Review Article |
Corresponding author: Sofia Branco ( sofiabranco@isa.ulisboa.pt ) Corresponding author: Jacob C. Douma ( bob.douma@wur.nl ) Academic editor: Andrea Battisti
© 2023 Sofia Branco, Jacob C. Douma, Eckehard G. Brockerhoff, Mireia Gomez-Gallego, Benoit Marcais, Simone Prospero, José Carlos Franco, Hervé Jactel, Manuela Branco.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Branco S, Douma JC, Brockerhoff EG, Gomez-Gallego M, Marcais B, Prospero S, Franco JC, Jactel H, Branco M (2023) Eradication programs against non-native pests and pathogens of woody plants in Europe: which factors influence their success or failure? In: Jactel H, Orazio C, Robinet C, Douma JC, Santini A, Battisti A, Branco M, Seehausen L, Kenis M (Eds) Conceptual and technical innovations to better manage invasions of alien pests and pathogens in forests. NeoBiota 84: 281-317. https://doi.org/10.3897/neobiota.84.95687
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When a non-native species succeeds in establishing in a new habitat, one of the possible responses is to attempt its eradication. In the present study, we analysed European eradication programmes against non-native pests and pathogens of woody plants (PPWP) from 1945 to date. Our main goal was to identify which factors affect the success of an eradication programme, reinforcing guidelines for future eradication of PPWP. Data on eradication campaigns were obtained from online databases, scientific and grey literature, and Plant Protection Organizations’ reports. Factors influencing eradication success for both arthropods and pathogens were analysed with LASSO regression and decision tree learning.
A total of 848 cases officially declared as eradication attempts were documented in our database (8-fold higher than previous reports). Both the number of programmes and their rate of success increased sharply over the last two decades. Only less than 10% of the non-native organisms affecting woody plants were targeted for attempted eradication despite the high economic and ecological impacts caused by some species for which no efforts were undertaken. Almost one-third of the officially declared cases of eradication concerned organisms that were still restricted to the material with which they were introduced. For these cases the success rate was 100%. The success rate of established species was only 50% for arthropods and 61% for pathogens. The spatial extent of the outbreak was the factor that most affected the outcome of eradication campaigns. The eradication success decreased abruptly above 100 ha for arthropods and 10 ha for pathogens. Additionally, other variables were shown to influence the outcome of eradication programmes, in particular the type of environment, with the highest eradication success rate found in nurseries and glasshouses, with successful outcomes increasing if quarantine measures were applied and when monitoring included asymptomatic plants. Particular species traits may reduce eradication success: parthenogenetic arthropods, saprotrophic pathogens, wind dispersal, the possibility to remain asymptomatic indefinitely, and the existence of resting spores or stages.
In conclusion, small affected areas, quick response, and efficient implementation of quarantine restrictions, together with particular species traits, may allow a high probability of eradication success. Preparedness at the country and European level would allow a larger number of target species to be included in future eradication programmes.
Biological invasions, pest and pathogen management, surveillance
The rate of biological invasions has sharply increased over the last century mainly due to globalization trends, including intensified travel, population growth, migratory fluxes, liberalisation of international trade and the consequent increase in global trade (
The first line of defence against biological invasions relies on preventing the introduction of non-native organisms into a new area. This is considered the most effective strategy for dealing with invasive species and is achieved through international quarantine measures, such as banning the import of goods from contaminated regions or requiring that these goods can only be imported after appropriate phytosanitary treatments (
Several factors are well accepted as contributing to the success of an eradication programme, among which, early detection and quick response are crucial (
Previous reviews have attempted to better identify which factors determine the success of an eradication programme (e.g.,
In the present study, a systematic analysis of European eradication programmes against non-native pests and pathogens of woody plants (PPWP) is addressed. We note that in some cases of pests or pathogens, the species might be native to one region of Europe but non-native to other regions. An example is the oak processionary moth (Thaumetopoea processionea) which is native to Central Europe and non-native in the UK. For pathogens there are a few cases for which the species origin was unknown. The main goal of our analysis was to identify key determinants of eradication success/failure against non-native PPWP in the European region (considered all countries in the European Continent except for Russia) so that guidelines can be developed for countries that are subject to EU legislation. Explanatory variables applicable for the European region, and countries subject to common legislation, may differ from other world regions, so the results of previous studies may not be able to fully explain the causes of success or failure of eradication programmes in this specific region. To this aim we collected and made available a comprehensive dataset of eradication attempts against PPWP for the European region, with data not previously available in other databases as GERDA. A new methodological approach was also proposed, based on LASSO regression and decision trees.
To identify introduced species of insects associated with woody plants in Europe, we used the list provided in
We used the following definitions for the terms:
According to (ISPM no. 5) the term “alien” only applies to individuals or populations that have entered by human agency into the area. However, in some cases it is not clear whether the introduction was human-mediated or just the result of natural spread. Here we consider all the non-native species independently of the introduction pathways, which in some cases are unknown.
For both arthropods and pathogens, the full list of species for which eradication was considered also includes species that are native to parts of Europe, but non-native in the regions where eradication was attempted. For arthropods these include the species Dendroctonus micans (Kugelann), Ips typographus (Linnaeus), Lymantria dispar (Linnaeus) Thaumetopoea processionea (Linnaeus) and Thaumetopoea pityocampa (Denis & Schiffermüller) and for pathogens the species Phytoplasma mali (Seemüller & Schneider, 2004), Phytoplasma pyri (Seemüller & Schneider, 2004), Plum pox virus and Dothistroma septosporum (Dorogin) Morelet. For three species of fungi the origin is still unknown: Cylindrocladium buxicola (Henricot & Culham, 2002), Dothistroma pini Hulbary, and Plenodomus tracheiphilus (Petri) Gruyter, Aveskamp and Verkley. We included in the analysis all the pathogens for which an eradication programme was implemented, including non-native (either for Europe or for the region where the programme was implemented) and species of unknown origin.
Although commonly referred to as “under eradication” in EPPO and NPPO reports and GERDA, some of the cases reported as “subject to eradication” corresponded to measures taken against a detected pest or pathogen that was still restricted to the material with which it was introduced or for which only adult insects were found. We considered these cases as post-border interceptions. According to
For both arthropods and pathogens, an establishment was considered “new” to an area if no report of the particular species was made previously from that area. Also, we considered an establishment as new if it occurred in an area previously infested, but where the population was assumed to have been previously eradicated, with an official declaration of eradication by the relevant authorities. For arthropods, we also considered an establishment as new when it was located within an isolated demarcated area – to guarantee non-overlapping demarcated areas between newly detected establishments. For pathogens, the demarcated area of the infected plants was often not reported, due to the high number of reported cases in nurseries and associated commercial confidentiality. We thus considered a new establishment when the pathogen was first detected in a given NUTS III unit (Nomenclature of territorial units for statistical purposes, created by Eurostat).
The infested/infected areas comprised the limited areas determined by the pest or pathogen presence. When the extent of these areas was numerically reported, we used the published values (in hectares). When only distribution maps were available, affected areas were measured using either ArcGIS online measure tool or by transposing the points of infested/infected plants to Google Earth Pro (version 7.3.4.8642) and measuring the area delimited by them.
The demarcated area corresponds to the area legally established by each national plant protection organization (NPPO) as subject to eradication and containment measures, and usually comprises an infested core zone, where the pest is present, and a buffer zone around the infested zone. We followed the ISPM no. 5 definition of a buffer zone (
A comprehensive database was constructed including the following information for each case (when available): i) species under eradication, ii) detection date, country, and location; iii) detection method, passive surveillance (i.e. casual observations reported by researchers, technician or citizens) or official survey conducted with that purpose; iv) establishment status (established or post-border interception); v) affected hosts; vi) host type (broadleaves, conifers, palms), vi) control methods used (chemical, host removal, biological, traps); vii) size of the infested area (as exact area information was not always available we defined it in categories ≤ 1 ha, > 1 ≤ 10, > 10 ≤ 100, > 100 ≤ 1000 or > 1000 ha); viii) environments infested (urban/peri-urban, protected green-houses, countryside); ix) climate, categorized as Temperate, Mediterranean or Continental according to Köppen classification system (
For some parameters, information was not always available and so we defined additional criteria. For the establishment status, the pest or pathogen was considered established unless stated that it was found only on the imported plant material and not in other plants at that time or posteriorly to the destruction of the original plant material. For the outcome, we consider a pest or pathogen to be eradicated when there was an official confirmation, or if no further future records were reported. If the official status changed to restricted distribution or containment and it continued to spread, it was considered a failure. Otherwise, it was still considered under eradication.
For pathogens, in many cases, the exact location of detection was not known and thus, we used the NUTS3. If the pathogen was no longer detected during the next two-yearly surveys (or two consecutive surveys when surveys were separated by more than one year) in that region, it was considered eradicated.
Some of this information was used only for descriptive analysis whereas other parameters were used in the modelling analysis (Table
Variables used as predictors in the modelling analysis and their categories.
List of predictors for arthropods | |
Control | |
Control methods | Host removal; other (including methods such as chemical, biological or traps; or combo (combination of host removal with other methods) |
Restrictions on the movement/quarantine | Yes; or no |
Monitoring method | Visual observation; or visual observation + traps |
Response time | ≤1 year; or > 1 year |
Use of a semiochemical lure | Yes; or no |
Environment | |
Location | Island; or mainland |
Initial infested area | ≤1 ha; > 1 ≤ 10 ha; > 10 ≤ 100 ha; > 100 ≤ 1000 ha; or > 1000 ha |
Main type of environment affected at start of program | Confined (nurseries, glasshouses and garden centers); urban/peri-urban (private and public gardens, along roadsides of habited areas, industrial areas, etc.); or countryside (orchards and woodlands or forests) |
Climate | Mediterranean; Temperate; or Continental (according to Köppen classification) |
Species traits | |
Host type | Broadleaf; conifer; or palm |
Phytophagous specialisation | Monophagous; oligophagous; or polyphagous |
Feeding behaviour | External; or Internal feeders |
Body size | small (≤ 2 mm); medium (> 2 mm ≤ 10 mm); or large (> 10 mm) |
Voltinism | Multivoltine; univoltine; or semivoltine |
Main reproduction method | Parthenogenesis; or sexual |
Yearly flight duration | < 4 months; ≥ 4 months < 9 months; or ≥ 9 months |
Existence of resistant stages | Yes; or no |
List of predictors for pathogens | |
Control | |
Control methods | Host removal or combo (combination with other methods such as chemical or biological) |
Restrictions on the movement/quarantine | Yes; or no |
Preventive felling conducted | Yes; or no |
Surveys at least annual | Yes; or no |
Response time | ≤ 1 year or > 1 year |
Environment | |
Location | Island or mainland |
Initial infested area | ≤1 ha; > 1 ≤ 10 ha; > 10 ≤ 100 ha; > 100 ≤ 1000 ha; or > 1000 ha |
Main type of environment affected at start of programme | Confined (nurseries, glasshouses and garden centers); urban/peri-urban (private and public gardens, along roadsides of habited areas, industrial areas, etc.); or countryside (orchards and woodlands or forests) |
Native susceptible hosts in the area | Yes; or no |
Species present in adjacent NUTSIII | Yes; or no |
Climate | Mediterranean; Temperate; or Continental (according to Köppen classification) |
Species traits | |
Host type | Broadleaf; broadleaf + conifer; or conifer |
Group | Fungi/oomycete; bacteria; nematode; or virus/viroid |
Host range | Specialist (one or a few taxonomically related species); or generalist (which infect multiple hosts, and are transmitted efficiently in hosts from different species, often from unrelated taxa) |
Incubation period | Time since infection until symptom development: ≤ 1 month; > 1 ≤ 12 months; or > 12 months |
Possibility to remain asymptomatic for long periods or indefinitely | Yes; or no |
Sporulation/replication ability | High; or low |
Existence of resting spores or stages | Yes; or no |
Main dispersal mechanism | Wind; biotic vectors; or water |
Possible saprotroph | Yes; or no |
The statistical modelling aimed to predict the probability that the species became established (i.e., no longer found only on primary material) and next, once established, the probability of successful eradication as a function of different explanatory variables. Three main categories of factors were distinguished: i) control options, ii) characteristics of the environment/location of the outbreak, and iii) biological traits of the species. All analyses were performed for arthropods and pathogens separately.
When testing how and which combination of predictors affect eradication success, we employed two different statistical methods: LASSO regression and regression trees. Both methods have two features that are important for our analysis: 1) they can handle collinearity between predictors – which is important because some variables might be confounded, for example because a certain management strategy is predominantly applied to particular groups of taxa, and 2) they both select variables based on the ability of the model to predict new outbreak cases (cases that were not seen by the model during the training phase through so-called holdout-validation). The LASSO binomial regression model adds a penalty that scales with the size of the regression coefficient. As a result, the parameter estimates will become smaller, and, importantly, the parameter values of the non-important predictors become zero (
Eradications and post-border interceptions
A total of 848 cases officially declared as eradication attempts were documented in our database, 314 against arthropods and 534 against pathogens. These cases concerned 49 species of arthropods (47 insect and 2 mite species) and 34 species of pathogens (21 fungi and oomycetes, 8 bacteria, 2 nematodes, and 3 virus/viroids). A large number of reports corresponded to post-border interceptions. These cases represented 49% (154) of reports on arthropods and 19% (87) on pathogens.
In the case of insects, these data show that for only 9% of the compiled list of 487 non-native insect species of woody plants detected in Europe, eradication measures were taken (42/487, Fig.
Cumulative number of non-native species of insects of woody plants for which eradication of established or intercepted populations was attempted, and the cumulated number of alien insect species reported for Europe until 2019.
The total number of insect species for which “eradication” measures were taken (both established populations and post-border interceptions), increased in the last two decades (Fig.
Post- border interceptions were observed for only a few species. For arthropods, 43% of reported interceptions are linked to the oak processionary moth (Thaumetopoea processionea, OPM) in the UK, outside of the containment area in London and South East England where the pest has established, after being accidentally introduced from mainland Europe (
Concomitantly, there is a discrepancy between the number of alien insect species reported and the number of eradication attempts by taxa. Most of the non-native species (52%) are hemipteran sap suckers, but eradication was attempted for only 6% of these (Fig.
Total number of non-native insect species on woody plants reported for Europe by order (bars) and proportion of species attempted to eradicate (established species).
For pathogens, 11 species have been intercepted outside of import-associated inspections, mostly in confined environments (72%). Phytophthora ramorum ranks first in the number of interceptions (63%), distributed among 12 European countries, followed by Cryphonectria parasitica (13%), the causal agent of chestnut blight, for which most interceptions were reported in the UK, where it has only recently established (
For arthropods 49% of detections occurred during official surveys (53/108). The remaining cases were detected by passive surveillance which corresponded mostly to members of the public who reported symptoms of infested plants or sightings of adult insects to the competent phytosanitary authorities, by operators of nurseries and greenhouses and growers. In contrast, pathogen detections occurred mostly during official surveys, in 90% (247/275) of cases.
Eradication measures taken against organisms still restricted to the primary material with which they were introduced, here defined as post-border interceptions, were 100% successful. From here on we will consider only eradication programmes targeted at established populations in Europe. In total, 160 programmes were launched against 41 species of arthropods (Fig.
Attempts to eradicate arthropods were mostly concentrated on bark and wood borers, followed by sap-suckers, and defoliators. Other guilds were rarely targeted. In 50% of the concluded programmes (55/111), species were confirmed eradicated. Eradication is still in progress in 46 cases (29%). Three species rank the highest in the number of eradication attempts: Anoplophora glabripennis (39), A. chinensis (18) and Rhynchophorus ferrugineus (17). Eradication success differed greatly between species (Fig.
Concluded programmes against established pathogens accounted for 359 cases. In addition, 80 cases are still in progress and for 8 cases the outcome is still unknown. Eradication programmes targeted 31 species, including fungi/oomycete, bacteria, nematodes and viruses (Fig.
As observed for arthropods, eradication of pathogens was mostly focused on a few species. Three species alone account for over half of total eradication attempts: Phytophthora ramorum (21%), Erwinia amylovora (21%) and Plum pox virus (PPV) (14%). Phytophthora ramorum (sudden oak death) was first detected in Europe on Rhododendron and Viburnum plants in nurseries (
For both arthropods and pathogens, the total number of eradication programmes against established populations increased abruptly in the last two decades, (Fig.
Eradication attempts in Europe by decade and corresponding rate of success of programmes targeting a arthropods and b pathogens.
In terms of geographic distribution, the highest number of eradication attempts per country were reported for France (81), Spain (61), Italy (57) and Germany (56) (Fig.
For arthropods, most of the attempts were carried out within one year after first detection (84%), and 10.6% were carried out in the second year, with similar success rates (53% in both cases). All five programmes starting later than 2 years after detection failed. Similarly, for pathogens, 89% of the eradication programmes were launched within one year after the first detection, with a success rate of 66%. The rate of success dropped to 42% and 25% when they were launched in the second or third year, respectively. Of the 12 programmes launched more than three years after detection, one is still in progress and the remaining failed.
The duration of failed eradication programmes was on average 5.8 ± 4.5 years (mean ± SD) for arthropods and 6.5 ± 6.5 for pathogens. For successful programmes, the duration from the start until the last detection was shorter, with 2.0 ± 2.6 and 2.0 ± 3.2 years for arthropods and pathogens respectively. Still, monitoring could continue for several years after the last observations of the species.
For both arthropods and pathogens, the success rate was the highest for infestations restricted to small areas (Fig.
Eradication attempts conducted in Europe by infested area and corresponding rate of success against a arthropods and b pathogens. Information on the approximate area affected at the time of programme start was retrieved for 139/160 cases for arthropods and 408/447 cases for pathogens.
For areas above 1000 ha, success for pathogens was only achieved once out of 40 concluded programmes (2.5%). This unique success concerned E. amylovora in Norway. The programme started in 1986 in an infested area of 30,000 ha where all the hosts were removed (i.e., all Cotoneaster, Sorbus and Pyracantha). Within the quarantine area (70,000 ha), the production and sale of all common fire blight hosts was prohibited and bee hives were moved to areas that were free from hosts of E. amylovora. From 1993 to 2000, no new detections were made and the outbreak was declared eradicated in 1998. Although fire blight was again detected within the restriction zone in 2000, it is unknown whether a re-emergence or a new introduction occurred (
Regarding the role of climate, for arthropods, the lowest eradication success was reported in Mediterranean climates (Köppen Csa, Csb) (29%), and higher success rates were observed for temperate (Köppen Cfa, Cfb) (63%) and continental climates (Köppen Dfb) (67%). For pathogens, the success rate related to climate varied depending on the group considered: i) for fungi and oomycetes the highest rate of eradication success was reported in Mediterranean climates (93%), intermediate for continental (71%), and the lowest for temperate climates (60%); ii) for bacteria the lowest success rate was again reported for temperate climates (34%), yet the highest success rate was registered in continental climates (77%), with an intermediate rate of success for Mediterranean climates (46%); iii) for viruses and viroids, the eradication success was low in the Mediterranean and temperate climates, with 62% and 64%, respectively, and high in continental ones (93%). Most attempts to eradicate nematodes were conducted in Mediterranean climates, with an overall success rate of 67%.
New establishments of arthropods were most often detected in urban or peri-urban areas, including residential and industrial areas (65% of cases). The rate of eradication success was highest (74%) in confined environments, where the plant materials were delimited (nurseries, glasshouses and garden centres), intermediate in residential areas (52%), and lowest (26%) in the countryside (orchards, woodlands /forests). Pathogen detection, on the other hand, occurred in the countryside in 50% of cases (mostly orchards, Fig.
Eradication attempts conducted in Europe against a arthropods and b pathogens, by detection site and with the corresponding rate of success. Information on the main type of environment affected at the time of the programme start was retrieved for 157/160 cases for arthropods and 405/447 cases for pathogens. * in woodlands or forests.
Most eradication programmes targeted PPWPs attacking broadleaves (79%, both for arthropods and pathogens). For arthropods attacking broadleaves in urban and peri-urban areas, the eradication success rate was 63%, while in the five cases reported in confined environments, the success rate was 100%. The lowest success rates were reported for pests on countryside woodland and forest conifers and on urban and peri-urban shrubs, where all six launched eradication programmes have failed (Fig.
Information on the eradication methods applied was available for 149 out of 160 cases for arthropods and for 427 out of 447 cases for pathogens. Eradication methods consisted mainly of host removal or destruction of host plants, which was used in 81% and 99.8% of the programmes against arthropods and pathogens, respectively. For arthropods, this proportion increases to 94% when only wood borers were considered.
When host removal was used alone, or in combination with other methods, the rate of success was 58% (48/82) for arthropods and 62% (217/350) for pathogens. Host removal was commonly combined with quarantine or movement control restrictions imposed by legislation, preventing the movement of host plants or potential host plant material outside of the demarcated areas. For nurseries, these measures usually implied that for a given period of time, neither potentially affected, nor susceptible plants, could be traded. In the field, the quarantine area usually included the infested zone and a buffer zone delimited around the infested/infected zone, which together represented the demarcated area of the outbreak. When host removal was combined with quarantine measures the success rate increased to 70% for arthropods and 65% for pathogens. When treatment of a surrounding area of predefined extent around the focus zone was imposed, either by removal of all or part of sensitive hosts or by chemical control measures, the success rate was overall higher, 67% for arthropods and 70% for pathogens, than when no such measures were applied, with 38% for arthropods and 46% for pathogens.
For arthropods, the combination of host removal with chemical treatments was reported in 31% of concluded cases, with an overall success rate of 37%. Chemical treatment without host removal was reported only in 20 cases with low success (25% success rate). Other control methods such as biological control or traps were seldom used, alone or in combination with other methods (used in 8% and 9% of programmes, respectively).
Against pathogens, disinfection of associated material, such as production machinery and tools used was reported for E. amylovora and F. circinatum (
For arthropods, visual observation was the only monitoring method used in 43% of the eradication programmes. Detection dogs were used in 29 eradication programmes against the two Anoplophora species, and tree climbers were further used for monitoring A. glabripennis, for which these methods were frequently used simultaneously, with a 100% success rate. However, it is important to note that 16 eradication programmes against this species are still in progress.
For pathogens, monitoring consisted of visual observation for symptoms and the sampling of plant material for laboratory analysis, either by morphological or, more commonly, by molecular methods. For some species, such as P. ramorum and the pine wood nematode (PWN), only symptomatic plants were commonly sampled, whereas for others, such as Citrus Tristeza Virus (CTV) and F. circinatum sampling of asymptomatic hosts is regularly conducted. For E. amylovora and PPV for example, an overall higher success rate of eradication was observed when asymptomatic plants were also sampled (60% and 92%, vs 51% and 74%, respectively). Annual surveys at places of production or other specified areas are mandatory in some cases, and were conducted in 84% of concluded cases. Conducting annual surveys provided a higher success rate (67%, 185/276) than when surveys were conducted less frequently (44%, 16/36). For P. ramorum in the UK, in addition to visual inspection in nurseries and ground surveys, aerial surveys were also used in forested areas with larch (Larix spp.), looking for visible symptoms. This method was also used for Phytophthora lateralis in UK forests. When symptoms were detected, confirmation was then attained by laboratory analysis of plant samples. In many European countries, traps were also commonly used to monitor vectors of pathogens transmitted or potentially transmitted by insects.
Of the eradication attempts reported, the vast majority were against species present in EPPO Alert, A1 or A2 lists (
Information about the citizens’ education and the engagement of stakeholders during the eradication programmes is scarce. The involvement of citizens was reported for 75/160 cases of arthropod eradication programmes. In approximately half of these cases (51%), involvement was limited to the reporting of insects or symptoms to the phytosanitary authorities. For the remaining cases, involvement was compulsory, imposed by legislation, such as the obligation to report sightings or to cut infested/infected trees. Targeted species were A. glabripennis, A. bungii, D. kuriphilus, R. cingulata, R. ferrugineus, S. dorsalis, Toxoptera citricidus, and T. erytreae. A volunteer collaboration was recorded in 15 cases, concerning A. chinensis, A. glabripennis, D. kuriphilus and R. ferrugineus. By contrast, a mainly negative attitude was recorded against the eradication of A. glabripennis in Kent, UK. The negative perception was due to unwillingness to cut historical trees or because citizens were angry claiming that contractors were cutting the wrong trees (
The results of the Cramers’ V index for the nominal variables highlighted a strong correlation between some of the variables (Suppl. material
Results for establishment probability are given in Suppl. material
The LASSO regression results showed that the area affected at the start of the eradication programme was the most important factor affecting the outcome of eradication success. For areas ≤ 1 ha and > 1 ≤ 10 ha, success is similar, but above this threshold, there is a negative relationship between the area affected and the probability of a successful eradication (β = -0.72 for > 10 ≤ 100 ha; β = -1.29 for > 100 ≤ 1000 ha and β =-2.69 for > 1000 ha; coefficients are reported at a log odds scale). Other environmental factors affecting the outcome of eradication success were the main type of environment affected at the start of the program, with a higher success rate in confined environments than in the countryside (β = 0.66), and a slightly higher success rate in mainland than in island locations (β = 0.01). Regarding control measures, only the implementation of quarantine/movement restrictions was positively associated with eradication success (β = 0.52). For species traits, internal feeders had a higher probability of eradication success than external feeders (β = 0.66), oligophagous species had a lower probability of eradication success (β =-0.22), and the group of fruit/seed feeders and gall makers had higher eradication success (β =-0.32). Considering the species targeted, A. glabripennis was associated with a higher eradication success (β = 2.35) than species for which less than five cases were reported. The optimal penalty value (λ) for the model was 0.028.
In the regression tree analysis, the optimised tree resulted in only one split, with higher eradication success for areas below 10 ha than for larger infested areas (82.6% vs 28.6%). When the area as explanatory factor was removed, a secondary tree was obtained (Fig.
Optimal classification tree (after removing the size of the affected area) for factors affecting eradication success and failures of 102 eradication programmes against non-native arthropods of woody plants in Europe. In the model, every species was given equal weight and thus the records of the same species were weighted by the inverse of the number of records per species. Light grey in bars represents successful eradication, dark grey represents failure to eradicate.
The LASSO regression estimated that the affected area was the most important factor associated with eradication failure and the higher the area the stronger the association (>1 ≤ 10 ha: β = -0.798; > 10 ≤ 100 ha: β = -1.825; > 100 ≤ 1000 ha: β = -3.246; > 1000 ha: β = -4.334). The type of environment affected also influenced the outcome, with success more likely in confined than in urban/peri urban (β = -0.196) and countryside environments (β = -0.237). Eradication success was more likely when the eradication programme started within the first year after detection (β = 0.369), in temperate than Mediterranean climates (β = 0.434), when surveys were conducted at least annually (β = 0.566), and when host removal alone was used compared to combined methods (β = 0.063). Possible saprotrophic species were harder to eradicate, although the effect was small (β = -0.050). At the species level, Fusarium circinatum (β = 0.771), Plum pox virus (β = 0.438) and Cryphonectria parasitica (β = 0.223) were easier to eradicate than species with lower than five eradication attempts, and Hymenoscyphus fraxineus (β = -2.013), Phytoplasma mali (β=-0.998), Xanthomonas arboricola pv. Corylina (β = -2.453), Xylella fastidiosa (β = -0.511), Citrus tristeza virus CTV (β=-0.059) and Lecanosticta acicula (β = 0.196) were harder to eradicate. The optimal penalty value (λ) for the model was 0.011.
In the regression tree analysis, the optimized tree resulted in only one split where the area was the only variable included, like the results for arthropods. However, here the separation occurred for areas below 1 ha, which had higher eradication success than larger areas (88.1% vs 34.6%). When the area was removed from the model (Fig.
Optimal classification tree (after the area affected removed) for factors affecting eradication success and failures of 344 eradication programmes against pathogens of woody plants in Europe. In the model, every species was given equal weight and thus the records of the same species were weighted by the inverse of the number of records per species. Light grey in bars represents successful eradication, dark grey represents failure to eradicate.
An increasing number of non-native forest pests and pathogens was observed in the last century in Europe (
We may deduce that species with higher economic or ecological impacts were those selected for eradication programmes. A low benefit: cost ratio has been suggested as one of the reasons for eradication not to be attempted (
At the European level, eradications were more concentrated in Western regions with minor numbers in the northern and eastern European countries. In part, this distribution coincides with the hotspots of first detections in Europe (
An optimistic conclusion of our study is that the overall rate of eradication success has been increasing over time for both pathogens and arthropods, and especially for the latter. In the last decade, eradication success attained levels of 76% for arthropods and 68% for pathogens. Yet, these figures include officially declared eradication measures taken against PPWP on imported materials or against adult insects, i.e. before establishment. The success for arthropods is similar to that reported by
On the other hand, eradication success relies on external drivers, and some species might be particularly difficult to eradicate which may be related to environmental factors or species traits. With this aim, we tried to understand the main factors determining eradication success.
One of the most consensual conclusions of previous studies is that eradication success is greater the smaller the affected area.
We observed that species with a higher number of eradication attempts are also those with the highest eradication success. This may reflect increased knowledge on how to deal with these particular invasive species, accumulated in the previous eradication attempts, which would also facilitate a quick reaction before its spreading and becoming then impossible to eradicate.
The similarity of symptoms to native or previously introduced species can mask the presence of invasive species for long periods, as occurred for Phytophthora cinnamomi and Heterobasidion irregulare, with similar symptoms as Phytophthora × cambivora and Heterobasidion annosum, respectively (
All these cases reinforce the concept that we should be able to identify potential invaders before they leave the country of origin to be prepared in advance. A good example is the case of P. ramorum, the causal agent of sudden oak death in California. The high potential risk identified early for this species, and the fear of having a similar epidemic in Europe, boosted the early detection and the rapid implementation of containment measures. However, not all potential invaders with high economic and ecological impacts have demonstrated this potential in its native region or other invaded regions. Frequently, an organism only becomes emergent in the invaded range, since resistance of native host plants and the communities of natural enemies keep them at low or imperceptible levels in its native range (
As expected, species found in confined or limited environments, usually subject to frequent intervention, such as greenhouses, are easier to eradicate. The same results were found by
Climate may play a role in the success of eradication programmes. Warmer climates may favour higher growth rates for arthropod populations. On the other hand, Mediterranean climates with harsher summer conditions, or a continental climate with severe winters may explain a lower probability of establishment and a higher probability of eradication success for some groups of insect pests and pathogens in these conditions. Still, a general trend of climate in the eradication success did not emerge from our analysis. The differences in the climate of origin and the one of the invaded range could have played a role in the eradication of specific species. Additional studies could address this hypothesis. Further, our dataset does not completely allow to disentangle climate effects from other factors, namely cultural and socio-economic ones.
Regarding species traits, we could associate some traits with a higher difficulty of eradication. For arthropods, the most remarkable outcome is the extremely low success in eradicating Hemipteran species. This is probably explained by several traits shared by many hemipteran species, such as the high dispersal ability, frequently mediated by wind and their difficulty of detection at low densities due to their often small size and cryptic stages, high fecundity and short life cycles. Concomitantly, in the LASSO models, species traits associated mostly with hemipterans in our group of species, such as parthenogenesis, were found to be relevant. An example is the psyllid T. erytreae, for which six eradication programmes were launched, and none succeeded, despite the huge effort invested in it. For pathogens, as expected, eradication proved to be harder for species with high saprotrophic abilities, for species dispersed by wind, for species that may remain indefinitely asymptomatic and for species with resting spores or stages. Unexpectedly, however, species with intermediate incubation periods (>1 ≤ 12 months) were overall easier to eradicate than those with shorter (≤ 1 month) or longer periods (>12 months). Short incubation periods may lead to faster population growth and dispersal thus challenging eradication efforts. The concomitant harder difficulty to eradicate species with incubation periods longer than one year may be associated with poor detection before planting infected material: if disease symptoms may appear after plantation, with a lag that may reach several years for some pathogens, the infected area may become large, hampering eradication success (
When calculating correlation between variables, most strong associations (V = 0.5) were obtained between pairs of different species traits, both for arthropods and pathogens. These correlations are justified given the high number of cases concentrated on only a few species. The statistical modelling used were able to deal with collinearity to an extent: for the LASSO regression when multiple variables are correlated they will be penalized leading to one unique predictor becoming important; for the tree-regression it chooses the variables that lead to the best split in the data. Nevertheless, it is important to note, that potentially some of the correlated variables could have been used as surrogate in the LASSO or tree regression.
An outstanding result of our study is that management options did not emerge as a relevant predictor variable of eradication success. This might be due to the fact that host plant removal, almost always combined with other treatments, was the commonly used management strategy for both arthropods and pathogens. Chemical control alone leads to very low success rates (25%). Other management options are very species-specific, such as the use of tree climbers for A. glabripennis monitoring, nest removal for oak and pine processionary moth control, and vector control for several vector transmitted pathogens and thus, do not allow extrapolation to general guidelines. Also, generally similar eradication measures were applied everywhere for a given species, because frequently these measures are mandatory according to European regulations.
Another main significant outcome of our review is the importance of quarantine measures for the success of arthropod eradication. For pathogens, however, the implementation of such measures was relevant only when the target organisms were wind-borne. The intensification of surveys, at least in an annual rhythm, was shown to be relevant both for the detection of pathogen infection before establishment and for the success of eradication. Giving up the efforts of surveillance and control after a while, especially when the populations are under low levels and difficult to detect, is a common error leading to unsuccessful eradication campaigns (
We conducted a thorough review of the eradication programmes carried out in Europe against arthropods and pathogens of woody plants and their successes or failures. Contrary to the general scepticism regarding the potential success of eradication measures, our review demonstrates that eradication programmes can be very successful, especially when detections occurred at an early stage of invasions and when the infested areas were still small. Difficulties in eradication are naturally higher in the countryside conditions in comparison with confined environments. In this respect, pests and pathogens of woody plants are as difficult to eradicate in urban and peri-urban areas as in rural forests and orchards.
We should be aware that the high success reported in previous studies and databases results in part from the inclusion of cases in which pests and pathogens were still restricted to the primary plant material with which they were introduced. After removing these cases the overall success dropped to 50%. Thus, particular attention should be paid to imported primary plant materials, involving the awareness of different actors and not only Plant Protection Inspectors.
It is surprising that eradication efforts in Europe targeted only a small group of non-native species (<10% of the non-native organisms affecting woody plants). Since the decision to carry out an eradication program is taken at the national level and frequently imposed also at the European level, we believe that more species could be considered for eradication if policymakers would be better informed about the advantages of eradication measures and actions taken quickly to ensure success of eradication. This leads to responsibilities for the scientific community in transmitting these pieces of information to policymakers.
Management strategies used in eradication programmes are very species specific and there is no general golden rule in this respect. Still, most of the successful programmes invested in integrating multiple methods combined with relentless and persistent monitoring.
This work was funded by the European Union’s Horizon 2020 Program for Research and Innovation under grant agreement no. 771271 “HOMED”
S. Branco, M. Branco, and J.C Franco were supported by Forest Research Centre (CEF), (UID/AGR/00239/2019 and (UIDB/00239/2020). and by the Laboratory for Sustainable Land Use and Ecosystem Services–TERRA (LA/P/0092/2020), research units funded by the Foundation for Science and Technology (FCT), Portugal.
We would also like to thank the plant protection organizations of the following countries (or regions), for kindly providing additional information on the reported eradication attempts: Austria- Federal Ministry Of Agriculture, Regions And Tourism; Belgium- Federal Agency for the Safety of the Food Chain; Croatia- Agency for Agriculture and Food; Finland- Plant Health Unit Ruokavirasto / Finnish Food Authority; France- Département de la Santé des Forêts (C. Husson); Germany- Julius Kühn-Institute – Federal Research Centre for Cultivated Plants, Institute for National and International Plant Health; Hungary- National Food Chain Safety Office; Italy (Piemonte)- Settore Fitosanitario e Servizi Tecnico-Scientifici, Regione Piemonte; Lithuania- State Plant Service under the Ministry of Agriculture; Netherlands- Netherlands Plant Protection Organization; Slovenia- Ministry of Agriculture, Forestry and Food; Spain- Área de Sanidad Vegetal y Forestal de Sanidad e Higiene Vegetal y Forestal; Switzerland- Federal Office for Agriculture, Plant Health and Varieties; United Kingdom – Department for Environment, Food and Rural Affairs.
Eradication database
Data type: List of eradication attempts against non-native pests and pathogens of woody plants in Europe (excel document)
Explanation note: Database including the following information for each case (when available): i) species under eradication, ii) detection date, country, and location; iii) detection method (passive surveillance (i.e. casual observations reported by researchers, technician or citizens) or official survey conducted with that purpose; iv) establishment status (established or post-border interception); v) affected hosts; vi) host type (broadleaves, conifers, palms), vi) control methods used (chemical, host removal, biological, traps); vii) size of the infested area (as exact area information was not always available we defined it in categories ≤ 1 ha, > 1 ≤ 10, > 10 ≤ 100, > 100 ≤ 1000 or > 1000 ha); viii) environments infested (urban/peri-urban, protected green-houses, countryside); ix) climate, categorized as Temperate, Mediterranean or Continental according to Köppen classification system (
Correlation matrix
Data type: Results of statistical analysis (excel document)
Explanation note: Correlations between predictor variables, using Cramers’ V.
Establishment success analysis, using LASSO regression and decision trees
Data type: Statistical analysis (word document)
Explanation note: Analysis of the factors affecting establishment success for non-native species of arthropods and pathogens of woody plants in Europe, using LASSO regression and decision trees.