Competition and Coexistence In a Multi-partner Mutualism: Interactions Between two Fungal Symbionts of the Mountain Pine Beetle In Beetle-attacked Trees

Despite overlap in niches, two fungal symbionts of the mountain pine beetle (Dendroctonus ponderosae), Grosmannia clavigera and Ophiostoma montium, appear to coexist with one another and their bark beetle host in the phloem of trees. We sampled the percent of phloem colonized by fungi four times over 1 year to investigate the nature of the interaction between these two fungi and to determine how changing conditions in the tree (e.g., moisture) affect the interaction. Both fungi colonized phloem at similar rates; however, G. clavigera colonized a disproportionately larger amount of phloem than O. montium considering their relative prevalence in the beetle population. High phloem moisture appeared to inhibit fungal growth shortly after beetle attack; however, by 1 year, low phloem moisture likely inhibited fungal growth and survival. There was no inverse relationship between the percent of phloem colonized by G. clavigera only and O. montium only, which would indicate competition between the species. However, the percent of phloem colonized by G. clavigera and O. montium together decreased after 1 year, while the percent of phloem from which no fungi were isolated increased. A reduction in living fungi in the phloem at this time may have significant impacts on both beetles and fungi. These results indicate that exploitation competition occurred after a year when the two fungi colonized the phloem together, but we found no evidence of strong interference competition. Each species also maintained an exclusive area, which may promote coexistence of species with similar resource use.     

Spatial Community Structure of Mountain Pine Beetle Fungal Symbionts Across a Latitudinal Gradient

Symbiont redundancy in obligate insect–fungal systems is thought to buffer the insect host against symbiont loss and to extend the environmental conditions under which the insect can persist. The mountain pine beetle is associated with at least three well-known and putatively obligate ophiostomatoid fungal symbionts that vary in their environmental tolerances. To better understand the spatial variation in beetle–fungal symbiotic associations, we examined the community composition of ophiostomatoid fungi associated with the mountain pine beetle as a function of latitude and elevation. The region investigated represents the leading edge of a recent outbreak of mountain pine beetle in western Canada. Using regression and principal components analysis, we identified significant spatial patterns in fungal species abundances that indicate symmetrical replacement between two of the three fungi along a latitudinal gradient and little variation in response to elevation. We also identified significant variation in the prevalence of pair-wise species combinations that occur within beetle galleries. Frequencies of pair-wise combinations were significantly different from what was expected given overall species abundances. These results suggest that complex processes of competitive exclusion and coexistence help determine fungal community composition and that the consequences of these processes vary spatially. The presence of three fungal symbionts in different proportions and combinations across a wide range of environmental conditions may help explain the success of mountain pine beetle attacks across a broad geographic range.     

In Vitro Interactions Between Yeasts and Bacteria and the Fungal Symbionts of the Mountain Pine Beetle (Dendroctonus ponderosae)

Multi-trophic interactions between prokaryotes, unicellular eukaryotes, and ecologically intertwined metazoans are presumably common in nature, yet rarely described. The mountain pine beetle, Dendroctonus ponderosae, is associated with two filamentous fungi, Grosmannia clavigera and Ophiostoma montium. Other microbes, including yeasts and bacteria, are also present in the phloem, but it is not known whether they interact with the symbiotic fungi or the host beetle. To test whether such interactions occur, we performed a suite of in vitro assays. Overall, relative yield of O. montium grown with microbes isolated from larval galleries was significantly greater than when the fungus was grown alone. Conversely, the yield of G. clavigera grown with these same microbes was less than or equal to when it was grown alone, suggesting that O. montium, and at least some microbes in larval galleries, have a mutualistic or commensal relationship, while G. clavigera and those same microbes have an antagonistic relationship. A bacterium isolated from phloem not colonized by beetles was found to inhibit growth of both G. clavigera and O. montium and appears to be an antagonist to both fungi. Our results suggest that bacteria and yeasts likely influence the distribution of mycangial fungi in the host tree, which, in turn, may affect the fitness of D. ponderosae.     

Nitrogen Cycling Responses to Mountain Pine Beetle Disturbance in a High Elevation Whitebark Pine Ecosystem

Ecological disturbances can significantly affect biogeochemical cycles in terrestrial ecosystems, but the biogeochemical consequences of the extensive mountain pine beetle outbreak in high elevation whitebark pine (WbP) (Pinus albicaulis) ecosystems of western North America have not been previously investigated. Mountain pine beetle attack has driven widespread WbP mortality, which could drive shifts in both the pools and fluxes of nitrogen (N) within these ecosystems. Because N availability can limit forest regrowth, understanding how beetle-induced mortality affects N cycling in WbP stands may be critical to understanding the trajectory of ecosystem recovery. Thus, we measured above- and belowground N pools and fluxes for trees representing three different times since beetle attack, including unattacked trees. Litterfall N inputs were more than ten times higher under recently attacked trees compared to unattacked trees. Soil inorganic N concentrations also increased following beetle attack, potentially driven by a more than two-fold increase in ammonium (NH₄ ⁺) concentrations in the surface soil organic horizon. However, there were no significant differences in mineral soil inorganic N or soil microbial biomass N concentrations between attacked and unattacked trees, implying that short-term changes in N cycling in response to the initial stages of WbP attack were restricted to the organic horizon. Our results suggest that while mountain pine beetle attack drives a pulse of N from the canopy to the forest floor, changes in litterfall quality and quantity do not have profound effects on soil biogeochemical cycling, at least in the short-term. However, continuous observation of these important ecosystems will be crucial to determining the long-term biogeochemical effects of mountain pine beetle outbreaks.     

Mountain Pine Beetle Presence Affects Nest Patch Choice of Red-Breasted Nuthatches

Abstract: The mountain pine beetle (Dendroctonus ponderosae) outbreak in western Canada poses significant conservation concern; thus, insights into its effects on wildlife habitat are essential. We used generalized linear mixed models to examine the influence of quaking aspen (Populus tremuloides) and mountain pine beetle—infected lodgepole pine (Pinus contortus) on nest patch selection of red-breasted nuthatches (Sitta canadensis) in central British Columbia, Canada. Prior to the outbreak, nuthatches selected nest patches with 64% more suitable nest trees (standing dead aspen, ≥12.5 cm dbh) than available (103 trees/ha vs. 63 trees/ha, respectively), but in outbreak years nuthatches chose nest patches with 37% more beetle-infected pine trees than available (63 trees/ha vs. 46 trees/ha, respectively). Our results suggest that nuthatches select sites that maximize nesting and foraging opportunities and, during food pulses, may trade off higher densities of suitable nest trees for higher densities of foraging trees. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):733–737; 2008)     

exo-Brevicomin biosynthetic pathway enzymes from the Mountain Pine Beetle,Dendroctonus ponderosae

exoBrevicomin (exo-7-ethyl-5-methyl-6,8-dioxabicyclo[3.2.1]octane) is an important semiochemical for a number of beetle species, including the highly destructive Mountain Pine Beetle (Dendroctonus ponderosae). It is also found in other insects and the African elephant. Despite its significance, very little is known about its biosynthesis. A recent microarray analysis implicated a small cluster of three D. ponderosae genes in exo-brevicomin biosynthesis, two of which had identifiable open reading frames (Aw et al., 2010; BMC Genomics 11:215). Here we report further expression profiling of two genes in that cluster and functional analysis of their recombinantly-produced enzymes. One encodes a short-chain dehydrogenase that used NAD(P)⁺ as a co-factor to catalyze the oxidation of (Z)-6-nonen-2-ol to (Z)-6-nonen-2-one. We therefore named the enzyme (Z)-6-nonen-2-ol dehydrogenase (ZnoDH). The other encodes the cytochrome P450, CYP6CR1, which epoxidized (Z)-6-nonen-2-one to 6,7-epoxynonan-2-one with very high specificity and substrate selectivity. Both the substrates and products of the two enzymes are intermediates in the exo-brevicomin biosynthetic pathway. Thus, ZnoDH and CYP6CR1 are enzymes that apparently catalyze the antepenultimate and penultimate steps in the exo-brevicomin biosynthetic pathway, respectively.     

The Influence of Previous Mountain Pine Beetle (Dendroctonus ponderosae) Activity on the 1988 Yellowstone Fires

We examined the historical record of mountain pine beetle (Dendroctonus ponderosae Hopkins) activity within Yellowstone National Park, Wyoming, for the 25-years period leading up to the 1988 Yellowstone fires (1963–86) to determine how prior beetle activity and the resulting tree mortality affected the spatial pattern of the 1988 Yellowstone fires. To obtain accurate estimates of our model parameters, we used a Markov chain Monte Carlo method to account for the high degree of spatial autocorrelation inherent to forest fires. Our final model included three statistically significant variables: drought, aspect, and sustained mountain pine beetle activity in the period 1972–75. Of the two major mountain pine beetle outbreaks that preceded the 1988 fires, the earlier outbreak (1972–75) was significantly correlated with the burn pattern, whereas the more recent one (1980–83) was not. Although regional drought and high winds were responsible for the large scale of this event, the analysis indicates that mountain pine beetle activity in the mid-1970s increased the odds of burning in 1988 by 11% over unaffected areas. Although relatively small in magnitude, this effect, combined with the effects of aspect and spatial variation in drought, had a dramatic impact on the spatial pattern of burned and unburned areas in 1988.     

Rapid Increases in Forest Understory Diversity and Productivity following a Mountain Pine Beetle (Dendroctonus ponderosae) Outbreak in Pine Forests

The current unprecedented outbreak of mountain pine beetle (Dendroctonus ponderosae) in lodgepole pine (Pinus contorta) forests of western Canada has resulted in a landscape consisting of a mosaic of forest stands at different stages of mortality. Within forest stands, understory communities are the reservoir of the majority of plant species diversity and influence the composition of future forests in response to disturbance. Although changes to stand composition following beetle outbreaks are well documented, information on immediate responses of forest understory plant communities is limited. The objective of this study was to examine the effects of D. ponderosae-induced tree mortality on initial changes in diversity and productivity of understory plant communities. We established a total of 110 1-m² plots across eleven mature lodgepole pine forests to measure changes in understory diversity and productivity as a function of tree mortality and below ground resource availability across multiple years. Overall, understory community diversity and productivity increased across the gradient of increased tree mortality. Richness of herbaceous perennials increased with tree mortality as well as soil moisture and nutrient levels. In contrast, the diversity of woody perennials did not change across the gradient of tree mortality. Understory vegetation, namely herbaceous perennials, showed an immediate response to improved growing conditions caused by increases in tree mortality. How this increased pulse in understory richness and productivity affects future forest trajectories in a novel system is unknown.     

Population Structure of Mountain Pine Beetle Symbiont Leptographium longiclavatum and the Implication on the Multipartite Beetle-Fungi Relationships

Over 18 million ha of forests have been destroyed in the past decade in Canada by the mountain pine beetle (MPB) and its fungal symbionts. Understanding their population dynamics is critical to improving modeling of beetle epidemics and providing potential clues to predict population expansion. Leptographium longiclavatum and Grosmannia clavigera are fungal symbionts of MPB that aid the beetle to colonize and kill their pine hosts. We investigated the genetic structure and demographic expansion of L. longiclavatum in populations established within the historic distribution range and in the newly colonized regions. We identified three genetic clusters/populations that coincide with independent geographic locations. The genetic profiles of the recently established populations in northern British Columbia (BC) and Alberta suggest that they originated from central and southern BC. Approximate Bayesian Computation supports the scenario that this recent expansion represents an admixture of individuals originating from BC and the Rocky Mountains. Highly significant correlations were found among genetic distance matrices of L. longiclavatum, G. clavigera, and MPB. This highlights the concordance of demographic processes in these interacting organisms sharing a highly specialized niche and supports the hypothesis of long-term multipartite beetle-fungus co-evolutionary history and mutualistic relationships.     

Pattern Formation in a Model for Mountain Pine Beetle Dispersal: Linking Model Predictions to Data

Pattern formation occurs in a wide range of biological systems. This pattern formation can occur in mathematical models because of diffusion-driven instability or due to the interaction between reaction, diffusion, and chemotaxis. In this paper, we investigate the spatial pattern formation of attack clusters in a system for Mountain Pine Beetle. The pattern formation (aggregation) of the Mountain Pine Beetle in order to attack susceptible trees is crucial for their survival and reproduction. We use a reaction-diffusion equation with chemotaxis to model the interaction between Mountain Pine Beetle, Mountain Pine Beetle pheromones, and susceptible trees. Mathematical analysis is utilized to discover the spacing in-between beetle attacks on the susceptible landscape. The model predictions are verified by analysing aerial detection survey data of Mountain Pine Beetle Attack from the Sawtooth National Recreation Area. We find that the distance between Mountain Pine Beetle attack clusters predicted by our model closely corresponds to the observed attack data in the Sawtooth National Recreation Area. These results clarify the spatial mechanisms controlling the transition from incipient to epidemic populations and may lead to control measures which protect forests from Mountain Pine Beetle outbreak.     

Life Cycle of the Mulberry Longicorn Beetle,Apriona germari Hope on an Artificial Diet

Mulberry longicorn beetle, Apriona germari, was reared on an artificial diet to investigate its life cycle. Average egg period was 17.95 days. Most larvae pupated at the 8th (33.3%) or 9th (33.3%) instars, but others emerged from the 7th to the 11th instars. The total duration of larval stage from the 1st to the end of the 9th and the 11th instars were 176.2 and 251.5 days, respectively. For terminatiopn of diapause and acceleration of pupation, low temperature treatment at 5°C for 60 days was highly effective. Average pupal period for female and male was 19.3 and 18.4 days, respectively. Average longevity of adults was similar with 40.5 days for female and 44.3 days for male. Mating had occurred from about 10 days after the adult emergence, and then a female adult laid one or two eggs per day. Average number of eggs oviposited by a female was approximately 47.7. Total life span of A. germari, when reared on an artificial diet in the laboratory, ranged broadly from 197.5 days to 331.5 days mainly depending on the larval period.     

Spatial Distribution of Mountain Pine Beetle Outbreaks in Relation to Climate and Stand Characteristics： A Dendroecological Analysis

Principal components analysis, followed by K-means cluster analysis, was used to detect variations in the timing and magnitude of Pinus contorta Dough ex Loud. growth releases attributed to mountain pine beetle outbreaks in 31 stands of central British Columbia. Four major growth release patterns were identified from 1970 to 2000. Variations in the timing of growth releases among clustered stands corresponded well to aerial survey data indicating the timing of beetle outbreaks in the study area. Redundancy analysis was used to determine how variations in the timing and magnitude of growth releases attributed to beetle outbreaks changed with variations in climate or stand conditions over the study area. The first RDA axis, which accounted for 39% of the variations in growth patterns among stands, was significantly （P〈0.05） correlated with gradients in the percentage of pine in stands killed by mountain pine beetle, summer aridity, variation in summer precipitation, distance from initial infestation site, average pine age, and maximum August temperatures. The second RDA axis explained 6% of the variations and was significantly correlated with gradients in the beetle climate suitability index, extreme cold month temperatures, and site index. Comparisons of growth release patterns with aerial survey data and redundancy analyses indicated that dendrochronological techniques are useful for identifying mountain pine beetle outbreaks in central British Columbia, particularly among stands that had a density high enough to produce a growth release signal. Provided future studies account for interannual weather fluctuations, identification of growth increases due to stand thinning caused by beetle outbreaks will be useful for reconstructing the history of beetle outbreaks over much longer time periods.     

Spatial Distibution of Mountain Pine Beetle Outbreaks in Relation to Climate and Stand Characteristics:A Dendroecological Analysis

Principal components analysis, followed by K-means cluster analysis, was used to detect variations in the timing and magnitude of Pinus contorta Dougl. ex Loud. growth releases attributed to mountain pine beetle outbreaks in 31 stands of central British Columbia. Four major growth release patterns were identified from 1970 to 2000.Variations in the timing of growth releases among clustered stands corresponded well to aerial survey data indicating the timing of beetle outbreaks in the study area. Redundancy analysis was used to determine how variations in the timing and magnitude of growth releases attributed to beetle outbreaks changed with variations in climate or stand conditions over the study area. The first RDA axis, which accounted for 39% of the variations in growth patterns among stands, was significantly (P＜0.05) correlated with gradients in the percentage of pine in stands killed by mountain pine beetle, summer aridity, variation in summer precipitation, distance from initial infestation site, average pine age, and maximum August temperatures. The second RDA axis explained 6% of the variations and was significantly correlated with gradients in the beetle climate suitability index, extreme cold month temperatures, and site index. Comparisons of growth release patterns with aerial survey data and redundancy analyses indicated that dendrochronological techniques are useful for identifying mountain pine beetle outbreaks in central British Columbia, particularly among stands that had a density high enough to produce a growth release signal. Provided future studies account for interannual weather fluctuations, identification of growth increases due to stand thinning caused by beetle outbreaks will be useful for reconstructing the history of beetle outbreaks over much longer time periods.     

Spatial Distribution of Mountain Pine Beetle Outbreaks in Relation to Climate and Stand Characteristics:A Dendroecological Analysis

Principal components analysis, followed by K-means cluster analysis, was used to detect variations in the timingand magnitude of Pinus contorfa Dougl. ex Loud. growth releases attributed to mountain pine beetle outbreaks in31 stands of central British Columbia. Four major growth release patterns were identified from 1970 to 2000.Variations in the timing of growth releases among clustered stands corresponded well to aerial survey dataindicating the timing of beetle outbreaks in the study area. Redundancy analysis was used to determine howvariations in the timing and magnitude of growth releases attributed to beetle outbreaks changed with variationsin climate or stand conditions over the study area. The first RDA axis, which accounted for 39% of the variations ingrowth patterns among stands, was significantly (P<0.05) correlated with gradients in the percentage of pine instands killed by mountain pine beetle, summer aridity, variation in summer precipitation, distance from initialinfestation site, average pine age, and maximum August temperatures. The second RDA axis explained 6% of thevariations and was significantly correlated with gradients in the beetle climate suitability index, extreme coldmonth temperatures, and site index. Comparisons of growth release patterns with aerial survey data and redun-dancy analyses indicated that dendrochronological techniques are useful for identifying mountain pine beetleoutbreaks in central British Columbia, particularly among stands that had a density high enough to produce agrowth release signal. Provided future studies account for interannual weather fluctuations, identification ofgrowth increases due to stand thinning caused by beetle outbreaks will be useful for reconstructing the history ofbeetle outbreaks over much longer time periods.     

Competitive Interactions among Symbiotic Fungi of the Southern Pine Beetle

The southern pine beetle, a damaging pest of conifers, is intimately linked to three symbiotic fungi. Two fungi, Ceratocystiopsis ranaculosus and Entomocorticium sp. A, are transported within specialized structures (mycangia) in the beetle exoskeleton and are mutualists of the beetle. A third fungus, Ophiostoma minus, is transported externally on the beetle exoskeleton (phoretically) and is an antagonist of the beetle. This study examined competitive interactions among these three fungi. The results of de Wit replacement series and primary and secondary resource capture assays with these fungi provide strong evidence for differential competition between the phoretic and mycangial fungi. O. minus was the most able to capture both uncolonized and colonized resources. Entomocorticium sp. A and C. ranaculosus, although equal to one another in competitive abilities, differed in their ability to compete with O. minus. Entomocorticium sp. A was able to maintain space free of O. minus to a much greater degree than was C. ranaculosus. The outcome of such competitive interactions may have significant impacts on the biology of this ecologically and economically important beetle.     

The Role of Wildfire,Prescribed Fire,and Mountain Pine Beetle Infestations on the Population Dynamics of Black-Backed Woodpeckers in the Black Hills,South Dakota

Wildfire and mountain pine beetle infestations are naturally occurring disturbances in western North American forests. Black-backed woodpeckers (Picoides arcticus) are emblematic of the role these disturbances play in creating wildlife habitat, since they are strongly associated with recently-killed forests. However, management practices aimed at reducing the economic impact of natural disturbances can result in habitat loss for this species. Although black-backed woodpeckers occupy habitats created by wildfire, prescribed fire, and mountain pine beetle infestations, the relative value of these habitats remains unknown. We studied habitat-specific adult and juvenile survival probabilities and reproductive rates between April 2008 and August 2012 in the Black Hills, South Dakota. We estimated habitat-specific adult and juvenile survival probability with Bayesian multi-state models and habitat-specific reproductive success with Bayesian nest survival models. We calculated asymptotic population growth rates from estimated demographic rates with matrix projection models. Adult and juvenile survival and nest success were highest in habitat created by summer wildfire, intermediate in MPB infestations, and lowest in habitat created by fall prescribed fire. Mean posterior distributions of population growth rates indicated growing populations in habitat created by summer wildfire and declining populations in fall prescribed fire and mountain pine beetle infestations. Our finding that population growth rates were positive only in habitat created by summer wildfire underscores the need to maintain early post-wildfire habitat across the landscape. The lower growth rates in fall prescribed fire and MPB infestations may be attributed to differences in predator communities and food resources relative to summer wildfire.