Invasion patterns of emerald ash borer and European earthworms in forested ecosystems

Invasive and exotic species present a serious threat to the health and sustainability of natural ecosystems. These species often benefit from anthropogenic activities that aid their introduction and dispersal. This dissertation focuses on invasion dynamics of the emerald ash borer, native to Asia, and European earthworms. These species have shown detrimental impacts in invaded forest ecosystems across the Great Lakes region, and continue to spread via human-assisted long distance dispersal and by natural modes of dispersal into interior forests from areas of introduction. Successful forest management requires that the impact and effect of invasive species be considered and incorporated into management plans. Understanding patterns and constraints of introduction, establishment, and spread will aid in this effort. To assist in efforts to locate introduction points of emerald ash borer, a multicriteria risk model was developed to predict the highest risk areas. Important parameters in the model were road proximity, land cover type, and campground proximity. The model correctly predicted 85% of known emerald ash borer invasion sites to be at high risk. The model’s predictions across northern Michigan can be used to focus and guide future monitoring efforts. Similar modeling efforts were applied to the prediction of European earthworm invasion in northern Michigan forests. Field sampling provided a means to improve upon modeling efforts for earthworms to create current and future predictions of earthworm invasion. Those sites with high soil pH and high basal area of earthworm preferred overstory species (such as basswood and maples) had the highest likelihood of European earthworm invasion. Expanding beyond Michigan into the Upper Great Lakes region, earthworm populations were sampled across six National Wildlife Refuges to identify potential correlates and deduce specific drivers and constraints of earthworm invasion. Earthworm communities across all refuges were influenced by patterns of anthropogenic activity both within refuges and in surrounding ecoregions of study. Forest composition, soil pH, soil organic matter, anthropogenic cover, and agriculture proximity also proved to be important drivers of earthworm abundance and community composition. While there are few management options to remove either emerald ash borer or European earthworms from forests after they have become well established, prevention and early detection are important and can be beneficial. An improved understanding the factors controlling the distribution and invasion patterns of exotic species across the landscape will aid efforts to determine their consequences and generate appropriate forest management solutions to sustain ecosystem health in the presence of these invaders.

Detection and landing behavior of emerald ash borer, Agrilus planipennis, at low population density

The exotic emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), was first discovered in North America in southeastern Michigan, USA, and Windsor, Ontario, Canada in 2002. Significant ash (Fraxinus spp.) mortality has been caused in areas where this insect has become well established, and new infestations continue to be discovered in several states in the United States and in Canada. This beetle is difficult to detect when it invades new areas or occurs at low density. Girdled trap tree and ground surveys have been important tools for detecting emerald ash borer populations, and more recently, purple baited prism traps have been used in detection efforts. Girdled trap trees were found to be more effective than purple prism traps at detecting emerald ash borer as they acted as sinks for larvae in an area of known low density emerald ash borer infestation. The canopy condition of the trap trees was not predictive of whether they were infested or not, indicating that ground surveys may not be effective for detection in an area of low density emerald ash borer population. When landing rates of low density emerald ash borer populations were monitored on non-girdled ash trees, landing rates were higher on larger, open grown trees with canopies that contain a few dead branches. As a result of these studies, we suggest that the threshold for emerald ash borer detection using baited purple prism traps hung at the canopy base of trees is higher than for girdled trap trees. In addition, detection of developing populations of EAB may be possible by selectively placing sticky trapping surfaces on non-girdled trap trees that are the larger and more open grown trees at a site.

EVALUATION AND MONITORING OF ASH (FRAXINUS SPP.) TOLERANT TO LONG-TERM EMERALD ASH BORER (AGRILUS PLANIPENNIS [COLEOPTERA: BUPRESTIDAE]) EXPOSURE

Invasive insects that successfully establish in introduced areas can significantly alter natural communities. These pests require specific establishment criteria (e.g. host suitability) that, when known, can help quantify potential damage to infested areas. Emerald ash borer (Agrilus planipennis [Coleoptera: Buprestidae]) is an invasive phloem-feeding pest which is responsible for the death of millions of ash trees (Fraxinus spp. L.). Over 200 surviving ash trees were previously identified in the Huron-Clinton Metroparks located in southeast Michigan. Trees were assessed over a four year period and a hierarchical cluster analysis was performed on dieback, vigor, and presence of signs and symptoms, in order to place trees into one of three tolerance groups. The clustering of trees with different responses to emerald ash borer attack suggests that there are different tolerance levels in North American ash trees in southeastern Michigan, and these groups were designated as apparently tolerant, not tolerant and intermediate tolerance. Adult landing rates and evidence of adult emergence were significantly lower in the apparently tolerant group compared with the not tolerant group, but larval survival from eggs placed on trees did not differ between tolerance groups. Therefore, it appears that apparently tolerant trees survive because they are less attractive to adult beetles which results in fewer eggs being laid on them. Trees in the apparently tolerant group remained of higher vigor over the four years of the study. North American ash may survive the emerald ash borer epidemic due to natural variation and inherent resistance regardless of the lack of co-evolutionary history with emerald ash borer.

DEVELOPMENT AND APPLICATIONS OF GENOMIC RESOURCES FOR TWO NORTH AMERICAN HARDWOOD TAXA

Hardwoods comprise about half of the biomass of forestlands in North America and present many uses including economic, ecological and aesthetic functions. Forest trees rely on the genetic variation within tree populations to overcome the many biotic, abiotic, anthropogenic factors which are further worsened by climate change, that threaten their continued survival and functionality. To harness these inherent genetic variations of tree populations, informed knowledge of the genomic resources and techniques, which are currently lacking or very limited, are imperative for forest managers. The current study therefore aimed to develop genomic microsatellite markers for the leguminous tree species, honey locust, Gleditsia triacanthos L. and test their applicability in assessing genetic variation, estimation of gene flow patterns and identification of a full-sib mapping population. We also aimed to test the usefulness of already developed nuclear and gene-based microsatellite markers in delineation of species and taxonomic relationships between four of the taxonomically difficult Section Lobatae species (Quercus coccinea, Q. ellipsoidalis, Q. rubra and Q. velutina. We recorded 100% amplification of G. triacanthos genomic microsatellites developed using Illumina sequencing techniques in a panel of seven unrelated individuals with 14 of these showing high polymorphism and reproducibility. When characterized in 36 natural population samples, we recorded 20 alleles per locus with no indication for null alleles at 13 of the 14 microsatellites. This is the first report of genomic microsatellites for this species. Honey locust trees occur in fragmented populations of abandoned farmlands and pastures and is described as essentially dioecious. Pollen dispersal if the main source of gene flow within and between populations with the ability to offset the effects of random genetic drift. Factors known to influence gene include fragmentation and degree of isolation, which make the patterns gene flow in fragmented populations of honey locust a necessity for their sustainable management. In this follow-up study, we used a subset of nine of the 14 developed gSSRs to estimate gene flow and identify a full-sib mapping population in two isolated fragments of honey locust. Our analyses indicated that the majority of the seedlings (65-100% - at both strict and relaxed assignment thresholds) were sired by pollen from outside the two fragment populations. Only one selfing event was recorded confirming the functional dioeciousness of honey locust and that the seed parents are almost completely outcrossed. From the Butternut Valley, TN population, pollen donor genotypes were reconstructed and used in paternity assignment analyses to identify a relatively large full-sib family comprised of 149 individuals, proving the usefulness of isolated forest fragments in identification of full-sib families. In the Ames Plantation stand, contemporary pollen dispersal followed a fat-tailed exponential-power distribution, an indication of effective gene flow. Our estimate of δ was 4,282.28 m, suggesting that insect pollinators of honey locust disperse pollen over very long distances. The high proportion of pollen influx into our sampled population implies that our fragment population forms part of a large effectively reproducing population. The high tendency of oak species to hybridize while still maintaining their species identity make it difficult to resolve their taxonomic relationships. Oaks of the section Lobatae are famous in this regard and remain unresolved at both morphological and genetic markers. We applied 28 microsatellite markers including outlier loci with potential roles in reproductive isolation and adaptive divergence between species to natural populations of four known interfertile red oaks, Q. coccinea, Q. ellpsoidalis, Q. rubra and Q. velutina. To better resolve the taxonomic relationships in this difficult clade, we assigned individual samples to species, identified hybrids and introgressive forms and reconstructed phylogenetic relationships among the four species after exclusion of genetically intermediate individuals. Genetic assignment analyses identified four distinct species clusters, with Q. rubra most differentiated from the three other species, but also with a comparatively large number of misclassified individuals (7.14%), hybrids (7.14%) and introgressive forms (18.83%) between Q. ellipsoidalis and Q. velutina. After the exclusion of genetically intermediate individuals, Q. ellipsoidalis grouped as sister species to the largely parapatric Q. coccinea with high bootstrap support (91 %). Genetically intermediate forms in a mixed species stand were located proximate to both potential parental species, which supports recent hybridization of Q. velutina with both Q. ellipsoidalis and Q. rubra. Analyses of genome-wide patterns of interspecific differentiation can provide a better understanding of speciation processes and taxonomic relationships in this taxonomically difficult group of red oak species.