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: 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.     

Water stress,leaf nutrients and defoliation: a model of dieback of rural eucalypts

Water stress, concentrations of foliar nutrients and damage of foliage by insects were studied over an eleven month period, for eight dieback eucalypts and eight closely matched healthy trees growing in close association on two grazing properties near Brisbane. Four healthy eucalypts in a neighbouring State Forest were also studied. The study region had suffered severe climatic stress between 1972 and 1976 when dieback was first observed by residents and when high populations of defoliating insects were observed. Dieback trees had a higher proportion of foliage damaged by insects and higher concentrations of foliar nutrients than did matched healthy trees. The study period was one of low climatic stress during which dieback and healthy trees followed similar seasonal patterns of predawn xylem pressure potential. Dieback trees developed lower daytime minimum xylem pressure potentials than did matched healthy trees, and differed in their stomatal responses. A model of initiation and development of rural eucalypt dieback is proposed. This may have general application to many non-specific rural diebacks in which heavy insect damage is implicated. The balance between rural eucalypts and their insect herbivores is precarious. Any factor capable of causing extensive defoliation, or an increase in foliar nitrogen, or an increase in populations of insect herbivores may upset this balance. A positive feedback loop may be activated, whereby the production of nitrogen rich epicormic foliage enhances a build up of insect populations. Repeated insect defoliation leads to tree dieback. Evidence in the literature supporting the model is reviewed and aspects requiring further research are outlined.     

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.     

Root growth response to defoliation in two Agropyron bunchgrasses: field observations with an improved root periscope

Summary Root growth responses to defoliation were observed in the field with an improved root periscope technique, which is described. The grazing tolerant, Eurasian bunchgrass, Agropyron desertorum, was compared with the very similar but grazing sensitive, North American bunchgrass, A. spicatum. Root length growth of clipped A. desertorum was about 50% of that of intact plants, while root elongation of clipped A. spicatum continued relatively unabated during ninety days of regrowth following severe defoliation. The reduced root growth in A. desertorum was correlated with the allocation of relatively more resources to aboveground regrowth, thus aiding reestablishment of the root: shoot balance. This balance was apparent in similar root mortality patterns of clipped and control A. desertorum plants in the season following defoliation. In clipped A. spicatum, however, root mortality increased in the winter following the season in which the clipping was done and continued into the subsequent growing season. Reduction of root growth following defoliation appears to be an effective mechanism to aid reestablishment of the photosynthetic canopy and the root: shoot balance. As such it contributes to both herbivory tolerance and maintenance of competitive ability.     

Leaf dynamics and insect herbivory in a Eucalyptus camaldulensis forest under moisture stress

Abstract The influence of soil moisture content on leaf dynamics and insect herbivory was examined between September 1991 and March 1992 in a river red gum (Eucalyptus camaldulensis) forest in southern central New South Wales. Long-term observations of leaves were made in trees standing either within intermittently flooded waterways or at an average of 37. 5m from the edge of the waterways. The mean soil moisture content was significantly (P≤0.05) greater in the waterways than in the non-flooded areas. Trees in the higher soil moisture regime produced significantly larger basal area increments and increased canopy leaf area. This increase in canopy leaf area was achieved, in part, through a significant increase in leaf longevity and mean leaf size. Although a greater number of leaves was initiated and abscissed per shoot from the non-flooded trees, more leaves were collected from litter traps beneath the denser canopies of the flooded trees. Consumption of foliage by insects on the trees subjected to flooding compared to the non-flooded trees was not significantly different. However, the relative impact of insect herbivory was significantly greater on the non-flooded trees. Leaf chewing was the most common form of damage by insects, particularly Chryso-melidae and Curculionidae. No species was present in outbreak during this study. Leaf survival decreased as the per cent area eaten per leaf increased. In addition, irrespective of the level of herbivory, leaf abscission tended to be higher in E. camaldulensis under moisture deficit. The influence of soil moisture content on the balance between river red gum growth and insect herbivory is discussed.     

Insect herbivory on the Australian woodland eucalypt,Eucalyptus blakelyi M.

This, the first study on herbivory in a woodland eucalypt in Australia, produced an estimate of annual foliage loss from Eucalyptus blakelyi to herbivorous insects of 40%. Further evidence on abscission of damaged foliage showed that this was an underestimate, a more accurate figure being closer to 70% annually.     

Plant responses and herbivory following simulated browsing and stem cutting of Combretum apiculatum

Abstract. Time and mode of herbivory on savanna trees and their subsequent responses are dependent on, among other things, earlier herbivory and fire. We used clipping (simulated browsing) and stem cutting (simulated heavy browsing and to some extent simulated fire) to evaluate such interactions. Study organisms were a deciduous, broad‐leaved tree species, Combretum apiculatum (Combretaceae), browsing large herbivores and leaf‐eating insects. The treatments were done in the late dry season before bud break. Late in the following wet season, we recorded plant responses to treatment and browsing. The treated trees, especially the cut ones, responded by producing larger and fewer annual shoots. Compared to control trees, there was a slight increase in shoot biomass of clipped trees and a strong reduction of cut ones. Leaf area increased in clipped trees, but decreased in cut ones. A marked increase in the number of browsed trees was recorded amongst treated trees. Number of bites, consumption and utilization also increased with severity of treatment. In contrast, insect herbivory was reduced on both clipped and cut trees. The observed patterns are discussed in relation to current ideas on plant ‐ herbivore interactions.     

Intraspecific variation in food plant favourability to phytophagous insects: psyllids on Eucalyptus blakelyi M.

Abstract.

• 1 A combination of variables reflecting leaf quality provided the best predictive model explaining differences in population trend of Glycaspis spp. among individuals of the food plant Eucalyptus blakelyi, measured under field conditions on an egg to egg basis. The equation incorporated the product of: (1) proportion of foliage in each age class; (2) probability of foliage escape from herbivory; (3) preference for the foliage class measured as the proportion of eggs oviposited on it by the female; these variables being summed over the young and mature age classes.
• 2 In addition, significant and consistent differences in insect survivorship among trees were demonstrated by transfer experiments. These experiments established that young foliage was preferable to mature foliage for first instar survival. Differences in insect survivorship also showed a consistent pattern among the study trees. The most probable explanation for this consistent pattern was the influence of the trees on the insects, particularly physiological or biochemical differences among trees. It was not, however, possible to identify the cause of the differences.

     

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.     

Growth responses of arctic graminoids following grazing by captive lesser snow geese

The effects of grazing by captive goslings of the Lesser Snow Goose on coastal vegetation at La Pérouse By. Manitoba were investigated. Swards of Carex subspathacea, Festuca rubra and Calamagrostis deschampsioides were grazed once for different periods (0–180 min) and regrowth of vegetation determined, based on measurements of standing crop, net above-ground primary production (NAPP) and forage quality (leaf nitrogen content). The amounts of foliage removed from swards of Carex subspathacea increased with the length of the grazing period, but after 44 days of regrowth there were no significant differences in above-ground biomass between control and grazed plots. While the amount of foliage removed by goslings from swards of Festuca rubra increased with the length of the grazing period (except after 150 min of grazing), the increase in biomass following defoliation was similar among treatments. Goslings removed little biomass from swards of Calamagrostis deschampsioides, even when the opportunity for grazing was 180 min. No significant differences in standing-crop or NAPP between grazed and ungrazed plots were detected by the end of summer. Grazing had no significant effect on amounts of nitrogen in leaf tissue of all species, suggesting that faecal nitrogen was not rapidly incorporated into plant biomass within the growing season. Patterns of regrowth of these species are compared to that of Puccinellia phryganodes. An increase in goose numbers in recent years has led to birds foraging on less preferred species, such as Calamagrostis deschampsiodes and Festuca rubra. Their poor nutritional quality and a lack of a rapid growth response following defoliation may explain, in part, the decline in the weight of wild goslings recorded over the last decade.     

Augmentation of soil detritus affects the spider community and herbivory in a soybean agroecosystem

If soil detritivores provide a significant prey source for predators in the vegetation, then augmentation of the soil community could affect the grazing food web. Specifically, increases in predator density could enhance any top‐down effects and reduce herbivory. We tested this hypothesis by providing detrital subsidies in the form of composted vegetable matter to 36 m² plots in soybean, Glycine max (L.) Merr. (Fabales: Fabaceae), fields that were managed using either conventional or conservation tillage practices. The foliage‐dwelling spiders, insect predators, and leaf‐chewing insects were censused and the body size of one large spider species, Argiope trifasciata (Forskål) (Araneae: Araneidae), was measured. In addition, the density and size of the plants were assessed and leaf damage was quantified. Any effects of treatments on the palatability of soybean plants to herbivores were determined in two laboratory experiments. Compost increased the density of foliage dwelling spiders and the abdomen size of A. trifasciata. We uncovered no treatment effects on insect predators, herbivorous insects, or plant characteristics except that compost addition reduced leaf damage. In addition, there was a negative correlation across plots between spider abundance and soybean leaf damage and abdomen width of A. trifasciata and weed herbivory levels across plots. These results suggest a connection between the soil community and the foliage food web, but the spiders appear to have exerted a top‐down effect without a shift in herbivore abundance. Further study of the specific seasonality of the herbivores and their behavior in the presence of spiders are needed to uncover the underlying mechanism. Nevertheless, these results provide evidence for complex linkage between the soil and grazing food webs that may be important to biological control.     

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.     

Growth,chemical responses and herbivory after simulated leaf browsing in <Emphasis Type="Italic">Combretum apiculatum</Emphasis>

Vegetative and chemical responses to simulated leaf browsing during the growth season, and their subsequent effect on herbivory, were studied on Combretum apiculatum Sonder (Combretaceae) in Botswana. Treatments (50% and 100% leaf and shoot apex removal) were performed just before the shoot growth curve levelled out, and responses recorded 3 months later, just before leaf fall. Compared to controls, defoliation treatments, removing apical dominance, reduced growth in tree height and increased shoot mortality, although the production of lateral shoots increased. At the end of the trial, there was no difference in total length of annual shoots between treatment groups. Significant refoliation occurred only after 100% defoliation. Refoliated leaves were smaller and the 100% defoliated trees had a lower final leaf biomass. Total leaf biomass production was, however, equal for all treatment groups. Refoliated leaves contained higher levels of N, lower levels of acid-detergent fibre (ADF) and total phenolics, and showed a trend towards lower levels of condensed tannins, compared to leaves on control trees. Such chemical changes may be due to either carbon stress or to younger physiological age of new leaves. In spite of the observed potential increase in food quality, we found no evidence of increased levels of insect or ungulate herbivory on refoliated leaves, which, at least for insect herbivory, may be explained by the reduction in temporal availability of leaves. We conclude that the single severe defoliation was not detrimental to C. apiculatum in the short-term, although the resource loss and induced compensatory growth may produce negative effects during subsequent growth seasons.     

A test of compensatory photosynthesis in the field: Implications for herbivory tolerance

Summary The occurrence of compensatory photosynthesis was examined in the field for all foliage elements on two Agropyron bunchgrass species that differ in their evolutionary history of grazing pressure. This is the first reported field study of compensatory photosynthesis in individual foliage elements of graminoids. Compensatory photosynthesis was defined as an increase in the photosynthetic rates of foliage on partially defoliated plants relative to foliage of the same age on undefoliated plants. Compensatory photosynthesis did occur in many individual foliage elements during at least part of their ontogeny. For both species, compensatory photosynthesis was related primarily to delayed leaf senescence and increased soluble protein concentrations, but not to an improvement in the water status of clipped plants. Soluble protein concentration increased in all foliage elements. A delay in senescence on clipped plants was documented for the two oldest, fully-expanded leaves that were present when the plants were initially clipped, but the initiation and senescence of all other foliage elements were not affected by the clipping treatments. Photosynthetic water use efficiency and photosynthetic rates per unit soluble protein of foliage on partially defoliated plants were not increased following the clipping treatments. Although A. desertorum and A. spicatum were exposed to different levels of grazing pressure during their evolutionary history, the phenology, water status, and gas exchange rates of foliage were very similar both for undefoliated as well as partially defoliated plants. Thus, we conclude that compensatory photosynthesis does not appear to be an important ecological component of herbivory tolerance for these species.     

Regrowth capacity in relation to defence strategy in Stipa clarazii and Stipa trichotoma,native to semiarid Argentina

Abstract Plants can defend themselves against herbivores by either avoiding or tolerating herbivory. Since avoidance mechanisms divert resources to other than growth processes, it could be expected a lower regrowth capacity in species that avoid herbivory than in species that tolerate herbivory, particularly under competition for resources. We tested this hypothesis by quantifying the regrowth of a grazing‐avoidant (Stipa trichotoma Nees, synonymous Nasella trichotoma (Nees) Hackel ex Arechav.) and a grazing‐tolerant (Stipa clarazii Ball, synonymous Nasella clarazii (Ball) Barkworth) grass species native to semiarid Argentina, when growing either singly or in pairs (one individual of each species) under repeated defoliation in field conditions. Twenty pairs of plants were selected in an area codominated by both species. Plants were protected by a 60 cm‐diameter exclosure, in which the rest of the vegetation had been removed. The same procedure was followed with 20 single plants of each species. The same plants were clipped four times in 1996 and 1998 and five times in 1997. The response variable was the cumulative regrowth per plant at the end of each year. The regrowth was analysed for neutral detergent fibre and nitrogen content. Cumulative regrowth of S. clarazii was higher, similar, or lower than the cumulative regrowth of S. trichotoma in 1996, 1997, and 1998, respectively. Regrowth was reduced by interspecific competition, although there was no interaction between species and growing conditions (single or in pairs). Neutral detergent fibre content was consistently higher, whereas nitrogen content was consistently lower, in S. trichotoma than in S. clarazii. Collectively, our results did not support the hypothesis of higher regrowth capacity in the grazing‐tolerant species than in the grazing‐avoidant species. Further, our findings suggest herbivore tolerance is a previously unappreciated trait of S. trichotoma.     

Effects of competitive stress on vegetative growth, storage, and regrowth after defoliation in Phleum pratense

The capacity for resource storage is important to population persistence in nonforaging plants with a consolidation strategy. In a competitive environment, selection may favor genetic variants with a well-developed ability to store resources for future vegetative growth or to regrow following herbivory. To determine the evolutionary potential for changes in vegetative growth, storage and regrowth after defoliation in response to competitive stress, half-sib families of the caespitose grass Phleum pratense were grown in pots in a glasshouse either alone or in competition with four individuals of Lolium perenne . They were defoliated after 16 wk and permitted to regrow for 8 wk. Production of new tillers, leaf area and leaf dry mass were recorded before and after defoliation; resource storage was estimated by the dry mass of stem bases. Tiller numbers, leaf area and mass, regrowth, and stem base mass were significantly reduced by competition; however, there was significant variation among families for many variables. A significant proportion of the variation in clipped and regrowth leaf mass, and in stem base mass, was due to a competition by family interaction. Storage in stem bases was correlated with total accumulated leaf mass in both control and competition groups. Genetic variation for competitive ability and the ability to regrow rapidly after defoliation exist in this P. pratense population. A well-developed ability to regrow following release from competitive or grazing pressures is likely to be a critical adaptation of caespitose grasses.     

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     

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.     

Changes in western wheatgrass foliage quality following defoliation: consequences for a graminivorous grasshopper

We determined the effects of defoliation by a graminivorous grasshopper on the foliage quality of the C3 plant, western wheatgrass (Pascopyrum smithii [Rydb] A. Love). Additionally, we determined the effects of this defoliation upon the subsequent feeding of the graminivorous grasshopper Phoetaliotes nebrascensis Thomas (Orthoptera: Acrididae). In field and greenhouse studies, graminivorous grasshopper herbivory altered the quality of remaining western wheatgrass foliage. In the greenhouse, severe (50% foliage removal) grasshopper grazing (638 grasshoppers/m² for 72h) resulted in decreased foliar nitrogen (–12%), carbohydrate (–11%) and water (–2.5%) concentrations, and increased phenolic concentrations (+43%). These changes were associated with decreased adult female grasshopper mass gain, consumption rate, approximate digestibility, and food conversion efficiencies. In the field, moderate (14% foliage removal) grasshopper grazing (20 grasshoppers/m² for 20 days) led to a 10% reduction in foliar nitrogen concentrations. Foliage quality changes in the field were not associated with any reductions in grasshopper mass gain, consumption rates, food digestibility, or conversion efficiencies. The results presented here are consistent with the hypothesis that defoliation leads to a reallocation of carbon and nitrogen compounds within the plant such that foliage quality for P. nebrascensis is reduced.