most other deciduous species occurs. Thus, the availability of fresh leaves is not acting as a regulating factor in seasonality of Neoboutonia herbivory.     

Effects of amount and recurrence of leaf herbivory on the induction of direct and indirect defences in wild cotton

• The induction of defences in response to herbivory is a key mechanism of plant resistance. While a number of studies have investigated the time course and magnitude of plant induction in response to a single event of herbivory, few have looked at the effects of recurrent herbivory. Furthermore, studies measuring the effects of the total amount and recurrence of herbivory on both direct and indirect plant defences are lacking. To address this gap, here we asked whether insect leaf herbivory induced changes in the amount and concentration of extrafloral nectar (an indirect defence) and concentration of leaf phenolic compounds (a direct defence) in wild cotton (Gossypium hirsutum).
• We conducted a greenhouse experiment where we tested single event or recurrent herbivory effects on defence induction by applying mechanical leaf damage and caterpillar (Spodoptera frugiperda) regurgitant.
• Single events of 25% and 50% leaf damage did not significantly influence extrafloral nectar production or concentration. Extrafloral nectar traits did, however, increase significantly relative to controls when plants were exposed to recurrent herbivory (two episodes of 25% damage). In contrast, phenolic compounds increased significantly in response to single events of  leaf damage but not to recurrent damage. In addition, we found. that local induction of extrafloral nectar production was stronger than systemic induction, whereas the reverse pattern was observed for phenolics.
• Together, these results reveal seemingly inverse patterns of induction of direct and indirect defences in response to herbivory in wild cotton.

     

The Herbivore Assemblage, Herbivory and Leaf Chemistry of the Mangrove Kandelia obovata in Two Contrasting Forests in Hong Kong

The herbivore assemblage, intensity of herbivory and factors determining herbivory levels on the mangrove Kandelia obovata (previously K. candel, Rhizophoraceae) were studied over a 13-month period at two forests with contrasting growing conditions in Hong Kong. Mai Po was part of an eutrophic embayment in the Pearl River estuary and generally offered more favourable conditions for mangrove growth, whereas Ting Kok had a rocky substratum and oceanic salinity. Twenty-four insect herbivore species were recorded on K. obovata, with lepidopteran larvae that consume leaf lamina being the dominant species. While leaf litter production was similar at the two forests, herbivory level at Mai Po (mean = 3.9% in terms of leaf area loss) was more severe than that at Ting Kok (mean = 2.3%). Peak herbivory levels were found in summer at both locations (6.5% for Mai Po and 3.8% for Ting Kok). Young leaves of K. obovata at both locations were generally preferred by the herbivores from the period of late spring to summer. Concentrations of most feeding deterrents (ash, crude fibre, and total soluble tannins) were significantly higher in both young and mature leaves at Ting Kok, whereas leaf nutrients (total nitrogen and water) were the same at the two sites. Young leaves at Ting Kok contained about 30% more tannins than their counterparts at Mai Po. Significant differences in leaf chemistry also existed between young and mature leaves at either site. The differences were concomitant with the observed patterns of leaf herbivory on K. obovata, and suggest a potential relationship between environmental quality and plant defence against herbivory.     

Testing the enemy release hypothesis: a comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. saccharum L.)

Norway maple (Acer platanoides) is a Eurasian introduced tree species which has invaded the North American range of its native congener, sugar maple (A. saccharum). One hypothesis used to explain the success of an invasive species is the enemy release hypothesis (ERH), which states that invasive species are often particularly successful in their new range because they lack the enemies of their native range. In this study, we hypothesized that Norway maple would have less insect damage than sugar maple due to such enemy release. Autumn 2005 and summer 2006 leaves of Norway and sugar maple were collected from six sites in New Jersey and Pennsylvania to compare percent leaf area loss, gall damage, fungal damage, and specific leaf area (cm²/g). Although both species had low overall mean levels of leaf damage (0.4–2.5%), in both years/seasons Norway maple had significantly less leaf damage than sugar maple. Insects were also collected to compare insect assemblies present on each tree species. The numbers of insect taxa and individuals found on each species were nearly equivalent. Overall, the results of this study are consistent with the enemy release hypothesis for Norway maple. In addition, sugar maples when surrounded by Norway maples tended to show reduced herbivory. This suggests that the spread of Norway maple in North America, by reducing amounts of insect herbivory, may have further ecosystem-wide impacts.     

Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic–Cambrian changes in atmospheric composition

Photosynthetic uptake of inorganic carbon can raise the pH adjacent to cyanobacterial cells, promoting CaCO₃ precipitation. This effect is enhanced by CO₂ concentrating mechanisms that actively transport into cells for carbon fixation. CO₂ concentrating mechanisms presumably developed in response to atmospheric decrease in CO₂ and increase in O₂ over geological timescales. In present‐day cyanobacteria, CO₂ concentrating mechanisms are induced when the atmospheric partial pressure of CO₂ (p_CO2) falls below ～0.4%. Reduction in p_CO2 during the Proterozoic may have had two successive effects on cyanobacterial calcification. First, fall in p_CO2 below ～1% (33 times present atmospheric level, PAL) resulted in lower dissolved inorganic carbon (DIC) concentrations that reduced pH buffering sufficiently for isolated CaCO₃ crystals to begin to nucleate adjacent to cyanobacterial cells. As a result, blooms of planktic cyanobacteria induced precipitated ‘whitings’ of carbonate mud in the water column whose sedimentary accumulation began to dominate carbonate platforms ～1400–1300 Ma. Second, fall in p_CO2 below ～0.4% (10 PAL) induced CO₂‐concentrating mechanisms that further increased pH rise adjacent to cells and promoted in vivo cyanobacterial sheath calcification. Crossing of this second threshold is indicated in the fossil record by the appearance of Girvanella 750–700 Ma. Coeval acquisition of CO₂ concentrating mechanisms by planktic cyanobacteria further stimulated whiting production. These inferences, that p_CO2 fell below ～1%～1400–1300 Ma and below ～0.4% 750–700 Ma, are consistent with empirical and modelled palaeo‐atmosphere estimates. Development of CO₂ concentrating mechanisms was probably temporarily slowed by global cooling ～700–570 Ma that favoured diffusive entry of CO₂ into cells. Lower levels of temperature and DIC at this time would have reduced seawater carbonate saturation state, also hindering cyanobacterial calcification. It is suggested that as Earth emerged from ‘Snowball’ glaciations in the late Neoproterozoic, global warming and O₂ rise reactivated the development of CO₂ concentrating mechanisms. At the same time, rising levels of temperature, calcium ions and DIC increased seawater carbonate saturation state, stimulating widespread cyanobacterial in vivo sheath calcification in the Early Cambrian. This biocalcification event promoted rapid widespread development of calcified cyanobacterial reefs and transformed benthic microbial carbonate fabrics.     

Environmental and genetic control of insect abundance and herbivory along a forest elevational gradient

Environmental conditions and plant genotype may influence insect herbivory along elevational gradients. Plant damage would decrease with elevation as temperature declines to suboptimal levels for insects. However, host plants at higher elevations may exhibit traits that either reduce or enhance leaf quality to insects, with uncertain net effects on herbivory. We examined folivory, insect abundance and leaf traits along six replicated elevational ranges in Nothofagus pumilio forests of the northern Patagonian Andes, Argentina. We also conducted a reciprocal transplant experiment between low- and high-elevation sites to test the extent of environmental and plant genetic control on insect abundance and folivory. We found that insect abundance, leaf size and specific leaf area decreased, whereas foliar phosphorous content increased, from low-, through mid- to high-elevation sites. Path analysis indicated that changes in both insect abundance and leaf traits were important in reducing folivory with increasing elevation and decreasing mean temperature. At both planting sites, plants from a low-elevation origin experienced higher damage and supported greater insect loads than plants from a high-elevation origin. The differences in leaf damage between sites were twofold larger than those between plant origins, suggesting that local environment was more important than host genotype in explaining folivory patterns. Different folivore guilds exhibited qualitatively similar responses to elevation. Our results suggest an increase in insect folivory on high-elevation N. pumilio forests under future climate warming scenarios. However, in the short-term, folivory increases might be smaller than expected from insect abundance only because at high elevations herbivores would encounter more resistant tree genotypes.     

Testing for the effects and consequences of mid paleogene climate change on insect herbivory

Background

The Eocene, a time of fluctuating environmental change and biome evolution, was generally driven by exceptionally warm temperatures. The Messel (47.8 Ma) and Eckfeld (44.3 Ma) deposits offer a rare opportunity to take a census of two, deep-time ecosystems occurring during a greenhouse system. An understanding of the long-term consequences of extreme warming and cooling events during this interval, particularly on angiosperms and insects that dominate terrestrial biodiversity, can provide insights into the biotic consequences of current global climatic warming.

Methodology/Principal Findings

We compare insect-feeding damage within two middle Eocene fossil floras, Messel and Eckfeld, in Germany. From these small lake deposits, we studied 16,082 angiosperm leaves and scored each specimen for the presence or absence of 89 distinctive and diagnosable insect damage types (DTs), each of which was allocated to a major functional feeding group, including four varieties of external foliage feeding, piercing- and-sucking, leaf mining, galling, seed predation, and oviposition. Methods used for treatment of presence–absence data included general linear models and standard univariate, bivariate and multivariate statistical techniques.

Conclusions/Significance

Our results show an unexpectedly high diversity and level of insect feeding than comparable, penecontemporaneous floras from North and South America. In addition, we found a higher level of herbivory on evergreen, rather than deciduous taxa at Messel. This pattern is explained by a ca. 2.5-fold increase in atmospheric CO₂ that overwhelmed evergreen antiherbivore defenses, subsequently lessened during the more ameliorated levels of Eckfeld times. These patterns reveal important, previously undocumented features of plant-host and insect-herbivore diversification during the European mid Eocene.     

CO2‐mediated changes of plant traits and their effects on herbivores are determined by leaf age

1. Concentration of atmospheric CO₂ is predicted to double during the 21st century. However, quantitative effects of increased CO₂ levels on natural herbivore–plant interactions are still little understood. 2. In this study, we assess whether increased CO₂ quantitatively affects multiple defensive and nutritive traits in different leaf stages of cyanogenic wildtype lima bean plants (Phaseolus lunatus), and whether plant responses influence performance and choice behaviour of a natural insect herbivore, the Mexican bean beetle (Epilachna varivestis). 3. We cultivated lima bean plants in climate chambers at ambient, 500, 700, and 1000 ppm CO₂ and analysed cyanogenic precursor concentration (nitrogen‐based defence), total phenolics (carbon‐based defence), leaf mass per area (LMA; physical defence), and soluble proteins (nutritive parameter) of three defined leaf age groups. 4. In young leaves, cyanide concentration was the only parameter that quantitatively decreased in response to CO₂ treatments. In intermediate and mature leaves, cyanide and protein concentrations decreased while total phenolics and LMA increased. 5. Depending on leaf stage, CO₂‐mediated changes in leaf traits significantly affected larval performance and choice behaviour of adult beetles. We observed a complete shift from highest herbivore damage in mature leaves under natural CO₂ to highest damage of young leaves under elevated CO_2. Our study shows that leaf stage is an essential factor when considering CO₂‐mediated changes of plant defences against herbivores. Since in the long run preferred consumption of young leaves can strongly affect plant fitness, variable effects of elevated CO₂ on different leaf stages should receive highlighted attention in future research.     

Leaf age effects of elevated CO2-grown white oak leaves on spring-feeding lepidopterans

Folivorous insect responses to elevated CO₂-grown tree species may be complicated by phytochemical changes as leaves age. For example, young expanding leaves in tree species may be less affected by enriched CO₂-alterations in leaf phytochemistry than older mature leaves due to shorter exposure times to elevated CO₂ atmospheres. This, in turn, could result in different effects on early vs. late instar larvae of herbivorous insects. To address this, seedlings of white oak (Quercus alba L.), grown in open-top chambers under ambient and elevated CO₂, were fed to two important early spring feeding herbivores; gypsy moth (Lymantria dispar L.), and forest tent caterpillar (Malacosoma disstria Hübner). Young, expanding leaves were presented to early instar larvae, and older fully expanded or mature leaves to late instar larvae. Young leaves had significantly lower leaf nitrogen content and significantly higher total nonstructural carbohydrate:nitrogen ratio as plant CO₂ concentration rose, while nonstructural carbohydrates and total carbon-based phenolics were unaffected by plant CO₂ treatment. These phytochemical changes contributed to a significant reduction in the growth rate of early instar gypsy moth larvae, while growth rates of forest tent caterpillar were unaffected. The differences in insect responses were attributed to an increase in the nitrogen utilization efficiency (NUE) of early instar forest tent caterpillar larvae feeding on elevated CO₂-grown leaves, while early instar gypsy moth larval NUE remained unchanged among the treatments. Later instar larvae of both insect species experienced larger reductions in foliage quality on elevated CO₂-grown leaves than earlier instars, as the carbohydrate:nitrogen ratio of leaves substantially increased. Despite this, neither insect species exhibited changes in growth or consumption rates between CO₂ treatments in the later instar. An increase in NUE was apparently responsible for offsetting reduced foliar nitrogen for the late instar larvae of both species.     

Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats

According to the associational resistance hypothesis, neighbouring plants are expected to influence both the insect herbivore communities and their natural enemies. However, this has rarely been tested for the effects of canopy trees on herbivory of seedlings. One possible mechanism responsible for associational resistance is the indirect impact of natural enemies on insect herbivory, such as insectivorous birds. But it remains unclear to what extent such trophic cascades are influenced by the composition of plant associations (i.e. identity of ‘associated’ plants). Here, we compared the effect of bird exclusion on insect leaf damage for seedlings of three broadleaved tree species in three different forest habitats. Exclusion of insectivorous birds affected insect herbivory in a species-specific manner: leaf damage increased on Betula pendula seedlings whereas bird exclusion had no effect for two oaks (Quercus robur and Q. ilex). Forest habitat influenced both the extent of insect herbivory and the effect of bird exclusion. Broadleaved seedlings had lower overall leaf damage within pine plantations than within broadleaved stands, consistent with the resource concentration hypothesis. The indirect effect of bird exclusion on leaf damage was only significant in pine plantations, but not in exotic and native broadleaved woodlands. Our results support the enemies hypothesis, which predicts that the effects of insectivorous birds on insect herbivory on seedlings are greater beneath non-congeneric canopy trees. Although bird species richness and abundance were greater in broadleaved woodlands, birds were unable to regulate insect herbivory on seedlings in forests of more closely related tree species.