Center for Invasive Species Prevention

Climate Change & Habitat Disruptions: Connected by Carbon Dioxide

Wildfire: one of the widely recognized results of climate change (The Pioneer Fire located in the Boise National Forest near Idaho City, ID began on Jul. 18, 2016 and the cause is under investigation. The Pioneer Fire has consumed 96,469 acres. U.S. Forest Service photo. Original public domain image from Flickr)

A guest blog by Michael Aucott. Mike is a retired research scientist of the NJ Department of Environmental Protection. He has also taught chemistry at the College of New Jersey. He is currently a member of the NJDEP Science Advisory Board Standing Committee on Climate and Atmospheric Sciences, and on the board of directors of the PA/NJ Chapter of the American Chestnut Foundation. If you wish to contact Mike, use the contact button on this website. You MUST include your email address; it is not recorded automatically.

Two major perturbations affect Earth and its living systems, climate change and habitat disruptions. Emerging data show that these are more closely related than previously realized; they are connected by carbon dioxide, CO₂.

Climate change basics: the physics

Climate change concerns have focused on the alteration of weather and climate due to the increase in atmospheric concentrations of greenhouse gases, primarily carbon dioxide, CO₂. The impact of CO₂ on climate has been understood for at least 120 years. In 1896 the Nobel-Prize-winning Swedish chemist Svante Arhennius published calculations demonstrating that human emission of CO₂, when combined with the positive feedback effects of water vapor, would warm the Earth (Arhennius, 1896). His equation, ΔF = α ln(C/C₀), relates the change in climate “forcing” (the degree to which temperature change is forced) to the ratio of the concentration of CO₂ currently in the atmosphere (C) to a previous concentration (C₀). This equation is still in use today. Arhennius estimated that a doubling of CO₂ would warm the Earth by about 4 degrees C. This estimate is not far off from current estimates based on much more elaborate calculations.

This warming impact is caused by the physics of CO₂, water vapor, and other “greenhouse” gases. Infrared radiation causes the CO₂, water, and other greenhouse gas molecules to vibrate, leading to the absorption of the energy carried by that radiation. Much of the solar energy coming from the sun is not in the infrared frequency range, so it passes through the atmosphere without being absorbed. However, when this energy is absorbed by the surfaces of the Earth and its biota, and is re-radiated as infrared radiation, it is then absorbed by greenhouse gases, warming the planet.

The amount of water vapor in the atmosphere is directly related to the atmosphere’s temperature: warm air holds more water vapor. Human activity hasn’t directly changed the concentration of water vapor in the atmosphere significantly. But by burning fossil fuels, humans have dramatically increased the atmospheric concentration of CO₂ and in so doing, also indirectly increased the concentration of water vapor. Just as Arhennius predicted over 120 years ago, this increase in CO₂ is warming the Earth.

Ramifications of this warming include increased heat episodes, the intensification of the hydrological cycle (greater frequency of both heavy precipitation events and of droughts), sea level rise due to the melting of land-based glaciers and the thermal expansion of ocean water, and, almost certainly, intensification of storms and an increase in extreme weather. These climate-warming- based perturbations have the potential to influence the functioning of Earth’s biota in many deleterious ways, and clearly can be associated with the many facets of habitat disruption.

Climate change amplifications: the chemistry

But there’s another aspect of CO₂ that may be more important insofar as habitat disruption is concerned and that has been largely ignored: chemistry. CO₂ is a trace gas as far as we humans and other animals are concerned, unnoticed by our bodies in normal life. But to plants it is a vital food. It is taken up by plants as an essential input to photosynthesis. In this chemical reaction, using the energy of sunlight, plants combine CO₂ and water vapor to make oxygen and carbohydrates, represented with a generic formula of CH₂O, according to the equation CO₂ + H₂O → CH₂O + O₂. Without this reaction, life as we know it would not exist.

The atmospheric concentration of CO₂ has varied over time; some 50 million years ago it was considerably higher than today. However, for at least the last three million years, the concentration of CO₂ has been in the range of 280 ppm. Over these millions of years biota have adapted to this concentration. But within the last 300 years, one ten thousandth of this period – a blink of an eye in the geological or evolutionary time scale – the concentration of CO₂ has shot up to 420 ppm, a 50% increase, due to humanity’s burning of fossil fuels and forests.

Imagine what might happen to a person who had been on a tight dietary budget for most of his or her life but suddenly got access to 50% more carbohydrates, but no more protein or minerals? We could expect major changes in the metabolism of that person. This dramatic change is what has, in effect, happened to the whole of life on Earth. Our planet’s primary biota, plants, now suddenly have the opportunity to gorge on CO₂. But their access to other important substances such as nitrogen has not changed. Evidence is accumulating that CO₂ at its elevated level of 420 ppm is not, as has been proclaimed by some, a healthy influence but is instead throwing Earth’s ecosystem into disarray.

Much of the recent experimental evidence on the impacts of enriched atmospheric CO₂has been assembled by Lewis Ziska and presented in his new book, Greenhouse Planet: How Rising CO₂ Changes Plants and Life as We Know It (Ziska, 2022; see full citation at the end of the blog). The findings documented in this book reveal a variety of impacts of elevated CO₂. These impacts include stimulation of growth of invasive plants, decreases in the nutrient content of major crops, and changes in plants’ production of insecticidal, allergenic, and other compounds. The changing chemistry of plants may be contributing to a major die-off of insects and insect-eating animals including birds. Below are some details.

Habitat Disruptions: Stimulation of Invasive Plants

The generally accepted explanation for why some plants are invasive is that they have been introduced to new regions where their historic predators and parasites aren’t present. Without these drags on their growth, they have flourished. That some alien plants are not browsed by white-tailed deer contributes significantly to their invasiveness in Eastern North America. Other factors are clearly involved as well, including changes in the temperature regime and the availability of water and other resources such as nitrogen.

But elevated CO₂ is also a factor. In recent years, techniques for measuring responses of organisms in situ under elevated CO₂ conditions have been developed, making possible investigations of the impacts of CO₂ concentrations that could exist in the future under otherwise relatively realistic conditions. What the actual atmospheric CO₂ concentration will be in 2050 or 2100 is difficult to predict; it depends on what humanity does to control emissions. Various scenarios suggest that levels could exceed 500 ppm by 2050 and might exceed 1000 ppm by 2100 (Tollefson, 2020).

One study found that the invasive weed Canada thistle, Cirsium arvense, responds more strongly to elevated CO₂ than soybean, a crop that it often plagues. In a high CO₂ environment, this weed’s root system grows strongly enough to make it significantly more resistant to herbicides (Ziska, et al., 2004) (Ziska, 2010). The highly invasive and dangerously flammable cheatgrass (Bromus tectorum), nicknamed “grassoline” by the U.S. Forest Service because of its propensity to intensify wildfires, also responds strongly to elevated CO₂ (Ziska, et al., 2005). Also found to be boosted by enriched CO₂ is yellow star-thistle (Centaurea solstitialis), considered one of California’s worst weeds. In one study (Dukes, et al., 2011) this plant grew 600% larger in elevated CO₂ relative to ambient, while native plants responded much less strongly or not at all. Japanese honeysuckle, Lonicera japonica, which plagues many areas in the U.S., was found to increase in biomass by 135% at a CO₂ concentration of 675 ppm while a similar native plant, coral honeysuckle (Lonicera sempervirens) increased by only 40% (Sasek & Strain, 1991). In a field study also involving Japanese honeysuckle (Belote, et al., 2004), researchers found that its above ground net production (ANPP) approximately tripled under enriched CO₂ while other plants in the trial showed showed lesser increases or actual decreases.

Other plants have been found to be selectively encouraged by enriched CO₂ including cherry laurel (Prunus laurocerasus), invasive in the Pacific Northwest U.S. and the U.K., (Hattenschwiler & Korner, 2002); dalmation toadflax (Linaria dalmatica), invasive in much of North America (Blumenthal, et al., 2013); honey mesquite (Prosopis glandulosa) , invasive in Australia and parts of Africa (Polley, et al., 1996); and kudzu (Pueraria lobata), which afflicts the Southeast U.S. (Sasek & Strain, 1988). Three plants invasive in China or Southeast Asia, American rope (Mikania micrantha), Creeping oxeye (Wedelia trilobata), and a morning glory species (Ipomoea cairica), were found to produce 70.3% greater biomass when grown at a CO₂ concentration of 700 ppm while three corresponding indigenous plants Paederia scandens, Wedelia chinensis and Ipomoea pescaprae, produced only 30.5% more biomass (Song, et al., 2009).

yellow star thistle; photo by Eugene Zelenko

The list goes on of studies showing increased growth of some plants under enriched CO₂ conditions. As more in situ investigations are undertaken, it seems likely it will become clearer that today’s enriched level of CO₂ is helping some plants to become invasive.

Complexities and contradictory findings exist however. Not all plants are stimulated by enriched CO₂. An important difference in the response to higher levels of CO₂ is whether a plant has a C₃or a C₄ photosynthetic mechanism. C₄plants contain a biochemical pump that concentrates CO₂, making them more adapted to low CO₂ conditions (Hager, et al., 2016). At current levels of CO₂, such plants’ need for CO₂ is easily met. C₃ plants do not have this CO₂ concentrating ability, and so higher levels boost their growth. In a broad meta-analysis of literature, the average response to elevated CO₂ of 365 C₃ plant species and 37 C₄ plant species was noted; the response was significantly increased in C₃ species but was unchanged in C₄ species (Robinson, et al. 2012). One striking example of such a difference was observed in the field study noted above (Belote, et al., 2004), wherein researchers found that Japanese honeysuckle (a C₃ plant) was significantly encouraged by elevated CO₂relative to other plants at the same locale. The same study found that another aggressive invader, Japanese stiltgrass (Microstegium vimineum), a C₄ plant, was unaffected or even slightly inhibited relative to competing plants’ growth by elevated CO₂.

Habitat Disruptions: Changing of Plants’ C/N Ratio and Nutrient Content

One finding is widespread; most plants studied under enriched CO₂ regimes show an increase in biomass and evince a higher ratio of carbon to nitrogen (C/N ratio) in their tissues and an overall decline in nitrogen concentrations than when grown under ambient conditions. Since nitrogen is a key component of protein, this change can be expected to lead to lowered protein content of critical food crops. Some impacts of this change are already well underway because of today’s elevated CO₂ concentration. Changes since 1850 in the C/N ratio and in the estimated protein content of an important plant product, pollen, were discovered in a striking study by Lewis Ziska and colleagues (Ziska, et al., 2016). Using archived museum samples, these researchers determined the nitrogen content of pollen of Solidago canadensis (Canada goldenrod) going back to the 1850s. They estimated that the protein content of goldenrod pollen, a vital nutrient for North American bees, has declined in inverse proportion to the rise in atmospheric CO₂, dropping from a concentration of approximately 18% in the mid-1800s to approximately 12% today. They pointed out that it is possible that bees are now unable to provide sufficient protein and other nutrients to larvae, and that one of the main reasons for bee declines is malnutrition caused by enriched atmospheric CO₂. Other studies also indicate that elevated CO₂ could cause lower nitrogen concentrations in plants and lead to less proteinaceous plant parts, including pollen, being available to plant-feeding insects (Hall, et al., 2005; Knepp, et al., 2007).

The changing C/N ratio is almost certainly already affecting the human food supply. As documented in an extensive review of published findings (Soares, et al., 2019), elevated CO₂ has a considerable impact on the accumulation of minerals and protein in plants, with many plant species showing declines in both quality and quantity of key nutrients. These changes have worrisome implications for human nutrition and may already be responsible for increasing incidences of dietary deficiency in some areas. Lewis Ziska discusses the likely impact of rising CO₂ on the future human food supply in his recent post. A number of studies showing declines in protein and also other nutrients such as zinc in food crops important to humanity are also described in Ziska’s new book, Greenhouse Planet, noted above.

Habitat Disruptions: Other Changes in Plant Chemistry

Other changes in plants besides nutritional content may be driven by enriched CO₂. Plants produce a variety of secondary metabolites. Most plants use the C₃ mechanism; with 50% more available of a key input, some changes in these plants’ production of such chemicals can be expected. Some changes have been observed. Mohan et al. (2006) report that enriched CO₂ in an intact forest system increased water use efficiency, growth, and population biomass of poison ivy (Toxicodendron radicans) and that high-CO₂ plants also produced a more toxic form of the allergenic compound urushiol.

*Quercus chapmanii*; photo by Mary Keim at Seminole State Forest, Florida

Many of the phytochemicals plants produce function as defenses against insect predation, and changes in such production have been found to impact herbivore feeding. For example, Landosky and Karowe (2014) suggest that specialist herbivores may have to contend with more effective chemical defenses by plants under elevated CO₂. Hall, et al. (2005), in a study involving several oak and one legume species in a scrub oak ecosystem in Florida (see photo above), found that 700 ppm CO₂ levels led to decreased damage to plants by four of six insect groups investigated. They did not see increases in plants’ production of carbon-based secondary metabolites, including total phenolic compounds, condensed tannins, hydrolyzable tannins, cellulose, hemicellulose, and lignin however. They concluded that the primary driver of decreased insect predation under elevated CO₂ was lower overall plant nitrogen levels. They stated that the decline of nitrogen levels in foliage under elevated CO₂ indicated lower foliar quality and hypothesized that the reductions in insect feeding stemmed from the combined effects of nutrient limitation and increases in parasitism and predation on the nutrient-constrained insects. They further stated that although insects try to compensate for lower nutrient content of leaves by eating more, they did not see an increased portion of damaged leaves in their study. These researchers did not report measurements of terpenoid compounds however, which are reported to represent the largest class of secondary metabolites (Wikipedia, 2022). In another study (Hall, et al., 2005a) found that concentrations of condensed tannins were higher in oak leaf litter under elevated CO₂, which suggests that enhanced production of insecticidal compounds or other changes to plant tissues could affect not only insects that consume living plant tissue, but also detritivores.

Robinson et al. (2012) also investigated plants’ production of secondary metabolites in their literature review. Looking at all plant groups, they found that under elevated CO₂ the production of nitrogen-based secondary metabolites (e.g., alkaloids, cyanogenic glycosides, and glucosinolates) decreased by 16% while the carbon-based secondary metabolites total phenolics, condensed tannins, and flavonoids increased by 19%, 22%, and 27% respectively. Another carbon-based metabolite, terpenoids, declined by 13%. They further divided plants into grasses, shrubs, herbs/forbs, and trees and found differing responses to elevated CO₂. Trees, for example, showed increased production of total glycosides and total phenolics, little change in production of total flavonoids, and a decline in the production of total terpenes. Like Hall et al., (2005), Robinson et al. found a strong and significant decrease in nitrogen concentrations under elevated CO₂ for C₃ plants. A decrease did not show up for C₄ plants.

In addition to chemical defenses, plants have physical characteristics such as surface waxes, trichomes, secretory canals, and tissue toughness-enhancing substances such as lignin. All of these features can reduce the edibility of plants for arthropod herbivores. Robinson et al. (2012) found consistent responses to these characteristics under elevated CO₂; leaf toughness and specific leaf weight increased by 11% and 18%, respectively, while specific leaf area did not show a significant change. They concluded that there is an increase in general “toughness” of leaves under elevated CO₂. As did Hall et al., (2005), Robinson et al. concluded that elevated CO₂ will induce changes in plant chemistry, physiology, and morphology that are likely to impact the nutritional quality of host plants for insect herbivores.

Habitat Disruptions: Changes in Plant Chemistry and Insect Decline

Numerous studies have documented a recent and dramatic decline in insect populations and discussed the probable cascading impacts of such declines through the food chain, affecting spiders, lizards, birds, and other organisms (Samways, et al., 2020; Cardoso, et al., 2020; Sánchez-Bayoa & Wyckhuys, 2019; Tallamy & Shriver, 2021). It has been argued that the main drivers of insect species declines are habitat loss and conversion to intensive agriculture and urbanization; pollution, mainly by synthetic pesticides and fertilizers; biological factors, including pathogens and introduced species; and climate change.

But a puzzling aspect is that some insect declines have been observed in nature preserves (Vogel, 2017) that presumably are not greatly affected by most of the above drivers. One example is a study spanning 27 years that found a 76% decline in flying insect biomass at several of Germany’s protected areas subject to rather low levels of human disturbance (Hallmann et al., 2017). Another study in rainforests of Puerto Rico, apparently not subject to influences such as light pollution, habitat loss, pesticides, or agriculture, reported biomass losses between 98% and 78% for ground-foraging and canopy-dwelling arthropods over a 36-year period, (Lister and Garcia, 2018). This leaves climate change as the likely culprit. But although the varied impacts of climate change, including heat episodes, drought, and other episodes of extreme weather could impact insect populations in remote as well as populated areas, the trends observed appear to far exceed the magnitude of such climate-related disturbances over the last several decades.

tent caterpillars; Shiela Brown, Public Domain Pics

Another puzzling aspect is that not all insect orders or feeding guilds seem to be equally affected. Sanchez-Bayoa & Wychuys (2019) whose article reports on a review of 73 historical reports, state that Lepidoptera, Hymenoptera and dung beetles (Coleoptera) appear to be the taxa most affected in terrestrial environments. Robinson et al. (2012) found that phloem feeders such as Homoptera respond positively to elevated CO₂ while foliage feeders/Lepidoptera respond negatively. Lepidoptera were among the most impacted; relative growth rate, fecundity, and abundance all declined under high CO₂ conditions, while relative consumption rate, total consumption, and development time all increased.

Most Lepidoptera are herbivorous, feeding in their larval stage, caterpillars, on plants. Caterpillars are key components of the terrestrial ecology; in most forests of the world, caterpillars consume more living leaves than all other animals combined (Janzen, 1988). Insect herbivores such as caterpillars are near the hub of most terrestrial food webs, comprising essential food for insect predators and parasitoids, spiders, amphibians, lizards, rodents, bats, birds, and even higher predators such as foxes and bears (Burghardt et al., 2010). At least 310 North American bird species are known to feed extensively on caterpillars, and the majority of terrestrial birds rely on insects during reproduction and other nutrient-limited periods in the annual cycle (Narango, Tallamy & Marra, 2018). Caterpillars and moths are the largest component of nestling diets in hundreds of species of migrant bird species (Tallamy & Shriver, 2021); they are among the “little things that run the world” (Wilson, 1987).

Carolina chickadee; one of the birds Dr. Tallamy focuses on because it feeds its young on caterpillars; photo by Dan Pancamo; through Wikimedia

Habitat Disruptions and Climate Change: Connected by CO₂

The apparently heightened rate of decline of insect herbivores such as caterpillars compared to some other insects, and the findings that many declines have been observed in areas relatively unimpacted by direct human influences such as light pollution, pesticides, and land-use change, point to the likelihood of a broad, perhaps ubiquitous, cause. Climate change is such a broad cause. Even broader and more ubiquitous is the main driver of climate change, CO₂. Every plant in the world is constantly bathed in an enriched concentration of this gas. A conclusion seems likely: CO₂ is not only causing global warming and climate change but is also affecting life on this planet in ways that, while still poorly understood, are already reducing the nutritive value of food crops, may be a significant cause of the spread of invasive plants, and may be the main driver of insect declines and the cascading impacts of such declines on insect-eating animals such as birds.

What to do?

To mitigate climate change and, as argued here, to mitigate habitat disruption, the steady rise in the atmosphere’s burden of CO₂ must be halted, and then steps must be taken to lower the current concentration to a healthier level. These are not hopeless tasks. Although what has been a relentless rise in CO₂ emissions at the global level continues, increases have slowed and even stopped in some parts of the world. Accelerating the development of low- and zero-carbon energy sources and encouraging energy conservation, as will be done through the U.S.’s Inflation Reduction Act, will further this progress.

More will be needed. Putting a significant and steadily increasing price on the carbon in fossil fuels is arguably the most important next step. Fossil fuels enjoy a free ride. The byproduct of their combustion, CO₂, is dumped with little or no restrictions into the world’s atmosphere. A price on carbon would end this inequity. There are ways this could be done in a revenue-neutral (“fee and rebate”) manner that would avoid harm to economies and those with low- and moderate-incomes. A major step forward in pricing carbon by the European Union, a carbon border adjustment mechanism, is close to implementation. For more on this and other developments in cutting CO₂ emissions, see the analyses and insights of the Carbon Tax Center and learn more about actions you can take to influence governments with Citizens’ Climate Lobby.

Not discussed here, but another stark example of habitat disruption is the increasing acidification of the world’s oceans caused by the dissolution of atmospheric CO₂ in the waters. The ocean’s average pH has dropped from 8.2 to 8.1 within the last 200 years. Because pH is a logarithmic scale, this represents an increase in hydrogen ion concentration of over 25%, a change that is already threatening some marine creatures. More on this is available from many sources; e.g., Kolbert (2014).

References

Arhennius, Svante, 1896, On the Influence of Carbonic Acid in the Air upon the Temperature on the Ground, Philosophical Magazine and Journal of Science, 41, 237-276.

Belote, R., J. Weltzin, and R. Norby, 2004, Response of an Understory Plant Community to Elevated [CO₂] Depends on Differential Responses of Dominant Invasive Species and Is Mediated by Soil Water Availability, New Phytologist 161, 827-835.

Blumenthal, D., V. Resco, J. Morgan, D. Williams, D. LeCain, E. Hardy, E. Pendall, and E. Bladyka, 2013, Invasive Forb Benefits from Water Savings by Native Plants and Carbon Fertilization Under Elevated CO₂ and Warming, New Phytologist 200, 1156-1165.

Burghardt, Karin T., D. W. Tallamy, C. Philips, and K. Shropshire, 2010, Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities, Ecosphere 1: 1-22.

Cardoso, P., et al. 2020, Scientists’ warning to humanity on insect extinctions, Biological Conservation 242, 108426. https://doi.org/10.1016/j.biocon.2020.108426

Dukes, J., N. Chiariello, S. Loarie, and C. Field, 2011, Strong Response of an Invasive Plant Species (Centaurea solstitialis L.) to Global Environmental Changes, Ecological Applications 21, 1887-1894.

Hall, M., P. Stiling, B. Hungate, B. Drake, and M. Hunter, 2005a, Effects of elevated CO₂ and herbivore damage on litter quality in a scrub oak ecosystem, Journal of Chemical Ecology, 31, 2343-2356.

Hall, M., P. Stiling, D. Moon, B. Drake, and M. Hunter, 2005, Effects of elevated CO₂ of foliar quality and herbivore damage in a scrub oak ecosystem. Journal of Chemical Ecology 31, 267-286.

Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D., de Kroon, H., 2017, More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12, e0185809.

Hattenschwiler, S. and C. Korner, 2003, Does Elevated CO₂ Facilitate Naturalization of the Non-indegenous Prunus laurocerasus in Swiss Temperate Forests?, Functional Ecology 17, 778-785.

Janzen, Daniel H., 1988, Ecological Characterization of a Costa Rican Dry Forest Caterpillar Fauna, Biotropica, 20, 120-135.

Knepp, R., J. Hamilton, A. Zangeri, M. Berenbaum, and E. Delucia, 2007, Foliage of oaks grown under elevated CO₂ reduces performance of Antherae Polyphemus (Lepidoptera: Saturnidae), Environmental Entomology 36, 609-617.

Kolbert, E., 2014, The Sixth Extinction, Henry Holt & Co., NY

Landosky, J., and D. Karowe, 2014, Will chemical defenses become more effective against specialist herbivores under elevated CO₂? Global Change Biology, 20, 3159–3176.

Lister, B., and A. Garcia, 2018, Climate-driven declines in arthropod abundance restructure a rainforest food web, PNAS 115, E10397–E10406

Mohan, J., L. Ziska, W. Schlesinger, R. Thomas, R. Sicher, K. George, and J. Clark, 2006, Biomass and toxicity responses of poison ivy (Toxicodendron radicans) to elevated atmospheric CO₂. PNAS 103, 9086-9089.

Narango, D., D. Tallamy, and P. Marra, 2018, Nonnative plants reduce population growth of an insectivorous bird, PNAS 115: 11549–11554.

Polley, H., H. Johnson, H. Mayeux, C. Tischler, and D. Brown, 1996, Carbon Dioxide Enrichment Improves Growth, Water Relations, and Survival of Droughted Honey Mesquite (Prosopis glandulosa) Seedlings, Tree Physiology, 16, 817-823.

Robinson, E., G. Ryan, and J. Newman, 2012, A meta-analytical review of the effects of elevated CO₂ on plant-arthropod interactions highlights the importance of interacting environmental and biological variables, New Phytologist 194, 321-336.

Samways, M., et al., 2020, Solutions for humanity on how to conserve insects, Biological Conservation 242, 108427. https://doi.org/10.1016/j.biocon.2020.108427

Sánchez-Bayoa, F. and K. Wyckhuys, 2019, Worldwide decline of the entomofauna: A review of its drivers, Biological Conservation 232, 8-27.

Sasek, T. and B. Strain, 1988, Effects of Carbon Dioxide Enrichment on the Growth and Morphology of Kudzu (Pueraria lobata), Weed Science 36, 28 – 36, DOI: https://doi.org/10.1017/S0043174500074415

Sasek, T. and B. Strain, 1991, Effects of CO₂ Enrichment on the Growth and Morphology of a Native and Introduced Honeysuckle Vine, American Journal of Botany 78, 69-75.

Soares, J., C. Santos, S Carvalho, M Pintado, and M. Vasconceios, 2019, Preserving the nutritional quality of crop plants under a changing climate: importance and strategies. Plant and Soil 443, 1-26. https://doi.org/10.1007/s11104-019-04229-0

Song, L., J. Wu, C. Li, F. Li, S. Peng, and B. Chen, 2009, Different responses of invasive and native species to elevated CO₂ concentration, Acta Oecologica 35, 128-135.

Tallamy, D. and W.G. Shriver, 2021, Are declines in insects and insectivorous birds related? Ornithological Applications 123: 1–8, DOI: 10.1093/ornithapp/duaa059

Tollefson, J., 2020, How hot will Earth get by 2100? Nature News Feature, https://www.nature.com/articles/d41586-020-01125-x accessed 12/15/2022

Vogel, G., 2017, Where Have All the Insects Gone? Surveys in German nature preserves point to a dramatic decline in insect biomass. Key members of ecosystems may be slipping away, Science 356, 376-379.

Wikipedia, 2022, Terpenoid, https://en.wikipedia.org/wiki/Terpenoid accessed 12/16/22.

Wilson, Edward O., 1987, The Little Things That Run the World (The Importance and Conservation of Invertebrates), Conservation Biology, 1, 344-346.

Ziska, L., 2010, Elevated Carbon Dioxide Alters Chemical Management of Canada Thistle in No-till Soybean, Field Crops Research 119, 299-303.

Ziska, L., Shaun Falukner, and John Lydon, 2004, Changes in biomass and root: Shoot Ratio of Field-grown Canada Thistle (Cirsium arvense), a Noxious, Invasive Wed, with Elevated CO2: Implications for Control with Glyphosate, Weed Science 52, 584-588.

Ziska, L.H., J.S. Pettis, J. Edwards, J.E. Hancock, M.B. Tomecek, A. Clark, J.S. Dukes, I. Loladze, and H.W. Polley, 2016, Rising atmospheric CO₂ is reducing the protein concentration of a floral pollen source essential for North American bees, Proc. R. Soc. B, 283, 20160414, http://dx.doi.org/10.1098/rspb.2016.0414

Ziska, Lewis, 2022, Greenhouse Planet: How Rising CO₂ Changes Plants and Life as We Know It, Columbia University Press, NY.

Wood Packaging: Pests Still Coming, USDA Not Taking Action

photo courtesy of Oregon Department of Agriculture

As we know, wood packaging (SWPM; crates, pallets, spools, etc.) is a high-risk pathway for introduction of bark- and wood-infesting insects (borers). (To see my 40 earlier blogs about wood packaging material, scroll down below archives to “Categories,” click on “wood packaging”.) Examples of highly damaging pests introduced to North America include Asian longhorned beetle; emerald ash borer; redbay ambrosia beetle; sirex woodwasp; possibly the polyphagous and Kuroshio shot hole borers; Mediterranean oak borer; and dozens of others. (As of 2014, 58 new species of non-native wood- or bark-boring insects had been detected in the past 30 years [Leung et al. 2014]).

The Asian longhorned beetle and emerald ash borer were probably introduced before the World Trade Organization (WTO) came into effect in 1994; many of the others were detected – if not introduced – after that date. This global trade agreement not only facilitated rapid growth in trade volumes; it also imposed stringent conditions for adoption of plant health (= phytosanitary) measures aimed at preventing pest introductions. (For a review of the WTO restrictions, see my Fading Forests II report, here).

While the risk of pests travelling in raw wood was well known, U.S. and international phytosanitary agencies became aware that wood packaging fit into that category with detection of the ALB in New York and other wood-borer introductions. They acted remarkably rapidly to reduce this risk by negotiating and adopting International Standard for Phytosanitary Measures (ISPM) #15 in 2002.

The goal of ISPM#15 is to “significantly reduce” [not eliminate] the risk of pests associated with solid wood used for constructing packaging (e.g., crates, pallets), from being introduced to other countries through international trade.

This first international standard addressing a pathway of introductions was adopted 20 years ago. (The U.S. fully implemented ISPM#15 in 2006; see either article by Haack for a description of the phase-in period.) So – how great is the risk of pest introduction in wood packaging now? What proportion of these incoming containers are likely to be harboring tree-killing insects? Since it is impossible to reduce that risk to 0 while continuing trade using wood packaging, what is an acceptable level of risk? In determining that level, we must keep in mind the huge volumes of wood packaging being used in international trade, and the serious damage these wood-borers can cause. (See the pest profiles in the links provided above.)

I applaud the international phytosanitary community for acting fast and for choosing a pathway standard rather than try to differentiate the level of risk associated with any particular transaction – given that wood packaging could be made from dozens or hundreds of tree taxa, there are thousands of species of wood-boring insects, and the likelihood of an introduction depends in part on the exporting and importing countries. Plus, international trade involves huge volumes of goods. According to Haack et al. (2022), ~ 55 million TEU (shipping containers measured as twenty-foot equivalents) entered the U.S. in 2020. This is a 68% increase over the volume in 2003. Imports in the first half of 2020 were down because of the COVID epidemic. They then grew rapidly through the first half of 2022; imports from Asia in the first 10 months of 2022 were 21% higher than in the same period in 2019 (Mongelluzzo 2022). Haack et al. (2022) note that the number of countries from which SWPM originated more than doubled from 2003–2004 to 2010–2020, although it dropped after 2018.

In 2014, Haack et al. published an estimate of the pest approach rate in wood packaging as of 2009. Depending on which countries were included and how the time periods were selected to separate pre- and post-adoption of ISPM#15, they reported a 36–52% reduction in the SWPM infestation rate following ISPM#15 implementation. This resulted in an estimated infestation rate of 0.1% (1/10^th of 1%). In a recent blog, I applied this estimated approach rate to find that probably 11,000 containers per year transported pests to North America in 2021; 80% of these shipments came to the United States.

Since 2009, traders have gained 13 more years of experience. More important, in 2009 the standard was changed to require that wood packaging be constructed from wood that had been debarked before treatment. There is a tolerance limit for small patches of residual bark. Given that bark provides shelter both for insects already there, and facilitates any new infestation after the treatment was performed, it was expected that this change would further reduce the pest risk.

Since more than a decade has passed since the original analysis, and wood-borers continue to be found in wood packaging – in the U.S. and elsewhere – Haack and colleagues have re-analyzed the pest approach rates (see Haack et al. 2022). Their objectives were to

(1) compare pre-and post-ISPM#15 borer-infestation rates;

(2) compare the borer detection rates individually for three kinds of imports and key US trading partners;

(3) see whether wood borer presence varies by season; and

(4) assess the diversity of borer taxa detected overall, and by cargo category and country of origin.

Over the entire 17-year period 2003 – 2020, 87,571 consignments met the conditions for the study: they contained wood packaging that bore the ISPM#15 mark (from 2006 and onwards) indicating it had been treated as required; and the shipment was not from Canada (the U.S. does not require wood packaging from Canada to comply with ISPM#15).

They analyzed the data for the entire 17-year period and separately for four phases:

1) before the U.S. implemented ISPM#15 (2003-2004);

2) phasing-in of U.S. implementation (2005 – 2006);

3) full implementation – but without any restriction on THE presence of bark (2007-2009); and

4) full implementation with restrictions on bark (2010 – 2021).

Over the period 2003– 2020, wood borers were detected in 180 of the 87,571 consignments, or 0.21%. This was 38% less than the 0.34% infestation rate in 2003-2004, before the U.S. implemented ISPM#15. Still, the US had required China to treat its wood packaging as of December 1998 because of introduction of ALB. However, the reduction was greatest in the first phase (2005-2006); in subsequent periods the pest approach rate inched back up. Detection rates have been relatively constant since 2005 despite the requirement in 2009 that bark be removed and a resulting reduction in the presence of bark (it fell from 40% or more of inspected consignments before 2009 to 15% after 2010).

Unfortunately, the data used in the study do not indicate if borers detected on wood were located under any bark that was present. There might be some indication from the species detected: 100% of Scolytinae identified to genus or species detected before 2007 were true bark beetles (which develop primarily under bark), but only 23% in 2010–2020 period.

The data revealed no strong seasonal pattern.

Types of Wood Packaging

The study findings indicate that crates are the type of wood packaging most likely to be infested by insects. While crates constituted only 7.5% of the wood packaging inspected, they made up 29.4% of the infested packaging – or four times greater than their proportion of the dataset. Pallets constituted 88.6% of the inspected wood packaging, but only 67.2% of the infested shipments. Dunnage and “other” wood packaging made up insignificant proportions of both total wood packaging inspected and wood packaging found to be infested. (Of course, dunnage can still pose a threat; see my blog about issues in Houston with dunnage bracing breakbulk cargo.) The Haack et al. (2022) study did not examine dunnage accompanying breakbulk shipments.

Records of Various countries

The 180 infested consignments originated from 30 countries. For two of these countries, the percentage of wood packaging found to be infested was higher than the proportion of all wood packaging from that country that was inspected. Packaging from China made up 4.6% of all shipments inspected, but 22% of the 180 consignments with infested wood packaging. Thus the proportion Chinese consignments with infested wood is five times greater than expected based on their proportion of the dataset. The rate of wood packaging from China that is infested has remained relatively steady – as I noted above. The Chinese infestation rate was 1.26% during 2003–2004, and ranged from 0.58 to 1.11% during the next three periods.

I remind you, again, that the U.S. has required treatment of wood packaging from China since December 1998. Why does this country continue to ship pest-infested wood packaging to the United States? Why are the responsible agencies in the United States not taking action to correct this problem? (DHS Bureau of Customs and Border Protection enhanced its enforcement in 2017; see my blogs.)

A second country with a record of non-compliant wood packaging – Italy – has done better. The level of pest detection still exceeded their expected proportional level – that is, Italy constituted 12.7% of all inspected shipments, but had 15% of infested consignments. Still, Italy has reduced detection rates by almost two-thirds over the 17 years of the study. The Italian statistics would have been even better if there had not been a spike of infested wood in 2015 – 2018 – for unknown reasons.

The data indicate that a third country, Mexico, has improved the pest-free quality of wood packaging accompanying it exports.

Wood from Costa Rica and Turkey has deteriorated as regards pest infestation rates.The borer detection rate on Costa Rican shipments rose from 0.072% during all of 2003–2009 to 0.665% during 2010–2020. Pest-detection rates for Turkey were actually 0 during 2003–2004 (only 59 consignments) but rose to 1.05% during 2010– 2020.

Disturbing Trends

The data reveal other trends that I find disturbing:

While the pest approach rate has fallen since U.S. implementation of ISPM#15, the extent of the decline has progressively decreased during each period studied: the reduction during 2005–2006 was 61%; during 2007–2009, 47%; during 2010-2020 only 36%.
The 2010 – 2020 pest approach rate was calculated at 0.22%. This is more than double the rate based on 2009 data (0.1%, as stated in the 2014 paper). However, we should be cautious in making this comparison because the 2014 and 2022 studies used different methods (see below). The bottom line, however, is that the approach rate remains too high, in my view. Our forests continue to be exposed to the risk of introduction of highly damaging wood-boring pests. Furthermore, since the number of countries sending us infested wood packaging has increased, those potential pests include insects from a greater variety of countries (biomes).
Given the higher number of countries involved and rising proportion of wood that is infested, it is not surprising that the diversity of wood borers found in wood packaging increased. Cerambycidae were consistently the most commonly intercepted borers – making up just under half of the total for the 17 years. Scolytinae were consistently second, at 39%. Still, all major families of borers had been intercepted throughout the period.

Explanation

From the perspective of protecting our forests, what matters is whether the “current” infestation rate is significantly below the rate before ISPM#15 was implemented. As noted, the infestation rate in the 2010-2020 period (0.22%) is, on first glance, more than twice as high as the 2009 approach rate as calculated in the 2014 paper (0.1%). However, the earlier calculation excluded reports of wood packaging from China and Mexico for reasons given in the 2014 paper. Since these countries are among the top three sources of imports to the U.S., and all have had relatively high levels of infested wood packaging, this difference must have had a significant impact on the final finding.

Indeed, the supplementary materials in Haack et al. (2022) show just such a big impact. When records from China and Mexico are excluded from the calculation, the 2010-2020 approach rate appears to have been even higher — 0.272%. This is a reduction from the pre-ISPM#15 approach rate (0.299%) of only 9% — a quarter of the reduction found when data from China and Mexico were included (note the 36% reduction noted above). This difference in approach rate estimates reflects Mexico’s success in cleaning up its wood packaging (as noted above). Since China had “steady” infestation rates throughout, adding or dropping China had less of an impact.

The data do not show a significant drop in pest approach rates during the period 2010-2020 compared to pre-ISPM#15 levels, which is disappointing. Scientists do not know why this happened. It could reflect many of the reasons discussed in the 2022 paper. Perhaps the most important factor is that reporting data on a consignment basis does not allow us to detect whether the numbers of a pest species present have decreased. [See point 5 below.]

The fact is that a pallet or crate bearing the ISPM#15 mark has not proved to be reliable as to whether the wood is pest-free. (This might be because the wood had not been treated, or that it was, but the treatment failed). All the pests detected in study (after 2006) were in wood packaging bearing the ISPM#15 mark. I have noted in past blogs [click on the “wood packaging” category to bring up blogs about wood packaging and enforcement] that Customs and Border Protection also reported that nearly all the wood packaging in which that they detected insect pests bore the mark.

Conclusions: Haack et al. (2022)

Haack et al. (2022) note that U.S. imports have risen 68% by volume from 2003 to 2020 (with additional growth since; see above); however, borer detection rates have remained rather steady. This, plus the apparently lower number of woodborers established in recent years, suggest that ISPM#15 is helping to mitigate risks. However, the reduction in detection rates is less than hoped. They discuss ten possible explanations. Six of these factors were discussed in the original analysis (Haack et al. 2014); four others are new.

(1) Pest Thermotolerance. Can pests tolerate the heat treatment schedule mandated by ISPM#15? Haack et al. (2022) note that this schedule was based on one intended to kill the pinewood nematode and that it was recognized that some pests might be able to tolerate those conditions (Haack et al. 2014). The authors review the literature and conclude that some of the live borers found in heat-treated wood packaging in the study probably did survive the heat treatment. They note that studies are now under way to test temperatures that are lethal to various borers. I have raised the issue that standards must be based on lethal temperatures that can be achieved in practice; otherwise, they won’t protect forests from introduced pests.

(2) Unintentional non-compliance. The authors concluded that accidental treatment failures are likely. They note that the International Plant Protection Convention (IPPC) has issued guidance on handling and testing during heat treatment and fumigation.

(3) Fraud. The authors conclude that fraud is possible, but that the incidence at the global scale is unknown. Each country is responsible for their own compliance. Unfortunately, there is no effective means for independently testing whether treatments have been applied. Still, we note that all live insects evaluated in this paper were in wood package that bore the required stamp and was apparently compliant.

(4) Post-treatment colonization. Haack et al. (2022) note that adoption of the bark requirements in 2009 was intended to reduce re-infestation risk. They note that fewer true bark beetles (that develop under bark) have been detected in recent years compared w/ ambrosia beetles (that develop in wood). As I noted above, the survey data do not reveal whether insects detected by inspectors were under any remaining bark.

(5) AQIM data collection protocols. The authors note that reporting of wood borer detections by consignment conceals the per-piece infestation rate. There might be many fewer individuals of a pest in a container now – and this is important because fewer individuals pose a lower establishment risk (lower propagule pressure).

(6) Pre-ISPM actions. Some countries had begun requiring treatment of wood packaging before 2003, when data collection for the study began. Thus the approach rate might have already been reduced before ISPM#15 was implemented in the U.S., leading to a smaller apparent change.

(7) Level of detection. All the analyses assumed that the detection abilities of port inspectors remained the same over the 17 years of the study. However, inspectors might have improved their efficacy through improvements in training, inspection techniques, or technology. If so, the apparent impact of ISPM#15 would be lessened in recent years. Haack et al. (2022) say estimating the effectiveness of inspections is not possible in the absence of a “leakage survey” conducted on inspected goods to see how often target pests are missed.

(8) Changing trade partners. Countries have varying levels of effort and efficacy in enforcing ISPM#15.

(9) Varying trees and their associated borers. Countries and global regions are home to different tree species and associated insects. Therefore, changes in trading partners – or forest pest conditions within a country – can affect the number and species of potential pests harbored in the wood packaging approaching our borders.

(10) Practical limits on compliance. Reducing infestation levels to near zero through reliance on application of the ISPM#15 standard would require nearly universal compliance by industry, using highly effective treatments. Haack et al. (2022) note that such compliance levels might be difficult to achieve without either very strong incentives or intensive oversight and significant penalties for noncompliant exporters. I note that I have urged the U.S. to enhance both; link to blogs at least CBP has taken action to step up enforcement.

Haack et al. (2022) call for improved education and outreach by the IPPC, plus greater cooperation and information sharing among trading countries. I note that the Cary Institute is pursuing opening data on treatment facilities’ records so importers can hire the best.

Haack et al. (2022) conclude that ISPM#15 has resulted in marked decreases in rates of borer detection in wood packaging. However, problem areas remain re: some types of commercial goods and exporting countries. Given the enormous and growing volume of international trade, the relatively low risk associated with individual crates or pallets still poses a real risk for pest intro.

Still, they consider that the near global acceptance of ISPM#15 indicates a strong commitment by the world community to minimize movement of wood pests in SWPM through international trade.

Haack et al. (2022) call for several improvements. Some concern data to support analysis of the risk level. First, recording the numbers of infested pieces instead of reporting only consignments would help determine the numbers of insects reaching our borders. They also wish to learn whether when bark is present if it exceeds the current tolerance limits; and the type of treatment applied to each infested piece of wood packaging.

They also note opportunities to improve ISPM#15 implementation and enforcement through training on applying treatments, marking and repairing wood packaging, compiling the required records, and inspecting treatment facilities.

Oregon ash swamp; photo by Wyatt Williams, Oregon Department of Forestr

Faith’s Conclusions

In my view, it is less important whether the current approach rate is exactly 0.22% or somewhat less or more. What is important:

the pest approach rate is not acceptable given the huge and rising volume of imports, potential for introductions from new trading partners (with different insect faunas), and the great damage caused by wood-boring insects.

long-standing enforcement problems have not been resolved (i.e., Chinese wood packaging). Perhaps DHS CBP’s enhanced enforcement will bring improvements. CBP staff expressed disappointment in August 2022.

American government agencies must take more effective action to ensure that trade partners comply with ISPM#15. They should also look more aggressively at other actions to curtail introductions via this pathway, e.g.,

U.S. and Canada refuse to accept wood packaging from foreign suppliers that have a record of repeated violations – whatever the apparent cause of the non-compliance. Institute severe penalties to deter foreign suppliers from taking devious steps to escape being associated with their violation record.
APHIS and CBP and their Canadian counterparts provide guidance to importers on which foreign treatment facilities have a record of poor compliance or suspected fraud – so they can avoid purchasing SWPM from them. I am hopeful that the voluntary industry program described here will help importers avoid using wood packaging from unreliable suppliers in the exporting country.
Encourage a rapid switch to materials that won’t transport wood-borers. Plastic is one such material. While no one wants to encourage production of more plastic, the Earth is drowning under discarded plastic. Some firms are recycling plastic waste into pallets.

The two articles by Haack et al. – 2014 and 2022 – fully describe the methodology used, the structure of USDA’s Agriculture Quarantine Inspection Monitoring (AQIM) program, detailed requirements of ISPM#15, the phases of U.S. implementation, etc. Also see the supplemental data sheet in Haack et al. (2022) that compares the methods used in each analysis.

SOURCES

Haack RA, Britton KO, Brockerhoff EG, Cavey JF, Garrett LJ, et al. (2014) Effectiveness of the International Phytosanitary Standard ISPM No. 15 on Reducing Wood Borer Infestation Rates in Wood Packaging Material Entering the United States. PLoS ONE 9(5): e96611. doi:10.1371/journal.pone.0096611

Haack RA, Hardin JA, Caton BP and Petrice TR (2022) Wood borer detection rates on wood packaging materials entering the United States during different phases of ISPM#15 implementation and regulatory changes. Frontiers in Forests and Global Change 5:1069117. doi: 10.3389/ffgc.2022.1069117

Leung, B., M.R. Springborn, J.A. Turner, and E.G. Brockerhoff. 2014. Pathway-level risk analysis: the net present value of an invasive species policy in the US. Front Ecol Environ. 2014. doi:10.1890/130311

Mongelluzzo, B. Trans-Pacific volume decline picks up pace in October. JOC. November 17, 2022. https://www.joc.com/maritime-news/container-lines/trans-pacific-volume-decline-picks-pace-october_20221117.html?utm_source=Eloqua&utm_medium=email&utm_campaign=CL_JOC%20Daily%2011%2F18%2F22%20NONSUBSCRIBER_PC015255_e-production_E-148476_KB_1118_0617

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

www.fadingforests.org

Global Weirding: Rising CO2 Impacts Plants & People

Guest blog by Lewis Ziska, Associate Professor, Environmental Health Sciences at the Columbia University

[Dr. Ziska has spent his career analyzing the impacts of CO2 and climate change on plants – and therefore on people. He served as Project Leader for global climate change at the International Rice Research Institute; then spent 24 years at the USDA’s Agricultural Research Service, where he worked primarily on documenting the impact of climate change and rising carbon dioxide levels on: Crop selection improves production; Climate and agronomic pests, including chemical management; Climate, plant biology and public health impacts on food security with a focus on nutrition and pesticide use.]

No question you’ve heard the term, “Climate Change” or “Global Warming”, or my personal favorite, “Global Weirding”. The consequences are talked and discussed in the media—as they should be—but often the media, like many Americans, is focus challenged. Or in more polite terms, they have the attention span of a hummingbird on crack. Which is to say, that simple physical consequences, like sea level rise (heat melts ice!), and stranded animals on ice (Poor polar bear!), or intense storms (newscaster whipped about in the rain, yelling to be understood) are repeated, over and over again. Understandable, makes for good TV.

But it also makes you feel separate from what is happening, these consequences of climate change are to the “other”. I don’t live near the ocean, I don’t interact with polar bears; sure we have storms, but I live in the Midwest, in one of those states that begins with a vowel. Shoot, I commute to work, try and make ends meet, I’m not some damn tree hugger. Why should I care?

To understand why, you need a bit more background, some science that isn’t always available on TV or social media when it comes to global weirding.

First, while you may not be a tree hugger, you do, in fact, interact with nature. Several times. Every day. We call those times, “breakfast”, “lunch” and “dinner”.

You depend on nature for food. And clothing. And paper. And medicine. And oxygen. And construction materials (wood), and many, many other things. So, if nature gets hinky, and the climate becomes uncertain, it might be worth your while to think about climate change, or global weirding, in a different light. What I want to do here then, is to illuminate two examples that I hope will help you see why climate could affect you, directly and significantly.

Let’s begin with plants. Those green living things that comprise the bulk of the natural world (literally, if you were to weigh the natural world, 97% would be plants, 3% animals). Then let’s look at them through two different lenses—how will climate weirding alter your food; shoot, how will it alter the air that I breathe?

Let’s start with a basic food, rice. Obviously you don’t want to mess with its production, or its nutritional quality. But that is exactly what global weirding is doing.

Rice has flowers. Not big showy ones, but flowers none the less—ones that get fertilized with pollen, and seed is produced. The seed that feeds some two billion people– or about a quarter of the earth’s population.

Like all living things, plants are heat sensitive, and for rice, and many crop plants, the degree of sensitivity varies, depending on the part of the plant in question. Take a look at the table. The crops that are listed, including rice, are the core of what the world eats. Now notice the difference in temperature sensitivity. Vegetative parts of the plant, leaves and stems, are reasonably tolerant of higher temperatures, but flowers are not. Pollen, the plant equivalent of animal sperm, is highly temperature sensitive, and if the temperatures get into the high 90s (37-38^oC), they become deformed, and the rice plant doesn’t produce seeds. Same for a number of plants, ones necessary to feed 8 billion people.

Crop	Opt. Temp. Vegetative	Opt. Temp. Flowering	Failure Temp. Flowering
Maize	28-35^oC	18-22^oC	35^oC
Soybean	25-37^oC	22-24^oC	39^oC
Wheat	20-30^oC	15^oC	34^oC
Rice	28-35^oC	23-26^oC	36^oC
Sorghum	26-34^oC	25^oC	35^oC
Cotton	34^oC	25-26^oC	35^oC
Peanut	31-35^oC	20-26^oC	39^oC

Data are adapted from Hatfield et al., 2011.

Doubtful you’ve seen this climate threat to the global food supply on TV or a streaming service. I caught a glimpse once of temperature and agriculture on a CNN newscast, but with the “expert” calmly stating that we would just have to grow our corn in Canada, ha-ha. (Somehow, at least for rice, it’s hard to imagine India, one of the world’s largest rice producers, moving its rice production northward to the Himalaya’s, but I digress.)

Food is fundamental. If production, especially that of a global staple like rice, is impacted by rising temperatures there will be consequences. Rising prices, reduced availability, and wide-spread hunger.

But there is more to consider. Given the global dependence on rice, any change in its nutritional quality will also have effects, especially on poorer countries that rely heavily on rice as a major food source. And here we need to delve a little deeper into another aspect of climate weirding that doesn’t make it to the popular media—that rising carbon dioxide (CO₂), the primary greenhouse gas, can also directly influence plant nutrition. The reasons are complicated, but in simple terms all living things consist of elements, carbon, nitrogen, phosphorous, sulfur, copper, etc., etc. A plant gets it’s carbon from the air (CO₂), but everything else (nitrogen, potassium) from the soil.

And there is an imbalance. In the last 50 years, atmospheric CO₂ has increased by about 30%, and is projected to increase another 50% by the end of the century. With more CO₂, plants are becoming carbon rich, but nutrient poor. Nutrient poor, because while CO₂ has increased in the air, nutrients in the soil have not kept pace. A perverse carb loading at the plant level.

As a consequence, rice, and many other plants, are shifting their chemistry. For example, there is a general decline in protein, in part because protein requires nitrogen. There are similar ubiquitous declines in iron and zinc, important micro-nutrients needed for human development.

Such nutritional degradation is of obvious global importance, and does, on occasion, show up on basic media when warming / weirding is mentioned, but you’d be hard pressed to find it.

Let’s move our light to another hidden bit of science. How plants can influence the air we breathe.

As humans, we like to trade things. And a large percentage of what we trade are living organisms, from fish to trees. But what began as local, regionalized trading has grown with the global population and the needs of that population—a population of 1.6 billion at the beginning of the 20^th century is now ~8 billion at the beginning of the 21^st. And we haven’t stopped trading. Biological trade is not inherently bad, but it represents a historically unprecedented global movement of DNA across continents, across countries, regions, towns, cities and ecosystems. And some of the DNA, when introduced, can do great harm to the environment, the economy and to human health. That harm has a name, “Invasive Species”.

Let us focus on one such plant species introduced to Eastern Europe, one that almost every American has personal experience (ACHOO!) come fall. The species is common ragweed. An invasive plant whose introduction and spread in Eastern Europe—introduced accidently through imported seeds or contaminated hay – has resulted in enormous environmental and economic losses in agriculture and public health in recent decades. In Hungary, the most important ambient biological air pollutant is: ragweed.

collecting ragweed pollen under different climates (Author’s photo)

The photo is from studies that I led looking at how ragweed pollen would respond to temperature and carbon dioxide. (If you’re curious, ragweed likes both.) Warmer temperatures, earlier Springs, later Autumns can extend its pollen season; not only extend, but increase the amount of pollen being generated. There is even some data suggesting that rising CO₂ can alter pollen chemistry, making it more allergenic (REFS). Sadly, ragweed pollen doesn’t appear as temperature sensitive as that of rice, or other agricultural plants.

I wish I could say that ragweed was the exception among allergenic plants, but it’s the rule. Parthenium weed is a highly invasive species that has spread to more than 40 countries around the world. Like ragweed its pollen are highly allergenic, but it can also produce severe rashes, like poison ivy, and is known to be poisonous to livestock. It is highly aggressive, and arriving in a new location (where it has no natural enemies) can dominate landscapes, reducing biodiversity. And as with ragweed, high temperatures, longer growing seasons, heatwaves and droughts are expanding its range, and for that matter, make controlling its spread more difficult.

Such responses among invasive species will have direct impacts on air quality, especially among those (myself included) who suffer from seasonal allergies. Gasping for air is never fun.

Estimates are that pollen and seasonal asthma affects more than 24 million of us, including 6 million kids. And yet, when watching news reports of climate change, how many times have you seen a report on pollen and air quality? On increasing allergies or asthma? Once? Twice?

I could go on, (and if you need more examples, read “Greenhouse Planet”, my latest book). But my point is this: Not all of the consequences of rising carbon dioxide and climate change, warming, weirding, whatever, make for “good” TV. There is so much more to explore. So, do yourself a favor. Take a deeper dive, find out what is happening behind the scenes.

Because if we are going to rise to the challenge, we need to know what we are fighting against. Right now, the media is exemplary on showing some things, but silent on much else of importance. Watching news coverage of climate change is a bystander watching a cataclysm, and thinking, “Boy, glad I’m not experiencing THAT!”. Yet in the simplest and most basic of terms, you are, or will be, affected– from food choices to nutrition, even your allergies. And so much more.

It isn’t just about polar bears. It’s about you. Read, Understand, Act.

Now.

EAB in Eastern Europe – Worse (+ war!)

A special issue of the journal Forests (Vol. 13 2022) seeks to improve understanding of the root causes of exacerbated threats from insect pests. The issue contains 15 papers; most focus on geographic areas other than North America. The journal is open access!

Choi and Park (full citations below) link increased pest risk to climate change and increased international trade. They provide brief summaries of all 15 papers. My focus here is on two articles that provide updates on the status of the emerald ash borer (EAB Agrilus planipennis) in Russia and Ukraine. The article by Davydenko et al. also examines interactions between EAB and the invasive pathogen Hymenoscyphus fraxineus, which causes ash dieback disease. In other blogs I will look at insects linked to North America (both species from North America that threaten forests on other continents, and species in Russia that pose a threat to North America) and at the overall Russian experience.

I blogged about EAB invasion of Russia in April 2021 so this is an update.

Musolin et al. (2022) (full citations below) remind us that the EAB invasions of North America and Russia were detected almost simultaneously: in Michigan and Ontario in 2002 and in European Russia (Moscow) in 2003. They conclude that both invasions probably originated from a common source (most probably China). They date the introduction to the late 1980s or early 1990s; pathways might have been wooden crafts, wood packaging, or ash seedlings. Nate Siegert used dendrological studies to estimate a similar introduction date for the North American invasion.

European ash (*Fraxinus excelsior*) specimen in Belgium; photo by Jean-Pol Granmont

EAB has spread far in the intervening 30 + years. By early 2022, outbreaks were recorded in five Canadian provinces, 35 US states, 18 provinces and several cities in European Russia, and two provinces in Ukraine (Musolin et al. 2022) Davydenko et al. report that EAB had also established in eastern Belarus, but provide no details.

As demonstrated in the earlier blog and confirmed by Musolin et al. (2022) and Davydenko et al., the EAB has spread much faster to the southwest than directly West and to the Northwest. Davydenko et al. attribute the slower spread in the St. Petersburg area to the colder and wetter climate of this region – which is ~1200 km north of Ukraine. While the EAB reproduces in two cohorts in Eastern Ukraine, to the north the beetle requires more than one year to complete its life cycle, at least two years in the St. Petersburg area. In 2021, Musolin et al. 2021 speculated that pressure by the native parasitoid Spathius polonicus Niezabitowski might also be slowing EAB’s spread in the North. In 2022, Musolin does not address this possibility. (I note that APHIS has approved two Spathius species as biocontrol agents in the U.S.).

Musolin et al. (2022) and Davydenko et al. agree that the EAB poses real threat to ash in central and western Europe. In both the south (Davydenko et al.) and in the northwestern area around St. Petersburg ash grows in continuous stretches, linking Russia or Ukraine to Romania, Hungary, Slovakia, and Poland. These ash consist of both natural woodlands, and extensive plantings of both one of the European ash species, F. excelsior and the highly-susceptible North America green ash (F. pennsyvanica). Furthermore, the EAB is an excellent hitchhiker on vehicles & railway cars. Davydenko et al. also consider the beetle to be a strong flyer. Musolin et al. (2022) cite a separate analysis in stating that EAB can probably invade most European countries. Only some regions of Norway, Sweden, Finland, Ireland, and Great Britain are probably protected by their low temperatures.

Both articles were written too early to consider how the current war in the relevant area of Ukraine might affect spread of the EAB, although we know Ukrainians are cutting firewood. The war has certainly interrupted monitoring and other efforts.

The sources agree on EAB’s severe impacts. Musolin et al. (2022) notes that the beetle has killed millions of trees in the forests and urban plantings in North America, European Russia, and Eastern Ukraine. Davydenko et al. note that the Fraxinus genus is one of the most widely distributed tree genera in North America. They then assert that the EAB could virtually eliminate it. I know that North American scientists agree that the beetle threatens many species in the genus; but do they agree that the genus would be “virtually eliminated”? Davydenko et al. think the EAB could pose similar threat to Euro ash F. excelsior.

Musolin et al. 2022 estimate that potential economic losses in Europe could reach US$1.81 billion. By this indicator, the species ranks fourth among the most “costly” invasive pests. Russia spent an estimated US$258.9 million between 2011 and 2016.

areas of Ukraine where studies conducted

Species’ varying vulnerability

Musolin et al. (2022) cite experience in the Moscow Botanical Garden as showing that only two Asian species — Chinese ash, F. chinensis, and Manchurian ash, F. mandshurica — are were resistant to the EAB. The beetle killed both North American ash (i.e., F. pennsylvanica and F. americana) and European ash (i.e., F. excelsior, F. angustifolia, and F. ornus).

Experience in the field in Ukraine (Davydenko et al.) suggests that F. excelsior is less vulnerable to EAB than F. pennsyvanica. The overwhelming majority of EAB infestations were found on the American species. Furthermore, although similar densities of EAB larvae were found in colonized branches of both species, the proportion of larvae that were viable was significantly higher on F. pennsyvnica (91.4%) than on F. excelsior (76.1%). However, the reverse was found in the Moscow and St. Petersburg regions. Davydenko et al. don’t address directly whether they think this discrepancy is attributable to climatic factors or to differences in vulnerability between trees growing in native forests vs. human plantings. They did note that all observed cases of infestation of the native F. excelsior in Ukraine occurred in artificial plantings rather than in natural woodlands.

Interactions with Ash Decline

ash dieback disease – unfortunately pictured in the UK.
cc-by-sa/2.0 – © Adrian Diack – geograph.org.uk/p/6497286

Davydenko et al. studied parts of Eastern Ukraine where EAB was entering areas already infected by the invasive ascomycete fungus Hymenoscyphus fraxineus (cause of ash dieback, ADB). [Two of these regions — Luhansk and Kharkiv – have been the very center of the current war.] Other studies have shown that ~1 to 5% of F. excelsior trees exhibit some resistance to ADB. These trees are thus a potential foundation for future propagation and restoration of ash in Europe – if enough of them survive attack by EAB.

They found that F. excelsior is more resistant to EAB than F. pennsylvanica, but more susceptible to ADB.

The Luhansk and Kharkiv regions have both EAB and ADB; the Sumy region has only the pathogen. EAB probably invaded the Luhansk region by 2016 (although it was detected only in 2019). The proportion of ash trees (both native and introduced species) infested rose from ~ 10–30% in 2019 to 60 – 90% by 2020–2021. The EAB arrived later in the Kharkiv region, to the Northwest, but the proportion of infested trees was similar by 2021. Combining the two regions, 75% of F. pennsylvanica trees were EAB-infested, whereas only 31% of F. excelsior trees were.

Frequencies of infections by ADB were the reverse. Pooled data from all three study regions showed 21% of F. pennsylvanica trees were infected vs. 42% of F. excelsior. In the plots invaded by both EAB and ADB (in Luhansk and Kherson regions), 4%of F. pennsylvanica were affected by both invasive species vs. 14% of F. excelsior trees. Davydenko et al. conclude that ADB facilitates EAB attack on F. excelsior trees

The impact of EAB is seen in the fact that overall mortality rates were higher in F. pennsylvanica despite the fact that in the Sumy region mortality rates were higher in F. excelsior because of the disease (EAB was absent from this region). On the other hand, EAB infests and kills F. pennsylvanica trees regardless of their prior health condition (i.e., regardless of presence/absence of ADB).

Still, fewer than half the F. excelsior trees in sites affected by both EAB & ADB (in Luhansk and Kherson regions) have died. Davydenko et al. think the survivors constitute a source of material for eventual propagation. These trees need to be carefully mapped – a task certainly not facilitated by the war!

Davydenko et al. conclude that

1. Invasion of EAB in Ukraine occurred 2–3 years before detection in 2019 [I think this is actually quite prompt for detection of EAB invasions]; the invasion is currently expanding both in terms of newly infested trees and invaded geographic area.

2. Fraxinus excelsior (at least when growing in the interior of forest stands) is more resistant to EAB than F. pennsylvanica (when growing in field shelterbelts).

3. Fraxinus excelsior is more susceptible to ADB than F. pennsylvanica.

4. Infection by ADB is likely to predispose F. excelsior to infestation by EAB.

5. Ash trees infected by ADB are predisposed for the colonization by ash bark beetles Hylesinus spp. [I did not discuss these data.]

6. Inventory and mapping of surviving F. excelsior, affected by both ADB and EAB, is necessary to acquire genetic resources for the work on strategic, long-term restoration of devastated areas, thereby tackling a possible invasion of EAB to the EU.

I was surprised that Musolin et al. (2022) think EAB’s host shift from local Asian ash species to introduced North America ash planted in the Russian Far East and China triggered EAB outbreaks in Eastern China that contributed to the beetle’s introduction to North America and European Russia. American scientists apparently agree — Haack et al. (2022) refer to both this episode and a similar to one posited for Asian longhorned beetle (Anoplophora glabripennis) — that widespread planting of Populus plantations led to rapid expansion of ALB in northern China, and the pest-weakened wood was then used in wood packaging.

SOURCES

Choi, W.I.; Park, Y.-S. Management of Forest Pests and Diseases. Forests 2022, 13, 1765. https://doi.org/10.3390/f13111765

Davydenko, K.; Skrylnyk, Y.; Borysenko, O.; Menkis, A.; Vysotska, N.; Meshkova, V.; Olson, Å.; Elfstrand, M.; Vasaitis, R. Invasion of emerald ash borer Agrilus planipennis and ash dieback pathogen Hymenoscyphus fraxineus in Ukraine-A concerted action. Forests 2022, 13, 789.

Haack RA, Hardin JA, Caton BP and Petrice TR (2022) Wood borer detection rates on wood packaging materials entering the United States during different phases of ISPM#15 implementation and regulatory changes. Front. For. Glob. Change 5:1069117. doi: 10.3389/ffgc.2022.1069117

Musolin, D.L.; Selikhovkin, A.V.; Peregudova, E.Y.; Popovichev, B.G.; Mandelshtam, M.Y.; Baranchikov, Y.N.; Vasaitis, R. North-Westward Expansion of the Invasive Range of EAB, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) towards the EU: From Moscow to Saint Petersburg. Forests 2021, 12, 502. https://doi.org/10.3390/f12040502

Musolin, D.L.; Kirichenko, N.I.; Karpun, N.N.; Aksenenko, E.V.; Golub, V.B.; Kerchev, I.A.; Mandelshtam, M.Y.; Vasaitis, R.; Volkovitsh, M.G.; Zhuravleva, E.N.; et al. Invasive insect pests of forests and urban trees in Russia: Origin, pathways, damage, and management. Forests 2022, 13, 521.

Siegert, N.W. 2006. 17th USDA Interagency Research Forum on Gypsy Moth and Other Invasive Species. Annapolis, MD. January 10-13, 2006.

Posted by Faith Campbell

www.fadingforests.org

US invasive species — updated USGS database now on-line

ōhiʻa rust on Hawai`i; photo by J.B. Friday

The U.S. Geological Survey (USGS) has published an updated register of introduced species in the United States. The master list contains 14,700 records, of which 12,571 are unique scientific names. The database is divided into three sub-lists: Alaska, with 545 records; Hawai`i, with 5,628 records; and conterminous (lower 48) United States, with 8,527 records.

The project tracks all introduced (non-native) species that become established, because they might eventually become invasive. The list includes all taxa that are non-native everywhere in the locality (Alaska, Hawai`i, or 48 conterminous states) and established (reproducing) anywhere in that locality.

Each record has information on taxonomy, a vernacular name, establishment means (e.g., unintentionally, or assisted colonization), degree of establishment (established, invasive, or widespread invasive), hybrid status, pathway of introduction (if known), habitat (if known), whether a biocontrol species, dates of introduction (if known; currently 47% of the records), associated taxa (where applicable), native and introduced distributions (when known), and citations for the authoritative source(s) from which this information is drawn.

The 2022 version is more complete re: plant pathogens than earlier iterations; I thank the hard-working compilers for their efforts!

Hawai`i

wiliwili tree (Erythrina *sandwicensis*); photo by Forest and Kim Starr

Among the non-native species listed as being in Hawai`i are 3,603 Arthropods, including the following about which I have blogged:

three Euwallaceae,
Erythrina gall wasp (Quadrastichus erythrinae),
Klambothrips myopori,
eight species of mosquito in the Hawaiian islands, including the Culex and Aedes species that vector the diseases that have caused extinction of numerous endemic bird species on the Islands.

The list also includes 25 fungi, among them the two species of Ceratocystis that cause rapid ʻōhiʻa death; DMF & blog 270 and the ʻōhiʻa or myrtle rust, Austropuccinia psidii.

Also listed are 95 mollusk species and 20 earthworm species. I wonder who is studying the worms’ impacts? I doubt any is native to the Islands.

The Hawaiian list contains 1,557 non-native plant species. Families with largest representation are Poaceae (grass) – 223 species; Fabaceae (beans) – 156 species; and Asteraceae – 116 species. About a third of the plant species – 529 species – are designated as “widespread invaders”. This number is fifteen times higher than the numbers in lists maintained by either the Hawaiian Ecosystems At Risk project (106 species) [HEAR unfortunately had to shut down a decade ago due to lack of funds]; or Hawaiian Invasive Species Council (80 species). Furthermore, some of the species listed by HEAR and HISC are not yet widespread; the lists are intended to facilitate rapid responses to new detections. We always knew Hawai`i was being overrun by invasive species!

Among the 529 most “widespread invaders” are the following from the most introduced families:

Poaceae – Agrostis stolonifera, 6 Cenchrus spp, 2 Cortaderia spp, 3 Eragrostis,8 Paspalum, 4 Setaria spp, 2 Urochloa (Poacae)
Fabaceae – 3 Acacia, 2 Prosopis

Other families have fewer introduced species overall, but notable numbers of the most widespread invaders:

Euphorbiaceae – 8 spp. of Euphorbia
Cyperaceae – 6 spp. of Cyperus
Myrtaceae – Melaleuca quinquenervia, 2 Psidium, Rhodomyrtus tomentosa rose myrtle, 3 Syzygium [rose myrtle has been hard-hit by the introduced myrtle rust fungus]
Zingiberaceae – 3spp. Hedychium (ginger)
Anacardiaceae — Schinus molle (Peruvian peppertree); USGS considers congeneric S. terebinthifolia to be somewhat less widespread.

Plus many plant taxa familiar to those of us on the continent: English ivy, privet, castor bean, butterfly bush, Ipomoea vines … and in more limited regions, Japanese climbing fern Lygodium japonicum.

*Rhus sandwicensis*; photo by Forest and Kim Starr

I learned something alarming from the species profiles posted on the HISC website: the Hawaiʻi Division of Forestry and Wildlife and Hawaiʻi Department of Agriculture are considering introduction of a species of thrips, Pseudophilothrips ichini, as a biocontrol agent targetting S. terebinthifolia. I learned in early 2019, when preparing comments on Florida’s proposed release of this thrips, that Pseudophilothrips ichini can reproduce in low numbers on several non-target plant species, including two native Hawaiian plants that play important roles in revegetating disturbed areas. These are Hawaiian sumac Rhus sandwicensis and Dodonea viscosa. The latter in particular is being propagated and outplanted in large numbers to restore upland and dryland native ecosystems. While the environmental assessment prepared by the USDA Animal and Plant Service says the thrips causes minimal damage to D. viscosa, I am concerned because of the plant species’ ecological importance. Of course, the two Schinus species are very damaging invasive species in Hawai`i … but I think introducing this thrips is too risky. [To obtain a copy of CISP’s comments, put a request in comments section. Be sure to include your email address in your comment; the section algorithm does not include email addresses (how inconvenient!).]

Continental (lower 48) states

Among the 8,500 species listed in the USGS Register for the 48 continental states are 4,369 animals, among them 3,800 arthropods; 3,999 plants; and just 89 fungi. Among the arthropods, there are 1,045 beetles and 308 lepidopterans. The beetles listed include 12 Agrilus (the genus which includes emerald ash borer and goldspotted oak borer.) It does not include the elm zig-zag sawfly USGS staff have not found any publications documenting its U.S. occurrences. Among the microbes are six Phytophthora (P. cinnamomi, P. lateralis, P. pseudocryptogea, P. quercina, P. ramorum, P. tentaculata). Profiles of several of these species are posted at www.dontmovefirewood.org; click on “invasive species”, then scroll using either Latin or common name.

elm zig-zag sawfly; photo by Gyorgy Czoka via Bugwood

Citation:

Simpson, Annie, Pam Fuller, Kevin Faccenda, Neal Evenhuis, Janis Matsunaga, and Matt Bowser, 2022, United States Register of Introduced and Invasive Species (US-RIIS) (ver. 2.0, November 2022): U.S. Geological Survey data release, https://doi.org/10.5066/P9KFFTOD

United States Register of Introduced and Invasive Species; US-RIIS ver. 2.0, 2022

If you would like to contribute to future versions of the US-RIIS, please email the project leaders at us-riis@usgs.gov.

Posted by Faith Campbell

www.fadingforests.org

Plants Sold – Increasing % of Exotics

carnation (*Dianthus caryophyllus*) photo by Noordzee23 via Wikimedia; carnations have been big sellers for 250 years

Plants sold in nurseries directly influence urban landscapes by providing gardens and other habitats that support humans and birds, insects, and other organisms. Doug Tallamy, though, has described ways that non-native plants fall short in providing habitat for native wildlife. Of course, non-native plants also indirectly influence natural landscapes by acting as a major source of invasive species. [see blog – includes links to regional invasive plant lists; and here] Imported plants also can carry non-native insects and pathogens – about which I blog frequently! To review these blogs, scroll down below the archives to the “categories” section and click on “plants as pest vectors”.

Now Kinlock, Adams, and van Kleunen (full citation at the end of this blog) have published a new paper that sheds more light on these issues. They analyzed the ornamental plants sold in US nurseries over 225 years (from 1719 to 1946). Their database, drawn from an earlier publication by Adams (see Sources at end of blog), included records of 5,098 ornamental vascular plant species offered for sale by 319 US nursery catalogs published over this period.

They note that present-day urban yards in the continental United States are planted in a diverse array of plants and the plants are predominately non-native species. Also, there is relatively little variation in species planted from one region to another, especially when compared to regional variation in natural areas). These patterns reflect the history of US horticulture.

Seventy percent (3,587) of the 5,098 ornamental vascular plant species offered by the 319 nurseries over those 200 years were non-native to the continental United States. They believe that the number of non-native species offered for sale has probably continued to increase in the 70 years since their study ended. They cite a study showing that 91% of tree species sold by nurseries in southern California during the 20^th and early 21^st centuries were not native to that state. A similar figure comes from a study of cultivated plants grown in Minneapolis–Saint Paul. There 66% of plants were non-native. (Kinlock, Adams, and van Kleunen note that 70% of species cultivated in yards of five British cities are non-native. In contrast, only 23% of cultivated plants in 18 Chinese cities were non-native.)

Kinlock, Adams, and van Kleunen note that two examples of non-native plants that have become invasive were among most common species available from nurseries beginning in the mid-19^th Century: Japanese honeysuckle (Lonicera japonica) was available in 78 nurseries, and Japanese barberry (Berberis thunbergia) in 46 nurseries.

Japanese honeysuckle; photo by Chuck Bargeron, Bugwood

Historical Trends

The earliest commercial horticulture in colonies that became the United States was in the mid-17^th Century. It involved imports of Eurasian fruit trees to establish orchards to provide familiar foods. Ornamental horticulture became popular earlier than I expected. Prince Nurseries was established in 1732 in Flushing, NY. It was followed by additional nurseries in New York, Philadelphia, and Massachusetts. Originally these businesses imported Old World nursery stock and seeds – again to provide familiar foods and take advantage of relationships with European contacts.

Nurseries proliferated in the 1820s in the population centers of the Atlantic coast. As people of European ancestry moved west, so did nurseries. Kinlock, Adams, and van Kleunen point out an interesting aspect of these changes: proliferation of both was aided by technology: steamboats, canals, highways, and improved mail service. Before 1800, nearly all nurseries were in the Mid-Atlantic, New England, and South. Nurseries appeared in the Great Lakes region by the 1830s. Expansion of rail lines connected nurseries from coast to coast by the 1870s. By 1890, there were more than 4,500 nurseries across the continent.

California, Florida, and Oregon are now the states with the most horticultural operations and sales (as of 2019).

The types of plants offered for sale proliferated throughout the 19^th Century. The species richness of US nursery flora peaked in the early 20th Century. It decreased in the 1925 – 1946 period, possibly attributable to some combination of war-related interruptions to trade and a shift in gardeners’ focus away from ornamentals to vegetables. Another factor was adoption of international and interstate phytosanitary regulations in the early 20^th Century. The post-World War II economic boom led to a new diversification of US nursery flora. In one study, a Los Angeles nursery experienced the largest increase in species richness during 1990–2011. They believe this increase was probably matched across the country. Global plant collection and importation mediated by US botanical gardens and nurseries remain active.

planting of *Eucalyptus* seedlings in California during 1980s; National Archives photo

Over time, nursery floras in the various regions became more similar to each other. The floras of Mid-Atlantic and New England nurseries differed before 1775, then became similar. Nurseries in the Great Lakes region also shifted toward offerings in neighboring regions. Later, nurseries in the South and West also began offering a higher proportion of species commonly sold across the continent. The nursery floras of Great Lakes and Great Plains regions were consistently similar. Still, the flora in Western nurseries still retain some unique aspects. California is the only state with a Mediterranean climate. Nurseries there sought adapted plant species, especially from an entirely new source — Australasia. (The authors note that Acacia and Eucalyptus genera, while important in California horticulture, are invaders in Mediterranean zones worldwide.) One might expect the need for plants in the Southwest to be drought-tolerant would prompt a unique nursery flora. However, the ubiquity of irrigation since the late 19th Century has blunted this necessity. Still, nursery flora in the desert biome had the most phylogenetic uniformity. The article does not discuss pressure to choose xeriscapes or otherwise adjust to current water shortages.

*Pinus mogu* – sought for xerescapes; photo by Krysztof Ziamk Kenraiz via Wikimedia

Growing Importance of Non-Native Species – Especially from Asia

Kinlock, Adams, and van Kleunen define “native” species as those native to the state in which it is sold; “adventive” species as native to the continental United States but not the specific state; and non-native or alien species as not native to the continental United States.

Applying these definitions, the proportion of native species in nursery flora has been consistently around 30-40% — except during the American Revolution. It rose to 70% in catalogs or advertisements published from 1775 to 1799. The authors do not speculate whether this reflected jingoism or interruptions in trade. The proportion of plant species that were adventive was 4% in the earliest period, then rose to 13% with improved transportation.

A large proportion of the native species offered in the late 18^th and early 19^th centuries were grown for export to Europe (think John Bartram).

*Rhodendron maximum*; sent to Europe by John Bartram (& invasive in Great Britain and Ireland!); photo from Pl@ntNet.identify

Throughout the 19^th and 20^th centuries, plants from new regions of the world with unique genetic lineages became increasingly available. Until the mid-19^th Century, most non-native plants came from Europe and Eurasia. Beginning in 1850, plants native to temperate Asia composed an increasing percentage of non-native nursery flora. In the period 1900 – 1924, 19% of the ornamental nursery flora originated from temperate Asia. By the next period, 1925 – 1946, this percentage rose to 20.8%.At the same time, North American species (including some from Mexico, Canada, or Alaska) composed 21.9% of the nursery flora. (see graph).

% of species from various origins; North America – medium blue; temperate Asia – dark pink; Europe – tan; Eurasia – fuscia; Southern America – blue-green; Africa – yellow-green; Americas – olive

Plants from East Asia were particularly desirable for both biological and social reasons. First, because of climatic similarities between the two regions, East Asian plants thrived in the eastern United States. Second, popular ornamental genera had higher species richness in East Asia. Important social or cultural factors were a growing fascination with Japanese and Chinese-style gardens: forced “opening” of access to those countries in the 1840s and 1850s; and plant collecting expeditions sponsored by British and American institutions and private collectors. In 1898, the US Department of Agriculture established the Section of Seed & Plant Introduction; its purpose was to collect and cultivate economically useful non-native plants from throughout South America and Asia.

As I noted above, diversity of species in nursery offerings reached a peak in the first years of the 20^th Century, concurrent with the first wave of US-sponsored plant collections; indeed, 70 species that were first listed after 1911 in their dataset were introduced by the USDA introduction program between 1912 -1942.

Commodore Perry in Japan; Library of Congress

Counter-pressures and Counter-measures

There were counter pressures during this period that – as mentioned above—probably contributed to a decline in plant introductions in later years. In the 1890s, several US states began requiring inspection of imported plant materials (spurred by plant disease outbreaks caused by spread of San Jose scale from California).

Congress adopted the Plant Quarantine Act in 1912; USDA implemented it through stringent regulations issued in 1919 (Quarantine-37). I have already noted interruption of trade associated with WWI and WWII. Kinlock et al. don’t mention the Great Depression that intervened, but I think it played a role, too. On the other hand, Q-37 was relaxed to target particular species or regions based on pest risk analysis. The article says the relaxation began in the 1930s, but I believe it actually was during the 1970s; see Liebhold et al. 2012. I have blogged several times about how well the current regulations – including the “NAPPRA” program – prevent introductions of invasive plants or damaging plant pests. To review these blogs, scroll down below the archives to the “categories” section and click on “plants as pest vectors”.

dogwood anthracnose; photo by Robert Anderson, USFS; via Bugwood

SOURCES

Adams, D.W. 2004. Restoring American Gardens: An encyclopedia of heirloom ornamental plants. Timber Press

Kinlock, N.L., D.W. Adams, M. van Kleunen. 2022. An ecological and evolutionary perspective of the historical US nursery flora. Plants People Planet. 2022;1–14. wileyonlinelibrary.com/journal/ppp3

Liebhold, A.M., E.G. Brockerhoff, L.J. Garrett, J.L. Parke, and K.O. Britton. 2012. Live Plant Imports: the Major Pathway for Forest Insect and Pathogen Invasions of the US. www.frontiersinecology.org

Posted by Faith Campbell

www.fadingforests.org

New Publication on Threats to World’s Forests – including Invasives

In a new paper, “Forest Resources of the World: Present Status and Future Prospects,” Singh et al. affirm the importance of forests for terrestrial biodiversity, provision of multiple ecosystem services, and supporting the economic well-being of approximately 1.6 billion people directly. This equals about a quarter of Earth’s population. The authors conclude that achieving global Sustainable Development Goals (SDGs), including poverty reduction, food security, and mitigating and adapting to climate change — all depend on sustaining forests.

According to the 2020 Global Forest Resource Assessment, Earth’s forested area comprises ~4.06 billion hectares, or 31% of the total land surface.More than half (54%) of all global forest area is found in five countries: the Russian Federation, Brazil, Canada, the United States, and China. Tropical forests constitute 45% of this total; boreal forests, 27%; temperate forests, 16%; and subtropical forests, 11%. An estimated 93% (3.75 billion ha) regenerate through natural processes; 7% (290 million ha) is planted forest.

The extent of global forest area has been declining for decades but the rate of loss slowed significantly between 1990 and 2020. This reflects decreased deforestation in some countries and an increase in forest area in others. The latter is due to both afforestation and also natural forest growth. However, conversion of tropical forests to agriculture continues apace. From 2010 to 2020, the net loss of forest area was highest in Africa (3.9 million ha) and South America (2.6 million ha). Increases in net forest area occurred in Asia, Oceania and Europe. The status of the top 10 countries or territories in global forest resources as of 2020 is given in Table 1.2 of the chapter. [News sources document that rapid deforestation continues in Brazil, at least.]

Several trends are concerning to those of us who value primary or undisturbed forests. First, the area of naturally regenerating forest has decreased, while the area of planted forest has expanded – but only by 123 million ha. In the last decade, the rate of increase in the area of planted forests has also slowed.

Second, total carbon stock in forests declined from 668 gigatons to 662 gt in 1990–2020. This is only 6%, but it is trending in the wrong direction. As we know, forest conservation counters climate change in two ways: conserved forests are a carbon sink, while degraded or destroyed forests are a significant source of atmospheric CO₂. In fact, forests are the 2^nd largest storehouses of carbon, after oceans. Global forests sequester about one-third of total CO₂ emission from the combustion of fossil fuels. Almost all forest carbon is found in living biomass (44%) and soil organic matter (45%).

Costa Rican rainforest; photo by eflon via Flickr

Third, primary forests are already severely reduced and continue to shrink. Primary forests are those composed of native species, and supporting relatively undisturbed ecological processes. They are irreplaceable for sustaining biological diversity. These forests are already severely reduced – they cover only ~ 1 billion ha. Since 1990, the extent of primary forest has decreased by 81 million ha. More than half are in Brazil, Canada, and Russia.

Singh et al. report that only about 10% of the world’s forests are set aside for biodiversity conservation. Again, trends are in the wrong direction. The rate of increase in the area of forest designated largely for biodiversity conservation has slowed. On the other hand, forest areas designated for other non-extractive purposes have increased: soil and water conservation, recreation, tourism, education, research, and the protection of cultural and spiritual sites.

Singh et al. are cheered by the fact that more than 2 billion hectares are under management with well-defined management plans. The extent of forests under management plans has increased by 233 million ha since 2000.

Singh et al. say that continuously increasing anthropogenic pressure is the main cause of deforestation and forest degradation in unmanaged forests. Citing projections that the world’s population will reach almost 10 billion by 2050, they say this growth will make reconciling the need for forest conservation with the basic requirements of humans for food, shelter, and fuel more difficult than ever.

I appreciate this honesty. Too many experts interviewed on the day that the global population was estimated at 8 billion made optimistic statements about the consequences. They mentioned Earth’s carrying capacity only in reference to First World people demanding excessive resources. There was minimal discussion of humanity’s carbon footprint and no reference to ever-increasing threats to biological diversity. Nor to the fact that people in developing countries want to raise their standards of living – which entails higher demand for resources, including energy. For an example, see The Washington Post editorial, here.

On the other hand, Ruby Mellen in the Post on 15 November mentioned that, according to the World Wildlife Fund, 75% of Earth’s ice-free land has been significantly altered by people, and two-thirds of mammal, fish, reptile, and amphibian species have become endangered in the last ~50 years. Unfortunately, the on-line version of the paper doesn’t have this specific article!

fires in Siberian forest in 2016; European Space Agency

Threats to Forests: Fire

Singh et al. rank fire as the most disastrous threat, affecting biodiversity and carbon sequestration potential. According to the U.N. Food and Agriculture Organization, about 29% of the total geographical area in the world was affected by forest fires during 2001–2018; more than two-thirds of these fires occurred in Africa. U.S. media, however, focused on fires in the Amazon, temperate areas (U.S., Europe), and, sometimes, boreal forests or Australia. Singh et al. say that areas that are frequently affected by fire are prone to other types of disturbances like drought and outbreaks of insect pests.

tanoaks killed by *Phytophthora ramorum* in Oregon; photo by Oregon Department of Forestry

Threats to Forests: Diseases and Pests

I am glad that Singh et al. recognize the damage to forest productivity caused by disease and pest infestations. In doing so, they cite familiar sources – Clive Brasier, Peter Vitousek, Juliann Aukema, Gary Lovett, Sandy Liebhold, Kerry Britton, Bitty Roy, Hanno Seebens – regarding surges in pest attacks; the growing diversity of damaging pests; resulting changes in forest species composition and structure that impede ecosystem functions and productivity. Singh et al. follow these sources in calling for improved hygiene in nurseries, adoption of scientific silvicultural practices reducing physical damage to the vegetation, selection of genotypes that are resistant, and reinforcing national and international policies on quarantine and biosecurity measures to minimize pest impacts in the future. They also mention adoption of remote sensing technologies to detect the trees under stress and use of sentinel plantings. They list the 10 most important international agreements dealing with invasive species issues as the International Plant Protection Convention, Ramsar Convention, Convention on International Trade in Endangered Species of Wild Fauna and Flora, Convention on Migratory Species, Convention on Biological Diversity and its Cartagena Protocol on Biosafety, IUCN Invasive Species Specialist Group, World Trade Organization Agreement on Sanitary and Phytosanitary Measures, Global Invasive Species Program, and International Civil Aviation Organization, and Cartagena.

slash and burn agriculture in Bolivia; photo Neil Palmer

Threats to forests: Development Projects

Singh et al. consider development projects to be the third threat to forest conservation. Their roads, powerlines, and other linear developments cause habitat loss and fragment landscapes. In their view, environmental impact assessments and other similar requirements are not yet sufficient to safeguard sustainable use of forest resources.

Policy Responses

Singh et al. call for more inclusive forest management structures to respond to the threat climate change poses to forests, industries, and forest-dependent communities. They all for partnerships that bring together researchers from several disciplines with forest managers and local stakeholders. Geoffrey M. Williams and others (including me) advocate for similar conservation approaches. (See pre-print here.)

In this context, Singh et al. mention several reports, plans, and agreements aimed at global forest conservation. Participants in global fora have recognized the importance of forests in contributing to food security and sustainable development. Among agreements mentioned are the UN’s Strategic Plan for Forests 2030 and recommendations of the International Institute for Sustainable Development (IISD) published in 1994. The former tries to generate greater coherence, collaboration, and synergy across UN programs aimed at encouraging volunteer forest conservation by countries, international, regional, and local organizations, partners, and stakeholders. Unfortunately, they do not discuss the extent to which the 30-year old IISD recommendations have – or have not – been implemented.

They also describe Forest Landscape Restoration as an effective strategy to restore the functionality of forests.Again, the focus is on a collaborative approach aimed at integrating efforts by all forestry-related stakeholders, e.g., scientific and academic organizations, local communities, indigenous peoples, and private sectors, including forest-based enterprises and NGOs.

Also praised is rising attention to trees outside forest. This includes fostering use of trees in agroforestry systems ranging from home gardens to farm forestry systems, shelterbelts, and woodlots. This approach helps to sustain the livelihoods of rural communities and maintain a stable and secure food supply. Meanwhile, it reduces dependence on natural forests

Singh et al. say community forest management and decentralized governance have gained acceptance. They describe examples from Gambia and Rwanda. They concede that such decentralization has its own risks and challenges. For example, e the most marginalized sections of the community must be ensured adequate capacity for robust conflict resolution.

Singh et al. advocate that all nations seek to increase their forest cover; affluent countries that are hampered by physical and climatic conditions should aid poorer nations in increasing and upgrading their forest cover. They suggest “recognition” and encouragement of countries that maintain forest cover above 30% of territory.

See also about loss of floral diversity and blog about IUCN’s global forest assessment.

SOURCE

Singh, M., N.N. Shahina, S. Das, A. Arshad, S. Siril, D. Barman, U. Mog, P. Panwar, G. Shukla, and S. Chakravarty. 2022. Forest Resources of the World: Present Status and Future Prospects. In Panwar, P., G. Shukla, J.A. Bhat, S. Chakravarty. 2022. Editors. Land Degradation Neutrality: Achieving SDG 15 by Forest Management; ISBN 978-981-19-5477-1 ISBN 978-981-19-5478-8 (eBook)

https://doi.org/10.1007/978-981-19-5478-8

Posted by Faith Campbell

www.fadingforests.org

A Forest without Big Trees — Which Animals Will be Decimated?

In an earlier blog about tree extinctions, I commented that less drastic impacts by pests can also be important. I mentioned specifically that clumps of beech root sprouts cannot duplicate the quantities of nuts and cavities provided by mature beech trees.

This thought prompted me to search for information about use of tree cavities by wildlife. The articles I have found are decades old and largely focus on implications for management of forests for timber. Timber production conflicts with a goal of ensuring the presence of large (“overmature”), trees, especially those with dead branches, and completely dead trees (“snags”). These articles were written too long ago to address the possible impacts of non-native insects and pathogens – although there is some discussion of widespread mortality of pines caused by the mountain pine beetle.

These sources make clear that species that make cavities are keystone species. Many other wildlife species depend on them — birds, bats and terrestrial animals – mammals and herps. Furthermore, these cavity-associated species require forests with significant numbers of large, old, declining trees. When non-native insects or pathogens kill those trees, there might be a short-term bonanza of dying trees – suitable for nesting and foraging; and wood-feeding insects to provide food. But afterwards – for decades or longer – there will probably be small-diameter trees, and different species. Can the cavity-dependent species find habitat or food under these circumstances?

[By coincidence, the PBS program “Nature” broadcast an episode on woodpeckers on the 2^nd of November! The title is “The Hole Story”. ]

Cavities provide a variety of habitats for many species – including some not usually thought of as “forest” species. Among the 85 North American bird species identified by Scott et al. as associated with cavities are seven species of ducks, two vultures, three falcons, 12 owls, two swifts, six flycatchers, two swallows, purple martin, seven chickadees, three titmice, four nuthatches, brown creeper, five wrens, three bluebirds, and two warblers. They point out that the majority of these birds are insectivores. Woodpeckers are especially important predators of tree-killing bark beetles.

Goodburn and Lorimer found that more than 40 species of birds and mammals in hardwood forests of Wisconsin and Michigan use cavities in snags and dead portions of live trees for nest sites, dens, escape cover, and winter shelter. Bunnell reported that 67 vertebrate species commonly use cavities in the Pacific Northwest. Chepps et al., Daily et al., and Wiggins focus on specific species in the Rocky Mountains. (Full citations for all sources are at the end of the blog.)

While Scott et al. (published in 1977) do not address the impact of non-native pests, their profiles of individual bird species sometimes name specific types of trees favored. Several of these tree taxa have been decimated by such non-native pests, or face such attack in the near future. Thus, concern appears warranted for:

pileated woodpecker; photo by Jo Zimni via Flickr

birds nesting in American elm, including two that are quite large so they require large trees to accommodate their nests: common goldeneye (a duck) and pileated woodpecker (larger than a crow).
the pileated woodpecker also nests in ash and beech and here
the yellow-bellied sapsucker nests in butternut.

How many species depended on American chestnut, which – before the blight — grew to diameters up to 5 feet, heights of 70 to 100 feet, and had hollow centers (USDA 2022)?

In the West, some nesting tree species are under imminent threat from invasive shot hole borers, goldspotted oak borer, or sudden oak death. Detection of the emerald ash borer in Oregon portends a longer-term threat. Birds likely to feel these impacts include the acorn woodpecker, ash-throated flycatcher, and purple martin. The golden-fronted woodpecker is associated with oaks in parts of Texas where oak wilt is severely affecting live oaks.

ash-throated flycatcher; photo by Mick Thompson via Flickr

At the beginning of the 21^st Century – before widespread mortality caused by the emerald ash borer — densities of snags in the managed forests in the Lake States were apparently already insufficient to sustain population densities of cavity nesting birds. Pileated woodpeckers and chimney swifts both prefer snags greater than 50 cm dbh, which are significantly less abundant in harvested stands. For six of eight bird species studied, the number of breeding pairs was significantly higher in old-growth northern hardwood stands than in those under management (Goodburn and Lorimer).

Strong Primary Excavators are Keystone Species

Cavity nesters are commonly divided into:

1) primary excavators that excavate their own cavities. These are further divided into strong excavators – those species that forage by drilling, boring, or hammering into wood or soil; and weak excavators – those species that probe or glean bark, branches, and leaves to acquire prey.

2) secondary cavity users, that use holes made by primary cavity excavators (Bunnell).

Strong primary excavators tend to be large, e.g., most woodpeckers, sapsuckers, and the northern flicker. Weak excavators are mostly smaller species, such as chickadees and nuthatches; plus those woodpeckers that forage primarily by probing and gleaning, extracting seeds, or capturing insects in flight [e.g., acorn woodpecker (Melanerpes formicivorus), downy woodpecker (Picoides pubescens)] (Bunnell).

Bunnell considers strong excavators to be keystone species because so many other cavity users depend on them. Their loss would seriously disrupt forest ecosystems. For example, in the Pacific Northwest, only nine of 22 avian primary excavators are strong excavators. Another 45 species are secondary cavity users. These include waterfowl, tree swallows, and some mammals such as flying squirrels. Some cavity nesters support an even wider group of species: in the Pacific Northwest, at least 23 bird species, six mammal species, and numerous arthropods (nine orders and 22 families) feed on sap and insects collected at holes drilled by sapsuckers (Bunnell). [I discuss sapsuckers’ ecosystem role in greater detail later.]

Tree Characteristics

There is general agreement that animals dependent on tree cavities “prefer” (actually, require) trees that are large – tall, of large circumference, and sturdy – while having decayed interiors.

Size:

As Bunnell notes, larger snags provide more room and tend to stand longer without breaking, so they provide greater opportunities for cavity use. They also tend to be taller, so they offer higher nest sites that provide better protection from ground-dwelling predators. While larger-diameter trees remain standing longer regardless of the cause of mortality, snags created by fire usually fall sooner than do other snags. Beetle-killed trees are more attractive to cavity nesters that tend to excavate nest sites in trees on which they have foraged.

In the upper Midwest, cavity trees were a scare resource, even in unmanaged forests. Mean diameters for live cavity trees were twice as large as the mean diameter of the live trees in stands under a management regime. Such larger-diameter snags were more numerous in old-growth than in managed stands, especially in mixed hemlock-hardwood stands (Goodburn and Lorimer).

The Importance of Decay

Excavating a cavity demands considerable energy, so birds seek sites where a fungal infection has softened the interior wood. The exterior wood must remain strong to prevent collapse of the nest. These rots take time to develop, so they appear more often in older, even dying, trees. Bunnell, Scott et al., Chepps et al., and Goodburn and Lorimer all emphasize the role of decay in providing suitable cavity sites. Chepps et al. compared the aspen trees used by four species of cavity-nesting birds in central Arizona. Not only were nest trees softer than neighboring trees; they were softer at the spot where the nests were excavated than at other heights. [Spring (1965) provides a fun discussion of different species’ adaptations to the energy demands of hard pecking and climbing vertical trunks.]

Live v. Dead Trees

However, the need for decay does not necessarily mean birds prefer dead trees. Goodburn and Lorimer found that in Wisconsin and Michigan, a large percentage of all cavities found were in live trees.

Bunnell found that strong excavators select trees with less visible signs of decay. Where possible, secondary users will also use live trees. However, intense competition often forces them to use dead trees.

Hardwoods v. Conifers

Bunnell states that deciduous trees more often contain internal rot surrounded by a sound outer shell than do conifers (at least this is true in the Pacific Northwest). He found that cavity nesters chose hardwoods for 80–95% of their nest sites even where hardwoods comprised only 5–15% of the available tree stems. He concluded that availability of living hardwoods had a significant influence on strong excavators in the West, although probably was less important in hardwood stands in the East.

Taxa Dependent on Other Types of Cavity

Some species depend on cavities created by forces other than bird excavations, such as decay or fire. These include most of the mammals, especially the larger ones e.g., American martens, fishers, porcupines, and black bears. These natural cavities are often uncommon. Vaux’s swifts nest and roost in hollow snags large enough that they can fly in a spiral formation to enter and leave (Bunnell).

little brown bat *Myotis* sp. photo by S.M. Bishop via Wikimedia Commons

Bats are a special case. Bats are unique among mammals of their size in having long lives, low reproductive rates, and relatively long periods of infant dependency. They also play a key ecological role as the major predators of nocturnal flying insects (van den Driesche 1999). Also many species are in perilous conservation status: half of the 16 bat species in British Columbia were listed as threatened or endangered as of 1998 (van den Driesche). This was before the deadly disease whitenose syndrome had been detected in North America.

Bats require larger trees. In the Pacific Northwest at least, that choice often means conifers (Bunnell). Roosts are difficult to find, so samples are small. A study on the west coast of Vancouver Island (van den Driessche), located only nine roosts despite searching during three summers. Five roosts were in large-diameter (old) western red cedar, with dead tops and extensive cracks.

Brown creepers and some amphibians and reptiles nest or seek cover under slabs of loose bark, which are typically found on dead or dying trees. The same large, mature and old-growth conifer trees also provide preferred foraging habitat, since there is a higher density of arthropod prey on their deeply furrowed bark. While Wiggins (2005) studied bird populations in the Rocky Mountains, he cited studies in the eastern United States, specifically in the Blue Ridge and Allegheny mountains, that have found similar results. Goodburn and Lorimer found that in National forests in Wisconsin and Michigan, only 15% of trees consisted of the necessary snags with loose bark plates. Suitable trees were most frequent old-growth hemlock-hardwood stands, and on larger-diameter snags. A high proportion of the snags with loose bark were yellow birch (Betula alleghaniensis).

Importance of foraging sites

As Bunnell points out, a bird must feed itself before it can nest. Foraging trees and snags are usually smaller than nesting trees. Furthermore, birds need many more foraging sites than nesting sites. The situation perhaps most pertinent to our usual focus on invasive pests concerns bird species’ response to mountain pine beetle outbreaks. Red-breasted nuthatches and mountain chickadees increasing dramatically in apparent response to the beetle epidemic. When most of the conifers had been killed, and numbers of beetles diminished, numbers of these bird species also declined–despite the increased availability of conifer snags for nesting. Indeed, the birds continued to nest primarily in aspen during the epidemic.

Bunnell reiterates that snags of all sizes are needed; they provide perching, foraging, and hawking sites for bird species beyond cavity nesters as well as sustenance for bryophytes, insects, and terrestrial breeding salamanders. He says more than 200 studies reported harvesting of standing dead trees in beetle-killed forests had negative effects on bird, mammal, and fish species.

Other Dependencies – Food Sources

yellow-bellied flycather; photo by Dennis Church via Flickr

A few studies looked at the role of cavity-creating birds in providing food sources. The focus was on sapsuckers. They drill sapwells into trees’ phloem; sap flowing into these wells attracts many other species. In Michigan, Rissler determined that yellow-bellied sapsuckers’ sapwells attracted insects in seven orders and 20 families, especially Coleoptera, Diptera (other than Tephritidae), bald-faced hornets, and Lepidoptera. Daily et al. (1993) cites other studies showing that ruby throat and rufous hummingbirds have extended their breeding ranges by relying on these sapwells for nutrition in early spring before flowers open. [The “Nature” program covers this behavior.]

In a subalpine ecosystem in Colorado, Daily et al. found that red-naped sapsuckers support other species in two ways. First, they excavate nest cavities in fungus-infected aspens that are utilized by at least seven secondary cavity nesting bird species. When they feed, they drill sapwells that nourish more than 40 species – including hummingbirds, warblers, and chipmunks. Daily et al. called this a keystone species complex comprised of sapsuckers, willows, aspens, and a heartwood fungus. Disappearance of any element of the complex could cause an unanticipated unraveling of the community.

Goodburn and Lorimer looked at the availability of downed wood but did not discuss the implications of the presence of only small-diameter coarse woody debris.

Efforts to Accommodate Biodiversity Needs

Scott et al. reported in 1977 that the USDA Forest Service had required staff at regional and National Forest levels to develop snag retention policies. Twenty years later, Goodburn and Lorimer noted that Forest Service management guidelines for some Wisconsin and Michigan National forests since the early 1980s have called for the retention of all active cavity trees and 5-10 snags (larger than 30 cm dbh)/ha. However, as I noted above, they fear that these recommended snag retention levels might still be too limited to support cavity nesters. They found that two species that prefer snags greater than 50 cm dbh, pileated woodpeckers and chimney swifts, were significantly more abundant in old-growth than in selection stands. Furthermore, the number of breeding pairs of six species was at least 30% higher in old-growth northern hardwood than in selection stands and more than 85% higher in selection cuts than even-aged.

Goodburn and Lorimer cited others’ findings that removal of some live timber and snags in an Arizona ponderosa pine forest reduced cavity-nesting bird populations by 50%. Species affected were primarily violet-green swallows, pygmy nuthatches, and northern three-toed woodpeckers.

Female mountain bluebird by Jacob W. Frank. Original public domain image from Flickr

As I noted, none of these experts has addressed the impacts of wide-spread pest-caused tree mortality. If I may speculate, it seems likely that when the first wave of mortality sweeps through a forest, the result might be an expansion of both nesting opportunities (in dead or dying trees) and food availability for those that feed on wood borers. These would probably be more plentiful even in trees killed by pathogens or nematodes. Sapsuckers and those that depend on them might experience an immediate decline in sap sources. Over the longer term it seems likely that all cavity-dependent species will confront a much lower supply of large mature trees. I note that many deciduous/hardwood tree species are being affected by introduced pests.

Are there current studies in Michigan, where so many ash have died?

SOURCES

Bunnell, F.L. 2013. Sustaining Cavity-Using Species: Patterns of Cavity Use and Implications to Forest Management. Hindawi Publishing Corporation. ISRN Forestry. Volume 2013, Article ID 457698

Chepps, J., S. Lohr, and T.E. Martin. 1999. Does Tree Hardness Influence Nest-Tree Selection by Primary Cavity Nesters? The Auk 116(3):658-665, 1999

Daily, G.C., P.R. Ehrlich, and N.M. Haddad. 1993. Double keystone bird in a keystone species complex. Proc. Natl. Acad. Sci. USA Vol. 90, pp. 592-594, January 1993 Ecology

Goodburn, J.M. and C.G. Lorimer. 1998. Cavity trees and coarse woody debris in old-growth and managed northern hardwood forests in Wisconsin and Michigan. Can. For. Res. 28: 427.438 (1998)

Rissler, L.J., D.N. Karowe, F. Cuthbert, B. Scholtens. 1995. Wilson Bull., 107(4), 1995, pp. 746-752

Spring, L.W. 1965. Climbing and Pecking Adaptations in Some North American Woodpeckers.

Scott, V.E., K.E. Evans, D.R. Patton, C.P. Stone. 1977. Cavity-Nesting Birds of North American Forests. Agriculture Handbook 511 USDA Forest Service. https://www.gutenberg.org/files/49172/49172-h/49172-h.htm

United States Department of Agriculture, Animal and Plant Health Inspection Service. Draft Enviromental Impact Statement. 2022. State University of New York College of Enviromental Science and Forestry Petition (19-309-01p) for Determination of Nonregulated Status for Blight-Tolerant Darling 58 c’nut (Castanea dentata)

van den Driessche, R., M. Mather, T. Chatwin. 1999. Habitat use by bats in temperate old-growth forests, Clayoquot Sound, British Columbia

Wiggins, D.A. (2005, January 27). Brown Creeper (Certhia americana): a technical conservation assessment. [Online]. USDA Forest Service, Rocky Mountain Region. Available: http://www.fs.fed.us/r2/projects/scp/assessments/browncreeper.pdf [date of access].

Posted by Faith Campbell

www.fadingforests.org

Australia Builds Capacity to Address Forest Pests

Australian Eucalypts; photo by John Turnbull via Flickr

I congratulate Australian scientists for bringing about substantial improvements of their country’s biosecurity program for forest pests. While it is too early to know how effective the changes will be in preventing new introductions, they are promising. What can we Americans learn from the Australian efforts? [I have previously praised South Africa’s efforts – there is much to learn there, too.]

Australia has a reputation of being very active in managing the invasive species threat. However, until recently biosecurity programs targetting forest pests were minimal and ad hoc. Scientists spent 30 years trying to close those gaps (Carnegie et al. 2022). Their efforts included publishing several reports or publications (listed at the end of the blog) and an international webinar on myrtle rust. Scientists are hopeful that the new early detection program (described below) will greatly enhance forest protection. However, thorough pest risk assessments are still not routinely conducted for forest pests. (Nahrung and Carnegie 2022).

The native flora of Australia is unique. That uniqueness has provided protection because fewer of the non-native insects and pathogens familiar to us in the Northern Hemisphere have found suitable hosts (Nahrung and Carnegie 2020). Also – I would argue – the uniqueness of this flora imposes a special responsibility to protect it from threats that do arise.

Only 17% of Australia’s landmass is covered by forests. Australia is large, however; consequently, these forests cover 134 million hectares (Nahrung and Carnegie 2020). This is the 7th largest forest estate in the world (Carnegie et al. 2022).

Australia’s forests are dominated by eucalypts (Eucalyptus, Corymbia and Angophora). These cover 101 million ha; or 75% of the forest). Acacia (11 million ha; 8%); and Melaleuca (6 million ha) are also significant. The forest also includes one million ha of plantations dominated by Pinus species native to North America (Carnegie et al. 2022). A wide range of native and exotic genera have been planted as amenity trees in urban and peri-urban areas, including pines, sycamores, poplars, oaks, and elms (Carnegie et al. 2022). These urban trees are highly valued for their ecosystem services as well as social, cultural, and property values (Nahrung and Carnegie 2020). Of course, these exotic trees can support establishment and spread of the forest pest species familiar to us in the Northern Hemisphere. On the positive side, they can also be used as sentinel plantings for early detection of non-native species (Carnegie et al. 2022 and Nahrung and Carnegie 2020).

Despite Australia’s geographic isolation, its unique native flora, and what is widely considered to be one of the world’s most robust biosecurity system, at least 260 non-native arthropods and pathogens of forests have established in Australia since 1885 (Nahrung and Carnegie 2020). [(This number is about half the number of non-native forest insects and pathogens that have established in the United States over a period just 25 years longer (Aukema et al. 2010).] As I noted, forest scientists have cited these introductions as a reason to strengthen Australia’s biosecurity system specifically as it applies to forest pests.

What steps have been taken to address this onslaught? For which pests? With what impacts? What gaps have been identified?

Which Pests?

Nahrung and Carnegie (2020) compiled the first comprehensive database of tree and forest pests established in Australia. The 260 species of non-native forest insect pests and pathogens comprise 143 arthropods, 117 pathogens. Nineteen of them (17 insects and 2 fungal species) had been detected before 1900. These species have accumulated at an overall rate of 1.9 species per year; the rate of accumulation after 1955 is slightly higher than during the earlier period, but it has not grown at the exponential rate of import volumes.

While over the entire period insects and pathogens were detected at an almost equal rate (insects at 1.1/year; pathogens at 0.9/year), this disguises an interesting disparity: half of the arthropods were detected before 1940; half of the pathogens after 1960 (Nahrung and Carnegie (2020). By 2022, Nahrung and Carnegie (2022) said that, on average, one new forest insect is introduced each year. Some of these recently detected organisms have probably been established for years. More robust surveillance has just detected them recently. I have blogged often about an apparent explosion of pathogens being transported globally in recent decades.

In a more recent article (Nahrung and Carnegie, 2022), gave 135 as the number of non-native forest insect pests. The authors don’t explain why this differs from the 143 arthropods listed before.

damage to pine plantations caused by *Sirex noctilio*; photo courtesy of Helen Nahrung

Eighty-seven percent of the established alien arthropods are associated with non-native hosts (e.g., Pinus, Platanus, Populus, Quercus, Ulmus) (Carnegie et al. 2022). Some of these have escaped eradication attempts and caused financial impact to commercial plantations (e.g., sirex wood wasp, Sirex noctilio) and amenity forests (e.g., elm leaf beetle, Xanthogaleruca luteola) (Carnegie and Nahrung 2019).

About 40% of the alien arthropods were largely cosmopolitan at the time of their introduction in Australia (Carnegie et al. 2022). Only six insects and six fungal species are not recorded as invasive elsewhere (Nahrung and Carnegie 2020). Of the species not yet established, 91% of interceptions from 2003 to- 2016 were known to be invasive elsewhere. There is strong evidence of the bridgehead effect: 95% of interceptions of three species were from their invaded range (Nahrung and Carnegie 2022). These included most of the insects detected in shipments from North America, Europe and New Zealand. These ubiquitous “superinvaders” have been circulating in trade for decades and continue to be intercepted at Australia’s borders. This situation suggests that higher interception rates of these species reflect their invasion success rather than predict it (Nahrung and Carnegie 2021).

I find it alarming that most species detected in shipments from Africa, South America, and New Zealand were of species not even recorded as established in those regions (Nahrung and Carnegie 2021; Nahrung and Carnegie 2022).

*Arhopalus ferus*, a Eurasian pine insect often detected in wood from New Zealand; photo by Jon Sullivan – in New Zealand; via Flickr

Half of the alien forest pests established in Australia are highly polyphagous. This includes 73% of Asian-origin pests but only 15% of those from Europe (Nahrung and Carnegie 2021). Nahrung and Carnegie (2022) confirm that polyphagous species are more likely to be detected during border inspections.

PATHWAYS

As in North America and Europe, introductions of Hemiptera are overwhelmingly (98%) associated with fresh plant material (e.g. nursery stock, fruit, foliage). Coleoptera introductions are predominantly (64%) associated with wood (e.g. packaging, timber, furniture, and artefacts). Both pathways are subject to strict regulations by Australia (Nahrung and Carnegie 2021).

Eradication of High-Priority Pests

Eight-five percent of all new detections were not considered high-priority risks. Of the four that were, two had not previously been recognized as threats (Carnegie and Nahrung 2019). One high-priority pest – expected to pose a severe threat to at least some of Australia’s endemic plant species – is myrtle rust, Austropuccinia psidii. Despite this designation, when the rust appeared in Australia in 2010, the response was confused and ended in an early decision that eradication was impossible. Myrtle rust has now spread along the continent’s east coast, with localized distribution in Victoria, Tasmania, the Northern Territory, and – in 2022, Western Australia. `

*Melaleuca quinquenervia* forest; photo by Doug Beckers via Wikimedia

There have been significant impacts to native plant communities. Several reviews of the emergency response criticized the haste with which the initial decision was made to end eradication (Carnegie and Nahrung 2019). (A review of these impacts is here; unfortunately, it is behind a paywall.)

A second newly introduced species has been recognized as a significant threat, but only after its introduction to offshore islands. This is Erythina gall wasp Quadrastichus erythrinae (Carnegie and Nahrung 2019). DMF Although Australia is home to at least one native species in the Erythrina genus, E. vespertilio,, the gall wasp is not included on the environmental pest watch list.

Four of the recently detected species were considered to be high impact. Therefore eradication was attempted. Unfortunately, these attempts failed in three cases. The single success involved a pinewood nematode, Bursaphelenchus hunanesis. See Nahrung and Carnegie (2021) for a discussion of the reasons. This means three species recognized as high-impact pests have established in Australia over 15 years (Nahrung and Carnegie (2021). In fact, Australia’s record of successful forest pest eradications is only half the global average (Carnegie and Nahrung (2019).

Carnegie and Nahrung (2019) conclude that improving early detection strategies is key to increasing the likelihood of eradication. They discuss the strengths and weaknesses of various strategies. Non-officials (citizen scientists) reported 59% of the 260 forest pests detected (Carnegie and Nahrung 2019). Few alien pests have been detected by official surveillance (Carnegie et al 2022). However, managing citizen scientists’ reports involves a significant workload. Futhermore, surveillance by industry, while appreciated, is likely to detect only established species (Carnegie and Nahrung 2019).

Interception Frequency Is Not an Indicator of Likelihood of Establishment

Nahrung & Carnegie (2021) document that taxonomic groups already established in Australia are rarely detected at the border. Furthermore, only two species were intercepted before they were discovered to be established in Australia.

Indeed, 76% of species established in Australia were either never or rarely intercepted at the border. While more Hemiptera species are established in Australia, significantly more species of Coleoptera are intercepted at the border. Among beetles, the most-intercepted family is Bostrichid borers (powderpost beetles). Over the period 2003 – 2016, Bostrichid beetles made up 82% of interceptions in wood packaging and 44% in wood products (Nahrung and Carnegie 2022). This beetle family is not considered a quarantine concern by either Australian or American phytosanitary officials. I believe USDA APHIS does not even bother recording detections of powderpost beetles. Nahrung and Carnegie (2021) think the high proportion of Bostrichids might be partially explained by intense inspection of baggage, mail, and personal effects. While Australia actively instructs travelers not to bring in fruits and vegetables because of the pest risk, there are fewer warnings about risks associated with wood products.

Nahrung & Carnegie (2021) concluded that interception frequencies did not provide a good overall indicator of likelihood of risk of contemporaneous establishment.

Do Programs Focus on the Right Species?

Although Hemiptera comprise about a third of recent detections and establishments, and four of eight established species are causing medium-to-high impact, no Hemiptera are currently listed as high priority forestry pests by Australian phytosanitary agencies (Nahrung & Carnegie (2021). On the other hand, Lepidoptera make up about a third of the high-priority species, yet only two have established in Australia over 130 years. Similarly, Cerambycidae are the most frequently intercepted forest pests and several are listed as high risk. But only three forest-related species have established (Nahrung and Carnegie 2020). (Note discussion of Bostrichidae above.).

Unlike the transcontinental exchanges under way in the Northern Hemisphere, none of the established beetles is from Asia; all are native to Europe. This is especially striking since interceptions from Asia-Pacific areas account for more than half of all interceptions Nahrung and Carnegie (2021).

Interestingly, 32 Australian Lepidopteran and eight Cerambycid species are considered pests in New Zealand. However, no forest pests native to New Zealand have established in Australia despite high levels of trade, geographic proximity, and the high number of shared exotic tree forest species (Nahrung and Carnegie 2020).

STRUCTURE OF PROGRAM

The structure of Australia’s plant biosecurity system is described in detail in Carnegie et al. (2022). These authors call the program “comprehensive” but to me it looks highly fragmented. The federal Department of Agriculture and Water Resources (DAWR,[recently renamed the Department of Agriculture, Fisheries, and Forestry, or DAFF) is responsible for pre-border (e.g., off-shore compliance) and border (e.g., import inspection) activities. The seven state governments, along with DAFF, are responsible for surveillance within the country, management of pest incursions, and regulation of pests. Once an alien pest has become established, its management becomes the responsibility of the land manager. In Australia, then, biosecurity is considered to be a responsibility shared between governments, industry and individuals.

Even this fragmented approach was developed more recently than one might expect given Australia’s reputation for having a stringent biosecurity system. Perhaps this reflects the earlier worldwide neglect of the Plant Kingdom? Carnegie and Nahrung (2019) describe recent improvements. Until the year 2000, Australia’s response to the detection of exotic plant pests was primarily case-by-case. In that year Plant Health Australia (PHA) was incorporated. Its purpose was to facilitate preparedness and response arrangements between governments and industry for plant pests. In 2005, the Emergency Plant Pest Response Deed (EPPRD) was created. It is a legally-binding agreement between the federal, state, and territorial governments and plant industry bodies. As of 2022, 38 were engaged. It sets up a process to implement management and funding of agreed responses to the detection of exotic plant pests – including cost-sharing and owner reimbursement. A national response plan (PLANTPLAN) provides management guidelines and outlines procedures, roles and responsibilities for all parties. A national committee (Consultative Committee on Emergency Plant Pests (CCEPP) works with surveys to determine invaded areas (delimitation surveys) and other data to determine whether eradicating the pest is technically feasible and has higher economic benefits than costs..

*Austropuccinia psidii* on *Melaleuca quinquenervia*; photo by John Tann via Flickr

Even after creation of EPPRD in 2005, studies revealed significant gaps in Australia’s post-border forest biosecurity systems regarding forest pests (Carnegie et al. 2022; Carnegie and Nahrung 2019). These studies – and the disappointing response to the arrival of myrtle rust – led to development of the National Forest Biosecurity Surveillance Strategy (NFBSS) – published in 2018; accompanied by an Implementation Plan. A National Forest Biosecurity Coordinator was appointed.

The forest sector is funding a significant proportion of the proposed activities for the next five years; extension is probable. Drs. Carnegie and Nahrung are pleased that the national surveillance program has been established. It includes specific surveillance at high-risk sites and training of stakeholders who can be additional eyes on the ground. The Australian Forest Products Association has appointed a biosecurity manager (pers. comm.)

This mechanism is expected to ensure that current and future needs of the plant biosecurity system can be mutually agreed on, issues identified, and solutions found. Plant Health Australia’s independence and impartiality allow the company to put the interests of the plant biosecurity system first. It also supports a longer-term perspective (Carnegie et al. (2022). Leading natural resource management organizations are also engaged (Carnegie, pers. comm.).

Presumably the forest surveillance strategy (NFBSS) structure is intended to address the following problems (Carnegie and Nahrung 2019):

Alien forest pests are monitored offshore and at the border, but post-border surveillance is less structured and poorly resourced. Australia still lacks a surveillance strategy for environmental pests.
Several plant industries have developed their own biosecurity programs, co-funded by the government. These include the National Forest Biosecurity Surveillance Strategy (NFBSS).

Some pilot projects targetting high risk sites were initiated in the early 2000s. By 2019, only one surveillance program remained — trapping for Asian spongy (gypsy) moth.

The states of Victoria and New South Wales have set up sentinel site programs. Victoria’s uses local council tree databases. It is apparently focused on urban trees and is primarily pest-specific – e.g., Dutch elm disease. The New South Wales program monitors more than 1,500 sentinel trees and traps insects near ports. This program is funded by a single forest grower through 2022.

Dr. Carnegie states: “With the start of the national forest biosecurity surveillance program in December 2022, the issues and gaps identified by Carnegie et al. 2022 are starting to be addressed. The program will conduct biosecurity surveillance specifically for forest pests and pathogens and be integrated with national and state biosecurity activities. While biosecurity in Australia is still agri-centric, a concerted and sustained effort from technical experts from the forest industry is changing this. And finally, the new Biosecurity Levy should ensure sustained funding for biosecurity surveillance.”

There is a separate National Environmental Biosecurity Response Agreement (NEBRA), adopted in 2012. It is intended to provide guidelines for responding, cost-sharing arrangements, etc. when the alien pest threatens predominantly the environment or public amenity assets (Carnegie et al. (2022). However, when the polyphagous shot hole borer was detected, the system didn’t work as might have been expected. While PSHB had previously been identified as an environmental priority pest, specifically to Acacia, the decision whether to engage was made under auspices of the the Emergency Plant Pest Response Deed (EPPRD) rather than the environmental agreement (NEBRA). As a result, stakeholders focused on environmental, amenity and indigenous concerns had no formal representation in decision-making processes; instead, industries that had assessed the species as a low priority (e.g., avocado and plantation forestry) did (Nahrung, pers.comm.).

Additional Issues Needing Attention

Some needs are not addressed by the National Forest Pest Strategic Plan (Carnegie et al. 2022) (Nahrung, pers. comm.):

1) The long-term strategic investment from the commercial forestry sector and government needed to maintain surveillance and diagnostic expertise;

2) Studies to assess social acceptance of response and eradication activities such as tree removal;

3) Studies to improve pest risk prioritization and assessment methods; and

4) Resolving the biosecurity responsibilities for pests of timber that has been cut and used in construction.

In 2019, Carnegie and Nahrung (2019) called for developing more effective methods of detection, especially of Hemiptera and pathogens. They also promoted national standardization of data collection. Finally, they advocated inclusion of technical experts from state governments, research organizations and industry in developing and implementing responses to pest incursions. They note that surveillance and management programs must be prepared to expect and respond to the unexpected since 85% of the pests detected over the last 20 years—and 75% of subsequently mid-to high-impact species established—were not on high-priority pest list. See Nahrung and Carnegie 2022 for a thorough discussion of the usefulness and weaknesses of predictive pest listing.

SOURCES

Aukema, J.E., D.G. McCullough, B. Von Holle, A.M. Liebhold, K. Britton, & S.J. Frankel. 2010. Historical Accumulation of Nonindigenous Forest Pests in the Continental United States. Bioscience. December 2010 / Vol. 60 No. 11

Carnegie A.J. and H.F. Nahrung. 2019. Post-Border Forest Biosecurity in AU: Response to Recent Exotic Detections, Current Surveillance and Ongoing Needs. Forests 2019, 10, 336; doi:10.3390/f10040336 www.mdpi.com/journal/forests

Carnegie A.J., F. Tovar, S. Collins, S.A. Lawson, and H.F. Nahrung. 2022. A Coordinated, Risk-Based, National Forest Biosecurity Surveillance Program for AU Forests. Front. For. Glob. Change 4:756885. doi: 10.3389/ffgc.2021.756885

Nahrung H.F. and A.J. Carnegie. 2020. NIS Forest Insects and Pathogens in Australia: Establishmebt, Spread, and Impact. Frontiers in Forests and Global Change 3:37. doi: 10.3389/ffgc.2020.00037 March 2020 | Volume 3 | Article 37

Nahrung, H.F. and A.J. Carnegie. 2021. Border interceps of forest insects estab in AU: intercepted invaders travel early and often. NeoBiota 64: 69–86. https://doi.org/10.3897/neobiota.64.60424

Nahrung, H.F. & A.J. Carnegie. 2022. Predicting Forest Pest Threats in Australia: Are Risk Lists Worth the Paper they’re Written on? Global Biosecurity, 2022; 4(1).

Posted by Faith Campbell

www.fadingforests.org

We Need Analyses of Pest Approach Rates, but Detection Data Are Not Adequate Basis

plants for sale in UK; Evelyn Grimak via Geograph what pests could be here?

There has recently been a series of studies trying to use port detection data to determine which types of insects are most likely to arrive and possibly establish in the country. These studies – and related sources – are listed at the end of this blog. Some of the studies focus on the U.S. experience, but not all. Their – and my – conclusions are meant to be relevant around the globe.

I agree with Nahrung et al. (2022) as a correct definition of the problem:

“… despite decades of research on and implementation of [biosecurity] measures, insect invasions continue to occur with no evidence of saturation, and are even predicted to accelerate.”

I also think the issue they raise applies more broadly. As these experts point out, forest pests have received considerable attention, are the subject of a specific international regulation (ISPM#15), and the pest risks to a range of forests is relatively well understood and appreciated. So what does failing to control this group of pests – as I say the international phytosanitary system is – imply for other pests and pathways?

I appreciate these experts’ efforts to improve the many elements of excluding pests: prediction, pest risk analysis, targeted phytosanitary measures, enforcement actions, and early detection. However, we have a long way to go before we can confidently apply port data to determine pest approach rates as well as the efficacy of phytosanitary measures.

Problems with the Quality of the Port Detection Data

There is general agreement that detection data are not a reliable indicator of the true pest approach / arrival rate. Even Turner et al. (2022) – who titled their article “Worldwide border interceptions provide a window …” — concede this, although they try to find ways to apply the detection data anyway. According to pages 2 and 15 of Turner et al., true arrival rates of potentially invading species are usually difficult to estimate and probably exceed the number reported in the article. Allison et al. (2021) agree.

Turner et al. and Nahrung & Carnegie both note that many insect species established in the destination country are never or rarely detected. Turner et al. cite as an example spotted lanternfly, Lycorma delicatula, which appeared only once out of almost 1.9 million interceptions recorded in the combined global data. Nahrung & Carnegie note that 76% of species established in Australia were either never or rarely intercepted at the border.

Turner et al. explain that interception frequencies are a function of both the true arrival rates and the probability of (1) being detected during inspections (which depends on how these are carried out) and (2) being recorded. They say the data are more reliable when they report detections at the family-level. . The authors call on countries to base port inspections on a statistically based sampling program that would better reflect pest approach rates than do data biased by inspection priorities.

The issue of data quality might be broader. Certain kinds of pests travelling in certain types of imports might be sufficiently cryptic as to be rarely detected by even the best border inspections. Liebhold et al. (2012) found that APHIS inspectors detected actionable pests in only 2.6% of incoming shipments of plants, whereas a statistically valid audit determined that the actual approach rate was 12%. It is probable that many pests are never or rarely reported in official port detection data.

See a thorough discussion of the issues undermining use of interception data in Nahrung and Carnegie 2022, cited at the end of this blog.

Problems Due to Narrow Taxonomic Range of Pests Studied

Protection of our forests requires preventing introductions of many taxonomic groups, e.g., nematodes, fungal and other pathogens, viruses, and arthropods other than ambrosia beetles and Hemiptera.

I recognize that it is much more difficult to study and manage organisms other than common beetles. But the impacts of some introduced organisms in other categories have been devastating. I list some of the pathogens that have been introduced to the United States in recent decades, probably on imported plants: several Phytophthoras, ohia rust (Austropuccinia psidii), rapid ohia death (Ceratocystis lukuohia and C. huliohia), beech leaf disease, and the boxwood blight fungi. See Garbelotto and Gonthier (2022) for a thorough discussion of impacts of introduced forest pathogens.

boxwood hedge at Longwood Gardens; photo by F.T. Campbell

Points of Agreement

I agree with Nahrung et al. that:

Biosecurity successes are probably under-recognized because they are difficult to see whereas failures are more evident. They call this the “Biosecurity Paradox”: the more successful biosecurity is, the fewer new species establish so the less important it appears.
Uncertainty regarding the costs and benefits of forest border biosecurity measures appears to have led to under-regulation and wait-and-see approaches. Some recent reviews (Cuthbert et al.) show that delay substantially increases the costs associated with bioinvasion. 297https://www.nivemnic.us/?p=3209
Helping “weakest links” improve their performance is crucial. (see Geoff Williams et al.
We need to revise international and national biosecurity practices. However, my proposals differ from those cited on page 221 of Nahrung et al.; see my “Fading Forests” reports [links at end of this blog] and earlier blogs here and here. A new complication is that pathologists complain that proposed systems proposed by various invasive species experts don’t reflect realities of managing plant pathogens (Paap et al. 2022).

I wish Nahrung et al. had suggested bolder interim steps that go beyond data management and research.

I appreciate that the Canadian report on forest biosecurity (Allison et al.) notes that claiming most introduced forest pests are reported to cause no measurable impact probably reflects our ignorance. I wish others who repeat this assertion, e.g., Nahrung et al. 2022, would explore this claim’s truth more carefully.

Points of Disagreement

Customs and Border Protection officers inspecting infested pallet

I also found other statements about the efficacy of existing efforts to be too uncritical. So yes, ISPM#15 has resulted in decreased arrivals of bark- and wood-boring insects, as stated by Nahrung et al. 2022. However, the 36-52% decrease documented by Haack et al. (2014) is not sufficient to protect forests, in my view. Many publications have documented continuing introductions of damaging pests via the wood packaging pathway. For example, there have been 16 outbreaks of the Asian longhorned beetle (ALB) detected around the globe between 2012 and 2015 (Wang). Before we conclude that ISPM#15 has been a success, let’s see what the just-completed new study by Haack and colleagues shows. In addition, there has been controversy for a decade or more about what causes continuing introductions, that is, whether they result from treatment inadequacy v. sloppy application of treatments v. fraud. Why have scientists and regulators not collaborated to clarify this issue during this time?

I note – again – that many pathogens have been introduced widely over the last couple of decades. This is a global problem. My recent blogs have discussed introductions of tens of species of Phytophthora to countries around the world. Other examples include myrtle rust (Austropuccinia psidii) to 27 countries and the two causal agents of boxwood blight to at least 24 countries in Eurasia, New Zealand, and North America. Most of these species were unknown to science at the time of their introduction. Other species were known – but not believed to pose a threat because, in their native regions, their co-evolved hosts are not harmed.

*Rhodomyrtus psidioidis* in Australia killed by myrtle rust; photo by Peter Entwistle

I think Helen Nahrung (Nahrung et al.) exaggerates when she says that Australia has one of the strictest biosecurity systems in world. Several publications – some coauthored by her! – cite numerous shortfalls in applying the country’s phytosanitary programs to forest pests (Carnegie et al 2022). This latter group’s efforts have determined that at least 260 non-native arthropods and pathogens of forest hosts have established in Australia since 1885 (Nahrung and Carnegie 2020). True, this number is about half the number of non-native forest insects and pathogens that have established in the United States over a period just 25 years longer (Aukema et al. 2010). However, it is enough – and they have had sufficient impact – to prod these scientists to spend 30 years pushing for improvements.

Lessons Learned

Still, we can learn from these studies. Turner et al. compared insect interception data from nine regions over a 25-year period (1995 to 2019) – at ports in New Zealand, Australia, South Korea, Japan, Canada, mainland United States, Hawai`i, United Kingdom, and the region united under European Plant Protection Organization (EPPO) – Europe and the Mediterranean region.

They found that 174 species (2% of the total) were “superinvaders.” They were intercepted more than 100 times, and constituted 81% of all interceptions across all regions. Most of the same types of insects – even the same species – are arriving at ports around the world. The three species most frequently intercepted are all sap-feeding insects commonly associated with widely traded plants. In a separate study, Australian scientists found the same: about 40% of the alien pests detected at Australian borders were already widely introduced at the time of their introduction in Australia (Carnegie et al. 2022). The Australians report strong evidence of the bridgehead effect [that is, species being spread from locations to which they have been introduced] (Nahrung and Carnegie 2021). In fact, they conclude that higher interception rates might confirm invasion success rather than predict it.

Most of the species, however, are intercepted rarely. Turner et al. found that 75% of species reported in their nine regions were intercepted in only a single region. In fact, 44% of all species were intercepted only once (= “singletons”). Such singletons made up about half of individual species in five insect orders; the exception was Thysanoptera – 29% of those species were intercepted only once.

The 75% of all species that were intercepted in only one region included both species rarely intercepted anywhere and species intercepted numerous times – but only in that one region. The authors note that several possible factors might explain these differences. Some species are less likely to be intercepted, so it is not odd that they are detected infrequently, especially if all the regions have the same blind spots. Countries also have their unique approaches to data collection and inspection prioritization that could introduce biases in the data. Finally, countries vary in the sources of goods they import. Unfortunately, some of the data sets Turner at al. analyzed said nothing about the source country, pathway, or commodity. Consequently, they were unable to evaluate the influence of these factors.

Improving Our Understanding of the Current Risk to the U.S.

Dendrobium officinale via Wikipedia; Fusarium stilboides has been detected on this orchid in China; F. stilboides is reported to attack pine trees

As I noted in a previous blog, U.S. imports of plants have increased by more than 400% since the 1960s; 35% in just the last 15 years (MacLachlan et al. 2022). In 2011, APHIS adopted an important new policy: temporary prohibition of plant taxa determined to be “Not Authorized for Importation Pending Pest Risk Assessment” (NAPPRA). Now we have a decade of experience with NAPPRA. Given that, and because the “plants for planting” pathway is among the most risky, APHIS should update the Liebhold et al. 2012 study to determine the current approach rate for all types of organisms that threaten North American tree species. Unlike the previous study, the update should include trees on Hawai`i, Guam, Puerto Rico and the other U.S possessions and territories. Finally, the study should try to evaluate the difference in risks associated with various types of plants and – possibly – also source regions.

Hawaiian native plant naio; photo by Forrest and Kim Starr

Unknown Unknowns

As I noted above, problems curtailing introduction of tree-killing pests are not limited to the U.S. For more than a decade, scientists have noted that the international phytosanitary system has failed to prevent the rapid worldwide spread of significant pathogens via the international nursery trade. Examples include Brasier 2008; Liebhold el. al. 2012; Santini et al. 2013; Roy et al. 2014; Eschen et al. 2015; Jung et al. 2015; Meurisse et al. 2019; O’Hanlon et al. 2021. One of the principal concerns is the fact that most species of microorganisms have not been named by science, much less evaluated for their potential impacts on naïve hosts. This issue was raised by Sarah Green of British Forest Research at the annual meeting of the Continental Dialogue on Non-Native Forest Insects and Pathogens. She asked the APHIS representative whether the agency’s phytosanitary procedures (described here) are working to prevent introductions. She pointed to the issues raised by numerous scientific experts: pest risk analyses address only known organisms, so they cannot protect importers from unknown organisms.

U.S. scientists are beginning to address the issue of “unknown unknowns”. Some studies have taken a stab at evaluating traits of insects that are more likely to damage conifers (Mech et al.) and hardwoods (Schultz et al.). Jiri Hulcr – of the University of Florida — assessed the threat posed by 55 insect-vectored fungi to two species of oak and two species of pines. However, the forests of the southeastern U.S. comprise many other tree genera! He also set a very high bar for defining a threat as serious: the damage to the host must be equivalent to that caused by Dutch elm disease or laurel wilt. We urgently need APHIS, USDA/Forest Service, and academia to sponsor more similar studies to evaluate the full range of risks more thoroughly.

SOURCES

Allison J.D., M. Marcotte, M. Noseworthy and T. Ramsfield. 2021. Forest Biosecurity in Canada – An Integrated Multi-Agency Approach. Front. For. Glob. Change 4:700825. doi: 10.3389/ffgc. 2021.700825 Frontiers in Forests and Global Change July 2021 | Volume 4 | Article 700825

Cuthbert, R.N., C. Diagne, E.J. Hudgins, A. Turbelin, D.A. Ahmed, C. Albert, T.W. Bodey, E. Briski, F. Essl, P. J. Haubrock, R.E. Gozlan, N. Kirichenko, M. Kourantidou, A.M. Kramer, F. Courchamp. 2022. Bioinvasion costs reveal insufficient proactive management worldwide. Science of The Total Environment Volume 819, 1 May 2022, 153404

Garbelotto M. and P. Gonthier. 2022. Ecological, evolutionary, and societal impacts of invasions by emergent forest pathogens. Chapter 7, Forest Microbiology. Elsevier 2022.

Li, Y. C. Bateman, J. Skilton, B. Wang, A. Black, Y-T. Huang, A. Gonzalez, M.A. Jusino, Z.J. Nolen, S. Freemen, Z. Mendel, C-Y. Chen, H-F. Li, M. Kolarik, M. Knizek, J-H. Park, W. Sittichaya, P.H. Thai, S-I. Ito, M. Torii, L. Gao, A.J. Johnson, M. Lu, J. Sun, Z. Zhang, D.C. Adams, J. Hulcr. 2021. Pre-invasion assessment of exotic bark beetle-vectored fungi to detect tree-killing pathogens. Phytopathology. https://doi.org/10.1094/PHYTO-01-21-0041-R

MacLachlan, M.J., A. M. Liebhold, T. Yamanaka, M. R. Springborn. 2022. Hidden patterns of insect establishment risk revealed from two centuries of alien species discoveries. Sci. Adv. 7, eabj1012 (2021).

Mech, A.M., K.A. Thomas, T.D. Marsico, D.A. Herms, C.R. Allen, M.P. Ayres, K.J. K. Gandhi, J. Gurevitch, N.P. Havill, R.A. Hufbauer, A.M. Liebhold, K.F. Raffa, A.N. Schulz, D.R. Uden, & P.C. Tobin. 2019. Evolutionary history predicts high-impact invasions by herbivorous insects. Ecol Evol. 2019 Nov; 9(21): 12216–12230.

Nahrung, H.F. and A.J. Carnegie. 2020. NIS Forest Insects and Pathogens in Australia: Establishment, Spread, and Impact. Front. For. Glob. Change 3:37. doi: 10.3389/ffgc.2020.00037 Frontiers in Forests and Global Change | www.frontiersin.org 2 March 2020 | Volume 3 | Article 37

Nahrung, H.F. and A.J. Carnegie. 2021. Border interceptions of forest insects established in Australia: intercepted invaders travel early and often. NeoBiota 64: 69–86. https://doi.org/10.3897/neobiota.64.604

Nahrung, H.F. & A.J. Carnegie. 2022. Predicting Forest Pest Threats in Australia: Are Risk Lists Worth the Paper they’re Written on? Global Biosecurity, 2022; 4(1).

Nahrung, H.F., A.M. Liebhold, E.G. Brockerhoff, and D. Rassati. 2022. Forest Insect Biosecurity: Processes, Patterns, Predictions, Pitfalls. Annu. Rev. Entomol. 2023.68.

Paap, T., M.J. Wingfield, T.I. Burgess, J.R.U. Wilson, D.M. Richardson, A. Santini. 2022. Invasion Frameworks: a Forest Pathogen Perspective. FOREST PATHOLOGY https://doi.org/10.1007/s40725-021-00157-4

Schulz, A.N., A.M. Mech, M.P. Ayres, K. J. K. Gandhi, N.P. Havill, D.A. Herms, A.M. Hoover, R.A. Hufbauer, A.M. Liebhold, T.D. Marsico, K.F. Raffa, P.C. Tobin, D.R. Uden, K.A. Thomas. 2021. Predicting non-native insect impact: focusing on the trees to see the forest. Biological Invasions.

Turner, R. M., E. G. Brockerhoff, C. Bertelsmeier, R. E. Blake, B. Caton, A. James, A. MacLeod, H. F. Nahrung, S. M. Pawson, M. J. Plank, D. S. Pureswaran, H. Seebens, T. Yamanaka, and A. M. Liebhold. 2021. Worldwide border interceptions provide a window into human-mediated global insect movement. Ecological Applications 31(7):e02412. 10.1002/eap.2412

Wang, Q. (Ed.). 2017. Cerambycidae of the world: biology and pest management. Boca Raton, FL: CRC Press

Posted by Faith Campbell