REVIEW OF THE KNOWN AND POTENTIAL BIODIVERSITY IMPACTS OF

PHYTOPHTHORA AND THE LIKELY IMPACT ON ECOSYSTEM

SERVICES

JANUARY 2011

Simon Conyers Kate Somerwill Carmel Ramwell John Hughes Ruth Laybourn Naomi Jones

Food and Environment Research Agency Sand Hutton, York, YO41 1LZ

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CONTENTS

Executive Summary ...... 8 1. Introduction ...... 13 1.1 Background ...... 13 1.2 Objectives ...... 15 2. Review of the potential impacts on species of higher trophic groups ...... 16 2.1 Introduction ...... 16 2.2 Methods ...... 16 2.3 Results ...... 17 2.4 Discussion ...... 44 3. Review of the potential impacts on ecosystem services ...... 46 3.1 Introduction ...... Error! Bookmark not defined. 3.2 Heathland in the UK ...... Error! Bookmark not defined. 3.3 Ecosystem services ...... Error! Bookmark not defined. 3.4 Services from heathland ...... Error! Bookmark not defined. 3.4.1 Provisioning services ...... Error! Bookmark not defined. 3.4.2 Regulating services ...... Error! Bookmark not defined. 3.4.3 Cultural services ...... Error! Bookmark not defined. 3.4.4 Supporting services ...... Error! Bookmark not defined. 3.4.5 Additional services ...... Error! Bookmark not defined. 3.5 Discussion ...... Error! Bookmark not defined. 4. Impact on Ericaceous Host Species ...... 46 4.1 Introduction ...... 56 4.2 Host Mapping ...... 56 4.2.1 Methods ...... 56 4.2.2 Results ...... 63 4.3 Risk Scenarios ...... 73 4.3.1 Methods ...... 73 4.3.2 Results ...... 75 4.4 Discussion ...... 80 5. Options to predict climate driven changes on the potential UK distribution of Phytophthora. 82

3 5.1 Introduction ...... 82 5.2 CLIMEX model ...... 82 5.3 Incorporation into Epidemiological models ...... 83 5.4 General Conclusions ...... 84 6. Designated Sites and BAP Habitats ...... 86 6.1 Introduction ...... 86 6.2 Potential impact of Phytophthora infection on habitat condition ...... 86 6.2.1 Habitat specific Common Standards Monitoring Guidance...... 87 6.2.2 Likely impact of Phytophthora on condition criteria ...... 90 6.3 Mapping of Designated Sites ...... 91 6.3.2 National Inventory of Heathland ...... 95 6.4 Results ...... 95 6.4.1 Designated Sites ...... 95 6.4.2 National Inventory of Heathland ...... 98 7. Synthesis and Conclusions ...... 99 7.1 Summary of likely impacts ...... 99 7.1.1 Other species ...... 99 7.1.2 Ecosystem services ...... 100 7.1.3 Designated sites ...... 101 7.2 Likely impact of each scenario ...... 102 7.2.1 High ...... 102 7.2.2 Medium ...... 102 7.2.3 Low ...... 102 7.3 Future Research Priorities ...... 103 8. References ...... 104 8.1 Associated Species References ...... 108

4 Table 1 Susceptibility of a range of heathland species to P. kernoviae and P. ramorum under laboratory conditions (CSL, 2007)...... 14 Table 2 Phytophagous invertebrates that may vulnerable to the loss of, Vaccinium myrtillus (1), Vaccinium vitis-idaea (2) or Arctostaphylos uva-ursi (3) or a combination which may include Calluna vulgaris (4)...... 19 Table 3 Phytophagous invertebrates which were included in a list of of insects using, Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3) or Calluna vulgaris (4) or a combination as host plants but may need to be included even though there is uncertainty in their distribution data or host plant range...... 26 Table 4 Phytophagous invertebrates which were included in a list of of insects recorded as feeding on Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3) or Calluna vulgaris (4) or a combination but were listed under a synonym...... 27 Table 5 Phytophagous invertebrates which were included in a list of of insects using Vaccinium myrtillus as a host plant but were excluded as they are immigrants or extinct...... 28 Table 6 Phytophagous invertebrates which were included in a list of of insects using Vaccinium myrtillus or Calluna vulgaris as a host plant but were excluded as they use different food plants ...... 29 Table 7 Phytophagous fungi and invertebrates which were recorded as using Vaccinium myrtillus (1), V. vitis-idaea (2) or Calluna vulgaris (4) as a host plant but were excluded as they were introduced to England and Wales ...... 30 Table 8 Invertebrates which have been recorded visiting flowers to collect pollen and/or nectar of Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Calluna vulgaris (4) or a combination and may be vulnerable to the loss of one or more of these species ...... 31 Table 9 Fungi found in England and Wales that may vulnerable to the loss of Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3), Calluna vulgaris (4) or a combination...... 32 Table 10 Birds found in England and Wales that may vulnerable to the loss of Vaccinium myrtillus (1), Vaccinium vitis-idaea (2) or Calluna vulgaris (4) or a combination ...... 34 Table 11 Phytophagous invertebrates that may vulnerable to the loss of Calluna vulgaris ...... 35 Table 12 Invertebrates which have been recorded visiting flowers to collect pollen and/or nectar of Calluna vulgaris ...... 42 Table 13 Fungi which have been recorded as associated with Calluna vulgaris and may be threatened as it is their only host ...... 43 Table 14 Details of principal components derived from the PCA of climate variables...... 58 Table 15 Environmental variables included in the MaxENT modelling...... 61 Table 16 Selected LCM categories and the habitats used to assess the amount of land available in each 1 km square for each host species. Categories listed as ‘yes’ are included in the suitable area...... 63 Table 17 Number of presence points and associated AUC scores for the four MaxENT models. .. 63 Table 18 Permutation Importance and Percentage Contribution figures for each model...... 64 Table 19 Parameters and associated assumptions in the MPEM model1...... 74 Table 20 Total area at risk under the three risk scenarios expressed as a proportion of the total habitat available. Scenario 1 = High Risk, scenario 2 = Medium Risk and scenario 3 = Low. 80

5 Table 21 The positive and negative aspects of the three proposed methods...... 84 Table 22 Condition assessment criteria for Alpine dwarf shrub heath, which includes Annex I – Alpine and boreal heaths (H4060)...... 88 Table 23 SSSI habitats included in the selection of SSSIs at risk from a Phytophthora outbreak. . 92 Table 24 SPA habitats included in the selection of SPAs at risk from a Phytophthora outbreak. ... 92 Table 25 Habitat types included in the selection of SACs that may be vulnerable to a Phytophthora outbreak...... 94 Table 26 Numbers of designated sites containing suitable habitat that have a low area of suitable habitat, a low proportion of suitable habitat, or both...... 95 Table 27 Numbers of designated sites at risk in each scenario...... 96 Table 28 Total areas of designated sites that matched up/did not match up with the predicted host maps...... 97 Table 29 Total area of National Inventory Heathland at risk under each different risk scenario for the four species...... 98 Table 30 Number of monophagous/oligophagous species (BAP/NS status species presented separately) potentially affected by Phytophthora infection of heath species across all or part of their range under the different risk scenarios: numbers of species with % of the total in each category in parentheses...... 100

6 Figure 1 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Vaccinium myrtillus...... 66 Figure 2 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Vaccinium vitis-idaea...... 67 Figure 3 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Arctostaphylos uva-ursi. ... 68 Figure 4 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Calluna vulgaris...... 69 Figure 5 Extracted principal component values for climate variable PCs 1 and 2, across England & Wales and Scotland. The proportion of cells at each PC value shows large differences between the two regions ...... 71 Figure 6 Presence point locations used in the MaxENT modelling for all four species...... 72 Figure 7 Final host map created by incorporating MaxENT modelled species with the NIWT and Forestry Commission sub-compartment database for larch ...... 76 Figure 8 Locations of wild outbreaks of P. ramorum and P. kernoviae used in the MPEM model. . 77 Figure 9 Outputs from the MPEM model. a) = probability of Phytophthora spreading from the current locations in the next 20 years, b) = hazard map, showing the locations or number of extra 1 km2 cells that would be at risk assuming the disease had reached all cells of the map...... 77 Figure 10 Maps showing the three different risk scenarios ...... 79 Figure 11 CLIMEX match climates example output. UKs climate is matched to that of California where Phytophthora is known to be established...... 83

7 EXECUTIVE SUMMARY

Background 1. Two exotic species of Phytophthora (P. kernoviae and P. ramorum) have, in the last decade, been found to infect, and kill, a range of native and non-native woody species. Initially, infection was largely restricted to nurseries and Rhododendron ponticum in the wild. However, in 2007 Vaccinium myrtillus infected with Phytophthora kernoviae was recorded. Laboratory studies have indicated that other ericaceous species (V. myrtillus, Vaccinium vitis-idaea, Arctostaphylos uva-ursi and Calluna vulgaris) may be susceptible to one or both species of Phytophthora and V. myrtillus has the potential to support very high levels of sporulation. However, there have been no records of C. vulgaris infection in the wild therefore this species may not be affected by Phytophthora and is considered separately. 2. Ericaceous species are the dominant component of upland and lowland heathland, but are also important in a range of other communities. Widespread loss of these species as a result of Phytophthora infection or control treatments would therefore have the potential to seriously impact on the value of a number of important and sensitive habitats in terms of wider biodiversity and ecosystem services. 3. This study reviews the range of species dependent on these four ericaceous species to understand more fully the potential impact of Phytophthora infection on other groups. Ecosystem services of heathland are also reviewed. Host mapping of the four species was undertaken and the results used to assess the impact of Phytophthora infection under three risk scenarios. 4. The potential impact on designated sites and Biodiversity Action Plan (BAP) habitats is considered, by identifying sites likely to be affected by Phytophthora infection of the four ericaceous species. These were then considered in relation to the risk scenarios. Biodiversity impacts 5. The potential range of organisms that would be most affected by the loss of heathland species were identified on the basis of loss of food or habitat. Data were collated on host plant range, habitat requirement, species distribution, dispersibility and conservation status. Data were derived from web based database searches and thorough cross-referencing. Organisms most impacted were largely phytophagous insects, pollinators and fungi. The dependence of species at higher trophic levels was more difficult to assess, but predators that feed exclusively on a monophagous species of a target species were included. Species associated with C. vulgaris are identified separately. 6. A total of 417 phytophagous invertebrates were found to be associated with the four host plant species, of which 58 were classed as vulnerable to the loss of V. myrtillus, V. vitis- idaea or A. uva-ursi, of which five are BAP species and two are categorised as Nationally Scarce B. The classification was due to their monophagous habit, limited range, reduced habitat availability or a combination of these factors. In addition, these host species are important sources of pollen and nectar for four species. Other phytophagous invertebrates associated with the four potential host species were polyphagous and had low habitat specificity. 7. Loss of C. vulgaris would threaten 69 additional invertebrate species directly because they are monophagous/oligophagous. These include 5 BAP, 16 Nationally Scarce and 5 Red Data Book species. In addition, four species were found to be dependent on C. vulgaris for pollen. 8. A total of 15 species of fungi were deemed to be at risk from the loss of V. myrtillus, V. vitis- idaea or A. uva-ursi, being either monophagous or having a very restricted host plant range. Nine species were monophagous on one of the Vaccinium species. A further 7 spcies were monophagous on C. vulgaris. 8 9. Although many bird species benefit from the resources provided by these heath species (directly and indirectly) only two (red and black grouse) are likely to be significantly affected by the loss of these ericaceous species. 10. Overall, a number of species, some of which are scarce, could be adversely affected by the loss of the host plant species in question, with phytophagous invertebrates the largest group. The number of species dependent on a plant host species was related to the frequency that the plant is found. Thus, the greatest number of species at risk was associated with C. vulgaris and fewest were associated with A. uva-ursi. However, no known infection of C. vulgaris currently in the wild, means that these species may not be at risk. 11. The potential impacts of Phytophthora on species at higher trophic levels or based on habitat are more difficult to predict. 12. This review has highlighted a large number of species that may be affected by Phytophthora infection of the ericaceous host plants in terms of host plant specificity, distribution etc.. However, the actual impact will be dependent on the scale and extent of infection and control treatments in relation to the habitat in question and the dispersibility of the species at risk. A small scale outbreak of infection within a site would likely have limited impact in the long term, assuming that recolonisation was possible from adjacent areas. However, an outbreak that destroyed a habitat, which was sufficiently isolated from other similar habitats, could prevent recolonisation by less mobile species. Impacts on ecosystem services 13. For provisioning and regulating services, on the whole, these services are not dependent specifically on Vaccinium and Calluna, and, assuming rapid recolonisation occurs, the majority of provisioning and regulating services will not be overly affected. The exceptions to this are wild species diversity, and heather honey production. There is also the potential for adverse effects arising from soil erosion if large expanses of land have to be cleared of vegetation. 14. Heathland has considerable aesthetic appeal and historical importance. It is a major habitat for game shooting and walking, cycling, and other outdoor activities attract visitors and tourist revenue. Cultural services can be considered the most important ecosystem service provided by heathland as the vegetation type underpins the service. As these services are heavily dependent on appearance and access, they are also the services most likely to be affected by Phytophthora infection. Loss of characteristic species may deter visitors and more widespread loss of vegetation will reduce the appeal of heathland still further. Restrictions on movement or other activities imposed to contain the disease would also reduce the desirability of tourism in heathland habitats. These effects may persist even if vegetation recovers as the reputation of heathland as a recreation venue remains damaged. 15. Whilst heathlands may not provide a large source of income for recreation or food in the context of England and Wales as a whole, they may be crucial to the economic survival of those who work with, and within the evirons of heathlands. Employment in such areas is commonly limited and any adverse impact on heathlands due to Phytophthora could have knock-on effects within the community. Impacts on host species 16. Mapping of host species distribution 17. MaxENT modelling was used to produce host maps for the four potential host species considered at a 1 km scale using species presence data and information on climate, land cover, soil and landform. These MaxENT distributions were further refined by clipping with certain categories of the Land Cover Map 2000 (LCM2000). These categories corresponded to habitats, judged, as suitable for growth of the specific host species.

9 Without this refinement, it is assumed that the host species will fill the entirety of each 1 km by 1 km square that it is judged to be present in. By clipping with suitable habitats, this incorrect assumption is removed. 18. C. vulgaris and V. myrtillus spatial distributions were similar, although C. vulgaris was unsurprisingly more common. Both species were concentrated in upland areas of England and Wales and in lowland heathland and woodland in southern England. V. vitis-idaea was largely confined to upland heathland. Too few presence locations outside Scotland were available to adequately map the distribution of A. uva-ursi. Risk scenarios 19. The LCM2000 refined MaxENT outputs for all species (excluding C. vulgaris because it is not currently infected in the wild) were incorporated into the full host map for the Metapopulation Epidemic Model (MPEM) to estimate the potential spread of Phytophthora (full host map consists of Fera host maps plus the National Inventory of Woodland and Trees (NIWT) and larch distribution from the sub-compartment database). The MPEM ran the data for a 20 year simulation. 20. The final risk map was split in to high, medium and low risk scenarios. The high risk scenario (scenario 1) was defined as a situation where Phytophthora had spread to all areas of the UK that contain suitable host species. The medium risk scenario (scenario 2) showed the situation that would occur if the disease was only able to spread as far as the MPEM model suggests (areas with very low risk values were removed from the scenario as they were skewing the impression of risk). The low risk scenario (scenario 3) looked at the current situation and assumed that the disease will not spread any further than it has already. For each species and for each scenario, the area at risk was identified. 21. Risk areas were concentrated in Cornwall, Wales, Southern England and the Lake District. Greatest spread was within an area most likely in the New Forest, Forest of Dean, the Brecon Beacons, Crychan Forest, southern Snowdonia (Dovey Forest) and the southern Lake District (Grizedale Forest). 22. The proportion of the area of each species at risk under scenario 2, represented only 5% (V. vitis-idaea) to 7% (V. myrtillus) of the area covered by each species. For scenario 3, less than 1% of the area of land covered by each species was considered at risk from Phytophthora infection. Although overall, these figures are low, there could be significant local impact. Although C. vulgaris is currently not infected in the wild, measures to control infected Vaccinium spp. could have an indirect effect on C. vulgaris. Potential to estimate the effect of climate change 23. The distribution of Phytophthora infection will be affected by weather, since it is transmitted through wind and water. Hence climate change will affect the distribution of the pathogens. Understanding and quantifying this potential change is vital for successful disease management strategies. Methods are available to predict the likely impacts on disease distribution, but they are very different in the levels of uncertainty attached to the models and the costs associated with the analysis. 24. CLIMEX models offer simple and relatively quick ways to assess future pathogen distribution using the two sub-models described. A more complex, but far more accurate method, is to incorporate future climate scenarios (from the UKCIP projections) into existing epidemiology models. Regardless of model choice, consideration should also be paid to the many other factors that could affect pathogen distribution in a changing climate such as land use change and changes in the distribution of host species. Impact on designated sites and BAP habitats 25. Designated sites that may be affected by Phytophthora are Sites of Special Scientific Interest (SSSIs), Special Areas of Conservation (SACs) and Special Protection Areas

10 (SPAs) and a range of BAP habitats may also be at risk, only of heathland BAP habitats were considered in this context because of the uncertainty of target species presence in other habitats. 26. It is a requirement of the Habitats Directive that the condition of designated sites (SACs) is assessed and this is undertaken through common standards monitoring. Condition criteria that could be affected by infection or treatment to control Phytophthora are: proportion of bare ground, dwarf shrub heath cover, diverse vegetation structure and presence/proportion of indicator species. Although Phytophthora infection of ericaceous species could affect a range of habitats, the effects of either the disease or its treatment on condition will be greatest for heathland habitats where cover of dwarf shrub heath species is highest. In other habitats the impact of the disease on condition criteria will generally be limited because ericaceous species are less abundant, although bare ground criteria could be affected. 27. Impacts on condition will be highly site specific depending on the species composition and scale of the habitat mosaic. The range of species infected will also be important, although control treatments are likely to affect all species present. Restoration of condition after an outbreak will also be highly site specific, depending on the scale of the outbreak and the type, frequency and timing of any control treatments applied. 28. Over 5,000 SSSIs across England and Wales were imported in to ArcMAP. The number of these was reduced by systematically searching for sites that contained any suitable habitat. Designated sites were classified on the basis of the likelihood of target species presence based on the habitat descriptions, where 1 = highly suitable for the species and 2 = species may be present in low densities or only in specific habitats within a broad habitat definition. However, even where the habitat is classed as suitable, the species will not always be present. The number of SACs and SPAs were reduced using the same process as described above. However, due to differences in habitat classification on SACs and SPAs a different set of habitat names were selected and categorised. 29. For each species and for each scenario, the number and area of designated sites that remained after the sorting and that fell within the risk areas were summed. 30. Scenario 3 shows the situation as it currently exists, and shows The River Camel and Coedydd Nedd a Mellte as the highest risk sites, the area of habitat at risk within these sites was 17% and 47% respectively. In scenario 2, 19 additional SACs, 2 additional SPAs and 34 additional SSSIs are predicted to be at risk. 31. The area of upland and lowland heath at risk under scenario 2, due to the presence of C. vulgaris and V. myrtillus was 12 000 ha for each species, although it is likely that most of the area contains both species. Conclusion 32. The likely impact of Phytophthora infection of ericaceous species is highly dependent on the scale of the infection and control treatment and on habitat specific attributes (range and cover of species present, scale of any vegetation mosaic). Many associated species, designated sites and ecosystem services are likely to be affected to some degree by Phytophthora infection, however it is not possible to accurately predict the scale of the impacts. 33. The high risk scenario would undoubtedly affect a large number of associated species and a significant number of designated sites. In terms of ecosystem services, provisioning and regulating services could be affected in the short term with the loss of vegetation, but are not specifically dependent on particular species. Greatest tangible effects would be on the cultural value, with associated effects on tourism and the impacts, although not nationally important, could be significant at a local level.

11 34. Under the medium risk scenario, projected by the current disease models, a much smaller number of species and sites would be affected, although impacts on associated species would largely affect only part of the species’ range. Ecosystem services would be affected, but only at a local level. However, the local impact on all aspects considered here could be significant. 35. The low risk scenario would affect fewer designated sites and would only impact on associated species over part of their range, although again, the local impact could be significant. 36. In future, work should be undertaken to further validate the models developed here. New remotely sensed habitat data will be particularly useful once this is published. Modelling with respect to climate change scenarios would allow the likely impacts on Phytophthora infection to be evaluated. Further work on associated species could focus on areas shown to be at risk from the modelling exercise, to allow more detailed seasonal and site-specific assessment of the likely impacts. The impacts of habitat loss on species not directly associated with ericaceous host species would also be valuable.

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1. INTRODUCTION

1.1 BACKGROUND

Phytophthora is a genus of plant-damaging water moulds, which are responsible for a range of economically damaging diseases including potato blight. Two species, Phytophthora ramorum and Phytophthora kernoviae are exotic species, which infect a range of native and non-native woody species (Fera, 2010a & b). They are notifiable pathogens under European legislation, which were first confirmed present in the UK in 2002 and 2003 respectively. P. ramorum has a very wide host range. Although a number of native species have been infected (e.g. Fagus sylvatica, Betula pendula, Fraxinus excelsior) most host species are non-natives (Fera, 2010a). P. kernoviae has a much smaller host range and the majority of species are in the Magnoliaceae family. However, native hosts include Fagus sylvatica, Hedera helix and Quercus robur (Fera, 2010b).

Although many species susceptible to P. ramorum and P. kernoviae may be killed by the disease, tree species generally do not produce spores therefore only become infected if in close contact with other infected plants. Until recently, although infection was recorded on a range of species in nurseries and gardens, infection in the natural environment was restricted to Rhododendron ponticum and adjacent, non-sporulating trees. However, in 2009 the non-native Japanese larch (Larix kaempferi) was recorded infected by P. ramorum in the south-west. Research has indicated that it can produce very high levels of spores, when actively growing during spring and summer (Foresty Commission, 2010).

Native hosts have been found to include ericaceous heath species. P. kernoviae was first recorded on Vaccinium myrtillus in the natural environment in woodland in Cornwall in 2007 (Turner et al., 2009) and P. ramorum infection has since been recorded on V. myrtillus in woodland (2009) and in November 2010 in open heathland (Fera, 2010a). Vaccinium vitis-idaea, Vaccinium intermedium and Arctostaphylos uva-ursi have all been reported infected with P. ramorum, although all these records are from nursery stock and A. uva-ursi infection has not been reported in the UK. Calluna vulgaris has been reported infected with P. ramorum, however this represents a single nursery record from Poland (Fera, 2010a).

Symptoms of Phytophthora infection of Vaccinium initially include stem and leaf blackening followed by petiole necrosis and stem dieback (Beales et al., 2009). Early symptoms on V. myrtillus occur towards the top of the plant and then spread down the plant leading to a banding effect of alternating infected and healthy tissue (Turner et al., 2009). Both species produce reproductive structures known as sporangia which release mobile zoospores that enter plant mainly through wounds. The pathogen can spread by: aerial spore dispersal, through waterways, by direct plant to plant contact and by movement of contaminated soil and debris. Infected V. myrtillus can support very high levels of sporulation of P. kernoviae, therefore there is the potential for the disease to spread rapidly through a habitat.

Previously, laboratory studies were undertaken to establish the susceptibility of a range of heathland species using commercially available plants (CSL, 2007). The level of susceptibility was based on the proportion of the plant infected and the requirement to wound the plant in order to initiate infection. This work indicated that V. myrtillus, Vaccinium vitis-idaea and Arctostaphyllos uva-ursi were highly susceptible to P. kernoviae and that V. myrtillus and Calluna vulgaris were highly susceptible to P. ramorum (Table 1; CSL, 2007). These four species were therefore selected by Defra/JNCC for a review of the potential impacts of Phytophthora infection on biodiversity and ecosystem services and an assessment of the potential impact on sites of high conservation value.

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Table 1 Susceptibility of a range of heathland species to P. kernoviae and P. ramorum under laboratory conditions (CSL, 2007).

P. kernoviae P. ramorum Heathland species Common name susceptibility susceptibility

Arctostaphylos uva-ursi Bearberry Slightly susceptible Tolerant

Calluna vulgaris Heather Slightly susceptible Highly susceptible

Empetrum nigrum Crowberry Slightly susceptible Resistant

Erica cinerea Bell heather Tolerant Tolerant

Erica tetralix Cross-leaved heath Tolerant Tolerant

Vaccinium macrocarpon American cranberry Resistant Not tested

Vaccinium myrtillus Bilberry Highly susceptible Highly susceptible

Vaccinium vitis-idaea Cowberry Highly susceptible Slightly susceptible

In addition, there is another species (Phytophthora pseudosyringae) which is affecting V. myrtillus in woodland and heathland in Staffordshire (Beales et al., 2010). However, although rarely recorded in the UK, this species is currently considered a native species, therefore, although control measures are in place, this disease is not a quarantine organism. It is therefore not specifically considered in this study, although the effects on native species and habitats may be similar to those of P. kernoviae and P. ramorum. The presence of V. x intermedium (the nationally rare hybrid of V. myrtillus and Vaccinium vitis-idaea) in Staffordshire is an additional concern.

Heath species are dominant on lowland and upland heathlands, both of which are priority BAP habitats. These habitats are particularly important because the UK has 20% of the total lowland and 75% of the world’s upland heathland (http://www.ukbap.org.uk/habitats.aspx). However, heath species are an important component of other habitats including woodland, mires and bogs, montane communities and some grasslands. There is therefore considerable concern that Phytophthora infection of heath species could have significant impacts on a range of sensitive and valuable habitats in the UK.

There have, as yet, been no records of C. vulgaris infection in the wild and there is some doubt over its susceptibility status. However, until November 2010, only P. kernoviae had been recorded on heathland. Since C. vulgaris is apparently highly susceptible only to P. ramorum, it is possible that heathland infection by P. ramorum will have greater consequences for C. vulgaris than have been recorded to date. C. vulgaris is more common than the other species considered here, therefore the implications for semi-natural communities would be significantly greater if infection occurred in the wild. The implications of C. vulgaris infection are therefore considered separately in this report. Although data from Scotland have been used in the modelling of host species distribution, the implications for habitats and species is only considered in detail for England and Wales.

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1.2 OBJECTIVES

This desk study was initiated in order to assess the likely potential impacts on wider biodiversity and ecosystem services of Phytophthora infection of heath species under different risk scenarios. The specific objectives of the study, in relation to V. myrtillus, V. vitis-idaea, A. uva-ursi and C. vulgaris, were:

• To review the potential impact of Phytophthora infection of heathland species on other species.

• To undertake a qualitative review of the potential effect on ecosystem services.

• Model the distribution of the host species and assess the potential impact under three different risk scenarios.

• Investigate the potential for climate projections to assess the future range of host and disease species.

• Assess the potential impact on designated sites and BAP habitats.

15 2. REVIEW OF THE POTENTIAL IMPACTS ON SPECIES ASSOCIATED WITH POTENTIAL HOSTS

2.1 INTRODUCTION

The purpose of this review was to identify those organisms which would be most affected by the loss of heathland species which may be susceptible to Phytophthora infection. The loss of resource may be in the form of food or the habitat that these species of plant provide. The criteria for selecting the most vulnerable species was their host plant range, habitat requirement, range within England and Wales, the dispersability of the species, and conservation/rarity status.

2.2 METHODS

The potential species at risk were assessed initially from the largest group of primary consumers, the herbivores. In most terrestrial ecosystems invertebrates are an important constituent at this trophic level and the main source for records of these relationships was the web-based Database of Insects and their Food Plants produced by the Biological Records Centre, the national focus for terrestrial and freshwater species recording in the UK. Queries with the plant species produce all known insects that have been recorded as associates of each plant. A similar list of phytophagous insects can be generated from the web-based Ecological Database of the British Isles, based at the University of York, with support from the British Ecological Society and the Natural Environment Research Council. These two resources were the main source of information concerning insects and each species of insect was checked against the sources of information for each recorded relationship. Relevant supporting evidence was recorded that included other host plants which each species used together with the life stage which required the plant. This would be significant in determining the importance of the target host plant species to each species. Cross-referencing was carried out using as many sources as possible to generate an accurate host plant range for each species. Records of plant species used for captive breeding were discarded, as were foreign records as both these sources may provide an inaccurate representation of the true host plant range used in England and Wales. Other sources were also sought to encompass as many possible groups especially for pollinators, which were under-recorded from the phytophagous lists, and fungi. It was much more difficult to assess the dependence of higher trophic levels but predators which fed exclusively on a prey feeding only on the target species were included. The distribution of each species within England and Wales was ascertained by checking the species distribution records of the National Biodiversity Network Gateway, the main centre for storing all UK Biodiversity records. The number of 10 km square records for each species was noted if they were twenty or less for each country separately. The range within each country was recorded by county with the boundaries revised as of October 2009 (Ordnance Survey, 2010). The habitat requirement for each species was obtained from web-based and literature sources. This was recorded to further characterise the importance of habitat within the host plants’ ranges. The conservation status of each species was also checked, using BAP status as the main indicator (JNCC UK Priority Species, 2010), and the perceived risk and/or rarity status (Red Data Book Data/National scarcity) was also noted. The size of the wings/lack of wings of the organism was recorded to try and determine whether the species would be able to disperse from the affected habitats, although the period of infection of the plant may negate this relationship if it occurs outside the dispersal stage. Any species that was identified as vulnerable due to loss of the plant hosts was entered into the Universal Chalcidoidea Database to find Chalcidoid (parasitoid wasps) associates of named taxon. These would represent other species that may be vulnerable depending on their host range, if any of the plant hosts were lost.

16 2.3 RESULTS

A total of 417 invertebrate species were recorded as associated with the four host plant species and this status was assessed with all available sources. Of these, 44 were classified as being vulnerable to the loss of A. uva-ursi, V. myrtillus and V. vitis-idaea from England and/or Wales (Table 2). This may be due to their use of only one of these foodplants such as Elasmucha ferrugata and Pasiphila debilata, a limited range which includes the species Coscinia cribraria and Cepphis advenaria, or reduced habitat availability such as Xestia alpicola. Often it was a combination of all these factors as in the case of Cepphis advenaria. These did include some species which would lose particular ecotypes such as Callophrys rubi, which is reliant on V. myrtillus on moorland in the northern part of its range and Plebeius argus, which also has a distinctive heathland ecotype. They included five BAP species and two species categorised as Nationally Scarce B. The majority of the remaining invertebrate species were categorised as polyphagous and the target plants were only a small part of their plant host range. Furthermore their habitat specificity was low and therefore it was unlikely that the loss of these hosts would be critical for their survival. They included four BAP species, two of which were Rheumaptera hastate and Trichiura crataegi whose main hosts are Betula spp. and Myrica gale, and Crataegus monogyna and Prunus spinosa respectively. The relevant information on host plant range, habitat, geographic range, conservation status and life history stage requiring the species is presented in Appendix 1, Table 1. Some of the species information within the databases was incorrect and various species may need to be included despite these uncertainties. Five species were found whose status within England and Wales were uncertain. They have no distribution data on the NBN Gateway and limited supporting data (Table 3). A further species, Polia bombycina, a BAP species, is in this category as its host plant range is unknown in Great Britain. There were errors in the data found on the databases. Thirteen species were listed under old synonyms which are shown in Table 4 and their main details are shown under their current taxon within the other Tables. Two species of moth, Actebia fennica and Lithophane lamda, do use one or more of the host plants but are categorised as immigrants because they have never been recorded as breeding in England or Wales (Table 5). Another three species were discarded as they are categorised as extinct, the most recent being Phyllodesma illicifolia which has not been found since the 1960s (Table 5). A further four species were rejected as their food plants were incorrect, such as Boloria selene, a BAP species, and Glacies coracina, a Nationally Scarce A species (Table 6). One fungal species and eight invertebrates were also rejected as they were introductions (Table 7).

Table 8 details the invertebrate species that use V. myrtillus V. vitis-idaea and A. uva-ursi as sources of nectar and pollen. Pollen is far more crucial for a species survival as it is used to provision brood cells for developing larvae and is therefore a better criterion for determining the importance of a plant species to a particular insect species recorded visiting its flowers. This has been found with Andrena lapponica which visits a wide range of species for nectar but V. myrtillus is the only species from which it collects pollen to provision its larval cells. The other species which have been recorded visiting flowers of the target species but with a lower specificity are shown in Appendix 1, Table 3. Fungi are also reliant on plant hosts and, like invertebrates, they may proliferate on one host plant only or related ericoid species such as the mycorrhiza Hymenoscyphus ericae. The 16 species that are at the greatest risk if these host plant species were lost are listed in Table 9. Twelve of the 16 have only one or two hosts from V. myrtillus V. vitis-idaea and A. uva-ursi. The same number was classified as Nationally Rare which included Exobasidium arescens. The other species which have been recorded using the target species but which have a larger host range are shown in Appendix 1, Table 2. Many birds benefit from the resources that are provided directly through leaves (all species) and fruits (V. myrtillus V. vitis-idaea and A. uva-ursi) and indirectly through the invertebrate larvae that feed on them. There are certainly relationships with the host plants through associated habitat

17 types such as the Stonechat Saxicola torquata (Pearce-Higgins & Grant, 2006), and Dotterel (Charadrius morinellus) and Golden Plover (Pluvialis apricaria) (Pearce-Higgins, 2010). Many of these birds do breed over a range of habitat such as the Stonechat (Cramp, 1988) and it is difficult to know how the change in the constituents of one of their habitats would affect the population of these birds. Those breeders with more specialist requirements for breeding habitat such as the Dotterel and the Golden Plover do not feed directly from insects on the plant species in question but search for their prey species on the ground in the open areas (Cramp & Simmons, 1983). Some of these prey species will be from the target plant species and will be taken whilst dispersing from these plants. The relative importance of this portion of the diet is known for these species but it is not known whether this would be replaced by the insect species that would be found on the subsequent plant communities that would develop after the loss of the target plant species. However these plants are especially important for Galliformes, ground birds, and two species within this Order, both with BAP status Red Grouse Lagopus lagopus ssp. scotica and Black Grouse Tetrao tetrix ssp. Britannicus, may be affected by the loss of V. myrtillus or C. vulgaris in particular (Table 10). Two other species in this order were not included, even though Perdix perdix has BAP status, as they have much wider habitat ranges and also Phasianus colchicus is an introduction (Appendix 1, Table 1.4). Two further species, Lagopus mutus and Tetrao urogallus, also have BAP status and may be even more dependent on V. myrtillus, however their range is entirely within Scotland (Appendix 1, Table 11). The loss of C. vulgaris would threaten a separate set of 65 invertebrate species directly (Table 11). These included 5 BAP species and 16 Nationally Scarce species together with a further five Red Data Book species. Several of the species such as the coleopterans Lochmaea suturalis and RDB status Conioclerus nebulosus and lepidopteran Xestia agathina were dependent on C. vulgaris and Erica spp.. Fifty five species were more polyphagous in their host plant selection, and therefore are unlikely to be at risk though the loss of C. vulgaris, although these included seven species with BAP status (Appendix 1, Table 5). A further 24 species were found in Scotland exclusively (Appendix 1, Table 8). Seventeen species were found to be pollinators of C. vulgaris but only four of these were totally dependent on this species (Table 12). Andrena fuscipes and Collestes succinctus like the herbivorous insects used only heaths, both Calluna and Erica spp.. In addition to invertebrates there were also species of fungi for which C. vulgaris was the host. Seven species found only in England and Wales may be threatened by its loss (Table 13). The rest of the species with a broader host range that included 7 BAP species are found in Appendix 1 (Table 7) along with a further 14 species that were only found in Scotland (Table 9). A survey of the fungi associated with C. vulgaris produced 16 that may be vulnerable to its loss. All were classified as Nationally Rare such as Godronia callunigena which has been found in only two hectads in England (Table 13). The remaining species which include C. vulgaris in their host range are to be found in Appendix 1.

18 Table 2 Phytophagous invertebrates that may vulnerable to the loss of, Vaccinium myrtillus (1), Vaccinium vitis-idaea (2) or Arctostaphylos uva-ursi (3) or a combination which may include Calluna vulgaris (4).

** No information on NBN Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 2 Diptera Cecidomyiidae Dasineura Gall midge 1; 8; 72; 77; Monophagous: Vaccinium England: Tyne, Lake District Larva: Adult No record vitisidaea 79 ** vitis‐idaea (79) (77) Forms (Kieffer) gall 1, 2 Hemiptera Acanthosomati Elasmucha 1; 9; 10; 11; Monophagous: Vaccinium Wales: North, Rare Moorland All No record (Heteroptera‐ dae ferrugata 12; 89 myrtillus bugs) (F.) 1, 2 Hemiptera Aphididae Aphis Aphid 1; 2; 21; 22; Oligophagous: Andromeda England: Rare, local; Ant attended Larvae + Adult No record vaccinii 24; 25 ** polifolia, Vaccinium Yorkshire, Lincolnshire (24; adults (Borner) myrtillus, Vaccinium 25) uliginosum, Vaccinium vitis‐idaea 1, 2, 3 Hemiptera Aphididae Wahlgreniel Aphid 1; 2; 22; Oligophagous: Vaccinium Unknown Nymphs Adult (Asaphes la vaccinii 176; 177; vitis‐idaea and and hirsutus ‐ (Theobald) 180 ** Arctostaphylos uva‐ursi adults Italy, Norway) 1 Hymenoptera Tenthredinidae Pristiphora Sawfly 1; 36; 38; Monophagous: Vaccinium England: North Yorkshire Moorland Larva: Adult No record (sawflies) mollis 89; 174 myrtillus (West: One 10 km square, leaf (Hartig) last recorded 1973 (89)), Devon 1 Hymenoptera Tenthredinidae Pristiphora Sawfly 1; 36; 38; Oligophagous: Vaccinium England: (Three 10 km Moorland Larva: Adult No record (sawflies) cincta 89 myrtillus, also Betula spp. records) Surrey, leaf (Newman) Bedfordshire, Cumbria (N); Wales: (Three 10 km records) Gwynedd, Conwy, Denbighshire 1, 2 Hymenoptera Tenthredinidae Caliroa Oak Slug 1; 31; 32; Polyphagous: Betula spp., England: Hants, Wilts, Larva: (sawflies) annulipes Sawfly 33; 34; 35; Crataegus monogyna, Greater London, Essex leaf (Klug) 36; 37; 47; Corylus avellana, Fagus (Thames estuary), Humber 89 sylvatica, Prunus cerasus, Quercus spp., Salix spp., Tilia spp., Vaccinium myrtillus, Vaccinium vitis‐ idaea

Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1, 2, 3 Lepidoptera Lycaenidae Callophrys Green 1; 39; 40; Polyphagous: Vaccinium Britain: Throughout Calcareous Larva Adult No record (butterflies) rubi (L.) Hairstreak 41; 42; 43; myrtillus used almost grassland, 44; 45; 46; exclusively on acid woodland 89; 91; 173 moorland, particularly clearings, Scotland (91), Ulex spp. On heathland, heaths and neutral soils, moorland, bogs, and Helianthemum and scrubby nummularium on chalk grassland. downs, also Cytisus Strongly scoparius, Lotus associated with corniculatus, Vicia spp., warm, sheltered and flowers of Cornus sites with scrub sanguinea, Genista and shrubs and tinctoria, Rhamnus high densities of cathartica and Rubus ants may be fruticosus required for pupal survival. (173) 1 Lepidoptera Lycaenidae Plebejus Silver BAP 1; 41; 42; Polyphagous: Wide variety England: Restricted Heathland, Larva; Adult (butterflies) argus (L.) spotted 44;46; 48; of ericaceous and distribution but occurs in calcareous Ant Blue 49; 89 leguminous plants: large numbers in suitable grassland, coastal attended Heathland ‐ Calluna heathland (Dorset, Hants, vulgaris, Erica cinerea, E. Sussex, Surrey) and coastal tetralix, Ulex spp., habitats (Cornwall, Devon, Vaccinium myrtillus; Norfolk, Suffolk; Wales: Calcareous sites mainly North (Coastal) Helianthemum nummularium, Hippocrepis comosa and Lotus corniculatus 1, 4 Lepidoptera Arctiidae Coscinia Speckled RDB, 1; 3; 50; 51; Oligophagous: Agrostis England: Rare and local Heathland areas Larvae Adult, No record (macro‐ cribraria (L.) Footman BAP 69; 89; 175 curtisii, Calluna vulgaris, species, S Dorset (3 sites), of southern Occasional moths) ssp. Erica cinerea, Erica tetralix Hants (south?), other Dorset (Dry, well‐ immigrant bivittata and Vaccinium myrtillus records immigrants of drained, humus‐ (South) continental subspecies free heath). Occasional migrants of the continental subspecies arenaria also turn up in southern England.

20

Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1 Lepidoptera Geometridae Cepphis Little NSB 1; 2; 3; 41; Polyphagous: Mainly England: Gloucestershire, Woodland Larva Adult (Day No record (macro‐ advenaria Thorn 42; 50; 52; Vaccinium myrtillus, other Somerset, Hants & Sussex species, quite flying) moths) (Hubner) 89 hosts include Cornus local. sanguineum, Fraxinus excelsior, Rosa spp., Rubus fructicosus and Salix caprea 1, 2 Lepidoptera Geometridae Carsia Mancheste 1; 3; 41; 42; Oligophagous: Vaccinium England: Northern (From Peat‐bogs, Larva Adult No record (macro‐ sororiata r Treble‐bar 50; 89 oxycoccos, Vaccinium Shropshire); Scotland. mosses and damp moths) (Hubner) myrtillus, Vaccinium vitis‐ moorland idaea, Empetrum nigrum. 1, 2 Lepidoptera Geometridae Eulithis Northern 1; 2; 3; 41; Oligophagous: Vaccinium Britain: Distributed Peat moorland Larva Adult No record (macro‐ populata Spinach 42; 43; 50; myrtillus (3), Vaccinium throughout, though less and grassland moths) (L.) 52; 89 vitis‐idaea common in the south and east 1 Lepidoptera Geometridae Pasiphila Bilberry 1; 2; 3; 50; Monophagous: Vaccinium England: Locally distribution Open woodland Larva Adult No record (macro‐ debiliata Pug 59; 89 myrtillus (SW, Hants, West Midlands); Wingspan moths) (Hb.) Wales; Ireland 17‐19 mm. 1 Lepidoptera Geometridae Rheumapte Scallop 1; 2; 3; 41; Oligophagous: Populus Britain: Occurs locally over a Open woodland Larva Adult No record (macro‐ ra undulata Shell 42; 50; 89 tremula, Salix caprea, Salix large part as far north as with an moths) (L.) cinerea, Vaccinium southern Scotland undergrowth of myrtillus bilberry, and marshy areas. 1, 2, 4 Lepidoptera Geometridae Entephria Grey BAP 1; 3; 41; 42; Polyphagous: Calluna England: Midlands Mountain and Larva Adult No record (macro‐ caesiata Mountain 43; 50; 52 ; vulgaris, Erica tetralix, E. northwards; Wales; moorland species moths) (Denis & Carpet 89 cinerea, Empetrum Scotland; Ireland. Schiffermull nigrum, Salix alba, S. er) repens, Saxifraga aizoides, Vaccinium myrtillus, Vaccinium vitis‐idaea, 1 Lepidoptera Geometridae Scopula Smoky 1; 3; 41; Oligophagous: Vaccinium England: distributed locally Heathland and Larva Adult No record (macro‐ ternata Wave 42; 43; 50; myrtillus and Calluna in the north, less frequent mossland moths) (Schrank) 89 mainly, also Salix spp. elsewhere; Wales: North; Scotland 1, 2, 3, Lepidoptera Noctuidae Lithomoia Golden‐rod 1; 3; 41; Polyphagous: Calluna England: North, migrants in Mainly moorland Larva Adult Euplectrus 4 (macro‐ solidaginis Brindle 42; 50; 61; vulgaris and Vaccinium south; Wales: North; species, though bicolor (E) moths) (Hubner) 89 myrtillus, also Scotland: Central. also occurring in Arctostaphylos uva‐ursi, open woodland in Betula pendula, Crataegus places spp., Myrica gale, Salix caprea, Vaccinium vitis‐ idaea

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Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1, 3, 4 Lepidoptera Noctuidae Papestra Glaucous 1; 3; 41; Oligophagous: Calluna and Britain: Occurring sparsely Moorland Larva Adult No record (macro‐ biren Shears 42; 50; 51; Myrica gale as well as throughout western and moths) (Goeze) 89 Arctylostaphylos uva‐ursi, northern , commoner in the Erica spp., Filipendula north ulmaria, Salix spp., Vaccinium myrtillus 1 Lepidoptera Noctuidae Hypena Beautiful 1; 3; 41; Oligophagous: Vaccinium England: Locally distributed Woodland and Larva Adult No record (macro‐ crassalis (F.) Snout 42; 50; 61; myrtillus mainly, also Erica South and West; Wales; peat‐bogs, moths) 89 tetralix and E. cinerea Ireland: South 1, 2, 3, Lepidoptera Noctuidae Xestia Northern BAP 1; 3; 41; Oligophagous: Empetrum England: Northumberland; Occupying Larva Adult 15 ‐ Coelopisthia 4 (macro‐ alpicola Dart 42; 50; 51; nigrum mainly, also Scotland: Highland, Moray montane habitat 17 mm caledonica moths) (Zetterstedt 89 Arctostaphylos uva‐ursi, and Aberdeenshire, Mainly usually above (ES) ) ssp. alpina Calluna vulgaris, distributed in the mountains. 450m elevation. (Humphreys Loiseleuria procumbens, There are also colonies on & Vaccinium myrtillus, and the Scottish islands Westwood) Vaccinium vitis‐idaea 1, 4 Lepidoptera Noctuidae Syngrapha Scarce 1; 3; 41; Oligophagous: Calluna, England (North) and Moorland Larva Adult No record (macro‐ interrogatio Silver Y 42; 50; 61; Vaccinium myrtillus and V. Scotland: Throughout in moths) nis (L.) 89 uliginosum suitable habitat. England (south‐west) and Wales: occurs sparingly 2 Lepidoptera Coleophoridae Coleophora Northern 1; 2; 3; 65; Monophagous: Vaccinium England: Staffs, Derbys; Sheltered parts of Larval Wingspan No record (micro‐ vitisella Casebearer 76; 84; 89 vitis‐idaea (and Pyrola in Scotland: Highland, moors and Scots leaf 10‐13 mm. moths) Gregson Europe (84)) Aberdeenshire (3; 74) pine woodland miner 2 year life where its (84) cycle foodplant occurs 1, 2, 4 Lepidoptera Gelechiidae Prolita 1; 3; 64; 89 Oligophagous: Calluna England (North); Wales; Heather Larva Adult No record (micro‐ sexpunctell vulgaris also Empetrum Scotland moorland and Wingspan moths) a (Fabricius) nigrum, Erica spp., occurs up to quite c.17 mm Vaccinium myrtillus, high altitudes Vaccinium vitis‐idaea 2 Lepidoptera Gracillariidae Phyllonoryc Upland 1; 2; 3; 65; Monophagous: Vaccinium England: Pennines (Cheshire Higher ground, Larval Wingspan No record (micro‐ ter Midget 68; 89 vitis‐idaea and Derbyshire), Wales: particularly leaf 7‐8 mm; moths) junoniella North, Scotland moorland miner (3) Can be (Zeller) (Aberdeenshire, Angus and double Moray) brooded 1 Lepidoptera Incurvariidae Incurvaria 1; 3; 65; 89 Oligophagous: Vaccinium Britain: Patchy and local, in Moorland but not Larva: Adult No record (micro‐ oehlmanniel myrtillus and Rubus the north it can be found at far inland mining Wingspan moths) la (Hubner) chamaemorus (also Cornus high altitudes the c.14 mm. & Prunus?) leaves,

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Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1 Lepidoptera Micropterigid Micropterix Yellow‐ 3; 69; 75; Monophagous: Vaccinium England: Staffs, Worcs, & Woodland, Adult No record (micro‐ ae aureatella barred 89 myrtillus?, food plant not Warwick, and Cumbria & especially on Wingspan moths) (Scopoli) Gold found in Britain; adults North Yorks main areas, also neutral or acid 9‐11 mm. feed on pollen particularly widely scattered in Cornwall, soils, and high Carex spp. Devon, Somerset Wilts, moorland Surrey; Wales: (Fifteen 10 km records) Glamorgan, Gwynedd, Conwy, Denbighshire; Scotland: Highland, Moray, Aberdeenshire 1 Lepidoptera Nepticulidae Stigmella 1; 2; 3; 65; Oligophagous: Vaccinium England: N. Devon, Worcs, Local species, but Larva Adult Primary host (micro‐ myrtillella 66; 89 myrtillus and V. uliginosum Cumbria; Wales: Gwynedd; hard to find and Wingspan for moths) (Stainton) Scotland: Aberdeenshire, probably 4‐6 mm. Chrysocharis moray, Perth & Kinross, overlooked in nephereus Highland many places due (EWS), to its upland bias. Chrysocharis pallipes (EW), Chrysocharis pentheus (E), Cirrospilus vittatus (EWS), Derostenus gemmeus (ES) 2 Lepidoptera Nepticulidae Ectoedemia Cowberry 1; 2; 3; 65; Monophagous: Vaccinium England: Pennines ‐ Submontane Larval Wingspan No record (micro‐ weaveri Pigmy 89 vitis‐idaea Derbyshire & Cheshire, species, occurring leaf c.7 mm moths) (Stainton) Wales: North, Scotland: on high moorland miner North and mountains 1 Lepidoptera Oecophoridae Denisia 1; 67; 89, Monophagous: Vaccinium England: Cornwall, Devon, Open heathland Larva Adult No record (micro‐ subaquilea 202 myrtillus: Feeds on dead Notts; N. Wales; Scotland and moorland Wingspan moths) (Stainton) leaves and decaying (Invernessshire, 12‐14mm. vegetable matter, Aberdeenshire) Day‐flying therefore effect of disease may not beas immediate for this species

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Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1 Lepidoptera Oecophoridae Pseudatemeli 1; 3; 65; 67; Monophagous: Feeds on England: Cornwall, Devon, Woodland species Larva Adult No record (micro‐ a josephinae 89 dead and decaying leaves Hants, Gloucs, Greater occurs locally in a Wingspan moths) (Toll) (of Vaccinium myrtillus?) London, Surrey, Essex, S. disjunct c. 20mm therefore effect of disease Cumbria; Wales: north; distribution may not beas immediate Scotland: Highland, covering southern for this species Aberdeenshire England and south Wales, and in northern E. & Scotland. Lives in a portable case on the ground 1 Lepidoptera Tortricidae Ancylis 1; 2; 3; 65; Oligophagous: Vaccinium England: Devon, Derbyshire, Moorland Larva Adult Colpoclypeus (micro‐ myrtillana 66; 89 myrtillus and V. uliginosum Shropshire, N. Yorkshire habitats, high Wingspan florus (UK) moths) (Treitschke) (Also Calluna and Dryas (Coastal), S. Cumbria moors in N c.14mm. octopetala?) (Coastal); N. Wales; Scotland England and (Invernesshire, Scotland, low Aberdeenshire, Banff) heaths in Devon and Wales 1 Lepidoptera Tortricidae Apotomis 1; 2; 3; 65; Monophagous: Vaccinium England: Local (Hants, Moorland and hill Larva Adult No record (micro‐ sauciana 66; 69; 89 myrtillus Derbyshire); North Wales: districts, although Wingspan moths) (Frolich) ssp. Local it is found 13‐16 mm sauciana sometimes in (Frolich) lower elevations too. 1 Lepidoptera Tortricidae Epinotia 1; 3; 65; 66; Oligophagous: Low‐ England: Derbyshire Found locally in Larva Adult No record (micro‐ mercuriana 89 growing moorland plants, (Penines), N. Wales, Scotland moorland and Wingspan moths) (Frolich) including Calluna vulgaris (Invernesshire, mountainous c.13 mm and Vaccinium myrtillus, Aberdeenshire) habitats also Dryas octopetala 1 Lepidoptera Tortricidae Rhopobota 1; 2; 3; 66; Monophagous: Vaccinium England: Cornwall; Wales; Moorland and Larva Adult No record (micro‐ myrtillana 69; 89 myrtillus North; Scotland heathland Wingspan 9 moths) (Humph.& Aberdeenshire, Banff & species, with a to 12mm. Westw.) Moray more 2, 3 Lepidoptera Tortricidae Olethreutes Cowberry 1; 2; 3; 65; Oligophagous: Vaccinium England: Staffordshire, Heathland and Larval Wingspan No record (micro‐ mygindiana Marble 68; 89 vitis‐idaea, Arctostaphylos Derbyshire; Wales: North; moorland leaf 15‐20mm. moths) (Denis & uva‐ursi and Myrica gale Scotland: E Highlands miner Schiffermuller (Aberdeenshire, Angus, ) Moray, ) 1, 2, 3 Lepidoptera Tortricidae Rhopobota Northern 2; 3; 65; 68; Oligophagous: Vaccinium Wales: North, Scotland: Local species, Larva Adult No record (micro‐ ustomaculan Bell 69; 89 vitis‐idaea, Arctostaphylos Central occurring in Wingspan moths) a (Curtis) uva‐ursi, Myrica gale upland districts c.13 mm.

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Phytopag Host Common BAP Dispersabili Order Family Species Evidence Host plant range UK range Habitat ous Parasitoid plant name Species ty Stage 1, 3 Lepidoptera Tortricidae Olethreutes 3; 65; 69; Oligophagous: Little is Scotland: Aberdeenshire, High mountain Adult No record (micro‐ obsoletana 89; known about its life Highland, Perth & Kinross slopes wingspan moths) (Zetterstedt, history, but it is often (high mountain slopes) 16 mm 1840) found amongst Arctostaphylos uva‐ursi and Vaccinium vitis‐idaea 1, 2 Lepidoptera Tortricidae Acleris 1; 3; 65; 66; Oligophagous: Vaccinium England: Very local species (S High moors and Larva Adult Primary host (micro‐ lipsiana 69; 89 myrtillus and Myrica gale Cumbria 1 10 km square); mountains of Eulophus moths) (Denis & also Vaccinium vitis‐idaea, Scotland (Invernesshire 1 10 abdominalis Schiffermuller Betula spp. km square) (UK), ) Colpoclypeus florus (UK) 1, 4 Lepidoptera Tortricidae Philedonides 1; 3; 65; 69 Polyphagous: Wide variety England: (Only 5 10 km Heath and Larvae No record (micro‐ lunana of moorland plants, squares) Derby, Staffs, moorland moths) (Thunberg) including Calluna vulgaris, Shropshire; Wales: (Only 5 Erica spp., Myrica gale, 10 km squares) Conwy, Vaccinium spp. Denbighshire, Gwynedd, Wrexham; Scotland: (Only 2 10 km squares) Highland, Isle of Rhum 1, 2, 4 Lepidoptera Tortricidae Philedonides 1; 3; 65; 69 Polyphagous: Wide variety England: (Only Five 10 km Heath and Larvae No record (micro‐ lunana of moorland plants, squares) Derby, Staffs, moorland moths) (Thunberg) including Calluna vulgaris, Shropshire, ; Wales: (Only Erica spp., Vaccinium spp. Five 10 km squares) Conwy, and Myrica gale Denbighshire, Gwynedd, Wrexham; Scotland: (Only Two 10 km squares) Highland, Isle of Rhum 2 Lepidoptera Tortricidae Rhopobota 1; 2; 3; 65; Monophagous: Vaccinium Wales (North) and Scotland Occurring in Larva Adult No record (micro‐ ustomaculan 66; 69; 89 vitis‐idaea (Central): Local upland districts Wingspan moths) a (Curtis) c.13 mm. 3 Lepidoptera Noctuidae Anarta Small Dark BAP 1; 3; 41; 42; Monophagous: Scotland: Local and scarce High moorland of Larva Adult No record (macro‐ cordigera Yellow 50; 89 Arctylostaphylos uva‐ursi species, Highland, Moray, central Scotland moths) (Thunberg) Underwing (Captive reared Arbutus Aberdeenshire, Perth & unedo, Vaccinium Kinross uliginosum, Vaccinium myrtillus, Vaccinium vitis‐ idaea) 1, 2, 4 Coleoptera Curculionidae Caenopsis a weevil NSB 89; 98; 104; Oligophagous: Calluna England: (Nineteen 10 km Heath with bare is No record fissirostris 169 vulgaris, Erica spp. and records) Cornwall, Devon, ground associate Vaccinium spp. Dorset, Hants, East Sussex, of Kent, Norfolk, Staffs, Leics, Cumbria ; Wales: (Eight 10 km records) Gwynedd and Powys

25

Table 3 Phytophagous invertebrates which were included in a list of of insects using, Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3) or Calluna vulgaris (4) or a combination as host plants but may need to be included even though there is uncertainty in their distribution data or host plant range. ** No information on NBN Host Phytopagous Dispers Order Family Species Evidence Host plant range UK range Habitat Parasitoid plant Stage ability 1 Diptera Cecidomyii Jaapiella 1; 6; 7; 8 ** Monophagous: Vaccinium myrtillus Unknown Moorland, Larvae; Adult No record dae vacciniorum Boreal and Phytophagous; (Kieffer) subalpine Galling in terminal leaves ; Leaves & Shoots; Jun, Jul, Aug 1, 4 Hemiptera Coccidae Eulecanium 1; 15; 149 Oligophagous: Calluna vulgaris and England: Essex, Heathland All Nymph Primary host for (Sternorrhync franconicum ** Vaccinium myrtillus Kent, s Coccophagus insidiator ha‐ scales) Lindinger Lancashire(15); (UK), Blastothrix Rare trans‐ truncatipennis (E), Palaearctic Cheiloneurus elegans (E), species that feeds Cheiloneurus paralia (E), on Ericaceae (149) Discodes aeneus (E), Encyrtus infidus (EWS), Metaphycus melanostomatus (UK), Metaphycus punctipes (EW) 1 Hemiptera Diaspididae Quadraspidiotu 1; 18 (15; Polyphagous: Over 22 spp of shrubs and Unknown Unknown Larvae + adults (Sternorrhync s zonatus 17) ** trees, Vaccinium myrtillus only No record ha‐ scales) (Frauenfeldt) representative from Ericaceae 1, 4 Hemiptera Ortheziidae Orthezia urticae 1; 15 ** Polyphagous; sub‐shrubs and herbs. Unknown Unknown No record (Sternorrhync (L.) Teucrium, Calluna, Solanum, Centaurea, Larvae + adults ha‐ scales) Clinopodium vulgare, Atriplex nuttallii , Arenaria pungens, Atriplex tridentate, Artemisia maritime, Stellaria holostea, Vaccinium myrtillus 1 Hemiptera Aleyrodida Asterobemisia 1; 26; 27; Oligophagous: Corylus avellana, Castanea Unknown Unknow Larvae + adults Eretmocerus sp. (Sternorrhync e avellanae 28 ** sativa, Carpinus betulus, Linnaea borealis, Unknown ha‐whiteflies) (Signoret) Rosa spinosissima, Rubus spp., Vaccinium myrtillus, Vaccinium uliginosum 1 Lepidoptera Noctuidae Polia 1; 3; 42; 41; Polyphagous: Life history is imperfectly England: range Larva Adult (macro‐ bombycina 50; 51; 89 known. Most known food plants used for retraction, mostly moths) (Hufnagel) captive rearing Lactuca sativa, Ononis found in south‐ spinosa, Polygonum aviculare, Salix, Sonchus east (Calcareous spp., Rumex spp., Taraxacum agg., soils preferred?). Vaccinium myrtillus Occasional coastal records probably migrants

26

Table 4 Phytophagous invertebrates which were included in a list of of insects recorded as feeding on Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3) or Calluna vulgaris (4) or a combination but were listed under a synonym.

Plant host Order Family Synonym Proper name 4 Coleoptera Chrysomelidae Altica britteni Sharp Altica ericeti (Allard) 4 Coleoptera Chrysomelidae Altica longicollis (Allard) Altica ericeti (Allard) 1 Hymenoptera (sawflies) Tenthredinidae Pristiphora quercus (Hartig) Pristiphora cincta 1 Lepidoptera (macro‐moths) Geometridae Chloroclystis debiliata (Hubner) Pasiphila debiliata 1 Lepidoptera (macro‐moths) Geometridae Semiothisa brunneata (Thunberg) Itame brunneata 1 Lepidoptera (macro‐moths) Geometridae Semiothisa carbonaria (Clerck) Macaria carbonaria 4 Lepidoptera (macro‐moths) Noctuidae Ceramica pisi (L.) Melanchra pisi 4 Lepidoptera (macro‐moths) Noctuidae Eugraphe subrosea (Stephens) Coenophila subrosea 4 Lepidoptera (macro‐moths) Noctuidae Paradiarsia glareosa (Esper) Eugnorisma glareosa 1 Lepidoptera (macro‐moths) Noctuidae Paradiarsia sobrina (Duponchel) Protolampra sobrina 2 Lepidoptera (micro‐moths) Nepticulidae Fomoria weaveri (Stt.) Ectoedemia weaver 1 Lepidoptera (micro‐moths) Oecophoridae Diurnea phryganella (Hubner) Diurnea lipsiella 1 Lepidoptera (micro‐moths) Tortricidae Griselda myrtillana (Humphreys & Westwood) Rhopobota myrtillana

27 Table 5 Phytophagous invertebrates which were included in a list of of insects using Vaccinium myrtillus as a host plant but were excluded as they are immigrants or extinct.

** No information on NBN

Category Order Family Species Commo BAP Evidenc Host plant range UK range Habitat Phytopagous Dispersibility n name Species e Stage Polyphagous: Chamerion angustifolium, Epilobium Britain: North, Very rare Lepidoptera Actebia fennica Eversma 1; 3; 50; hirsutum, Pinus contorta immigrant from eastern Immigrant (macro‐ Noctuidae Moorland: Larva Adult (Tauscher) nn's 51; 89 and various herbaceous Europe. No evidence of moths) Rustic plants and Vaccinium breeding in UK myrtillus Oligophagous: Myrica gale, Salix repens, The 1; 3; 42; Vaccinium myrtillus, England: Only 2 records Lepidoptera Lithophane Immigrant Immigrant Noctuidae Nonconf 50; 61; Vaccinium uliginosum, from coast of east Moorland Larva Adult (macro‐moths lamda (F.) (SMP ormist Status 4) 89 also Populus, Salix aurita, Anglia Salix caprea, Salix cinerea, Arbutus unedo England: Originally described from Eulecanium Delamere Forest, A soft Monophagous: Vaccinium Larvae + Extinct Hemiptera Coccidae distinguendum 152 ** Cheshire on Vaccinium Woodland scale myrtillus adults (Douglas, 1891) myrtillus (Douglas, 1891). It has not been collected since Formerly found in moorland 1; 3; 41; British Isles: Possibly Lepidoptera Monophagous: Vaccinium and woodland Lasiocampida Phyllodesma Small 42; 43; now extinct as no Extinct (macro‐ myrtillus; (Also Salix and habitat in parts Larva Adult e ilicifolia (L.) Lappet 50; 60; confirmed records since moths) Betula?) of mid‐England 89 the 1960's and the south‐ west England: Extinct as a Acronicta Polyphagous: Range of Lepidoptera 1; 3; 50; breeding species in the auricoma (Denis Scarce foodplants including Extinct (macro‐ Noctuidae 41; 42; early 1900s, Immigrants Woodland Larva Adult & Dagger Quercus, Rubus, Betula, moths) 61; 89 (South and south‐east Schiffermuller) Vaccinium myrtillus coasts)

28

Table 6 Phytophagous invertebrates which were included in a list of of insects using Vaccinium myrtillus or Calluna vulgaris as a host plant but were excluded as they use different food plants

Common BAP Phytopagous Order Family Species Evidence Host plant range UK range Habitat Dispersibility name Species Stage Hemiptera Berytidae Berytinus 1; 9; 98; Monophagous: England: (Thirteen Sandy or chalk habitats, Larva Adult (Heteroptera‐ (Berytinidae) clavipes (F.) 135; 142 Ononis spp. 10 km records) feeding on rest‐harrow (142) bugs) Limited to Hants, IOW, Surrey, Sussex, Berks, Beds, East Anglia, Leics, Lincs Lepidoptera Nepticulidae Stigmella 2; 3; 69; 75; Oligophagous: England: Woodland Larva Adult (micro‐moths) microtheriel 89 Corylus avellana Gloucs/Somerset, la (Stainton) and Carpinus Greater London, betulus. (Vaccinium Cambs/Suffolk, myrtillus cited in (2) Hereford/Worcs/W but no supporting arwicks; Wales: literature) North Lepidoptera Nymphalidae Boloria Small BAP Unreliable Viola spp. England: (SW, West Damp, grassy vegetation with Larva Adult (butterflies) selene Pearl‐ 1; 49, all Midlands; N. abundant foodplant‐ (Denis & bordered other food Yorkshire; Woodland glades and Schiffermull Fritillary plants Viola Cumbria); Wales; clearings (mainly in S Britain); er) spp. (39; 42; Scotland damp grassland and 43; 45; 46) moorland (Western and N 89 Britain); grassland with bracken and/or patches of scrub; and open wood‐ pasture and wood edges (Scotland). Also dune slacks and coastal cliffs. Lepidoptera Geometridae Glacies Black RDB: 1; 3; 50; 69 Monophagous: Scotland: High‐mountain species, Larva Adult (macro‐ coracina Mountain NSA Empetrum nigrum Widespread and occurring usually at altitudes moths) (Esp.) Moth (Captive reared on quite well of 600 m or more Calluna vulgaris and distributed in partly on Erica central Highlands, tetralix) also Ross‐shire, Sutherland and Perthshire

29

Table 7 Phytophagous fungi and invertebrates which were recorded as using Vaccinium myrtillus (1), V. vitis-idaea (2) or Calluna vulgaris (4) as a host plant but were excluded as they were introduced to England and Wales ** No information on NBN Host Order Family Species Common Evidence Host plant range UK range Habitat plant name 2 Pythiales Pythiaceae Phytophthora a blight 98; 113 Oligophagous: Gaultheria shallon, Vaccinium England: (One 10 km record) Suffolk Plant inflata fungus vitis‐idaea Nursery 1 Hemiptera Coccidae Eulecanium Nut scale 1; 15; 150; Polyphagous: Acer pseudoplatanus, Alnus England, Wales, Scotland: Widespread and Wide range (Sternorrhyncha‐ tiliae (L.) 197 ** glutinosa, Arbutus unedo, Calluna vulgaris, locally common. In Beds at Dunstable scales) Carpinus betulus, Corylus avellana, Crataegus Downs, Luton and Whipsnade spp., Fagus sylvatica, Malus sylvestris, Myrica gale, Populus tremula, Pyrus spp., Ribes spp., Rosa spp., Rubus spp., Salix alba, Ulmus spp., Vaccinium myrtillus. 4 Hemiptera Coccidae Eulecanium Nut scale 1; 15; 150; Polyphagous: Acer pseudoplatanus, Alnus England, Wales, Scotland: Widespread and Wide range (Sternorrhyncha‐ tiliae (L.) 197 ** glutinosa, Arbutus unedo, Calluna vulgaris, locally common. In Beds at Dunstable scales) Carpinus betulus, Corylus avellana, Crataegus Downs, Luton and Whipsnade spp., Fagus sylvatica, Malus sylvestris, Myrica gale, Populus tremula, Pyrus spp., Ribes spp., Rosa spp., Rubus spp., Salix alba, Ulmus spp., Vaccinium myrtillus 1 Hemiptera Coccidae Parthenolecaniu European 1; 15; 16; Polyphagous: Over 100 spp. of shrubs and Britain: Non‐native; locally common (Sternorrhyncha‐ m corni Fruit 17; 150 ** trees including Calluna vulgaris and Vaccinium throughout (Channel, Thames, Ouse, Severn, scales) (Bouche) Lecanium myrtillus Trent, Mersey, Humber, Tyne, N. Wales (15)) 2 Hemiptera Coccidae Pulvinaria Cottony 150 Polyphagous: It has been recorded feeding on Britain: An Asian species that is widely (Sternorrhyncha‐ floccifera camellia Vaccinium vitis‐idaea. naturalised throughout (Malumphy, 2009) scales) (Westwood) scale 1 Hemiptera Coccidae Saissetia oleae Black scale 150 ** Polyphagous: recorded on Vaccinium sp.. Britain: Introduced. Cosmopolitan, found on (Sternorrhyncha‐ (Olivier) Recently found breeding outdoors in London indoor plantings throughout. scales) (Malumphy, 2009) 1 Hemiptera Diaspididae Abgrallaspis Cyanophyllu 150 ** Polyphagous: recorded on Vaccinium sp.. Britain: Introduced, Cosmopolitan, found on (Sternorrhyncha‐ cyanophylli m scale Cosmopolitan, found on indoor plantings indoor plantings throughout . Breeds scales) (Signoret) outdoors in sheltered conditions in south west England 1 Hemiptera Diaspididae Aspidiotus nerii Oleander 150 ** Broadly polyphagous: recorded on Britain: Introduced Cosmopolitan, found on (Sternorrhyncha‐ Bouche scale Arctostaphylos sp. and Vaccinium sp.. indoor plantings throughout. Breeds scales) outdoors in sheltered conditions in southern England 1, 2 Hemiptera Pseudococci Pseudococcus Glasshouse 152 ** Polypahgous, Introduced cosmopolitan. Common throughout Britain on indoor (Sternorrhyncha‐ dae viburni mealybug Recorded on Vaccinium spp. plantings. scales) (Signoret) 30 Table 8 Invertebrates which have been recorded visiting flowers to collect pollen and/or nectar of Vaccinium myrtillus (1), Vaccinium vitis- idaea (2), Calluna vulgaris (4) or a combination and may be vulnerable to the loss of one or more of these species

Host Order Family Species Evidence Host plant range UK range Habitat Parasites plant 1 Hymenoptera Andrenidae Andrena 89; 163 Polyphagous: Ranunculus sp., England; Wales; Scotland: Found Woodland, Cleptoparasite fucata Potentilla sp., Helianthemum throughout, rarely abundant heaths, moors probably Nomada nummularium, Rubus caesius, and coastal panzeri Rubus idaeus, Rosa sp., dunes. Chaerophyllum temulum, Rumex acetosella, Veronica spp., Barbarea vulgaris, Vaccinium myrtillus, Crataegus sp., Prunus sp., Oenanthe sp., Euphorbia amygdaloides 1, 2 Hymenoptera Andrenidae Andrena 89; 98; 99; Polyphagous: Prunus spinosa, Salix England: Patchy distribution Open Inquilline: Myopa lapponica 163 spp., Taraxacum agg., Thymus concentrated in Hants, Surrey, woodland, buccata (Conopid fly) polytrichus, Ulex europaeus, and West Sussex, and Derbyshire, moors and lives commensally in Vaccinium myrtillus (Main pollen Yorkshire and Lancashire, also montane sites same burrow. source), V. vitis‐idaea, Viola canina Devon, Dorset and Cumbria; Cleptoparasite: Wales: (Seven 10 km records) Nomada panzeri Monmouthshire, Ceredigion, Gwynedd, Wrexham; Scotland: Firth of Forth, Glen More 1, 4 Hymenoptera Apidae Bombus 89; 160; Polyphagous: Wide variety of England: Cornwall, Devon, Heaths, Parasite: Bombus jonellus 162; 170; flowers for both pollen and nectar. Dorset, Hants, Surrey, Sussex Moorland, sylvestris 180 In heathland areas Salix and Kent, scattered populations from calcareous Vaccinium spp. pollen in spring, Derbyshire northwards; Wales: grasslands, Calluna vulgaris in summer mainly coastal; Scotland: coastal dunes, Highland Largest populations suburban gardens 1, 2, 4 Hymenoptera Apidae Bombus 89; 98; Polyphagous but strong association England: Declining everywhere. Montane Parasite: Bombus monticola 163; 170; with extensive areas of tall Mainly north of a line between moorland sylvestris 180; 184 Vaccinium myrtillus: Salix (nectar) the Severn and the Humber, also habitat with and Vaccinium myrtillus (Pollen and Cornwall, Devon and Somerset; grassland nectar) in spring; Lotus spp., Rubus Wales; Scotland associations fruticosus, R. idaeus and Trifolium Adult spp. in early to mid summer; Erica cinerea and Vaccinium myrtillus in mid to late summer

31 Table 9 Fungi found in England and Wales that may vulnerable to the loss of Vaccinium myrtillus (1), Vaccinium vitis-idaea (2), Arctostaphylos uva-ursi (3), Calluna vulgaris (4) or a combination.

Host Order Family Species Common Evidence Host plant range UK range Habitat Part of plant infected plant name 1, 2 Erysiphales Erysiphacea Podosphaera Bilberry 95; 98 Oligophagous: Vaccinium England: Devon, Heaths, moors Live leaf is parasitised by e myrtillina Mildew myrtillus and V. vitis‐idaea Hants/Sussex/Surrey, cleistothecium Cumbria, Lancashire; Wales: Mid, Scotland: More frequent 1 Exobasidiales Exobasidiac Exobasidium A redleaf 93; 94; 98 Monophagous: Vaccinium Rare, localised (Only four 10 Montane Live leaf is galled by eae arescens fungus myrtillus km records) Wales: North, fruitbody Scotland: East Highlands 2 Exobasidiales Exobasidiac Exobasidium A redleaf 93; 98; Monophagous: Vaccinium vitis‐ Wales: (Two 10 km records) Moors eae juelianum fungus 178 idaea Denbighshire, Wrexham; Scotland: (Nine 10 km records) Highlands 1 Exobasidiales Exobasidiac Exobasidium A redleaf 93; 94; 98 Monophagous: Vaccinium Britain: Throughout, Moors Leaf is parasitised by eae myrtilli fungus myrtillus commoner north of a line fruitbody, shoot is galled from the Severn Estuary to by fruitbody the Humber Estuary 2 Exobasidiales Exobasidiac Exobasidium Cowberry 93; 98; Oligophagous: Empetrum England: West Midlands, Common on eae vaccinii Redleaf 114; 178 nigrum, Vaccinium vitis‐idaea Pennines, Cumbria, Yorks, moorland and in high Northumberland; Wales: (4 pine forest sites) Gwynedd, Conwy; Scotland: Highland, Moray, Aberdeenshire, Angus, Perth & Kinross, Stirling, Argyll & Bute. It is clearly under‐ recorded 1 Helotiales Dermateace Pezicula 97; 98 Monophagous: Vaccinium England:(Only six 10 km Moors Dead, dry branch is ae myrtillina myrtillus records) N. Yorks Moors, decayed by erumpent, Worcs, Warks, S. stromatic apothecium Gloucs/Wales Monmouthshire 1, 2, 4 Helotiales Helotiaceae Hymenoscyph 93; 183; Oligophagous: Calluna vulgaris, England: Yorkshire Heaths, moors Roots us ericae 198; 199; Vaccinium myrtillus, Vaccinium 200; 201 oxycoccus, Vaccinium vitis‐ idaea 1 Helotiales Sclerotiniac Monilinia 97; 98 Monophagous: Vaccinium England, Wales and Scotland: Moors Young branches site of eae baccarum myrtillus Only Nine 10 km records entry scattered throughout

32

Host Order Family Species Common Evidence Host plant range UK range Habitat Part of plant infected plant name 2, 3 Helotiales Phacidiacea Phacidium 98; 180; Oligophagous: Arctostaphylos England: (One 10 km record) Moors e vaccinii Fr. 183 uva‐ursi, Vaccinium vitis‐idaea Yorkshire; Scotland: (Three 10 km records) Shetland, Highland, Argyll & Bute 1 Pleosporales Venturiacea Protoventuria 97; 98 Oligophagous: Vaccinium England: (Four 10 km Heath and moors leaf (live, senescing, e myrtilli myrtillus and V. uliginosum records) Exmoor, Worcs, dead) Warks; Scotland: Far north (One 10 km only) 1, 2 Rhytismatales Rhytismatac Coccomyces an 97; 98 Oligophagous: Vaccinium vitis‐ England: (Three 10 km eae leptideus ascomycete idaea and V. myrtillus records) S. Yorks; Wales: (One 10 km records) Denbighshire; Scotland: Highlands 2 Rhytismales Rhytismatac Lophodermiu an 97; 98 Monophagous: Vaccinium vitis‐ England: (Two 10 km records) eae m ascomycete idaea S. Yorks, Lancs; Wales: (One melaleucum 10 km records) Powys; Scotland: (Six 10 km records) Highlands, Outer Hebrides 1 Rhytismatales Rhytismatac Terriera 97; 98 Monophagous: Vaccinium England: (Ten 10 km records) dead, attached twig is eae cladophila myrtillus Exmoor, Devon, Cornwall; decayed by opening by (Lév.) B. Wales: (Five 10 km records) slit apothecium Erikss. Conwy and Gwynedd; Scotland: Highlands 1, 2 Uredinales Pucciniastra Naohidemyce a rust 93; 98 Oligophagous: Vaccinium spp. Britain: Widespread Leaf ceae s vacciniorum fungus eg Vaccinium x intermedium, throughout but absent from Vaccinium uliginosum, East Anglia and most of East Vaccinium vitis‐idaea, Midlands Vaccinium oxycoccos 1 Xylariales Amphisphae Seimatosporiu 97; 98 Monophagous: Vaccinium England: (One 10 km record) dead twig is decayed riaceae m vaccinii myrtillus Durham 1 Xylariales Hyponectria Pseudomassar 97; 98 Monophagous: Vaccinium England: (Two 10 km records) dead twig is decayed ceae ia vaccinii myrtillus Worcs, Warks

33

Table 10 Birds found in England and Wales that may vulnerable to the loss of Vaccinium myrtillus (1), Vaccinium vitis-idaea (2) or Calluna vulgaris (4) or a combination

Host Order Family Species Common BAP Evidenc Host plant range UK range Habitat plant name e 1, 2, 4 Galliformes Tetraonidae Lagopus Red BAP 177; Oligophagous: Mostly Calluna England: Devon; Derbyshire Subalpine and subarctic lagopus ssp. Grouse 190 vulgaris, also Vaccinium spp. northwards mainly in west and central moor, heathland, bog, scotica northern England and North York marsh moors; Wales: Throughout exceptPembrokeshire and extreme south 1, 2, 4 Galliformes Tetraonidae Tetrao tetrix Black BAP 177; Polyphagous: Plant material, England: Derbys, N. Yorks, Cumbria, Co. Conifer forest and forest ssp. britannicus Grouse 189 according to availability (eg Durham, Northumberland; Wales: edge, moorland Betula spp., Calluna vulgaris, Ceredigion, Powys, Gwynedd, Conwy, Vaccinium spp., Empetrum Denbighshire; Scotland: Throughout nigrum, Pinus spp.) except northwest, Northeast and central lowlands

34

Table 11 Phytophagous invertebrates that may vulnerable to the loss of Calluna vulgaris ** No information on NBN

Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Coleoptera Carabidae Amara (Celia) a ground NSA, rare 89; 98; Oligophagous: adults eat seeds England: (Sixteen 10 km records) Dorset, IOW, Lowland heathland infima beetle 103; 143; Surrey, Kent, Beds, Suffolk, Norfolk, Lincs ; 166 Wales: (One 10 km record) Glamorgan Coleoptera Chrysomelidae Altica ericeti Flea beetle NSB 1; 117; Oligophagous: Calluna vulgaris, England: Hants, Surrey, Berks, Midlands Lowland heathland (Allard) 120; 121; Erica spp., Empetrum nigrum (scattered), North York Moors, Cumbria, 122; 123 Durham, Northumberland; Wales (Nine 10 km records) Scattered; Scotland: Highlands and northwards Coleoptera Chrysomelidae Lochmaea Heather 1; 4; 103; Oligophagous: Calluna vulgaris, England, Wales, Scotland: Widespread Lowland heath suturalis Beetle 117; 122 Erica spp. throughout in suitable habitat (Thomson, C.G.) Coleoptera Curculionidae Caenopsis a weevil NSB 89; 98; Oligophagous: Calluna vulgaris, England: (Nineteen 10 km records) Cornwall, Heath with bare ground fissirostris 104; 169 Erica spp. and Vaccinium spp. Devon, Dorset, Hants, East Sussex, Kent, Norfolk, Staffs, Leics, Cumbria ; Wales: (Eight 10 km records) Gwynedd and Powys Coleoptera Curculionidae Coniocleonus RDB3 1; 2; 103; Oligophagous: Calluna vulgaris, England: (Seven 10 km records) Limited to Dry heath nebulosus (L.) 105; 117 Erica spp. Dorset, Hants, Surrey, Kent, Norfolk Coleoptera Curculionidae Micrelus ericae Small Heather 1; 2; 103; Oligophagous: Calluna vulgaris, England: Limited to Dorset/Hants, Surrey, Heathland and moorland (Gyllenhal) Weevil 117; 124 Erica spp. Sussex, Kent, East Anglia, Leics, Cumbria; Wales: (Europea Throughout especially Anglesey, Gwynedd, n); 125; Ceredigion, Pembroke; Scotland: Higland 126 Coleoptera Curculionidae Neliocarus sus Heather 1; 103; Oligophagous: Calluna vulgaris, England: Limited to Dorset, Hants, Surrey, Heathland van Emden 1939 Weevil 104; 117; Erica spp. Sussex, Suffolk (Coastal) and Cumbia, more (Synonym 129 scattered distibution in W. & E. Midlands; Wales: Strophosomus sus (Europea West; Scotland: E. Higland scattered Stephens) n) Coleoptera Curculionidae Strophosoma RDB2/3 1; 103; Oligophagous: Calluna vulgaris, England: (One 10 km record) Limited to Isle of Dry heath fulvicorne Walton 104; 129 Quercus spp., Salix spp. Purbeck, Dorset 1849 (Europea n) Hemiptera Cicadellidae Erythria aureola RDBK ‐ 1; 2; 89; Oligophagous: Calluna vulgaris, England: Worcestershire (1 record 10 km (Auchenorrhynch (Fallen) Insufficientl 131; 132; Carex spp. square) Scotland: Eastern Highlands a) y Known 142 ** Hemiptera Cicadellidae Ulopa reticulata 2; 89; Oligophagus: Calluna vulgaris, England: Hants, Surrey, Sussex, Suffolk, Heathland (Auchenorrhynch 142 Erica cinerea, Erica tetralix Shropshire, Cumbria (Most records); Wales: a) Pembrokeshire, Carmarthenshire, Ceredigion, Gwynedd, Conwy, Anglesey; Scotland: Highland Hemiptera Cicadellidae Zygina NSB 1; 2; 131; Monophagous: Calluna vulgaris England: (Three 10 km records) Limited to Berks Dry heath (Auchenorrhynch rubrovittata 133 & Surrey a) (Lethierry) (Europea n); 142 35 Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Hemiptera Lygaeidae Nysius helveticus RDB3 1; 9; 13; Oligophagous: Calluna vulgaris, England: Rare (Seven 10 km records) Limited to (Heteroptera‐ (Herrich‐Schaffer) 142 Erica spp. Dorset, Hants, Surrey bugs) Hemiptera Miridae Globiceps juniperi NSB 1; 9; 142 Oligophagous: Calluna vulgaris, England: (Seven 10 km records) Surrey, (Heteroptera‐ (Synonym Erica spp., Salix herbacea Shropshire, Lincs, Yorks, Cumbria; Scotland: bugs) Globiceps (One 10 km record) Moray Firth woodroffei Wagner, Globiceps salicicola) Lepidoptera Geometridae Chlorissa viridata Small Grass NSA 1; 2; 3; Polyphagous: Calluna vulgaris, England: Hampshire (New Forest), also very local Damp Heaths (macro‐moths) (L.) Emerald 41; 42; Erica tetralix, Betula spp., Salix Cornwall, Devon, Somerset, Dorset, Surrey, 43; 50; repens, Rubus fruticosus and Sussex 69 Ulex spp. Lepidoptera Geometridae Eupithecia Ling Pug 1; 2; 3; Oligophagous: Calluna vulgaris England, Wales and Scotland: Widespread and Heathland and moorland (macro‐moths) absinthiata f. 50; 59 (Flowers), also Erica spp.(3) often abundant in suitable habitat goossensiata (Mab.) (Just a form of Eupithecia absinthiata (Genitalia identical)) Lepidoptera Geometridae Eupithecia nanata Narrow‐ 1; 2; 3; Oligophagous: Calluna vulgaris England, Wales and Scotland: fairly commonly Heathland and moorland (macro‐moths) (Hubner) winged Pug 41; 42; (Flowers) also Erica tetralix distributed throughout. 50; 58; (Flowers) (59) 59 Lepidoptera Geometridae Idaea contiguaria Weaver's NSA 1; 3; 41; Oligophagous: Calluna vulgaris Wales: Hillsides of Gwynedd. Montane heather (macro‐moths) (Hubner) Wave 42; 43; mostly, but also Empetrum moorland 50; 69 nigrum and Umbilicus rupestris Lepidoptera Geometridae Pachycnemia Horse NSB 1; 2; 3; Oligophagous: Calluna vulgaris, England: Heaths of the southernmost counties Lowland heaths (macro‐moths) hippocastanaria Chestnut 41; 42; Erica tetralix (Dorset, Hants, Isle of Wight, Surrey), also (Hubner) 50; 69 Berkshire, Sussex, Devon, Somerset, Lincolnshire Lepidoptera Geometridae Selidosema Bordered NSA 1; 3; 41; Oligophagous: Calluna vulgaris England: Hampshire, Dorset, Surrey, also Heathland and downland (macro‐moths) brunnearia Grey 42; 50; (Heath and moorland) and Cumbria and Shropshire; Scotland: Canna, Rum, (Villers) 69 Lotus corniculatus (calcareous Argyll, Kincardineshire grassland and sand‐dune) also Ononis repens, Trifolium spp., Erica spp. Lepidoptera Noctuidae Anarta myrtilli (L.) Beautiful 1; 2; 3; Oligophagous: Calluna vulgaris England: Resident. Common in suitable habitat, Heathland and moorland. (macro‐moths) Yellow 42; 43; and Erica cinerea distributed widely, but locally and Underwing 51; 62 discontinuously. The same applies to Wales and Scotland

36

Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Lepidoptera Noctuidae Hypenodes Marsh NSB 1; 3; 42; Unknown: Larva not found in Britain: Resident. Scattered distribution up the Boggy moorland, (macro‐moths) humidalis Oblique‐ 50; 51 wild ‐ reported reared on Erica west side of Britain from Devon to Scotland, heathland, bogs, swamps, Doubleday barred tetralix and, in mainland north of the Moray Firth. Also occurs on the fens, marshes and water‐ Europe, on Sphagnum moss Norfolk coast. meadows, including small and Potentilla palustris. At one sites of only 1‐2 hectares. British breeding site only plants in addition to those already mentioned were Calluna vulgaris and Molinia caerulea Lepidoptera Noctuidae Lycophotia True lover's 1; 3; 2; Oligophagous: Calluna vulgaris, Britain: Resident. Common. In suitable habitats, Acid heathland and high (macro‐moths) porphyrea (Denis knot 41; 42; Erica cinerea (needs often abundant. moorland. & Schiffermuller) 50; 51 confirmation) and Erica tetralix. Lepidoptera Noctuidae Xestia agathina Heath Rustic BAP 1; 2; 3; Oligophagous: Calluna vulgaris, England: Resident. Local. Widespread cheifly in Acid heathland and (macro‐moths) (Duponchel) 41; 42; Erica tetralix and Erica cinerea. the south and south‐west, north Midlands, and moorland. Most numerous 50; 51; North; Wales: Widespread, localised; Scotland: where heather is tall. Local. Widespread including the Hebrides and Orkney. Lepidoptera Noctuidae Xestia ashworthii Ashworth's BAP NSA 1; 2; 3; Polyphagous: Many low‐ Wales: Resident. Confined to north west On many geological strata (macro‐moths) (Doubleday) Rustic 41; 42; growing plants, including . including slate and 50; 51; Calluna vulgaris, Campanula limestone, on hillsides, 69; rotundifolia, Digitalis purpurea quarries and mountain‐ Erica cinerea, Helianthemum sides. Small, isolated nummelarium, Galium verum, patches of foodplant Hieracium agg., Rumex growing on steep, rocky acetocella, Salix repens, ground and scree seem to Sanguisorba minor, Solidago be preferred virgaurea and Thymus polytrichus Lepidoptera Noctuidae Xestia castanea Neglected BAP 1; 2; 3; Oligophagous: Calluna vulgaris, England: Resident. Local. Widespread but found Open woodland and (macro‐moths) (Esper) Rustic 41;42; Erica cinerea and Erica tetralix mainly on heaths. Local on Man. In the Channel wooded heathland, 50; 51 Islands Local and occasional on Jersey, rare on moorland and raised bogs Guernsey; Wales: Resident. Local. Widespread; Scotland: Widespread including Hebrides and Orkney.

Lepidoptera Coleophoridae Coleophora Least Case‐ 1; 2; 51; Oligophagous: Calluna vulgaris, England: Surrey, Kent, Beds, Worcs, Staffs, Heaths, moors and, (micro‐moths) juncicolella bearer 69; 76 Erica cinerea Suffolk, Cumbria; Wales: Glamorgan, Gwynedd, occasionally, gardens Stainton Conwy; Scotland: Aberdeenshire, Highland

37 Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Lepidoptera Coleophoridae Coleophora Ling Case‐ 1; 2; 51; Oligophagous: Calluna vulgaris, England: Cornwall, Beds, Staffs, Suffolk; Wales: Moorland, heaths and (micro‐moths) pyrrhulipennella bearer 69; 76 Erica cinerea, E. tetralix Glamorgan, Gwynedd; Scotland: Aberdeenshire bogs Zeller Lepidoptera Gelechiidae Aristotelia 1; 2; 51; Monophagous: Calluna vulgaris England: Hants, Surrey, Beds, Staffs, Shropshire, Heathland (micro‐moths) ericinella (Zeller) 64; 69 Suffolk; Wales: Glamorgan; Scotland: Patchy distribution Lepidoptera Gelechiidae Lita sexpunctella 1; 2; 64; Monophagous: Calluna vulgaris England: Staffs, Derbys, Cumbria ; Wales: North ; Heather moorland and (micro‐moths) (Fabricius) 69 Scotland: Highland, Aberdeenshire occurs up to quite high (Synonym for altitudes Prolita sexpunctella) Lepidoptera Gelechiidae Neofaculta 1; 2; 51; Oligophagous: Calluna vulgaris, Britain: Common throughout wherever heather Heathland (micro‐moths) ericetella (Geyer) 64; 69 Erica cinerea, E. tetralix grows Lepidoptera Oecophoridae Amphisbatis 1; 3; 51; Oligophagous: Calluna vulgaris, England : (Only 13 10 km squares) Cornwall Heathland (micro‐moths) incongruella 67; 69 Pilosella officinarum and (Lizard), Hants (157), Middlesex, Sufflok, Worcs, (Stainton) Thymus polytrichus (157). Staffs, Shropshire; Wales: North; Scotland Lepidoptera Psychidae Pachythelia RDB 1; 3; 63; Oligophagous: Calluna vulgaris England: (Only 3 10 km squares) Dorset and Heathland (micro‐moths) villosella 65; 66; and Erica spp. Hampshire (New forest heathland), also Suffolk? (Ochsenheimer) 69 Lepidoptera Scythrididae Scythris RDB 1; 3; 65; Oligophagous: Calluna vulgaris, England: (Only 1 10 km square (Surrey?)) Dorset Sandy heaths (micro‐moths) empetrella 67; 69; Erica spp. rare and local, currently known only from a few Karsholt & Nielsen 156 localities, Hampshire (near Lyndhurst) Lepidoptera Tortricidae Eupoecilia 1; 69 Polyphagous: F. fasciella: England: Cornwall, Devon, Wiltshire, Hampshire, Nominate form angustana (micro‐moths) angustana Calluna vulgaris, Nominate Surrey, Norfolk, Sufolk, Beds, Herts, West occurs in woodland edges, (Hubner) ssp. form angustana: variety of Midlands, Cumbria; Wales: North and South; meadows and similar fasciella Donovan plants including Plantago and Scotland: Moray Firth, Coastal Aberdeenshire locations. The F. fasciella is Achillea. . found on heathland Coleoptera Carabidae Agonum 1; 115 Monophagous: Calluna vulgaris England: Much more widespread to the east of a Damp habitats obscurum (Europea line between the Severn and Tees estuaries; (Herbst) n) Wales: South Coleoptera Carabidae Amara lunicollis 1; 115 Monophagous: Calluna vulgaris England, Wales, Scotland: Common and Open or semi‐open Schioedte (Europea widespread throughout, often abundant habitats esp if well‐drained n); 143 Coleoptera Carabidae Bradycellus 1, 103; Monophagous: Calluna vulgaris England: Much commoner north of a line Dry heaths usually with caucasius 115 between Severn and Humber Estuaries; Wales Calluna on sand or gravel (Chaudoir) (Europea (Seven 10 km records); Scotland: Mainly soils (Synonym n); 143 Highlands Bradycellus collaris (Paykull)) Coleoptera Carabidae Bradycellus 1; 115 Monophagous: Calluna vulgaris England, Wales, Scotland: Abundant and Dry habitats ‐ grassland, harpalinus (Europea widespread throughout heath, arable, woodland (Serville) n); 143 Coleoptera Carabidae Bradycellus 1; 115 Monophagous: Calluna vulgaris England: Abundant and widespread north, more Well‐drained heaths and ruficollis (Europea local south; Wales: Commoner in north; moors with Calluna (Stephens) n); 143 Scotland: Widespread and abundant (143)

38 Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Coleoptera Carabidae Calathus 1; 115 Monophagous: Calluna vulgaris England, Wales, Scotland: Very abundant and Grasslands, heaths, arable, melanocephalus (Europea widespread throughout gardens (L.) n); 143 Coleoptera Carabidae Dyschirius 1; 115 Monophagous: Calluna vulgaris England, Wales, Scotland: Widespread Damp, bare peaty or sandy globosus (Herbst) (Europea throughout with some areas of increased ground in many types of n) prevalence habitat Coleoptera Carabidae Pterostichus 1; 115 Monophagous: Calluna England, Wales, Scotland: Common and In marshes, shaded or diligens (Sturm) (Europea vulgaris, (also Sphagnum widespread throughout, very abundant damp grassland and n); 143 spp.?) upland moors Coleoptera Carabidae Trichocellus 1; 103; Monophagous: Calluna vulgaris England: Widespread and often abundant north Moors, heaths usually with cognatus 115 of a line between Severn and Humber Estuaries, Calluna (Gyllenhal) (Europea mainly Peninnes and N. York moors; Wales (Five n); 116; 10 km records) Local; Scotland: Mainly Highlands 143 Coleoptera Chrysomelidae Calomicrus NSA 1; 4; 98; Oligophagous: Calluna vulgaris, England: Southwest (Coastal), Dorset, Hants, Heath and moorland circumfusus 117; 118; Ulex spp., Genista spp., Cytisus Sussex, Greater London with few records north (Marsham) 119 spp. of these; Wales (Five 10 km records); Scotland: (Europea (One 10 km record) n) Coleoptera Coccinellidae Coccinella Hieroglyphic 8 89; 98; Monophagous: Feeds entirely England: Dorset to Kent, East Anglia, West Heather (Calluna vulgaris hieroglyphica Ladybird 103; 16 on larvae of heather beetle Midlands, Cheshire, Lincs, Yorks, Lancashire, and Erica spp.) heathland (Lochmaea suturalis) Cumbria; Wales: Throughout; Scotland: Dumfries and Galloway, Ayrshire, Argyll and Bute, Perth and Kinross, Highland Coleoptera Curculionidae Acalles ptinoides a weevil 98; 105 Oligophagous: Calluna vulgaris, England: Scattered throughout most frequent in Heathland and Quercus spp. Southeast, Norfolk and Cumbria; Wales: Scattered throughout except northeast; Scotland: (Three 10 km records) Dumfries and Galloway Coleoptera Curculionidae Caenopsis waltoni 98; 104; Oligophagous: Calluna vulgaris England: Coastal Cornwall, Devon, Dorset, East Heath with bare ground 169 and Erica spp. Sussex and Kent, also Surrey, Cambs, Suffolk, Leics, Staffs, Shropshire, Cheshire, Cumbria; Wales: Coastal Swansea, Carmarthenshire, Pembrokeshire, Ceredigion, Gwynedd, Anglesey, also Powys Coleoptera Curculionidae Neliocarus 1; 98; Oligophagous: Calluna vulgaris, England: Scattered distribution in South, Gloucs, Heathland nebulosus 103; 104; Erica spp., Thymus spp., Ulex W. & E. Midlands, East Anglia, Yorks and Stephens 117; 124 spp Cumbria; Wales: Widespread throughout (Europea n); 127; 129. Hemiptera Lygaeidae Kleidocerys ericae 1; 9; 13; Oligophagous: Betula spp., England: Hants, Surrey, Sussex, Greater London, Heathland, associated with (Heteroptera‐ Horvath 98; 142 Calluna vulgaris, Erica spp., Gloucs, East Anglia, Lancs, Yorks, Cumbria; heather bugs) Hypericum spp. Wales (Five 10 km records) north; Scotland: Highland (Around Moray Firth)

39 Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Hemiptera Lygaeidae Macrodema 98; 142 Oligophagous: Calluna vulgaris England: Dorset, Hants, Surrey, Sussex, Norfolk, Abundant on heathland (Heteroptera‐ micropterum and probably other plants Suffolk, Lincs, Yorks, Cumbria, Northumberland; bugs) Wales: (Seven 10 km records) Anglesey, Gwynedd, Wrexham, Ceredigion; Scotland: (Three 10 km records) Highland, Moray Hemiptera Lygaeidae Rhyparochromus Ground Bug NSB 1; 9; 98; Oligophagous: Calluna vulgaris, England: (Twenty one 10 km records) Limited to Heathland, often under (Heteroptera‐ pini (L.) 142 Erica spp. Devon, Somerset, Dorset, Surrey, Sussex, Kent, heather or in leaf litter. bugs) Essex; Wales: (Seven 10 km records) South Further west, it is mainly coastal coastal and associated with sand dunes. It is likely to have a variety of foodplants Fruits/seeds Hemiptera Lygaeidae Scolopostethus 98; 142 Monophagous: Always England: Cornwall, Dorset, Surrey, Sussex, Essex, Found commonly on (Heteroptera‐ decoratus associated with Calluna Suffolk, Gloucs, Worcs, Cumbria, heathland throughout the bugs) vulgaris Northumberland; Wales: (Fifteen 10 km records) UK Anglesey, Gwynedd, Denbigh, Wrexham, Powys, Ceredigion, Swansea, Carmarthenshire, Pembrokeshire; Scotland: (Three 10 km records) Dumfries and Galloway Hemiptera Miridae Orthotylus 1; 9; 142 Oligophagous: Calluna vulgaris, England: Cumbria (Main population), Heathland (Heteroptera‐ ericetorum Erica tetralix Widespread in SE, East Anglia, West Midlands; bugs) (Fallen) Wales: coastal; Scotland: Moray Firth and further north Hemiptera Pseudococcidae Spinococcus 1; 139 Oligophagous: Calluna vulgaris, England: Rare, scattered Thames, Mersey (Sternorrhyncha‐ calluneti Erica cinerea scales) (Lindinger) Hemiptera Aphididae Aphis callunae 1; 2; 22; Monophagous: Calluna vulgaris England: Sussex, Essex, Kent, Lincs, Yorks, (Sternorrhyncha‐ Theobald 24; 25 Cumbria,; Wales: South, North; Scotland: W. aphids) Highlands, (24, 25) Hemiptera Aphalaridae Strophingia ericae 1; 2; 140; Oligophagous: Calluna vulgaris, Britain: Common and widespread on Calluna Heathland with Calluna (Sternorrhyncha‐ (Psylloidea) (Curtis) 141; 142 Erica cinerea vulgaris plant lice) Lepidoptera Lycaenidae Plebeius argus Silver‐ BAP 1; 41; 42; Oligophagous: Heathland ‐ England: Devon, Dorset, Hants, Surrey, Sussex Three main habitats are (butterflies) studded Blue 44; 48; Calluna vulgaris, Erica cinerea, and the Isle of Portland in Dorset; and sand used with ants Lasius 91 E. tetralix, Ulex spp.; dunes in Cornwall, Norfolk and Suffolk; Wales: alienus and L. niger: Calcareous sites ‐ Lotus calcareous grasslands in Pembrokeshire lowland heathland (the corniculatus, Helianthemum most widely used); nummularium, Hippocrepis calcareous grasslands; comosa, Ornithopus sand dunes; occasionally perpusillus. occurs in other habitats such as bogs. Lepidoptera Geometridae Dyscia fagaria Grey 1; 2; 3; Oligophagous: Calluna vulgaris, England: Locally distributed mainly in the north Shorter swards on (macro‐moths) (Thunberg) Scalloped Bar 41; 42; Erica cinerea, Erica tetralix also locally in the very south; Wales: locally moorland, heathland and 50; 69 distributed mainly in the north; Scotland: peat bogs scattered throughout

40 Common Order Family Species BAP status Evidence Host plant range UK range Habitat name Lepidoptera Geometridae Ematurga Common 1; 2; 3; Oligophagous: Calluna vulgaris, England: Most densely distributed in the south‐ Most abundant on acid (macro‐moths) atomaria (L.) Heath 41; 42; Erica cinerea and Erica tetralix east but found locally and sometimes in heaths and moorland also 50; 69 on heathland and moorland; abundance throughout; Wales: Throughout; meadows and grassland Trifolium spp. and Lotus spp. Scotland: Throughout and open woodland elsewhere Lepidoptera Noctuidae Coenophila Rosy Marsh RDB 1; 3; 41; Oligophagous: Myrica gale England: Cumbria (South)(Two 10 km records); Fens, Bogs (macro‐moths) subrosea Moth 50; 51; mainly, also Empetrum nigrum Wales: Tregaron and Borth bogs (Six 10 km (Stephens) 69 and Andromeda polifolia records) (Coastal mid‐Wales ‐ Ceredigion and (Winter) (Calluna vulgaris, Gwynedd) captive reared) Lepidoptera Noctuidae Heliothis Shoulder‐ BAP 1; 3; 42; Oligophagous: Calluna vulgaris, England: Resident. Very local to Dorset, Acid Heathland, where E. (macro‐moths) maritima Graslin striped Clover 50; 51; Erica tetralix and Narthecium Hampshire and Surrey. No records for Wales or tetralix is abundant. ssp. warneckei 63; ossifragum. Scotland. Boursin Lepidoptera Pyralidae Pempelia 1; 3; 65; Oligophagous: Calluna vulgaris England: Cornwall, Dorset, Hants, Wilts, Surrey, Mainly heathland (micro‐moths) palumbella (Denis 67; 69; and Erica spp., also Polygala Cambridgeshire, Suffolk, Worcs, Staffs, Cumbria; & Schiffermuller) 92 spp., Thymus drucei and T. Wales: Glamorgan, Gwynedd, Anglesey praecox Lepidoptera Tortricidae Ancylis unguicella Broken‐ 1; 3; 65; Oligophagous: Calluna vulgaris England: (Only 14 10 km squares) Hampshire, Hills and moors and is (micro‐moths) (L.) barred Roller 66; 69 and Erica cinerea, also Betula Kent, Middlesex, Suffolk, Cambridgeshire, generally commoner in the spp. Shropshire, Cumbra; Wales: (Only 8 10 km more upland regions squares) Gwynedd, Conwy, Glamorgan; Scotland: (Only 12 10 km squares) Highland, Moray, Aberdeenshire, Perth and Kinross Lepidoptera Tortricidae Olethreutes 1; 3; 65; Oligophagous: Calluna vulgaris England: Commonest in the north of (Cumbria), Moorland (micro‐moths) schulziana (F.) 66; 69 and Empetrum nigrum, also scarce in the south (Staffs and Shropshire); Vaccinium oxycoccos Wales: north; Scotland: less common Thysanoptera Thripidae Ceratothrips Heather No info Oligophagous: Calluna vulgaris Britain: in suitable habitat Heathland, live flower is ericae Thrips on NBN; and Erica spp. foodplant of larva, adult 106; 171; 172

41

Table 12 Invertebrates which have been recorded visiting flowers to collect pollen and/or nectar of Calluna vulgaris

Order Family Species BAP status Evidence Host plant range UK range Habitat Parasite Hymenoptera Andrenidae Andrena NSA, rare 89; 98; 99; Oligphagous: Calluna England: Main areas are Dorset, and Heaths with dry Cleptoparasite: argentata 160; 162; vulgaris and Erica spp. Hants, West Sussex, and Surrey, also loose sandy Nomada baccata, 165; 166; (species with strong or Worcestershire and Norfolk areas also Sphecodes 167; 184 obligate requirement for reticulatus heathers) also Pyrola spp. Hymenoptera Andrenidae Andrena fuscipes 89; 99; Oligophagous: Calluna England: Cornwall, Devon, Dorset, Heather‐ Cleptoparasite: 160; 162; vulgaris (Both males and Hants, Surrey, Sussex, Kent, Bucks, dominated Nomada rufipes 184 females), rarely found on Herts, east Anglia, Worcs, Shropshire, heaths anything else. Staffs, Notts, Yorks, Lincs; Wales: (Six 10 km records) Swansea, Pembrokeshire, Gwynedd; Scotland: (Five 10 km records) Ayrshire, Dumfries and Galloway, Highland Hymenoptera Colletidae Colletes 74; 89; 99; Oligophagous: Pollen from England: Local, Cornwall to Kent, East Dry heathland Cleptoparasites: succinctus 159; 160 Calluna vulgaris and Erica Anglia, Herefordshire north to and moorland Anthophorine bee spp. Cumbria and North York Moors; with south‐ Epeolus cruciger Wales: (Six 10 km records) Swansea, facing, thinly‐ and Bee‐fly Pembrokeshire, Flintshire, Wrexham; vegetated earth Bombylius minor Scotland: Borders, Argyll and Bute, banks for Highland, Outer Hebrides underground nests, also coastal Hymenoptera Halictidae Lasioglossum 89; 160; Polyphagous: Calluna England: Restricted range, Main Sandy heaths Cleptoparasite: prasinum 161 vulgaris, Erica cinerea and areas Dorset and Hants/Surrey/West Sphecodes E. tetralix preferred during Sussex with isolated populations in reticulatus mid and late summer, also Cornwall, Devon, IOW, Kent and Crepis sp., Myosotis sp. and Suffolk; Wales: (Four 10 km records) Taraxacum agg. Swansea, Carmarthenshire

42

Table 13 Fungi which have been recorded as associated with Calluna vulgaris and may be threatened as it is their only host

BAP Order Family Species Evidence Host plant range UK range Habitat status Helotiales Dermateaceae Belonopsis 89; 97; 183 Calluna vulgaris England: (Eighteen 10 km Heath and moor obscura records) Surrey, Hants, Suffolk, Yorks, Lancs, Northumberland, Cumbria; Wales: (One 10 km record) North; Scotland (Five 10 km records) Helotiales Dermateaceae Tapesia 89; 97; 183 Calluna vulgaris England: (Six 10 km records) Heath and moor cinerella Hants, Surrey, Gloucs, Yorks; Scotland: (Three 10 km records) Dumfries, Highlands Helotiales Helotiaceae Godronia 95; 183 Calluna vulgaris England: (Two 10 km records) Heath and moor callunigena Surrey, Norfolk; Scotland: (Five 10 km records) Islay, Rum, Stirling Helotiales Helotiaceae Godronia 89; 95; 183 Calluna vulgaris England: (Two 10 km records) Heathland cassandrae f. Norfolk; Wales: (One 10 km Callunae record) Pembroke Pleosporales Pleosporaceae Pithomyces 89; 95; 183 Calluna vulgaris England: (One 10 km record) Heathland valparadisiacus Surrey Polyporales Corticiaceae Vuilleminia 89; 93; 183 Calluna vulgaris England: (One 10 km record) Coastal heath macrospora North Norfolk Coast; Scotland: (One 10 km record) Colonsay Russulales Stereaceae Aleurodiscus 89; 93; 108; Calluna vulgaris England: (Three 10 km records) Heath and moorland norvegicus 183 Hants, Surrey, Kent; Scotland: (Two 10 km records) Dumfries, Arran

43 2.4 DISCUSSION

This exercise involved extensive searching through many databases and it was often difficult to find the source of the original information and to test the veracity of this information. Databases are important sources of information and are also quick means of producing data about a particular organism. However this is not always the best method and it is still important to check the accuracy of the source. The confirmation of the target host plants within each species’ range was an important starting point. However further detail was required on the reported range of each organism within England and Wales together with details of the type of habitat where the organism was found before an accurate decision on how the loss of each of the host plants might affect each candidate species. Conservation status such as BAP was an important indicator of a species population level and its trend which supports the criteria of this assessment but the reason for its inclusion in BAP may not necessarily be due to host plant, which is why some BAP species were discounted. The relative importance of the four plant species is notable when a comparison is made of the species within the invertebrates, fungi and birds which require them for their survival. C. vulgaris has the largest range of species which use its resources separate to the other three species at 150 with a further 87 shared with one or more of the other three species. This compares with 68 and 90, 14 and 40, and 3 and 14 species for V. myrtillus, V. vitis-idaea and A. uva-ursi respectively. C. vulgaris covers more land area than the other species and is also a major constituent in a larger number of plant communities. However, it’s lower sensitivity to P. kernoviae and the absence of infected plants in the wild means that there is currently no potential effect on other species. Vaccinium species and the higher trophic levels that they support, however may be lost if there is considerable range extension of P. kernoviae. V. myrtillus is a source of food through its foliage and, uniquely amongst the four species, it also flowers and fruits twice each year thus providing twice the resource and over a greater period than the other species. Species which were monophagous for any of the host plant species were easier to assess than those which had small host ranges. It is often difficult to know the relative importance of each plant species and whether the loss of one host would be compensated by the others. In the case of C. vulgaris, many species often use Erica spp. in addition. Therefore it is possible that these species may be able to support a viable population. The extent of the loss particularly at higher trophic levels is hard to gauge. The habitats of which the plants are constituents are also important in supporting other Orders such as Arachnida and Diptera where the relationship between specific plants and their various species is not so direct. Buglife, the leading trust for the conservation of invertebrates, lists 76 notable species of Arachnida and 130 species of Hymenoptera associated with lowland heathland. This demonstrates the importance of this habitat and the potential damage that may occur with the loss of any of the main constituents of this ecosystem, such as C. vulgaris. This is also true of other plants within the communities and these may also be affected by a change in the vegetation compostion and structure. There can be prominent carpets of bryophytes in short, woodland ground vegetation, but they may be just as abundant and diverse among tall C. vulgaris and V. myrtillus. Tall C. vulgaris and V. myrtillus provide extra habitat for epiphytic bryophytes and lichens. Therefore the potential loss may be much higher if other organisms, where the relationship is not as direct, are also affected through habitat loss and other changes which may occur when there is a major change within plant communities. Invertebrates are able to move between patches to compensate for the loss of food plant or habitat. Size is not a restriction to dispersal as shown by Celastrina argiolus, a Lycaenid one of the smallest butterflies in England (adult wingspan 26 – 34 mm) and yet it is highly mobile and able to colonise new sites quickly. However this perceived dispersion ability may not necessarily occur. Many species are not adapted for dispersion due to their habitat specificity and are therefore poor colonisers. It is a riskier strategy to search within the wider landsape than to stay within a location where they are able to find mates and foodplants. Some species of moth such as Amphisbatis incongruella and Pachythelia villosella have apterous females, which limits their dispersion and the same is true for many Hemiptera such as Nabis ericetorum, where the commonest form is wingless. However this separation of suitable habitats may also be the best protection against the dispersal of Phytophthora if distances between habitat patches are beyond the spread of spores. There are certainly a group of species which would potentially be lost if the spread of Phytophthora was to continue. Their reliance on one or more of the susceptible plant species means that there would be no alternatives. Habitat specificity and environmental factors also mean that dispersal to other habitats would not occur. Adaptation to their existing environment and the life strategy that has developed means that a change in the environmental factors such as elevation to take advantage of the loss of a host plant species may not be physiologically possible. Often the continuity in host plant species is not present to support such a transition if such an adaptation was possible. It is also likely that this loss of species may be higher due to the change in the plant communities which would result from such a loss.

45 3. REVIEW OF THE POTENTIAL IMPACTS ON ECOSYSTEM SERVICES

This review considers the potential impact of Phytophthora on heathland. In this report the term heathland is used generically to include dwarf shrub heath (found in both lowlands and uplands), montane heath and some bogs. Although the species under consideration here can also occur in other habitats such as lowland wood pastures, the impact of Phytophthora infection of ericaceous species in these habitats is likely to be much less important than infection of the trees themselves. The purpose of this review is to provide a qualitative assessment of the scope of the potential impact on ecosystem services. It does not encompass a quantitative valuation, nor does it include the impact of woodland infection, as this is the objective of PG0102 (Measuring the economic, environmental and ecosystem services value of woodland, heathland and heritage gardens in the context of determining potential impacts from the regulated plant pathogens, Phytophthora ramorum and Phytophthora kernoviae).

3.1 INTRODUCTION

Heathland is a managed habitat peculiar to western and northern Europe and generally considered to be of international conservation importance. Heathland was formed as a result of ancient forest clearance and agricultural practices, and it remained an important grazing resource throughout pre-industrial history (Webb, 1998). During the last 200 years, afforestation, intensification of agriculture, and development have led to a long-term decline in the extent of heathland in the UK. However heathlands remain an important part of the British heritage; they are a source of income for upland farmers and for landowners (for shooting), and they provide enjoyment in terms of recreation. Without continuous human intervention, natural succession results in the conversion of most heathland to woodland or grass/bracken-dominated habitats, but the unique character and composition of heathland ecosystems is now further threatened by various species of Phytophthora.

This report uses the ecosystem services approach to provide a broad, qualitative assessment of the value of UK heathland ecosystems to human well-being. Ecosystem services have been defined as “the benefits people obtain from ecosystems” (Millennium Ecosystem Assessment, 2005). These include products and services obtained directly from natural systems as well as more subjective cultural, historical, and aesthetic services. More recently, a National Ecosystem Assessment (NEA) has been undertaken for the UK and the methodology employed by the UK NEA (see section 3.4) has been adopted in this revised report.

3.1.1 Heathland

Most heathland ecosystems found across northern and western Europe were formed around 6000 years ago as a result of forest clearance and extensive livestock grazing by prehistoric agricultural communities (Price, 2003). A few heathland sites are the climax vegetation in exposed areas, such as mountains or coastal areas. The removal of woody biomass reduced the input of organic matter to soils and grazing gradually lowered the nitrogen content of the system and prevented the growth of tree species. The result of this process was a managed landscape dominated by slow-growing species adapted to low nitrogen conditions, particularly ling heather (Calluna vulgaris) and bell heather (Erica cinerea). Heathland soils are typically sandy and acidic podzols, which are rare in natural ecosystems, with peat formation more common in wetter areas (Friedlander, 1960). Numerous species of plants and animals now rely on heathland as an important feeding or breeding habitat, including endangered species such as nightjars and woodlarks. The Dartford warbler is now only found in heathland habitats (RSPB, 2009).

Heathland was an important economic resource, in terms of grazing, fuel, animal bedding, thatching, industrial processes, food, honey production and as a source of medicinal plants, until the intensification of European agriculture began in the early 19th century. During the last 200 years, the area of heathland in the UK has declined to just one sixth of its extent in 1800 (Newton 46 et al., 2009). Approximately 25,800 ha were lost between 1947 and 1969 alone (Newton et al., 2009). Some areas of heathland have been converted to improved grassland enclosures for intensive livestock grazing and nowadays, heathlands are appreciated for their biodiversity, aesthetic and recreational values, with more limited agricultural use. Other areas have been lost to urbanization and forestry. However, one of the most significant threats to contemporary heathland is natural succession (Haines-Young & Potschin, 2007; Price, 2003). Management is required to maintain heathland and without it, succession changes the landscape to open birch woodland and then either pine or oak forest, depending on local climate and soil conditions (Friedlander, 1960). Long-term stages of bracken, gorse and/or rough grasses, such as Molinia caerulea, are also frequent.

During the 20th century, increased nitrogen deposition has accelerated the loss of heathland, favouring faster-growing species, such as grasses, adapted to higher soil nitrogen concentrations (Tomassen et al., 2004). Management of the remaining heathland area has also changed over the last century, with increased use of burning in upland areas to stimulate new plant growth and improve food resources, particularly for grouse (Yallop et al., 2006). Continued management of the remaining heathland is mainly driven by remaining livestock grazing, and by the demand for grouse shooting. Although there has been some interest in increasing the use of grazing to manage lowland heathland, public opinion is not always supportive of this management practice (Newton et al., 2009), particularly because of the need for fencing. Despite the large losses of heathland over the last 200 years, the UK still accounts for 75% and 25% of the world’s upland and lowland heath respectively (http://www.ukbap.org.uk/habitats.aspx), and in England and Wales alone, 41% of the European Dry Heath SACs are class A or B, i.e. outstanding, or excellent examples of the feature in a European context (JNCC, 2011) However, the unique character and composition of heathland ecosystems are now threatened by various species of Phytophthora.

As a recognised ecosystem of importance, heathlands provide many benefits to humans, and the threat of Phytophthora infection in these habitats could have far reaching consequences. In order to assess the potential impact, the ecosystems services approach (discussed in the following section) has been adopted. Evidence of the ecosystem service has been provided from the literature where possible although this has been hindered by the fact that the current study is concerned with England and Wales alone, whereas much literature relating to heathlands refers to the UK or Britain as a whole - Scotland supports 66% of the UK’s dwarf shrub heath, compared to 25% and 9% in England and Wales, respectively (Countryside Survey, 2007). Efforts have therefore been made to highlight where the data refers to Britain or the UK, as opposed to England or Wales.

3.1.2 Ecosystem services

Ecosystem services are the “benefits provided by ecosystems that contribute to making human life both possible and worth living” (Millennium Ecosystem Assessment (MA), 2005). The ecosystem approach recognises that many functions and processes underpin the interactions that occur within an ecosystem and it places humans within the ecosystem so it can consider feedback processes. The MA categorised the benefits that an ecosystem provides to humans by functionality. Four classes of ‘service’ were identified:

1. Provisioning – The products obtained from ecosystems;

2. Regulating - The benefits obtained from the regulation of ecosystem processes;

3. Supporting - Ecosystem services that are necessary for the production of all other ecosystem services;

4. Cultural - The non-material benefits people obtain from ecosystems.

The MA was a global effort to provide an assessment of the current status and trends of the world’s ecosystems. It also recognised that human well-being is situation-dependent, reflecting 47 local geography, culture and ecological circumstances. Consequently the value of a service can differ depending on the context, and what is highly valued by one person, may not necessarily have the same value to all.

In order to evaluate our own natural assets, a UK-specific assessment has been conducted - the UK National Ecosystem Assessment (NEA). This has used the MA as a framework, but some refinements have been made. Specifically, the UK NEA includes wild species diversity as both a provisioning and a cultural service, and it has identified three roles of biodiversity: 1) that involved with underlying processes (e.g. nutrient cycling and decomposition); 2) the physical provision of genes and species; and 3) the provision of wildlife and scenic places which are appreciated by humans. The UK NEA also separates out the underpinning natural and social processes (primary and intermediate processes) from the outputs from ecosystems from which people benefit. Consequently, the MA’s supporting services are assumed where another service occurs, as it is not possible to receive the final service without the underpinning, ‘supporting’ service.

Another aspect of the ecosystem services approach is to consider what the drivers of change are, how these may impact on an ecosystem, and therefore what policy intervention is required to ensure that any trade-offs optimise the positive ecosystem services. The approach also allows provides a framework for the valuation of services, but such quantitative measures are beyond the scope of this study.

Infection by Phytophthora is a driver of change that has not previously been evaluated. The aim of this section of the study was therefore to identify the range of ecosystem services provided by heathland in the UK and to describe, in broad terms, the likely impact of the loss of those services. An awareness of these services will inform future research into Phytophthora disease control options, which may in turn take a more quantitative approach to measuring the impact of disease management on heathland ecosystem services.

3.2 ECOSYSTEM SERVICES FROM HEATHLAND

The following is a list of ecosystem services attributed to, or strongly affected by heathland ecosystems in the UK. On the whole, the categories conform to those used in the UK National Ecosystem Assessment Draft Assessment, 18 October 2010. It should be emphasised that this is a broad, qualitative assessment and no attempt has been made to quantify the services identified or the results of their loss. It is also assumed that an overall aim is to maintain heathland and that the natural succession to woodland will be prevented.

3.2.1 Provisioning services 3.2.1.1 Food

Heathland is used for extensive livestock grazing, although the most commercially important livestock are now kept on more intensively managed grazing land. Therefore, the overall economic importance of heathland as a grazing resource is slight (Natural England, 2010). There is likely to be a proportionally greater impact on the upland farmer who is more dependent on heathlands, although loss of particular species (e.g. Vaccinium spp.) will have a limited effect on grazing, as other species could recolonise the land, such as Molina, which is actually more palatable to summer-grazing cattle (Anon, 2007). However, the impact of large-scale clearance to eradicate diseased material will prevent grazing taking place until re-vegetation has occurred. In the total absence of grazing, re-vegetation by heather can occur within 2 - 6 years although it can take longer (Imeson, 1971; Evans, 2005) and a seed bank must be available, thus any long-term impact on grazing is likely to be negligible. Commercial harvest of bilberries still occurs in the UK, although at a very small scale. Sanderson & Prendergast (2002) estimated that bilberry sales represented at least £10,000 in Shropshire. Harvesting of bilberries for personal consumption is still common practice throughout England and Wales (and Scotland). Some of the harvest could provide a commercial income if it is turned into 48 jam or pies which are then sold in cafes etc. There is no published literature on this, but an internet search provided some evidence (e.g. Stiperstones Inn, Shropshire; Goetre Farm Preserves, Gwynedd; The Whortleberry Tearoom, Somerset). Phytophthora infection would have some negative impact on these businesses and personal consumption, but as the bilberry is not the main source of income/food, the impact is unlikely to be significant (but see cultural services). Heathland species provide a resource for insect pollinators, including the honey bee. Therefore, honey is an indirect food product of heathland ecosystems. The value of honey production from all habitats is estimated to be between £10 and £35 million per year (National Audit Office, 2009). The Chainbridge Honey Farm in the Borders sells heather honey, but also uses the beeswax to make and sell candles, polishes and lip balms. Heather is clearly required for heather honey, but other honey is made using different flowers at times of the year when heather is not in flower; the by- products of the honey production are also not heather-specific. Similar products are made in Wales (e.g. Newquay Honey Farm) which also has a meadery. At present, Calluna is not infected in the wild, and other pollen could be used to make honey.

Heather is also an essential ingredient of a beer called Heather Ale, although this is currently brewed in Scotland rather than England or Wales. Similarly, deer are common in Scotland, but not in England or Wales.

Grouse shooting underpins the maintenance and restoration of many moorlands, but these benefits are considered under cultural services as a form of recreation, rather than as a form of food production per se. The localised, small nature of some of the businesses associated with heathlands means that the impact of Phytophthora infection could be significant to a small number of individuals which could have knock-on effects within the community where opportunities for employment are limited.

3.2.1.2 Fibre Heathland provides few fibre products although cut heather has been used in moorland restoration projects as a material to block grips (Armstrong et al., 2009). Tucker (2003) reports that “Cuttings can also be baled and in some cases sold for mulch (e.g. to restore burnt or eroded areas) and filtration uses” although no supporting information was supplied. Sheep wool is another potential fibre resulting from heathlands, but it is a by-product of the meat industry and it does not rely on bilberry or heather for production. The role of heathlands in producing fibre is negligible.

3.2.1.3 Energy

Some small-scale peat cutting still takes place in wetland regions to provide fuel. However, its use is strongly discouraged by conservation groups due to the associated habitat destruction and carbon dioxide emissions. The use of peat for fuel is of negligible importance to the UK economy or energy supply (MacLeay et al., 2009). Due to the economics of grouse shooting, it is unlikely that peat cutting would be common on heathlands. Damage to Vaccinium species is unlikely to have a significant impact on the supply or use of peat.

3.2.1.4 Drinking water

Upland areas of the UK, by their very nature, are typified by high rainfall. Consequently, the uplands provide 70% of the UK’s drinking water (UK NEA, 2010), although this figure does include Scotland, and it is likely to be lower for England and Wales alone. The Peak District National Park alone holds 55 reservoirs serving large conurbations (Anon, 2009); Wales has large reservoirs such as the Elan and Vrynwy, as well as many other medium and small reservoirs. Assuming that Phytophthora-infected bilberry is replaced with another form of vegetation, this change in vegetation is unlikely to have an impact on the provision on the quantity of drinking water. Work in

49 Denmark has demonstrated that the destruction of heather due to beetle infestation did not have any lasting impact (after 4 years) on the water balance as the area was re-vegetated (Ladekarl, 2001) (water quality is discussed in section 3.4.2.2).

3.2.1.5 Wild Species diversity

Genetic resources include the use of species for plant breeding or biotechnology. Both V. myrtillus and V. vitis-idaea are classed as crop wild relatives (CWRs) which have the potential to be used in plant breeding (Defra, 2010). No other information was found indicating that heathland could provide any other genetic resources at present.

3.2.1.6 Natural pharmaceuticals

Bilberry berries and leaves contain high amounts of phenolic compounds, and bilberries contain exceptionally high amounts of anthocyanins which have powerful antioxidant capacity (Hohtola, 2010). It is reported that Europeans have used both the leaves and the berries for health benefits for hundreds of years (e.g. University of Maryland Medical Center), and bilberry tea, tinctures and extracts are currently available on the market. The Defra-funded study “The Exploitation of Upland Plant Species in the UK as a Feedstock for Novel Conversion to Pharmaceuticals” identified both heather and bilberry as potential sources of polyphenolic compounds that could, in theory, be used to make high-value pharmaceuticals. However, the same project indicated that the economics of commercialising bilberry production for such uses were not favourable, and that the optimum time for heather harvesting for flavanoids would coincide with the shooting season. Heathlands currently provide negligible natural pharmaceutical ecosystem services, and other natural products such as green tea are more commonly used for the extraction of flavanoids, thus it is likely that the status quo will remain in the future.

3.2.2 Regulating services 3.2.2.1 Pollution control - Air quality

Heathlands have a relatively limited role in regulating air quality and they can have an adverse impact during times of burning. Burning is used as a management tool to create a mosaic of different ages and structures of heather to create a habitat supportive of grouse. The legal burning period in the UK runs from 1 October to 15 April (Davies et al., 2009) and approximately 4 per cent of heathland is burned annually over a 15–20 year rotation (Chapman et al., 2009). Yallop et al., (2006) similarly reported that in 2000, 17% of heathlands had been burnt in England over the last 4 years. Burning can release polycyclic aromatic hydrocarbons (PAHs), but the quantity is not known and is likely to be insignificant compared to other sources (European Commission, 2001). 3.2.2.2 Pollution control - Water quality

Anthropogenic inputs of agro- and other chemicals to an ecosystem often impact on water quality. In heathlands, external pollutants are primarily derived from the atmosphere (with the exception of asulam for bracken control), although naturally occurring compounds can still be a pollutant. Heathlands offer some buffering capacity to atmospheric inputs of pollutants such as nitrogen, retaining them within the ecosystem (Hardtle et al., 2007). Calluna biomass initially increases with N inputs, although in the long term, grasses can dominate (Terry et al., 2004). Dissolved and particulate organic carbon are significant components of the carbon cycle in upland peat (Worral et al., 2003) which has implications for climate regulation (see below). However, it also has implications for water quality. Dissolved organic carbon (including humic substances) gives the water a distinctive, brown colour, which is often termed ‘peaty’. There is a limit to the amount of

50 colour allowed in drinking water in order to comply with regulations, hence it must be removed at treatment works and this process can result in the production of carcinogenic trihalomethanes (Uyguner et al., 2004). On the whole, burning leads to a marginal increase in loss of nutrients in water (e.g. Pilkington et al., 2007; Niemeyer et al., 2005) and dissolved organic carbon (over 40 years) (Clutterbuck & Yallop, 2010), although Clay et al. (2010) did not find any significant increase in DOC after 10 years from burnt areas, although there were flushes of DOC loss immediately following burning.

Compared to other ecosystems, heathlands have relatively little adverse impact on water quality. Burning as a means of infection-control, could have a short-term adverse impact on water quality, but, assuming infected-bilberry is replaced by other vegetation (and so preventing erosion and sedimentation of water), the impact of Phytophthora on water quality is negligible, with the exception that the Phytophthora itself can pollute water courses which can be transported to previously uninfected areas. 3.2.2.3 Climate

Climate regulation is an important ecosystem service provided by heathlands in that the vegetation cover protects the underlying soil which, amongst other functions, is a store of carbon1. The importance of this service will be greater where the underlying soil is peat. The restoration of peat areas can almost halve the export of carbon and dissolved organic carbon (Waddington et al., 2008; Wallage et al., 2006), thus it can be inferred that protecting the peat will reduce carbon losses. Gully erosion not only entails primary removal of particulate carbon from peatland systems, but also has secondary effects in that it enhances drainage and lowers water tables, potentially enhancing decomposition of surface peats (Evans & Lindsay, 2010) further highlighting the role of soil protection in reducing carbon losses.

Nitrous oxide is a more potent greenhouse gas than carbon dioxide and it is released from soils (particularly after fertilisation, and from urine patches), but it can also be released from peat. Although nitrous oxide losses are higher from drained peat than form intact peat, there is no indication that overall emissions will be greater from naturally drier peat (that could occur where there are bare areas) although insufficient work has been conducted to have confidence in the findings (Bussell et al., 2010).

Burning will clearly lead to a direct loss of carbon to the atmosphere, although there can be subsequent losses associated with soil erosion as well. Farage et al. (2009) used measured data with modelling to predict the carbon loss from moorland in the Yorkshire Dales burnt over 15-20 years and they calculated that < 10% of the total carbon storage would be lost. Worral et al (2010) also demonstrated the high probability of burning resulting in a net carbon loss from peat.

Assuming that no large scale erosion occurs during the period of re-vegetation if there are vegetative losses due to Phytophthora, the long-term impact is likely to be negligible. There is the possibility that greater amounts of carbon could be stored if grasses replace bilberry, as Molina, Nardus and Agrostis-Festuca have a higher dry matter biomass per metre squared than bilberry (Milne et al., 2002), although a further feedback mechanism could be increased grazing due to the enhanced palatability, with the subsequent potential for erosion, but research would be needed to confirm these hypotheses. Burning as a form of Phytophthora control will have the same impact as burning heather as discussed above.

Soil quality underpins the processes discussed above in sections 3.4.2.1, 3.4.2.2, and 3.4.2.3 thus the evidence is not repeated further.

1 Although the importance of the UK’s peatlands in carbon storage is frequently reported, it must be remembered that 75% of the UK’s soil organic carbon is in Scottish peat (Howard et al., 1995), thus storage in England and Wales is far less than implied by ‘UK’ storage. 51 3.2.2.4 Hazard regulation Heathland is not known to provide particular protection against natural hazards, having little resistance to wind and being susceptible to fire during dry periods. The fire-risk may be exacerbated by the accessible nature of many heathlands for recreation. Research on mitigating the economic loss by fire in uplands is currently on-going (http://www.fireman-europe.com). Some heathlands can contribute to flood regulation, and by similar means, soil erosion, particularly where previously-drained areas are in-filled. The blocking of drains in The Exmoor Mires Restoration Project has also reduced flooding downstream. Wilson et al. (2010) blocked drains in the Lake Vrynwy catchment which resulted in an increase in the water table. In turn, this caused an increase in surface water during rain events, but, it did not lead to greater discharge in the streams which they proposed could have been due to a reduced connectivity. However, other work has demonstrated no benefits of upland areas in reducing flooding (Anon, 2009). The role of heathlands in regulating against flooding is therefore site-specific. Although reservoirs can serve to regulate flows, these are not part of heathland per se. Assuming, re-vegetation occurs, the impact of Phytophthora on this ecosystem service is likely to be negligible.

3.2.2.5 Disease & pests

On the whole, the role of heathlands in regulating disease and pests is of low importance. It is possible that heathland provides a barrier between arable fields reducing the potential spread of pathogens between crops, but this service may also be provided other ecosystems with species compositions different from adjacent cropping systems. However, the relatively uniform biodiversity of heathland and the susceptibility of its dominant plant species to Phytophthora make heathland an ineffective system for disease regulation. Heathlands are also a habitat for ticks, which can infect humans with Lyme borreliosis. A variety of vegetation can support ticks thus the replacement of Phytophthora-infected vegetation with other vegetation is unlikely to reduce the tick population. 3.2.2.6 Noise

The importance of heathlands in regulating noise is low (UK NEA, 2010) and this service is unlikely to be affected by Phytophthora. 3.2.2.7 Pollination

The role of heathland in providing a habitat for pollinator species is discussed in section 2. Whilst the production of heather honey is dependent with heathlands, Calluna is in flower for only a few weeks of the year, and the bees are transported to the heather, i.e. these bees do not play a significant role in pollination of crops or wild flowers.

3.2.3 Cultural Services 3.2.3.1 Aesthetic and inspiration

Interest from conservation groups and tourists, as well as direct research (White & Lovett, 1999), indicate that upland heathland has considerable aesthetic appeal.2 This is exemplified by the number of organisations, or networks that exist in order to support heathlands and uplands (e.g. The Heather Trust, Moorland Association, Moors for the Future, IUCN UK Peatland Programme, The Heathland Conservation Society).

2 It is important to note that the aesthetic appeal of habitats, and the acceptance of the present appearance of habitats, may depend on knowledge of how the appearance of habitats has changed over time (Hanley, 2009).

52 It is the aesthetics of heathlands that underpin recreation and tourism, as well as inspiration. Heathland is the subject of many paintings (from personal observation) and reference is made to heather in the literature. For example “the purple-headed mountain” in the classic hymn, “All Things Bright and Beautiful”; “High Waving Heather” by Emily Bronte; “Heatherland and Bent Land” by Wilfrid Gibson.

3.2.3.2 Recreation & tourism

In England and Wales, grouse shooting is one of the major sources of income provided by heathlands. The Moorland Association reports that: In England and Wales there are about 149 estates where grouse shooting occurs and Moorland Association members pay £52.5 million a year to manage their moors. [This figure excludes owners not in the Moorland Association, and it is not the full worth of shooting]. In a typical year 1,235 days shooting will occur in England and Wales and an average of 30 people are employed per day to help run the shoot on each moor resulting in 37,050 extra casual days of labour. Moorland contractors are paid for a further 5,470 further days work outside of the shooting season from a whole host of trades that benefit from the grouse industry including e.g. for heather re-seeding, bracken control, moorland track construction and/ or maintenance. Accommodation providers in the immediate vicinity to the moors also benefit, and over 6,500 bed-nights can be booked in one season. If Molinia is the dominant vegetation type replacing the bilberry, then this could have a negative impact on shooting as there is negative correlation between red grouse and Molina cover (Anon, 2007). Many heathlands are found in National Parks. In those Parks typified by expanses of heathland such as the North York Moors, Northumberland and Peak District, annual spend, in millions, was £317, £104, and £97 respectively in 2010 with a total number of visitors for these Parks of 18.1 million per year (State of the Countryside, 2010). Research has shown some willingness to pay more for recreation in heathland ecosystems in the UK (White & Lovett, 1999). Despite the economic importance on recreation and tourism, habitats can become damaged as a result of this service (Sun & Walsh, 1998). The collection of bilberries as a recreational activity could have greater value to individuals than bilberries as a food source. It is the entire process of being in the outdoors, socialising with, or escaping from others, and the satisfaction of picking the berries which contributes to positive well- being. Phytophthora infection could clearly have a significant impact on this activity.

3.2.3.3 Knowledge & education

Heathland has a potential use in general biology and ecology education and it underpins our current understanding of the habitat, as discussed in previous chapters. Areas underlain by peat can hold knowledge of paleo-archaeological significance, and physical records of the historical management of heathlands provide information regarding our social, agricultural, and environmental history. There is also knowledge associated with the management techniques specific to moors such as burning, and the dynamics of grouse populations.

3.2.3.4 Spiritual and religious

Heathland conservation is generally portrayed as a good thing regardless of its social and material benefits. However, this assertion does not appear to be associated with any particular religious or spiritual belief.

53 3.2.3.5 Cultural heritage & sense of place

Heathland is a relatively rare habitat characteristic of northern and western Europe, but with many fine examples in the UK. It has a very distinctive colour and structure and defines specific areas, as illustrated in paintings and postcards etc. The management of the remaining heathland area may contribute to the diversity of cultures in the UK by maintaining traditional activities and settlements. The various names given to Vaccinium myrtillus illustrate the role of this plant in cultural identity. It is known as whortleberry (worts, hurts or urts) in the south, whinberry (winberry or wimberry) in the west (Wales, Shropshire), bilberry in the north, blaeberry in Scotland and Fraughn in Ireland. Bilberry is the county flower of Leeds, as it is “a symbol of the open air of the hills, especially around Leeds, where the plant will be forever associated with the novels and poetry of the Bronte sisters” (Plantlife.org.uk, 2011); Calluna vulgaris is the county flower of Staffordshire.

3.3 DISCUSSION

In the sections above it is assumed that any Phytophthora-infected bilberry is replaced by other vegetation such as Calluna, Molinia, Nardus or other grasses within a few years, and at no time is there any great expanse of bare soil. This is a reasonable assumption from the available literature (Imeson, 1971; Rawes & Hobbs, 1979; Evans, 2006; Anon, 2007) although for the regeneration of Calluna in particular, there must be an available seed bank. There is also the assumption that large areas of heathland are not infected, given that bilberry is often, although not always, interspersed with Calluna. In effect this means that bilberry is surrounded by non-infected Calluna which can colonise the area when the infected vegetation is removed, so, at any one time, there are no large expanses of bare soil. If the control of Phytophthora requires the removal of large expanses of vegetation there is risk of soil erosion which will adversely impact on water quality (sediment, colour, nutrients), it could enhance the risk of flooding downstream, the peat could dry out which enhances runoff and fire risk, and there will be a loss of carbon. This situation will also clearly have a negative impact on cultural services. With the exception of wild species diversity, heather honey production and the consumption of bilberries, the regulating and provisioning services provided by heathlands could be provided by other vegetation types, and protecting the soil underpins the provision of these services. However, cultural services could be severely affected. Heathland is a characteristic habitat of northern Europe and has been a feature of the UK landscape for around 6000 years. It currently has considerable aesthetic appeal and historical importance. The cultural services provided by heathland are most obvious in the form of tourism and recreation. Walking, cycling, and other outdoor activities attract visitors and tourist revenue. Heathland is also a major habitat for game shooting, and a key quarry species, the red grouse, is dependent on heather as a food plant. Therefore, cultural services in general, and tourism in particular, can be considered the most important ecosystem service provided by heathland. As these services are heavily dependent on appearance and access, they are also the services most likely to be affected by Phytophthora infection. Loss of characteristic species may deter visitors and more widespread loss of vegetation will reduce the appeal of heathland still further. Restrictions on movement or other activities imposed to contain the disease would also reduce the desirability of tourism in heathland habitats. These effects may persist even if vegetation recovers as the reputation of heathland as a recreation venue remains damaged. The value of the impact of Phytophthora on ecosystem services could depend on the proximity of the valuer to the heathlands. Whilst heathlands may not provide a large source of income for recreation or food in the context of England and Wales as a whole, they may be crucial to the economic survival of those who work with, and within the evirons of heathlands. Employment in such areas is commonly limited and any adverse impact on heathlands due to Phytophthora could have knock-on effects within the community. 54 The extent of the impact of Phytophthora on ecosystem services will depend on the extent of the spread amongst Vaccinium and, whether or not it spread to Calluna in the wild. The potential impacts of the different scenarios are summarised in section 7.

55 4. IMPACT ON ERICACEOUS HOST SPECIES

4.1 INTRODUCTION

The potential impact of Phytophthora on heath species will depend on the host species’ distribution and the spread of the disease. The spread of the disease will depend on the distribution of all host species that are capable of sporulation. In order to assess the likely impact, distribution of the four potential host species was modelled using MaxENT. This is a niche based modelling system that predicts a target species’ realised niche within a study area and within the environmental variables being considered based on presence only data (Phillips et al., 2006). The output is a probability distribution that should be viewed as a relative index of environmental suitability (higher values mean better conditions for the target species). Phytophthora, disease models developed as part of other Defra funded work were combined with MaxENT models to estimate the potential impact of the disease on host species. The Metapopulation Epidemic Model (MPEM) is a modelling package that outputs GIS compatible files showing the disease landscape (including risk of spread maps and likely areas to be infected in a given time period) and disease progress curves. The model requires information on the host landscape and characteristics of the disease. Users can also include disease control options and information on detection.

4.2 HOST MAPPING

4.2.1 Methods

4.2.1.1 Summary of MaxENT Modelling

Each cell/pixel (in this case each 1 km grid square) within the study area is assigned a probability of suitability for the species being modelled. The probability is derived from the probability distribution with greatest entropy (closest to uniform). However, this probability does not relate to the ‘amount’ or area that the species is predicted to cover within each cell. In order to get some estimate of this, data from LCM2000 was incorporated to remove areas of unsuitable habitat from the prediction (as suggested in Phillips et al., 2006).

Within each 1 km cell, all areas that are deemed to have ecologically suitable habitat for the target species will be summed. This will give the total amount of available habitat within cells, or the ‘potential area affected’ by Phytophthora, in each 1 km cell.

4.2.1.2 GIS Methods

The distribution of potential host species for Phytophthora will affect the spread of the disease across England and Wales. In order to model the predicted spread of host plant species key variables must be created and converted in to ASCII format to enable use in MaxENT. The following section contains details of the data processing used to create the necessary variables. Climate data Climate data was extracted from the UKCIP dataset on a 5 km scale. It was decided to focus on average maximum temperature, average minimum temperature and total rainfall across all the quarters of 2001-2006. As there were varying conditions across those years, it was felt that this was an adequate representation of climate for the UK. Using these, results in 72 climate variables to consider (6 years * 4 quarters * 3 climate variables) for 10359 25 km grid cells across the UK.

56 Principal component analysis (PCA) was used to find patterns in the data such that the variation in the 72 climate variables can be described using just n (<<72) variables. The data was first standardised by subtracting the mean for each variable from the corresponding part of the data vector and dividing that same part by the standard deviation.

The first six principal components from the PCA explain 96.5% of the variance in the standardised dataset, with the first four accounting for nearly 94% of the variance. There is some interpretation for the principal components. Plotting principal component (PC) 1 against PC2 for the 10 359 locations shows there is little correlation between the two inputs. For PC1, there is a clear divide in the influence of temperature and precipitation, and, for PC2, there is a divide between the influence of maximum Q2 and Q3 temperatures and the other outputs.

It was decided to use the first six principal components (PCs) processed in ArcMAP 10 as outlined below. In Table 14 the reasons for the first six principal components being relatively high or low for any particular grid cell are highlighted.

The PCs and their corresponding coordinates were imported into ArcMAP10 to create a point shapefile. This shapefile was spatially joined to a 5 km grid and a 5 km raster created for each of the six PCs. The raster was resampled to a 1 km scale. The value of each 5 km square was assigned to the 1 km squares it was split into. These rasters were multiplied (using the raster calculator) by a second raster which contained a value of ‘1’ over England, Scotland and Wales and ‘No Data’ values over areas of sea. This resulted in a calculation layer containing data in each raster cell over England, Scotland and Wales only. The six resulting calculation rasters were converted into ASCI layers to enable their use in MaxENT.

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Table 14 Details of principal components derived from the PCA of climate variables.

Principal Reasons for negative values Reasons for positive values component PC1 High precipitation throughout year. Low precipitation throughout year. Low temperatures throughout year. High temperatures throughout year. PC2 High maximum daily temperature over Q2 Low maximum daily temperature over Q2 and Q3. and Q3. Low minimum temperatures over Q1 and Q4. High minimum temperatures over Q1 and Q4. High precipitation throughout year.

Could be interpreted as having defined Could be interpreted as having less seasons; that is, warm/hot summers and cold extreme changes in temperature over the winters. year. PC3 High minimum temperatures throughout the Low minimum temperatures throughout the year. year. Low maximum temperatures over Q2 and High maximum temperatures over Q2 and Q3. Q3. Low precipitation throughout the year. High precipitation throughout the year. High minimums and low maximums, means Here more variability in temperature over less variability in temperature is experienced summer is experienced. over the Q2 and Q3 periods. PC4 High values for observations from 2003 to Low values for observations from 2003 to 2006. 2006. Low values for observations from 2001 to High values for observations from 2001 to 2002. 2002. PC5 Low values for maximum temperatures in Q1. High values for maximum temperatures in Q1. High values for minimum temperatures and Low values for minimum temperatures and precipitation in Q3. precipitation in Q3. PC6 High values for Q1 and Q4 precipitation. Low values for Q1 and Q4 precipitation. No other clear trends. No other clear trends. Note that all the highs and lows here are relative to the range of climatic conditions that were experienced over the UK in the years 2001 to 2006.

Processing land cover map 2000 (LCM2000)

The distribution of potential host species for Phytophthora will affect the spread of the disease across England and Wales. In order to model the predicted distribution of host plant species such as Vaccinium, key habitats from the LCM must be converted in to ASCII format to enable use in MaxENT.

A set of rasters were produced with a cell size of 1x1 km covering England, Wales and Scotland. Creation of the rasters followed the process as outlined below:

• The relevant land class was extracted from the LCM2000 using ‘select by attribute’ and ‘export data’.

58 • The extracted land class was overlayed with a 1x1 km grid covering England, Scotland and Wales, using the ‘Intersect’ tool. • This intersected layer was then ‘dissolved’, based on the 1x1 km grid id code, to create multi part features. • The areas of these multipart features were calculated. • The data was then opened in MS Excel 2007 and the total area in each 1 km cell was calculated. Some of these areas were greater than 100 ha due to overlapping polygons in the LCM2000 dataset. To overcome this problem, the relative proportion of each landclass considered was calculated. For squares with areas greater than 100ha the following calculation was used: Original area (ha)/original sum (ha) * 100

• For squares with less than 100 ha the formula below was used (this was used as in certain squares, only 0.1% of land was contained in the selected classifiers. Using the equation above would suggest that a greater proportion of the 100ha was covered by this 0.1% than was true in reality): Original area (ha)/100 (ha) * 100)

• Once areas had been calculated the dissolved layer was joined to the respective grid, based on the grid ID code (FID) of the 1x1 km grid • The shapefile created in the previous step was used to create a raster with a cell size of 1 km which was multiplied (using the raster calculator) by a second raster that contained ‘1’ values over England, Scotland and Wales and ‘No Data’ values over areas of sea. This resulted in a calculation layer containing the area of the extracted land class in each raster cell over England, Scotland and Wales only • This calculated raster was converted to an ASCII file to enable its use in MaxENT modelling

Corine soil data

Soil type was assessed as important to establishment of host plants as it would directly affect the areas certain species could grow in.

• Data for England, Scotland and Wales was extracted from the Corine Soil Database raster. • This raster was then resampled to show the major soil group code from the 1990 FAO- UNESCO soil legend. • The raster was multiplied by a second raster which contained ‘1’ values over England, Scotland and Wales and ‘No Data’ values over areas of sea. This resulted in a calculation layer containing the soil class in each raster cell over England, Scotland and Wales only. • This calculated raster was converted to an ASCII file to enable its use in MaxENT modelling.

Land-form Panorama data

• The Panorama height raster was re-processed to a 1 km square resolution (from 50 m squares) using the aggregate tool in ArcMAP. Rasters of maximum, minimum and mean height across England, Scotland and Wales were produced in this way.

59 • The ‘slope’ and ‘aspect’ tools in ArcMAP10 were used to create slope and aspect rasters from the original height raster. • These slope and aspect rasters were then re-processed using the aggregate tools to a 1 km scale. • The five resulting rasters were then multiplied (using the raster calculator) by a second raster which contained ‘1’ values over England, Scotland and Wales and ‘No Data’ values over areas of sea. This resulted in a calculation layers containing mean, maximum, minimum heights and slope and aspect values in each raster cell over England, Scotland and Wales only. • These calculated rasters were converted to an ASCII file to enable their use in MaxENT modelling.

4.2.1.3 Modelling Inputs

Data of known presence points for all four potential host species was extracted from the National Biodiversity Network (NBN). Data from all habitats were included, however since the data as a whole do not represent systematic sampling of either habitats or geographic regions, there may be underrepresentation of some habitats or areas in the dataset. Only data with a resolution of 1 km or better were included. Although this excludes data collected at the 2 km scale, the greater precision was considered important. Data from 1980 onwards were used in order to increase the number of presence records. NBN data at a 1 km resolution or better came from a range of data sources including the Botanical Society of the British Isles, the Royal Horticultural Society, the Joint Nature Conservation Committee, Scottish Natural Heritage, local biodiversity records centres, wildlife trusts, national parks, local government ecology units, individuals and some commercial businesses.

All data extracted from Section 4.2.1.2 were supplied to all models (Table 15). The data was randomly split by the MaxENT model, with 70% of the data used for training the model and 30% used to test. One model was created for each host species and associated response curves and model performance statistics were produced.

AUC scores were used as an assessment of model performance. They are usually a number between 0 and 1 however, in the case of MaxENT modelling the maximum AUC possible is just less than 1 (see Phillips et al., 2006 for details). Higher scoring models are better at predicting the species distribution. Scores of 0.6 – 0.7 = poor, 0.7 – 0.8 = average, 0.8 – 0.9 = good and 0.9 – 1 = excellent (Araujo & Guisan, 2006).

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Table 15 Environmental variables included in the MaxENT modelling.

Source Variable in model Explanation PC1 Value of principal component 1 from the climate PCA PC2 Value of principal component 2 from the climate PCA

Climate Data PC3 Value of principal component 3 from the climate PCA - UKCP PC4 Value of principal component 4 from the climate PCA PC5 Value of principal component 5 from the climate PCA PC6 Value of principal component 6 from the climate PCA Acid Grassland Area of acid grassland within each 1 km square Arable Area of arable land within each 1 km square Bare Ground Area of bare ground within each 1 km square Bog Area of bog within each 1 km square Bracken Area of bracken within each 1 km square Broadleaved / Mixed Area of broadleaved/mixed woodland within each 1 km Woodland square Coniferous Woodland Area of coniferous woodland within each 1 km square Dwarf Shrub Heath Area of dwarf shrub heath within each 1 km square Fen Area of fen within each 1 km square

LCM2000 Urban areas and Area of urban and associated gardens within each 1 km associated gardens square Improved Grassland Area of improved grassland within each 1 km square Other Grassland Area of other grassland within each 1 km square Littoral Rock and Area of littoral rock and sediment within each 1 km square Sediment Montane Area of montane within each 1 km square Sea Area of sea within each 1 km square Supra Littoral Rock Area of supra littoral rock within each 1 km square Supra Littoral Area of supra littoral sediment within each 1 km square Sediment Water Area of water within each 1 km square Corine Soil 1 km summary raster from the Corine soil Database was Soil class Database used Maximum Elevation Maximum height within each 1 km square Mean Elevation Mean height within each 1 km square Land-form Panorama Minimum Elevation Minimum height within each 1 km square Data Aspect Mean Aspect within each 1 km square Slope Mean slope within each 1 km square

61 4.2.1.4 Refinement of MaxENT Outputs

The MaxENT output assumes that everything within each 1 km raster cell has the same probability of containing a host species. This may not be the case as only part of the cell could contain suitable habitat for the growth of a host species. To overcome this issue and in order to give a figure on the total area at risk from Phytophthora, the LCM was used to clip out suitable areas of habitat within each raster cell.

Using the values derived from the process in Section 4.2.1.2 a raster layer was produced which contained a probability of a host species being present, weighted by the amount of habitat available for that species. To do this a random raster was generated (‘random’) and the raster calculator used to create a possible landscape from the MaxENT outputs for each species using the code below:

‘random’ < ‘maxENT_output’.

This produced a raster (‘possible_host_landscape’) with 0 or 1 as cell entries, where 0 = no host and 1 = host species is present. It has the effect of pixelating the MaxENT output. A second raster was created that contained the total area at risk from Phytophthora in each 1 km cell (‘available_area’). Multiplying the ‘possible_host_landscape’ by the ‘available_land’ would create a raster with each cell containing a host being scaled down to the fraction of available land. However, this assumes the entire suitable land cover within a cell is filled with a host. Therefore, we assumed that the amount of available area actually filled is proportional to the probability of that cell containing hosts. This final raster was generated using the raster calculator and the code below:

‘possible_host_landscape’ * ‘available_area’ * ‘maxENT_output’

The suitable habitats from the LCM2000, for the four host species modelled, are listed in Table 16.

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Table 16 Selected LCM categories and the habitats used to assess the amount of land available in each 1 km square for each host species. Categories listed as ‘yes’ are included in the suitable area.

Vaccinium Vaccinium vitis- Arctostaphylos Calluna LCM category myrtillus idaea uva-ursi vulgaris Acid Grass rare rare rare Arable Bare Ground Bog yes rare yes Bracken yes possibly yes Broadleaf / Mixed Woodland yes (acid) yes (acid) Coniferous Woodland yes (acid) yes (acid) rare yes (acid) Dwarf Shrub Heath yes yes rare yes Fen Urban Areas and Associated Gardens Grass - Other rare rare rare rare Grass - Improved Littoral Rock and Sediment Montane yes yes yes yes Sea Supra Littoral Rock Supra Littoral Sediment Water

4.2.2 Results

4.2.2.1 Model Fit

All MaxENT models produced high average to excellent AUC scores (as defined by Araujo & Guisan, 2006) with a minimum test AUC of 0.79 (for C. vulgaris) to a maximum of 0.92 (for A. uva- ursi), showing the models produced good predictions of the test data set (Table 17).

Table 17 Number of presence points and associated AUC scores for the four MaxENT models.

Presence Points AUC AUC Species Used in MaxENT (train) (test) Vaccinium myrtillus 2468 0.85 0.82 Vaccinium vitis-idaea 591 0.95 0.90 Arctostaphylos uva-ursi 201 0.98 0.92 Calluna vulgaris 3212 0.81 0.79

63 The final model outputs are shown in Figure 1, Figure 2, Figure 3 and Figure 4. For each MaxENT model two sets of values (percentage contribution and permutation importance) were given that show the relative importance of each variable to the overall final model. Both these measures, which are created by the MaxENT programme, need to be interpreted carefully. Firstly, the percentage contribution makes assumptions regarding independence of presence points and variables that are violated in this dataset. Secondly, the permutation importance may permutate variables to values that are not possible within the confines of the data (e.g. may create permutations where the total area of LCM variables exceeds 100 ha). Looking at the permutation importance figures for each model gives us an idea of the impact each variable has on the model. The main variables of interest (any variable with a permutation importance of 5 or more) for each species are listed in Table 18.

Occasionally variables are seen that have a high percentage contribution but a low value for permutation importance (e.g. Maximum Elevation variable for V. vitis-idaea, percentage contribution = 24% and permutation importance = 0.1) and this is most likely due to correlations of variables in the model. The reverse is also seen, with low percentage contribution values matched with high permutation figures (e.g. broadleaved/mixed woodland variable for A. uva-ursi). This is likely due to small numbers of presence points located in cells with values for the variable in question.

Table 18 Permutation Importance and Percentage Contribution figures for each model.

Permutation Percentage Species Variable Importance Contribution Arable 17 16.8 Urban areas and Associated Gardens 12.4 2.4 Maximum Elevation 6.2 19.5 PC1 9 18.1 V. myrtillus PC5 9 5.6 PC6 5.5 5.1

Arable 6.8 6.3 Dwarf Shrub Heath 9.3 5.8 Urban areas and Associated Gardens 21.7 0.5 Improved Grassland 5.5 4.1 V. vitis idaea V. vitis idaea PC1 19.1 22.5

Arable 23.8 18.1 Broadleaved/mixed Woodland 22 1 Urban areas and Associated Gardens 6.3 11.1 A. uva-ursi A. uva-ursi Improved Grassland 19.9 5.9

Arable 20.8 28.6 Dwarf Shrub Heath 8.8 19.2 Urban areas and Associated Gardens 10 1.9 C. vulgaris C. vulgaris PC5 11.3 9.7

64 4.2.2.2 Host Maps

C. vulgaris and V. myrtillus are common species of heathland and woodland on acid soils, with C. vulgaris, in particular, present in some bog habitats. Overall, the species distribution maps for these species are similar, with high concentrations in upland areas and lowland heathland areas of southern England, although C. vulgaris is more common, particularly in lowland heathland. V. vitis- idaea is a species of upland moorland and largely coniferous woodland. Therefore, as expected, it is largely restricted to upland areas in Wales and northern England. The small number of records outside Scotland for A. uva-ursi presented difficulties for modelling the distribution. Vaccinium myrtillus Suitable areas for V. myrtillus are predicted to be in northern England and Wales with some suitability highlighted in southern England. Arable and urban areas may be excluding the species from areas with high values for these variables. PC5 and PC6 suggest the species tends to be located in areas that are not too hot during the first 3 months of the year, and not too hot or rainy from July to September and areas with low rainfalls between October and March, relative to the UK. There is a good spread of presence data across the range of all important variables and so we can have a high degree of confidence in this model.

Vaccinium vitis-idaea North west England and Wales are predicted as being suitable for V. vitis idaea. Again the presence of Dwarf Shrub in the model is to be expected. The histogram for the PC1 variable suggests the species is present in areas that are not low in precipitation levels or have high temperatures relative to those in the UK. There is not a good spread of presence points along the range of the arable variable and so the importance this variable should be viewed critically.

Arctostaphylos uva-ursi The host map predicts no suitable areas for A. uva ursi in England or Wales. This is due to the limited presence of suitable habitat in the LCM2000 in these areas. The amount of arable land seems to have a high degree of influence on the model (permutation importance = 23.8). However due to the small number of presence points, and the aggregated spread of these points, we cannot have a high degree of confidence in this model, when it is predicting outside of the spatial extent of the presence points. The sparse nature of the presence data (Figure 6) means there is little information on the effects of environmental variables across their full range of values.

Calluna vulgaris C. vulgaris is predicted to have suitable areas across Wales and the majority of England (excluding the east coast and central areas). Dwarf shrub heath is important in the model and this is to be expected as a major component of shrub heath habitats as categorised by the LCM2000 is the presence of C. vulgaris. PC5 is also important in the model. Looking at the presence points’ distribution over PC5 shows the species tends to be distributed around zero, suggesting a tendency towards locations that are not too hot during the first 3 months of the year, and not too hot or rainy from July to September.

Urban areas are also important and this could be due to the growth of heather as an ornamental plant in many areas. The arable variable is also important probably because the species would not be present on arable land and so areas containing a high degree of arable land would be less suitable for C. vulgaris. The presence of arable land in all models is most likely due to this reason. There is a good spread of presence data across the range of all important variables and so we can have a high degree of confidence in this model.

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Figure 1 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Vaccinium myrtillus.

Figure 2 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Vaccinium vitis-idaea.

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Figure 3 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Arctostaphylos uva-ursi.

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Figure 4 Maps showing the initial MaxENT Output (left), the land available according to the LCM2000 (middle) and the final host map (right) for host species Calluna vulgaris.

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4.2.2.3 Model Limitations

Despite the good AUC scores and ecologically sensible variable selection of the models, careful consideration should be used when interpreting the results. The MaxENT model does have some limitations associated with it and these need to be remembered. Firstly, MaxENT is prone to overfitting data and this especially true with the small input datasets associated with modelling rare species. This may be of importance when considering V. vitis-idaea and A. uva-ursi due to the limited number of presence points for this species. Standard practice when using MaxENT is to include all environmental variables regardless of their auto-correlation (Pearson et al., 2007, Peterson et al., 2007). However, MaxENT is better able to deal with these correlated variables than other modelling techniques (Elith et al., 2011).

There is also the problem of spatial correlation in the presence points. Having gaps in the distribution of the presence points means care must be taken when interpreting the modelling output from these ‘gap’ regions as no information is available on the species responses to variables in these regions. This is the case for A. uva-ursi and V. vitis-idaea, where most or all of the species presence points are located in Scotland, with few in England and Wales. There are differences between the input variables between the two regions (Figure 5), and despite some degree of overlap this means the modelled outputs for England and Wales should be interpreted critically. This issue effects all species modelled to a lesser extent, as gaps in species presence points can be seen (Figure 6).

Finally, the area of suitable habitat (as listed in Table 16) is taken from the LCM2000. We have assumed this dataset to be complete and accurate, however this may not be the case. The only way to improve this assumption is to improve the data available for the land use inputs. This could potentially come from the LCM2007 (when available) since this will be more accurate than LCM2000. In Wales, the new ‘Habitat Inventory for Wales’ is a full inventory derived from remote sensing, that is due for completion in 2012 (http://www.gwylio.org.uk/). This work will produce detailed map data of over 100 semi-natural vegetation communities across Wales and, in addition, is able to distinguish between heath dominated by V. myrtillus and C. vulgaris. However, there is no comparable inventory data set for England or Scotland and so, if this dataset was used, Wales would have to be modelled separately (perhaps not possible due to the distribution of presence points). However, this data set could be used to validate the current models in Wales.

Figure 5 Extracted principal component values for climate variable PCs 1 and 2, across England & Wales and Scotland. The proportion of cells at each PC value shows large differences between the two regions

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Figure 6 Presence point locations used in the MaxENT modelling for all four species.

72 4.3 RISK SCENARIOS

4.3.1 Methods

4.3.1.1 MPEM

The user defined parameters and associated assumptions in the model are shown in Table 19. For our purposes no control options were included as the effectiveness of current controls is not known. The model also assumes no mortality at infected locations, it simply states that infection is there and does not consider how long an area may be infected for. Therefore, this project takes a highly conservative approach to the impacts of Phytophthora.

To get a final risk value, the locations variable was multiplied by the probability of the disease spreading to the 'original cell' from its current locations. The location variable was weighted by the probability of spread. This enabled the risk map to account for situations where the location figure was high, but there was little to no probability of Phytophthora reaching the area in the next 20 years.

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Table 19 Parameters and associated assumptions in the MPEM model1.

Variable Assumptions Simulation settings The number of hosts can be grouped into discrete units of the (including time period to metapopulation level. The more bins used the closer to the use and maximum number natural state of the system and less important this assumption of hosts possible per becomes location) Landscape Data Assumes that all hosts with the greatest sporulation hazard have been included Kernel Data (dispersal Assuming that the canopy level spread in the UK is similar to data) that observed in California Rate parameters (rate of Assuming that the infection rate is higher than that in spread) California, based upon manual history matching of the current Master File state of larch infections in the UK Data Output Output shows the exact state of the simulation and so assumes 100% detection and surveillance Detection and Control When used, detection uses a non-linear detection probability Interventions response function. This means that the more hosts that are infected in a region the greater the chance of detection. The current control is removal of stands and in the simulation the removal is assumed to be 100% effective Host Density We assume that we can approximate this host density from large scale datasets such as the Woodland sub compartment database and the LCM clipped - MaxEnt models for the host species modelled at Fera Susceptible We assume that all hosts are initially susceptible unless they are previously detected as having infection Exposed Initially assumed to be zero Essential Infected Initially only infected at sites known from inspection/ surveillance Detectable Initially assumed to be zero Removed Initially assumed to be zero

Kernel Assuming that the canopy level spread in the UK is similar to that observed in California Infectivity Assuming the wild infectivity is similar to measured temperature and moisture response from lab trials Susceptibility Currently assuming only proportional to host density - although with new lab data from FERA this can be tied to the environmental conditions Detection: Search Random initial survey with intense survey around detected

Optional infection sites Detection: Known known actual infection data is seeded into the initial conditions to begin the simulation Spray (antisporulant state) That such a spray exists and could be sprayed across the wild environment Spray (Protectant state) That such a spray exists and could be sprayed across the wild environment 1 Assumptions supplied by Erik DeSimone of the MPEM team. 74 4.3.1.2 Final Host Map

The LCM2000 clipped MaxENT outputs created in Section 4.2.1.4, were passed to the MPEM team. MaxENT models of V. myrtillus, V. vitis-idaea, A. uva-ursi and Rhododendron ponticum were included in the final host map. C. vulgaris was excluded because there are no records of infection in the wild. Also, it has not been shown to sporulate in the laboratory, therefore could not be included in the model. The rasters were then combined into one final host map that incorporated the MaxENT modelled species, the distribution of larch (from the sub-compartment database) and the National inventory of Woodland and Trees (NIWT). These two additional datasets may lead to a double counting of larch, however, the NIWT is included purely as a “low level fill for unknown possible sporulation” and so any double counting would have very little impact on the final risk maps.

4.3.1.3 MPEM Modelling

The MPEM model was run for a 20 year simulation with no Phytophthora control measures. The model outputs two raster files i) a hazard map, which which details the number of new locations at risk and ii) a map that shows the probability of the disease spreading from its current locations. The ‘location’ value is the number of additional cells that could be infected by a Phytophthora outbreak starting in the 'original cell' that contains the location value. At this stage the model looks at each 1 km2 cell in turn, and assumes the disease has managed to reach that cell. It asks 'how much further could the disease spread if it reaches this point?'.

4.3.2 Results

4.3.2.1 Final Host Map

The final host map was created as part of the MPEM modelling process including MaxENT models produced for this study (Figure 7).

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Figure 7 Final host map created by incorporating MaxENT modelled species with the NIWT and Forestry Commission sub-compartment database for larch

4.3.2.2 Risk Maps

Locations of wild Phytophthora ramorum and Phytophthora kernoviae outbreaks as of December 2010 were used to seed the MPEM model (Figure 8). Information regarding outbreaks on larch was sourced from the Forestry Commission, whilst data on outbreaks on other species was sourced from Fera.

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Figure 8 Locations of wild outbreaks of P. ramorum and P. kernoviae used in the MPEM model. The two outputted raster files described in section 4.2.1.3 are shown in Figure 9. High probabilities of Phytophthora spread from its current locations can be seen in Southern Wales (Breacon Beacons and Crychan Forest), Northern Wales (Dovey Forest), the Lake District (Grizedale Forest), New Forest and St. Leonards Forest in the South of England and Cornwall. All these areas also show a degree of hazard indicating that should the disease reach these areas, it will be capable of spreading further and infecting new 1 km2 areas. a) b)

Figure 9 Outputs from the MPEM model. a) = probability of Phytophthora spreading from the current locations in the next 20 years, b) = hazard map, showing the locations or number of extra 1 km2 cells that would be at risk assuming the disease had reached all cells of the map. 77 4.3.2.3 Risk Scenarios

The three risk scenarios were developed using the full host map and the MPEM outputs. These scenarios were later refined to be specific for each species by using the individual host maps for the four species to be considered (Section 4.3.2.4). Risk scenario 1, shows the situation should all possible hosts become infected whilst scenario 3 shows the current situation (Figure 10). Scenario 2 shows the full 20 year spread as predicted by the MPEM. The raw output from the model suggests about half of England and Wales is at risk (see Appendix 2) however, most cells in this area had a value of less than 1 (0.2% of maximum risk value) and so were excluded from the scenario. Risk areas can be seen to mirror the probability map, with areas at risk in Cornwall, Wales, Southern England and the Lake District. Comparison of the current and projected situation in 20 years indicates that significant spread from an existing infection is most likely in the New Forest, Forest of Dean, the Brecon Beacons and Crychan Forest, southern Snowdonia (Dovey Forest) and the southern Lake District (Grizedale Forest) and may be related to relative contiguity of habitat. In Wales, the risk is largely due to the presence of larch and upland heathland. Grizedale Forest and the Forest of Dean are at risk largely due to the presence of larch and the New Forest is at risk predominantly through a combination of heathland and woodland.

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Figure 10 Maps showing the three different risk scenarios

4.3.2.4 Individual Species

The total area at risk was calculated, by clipping species host maps with the three risk scenarios (Table 20). No suitable areas were predicted for A. uva-ursi in England or in Wales. In scenario 1, the entire habitat is at risk as it is assumed Phytophthora has spread to all available hosts. However, the proportion of area for each species at risk under the projected 20 year model ranges between only 5% for V. vitis-idaea and 7% for V. myrtillus. Under the ‘no further spread’ scenario only 0.4% of V. myrtillus and C. vulgaris and 0.1% of V. vitis-idaea are at risk, although this still represents a significant area of land for both V. myrtillus and C. vulgaris. Maps of the risk scenario for each species (excluding A. uva-ursi) are shown in Appendix 2.

Table 20 Total area at risk under the three risk scenarios expressed as a proportion of the total habitat available. Scenario 1 = High Risk, scenario 2 = Medium Risk and scenario 3 = Low.

Scenario 1 Scenario 2 Scenario 3 Host Map Coverage Area at Proportion Area at Proportion Area at Proportion Species (ha) risk at risk risk at risk risk at risk V. myrtillus 1,648,000 1,648,000 1 117,200 0.07 7100 0.004 V. vitis-idaea 231,700 231,700 1 11,400 0.05 300 0.001 A. uva-ursi 0 NA NA NA NA NA NA C. vulgaris 1,983,100 1,983,100 1 111,900 0.06 8300 0.004

4.4 DISCUSSION

As discussed in section 4.2.2.3., the model has some limitations that need to be considered. Autocorrelation in environmental variables and overfitting by MaxENT may affect the model, as will potential correlation in the presence points meaning that predictions into areas with no presence points should be treated with caution. The model accuracy is limited by the accuracy and completeness of the input data. This is especially relevant with the LCM2000 which is known to be highly inaccurate in some areas. Repeating this modelling work using the LCM2007 (when available) may be of benefit. It has been suggested that the model may underrepresent the extent of blanket bog. In the short term, this could be investigated by validation with the Welsh phase 1 habitat data.

Modelling at a 2 km resolution may prove to be more accurate, particularly for the less common species, as additional presence points would become available for use as input data, and would potentially cover a wider area reducing the number of ‘gaps’ in the spatial distribution of presence points. Further validation of the model could also be considered. As discussed earlier, using the new habitat inventory in Wales would provide a way to validate the model in this area (providing the remotely sensed data has itself been sufficiently validated).

The MPEM model is undergoing continual improvements as more accurate and UK relevant data becomes available. Currently, certain assumptions in the model refer to the Californian Phytophthora situation. Continual updates of the MPEM modelling outputs should be considered as these assumptions are replaced by accurate data.

Although it is unlikely that Phytophthora will spread to affect all possible host plants, this high risk scenario would obviously affect a significant area of land, even in the absence of infection of C. vulgaris. There could also be an indirect effect on C. vulgaris in many habitats, even if no infection of this species occurred, if control measures were applied to other infected species. The impact would depend on the scale of the outbreak, the scale of control measures required and, potentially the scale of the habitat mosaic. In a habitat with discrete areas of Vaccinium spp. and C. vulgaris, it may be possible to control a Phytophthora outbreak with minimal impact on a non-target species. Whereas a more intricate mosaic would be likely to preclude very targeted treatment of infected plants.

Under a more likely risk scenario based on disease modelling, the impact of Phytophthora on the extent of ericaceous species is much reduced. However, specific areas, possibly related to the high contiguity of suitable habitat, could be severely affected by the disease.

The low risk scenario suggests that less than 1% of the area of these species across England and Wales would be affected.

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5. OPTIONS TO PREDICT CLIMATE DRIVEN CHANGES ON THE POTENTIAL UK DISTRIBUTION OF PHYTOPHTHORA.

5.1 INTRODUCTION

Climate factors have a large influence on plant pathogens (Bergot et al., 2004) and as such climate change can affect their distribution (Garrett et al., 2006, Coakley et al., 1999). There is concern that as the climate changes, the impacts pathogens can have will worsen (Evans et al., 2008, Bergot et al., 2004). Warmer climates can increase the spread of pathogens, the likelihood of hosts becoming infected and pathogen survival and development rates (Harvell et al., 2002). Two main spatial methods exist to try and capture this potential change. Firstly a climate envelope approach can be used (Garrett et al., 2006, Braiser, 1996), where details of the climate from the pathogens original/well established distribution can be used and ‘matched’ to the climate of the study area. Whilst this approach is quick and can work with limited inputs it does not include any information on the pathology of the species. A more accurate method involves the incorporation of future climate scenarios into an existing epidemiological model of the species spread (Evans et al., 2008, Garrett et al., 2006, Bergot et al., 2004). This requires extensive programming and some knowledge of the pathogens reaction to different climatic variables. However, it does ensure that physiology and epidemiology are considered when predicting pathogen spread with climate change. The following section will review both methods and discuss their relative benefits. In addition, an indicative assessment of time required to complete the analyses is presented.

5.2 CLIMEX MODEL

The CLIMEX model allows the impacts of climate change, in terms of a species’ range, to be assessed (Sutherst et al., 2007). It is a spatial based model and comes in two forms. Firstly, there is the true CLIMEX model and this is species based. It operates in two functions, compare locations and compare years. Compare locations uses long term averages of climate data at different locations and can give an idea of the potential distribution of a species. The compare years function uses years of monthly climatic data to show a species’ response to changes in climate through a set time period at the same location. It allows the potential population growth and survival to be estimated. In these models, details of the species responses to different climates need to be included. These parameters can be estimated in the model, however this requires full details of the species geographic distribution and experience on the part of the user. However, a large degree of uncertainty will remain around these estimates. This type of modelling could take up to 6 months to complete for Phytophthora. The other model type is a climate matching model that allows users to compare the climate of different locations. It can be run with limited knowledge of the species’ geographical range and no knowledge of the species’ climatic preferences. This model type is particularly useful in providing estimates of potential distributions for invasive species and pathogens. It could be used to match existing climates from areas in the distribution of Phytophthora (e.g. California), to future climates in the UK. Similar work has previously been carried out by Richard Baker (Fera) who compared current climate in California to the current UK climate (Figure 11). This is by far the quickest way to model the change in climate, but has no real link to the responses of the species to climate. The work would take one month to complete depending on the number of climate scenarios to be considered, and could be incorporated into the current host maps.

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Figure 11 CLIMEX match climates example output. UKs climate is matched to that of California where Phytophthora is known to be established.

5.3 INCORPORATION INTO EPIDEMIOLOGICAL MODELS

Incorporation of future climate scenarios into existing epidemiology models enables any predictions to be based on the physiology of the species and not only on its reaction to climate. One such model for Phytophthora already exists and this model is being improved all the time. The team

83 working on the model based at the University of Cambridge are headed by Prof Chris Gilligan. This model is called a Metapopulation Epidemic Model (MPEM).

MPEM is a modelling package that outputs GIS compatible files showing the disease landscape (including risk of spread maps and likely areas to be infected in a given time period) and disease progress curves. The model requires information on the host landscape and characteristics of the disease. Users can also include disease control options and information on detection. Climatic information is included and influences the infectivity and susceptibility parameters in the model.

In its present state the model can accept a set of future climate data (say, UKCIP projections for 2030), and model to the corresponding year (in this case, 2030). However, this would be a static climate MPEM with one set of climatic averages and not a rolling gradual change in climate over several years (i.e. incorporation of a full set of UKCIP data from 2010 to 2030, covering each month of each year). The team at Cambridge University are currently working on a more flexible way to include changing climate data in the model and this would enable climate change between years to be assessed in terms of its influence on Phytophthora. It is estimated that this work could take 12 – 18 months to complete.

5.4 GENERAL CONCLUSIONS

Obviously the approach to modelling the potential impact of climate change will depend on many factors. Table 21 summarises the pros and cons of the three methods discussed.

Table 21 The positive and negative aspects of the three proposed methods.

Method Pros Cons Only needs limited knowledge of No real link to diseases epidemiology geographic range and disease response to CLIMEX ‐ climate or population dynamics climate matching Quick modelling time (around 1‐ 2 Modelled results would be highly months) uncertain Aims to capture population growth and Needs details of the disease CLIMEX ‐ compare survival as a result of climate change response to climate locations / compare 6 months to complete work OR years Needs full geographic range of disease to estimate the responses Would need some model Would account for species physiology in development to automate the modelled responses process MPEM ‐ climate Could incorporate current host maps or Would require longer term scenario integration those modelled under future climates modelling (12 ‐ 18 months) Would potentially produce the most accurate predictions as accounting for

more variables

Predicting the potential impact of Phytophthora under future climate scenarios is crucial if appropriate management action is to be taken. The CLIMEX model provides a potentially fast way to compare the changing distribution of Phytophthora across years of future climate data. However, this method would be less accurate than incorporating future weather scenarios in to the MPEM model. If it is possible to enable this model to flexibly incorporate different climatic situations into its epidemiology runs, this may be the better way forward in terms of predicting future Phytophthora

84 distribution in the UK. The use of a flexible MPEM model will require larger inputs of time and resources and will take longer to create outputs than the CLIMEX or static climate MPEM.

Consideration should also be paid to the many other factors that could affect pathogen distribution in a changing climate such as land use change and changes in the distribution of host species. All models that are used to predict climate driven responses in plant pathogens have associated errors and these have been summarised by Garrett et al. (2006) as i) large degrees of uncertainty around variables used in models, ii) there is no accounting for any non linear relationships between epidemiological responses and climate, and iii) the potential for adaptation of the pathogen or host is not accounted for.

A further recommendation of Garrett et al. (2006) is the use of climate scenarios from General Circulation Models (GCMs). The UKCIP projections are based on the GCM HadCM3 and so these sets of data would be the best to use.

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6. DESIGNATED SITES AND BAP HABITATS

6.1 INTRODUCTION

Three types of designated sites were considered in this project and these are outlined below. All data regarding these sites were provided by Natural England and Countryside Council for Wales. • Sites of Special Scientific Interest (SSSI) – areas protected under the Wildlife and Countryside Act 1981, due to their special flora, fauna or geological interests.

• Special Areas of Conservation (SAC) – areas which have been given special protection under the European Union’s Habitat Directive (Council Directive 92/43/EEC 21 May 1992). Under this directive EU members were required to create a network of high quality conservation areas, known as Natura 2000 (Natura 2000 was led in England by then English Nature in the form of SACs and SPAs (see below). The Habitat Directive identifies 189 habitat types and 788 species in Annexes I and II of the Directive that are considered to be most at need of conservation within Europe. Of these habitats, 78 are relevant to the UK and it is from this list of 78 Annex I Habitats that the SACs in the UK were selected.

All SAC are also SSSI, the additional SAC designation is recognition that some or all of the wildlife and habitats are particularly valued in a European Context. • Special Protection Areas (SPAs) – areas that have been identified as being of national and international importance for the feeding, wintering or the migration of rare and vulnerable species of birds found within Europe. SPAs are also designated as SSSIs.

6.2 POTENTIAL IMPACT OF PHYTOPHTHORA INFECTION ON HABITAT CONDITION

The Common standards monitoring was derived by the JNCC in response to the need for a consistent and effective way to monitor sites within the UK that were established as a result of the legally binding EC Birds and Habitats Directive. The European Union Habitats Directive (Council Directive 92/43/EEC 21 May 1992) required all signatories to establish a ‘coherent European ecological network of special areas of conservation’3; these would be under the overarching European title of Natura 2000. To meet this obligation the UK created a network of SACs. The habitat directive states ‘a system should be set up for surveillance of the conservation status of the natural habitats and species of this directive’1. To meet this requirement the Joint Nature Common Standards Monitoring for Designated Sites was developed. Under the methodology it is the interest feature that is assessed, this is the one for which the site has been notified or designated. Many sites will have multiple interest features and so multiple assessments will need to be carried out. This monitoring method has now been applied to other designated sites that are under national legislation; in Britain this includes SSSIs. The underpinning aim of the CSM is to monitor the special features for which the site was designated, in order to determine if the feature is in satisfactory condition as required under the Habitat Directive. In order to ascertain the condition of each site there are conservation objectives that contain targets that are to be met if the feature is to be regarded as favourable. As a general

3 Council Directive 92/43/EEC 21 May 1992 86 rule, to be classified as favourable the interest feature should maintain the state/condition it was in at the time of designation. Article 3 of the Directive, states with reference to the creation of SACs; this network, composed of sites hosting the natural habitat types listed in Annex I and habitats of the species listed in Annex II, shall enable the natural habitat types and the species’ habitats concerned to be maintained or, where appropriate, restored at a favourable conservation status in their natural range.

Once an assessment of a feature is completed it is classified under one of the following seven categories; i) Favourable-maintained ii) Favourable-recovered iii) Unfavourable-recovering iv) Unfavourable-no-change v) Unfavourable-declining vi) Partially-destroyed vii) Destroyed The current timeline of monitoring within the UK aims for each designated site to be monitored on a 6 year rolling cycle, with reports published to coincide with this cycle (Williams, 2006).

6.2.1 Habitat specific Common Standards Monitoring Guidance.

There are specific guidance documents, published by the JNCC4, for the following broad habitat groups: Coastal, Freshwater, Lowland grassland, Lowland heathland, Lowland wetland, Marine, Upland habitats and Woodland. Within each document there are detailed conservation objectives that are used to monitor designated sites. These include the attribute of the habitat feature to be monitored (such as habitat extent, composition, and structure), the target of this attribute and the method of assessment of this attribute. Table 22, adapted from Common Standards Monitoring Guidance for Alpine dwarf shrub heath5, gives an example of the assessment criteria. Each individual SAC and SSSI has an accompanying report that is site specific. These are taken into consideration when carrying out a condition assessment as habitas are likely to be variable.

4 http://www.jncc.gov.uk/page-2217 5 http://www.jncc.gov.uk/page-2237 87

Table 22 Condition assessment criteria for Alpine dwarf shrub heath, which includes Annex I – Alpine and boreal heaths (H4060).

Atribute Targets Method of assessment / Comments Feature extent There should be no measurable decline in the Field comparison with baseline map of area of the feature. features, or occurrence of feature at sample points on a systematic sample grid. Vegetation (1) At least 1 species from each of the following Target (1) assessed against visual composition — should be present: estimate at 4 m2 scale. frequency of (a) dwarf-shrub, and dwarf-shrubs, (b) moss, liverwort or non-crustose lichen. bryophytes and lichens. Vegetation (1) The collective cover of indicator species Target (1) assessed against visual composition — should make up at least 66% of the vegetation estimate at 4 m2 scale. Target (2) cover. cover (listed below). assessed against visual estimate for (2) Less than 1% of the vegetation cover should as much of the feature as is visible be made up of non-native species. while standing at a sample location. Vegetation (1) Less than 10% of the vegetation cover Targets (1-3) assessed against visual composition — should consist of, collectively, Agrostis capillaris, estimate at 4 m2 scale. Assessment is indicators of A. vinealis, Anthoxanthum odoratum, best done in late winter through current grazing. Deschampsia flexuosa, Festuca ovina / vivipara, spring. Galium saxatile, Poa spp. (other than arctic- alpine spp.) and Potentilla erecta. (2) Signs of grazing on less than 10% of live leaves of any of Carex bigelowii, Deschampsia flexuosa, Festuca ovina, Festuca vivipara, Juncus trifidus. (3) Less than 33% of the last complete growing season’s shoots of dwarf-shrub species (collectively) should show signs of browsing. Vegetation 1) There should be no signs of burning inside Target (1) assessed against visual structure — the feature boundaries. estimate for as much of the feature as presence of Qualifiers: Failure of this target should also be is visible while standing at a sample burnt recorded if any evidence of this is found while location. If a feature is viewed at a vegetation. walking between sample locations. distance, and there is uncertainty about whether or not a burn has actually entered the feature, then use a rough guide of 25 m (ie. if the burn is further than 25 m inside the feature, it is considered damaging). Physical (1) Less than 10% of the ground cover should Target (1) should be assessed in the structure — be disturbed bare ground. (Disturbed bare following two ways: (a) for indicators of ground is where a substrate of bare humus, bare diffuse/scattered disturbance of the ground peat, bare mineral soil, bare gravel, or soil ground, not on clearly defined paths or disturbance due covered only by an algal mat, has its surface tracks, by visual estimate at 4 m2 to herbivore and broken and imprinted by hoof marks, wallows, scale; and (b) for distinct and clearly human activity. human foot prints, or vehicle and machinery defined paths and tracks (exclude tracks. The emphasis is on ‘disturbed’ rather constructed tracks) by visual estimate than ‘bare’). for as much of the feature as is visible while standing at a sample location. Indicator species: Arctostaphylos alpines, Arctostaphylos uva-ursi, Calluna vulgaris, Cetraria islandica, Cladonia arbuscula, Cladonia portentosa, Cladonia rangiferina, Cladonia uncialis, Ampetrum nigrum spp.hermaphroditum, Erica cinerea, Erica tetralix, loiseleuria procumbens, Juniperus communis spp. Nana, Racomitrium lanuginosum, Sphagnum capillifolium, Vaccinium myrtillus, Vaccinium uliginosum, Vaccinium vitis-idaea.

88 It is clear that an outbreak of Phytophthora could impact on the final assessment of the habitat. This could be as a result of a change in the species composition through death of host species, or through the removal of potential host species as part of control measures. In some cases it is possible that the effect will be to change the habitat classification from favourable to less favourable, and so failing to meet the objectives of the Habitat Directive. In all cases there should be no reduction on the total extent of the area covered by the feature, although in the short term the feature might not correspond to any habitat definition if disease or control measures were extensive. SACs with the following habitat types (from the Habitat directive and mapped due to the potential presence of host species – see Section 6.3) could be specifically affected by outbreaks of Phytophthora and as a result their condition category could decline. The assessment attributes that are likely to be impacted, and lead to a decline in the condition classification, are listed below the habitat type. 4010 North Atlantic wet heaths Attribute: Bare ground must not exceed more than 10%. Dwarf shrub cover must be between 25-90%. Vegetation composition must include at least two species of dwarf shrub present and at least frequent (dwarf shrub includes Arctostaphylos uva-ursi, Calluna vulgaris, Vaccinium myrtillus, V. Vitis-idaea).

4010 Northern Atlantic wet heaths with Erica tetralix Attribute: At least 50% of the vegetation should consist of species listed - including Calluna vulgaris. Less than 10% of the ground should be disturbed bare ground.

4030 European dry heaths Attribute: Vegetation composition should contain proportions of indicator species including Vaccinium spp., Arctostaphylos spp. Calluna vulgaris at various percentages from 25-75% depending on the type of heath. Less than 10% of area should be disturbed bare ground.

4060 Alpine and Boreal Heaths Attribute: Vegetation composition must include at least one dwarf shrub species. Collective cover of the indicator species must make up at least 66% of the vegetation cover- the indicator species include Calluna vulgaris, Vaccinium myrtillus and V. Vitis-idaea.

5130 Juniperus communis formations on heaths and grasslands Attribute: Less than 5% of the area should show severe disturbance.

6410 Molinia meadows Attribute: Bare ground should not exceed more than 10%. Sward composition-targets should be set to register a low or declining frequency of key indicators as unfavourable. One of these key indicators to be monitored may be Calluna vulgaris.

6150 Siliceous alpine boreal grasslands

89 Attribute: At least 25% of the vegetation cover should consist of indicator species - Vaccinium myrtillus is an indicator species. Less than 10% of ground cover should be disturbed bare ground.

6130 Calamarian grasslands of the Violetalia calaminariae Attribute: Less that 10% of the ground cover should be disturbed bare ground.

6170 Alpine and subalpine calcareous grassland, 6230 Species rich Nardus grassland Attribute: Less than 10% of the ground cover should be disturbed bare ground.

6430 Hydrophilous tall herb fringe communities of plains and of the montane to alpine levels Atribute: At least 50% of the vegetation cover should be made up of indicator species- these include Calluna vulgaris and Vaccinium spp.. Less than 25% of the ground should be disturbed bare ground.

7110 Active raised bogs, 7120 Degraded raised bogs, 7150 Depression on peat substrates Attribute: Less than 10% exposed substrate. For the mire expanses, a least 3 species out of Calluna vulgaris, Erica tetralix, Erioporum angustifolium, E. Vaginatum & Trichophorum cespitosum constant, with a combined cover not exceeding 80%. No single species should cover more than 50%. Less than 10% of the ground cover should be disturbed bare ground.

7130 Blanket bogs, 7150 Depressions on peat substrates of the Rhynchosporion Attribute: At least six indicator species present (Vaccinium spp., Arctostaphylos spp. Calluna vulgaris are in this list). 50% of the vegetation should consist of at least 3 indicator species. Less than 10% of the area should be disturbed bare ground.

8110 Siliceous scree of the montane to snow levels Attribute: Less than 10% of the ground cover should be disturbed bare ground.

6.2.2 Likely impact of Phytophthora on condition criteria

The condition of heathland habitats are most likely to be affected by Phytophthora infection. Other habitats will infrequently support ericaceous species at sufficient densities for Phytophthora to have a significant effect on condition.

The most likely condition criteria that would be affected by Phytophthora infection or measures to control the disease are: bare ground cover, dwarf shrub heath cover and presence/proportion of indicator species. The likelihood of these factors being affected by Phytophthora will depend on the specific situation at each site (including species composition and scale of the habitat mosaic), the range of species that are infected and the scale of infection. In general terms, greater impacts will result if C. vulgaris becomes infected since it represents a greater proportion of dwarf shrub heath than other ericaceous species. However, at an individual site level, infection of Vaccinium could have significant effects on condition assessment and control measures are likely to affect all species to some extent.

90 In the short term, dwarf shrub heath cover and bare ground may be affected by both infection of ericaceous species and measures to control the disease. Recolonisation may, over time, restore sites to their original condition, but this process may take many decades (Miller & Miles, 1970). Depending on the community, scale of infection and type, timing and frequency of treatment used, the balance of the species in the community may be changed. The likely impact on the presence of indicator species will be highly variable between habitats and sites.

6.3 MAPPING OF DESIGNATED SITES

Four plant species were considered as highly important in light of the Pytophthora outbreaks and these are Vaccinium myrtillus (Bilberry), Vaccinium vitis-idaea (Cowberry), Arctostaphylos uva-ursi (Bearberry) and Calluna vulgaris (Heather). C. vulgaris was considered separately from the other species as the importance of this species as a sporulating host is unclear.

Destruction of the above species in the event of an outbreak is likely to have an impact irrespective of the location but there may be greater consequences if it occurs on a ‘protected site’.

Several coastal and marine sites with small amounts of suitable habitats (usually on cliffs) were removed as they would not be covered by the terrestrial MaxENT modelling or final host maps.

6.3.1.1 SSSIs

Any SSSIs that were also classed as SACs or SPAs were removed and so would only be assessed with these higher levels of designated site. Information on the main habitat type for each SSSI unit in England and Wales was used to select SSSIs that contained habitat suitable for the growth of the four species of concern. Each of the suitable habitats was given a rating showing the likelihood of the habitat containing our species of interest (Table 23). A rating of 1 = a species of concern is likely to be present and abundant, 2 = relevant species are present only in a proportion of habitats within the broad habitat or are uncommon in the habitat. The amount of suitable habitat within each SSSI was then summed.

6.3.1.2 SPAs

For SPAs data on the broad habitat type present at each site was used to filter out sites that would not be impacted by a Phytophthora outbreak. The habitats selected as suitable were given a rating of 1 or 2 (as with SSSIs) and are shown in Table 24.

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Table 23 SSSI habitats included in the selection of SSSIs at risk from a Phytophthora outbreak.

Country SSSI habitat Feature Rating Acid grassland - 2 Bogs - 2 Bracken - 2

England Broadleaved, mixed and yew woodland - 2 Dwarf shrub heath - 1 Montane habitats - 2 Bracken Continuous bracken 2 Maritime cliff & associated ledges & Coastal cliff crevices 2 Grassland Acid grassland 2 Coastal heath land 1

Wales Dry heath 1 Heath Montane heath 1 Wet heath 1 Blanket bog -other ombrogenous mire 2 Mire Raised bog -ombrogenous 2 Woodland Semi-natural woodland 2 acid

Table 24 SPA habitats included in the selection of SPAs at risk from a Phytophthora outbreak.

SPA Habitat Rating Alpine and sub-alpine grassland 2 Bogs. Marshes. Water fringed vegetation. Fens 2 Broad-leaved deciduous woodland 2 Coniferous woodland 2 Heath. Scrub. Maquis and garrigue. Phygrana 1 Mixed woodland 2

6.3.1.3 SACs

Each SAC has an associated report that states the main reasons for its designation as an SAC. Under Directive 92/43/EEC Annex 1 contained an extensive list of habitats (189) ‘Natural habitat types of community interest whose conservation requires the designation of special areas of 92 conservation’. From this list the UK (and all other EU signatories) selected habitats relevant to the specific country and environment-for the UK this amounted to a total of 78 selected habitat types. For the UK these habitats fall under 9 general headings

• Marine, coastal and holophytic habitats • Coastal sand dunes and continental dunes • Freshwater habitats • Temperate heath and scrub • Sclerophyllous scrub (matorral) • Natural and semi-natural grassland formations • Raised bogs and mires and fens • Rocky habitats and caves • Forests Of the 78 selected habitat types from Annex 1 of 92/43/EEC considered relevant to the UK there are thought to be 28 that could potentially be of concern in relation to the current/potential Phytophthora outbreak due to the composition of the vegetation. This estimation was derived by consideration of each of the 78 habitat types independently, taking into account the habitat description and NVC information that was available. Each abitat type was then ranked to give a rating as with the SSSIs and SPAs. SACs that contained any of the resulting 28 habitat types shown in Table 25 were selected and the total area of suitable habitat within the SAC was summed.

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Table 25 Habitat types included in the selection of SACs that may be vulnerable to a Phytophthora outbreak.

Annex 1 Rating Rating for habitat excluding C. vulgaris type Description C. vulgaris 1220 Perennial vegetation of stony banks 2 0 1230 Vegetated sea cliffs of the Atlantic and Baltic coasts 2 0 2130 * Fixed dunes with herbaceous vegetation (`grey dunes`) 2 0 2150 * Atlantic decalcified fixed dunes (Calluno-Ulicetea) 1 0 2330 Inland dunes with open Corynephorus and Agrostis grasslands 2 0 4010 Northern Atlantic wet heaths with Erica tetralix 1 0 4020 * Temperate Atlantic wet heaths with Erica ciliaris and Erica tetralix 1 0 4030 European dry heaths 1 1 4040 * Dry Atlantic coastal heaths with Erica vagans 1 0 4060 Alpine and Boreal heaths 1 1 4080 Sub-Arctic Salix spp. scrub 2 2 5130 Juniperus communis formations on heaths or calcareous grasslands 2 2 6150 Siliceous alpine and boreal grasslands 0 2 6170 Alpine and subalpine calcareous grasslands 2 2 * Species-rich Nardus grassland, on siliceous substrates in mountain 6230 2 2 areas (and submountain areas in continental Europe) Molinia meadows on calcareous, peaty or clayey-silt-laden soils 6410 2 0 (Molinion caeruleae) Hydrophilous tall herb fringe communities of plains and of the 6430 2 2 montane to alpine levels 7110 * Active raised bogs 2 2 7120 Degraded raised bogs still capable of natural regeneration 2 0 7130 * Blanket bogs 1 2 7150 Depressions on peat substrates of the Rhynchosporion 2 2 * Calcareous fens with Cladium mariscus and species of the Caricion 7210 2 0 davallianae 7230 Alkaline fens 2 0 Siliceous scree of the montane to snow levels (Androsacetalia alpine 8110 2 2 and Galeopsietalia ladani) 8220 Siliceous rocky slopes with chasmophytic vegetation 2 2 9190 Old acidophilous oak woods with Quercus robur on sandy plains 2 2 91A0 Old sessile oak woods with Ilex and Blechnum in the British Isles 2 1 91D0 * Bog woodland 2 2 *Denotes Priority Habitat as listed in 92/43/EEC, ANNEX 1. Definition under Article 1 ‘ priority natural habitat types means habitat types in danger of disappearance, which are present in the territory referred o in Article 2 and for the conservation of which the community has particular responsibility in view of the proportion of their natural range which falls within he territory referred to in article 2.

6.3.1.4 Assessment of at risk designated sites in risk zones

Assessment of the final designated sites to be considered ‘at risk’ was carried out twice. Once for all species excluding C. vulgaris and once with C. vulgaris included. The three risk scenarios were clipped by the final host maps to show only the areas of the predicted distribution of hosts that

94 were considered to be at risk. The number of designated sites remaining from Sections 6.3.1.1 to 6.3.1.3 that fell within these areas were summed and listed. This was done for each risk scenario.

6.3.2 National Inventory of Heathland

Lowland and upland heathland are both BAP priority habitats, therefore habitat inventories from England and Wales were analysed to establish the extent of potential Phytophthora infection under the three different scenarios. Although other BAP habitats that may be affected by Phytophthora, habitat inventories at the national scale do not identify habitats in sufficient detail to establish which sites contain ericaceous species.

6.4 RESULTS

6.4.1 Designated Sites

6.4.1.1 Risk Scenarios

The designated sites selected as potentially being at risk from Phytophthora are listed in Appendix 2. Several of these sites contained only low amounts of suitable habitat when compared to the entire area designated (Table 26).

Table 26 Numbers of designated sites containing suitable habitat that have a low area of suitable habitat, a low proportion of suitable habitat, or both.

Low area of suitable habitat Low proportion of suitable Both low area and Designation (<5ha) habitat (<0.05) proportion

Rating 1 Rating 2 Rating 1 Rating 2 Rating 1 Rating 2 SAC (excluding C. vulgaris) 9 4 16 6 6 3 SAC (including C. vulgaris) 7 15 10 23 2 11 SSSI 13 199 2 20 2 16 SPA 0 3 1 17 0 3

6.4.1.2 SACs

In summary there are 183 SACs in England and Wales that are potentially at risk from Phytophthora as they contain V. myrtillus, C. vulgaris, V. vitis-idaea or A. uva-ursi within the vegetation. Many of these SACs are only considered to be at risk due to the presence of C. vulgaris. At present it is inconclusive as to whether this species is susceptible to Phytophthora, and if the sites that contain only this species are removed it leaves 127 SACs at risk. When including C. vulgaris, 90 sites have a rating of 1 and 93 have a rating of 2. Excluding C. vulgaris, leads to 71 sites with a rating of 1 and 56 sites have a rating of 2.

Looking in more detail, for C. vulgaris sites, 33 contain <5% suitable habitat (of these 26 are rating 2). The South Pennine and North Yorkshire Moors have the largest at risk areas with 88% (57,640 ha) and 74% (32,767 ha) vulnerable respectively. For the three remaining species, 22 sites contain <5% suitable habitat and only 7 are rating 2. Cwm Doethie û Mynydd Mallaen has the largest area at risk with 2,805 ha vulnerable around, 68% of the SAC. Simonside Hills also has a large area at risk (2,013 ha), but this accounts for nearly 97% of the SAC area.

95 6.4.1.3 SSSIs

In total 1344 SSSIs across England and Wales were considered to potentially be at risk. Of these, 209 contain heath and have a rating of 1. 23 sites contain < 5% suitable habitat (of these 21 are rating 2). The site with the largest area at risk is The Cheviot. This site has a rating of 1 and 100% of the habitat is at risk. This equates to 3492 ha.

6.4.1.4 SPAs

A total of 67 SPAs were selected as being potentially at risk from Phytophthora, and of these 30 have a rating of 1. There are 18 sites that contain <5% suitable habitat (17 are rating 2). The North Pennine Moors has the highest amount of vulnerable habitat with a rating of 1. The proportion of vulnerable habitat is 0.94 which equates to 137705 ha at risk.

6.4.1.5 Designated sites at risk

The number and area of sites at risk was calculated by intersecting the designated site polygons with the different risk scenarios that had been clipped with the host maps. Two sets of these were produced, firstly the host maps for all four species were clipped with the risk scenarios and any designated site that intersected an area of the resultant risk was selected. Secondly, this process was repeated, but without the inclusion of C. vulgaris in the host map clipping. At risk sites have been mapped and listed in Appendix 2. Summary figures are provided in Table 27 and Table 28, and results under each risk scenario are explored in more detail in sections 6.4.1.6 to 6.4.1.8. However, within each site, the area of suitable habitat may be relatively small.

In all designations, the total number of sites shown to be at risk was less than the number initially selected in Section 6.3. The proportion of sites not shown as being at risk (not matching up with the risk scenario maps), increased with decreasing detail in the habitat information used for the initial assessment. For SSSIs (limited habitat information available for initial assessment) only 52% (C. vulgaris excluded) and 65% (C. vulgaris included) were selected using the risk scenarios. This increased with SPAs to 70% and 83% respectively, and further increased for SACs (the most detailed habitat information available) to 77% and 90%. The areas of these sites (those that did not match up with the species risk scenario maps) are shown in Table 28.

Table 27 Numbers of designated sites at risk in each scenario.

Number of sites Scenario 1 Scenario 2 Scenario 3 Rating Rating Rating Rating Rating Rating Designation 1 2 1 2 1 2 SSSI (including C. vulgaris) 136 405 6 32 2 2 SSSI (excluding C. vulgaris) 108 316 6 32 2 2 SPA (including C. vulgaris) 25 12 3 0 1 0 SPA (excluding C. vulgaris) 21 10 3 0 1 0 SAC (including C. vulgaris) 81 63 18 8 6 1 SAC (excluding C.vulgaris)* 55 48 10 12 3 4 *22 (totalling 5041 ha) SACs under scenario 1 and 4 (totalling 76 ha) under scenario 2, had no rating as the habitat details for the sites did not suggest V. vitits-idaea, V. myrtillus and A. uva-ursi would grow in these areas.

96 Table 28 Total areas of designated sites that matched up/did not match up with the predicted host maps.

Area of sites (ha) Matched up with species risk Not matched up with species maps risk maps Designation Rating 1 Rating 2 Rating 1 Rating 2 SSSI (including C. vulgaris) 28,939 25,694 2,675 26,043 SSSI (excluding C. vulgaris) 26,622 20,183 4,993 31,554 SPA (including C. vulgaris) 351,721 1,569 350 4,287 SPA (excluding C. vulgaris) 349,901 1,446 2,107 4,410 SAC (including C. vulgaris) 217,549 129,335 1,756 3,151 SAC (excluding C. vulgaris) 24,291 310,508 2,987 1,253

6.4.1.6 Designated sites at risk – Scenario 1

A spread of designated sites are at risk across England and Wales. In several cases a site is classed as both an SAC and an SPA and may show different proportions of suitable habitat due to the different habitat classifications considered in the initial selection (the finer detailed habitat classifications available with SACs meant it was possible to be more selective over which habitat types to include). This is true of the North Pennine Moors, Upper Teasdale, The North York Moors and The New Forest where all these sites have a lower proportion of suitable habitat in the SAC than in the SPA classifications.

In all cases, exclusion of C. vulgaris appears to exclude several coastal sites (e.g. Dungness and Holy Island Coast) along with some inland sites. For the at risk SSSIs, these excluded inland sites are seen particularly in the South East and East Anglia.

6.4.1.7 Designated sites at risk – Scenario 2

The number of sites at risk in scenario 2 dramatically decreases, and the removal of C. vulgaris no longer has an effect on the overall numbers of sites, although the rating for these sites can change (SACs).

Three sites are classed as both SPAs and SACs and are considered to be at risk in this scenario. These are Mynydd Mallaen, Berwyn and South Clwyd Mountains and The New Forest. Dartmoor is also highlighted as at risk and it contains nearly 80% suitable habitat.

6.4.1.8 Designated sites at risk – Scenario 3

The number of SSSIs at risk in this scenario is dramatically lower than in scenario 1 (<1% of original). The New Forest (designated as both a SPA and SAC) is still at risk even in this low scenario, as are Mynydd Epynt, Dartmoor and Exmoor Heaths. All these sites have been given the rating 1 for C. vulgaris (except Mynydd Epynt which has a rating 2 for the species) and 2 for the remaining three species, suggesting these sites may be at a lower risk of damage if it is found that C. vulgaris is not a sporulating host. Two other SACs that are also considered at risk in this scenario are The River Camel and Coedydd Nedd a Mellte. Both these sites have a rating of 1 for all four species considered. However, within each site, the area of suitable habitat may be relatively small.

97 6.4.2 National Inventory of Heathland

A total of 423,717 ha of National Inventory Heathland (NIH) were considered for risk assessment across England and Wales. Of this 315,820 ha was in England and 107,897 was in Wales.

The total area of National Inventory Heathland (NIH) at risk was also calculated by clipping the individual species risk scenarios created above, with the NIH polygons (Table 29). The overlapping area was calculated, although the areas calculated for each species are obviously not mutually exclusive. This exercise suggests that, under scenario 2, between 4 and 8% of heathland is at risk, based on the presence of individual host species. Under the low risk scenario 3, which assumes no expansion of the disease from current infected sites, only a very small (<0.1%) proportion of heathland is at risk.

Table 29 Total area of National Inventory Heathland at risk under each different risk scenario for the four species.

Scenario 1 Scenario 2 Scenario 3 Total Area Area of Area of Area of Species Proportion Proportion Proportion of NIH (ha) NIH at NIH at NIH at at Risk at Risk at Risk Risk Risk Risk V. myrtillus 147,631 147,631 1 12,042 0.08 100 0.0007 V. vitis-idaea 49,533 49,533 1 1717 0.04 0 0 A. uva-ursi 0 NA NA NA NA NA NA C. vulgaris 162,697 162,697 1 12,101 0.07 100 0.0006

98 7. SYNTHESIS AND CONCLUSIONS

This study has identified the primary consumer species, ecosystem services and designated sites that could potentially be affected by Phytophthora infection of ericaceous species in England and Wales. Here we aim to summarise the likely impacts of infection under the three risk scenarios and estimate the overall impact of each scenario.

7.1 SUMMARY OF LIKELY IMPACTS

7.1.1 Other species

The review of the effects on other species associated with the four host species under consideration has focussed on primary ‘consumers’. It is beyond the scope of this study to attempt to evaluate the impact at higher trophic levels or on the basis of habitat structural change that could occur as a result of Phytophthora infection. A wide range of species, most commonly invertebrates (both as consumers and pollinators) but also fungi and birds are primary ‘consumers’ of these host species, but most species associated with these hosts are polyphagous. Populations of polyphagous species would therefore only be affected by Phytophthora infection at a local level where other host species were absent. However, there are a number of species monophagous on each of the four species considered here, which include BAP species. These species could be significantly affected by Phytophthora infection and control. Locally, the impact would depend on the extent of infection and control within sites, habitat continuity and the ability of species to disperse to other suitable habitats. The national impact would depend on the scale of infection and species distribution range. An overall assessment of the likely impact under the three scenarios described in section 4.3 is made on the basis of species that are monophagous on one of the four host species or are oligophagous including one or more of these hosts. Distributions, based on counties (section 2.3) were compared with Phytophthora distributions under the three scenarios, although assessments made at this spatial scale could overestimate the potential impacts. Under the high risk scenario, where all possible hosts are infected, it was assumed that species would be affected over their entire range in England and Wales. Although this scenario does not include C. vulgaris as a host species in the MPEM models, since there are no current records of infection in the wild, the distribution of currently identified host species is likely to include the distribution of C. vulgaris. For the medium and low risk scenarios, species were not considered to be potentially affected where their distribution was limited to counties where only a small number of current outbreaks had been recorded and no spread of infection was anticipated under the medium risk scenario. Species susceptibility to Phytophthora infection in England and Wales was assessed in relation to their use of Vaccinium spp. and A. uva-ursi separately from C. vulgaris. Those that include C. vulgaris in their host range have been included with those dependent on C. vulgaris because, in general, the likelihood of an impact will be greatest in the event that C. vulgaris is infected. No BAP/Nationally Scarce species that were monophagous/oligophagous were found to be associated with Vaccinium spp. or A. uva-ursi but not C. vulgaris. However, little is known about many of the species reviewed in this study, therefore the number of rare species at risk from Phytophthora is likely to be higher. Under the high risk scenario 26 species of invertebrates and 15 species of fungi were mono/oligophagous on Vaccinium spp. or A. uva-ursi and could therefore be severely affected under this scenario (Table 30). Twenty seven BAP/NS invertebrate species plus one pollinator were associated with C. vulgaris and a further 44 invertebrates, two pollinators and eight fungi were mono/oligophagous and associated with C. vulgaris. Under the medium risk scenario, most of these species would potentially be affected by Phytophthora, but only over part of their range. A smaller proportion of these species would be affected under the low risk scenario and for all species it is likely that this would occur over a smaller geographic range.

99 Table 30 Number of monophagous/oligophagous species (BAP/NS status species presented separately) potentially affected by Phytophthora infection of heath species across all or part of their range under the different risk scenarios: numbers of species with % of the total potentially affected in the high risk scenario in parentheses.

High risk (entire range) Vacc. spp. & Arcto. C. vulgaris (BAP etc.) C. vulgaris

Invertebrates 26 27 44

Pollinators 0 1 2

Fungi 15 0 8

Medium risk (part range) Vacc. spp. & Arcto. C. vulgaris (BAP etc.) C. vulgaris

Invertebrates 21* (81) 22 (81) 42 (95)

Pollinators - 1 (100) 2 (100)

Fungi 9 (60) - 2 (25)

Low risk (part range) Vacc. spp. & Arcto. C. vulgaris (BAP etc.) C. vulgaris

Invertebrates 11 (42) 13 (48) 31 (71)

Pollinators - 1 (100) 2 (100)

Fungi 6 (40) - 0

* One species may potentially be affected across its entire range in the medium risk scenario.

7.1.2 Ecosystem services

Table 31 provides a summary of the overall impact of Phytophthora on ecosystem services under different risk scenarios where Vaccinium alone is infected, or Vaccinium + Calluna is infected. The colour shading follows that of the NEA indicating the importance of the ecosystem service to the ecosystem (NB in the NEA heathlands form part of the mountain, moors and heaths ecosystem, thus the importance of an ecosystem service is not necessarily exactly the same as heathlands alone). It is reiterated here that the assessment is qualitative. It assumes that significant bare areas of soil are not created, i.e. re-colonisation by other plant species occurs, and any removal of diseased plants occurs at the small scale, although the assessment makes some account for the fact that greater areas of vegetation may have to be destroyed with higher levels of infection. In the table below it assumes that, in general, Vaccinium will be more interspersed amongst Calluna and other vegetation, so that the total area affected (and hence the potential for soil to be exposed) is smaller than when both Vaccinium + Calluna are infected, although it is acknowledged that larger swathes of Vaccinium can occur in some areas, in which case the impact is more akin to Vaccinium + Calluna rather than Vaccinium alone. If localised, large areas of infected Vaccinium exist, then specific management techniques will be required to prevent the underlying soil from drying out and to prevent soil erosion. The infection scenarios discussed in the previous section consist of three scenarios, but, given the uncertainty in both the spread of Phytophthora and the impacts this may have on ecosystem services, the scenarios have been simplified to low and high infection rates for ecosystem services. It is also reiterated that heathlands occur in specific areas of England and Wales, and their existence can form a substantial part of local communities and their economies, where other sources of income are limited. These people will clearly be affected to a far greater extent than others within England and Wales. In terms of cultural services, it assumed that for under the high risk scenario public access will be restricted in order to reduce the spread of Phytophthora which

100 will have knock-on effects for tourism; at high levels of infection, livestock movement may also be restricted to prevent further spread.

Table 31 Summary of the potential impact of different risk scenarios on ecosystem services.

Vaccinium Vaccinium + Calluna Ecosystem Service Risk scenario Risk scenario Provisioning Low High Low High Food 1 4 2 4 Fibre 1 2 1 2 Energy 1 1 1 1 Water supply 1 2 1 2 Wild species diversity 2 4 2 4 Natural pharmaceuticals 1 1 1 1 Regulating Air quality 1 2 1 2 Water quality 1 3 2 3 Climate 1 3 2 3 Hazard regulation 1 3 3 4 Disease & pests 2 3 2 3 Noise 1 1 1 1 Cultural Aesthetic & inspiration 1 3 3 4 Recreation & tourism 1 4 3 4 Knowledge & education 1 3 1 4 Spiritual & religious ? ? ? ? Cultural heritage & sense of place 1 3 2 4

Key High High - medium Medium - low Low Importance of service High Medium Low Negligible Scale of impact 4 3 2 1

7.1.3 Designated sites

The analysis undertaken here has identified the number and area of designated sites that could be affected by Phytophthora under the three risk scenarios. This has been based on an assessment of the likely presence of ericaceous host species in each habitat, however the accuracy of this assessment is dependent on the level of detail provided with the designation. A more accurate assessment would require either more detailed habitat mapping or more detailed assessment of individual designated sites to establish whether specific host species were present. In addition it must be remembered that a designated site will usually be constituted by a range of habitats, therefore only a proportion of a site may be affected. The impact on condition of designated sites will depend on the scale of infection and the range of species infected in the natural environment, but for many sites will be dependent on the specific vegetation composition. Condition assessments most likely to be affected (depending on the habitat) will be: cover of dwarf shrub heath, disturbed bare ground cover and presence of indicator species. If an affected host plant is the dominant species and infection or control treatments

101 extend over significant areas, then it is likely that condition will be compromised. However, the condition of other habitats will depend to a much greater extent on the site specific circumstances. A large number of designated sites could be affected if infection were to spread to all areas in the high risk scenario. However, many of these sites were classed as habitats ‘possibly containing a host species or only at lower abundance’ (rating 2) and therefore may not be affected by Phytophthora infection (Table 27). Only around one quarter of SSSIs were highly likely to support abundant populations of one or more host species. This uncertainty in vegetation composition of many sites based on the habitat information available from designation categories is highlighted by the large land areas under rating 2 that do not match species risk maps. If C. vulgaris is not infected, around 70% of all sites at risk could still be affected based on the presence of other ericaceous host species. Under the medium risk scenario, a much smaller number and area of designated sites is at risk from Phytophthora infection, with only 27 sites that are likely to be dominated by one of the four host species affected. Of these 19 are likely to be affected even if C. vulgaris is not infected. The low risk scenario suggests that only nine designated sites dominated by ericaceous host species are at risk from Phytophthora infection of which six would be affected in the absence of C. vulgaris infection.

7.2 LIKELY IMPACT OF EACH SCENARIO

7.2.1 High

The high risk scenario therefore has the potential to significantly affect a large number of species directly associated with ericaceous heath species, including a number of rare species. However, if C. vulgaris remains unaffected by the pathogen, the effects, particularly on rare BAP/NS species, would be much more limited. The scale of infection or control treatment will also be important; if spread within a site can be controlled, populations of species associated with these ericaceous hosts may be able to recover. Significant effects on a wide range of ecosystem services are likely with widespread infection of ericaceous species. The impact on designated sites and BAP habitats could be very serious, although the precise impact would depend on: infection of C. vulgaris, the scale of infection and control treatments, the proportion of susceptible habitat within each site and the proportion of affected host species within the site.

7.2.2 Medium

Under a more likely scenario defined by model projections for 20 years’ time, although many associated species may be affected, the impact will be restricted to only part of their range. Although one invertebrate species may be affected across its entire range as a result of Vaccinium spp. infection. It is likely that most species would survive in other locations, although the local impact could be significant. Overall, only a small proportion of designated sites that could be affected under the high risk scenario would be affected under this scenario. However, around one fifth of SACs containing habitats likely to be dominated by one or more host species could be affected.

7.2.3 Low

Under the low risk scenario a smaller proportion of associated species are likely to be affected and only over part of their range. Only a small number of designated sites would be affected if there is

102 no expansion of infection. Effects on ecosystem services are likely to be negligible in the absence of widespread infection, unless C. vulgaris is infected. The impact of this scenario is therefore unlikely to be great at a national level, although the implications at a local level could be significant.

7.3 FUTURE RESEARCH PRIORITIES

As a relatively new disease to the UK, the scope and understanding of Phytophthora infection is developing continuously. This study has reviewed the range of primary consumers and ecosystem services that may be affected by infection of four host species and has mapped the range of these species. Further work could, in particular, develop a better understanding of the potential scale of the impact on primary consumers, but also consider the indirect effects Phytophthora may have, in terms of habitat loss, in more detail. The models could be developed and refined, to allow better determination of likely areas at risk. Potential future research includes:

• Modelling host species based on 2 km data from the NBN. This would be particularly useful for V. vitis-idaea and A. uva-ursi, since current models are based on limited data at the 1 km scale and as such, the current models should be viewed critically.

• The models use LCM2000 data to assess the likely area of habitat within each 1 km cell that could be affected. However, LCM2000 is known to be somewhat inaccurate. Reanalysis with the improved LCM2007 data when it is available should improve the accuracy of the models.

• Further model validation would ensure a better understanding of the accuracy of the models developed here. In the short term phase 1 habitat data from Wales could be used. Once the ‘New Habitat Inventory for Wales’ is complete, this dataset will allow better validation since these data distinguish between heath dominated by Vaccinium spp. and that dominated by C. vulgaris.

• Climate change modelling based on the Cambridge Metapopulation Epidemic Model would allow assessment of the potential long term impact of climate change on Phytophthora infection.

• Further review of the life cycle stage and timing of dependence of ‘primary consumers’ on the host species, would refine the assessments of species sensitive to the loss of host plants.

• More detailed assessment could be made of the indirect effects of Phytophthora infection and control as a result of potential habitat loss and vegetation community or structural change.

• These direct and indirect effects on other species could be assessed on the basis of areas that are likely to be affected under model predictions in order to better target resources.

• The scale (with respect to both area and timeframe) of infection and treatment will be very important in determining the scale of impacts of Phytophthora on host species and associated species. Therefore field monitoring of community response to infection and control is important to set the potential effects outlined here in the context of the likely effects.

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