Bernhard Stadler

Hemlock woolly adelgid in New England forests : canopy impacts transforming ecosystem processes and landscapes

Exotic insect pests may strongly disrupt forest ecosystems and trigger major shifts in nutrient cycling, structure, and composition. We examined the relationship between these diverse effects for the hemlock woolly adelgid (HWA, Adelges tsugae Annand) in New England forests by studying its impacts on local canopy processes in stands differing in infestation levels and linking these impacts to shifts in canopy nutrient cycling and stand and landscape effects. HWA initiated major changes in canopy biomass and distribution. Whereas uninfested trees exhibit a significant decline in canopy biomass from the center to the periphery and a positive correlation between total needle litter and estimated biomass, infested trees have significantly less total canopy biomass, produce less new foliage, shed relatively more needles, and exhibit no correlation between litter and canopy biomass. Foliar N content of infested trees was 20%–40% higher than reference trees, with the strongest increase in young foliage supporting the highest densities of HWA. Foliar %C was unaffected by HWA or foliar age. Epiphytic microorganisms on hemlock needles exhibited little variation in abundance within canopies, but colony-forming units of bacteria, yeast, and filamentous fungi were 2–3 orders of magnitude more abundant on medium and heavily infested than uninfested trees. Throughfall chemistry, quantity, and spatial pattern were strongly altered by HWA. Throughfall exhibits a strong gradient beneath uninfested trees, decreasing in volumes from the canopy periphery to the trunk by more than 45%. The amount of throughfall beneath infested trees exhibits no spatial pattern, reaches 80%–90% of the bulk precipitation, and is characterized by significantly higher concentrations of nitrogen compounds, dissolved organic carbon, and cations. Across the southern New England landscape there is a strong south-to-north gradient of decreasing hemlock tree and sapling mortality and understory compositional change that corresponds to the duration of infestation. Regionally, black birch (Betula lenta L.) is profiting most from hemlock decline by significantly increasing in density and cover. These findings suggest that it is necessary to study the connections between fast/small-scale processes such as changes in nutrient cycling in tree canopies and slow/integrative processes like shifts in biogeochemieal cycling and compositional changes at forest stands and landscapes to better understand the effects of an exotic pest species like HWA on forest ecosystem structure and function.

Insect herbivores and the nutrient flow from the canopy to the soil in coniferous and deciduous forests

Phytophagous insects can have severe impacts on forested ecosystems in outbreak situations but their contribution to flows of energy and matter is otherwise not so well known. Identifying the role of phytophagous insects in forested ecosystems is partly hindered by the difficulty of combining results from population and community ecology with those from ecosystem ecology. In our study we compared the effects of aphids and leaf-feeding lepidopterous larvae on the epiphytic micro-organisms in the canopies of spruce, beech and oak, and on the vertical flow of energy and nutrients from the canopies down to the forest floor. We particularly searched for patterns resulting from endemic herbivory rather than outbreak situations. Excreta of lepidopterous larvae and aphids promoted the growth of epiphytic micro-organisms (bacteria, yeasts, filamentous fungi) on needles and leaves, which suggests that micro-organisms were energy limited. Leachates from needles and leaves of infested trees contained higher concentrations of dissolved organic C and lower concentrations of NH4-N and NO3-N, relative to uninfested trees. The seasonal abundance of herbivores and micro-organisms significantly affected the dynamics of throughfall chemistry; for instance, concentrations of inorganic N were lower underneath infested than uninfested trees during June and July. There was little difference between the chemistry of soil solutions collected from the forest floor beneath infested and uninfested trees. Thus, under moderate to low levels of infestation the effects of above-ground herbivory seems to be obscured in the soil through buffering biological processes.

Linking aphid ecology with nutrient fluxes in a coniferous forest

Flows of dissolved organic carbon (DOC) in throughfall and soil solutions in forest ecosystems vary spatially and temporally. However, the reasons for the variability of DOC flows are unknown. Phytophagous insects such as aphids have not been considered a potential source of organic carbon, even though aphids feeding on trees excrete copious amounts of honeydew. We followed the key processes determining the origin, flow, and path of honeydew from the phyllosphere of a Norway spruce stand to the soil. We analyzed the chemical composition of needle leachates, throughfall, and soil solution to calculate fluxes of DOC and hexose-C in an aphid-infested and an uninfested Norway spruce stand. At the individual aphid level, the amount of honeydew produced was dependent on temperature, developmental stage, and the nutritional status of spruce. At the population level, colony growth and natural enemies influenced the amount of honeydew available in the phyllosphere. The growth rates of microorganisms on spruce needles were significantly increased when honeydew was available. This study of the fate of honeydew and associated metabolites within a forest stand shows that the concentrations of DOC and hexose-C in throughfall were reduced on the way to the soil and that there were no differences in the soil solutions from infested and uninfested stands. However, the distribution and abundance of honeydew-producing Homoptera had a marked effect on the spatial and temporal variability in the DOC concentrations in throughfall. High DOC concentrations in throughfall during summer are not exclusively due to the leaching of nutrients from leaves, but may also be attributed to the excreta of aphids. Our results highlight the importance of studying physiological and life history processes in addition to taking the traditional biomass approach to ecosystem studies. We discuss our results with regard to the types of information that are preserved, transformed, or lost when crossing the conceptual border between one scale of observation and another. We emphasize the importance of identifying key processes at different spatiotemporal scales by linking the biology of individuals and populations with flows of energy and matter within an ecosystem, while stressing the need to identify ecosystem changes at different scales of observation.

The ecology of energy and nutrient fluxes in hemlock forests invaded by hemlock woolly adelgid

The hemlock woolly adelgid (HWA, Adelges tsugae Annand) is currently causing a severe decline in vitality and survival of eastern hemlock in North American forests. We analyzed the effects of light HWA infestation on vertical energy and nutrient fluxes from the canopy to the forest floor. Canopy throughfall, litter lysimeters, and laboratory litter microcosms were used to examine the effects of HWA-affected and unaffected throughfall on litter type, leachate, and litter chemistry. Early in the season adelgid infestation caused higher dissolved organic carbon (DOC; +24.6%), dissolved organic nitrogen (DON; +28.5%), and K (+39.3%) fluxes and lower inorganic nitrogen fluxes (-39.8%) in throughfall and in adjacent litter solutions collected beneath infested compared to uninfested trees. Needle litter collected beneath uninfested hemlock had significantly lower N concentrations compared to needles collected beneath infested trees, while no difference in N concentrations was found in birch litter. Bacteria were significantly more abundant on hemlock and birch litter beneath infested trees, while yeasts and filamentous fungi showed no consistent response to HWA throughfall. Litter microcosms showed that less DOC was leaching from birch than from hemlock needles when exposed to HWA throughfall. Overall, NH4-N and DON leachate concentrations were higher from birch than from hemlock litter. Thus, HWA-affected throughfall leads to qualitative and quantitative differences in nitrogen export from the litter layer. The N concentration of hemlock litter did not change with time, but the N concentration in birch litter increased significantly during the course of the experiment, especially when HWA-affected throughfall was applied. We suggest a nonlinear conceptual model for the temporal and vertical transition of energy and nutrient fluxes relative to progressing HWA infestation from a pure hemlock to a birch/maple-dominated forest. Progressive needle loss and changes in needle chemistry are likely to produce a humped-shaped DOC curve, while N fluxes initially decrease as infestation continues but rise eventually with hemlock decline and immigration of hardwood species. These findings suggest that it is necessary to understand the biology and specific physiological/trophic effects of exotic pests on their hosts and associated ecosystem processes in order to decipher the temporal dynamics, direction of change, and functional consequences.

Aphid honeydew and its effect on the phyllosphere microflora of Picea abies (L.) Karst

Aphids of the genus Cinara, feeding on Norway spruce, excrete copious amounts of honeydew, a carbon-rich waste product, which accumulates locally on needles and twigs. We investigated the role of honeydew as a potential source of energy which might promote the growth of micro-organisms in the phyllosphere of conifer trees. To approach this question, we followed the population dynamics of Cinara spp. in a natural forest stand over two seasons. We also studied the amounts of honeydew produced by individual aphids and identified potential parameters which might influence honeydew production. Finally, we determined the growth of micro-organisms on infested and uninfested needles of Norway spruce during the growing season. Confined to Picea abies, the investigated Cinara species only became abundant in midsummer, when needles and shoots were expanding. The populations showed only a single peak in abundance, the timing and magnitude of which may vary from year to year due to weather conditions, changes in plant quality in a yearly cycle or the impact of natural enemies. The amount of honeydew produced by individual aphids was dependent on the developmental stage of the aphid, the nutritional supply of its host plant and on the developmental state of the Norway spruce (e.g. bud burst, end of shoot extension). The presence of honeydew significantly increased the growth of bacteria, yeast and filamentous fungi on the surface of needles and there was a pronounced seasonal trend, with the highest abundance in midsummer correlating with the period of peak aphid abundance. Taken together, these findings indicate that aphids have an influence on microbial ecology in the phyllosphere of trees. The implication of our study, from interactions at the population level to effects and potential consequences for C and N fluxes at the level of forest ecosystems, is discussed.

A comparative analysis of morphological and ecological characters of European aphids and lycaenids in relation to ant attendance

Ants are a major environmental factor for many insect species. For example, aphids and lycaenids have evolved an array of associations with ants ranging from obligate myrmecophily to the avoidance of contact. Here we (1) analyze the predictive power of different ecological and morphological traits for explaining the strength of the association between ants and aphids/lycaenids and (2) contrast different taxonomic levels with respect to the variance explained by ant attendance. Data come from a literature survey including 112 species of aphids and 103 species of lycaenids from Europe. For aphids, feeding on woody plant parts is positively associated with ant attendance, while a high degree of mobility, feeding in isolation, and the possession of wings in the adult stage are negatively associated with ant attendance. In lycaenids, feeding on inflorescences and feeding on Fabaceae host plants is closely associated with ant attendance, while living in forests bears a smaller likelihood to establish mutualistic relationships. Body size always appeared to be a poor predictor for the degree of ant attendance. Overall, in both insect groups less than 10% of the variation in the ecological traits recorded is explained by the different modes of ant association. When decomposing the variance in traits explained by ant attendance at different taxonomic levels, aphids and lycaenids show contrasting results. In aphids, most variance in the degree of ant attendance is explained at the subfamily level and least at the species level. The opposite is true for lycaenids, where most variance is explained at the lowest taxonomic level. Possible mechanisms explaining these different patterns of associations with ants are suggested.

Defence reactions in aphids: the influence of state and future reproductive success

This paper investigates the influence of life-history traits on the defence reactions shown by aphids. In particular, we combine experimental data on the reproductive biology of the monophagous aphid Uroleucon jaceae (L.) feeding on Centaurea jacea L. with theoretical considerations to predict the behaviour of this aphid when attacked by a predator. In laboratory experiments we first determine the reproductive behaviour of this aphid on different plant developmental stages and plant qualities. In food deprivation experiments we examine the effect of different patterns of resource allocation to soma and gonads on the ability to survive without food. Aphids feeding on the shooting stage of high-quality plants had high reproductive rates and survived longest when deprived of food

Wedged between bottom-up and top-down processes: aphids on tansy

Abstract.  1. Many species of aphids exploit a single host‐plant species and have to cope with changing environmental conditions. They often vary greatly in abundance even when feeding on the same host. In a field experiment, the bottom‐up (plant quality/patch type frequency) and top‐down (ant attendance/predation) effects on the abundance of four species of aphids feeding on tansy (Tanacetum vulgare) were tested using a full factorial design. In addition, a model was used to examine these patch characteristics for their relative effects on the population dynamics and abundance of different aphid species.

Foraging patterns of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani on banana

The searching behaviour of two aphid parasitoids, Lysiphlebus testaceipes (Cresson) and Aphidius colemani Viereck (Hymenoptera, Aphidiidae), was analysed. Both species searched banana plants (Musa spec.) infested with the banana aphid Pemalonia nigronervosa Coq. in a different way. L. testaceipes restricted its search to open plant structures and avoided concealed areas. A. colemani partitioned its time spent on the plant between open and concealed areas. This general pattern was independent of aphid colony size and was also observed in the absence of aphids. As a consequence of these searching tactics, the borders of a host patch differed for both parasitoid species. For L. testaceipes, the patch consisted only of aphids feeding on open structures, while it comprised the whole aphid colony for A. colemani. The observed searching patterns resulted in a different exploitation of the aphid colonies.

Adaptive allocation of resources and life-history trade-offs in aphids relative to plant quality

The need to allocate a limited amount of energy between different life-history traits is a fundamental assumption in life-history theory. However, it has often turned out to be extremely difficult to measure the competing processes that contribute to costs or benefits for individual organisms. The present investigation begins by analysing how an aphid clonal lineage adapts its reproductive investment to moderate changes in host plant quality (e.g. during the life cycle of its host). Using Centaurea jacea and Uroleucon jaceae as a model plantaphid system, I show that reproductive investment can be far more complex than indicated by dry or wet mass of the gonads alone. The number of embryos of a particular size class or developmental state present in the reproductive system of an aphid is highly flexible and is influenced by the quality of the host plant. Next, the effects of a particular reproductive investment on survival during periods of food deprivation are analysed for aphids originating from host-plants of different qualities. When food stress is severe the ability to rapidly resorb and reallocate resources committed to offspring is important for survival. However, this ability is limited. I argue that, in periods of food stress, young, unsclerotized embryos might serve as a kind of energy buffer similar to a fat body and are therefore not relevant to cost-benefit calculations. However, embryos that are beginning to sclerotize within the ovarioles are not available for resorption and resource reallocation. They compete for nutrients with their mother and contribute to costs. Therefore, it is suggested that the reproductive investment of an aphid should not be equated with reproductive costs in a general al way. The dynamics of adaptive resource allocation and resorption are a key feature of an aphids life history, and the implications for life-history theory are discussed.