Protect salamanders from fatal disease

The U.S. Fish and Wildlife Service (USFWS) has taken new action to protect North America’s salamanders from the pathogenic Salamander Chytrid Fungus Batrachochytrium salamandrivorans; Bsal). The Center for Invasive Species Prevention (CISP) welcomes this action and urges you to help the Service to finalize it.

To read and comment on the interim rule, go here. The comment period closes on March 11.

oriental fire-bellied newt (*Cynops orientalis*); one of the non-native species imported in largest numbers before the 2016 Lacey Act interim rule; photo by Sebastian Voitel

USFWS acted under its authority to contained in the “injurious wildlife” provisions of the Lacey Act [18 U.S.C. 42(a)]. This statute, first adopted in 1900, empowers the Secretary of Interior to regulate human-mediated transport of any species of wild mammal, wild bird, fish, mollusk, crustacean, amphibian, or reptile found to be injurious to human beings; to the interests of agriculture, horticulture, or forestry; or to America’s wildlife or wildlife resources. Regulated articles include offspring or eggs of the listed species, dead specimens, and animal parts.

Any importation of a listed taxon into the U.S. is regulated. However, regulation of transport within the United States is complicated because of clumsy wording of the statute. In 2017, the D.C. Circuit Court of Appeals [U.S. Association of Reptile Keepers, Inc. v. Zinke [852 F.3d 1131 (D.C. Cir. 2017)] ruled that the law regulates transport of listed species (and their progeny, parts, etc.) between the contiguous 48 States and several other jurisdictions: Hawai`i, Puerto Rico, other U.S. territories, and the District of Columbia. However, transport among the “lower 48” states (e.g., from Virginia to Kentucky) or from the “lower 48” states to Alaska, is not regulated (unless the route to or from Alaska passes through Canada). In past years conservationists asked Congress to amend the law to close this obvious gap in protection, but without success.

It is still illegal to transport listed species across any state borders if the wildlife specimen was either imported to the U.S. or transported between the above-enumerated jurisdictions in violation of any U.S. law. [Lacey Act Amendments of 1981, 16 U.S.C. 3372(a)(1)]

Those wishing to transport a listed species for zoological, educational, medical, or scientific purposes may apply for a permit from USFWS to do so.

The threat to salamanders

The United States is a center of diversity for salamanders. Our nation is home to 221 species of salamanders, more than any other country. These species are in 23 genera in nine families. In fact, nine of the 10 families of salamanders worldwide are found in the U.S. Highest diversity is found along the Pacific Coast and in the southern Appalachian Mountains. As the most abundant vertebrates in their forest habitats, salamanders make significant contributions to nutrient cycling and even carbon sequestration.

Because they depend on both aquatic and terrestrial habitats, salamanders face many threats to their existence. Twenty species of American salamanders from 6 genera (Ambystoma, Batrachoseps, Eurycea, Necturus, Phaeognathus, Plethodon) are listed under the Endangered Species Act link as endangered or threatened. A subspecies of hellbender salamander (Cryptobranchus alleganiensis alleghaniensis) has been proposed for listing.

*Amylosterium* xxx – marbled salamander; photo by John B. Clare via Flickr

Over the last 12 years, they have faced an alarming new threat.

In 2013, European scientists detected rapid, widespread death of salamander populations in the Netherlands. They determined that the cause was a fungal disease caused by Batrachochytrium salamandrivoran (Bsal). Their alarm was heightened because this fungus is closely related to another, Batrachochytrium dendrobatidis (Bd), which had recently caused serious decline of more than 100 frog and toad species, including driving several to extinction, and had been transported to all continents except Antartica.

Responding to this new threat, amphibian conservation specialists and wildlife groups generally banded together to put pressure on the USFWS to take regulatory action. In response, in 2016, the USFWS adopted an interim rule link prohibiting importation of 20 genera of salamanders. These genera had been shown by scientists to contain at least one species which either suffered mortality when it was exposed to Bsal or could transmit the disease to other salamanders. At the time, Bsal had been shown by scientific studies to be lethal to two American species; USFWS had evidence that U.S. species in other genera could “carry” the pathogen and infect other animals. Three of the species included in the 2016 action had already been listed as endangered or threatened. USFWS’ action cut down the number of salamanders being imported annually by ~95% (based on official import data compiled by the USFWS’ Office of Law Enforcement).

Now, 8 years later, the USFWS is acting to finalize the 2016 “interim” rule and to regulate importation and transportation of an additional 16 genera of salamanders. This step had been urged by the National Environmental Coalition on Invasive Species (NECIS), and many others, in their public comments on that Interim Rule. Extending protection to these 16 genera is based on research conducted since the 2016 Rule. Species in 13 of the newly protected genera are considered likely carriers of the disease. Nine species have been demonstrated to be killed by Bsal. No studies have yet determined the vulnerability of more than 50 species in 10 genera of North American salamanders, including four species listed under the Endangered Species Act.

The 36 genera covered by the combined actions of 2016 and 2025 actions are currently considered to comprise ~ 426 species. However, changes in taxonomy are frequent. So USFWS is no longer enumerating the species protected, but is instead relying on listing genera. The regulations apply to all species in a listed genus (whether so classified now or in the future) as well as hybrids of species in any listed genus, including offspring from a pair in which only one of the parents is in a genus listed as injurious.

Appalachian hellbender *Cryptobranchus alleganiensis alleghaniensis*; historic book illustration via Flickr

USFWS chose to issue “interim” rules in both 2016 and 2025 because that action takes effect almost immediately. (The 2025 interim rule take effect on January 25^th.) The usual rulemaking process governed by the Administrative Procedure Act (5 U.S.C. 551 et seq.) often takes years to complete. During that time, the species proposed for listing may still be imported and transported – that is, they could place additional salamander populations at risk of infection by Bsal. The USFWS states that it is unlikely to be able to protect or restore species and ecosystems if the pathogen does become established in the U.S.

In the interval between 2016 and now, Canada banned importation of all living or dead salamanders, eggs, sperm, tissue cultures, and embryos in response to the Bsal threat.

During these years scientists also completed several studies aimed at clarifying which salamander species are either at risk of infection by Bsal or are able to harbor and transmit the pathogen to other salamanders. The USFWS cites studies by, inter alia, Yuan et al. 2018, Carter et al. 2020, Barnhart et al. 2020, Grear et al. 2021, and Gray et al. 2023. USFWS says it cannot act in the absence of such studies, since it must justify its protective actions on scientifically defensible information.

Another relevant question is whether Bsal is already established in North America? Waddle et al. 2020 carried out an intensive search in 35 states that found no evidence that it is. The USFWS concludes that prohibiting importation of additional salamander taxa is still an effective measure to protect North American biodiversity. This is because the international commercial trade in salamanders is the most likely pathway by which Bsal would be introduced to the United States. We note in support of this assertion that former USFWS employee Su Jewell found years ago that none of the 288 non-indigenous species listed as injurious while they are not established in the U.S. has become established since the listing.

The Federal Register document includes a lengthy discussions of why the USFWS has chosen to act under the Lacey Act rather than try some other approach, e.g., setting up quarantine areas or a disease-free certification program for traded salamanders. Among the factors they considered were the current absence of certainty in testing procedures and the possibility of falsified documentation.

WEAKNESSES THE LACEY ACT

The Lacey Act is the principal statute under which the U.S. Government tries to manage invasive species of wildlife – at least those that are not considered “plant pests”. It is not surprising that a law written 125 years ago is no longer the best fit for current conservation needs. See our earlier blog and discussions by, inter alia, Fowler, Lodge, and Hsia and Anderson.

Here, the USFWS lacks authority to regulate pathogens [viruses, bacteria, and fungi that cause disease] or fomites (materials, such as water, that can act as passive carriers and transfer pathogens). Instead, USFWS regulates the hosts. The USFWS previously listed dead salmonids as “injurious” because their carcasses can transmit several viruses.

Another issue is that USFWS cannot designate a taxon “injurious” and regulate trade in it until the Service has conclusive scientific evidence that the species or genus meets the definition. The USFWS has chosen to rely on genus-level data rather than require that each species be tested. Still, as we noted above, American salamanders in 10 genera remain outside the Lacey Act’s protections because studies have not yet been conducted. The USFWS concedes that many of these genera might contain species that are vulnerable to this potentially deadly fungus.

As to relying on laboratory tests of a taxon’s response to the pathogen, the USFWS believes that environmental stresses inherent living in the wild might exacerbate a salamander species’ vulnerability to the disease.

The USFWS is requesting public comment specifically on:

(1) the extent to which species in the 16 genera listed by this interim rule are currently in domestic production for sale – and in which States this occurs? How many businesses sell salamanders from the listed genera between enumerated jurisdictions (e.g., between “lower 48” states and Hawai`i or the District of Columbia)?

(2) What state-listed endangered or threatened species would be affected by introduction of Bsal?

(3) How could this interim rule be modified to reduce costs or burdens for some or all entities, including small entities, while still meeting USFWS’s goals? What are the costs and benefits of the modifications?

(4) Is there any evidence suggesting that Bsal has been established in the U.S.? Or that any of these genera are not carriers of Bsal? Or that additional genera are carriers of Bsal? Is there evidence that eggs or other reproductive material pose a greater risk than USFWS determined, so should be regulated?

(5) Could a reliable health certificate system be developed that would allow imports of Bsal-free salamanders? Are there treatments that would ensure imported salamanders are reliably free of Bsal? How could compliance be monitored? As to salamander specimens, parts, or products, are there other treatments proven adequate to render Bsal non-viable?

(6) Do any Federal, State, or local rules duplicate, overlap, or conflict w/ this interim rule?

CISP encourages those with knowledge of amphibian conservation and disease to comment. Slow progress has been made toward blocking Bsal from the U.S., but the story is not yet closed.

Import volumes continue to rise (although exact numbers elusive)

obvious risk of pest introduction! photo by F.T. Campbell

Because of the many damaging insects introduced in wood packaging, I often blog about numbers of shipping containers entering the country. [On the “nivemnic.us” website, scroll down below “archives” to “categories”, then click on “wood packaging” to see my previous blogs discussing this issue.]

The Department of Homeland Security’s Bureau of Customs and Border Protection (CBP) reports processing 36.6 million shipping containers holding imports in Fiscal Year 2023 – which ended in September 2023. These presumably included about 13 – 16 million containers arriving via ship from Asia, Europe, and other overseas trading partners. The remaining millions probably entering from Mexico and Canada via land transport. Together, Mexico and Canada provided 30% of U.S. imports in 2022.

It is difficult to pin down the actual number of containers entering the country. In contrast to the figure provided by CBP, Laura Robb of the Journal of Commerce reports that 25.6 million TEUs carrying imports entered the country in 2024. This figure apparently includes containers carried by all forms of transport. CBP counts containers by actual numbers, and about 90% of waterborne containers are actually 40 feet long, not the 20 feet measured by “TEU” (U.S. DoT). Halving the JOC number results in a total of about 13 million – well below that reported by CBP.

Overall volumes of imports carried by ship continue to rise. The monetary value of goods imported by the U.S. in maritime trade grew 15% from 2021 to 2022 (U.S. DoT). Robb reported that trade experts believe imports rose another 15% between 2023 and 2024. This rise is driven by retailers trying to protect themselves from a possible longshoremen’s strike (which might occur beginning 15 January), Trump’s threatened tariffs (he might act as early as 20 January); and the annual slowdown of production in Asia during Tet (which begins on 29 January). If import volumes meet expectations and continue through April, the series will outdo the previous (pandemic-era) record of 19 straight months when imports exceeded 2 million TEUs. What happens later in 2025 depends in part on whether the anticipated strike happens and/or actual levels of any new tariffs.

One concern about imports from Mexico and Canada is that some proportion of these goods actually originated in Asia or Europe, but were shipped through Mexican or Canadian ports. I have not found a source to clarify how many shipments fit this pattern. USDA APHIS used to blame forest pests introduced to the Great Lakes region on goods transported from the principal Canadian Atlantic port, St. John, Nova Scotia.

A useful publication for identifying where the pest-introduction risk is highest are the annual reports issued by U.S. Department of Transportation’s Bureau of Transportation Statistics. In calendar year 2022, U.S. maritime ports handled just under 43% of U.S. international trade (measured by value). There are two caveats: the data include both imports and exports; and the most recent data are from 2021.

Two-thirds of America’s maritime cargo (imports and exports) is shipped in traditional containers. This includes most consumer goods. The top 25 container ports handled a total of 45.6 million TEU (U.S. DoT). Map 4-3 in the report shows these ports and the proportions that are imports and exports.

The highest-ranking Container Ports in 2021 are those we expect. The ports of Los Angeles and Long Beach were numbers one and two. Together they received 10.7 million TEU. The third highest number of containers entered through the Port of New York & New Jersey. Nearly 5 million TEU entered there. The Port of Savannah ranked fourth. Savannah and nearby Charleston (ranked seventh) handled 4.2 million incoming TEUs in 2021.

Ranked above Charleston were the Port of Virginia and Houston. Each processed approximately 1.8 million containers filled with imports. Three West coast ports follow: Oakland, California and Tacoma and Seattle. Just over 1 million TEUs entered Oakland. The two Washington ports received a little over 1.5 million. Florida has four ports ranked in the “top 25”. In total, they processed 1.2 million TEU; most entered through PortMiami and Port Everglades. Baltimore, Philadelphia, Mobile, New Orleans, Wilmington, North Carolina and Wilmington, Delaware, South Jersey Port Corporation, and Boston all handled less than 500 imported containers in 2021. Domestic shipments from other U.S. states dominated containers processed through the ports of San Juan, Honolulu, and Alaska.

gantry crane in operation at the Port of Savannah; photo by F.T. Campbell

The top ports must have appropriate facilities needed to load / unload container vessels efficiently– that is, adequate numbers of gantry cranes, especially super post-Panamax cranes, which have the greatest capacity. The top 25 container ports of 2021 operated a total of 539 ship-to-shore gantry cranes in 2023, of which 322 (60%) are post-Panamax cranes. Ports are adding cranes – there were 29 more in 2023 than in 2021. The Port of Virginia appears to be striving for significant increases in tonnage; it has 28 Panamax cranes, more than Charleston and almost as many as Savannah (U.S. DoT).

Another important port component is efficient facilities to load containers onto rail cars or trucks for transfer to land-based warehouses and retailers. Ports have more than one terminal; for example, the Port of Long Beach has six, New York/New Jersey has five. Nationwide, 70% of container terminals have on-dock facilities to transfer containers directly onto rail cars. All but three of the 33 terminals located at Long Beach. Los Angeles, New York, Savannah, Charleston, Houston 2/2, Seattle, and Tacoma have on-dock transfer equipment.

The U.S. DoT reports also inform us about the top 25 ports that handle other categories of cargo: overall tonnage, dry and liquid bulk cargo, break bulk cargo, and roll-on-roll-off cargo. Visit the report to view these data.

SOURCES

Robb, L. 2024. U.S. import “surge” to persist into spring amid continued frontloading: retailers. Journal of Commerce Daily Newswire December 10, 2024

U.S. Customs and Border Protection FY 2023 CBP TRADE SHEET https://www.cbp.gov/document/annual-report/fy-2023-cbp-trade-fact-sheet

U.S. Department of Transportation, Bureau of Transportation Statistics, Annual Report 2024 Port Performance Freight Statistics January 2024 https://www.bts.gov/explore-topics-and-geography/modes/maritime-and-inland-waterways/2024-port-performance-freight

Posted by Faith Campbell

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 https://treeimprovement.tennessee.edu/

www.fadingforests.org

How beech leaf disease spreads in the forest

BLD symptoms; photo by Matt Borden, Bartlett Tree Experts

As beech leaf disease (BLD) is detected in an ever-expanding number of counties from Michigan to Maine south to Virginia, scientists are trying to clarify how the causal nematode — Litylenchus crenatae ssp. mccannii (Lcm) – spreads. One focus is on local spread from tree to tree. Mankanwal Goraya and colleagues set up an experiment in Stone Valley Forest, a recreation and research site managed by Penn State in Huntington County, Pennsylvania. BLD is present – although I have not been able to determine for how many years. [The full citation to Goraya et al. is provided at the end of this blog.]

Goraya et al. (2024) set up four stands, each bearing three funnels, at varying distances from naturally BLD-infected American beech (Fagus grandifolia) trees. Two stands were at 3.51 m from symptomatic trees of starkly different sizes: one of the trees had a dbh of 50 cm, the other of only 5.6 cm. A third close-up stand was set up at 2.20 m from another large tree, having a dbh of 46 cm. The fourth stand was set up at a significantly longer distance, 11.74 m from a symptomatic beech tree; this tree was also small, with a dbh of 5 cm. This arrangement allowed the scientists to detect influences of both distance from the source of infection and relative canopy size of the source tree. They consider dbh to be an adequate substitute for canopy size. There was apparently no other effort to determine or vary the height of “source” trees, although I think that might influence speed of the wind flowing through the canopy.

Goraya et al. also tested whether it is possible to detect the presence of Lcm in association with other invertebrates that live in beech forests. To do this, they counted numbers of nematodes in frass from six species of caterpillars that had been feeding on leaves of infected trees, and in two spider webs spun in the branches of symptomatic trees. They also determined whether these nematodes were alive (active) or inactive – presumably dead.

The study makes clear that Lcm’s life cycle and impact are not as surprising as initially thought. Several species in the family Anguinidae – to which Lcm belongs – are considered significant pests. These nematodes can parasitize aerial parts of the plants (leaves, stems, inflorescences and seeds), causing swellings and galls. Furthermore, they are migratory; they can move across the surface of host tissues using water films. Once they have penetrated the host tissues, they can induce host cell hyperplasia and hypertrophy, resulting in leaf or bulb deformities, shorter internodes, and neoplastic tissues. Furthermore, heavy rainfall and wind are known to play significant roles in the dissemination of plant-infecting nematodes. In their desiccated state on infected seeds, some species of this family can survive passage through animals’ gastrointestinal digestive tract (e.g., domestic livestock, insects, & birds).

A crucial factor is that Lcm can reach densities of thousands of nematodes per leaf by late summer or early fall, increasing the likelihood of their exposure to facilitating environmental conditions at the time they migrate from leaves to buds. And once established within the bud tissues, the nematodes feed on bud scales and newly forming leaves to develop & increase their pop #s. They also use the bud as protection from adverse environmental conditions.

Goraya and colleagues collected samples every other day from September 9 to November 23, 2023 – the period when Lcm migrate from highly infected leaves to newly forming buds. [I note that it in the mid-Atlantic – where Lcm is spreading – we had an extensive drought in autumn 2024 – more than 30 days without any rain from early October into November. I hope scientists are monitoring BLD spread sufficient closely to see whether this drought affected dispersal.]

Nematodes dispersal linked to weather

Goraya and colleagues collected 324 samples from the funnels. Eighty-two percent (n =266) of the samples had nematodes; up to 92% were identified as Lcm. Non-Lcm nematodes were distributed across different genera, mostly classified as free-living nematodes. While several hundred nematodes were found in the funnels on most days, numbers peaked noticeably on some days in September and October. A startling 2,452 nematodes were recovered from a single funnel in October. Depending on the sample, up to 67% of Lcm recovered from the funnels were active.

Analysis of the environmental (weather) variables found that increases in wind speed, humidity, and precipitation (rainfall) coincided with higher numbers of Lcm being recovered from the funnels. However, the effect of wind speed becomes less positive as precipitation increases or vice versa. Goraya et al. suggest a pronounced negative interaction between wind and rain. At low precipitation levels, increased wind speed might facilitate Lcm dispersal. As rainfall increases, higher wind speeds might carry the Lcm nematodes farther away. Support is seen in the fact that fewer nematodes were found in the funnels closer to the BLD-infected trees during these periods. Really heavy rain might push a significant preponderance of nematodes to the ground. The scientists point to a very complex interplay between weather patterns and Lcm population dynamics and dispersal.

BLD symptoms on beech tree in Fairfax County, Virginia – a dozen miles from known infestation; photo by F.T. Campbell

The model did not show any significant influence of maximum temperature on nematode numbers in autumn. Goraya et al. do not speculate on whether temperatures might play a role during summer, as distinct from cooler autumn periods.

Goraya et al.’s findings differ from those of previous studies. Earlier documentation of wind dispersal of nematodes concerned primarily free-living species. It was unexpected to find consistently much higher numbers of Lcm – especially because Lcm is a plant-parasitic nematode. Another surprise is the high proportion of nematodes that are active.

Goraya et al. conclude that because Lcm is actively migrating in large numbers during autumn months, it is primed to take advantage of favorable weather. This nematode will likely survive and thrive in the environmental conditions of beech forests in northeastern North America.

Considering the effect of distance, some findings fit expectations: significantly more Lcm were recovered from funnels placed near symptomatic “source” trees than from those farther away. However, this was not a simple relationship. For example, in two cases the scenarios seemed nearly alike: both “source” trees were large (dbh 46 or 50 cm) and symptoms were “medium-high” (more than half of leaves presenting dark-green interveinal bands). Distance of funnels from the “source” tree differed minimally: 2.2 m versus 3.51 m. Still, the number of nematodes retrieved from the two sets of funnels differed significantly: one set of funnels recovered the highest number of Lcm nematodes obtained during the entire experiment – 2,452; the second contained only up to 600 nematodes. The authors do not offer an explanation.

I am not surprised by the apparently strong correlation between numbers and proximity to the disease source (a symptomatic tree). Nor am I surprised that Lcm nematodes were also found in funnels 11 meters away. I do wonder, however, why they are certain that no source was closer. Detecting early stage infections is notoriously difficult.

beech with large canopy; photo by F.T. Campbell

Goraya et al. also evaluated the effect of size of the source tree. They used dbh a substitute for larger canopies. Trees with larger canopies can host more nematodes, so are likely to contribute more to dispersal events. Two sets of funnels were equidistant from separate “source” trees – 3.51 m. One tree was small – 5.6 cm dbh, 11% as large as the other tree (50 cm). They collected many fewer Lcm nematodes from the smaller tree – the maximum was only 132 compared to 600 (a decrease of 78%).

Still, small trees can apparently support spread of the nematode to a reasonable distance. The fourth set of funnels was set up more than three times farther away (11.74 m) from an infected tree of a similar size (dbh = 5 cm) but recovered almost the same number of Lcm nematodes (0 – 119).

I find it alarming that both small trees in this part of the experiment had low BLD symptoms – only a few leaves were banded. Yet they apparently are the source of Lcm spread. The alternative, as I noted above, is that other “source” trees were in the vicinity but were not detected, possibly because they did not yet display symptoms?

Goraya et al. conclude that “source” tree size directly impacts the number of recovered nematodes. In addition, wind plays a pivotal role in their local distribution. This suggests a complex dispersal pattern in which proximity to the source leads to higher numbers of nematodes but longer-distance spread is possible.

Tussock moth; photo by Jon Yuschock via Bugwood

Nematodes’ association with other organisms

Goraya et al. (2024) collected one each of six caterpillar species from BLD-symptomatic trees. The frass of one – the tussock moth caterpillar (Halysidota tessellaris) — contained 12 nematode specimens — 10 of them Lcm. Two of the Lcm were alive and active. Their presence indicates that Lcm can survive passage through the caterpillar’s gastrointestinal tract. The authors conclude that caterpillars feeding on symptomatic leaves might contribute to local dispersal of Lcm.

Hundreds of Lcm were recovered from the two spider webs collected from the branches of a BLD-infected beech tree. From one web, 255 nematodes were captured; 58 were active. In the second web there were only 34 Lcm, but one-third — 10 – were active.

Goraya et al. (2024) hypothesized that any biotic form having the ability to move from a BLD-infected tree would be able to transport Lcm to other non-infected trees. Beyond caterpillars, they speculate that birds consuming these caterpillars might also disperse Lcm. Doug Tallamy has documented that many birds feed on caterpillars, link although he is focused on those that consume caterpillars in the spring, not the autumn. They note that others are studying that the bird species that feed on beech buds (e.g., finches) might transport nematodes. They note the need for additional research to clarify whether the nematode can survive birds’ digestive system.

Re: detection of live Lcm in spider webs, Goraya et al. suggest two possible interpretations: 1) this finding demonstrates that nematodes might fall from leaves, potentially spreading the infection to other trees beneath the canopy. (Supporting this idea is the fact that sub-canopy trees are often heavily infected with BLD and are frequently the first to exhibit BLD symptoms.) 2) Nematodes in spider webs are very likely to be transported by other “incidental organisms” (e.g., insects, birds, mammals) that feed on invertebrates trapped in webs — thereby potentially increasing the number and impact of nonspecific nematode vectors.

In conclusion, Goraya et al. found that many factors, e.g., distance & size of infected beech trees, wind speed, & humidity, contribute significantly to Lcm dispersal. The multitude of organisms interacting beneath the canopy also play a role.

They suggest that several major questions still need to be explored. These include how Lcm navigate environmental factors in their spread; and whether Lcm can survive – perhaps in a anhydrobioses state –transport over long distances, whether by abiotic or biotic vectors.

I remind my readers of the importance of beech in the hardwood forests in northeastern North America. Many wild animals, including squirrels, wild turkeys, white-tailed deer, and bears depend on beechnuts for fats and proteins. Moreover, some insects birds rely on beech tree canopies for shelter & nesting.

Other Hosts

Beech leaf disease attacks not just American beech (Fagus grandifolia). In North America, it has also attacked planted European beech(F. sylvatica), Chinese beech (F. engleriana), and Oriental beech (F. orientalis). Thus if it spreads it could have severe impacts across forests of much of the Northern Hemisphere.

range of European beech; from Royal Botanic Gardens, Kew

I appreciate that this project was funded by the USDA Forest Service International Program. I will pursue information concerning efforts by USFS Research and Development and the Forest Health Protection program.

SOURCE

Goraya, M., C. Kantor, P. Vieira, D. Martin, M. Kantor. 2024 Deciphering the vectors: Unveiling the local dispersal of Litylenchus crenatae ssp mccanni in the American beech (Fagus grandifolia) forest ecosystem PLOS ONE |https://doi.org/10.1371/journal.pone.0311830 November 8, 2024 1 / 16

Posted by Faith Campbell

www.fadingforests.org

Again – analysts of changing forests leave out key factors

oak & beech seedlings; photo by F.T. Campbell

Yet again, studies focusing on issues of regeneration and mortality failing to consider all aspects.

Two studies focused on persistence of oak forests – a topic of great concern because of economic and ecological importance of oak-dominated forests. Since they dominate forests covering 78.5 million ha (51% of all forestland in the eastern United States) (Dey 2013), oaks shape stand structure and composition; their extensive crowns support many bird and arboreal mammal species; their acorns and leaf litter are the foundation of complex food webs; they live in symbiotic relationships with mycorrhizal fungi that enhance nutrient cycling and uptake within forest ecosystems. Deep roots prevent soil erosion. Oaks play a pivotal role in carbon sequestration (Khadka, Hong, and Bardhan 2024).

Until recently concern has focused on mortality of species in the red oak group (Section Lobatae). Now there is increasing concern about white oak (Quercus alba) mortality. Forest managers reported elevated mortality not just in resource-limited sites,e.g., those characterized by drought conditions, poor drainage, and soil nutrient deficiencies. Deaths are also occurring in higher-quality mesic sites, especially in forests with high stand density and advanced maturity stages. While white oaks go through a self-thinning phase – when dense stands of younger trees compete intensely for limited resources –it appears that some of the concern is focused on this stage (Khadka, Hong, and Bardhan 2024).

I think much of the concern is driven by economic rather than ecological considerations. None of oak species mentioned by Duana et al. (2024) is considered at risk by the authors of the recent conservation gap analysis (Beckman et al. 2019). (This is not surprising since presumably these species are sufficiently numerous to support commercial harvests). Furthermore, complaints about forest regeneration in the East are broader than oaks. A multi-author examination of the future of the northern forest projected decreases for four forest types = aspen-birch, elm-ash-cottonwood, oak-hickory, and spruce-fir. One type –maple-beech-birch – was expected to expand (Shifley and Moser 2016).

Regarding oaks specifically, Khadka, Hong, and Bardhan (2024) found that 30% of FIA plots in ten states composed primarily of white oak met their criteria for considering white oaks to be “declining”. However, higher mortality was limited to scattered areas (see map in Fig. 2B in the article). They suggested that contributing factors included higher elevation and distance from water in the north, intense competition in central regions, and drought stress in oak-hickory forests in the south. They also mentioned mature stands which are not replacing themselves in the southern region. Khadka, Hong, and Bardhan (2024) noted that oak decline complex is a factor in the southern region, and localized non-native insect pests (apparently spongy moth) in the northern region. (I will discuss both regeneration failures and the impacts of non-native pests below.) Still, these authors focus most attention to environmental stresses, e.g., droughts or water logging, poor soils, extreme weather events; and to human management, e.g., fire suppression, logging intensity, edge effects. They suggest strategies for mitigating these factors.

A second study, published by Duana et al. (2024), considered stocking levels of several species of oaks (Q. alba, Q. coccinea, Q. prinus, Q. rubra, and Q. velutina) but limited themselves to a large, temperate hardwood forest landscape in southeastern Ohio. Their purpose was to evaluate the efficacy of two levels of silvicultural intervention in sustaining oaks and restraining maples over the long-term, defined as 150-years (to 2060).

red oak (*Quercus rubra*); photo by F.T. Campbell

Their model suggested that continuing “business as usual” management would result in oaks shrinking from 22.8% dominance in 2010 to 12% dominance in 2160. Many of the remaining oaks would be large — in the 70 cm DBH class. The undesired maples would rise from 23% of total relative dominance in 2010 to 58% in 2160. The maples grew to almost the same size as the oaks: 50–65 cm DBH. As a result of these developments, the maple basal area increase by more than five times. The basal area of early successional species, e.g., poplars and aspens, decreased from 25% dominance to 11% dominance by 2160. Shade-tolerant species like elms, hickories, beech, and hemlock were suppressed by more competitive maples, occupying 17% of the total dominance.

Under the more manipulative alternative management strategy, oaks’ relative dominance on private land would stay above 20% of total relative dominance; all ages and sizes would be present. Maples would hold steadier at 23% to 33%. Shade-tolerant species would also rise, reaching a quarter of relative dominance on private some site (private public lands).

Duana et al. (2024) explained the outcome of “business as usual” management on maples’ ability to thrive in shaded conditions while oak regeneration requires sunlight to reach the forest floor. Another factor is the prevalence of high-grading harvesting practices. These factors result in a significant absence of oak trees in the sapling and midstory sizes, reflecting challenges to both oak seedlings and saplings. In other words, despite the continued growth of mature overstory oaks, the trees cannot reproduce. As Duana et al. (2024) point out, these results are supported by other field-based studies — including ones I have blogged about. Duana et al. (2024) discuss barriers and incentives to private landowners adopting more active management.

However, as I pointed out above, many tree species are regenerating poorly, not just oaks. Indeed, none of the eastern species fulfilling Potter and Riitters’ (2022) criteria for species threatened by poor regeneration was an oak. See Table 2 in Potter and Riitters (2022).

American sycamore (*Platanus occidentalis*) – one of the tree species not regenerating adequately; photo by F.T. Campbell

Hanberry et al. (2020) found that actual changes in forest species composition and density do not conform to expectations arising from three factors proposed as drivers: increased precipitation, increased white-tailed deer densities, and functional extinction of American chestnut. They found disappearance of frequent low-intensity fires to be determinative. However, Hanberry et al. (2020) also do not mention invasive plants or non-native pests other than chestnut blight.

Here I review others’ discussion of browsing by overabundant deer and competition from non-native plants as factors widely recognized as impeding regeneration of canopy trees, including oaks.

Deer

There is widespread agreement that browsing by overabundant deer is a major cause of poor regeneration of deciduous forests, especially but not limited to oaks (Quercus species.). Sources cited in my previous blogs include most studies discussed at the 2023 Northern Hardwood research forum (USDA, FS 2023b Proceedings), Spicer et al. (2023), Miller et al., and two studies based in either Ohio (the location of the study by Duana et al. [2024]) or neighboring Pennsylvania: Yaccuci et al. (2023) and Reed et al. 2023. Yacucci et al. reported that stem density of red (Q. rubra) and pin oaks (Q. palustris) was 13 times higher in canopy gaps located in areas with low densities of deer than in gaps in high-deer-density locations. In these gaps, oak saplings were growing into the subcanopy. Reed et al. said deer herbivory might be one of the most important drivers of forest composition and canopy structure over long time-scales.

Deer might be less important in New England. Stern et al. (2023), working in Vermont, focused on the importance of changing precipitation patterns in shifting numbers of red maple (Acer rubrum), sugar maple (Acer saccharum), American beech (Fagus grandifolia), and yellow birch (Betula alleghaniensis). Northern red oak was described as a common co-occurring dominant species in their plots, but was not discussed. In New Hampshire, Ducey et al. reported changing species composition as the forest ages but did not mention deer.

Some of these authors advocated wide-scale efforts to reduce deer populations in order to restore forest ecosystems. Yacucci et al. proposed enlisting those military posts that regularly cull deer into efforts to conserve and regenerate native plants. Otherwise, they say, the prognosis for regeneration is poor. Blossey et al. urged creation of a nation-wide lethal removal program.

Some of these studies indicated that additional biological entities were also important. Miller et al. stressed the role of invasive plants in suppressing forest regeneration in National parks from Virginia to Maine. Reed et al. focused on invading earthworms. One study – again, conducted in Ohio – Hovena et al. (2022), found that interactions between non-native shrubs and soil wetness overshadowed even the impact of deer herbivory on the species richness and abundance of seedlings.

Invasive Plants

FIA data indicate that 46% of forests in the eastern United States are invaded by alien plant species (Oswalt et al. 2016). Across the region, hundreds of non-native plant species are established in forests and woodlands. (See lists compiled by the Southeast Exotic Pest Plant Council, Mid-Atlantic Invasive Plant Council, Midwest Invasive Plants Network). Forests of the northern Midwest are among the most heavily invaded; in Ohio specifically, two studies found that more than 90% of FIA plots harbor at least one invasive plant species (Oswalt et al. [2016] and Kurtz (USDA NRS 311).

Many of these invaders are herbs, shrubs, or trees which can invade shaded environments. I remind you that a high proportion of these invasive plant species have been deliberately planted either directly in “natural” areas or in yards and gardens throughout the region.

Invasive plants can reduce native diversity, alter forest structure, suppress tree regeneration, alter nutrient cycling, and modify disturbance regimes (Miller et al. 2023).

Japanese stiltgrass (Microstegium vimineum) is widespread in forests of both Northeast (Oswalt et al. (2016) and Southeast. Stiltgrass invasions can suppress oak regeneration – at least as part of interactions with herbivore browsing and harvest history (Johnson et al. 2015).

Several non-native shrub and vine species are also widespread. For example, multiflora rose (Rosa multiflora) is the most frequently recorded invasive plant, present on 16.6% of surveyed plots in 39 states and five Canadian provinces. Again, the state with the highest proportion of plots invaded is Ohio – 85% (USDA Forest Service NRS-109). A study in central Ohio found that the presence of Amur honeysuckle (Lonicera mackii) had a stronger influence on tree species diversity than on the size or number of trees. Removing honeysuckle from heavily invaded areas promoted native tree growth (e.g., the height of tallest trees) and increased the tree canopy’s structural complexity for up to 10 years. Forest recovery began within two years of honeysuckle removal Fotis et al. (2022). (To access earlier blogs, visit www.nivemnic.us; scroll below “archives” to “categories”, click on “invasive plants.)

This impediment to forest regeneration is expected to get worse: non-native plant species are already more widely distributed than native species although the average invasive plant inhabits only about 50% of its expected range (Bradley, Early and Sorte 2015). From Virginia and West Virginia north to Maine, 80% of National Park units have experienced a significant increase in at least one trend measuring abundance of invasive plants in recent decades. In 10 parks (a quarter of all parks studied), total invasives increased significantly in two of three metrics (Miller et al. 2023).

Non-native Pests

Another set of biological factors affecting forest persistence and possibly regeneration is non-native pests that kill North American trees. I have complained that too few of the studies of regeneration discuss implications of these bioinvasions. So Khadka, Hong, and Bardhan (2024), Duana et al. (2024), and Hanberry et al. (2020) continue a tradition that I think is most unfortunate.

American elm in full glory; photo by F.T. Campbell

In Ohio specifically, Hovena et al. and Yacucci et al. did not mention loss of canopy elms, or ash, or the impending threat from beech leaf disease. All these trees are – or used to be – quite common in Ohio. More understandable, perhaps, is lack of attention to laurel wilt disease, which is just now at the state’s southern border. It might decimate an important native shrub, Lindera benzoin. American chestnut was also present in Ohio before its near disappearance following introduction of the chestnut blight fungus early in the 20^th Century.

Another possibly damaging pest that has recently turned up in Ohio is the elm zigzag sawfly Aproceros leucopoda. This Asian insect was first detected in North America in 2020 in Ontario. It quickly became apparent that it was more widespread. The Ohio detection came in 2023 – too recent to be discussed by Hovena et al. or Yacucci et al. Its impact several elm species is currently unknown.

There are exceptions. Both Stern et al. (2023) and Ducey at al. (2023) reported robust growth rates of American beech (Fagus grandifolia) despite decades-long establishment of beech bark disease. DMF Neither mentioned beech leaf disease – to be fair, this bioinvader is just starting to appear in New England. Stern et al. (2023) did not discuss hemlock woolly adelgid although Eastern hemlock (Tsuga canadensis) is also a common co-occurring dominant species in their plots. Ducey et al. did anticipate pest-driven reversals of increased numbers of eastern hemlock (Tsuga canadensis) and of white ash (Fraxinus americana). Stern et al. (2023) also did not mention oak wilt, despite a vulnerable host — northern red oak — being a common co-dominant species in his study site in Vermont. To be fair, oak wilt is not yet established in New England, although it is in New York and in western Ontario.

The most complete discussion of non-native pests is by Payne and Peet, working in the Piedmont of North Carolina. They state that several “specialist” pathogens have caused loss of important tree species, resulting in drastic and long-lasting shifts in community dynamics. They mention elms and dogwoods plus impending insect-caused widespread mortality of ash.

flowering dogwood (*Cornus florida*); photo by F.T. Campbell

Miller et al. describe the impact of EAB on ash resources in the National parks and express concern that BLD will cause considerable damage to some units of the system.

I think the failure of scientists to integrate invasive species’ impacts into assessments of changes in forest tree composition will mean that recommendations for management will be – at best – incomplete; at worst – wrong.

SOURCES

Beckman, E., Meyer, A., Denvir, A., Gill, D., Man, G., Pivorunas, D., Shaw, K., and Westwood, M. (2019). Conservation Gap Analysis of Native U.S. Oaks. Lisle, IL: The Morton Arboretum.

Blossey. B., D. Hare, and D.M. Waller, 2024. Where have all the flowers gone? A call for federal leadership in deer management in the US. Front. Conserv. Sci. 5:1382132. doi: 10.3389/fcosc.2024.1382132

Bradley, B.A., R. Early and C. J. B. Sorte. 2015. Space to invade? Comparative range infilling and potential range of invasive and native plants. Global Ecology and Biogeography

Dey, D.C. 2013. Sustaining Oak Forests in Eastern North America: Regeneration and Recruitment, the Pillars of Sustainability. For. Sci. 60(5):926–942 October 2013. http://dx.doi.org/10.5849/forsci.13-114

Duana, S., H.S. He, L.S. Pile Knapp, T.W. Bonnot, J.S. Fraser. 2024. Private land management is more important than public land in sustaining oaks in temperate forests in the eastern U.S. Journal of Environmental Management 352 (2024) 120013

Ducey, M.J, O.L. Fraser, M. Yamasaki, E.P. Belair, W.B. Leak. 2023. Eight decades of compositional change in a managed northern hardwood landscape. Forest Ecosystems 10 (2023) 100121

Fotis, A., Flower, C.E.; Atkins, J.W. Pinchot, C.C., Rodewald, A.D., Matthews, S. 2022. The short-term and long-term effects of honeysuckle removal on canopy structure and implications for urban forest management. Forest Ecology and Management. 517(6): 120251. 10 p. https://doi.org/10.1016/j.foreco.2022.120251

Hanberry, B.B., M.D. Abrams, M.A. Arthur & J.M. Varner. 2020. Reviewing Fire, Climate, Deer, & Foundation Spp as Drivers of Historically Open Oak & Pine Forests & Transition to Closed Forests. Front. For. Glob. Change 3:56. doi: 10.3389/ffgc.2020.00056

Hovena, B.M., K.S. Knight, V.E. Peters, and D.L Gorchov. 2022. Woody seedling community responses to deer herbivory, intro shrubs, and ash mortality depend on canopy competition and site wetness. Forest Ecology and Management. 523 (2022) 120488

Johnson, D.J., S.L. Flory, A. Shelton, C. Huebner and Keith Clay. 2015 Interactive effects of a non-native invasive grass Microstegium vimineum and herbivore exclusion on experimental tree regeneration under differing forest management. Journal of Applied Ecology 2015, 52, 210–219 doi: 10.1111/1365-2664.12356

Khadka, H.S. Hong, S. Bardhan. 2024. Investigating the Spatial Pattern of White Oak (Q. alba L.) Mortality Using Ripley’s K Function across the Ten States of the eastern United States. Forests 2024, 15, 1809. https://doi.org/10.3390/f15101809

Miller, K.M., S.J. Perles, J.P. Schmit, E.R. Matthews, and M.R. Marshall. 2023. Overabundant deer and invasive plants drive widespread regeneration debt in eastern United States national parks. Ecological Applications. 2023;33:e2837. https://onlinelibrary.wiley.com/r/eap Open Access

48489

Payne, C.J. and R.K. Peet. 2023. Revisiting the model system for forest succession: Eighty years of resampling Piedmont forests reveals need for an improved suite of indicators of successional change. Ecological Indicators 154 (2023) 110679

Pinchot, C.C., A.A. Royo, J.S. Stanovick, S.E. Schlarbaum, A.M. Sharp, S.L. Anagnostakis. YEAR

Deer browse susceptibility limits c’nut restoration success in northern hardwood forests PUBLIC

Potter, K.M and Riitters, K. 2022. A National Multi-Scale Assessment of Regeneration Deficit as an Indicator of Potential Risk of Forest Genetic Variation Loss. Forests 2022, 13, 19.

https://doi.org/10.3390/f13010019.

Reed, S.P., D.R. Bronson, J.A. Forrester, L.M. Prudent, A.M. Yang, A.M. Yantes, P.B. Reich, and L.E. Frelich. 2023. Linked disturbance in the temperate forest: Earthworms, deer, and canopy gaps. Ecology. 2023;104:e4040. https://onlinelibrary.wiley.com/r/ecy

Shifley, S.R. and W.K. Moser, editors. 2016. Future Forests of the Northern United States

Simpson, A., and Eyler, M.C., 2018, First comprehensive list of non-native species established in three major regions of the United States: U.S. Geological Survey Open-File Report 2018-1156, 15 p., https://doi.org/10.3133/ofr20181156.

ISSN 2331-1258 (online)

Spicer, M.E., A.A. Royo, J.W. Wenzel, and W.P. Carson. 2023. Understory plant growth forms respond independently to combined natural and anthropogenic disturbances. Forest Ecology and Management 543 (2023) 12077

Stern, R.L., P.G. Schaberg, S.A. Rayback, C.F. Hansen, P.F. Murakami, G.J. Hawley. 2023.

Growth trends and environmental drivers of major tree species of the northern hardwood forest of eastern North America J. For. Res. (2023) 34:37–50 https://doi.org/10.1007/s11676-022-01553-7

Stout, S.L., A.T. Hille, and A.A. Royo. 2023. Science-Management Collaboration is Essential to Address Current and Future Forestry Challenges. IN United States Department of Agriculture. Forest Service. 2023. Proceedings of the First Biennial Northern Hardwood Conference 2021: Bridging Science and Management for the Future. Northern Research Station General Technical Report NRS-P-211 May 2023

United States Department of Agriculture, Forest Service. 2023a. Proceedings of the First Biennial Northern Hardwood Conference 2021: Bridging Science and Management for the Future. Northern Research Station General Technical Report NRS-P-211 May 2023

USDA Forest Service Northern Research Station Rooted in Research ISSUE 18 | SEPTEMBER 2023

Kurtz, C.M. 2023. An assessment of invasive plant species in northern U.S. forests. Res. Note NRS-311. http://doi.org/10.2737/NRS-RN-311

United States Department of Agriculture Forest Service General Technical Report NRS-109. An Assessment of Invasive Plant Species Monitored by the Northern Research Station

Forest Inventory and Analysis Program, 2005 through 2010.

Yacucci, A.C., W.P. Carson, J.C. Martineau, C.D. Burns, B.P. Riley, A.A. Royo, T.P. Diggins, I.J. Renne. 2023. Native tree species prosper while exotics falter during gap-phase regeneration, but only where deer densities are near historical levels New Forests https://doi.org/10.1007/s11056-023-10022-w

Posted by Faith Campbell

www.fadingforests.org

Hawaiian Efforts to Restore Threatened Trees

ʻŌhiʻa trees killed by ROD; photo by Richard Sniezko, USFS

Several Hawaiian tree species are at risk due to introduced forest pests. Two of the Islands’ most widespread species are among the at-risk taxa. Their continuing loss would expose watersheds on which human life and agriculture depend. Habitats for hundreds of other species – many endemic and already endangered – would lose their foundations. These trees also are of the greatest cultural importance to Native Hawaiians.

I am pleased to report that Hawaiian scientists and conservationists are trying to protect and restore them.

Other tree species enjoy less recognition … and efforts to protect them have struggled to obtain support.

1) koa (Acacia koa)

Koa is both a dominant canopy tree and the second-most abundant native tree species in Hawai`i in terms of areas covered. The species is endemic to the Hawaiian archipelago. Koa forests provide habitat for 30 of the islands’ remaining 35 native bird species, many of which are listed under the U.S. Endangered Species Act. Also dependent on koa forests are native plant and invertebrate species and the Islands’ only native terrestrial mammal, the Hawaiian hoary bat. Finally, koa forests protect watersheds, add nitrogen to degraded soils, and store carbon [Inman-Narahari et al.]

Koa forests once ranged from near sea level to above 7000 ft (2100 m) on both the wet and dry sides of all the large Hawaiian Islands. Conversion of forests to livestock grazing and row-crop agriculture has reduced koa’s range. Significant koa forests are now found on four islands – Hawai’i, Maui, O‘ahu, and Kauaʻi. More than 90% of the remaining koa forests occur on Hawai`i Island (the “Big Island) [Inman-Narahari et al.]

In addition to its fundamental environmental role, koa has immense cultural importance. Koa represents strength and the warrior spirit. The wood was used traditionally to make sea-going canoes. Now Koa is widely used for making musical instruments, especially guitars and ukuleles; furniture, surfboards, ornaments, and art [Inman-Narahari et al.]

Koa timber has the highest monetary value of any wood harvested on the Islands. However, supplies of commercial-quality trees are very limited (Dudley et al. 2020). Harvesting is entirely from old-growth forests on private land. [Inman-Narahari et al.]

Koa forests are under threat by a vascular wilt disease caused by Fusarium oxysporum f. sp. koae (FOXY). This disease can kill up to 90% of young trees and – sometimes — mature trees in native forests. The fungus is a soil-dwelling organism that spreads in soil and infects susceptible plants through the root system (Dudley et al. 2020).

Conservation and commercial considerations have converged to prompt efforts to breed koa resistant to FOXY. Conservationists hope to restore native forests on large areas where agriculture has declined. The forestry industry seeks to enhance supplies of the Islands’ most valuable wood. Finally, science indicated that a breeding program would probably be successful. Field trials in the 1990s demonstrated great differences in wilt-disease mortality among seed sources (the proportion of seedlings surviving inoculation ranged from 4% to 91.6%) [Sniezko 2003; Dudley et al. 2009].

In 2003, Dudley and Sniezko outlined a long-term strategy for exploring and utilizing genetic resistance in koa. Since then, a team of scientists and foresters has implemented different phases of the strategy and refined it further (Dudley et al. 2012, 2015, 2017; Sniezko et al. 2016]

First, scientists determined that the wilt disease is established on the four main islands. Having obtained more than 500 isolates of the pathogen from 386 trees sampled at 46 sites, scientists tested more than 700 koa families from 11 ecoregions for resistance against ten of the most highly virulent isolates (Dudley et al. 2020).

The Hawaiian Agricultural Research Center (HARC), supported by public and private partners, has converted the field-testing facilities on Hawai`i, Maui, and Oahu into seed orchards. The best-performing tree families are being grown to maturity to produce seeds for planting. It is essential that the seedlings be not just resistant to FOXY but also adapted to the ecological conditions of the specific site where they are to be planted [Dudley et al. 2020; Inman-Narahari et al. ] Locally adapted, wilt-resistant seed has been planted on Kauaʻi and Hawai`i. Preparations are being made to plant seed on Maui and O‘ahu also. Scientists are also exploring methods to scale up planting in both restoration and commercial forests [R. Hauff pers. comm.].

Restoration of koa on the approximately half of lands in the species’ former range that are privately owned will require that the trees provide superior timber. Private landowners might also need financial incentives since the rotation time for a koa plantation is thought to be 30-80 years. [Inman-Narahari et al.]

Plantings on both private and public lands will need to be protected from grazing by feral ungulates and encroachment by competing plants. These management actions are intensive, expensive, and must be maintained for years.

Some additional challenges are scientific: uncertainties about appropriate seed zones, efficacy of silvicultural approaches to managing the disease, and whether koa can be managed for sustainable harvests. Human considerations are also important: Hawai`i lacks sufficient professional tree improvement or silvicultural personnel, a functioning seed distribution and banking network — and supporting resources. Finally, some segments of the public oppose ungulate control programs. Inman-Narahari et al.

Finally, scientists must monitor seed orchards and field plantings for any signs of maladaptation to climate change. (Dudley et al. 2020).

2) ʻŌhiʻa Metrosideros polymorpha)

ʻŌhiʻa lehua is the most widespread tree on the Islands. It dominates approximately 80% the biomass of Hawaii’s remaining native forest, in both wet and dry habitats. ʻŌhiʻa illustrates adaptive radiation and appears to be undergoing incipient speciation. The multitude of ecological niches and their isolation on the separate islands has resulted in five recognized species in the genus Metrosideros. Even the species found throughout the state, Metrosideros polymorpha, has eight recognized varieties (Luiz et al. (2023) (some authorities say there are more).

Loss of this iconic species could result in significant changes to the structure, composition, and potentially, the function, of forests on a landscape level. High elevation ‘ohi‘a forests protect watersheds across the state. ʻŌhiʻa forests shelter the Islands’ one native terrestrial mammal (Hawaiian hoary bat), 30 species of forest birds, and more than 500 endemic arthropod species. Many species in all these taxa are endangered or threatened (Luiz et al. 2023). The increased light penetrating interior forests following canopy dieback facilitates invasion by light-loving non-native plant species, of which Hawai`i has dozens. There is perhaps no other species in the United States that supports more endangered taxa or that plays such a geographical dominant ecological keystone role [Luiz et al. 2023]

For many Native Hawaiians, ‘ōhi‘a is a physical manifestation of multiple Hawaiian deities and the subject of many Hawaiian proverbs, chants, and stories; and foundational to the scared practice of many hula. The wood has numerous uses. Flowers, shoots, and aerial roots are used medicinally and for making lei. The importance of the biocultural link between ‘ōhi‘a and the people of Hawai`i is described by Loope and LaRosa (2008) and Luiz et al. (2023).

In 2010 scientists detected rapid mortality affecting ‘ōhi‘a on Hawai‘i Island. Scientists determined that the disease is caused by two recently-described pathogenic fungi, Ceratocystis lukuohia and Ceratocystis huliohia. The two diseases, Ceratocystis wilt and Ceratocystis canker of ʻōhiʻa, are jointly called “rapid ‘ōhi‘a death”, or ROD. The more virulent species, C. lukuohia, has since spread across Hawai`i Island and been detected on Kaua‘i. The less virulent C. huliohia is established on Hawai`i and Kaua‘i and in about a dozen trees on O‘ahu. One tree on Maui was infected; it was destroyed, and no new infection has been detected [M. Hughes pers. comm.] As of 2023, significant mortality has occurred on more than one third of the vulnerable forest on Hawai`i Island, although mortality is patchy.

[ʻŌhiʻa is also facing a separate disease called myrtle rust caused by the fungus Austropuccinia psidii; to date this rust has caused less virulent infections on ‘ōhi‘a.]

rust-killed ‘ōhi‘a in 2016; photo by J.B. Friday

Because of the ecological importance of ‘ōhi‘a and the rapid spread of these lethal diseases, research into possible resistance to the more virulent pathogen, C. lukiohia began fairly quickly, in 2016. Some ‘ōhi‘a survive in forests on the Big Island in the presence of ROD, raising hopes that some trees might possess natural resistance. Scientists are collecting germplasm from these lightly impacted stands near high-mortality stands (Luiz et al. 2023). Five seedlings representing four varieties of M. polymorpha that survived several years’ exposure to the disease are being used to produce rooted cuttings and seeds for further evaluation of these genotypes.

Encouraged by these developments, and recognizing the scope of additional work needed, in 2018 stakeholders created a collaborative partnership that includes state, federal, and non-profit agencies and entities, ʻŌhiʻa Disease Resistance Program (‘ODRP) (Luiz et al. 2023). The partnership seeks to provide baseline information on genetic resistance present in all Hawaiian taxa in the genus Metrosideros. It aims further to develop sources of ROD-resistant germplasm for restoration intended to serve several purposes: cultural plantings, landscaping, and ecological restoration. ‘ODRP is pursuing screenings of seedlings and rooted cuttings sampled from native Metrosideros throughout Hawai`i while trying to improve screening and growing methods. Progress will depend on expanding these efforts to include field trials; research into environmental and genetic drivers of susceptibility and resistance; developing remote sensing and molecular methods to rapidly detect ROD-resistant individuals; and support already ongoing Metrosideros conservation. If levels of resistance in wild populations prove to be insufficient, the program will also undertake breeding (Luiz et al. 2023).

To be successful, ‘ODRP must surmount several challenges (Luiz et al. 2022):

increase capacity to screen seedlings from several hundred plants per year to several thousand;
optimize artificial inoculation methodologies;
determine the effects of temperature and season on infection rates and disease progression;
find ways to speed up seedlings’ attaining sufficient size for testing;
develop improved ways to propagate ʻōhiʻa from seed and rooted cuttings;
establish sites for field testing of putatively resistant trees across a wide range of climatic and edaphic conditions;
establish seed orchard, preferably on several islands;
establish systems for seed collection from the wide variety of subspecies/varieties;
if breeding to enhance resistance is appropriate, it will be useful to develop high-throughput phenotyping of the seed orchard plantings.

[See DMF profile for more details.]

Developing ROD-resistant ‘ōhi‘a is only one part of a holistic conservation program. Luiz et al. (2023) reiterate the importance of quarantines and education to curtail movement of infected material and countering activities that injure the trees. Fencing to protect these forests from grazing by feral animals can drastically reduce the amount of disease. Finally, scientists must overcome the factors there caused the almost complete lack of natural regeneration of ‘ōhi‘a in lower elevation forests. Most important are competition by invasive plants, predation by feral ungulates, and the presence of other diseases, e.g., Austropuccinia psidii.

Hawaii’s dryland forests are highly endangered: more than 90% of dry forests are already lost due to habitat destruction and the spread of invasive plant and animal species. Two tree species are the focus of species-specific programs aimed at restoring them to remaining dryland forests. However, support for both programs seems precarious and requires stable long-term funding; disease resistance programs often necessitate decades-long endeavors.

naio in bloom; photo by Forrest & Kim Starr via Creative Commons

1) naio (Myoporum sandwicense)

Naio grows on all of the main Hawaiian Islands at elevations ranging from sea level to 3000 m. While it occurs in the full range of forest types from dry to wet, naio is one of two tree species that dominate upland dry forests. The other species is mamane, Sophora chrysophylla. Naio is a key forage tree for two endangered honeycreepers, palila (Loxioides bailleui) and `akiapola`au (Hemignathus munroi). The tree is also an important host of many species of native yellow-face bees (Hylaeus spp). Finally, loss of a native tree species in priority watersheds might lead to invasions by non-native plants that consume more water or increase runoff.

The invasive non-native Myoporum thrips, Klambothrips myopori, was detected on Hawai‘i Island in December 2008 (L. Kaufman website). In 2018 the thrips was found also on Oahu (work plan). The Myoporum thrips feeds on and causes galls on plants’ terminal growth. This can eventually lead to death of the plant.

Aware of thrips-caused death of plants in the Myoporum genus in California, the Hawaii Department of Lands and Natural Resources Division of Forestry and Wildlife and the University of Hawai‘i began efforts to determine the insect’s distribution and infestation rates, as well as the overall health of naio populations on the Big Island. This initiative began in September 2010, nearly two years after the thrips’ detection. Scientists monitored nine protected natural habitats for four years. This monitoring program was supported by the USFS Forest Health Protection program. This program is described by Kaufman.

naio monitoring sites from L. Kaufman article

The monitoring program determined that by 2013, the thrips has spread across most of Hawi`i Island, on its own and aided by human movement of landscaping plants. More than 60% of trees being monitored had died. Infestation and dieback levels had both increased, especially at medium elevation sites. The authors feared that mortality at high elevations would increase in the future. They found no evidence that natural enemies are effective controlling naio thrips populations on Hawai`i Island.

Kaufman was skeptical that biological control would be effective. She suggested, instead, a breeding program, including hybridizing M. sandwicensis with non-Hawaiian Myoporum species that appear to be resistant to thrips. Kaufman also called for additional programs: active monitoring to prevent thrips from establishing on neighboring islands; and collection and storage of naio seeds.

Ten years later, in February 2024, DLNR Division of Forestry and Wildlife adopted a draft work plan for exploring possible resistance to the Myoporum thrips. Early steps include establishing a database to record data needed to track parent trees, associated propagules, and the results of tests. These data are crucial to keeping track of which trees show the most promise. Other actions will aim to hone methods and processes. Among practical questions to be answered are a) whether scientists can grow even-aged stands of naio seedlings; b) identifying the most efficient resistance screening techniques; and c) whether K. myopori thrips are naturally present in sufficient numbers to be used in tests, or – alternatively – whether they must be augmented. [Plan]

Meanwhile, scientists have begun collecting seed from unaffected or lightly affected naio in hotspots where mortality is high. They have focused on the dry and mesic forests of the western side of Hawai`i (“Big”) Island, where the largest number of naio populations still occur and are at high risk. Unfortunately, these “lingering” trees remain vulnerable to other threats, such as browsing by feral ungulates, competition with invasive plants, drought, and reduced fecundity & regeneration.

Hawai`i DLNR has secured initial funding from the Department of Defense’s REPI program to begin a pest resistance project and is seeking a partnership with University of Hawai`i to carry out tests “challenging” different naio families’ resistance to the thrips [R. Hauff pers. comm.]

2) wiliwili (Erythrina sandwicensis)

Efforts to protect the wiliwili have focused on biological control. The introduced Erythrina gall wasp, Quadrastichus erythrinae (EGW) was detected on the islands in 2005. It immediately caused considerable damage to the native tree and cultivated nonnative coral trees.

A parasitic wasp, Eurytoma erythrinae, was approved for release in November 2008 – only 3 ½ years after EGW was detected on O‘ahu. The parasitic wasp quickly suppressed the gall wasp’s impacts to both wiliwili trees and non-native Erythrina. By 2024, managers are once again planting the tree in restoration projects.

However, both the gall wasp and a second insect pest – a bruchid, Specularius impressithorax – can cause loss of more than 75% of the seed crop. This damage means that the tree cannot regenerate. By 2019, Hawaiian authorities began seeking permission to release a second biocontrol gent, Aprostocitus nites.Unfortunately, the Hawai’i Department of Agriculture still has not approved the release permit despite five years having passed. Once they have this approval, the scientists will then need to ask USDA Animal and Plant Health Inspection Service (APHIS) for its approval [R. Hauff, pers. comm.]

SOURCES

www.RapidOhiaDeath.org

Dudley, N., R. James, R. Sniezko, P. Cannon, A. Yeh, T. Jones, & Michael Kaufmann. 2009? Operational Disease Screening Program for Resistance to Wilt in Acacia koa in Hawai`i. Hawai`i Forestry Association Newsletter August 29 2009

Dudley, N., T. Jones, K. Gerber, A.L. Ross-Davis, R.A. Sniezko, P. Cannon & J. Dobbs. 2020. Establishment of a Genetically Diverse, Disease-Resistant Acacia koa Seed Orchard in Kokee, Kauai: Early Growth, Form, & Survival. Forests 2020, 11, 1276; doi:10.3390/f11121276 www.mdpi.com/journal/forests

Friday, J. B., L. Keith, and F. Hughes. 2015. Rapid ʻŌhiʻa Death (Ceratocystis Wilt of ʻŌhiʻa). PD-107, College of Tropical Agriculture and Human Resources, University of Hawai‘i, Honolulu, HI. URL: https://www.ctahr.HI.edu/oc/freepubs/pdf/PD-107.pdf Accessed April 3, 2018.

Friday, J.B. 2018. Rapid ??hi?a Death Symposium -West Hawai`i (“West Side Symposium”) March 3rd 2018, https://vimeo.com/258704469 Accessed April 4, 2018 (see also full video archive at https://vimeo.com/user10051674)

Inman-Narahari, F., R. Hauff, S.S. Mann, I. Sprecher, & L. Hadway. Koa Action Plan: Management & research priorities for Acacia koa forestry in Hawai`i. State of Hawai`i Department of Land & Natural Resources Division of Forestry & Wildlife no date

Kaufman, L.V, J. Yalemar, M.G. Wright. In press. Classical biological control of the erythrina gall wasp, Quadrastichus erythrinae, in Hawaii: Conserving an endangered habitat. Biological Control. Vol. 142, March 2020

Loope, L. and A.M. LaRosa. 2008. ‘Ohi’a Rust (Eucalyptus Rust) (Puccinia psidii Winter) Risk Assessment for Hawai‘i.

Luiz, B.C. 2017. Understanding Ceratocystis. sp A: Growth, morphology, and host resistance. MS thesis, University of Hawai‘i at Hilo.

Luiz, B.C., C.P. Giardina, L.M. Keith, D.F. Jacobs, R.A. Sniezko, M.A. Hughes, J.B. Friday, P. Cannon, R. Hauff, K. Francisco, M.M. Chau, N. Dudley, A. Yeh, G. Asner, R.E. Martin, R. Perroy, B.J. Tucker, A. Evangelista, V. Fernandez, C. Martins-Keli’iho.omalu, K. Santos, R. Ohara. 2023. A framework for establishlishing a rapid ‘Ohi‘a death resistance program New Forests 54, 637–660. https://doi.org/10.1007/s11056-021-09896-5

Additional information on the koa resistance program is posted at http://www.harc-hspa.com/forestry.html

Sniezko, R.A., N. Dudley, T. Jones, & P. Cannon. 2016. Koa wilt resistance & koa genetics – key to successful restoration & reforestation of koa (Acacia koa). Acacia koa in Hawai‘i: Facing the Future. Proceedings of the 2016 Symposium, Hilo, HI: www.TropHTIRC.org , www.ctahr.HI.edu/forestry

Posted by Faith Campbell

www.fadingforests.org

Scientists: Introduced forest pest reshaping forests, with many bad consequences … will regulators step up?

The number of introduced forest pathogens are increasing – creating a crisis that is recognized by more scientists. These experts say tree diseases are reshaping both native and planted forests around the globe. The diseases are threatening biodiversity, ecosystem services, provision of products, and related human wellbeing. Some suggest that bioinvasions might threaten forests as much as climate change, while also undermining forests’ role in carbon sequestration.

Unfortunately, I see little willingness within the plant health regulatory community to tackle improving programs to slow introductions. Even when the scientists documenting the damage work for the U.S. Department of Agriculture – usually the U.S. Forest Service — USDA policy-makers don’t act on their findings. [I tried to spur a conversation with USDA 2 years ago. So far, no response.]

counties where beech leaf disease has been detected

What the scientists say about these pests’ impacts

Andrew Gougherty (2023) – one of the researchers employed by the USDA Forest Service – says that emerging infectious tree diseases are reshaping forests around the globe. Furthermore, new diseases are likely to continue appearing in the future and threaten native and planted forests worldwide. [Full references are provided at the end of the blog.] Haoran Wu (2023/24) – a Master’s Degree student at Oxford University – agrees that arrival of previously unknown pathogens are likely to alter the structure and composition of forests worldwide. Weed, Ayers, and Hicke (2013) [academics] note that forest pests — native and introduced — are the dominant sources of disturbance to North American forests. They suggest that, globally, bioinvasions might be at least as important as climate change as threats to the sustainability of forest ecosystems. They are concerned that recurrent forest disturbances caused by pests might counteract carbon mitigation strategies.

Scientists have proclaimed these warnings for years. Five years ago, Fei et al. (2019) reported that the 15 most damaging pests introduced to the United States — cumulatively — had already caused tree mortality to exceed background levels by 5.53 teragrams of carbon per year. As these 15 pests spread and invasions intensify, they threaten 41.1% of the total live forest biomass in the 48 coterminous states. Poland et al. (2019) (again – written by USFS employees) document the damage to America’s forest ecosystems caused by the full range of invasive species, terrestrial and aquatic.

Fei et al. and Weed, Ayers, and Hicke (2013) also support the finding that old, large trees are the most important trees with regard to carbon storage. This understanding leads them to conclude that the most damaging non-native pests are the emerald ash borer, Dutch elm disease fungi, beech bark disease, and hemlock woolly adelgid. As I pointed out in earlier blogs, other large trees, e.g., American chestnut and several of the white pines, were virtually eliminated from much of their historical ranges by non-native pathogens decades ago. These same large, old, trees also maintain important aspects of biological diversity.

It is true that not all tree species are killed by any particular pest. Some tree genera or species decrease while others thrive, thus altering the species composition of the affected stands (Weed, Ayers, and Hicke). This mode of protection is being undermined by the proliferation of insects and pathogens that cumulatively attack ever more tree taxa. And while it is true that some of the carbon storage capacity lost to pest attack will be restored by compensatory growth in unaffected trees, this faster growth is delayed by as much as two or more decades after pest invasions begin (Fei et al.).

ash forest after EAB infestation; Photo by Nate Siegert, USFS

Still, despite the rapid rise of destructive tree pests and disease outbreaks, scientists cannot yet resolve critical aspects of pathogens’ ecological impacts or relationship to climate change. Gougherty notes that numerous tree diseases have been linked to climate change or are predicted to be impacted by future changes in the climate. However, various studies’ findings on the effects of changes in moisture and precipitation are contradictory. Wu reports that his study of ash decline in a forest in Oxfordshire found that climate change will have a very small positive impact on disease severity through increased pathogen virulence. Weed, Ayers, and Hicke go farther, making the general statement that despite scientists’ broad knowledge of climate effects on insect and pathogen demography, they still lack the capacity to predict pest outbreaks under climate change. As a result, responses intended to maintain ecosystem productivity under changing climates are plagued by uncertainty.

Clarifying how disease systems are likely to interact with predicted changes in specific characteristics of climate is important — because maintaining carbon storage levels is important. Quirion et al. (2021) estimate that, nation-wide, native and non-native pests have decreased carbon sequestration by live forest trees by at least 12.83 teragrams carbon per year. This equals approximately 9% of the contiguous states’ total annual forest carbon sequestration and is equivalent to the CO₂ emissions from more than 10 million passenger vehicles driven for one year. Continuing introductions of new pests, along with worsening effects of native pests associated with climate change, could cause about 30% less carbon sequestration in living trees. These impacts — combined with more frequent and severe fires and other forest disturbances — are likely to negate any efforts to improve forests’ capacity for storing carbon.

Understanding pathogens’ interaction with their hosts is intrinsically complicated. There are multiple biological and environmental factors. What’s more, each taxon adapts individually to the several environmental factors. Wu says there is no general agreement on the relative importance of the various environmental factors. The fact that most forest diseases are not detected until years after their introduction also complicates efforts to understand factors affecting infection and colonization.

The fungal-caused ash decline in Europe is a particularly alarming example of the possible extent of such delays. According to Wu, when the disease was first detected – in Poland in 1992 – it had already been present perhaps 30 years, since the 1960s. Even then, the causal agent was not isolated until 2006 – or about 40 years after introduction. The disease had already spread through about half the European continent before plant health officials could even name the organism. The pathogen’s arrival in the United Kingdom was not detected until perhaps five years after its introduction – despite the country possessing some of the world’s premier forest pathologists who by then (2012) knew what they to look for.

Clearly, improving scientific understanding of forest pathogens will be difficult. In addition, effective policy depends on understanding the social and economic drivers of trade, development, and political decisions are primary drivers of the movement of pathogens. Wu calls for collaboration of ecologists, geneticists, earth scientists, and social scientists to understand the complexity of the host-pathogen-surrounding system. Bringing about this new way of working and obtaining needed resources will take time – time that forests cannot afford.

However, Earth’s forests are under severe threat now. Preventing their collapse depends on plant health officials integrating recognition of these difficulties into their policy formulation. It is time to be realistic: develop and implement policies that reflect the true level of threat and limits of current science.

Background: Rising Numbers of Introductions

Gougherty’s analysis of rising detections of emerging tree diseases found little evidence of saturation globally – in accord with the findings of Seebens et al. (2017) regarding all taxa. Relying on data for 24 tree genera, nearly all native to the Northern Hemisphere, Gougherty found that the number of new pests attacking these tree genera are doubling on average every 11.2 years. Disease accumulation is increasing rapidly in both regions where hosts are native and where they are introduced, but more rapidly in trees’ native ranges.This finding is consistent with most new diseases arise from introductions of pathogens to naïve hosts.

Gougherty says his estimates are almost certainly underestimates for a number of reasons. Countries differ in scientific resources and their scientists’ facility with English. Scientists are more likely to notice and report high-impact pathogens and those in high-visibility locations. Where national borders are closer, e.g., in Europe, a minor pest expansion can be reported as “new” in several countries. New pathogens in North America appear to occur more slowly, possibly because the United States and Canada are very large. He suggests that another possible factor is the U.S. (I would add Canada) have adopted pest-prevention regulations that might be more effective than those in place in other regions. (See my blogs and the Fading Forest reports linked to below for my view of these measures’ effectiveness.)

Wu notes that reports of tree pathogens in Europe began rising suddenly after the 1980s. He cites the findings by Santini et al. (2012) that not only were twice as many pathogens detected in the period after 1950 than in the previous 40 years, the region of origin also changed. During the earlier period, two-thirds of the introduced pathogens came from temperate North America. After 1950, about one-third of previously unknown disease agents were from temperate North America. Another one-third was from Asia. By 2012, more than half of plant infectious diseases were caused by introduction of previously unknown pathogens.

What is to be done?

Most emerging disease agents do not have the same dramatic effects as chestnut blight in North America, ash dieback in Europe, or Jarrah dieback in Australia. Nevertheless, as Gougherty notes, their continued emergence in naïve biomes increases the likelihood of especially damaging diseases emerging and changing forest community composition.

Gougherty calls for policies intended to address both the agents being introduced through trade, etc., and those that emerge from shifts in virulence or host range of native pathogens or changing environmental conditions. In his view, stronger phytosanitary programs are not sufficient.

Wu recommends enhanced monitoring of key patterns of biodiversity and ecosystem functioning, He says these studies should focus on the net outcome of complex interactions. Wu also calls for increasing understanding of key “spillover” effects – outcomes that cannot be currently assessed but might impact the predicted outcome. He lists several examples:

the effects of drought–disease interactions on tree health in southern Europe,
interaction between host density and pathogen virulence,
reproductive performance of trees experiencing disease,
effect of secondary infections,
potential for pathogens to gain increased virulence through hybridization.
potential for breeding resistant trees to create a population buffer for saving biological diversity. Wu says his study of ash decline in Oxfordshire demonstrates that maintaining a small proportion of resistant trees could help tree population recovery.

Quirion et al. provide separate recommendations with regard to native and introduced pests. To minimize damage from the former, they call for improved forest management – tailored to the target species and the environmental context. When confronting introduced pests, however, thinning is not effective. Instead, they recommend specific steps to minimize introductions via two principal pathways, wood packaging and imports of living plants. In addition, since even the most stringent prevention and enforcement will not eliminate all risk, Quirion et al. advocate increased funding for and research into improved strategies for inspection, early detection of new outbreaks, and strategic rapid response to newly detected incursions. Finally, to reduce impacts of established pests, they recommend providing increased and more stable funding for classical biocontrol, research into technologies such as sterile-insect release and gene drive, and host resistance breeding.

Remember: reducing forest pest impacts can simultaneously serve several goals—carbon sequestration, biodiversity conservation, and perpetuating the myriad economic and societal benefits of forests. See Poland et al. and the recent IUCN report on threatened tree species.

SOURCES

Barrett, T.M. and G.C. Robertson, Editors. 2021. Disturbance and Sustainability in Forests of the Western United States. USDA Forest Service Pacific Northwest Research Station. General Technical Report PNW-GTR-992. March 2021

Clark, P.W. and A.W. D’Amato. 2021. Long-term development of transition hardwood and Pinus strobus – Quercus mixedwood forests with implications for future adaptation and mitigation potential. Forest Ecology and Management 501 (2021) 119654

Fei, S., R.S. Morin, C.M. Oswalt, and A.M. 2019. Biomass losses resulting from insect and disease invasions in United States forests. Proceedings of the National Academy of Sciences. www.pnas.org/cgi/doi/10.1073/pnas.1820601116

Gougherty AV (2023) Emerging tree diseases are accumulating rapidly in the native and non-native ranges of Holarctic trees. NeoBiota 87: 143–160. https://doi.org/10.3897/neobiota.87.103525

Lovett, G.M., C.D. Canham, M.A. Arthur, K.C. Weathers, and R.D. Fitzhugh. 2006. Forest Ecosystem Responses to Exotic Pests and Pathogens in Eastern North America. BioScience Vol. 56 No. 5 May 2006

Lovett, G.M., M. Weiss, A.M. Liebhold, T.P. Holmes, B. Leung, K.F. Lambert, D.A. Orwig, F.T. Campbell, J. Rosenthal, D.G. MCCullough, R. Wildova, M.P. Ayres, C.D. Canham, D.R. Foster, S.L. Ladeau, and T. Weldy. 2016. Nonnative forest insects and pathogens in the United States: Impacts and policy options. Ecological Applications, 26(5), 2016, pp. 1437-1455

Poland, T.M., Patel-Weynand, T., Finch, D., Miniat, C. F., and Lopez, V. (Eds) (2019), Invasive Species in Forests and Grasslands of the United States: A Comprehensive Science Synthesis for the United States Forest Sector. Springer Verlag.

Quirion, B.R., G.M. Domke, B.F. Walters, G.M. Lovett, J.E. Fargione, L. Greenwood, K. Serbesoff-King, J.M. Randall, and S. Fei. 2021 Insect and Disease Disturbance Correlate With Reduced Carbon Sequestration in Forests of the Contiguous US. Front. For. Glob. Change 4:716582. [Volume 4 | Article 716582] doi: 10.3389/ffgc.2021.716582

Weed, A.S., M.P. Ayers, and J.A. Hicke. 2013. Consequences of climate change for biotic disturbances in North American forests. Ecological Monographs, 83(4), 2013, pp. 441–470

Wu, H. 2023/24. Modelling Tree Mortality Caused by Ash Dieback in a Changing World: A Complexity-based Approach MSc/MPhil Dissertation Submitted August 12, 2024. School of Geography and the Environment, Oxford University.

Posted by Faith Campbell

www.fadingforests.org

Impacts of introduced rust on unique flora — New Zealand’s expectations

predicted community vulnerability from A. psidii mediated mortality of Kunzea ericoides & Leptospermum scoparium; from McCarthy et al.

Scientists in New Zealand have recently completed a study of the probable impact of myrtle rust – caused by Austropuccinia psidii – on plants in the plant family Myrtaceae. McCarthy et al. say their results should guide management actions to protect not only the unique flora of those islands but also on Australia and Hawai`i – other places where key dominant tree species are susceptible to myrtle rust. The disease attacks young tissue; susceptible Myrtaceae become unable to recruit new individuals or to recover from disturbance. Severe cases can result in tree death & localized extinctions

[I note that myrtle rust is not the only threat to the native trees of these biologically unique island systems. New Zealand’s largest tree, kauri (Agathis australis), is threatened by kauri dieback (caused by Phytophthora agathidicida). On Hawai`i, while the most widespread tree, ‘ōhi‘a (Metrosideros polymorpha) is somewhat vulnerable to the strain of rust introduced to the Islands, the greater threat is from a different group of fungi, Ceratocystis lukuohia and C. huliohia, collectively known as rapid ‘ōhi‘a death. On Australia, hundreds of endemic species on the western side of the continent are being killed by Phytophthora dieback, caused by Phytophthora cinnamomi. [I note the proliferation of tree-kiling pathogens; I will blog more about this in the near future.]

Myrtle rust arrived in New Zealand in 2017, probably blown on the wind from Australia (where it was detected in 2010). In New Zealand, myrtle rust infects at least 12 of 18 native tree, shrub, and vine species in the Myrtaceae plant family. Several of these species are important in the structure and succession of native ecosystems. They also have enormous cultural significance.

McCarthy et al. note that species differ in their contribution to forest structure and function. They sought to determine where loss of vulnerable species might have the greatest impact on community functionality. They also explored whether compensatory infilling by co-occurring, non-vulnerable species in the Myrtaceae would reduce the community’s vulnerability. Even when co-occurring Myrtaceae are relatively immune to the pathogen, only some of them – the fast-growing species – are likely to fill the gaps. They might lack the functional attributes of the decimated species.

To identify areas at greatest risk, McCarthy et al. took advantage of a nationwide vegetation plot dataset that covers all the country’s native forests and shrublands. The plot data enabled McCarthy et al. to determine which plant species not vulnerable to the rust are present and so are likely to replace the rust host species as they are killed.

*Leptospermum scoparium*; photo by Alyenaa Buckles via Flickr

McCarthy et al. concluded that forests and shrublands containing Kunzea ericoides and Leptospermum scoparium are highly vulnerable to their loss. Ecosystems with these species are found predominantly in central and southeastern North Island, northeastern South Island, and Stewart Island. While compensatory infilling by other species in the Myrtaceae would moderate the impact of the loss of vulnerable species, if these co-occurring species were unable to respond for various reasons, such as also being infected by the rust pathogen, community vulnerability almost always increased. In these cases the infilling species would probably have different functional attributes. In many areas the species most likely to replace the rust-killed native species would be non-native shrubs. Consequently, early successional woody plant communities, where K. ericoides and L. scoparium dominate, are at most risk.

Because the risk of A. psidii infection is lower in cooler montane and southern coastal areas, parts of inland Fiordland, the northwestern South Island and the west coast of the North Island might be less vulnerable.

Austropuccinia psidii has been spreading in Myrtaceae-dominated forests of the Southern Hemisphere since the beginning of the 21^st Century. It was detected in Hawai`i in 2005; in Australia in 2010; in New Caledonia in 2013, and finally in New Zealand in 2017. Within 12 months of its first detection in the northern part of the North Island it had spread to the northern regions of the South Island.

Specific types of Threat

Succession

The ecosystem process most at risk to loss of Myrtaceae species to A. psidii is succession. About 10% of once-forested areas of New Zealand are in successional shrublands, mostly dominated by Kunzea ericoides and Leptospermum scoparium. Both species are wind dispersed, grow quickly, are resistant to browsing by introduced deer, and are favored by disturbance, especially fire. Both are tolerant of exposure and have a wide edaphic range (including geothermal soils). Still, K. ericoides prefers drier, warmer sites while L. scoparium tolerates saturated soils, frost hollows and subalpine settings.

*Kunzea ericoides*; photo by Tony Foster via Flickr

Loss of these two species would result in a considerable change in stand-level functional composition across a wide variety of locations. Their extensive ranges mean that it would be difficult for other species – even if functionally equivalent – to expand sufficiently quickly. Second, non-native species are common in these communities. All of these invaders – Ulex europaeus, Cytisus scoparius and species of Acacia, Hakea and Erica – promote fire. Some are nitrogen fixers. While they can facilitate succession, the resulting native forest will differ from that formed via Leptospermeae succession. Furthermore, compensatory infilling by the invasive species might also reduce carbon sequestration. Successional forests dominated by K. ericoides are significant carbon sinks owing to the tree’s size (up to 25 m under favorable conditions), high wood density, and long lifespan (up to ~150 years). In contrast, shrublands dominated by at least one of the non-native species, U. europaeus, are significant carbon sources.

Northern and central regions of the North Island and the northeastern and interior parts of the South Island are most vulnerable to the loss of these species since these successional shrub communities are widespread and the area’s climate is highly suitable for A. psidii infection. The southern regions of the South Island, including Stewart Island, are somewhat protected by the cooler climate.

Fortunately, neither Kunzea ericoides nor Leptospermum scoparium has yet been infected in nature. Laboratory trials indicate that some families of K. ericoides are resistant. Vulnerability also varies among types of tissue – i.e., leaf, stem, seed capsule.

*Metrosideros umbellata*; photo by Stan Shebs via Wikimedia

Forest biomass

Although from the overall community perspective loss of species in the Metrosidereae would have a lower impact than loss of those in the Leptospermeae, there would be significant changes associated with loss of Metrosideros umbellata. This species can grow quite large (dbh often > 2 m; heights up to 20 m). That size and its exceptionally dense wood means that M. umbellata stores high amounts of carbon. Also, its slow decomposition provides habitat for decomposers. Lessening the potential impact of loss of this species are two facts: its litter nutrient concentrations and decomposition rates do not differ from dominant co-occurring trees; and, most important, it grows primarily in the south, where weather conditions are less suitable for A. psidii infection. One note of caution: if A. psidii proves able to spread into these regions, not only M. umbellata but also susceptible co-occurring Myrtaceae species are likely to be damaged by the pathogen.

Highly specific habitats

McCarthy et al. note that their study might underestimate the impact of loss of species with unique traits that occupy specialized habitats. They focus on the climber Metrosideros excelsa. This is an important successional species that helps restore ecosystems following fire, landslides, or volcanic eruptions. The species’ tough and nutrient poor leaves promote later successional species by forming a humus layer and altering the microenvironment beneath the plant. Its litter has high concentrations of phenolics and decomposes more slowly than any co-occurring tree species. [They say its role is analogous to that of M. polymorpha in primary successions on lava flows in Hawai`i.] M. excelsa dominates succession on many small offshore volcanic islands, rocky coastal headlands and cliffs.

Another example is Lophomyrtus bullata, a small tree that is patchily distributed primarily in forest margins and streamside vegetation. This is the native species most affected by A. psidii; the pathogen is likely to cause its localized extinction. McCarthy et al. call for assessment of ex situ conservation strategies for this species.

Each of these species is represented in only seven of the plots used in the analysis, so community vulnerability to their loss might be underestimated.

Another habitat specialist, Syzygium maire, is found mostly in lowland forests, usually on saturated soils. It currently occupies only a fraction of its natural range due to deforestation and land drainage. Evaluating the impact of loss of S. maire is complicated by its poor representation in the database (only six plots), and the fact that many of the co-occurring species are also Myrtaceae.

Lack of data similarly prevents detailed assessment of the impacts from possible loss of other species, including M. parkinsonii, M. perforata and L. obcordata. McCarthy et al. say only that their disappearance will “take the community even further from its original state”.

McCarthy et al. warn that the risk could increase if more virulent strains of A. psidii were introduced or evolved through sexual recombination of the current pandemic strain. Other scientists have discovered strong evidence that the many strains of A. psidii attack different host species (see Costa da Silva et al. 2014).

New Zealand bell bird (*Anthornis melanura*); photo from https://animalia.bio/new-zealand-bellbird

McCarthy et al. note that other factors are also important in determining the impact of loss of a plant species. Especially significant is the host plant species’ association with other species. They say these relationships are poorly understood. One example is that only four Myrtaceae species produce fleshy fruits. Loss or decline of these four species might severely affect populations of native birds, many of which are endemic. Many invertebrates – also highly endemic — are dependent on nectar from other plants in the family.

In their conclusion, McCarthy et al. note that A. psidii has been introduced relatively recently so there is still time to reduce the disease’s potential consequences. They suggest such management interventions as identifying and planting resistant genotypes and applying chemical controls to protect important individual specimens. They hope their work will guide prioritization of both species and spatial locations. They believe such efforts have substantial potential to reduce myrtle rust’s overall functional impact to New Zealand’s unique ecosystems.

SOURCES

Costa da Silva, A; P.M. Teixeira de Andrade, A. Couto Alfenas, R. Neves Graca, P. Cannon, R. Hauff, D. Cristiano Ferreira, and S. Mori. 2014. Virulence and Impact of Brazilian Strains of Puccinia psidii on Hawaiian Ohia (Metrosideros polymorpha). Pacific Science 68(1):47-56. doi: https://dx.doi.org/10.2984/68.1.4

McCarthy, J.K., S.J. Richardson, I. Jo, S.K. Wiser, T.A. Easdale, J.D. Shepherd, P.J. Bellingham. 2024. A Functional Assessment of Community Vulnerability to the Loss of Myrtaceae From Myrtle Rust. Diversity & Distributions, 2024; https://doi.org/10.1111/ddi.13928

Posted by Faith Campbell

www.fadingforests.org

New Attention to Threats to Trees — While They Worsen

ohia (*Metrosideros polymorpha*) — one subspecies designated as Vulnerable due to restricted range
The species is under attack by rapid ohia death [https://www.dontmovefirewood.org/pest_pathogen/ceratocystis-wilt-ohi-html/]

I welcome new attention to the threats posed to tree species around world.

Last week, at the conclusion of Conference of the Parties (COP) to the Convention on Biodiversity (CBD), the International Union for the Conservation of nature (IUCN) released its most recent iteration of the Red List of Threatened Species. The headline was that 38% of the world’s trees are at risk of extinction.

This is the finding of a decade-long Global Tree Assessment. The assessment was led by Botanic Gardens Conservation International and IUCN’s Species Survival Commission Global Tree Specialist Group. Partners in the effort included Conservation International, NatureServe, Missouri Botanical Garden and Royal Botanic Gardens, Kew. The project was funded primarily by Fondation Franklinia. The foundation was formed in 2005 expressly to conserve threatened tree species! I regret that I had not heard about it before.

At least 16,425 of the 47,282 tree species assessed are at risk of extinction. Trees now account for over one quarter of species on the IUCN Red List, and the number of threatened trees is more than double the number of all threatened birds, mammals, reptiles and amphibians combined. Tree species are at risk of extinction in 192 countries around the world.

No surprise: the highest proportion of threatened trees is found on islands. Island trees are at particularly high risk due to deforestation for urban development, conversion to agriculture, invasive species, pests and diseases. Climate change is increasingly threatening trees, especially in the tropics, through sea-level rise and stronger, more frequent storms.

The COP was held in Cali, Columbia. This is fitting because South America is home to the greatest diversity of trees in the world. Twenty-five percent – 3,356 out of 13,668 assessed species are at risk of extinction. Forest clearance for crop farming and livestock ranching are the largest threats on the continent. Dr Eimear Nic Lughadha, Senior Research Leader in Conservation Assessment and Analysis at the Royal Botanic Gardens, Kew, said this percentage is sure to increase as many additional tree species are described for science.

IUCN spokespeople emphasized that the loss of trees is a major threat to thousands of other plants, fungi and animals. Cleo Cunningham, Head of Climate and Forests at Birdlife International pointed out that over two-thirds of globally threatened bird species are dependent on forests. Speakers also noted that people depend on trees; over 5,000 of the tree species on the Red List are used in construction, and over 2,000 species provide medicines, food and fuels.

Sam Ross, Sustainable Business Project Analyst at ZSL, noted that “Despite growing pressure to halt worldwide deforestation by 2030, … most of the world’s 100 most significant tropical timber and pulp companies have made limited progress in disclosing their zero deforestation and traceability commitments. We must all do more to safeguard these vital forest ecosystems, especially consumer goods manufacturers, financial institutions funding forestry, and agriculture companies.”

IUCN and the Red List Partners are launching a global social media campaign to raise awareness and funds to accelerate species assessments and reassessments. The campaign will culminate at the IUCN World Conservation Congress in Abu Dhabi, in October 2025.

Impacts from Pathogens Continue to Increase

Meanwhile, in North America and elsewhere, infections by tree-killing pathogens are spreading and intensifying.

tanoak at Big Sur killed by *P. ramorum*

Phytophthora ramorum (sudden oak death)

In California, P. ramorum the statewide rate of tree infection in 2024 doubled from 2023. Expansions were most obvious in Mendocino and Del Norte counties. Worse, California has now detected a third strain of P. ramorum in its forests. The NA2 strain was first detected in Del Norte County in 2020. Now it has been found in five sites closer to the “core” of the infestation closer to San Francisco Bay. Dr. Matteo Garbelotto believes the strain – formerly known only in nurseries – had been present for some years. It appears to be more aggressive than the strain long present in forests – NA1 – and might be favored by warmer temperatures. [The EU1 strain was detected in Del Norte County in 2021.]

Oregon has been wrestling with the EU1 strain since 2015; the NA2 strain since 2021. Beginning in late 2022, authorities have discovered multiple disease outbreaks between the Rogue River and Port Orford (farther north than the area previously known to be infected). Many of these new outbreaks are the EU1 lineage. The state is struggling to carry out eradication treatments using funds from state legislative appropriations, support from USDA Forest Service and USDI Bureau of Land Management, USDA Agriculture Research Service, and direct Congressional appropriations. The last resulted from assertive lobbying!

The Government Accountability Office is studying interactions between climate change and agricultural pests; sudden oak death is one of four focal pests. The report is expected to be released in 2025.

[Most of this information is from the California Oak Mortality Task Force (COMTF) webinar on 29 October, 2024. Recording available here.]

limber pine in Rocky Mountain National Park; photo by F.T. Campbell

Cronartium ribicola White Pine Blister Rust

Limber pine (Pinus flexilis) is heavily infected by blister rust in Alberta; in its U.S. range

the disease is increasing. Scientists had been cheered by the presence of major gene resistance (MGR) in limber pine to the rust. However, a strain of blister rust in Alberta has been determined to be virulent despite this gene (Liu et al. 2024). Scientists might have to launch a breeding program to try to enhance quantitative disease resistance (QDR) in the species. Unfortunately, the frequency and level of partial resistance in limber pine has been very low in trees tested so far. Scientists now must test more limber pines to see whether some have higher levels of QDR.

Southwestern white pine (Pinus strobiformis) presents the same problem; the MGR gene might even be the same gene. Some some populations of SWWP have higher partial or quantitative disease resistance.

Beech leaf disease

BLD continues to be detected in new sites. According to Matthew Borden of Bartlett Tree Research Laboratories, since 2021, BLD has been detected in five counties in Virginia:

Prince William County — Prince William Forest Park;
Fairfax County: southern Fairfax County on the border with Prince William County (Fountainhead Park, Hemlock Overlook Park, and Meadowood Special Recreation Area), somewhat farther north (Burke Lake Park), and northern edge (Great Falls);
Loudoun County;
Stafford County – just outside the city of Fredricksburg and along the Spotsylvania river
New Kent County in Wahrani Natural Preserve

Several of these outbreaks – e.g., southern Fairfax County, Stafford County, and Loudoun County – are 20 miles or more away from other known outbreaks. Virginia Department of Agriculture staff are monitoring the disease. All these sites are near water – although the Potomac River in Loudoun County is above the fall line so narrower than at the other sites.

SOURCE

Liu, J-J., R.A. Sniezko, S. Houston, G. Alger, J. Krakowski, A.W. Schoettle, R. Sissons, A. Zamany, H. Williams, B. Rancourt, A. Kegley. 2024. A New Threat to Limber Pine (Pinus flexilis) Restoration in Alberta and Beyond: First Documentation of a Cronartium ribicola race (vcr4) Virulent to Cr4-Controlled Major Gene Resistance. Phytopathology. Published Online:25 Sep 2024 https://doi.org/10.1094/PHYTO-04-24-0129-R

Posted by Faith Campbell

www.fadingforests.org

Non-Native Moths in England: Ever Upward

*Platyperigea kadenii* — one of the moth species that feeds on native plant species introduced recently to Great Britain. Photo by Tony Morris via Flickr

Will phytosanitary agencies and the international system respond to continuing introductions of non-native species?

A new study confirms that introductions of insects continue apace, links this pattern to the horticultural trade, and examines the role of climate change in facilitating introductions. This study focuses on moths introduced to the United Kingdom (Hordley et al.; full citation at the end of the blog). The study sought to detect any trends in numbers of species establishing and the relative importance of natural dispersal vs. those assisted – intentionally or inadvertently – by human activities.

The authors determined that moths continue to be introduced by both processes; there is no sign of “saturation”. This finding agrees with that of Seebens and 44 others (2017; citation below), which analyzed establishments of all types of non-native species globally. The British scientists found that rapidly increasing global trade is the probable driver of the recent acceleration of human-assisted introductions. They emphasize the horticultural trade’s role specifically. Climate change might play a role in facilitating establishment of species entering the UK via human activities.

Hordley et al. found that long-term changes in climate, not recent rapid anthropogenic warming, was important in facilitating introductions of even those moth species that arrived without human assistance. As they note, temperatures in Great Britain have been rising since the 17^th Century. These changes in temperature have probably made the British climate more suitable for a large number of Lepidoptera. The data show that the rate of natural establishments began rising in the 1930s, 60 years before anthropogenic changes in temperatures became evident. Hordley et al. point out that an earlier study that posited a more significant role for climate change did not distinguish between insect species which have colonized naturally and those benefitting from human assistance.

The authors expect introductions to continue, spurred by ongoing environmental and economic changes. Fortunately, very few of the introduced moths had any direct or indirect negative impacts. (The box-tree moth (Cydalima perspectalis) is the exception. [Box-tree moth is also killing plants in North America.]

boxtree moth; photo by Tony Morris via Flickr

Still, they consider that introductions pose an ongoing potential risk to native biodiversity and related human interests. Therefore, they advocate enhanced biosecurity. Specifically, they urge improved monitoring of natural colonizations and regulation of the horticultural trade.

Hordley et al. estimated the rate of establishment during the period 1900 – 2019 for (i) all moth species; (ii) immigrants (i.e., those introduced without any human assistance); (iii) immigrants which feed on native hosts; (iv) immigrants which feed on non-native hosts; (v) adventives (i.e., species introduced with human assistance); (vi) adventives which feed on native hosts; and (vii) adventives which feed on NIS hosts.

Their analysis used data on 116 moth species that have become established in Great Britain since 1900. Nearly two-thirds of these species – 63% – feed on plant species native to Great Britain; 34% on plant species that have been imported – intentionally or not. Data were lacking on the hosts of 3 species.

Considering the mode of introduction, the authors found that 67% arrived through natural colonization; 33% via human assistance. Sixty-nine percent of the 78 species that were introduced through natural processes (54 species) feed on plant species native to Great Britain; 31% (24 species) feed on non-native plants. Among the 38 species whose introduction was assisted by human activities, one-half (19 species) feed on native plant species; 42% (16 species) feed on introduced hosts.

Regarding trends, they found that when considering all moth species over the full period, 21.5% more species established in each decade than in the previous decade. This average somewhat obscured the startling acceleration of introductions over time: one species was reported as established in the first decade (1900–1909) compared to 18 species in the final decade (2010–2019).

The rate of introduction for all immigrant (naturally introduced) species was 22% increase per decade. Considering immigrant species that feed on native plants, the rate of establishment was nearly the same – 23% increase per decade – when averaged over the 120-year period. However, a more detailed analysis demonstrated that these introductions proceeded at a steady rate until 1935, then accelerated by 11% per decade thereafter. In contrast, immigrants that feed on non-native plants have maintained a steady rate of increasing establishments – 13% per decade since 1900.

Adventive species (those introduced via human assistance) increased by 26% per decade. The data showed no signs of saturation. The rates of introduction were similar for adventives that feed on both native plants (22%) and non-native hosts (26%). Again, additional analysis demonstrated a break in rates for adventives that feed on native hosts. The rate was steady until the 1970s, then significantly increased during the years up to 2010. (The scientists dropped data from the final decade since lags in detection might artificially suppress that number.)

In summary, Hordley et al. found no significant differences in trends between

the number of species that established naturally (20%) vs. adventives (26%).
immigrant or adventive species that feed on native vs. non-native hosts.

The authors discuss the role of climate change facilitating bioinvasion by spurring natural dispersal, changing propagule pressure in source habitats, changing the suitability of receiving habitat, and changing in pathways for natural spread, e.g., altered wind and ocean currents. They recognize that the two modes of colonization – adventives and immigrants – can interact. They stress, however, that the two colonization modes require different interventions.

Although their findings don’t support the premise that a surge of natural colonizers has been prompted by anthropogenic warming, Hordley et al. assert that climate clearly links to increased moth immigration to Britain and increased probability of establishment. They note that even so assisted, colonists still must overcome both the natural barrier of the English Channel and find habitats that are so configured as to facilitate breeding success. They report that source pools do not appear to be depleted — moth species richness of neighboring European countries greatly exceeds that in Great Britain.

I would have liked to learn what factors they think might explain the acceleration in both natural and human-assisted introductions of species that feed on plant species native to Great Britain. In 2023 I noted that scientists have found that numbers of established non-native insect species are driven primarily by diversity of plants – both native and non-indigenous.

Hordley et al. assert that Great Britain has advantages as a study location because as a large island separated from continental Europe by the sea – a natural barrier – colonization events are relatively easy to detect. However the English Channel is only 32 km across at its narrowest point. I wonder, whether this relatively narrow natural barrier might lead to a misleadingly large proportion of introduced species being natural immigrants. I do agree with the authors that moths are an appropriate focal taxon because they are sensitive to climate and can be introduced by international trade. Furthermore, Britain has a long tradition of citizen scientists recording moth sightings, so trends can be assessed over a long period.

Hordley et al. stress that they measured only the temporal rate of new species’ establishments, not colonization pressure or establishment success rate. They had no access to systematic data regarding species that arrived but failed to establish. Therefore, they could not deduce whether the observed increase in establishment rates are due to:

(1) more species arriving—due either to climate-driven changes in dispersal or to accessibility of source pools; or

(2) higher establishment success due to improved habitat and resource availability; or

(3) both.

Hordley et al. noted two limitations to their study. First, they concede that there is unavoidably some subjectivity in classifying each species as colonizing naturally or with human assistance. They tried to minimize this factor by consulting two experts independently and including in the analysis only those species on which there was consensus.

Second, increases in detection effort and effectiveness might explain the recent increases in establishment rates. They agree that more people have become “citizen scientists” since 1970. Also, sampling techniques and resources for species identification have improved considerably. They note, however, that Seebens et al. (2018) tested these factors in their global assessment and found little effect on trends.

Hordley et al. believe that they have addressed a third possible limitation – the lag between introduction and detection – by running their analyses both with and without data from final decade (2010-2019). The results were very similar qualitatively.

SOURCE

Hordley, L.A., E.B. Dennis, R. Fox, M.S. Parsons, T.M. Davis, N.A.D. Bourn. 2024. Increasing rate of moth species establishment over 120 years shows no deceleration. Insect Conserv. Divers. 2024;1–10. DOI: 10.1111/icad.12783

Seebens, H. et al. 2017. No saturation in the accumulation of alien species worldwide. Nature Communications. January 2017. DOI: 10.1038/ncomms14435

Seebens, H. et al. 2018. Global rise in emerging IAS results from increased accessibility of new source pools. Proceedings of the National Academy of Sciences. www.pnas.org/cgi/doi/10.1073/pnas.1719429115

Posted by Faith Campbell

www.fadingforests.org

Phytophthora here, Phytopthora there … level of threat is unclear

Mt. Triglav – highest peak in the Slovenian (Julian) Alps; photo by Gunter Nuyts via Pexel

Scientists have discovered sizable diversity of pathogenic Phytophthora species in Europe, specifically in the Alps of northeastern Italy and western Slovenija. They have also named a new species, and noted the need to change the definition of species previously named. See Bregant et al. – full citation at the end of this blog – open access!

Two of its findings are especially important for the US

First, the authors document the vulnerability of alpine areas to 18 Phythophthora species. Most of the plant hosts they studied have congenerics in mountainous areas of North America: Acer, Alnus, Betula, Fagus, Fragaria, Fraxinus, Ilex, Juniperus, Larix, Lonicera, Lycopodium, Pinus, Populus, Quercus, Rhododendron, Rubus, Salix, Sorbus, Taxus, and Vaccinium.

Second, the paper discusses how junipers are at particular risk. I remind you that P. austrocedrii has recently been detected in nurseries in Ohio and Oregon. This is another non-native Phythophthora that attacks junipers. I hope authorities are actively seeking to determine whether P. austrocedrii is present in nurseries or natural systems in other parts of the country.

The genus Phytophthora includes many serious plant pathogens, from the one that caused the disastrous potato blight of Ireland (Phytophthora infestans) to globally important forest-destroying invasive species, e.g., P. cinnamomi and “sudden oak death” P. ramorum.

Bregant et al. surveyed 33 small tree, shrub, and herbaceous plant species in 54 sites on the Italian island of Sardinia and the Alps of both northeastern Italy and western Slovenija. Altitudes varied from the valley bottom (700 m) to above tree line (2100 m). Sites included typical forests, riparian ecosystems, and heathlands.

The 360 isolates taken from 397 samples belonged to 17 known Phytophthora species. Some species are widespread and well-known, e.g., P. pseudosyringae. Three isolates belonged to a putative new species described by Bregant et al. – Phytophthora pseudogregata sp. nov. This total of 18 taxa was unexpectedly high. Many of the species are able to cause aerial infections via production of caducous sporangia. These can infect various organs of the plant host: fruits, leaves, shoots, twigs and branches; and cause necrosis and rots. They detected 56 new host–pathogen associations. All are listed, by type of host, in Tables 4 – 6 of the paper.

The surprising diversity and detection of taxa previously described in Australia (see below) illustrate scientists’ still poor understanding of this genus. They also confirm fears that the global phytosanitary system is unable control intercontinental movement of Phytophthora.

The authors express concern because Alpine and subalpine regions are important hotspots for floral biodiversity. The great variation in altitude, aspect, moisture regimes, etc. – including extreme conditions – results in many different habitats on small spatial scales, with large numbers of both plant species and endemics in very confined spaces. The pathogens they discovered are spreading and compromising the biodiversity of these ecologically fragile habitats.

The authors say their study emphasizes the need to assess the full diversity of Phytophthora species and the factors driving the emergence and local spread of these invasive pathogens. They specify studying the Phytophthora communities on fallen leaves to evaluate host specificity, geographic distribution and survival strategies of the main Phytophthora species detected in this study. They report that scientists are currently mapping the distribution of the new species, P. pseudogregata, in the Alpine habitats and trying to establish its natural host range.

another view of the Julian Alps; photo via Rawpixl

Bregant et al. point out that increased scientific interest over the last 30 years has led to discovery of several previously unknown Phytophthora species and pathogen-host associations. They note that all but two of the taxa in one taxonomic grouping, Sub-clade 6b, have been described in the last 12 years. The majority of taxa have been described from forest ecosystems. This trend is depicted in Figure 8 of the article. This figure also displays which species were isolated from nurseries, agricultural systems, and forest ecosystems.

Results by Plant Type – Disease incidence was highest in shrub vegetation, alpine heathlands and along the mountain riparian systems. The most impacted ecosystems were heathlands dominated by common juniper & blueberry, and riparian systems dominated by alders. In these ecosystems, the Phytophthora-caused outbreaks had reached epidemic levels trend with a high mortality rate. On shrubs and heath formations, disease was initially observed in small areas and progressively spread in a concentric manner affecting more plant species.

Hosts and Diseases – Table 3 in the article lists the 33 host plant species, briefly describes the symptoms, and in some cases provides incidence and mortality rates. Those hosts described as suffering “sudden death” included Alnus viridis, Calluna vulgaris, Genista corsica, Juniperus communis, Lycopodium clavatum, Pinus mugo,Rhododendron ferrugineum, Salix alpine, Vaccinium myrtillus and Vaccinium vitis-idaea

Role of P. pseudosyringae – The most common and widespread species detected was P. pseudosyringae. It constituted more than half of the isolates (201 of the 360). Also, it infected the highest number of hosts (25 out of 33, including all three plant types). It was isolated at 36 of the 54 sites distributed throughout all geographic regions. Seventeen of the host–pathogen associations were new to science. (See Tables 4-6, in the paper.)

*Vaccinium myrtillis* – a vulnerable host; photo by Tatyana Prozovora via Wikimedia

P. pseudosyringae dominated disease agents in the shrub community, especially among high-altitude shrubs and heaths, e.g., blueberry, dwarf pine, juniper, rhododendron, and alpine willows. Bregant et al. note that these shrubs are extremely low-growing (an adaptation to high elevation conditions). This form might favor attack by Phytophthora sporangia and zoospores present in fallen leaves. Vaccinium myrtillus suffers particularly severe disease – as previously reported in Ireland. In their laboratory studies, Bregant et al. found P. pseudosyringae to be highly aggresse on common juniper (Juniperus communis), producing wood necrosis and shoot blight only four weeks after inoculation.

The importance of P. pseudosyringae in mountainous regions has been found in previous studies in Asia, Europe, and North and South America. However, the authors call for further study of certain aspects of the species. These regard infectivity and survival of the species’ sporangia in infected tissues fallen to the ground; and the ability of oospores to persist for years in environments subject to extreme low temperatures. The former could increase the risk of outbreaks and promote faster disease progression.

The authors suggest P. pseudosyringae’s survival stems from its production of very large and thick-walled chlamydospores. This reported feature is in contradiction with the original species description, which prompts Bregant et al. to call for a correction.

Other Species, Old and New – P. cactorum was the only Phytophthora species other than P. pseudosyringae detected on all three types of hosts (small trees, shrubs, and herbaceous plants). Phytophthora plurivora was the second-most isolated species. It was detected on 12 hosts in 24 sites.

The new putative species — Phytophthora pseudogregata sp. nov. – was detected on Alnus viridis, Juniperus communis, and Rhododendron ferrugineum. As noted above, scientists are now testing whether other plant species are also hosts. It was detected at two sites in Italy — Borso del Grappa and San Nicolò di Comelico; and one site in Slovenija.

*Juniperus communis*; photo by Joan Simon via Flickr

Diseases of Juniper – Koch’s postulates have been fulfilled, demonstrating that eight Phytophthora species – the new P. pseudogregata sp. nov. as well as P. acerina, P. bilorang, P. gonapodyides, P. plurivora, P. pseudocryptogea, P. pseudosyringae, P. rosacearum – are pathogenic on common juniper (Juniperus communis). The lesions caused by P. pseudosyringae were significantly larger than those caused by other species. Lesions caused by P. pseudosyringae, P. plurivora and acerina progressively girdled the twigs causing shoot blight, browned foliage & wilting symptoms.

Most Threatening Phytophthora clades – The most-frequently isolated Phytophthora species belong mainly to clades 1 and 3 – including P. pseudosyringae. Bregant et al. say these species have several advantages for surviving in mountainous ecosystems: they produce caducous sporangia useful for aerial infections and they tolerate relatively low temperatures. Twoother species in clade 3 were isolated only from the mountains of Sardinia. One, P. psychrophila, was isolated from bleeding cankers on an oak species, Quercus pubescens. Its geographic distribution and impact are still unknown. A second species, P. ilicis, is a well-known pathogen on various hollies in Europe and North America.

Four species belonging to subclade 1a were isolated in the Alps of northeastern Italy and Slovenija. P. cactorum is a widespread polyphagous pathogen found from tropical to temperate climates. It has been responsible for severe diseases on agricultural crops and forest trees. Its occurrence in cold areas has recently been reported in Europe and Australia. The recently described P. alpina has the highest ability to survive in extremely cold conditions. It was detected on four hosts – Alnus viridis, Lonicera alpigena, Vaccinium myrtillus, and V. vitis-idaea.

Some species, e.g., P. hedraiandra and P. idaei, were reported for the first time in natural ecosystems in Europe. They have previously been linked to root and foliar disease in agricultural and ornamental nurseries.

The second-most common species in the Bregant et al. study, P. plurivora, was isolated from 54 symptomatic samples from 12 plant species; eight of the hosts are new. It is common in forest ecosystems of Central Europe – which is now considered to be its region of origin. Little is known about the closely related P. acerina. To date, the latter has been detected widely in agricultural systems, nurseries, forests, and ornamental trees in northern Italy and Sardinia. It is much more rarely found elsewhere. Both P. acerina and P. plurivora are already known to be primary pathogens involved in decline of common and grey alder in Italy.

Five of the Phytophthora species in this study, including the new species P. pseudogregata, are in Clade 6. These include pathogens very common in European forests, e.g., P. bilorbang and P. gonapodyides. Others have more limited or still unknown distributions, e.g., P. amnicola and P. rosacearum. These five species’ ability to cause aerial infections on mountain vegetation might warrant re-evaluation of the reputation of species in this clade being saprophytes or only occasional weak opportunistic pathogens.

P. pseudogregata – in sub-clade 6a – was originally described in 2011 in wet native forests in Australia and on dying alpine heathland vegetation in Tasmania. It has recently been reported in the Czech Republic and Finland. The related P. gibbosa is known to occur only in Australia, where it is associated with dying native vegetation on seasonally wet sites.

Two species of clade 8 — P. kelmanii & P. syringae — have a very limited distribution. A third – P. pseudocryptogea — is widespread in Italian ecosystems from Mediterranean areas to the tree line in the Dolomites. One species from clade 7 (P. cambivora) isolated, mainly from stem bleeding cankers of small trees and shrubs. It has two mating types; bothoccurr in the Alps of northeastern Italy and neighboring Slovenija — on Alnus incana, Laburnum alpinum and Sorbus aucuparia.

SOURCE

Bregant, C., G. Rossetto, L. Meli, N. Sasso, L. Montecchio, A. Brglez, B. Piškur, N. Ogris, L. Maddau, B.T. Linaldeddu. 2024. Diversity of Phytophthora Species Involved in New Diseases of Mountain Vegetation in Europe with the Description of Phytophthora pseudogregata sp. nov. Forests 2023, 14, 1515. https://doi.org/10.3390/f14081515 https://www.mdpi.com/journal/forests

Posted by Faith Campbell