In November, scientists discovered a new ambrosia beetle in symptomatic valley oaks (Quercus lobata) trees in Calistoga, Napa County. Some blue oaks (Q. douglasii) have also been attacked (Rabaglia et al. 2020). Trees associated with this outbreak showed wilting, defoliation, and broken branches. The infested wood was discolored, presumably by the fungus. The insect, Xyleborus monographus, is native to Europe.
Officials now know that this beetle is found throughout a 15-mile-long area in Napa and neighboring Lake and Sonoma counties. It has probably been there for several years (Rabaglia et al. 2020). One specimen of the beetle was trapped in Portland, Oregon in 2018, but no infestation was detected. The beetle has never been intercepted in California. Nor has it been found in traps designed to detect bark beetles which have been deployed in 11 counties – including several in the San Francisco Bay area but not including Napa or Sonoma.
Like
all Xyleborus, adult females tunnel
into tree’s trunks, carrying fungal spores in their mycangia (structures in the
jaws in which microbes are harbored). Beetle larvae eat the fungi. Beetle
reproduction is facilitated by sibling mating within the gallery and by the
ability of unmated females to produce male offspring.
Sometimes
the beetle’s associated fungi are pathogenic to living trees. One of the fungal
species detected in the Calistoga infestation is Raffaelea montetyi, which is reported to be pathogenic to cork oak.
The presence of this fungus had been reported in 2018, although the beetle
species carrying it was not identified then. This is apparently the first report
of this fungus in North America.
Known
hosts of beetle X. monographus include
European or Eurasian chestnut (Castanea
sativa), beech (Fagus orientalis),
and European and American oaks (including
Q. lobata and Q. rubra). The possible effects of the beetle and
associated fungi on other oak species is unknown. Oaks are acknowledged to be important
components of forests and woodlands in California. Ambrosia beetles often attack
stressed trees. Since California forests are increasingly frequently stressed
by drought, fire, and other pests, they might be especially vulnerable.
The California Department of Food and Agriculture is currently seeking comments on what pest rank to assign the insect. The comment period closes on March 6th and I encourage you to consider providing your views.
In
their draft document ranking risk, state officials note that a proven host — Q. lobata — is widespread in California
and the insect is probably capable of establishing over much of the state. The possible
economic impact was described as possibly affecting production of oaks in California
nurseries and triggering quarantines. (Does
this mean CDFA expects impacts only on saplings? Is this realistic? CDFA made
no mention of costs to urban areas for hazard tree management.)
The risk assessment notes that research by McPherson, et al. (2008) found that ambrosia beetles are attracted to oak trees already infected with sudden oak death (SOD) (Phytophthora ramorum). Therefore, X. monographus could have a synergistic impact with SOD on California oaks – which has already killed an estimated 1.9 to 3.3 million coast live and Shreve oaks.
SOURCE
Rabaglia, R.J. S.L. Smigh, P. Rurgman-Jones, M.F. Digirolomo, C. Ewing, and A. Eskalen. 2020. Establishment of a non-native xyleborine ambrosia beetle, Xyleborus monographus (Fabricius) (Coleoptera: Curculionidae: Scolytinae), new to North America in California. Zootaxa 478 (2): 269-276
Posted
by Faith Campbell
We
welcome comments that supplement or correct factual information, suggest new
approaches, or promote thoughtful consideration. We post comments that disagree
with us — but not those we judge to be not civil or inflammatory.
APHIS has released a risk assessment in response to a petition from the Republic of Korea (ROK) seeking permission to export to the United States bunjae of three maple species (Acer buergerianum Miq., A. palmatum Thunb., and A. pseudosieboldianum Nakai). The risk assessment is available here. Scroll down to the deadline February 3.
Comments are accepted until 3 February. To comment, send an email to PPQPRAcomments@aphis.usda.gov. Include the name of the commodity assessed by the draft document (e.g., Korean maple bunjae) in the Subject line.
“Bunjae”
is the Korean term for plants for planting equivalent to Japanese “bonsai” or
Chinese “penjing”. In this practice,
trees are grown – often for years – using cultivation techniques such as
pruning, root reduction, potting, defoliation, and grafting, to produce
miniature specimens.
Importation of bunjae plants for planting in the Acer genus from several Asian countries was prohibited temporarily under the agency’s authority under the Plant Protection Act and regulations in 7 CFR 319.37, Subpart H- P4P to limit imports of a new suite of plant taxa as “not authorized pending pest risk analysis” (NAPPRA).
The NAPPRA listing, finalized in 2013, followed numerous detections of Anoplophora and possibly other pests in penjing shipped from China to the United States, and one outbreak (in Takohma, Washington) that required expensive and destructive eradication measures. At that time, APHIS made the case that no effective mitigation existed to provide protection adequate to the risk. If APHIS is to agree to the ROK petition, it must demonstrate that any mitigation measures it accepts have overcome deficiencies identified in the original proposal to include Acer in the NAPPRA category.
APHIS will address risk management aspects, including and risk mitigation
measures, after it has assessed stakeholder and country comments on each pest
list or risk assessment. There will be an opportunity to comment on any proposed
mitigation measures later.
The
risk assessment now open for comment clearly demonstrates that the risks are
severe. It concludes that 17 or 18 taxa or groups of species pose a “high”
overall risk of introduction, establishment, and impacts. Another 10 pose an overall “moderate” risk.
In each case, the risk assessors concluded that the harvest and shipment
procedures outlined in Section 1.4 of the Korean petition would not mitigate
the risk.
While the risk is greatest for maples (Acer spp.), many other types of plants also host pests evaluated in the risk assessment. Thus, the risk often affects fruit trees and grapes as well as alders, birches, dogwoods, elms, magnolias, oaks, poplars, walnuts, willows, rhododendron, even redwood.
My questions and concerns
I note that Table 3 of the risk assessment omits the Asian longhorned beetle (Anoplophora glabripennis), even ‘tho the species is discussed in the text and received an overall risk ranking of “high”. Is this a mistake? If the omission is deliberate, why is the reasoning not discussed in the risk assessment?
The assessments included in this document are brief and leave out many easily obtainable facts regarding damage, especially with regard to the Anoplophora, Lymantria, and Lycorma genera. The risk assessment notes when pest species are polyphagous, but it is uncertain how it incorporates that heightened risk of potential damage.
I
am also concerned about the document’s treatment of uncertainty. First, “moderate uncertainty” is defined as
“Additional or better evidence may or may not change rating.” How do the
assessors evaluate this 50/50 tossup? My
concern is heightened by a statement in the text regarding two taxa, Cacopsylla albopontis & C. pseudosieboldiani. The assessment
notes an absence of literature documenting that these taxa are pests in their
native range, so their ability to cause damage if introduced to the U.S. is
unknown. Consequently, the assessors did not analyze them further “as they are
unlikely to cause unacceptable impacts.” As we all know, numerous arthropods
and pathogens highly damaging in naïve environments – including in the US — were
not pests / were barely known in their native ranges.
Regarding individual species, I note that the assessment says the wood-root fungus Daedalea dickinsii is usually found in older heartwood of roots, trunks, or branches. The assessors conclude that it is unlikely that this fungus would be associated with maple seedlings. However, bunjae trees are not seedlings; they are deliberately miniaturized woody plants that are often years old.
Re: Anomala cuprea, the assessor seems to downplay the risk because the insect lacks a specific attraction to maples. While I agree that a generalist might be somewhat less likely to be on the bunjae when they are exported, a generalist might pose a threat to a wide range of woody plants if introduced. This higher level of possible impacts needs to be recognized in the assessment.
Several
insect groups were excluded from further valuation despite being described as
established in Korea and “only associated with Acer species”. Included in this group are several beetles, true
bugs (including aphids and leafhoppers), and butterflies/moths (pp. 13-14 of
the PRA). I found this language to be completely unclear. If the pests are in
Korea and associated with maples, why were they not evaluated?
Posted
by Faith Campbell
We
welcome comments that supplement or correct factual information, suggest new
approaches, or promote thoughtful consideration. We post comments that disagree
with us — but not those we judge to be not civil or inflammatory.
As I blogged in December, APHIS is seeking input on a proposal to place several plant taxa in the category “not authorized pending pest risk analysis” (NAPPRA). The purpose of this proposed listing is to prevent introduction of plant pests or probable invasive plant species.
I urge you to comment before the deadline – this Friday, January 24.
In
comments prepared for the Center for Invasive species Prevention (CISP), I
applauded APHIS’ continued reliance on this authority to improve phytosanitary protections
for our natural and agricultural resources. I noted, however, several
weaknesses in the proposal – including several pathogens that I think should
have been included, but were not. I summarize these comments here.
1)
There have been lengthy delays in proposing and finalizing lists of species to
be regulated under this authority. While I strongly support listing of all
plants in the family Myrtaceae that are destined for Hawai`i in order to reduce
the risk that additional strains of the `ohi`a rust pathogen Austropuccinia psidii might be
introduced and prove more damaging to native Hawaiian vegetation than the
strain already present on the islands. However, this proposal comes 15 years
after the pathogen was detected in Hawai`i and six years after publication of
scientific documentation of the existence of more damaging strains of the
pathogen.
2)
When lists have been presented, they failed to include all appropriate species.
I
am disturbed that APHIS did not include in the NAPPRA proposal Ceratocystis lukuohia and Ceratocystis huliohia, two pathogens that
are killing millions of ‘ōhi‘a trees in Hawai`i under the name “rapid ‘ōhi‘a death”.
3)
APHIS must act under other regulatory provisions to close some of the gaps left
by this proposal.
The listing of plants in the Myrtaceae
(see number 1 above) under NAPPRA does nothing to halt imports of cut flowers
and foliage, which are widely recognized to be the pathway by which the rust
was introduced to Hawai`i. APHIS notes
that is should act under other regulatory authority to close this pathway; I
hope you will urge APHIS to take such action quickly, preferably initially by
issuing a Federal Order.
4) APHIS has proposed 26 plant taxa for
inclusion in the NAPPRA category because they might themselves be invasive. These
proposals are generally well supported and deserve your support. Several plant
taxa appear to pose significant ecological threats: two taxa of mangroves (Bruguiera gymnorhiza and Lumnitzera racemose); a vine that grows
in Asian and Indian Ocean mangrove forests,
Derris trifoliate; and several aquatic plants (Crassula helmsii, Elatine ambigua, Luziola subintegra, Philydrum lanuginosum, Stratiotes
aloides); and Ligustrum robustum.
Remember that at least 50 species of aquatic plants are already considered invasive in the United States. At least eight species of Ligustrum are also invasive.
Update: Listing finalized
On June 2, 2021 APHIS finalized the NAPPRA listing originally proposed in November 2019.
The agency added to the category 26 plant taxa because they are invasive; all plants in the Myrtaceae family when destined to Hawai`i, and 43 other plant taxa that are hosts of 17 quarantine pests.
The only change from the proposed action was to drop listing of the subfamily Bambusoideae because it is already regulated under NAPPRA to prevent introduction of other quarantine pests.
APHIS had received 132 comments from producers, importers, industry groups, conservationists, scientists, plant pathologists, ecologists, administrators, teachers, students, and private citizens. Most reportedly supported the proposed listing of Myrtaceae destined for Hawai`i and expressed no concerns about the proposed listing of most other taxa. I have blogged previously about the threat to Hawaii’s unique flora posed by the pathogenAustralopuccinia psidii (the subject of this NAPPRA listing) and other non-native organisms – here and here.
We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.
For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm
We know that the international trade in living plants is a major pathway by which tree-killing pathogens are being spread – some of them again and again. According to Grünwald etal. (2019), Phytophthora ramorum, the pathogen that causes Sudden Oak Death (SOD), has been introduced to North America and Europe – probably from Asia – at least five times. One lineage or genetic strain – EU1 – has been established on both continents (strains explained here). There is strong evidence of two separate introductions to Oregon, at least 12 to California.
Jung
et al. 2015 state definitively that
the international movement of infested nursery stock and planting of
reforestation stock from infested nurseries have been the main pathway of
introduction and establishment of Phytophthora
species in European forests.
Jung et al. 2020 have demonstrated that P. ramorum probably originated in
Vietnam. This region appears to be a center of
diversity for Phytophtoras and other
Oomycetes: baiting of soil and streams resulted in the detection of 13
described species, five informally designated taxa, and 21 previously unknown
taxa of Phytophthoras plus at least
15 species in other genera. Noting the risk associated with any trade in plants
from this region, the authors re-iterated past appeals that the international
phytosanitary system replace the “outdated and scientifically flawed
species-by-species regulation approach based on random visual inspections for
symptoms of described pests and pathogens” by instituting “a sophisticated
pathway regulation approach using pathway risk analyses, risk-based inspection
regimes and molecular high-throughput detection tools.”
Pathogen’s Spread Proves U.S.
Domestic Regulations Governing Nursery Trade Are Inadequate
Last year I blogged about the most recent spread of Phytophthora ramorum through the nursery trade. As of now, we know that shipments of potentially infected plants had been sent to 18 states. Infected stock had been detected in nurseries in seven of these (Iowa, Illinois, Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus the source state, Washington [COMTF Newsletter August 2019].
Since then, I learned [COMTF newsletter for December 2019] that these plants were infected by the NA2 strain of the pathogen. This is the first time that this strain has been shipped to states outside the West Coast. It is unclear what the impact will be if – as is likely – infested plants are still extant in purchasers’ yards. Both the NA1 strain (the strain established in most infested forests of California and Oregon) and the NA2 strain belong primarily to the A2 mating type, so the potential spread of NA2 lineages might not exacerbate the probability of sexual reproduction of the pathogen.
I applaud agencies’ funding of
genetic studies to determine the lineage of the pathogen involved. It not only
helps narrow the possible sources of infected plants, but also could be
important in determining risk and management options.
I have long criticized USDA’s P. ramorum regulatory program – see Fading Forests III and my blogs discussing the most recent revisions to the regulations here and here. I believe that both the earlier regulations and the revisions finalized last May provide inadequate protection for America’s forests.
The updated regulations do take a couple of important positive steps. First, APHIS is now authorized to sample water, soil, pots, etc. – and to act when it finds evidence of the pathogen’s presence. APHIS also now mandated nurseries found to be infested to carry out a “critical control point analysis” to determine practices which facilitated establishment and persistence of P. ramorum.
However, these improvements are
severely undermined by continuing the five-year-old practice of limiting close
scrutiny to only those nurseries that tested positive for the pathogen in the
recent past. The flaw in this approach was starkly demonstrated by the
pathogen’s spread in 2019. The Washington State nursery that was the source of
the infected plants had not previously been positive, so it was under routine
nursery regulation, not the more stringent federal P. ramorum program.
Too often various iterations of the regulations have allowed infected plants to be shipped. Between 2003 and 2011, a total of 464 nurseries located in 27 states tested positive for the pathogen, the majority as a result of shipments traced from infested wholesalers (Campbell). The number of nurseries found to have infected plants has since declined, but not dropped to zero. These include 34 nurseries in 2010 (COMTF February 2011 newsletter), 21 in 2012, and 17 in 2013 (Pfister). During 2014, state inspectors detected the SOD pathogen in 19 nurseries – 11 in the three west-coast states and eight in other parts of the country (Maine-1, New York-2, Texas-1, and Virginia-4) COMTF newsletter December 2014). Despite the continuing presence of the pathogen in the nursery trade, APHIS formalized existing practices that narrowed the regulators’ focus to only those nurseries with a history of pathogen presence. This approach has been shown to fail – we need APHIS and the states to find a way to broaden their scrutiny.
The most immediate impact of the continuing presence of P. ramorum in the nursery trade is the burden borne by eastern states’ departments of agriculture. They are obligated to seek out in-state nurseries that might have received infected plants; inspect those plants; and destroy the infected plants, test nearby plants, and try to find and retrieve plants that had been sold. The heaviest, and most direct, burden is borne by the receiving nurseries. Anger about bearing this burden for 15 years doubtless prompted the National Plant Board to adopt a tart resolution calling on APHIS to carry out a review of its communications to the states during the 2019 incident. The NPB also questioned whether current program processes and guidance are effective in preventing spread of this pathogen.
Unfortunately, the NPB had not
commented formally on the rule change when it was proposed.
The states’ frustration is
exacerbated by the fact that under
the Plant Protection Act, when APHIS takes a regulatory action it prevents
states from adopting more stringent regulations. While the law allows for
exceptions if the state can demonstrate a special need, none of the five
applications for an exemption pertaining to P.
ramorum was approved (Porter and Robertson 2011). I have been unable to
find evidence of petitions submitted in the nine years since 2011.
In Case You Needed A
Reminder: P. ramorum is a Dangerous Pathogen
– as Proved by the Situation in the West states and Abroad
Continuing Intensification of the Already Bad Infestations in the West
As of 2014 (see COMTF November 2018 newsletter available here), perhaps 50 million trees had been killed by P. ramorum in California and Oregon. The vast majority were tanoaks (Notholithocarpus densiflorus) – an ecologically important tree.
Since
2014, the disease has intensified and spread in
response to recent wet winters. In 2016 (see COMTF
November 2016 newsletter here) disease was detected for the first time in a fifteenth California county and new outbreaks or more severe infestations were recorded in seven other counties. In 2019, SOD was detected in the sixteenth county. Tanoak mortality in California increased by more than 1.6 million trees across 106,000 acres in 2018.
Perhaps more disturbing, the disease has also intensified on the eastern side of San Francisco Bay – an area thought to be less vulnerable because it is drier and where there are fewer of the principal sporulation host, California bay laurel (see COMTF March 2017 newsletter here).
A second disturbing event is the detection in Oregon forests of the EU1 strain of Phytophthora ramorum. The August 2015 detection was the first instance of this strain being detected in a forest in North America. Oregon authorities prioritized removing EU1-infected trees and treating (burning) the immediate area, which had expanded to more than 355 acres – all within the quarantine area in Curry County. The legislature provided $2.3 million for SOD treatments for 2017-2019 (Presentation by Chris Benemann of Oregon Department of Agriculture to the Continental Dialogue on Non-Native Forest Insects and Diseases; reported here).
The EU1 lineage is a different
mating type than the NA1 lineage already established in Oregon. Scientists
should study P. ramorum populations
in Vietnam and Japan, where both mating types are present, to determine whether
they are reproducing sexually. There is also the risk that the EU1 lineage
might be more aggressive on conifers – as it has been in the United Kingdom (Grünwald etal. 2019).
The EU1 infestation was introduced to the forest from a nursery. The nursery had carried out the APHIS-mandated Confirmed Nursery Protocol, then closed. I ask, what does this apparent transmission from nursery to forest say about the risk of transmission? Does it raise questions about the efficacy of the confirmed nursery protocol to clean up the area? Remember that a pond at the botanical garden in Kitsap, Washington has repeatedly tested positive, despite several applications of the clean-up protocols.
(For a discussion of the implications of mixing the various strains of P. ramorum, visit here)
These disasters remind us how sad it
is that California and federal officials did not adopt aggressive management
efforts aimed at slowing the pathogen’s spread at an early stage of the epidemic. Experts on modeling the
epidemiology of plant disease concluded three years ago that the sudden oak
death epidemic in California could have been slowed considerably if aggressive and
well-funded management actions had started in 2002 (Cunniffe, Cobb,
Meentemeyer, Rizzo, and Gilligan 2016).
The Oregon Department of Forestry commissioned a study of the economic impact of the P. ramorum infestation that found few economic impacts to date, but potentially significant impacts in the future. It also noted potential harms to tribal cultural values and the “existence value” of tanoak-dominated forests and associated obligate species.
Situation Abroad
The situation in Europe is even worse than in North America. Two strains of P. ramorum are widespread in European nurseries and in tree plantations and wild heathlands of western the United Kingdom and Ireland. and here and here. Jung et al. 2015 found 56 Phytophthora taxa in 66% of 2,525 forest and landscape planting sites across Europe that were probably introduced to those sites via nursery plantings.
In Australia, Phytophthora dieback has infected more than one million hectares in Western Australia. More than 40% of the native plant species of the region are vulnerable to the causal agent,P. cinnamomi
Barber
et al. 2013 reported 9 species of Phytophthora associated with a wide variety
of host species in urban streetscapes, parks, gardens, and remnant native
vegetation in urban settings in Western Australia. Phytophthora species were recovered from 30% of sampled sites.
In
New Zealand, the endemic – and huge, long-lived – kauri tree (Agathis australis) is also suffering
severe impacts from Phytophtoras and
other pathogens (Bradshaw et al.
2020)
See
the IUFRO Working Party 7.02.09 ‘Phytophthora Diseases of Forest Trees’ global
overview (Jung et al. 2018), which covers
13 outbreaks of Phytophthora-caused
disease in forests and natural ecosystems of Europe, Australia and the
Americas.
The situation in
the Eastern United States is Unclear
After 15 years of the nursery trade carrying P. ramorum to nurseries – and possibly yards and other plantings – in states east of the 100th Meridian, what is the risk that these forests will become infested? No one knows. We do known that the pathogen has been detected from 11 streams in six eastern states – four in Alabama; one in Florida; two in Georgia; one in Mississippi; one in North Carolina; and two in Texas. P. ramorum has been found multiple times in eight of these streams – two steams in Alabama, one each in Mississippi and North Carolina (see COMTF April 2019 newsletter available here). While established vegetative infections have not been detected, the question remains: how is the pathogen persisting? Scientists agree that P. ramorum cannot persist in the water; it must be established on some plant parts (roots?) or in the soil. Still, Grünwald etal. (2019) report that there is little evidence of plant infections resulting from stream splash in Oregon.
Unfortunately, fewer states are participating in the stream surveys – which are operated by the USDA Forest Service. In 2010, 14 states participated; in 2018, only seven (Alabama, Georgia, Mississippi, North Carolina, Pennsylvania, South Carolina, and Texas). Florida and Tennessee recently dropped out. The number of streams surveyed annually also has dropped – from 95 at the highest to only 47 in 2018 (see COMTF April 2019 newsletter available here). This reduced scrutiny makes it less likely that any infestation on plants will be detected. Risk maps (reproduced in Chapter 5 of Fading Forests III here) developed over more than a decade indicate that forests in the southern Appalachians and Ozarks are vulnerable to SOD.
Risks to other
plants
The risk from Phytophthoras is not just P. ramorum and trees! Swiecki et al. 2018 report a large and increasingly diverse suite of introduced Phytophthora species pose an ever greater threat to both urban and non-urban plant communities in California. These threats are linked to planting of nursery stock. See also the information posted here.
Jung et al. 2018 cite numerous other authors’ findings of multiple Phytophthoras in Oregon and. California nurseries as well as in nurseries in various eastern states.
Nor is Phytophthoras the only pathogenic genus to pose a serious risk to America’s trees. I remind you of the fungus Fusariumeuwallacea associated with the Kuroshio and polyphagous shot hole borers, which is known to kill at least 18 species of native plants in California and additional species in South Africa. The laurel wilt fungus kills many trees and shrubs in the Lauraceae family. ‘Ohi‘a or myrtle rust kills several shrubs native to Hawai`i and threatens a wide range of plants in the Myrtaceae family in Australia and New Zealand; rapid ‘ohi‘a death fungi (Ceratocystis huliohia and Ceratocystis lukuohia) [All described here] are killing the most widespread tree on the Hawaiian Islands.
Solutions – complete &
implement modernized international and domestic phytosanitary regulations
Clearly,
standard phytosanitary practice of regulating pests known to pose a threat
does not work when many – if not most – of the damaging pests are unknown to
science until introduced to a naïve ecosystem where they start causing
noticeable levels of damage. We need a more proactive approach – as has long been
advocated by forest pathologists, including Clive Brasier 2008 and later,
Santini et al. 2013, Jung et al. 2016, Eschen et al. 2017.
National and international phytosanitary agencies have taken some steps toward adopting policies and programs that all hope will be more effective in preventing the continued spread of these highly damaging tree-killing pests. First, APHIS has had authority since 2011 – through the Not Authorized for Importation Pending Pest Risk Assessment (NAPPRA) program — to prohibit temporarily imports of plants suspected of transporting known damaging pathogens until the agency has conducted a pest risk analysis. However, utilization has lagged: only three sets of species have been proposed for listing in NAPPRA in the eight and a half years since the program was instituted in 2011. The third list of proposed species is currently open for public comment.
Another
weakness is that the program still focuses on organisms known to pose a risk.
Second, in 2018 APHIS completed a decades-long effort to revise its plant import regulations (the “Q-37” regulations). APHIS now has authority to require foreign suppliers of living plants to carry out “hazard analysis and critical control point” programs and adopt integrated pest management strategies to ensure that the plants are pest-free during production and transport.
However, implementation of this new
authority depends on APHIS negotiating agreements with individual countries
that would govern specific types of plants exported to the U.S. APHIS has not
yet announced completion of any programs under this authority. Nor is it clear
which taxa or countries APHIS will prioritize.
APHIS’ action was anticipated by the international plant health community. In 2012, member states in the International Plant Protection Convention adopted International Standard for Phytosanitary Measure 36 (ISPM#36) The standard sets up a two-level system of integrated measures, which are to be applied depending on the pest risk identified through pest risk analysis or a similar process. The “general” integrated measures are widely applicable to all imported plants for planting. The second level includes additional elements designed to address higher pest-risk situations that have been identified through pest risk analysis or other similar processes.
However,
the preponderance of international efforts to protect plant health continues to
rely on visual inspections that look for species on a list of those known to be
harmful. Yet we know that most damaging Phytophthoras
were unknown before their introduction to naïve ecosystems.
Furthermore,
use of fungicides and fungistatic chemicals – that mask infections but do not
kill that pathogen – is still allowed before shipment.
(For more complete analyses of the Q-37 revision and ISPM#36, see chapters five and four, respectively, of Fading Forests III.)
The
nursery industry is working with state regulators and APHIS to develop a voluntary
program utilizing integrated measures –
the Systems Approach to Nursery Certification (SANC) program. https://sanc.nationalplantboard.org/
SOURCES
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Four phenotypically and phylogenetically distinct lineages in Phytophthora lateralis
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Cunniffe, N.J., R.C. Cobb, R.K.
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A, Ghelardini L, De Pace C, et al.
2013. Biogeographic patterns and determinants of invasion by alien forest
pathogens in Europe. New Phytologist 197: 238–250.
Swiecki,
T.J., E.A. Bernhardt, and S.J. Frankel. 2018. Phytophthora root disease and the need for clean nursery stock in
urban forests: Part 1 Phytophthora
invasions in the urban forest & beyond. Western Arborist Fall 2018
Tsao PH.
1990. Why many Phytophthora root rots and crown rots of tree and horticultural
crops remain undetected
Fiscal Year 2020 began on October 1, 2019. In December Congress adopted funding bills (appropriations) for the full fiscal year – which ends next September.
APHIS
In
its Agriculture Appropriations bill, Congress is holding steady or increasing
funding for several APHIS programs that are important for addressing
tree-killing pests:
tree and wood pests program – $60 million (this is the same as FY2019, and $4 million above the Administration’s request);
Pest Detection – $27.4 million (this is same as FY219 and as the Administration’s request);
Methods development – $20.686 million (about the same as in FY2019 and the Administration’s request).
Specialty crops program – increased to $192.013 million. The accompanying report mentions two specific organisms as priorities – navel orangeworm and sudden oak death (apparently in response to an Oregon economic study and because Sen. Merkley is on the Appropriations Committee). This was above the $186 million in both the House and Senate bills and considerably above the Administration’s request of $176 million.
The Agriculture Appropriations bill reiterates helpful language from past laws authorizing the Secretary of Agriculture “to transfer … funds available to … the Department [of Agriculture] such sums as may be deemed necessary” to respond to disease or pest emergencies that threaten any segment of the U.S. agricultural production industry. However, for the past decade the Office of Management and Budget has prevented frequent use of this power. APHIS did receive emergency funds to address the spotted lanternfly in February 2018 (APHIS Press Release No. 0031.18)
(You might remember that in 2017-2018 I put forward
amendments to the Farm Bill that would have broadened APHIS’ access to
emergency funds. I sought especially to ensure that efforts to protect native
vegetation and urban trees would be eligible for funding. Unfortunately, this
amendment was not enacted.)
USDA Forest Service
The overall Research and Development program is funded
at $305 million – a few million above what I advocated for. Of this total, $77 million is allocated to the
Forest Inventory and Analysis program. In the past, research on invasive
species has received about 10% of the total research funds. The USFS has been
directed by Congress to restructure its research program. I will monitor any
changes and determine the implications for invasive species concerns.
USFS engagement on pest issues with other federal
agencies and state, local government, and private land managers is carried out
through the Forest Health Management program under the State and Private
Forestry division. While neither the appropriations legislation nor the
accompanying report provides any direction on forest health activities,
program staff report that funding for the overall program totals $104 million –
about $6 million more than in FY2019. Program work on federal lands is funded
at $66
million. However, $3 million has been deducted as part of a budget reform. After the deduction, this allocation is about $7 million above the
funding level for FY 2019. Program work on non-federal “cooperative” lands is funded at $44 million. Congress has instructed that $2 million of this total be given to the eastern
states’ forest health monitoring cooperative. The total “cooperative” lands allocation is
$2 million above the FY2019 allocation.
Conclusion
I am very pleased by Congress maintaining or
increasing funds for APHIS’ forestry programs. I am somewhat concerned by the pressure
to reform USFS programs. I worry especially about the increasing focus on
managing pests on federal lands compared to non-federal lands because nearly
all damaging invasions begin on non-federal lands.
Posted by Faith Campbell
We
welcome comments that supplement or correct factual information, suggest new
approaches, or promote thoughtful consideration. We post comments that disagree
with us — but not those we judge to be not civil or inflammatory.
Hawaii’s
dryland forest is a highly endangered ecosystem. More than 90% of dry forests
are already lost due to habitat destruction and the spread of invasive plant
and animal species. However, a new publication documents some recovery of
wiliwili trees from one major pest. At the same time, a new pest is spreading
and killing naio, a critical dryland shrub. Both pests originated in countries that have rarely
if ever been a source of U.S. pests. This is worrying because phytosanitary
agencies have their hands full with imports from the usual sources. The role of
California as a source of invasive species in Hawai`i has long deserved federal
attention – but as far as I know has not received it.
Hope for Wiliwili Trees
The
Hawaiian endemic wiliwili tree, Erythrina
sandwicensis, occurs in lowland dry forests on all the major islands from
sea level to 600 m. Wililwili is a dominant overstory tree in these habitats.
(Unless otherwise noted, the principal source is Kaufman et al. in press – full
citation at end of blog.)
The tree has been severely affected by the introduced Erythrina gall wasp, Quadrastichus erythrinae (EGW). The gall wasp was detected on Oahu in 2005 and quickly spread to the other Hawaiian islands.
Arrival
of the EGW on Oahu was part of the insect’s rapid global range expansion. Originally from East Africa, it was first
detected in the Mascarene Islands and Singapore in 2003. At the time, it was unknown
to science. Within a few years it had spread across Asia, many Pacific islands
(including Hawai`i), and to the Americas, including Florida in 2006, Brazil in 2014
(Culik 2014), and Mexico in 2017 (Palacios-Torres 2017). Although apparently restricted
to the Erythrina genus as host, it
has lots of opportunities. This genus has 116 species distributed across
tropical and subtropical regions: 72 species in the Americas, 31 in Africa, and
12 in Asia.
The
severe damage to wiliwili (and to non-native Erythrina trees planted in urban areas and as windbreaks) prompted Hawaiian
officials to immediately initiate efforts to find a classical biological
control agent. The process moved rapidly. A candidate – a parasitic wasp
species new to science, Eurytoma
erythrinae – was found in East Africa in 2006. Host specificity testing was
carried out. Scientists quickly learned to rear the parasitic wasp in laboratories.
Release of the biocontrol agent was approved in November 2008 – only three and
a half years after the EGW was detected on Oahu.
The
biocontrol agent’s impact was quickly apparent. Establishment was confirmed
within 1–4 months at all release locations throughout Hawai`i. Reduced pest impacts
to trees were detected within two years. By 2018, only 33% of the foliage was
damaged on the majority of wiliwili trees. Damage to non-native Erythrina had also declined.
Results of Biocontrol
Agent’s Release
The
biocontrol agent’s efficacy in reducing EGW’s impacts on trees has been
evaluated for 10 years after the agent’s release. Monitoring was conducted at
sites on four of the six main islands. (The monitoring program and its findings
are described in Kaufman et al. in press).
I wonder how
many other biocontrol agents have been monitored so closely for such a long
time? Shouldn’t they all be?
Given
the uniqueness and importance of such long-term assessment, it is worth looking
at the data in detail.
1) Foliar Damage
and Tree Health
In
2008, before release of the biocontrol agent, more than 70% of young shoots in
wiliwili trees that were inspected were severely infested. The damage rating of
“severe” fell from about 80% of trees in 2008 to about 40% in 2011. About 20%
of trees surveyed – at sites on all islands – had no gall damage.
By
three years after release of the biocontrol agent (2011), mortality rates
attributed to stress from the EGW infestation for trees in natural areas fell
to 21%. Mortality rates for trees in botanical gardens was somewhat higher –
34%. Kaufman et al. proposed several
possible reasons: a) lingering presence of systemic insecticides that might
have harmed the biocontrol agents early in the releases; b) year-round sustenance
for the EGW as a result of the i) presence of alternative hosts and ii) supplemental
irrigation which maintained fresh foliage on the trees.
Less
intensive monitoring occurred during 2013 – 2018. It showed continuing substantial
suppression of EGW damage on Erythrina
foliage, although levels varied among locations. Sites with the lowest
precipitation and higher temperatures throughout the year had the slowest
recovery of wiliwili. Still, trees are now producing vegetative flushes and
healthier canopies during non-dormant periods.
2) Flower and Seed
Damage
Successful
reduction of infestations in flowers and seedpods was less immediate. Still, by
2011, seed-set had increased from less than 3% of trees setting and maturing
seed, to almost 30% with mature seed. The proportion of trees bearing
inflorescences also increased, with more than 60% of trees blooming three years
after introduction of the biocontrol agent. There was also a slow but steady
increase in seed production.
However,
in 2019, it remains unclear how infestation of seedpods will affect germination
and therefore future plant recruitment.
More
worrying, little recruitment was observed over the 10 years. Hawaiian
authorities have completed tests on, and are preparing a petition for release of,
a second biocontrol agent, Aprostocitus
nites. It is hoped that it will further suppress EGW in flowers and
seedpods.
Still, poor recruitment is likely due to the combined impacts of multiple invasive species in native environments. A significant factor is a second insect pest – a bruchid, Specularius impressithorax – which can cause loss of more than 75% of the seed crop. I hope authorities are seeking methods to reduce this insect’s impacts.
The Hawaiian species group of the IUCN has given the wiliwili tree the Reed Book designation of “vulnerable”.
Worries for Naio
Naio
(Myoporum sandwicense)is an integral component of native Hawaiian
ecosystems, especially in dry forests, lowlands, and upland shrublands.
However, it is also found in mesic and wet forest habitats. Naio is found on all
of the main Hawaiian Islands at elevations ranging from sea level to 3000 m.
The loss of this species would be not only a significant loss of native biological
diversity but also a structural loss to native forest habitats.
The
invasive non-native Myoporum thrips, Klambothrips
myopori, was detected on the Big Island (Hawai‘i Island) in 2009 – four
years after it was first detected on ornamental Myoporum species in California. At the time of the California
detection, the species was unknown to science. It is now known that this
species is native to Tasmania.
The
thrips feeds on and causes galls on plants’ terminal growth and can eventually
lead to death of the plant.
For close to a decade, the Myoporum thrips was restricted to the Big Island. It has now been found on Oahu (Wright pers. comm.) Alarmed by the high mortality of plants in California, in September 2010, the Hawaii Department of Lands and Natural Resources Division of Forestry and Wildlife and the University of Hawai‘i initiated efforts to determine spatial distribution, infestation rates, and overall tree health of naio populations on the Big Island. Monitoring took place at nine protected natural habitats for four years. This monitoring program was supported by the USFS Forest Health Protection program. (See also the chapter on naio by Kaufman et al. 2019 in Potter et al. 2019 – full citation at the end of this blog.)
The monitoring confirmed that the myoporum thrips has spread and colonized natural habitats on the leeward side of Hawai`i Island. Infestation rates increased considerably at all sites over the duration of the four-year sampling period. Trees experiencing high infestation levels also showed branch dieback.
Medium-elevation sites (between 500–999 m) had the highest infestations and dieback: over 70% of the shoots had the worst damage.. At two sites, over 70% of the monitored trees have died.
Even
though flowers and fruits were still seen at all sites, little to no plant
recruitment was observed at these sites. Thus another plant species important
in this endangered plant community is in decline.
Few
management strategies are available for this pest. They include preventing
spread to other islands and early detection followed by rapid application of pesticides.
Implications
and Conclusions
The Erythrina gall wasp and myoporum thrips are only two of the thousands of invasive species established in Hawai`i. Island ecosystems, especially Hawai`i, are well recognized as especially vulnerable to invasive species. It has been estimated that on average 20 new arthropod species become established in Hawai`i every year.
East Africa and Tasmania are new sources for invasive species. Phytosanitary agencies need to adjust their targetting of high-risk imports to recognize this reality. Regarding the Hawaiian introduction of the thrips, there was probably made an intermediary stop in California – which is not unusual. (See also ohia rust.)
I
applaud Hawaiian officials’ quick action to counter these pests. I wish their
counterparts in other states did the same.
There
are multiple threats to Hawaii’s dry forests, including habitat modification
and fragmentation; wild fires; seed predation by rodents; predation on seeds, seedling,
and saplings by introduced ungulates (e.g.
feral goats, pigs and deer); competition with invasive weeds; and damage by
invasive insect pests and diseases.
With
so much of Hawaii’s dry forests already lost, the release of biocontrol agents
targetting specific pests is only one element of a much-needed effort. Long-term protection of wiliwili and naio
depends on greater efforts to reduce all threats and to stimulate natural
regeneration of this ecosystem. These programs could include predator-proof
fencing to keep out ungulates; baiting rodents and snails; and active
collection. Breeding, and planting of threatened plant species in an effort to
protect both the individual species and the habitat.
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
Potter,
K.M. B.L. Conkling. 2019. Forest Health Monitoring: National Status, Trends,
and Analysis 2018. Forest Service Research & Development Southern Research
Station General Technical Report SRS-239
Kaufman,
L.V, E. Parsons, D. Zarders, C. King, and R. Hauff. 2019. CHAPTER 9. Monitoring
Myoporum thrips, Klambothrips myopori (Thysanoptera: Phlaeothripidae), in
Hawaii
Wright, Mark. 2005. Assistant
Professor and Extension Specialist, University of Hawaii. Personal
communication.
The National Park Service has a legal mandate to manage lands and waters under its jurisdiction so as to “preserve unimpaired” their natural and cultural resources (NPS Organic Act 54 U.S.C. § 100101, et seq.) Invasive species undermine efforts to achieve that mission. In 2000, the NPS adopted a program to coordinate management of invasive plants. It’s not as effective as needed – see the strategic plan.
However, only recently has NPS begun trying to prioritize and coordinate programs targetting the many animals and animal diseases which threaten Park resources. These organisms range from emerald ash borer and quagga mussels; to pythons, goats, and pigs; to diseases such as white nose syndrome of bats and avian malaria in Hawai`i.
In 2017, NPS released an internal study of the pervasive threat to Park resources posed by invasive animals and discussed steps to overcome barriers to more effective responses (Redford et al., 2017; full citation at end of this blog). The Chief of the Biological Resources Division initiated this report by asking a Science Panel to evaluate the extent of the invasive animal problem, assess management needs, review best practices, and assess potential models that could serve as a service-wide organizational framework. The report was to pay particular attention to innovative and creative approaches including, but not limited to, new genomic tools. I summarized the Panel’s findings and conclusions in a blog when its report appeared in 2017.
Significantly, the
Panel’s final report states that “a general record of failure to control
invasive species across the system” was caused principally by a lack of support
for invasive species programs from NPS leadership.
This
report has now appeared in the form of a peer-reviewed article in the journal Biological Invasions by Dayer et al. 2019 (full citation at end of
this blog). Although nine of the ten authors are the same on both reports there
are substantive differences in content. For example, the journal article
reiterates the principal findings and conclusions of the Panel’s final report,
but in less blunt language.
What’s Been Watered
Down
The
toning down is seen clearly in the statements some of the panel’s six key
findings.
Finding
#1
The panel’s report says: invasive animals pose a significant threat to
the cultural and natural values and the infrastructure of U.S. national parks.
To date, the NPS has not effectively addressed the threat they pose.
Dayer et al. says: the ubiquitous presence of invasive animals in parks
undermines the NPS mission.
Finding
#2
The panel’s report says: managing
invasive animals will require action starting at the highest levels, engaging
all levels of NPS management, and will require changes in NPS culture and
capacity.
Dayer et al. says: coordinated action is required to meet the challenge.
Finding
#4
The panel’s report states: effective
management of invasive animals will require stakeholder engagement, education,
and behavior change.
Dayer et al. says: public engagement, cooperation and support is [sic]
critical.
Wording
of the other three “key findings” was also changed, but these changes are less
substantive.
Drayer
et al. also avoid the word “failure”
in describing the current status of NPS” efforts to manage invasive animal
species. Instead, these authors conclude that the invasive species threat “is
of sufficient magnitude and urgency that it would be appropriate for the NPS to
formally declare invasive animals as a service-wide priority.”
Where the
Documents Agree – Sort of
Both
the Panel’s report and Dayer et al.
state that invasive animal threats are under-prioritized and under-funded. They
say that addressing this challenge must begin at the highest levels within the
NPS, engage all levels of management, and will require investments from the NPS
leadership. Even within individual parks,
they acknowledge that staffs struggle to communicate the importance of invasive
animal control efforts to their park leadership, especially given competition with
other concerns that appear to be more urgent. And they admit that parks also
lack staff capacity in both numbers and expertise.
Also,
both the Panel’s report and Dayer et al.
urge the NPS to acknowledge formally that invasive animals represent a crisis
on par with each of the three major crises that drove Service-wide change in
the past: over-abundance of ungulates due to predator control; Yellowstone fire
crisis (which led to new wildfire awareness in the country); and recognition of
the importance of climate change.
The
Panel suggested ways to update NPS’ culture and capacity: providing incentives
for staff to (1) address long-term threats (not just “urgent” ones) and (2) put
time and effort into coordinating with potential partners, including other park
units, agencies at all levels of government, non-governmental organizations,
private landowners, and economic entities. Dayer et al. mention these barriers but does not directly mention
changing incentives as one way to overcome them.
Both
the Panel’s report and Dayer et al.
suggest integrating invasive animal threats and management into long-range
planning goals for natural and cultural landscapes and day-to-day operations of
parks and relevant technical programs (e.g., Biological Resources Division,
Water Resources Division, and Inventory and Monitoring Division).
What is Missing
from the Journal Publication
The
Panel’s final report noted the need for increased funding. It said that such
funding would need to be both consistent and sufficiently flexible to allow
parks to respond to time-sensitive management issues. It proposes several
approaches. These include incorporating some invasive species control programs
(e.g., for weeds and wood borers)
into infrastructure maintenance budgets; adopting invasive species as
fundraising challenges for non-governmental partners (e.g., “Friends of Park” and the National Park Foundation); and
adopting invasive species as a priority threat. Dayer et al. do not discuss funding issues.
The final internal report envisioned the
NPS becoming a leader on the invasive species issue by 1) testing emerging best
management practices, and 2) educating visitors on the serious threat that
invasive species pose to parks’ biodiversity. As part of this process, the
authors suggest that the NPS also take the lead in countering invasive species
denialism. Dayer et al. do not mention the issue of invasive species deniers.
Common Ground:
Status of Invasive Animals in the Parks
The
Panel’s report and Dayer et al. describe
the current situation similarly:
More than half of the National parks that responded to the internal survey (245 of the 326 parks) reported problems associated with one or more invasive animal species.
The total number of species recorded was 331. This is considered to be an underestimate since staffs often lack the ability to thoroughly survey their parks – especially for invertebrates.
Invasive species threats to Parks’ resources have been recognized for nearly 100 years. The original report notes that 155 parks reported the presence of one or more exotic vertebrate species in 1977. At that time, exotic animals were the fourth most commonly reported source of threats. In 1991, parks identified 200 unfunded projects to address exotic species, costing almost $30 million.
Only a small percentage of non-native animal invasions are under active management. Dayer et al. stated that 23% have management plans at the park unit level, and only 11% are reported as being ‘‘under control”.
Individual parks have effective programs targetting specific bioinvaders (examples are described in Redford et al; a brief summary of these efforts is provided in my previous blog.
Common Ground on
Some Solutions
The
report and Dayer et al. promote the
same steps to improve invasive animal management across the Service. Both note
that the NPS is adopting formal decision support tactics to update and
strengthen natural resource management across the board. More specific steps include
establishing
a coordination mechanism that enables ongoing and timely information sharing.
mainstreaming
invasive species issue across the NPS branches or creating a cross-cutting IAS
initiative among the Biological Resources Division, Water Resources Division,
Inventory and Monitoring Division, Climate Change Response Program, and the
regional offices.
While
both documents call on the NPS to develop and test emerging technologies, the
Panel’s final report is more detailed,
providing, in Table 5, a list of several areas of special interest, including
remotely triggered traps, species-specific toxicants, toxicant delivery
systems, drones, environmental DNA, and sterile-male releases. Dayer et al. mention eDNA and metabarcoding
for ED/RR, biocontrol, and gene drives to control invasive pathogens. (Neither
document discusses possible concerns regarding use of CRISPR and other
gene-altering technologies, other than to say there would be public concerns that
would need to be addressed.)
Both
documents note the necessity of working with resource managers beyond park
boundaries to detect and manage species before they arrive in parks. They note
that developing and operationalizing such partnerships requires time and
resources. Furthermore, invasive species prevention, eradication, and
containment programs can be effective only with public support. They suggest
strengthening NPS’ highly regarded public outreach and interpretation program
to build such support, including through the use of citizen scientists.
The
Panel’s final report said that the NPS should recognize that the condition of
the ecosystem is the objective of efforts.
Its authors recognized that achieving this goal might require
reconsidering how ecosystem management is organized within NPS so interacting
stressors (e.g., fire) and management
levers (e.g., pest eradication/suppression, prescribed fire) would be addressed.
For this, the NPS would need to create a focused capacity to address the
pressing issue of invasive animals in such a way that fosters integrated
resource management within parks, focusing on fundamental values of ecosystem
states, and not eradication targets. Dayer et
al. called for the same changes without specifically labelling “condition
of the ecosystem” as the goal.
Publication of
Dayer et al. prompted me to find out
what progress the NPS has made in responding to the “key findings” in the
Panel’s final report (neither publication calls them “recommendations”).
The
National Park Service has acted on the recommendation to appoint an “invasive
animal coordinator” within the Biological Resources Division. That person is Jennifer Sieracki. However, I wonder whether a person located in BRD is of sufficient stature to
influence agency policy across all divisions. It is not clear whether there is active
coordination with the national-level invasive plant coordinator.
Dr.
Sieriaki responded to my query by noting the following new efforts 1) to
improve outreach to partners and
the public, and 2) to expand formal and informal partnerships with local,
state, federal and tribal entities and local communities near parks.
NPS should soon finalize
two formal partnerships with other agencies and organizations for outreach and
management of invasive animal species.
NPS is working with
researchers at the US Geological Survey to expand an existing modeling tool for
identifying potential suitable habitat for invasive plant species to include
invasive insects. This will help staff focus on the most likely locations for
introductions and thus assist with early detection and control.
NPS has created a
Community of Practice so NPS employees can seek each other’s advice on addressing
invasive animal issues. A workshop of regional invasive species coordinators is
planned for the coming months to guide direction of the service-wide program
and identify other top priorities. (Seriacki pers. comm.)
I also wonder whether the NPS can achieve the top-level coordination and outreach to the public called for by both reports while complying with the terms of Public Law 116-9 – the John N. Dingle Jr. Conservation, Management, and Recreation Act, which was enacted a year ago. Title VII, Section 10(i) of this law limits spending to carry out invasive species program management and oversight to 10% of appropriated funds. Less than 15% may be spent on investigations (research), development activities, and outreach and public awareness efforts (Section 10(h)). The law does allow spending for investigations regarding methods for early detection and rapid response, prevention, control, or management; as well as inspections and interception or confiscation of invasive species to prevent in-park introductions.
For more information, see my previous criticism of NPS failure to address invasive species issues here.
Posted by Faith Campbell
We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.
See also my earlier discussion of the new legislation here.
SOURCES
Dayer,
A.A., K.H. Redford, K.J. Campbell, C.R. Dickman, R.S. Epanchin-Niell, E.D.
Grosholz, D.E. Hallac, E.F. Leslie, L.A. Richardson, M.W. Schwartz. 2019. The
unaddressed threat of invasive animals in U.S. National Parks. Biol Invasions
Redford,
K.H., K. Campbell, A. Dayer, C. Dickman, R. Epanchin-Niell, T. Grosholz, D.
Hallac, L. Richardson, M. Schwartz. 2017. Invasive animals in U. S. National Parks:
By a science panel. Natural Resource Report NPS/NRSS/BRD/NRR—2017/1564. NPS,
Fort Collins, Colorado. Commissioned by the NPS Chief of Biological Resources
Division. https://irma.nps.gov/DataStore/DownloadFile/594922
Jennifer Sieracki, Invasive Animal Coordinator,
Biological Resources Division, National Park Service