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Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation

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A special issue of Forests (ISSN 1999-4907). This special issue belongs to the section "Forest Ecophysiology and Biology".

Deadline for manuscript submissions: closed (20 December 2020) | Viewed by 31004

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Dr. Sarah Green

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Centre for Ecology, Society and Biosecurity, Forest Research, Northern Research Station, Roslin, Midlothian EH25 9SY, UK
Interests: forest pathology; molecular detection of forest pathogens

Special Issue Information

Dear Colleagues,

Forests and natural ecosystems worldwide are under increasing threat from new diseases spread internationally through trade and other human-mediated pathways. A gathering body of evidence suggests that various human interventions are assisting the transfer of pathogens from sites of early introduction and establishment to trees in plantation forests and natural landscapes. These include, for example, commercial forestry and farming activities, conservation planting of native species into vulnerable natural habitats, and recreational activities. The purpose of this Special Issue is to bring together this evidence by collating global examples that document human-mediated spread of soilborne forest pathogens into wider environments, unravel the social and commercial challenges to curtailing risky practices, and explore methods for mitigation through improved biosecurity, diagnostics, social awareness, and policy. We encourage contributions to this Special Issue from all relevant fields, including experimental studies, reports on surveillance and diagnostics methodologies, and social and economic appraisals, in order to promote understanding of the risk of spread of soilborne pathogens into forests and methods for mitigation of that risk.

Dr. Sarah Green
Guest Editor

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Keywords

soilborne pathogens
human interventions
forest and conservation management
diagnostics and surveillance
biosecurity
social and economic challenges

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Published Papers (9 papers)

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Research

19 pages, 913 KiB

Open AccessArticle

Perceptions of Biosecurity-Based Accreditation in the Plant Trade: A UK Example

by Mariella Marzano, Michael Dunn and Sarah Green

Forests 2021, 12(12), 1741; https://doi.org/10.3390/f12121741 - 10 Dec 2021

Cited by 5 | Viewed by 2354

Abstract

It is widely acknowledged that a major threat to tree health biosecurity comes from trade, particularly through the importation of containerised live plants and associated growing media. Nurseries can collectively play a key role in mitigating pests and diseases through attention to their daily practices (e.g., procuring plants, storage and management). More widespread adoption of best practices in the sector could be promoted through the introduction of a UK-wide accreditation scheme. However, the success of such a scheme would depend not only on its uptake by nurseries but also on the attitudes of key consumers in the plant supply chain. To date, the perspectives of the nursery sector on the feasibility of plant biosecurity, as well as the sensitivity of these sectors to consumer opinion, have remained under-researched. Using the COM-B [Capability, Opportunity, Motivation—Behaviour] model as a framework, we draw on qualitative results to assess the appetite for a hypothetical accreditation scheme amongst UK nurseries and the capability, opportunities and motivations to enhance their biosecurity practices. Nineteen semi-structured interviews were conducted with plant nurseries and 22 with their consumers. Overall a plant health accreditation scheme should have actions that are: (1) viable within the confines of the site and supply chain; (2) affordable where the benefits of changes/improvements outweigh the costs; (3) beneficial in that they promote biosecurity; (4) attractive to consumers looking to purchase products from accredited nurseries; (5) fair and inclusive where everyone has responsibility for biosecurity; (6) transparent with the scheme involving a strong monitoring and auditing component. This study provides important insights that will feed into the development of plant biosecurity-focussed accreditation or certification. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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17 pages, 2729 KiB

Open AccessArticle

Cross-Cultural Leadership Enables Collaborative Approaches to Management of Kauri Dieback in Aotearoa New Zealand

by Lee Hill, Edward Ashby, Nick Waipara, Robin Taua-Gordon, Aleesha Gordon, Fredrik Hjelm, Stanley E. Bellgard, Emma Bodley and Linley K. Jesson

Forests 2021, 12(12), 1671; https://doi.org/10.3390/f12121671 - 30 Nov 2021

Cited by 14 | Viewed by 3719

Abstract

In Aotearoa/New Zealand, the soilborne pathogen Phytophthora agathidicida threatens the survival of the iconic kauri, and the ecosystem it supports. In 2011, a surveillance project to identify areas of kauri dieback caused by Phytophthora agathidicida within the Waitākere Ranges Regional Park (WRRP) highlighted the potential impact of the pathogen. A repeat of the surveillance in 2015/16 identified that approximately a quarter of the kauri area within the Regional Park was infected or possibly infected, an increase from previous surveys. The surveillance program mapped 344 distinct kauri areas and showed that 33.4% of the total kauri areas were affected or potentially affected by kauri dieback and over half (58.3%) of the substantial kauri areas (above 5 ha in size) were showing symptoms of kauri dieback. Proximity analysis showed 71% of kauri dieback zones to be within 50 m of the track network. Spatial analysis showed significantly higher proportions of disease presence along the track network compared to randomly generated theoretical track networks. Results suggest that human interaction is assisting the transfer of Phytophthora agathidicida within the area. The surveillance helped trigger the declaration of a cultural ban (rāhui) on recreational access. Te Kawerau ā Maki, the iwi of the area, placed a rāhui over the kauri forest eco-system of the Waitākere Forest (Te Wao Nui o Tiriwa) in December 2017. The purpose of the rāhui was to help prevent the anthropogenic spread of kauri dieback, to provide time for investment to be made into a degraded forest infrastructure and for research to be undertaken, and to help protect and support forest health (a concept encapsulated by the term mauri). Managing the spread and impact of the pathogen remains an urgent priority for this foundation species in the face of increasing pressures for recreational access. Complimentary quantitative and qualitative research programs into track utilization and ecologically sensitive design, collection of whakapapa seed from healthy and dying trees, and remedial phosphite treatments are part of the cross-cultural and community-enabled biosecurity initiatives to Kia Toitu He Kauri “Keep Kauri Standing”. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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22 pages, 6340 KiB

Open AccessArticle

PHYTO-THREATS: Addressing Threats to UK Forests and Woodlands from Phytophthora; Identifying Risks of Spread in Trade and Methods for Mitigation

by Sarah Green, David E. L. Cooke, Mike Dunn, Louise Barwell, Bethan Purse, Daniel S. Chapman, Gregory Valatin, Alexandra Schlenzig, Jane Barbrook, Tim Pettitt, Colin Price, Ana Pérez-Sierra, Debra Frederickson-Matika, Leighton Pritchard, Peter Thorpe, Peter J. A. Cock, Eva Randall, Beatrix Keillor and Mariella Marzano

Forests 2021, 12(12), 1617; https://doi.org/10.3390/f12121617 - 23 Nov 2021

Cited by 21 | Viewed by 4198

Abstract

The multidisciplinary ‘Phyto-threats’ project was initiated in 2016 to address the increasing risks to UK forest and woodland ecosystems from trade-disseminated Phytophthora. A major component of this project was to examine the risk of Phytophthora spread through nursery and trade practices. Close to 4000 water and root samples were collected from plant nurseries located across the UK over a three-year period. Approximately half of the samples tested positive for Phytophthora DNA using a metabarcoding approach with 63 Phytophthora species identified across nurseries, including quarantine-regulated pathogens and species not previously reported in the UK. Phytophthora diversity within nurseries was linked to high-risk management practices such as use of open rather than closed water sources. Analyses of global Phytophthora risks identified biological traits and trade pathways that explained global spread and host range, and which may be of value for horizon-scanning. Phytophthoras having a higher oospore wall index and faster growth rates had wider host ranges, whereas cold-tolerant species had broader geographic and latitudinal ranges. Annual workshops revealed how stakeholder and sector ‘appetite’ for nursery accreditation increased over three years, although an exploratory cost-benefit analysis indicated that the predicted benefits of introducing best practice expected by nurseries outweigh their costs only when a wider range of pests and diseases (for example, Xylella) is considered. However, scenario analyses demonstrated the significant potential carbon costs to society from the introduction and spread of a new tree-infecting Phytophthora: Thus, the overall net benefit to society from nurseries adopting best practice could be substantial. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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21 pages, 2212 KiB

Open AccessEditor’s ChoiceArticle

Investigating the Role of Restoration Plantings in Introducing Disease—A Case Study Using Phytophthora

by Flora Donald, Bethan V. Purse and Sarah Green

Forests 2021, 12(6), 764; https://doi.org/10.3390/f12060764 - 10 Jun 2021

Cited by 4 | Viewed by 3519

Abstract

Translocating plants to natural habitats is a long-standing conservation practice but is growing in magnitude to deliver international targets to mitigate climate change and reverse biodiversity loss. Concurrently, outbreaks of novel plant pests and pathogens are multiplying with increased global trade network connectivity and larger volumes of imported plants, raising concerns that restoration plantings may act as introductory disease pathways. We used UK common juniper, subject since ~1995 to conservation plantings and now experiencing significant mortality from the non-native pathogen Phytophthora austrocedri Gresl. & E. M. Hansen, as an example species to explore the availability of monitoring data that could be used to assess disease risks posed by planting. We compiled spatial records of juniper planting including qualitative data on sources of planting material, propagation settings and organization types that managed planting projects. We found that juniper planting activity expanded every decade since 1990 across the UK and while not all planting resulted in outbreaks, 19% of P. austrocedri detections were found within 2 km of a known planting. We highlight the scale and diversity of organizations raising and planting juniper, as well as the lack of source material traceability, and suggest that cross-sector collaboration and changes in practice are required to reduce the risks of pathogen introduction posed by restoration planting. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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26 pages, 2187 KiB

Open AccessEditor’s ChoiceArticle

Diversity of Phytophthora Species Detected in Disturbed and Undisturbed British Soils Using High-Throughput Sequencing Targeting ITS rRNA and COI mtDNA Regions

by Blanca B. Landa, Luis F. Arias-Giraldo, Béatrice Henricot, Miguel Montes-Borrego, Lucas A. Shuttleworth and Ana Pérez-Sierra

Forests 2021, 12(2), 229; https://doi.org/10.3390/f12020229 - 17 Feb 2021

Cited by 17 | Viewed by 3664

Abstract

Disease outbreaks caused by introduced Phytophthora species have been increasing in British forests and woodlands in recent years. A better knowledge of the Phytophthora communities already present in the UK is of great importance when developing management and mitigation strategies for these diseases. To do this, soils were sampled in “disturbed” sites, meaning sites frequently visited by the public, with recent and new plantings or soil disturbances versus more “natural” forest and woodland sites with little disturbance or management. Phytophthora diversity was assessed using high-throughput Illumina sequencing targeting the widely accepted barcoding Internal Transcribed Spacer 1 (ITS1) region of rRNA and comparing it with the mitochondrial cytochrome c oxidase I (COI) gene. Isolation of Phytophthora was run in parallel. Nothophytophthora spp. and Phytophthora spp. were detected in 79 and 41 of the 132 locations of the 14 studied sites when using ITS or COI, respectively. A total of 20 Phytophthora amplicon sequence variants (ASVs) were assigned to known Phytophthora species from eight clades (1a, 2, 2b, 3a, 5, 6b, 7a, 8b, 8c, 8d, 10a, and 10b) and 12 ASVs from six clades (1a, 2c, 3a, 3b, 6b, 7a, 8b, 8c, and 8d) when using ITS or COI, respectively. Only at two locations were the results in agreement for ITS, COI, and isolation. Additionally, 21 and 17 unknown Phytophthora phylotypes were detected using the ITS and COI, respectively. Several Phytophthora spp. within clades 7 and 8, including very important forest pathogens such as P. austrocedri and P. ramorum, were identified and found more frequently at “disturbed” sites. Additionally, eight ASVs identified as Nothophytophthora spp. were detected representing the first report of species within this new genus in Britain. Only three species not known to be present in Britain (P. castaneae, P. capsici, and P. fallax) were detected with the ITS primers and not with COI. To confirm the presence of these or any potential new Phytophthora species, sites should be re-sampled for confirmation. Additionally, there is a need to confirm if these species are a threat to British trees and try to establish any eradication measures required to mitigate Phytophthora spread in Britain. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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21 pages, 6515 KiB

Open AccessArticle

Phytophthora Introductions in Restoration Areas: Responding to Protect California Native Flora from Human-Assisted Pathogen Spread

by Susan J. Frankel, Christa Conforti, Janell Hillman, Mia Ingolia, Alisa Shor, Diana Benner, Janice M. Alexander, Elizabeth Bernhardt and Tedmund J. Swiecki

Forests 2020, 11(12), 1291; https://doi.org/10.3390/f11121291 - 30 Nov 2020

Cited by 21 | Viewed by 3559

Abstract

Over the past several years, plantings of California native plant nursery stock in restoration areas have become recognized as a pathway for invasive species introductions, in particular Phytophthora pathogens, including first in the U.S. detections (Phytophthora tentaculata, Phytophthora quercina), new taxa, new hybrid species, and dozens of other soilborne species. Restoration plantings may be conducted in high-value and limited habitats to sustain or re-establish rare plant populations. Once established, Phytophthora pathogens infest the site and are very difficult to eradicate or manage—they degrade the natural resources the plantings were intended to enhance. To respond to unintended Phytophthora introductions, vegetation ecologists took a variety of measures to prevent pathogen introduction and spread, including treating infested areas by solarization, suspending plantings, switching to direct seeding, applying stringent phytosanitation requirements on contracted nursery stock, and building their own nursery for clean plant production. These individual or collective actions, loosely coordinated by the Phytophthoras in Native Habitats Work Group ensued as demands intensified for protection from the inadvertent purchase of infected plants from commercial native plant nurseries. Regulation and management of the dozens of Phytophthora species and scores of plant hosts present a challenge to the state, county, and federal agriculture officials and to the ornamental and restoration nursery industries. To rebuild confidence in the health of restoration nursery stock and prevent further Phytophthora introductions, a voluntary, statewide accreditation pilot project is underway which, upon completion of validation, is planned for statewide implementation. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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24 pages, 3442 KiB

Open AccessArticle

Phytophthora austrocedri in Argentina and Co-Inhabiting Phytophthoras: Roles of Anthropogenic and Abiotic Factors in Species Distribution and Diversity

by María Laura Vélez, Ludmila La Manna, Manuela Tarabini, Federico Gomez, Matt Elliott, Pete E. Hedley, Peter Cock and Alina Greslebin

Forests 2020, 11(11), 1223; https://doi.org/10.3390/f11111223 - 20 Nov 2020

Cited by 12 | Viewed by 4408

Abstract

This work reports the first survey of Phytophthora diversity in the forests soils of Andean Patagonia. It also discusses the role of anthropogenic impact on Phytophthora distribution inferred from the findings on Phytophthora diversity and on the distribution of Phytophthora austrocedri-diseased forests. Invasive pathogen species threatening ecosystems and human activities contribute to their entry and spread. Information on pathogens already established, and early detection of potential invasive ones, are crucial to disease management and prevention. Phytophthora austrocedri causes the most damaging forest disease in Patagonia, affecting the endemic species Austrocedrus chilensis (D. Don) Pic. Sern. and Bizzarri. However, the relationship between anthropogenic impacts and the disease distribution has not been analyzed enough. The aims of this work were: to evaluate Phytophthora diversity in soils of Andean Patagonia using a metabarcoding method, and analyze this information in relation to soil type and land use; to assess the distribution of Austrocedrus disease over time in relation to anthropogenic and abiotic gradients in an area of interest; and to discuss the role of human activities in Phytophthora spread. High throughput Illumina sequencing was used to detect Phytophthora DNA in soil samples. The distribution of Austrocedrus disease over time was assessed by satellite imagery interpretation. Twenty-three Phytophthora species, 12 of which were new records for Argentina, were detected. The most abundant species was P. austrocedri, followed by P. × cambivora, P. ramorum and P. kernoviae. The most frequent was P. × cambivora, followed by P. austrocedri and P. ramorum. Phytophthora richness and abundance, and Austrocedrus disease distribution, were influenced by land use, anthropogenic impact and soil drainage. Results showed several Phytophthoras, including well-known pathogenic species. The threat they could present to Patagonian ecosystems and their relations to human activities are discussed. This study evidenced the need of management measures to control the spread of P. austrocedri and other invasive Phytophthora species in Patagonia. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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17 pages, 3188 KiB

Open AccessArticle

Anthropogenic Factors Control the Distribution of a Southern Conifer Phytophthora Disease in a Peri-Urban Area of Northern Patagonia, Argentina

by Guillermo Giordana, Thomas Kitzberger and Ludmila La Manna

Forests 2020, 11(11), 1183; https://doi.org/10.3390/f11111183 - 9 Nov 2020

Cited by 7 | Viewed by 2192

Abstract

Several mid-sized urban areas have established boundaries overlapping with the distribution of Austrocedruschilensis (D.Don) Pic.Serm. & Bizzarri forests in Patagonia. These forests suffer a disease whose primary cause is the aggressive pathogen Phytophthora austrocedri. This study analyzes the factors related to Austrocedrus disease in an urban and peri-urban environment, showing that anthropogenic factors related to Phytophthora dispersion predominantly influence the disease distribution. The study was developed in urban and suburban areas of San Carlos de Bariloche county (Río Negro Province, Argentina). A database of requests to fell A. chilensis trees, from the Forest Department of Río Negro Province, was cleaned up and improved through satellite images analysis and field sampling. Data were analyzed in order to set up a layer of Austrocedrus disease presence. From this layer, and from anthropogenic and environmental layers (distance to houses, distance to roads, precipitation, slope, aspect, altitude, distance to water courses), a risk model was developed using the Maximum Entropy (MaxEnt) algorithm. In turn, data from the field sampling were assessed by contingency tables and chi square analysis. The results show that disease occurrence in San Carlos de Bariloche county is associated with the insertion of the urban network over areas of native forests. Distance to houses, distance to roads and distance to gardens with irrigation were the most important variables associated with the disease occurrence. A risk model was generated for the study area, which shows the current risk situation for the disease. Urbanization’s advance over the forest modifies key variables related to Phytophthora dispersion, such as the distance from cypress trees to houses and roads, thus progressively increasing the area at risk of becoming diseased. Based on these results, plausible measures and actions are proposed. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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22 pages, 5882 KiB

Open AccessArticle

Towards Eradication of Phytophthora cinnamomi Using a Fallow Approach in a Mediterranean Climate

by William A. Dunstan, Kay Howard, Andrew Grigg, Christopher Shaw, Treena I. Burgess and Giles E. St. J. Hardy

Forests 2020, 11(10), 1101; https://doi.org/10.3390/f11101101 - 16 Oct 2020

Cited by 5 | Viewed by 2372

Abstract

While eradication from haul roads was achieved, more work is required to eradicate P. cinnamomi from stockpiles and bunds. We can now implement different management strategies to the construction of bunds and stockpiles to facilitate eradication. Infestation by Phytophthora cinnamomi results in large financial and management constraints to environmental managers. This pathogen was considered impossible to eradicate until recent success with treatments including host removal, herbicide and fungicide application, soil fumigation and physical root barriers. We investigated the most benign of these treatments; keeping the area devoid of living host material. In a Western Australian mine site within a Mediterranean climate, haul roads, stockpiles and roadside bunds had P. cinnamomi colonised Pinus stem plugs buried at multiple depths. Over time, we examined the effects of soil moisture and temperature in different soil conditions and types to compare the recovery of the pathogen. Results: Within 12 months, the pathogen could not be recovered from the haul roads. In the stockpiles, depth produced significantly different results. In 3 of the 4 sites, the pathogen was not recovered at 10 cm after 20 months. By 12 months, at 50 cm, there was an 80% reduction in recovery, but only one stockpile had no recovery from 50 cm, which occurred by 36 months. Bunds were up to 1.75 m high and had variable results for plugs buried at 30 cm, influenced by height, the types of soils and shading. One of the smallest bunds was the only bund where the pathogen was not recoverable (by 22 months). This study provides strong support for using a fallow period to reduce or eliminate P. cinnamomi inoculum. Full article

(This article belongs to the Special Issue Role of Human Interventions in Spread of Soilborne Forest Pathogens and Methods for Mitigation)

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