Matthew P. Ayres

Climate Change and Forest Disturbances

tudies of the effects of climate change on forestshave focused on the ability of species to tolerate tem-perature and moisture changes and to disperse,but they haveignored the effects of disturbances caused by climate change(e.g.,Ojima et al.1991).Yet modeling studies indicate the im-portance of climate effects on disturbance regimes (He et al.1999). Local, regional, and global changes in temperatureand precipitation can influence the occurrence, timing, fre-quency,duration,extent,and intensity of disturbances (Baker1995, Turner et al. 1998). Because trees can survive fromdecades to centuries and take years to become established,climate-change impacts are expressed in forests, in part,through alterations in disturbance regimes (Franklin et al.1992, Dale et al. 2000).Disturbances,both human-induced and natural,shape for-est systems by influencing their composition,structure,andfunctional processes.Indeed,the forests of the United Statesare molded by their land-use and disturbance history.Withinthe United States,natural disturbances having the greatest ef-fects on forests include fire,drought,introduced species,in-sect and pathogen outbreaks, hurricanes, windstorms, icestorms, and landslides (Figure 1). Each disturbance affectsforests differently. Some cause large-scale tree mortality,whereas others affect community structure and organizationwithout causing massive mortality (e.g., ground fires). For-est disturbances influence how much carbon is stored intrees or dead wood. All these natural disturbances interactwith human-induced effects on the environment,such as airpollution and land-use change resulting from resource ex-traction, agriculture, urban and suburban expansion, andrecreation.Some disturbances can be functions of both nat-ural and human conditions (e.g., forest fire ignition andspread) (Figure 2).

Assessing the consequences of global change for forest disturbance from herbivores and pathogens.

Herbivores and pathogens impact the species composition, ecosystem function, and socioeconomic value of forests. Herbivores and pathogens are an integral part of forests, but sometimes produce undesirable effects and a degradation of forest resources. In the United States, a few species of forest pests routinely have significant impacts on up to 20 million ha of forest with economic costs that probably exceed

Jensen's inequality predicts effects of environmental variation

1 billion/year. Climatic change could alter patterns of disturbance from herbivores and pathogens through: (1) direct effects on the development and survival of herbivores and pathogens; (2) physiological changes in tree defenses; and (3) indirect effects from changes in the abundance of natural enemies (e.g. parasitoids of insect herbivores), mutualists (e.g. insect vectors of tree pathogens), and competitors. Because of their short life cycles, mobility, reproductive potential, and physiological sensitivity to temperature, even modest climate change will have rapid impacts on the distribution and abundance of many forest insects and pathogens. We identify 32 syndromes of biotic disturbance in North American forests that should be carefully evaluated for their responses to climate change: 15 insect herbivores, browsing mammals; 12 pathogens; 1 plant parasite; and 3 undiagnosed patterns of forest decline. It is probable that climatic effects on some herbivores and pathogens will impact on biodiversity, recreation, property value, forest industry, and even water quality. Some scenarios are beneficial (e.g. decreased snow cover may increase winter mortality of some insect pests), but many are detrimental (e.g. warming tends to accelerate insect development rate and facilitate range expansions of pests and climate change tends to produce a mismatch between mature trees and their environment, which can increase vulnerability to herbivores and pathogens). Changes in forest disturbance can produce feedback to climate through affects on water and carbon flux in forest ecosystems; one alarming scenario is that climate warming may increase insect outbreaks in boreal forests, which would tend to increase forest fires and exacerbate further climate warming by releasing carbon stores from boreal ecosystems. We suggest a list of research priorities that will allow us to refine these risk assessments and adopt forest management strategies that anticipate changes in biotic disturbance regimes and mitigate the ecological, social, and economic risks.

Diversity of structure and antiherbivore activity in condensed tannins

Many biologists now recognize that environmental variance can exert important effects on patterns and processes in nature that are independent of average conditions. Jensens inequality is a mathematical proof that is seldom mentioned in the ecological literature but which provides a powerful tool for predicting some direct effects of environmental variance in biological systems. Qualitative predictions can be derived from the form of the relevant response functions (accelerating versus decelerating). Knowledge of the frequency distribution (especially the variance) of the driving variables allows quantitative estimates of the effects. Jensens inequality has relevance in every field of biology that includes nonlinear processes.

Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi

We characterized the structure of condensed tannins from 16 woody plant species (seven genera, six families) and determined their effects on six herbivorous insect species (four genera, two families). There were major differences in tannin structure, even between congeneric plant species. Condensed tannins differed markedly in their antiherbivore activity, averaged over these herbivores, and the herbivores differed in their sensitivity, averaged over these tannins. Furthermore, the same tannin can have different effects on different herbivores, presumably because of interactions between tannin structure and gut physiology. Results challenge the view that tannins provide an evolutionarily stable plant defense because of their uniform chemical properties. Condensed tannin can sometimes impact herbivore fitness through effects on survival and growth, but the largest effects in 45 insect–tannin combinations were less than that of many other plant metabolites at lower doses. Even at high doses, condensed tanni...

Local Adaptation to Regional Climates in Papilio Canadensis (Lepidoptera: Papilionidae)

The nitrogen content of plant tissue is low relative to that of herbivores; as a consequence, dietary N can limit the growth and reproduction of herbivores and select for attributes that increase N acquisition. Bark beetles face a particularly severe challenge because the phloem that they consume is very low in nitrogen and phosphorus relative to their requirements. We quantified variation in the phloem concentrations of N and P in the host tree, Pinus taeda, and evaluated the following hypotheses regarding the role of sym- biotic fungi in nutrient budgets of the herbivore Dendroctonus frontalis: D. frontalis ex- perience variation in phloem nutrient concentrations across several spatial scales (HI); mycangial fungi enhance the diet of D. frontalis larvae by contributing to the acquisition of N and P (H2); Ophiostoma minus, an apparently antagonistic fungal symbiont, hinders D. frontalis larvae because it does not enhance nutrient concentrations of the phloem as much as mycangial fungi do (H3); and larvae of bark beetle species that lack mycangial fungi must consume more phloem to accomplish the same growth as larvae of D. frontalis (H4). In addition, we developed a general model for the N budgets of herbivorous insects that identifies the possible combinations of dietary and physiological parameters that can allow developmental success on low-nutrient diets. Spatial variation in phloem N was mostly at the level of trees within sites (a scale of meters) while P mostly varied among sites (a scale of kilometers). Trees with higher N content produced larger D. frontalis adults. Prior to infestation by beetles, phloem nutrient concentrations were very uniform within trees and very low relative to that of the bark beetles (N and P concentrations of D. frontalis adults were 28 and 8 times greater, re- spectively). During infestation, phloem nutrient concentrations increased overall and be- came highly variable within trees. Nitrogen concentrations increased from 0.40 + 0.01% (mean + 1 SE) in uninfested phloem to 0.86 + 0.03% in the phloem surrounding successfully developing D. frontalis larvae, which are typically associated with one or two species of mutualistic mycangial fungi. Nitrogen concentrations were intermediate in other micro- habitats within infested trees, including regions with no adult colonization, with failed larval development, or colonized by the antagonistic bluestain fungus 0. minus. We pa- rameterized a general nutrient-budget model for D. frontalis and a sympatric non-mycangial bark beetle, Ips grandicollis, which indicated that (1) mycangial fungi provide their benefits by concentrating dietary N for larvae; (2) 0. minus may exert its antagonistic effects on D. frontalis larvae by failing to concentrate dietary N as much as mycangial fungi do; (3) non-mycangial bark beetles meet their N budgets through high consumption of unaltered, low-N phloem; and (4) larvae should easily meet their P requirements with any combination of consumption rate and development time that allows them to meet their N requirements. Alternative strategies for N acquisition may have general consequences for the population dynamics and community interactions of bark beetles.

Consequences of climate change for biotic disturbances in North American forests

Papilio canadensis encounters shorter, cooler summers in interior Alaska than in northern Michigan: average thermal sums are 583 vs. 985 Celsius degree—days (10°C base); mean daily temperature is 14.4 vs. 18.8°. The temperature physiology of P. canadensis could be evolutionarily conserved, or the species may be a composite of regionally adapted populations. We evaluated these hypotheses by comparing the developmental physiology of P. canadensis from Alaska and Michigan across a range of temperatures in the laboratory and field. Higher temperatures generally resulted in more rapid larval development, but the effects varied with insect population and host. At low temperatures (12°), Alaskan larvae grew faster than Michigan larvae (fifth instars doubled their fresh mass in 5.8 vs. 9.1 d), primarily due to 40% higher consumption rates. At high temperatures (30°), Alaskan larvae grew slower, faster, or the same as Michigan larvae, depending upon host. Effects of host quality were greatest at high temperatures. Elevated respiratory expenses in Alaskan larvae (35% higher than Michigan larvae) made them especially sensitive to host quality at high temperatures. Dry matter digestibility and nitrogen use efficiency differed across hosts, but not between populations or across temperatures. Molting accounted for 35—51% of development time. Alaskan larvae completed their fifth molt faster than Michigan larvae at 12° (11.8 vs. 17.8 d), but not at 30° (3.1 vs. 2.9 d). In both populations, molt was more temperature sensitive than growth at low temperatures (Q10 of 5.65 vs. 3.04 from 12 to 18°), but less temperature sensitive at high temperatures (Q10 of 1.60 vs. 2.06 from 18 to 30°). Survival differed across temperatures, but not between populations. Under ideal basking conditions, larvae in the field were able to elevate body temperatures °10° above ambient, but such conditions were rare in Alaska and larvae were usually near ambient temperature. Alaskan larvae were no better than Michigan larvae at selecting high radiation microsites or converting solar radiation into heat. Growth rates of Alaskan larvae were the same in the field and laboratory when fed the same foliage and exposed to the same mean daily air temperature. We incorporated P. canadensis temperature responses into a life history development model, then used a 48—yr climatic record to evaluate the fitness contributions of apparent adaptations to Alaskan summers. On a good host, at Alaskan temperatures, Alaskan P. canadensis had an estimated fitness 3.0 times greater than Michigan P. canadensis. Furthermore, the Michigan population was predicted to go extinct in 31 of 48 yr at Alaskan temperatures. Changes in growth temperature responses made the greatest contribution to enhanced fitness in Alaska, followed by increased mass of neonates, enhanced molting abilities at low temperatures, and a reduced size threshold for pupation. Analysis of fitness trade—offs suggested that extreme summers have been more important than average summers in shaping adaptive responses. Regional adaptation to climate allows P. canadensis to maintain a broader geographic distribution than would otherwise be possible, but northern distribution limits are probably still constrained by summer temperatures.

Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice

About one-third of North America is forested. These forests are of incalculable value to human society in terms of harvested resources and ecosystem services and are sensitive to disturbance regimes. Epidemics of forest insects and diseases are the dominant sources of disturbance to North American forests. Here we review current understanding of climatic effects on the abundance of forest insects and diseases in North America, and of the ecological and socioeconomic impacts of biotic disturbances. We identified 27 insects (6 nonindigenous) and 22 diseases (9 nonindigenous) that are notable agents of disturbance in North American forests. The distribution and abundance of forest insects and pathogens respond rapidly to climatic variation due to their physiological sensitivity to temperature, high mobility, short generation times, and high reproductive potential. Additionally, climate affects tree defenses, tree tolerance, and community interactions involving enemies, competitors, and mutualists of insects ...

Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle

Abstract Creating multiyear cycles in population density demands, in traditional models, causal factors that operate on local populations in a density-dependent way with time lags. However, cycles of the geometrid Epirrita autumnata in northern Europe may be regional, not local; i.e., successive outbreaks occur in different localities. We review possible causes of cycles of E. autumnata under both local and regional scenarios, including large-scale synchrony. Assuming cyclicity is a local phenomenon, individual populations of E. autumnata display peaks but populations all over the outbreak range fluctuate in synchrony. This concept assumes that the peaks at most localities are so low that they do not lead to visible defoliation and easily remain unnoticed. In this scenario, populations are able to start recovery a few years after the crash, i.e., at the time of the mitigation of detrimental delayed density-dependent factors, such as delayed inducible resistance of the host plant or parasitism. In that case, the same factors that lead to crashes also explain the periodicity of cyclic fluctuations. According to the regional cyclicity scenario, different factors can be important in different phases of the cycle. The key is to identify the factors that tend to produce outbreaks with a periodicity of about 10 years. Initiation of the increase phase seems to coincide with maxima in sunspot activity, but causal connections remain unclear. Climatic factor(s) associated with the solar cycle could contribute to the large-scale geographic synchrony.

IMPACT OF MINIMUM WINTER TEMPERATURES ON THE POPULATION DYNAMICS OF DENDROCTONUS FRONTALIS

Feedback from community interactions involving mutualisms are a rarely explored mechanism for generating complex population dynamics. We examined the effects of two linked mutualisms on the population dynamics of a beetle that exhibits outbreak dynamics. One mutualism involves an obligate association between the bark beetle, Dendroctonus frontalis and two mycangial fungi. The second mutualism involves Tarsonemus mites that are phoretic on D. frontalis (“commensal”), and a blue-staining fungus, Ophiostoma minus. The presence of O. minus reduces beetle larval survival (“antagonistic”) by outcompeting beetle-mutualistic fungi within trees yet supports mite populations by acting as a nutritional mutualist. These linked interactions potentially create an interaction system with the form of an endogenous negative feedback loop. We address four hypotheses: (1) Direct negative feedback: Beetles directly increase the abundance of O. minus, which reduces per capita reproduction of beetles. (2) Indirect negative feedback: Beetles indirectly increase mite abundance, which increases O. minus, which decreases beetle reproduction. (3) The effect of O. minus on beetles depends on mites, but mite abundance is independent of beetle abundance. (4) The effect of O. minus on beetles is independent of beetle and mite abundance. High Tarsonemus and O. minus abundances were strongly correlated with the decline and eventual local extinction of beetle populations. Manipulation experiments revealed strong negative effects of O. minus on beetles, but falsified the hypothesis that horizontal transmission of O. minus generates negative feedback. Surveys of beetle populations revealed that reproductive rates of Tarsonemus, O. minus, and beetles covaried in a manner consistent with strong indirect interactions between organisms. Co-occurrence of mutualisms embedded within a community may have stabilizing effects if both mutualisms limit each other. However, delays and/or non-linearities in the interaction systems may result in large population fluctuations.