High Herbivore Pressure Research Articles

Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores

Quaking aspen (Populus tremuloides) is a quintessential “foundation species” in early-successional forest ecosystems throughout much of North America. Although subject to damage by hundreds of species of herbivores, aspen has persisted in these environments due largely to a suite of defense strategies: resistance (traits that deter herbivores), tolerance (traits that facilitate recovery from damage) and escape (traits that reduce exposure to herbivores). Here, we review the current state of knowledge about aspen defense against herbivores, with particular focus on montane habitats of western North America.The principal chemical defenses of aspen are phenylpropanoid-derived compounds, including phenolic glycosides (salicinoids) and condensed tannins. Phenolic glycosides reduce feeding, growth and survival of insect herbivores and deter feeding by mammalian herbivores. Expression of chemical defense traits is strongly influenced by genotype, development, environment (biotic and abiotic) and interactions among those factors, and high levels of defense exact a cost to growth. The value of tolerance as a defense strategy likely increases with tree age. Both tolerance and escape via vertical growth are also highly genetically variable in aspen.The efficacy of aspen defense systems is context-dependent. Under conditions of low to moderate herbivore pressure, chemical defenses serve as effective deterrents, and well-defended genotypes are selectively favored. Under conditions of high herbivore pressure – whether insect or mammal – resistance fails and trees sustain high levels of damage. Under these conditions, genotypes with high levels of tolerance are likely selectively favored.Large-scale landscape modifiers, coupled with genetic, developmental and local environmental variation, produce temporal and spatial mosaics of defense across western landscapes. Competition with conifers, fire severity, and extreme climatic events all influence expression of defense and response to herbivore damage in aspen.Aspen’s extraordinary genetic variation and phenotypic plasticity are no match for the environmental stressors, particularly ungulate browsing, contributing to its decline in portions of the Interior West. Management approaches should capitalize on the genetic and environmental factors known to contribute to diverse expression of defense in aspen, while maintaining herbivore population densities below levels that overwhelm all combinations of defense traits.

What did European primeval forests under high herbivore pressure look like?

Jak wyglądały lasy pierwotne Europy pod presją dużych roślinożerców?

Nonconsumptive effects of a generalist ungulate herbivore drive decline of unpalatable forest herbs

High herbivore pressure is expected to benefit unpalatable species that co-occur with palatable browsed species. However, for five unpalatable understory species we found no evidence of benefit from deer browse. Detailed studies of one species in natural populations, Arisaema triphyllum, revealed surprising changes in its population structure and demography: deer browse level on a palatable species significantly correlates with reduced plant size and seed rain and male-biased sex ratios of co-occurring Arisaema populations. Analyses of individual size in five unpalatable forest plant species in long-term experimental paired deer exclosure/deer access plots corroborate the natural site results; all five species were smaller in deer access plots. Analyses of abiotic variables in natural and experimental sites suggest one potential mechanism for indirect effects of deer. Deer-mediated soil quality declines included increased soil penetration resistance and decreased leaf litter depth, which are known to hinder plant growth. Our results are likely applicable to other unpalatable forest species and have clear consequences for understory biodiversity. Unpalatable plant species in forests experiencing high deer numbers may be in decline along with their palatable neighbors. Our study implicates deer overabundance in the cascade of forest species decline and the urgency of this conservation issue in North America.

Browsing and fire interact to suppress tree density in an African savanna

Disturbances from fire and herbivory strongly affect savanna vegetation dynamics. In some savannas, fire especially may be instrumental in preserving the coexistence of trees and grasses. The role of herbivory by large mammals is less clear; herbivory has been shown variously to promote and to suppress tree establishment. Here we ask how interactions between herbivory and fire act to shape savanna vegetation dynamics via their effects on tree populations in Hluhluwe iMfolozi Park in KwaZulu Natal, South Africa, a savanna with a full complement of native large mammals. We examined the effects of herbivore exclusion on tree growth, mortality, and seedling establishment from 2000 to 2007 at 10 sites located in areas of low and high herbivore pressure throughout the park. Results were analyzed statistically and using Leslie matrix models of population dynamics. Herbivory and fire acted primarily to suppress sapling growth rather than on sapling mortality or seedling establishment. This indicates that browsing, like fire, suppresses tree density by imposing a demographic bottleneck on the maturation of saplings to adults. Model results suggest that, while browsing and fire each alone impacted growth, a combination of browsing and fire had much greater effects on tree density. Only fire and browsing together were able to prevent increases in tree density. These results suggest that, while soil resources, including nutrients and moisture, are probably instrumental in determining tree growth rates, disturbances from fire and herbivory may be instrumental in limiting tree cover and facilitating the coexistence of trees and grasses in savannas.

The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in ‘devil's gardens’ is increased herbivory on Duroia hirsuta trees

'Devil's gardens' are nearly pure stands of the myrmecophyte, Duroia hirsuta, that occur in Amazonian rainforests. Devil's gardens are created by Myrmelachista schumanni ants, which nest in D. hirsuta trees and kill other plants using formic acid as an herbicide. Here, we show that this ant-plant mutualism has an associated cost; by making devil's gardens, M. schumanni increases herbivory on D. hirsuta. We measured standing leaf herbivory on D. hirsuta trees and found that they sustain higher herbivory inside than outside devil's gardens. We also measured the rate of herbivory on nursery-grown D. hirsuta saplings planted inside and outside devil's gardens in ant-exclusion and control treatments. We found that when we excluded ants, herbivory on D. hirsuta was higher inside than outside devil's gardens. These results suggest that devil's gardens are a concentrated resource for herbivores. Myrmelachista schumanni workers defend D. hirsuta against herbivores, but do not fully counterbalance the high herbivore pressure in devil's gardens. We suggest that high herbivory may limit the spread of devil's gardens, possibly explaining why devil's gardens do not overrun Amazonian rainforests.

Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa)

The inevitable escape of transgenic pollen from cultivated fields will lead to the emergence of transgenic crop-wild plant hybrids in natural patches of wild plants. The fate of these hybrids and that of the transgene depend on their ability to compete with their wild relatives. Here we study ecological factors that may enhance the fitness of genetically modified hybrids relative to wild plants for a Bacillus thuringiensis ( Bt) transgene conferring resistance to insects. Mixed stands of wild plants and first-generation hybrids were grown under different conditions of herbivore pressure and density, with Bt oilseed rape ( Brassica napus) as the crop and B. rapa as the wild recipient. Biomass and fitness components were measured from plant germination to the germination of their offspring. The frequency of transgenic seedlings in the offspring generation was estimated using the green fluorescent protein marker. The biomass of F(1) Bt-transgenic hybrids relative to that of wild-type plants was found to be sensitive to both plant density and herbivore pressure, but herbivore pressure appeared as the major factor enhancing their relative fitnesses. In the absence of herbivore pressure, Bt hybrids produced 6.2-fold fewer seeds than their wild neighbors, and Bt plant frequency fell from 50% to 16% within a single generation. Under high herbivore pressure, Bt hybrids produced 1.4-fold more seeds, and Bt plant frequency was 42% in the offspring generation. We conclude that high-density patches of highly damaged wild plants are the most vulnerable to Bt-transgene invasion. They should be monitored early to detect potential transgene spread.

Effects of Fish Farm Loadings on Seagrass (Posidonia oceanica) Distribution, Growth and Photosynthesis

The spatial extent and timing of the impact of fish farms on the distribution and performance of a Posidonia oceanica meadow were examined in an embayment of the south-eastern coast of Spain (Hornillo Bay, Murcia). Changes in seagrass distribution were determined using available seagrass mapping (from 1988, i.e., before the onset of aquaculture activities and 1998) and by successive sampling in 1994 and 1998. Environmental variables (light attenuation coefficient, water-column dissolved nutrients and organic content of sediments) together with plant performance (shoot biomass, leaf growth rate, photosynthetic activity, carbohydrate reserves, the number of leaves per shoot, epiphyte loads and herbivore pressure) were measured in plants affected by organic discharges, and were compared with those found in reference healthy plants over an annual growth cycle. Since the onset of fish farm activity, 11.29 ha of P. oceanica meadow has been completely lost and 9.86 ha significantly degraded, thus resulting in a total affected area which accounts for about 53% of the former meadow, or 7-fold the fish farming area. Unequal propagation of seagrass die-off or degradation reflects the relevance of local factors such as depth and hydrodynamism on the true extent of fish farm impact. Water transparency decreases and dissolved nutrient and organic content of sediments increases in the vicinity of cages compared to distant reference stations, thus supporting the notion of environmental gradients caused by the organic release from cages, which spreads outwards. Shoot size, leaf growth rate and the number of leaves per shoot in plants close to the fish farm decreased. Moreover, low leaf growth and low rhizome carbohydrate concentration (always relative to that found in an undisturbed area) indicated carbon budget imbalances. Since light reduction in the affected area was only modest (31% of light reaching the sea surface, while at the same depth this figure was 39% at the reference site), and light availability was well above the minimum requirement estimated for this species, neither this factor nor epiphyte overgrowth (epiphyte load was lower in the affected area) seem to explain such carbon imbalances or the observed meadow regression. Alternatively, the high herbivore pressure found in the affected zone suggests that overgrazing is one of the main causes of decreasing shoot sizes and hence of carbon imbalance, reduced growth and shoot mortality. The impact of fish farms on seagrasses, therefore, seems to be highly variable and depends on complex interactions between a large number of processes.

Delayed greening of mountain birch leaves:Ecological and chemical correlates

Flushing leaves of deciduous trees can be exposed to high herbivore pressure. Young foliage provides high quality food for herbivores, and therefore herbivore pressure is much higher in young than mature foliage. Plants may escape the effects of herbivory in time by delaying leaf greening. We measured delayed greening as an intensity of redness in leaves in mountain birch at bud burst. Furthermore, we analyzed covariation of leaf redness with leaf growth and leaf consumption by the autumnal moth, Epirrita autumnata (Bkh.), a major defoliator of mountain birch. We also analyzed concentrations of amino acids, sugars and phenolic compounds of leaves. Leaf redness was positively associated with leaf growth, and consumption by E. autumnata indicated reduced leaf resistance against herbivores. Concentrations of protein-bound amino acids and gallotannins in young leaves were closely and positively correlated with leaf redness. Concentrations of glucose exhibited close positive correlations with leaf redness at the beginning of the season, whereas the correlation was negligible in mature leaves. Concentrations of other sugars increased with increasing degree of leaf redness towards the end of leaf development. This may be one reason for high leaf biomass losses in trees with delayed greening.

Effects of early season defoliation on above-ground growth ofAnthyllis cytisoides, a Mediterranean browse species

Anthyllis cytisoidesL. is a traditional forage species, well adapted to grazing pressure, and so might be expected to respond positively to moderate grazing. We performed a hierarchical design analysis of variance with three levels of plant defoliation (10, 50 and 90%) and three of stem defoliation (10, 50 and 90% of shoots removed), in three age classes based on trunk base perimeter (≤11cm, 11–20cm and >20cm). Response to herbivory was measured as total vegetative length, inflorescence length, leaf number, flower number, and the ratio of the number of floral axes to the total number of axes.We found thatA. cytisoidescompensated for herbivory. That is, above-ground growth ofA. cytisoidesincreased with the percentage of plant defoliation, with respect to elongation of the stem and increase in the total flower and leaf number. In contrast, growth following stem defoliation declined in the target stem as stem defoliation increases. Stem defoliation effect was more evident in young plants than in older ones. The increase in plant growth with plant defoliation was seen both in the average growth per floral axes and the number of floral axes per stem. However, only the number of floral axis per stem was responsible for the reduction in stem productivity with experimental defoliation.Stem overcompensation (greater elongation in defoliated stems than control) occurred only in stems suffering 10% defoliation when plants were under medium and high experimental herbivore pressure, indicating the ability ofA. cytisoidesto produce a compensatory response to herbivory. The growth consequences of early season defoliation persist after two growing periods, increasing above-ground growth differences among treatment groups.

Biodiversity Resources for Restoration Ecology

Biological resources can be more usefully incorporated into many aspects of restoration ecology. During the planning and design stage, the wide genotypic variation in natural plant populations must be recognized and exploited. This will ensure that genotypes used on a site are best adapted to local conditions and have a greater probability of survivorship than arbitrarily chosen material. Also, certain unusual genotypes can be located using the principles of evolutionary ecology and can be installed in areas with extreme conditions, such as soils contaminated with heavy metals, in areas where rapid colonizing ability (high seed set and/or clonal growth) is particularly advantageous, or where soils are of poor quality. Similarly, where high herbivore pressure is a threat to restoration, genotypes that are well defended, chemically or mechanically, against animal enemies should be selected to initiate the restoration process. The nursery industry can be encouraged to supply an ecologically wider selection of material for restoration, originating from local biological reserves and natural habitats. During the management phase of a restoration, local natural habitats are critical as reservoirs of biological control agents, seed sources for plant species, and members of higher trophic levels and additional plant species needed during succession. Mutualists such as pollinators, seed dispersers, and mycorrhizal fungi are vital to the success of a restoration project, and these must invade from nearby natural habitats or must be deliberately introduced. During the evaluation phase of restoration, local natural areas should be used as templates of community composition and structure from which one measures success. A functioning restoration project will interact biologically with surrounding areas, the exchange of species and genes being particularly important. Analysis of the microbial and invertebrate communities that have invaded the installed plant community may be useful and accurate determinants of ecological function. For these latter stages of the restoration process, the value of preserving local habitat remnants is high and complements their usefulness as a source of ecologically precise material for installation.

Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities?

Between-habitat differences in macrophyte consumption by herbivorous fishes were examined on three Caribbean and two Indian Ocean coral reefs. Transplanted sections of seagrasses were used as a bioassay to compare removal rates in reef-slope, reef-flat, sand-plain, and lagoon habitats. Herbivore susceptibility of fifty-two species of seaweeds from these habitats was also measured in the field. Seagrass consumption on shallow reef slopes was always significantly greater than on shallow reef flats, deep sand plains, or sandy lagoons. Reef-slope seaweeds were consistently resistant to herbivory while reef-flat seaweeds were consistently very susceptible to herbivory. This pattern supports the hypothesis that defenses against herbivores are costly in terms of fitness and are selected against in habitats with predictably low rates of herbivory.Sand-plain and lagoon seaweeds showed a mixed response when placed in habitats with high herbivore pressure; most fleshy red seaweeds were eaten rapidly, most fleshy green seaweeds were eaten at intermediate rates, and most calcified green seaweeds were avoided or eaten at very low rates. Differences in susceptibility between red and green seaweeds from sand-plain or lagoon habitats may result from differential competitive pressures experienced by these seaweed groups or from the differential probability of being encountered by herbivores. The susceptibility of a species to removal by herbivorous fishes was relatively consistent between reefs. Preferences of the sea urchin Diadema antillarum were also similar to those of the fish guilds.Unique secondary metabolites were characteristic of almost all of the most herbivore resistant seaweeds. However, some of the herbivore susceptible species also contain chemicals that have been proposed as defensive compounds. Genera such as Sargassum, Turbinaria, Thalassia, Halodule, and Thalassodendron, which produce polyphenolics or phenolic acids, were consumed at high to intermediate rates, suggesting that these compounds are not effective deterrents for some herbivorous fishes. Additionally, potential for the production of the compounds caulerpin, caulerpicin and caulerpenyne in various species of Caulerpa did not assure low susceptibility to herbivory.Heavily calcified seaweeds were very resistant to herbivory, but all of these species also produce toxic secondary metabolites which makes it difficult to distinguish between the effects of morphological and chemical defenses. Predictions of susceptibility to herbivory based on algal toughness and external morphology were of limited value in explaining differing resistances to herbivory.