Dieback of rural eucalypts: the effect of stress on the nutritional quality of foliage

Canopy dieback of Eucalyptus blakelyi trees is often associated with defoliation by insects: the foliage of trees with dieback is nutritionally superior for insects and is more heavily damaged by them. I investigated whether differences in the nutritional quality of foliage were genetically determined, or caused by environmental stress. In a series of glasshouse experiments, with seedlings and grafted plants derived from dieback and healthy populations of trees. I tested the influence of deprivation of nutrients, drought, waterlogging, saline waterlogging and addition of excess phosphate, on the nutritional quality of foliage. Differences in the foliar properties of plants from different genetic sources were not consistent with the differences between the source populations. Most of the environmental stresses applied caused a reduction in foliar quality (decreased water and nitrogen contents, and increased specific leaf weights). I hypothesize that the enhanced nutritional quality of the foliage of dieback trees is more likely to be a consequence of benign growing conditions (e.g. improved soil fertility) than of environmental stress. Field data for soil properties and the effect of drought on mature trees are consistent with this view.     

Dieback of rural eucalypts: Response of foliar dietary quality and herbivory to defoliation

Rural dieback of Eucalyptus blakelyi trees growing on pastoral properties near Canberra is associated with chronic defoliation by insects. In order to test the effect of defoliation on subsequent herbivory, I artificially defoliated three healthy trees by clipping their terminal branchlets. The foliage that regrew on the clipped trees was nutritionally superior to the foliage it replaced, and was much more heavily damaged by grazing insects. There was a transient increase in the tannin content of the regrowth foliage, but this was apparently ineffective in defending it from subsequent herbivory. Compared with the foliage on nearby E. blakelyi trees that also produced major flushes of leaf growth during the same period, the regrowth on the clipped trees had enhanced dietary qualities and suffered more insect damage. Leaf age contributed to many of the differences in dietary quality, but when adjustments were made for the effects of leaf age the same trends remained. Five of the nearby trees were suffering from the chronic insect grazing associated with rural dieback, and the other five appeared healthy. The dietary quality of regrowth foliage on the clipped trees was qualitatively more similar to that of foliage on the dieback trees. Thus the chronic herbivory associated with rural dieback may be partly self-perpetuating, given this positive feedback between defoliation and dietary quality, and an apparent absence of other effective controls on insect populations.     

The biomass of New England peppermint (Eucalyptus nova-anglica) in relation to insect damage associated with rural dieback

Two adjacent mature trees of New England peppermint (Eucalyptus nova-anglica) were harvested with the aid of a cherry picker to determine their biomass distribution and insect damage. One suffered from obvious symptoms of rural dieback and the other was healthy. Weights of foliage and wood were measured, and insect damage for all leaves and branches was quantified. For each tree 25% of the roots were extracted from the soil using a bulldozer and manual methods; they were then weighed and damage by insects estimated. The healthy tree lost more leaf surface area to insects (11% or 1.1 kg vs 9.2% or 0.3 kg); but the dieback tree had four times more wood affected by boring insects (19% cf. 5%); and only 20% root biomass remaining (92 kg cf. 488 kg). The accuracy of sampling techniques needed to measure defoliation and the consequences of insect damage to dieback of rural eucalypts are discussed.     

Dieback of rural eucalypts: Does insect herbivory relate to dietary quality of tree foliage?

Foliar dietary quality, and the damage that insects caused to the foliage of dieback-affected and healthy Eucalyptus blakelyi trees, were monitored for 3 years, on pastoral properties in the Australian Capital Territory. Compared with healthy trees, the foliage of dieback trees was more heavily grazed by insects, and its dietary quality was generally superior. Some of the differences in dietary quality were related to the average age of the foliage of healthy and dieback trees. But when statistical models were used to equalize the effects of differences in leaf ages, leaves on dieback trees nonetheless tended to have lower specific weights, and were sometimes rounder and contained more nitrogen. Regression analyses of herbivory against each of the dietary quality variables showed that the only significant relationship that was consistent for both of the years monitored was for foliar nitrogen and herbivory for both dieback and healthy trees. In the first year, regressions between herbivory and specific leaf weight, shape, or sugar content were also significant, but only amongst the dieback trees. This may indicate that these relationships were a response to, rather than a primary cause of, the repeated high defoliation of the dieback trees. Multiple regression equations incorporating annual means of several quality variables explained a high proportion of the variance in annual herbivory, but were grossly different between years.     

Dieback of rural eucalypts: Tree phenology and damage caused by leaf-feeding insects

During three growing seasons, phenology and damage on leafy shoots of healthy eucalypts and others with dieback were monitored on pastoral properties in the Australian Capital Territory. Leaves from the dieback trees tended to be younger than those from nearby healthy trees. Leaves that were not lost prematurely lived for similar lengths of time on both dieback and healthy trees, but more leaves were initiated on the dieback trees. Dieback trees were also less active reproductively. During the study, chewing insects caused most of the damage on leaves, and there was usually more of this damage on leaves from the dieback trees. Young leaves accumulated damage at a much faster rate than older leaves, and this probably contributed to the relatively greater damage on the leaves from the dieback trees. However, the differences in the amount of damage on the leaves from healthy and dieback trees were not solely due to the differences in ages of the leaves. Generalized linear models which equalized the effects of the differences in leafing phenology produced adjusted estimates for damage to leaves that were still higher for dieback trees.     

Nutrient stress: an explanation for plant anti-herbivore responses to defoliation

Summary A hypothesis is put forward that the long-lasting inducible responses of trees to herbivores, particularly lepidopteran defoliators, may not be active defensive responses, but a by-product of mechanisms which rearrange the plant carbon/nutrient balance in response to nutrient stress caused by defoliation. When defoliation removes the foliage nutrients of trees growing in nutrient-poor soils, it increases nutrient stress wich in turn results in a high production of carbon-based allelochemicals. The excess of carbon that cannot be diverted to growth due to nutrient stress is diverted to the production of plant secondary metabolites. The level of carbon-based secondary substances decays gradually depending on the rate at which nutrient stress is relaxed after defoliation. In nutrient-poor soils and in plant species with slow compensatory nutrient uptake rates the responses induced by defoliation can have relaxation times of several years. The changes in leaf nitrogen and phenolic content of mountain birch support this nutrient stress hypothesis. Defoliation reduces leaf nitrogen content while phenolic content increases. These responses of mountain birch to defoliation are relaxed within 3–4 years.     

Altitudinal patterns in host suitability for forest insects

Conspecific trees growing at high and low-elevations encounter different growing conditions and may vary in their suitability as hosts for herbivorous insects. Mountain tree populations may be more resistant to herbivory if low temperatures constrain growth more than they constrain photosynthesis, resulting in increased secondary metabolism (temperature hypothesis). Alternatively, mountain trees may be fertilized by atmospheric nitrogen deposition and become more palatable to insects (atmospheric deposition hypothesis). We evaluated these two hypotheses by comparing high- and low-elevation trees with insect bioassays and analyses of foliar nitrogen and condensed tannin. Contrary to the temperature hypothesis, high-elevation foliage had higher leaf nitrogen (six of six tree species) and allowed higher growth rates of Lymantria dispar larvae (five of six tree species). The nitrogen deposition hypothesis was broadly supported by measurements from two mountains showing that high-elevation trees tended to have higher leaf nitrogen, lower leaf tannins, and support higher insect growth performance than conspecific trees from lower elevations. The deposition hypothesis was further supported by fertilization studies showing that simulated atmospheric nitrogen deposition changed the foliar chemistry of valley trees to resemble that of high-elevation trees. Predictions that the altitudinal gradient in foliar chemistry and host suitability should be steepest on mountains receiving more deposition were largely not supported, but interpretations are complicated by lack of replication among mountains. In the northeastern United States, increased host suitability of high-elevation trees seems sufficient to influence the population dynamics and community composition of herbivores. Atmospheric nitrogen deposition offers a promising hypothesis to explain and predict some important spatial patterns in herbivory. Received: 21 September 1997 / Accepted: 12 June 1998     

Influence of leaf traits on the spatial distribution of insect herbivores associated with an overstorey rainforest tree

Summary The spatial distribution of insect herbivores associated with the Australian rainforest treeArgyrodendron actinophyllum (Sterculiaceae) was investigated by restricted canopy fogging. The foliage of this species was low in nitrogen and water content, and high in fibre content. Herbivore abundance was positively correlated with the amount of young foliage present within the samples and in adjacent samples, and with the nitrogen content of young leaves. In particular, the occurrence of phloem-feeders was correlated with the magnitude of translocation within the samples. The influence of leaf water content upon herbivore distribution was marginal, presumably because this factor is not limiting in rain-forest environments during the wet season, which usually coincides with the season of leaf-flush. Specific leaf weight, leaf size and foliage compactness had little or no apparent effect on herbivore distribution. Since the magnitude of leaf turnover affected both the quantity and the quality, as exemplified by translocation effects, of young foliage available, this factor may be critical to herbivores associated with evergreen rainforest trees which are particularly low in foliar nutrients, such asA. actinophyllum.     

Interplant variation in creosotebush foliage characteristics and canopy arthropods

Summary We conducted a field study to test the hypothesis that creosotebush (Larrea tridentata) shrubs growing in naturally nutrient-rich sites had better quality foliage and supported greater populations of foliage arthropods than shrubs growing in nutrient-poor sites. Nutrient-rich sites had significantly higher concentrations of soil nitrogen than nutrient-poor sites. Multivariate analysis of variance revealed significant differences between high nutrient and low nutrient shrubs based on a number of structural and chemical characteristics measured. High nutrient shrubs were larger, had denser foliage, greater foliage production, higher concentrations of foliar nitrogen and water, and lower concentrations of foliar resin than low nutrient shurbs. Numbers of foliage arthropods, particularly herbivores and predators, were significantly higher on high nutrient shrubs. Shrub characteristics and foliage arthropod abundances varied considerably from shrub to shrub. Shrub characteristics representing shrub size, foliage density, foliage growth, and foliar nitrogen and water concentrations were positively correlated with arthropod abundances. Foliar resin concentrations were negatively correlated with foliage arthropod abundances. The positive relationship between creosotebush productivity and foliage arthropods is contradictory to the tenet that physiologically stressed plants provide better quality foliage to insect herbivores.     

The effect of previous defoliation of pole-stage lodgepole pine on plant chemistry,and on the growth and survival of pine beauty moth (Panolis flammea) larvae

Summary A study of the effects of defoliation by insects on the chemistry of lodgepole pine (Pinus contorta), and on the performance of Panolis flammea (Lepidoptera; Noctuidae) larvae, was carried out in a forest in northwest Scotland I year after a severe outbreak of P. flammea had caused extensive defoliation. Larval weight and survival were not significantly different on trees that had experienced different levels of defoliation in 1986. The nitrogen and tannin content of current and previous years' pine needles was not significantly affected by defoliation (although both were slightly greater in the foliage of defoliated trees). Phosphorus content of young pine foliage was lower (but not significantly lower except on one occasion) on heavily defoliated trees. On all sampling occasions, however, the nitrogen: phosphorus ratio was significantly higher on heavily defoliated trees. There were large differences in monoterpene composition of the previous year's shoots associated with defoliation intensity, but these differences had largely disappeared in the new growth. The results are discussed in relation to other studies on the effects of insect damage on plant chemistry and insect performance and in relation to the abundance of P. flammea in Scotland.     

Variation in foliar nutrients in Eucalyptus trees in eastern and Western Australia

Abstract Levels of nitrogen, phosphorus and potassium were measured for the foliage of two co-dominant eucalypts at each of two sites, one in eastern Australia and the other in Western Australia. In eastern Australia, foliage was sampled in the canopy and subcanopy for narrow-leaved ironbark Eucalyptus crebra and grey box E. mollucana and in Western Australia, for jarrah E. marginata and marri E. calophylla. The Western Australian trees were also sampled for ‘young’ and ‘old’ leaves. Both eucalypts in eastern Australia had greater nitrogen and phosphorus levels, but lower potassium, than E. marginata or E. calophylla. Eucalyptus calophylla foliage had greater levels of all three nutrients than E. marginata foliage as did E. crebra relative to E. mollucana. At both sites, foliar nutrient levels were greater in the canopy than subcanopy foliage, and, at least in Western Australia, the younger leaves had greater nutrient levels than the older leaves. The observed differences in foliar nutrient levels are consistent with observed trends in the abundance and diversity of foliage arthropods and the use of the trees as foraging substrates by birds.     

The role of psyllids (Hemiptera: Psyllidae) and bell miners (Manorina melanophrys) in canopy dieback of Sydney blue gum (Eucalyptus saligna Sm.)

Abstract The presence of the aggressive, colony-forming honeyeater, Manorina melanophrys (bell miner), in the canopies of unhealthy eucalypts has been well reported. There is, however, some debate as to the actual mechanisms producing these unhealthy trees. To investigate further some of the processes that may be contributing to this form of canopy dieback, two field trials were carried out in Olney State Forest, near Wyong, New South Wales. The study site contained Eucalyptus saligna (Sydney blue gum) with canopy dieback and was occupied by a large colony of bell miners. Close examination of the foliage revealed a large and diverse suite of phytophagous insects, including at least 16 species of psyllid (Hemiptera: Psyllidae). In the first trial, the use of bird exclusion cages over selected branches significantly improved leaf survival compared to leaves exposed to a relatively high density of bell miners. It is proposed that colonization by bell miners may interfere with the efficacy of both other insectivorous birds (through aggressive interspecific territoriality) and the invertebrate predators and parasitoids. Interference with such regulatory factors may enable some phytophagous insect populations to rise to sustained damaging levels. In the second trial, an insecticide application combined with reduced competition from the dense understorey and neighbouring trees was required to significantly improve trunk diameter and crown condition scores. After 12 months, neither treatment, by itself, significantly improved both growth measures. Possibly both treatments were required because the E. saligna trees were suffering from another source of stress (e.g. drought) in addition to the relatively high level of insect attack.     

Drought and dieback of rural eucalypts

The possibility that drought causes dieback of eucalypts in rural Australia was investigated. Water potential and canopy condition in dieback and healthy rural Eucalyptus blakelyi and E. melliodora trees were compared during and after an extreme drought in the ACT. All the trees were drought affected, but the extent was independent of the condition of their canopies at the beginning of the study.     

Foliage phenols and nitrogen in relation to growth,insect damage,and ability to recover after defoliation,in the mountain birch Betula pubescens ssp tortuosa

We studied growth of the mountain birch, and the role of foliage phenols, nitrogen, and variance in the timing of bud burst, as potential defensive characters, in Finnish Lapland in 1975–1979. Annual and local variation both in phenol and nitrogen concentration of foliage were significant. Individual trees retained their position in the foliage and nitrogen distribution of the population in successive years, as well as in the order of leaf flush in spring. Growth of twigs, mature leaf size, and ability of trees to recover in the year following artificial defoliation correlated positively with the sum of degree days in the previous growing season. Foliage nitrogen correlated negatively with foliage phenols in within-site comparisons. Twig growth correlated negatively with foliage phenols, particularly in growing seasons following cool summers, but did not correlate with foliage nitrogen. Birches flushing early did not grow more than birches flushing late. Between-site differences in foliage phenol content were mainly determined by abiotic conditions, like temperature and nutrient availability. In a between-site comparison insect chewing marks in leaves correlated positively with foliage phenols as well as with nitrogen; intensity of invertebrate predation presumably explained variable herbivory between the sites. In a within-site comparison trees with the highest foliage phenol content had few herbivores only at the site with the highest average phenol level.     

Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest

This study evaluated whether herbivorous insects can be expected to have particular adaptations to withstand the harsh dry season in tropical dry forests (TDFs). We specifically investigated a possible escape in space, with herbivorous insects moving to the few evergreen trees that occur in this ecosystem; and escape in time, with herbivores presenting an increased nocturnal rather than diurnal activity during the dry season. We determined the variation in the free-feeding herbivorous insects (sap-sucking and leaf chewing) between seasons (beginning and middle of both rainy and dry seasons), plant phenological groups (deciduous and evergreen trees) and diel period (diurnal and nocturnal) in a Brazilian TDF. We sampled a total of 5827 insect herbivores in 72 flight-interception traps. Contrary to our expectations, we found a greater herbivore diversity during the dry season, with low species overlap among seasons. In the dry season, evergreen trees supported greater richness and abundance of herbivores as compared to deciduous trees. Insects were also more active at night during the dry season, but no diel differences in insect abundance were detected during the rainy season. These results indicate that the strategies used by insect herbivores to withstand the severe climatic conditions of TDFs during the dry season include both small-scale escape in space and time, with evergreen trees playing a key role in maintaining resident insect herbivore populations in TDFs. Relatively more nocturnal activity during the dry season may be related to the avoidance of harsh climatic conditions during the day. We suggest that the few evergreen tree species occurring in the TDF landscape should be especially targeted for protection in this threatened ecosystem, given their importance for insect conservation.     

Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance

We examined the effects of CO₂ and defoliation on tree chemistry and performance of the forest tent caterpillar, Malacosoma disstria. Quaking aspen (Populus tremuloides) and sugar maple (Acer saccharum) trees were grown in open-top chambers under ambient or elevated concentrations of CO₂. During the second year of growth, half of the trees were exposed to free-feeding forest tent caterpillars, while the remaining trees served as nondefoliated controls. Foliage was collected weekly for phytochemical analysis. Insect performance was evaluated on foliage from each of the treatments. At the sampling date coincident with insect bioassays, levels of foliar nitrogen and starch were lower and higher, respectively, in high CO₂ foliage, and this trend persisted throughout the study. CO₂-mediated increases in secondary compounds were observed for condensed tannins in aspen and gallotannins in maple. Defoliation reduced levels of water and nitrogen in aspen but had no effect on primary metabolites in maple. Similarly, defoliation induced accumulations of secondary compounds in aspen but not in maple. Larvae fed foliage from the enriched CO₂ or defoliated treatments exhibited reduced growth and food processing efficiencies, relative to larvae on ambient CO₂ or nondefoliated diets, but the patterns were host species-specific. Overall, CO₂ and defoliation appeared to exert independent effects on foliar chemistry and forest tent caterpillar performance.     

The impact of defoliation on the foliar chemistry of southern rātā (

Brushtail possums (Trichosurus vulpecula) tend to eat young canopy foliage in southern rätä (Metrosideros umbellata), and browsing tends to be concentrated on only a few trees. Samples collected as part of an artificial defoliation experiment were analysed for NPK (nitrogen, phosphorus, and potassium), carbohydrate, and polyphenolic concentrations to determine whether changes in foliar chemistry associated with defoliation provide an explanation for these patterns of browsing. In non-defoliated trees, NPK concentrations were highest in young leaves and declined with age, while concentrations of carbohydrates and polyphenolics were independent of leaf age. Nitrogen, phosphorus and polyphenolic concentrations were consistently higher in canopy (sun) versus subcanopy (shade) foliage regardless of leaf age, a trend that was reversed for potassium. Partial (50%) defoliation had little effect on foliar chemistry, regardless of its timing. Total (100%) defoliation stimulated NPK concentrations and depressed condensed tannin concentrations of new foliage produced by the surviving shoots. These results suggest that brushtail possums may focus their feeding on only a few trees because of nutritional changes to leaves as a result of browsing.     

Influence of previous frost damage on tree growth and insect herbivory of Eucalyptus globulus globulus

The plant stress hypothesis suggests that some herbivores favour stressed plants, whereas the plant vigour hypothesis proposes that other herbivores prefer vigorous plants. The effects of a prior stress, that of frost damage, were examined on the subsequent growth of Eucalyptus globulus globulus and on the response of insect herbivores. Frost damage affected tree growth by reducing new leaf area and increasing specific leaf area (SLA). However, herbivore abundance was not affected by prior frost damage. Two feeding trials using Anoplognathus chloropyrus and Hyalarcta huebneri and a morphometric study of Ctenarytaina eucalypti were conducted to assess the performance of herbivores on trees that had suffered more or less frost damage. Consumption by A. chloropyrus and H. huebneri was unaffected by foliage origin (damaged versus healthy). Hyalarcta huebneri grew faster when fed leaves from previously damaged trees, and C. eucalypti from previously damaged trees were larger than those from healthy trees. Enhanced insect performance on frost damaged plants may have resulted from the high specific leaf area (most likely thinner) leaves. The herbivore abundance data did not support the hypothesis that previously frost damaged plants are preferred by insects. However, increased growth of H. huebneri and larger body size of C. eucalypti on damaged trees indicates that previously stressed trees may produce leaves of higher nutritional value.     

Regional and local variation in insect herbivory,vegetation and soils of eucalypt associations in contrasted landscape positions along a climatic gradient

Abstract Relationships with climate and local resources are developed for soils, vegetation and tree foliage as well as levels of herbivory for the dominant eucalypts at sites representing a regional gradient in climate and local contrasts in landscape position. Indicators of site productivity such as soil nitrogen and phosphorus, canopy height and cover, foliar nitrogen and water, and average leaf area tended to increase as climate became more favourable. Many were also higher in locally richer parts of the landscape. In contrast, specific leaf weight, an indication of sclerophylly, decreased as climate and local resources became more favourable. Rates of herbivory tended to increase with increasing site productivity and the associated changes in soil, vegetation and foliar properties, in broad agreement with models relating herbivory to resource availability and plant vigour. We found no evidence to support models relating high herbivory to low-resource environments and plant stress. The apparent level of herbivore damage on mature leaves was highest at intermediate levels of resources; this could reflect interactions between resource availability, rates of herbivory and rates of leaf replacement. Implications of these findings are discussed with respect to ways of measuring herbivory, regional patterns in rates and levels of herbivory, and the regional distribution of rural dieback associated with high herbivory.     

Decreased losses of woody plant foliage to insects in large urban areas are explained by bird predation

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.