Recovery potential for a green ash floodplain forest using various emerald ash borer management strategies in a population viability analysis

https://doi.org/10.1016/j.foreco.2020.117925Get rights and content

Highlights

  • Management scenarios were simulated with stage based ash models.

  • Population persistence was influenced by adult and new seedling survival.

  • If aftermath conditions continue, the ash population is likely to persist.

  • Ash extinction was 33% lower when future predicted EAB impact was reduced.

  • Modeled scenarios suggest effective ways to conserve ash populations.

Abstract

The invasive emerald ash borer (Agrilus planipennis Fairmaire, EAB) has destroyed ash tree (Fraxinus spp.) populations across the US, but remnant populations including many small trees and, more rarely, larger trees remain after EAB had its first major impact across the landscape. The future survival of these remnant trees is critical to the viability of the ash species. Several different management options, including biocontrol, EAB-tolerant or resistant ash trees, and silvicultural strategies exist or are under development. Here we model changes that could occur in a preserve’s remnant population of green ash (Fraxinus pennsylvanica Marsh.) after EAB peak mortality to assess management strategies. We used population viability analysis (PVA) and created a stage based model with baseline conditions and a model with recurrent catastrophes, where a catastrophe was defined as a year with reduced ash survival from an EAB outbreak. The catastrophes model had an increasing probability of a catastrophe occurring over ten years and included a gradual increase in ash survival (decline in EAB impacts) over the 9 years following a catastrophic event. We explored management scenarios for the catastrophes model including, 1) the reduction of future EAB induced mortality events to mimic possible effects of biological control or other environmental constraints; 2) addition of trees with increased survival to mimic restoration by planting ash trees with resistance to EAB, which are currently under development, or mimic clusters of trees with natural resistance to EAB created by natural selection. We also performed a sensitivity analysis to assess which size class impacted the population persistence the most over time and found that new seedlings were the most influential. There was no risk of extinction under the baseline model. The reduced catastrophe scenario was an improvement from the catastrophes model, reducing probability of extinction by 33%. Adding healthy ash improved population abundances over time and reduced the probability of extinction when there were repeated plantings. These scenarios relied on assumptions about how the population would react to management treatments, based on the scientific literature and cautious estimates. This approach provides a starting point for experiments testing individual management treatments to generate testable hypotheses, and the model may be readily updated with new data as it becomes available. Our PVA has revealed potential outcomes of alternative management practices and can increase our understanding of natural ash populations remaining after EAB introduction.

Introduction

When new pests, pathogens, or environmental conditions threaten the future of a species, models can be useful tools to predict and understand the impacts and to plan for conservation management strategies. Populations of North American ash (Fraxinus spp. (Oleaceae)) trees are threatened by an invasive insect, the emerald ash borer (Agrilus planipennis Fairmaire, EAB), which has caused escalating depletion of ash tree populations. EAB was accidentally imported from Asia in the mid-1990s and was first discovered in the Detroit, MI area in 2002 (Haack et al., 2002). The ash species threatened by EAB are important ecologically as a component of riparian forest ecosystems (Nisbet et al., 2015), linked to reduced crime and increased human health as urban trees (Kondo et al., 2017, Donovan et al., 2013), and are economically valuable timber (Gould et al., 2012).

The EAB life cycle is carried out on ash trees and generally results in up to 99% mortality of large host trees within a population (Knight et al., 2013, Cappaert et al., 2005). However, trees smaller than the preferred larger size classes (Klooster et al., 2014), sprouts of dead trees (Kashian, 2016), and rare surviving trees (Knight et al., 2012b) may remain after the majority of the larger reproductive mature ash trees are killed. In areas of Northwest Ohio where mature ash trees have died off, our continued data collection reveals that EAB are still present and infesting smaller trees, though in fewer numbers (Kappler, 2018). The future dynamics of EAB and remnant ash populations are unknown.

Management options for conservation of ash species in EAB infested areas include insecticide injections, parasitic wasp biocontrols, and development of EAB-resistant trees. While insecticide usage to protect individual ash trees is very effective, it is mostly used for high-value urban trees rather than forest trees due to the expense of continued treatment over time (Smitley et al., 2015). In contrast, wasp parasitoids are more readily used in natural settings. Wasp parasitoids (herein called parasitoids) directly attack and kill EAB eggs or larvae. They are species released as classical biological controls (biocontrols), including non-native Oobius agrili Zhang and Huang, Spathius agrili Yang, Tetrasichus planipennisi Yang (Gould et al., 2012), and Spathius galinae Belokoblyskij and Strazenac (Watt et al., 2016). Parasitism rates vary based on numerous factors and have been shown to increase ash sapling survival in Michigan (Duan et al., 2018, Kashian et al., 2018), although the long-term survival of these trees as they mature is unknown. Biocontrol parasitoid releases may be used alone or in concert with other management options.

Reintroduction of EAB-resistant ash trees may be a future option for ash-dominated forests where most of the ash have died. Research has demonstrated that some identified individual native ash trees can resist EAB significantly better than susceptible controls and efforts to identify and use such trees in a resistance breeding program to improve EAB resistance are ongoing (Koch et al., 2015). Rare surviving ash trees of both F. americana L. and F. pennsylvanica are currently being used in this program. In this resistance breeding program testing of F1 progeny trees show some trees are able to survive infestation and kill most of the EAB larvae that tried to feed on them (J. Koch, pers. comm.). Several examples of successful breeding programs to develop forest trees with resistance to invasive insects and diseases have been reviewed recently by Sniezko and Koch (2017). Despite these successes, little is known about potential population changes resulting from tree augmentation plantings of resistant trees, due to the long-term nature of experimental exploration in the field. However, clusters of trees with natural resistance to EAB may also be created by natural selection. Population viability analysis models can provide more immediate estimates related to these possibilities.

Population viability analysis (PVA) is an effective tool to estimate the population viability of a species under various environmental conditions and quickly identify factors that influence a population’s viability (Akçakaya and Sjögren-Gulve, 2000, Morris and Doak, 2002, Caswell, 2001). Trees affected by pests and diseases, like whitebark pine (Pinus albicaulis Engelmann), have been evaluated with population models to help reveal that the native pests impacted the pine trees more than the invasive disease (Jules et al., 2016). Management actions are best conducted under circumstances where the affected species and its environment are heavily studied, but this is not always feasible. The potential changes from management can be added into models and evaluated for overall effectiveness in increasing population viability. For example, an individual based model was developed to examine how much harvest was detrimental to a big-leaf mahogany (Swietenia macrophylla King) population (Grogan et al., 2014). Models can also look at combinations of management strategies as well as individual ones to increase predictive power. For example, the endangered English yew tree (Taxus baccata L.), had management alternatives modeled to create a population viability risk management assessment to identify which management combinations were most beneficial (Dhar et al., 2008). EAB management options are continuously improving and will likely influence ash survival once implemented by land management authorities. Most augmentation predictions for forests are modelled in forest vegetation simulator (FVS), where forest stand growth and development are applied to ecosystem management (Dixon, 2002). The FVS program has successfully predicted short term changes (2 years) of reduced stem density and basal area for ash with EAB infestation (Levin-Nielsen and Rieske, 2015). Population viability analysis allows predictions to be projected for a longer period of time in a dynamic environment. The PVA provides a framework for evaluating potential outcomes for ash populations under specific conditions, while incorporating natural levels of environmental and demographic variation. By creating models for species in danger of decline we can better assess future scenarios, develop testable hypotheses, and potentially understand the underlying mechanisms driving changes in the populations.

The aim of this study was to compare, using PVA, the effects of simulated management interventions on the population persistence of a remnant green ash population after its initial decline from EAB. We modeled an extensively studied green ash population in Northwest Ohio that experienced >97% mortality of larger trees from EAB by 2009 and in which surviving ash trees have been monitored and studied (Knight et al., 2012b, Kappler et al., 2018, Kappler et al., 2019). Green ash is a deciduous tree with a broad range in Canada and the eastern United States which has adapted to live in multiple habitats, as it is able to tolerate a variety of environmental stressors, e.g., high salinity, flooding, drought, and high alkalinity (Kennedy, 1990, MacFarlane and Meyer, 2005, Stewart and Krajicek, 1973). We created two models, one without further EAB impacts (baseline model) and one with EAB as a potentially reoccurring catastrophe (catastrophes model). We added management scenarios to the catastrophes model using a literature search for ash species to create estimates for parameters. Management strategies that we focused on were (1) reduced catastrophe, to simulate the release of biocontrols or other environmental constraints which improved ash survival by reducing catastrophe impacts; and (2) additional healthy ash added, simulating restoration where additional EAB-resistant ash individuals are planted and produce resistant offspring. We expected that the persistence of the green ash population in this natural floodplain would increase with increased survival and reproduction of mature ash trees. Using population models, we can evaluate the alternatives for management of this highly impacted population before their implementation.

Section snippets

Survey site

Our focal population was in Northwest Ohio, in the floodplain forest of Swan creek, located in the Oak Openings Preserve Metropark (Swanton, Ohio, USA). This area had a high infestation of EAB from 2004 to 2010, and almost all large ash trees were dead by 2009 (Knight et al., 2010). It holds a remnant population of green ash trees where EAB are still present in low numbers. A few larger trees in this population are lingering ash trees, which are either the last to be infested or have rare

Results

Our results are from one of the larger remaining ash populations we have found in Ohio and the probability of extinction was of particular interest. We found significant differences (p < 0.001) in the interval extinction risk of this remnant population under multiple model scenarios. Final average total abundances varied, but the ash populations in all models and scenarios were predominantly smaller individuals at the end of the simulations (as is typical of tree populations). The model

Discussion

Our baseline model results showed that if vital rates for the aftermath ash forest population remained the same without another EAB outbreak or other detrimental events or factors, the ash population would persist. This result occurred because at our site the mortality rates in surviving trees were found to be lower than the mortality rates at the peak of EAB infestation. The largest ash trees in the baseline model had fewer individuals to start with, but with an average survival of 79% for

CRediT authorship contribution statement

R.H. Kappler: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing - original draft, Writing - review & editing. K.S. Knight: Data curation, Funding acquisition, Project administration, Resources, Supervision, Writing - review & editing. R. Bienemann: Data curation, Investigation, Writing - review & editing. K.V. Root: Conceptualization, Funding acquisition, Methodology, Project administration, Software, Supervision, Validation, Writing - review & editing.

Acknowledgments

We appreciate the permission to study at the Toledo Metroparks. This work would not be possible without the support of Bowling Green State University [grant 10010370 & 10009502] and the US Forest Service [Forest Health Protection STDP grant NA-2014-04 & Interagency grant 18-IA-11242316-105]. We would like to thank the many individuals who assisted with EAB and ash tree data collection over the years at Oak Openings Preserve.

References (59)

  • T.P. Rooney et al.

    Direct and indirect effects of white-tailed deer in forest ecosystems

    For. Eco. Manage.

    (2003)
  • C.R. Rossell et al.

    Effects of white-tailed deer on vegetation structure and woody seedling composition in three forest types on the Piedmont Plateau

    For. Eco. Manage.

    (2005)
  • T.J. Watt et al.

    Reproductive and developmental biology of the emerald ash borer parasitoid Spathius galinae (Hymenoptera: Braconidae) as affected by temperature

    Biol. Control

    (2016)
  • H.R. Akçakaya et al.

    Population viability analyses in conservation planning: an overview

    Ecol. Bull.

    (2000)
  • R.E.J. Boerner et al.

    Ten years of tree seedling establishment and mortality in an Ohio deciduous forest complex

    Bull. Torrey Bot. Club

    (1996)
  • M.S. Boyce

    Population viability analysis

    Annu. Rev. Ecol. Syst.

    (1992)
  • D. Cappaert et al.

    Emerald ash borer in North America: a research and regulatory challenge

    Am. Entomol.

    (2005)
  • H. Caswell

    Matrix population models: construction, analysis, and interpretation

    (2001)
  • K.C. Costilow et al.

    Disturbance severity and canopy position control the radial growth response of maple trees (Acer spp.) in forests of northwest Ohio impacted by emerald ash borer (Agrilus planipennis)

    Ann. Forest Sci.

    (2017)
  • Dixon, G.E., 2002. Essential FVS: a user ’s guide to the forest vegetation simulator. Fort Collins, CO.: U.S....
  • J.J. Duan et al.

    Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States

    Biocontrol

    (2012)
  • J.J. Duan et al.

    Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: Implications for biological control

    J. Appl. Ecol.

    (2015)
  • J.J. Duan et al.

    Progress and challenges of protecting North American ash trees from the emerald ash borer using biological control

    Forests

    (2018)
  • C.F. Fitzgerald et al.

    Characteristics and growth of natural green ash stands

    J. Forestry

    (1975)
  • C.E. Flower et al.

    Optimizing conservation strategies for a threatened tree species: in situ conservation of white ash (Fraxinus americana L.) genetic diversity through Insecticide treatment

    Forests

    (2018)
  • E.S. Gardiner et al.

    Root-collar diameter and third-year survival of three bottomland hardwoods planted on former agricultural fields in the lower Mississippi Alluvial Valley

  • H.C.J. Godfray et al.

    Predictive modelling in biological control: the mango mealy bug (Rastrococcus invadens) and its parasitoids

    J. Appl. Ecol.

    (1991)
  • Gould, J., Bauer, L., Lelito, J., Duan, J., 2012. Emerald ash borer, Agrilus planipennis (Fairmaire), biological...
  • J. Grogan et al.

    Big-leaf mahogany Swietenia macrophylla population dynamics and implications for sustainable management

    J. Appl. Ecol.

    (2014)
  • Cited by (0)

    View full text