Tree Pathology in a Changing World

Critical Essay: Silviculture in a changing world–a case study:

Impacts of tree pathology on silviculture in the UK and Ireland

1. Introduction

Epidemics of tree diseases such as Dutch Elm Disease (DED) in the UK (Lamb 1979) and Chestnut blight in the US may represent the most profound and sudden cases of irreversible environmental change in recent times (Potter et al 2011). Since 2012 the public’s awareness has been drawn to the threat to one of Britain’s principle landscape trees, the ash tree, from Chalara fraxinea (Rackham 2012).

Trees in the landscape provide valuable ecosystem services including erosion control and greater infiltration rates for floodwater, which are lost or impaired due to disease or mortality (Broadmeadow and Nisbet 2010). Disease can also have significant economic impacts for forestry and timber production. Beyond economic issues, loss of trees on such a scale carries great cultural implications. This essay will consider the need for silviculture to adapt to new challenges from current and novel diseases.

2. Definitions

Silviculture has been defined as:

The art and science of controlling the establishment, growth, composition, health and quality of stands to meet the diverse needs of landowners and society on a sustainable basis

(Nyland, R.D. 2002 Silviculture Concepts and Applications 2^nd edition, McGraw-Hill, New York, cited in Castello and Teale 2011).

Pathology can refer to damage and ill-health in trees from both biotic and abiotic causes (Smith 1970; Strouts and Winter 1994).

Abiotic causes include physical damage from fire, wind or floods; mechanical or chemical damage, for example from landscaping machinery;

biotic causes of ill-health include damage from animals herbivores and rodents. In particular, squirrels and deer have become major pests in the UK, impacting both amenity and commercial forest trees to the extent that it may be becoming economically unviable to grow quality timber hardwoods in this country (ICF 2015). Nematodes, viruses, and bacterial and fungal infections can cause disease leading to decay and death.

3. Current and Historical Threats

The major incidence of tree pathology in modern times in the UK is the Dutch Elm Disease (DED) responsible for the death of between 20 and 30million English elms from 1970-1980 (Potter et al 2011) including over 75% of elms in southern (Smith et al 1988). The fungal pathogen responsible Ophiostoma ulmi was first identified in the 1920s on continental Europe. The fungus is spread principally by the large elm bark beetle Scolytus scolytus  that overwinters in dead and decaying wood and moves to healthy trees in the spring. The fungus can also be transmitted through the roots of suckering species.  Earlier outbreaks had been containable and the later outbreak was at first thought to be merely another upsurge. The more virulent strain Ophiostoma novo-ulmi is believed to have been introduced to the UK on logs imported from Canada.

Elm trees have demonstrated the ability to shoot back from remaining live roots but the fungus also survives for many years in the old wood and returns to kill new growth on a 15-20 year cycle (Gibbs et al 1994).

Pockets of elms have survived, for example in east Sussex. The principle method of control to preserve them has been sanitized felling (Wainhouse 2005). This is costly and involves ongoing and sustained commitment to fell and remove any infected trees in the vicinity to prevent infection (Gibbs et al 1994).

Apart from DED and other diseases already present, a number of other diseases have entered the country in recent decades (Maynard and Allen 2012), mainly as a result of imports on either infected timber products or plant material, including:

• the great spruce bark beetle (Dendroctonus micans) and the green spruce aphid (Elatobium abietinum). Britain’s principle forestry tree Picea sitchensis has so far proved remarkably resilient to these known pests but a warming climate could lead to much more serious attacks (Cameron 2015);
• Cryphonectria parasitica sweet chestnut blight- killed the majority of American chestnuts Castanea dentata (some 3.5 billion trees) in the Eastern US in the early 20^th Century; the European chestnut C. sativa is less susceptible though the disease is also prevalent on continental Europe;
• Phytophthora cactorum and citricola- “Bleeding canker”-this now affects more than 70% of Horse Chestnut Aesculus trees in some parts of England and is likely to also affect Tilia, Acer, Betula, Quercus and Salix (Strouts and Winter 1994);
• Dothistroma Red Band Needle Blight was recorded on all Corsican pine stands in England by 2006, with lodgepole pine and Scots Pine also being at risk (Brown and Webber 2008, FC 2016);
• Phytophthora ramorum “Sudden Oak Death” has not affected oak yet in Britian but has been found on increasingly large numbers of Japanese Larch Larix kaempferi stands across England, Ireland and Scotland from 2009 (IBID) resulting in compulsory phytosanitary controls and sanitation felling;
• Acute Oak Decline (AOD) has occurred in Britain periodically with outbreaks lasting 5-10 years; the syndrome is caused primarily by Armillaria (Honeyfungus). The current outbreak is affecting several thousand mature trees across southern England, with high mortality rates.

4. Economic Impacts

CONFOR (2006) put the total gross value added directly and indirectly by all forest industries at £26.4billion, supporting 2.5% of the UK economy (CONFOR 2006).

Economic impacts from tree pathology are significant. A 2010 report by the Centre for Agriculture and Biosciences International put the total annual cost to forestry in England, Scotland and Wales from all causes including pests, diseases, clearance of non-native invasive species such as Rhododendron ponticum (which is also a host species for Phytophthora ramorum), and quarantine measures including sanitation felling to be over £100million; although £70million of this was calculated to be the cost of rabbit damage and control, and a further £10million for squirrel damage and control (Williams et al 2010).

Red band needle blight on Corsican pine has affected the majority of stands throughout Britain, equating to a 30% yield loss, amounting to a total direct loss in timber value of £756,000 Eradication efforts on the US have cost in excess of $1billion, but with limited effectiveness (Williams et al 2010).

DEFRA (2013) put the annual commercial value of ash to be £22million, a relatively small part of the economy as a whole. While only 20%-30% of ash woodlands are currently managed for timber, with ash products being primarily used for construction and furniture, fence posts, firewood and charcoal- ash is the principle hedgerow tree in England and of great cultural and environmental value (Mitchell et al 2014). DEFRA calculate the annual social and environmental benefits of ash trees at another £150million. This includes carbon sequestration, pollution mitigation, biodiversity habitat and recreational facilities. A total value for such ecosystem and social services of £1.8billion is given for UK woodlands.

5. Climate change

Warmer temperatures in some areas have been conducive to increased virulence of some pests and diseases (Raffa et al 2008). Climate change impacts include seasonal changes with earlier springs and shorter winter cold periods. Phenology change in oak shows flushing has been occurring on average two weeks earlier over last 30 years in Britain (FC 2008); wetter summers with consequent waterlogging common in the growing season has lead to stress and increased incidence of honey fungus.  Oak leaf roller moth has increased during wet summers. (Jones 2015).

A warmer climate could also benefit tree welfare for some conditions through natural selection. Smith (1970) suggests that some decline and dieback conditions may be a result of trees ongoing adaptation to long-term climate changes. This thesis is complicated by the evidence that tree species may still be migrating slowly northwards as a result of residual warming since the end of the last glaciation. (Svenning and Skov 2007), and the confluence of such natural variation with anthropogenic warming is uncertain.

It has been estimated that, partly as a result of increased susceptibility to pests and disease, timber yields in England could be reduced by more than a third under a high CO2 emissions scenario by 2080. (DEFRA 2012].

 

5. General management issues

 Poor management and conflicting landowner objectives can increase disease risk. The management of farm woodlands for scrub needed as pheasant shoots can lead to overstocking and poor crown development (GWTC 08-01-2016). Where firewood is taken, the better, straighter trees are often taken leaving the poorer and possibly less resilient trees.

Restocking may be from inappropriate seed sources, such as if collected from lowland stands for planting in upland areas with very different climatic and soil conditions. Improved birch trees produced in the dryer east of the country have not proved suitable for the wetter western parts.

Chestnut became more susceptible to Phytophthera when planted in clay soils that were more suitable for oak (Jones 2015).

5. Changes to silvicultural practice

Some recent changes in silvicultural practice may carry their own risks. There is evidence that the recent move to continuous cover forestry has lead to an increase in the incidence of honey fungus (Webber and Evans 2004). Other changes in silviculture may be needed as a response to disease threats:

Monitoring

The United Nations Economic Commission for Europe initiated co-ordination of forest health monitoring in 1985, based initially on monitoring visible crown health as an indicator of the condition of the trees. This system may not always be of sufficiently high resolution to monitor the cyclic nature of some diseases. Oak decline is known to be episodic, occurring repeatedly between 1910 and 1940, and again after 1987 and 1997, and lasting typically around 10 years. The disease is a result of a combination of circumstances; most notably severe insect defoliation combined with two or more years of climate extremes (such as drought). The European forest health monitoring system in operation uses standard measures of crown condition, but may use too coarse a sampling method to reveal such patterns with cycles of 10 years or less (Castello and Teale 2011). Periods of severe oak decline may lead to changes in the age structure and species composition of stands, but the difficulty in predicting the next outbreaks and uncertainty of their causes makes management decisions much harder.

Exclusion

The rapid expansion of global trade in plant materials for the forestry and horticultural industries, and particularly within Europe since the creation of a common market, has played a major role in the increase in plant pathogens arriving in Britain (Bolte et al 2009; Castello and Teale 2011; Rackham 2014; Jones 2015). There are concerns that new and more virulent pests and diseases, such as the Emerald Ash Borer Agrilus planipennis, already a serious pest in North America, will inevitably find their way to Britain without much stronger controls being put in place (Rackham 2014).

To remedy this it would be necessary to place severe restrictions on trade in all plant materials, admitting only those that have undergone a strict inspection process. This could lead to a boost in the indigenous nursery industry. More controls and regulations are also needed to address the issue of pests being imported on timber packaging, which are often only discovered once they are at their final destination, arriving in sealed containers (Jones 2015). The decline in the number tree pathologists in recent years would need to be reversed to provide sufficient professional expertise for early identification and control at entry points. (Rackham 2014, Maynard and Allen 2011).

In addition, Rackham (2014) blames unregulated and poorly informed conservation groups enthusiasm for tree planting during the 1970s’ “plant a Tree in ‘73” campaigns, which lead to over-enthusiastic tree-planting projects with little regard for the provenance of the stock. Developing an understanding that “new trees can kill old trees” through the spread of pathogens is of paramount importance in terms of public environmental awareness and education.

Direct controls

Once present, tree pathogens tend to be very hard to eradicate due to the rapid increase in pest populations and the spread of fungal spores on the wind. It is believed that Chalara in Ireland for example, although primarily found on new plantations, has also crossed the North Sea from Wales or Scotland on the wind (DARD and DAFM 2013). In some of the cases reviewed above affected species, including Fraxinus, Larix and Corsican pine (Pinus nigra ssp. laricio) are no longer viable as forest species (Wentworth 2011). Moratoria exist for the movement of all plant material of these species to prevent or slow the spread of the disease.

Direct methods of controlling pest and disease outbreaks include:

• applications of fungicides;
• the treatment of freshly cut pine stumps with urea or the competing saprophyte Peniophora gigantea to prevent their colonization by Heterobasidion annosum and the subsequent infection of surrounding trees by root contact with infected stumps (Smith et al 1988);
• Integrated Pest Management (IPM) methods such as pheromone traps, pest-predator attractants, shelterbelts and barrier species (Jactel et al 2005). These can be expensive and often only viable for small numbers of highly valued individuals.

While such controls can be effective, there will generally be a constant threat of re-infection from outside the controlled population.

Different silvicultural methods have been advocated for limiting certain conditions. Choice of site, rotation length and species selection are all important factors in limiting incidence of disease or build-up of pathogens (Smith 1970).

Statistical analysis methods such as survival analysis and crown condition indices can be used to determine which trees under which conditions have the greatest likelihood of survival (Edmonds et al 2011).

The most commonly used method of direct control used for epidemic outbreaks is sanitation felling. This may take the form of felling small blocks of infected trees or felling corridors of trees to preempt the spread from infected stands; or clear-felling of whole areas once infection is detected.

Sanitation felling can be costly and also controversial. A recent example is the case of olive trees in Greece infected with the bacterium Xylella fastidiosa, an infection first identified in Europe in 2013. Opposition to sanitation felling- involving the destruction of hundreds of olive trees, many over 100 years old, resulted in the practice being halted and several scientists being charged with spreading the disease themselves (SCI_AM 2015). The felling of a stand of European larch in West Cork in 2014 also lead to opposition from local environmental groups who did not accept the need for such action (Indymedia 2014). Quarantine felling also often falls to landowners and thus is hard to ensure it has been carried out effectively.

Indirect Controls- species diversification

While there is no simple relationship between complexity and stability or resilience (Murdoch 1975) there is some evidence that a diversity of tree species can reduce pest infestations (Jactel et al 2005, Bolte et al 2009) though the precise species mix may be more important than diversity per se (Koricheva 2005). Species diversity is of limited value in the case of polyphagous pest insects as these can jump from one species to another, or attack multiple species. Current Forestry Commission policy also favours greater diversification, with mosaics of clumps of conifers and broadleaves (FC 2006).

Indirect controls- thinning

Thinning can provide the remaining trees with more water, light and nutrients and disrupt beetle communication by increasing wind and air circulation but little research exists on long-term effectiveness. Different thinning regimes are showing some promise for control of red band needle blight on Corsican pine in the UK (Brown and Webber 2008), and thinning is the dominant indirect control method in the case of extensive pine mountain beetle infestations in North America (Six 2014).

Some researchers have argued that such indirect methods of control have exacerbated incidence of disease by creating the environmental conditions that favor such pest and disease outbreaks (Wainhouse 2005, Six 2014). Changes to fire regimes by suppressing fire outbreaks that might break pest cycles, increasing intensity of forest management, selection of fast-growing seedlings without concern over disease-resistance (Castello and Teale 2011) or decreasing shade through overstorey thinning (Wainhouse 2005) are all ways in which disease and pests may be increased.

Indirect control by thinning tends to select for even-aged and even-spaced trees and includes the removal of advanced regeneration resulting in fairly homogenous stands which themselves are more likely to be susceptible to future outbreaks. (Six 2014). An alternative but more long-term approach that may be gaining currency is adaptation.

Adaptation

Adaptation to disturbance is an inherent part of forests ecosystem development, with larger natural disturbances such as high mortality from disease potentially leading to new emerging states (Puettman et al 2009). In the sense referred to by Six (2014) silvicultural practices could learn from such adaptations.

In contrast to thinning by humans, pests such as beetles drive a natural selection process. Despite more than 90% losses from sustained beetle outbreaks in North America, exacerbated by recent years of sustained higher temperatures, a proportion of mature trees survive apparently with no beetle damage at all, the most likely reason being genetic resistance. The more clumpy, mosaic pattern left from this natural selection exhibits greater diversity, with sufficient advanced regeneration and multiple-age stands with greater resistance to fire as well as future insect attacks, and much better genetic resistance. (Six 2014, 2016).  Such diversity of forest structure is also being recommended now for adaptation to abiotic stress such as windthrow in upland conifer plantations (FC 2006). Such an approach is also congruent with recent research on continuous cover forestry (CCF) and low-impact silvicultural systems (LISS) (Forest Research).

In the case of pests such as bark beetles, diversity of age and stem diameter class, as tends to happen with natural selection and adaptive approaches, may be more important than diversity of species (Koricheva et al 2005). Small diameter trees are less affected, while mature, larger trees tend to be more resilient until certain tipping points of beetle populations are reached (Six 2014).

DEFRA (2013) make similar recommendations for adaptation with regard to Chalara in ash, arguing that short-term mitigation is a false economy and a wiser policy would be to plan for a world where most ash is infected in 15-20 years time. Measures should include improving deer-control to aid natural regeneration; earlier harvesting; and selecting and breeding resistant varieties, potentially including the use of genetic engineering as is being developed for the north American chestnut (New Scientist 2014).

6. Conclusion

Risks to forestry, semi-natural woodlands and amenity trees from novel and more virulent pathogens have increased considerably in recent decades. Responding to existing pathogens will require a range of short-term and local direct controls and more long-term adaptive changes in silvicultural practice.

The consequences of inaction are likely to be severe. Dominant species such as Castanea dentata in the US and English Elm Ulmus procera have all but disappeared, with the same fate potentially threatening Fraxinus excelsior and important plantation species such as Pinus nigra. Adjustment to ongoing threats of new incoming diseases will require far-reaching policy changes including stricter phytosanitation regulations and ultimately changes in the global trade of plant materials.  Greater efforts in funding, public education and monitoring will all be necessary. None of this will be easy or politically expedient and will require international cooperation and possibly new monitoring bodies to be created.

References

 Broadmeadow,S. and Nisbet, T. 2010. Opportunity Mapping for Woodland to Reduce Flooding in the River Derwent,  Cumbria. Forest Research, UK.

Bolte, A., Ammer, C., Löf, M., Madsen, P., Nabuurs, G.-J., Schall, P., Spathelf, P. and Rock, J. 2009. Adaptive forest management in central Europe: Climate change impacts, strategies and integrative concept. Scandinavian Journal of Forest Research 24(6), pp. 473–482.

Brown, A. and Webber, J. 2008 Red Band Needle Blight of Conifers in Britain Forestry Commission Research Note  June 2008

Cameron, A.D. 2015 Building Resilience into Sitka Spruce (Picea sitchensis (Bong.) Carr.) Forests in Scotland in Response to the Threat of Climate Change Forests 2015, 6, 398-415

Castello, J.D. and Teale, S.A. 2011 Forest Health- An Integrated Perspective Cambridge University Press

CONFOR 2006 The economic contribution of the forest industries to the UK economy Centre for Economics and business Research Ltd. available from: http://www.confor.org.uk/Upload/Documents/22_economic_contribution_of_the_forest_industries_report_June_2006.pdf

DARD and DAFM 2013 All Ireland Chalara Control Strategy Department of Agriculture, Food and the Marine https://www.agriculture.gov.ie/media/migration/forestry/ashdiebackchalara/AllIrelandChalaraControlStrategyJuly13.pdf

DEFRA 2012 [ONLINE] Independent Panel on Forestry- Final Report available from https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/183095/Independent-Panel-on-Forestry-Final-Report1.pdf [Accessed 07-01-2016]

DEFRA 2013 Chalara in Ash Trees: A framework for assessing ecosystem impacts and appraising options

Department of Environment and Rural Affairs [ONLINE- ACCESSED 06-01-2016] https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/200396/pb13906-chalara-socio-economic-framework.pdf

Edmonds, R.L., Agee, J.K., Gara, R.I., Forest Health and Protection Waveland Press 2^nd edition

FC 2006 Managing Mixed Stands of Conifers and Broadleaves
in Upland Forests in Britain Forestry Commission Information note http://www.forestry.gov.uk/pdf/FCIN083.pdf/$FILE/FCIN083.pdf

FC 2008 The Environmental Change Network at Alice Holt Research Forest Research Note http://www.forestry.gov.uk/pdf/FCRN001.pdf/$FILE/FCRN001.pdf

FC 2016a [ONLINE] Top Tree Diseases http://www.forestry.gov.uk/forestry/BEEH-9XLGXD  [ACCESSED 05-01-2016]

Forest Research [ONLINE] Impact of pests and pathogens under changing management [ACCESSED 11-01-16] http://www.forestry.gov.uk/fr/managementpestimpact

Gibbs, J., Brasier, C., Webber, J. 1994 Forestry Commission Research Information Note No. 252

Griess, V.C. and Knoke, T. Growth performance, windthrow, and insects: meta-analyses of parameters influencing performance of mixed-species stands in boreal and northern temperate biomes Canadian Journal of Forest Research 41(6), pp. 1141–1159

 GWTC [ONLINE] History of Woodland Management for Pheasants Game and Wildlife Conservation Trust [ACCESSED 08-01-2016] http://www.gwct.org.uk/game/research/species/pheasant/history-of-woodland-management-for-pheasants/

Indymedia 2014 [ONLINE] Coillte Forestry Fables In Regard To Tree Felling At Gougane Barra Heritage Site [ACCESSED 07-01-2015] http://www.indymedia.ie/article/104976

Jactel, H., Brockerhoff, E., Duelli, P. 2005 A Test of the Biodiversity-Stability Theory: Meta-analysis of Tree Species Diversity Effects on Insect Pest Infestations, and Re-examination of Responsible Factors Ecological Studies, Vol. 176
M. Scherer-Lorenzen, Ch. Körner, and E.-D. Schulze (Eds.) Forest Diversity and Function: Temperate and Boreal Systems Springer-Verlag Berlin Heidelberg 2005

Jones, C., 2015 [Personal Communication] Natural Resources Wales Presentation given at Institute of Chartered Foresters conference Thirty Years of Broadleaf forestry- A need for Change? North Wales November 2015

Koricheva, J., Vehviläinen, H., Riihimäki, J., Ruohomäki, K., Kaitaniemi, P., and Ranta, H. 2005 Diversification of tree stands as a means to manage pests and diseases in boreal forests: myth or reality? NRC Research Press

Lamb, R. 1979 World Without Trees- Dutch elm disease and other human errors Wildwood House London

Maynard, R. and Allen, S. 2012 The Threat to England’s Trees from Invasive Non-Native species of Pests and Disease. Briefing from Zac Goldsmith MP and the Countryside Restoration Trust

Mitchell, R.J., Bailey, S., Beaton, J.K., Bellamy, P.E., Brooker, R.W., Broome, A., Chetcuti, J., Eaton, S., Ellis, C.J., Farren, J., Gimona, A., Goldberg, E., Hall, J., Harmer, R., Hester, A.J., Hewison, R.L., Hodgetts, N.G., Hooper, R.J., Howe, L., Iason, G.R., Kerr, G., Littlewood, N.A., Morgan, V., Newey, S., Potts, J.M., Pozsgai, G., Ray, D., Sim, D.A., Stockan,J.A., Taylor, A.F.S. & Woodward,S. 2014. The potential ecological impact of ash dieback in the UK. JNCC Report No. 483

Murdoch, W.W., 1975 Diversity, Complexity, Stability and Pest Control Journal of Applied Ecology Vol. 12, No. 3 (Dec., 1975), pp. 795-807

New Scientist 2014 [ONLINE] [ACCESSED 09-01-2015] Into the Wildwood http://www.economist.com/news/science-and-technology/21577033-gm-species-may-soon-be-liberated-deliberately-wildwood?fsrc=scn/tw_ec/into_the_wildwood

Potter, C., Harwood, T., Knight, J., Tomlinson, I. 2011 Learning from history, predicting the future: the UK Dutch elm disease outbreak in relation to contemporary tree disease threats Phil. Trans. R. Soc. B (2011) 366, 1966–1974

 Puettmann, K.J., Coates, K.D., Messier, Christian 2009 Critique of Silviculture- Managing for Complexity

 Rackham, O. 2014 The Ash Tree Little Toller Books, Dorset

SCI-AM 2015 [ONLINE] Italian Scientists under Investigation after Olive-Tree Deaths Scientific American Dec 22^nd 2015  [ACCESSED 07-01-2016] http://www.scientificamerican.com/section/nature/italian-scientists-under-investigation-after-olive-tree-deaths/?wt.mc=SA_Twitter-Share

Six, D.L., Biber, E., Long, E. 2014 Management for Mountain Pine Beetle Outbreak Suppression: Does Relevant Science Support Current Policy? Forests 2014, 5, 103-133; doi:10.3390/f5010103

Six, D.L. 2016 [ONLINE] Interview How Science can help halt the western bark beetle plague [Accessed 07-01-2016] http://e360.yale.edu/feature/how_science_can_help_to_halt_the_western_bark_beetle_plague/2944/

Smith, I.M., Dunez, J., Lelliott, R.A., Phillips, D.H., Archer, 1988 S.A. European Handbook of Plant Diseases Blackwell Scientific Publications

Raffa, K.F., Aukema, B.H., Bentz, B.J., Carroll, A.L., Hicke, J.H., Turner, M.G., and Romme, W.H., 2008
 Cross-scale Drivers of Natural Disturbances Prone to Anthropogenic Amplification: The Dynamics of Bark Beetle Eruptions BioScience, 58(6):501-517. 2008.

Smith, W.H. 1970 Tree Pathology: A Short Introduction Academic Press (London)

Strouts, R.G., Winter, T.G. 1994 Diagnosis of ill-health in trees Forestry  Commission, Research for Amenity Trees No.2

Svenning, J-C., and Skov, F.  2007  Could the tree diversity pattern in Europe be generated by postglacial dispersal limitation? Ecology Letters, (2007) 10: 453–460

Wainhouse, D. 2005 Ecological Methods in Forest Pest Management Oxford University Press

Webber and Evans 2004 Pests and Diseases  In: Forest Research Annual report and Accounts 2003-2004 pp. 30-39.  The Stationery Office: Edinburgh. http://www.forestry.gov.uk/pdf/FR0102pests.pdf/$FILE/FR0102pests.pdf

Wentworth, J. 2011 Invasive Tree Pests and Diseases Parliamentary Office of Science and Technology

[ONLINE- ACCESSED 06-01-16: http://researchbriefings.parliament.uk/ResearchBriefing/Summary/POST-PN-394%5D

Williams, F., Eschen, R., Harris, A., Djeddour, D., Pratt, C., Shaw, R.S., Varia, S., Lamontagne-Godwin, J.,Thomas, S.E., Murphy, S.T.  2010 The Economic Cost of Invasive Non-Native Species on Great Britain Centre for Agriculture and Biosciences International