Boom-bust dynamics in biological invasions: towards an improved application of the concept.

Boom-bust dynamics - the rise of a population to outbreak levels, followed by a dramatic decline - have been associated with biological invasions and offered as a reason not to manage troublesome invaders. However, boom-bust dynamics rarely have been critically defined, analyzed, or interpreted. Here, we define boom-bust dynamics and provide specific suggestions for improving the application of the boom-bust concept. Boom-bust dynamics can arise from many causes, some closely associated with invasions, but others occurring across a wide range of ecological settings, especially when environmental conditions are changing rapidly. As a result, it is difficult to infer cause or predict future trajectories merely by observing the dynamic. We use tests with simulated data to show that a common metric for detecting and describing boom-bust dynamics, decline from an observed peak to a subsequent trough, tends to severely overestimate the frequency and severity of busts, and should be used cautiously if at all. We review and test other metrics that are better suited to describe boom-bust dynamics. Understanding the frequency and importance of boom-bust dynamics requires empirical studies of large, representative, long-term data sets that use clear definitions of boom-bust, appropriate analytical methods, and careful interpretations.

Quantifying a dynamic risk landscape: heterogeneous predator activity and implications for prey persistence.

Spatial heterogeneity in predation risk can ameliorate impacts on prey populations, particularly for prey of generalists. Spatially heterogeneous risk implies the existence of refugia, and the spatial scale of those refugia and their persistence over time affect whether prey can avoid predation by aggregating therein. Our objective was to quantify the magnitude, spatial scale, and temporal persistence of heterogeneity in risk of predation by white-footed mice (Peromyscus leucopus), an abundant generalist predator of gypsy moths (Lymantria dispar) and songbirds. We used track plates to measure white-footed mouse activity at > 170 trees in each of three forest plots in upstate New York during summers of 2003-2005. We quantified the mean and coefficient of variation of track activity among trees by fitting the beta-binomial distribution to data from each plot and study period. We measured temporal persistence by disattenuated autocorrelation, and spatial scale by fitting exponential variograms. Mice were much less abundant in 2005 than the other two years, leading to lower overall track activity but higher coefficient of variation among trees. Mouse track activity at individual trees was positively autocorrelated between monthly study periods in 2003 and 2004, and even between the two years, whereas temporal autocorrelation in 2005 was much weaker. Track activity showed positive spatial autocorrelation over lag distances from approximately 30 to > 1000 m. These findings indicate that mouse activity, and hence risk to their prey, varies substantially in space at spatial and temporal scales that appear responsive to mouse population dynamics. The spatial scale and temporal persistence of that variation imply that prey may benefit from returning to, or failing to disperse from, refugia.

A Darwinian view of metabolism: molecular properties determine fitness.

Why do organisms make the types of chemicals that they do? Evolutionary theory tells us that individuals within populations will be subject to mutation and that some of those mutations will be enzyme variants that make new chemicals. A mutant making a novel chemical for that species will only survive in the population if the 'cost' of making the new chemical is outweighed by the benefits that result from making that molecule. The benefits, or adverse consequences, that a novel chemical X can confer to the individual organism are not a property of the simple existence of X in the cell but can be traced to one of the multiple properties that X will possess because of its molecular structure. By considering only three basic types of molecular property and by considering how selection pressures will differ for each kind of property, it is possible to account for much of the chemical diversity made by organisms. Such an evolutionary model can also explain why the properties of enzymes will differ depending on the molecular properties of the chemicals they make, and why the widely accepted terms 'primary metabolism' and 'secondary metabolism' have been so misleading and unsatisfactory.

Leaf- and shoot-level plasticity in response to different nutrient and water availabilities.

Phenotypic plasticity in response to environmental variation occurs at all levels of organization and across temporal scales within plants. However, the magnitude and functional significance of plasticity is largely unexplored in perennial species. We measured the plasticity of leaf- and shoot-level physiological, morphological and developmental traits in nursery-grown Populus deltoides Bartr. ex Marsh. individuals subjected to different nutrient and water availabilities. We also examined the extent to which nutrient and water availability influenced the relationships between these traits and productivity. Populus deltoides responded to changes in resource availability with high plasticity in shoot-level traits and moderate plasticity in leaf-level traits. Although shoot-level traits generally correlated strongly with productivity across fertilization and irrigation treatments, few leaf-level traits correlated with productivity, and the relationships depended on the resource examined. In fertilized plants, leaf nitrogen concentration was negatively correlated with productivity, suggesting that growth, rather than enhanced leaf quality, is an important response to fertilization in this species. With the exception of photosynthetic nitrogen-use efficiency, traits associated with resource conservation (leaf senescence rate, water-use efficiency and leaf mass per area) were uncorrelated with short-term productivity in nutrient- and water-stressed plants. Our results suggest that plasticity in shoot-level growth traits has a greater impact on plant productivity than does plasticity in leaf-level traits and that the relationships between traits and productivity are highly resource dependent.

Spatial selection and inheritance: applying evolutionary concepts to population dynamics in heterogeneous space.

Organisms in highly suitable sites generally produce more offspring, and offspring can inherit this suitability by not dispersing far. This combination of spatial selection and spatial inheritance acts to bias the distribution of organisms toward suitable sites and thereby increase mean fitness (i.e., per capita population increase). Thus, population growth rates in heterogeneous space change over time by a process conceptually analogous to evolution by natural selection, opening avenues for theoretical cross-pollination between evolutionary biology and ecology. We operationally define spatial inheritance and spatial selective differential and then combine these two factors in a modification of the breeder's equation, derived from simple models of population growth in heterogeneous space. The modified breeder's equation yields a conservative criterion for persistence in hostile environments estimable from field measurements. We apply this framework for understanding gypsy moth population persistence amidst abundant predators and find that the predictions of the modified breeder's equation match initial changes in population growth rate in independent simulation output. The analogy between spatial dynamics and natural selection conceptually links ecology and evolution, provides a spatially implicit framework for modeling spatial population dynamics, and represents an important null model for studying habitat selection.

Ecosystem engineering in space and time.

The ecosystem engineering concept focuses on how organisms physically change the abiotic environment and how this feeds back to the biota. While the concept was formally introduced a little more than 10 years ago, the underpinning of the concept can be traced back to more than a century to the early work of Darwin. The formal application of the idea is yielding new insights into the role of species in ecosystems and many other areas of basic and applied ecology. Here we focus on how temporal, spatial and organizational scales usefully inform the roles played by ecosystem engineers and their incorporation into broader ecological contexts. Two particular, distinguishing features of ecosystem engineers are that they affect the physical space in which other species live and their direct effects can last longer than the lifetime of the organism--engineering can in essence outlive the engineer. Together, these factors identify critical considerations that need to be included in models, experimental and observational work. The ecosystem engineering concept holds particular promise in the area of ecological applications, where influence over abiotic variables and their consequent effects on biotic communities may facilitate ecological restoration and counterbalance anthropogenic influences.

Variation in Eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behavior of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae).

Apterous populations of Chaitophorous populicola Thomas (Homoptera: Aphididae) appear to track Eastern cottonwood (Populus deltoides Bartr.) leaf development. Few aphids occur on mature leaves. Marked individual aphids on leaves of different developmental stages were observed through a period of new leaf initiation. Nymph and adult C. populicola frequently track leaf development by moving up to younger leaves. A comparison of phloem sap constituents and leaf toughness among leaf developmental stages revealed some differences that could be used by C. populicola to determine leaf age. Phloem sap exudates, collected from P. deltoides leaves of different developmental stages, were analyzed by high-performance liquid chromatography for free amino acids and the phenolic glycoside salicin. Sucrose concentration in exudates, indicative of phloem sap exudation rate, was uniform among leaf stages. Of 20 amino acids examined, only aspartic acid and gamma-amino-n-butyric acid (GABA) concentrations differed significantly between leaf stages. Forward stepwise discriminant function analysis showed that seven of the amino acids analyzed are useful for classifying leaf maturity groupings. Aphid-infested cottonwoods had lower cystine concentrations in phloem sap than aphid-free plants. Salicin concentration was significantly higher in new leaves. Leaf toughness was assessed by lignin density and distance measurements in petiole cross-sections. Rapidly expanding leaves had significantly less lignification and new leaves had shorter distances to the vascular bundles than senescent leaves. These physiological and phytochemical differences among P. deltoides leaf developmental stages may contribute to the leaf stage selection patterns exhibited by the aphid, C. populicola.

Using ecosystem engineers to restore ecological systems.

Ecosystem engineers affect other organisms by creating, modifying, maintaining or destroying habitats. Despite widespread recognition of these often important effects, the ecosystem engineering concept has yet to be widely used in ecological applications. Here, we present a conceptual framework that shows how consideration of ecosystem engineers can be used to assess the likelihood of restoration of a system to a desired state, the type of changes necessary for successful restoration and how restoration efforts can be most effectively partitioned between direct human intervention and natural ecosystem engineers.

Physiological and developmental effects of O3 on cottonwood growth in urban and rural sites.

Previously we found that cloned cottonwood saplings (Populus deltoides) grew twice as large in New York, New York, USA, compared to surrounding rural environments and that soils, temperature, CO2, nutrient deposition, and microclimatic variables could not account for the greater urban plant biomass. Correlations between final season biomass and cumulative O3 exposures, combined with twofold growth reductions in an open-top chamber experiment provided strong evidence that higher cumulative O3 exposures in rural sites reduced growth in the country. Here, we assess the field gas exchange, growth and development, and allocation responses underlying the observed growth differences and compare them with isolated O3 responses documented in the open-top chamber experiment. Cottonwoods showed no visible foliar injury, reduced photosynthesis of recently expanded foliage, early leaf senescence, protective reduction in stomatal conductance, or compensatory allocation to shoot relative to root biomass for either the chamber or field experiment. Instead, O3-impacted chamber plants had significantly higher conductance and reduced photosynthesis of older foliage that led to reduced leaf area production and a twofold biomass reduction in the absence of visible injury. Rural-grown field plants showed the same pattern of significantly higher conductance in the absence of concomitant increases in photosynthesis that was indicative of a loss of stomatal control. Incremental changes in foliar production were also significantly inversely related to fluctuations in ambient O3 exposures. The similarity in biomass, gas exchange, phenological, and allocation responses between chamber and field experiments indicate that mechanisms accounting for reduced growth at rural sites were consistent with those in the open-top chamber O3 experiment. This study shows the limitation of visible symptoms as a sole diagnostic factor for documenting detrimental O3 impacts and points toward a new approach to show O3 impacts when visible injury is not present. Namely, O3-impacted vegetation showed an unusual inverse relationship of increased conductance with lower photosynthesis of older foliage that was indicative of a loss of stomatal control. This increased stomatal conductance of O3-impacted vegetation accentuates pollutant flux into affected foliage and has important implications for system water balance during warm, dry portions of the growing season when O3 concentrations are highest.

Natural products--a simple model to explain chemical diversity.

A simple evolutionary model is presented which explains why organisms produce so many natural products, why so many have low biological activity, why enzymes involved in natural product synthesis have the properties they do and why natural product metabolism is shaped as it is.

Urbanization effects on tree growth in the vicinity of New York City.

Plants in urban ecosystems are exposed to many pollutants and higher temperatures, CO2 and nitrogen deposition than plants in rural areas. Although each factor has a detrimental or beneficial influence on plant growth, the net effect of all factors and the key driving variables are unknown. We grew the same cottonwood clone in urban and rural sites and found that urban plant biomass was double that of rural sites. Using soil transplants, nutrient budgets, chamber experiments and multiple regression analyses, we show that soils, temperature, CO2, nutrient deposition, urban air pollutants and microclimatic variables could not account for increased growth in the city. Rather, higher rural ozone (O3) exposures reduced growth at rural sites. Urban precursors fuel the reactions of O3 formation, but NO(x) scavenging reactions resulted in lower cumulative urban O3 exposures compared to agricultural and forested sites throughout the northeastern USA. Our study shows the overriding effect of O3 despite a diversity of altered environmental factors, reveals 'footprints' of lower cumulative urban O3 exposures amidst a background of higher regional exposures, and shows a greater adverse effect of urban pollutant emissions beyond the urban core.

An ecosystem engineer, the beaver, increases species richness at the landscape scale.

Ecosystem engineering - the physical modification of habitats by organisms - has been proposed as an important mechanism for maintaining high species richness at the landscape scale by increasing habitat heterogeneity. Dams built by beaver (Castor canadensis) dramatically alter riparian landscapes throughout much of North America. In the central Adirondacks, New York, USA, ecosystem engineering by beaver leads to the formation of extensive wetland habitat capable of supporting herbaceous plant species not found elsewhere in the riparian zone. We show that by increasing habitat heterogeneity, beaver increase the number of species of herbaceous plants in the riparian zone by over 33% at a scale that encompasses both beaver-modified patches and patches with no history of beaver occupation. We suggest that ecosystem engineers will increase species richness at the landscape scale whenever there are species present in a landscape that are restricted to engineered habitats during at least some stages of their life cycle.

Defoliation effects on isoprene emission from Populus deltoides.

Isoprene emission from plants is one of the principal ways in which plant processes alter atmospheric chemistry. Despite the importance of this process, few long-term controls over basal emission rates have been identified. Stress-induced changes in carbon allocation within the entire plant, such as those produced by defoliation, have not been examined as potential mechanisms that may control isoprene production and emission. Eastern cottonwood (Populus deltoides) saplings were partially defoliated and physiological and growth responses were measured from undamaged and damaged leaves 7 days following damage. Defoliation reduced isoprene emission from undamaged and damaged leaves on partially defoliated plants. Photosynthetic rates and leaf carbon and nitrogen pools were unaffected by damage. Photosynthetic rate and isoprene emission were highly correlated in undamaged leaves on undamaged plants and damaged leaves on partially defoliated plants. There was no correlation between photosynthetic rate and isoprene emission in undamaged leaves on partially defoliated plants. Isoprene emission was also highly correlated with the number of source leaves on the apical shoot in damage treatments. Increased carbon export from source leaves in response to defoliation may have depleted the amount of carbon available for isoprene synthesis, decreasing isoprene emission. These results suggest that while isoprene emission is controlled at the leaf level in undamaged plants, emission from leaves on damaged plants is controlled by whole-branch allocation patterns.

The fraction of expanding to expanded leaves determines the biomass response of Populus to elevated CO2.

We examined whether the effects of elevated CO2 on growth of 1-year old Populus deltoides saplings was a function of the assimilation responses of particular leaf developmental stages. Saplings were grown for 100 days at ambient (approximately 350 ppm) and elevated (ambient + 200 ppm) CO2 in forced-air greenhouses. Biomass, biomass distribution, growth rates, and leaf initiation and expansion rates were unaffected by elevated CO2. Leaf nitrogen (N), the leaf C:N ratio, and leaf lignin concentrations were also unaffected. Carbon gain was significantly greater in expanding leaves of saplings grown at elevated compared to ambient CO2. The Rubisco content in expanding leaves was not affected by CO2 concentration. Carbon gain and Rubisco content were significantly lower in fully expanded leaves of saplings grown at elevated compared to ambient CO2, indicating CO2-induced down-regulation in fully expanded leaves. Elevated CO2 likely had no overall effect on biomass accumulation due to the more rapid decline in carbon gain as leaves matured in saplings grown at elevated compared to ambient CO2. This decline in carbon gain has been documented in other species and shown to be related to a balance between sink/source balance and acclimation. Our data suggest that variation in growth responses to elevated CO2 can result from differences in leaf assimilation responses in expanding versus expanded leaves as they develop under elevated CO2.

Caterpillar guts and ammonia volatilization: retention of nitrogen by gypsy moth larvae consuming oak foliage.

The gypsy moth (Lymantria dispar L.), a major defoliator of hardwood forests in the eastern U.S., has a highly alkaline midgut pH. We hypothesized that the high pH would cause high rates of ammonia (NH3) volatilization as larvae consumed foliage, leading to potentially large losses of N from the ecosystem to the atmosphere during gypsy moth outbreaks. We measured NH3 emission during the consumption of oak foliage by larvae in the laboratory. Surprisingly, we found very low amounts of NH3 release of about 0.1% of the N consumed in foliage. We speculate that digestive mechanisms may limit NH3 production in the midgut, and that the acidic environment of the hindgut traps most of the small amount of NH3 that is produced, effectively preventing a potentially very large N loss from both larvae and ecosystem. The estimated rate of NH3 emission from a defoliated forest is small compared to other inputs and outputs of N from the ecosystem, but could potentially enhance the neutralization of atmospheric acidity during the defoliation period.

Control of systemically induced herbivore resistance by plant vascular architecture.

Patterns of systemically induced resistance (SIR) in Eastern Cottonwood, Populus deltoides, measured by reduced feeding of the leaf-chewing beetle, Plagiodera versicolora, were shown to be directly related to the distribution of the plant vasculature. Mechanical damage to single leaves resulted in SIR in non-adjacent, orthostichous leaves (vertically aligned on the stem) with direct vascular connections, both up and down the shoot; but no SIR in adjacent, non-orthostichous leaves with less direct vascular connections. The control that the plant vasculature exerts over signal distribution following wounding can therefore be used to predict SIR patterns, explain variation in the distribution of SIR, and relate this ecologically important phenomenon to biochemical processes of systemic gene expression and biochemical resistance mechanisms.

Exposure of cottonwood plants to ozone alters subsequent leaf decomposition.

Cottonwood saplings were exposed to ozone or charcoal-filtered air in a closed chamber. After leaf abscission, decomposition of individual leaf discs was measured in containers of stream water. Exposure of plants to 200 ppb ozone for 5 h caused early leaf abscission and changes in the chemical composition of leaves at time of abscission. Early-abscised leaves from O3-exposed plants had higher nitrogen, but decomposed more slowly than leaves from control plants. Leaves from O3-exposed plants that abscised at the normal time had lower nitrogen content and lower specific leaf mass than control leaves, but decomposed at the same rate as leaves from control plants. The results imply that O3 exposure can alter fundamental processes important to the functioning of detritus-based aquatic ecosystems.

Plant stress and insect performance: cottonwood, ozone and a leaf beetle.

Leaf area consumption rates, development rates, survivorship, and fecundity of the imported willow leaf beetle (Plagiodera versicolora Laich) were examined on two clones of eastern cottonwood which were previously exposed to ozone or charcoal-filtered air. P. versicolora consumed more ozone treated foliage, but were more fecund when reared on charcoal-filtered air treated plants. Beetle development rates and survivorship were not significantly different on treated and control cottonwoods. We concluded that: 1) Ozone fumigation of cottonwood reduced foliage quality, and the reproductive success and overall performance of P. versicolora. 2) increased foliage consumption by beetles was probably a mechanism compensating for decreases in foliage quality. 3) Reductions in beetle fecundity were due to an initial reduction in oviposition rates. 4) Beetle feeding preference did not correlate with the suitability of foliage for beetle performance. These results are discussed in relation to the impact of air pollution on plant-insect interactions.

Plant stress and insect behavior: cottonwood, ozone and the feeding and oviposition preference of a beetle.

Adults and larvae of the beetle Plagiodera versicolora preferred to feed on and consumed more of cottonwood, Populus deltoides, plant material that had been previously exposed to an acute dose of ozone (0.20 ppm, 5 h), compared to controls in choice experiments. However, females preferred to oviposit on the unexposed controls. Results were consistent for 2 cottonwood clones over 3 years in disc, leaf and whole-plant choice tests. The differential feeding and oviposition response of this insect to stressed plants could have at least 3 unexpected consequences: 1. An immediate increase in damage to stressed trees, but a subsequent decrease in damage. 2. A subsequent increase in damage to unstressed adjacent trees. 3. Changes in the insect and pathogen communities of both stressed and unstressed trees. These complex scenarios show that predicting outcomes of plant stress on plant-insect interactions will require comprchensive examination of behavioral, growth and reproductive responses of insects to stressed plants.