Invasive Earthworms Need Action!

 worm_medAmynthes agrestis; National Park Service photo

 

Earthworms have been largely ignored as a class of invaders. But evidence is accumulating that their numbers and impacts are too significant to ignore.

 

Non-indigenous earthworms began arriving in the Americas with the first European colonists and they are now widespread. One study (see summary of Reynolds and Wetzel 2008 here) found 67 introduced species among the 253 earthworm species in North America (including Mexico, Puerto Rico, Hawaii, and Bermuda).  In Illinois, 20 of the 38 species are introduced. Nuzzo et al. 2009 recorded a total of 11 earthworm species – all nonnative – at 15 forest sites in central New York and northeastern Pennsylvania.

 

Earthworms are good invaders – they reproduce quickly and are easily transported to new places – both carelessly and deliberately for bait, composting, or other uses.

 

As ecosystem engineers, invasive earthworms cause significant impacts to the soil and leaf litter, as well as to plants and animals dependent on those strata.  However, they are little studied and few efforts been made to address their threat.  Wisconsin is the pioneer (see below).

 

Ecosystem Engineers: Impacts on Soil, Plants, and Animals

 

Invasive alien earthworms cause enormous damage in forest environments. (I have seen no information about the damage they might cause in other natural systems.)  Earthworms can change soil chemistry, soil structure, and the quantity and quality of the litter layer on the soil surface. Changes include rapid incorporation of leaf litter into the soil, alteration of soil chemistry, changes in soil pH, mixing among soil layers, and increased soil disturbance. Such changes have been shown to harm native plant species – both herbaceous ones on the forest floor as well as the regeneration of woody vegetation, including trees.  See the review just published by Craven et al. 2016 and Hale and Nuzzo references below).

 

Craven et al. (2016) conducted a meta-analysis of 645 observations in earlier publications. They sought to measure the effects of introduced earthworms on plant diversity, cover of plant functional groups, and cover of native and non-native plants. Sites with a higher the diversity of invading earthworms – with associated variety in behaviors (see below) – had greater declines in plant diversity.  Higher earthworm biomass or density did not reduce plant diversity but did change plant community composition:  cover of sedges and grasses and non-native plant species significantly increased, and cover of native plant species (of all functional groups) tended to decrease. The increase in non-native plant cover in areas with higher earthworm biomass is thus an example of ‘invasional meltdown’ as propounded by Simberloff and Von Holle in 1999.

 

Craven et al. 2016 propose several direct and indirect mechanisms by which introduced worms might affect plant species. These include ingestion of seeds or seedlings, burying seeds, and alteration of water or nutrient availability, mycorrhizal associations, and soil structure. European and Asian plant species that co-evolved in the presence of earthworms could better tolerate earthworms’ presence.

 

Important Questions

 

Craven et al. 2016 note that the interaction of the invader-related factors with other site-related conditions such as deer browsing, fire history, forest management, and land-use history require further study to disentangle. Many other questions need to be answered, too.


Although Craven et al. (2016) do not specify the geographic range of the studies analyzed, I believe most were conducted in the northern and northeastern regions of the United States and some parts of Canada. It would be interesting to see if these studies’ findings differed from those carried out in Great Smoky Mountains National Park on the Tennessee-North Carolina border. The latter is an area where – unlike the northern states – earthworms were not wiped out by the most recent glaciation.  (See references by Bruce Snyder and Jeremy Craft, below.)

 

The finding that worm species diversity is associated with decreased plant species diversity seems to indicate that worms’ impacts might vary depending on the behavior of the worm in question – especially whether the worms remain on or near the soil surface and — if not — how deeply they burrow.  Are studies under way to clarify these differences?

 

Furthermore, do the impacts of European worms – the subjects of most of the studies carried out in Minnesota, New York, and Pennsylvania – differ substantially from the impacts of Asian earthworms? Or are any differences explained better by the species’ activity in the soil (e.g., depth of burrows) than their origins?

 

Impacts of earthworms on wildlife are less studied and perhaps less clear.  Several studies have focused on salamanders because of their known dependence on leaf litter. In a study of 10 sites in central New York and northeastern Pennsylvania, Maertz et al. 2009 found that salamander abundance declined exponentially with decreasing volume of leaf litter. They suggested that the salamander declines were a response to declines in the abundance of small arthropods, a stable resource.

A study by Ziemba et al. (2016) in Ohio involved Asian worms (genera Amynthas and Metaphire) rather than the European worms most often included in studies carried out in Minnesota, New York, and Pennsylvania.  These authors found a complex picture: earthworm abundance was negatively associated with juvenile and male salamander abundance, but had no relationship with female abundance.

Craft (2009) found that reduced leaf litter mass in invaded areas of Great Smoky Mountains National Park diminished habitat for both salamanders and salamander prey.

Others have studied millipedes – a largely unappreciated example of biological diversity in the Southern Appalachian Mountains – in Great Smoky Mountains National Park. Snyder and colleagues (2013) found that earthworms in the genus Amynthas altered soils by decreasing the depth of partially decomposed organic horizons and increasing soil aggregation. The result was a significant decrease in millipede abundance and species richness – probably as a result of competition for food.

Results from a study of earthworms’ effects on the Park’s food web by Anita Juen and Daniela Straube, begun in 2010, have not yet been published (pers. comm. from GRSM staff).

Even birds might be affected by worm invasions. One study in Wisconsin found that hermit thrush and ovenbird populations are lower in areas infested by worms. Possible reasons for the decline are that nests (on the ground) are more vulnerable to predation when located in the grasses promoted by worms, and a reduction in invertebrates fed to nestlings.

 

Expanding Risks

Several non-native earthworm species have been collected (so far) only from greenhouses or other places of indoor cultivation.  But can we be sure that they are not being spread to yards, parks, and other places halfway to natural systems through movement of plants and mulch?

 

Earthworms are extremely difficult to manage once established.

Are these challenges the reasons why few official efforts to control earthworm spread have been adopted? Or is it the animals’ public image – they are widely regarded as “good” critters that enrich the soil and facilitate composting. Or is it that trying to control worms will require enhanced regulation of the nursery and green waste industries?

worms1Amynthes photo; from Wisconsin DNR website

Wisconsin Is the Policy Pioneer

Wisconsin stands out for trying to address the issue! The state’s conservation and phytosanitary officials became alarmed when they detected Amynthas species in the University of Wisconsin Arboretum in 2013.  This is the site of regular plant sales,a likely pathway for spread.  Wisconsin now knows this genus of worms to be present in 21 counties, mainly along urban corridors.  They have not yet been found in the state’s forests.

Wisconsin is acting to protect its forests despite Amynthas worms having been present in the United States for over a century: Snyder, Callaham and Hendrix 2010 say several species of Amynthas were documented in Illinois and Mississippi by the 1890’s.  Some 15 species are recorded as established and widespread across the eastern United States (Reynolds and Wetzel 2004).

 

Wisconsin has classified the Amynthas genus as “restricted” – so their movement is now regulated. The risk of spread appears to be greatest through mulch produced from leaves collected in residential communities. The state held a workshop during which the regulated industry developed best management practices to address that risk. The Wisconsin Department of Natural Resources has posted a web page with information about identifying the worms and the BMPs. (Wisconsin DNR has also been a leader in tackling the firewood pathway.) The Wisconsin Department of Agriculture put the worm issue on the agenda of the National Plant Board in August 2016 and urged other states to take action.

The Wisconsin DNR webpage has

  • ID cards and other information to aid identification, g., photos of worms and the “coffee ground” soil they create;
  • a brochure with the state’s new “best management practices”
  • educate yourself and others to recognize jumping worms;
  • watch for jumping worms and signs of their presence;
  • ARRIVE CLEAN, LEAVE CLEAN – Clean soil and debris from vehicles, equipment and personal gear before moving to and from a work or recreational area;
  • only use, sell, plant, purchase or trade landscape and gardening materials and plants that appear to be free of jumping worms; and
  • only sell, purchase or trade compost that was heated to appropriate temperatures and duration following protocols that reduce pathogens.

What’s Up Where You Are?

What is your state doing to slow the spread of invasive earthworms?

  • Do nursery inspectors look for earthworms when approving plant shipments? Craven et al. 2016 findings re: higher impacts on plants as number of worm species rises demonstrate the importance of slowing spread of new species even into areas that already have some non-native earthworms.
  • Are professional associations of nurserymen and green waste recyclers educating their members about the damage caused by invasive earthworms and steps they can take to minimize worms’ spread to new areas?
  • Are organizations of anglers and gardeners in your state educating their members about the damage caused by invasive earthworms and steps they can take to minimize worms’ spread to new areas?
  • Are ecologists studying earthworm invasion impacts in other parts of the country? In non-forested ecosystems?
  • Are conservation organizations initiating or joining outreach efforts?
  • Can worm-education efforts be joined with h more robust public and private outreach focused on aquatic invaders, invasive plants, or firewood?

 

SOURCES

Bohlen, P.J., S. Scheu, C.M. Hale, M.A. McLean, S. Migge, P.M. Groffman, and D. Parkinson. 2004.  Non-native invasive earthworms as agents of change in northern temperate forests. Front Ecol Environ 2004; 2(8): 427–435

Craft, J.J. 2009. Effects of an invasive earthworm on plethodontid salamanders in Great Smoky Mountans National Park. Thesis prepared at Western Carolina University.

Craven, D., M.P. Thakur, E.K. Cameron, L.E. Frelich, R.B. Ejour, R.B. Blair, B. Blossey, J. Burtis, A. Choi, A. Davalos, T.J. Fahey, N.A. Fisichelli, K. Gibson, I.T. Handa, K. Hopfensperger, S.R. Loss, V. Nuzzo, J.C. Maerz, T. Sackett, B.C. Scharenbroch, S.M. Smith, M. Vellend, L.G. Umek, and N. Eisenhauer. 2016.The unseen invaders: intro earthworms as drivers of change in plant communities in No Am forests (a meta-analysis). Global Change Biology (2016), doi: 10.1111/gcb.13446 available here.

Hendrix, P.F. 2010. Spatial variability of an invasive earthworm (Amynthas agrestis) population and potential impacts on soil characteristics and millipedes in the Great Smoky Mountains National Park, USA. Biological Invasions DOI 10.1007/s10530-010-9826-4

Maertz, J.C., V. Nuzzo, B. Blossey.  2009. Declines in Woodland Salamander Abundance Associated with Non-Native Earthworm and Plant Invasions. Conservation Biology Volume 23, Issue 4 August 2009  Pages 975–981

Nuzzo, V.A., J.C. Maerz, B. Blossey. 2009. Earthworm Invasion as the Driving Force Behind Plant Invasion and Community Change in Northeastern North American Forests. Conservation Biology Volume 23, Number 4, 966-974.

Simberloff, D.  and Von Holle, B. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological invasions 1, 21-32

Snyder, B.A., M.A. Callaham, C.N. Lowe, P.F. Hendrix. 2013. Earthworm invasion in North America: food resource competition affects native millipede survival and invasive earthworm reproduction. Soil Biology and Biochemistry 57, 212-216

Ziemba JL, Hickerson C-AM, Anthony CD. 2016. Invasive Asian Earthworms Negatively Impact Keystone Terrestrial Salamanders. PLoS ONE 11(5): e0151591. doi:10.1371/journal.pone.0151591

 

See also:

Global picture: https://www.newscientist.com/article/mg19325931-600-war-of-the-worms/

Great Lakes Wormwatch website: http://www.nrri.umn.edu/worms/research/publications.html  

Illinois Natural History Survey webpage: http://wwn.inhs.illinois.edu/~mjwetzel/IllinoisEarthworms.html

Wisconsin  DNR http://dnr.wi.gov/topic/invasives/fact/jumpingWorm/index.html

Information on western Canada:

http://bcinvasives.ca/news-events/recent-highlights/earthworm-invasion-calling-all-citizen-scientists/

http://ibis.geog.ubc.ca/biodiversity/efauna/EarthwormsofBritishColumbia.html

Native Earthworms of British Columbia Forests: http://www.cfs.nrcan.gc.ca/pubwarehouse/pdfs/5102.pdf

 

Posted by Faith Campbell

Dr. Sarah Reichard 1957-2016

We  mourn the sudden and unexpected death of Sarah Reichard, Professor in the School of Forest Resources at the University of Washington and Director of the UW Botanical Garden. For more than 25 years, Sarah was a leading researcher on invasive plants. She studied their traits; sought to predict  their invasive ability; searched for ways to detect new invaders early; and examined the effects of plant invaders on native ecosystems. She also engaged the nursery industry, botanical gardens, and other horticultural groups in addressing invasive plant threats. She brought an open style, compassion, deep thoughtfulness — and yet a burning desire for righteous change — to all this work.

Sarah established her expertise early and was long a recognized expert.She published widely — in academic journals, gardening magazines, and policy papers.  Most recently, she authored the well-received book, The Conscientious Gardener: Cultivating a Garden Ethic. Also, Sarah was a key organizer and participant in meetings — both international and national — that addressed invasive species. Many of us in the conservation community relied upon her work and advice to guide invasive plant policy.

We join her husband, her colleagues at the University of Washington, and invasive plant experts around the world in mourning Sarah’s untimely death. Our world is a poorer place without her bright and generous spirit.

 

Faith Campbell

Phyllis Windle

Peter Jenkins

 

 

A Red List for Trees!

16 dead sweet bay + grpF.T. Campbell  dead sweetbay, Florida Everglades

At the global level, the World Conservation Union (IUCN) is the recognized leader in conservation.  Information from the IUCN’s Red List has been widely used to inform conservation policies and legislation, as a tool for environmental monitoring and reporting, and to prioritize areas for conservation action.

 

The IUCN is holding its World Conservation Congress in Honolulu during the first half of September.  The several sessions focused on both invasive species and forests have been grouped into “Journeys”.  The invasive species Journey schedule is available here.  The schedule for the forest Journey is available here   I don’t think either puts much emphasis on the year-old Tree Specialist Group.

 

Over the decades, the Union has increasingly engaged on plant conservation issues. The plants under consideration now include trees! There are multiple ways that you can be part of this important effort. Details are below. One of the efforts’ leaders assures me that the IUCN process will address tree species not yet “endangered” but under severe pressure – currently or virtually certainly in the near future – from established non-native insects and pathogens.

 

The IUCN has noted that trees have high ecological, economic, and cultural value. Forests are being converted or degraded by many human-related activities, including overharvesting, fire and grazing – to say nothing of climate change and non-native pests. Yet – the impacts of forest conversion and degradation on tree species per se are largely unknown. How many tree species qualify for a “Red List” category: extinct, critically endangered, endangered, or vulnerable? (For a discussion of the criteria applied in assigning categories, go here.

(Of course, full-scale extinction or endangerment of a species is the extreme; ecological damage begins earlier and more locally, as the species declines as the result of a suite of pressures …)

 

The IUCN has formed a Global Tree Specialist Group to conduct a comprehensive conservation assessment of the world’s tree species, linked to IUCN’s Red List. The effort is being led by the Tree Specialist Group  and the Botanic Gardens Conservation International (BGCI). The group’s mission, underlying considerations and process are described in an article published in the Oryx article cited below.

 

IUCN has recently completed analyses of extinction risk in selected animal groups. They concluded that 14% of bird, 33% of amphibian, and 22% of mammal species are either threatened or extinct.

 

Preparing the same type of analysis for tree species will be more complicated. First there are many more plant species than ones in the selected groups of animals. Scientists don’t know the total number of extant tree species. One estimate is 60,000.  If that estimate is in the ballpark, the status of approximately 84% of tree species has not yet been assessed. Assessments of tree species begun in the 1990s have resulted in approximately 9,500 species being included in one of the Red List categories.  They represent slightly less than half of all plant species listed.

 

To achieve the goal of assessing the status of all tree species by 2020, organizers plan to adopt the approach used successfully in the recent assessments of vertebrate groups – mobilizing global data sets (which have become more numerous and easier to use) and hundreds of volunteer experts.

 

To start, the Group is focused on specific plant families with high numbers of trees, e.g., Aquifoliaceae, Fabaceae, Fagaceae, Lauraceae, Meliaceae and Myrtaceae. Combined, these families include more than 20,000 species. Assessments of Betulaceae and Ebenaceae have already started, led by BGCI and the Missouri Botanical Garden, respectively.

 

Project leaders hope to complete 5,000 more tree assessments – new or updates – during 2016.

 

What is Under Way

 

Other IUCN specialist groups are assisting in assessing the status of trees in various geographic regions or with particular human uses. The IUCN Plants for People initiative is already assessing timber, medicinal and crop wild relatives. The Crop Wild Relative Specialist Group has prepared draft assessments for over 90 woody species of Malus, Prunus, Pistacia and Mangifera. Specialist Groups and Red List authorities in South Africa, Brazil, and East Africa and several island groups are contributing.

 

A third focus will be tree species presumed to be most at risk from climate change, e.g., montane and island trees. IUCN Specialist Groups in Hawai`i, New Caledonia, Galapagos, Mascarene Islands, Fiji, and Madagascar are working.

 

The BGCI is making progress on assessing Europe’s non-coniferous trees. If you wish to help, contact Malin Rivers at malin.rivers@bgci.org.

 

In North America, the U.S. Forest Service hosted a meeting on “Gene Conservation of Tree Species” at the Morton Arboretum in Chicago in May 2016. Murphy Westwood facilitated a special session during which “listing” experts from IUCN, NatureServe, USFS CAPTURE Program, and the U.S. Fish and Wildlife Service compared their assessment processes and discussed how data might be shared more efficiently. A goal of completing the IUCN Red List of North American Trees was agreed on. The Morton Arboretum will help coordinate the effort. To contribute please contact Murphy Westwood at mwestwood@morton.org.  

 

One suggestion was to conduct an IUCN Red List assessment for the genus Fraxinus. Two ash species – one Asian, one Central American – are included in the IUCN Red List (although one needs to be updated). Jeanne Romero-Severson of Notre Dame University has offered to undertake assessments for green ash, Fraxinus pennsylvanica, and black ash, Fraxinus nigra. If you wish to help, contact Sara Oldfield at sara@saraoldfield.net.

 

(I think several other species also warrant IUCN assessment, including redbay Persea borbonia, tanoak Notholithocarpus densiflorus, and whitebark pine Pinus albicaulis)

 

This IUCN effort represents yet a fourth set of people examining tree-pest interactions – people integrated into traditional, internationally-focused conservation organizations. There are at least three other groups already involved: (1) forest pest experts in academia and government agencies, (2) people who focus on invasive species, and (3) phytosanitary officials. I think that these latter three groups already interact less smoothly than would be ideal. How can we all combine our efforts to enhance protection programs?

 

Might more of the scientists who work on insects and pathogens attacking tree species join the IUCN Tree Specialist group? Might organizers of meetings make a greater effort to engage people from all four silos in discussions of strategies? Might some virtual for a be established that could facilitate communication across the gaps – perhaps emphasizing the gap between invasive species experts and phytosanitary officials?

 

Finally, how can we use the new focus on tree species’ degree of endangerment to enhance efforts to prevent and respond to invasions by non-native insects and pathogens? How do we link these concerns to existing attention to the ecological and economic impacts – which begin to manifest long before a species qualifies as “endangered”.  How can the various approaches reinforce each other?

 

SOURCES

 

 

Newton, A., S. Oldfield, M. Rivers, J. Mark, G. Schatz, N. Tejedor Garavito, E. Cantarello, D. Golicher, L. Cayuela, and L. Miles. 2015. Towards a Global Tree Assessment. Oryx, Volume 49, Issue 3, July 2015, pp. 410-415.

 

Explanatory information available at

https://www.bgci.org/plant-conservation/globaltreeassessment/

Click to access GTALeaflet%20FINAL.pdf

 

The GTSG Newsletter is apparently available only to those who are part of the IUCN network.

 

For more information, contact Sara Oldfield, Co-Chair GTSG, at sara@saraoldfield.net

 

 

 

Posted by Faith Campbell

Biocontrol As a Strategy to Control Damage by Invasive Plants – is the Logjam Broken?

gmustard 

garlic mustard; Chris Evans,River to River CWMA;  Bugwood

As we all know, the United States is overrun by non-native plants.  As I noted in blogs posted in January and March, Rod Randall’s database lists more than 9,700 non-native plant species as naturalized in the U.S.  Not all 9,700 cause environmental damage. But hundreds do – a fact attested to by the various regional Invasive Plant and Exotic Pest Plant councils:

  • The Southeast Exotic Pest Plant Council lists approximately 400 invasive species.
  • The Mid-Atlantic Invasive Plant Council lists 285 invasive plants.
  • The Midwest Invasive Plant Network says the state agencies or state-level invasive plant councils in its region list more than 270 plant species as invasive, noxious, or pest species in the Midwest.
  • The California Invasive Plant Council lists 208.
  • Texas Invasives reports that there are more than 800 non-indigenous plant species in the state, of which 20 are considered invasive.

 

The Pacific Northwest and Northern Rockies councils do not provide lists on their websites.

 

The analysis of forest inventory data by Christopher Oswalt and colleagues — discussed in my blog in March — found that almost 40% of forest plots in the United States are invaded by alien plant species. Other than in Hawai`i, the most invaded region is forests in the eastern United States – where 46% of forest plots in the East harbor one or more of the invasive plant species included in the inventory process.

 

The March and earlier blogs discuss reasons why the invasive plant situation is likely to worsen over time.

 

Given the geographic extent of plant invasions and the environmental complications, expense, and other difficulties associated with managing invasive plants using mechanical or chemical tools, many place their hope in biological control. Scientists in the U.S. Forest Service, Agriculture Research Service, U.S Geological Survey, academia, and other institutions have devoted years to identifying promising biocontrol agents targeting some of the most widespread and damaging invasive plants.

 

Possible biocontrol agents have been identified for numerous invasive plant species  …  but relatively few have been approved for release.

 

Part of the delay is attributable to the necessity for caution to ensure that biocontrol agents are effective and do not become damaging invasive themselves.  This concern underlies the legal requirement that non-native biocontrol agents must be approved by USDA APHIS. APHIS permits are required for

  • Importation of live biocontrol agents into the U.S. or its territories
  • Interstate movement of live biocontrol agents (USDA policy allows movement of certain commercial entomophagous biocontrol agents without a permit)
  • Retaining live biocontrol agents after expiration of a permit
  • Movement of any live biocontrol agent from confinements of containment facility or for release into the environment.

The approval process is lengthy and complex – and frustrating! Its many steps were outlined in a presentation by a staffer in APHIS’ permit branch, Robert Tichenor, available here

 

As noted in the presentation, the process can take a decade or more between scientists initiating the search for possible agents to final approval. The scientists hoping to find useful biocontrol agents face possibly years of work to identify and obtain organisms that seem promising as biocontrol agents. The petitioner must then screen the putative agent(s) for efficacy and then for host specificity. Once this work has been completed, the scientist prepares a petition to APHIS asking that it approve release of the biocontrol agent(s).

At this stage, government agencies take over. When it receives a petition for release of a biocontrol agent, APHIS sends the petition to the Technical Advisory Group (TAG).  (For details about the TAG, go here.

Under the TAG charter, APHIS invites the following agencies to provide a representative to serve on the TAG: Army Corps of Engineers, Environmental Protection Agency; Department of Agriculture: APHIS, Agricultural Research Service, Forest Service, National Institute of Food and Agriculture, Natural Resource Conservation Service; Department of the Interior: Bureau of Indian Affairs, Bureau of Land Management, Bureau of Reclamation, National Park Service, Fish and Wildlife Service, Geological Survey. APHIS may also invite participation by State or other Federal government employees (one each) to represent the National Plant Board, Weed Science Society of America, and other Federal Agencies expressing interest.  Canada and Mexico are also asked their views.

 

The TAG reviews both the proposed plant list for host specificity testing and the petition for first-time field release. The TAG may suggest inclusion of certain test plants, identify conflicts of interest, and assess potential risks associated with an environmental release. In making their evaluations, TAG members are expected to represent their agency’s or organization’s perspective. The chairman seeks to build consensus. Then s/he conveys the recommendations to APHIS.

 

APHIS decides whether to proceed with the review process and so informs the petitioner and APHIS’ Policy and Program Development (PPD) division.  Using information in the Petition, APHIS prepares a Biological Assessment analyzing whether releasing the biocontrol agent might affect a species listed as endangered or threatened under the Endangered Species Act. This Biological Assessment is sent to the US Fish and Wildlife Service (FWS)  to initiate an “informal” consultation per Section 7 of the Endangered Species Act (16 U.S.C. Section 1536). The FWS’ review can take more than a year and can involve requests for additional information. For the proposed biocontrol project to proceed, APHIS must receive a letter from US FWS stating that US FWS  “concurs” with APHIS’ determination that release of the biocontrol agent is “not likely to adversely affect” listed species or designated Critical Habitat.

 

Upon receipt of the FWS concurrence letter, APHIS begins preparing an environmental assessment (EA), and consults with any affected Native American tribes. The draft EA is released for public comment, usually for a period of 30 days. Once the comments are received, APHIS reviews and responds to the comments, and issues the final EA and accompanying Finding of No Significant Impact (FONSI). A month later, the permit is issued to remove the biocontrol agent form containment and release it into the environment.

 

While APHIS normally waits for FWS approval before beginning the NEPA review – because APHIS cannot complete the FONSI until it receives FWS concurrence – staff are now considering ways to speed up the process.

 

This already lengthy process has been further hampered by retirement of key staff in both APHIS and the FWS. New staff were also probably more cautious about approving agents because of the controversy over the potential impact of biocontrol agents’ success in reducing populations of tamarisk (Tamarix spp.) on nesting habitat for the endangered southwest willow flycatcher.

 

Finally, the process itself causes delays. Petitioners are required to re-submit their proposal to the Technical Advisory Group each time it is revised to address a question raised by a reviewer. These requirements can cause delay and probably frustrate the petitioners.

Current status of weed biocontrol programs

air potato

air potato; Rebekah D. Wallace, University of Georgia; bugwood.org

The current status of weed biocontrol is partially revealed at this site, which shows the status of TAG and APHIS actions.  Some 36 biocontrol agents proposed for field release have been reviewed by the TAG since 2010.  Of these, two have completed the review process and been approved by APHIS for release: agents targeting hawkweeds (Hieracium spp.) and air potato (Dioscorea bulbifera). Both were approved in 2011. In his presentation, Dr. Tichenor said a third insect – a gall fly targeting Cape Ivy (Delairea odorata) – received a permit allowing release into the environment in May 2016.

The 33 other biocontrol agents that were approved by the TAG are still in other stages of the approval process. Dr. Tichenor reported that an environmental assessment is now being written for a leaf mining fly (Lasioptera donacis) intended to control Arundo (this agent was approved by the TAG only in April 2016 – remarkable speed in obtaining FWS clearance). Three agents are nearing the end of the Endangered Species Act §7 consultation process; these are agents targeting yellow toadflax (Linaria vulgaris), hoary cress (Lepidium draba), and the two swallow-worts (Cynanchum louiseae or Vincetoxicum nigrum; and Cynanchum rossicum or Vincetoxicum rossicum). APHIS has asked for additional information on two agents – targeting gorse and several knotweed species.

One agent intended for use against garlic mustard was rejected by the TAG in 2009.  A second agent is still under review by the TAG.

The other four species approved by the TAG in 2016 to date are presumably at the early stage of the biological assessment; these include two agents for Brazilian pepper, a beetle for Chinese tallowtree, and another insect targeting hawkweeds (genus now given as Pilosella).

 

Since 2010, the TAG has recommended against field release for eight proposed biocontrol agents.  These included species intended to control Chinese privet (Ligustrum sinense), Russian thistle (Salsola tragus), and Russian knapweed (Rhaponticum repens).  The TAG asked for additional information on four species.

 

Of course, garlic mustard and Chinese privet are among the top five most frequently detected invaders in the forest inventory study – garlic mustard in the Mid-Atlantic and Northeast, privet in the Southeast.

A fungus (Verticillium nonalfalfae ) is under study as a biocontrol agent for another widespread invasive plant, Ailanthus (tree of heaven). Research by USDA Forest Service scientists have found that a few native species of shrubs and trees are also mildly sensitive to the fungus.  Testing of additional native and agricultural species continues. The fungus occurs naturally in North America so it is not subject to the approval process described here.

 

An introduced insect, spotted lanternfly (Lycorma delicatula) also attacks Ailanthus. The lanternfly attacks a wide range of woody plants, including grapes and fruit trees. Consequently, Pennsylvania is attempting to eradicate it from the four counties in the eastern part of the state where it has been found.

 

Hundreds of invasive plant species are damaging ecosystems across the country. Biocontrol is one of the few tools available to counter the threat from invasive species – plants and others. I hope people concerned about invasive species will increase efforts to identify those bioinvaders for which biocontrol appears to offer promise, then to seek out potential biocontrol agents. And that regulatory bodies improve their ability to evaluate proposals promptly – while still being thorough. Doing nothing causes real harm.

 

Posed by Faith Campbell

New Alarms About Phytophthora species in U.S. Nurseries

 

CDFA photo monkeyflower

sticky monkey flower – plant on right is infested by P. tentaculata; photo by Suzanne Rooney-Latham, California Department of Food & Agriculture

 

In April, I posted a blog reporting on a study in Europe that documented 64 Phytophthora taxa detected in woody plant nurseries or forest restoration plantings. The presence of Phytophthora was widespread,  if not universal:  91% of the 732 nurseries analyzed and 66% of forest and landscape plantings had at least one Phytophthora taxon present.

The risk of serious disease in native European plants appears to be substantial:  one or more of 19 Phytophthora species which can attack native European or widely-planted trees and shubs were isolated from 84% of ornamental planted stands. Hundreds of previously unknown Phytophthora–host associations were observed.

These percentages could be underestimates, because detection of Phytophthora infestation is difficult. One of the principal difficiulties is that the majority of infested plants in nurseries did not display symptoms.

How does the situation in Europe compare to that that in the United States? We don’t know, because no-one has carried out a similarly wide-ranging, nation-wide study. However, some partial studies indicate reason for concern.

 

Knaus et al. 2015 summarized their own findings from Oregon and those of earlier state-by-state studies:

  • Knaus and colleagues surveyed symptomatic Rhododendron in seven nurseries in Oregon and found evidence of widespread infestation. P. syringae was found in all seven nurseries; P. plurivora in six. Nine other taxa were found in one or a few nurseries. Which Phytophthora species were present varied greatly across nurseries and – within individual nurseries – by season (spring or fall).
  • Surveys by Schwingle and colleagues of 45 nurseries in Minnesota in 2002-2003 and fewer nurseries in 2004 and 2005 found five Phytophthora species.
  • A survey by Warfield and colleagues of 14 North Carolina nurseries in 2003 found three Phytophthora species.
  • Donohue and Lamour surveyed 29 Tennessee nurseries in 2004-2005; they found seven Phytophthora species.
  • A survey of 1,619 California nurseries in 2005 and 2006 carried out by Yakabe and colleagues found eight Phytophthora species (but see below).
  • A survey of 10 Maryland nurseries by Bienapfl and Balci in 2010-2012 found 10 Phytophthora species; six of these were on plants that had arrived recently from West Coast suppliers.
  • A set of repeated surveys of four Oregon nurseries in 2006 – 2009 by Parke and colleagues found 16 Phytophthora species on rhododendron tissues (most of studies looked only at lesions on leaves)

All these studies found the P. citricola complex to be the most widespread. In West Coast nurseries, P. syringae was common.

Knaus et al. conclude that since there is a great amount of heterogeneity among Oregon nurseries, it is likely that, as more nurseries are surveyed, a greater amount of Phytophthora diversity may be discovered within nurseries.

Most of the surveys reported by Knaus and colleagues were done in response to detection of the sudden oak death pathogen (SOD), P. ramorum, on plants shipped from California and Oregon in the interstate plant trade. Since funding for tracking P. ramorum and other Phytophthora species in nursery stock has fallen considerably (see below), it is unlikely that such surveys will be repeated or expanded to other states – despite the apparent widespread presence of these actual or potential pathogens.

Crisis in Native Plant Nurseries in California – What Does it Mean for Other States?

California has discovered the widespread presence of Phytophthora in native plants used to restore native habitats after disturbance, e.g., construction of water or other projects. These pathogens were traced to native plant nurseries. Nursery stock had been planted before the infestation problem was realized – so restoration managers are now trying to clean up both the nurseries and the restoration sites. This situation was discussed during a special session of the 6th SOD Science Symposium in San Francisco in June 2016. More than 170 people attended the session – demonstrating a high level of concern in the native plant community. Abstracts and presentations will be available at http://ucanr.edu/sites/sod6/.

The problem was first discovered in 2012 when a nursery noted severe dieback of sticky monkey flower (Diplacus (Mimulus) aurantiacus). The California Department of Food and Agriculture (CDFA) identified the cause as P. tentaculata – which is a federally-designated “quarantine pest”. It had never before been detected in the United States.

Native plant nursery owners and restoration ecologists responded quickly by sending many samples for identification. Between January 2014 and June 2016, CDFA evaluated 1,500 samples from nurseries and field sites. One quarter of the samples were positive for at least one Phytophthora species. In total, 25 species were detected, although 70% of the samples belonged to one of six taxa.

Little is known about root pathogens of California’s native plants. The sample results revealed a long list of newly detected associations.  However, it has also proved especially difficult to detect symptoms on some plants. Finally, since only symptomatic plants were sampled, it is likely that additional plant-Phytophthora associations remain to be detected.

No one knows which plant-Phytophthora associations are capable of creating epidemics of plant disease. At least two species have raised particular concern:

Among the “lessons learned” are two previously identified following the detection of P. ramorum in horticultural nurseries a decade earlier and reinforced now:

  • artificial irrigation of plants in nurseries facilitates infestations and movement of infested plant material; and
  • re-use of infested pots facilitates spread of these infestations.

 

Therefore, both nursery managers and regulators need to be alert to this risk in all types of nurseries. The necessary changes in nursery practices will take time. See the talk by Alisa Shor from the Parks Conservancy, which operates the nursery for the Golden Gate National Recreation Area when the meeting presentations are posted at http://ucanr.edu/sites/sod6/. Shor described the extensive efforts made by Parks Conservancy nurseries to clean up and adopt new procedures.

 

Agencies responsible for restoration projects face a daunting task. They have found dozens of Phytophthora taxa at already-planted sites, including the two identified above as federal quarantine species. Managers must develop best management practices that apply to contract specifications for equipment and workers operating on those sites; for nurseries wishing to bid to supply plants; and for planting protocols. Meanwhile, existing restoration regulations require them to restore plant cover quickly – which cannot be done by relying on seed – which is less likely to harbor a pathogen than the containerized plants now used.

As noted above, the high-risk nursery practices identified in this case match those identified over the past decade in response to the spread of sudden oak death (SOD) through nursery stock. Ted Sweicki, an ecologist long engaged on SOD and related issues and now advising the restoration agencies, noted that it is easier to prevent introduction of a Phytophthora to a site then to clean up the site afterwards. He advocated adoption of systems approach to mitigate Phytophthora presence in nurseries. Ted said this is not a new idea! However, adoption of such practices has been far too slow in the horticultural trade. Ted was hopeful that this new crisis in California would have a different result because:

  • Owners of native plant nurseries are strongly concerned about the environment;
  • Restoration agencies are averse to being responsible for introduction of Phytophthora species to their lands; and
  • These agencies make purchases that are sufficiently large to empower the agencies to compel nurseries to comply with strict protocols.

People in other states should not rest easy. There is no reason to think this problem is limited to California. Other states need to be looking at the diversity of Phytophthora species in their nurseries and plantings. But are they doing so?

Meanwhile, federal funds that have supported studies of the genetics of P. ramorum in both West Coast forests and in nurseries are rapidly disappearing. The information provided by these studies has been crucial to tracing movement of various strains of the pathogen.

As noted in my earlier blog, none of the 59 Phytophthora taxa thought to be alien in Europe had been intercepted at European ports of entry. In the U.S., it has not been determined how the P. tentaculata detected in 2012 was introduced.  Authorities suspect it was introduced on plant imports.

These situations reinforce the importance of APHIS promptly finalizing its 2013 proposed revision to regulations governing imported plants [http://federalregister.gov/a/2013-09737]. The proposed rule would establish APHIS’ authority to require foreign plant suppliers to adopt “critical control point”-type systems approaches to improve the cleanliness of plants intended for export to the United States.  Such an approach is authorized by both a North American regional standard (RSPM#24; go here) and an international standard (ISPM#36; go here) for plant protection.

You can give APHIS a push by writing your member of Congress and Senators. Ask them to urge the Secretary of Agriculture to finalize this proposal.

As regards plants being shipped within the country, the U.S. nursery trade is working with federal and state regulators to develop and encourage adoption of similar, but voluntary, integrated systems approaches to minimize pest presence on plants being sold interstate. This proposed approach is being tested by eight nurseries across the country. However, full adoption is still years away. To learn more about the “SANC” program (“A Systems Approach to Nursery Certification”), go here.

 

See also http://www.suddenoakdeath.org/welcome-to-calphytos-org-phytophthoras-in-native-habitats/

SOURCES

Jung, T. et al. 2015 “Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease” Forest Pathology. November 2015; available from Resource Gate

Knaus, B.J., V.J. Fieland, N.J. Grunwald. 2015. Diversity of Foliar Phytophthora  Species on Rhododendron in Oregon Nurseries. Plant Disease Vol 99, No. 10 326 – 1332

 

Posted by Faith Campbell

Why doesn’t state government take action to contain pests that threaten to cost 20 million Californians $1,800 apiece?

(The total cost will exceed $36 billion – which will be borne largely by homeowners and municipalities – meaning their taxpayers.  The state will bear little of this cost.)

PB036597 fate-sm smwillow tree in Tijuana River riparian area felled by KSHB.  Photo by John Boland; used by permission

(To see more scary photos of the damage along the Tijuana River taken by John Boland, go here.

The polyphagous (PSHB) and Kuroshio (KSHB) shot hole borers pose a great threat to many tree species in California – native species in natural and urban settings; non-native species used in plantings; and agricultural crops. Yet the state government is frozen in inaction.

These two shot hole borers attack hundreds of tree species; at least 40 are reproductive hosts. For details, view the write-up here or visit the UC Riverside website here.

Some of the important reproductive hosts for PSHB are listed here; those that are also known to support reproduction of the Kuroshio shot hole borer are marked by an asterisk.

  • Box elder (Acer negundo)
  • Big leaf maple (Acer macrophyllum) *
  • California sycamore (Platanus racemosa)
  • Several willows (Salix spp.)
  • Cottonwoods  (Populus fremontii & P. trichocarpa)
  • Several  oaks (Quercus agrifolia, Q. engelmannii, Q. lobata)

Several widespread exotic species also support PSHB reproduction: they include the invasive castor bean (Ricinus communis) and widely-planted London plane tree (Platanus x acerifolia).

US Forest Service scientist Greg McPherson has analyzed the vulnerability to PSHB of urban forests in cities in three regions of southern California: the Inland Empire, Coastal Southern California, and Southwest Desert. Together, these comprise 4,244 sq. miles and have 20.5 million residents. Dr. McPherson found that:

1) Approximately 26.8 million trees – 37.8% of the region’s 70.8 million trees – are at risk. Trees at risk include

  • 5 million coast live oaks,
  • 4 million ash,
  • 3 million sycamores and plane trees,
  • 9 million stone fruit or flowering Prunus species,
  • 5 million avocadoes, and
  • 8 million citrus trees.

2) The cost for removing and replacing the 26.8 million trees would be approximately $36.2 billion. This amount averages to $1,768 per capita.

3) The value of ecosystem services forgone each year due to the loss of these trees is $1.4 billion.

4) These estimates are conservative because they:

  • do not include costs associated with damage to people and property from tree failures, as well as increased risk of fire and other hazards
  • may undervalue benefits of trees to human health and well-being; and
  • do not include newly detected host species or the shot borers’ spread.

These disasters are highly likely to occur given the extent of current infestations and difficulty in curtailing spread of the beetle/fungus complex.

 

Natural areas – especially riparian areas – are also at risk.  John Boland reports that 70% of willows studied in the Tijuana River riparian area on the California/Mexico border were infested by KSHB.  Tree branches and boles weakened by beetle attack broke in the first winter storms in early 2016.  In some sections, “native riparian forest … went from a dense stand of tall willows to a jumble of broken limbs in just a few months.”  Trees growing in the wettest parts of the riparian area were most heavily attacked and damaged.  Three highly invasive plant species – castor bean, salt cedar, and giant reed – are barely or not attacked by KSHB.  The result of the damage to native willows and likely proliferation of the invasive plants is likely to be significant alteration of the entire biological system.

(While no one knows how KSHB reached the Tijuana River, John Boland says there is a greenwaste “recycling” center in the valley. See picture below, taken by John Boland.)

OLYMPUS DIGITAL CAMERA

Regulatory action could help protect wildland, rural, and urban forests in the rest of the state – and possibly beyond. Scientists’ analysis of climate indicates that most of the urban and agricultural areas in California are at risk. The scientists have also begun analyzing the potential risk to other parts of country.

 

Why is the California government so unwilling to tackle a threat of this magnitude?

I have written about this inaction several times as it applies to the goldspotted oak borer. See my blogs on 1) California’s inaction on firewood in July 2015; 2) GSOB and firewood in September 2015;  3) contrasting states’ action on mussels with inaction on firewood posted in December 2015;  and 4) the threats to oaks, posted in April 2016.

In October CISP joined an eminent forest entomologist, Dr. David Wood of the Department of Natural Resources at the University of California, Berkeley.  We petitioned the California Department of Food and Agriculture to regulate movement of firewood within the state. CDFA refused, saying that the absence of control points through which firewood could be funneled made efforts to regulate its movements impractical. (For copies of our letter and CDFA’s reply, contact me through the “contact” button on the CISP website.)

While there are many questions about practical aspects of implementing and enforcing such regulations, I do not believe they are insurmountable.

I concede that CDFA has provided significant funds for firewood outreach campaigns. But people care about the threat posed by these pests and want CDFA to act. In the meantime, concerned people have formed formal partnerships linking local, county, state, and federal officials and academics to coordinate efforts to manage both GSOB and the PSHB and KSHB.  Groups’ efforts can be viewed here and here. CalFire and the California Fire Wood Task Force are active participants.

During a recent conference call sponsored by the California Agricultural Commissioners and Sealers Association’ Pest Prevention Committee, participants reinforced the damaging consequences of CDFA’s  inaction:

  • While scientists are developing new tools for detection of the polyphagous and Kuroshio beetles and the fungi, there are no funds to support their use in a more intensive detection trapping effort!!!!! Call participants discussed various potential funding sources (e.g., from competitive grant programs operated by various agencies).  Some survey efforts have been funded – by USDA APHIS:
    1. UC Riverside Professor Richard Stouthamer received Farm Bill §10007 funds for two years to develop traps and lures for PSHB.
    2. CDFA participates in a national woodborer survey which is funded by APHIS.
  • In the absence of CDFA designation of PSHB, KSHB, or GSOB as regulated pests, neither state nor county agencies have a firm foundation on which to base regulations to curtail movement of firewood, greenwaste, or other pathways by which these pests can be spread to new areas.

It is clear from the discussion during the call that many people understand the need for regulations to ban movement of firewood out of southern California. But so far they have not succeeded in building sufficient political support to bring this about.

 

Meanwhile, other federal agencies are beginning to perceive the risk posed by these pests – and are struggling to develop responses. The US Fish and Wildlife Service (USFWS) is trying to develop strategies to protect the forested wetlands, which are habitats for the endangered least Bell’s vireo (a bird) and other endangered species. However, the USFWS lacks funds to carry forward desired detection and other programs. The USFWS offices in California are trying to engage agency leadership on this threat. So far, Endangered Species Act §7 requirements have not restricted removal of infested trees in wetlands already invaded by PSHB or KSHB.

 

Santa Monica National Recreation Area is the first National Park Service unit to pay attention. I have written in the past that the National Park Service should adopt a nation-wide policy banning visitors from bringing their own firewood to campgrounds (see my blogs from August and October 2015). In the absence of a nation-wide policy, action by individual units is important.

 

The USDA Forest Service is already engaged, especially with detection and outreach. However, the USFS also does not have nation-wide policy restricting campers from taking their own firewood to campgrounds on National forests.

 

Many Californians are pushing for action … they need our help! If you live in California, contact your state legislators. If you live elsewhere, your forests are also at risk from the state’s failure to act.  So, if you know someone who lives there, ask that person to contact his/her legislators. Ask the legislators to demand state designation of PSHB, KSHB, and GSOB as quarantine pests and adoption of state firewood regulations.

 

SOURCE:

Memorandum from Greg McPherson, USDA Forest Service, to John Kabashima Re: Potential Impact of PSHB and FD on Urban Trees in Southern California, April 26, 2016

 

Posted by Faith Campbell

When will invasive species get the respect they deserve from conservationists?

i`iwi birdblogger i`iwi in Hawai`i

photo from www.TheBirdBlogger.com; used with permission

 

Evidence is growing that invasive species are among THE major threats to conservation goals worldwide.

In 2015 the IUCN called invasive species the second most significant threat to those World Heritage sites around the world that have outstanding natural values. (Poaching is the greatest threat.) My October 21, 2015 blog showed that the IUCN report actually underestimated the impact of invasive species. I listed briefly the principal invaders in several U.S. National parks. Earlier blogs criticized the National Park Service for failing to regulate the movement of firewood (August 2015) and described the invasive threat to Hawai`i (earlier in October 2015).

Now a second study shows invasive species are a principal driver of species extinction. The authors assessed the prevalence of alien species as a driver of extinctions among plants, amphibians, reptiles, birds, and mammals (which are the best-studied taxa) post-1500 AD. Overall, 58% of extinct or extinct-in-the-wild species had been driven to extinction at least in part by invasive species. Invasive alien species are the second most common threat overall. Indeed, invasive species are the most common threat for vertebrate extinctions (62% of extinct or extinct-in-the-wild species faced threats from invasive species). Invasive species ranked fourth as a cause of extinction for plants: 27% of listed plant species were threatened by invasive species.

For those species with just a single driver of extinction, invasive species is the cause for 47% of mammals, 27% of birds, 25% of reptiles, and 17% of plants. In no case were invasive species identified as the sole threat to an amphibian species – although invasive species are their second highest threat.

Although the paper lists invasive species as second, their threat was virtually identical to that of “overexploitation”, the threat ranked first. That is, 124 out of 215 species studied were threatened at least in part by invasive species; 125 were threatened by overexploitation.

Other principal threats were overexploitation, agriculture, aquaculture, and – in the case of plants – residential and commercial development. Categories related to habitat loss ranked surprisingly low. Only 61 of the 215 cases listed agriculture and aquaculture as threats.

The authors reflect on whether invasive species are not themselves causal agents of extinction, but rather symptoms of the real causes, especially habitat destruction. They conclude that that is unlikely.

Instead, they suggest that invasive species impacts might often be underestimated, as many interactions – especially those between alien parasites and native hosts – are very hard to detect.

Not surprisingly, 86% of island endemic species had invasive species as one extinction driver. Nevertheless, continental organisms are also threatened — 14% of alien-related extinctions have been of species with mainland populations. These include eight amphibians, five birds, and six mammals. Most of these invader-threatened mainland organisms are from the Americas

Among the approximately 30 alien taxa named as extinction drivers are rats, cats, and trout as threats to other vertebrates such as birds and mammals. All three were also ranked highly as damaging invasives in the earlier IUCN report on World Heritage sites. Diseases – especially chytridiomycosis and avian malaria – were causal agents of extinction for amphibians and birds. Several herbivores – especially goats, sheep, and European rabbits – and alien plants were drivers of extinction for plant species.

Of course, outright extinction is not the only damage to biological diversity caused by invasive species. American chestnut, Fraser fir, and redbay are not extinct, but their ecological role has been virtually eliminated as the vast majority of these forest trees die off. Other tree taxa are on same road – ash and eastern hemlocks across wide expanses of their ranges; tanoaks; whitebark pines …

Invasive species pose major threats to biological diversity and other conservation goals. These damages are on top of the acknowledged threat of invasive species to agriculture, forestry, or economic groups. (See, for example, Lovett et al. 2016 discussed in my previous blog.) The role of invasive species in extinction described in this new paper suggest a long-standing bias among conservationists’ priorities. Too often, we have focused on species threatened by overexploitation – which is such easier to see and involves an obvious “villain”.

Nevertheless, a host of practical suggestions have been put forward to address the root causes of species introductions and spread. Often, these ask some or many of us to stop doing what we have been doing. But much meaningful conservation action requires someone to accept limits or to make sacrifices.

Will the conservation community – including grant-making foundations, federal and state agencies, and the many conservation non-governmental organizations ranging from the IUCN to local groups – now take up the challenge of implementing suggested actions and actively advocating for the funding needed for practical steps that will begin to bring this threat under control?

 

Sources

Bellard C, Cassey P, Blackburn TM. 2016 Alien species as a driver of recent extinctions. Biol. Lett. 12: 20150623. http://dx.doi.org/10.1098/rsbl.2015.0623 http://rsbl.royalsocietypublishing.org /

 

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, 0(0), 2016, pp. 1–19. DOI 10.1890/15-1176.1

Available at www.caryinstitute.org/tree-smart-trade

 

Posted by Faith Campbell

Experts describe forest pests’ impact, call for action

 

Sixteen scientists and policy analysts (including me) have published a new study reviewing recent work on numbers, pathways and impacts of non-native, tree-killing insects and pathogens. I encourage you to read the article. It provides a concise and compelling overview of the threat to our wildland, rural, and urban forests from non-native insects and diseases and proposes some thought-provoking solutions.

SOD Parke diseased plant

rhododendron infected by sudden oak death; photo by Jennifer Parke, Oregon State University

Meanwhile, here are our conclusions:

Current policies for preventing introductions have reduced the numbers of pests introduced via the various pathways (e.g., wood packaging and horticultural plants – but not sufficiently to counter pests’ rising opportunities for introduction resulting from burgeoning global trade. [Emphasis mine.]

 

At the current efficacy of implementing the international regulations governing wood packaging [ISPM #15] ( Haack et al., 2014),  and given growing trade, Leung et al. 2014 project that by 2050 – just 35 years from now – up to three times as many wood-boring insects may be introduced to the U.S. as are currently here.

 

(I discussed this high risk in blogs posted at this site on July 15 and August 22, 2015.)

 

The new paper presents several options for improving prevention. These include: measures to ensure exporters ship “clean” plants and wood packaging; post-entry quarantines to raise the likelihood that pests will be detected; placing all genera of North American woody plants on USDA’s NAPPRA list of genera not currently approved for import and awaiting risk assessment; and improved surveillance and eradication programs. We also note the importance of improving data collection and allowing  researchers outside USDA access to those data to support independent evaluation of policy’s effectiveness.

 

As Aukema et al. demonstrated six years ago, non-native forest insects have accumulated in U.S. forests at a steady rate of about 2.5 per year over the last 150 yrs. While the rate of introduction has not changed, the types of insects introduced have. In the 20th Century, plant-associated insects dominated the introductions. In recent years wood-boring insects associated with wood packaging materials have dominated. Some of these wood-borers also are highly damaging! (See emerald ash borer, redbay ambrosia beetle/laurel wilt, and polyphagous shot hole borer/Fusarium here). Lack of information precludes a similar analysis for pathogens; although we all know that the 20 or so high-profile pathogens cause great devastation – see descriptions here.

 

The whole country is at risk; although the highest numbers of tree-killing insects and pathogens are established in the Northeast and Midwest, Pacific Coast states are catching up (and certainly already have their share of devastating insects and pathogens).  See the map below.  You can check the pests in your state by visiting the interactive map here .

map

map developed by USFS; published in Aukema et. al 2010.

Our new article notes that these non-native pests are the only disturbance agent that has effectively eliminated entire tree species or genera from U.S. forests in the span of decades. Follow-on effects include alterations of ecosystem functions and huge costs to various stakeholders, especially residents and governments of (sub)urban areas.

 

These impacts can persist for centuries as a result of altered species composition, which affects multiple trophic levels.

 

We followed Aukema et al. 2011’s results in estimating the direct annual economic impact of non-native forest insects to be at least:  $2 billion in municipal government expenditures, $1.5 billion in lost residential property values, and $1 billion in homeowner expenditures for tree removal and replacement or treatment. These costs and losses contrast with the paltry $216 million estimated in federal government expenditures.

 

Aukema et al. 2011 noted that these expenses cannot be summed across cost categories because of the potential for double-counting. We note that these figures are probably underestimates for several reasons. They did not include the introduced diseases such as sudden oak death. Nor do they  include pests detected recently, such as the polyphagous shot hole borer.  Finally, our paper excluded consideration of insects or pathogens native to some part of North America, such as the goldspotted oak borer. (For more information about these organisms, consult the write-ups here.)

 

As our article notes, the billions of dollars in annual economic damages (and un-quantified ecological impacts) are economic externalities. That is, the importers who benefit from the economic activity do not pay directly for preventing or responding to the associated pest introductions.

 

The article discusses several policy options that we believe would greatly reduce unacceptable risks. These options include several bold actions:

 

  • Require importers to switch from packaging made from wooden boards to packaging made from materials other than solid wood (fiberboards ok). This change is both highly protective and potentially cost-effective. Such a switch would have to be justified under the terms of international trade agreements – but given the high levels of damage caused by wood-boring pests, I don’t think that hurdle is insurmountable.
  • Greatly strengthen measures aimed at preventing pest introduction on imports of plants. One step would be restricting imports of all genera of “woody” plants native to North America by designating them as “not authorized for importation pending pest risk assessment” (NAPPRA). Another protective step would be to promptly finalize the Q-37 revision proposed by USDA in April 2013 and immediately initiate negotiations with principal foreign suppliers of temperate climate woody vegetation to implement the pest-minimization procedures contained in that revised regulation, as well as in ISPM#36.

 

Other options discussed are straight-forward and simpler:

 

  • Tighten enforcement of existing regulations by ending the practice of allowing an importer to be detected five times in a year with wood packaging that does not comply with regulatory requirements before imposing a penalty. When a new year starts, that importer gets a “clean slate”! Is this how agencies enforce regulations that they are serious about?
  • Expand efforts to assist trade partners in adopting clean trade measures.
  • Expand and integrate surveillance programs for new pest outbreaks, and providing timely and adequate funding for emergency eradication efforts.

 

SOURCES

 

Aukema, J.E., B. Leung, K. Kovacs, C. Chivers, K. O. Britton, J. Englin, S.J. Frankel, R. G. Haight, T. P. Holmes, A. Liebhold, D.G. McCullough, B. Von Holle.. 2011. Economic Impacts of Non-Native Forest Insects in the Continental United States PLoS One September 2011 (Volume 6 Issue 9)

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

 

Haack, R. A., K. O. Britton, E. G. Brockerhoff, J. F. Cavey, L. J. Garrett, M. Kimberley, F. Lowenstein, A. Nuding, L. J. Olson, J. Turner, and K. N. Vasilaky. 2014. Effectiveness of the international phytosanitary standard ISPM no. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. Plos One 9:e96611.

 

Leung, B., M. R. Springborn, J. A. Turner, and E. G. Brockerhoff. 2014. Pathway-level risk analysis: the net present value of an invasive species policy in the US. Frontiers in Ecology and the Environment 12:273-279.

 

 

Posted by Faith Campbell

Senate Hearing on Invasive Species Policy on Federal Lands

The Public Lands Subcommittee of the Senate Committee on Energy and Natural Resources held an oversight hearing on invasive species management on federal lands on April 28, 2016. This hearing is the result of lobbying effort by the Healthy Habitats Coalition, which drafted the initial bill and has worked for its passage for several years.  One specific aim was to gather comments on S. 2240.

yellow start thistle 1316001 Peggy Greb ARSyellow start thistle photo by Peggy Greb, USDA ARS  Bugwood # 1316001

The bill would, inter alia, require land-managing agencies to allocate their invasive species funds according to the following formula: 75% for on-the-ground activity; 15% for combined research and outreach; 10% or less for administrative costs. Priorities for federal agencies’ invasive species efforts would be set by state governors. The bill would also exempt some invasive species control programs from analysis under the National Environmental Policy Act (NEPA).

In December 2015 I posted a blog about an earlier hearing on the bill (H.R. 1485) held by the House Oversight Committee.

WHO WAS THERE?

Witnesses represented the USDA Forest Service, USDI Bureau of Land Management, the Wyoming Department of Agriculture, Healthy Habitats Coalition, and I, representing the Center for Invasive Species Prevention and Natural Areas Association. The witnesses’ written testimony and hearing video are archived here

Senators at the hearing were Chairman Barasso (WY), Franken (MN), and Hirono (HI).  Senators Risch (ID), Hoeven (ND), and Gardner (CO) attended briefly.  About 13 Congressional staffers were there, along with an audience of 15-20 and two from the press.

In their introductions, all senators spoke about the economic damage caused by invasive species Chairman Barasso said his bill – S. 2240 — is intended to fix western complaints about the ineffectiveness of federal agencies’ efforts.  Senators Franken and Hirono agreed on the need for new tools and strategies and better coordination among actors. However, they expressed concern about some components of the bill.

At the end of the day …

The Healthy Habitats Coalition and the Wyoming Department of Agriculture support the bill. The USFS  supported the bill’s goals and emphasis on collaboration but had some concerns. BLM praised changes made from earlier versions of the bill, hopes additional clarifications will be made, and explicitly opposed the categorical exclusion from NEPA. CISP and NAA (I) opposed the bill and suggested that the Senators take other actions to strengthen federal invasive species programs.

Will the bill move forward? I think action is unlikely … It is a shame that Congress has so little concern about invasive species.  If there were a forward impetus, we could work with the Senators and Representatives to develop an approach that I think would be more productive.

Witness Statements

The administration witnesses took the usual approach, speaking about their agencies’ efforts and successes. Glenn Casamassa, USFS, noted the Service’s “leadership role” and spoke about programs across the agency. He estimated that the USFS treats ~400,000 acres per year for invasive species; the agency has restored about 2 million acres, with great success.

I question how these claims of success fit with the findings of USFS researcher Dean Pearson in Montana? I blogged about his studies in January. Pearson found that both invasion by alien forbs such as spotted knapweed and weed control efforts using either herbicides or grazing can lead to suppression of the native forbs. Furthermore, suppressing invasion by one set of plants – whatever the strategy used – often facilitates a secondary invasion by some other plant species that might cause greater changes to the system or that are harder to control. Such secondary invasions are likely any time a “strong” invaders relatively insensitive to the control method used is present.  Often this secondary invader is cheatgrass.

Mike Pool, BLM, noted that invasive plants occupy ~79 million acres of lands it manages and described particular successes in CO and NM. Key is a comprehensive and coordinated response.

Doug Miyamoto, Wyoming Department of Agriculture, said S. 2240 would rely on local leadership; ensure consistent commitment by federal partners; specify a goal of reducing invasive species’ acreage by  5% annually; and halt delays caused by NEPA compliance. As an example, he cited a four-year delay in managing a USFS site following fire, which resulted in doubling of cheatgrass extent.

George Beck, a weed scientist at Colorado State University, representing the Healthy Habitats Coalition, took Federal agencies to task for inconsistent budgets; lack of cooperation; lack of coordination with states; and using NEPA as an excuse for delays. Not expecting leadership from the federal government, he called on Congress to enact binding requirements through S. 2240.

Faith Campbell, representing CISP and the Natural Areas Association. I agreed that Federal leadership has fallen short and that the Nation needs a comprehensive invasive species program. I raised concerns about provisions of S. 2240:

  • Funding allocations would undercut essential research, outreach, and other activities aimed at development and implementation of effective tools;
  • These restrictions are exacerbated when combined with the unrealistic goal of bringing about 5% per year net reduction in invasive species populations;
  • New reporting and coordination requirements that might further delay needed actions;
  • Priorities in managing invasive species on national lands should reflect the national perspective, not be set by states’ governors.
  • The NEPA Categorical Exclusion could expose the environment to additional damage.

I called on the Senators to take several practical steps:

  1. Amend the Lacey Act to enable the Fish and Wildlife Service to
  • apply scientific risk assessment tools in evaluating species proposed for importation;
  • act quickly when confronted by an emergency.

Plus clarify FWS’ authority to regulate

  • all animal taxa (in coordination with USDA);
  • the threat to wildlife from disease; and
  • interstate movement of species already listed under the Lacey Act as “injurious”.
  1. Provide higher appropriations for key agencies: APHIS, FWS, EPA, Corps of Engineers, and the land and water-managing agencies.
  2. Conduct oversight hearings at which Senators ask Secretaries (of USDA & USDI) and their Assistant/Under secretaries about their efforts to address invasive species, specifically:
    • Has the USFS implemented its 2011 internal directive amending the Forest Service Manual? (The directive calls for integrating invasive species activities across programs on National forests and grasslands.)
    • Why has neither the USFS nor NPS adopted a nation-wide policy to limit campground visitors from bringing their own firewood?
    • Has/when will the Council on Environmental Quality collaborate with the National Invasive Species Council re to develop guidance on applying the National Environmental Policy Act (NEPA) to invasive species management?
  3. Ensure that when the Senate confirms nomimees to be new secretaries or assistant/under secretaries of USDI and USDA in 2017, those nominees are asked about their goals with regard to invasive species prevention and management.

Questions from the Senators

Much of the discussion centered around the bill’s language excluding invasive species control programs from NEPA. Chairman Barrasso, Miyamoto of Wyoming, and Beck all said NEPA compliance had caused damaging delays and described the Categorical Exclusion language in the bill as “limited”.

Pool said BLM has successfully used programmatic environmental impact statements to evaluate options over large areas ahead of time in order to act quickly in a crisis. Pool said that BLM distinguishes between catastrophic wildfire – when no NEPA analysis is required; When deciding how to respond to long-lived problems that affect hundreds of thousands of acres, BLM  wants to inform and engage the public – and NEPA  is a good process to do that.

Casamassa said USFS emergency responses on significant burned areas are not subject to NEPA; instead its actions are guided by Forest Plans.  He supported rulemaking to clarify the bill’s categorical exclusions for invasive species.

I opposed a NEPA Categorical Exclusion because all actions – even those based on good intentions – have downsides that need to be evaluated. (See discussion of Pearson’s research from my blog in December.) APHIS has used programmatic EIS to help agency move quickly. I expressed frustration that CEQ has stonewalled NISC on developing guidance.

(Whether the NEPA exemption is “limited” is open to discussion!  It would apply to projects on federal lands that are or will be “located in a prioritized, high-risk area” and treat invasive species within 1,000 feet of, inter alia, a water body or waterway; a railroad line or roadside; a water project; a utility or telephone infrastructure or right-of-way; a campground; a National Heritage Area or National Monument; a park or other recreational site; a school; or “any other similar, valuable infrastructure”.)

In response to Chariman Barasso’s question about the Early Detection/Rapid Response plan recently released by the National Invasive Species Council, Beck said that in his view states should take the lead in slowing the spread of species within the country.  He criticized federal agencies’ failure to halt new introductions.

Senator Franken expressed dismay that only one of the five witnesses’ written statements mentioned climate change as a factor re: invasive species. In response, the USFS and BLM stressed their efforts to adapt.

Senator Hirono asked whether the prescribed funding allocations in S. 2240 (75% for “on the ground” work; 15% for research and outreach combined; 10% for administration, including strategy and oversight) would hamper needed actions?  She cited the need for research to develop tools to manage the sudden `ohi`a death fungus [described as “ohia wilt” here.]  Casamassa of the USFS said the agency’s spending on invasive species is already close to the S. 2240 funding allocation.  Nevertheless, the agency would sometimes need greater flexibility. On the other hand, Beck said research on invasive species should be left to other agencies, such as the U.S. Geological Survey and Agriculture Research Service.

Senator Hirono expressed concern that the bill’s requirement that agencies use the “least costly” method would expand use of pesticides – an approach that concerns Hawaiians.

Senator Hirono asked Campbell whether the 5% reduction goal is do-able? Especially re: insects and pathogens? I replied that all agencies are dealing with hundreds of invasive species at a time. Many of the insects and pathogens – as well as the aquatics – can’t even be detected, much less the extent of invasion. Managers lack tools to reduce their extent.  I also worried that the 5% goal will put pressure on agencies to tackle easily measured invasive species e.g., plants, and ignore others.

Chairman Barrasso concluded the hearing by telling me that he thinks our views are not mutually exclusive. He sees the need for both prevention and control of widespread species.

 

Posted by Faith Campbell & Phyllis Windle

 

European study buttresses case for revolutionary changes to phytosanitary system

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rhododendron in Europe sickened by P. ramorum; photo from EPPO website

 

A recently published study by European researchers [Jung, T. et al. 2015] documents the failure of current European and global phytosanitary programs and calls for “a new holistic and integrated systems approach”.  The authors specifically criticize Article VI.2 of the International Plant Protection Convention  because it requires that a plant pest be identified and its risks assessed before a country may adopt a phytosanitary measures.  The authors call this requirement “paradoxical” given the large number of potentially damaging plant pests that remain unknown to science.

 

The study focuses on the genus Phytophthora, which contains about 150 identified species and perhaps 500 species not yet identified by scientists.  The identified species include plant pathogens which are responsible for more than 66% of all fine root diseases & more than 90% of all collar rots of woody plant species.  Examples include the pathogens responsible for the Irish potato famine, sudden oak death, Port-Orford-cedar root disease, the die-off of many endemic plant species in Western Australia and damage to many other species in Europe and North America, and mortality and decline of oaks and alders across Europe.

 

The authors note that

  • Most of the ~150 currently known species and designated taxa of Phytophthora were unknown to science before they turned up in new environments on other continents as invasive aggressive pathogens of native plants.
  • Forty-four of the 64 Phytophthora taxa detected in the present study were unknown to science before 1990.
  • None of the 59 putatively exotic Phytophthora taxa detected in the present study had been intercepted at European ports of entry. (Some of these introductions are known to be recent; see UK reports on the 4th P. ramorum lineage ) and P. lawsonii detections in the U.K., France and the Netherlands in 2010.)
  • In many cases, had a Phytophthora been detected, the detection would not have resulted in rejection of the shipment because only 5 Phytophthora species are regulated under European regulations.
  • Spread of the quarantine organism ramorum was not halted despite the presence of strict quarantine regulations.

 

I have written several times about the threat to U.S. trees and forests from insects and – especially – pathogens introduced via the trade in live plants; see Fading Forests II and III .  Fading Forests II discusses the threat from unknown pests and the roadblocks to managing that threat raised by the World Trade Organization’s Agreement on the Application of Sanitary and Phytosanitary Measures and the implementing procedures adopted by the International Plant Protection Convention.  Fading Forests III discusses USDA APHIS efforts to adopt more effective regulatory approaches through adoption of both international and regional standards (ISPM#36 and RSPM#24) and revision of its own Q-37 regulations.

Jung and his 65 (!) coauthors present some frightening facts about the situation in European nurseries and forest, landscape, and ornamental plantings:

  • They found a total of 68 Phytophthora taxa (species, informally designated taxa, and previously unknown taxa). 49 taxa were found in nurseries, 56 in forest and landscape plantings.
  • 91% of the 732 nurseries analyzed had at least 1 Phytophthora taxon present; in the 101 infested nurseries in which more than 5 stands were tested, an average of 3.6 Phytophthora taxa per nursery were detected
  • 66% of forest & landscape plantings had at least 1 Phytophthora taxon present
  • The majority of infested plants in nurseries did not display symptoms; the sampling methods for plantings relied to a large extent on symptoms, so the presence of symptomless plants could not be evaluated.
  • Hundreds of previously unknown Phytophthora–host associations were observed.
  • One or more of 19 Phytophthora which can attack native European or widely-planted trees and shubs were isolated from 84% of ornamental planted stands. Two such pathogens were detected in 11.8% of those stands.
  • In a single British ornamental and amenity planting, 15 different Phytophthora taxa were isolated from 33 different species and varieties of plants. Smaller numbers were isolated from smaller numbers of sampled plants in other countries.
  • The infestation rate for various types of plantings ranged from 94% for riparian plantings through 83.1% for horticultural plantings to 79.3% for forest plantings. About half of amenity and ornamental plantings had one or more infestations.
  • 64% of oak plantings were infested by at least one Phytophthora species associated with decline of mature oak stands. Eight of the 9 plantings of Laurus nobilis in Spain and the UK hosted Phytophthora. Rates varied for other types of trees.
  • In total, 755 ornamental plantings of 281 broadleaved woody and herbaceous species were sampled in 8 countries. 45% had at least one of the 21 Phytophthora taxa known to damage a wide range of European and widely planted exotic tree and shrub species. About 10% of the tested stands had more than one.

 

As the authors state, their results clearly demonstrate that the vast preponderance of nursery stands across Europe are infested by a large array of Phytophthora species.  Nurseries and other plantings relied on as sources of plants for afforestation and other outplantings are routinely infected by the most aggressive Phytophthora pathogens that attack the respective tree or crop species. The result is continuous high-frequency spread of these aggressive pathogens to planted forests and horticultural systems — and will inevitably result in their introduction to the wider environment.

 

They estimate that 4.8 million ha of the 6 million ha of new forests planted in Europe over the past 20 years are potentially infested by Phytophthora pathogens.  Another 17.6 million ha of forests replanted after harvesting or fire were possibly established with Phytophthora-infested nursery stock.

 

Why has this happened? The authors note that under current nursery growing practices, individual plants often flow largely unregulated through several nurseries both within and between countries before being sold to a consumer. In addition, such common nursery practices as reusing containers, irrigating with unfiltered surface water or recirculated water, poor drainage and failure to remove dead plants and debris all contribute to establishment and spread of Phythothora.  These same criticisms have been made by U.S. scientists – and incorporated into APHIS’ revised regulations for management of sudden oak death and the nursery-regulatory SANC program now being tested.

 

Is the situation equally bad in North America?  Jung et al. cite several publications that cumulatively demonstrate high infestation rates of U.S. ornamental nurseries with at least 31 Phytophthora species.  They say that the situation in forest nurseries is largely unknown.

Certainly both continents are at high risk of additional introductions.  U.S. plant imports reached 3.2 billion in 2007 (Liebhold et al. 2012). I am unaware of a more recent calculation … In 2010, ten European countries cumulatively imported 4.3 billion living plants from overseas; almost all were imported first to the Netherlands.  The principal source was Africa (3.6 billion). Asia shipped 456 million plants; North America 181 million; South America 81 million; Oceania only 2.4 million plants. Between 2007 and 2010, the volume of imported woody plants increased by 44%, and in 2010, the proportion of woody plants reached 20.8% of all imported plants.  Only 3% of the imported consignments are subject to phytosanitary inspections.

 

As Jung et al. note, their study joins an ever-longer list of analyses that have concluded that current international plant health protocols based on random visual inspections for symptoms of listed quarantine organisms have failed and must be changed fundamentally.  (See, for example, the writing of Clive Brasier  and the Montesclaros Declaration.

 

Jung et al. call for adoption of a pathway regulation approach based on pathway risk analyses, and risk-based inspection regimes performed by an adequate number of skilled staff using molecular high-throughput detection tools. Nurseries wishing to ship plants internationally would have to comply with mandatory best practices. The requirements must be supported by rigorous enforcement and bold outreach campaigns. This approach would minimize the risks of further introductions and dissemination of both known and, even more importantly, unknown potential pathogens.

 

MY CONCLUSION

 

Revising the international phytosanitary regime will be difficult, requiring 170 countries to agree to amend both the World Trade Organization’s SPS Agreement and the International Plant Protection Convention. The difficulties will be not only political. Allowing countries to regulate unknown organisms that are potential pests will open a door to protectionist restrictions.  The countries that wrote these agreements have long sought to block protectionist restrictions by requiring that phytosanitary measures be based on scientific analyses of specific risks.

 

However, as Jung et al. – and before them many others, especially Clive Brasier  – have demonstrated, the current requirement that each pathogen be identified and its risk analyzed before  regulations are adopted is counter to the scientific fact that most pathogens and arthropods are not known to science.  The knowledge gap is many times greater when the question is how those microorganisms and arthropods will interact with millions of plant species if introduced to novel habitats.

 

Meanwhile, USDA APHIS has begun trying to close some of the regulatory gaps.  In 2011 APHIS adopted regulations creating a temporary holding category, called “Not Authorized (for importation) Pending Pest Risk Analysis,” or NAPPRA. Now, APHIS has authority to temporarily prohibit import of certain types of plants, from specific countries of origin, that it considers to pose a particular pest risk. The temporary ban gives APHIS time to complete a pest risk analysis and then enact appropriate safeguards to ensure that imported plants will be as pest-free as possible.  However, APHIS has been unable to utilize this new power.  The agency proposed a second round of “NAPPRA” species in May 2013, but nearly 3 years later it has not finalized that action. Even if fully implemented, NAPPRA does not address the problem of unknown pests and pathogens.

 

APHIS has also proposed a major revision of its plant import regulations (called “Q-37”).  This change would implement the IPPC standard on living plants (ISPM#36) and authorize APHIS to require foreign suppliers of plants to apply hazard identification and mitigation practices to ensure plants are pest-free. APHIS proposed this rule change 3 years ago, in 2013.  Again, the change has not yet been finalized.

 

What You Can Do

Write to your member of Congress and Senators and ask them to urge the Secretary of Agriculture to finalize the two pending regulations – to add the second round of species to the NAPPRA list and to update the Q-37 regulations.

 

SOURCES

Jung, T. et al. 2015 “Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease” Forest Pathology. November 2015; available from Resource Gate

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

 

 

Posted by Faith Campbell