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Introduction
Between the 18th century and the first half of the 20th century, forest ecosystems in eastern North America lost an iconic tree species, the American chestnut, to two introduced pathogens. The lower elevation southern portions of the American chestnut range experienced high mortality from root rot beginning in the 18th century, while the chestnut blight arrived from Asia in the late 1800s and devastated chestnut throughout its range into the 20th century. As a foundational species in the ecosystems it inhabited, the loss of the American chestnut (an estimated 4 billion trees) to chestnut blight and root rot caused a cascade of adverse effects on other species and disrupted livelihoods in communities that depended on chestnut products. During the same time period, white pine blister rust decimated many populations of white pines in the western United States; one of the affected species, whitebark pine, has been proposed for listing under the Endangered Species Act. In the early 21st century, most of the eastern North American species of ash began succumbing to an introduced insect pest, the emerald ash borer. Losses in the form of timber value and removal of urban trees made the borer a costly forest pest (Poland and McCullough, 2006; Kovacs et al., 2010; Hauer and Peterson, 2017). In some of the largest insect outbreaks ever recorded, a few species of native bark beetles have killed billions of spruce, fir, and pine trees since 1990 in the North American West. The most common native tree in Hawai`i, the `ōhi`a, has been severely affected by a fungal disease first detected in 2015. These massive, synchronous die-offs threaten the survival of these tree species on the landscape and negatively affect the ecosystem services provided by the living forests, such as water filtration, soil erosion prevention, carbon sequestration, livelihoods, and other social values.
These are just a few of the North American tree species that have been functionally lost or are in jeopardy of being extirpated from the environment due to insect pest and pathogen outbreaks. Outbreaks of native pests are common disturbances in forests, occurring across ecosystems and landscapes, and they account for a large proportion of tree mortality in North American forests (Krist et al., 2014; Kautz et al., 2017). These outbreaks can be integral to the functioning of forests and often renew ecosystems and contribute to the creation of temporal and spatial heterogeneity, which are critical for the maintenance of high levels of biodiversity (Perry, 1994; Barnes and Wagner, 2004).
However, ecosystems can be seriously disrupted when a nonnative, invasive pathogen or insect is introduced or when native pathogens or insects increase their geographic range or become more virulent because of external drivers such as climate change. Since 1860, North American forests have experienced an increase in the frequency and magnitude of outbreaks (Boyd et al., 2013) due to an increase in global trade and travel (Early et al., 2016) and the acceleration of climate change (Dukes et al., 2009). Of the more than 60 introduced insect species known to be established and to cause damage in continental U.S. forests, only two were detected before 1860 (Aukema et al., 2010). Of the 16 pathogens known to be introduced, all adversely affect North American forests (Aukema et al., 2010).
The impacts of introduced forest pests1 are being aggravated by climate change, which is expanding environmental conditions favorable for insect pests and pathogens, both native and introduced. Warmer winters, fewer days with extremely low temperatures, and longer warm seasons are simultaneously facilitating insect range expansion, local population growth, and reduced time between generations (Bentz et al., 2009, 2010; Sambaraju et al., 2012; Weed et al., 2013). Insect pests are moving higher in latitude and elevation (Berg et al., 2006), and cold areas that previously did not experience the population explosions associated with outbreaks have now become more favorable to such dynamics (Raffa et al., 2013). Similarly, some tree pathogens, such as Phytophthora cinnamomi (which causes root rot and dieback of thousands of species worldwide), are expected to expand their geographic ranges in response to climate change (Bergot et al., 2004).
In many cases, native trees may have little or no natural resistance to withstand insect or pathogen attack and are at risk of being extirpated. The decrease in abundance, or disappearance, of a tree species affected by outbreaks can in turn affect other species and trophic levels (Ford et al., 2012) and potentially result in a cascade of changes with profound impacts on the entire ecosystem (Ellison et al., 2005a,b; Morin and Liebhold, 2015) and the services it provides to humans and other species (Lewis and Lindgren, 2000; Fissore et al., 2012; Liebhold et al., 2017).
Many tools are available to mitigate the effects of insect and disease outbreaks. For introduced species, the most cost-effective measures are those that prevent the arrival of the invasive species in the first place (Lovett et al., 2016). Eradication through chemical traps, pesticide fumigations, and manual removal can eliminate small populations that are accidentally introduced (Sharov et al., 2002). Insecticides and fungicides may be used to some extent in forests even if eradication is not possible. Thinning tree stands or taking actions to promote diversity of tree species and age classes can reduce opportunities for native or introduced pests to spread (Jactel et al., 2012; DeRose and Long, 2014), and biocontrol measures—such as the introduction of predators of a damaging insect or the release of sterile insects to breed with the damaging population—may help regulate the insect pest population at lower levels (Bauer et al., 2014). Another approach is to exploit the natural genetic resistance within the affected tree species by identifying genotypes of the tree resistant to the insect or pathogen, then selectively breeding resistant trees, and ultimately introducing those bred trees into forests to continue the spread of the resistant phenotype in the forest tree population (Woodcock et al., 2017). When little or no resistance is found within a native tree species, breeding a native species with a related resistant species can be used to impart resistance.
Resistant trees can also be created through the use of biotechnology. This process may consist of inserting DNA from another tree species or an entirely unrelated species into the genome of the target tree to produce a genotype that will express resistance to the damaging insect or pathogen. The genome of the tree can also be molecularly manipulated to express resistance without the insertion of DNA from another organism. For example, many classes of chemicals are produced by forest trees that reduce herbivory and pathogen infection. Terpenes have been studied extensively in conifers and phenolics in broad-leaved trees as mechanisms of defense. However, biotechnology has significant
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1 The general term pest includes both insects and pathogens that cause damage to forests.
potential to increase secondary chemical production for plant defense (Peter, 2018). Another emerging tool in the biotechnology toolkit is the synthesis of DNA—that is, DNA created in a laboratory—that can then be inserted into the genome of the tree.
As of 2018, although research on incorporating resistance to insects or pathogens via biotechnology was being conducted in some forest tree species such as the American chestnut and poplar hybrids, no such resistant genotypes—created with the intent to spread resistance into a forest population—had been planted in a North American forest. Given the increase in the frequency and magnitude of pest outbreaks, and the threats they pose to the survival of many North American forest species, a number of federal agencies and a forest organization wanted to explore whether biotechnology held potential for addressing these threats to forest health. The U.S. Department of Agriculture’s Agricultural Research Service, Animal and Plant Health Inspection Service, Forest Service, and National Institute of Food and Agriculture as well as the U.S. Endowment for Forestry and Communities and the U.S. Environmental Protection Agency asked the National Academies of Sciences, Engineering, and Medicine (hereafter referred to as the National Academies) to convene a committee of experts to investigate that question.
THE COMMITTEE AND ITS CHARGE
The committee’s charge was to examine whether biotechnology has the potential to mitigate threats to forest health, particularly threats posed by insects and diseases. Its task included identifying the ecological, economic, and social implications of using biotechnology in forests and developing a research agenda to address areas where knowledge about such use might be lacking. The committee was instructed to use case studies to explore whether biotechnology could successfully protect forest tree species from insect pests, pathogens, or both. It was not asked to examine the potential for biotechnology to reduce threats to forest health by altering the pests affecting North American tree species. The full statement of task is in Box 1-1.
The president of the National Academy of Sciences appointed a committee with the diverse expertise and experience needed to address this statement of task. The committee contained experts in forest population genetics, tree gene flow and reproductive biology, quantitative genetics, and genomics. The disciplines of forest ecology and entomology were also represented as were the fields of sociology, ethics, economics, and U.S. environmental and regulatory law. Many committee members had extensive knowledge about selective breeding and genetic engineering of forest trees. The committee included researchers who studied conifer and deciduous trees in eastern, midwestern, intermountain, western, and Hawaiian forest ecosystems. As with all National Academies committees, members were appointed for their individual expertise, not their affiliation to any institution, and they volunteered their time to serve on this committee. The biography of each committee member can be found in Appendix A.
THE COMMITTEE’S PROCESS
The committee conducted its work between December 2017 and December 2018. Between December and April, it heard from 43 invited speakers over the course of 13 information-gathering sessions: 3 held in person in Washington, DC, and 10 conducted via webinar. All in-person meetings and webinars were open to the public, streamed over the Internet, and recorded and posted to the study’s website.2 Agendas for the meetings, topics for the webinars, and names of the invited speakers can be found in Appendix B.
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2 Recordings of the presentations made to the committee at its meetings and webinars can be found at http://nas.edu/forestbiotech.
The committee also reviewed the scientific literature and welcomed comments submitted by members of the public. Opportunities to make public statements to the committee were available at each in-person meeting, and the committee accepted written statements throughout the study process.3 Committee members read all submitted written comments, which were subsequently archived in the study’s public access file.4
Based on its expertise, experience, and the information it gathered through presentations, scientific literature, and written comments, the committee wrote a draft report in response to the statement of task. That draft was then reviewed by a number of peers with expertise complementary to that of the committee members in a process overseen by the National Academies’ Report Review Committee. The reviewers were anonymous to the committee during the review process, and their comments remain anonymous after the report has been published (see Acknowledgments). The Report Review Committee approved the report for publication after it determined that the committee had appropriately responded to the reviewers’ comments.
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3 For more information about the National Academies study process, see http://www.nationalacademies.org/studyprocess.
4 The public access file of any National Academies study can be obtained by contacting the Public Access Records Office at paro@nas.edu.
ORGANIZATION OF THE REPORT
The next chapter discusses the concept of forest health, including how the committee defined the term. It also reviews the threats to forest health from insect pests and pathogens, reviews the ecosystem services provided by forests, and introduces the case study species considered by the committee: American chestnut (Castanea dentata), whitebark pine (Pinus albicaulis), ash (Fraxinus spp.), and poplar (Populus spp.).
Chapter 3 outlines the options available for mitigating threats to forest health, including the current state of the science regarding the potential for using biotechnology in trees to improve forest health. The committee agreed that biotechnology included the following approaches: transgenesis, cisgenesis, RNA interference, genome editing, and the insertion of synthetic DNA. For simplicity’s sake, trees modified by one or more of these approaches are generally referred to in this report as biotech trees.
Chapter 4 reviews the ecological, economic, social, and ethical considerations related to the use of biotechnology in trees. It includes a synopsis of the potential ecological and economic impacts of deploying trees protected from insect pests and pathogens using biotechnology and a summary of what existing research reveals about public views on the use of biotechnology to improve forest health.
Chapter 5 emphasizes the importance of evaluating the risk of loss of ecosystem services over part, or all, of a species’ range against the potential to recover ecosystem services across that range with and without a biotechnological intervention and identifies information needs for a framework that would assess the impacts of using biotechnology to address forest health. It also explores how adaptive management could be used to test, assess, and improve the use of biotechnology as a tool to mitigate forest health threats.
Chapter 6 summarizes how forest health is considered in the U.S. regulatory systems for biotechnology and other forest health interventions. Chapter 7 describes research and investment needs to fill knowledge gaps about developing and using biotechnology as a tool to mitigate threats to forest health from insect pests and pathogens.
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