The new Pest Risk Analysis for <i>Tilletia indica</i> , the cause of Karnal bunt of wheat, continues to support the quarantine status of the pathogen in Europe

Abstract

Tilletia indica, the fungus that causes Karnal bunt of wheat, is listed as a I/AI quarantine pest for the European Union (EU) (Anon., 2000a). This means that it is considered absent from the EU, is potentially damaging and so its entry into the EU is banned. This listing was the result of a Pest Risk Analysis (PRA) (Sansford, 1996, 1998), which considered the potential for the pathogen to enter, establish and cause unacceptable impacts in the UK/EU following the first reports of the disease in the USA in 1996 (Ykema et al., 1996). This PRA was updated in 2004 (Sansford, 2004) and recently fully revised (Sansford et al., 2006) for the EU. This new EU-PRA continues to support the view that T. indica has the potential to enter, establish and cause unacceptable economic impacts throughout much of the wheat-growing area of the EU. Two recent papers (Jones, 2007a,b) have challenged these tenets and the new EU-PRA. In this letter, we summarise the work of a 4-year collaborative study and address the key points made by Jones (2007a,b) and refute his conclusions, particularly regarding (i) past opportunities for entry to Europe; (ii) the climatic requirements for the completion of the lifecycle of T. indica, leading to the disease Karnal bunt; (iii) inoculum thresholds; (iv) the potential economic damage caused by the disease in Europe; and (v) the cost of control. The full findings of the study can be accessed online (http://karnalpublic.pestrisk.net/) together with published accounts of teliospore survival and germination in Europe (Inman et al., 2008) and susceptibility of European wheat cultivars to T. indica (Riccioni et al., 2008). Tilletia indica is a floret-infecting smut pathogen of wheat (Triticum aestivum and T. durum) and triticale (×Triticosecale) causing the disease Karnal or partial bunt. Records on triticale are rare. The pathogen has not been reported in Europe. The full life cycle of the pathogen is reviewed in Carris et al. (2006). Key aspects of the lifecycle, which are relevant to the EU-PRA, include the following: In areas where T. indica is established, the pathogen survives as teliospores in the soil for up to 5 years (Agarwal et al., 1993). Fresh teliospores typically have a period of dormancy before they will germinate; only those on or very near to the soil surface break dormancy (Nagarajan et al., 1997). Germination of teliospores leads to an epiphytic phase involving the cycling of sporidia. Infective sporidia deposited on the flag leaf of wheat and washed into the boot cavity, or deposited directly on the emerging ear of wheat plants at the susceptible stage for infection, can under suitable climatic conditions infect the developing grain through the glumes. Warham (1986) indicated that low (moderate) temperatures and high humidity are necessary for infection to occur, while dry weather, high temperatures and bright sunshine are unfavourable. This is supported by studies in India (e.g. Nagarajan et al., 1997; Singh et al., 2003; Duhan et al., 2004; Kaur et al., 2005). Successful infection of wheat leads to production of teliospores which are restricted to the pericarp layers of the seed (Goates, 1988). Infected seeds are usually only partially colonized and, within a wheat ear, not all grains necessarily become infected; hence the alternative disease name of partial bunt. At harvest, teliospores of T. indica are usually dispersed locally from bunted grain by the mechanical action of harvesting. Long-distance dispersal occurs through the movement in trade of infected or contaminated seed for sowing or grain for consumption/processing. The finding of T. indica–infected crops in the USA in 1996 (Ykema et al., 1996) established a significant new origin on an existing trade pathway for entry into Europe. Wheat had been imported into Europe from the USA before 1996, but in the absence of the pathogen in the USA, there appeared to be no risk of entry along this pathway. Since 1996, there have been several reported or suspected interceptions of T. indica on wheat imported from India into Poland and the UK, from Mexico into Italy and from the USA into Greece (Sansford et al., 2006). The establishment of the significant new trade pathway for T. indica from the USA into Europe initiated a UK PRA (Sansford, 1996, 1998). The UK-PRA findings suggested that the pathogen could enter, establish and cause economic damage in the UK/EU. As a result, T. indica was added as a quarantine pest to the European Commission (EC) Plant Health Directive 77/93/EEC (now 2000/29/EC) in 1997 (Anon., 2000a). It was the first fungal pathogen and the only pathogen of cereals to have been added to the list since the Directive came into force. The EC Directive applies minimal quarantine requirements to seed and grain of Triticum, Secale and ×Triticosecale from countries where T. indica is known to occur (currently listed in the EC Directive as Afghanistan, India, Iran, Iraq, Mexico, Nepal, Pakistan, South Africa and the USA). The EC requirements are for area freedom for exports of seed from countries where T. indica occurs and area or place of production freedom for grain, the latter being based upon crop inspection and sampling and testing of grain for T. indica at harvest and pre-export. Rye (Secale cereale) is to be considered for deletion from the EC Plant Health Directive because it is no longer considered to be a natural host. Because data were not available on the behaviour of the pathogen in the UK/European Union (EU), such as teliospore survival, dormancy, germination and host susceptibility, the earlier UK-PRAs (Sansford, 1996, 1998) formulated conclusions from the existing biological information in the available literature. Subsequently, there has been much international debate as to whether T. indica poses a risk to wheat production and whether it should be listed as a quarantine organism by any country or Regional Plant Protection Organisation (e.g. Malik & Mathre, 1998). Some (e.g. Rush et al., 2005) contend that T. indica does not have significant effects on yield or quality and that its main effect is in the loss of export markets for countries where it occurs. In addition some scientists think T. indica has low invasive potential (e.g. Garrett & Bowden, 2002). If these opinions were correct T. indica might not be considered to fulfil the definition of a quarantine organism and in such circumstances would not be regulated. The prediction of the likelihood of T. indica completing its life cycle and establishing in wheat crops in the EU, as determined in the EU-PRA (Sansford et al., 2006), depends on four stages: A suitable pathway between origin and destination. The presence of susceptible host crops at the destination. The ability of the pathogen to survive between crops. The ability of the over-wintering phase of the pathogen (teliospores) to produce infective sporidia at the vulnerable growth stages for infection and under appropriate conditions to infect and cause disease. For the first stage, records of cereal imports from countries where T. indica occurs were examined, together with evidence of interceptions of T. indica over the past 10 years. The other three stages were investigated by experimental work and a review of the literature. Together, and through a multidisciplinary approach, an EU-PRA was produced (Sansford et al., 2006). The risk of establishment of T. indica in the wheat-growing areas of the EU has been estimated and mapped (Ewert et al., 2002; Baker et al., 2004, 2005) by combining crop phenology models (Porter et al., 2002) for bread and durum wheat with a disease model, the Humid Thermal Index (HTI) (Jhorar et al., 1992). The outputs were interpreted in light of the results of studies on teliospore survival and germination under European conditions (Peterson et al., 2006; Inman et al., 2008) and an evaluation of the susceptibility of European wheat cultivars (Riccioni et al., 2008). In addition, the potential socio-economic impact of T. indica in the EU arising from a small and a large outbreak scenario in a wheat-growing area of the UK was determined (Brennan et al., 2004a,b). The EU-PRA accounted for the results of these studies and concluded that T. indica should continue to be listed as a I/AI quarantine pest for the EU. Two recent papers (Jones, 2007a,b) have challenged the findings of the EU-PRA. In the first the author suggests that there is a low risk of establishment of T. indica for Europe, contrary to the view of the EU-PRA. Furthermore, Jones (2007b) concludes that T. indica does not warrant the status of a quarantine pest for Europe and considers that there should be "A reappraisal of the quarantine significance of T. indica by world plant health authorities ...". The following points are not a full review of these papers nor do they represent the full scope of the collaborative work undertaken to develop the EU-PRA, but they address the key points made by Jones (2007a,b). Jones (2007a) surmises that wheat seed contaminated with teliospores of T. indica has been sent into Europe over many years and therefore in the absence of any outbreaks of Karnal bunt there is a low risk of establishment. Jones (2007a) takes this as evidence that conditions are unsuitable. However, there are no specific data or evidence supporting the contention that there have been "numerous" opportunities for T. indica to enter or spread in Europe. Jones (2007a) presented new information (a personal communication from CIMMYT – the International Maize and Wheat Improvement Centre, Mexico) on shipments of wheat seed from CIMMYT for use in nursery trials in "24 European countries" (naming only England, France, Greece, Italy, Spain and Wales) but with no data from the receiving organisations, or on the health status of the seed, assuming that this seed was contaminated with teliospores. No evidence was given in Jones (2007a) as to whether the receiving organisations planted the seed in the field or the glasshouse. Nevertheless, Jones (2007a) uses this to express a view that the risk of establishment in EU countries is low, rather than high. Jones (2007a) proposes that Karnal bunt occurs only where the climate is solely "hot arid" or "semi-arid". This view seems to arise from the Indian usage of 'semi-arid', which is applied in India with annual rainfall of 400–800 mm. For example, Chausaria et al. (1991) described wheat production in Ludhiana, a "semi-arid" area of the Punjab, and noted that the average annual rainfall is 700 mm a year, with temperatures in the growing season (November to April) of 20 to 30°C (day) and 6 to 18°C (night). The general meteorological usage of 'semi-arid' refers to areas where there is some moisture stress to plants during the year and so it depends on rainfall distribution relative to evaporation (American Meteorological Society, undated), or more simply to areas with annual rainfall of 250–500 mm (Anon., 2006a). Areas of India with high incidence of Karnal bunt (Gill et al., 1993; Sharma et al., 2004) have annual rainfall of 500–1000 mm, while the incidence declines as the rainfall falls below 500 mm and seasonal temperatures are higher. An up-to-date review of the disease prevalence and severity in India by state is provided in Sansford et al. (2006). Europe has many areas with similar annual rainfall to India (Encarta, undated), although the seasonal pattern of rainfall varies (USDA, undated). Wheat needs moisture in order to grow, whether this comes from rainfall or irrigation or a combination of both. Parts of India produce wheat under irrigation, with the amount used, as with other wheat-growing areas of the world, varying with the available moisture during the growing season. Jones (2007a) does not mention that in the areas of India where Karnal bunt occurs, wheat is frequently grown in rotation with summer-irrigated crops such as rice and soybeans (G. Murray, unpublished data). Teliospores of the pathogen survive, ungerminated, in these wet soils between wheat crops, facilitating infection in the following wheat crop. Teliospores have also survived in summer-irrigated alfalfa fields in Arizona for at least 4 years (G. Peterson, personal communication). Survival for at least 3 years was recorded in wet European soils (Inman et al., 2008). Thus, rather than surviving just in dry soils, the teliospores also survive in wet soils in a range of locations. Jones (2007a) states that Karnal bunt is not found in (hot, dry) southern areas of India, but it would not be found in these areas as wheat is not grown there (Anon., 2000b). Jones (2007a) does not elaborate on the finding in Brazil even though it occurred in an area where the climate was neither hot nor semi-arid. et al. reported that T. indica was found in seed and that were in from the of the state of do to the (Anon., undated), the states of and do are for of wheat production and these states have a large of or The of do has a moisture to CIMMYT et al., of high rainfall 500 mm of with a Jones (2007b) suggests that in disease outbreaks are and This is because the of disease varies with the of the climate on an annual not because the be for as the author For infection of wheat to occur, the of teliospore germination and of the infective sporidia be in with the susceptible stage of the crop. et al. investigated the of this susceptible stage for European and durum wheat other reports (e.g. Nagarajan et al., which that the susceptible infection period is from the stage to the of growth stages – – – on the germination to produce occur at or before flag leaf for the infective sporidia to be available at the susceptible It is potentially for teliospores to earlier than this and for the stage to continue to cycle within the crop work published by suggests that sporidia might be more than teliospores that of the period for infection to produce sporidia which could cycle and be available at the susceptible stage to infect the host. Jones (2007a) is of the disease to the likelihood of establishment of T. indica in Europe, and to that it has been in for this in developing the EU-PRA. However, the prediction of the risk of establishment in the EU-PRA was based upon an of specific of the lifecycle in to its Thus, data were European wheat susceptibility were susceptible and some (Riccioni et al., teliospore survival under in the field in Italy, and the UK for at least 3 years and germination were and in the (Inman et al., and a study of the at which teliospores on the soil surface would under European climatic conditions to produce the infective sporidia. This (Peterson et al., 2006) was from the of wheat sowing to over 5 years for wheat growing in Mexico and The wheat sowing for the European and wheat in the for a in Mexico where the disease occurs. Jones (2007a) does not to this latter It was with soil (a with of three of the moisture and between the over a being at a which was in of field for this soil and known to be for germination of teliospores. soil was because that soil had no effect on the of teliospores. The teliospores that were were and so a would have at which was for a of teliospores of T. indica the period for Because such soil moisture conditions are to occur in wheat growing areas of Europe, an even of teliospores would be to in some soil moisture occur in Europe (Anon., germination of teliospores in a wheat crop even EU of soils more than and several on irrigation for production et al., The was with crop phenology models for bread wheat and durum wheat durum) phenology was in the EU-PRA to occurs between the susceptible stage of wheat and the meteorological within the range by the to be suitable for T. indica infection and disease of the experimental work and results are reported in et al. and Baker et al. a of the work is reported in et al. and in Baker et al. Jones (2007a) does not to this use of crop phenology models which have the prediction of the risk of establishment of T. indica in Europe. Jones (2007a) refers to of the three other disease the Index and the but not the of Nagarajan et al. that has been by other to the risk of establishment of T. reviewed all of the models and found the to be the suitable for to the risk of establishment in Europe for the stage of the life cycle that be investigated under field the period from from teliospores from to infection and the of teliospore of up found that the Index and the were while the was to & in the use of all the available models for the risk of establishment of T. indica in had concluded that the use of the as by Sansford 1998) was the appropriate for However, Jones (2007a) does not mention the study of The should be for the of the year wheat is between flag leaf through This will with seasonal conditions and to some with wheat and sowing In the EU-PRA, the was from leaf just to and as by Jones to wheat and durum wheat phenology models were to the of such based upon climatic data information wheat in Europe. were for several years period with the to high climatic the of European wheat cultivars being susceptible (Riccioni et al., the period of susceptibility determined et al., 2004) and in these within and the period over which the was The that teliospores the for infection of Jones (2007a) Sharma & that conditions in India germination of such that no infective sporidia are available at the period for infection, the does not However, this only occurred from to & Jones (2007a) does not to evidence provided by et al. which even under high soil moisture conditions for germination of some available and of germination at the for infection under a range of European field Jones (2007a) the work on the of teliospore germination in to wheat crop phenology and the was in the risk of establishment of T. indica in Europe. Jones (2007a) that there is a of teliospores below which infection and disease will not occur, but does not data to support a are in the literature. This has been made by & Bowden, 2002) and has been reviewed (Sansford et al., 2006) and & 2005) and is not supported by the Jones (2007a) states that there has not been a significant in the incidence and distribution of Karnal bunt in the USA in recent years and that the disease has spread very since it was first reported in However, this does not that teliospores of the pathogen have not been et al. soil sampling in wheat fields in USA in to the distribution of teliospores of T. indica in and areas the area teliospores were found in of the fields fields that had of disease. Since for T. indica in wheat grain of the areas have been based upon of Karnal bunt in small but not by for the pathogen T. et al. the from to to of into the USA based upon T. interceptions were made on wheat in Mexico and were at in and Arizona and in and and that the to enter the USA since at least not the first of a disease outbreak in the USA in 1996 (Ykema et al., 1996) and the of known specific requirements for infection and disease suggests a period of between and a established Rush et al. state that following the first of T. indica in the USA, of wheat by the Arizona of were for Karnal bunt and teliospores of T. indica were found in grain in that the disease had been in Arizona since at least disease is in and In it was to be (Anon., although this also past of contaminated wheat seed in combination with climatic conditions rather than natural upon these findings it seems that because of the ability of the pathogen to survive as teliospores before and the wheat crop to produce of it is not to where it has spread to within the It is also that establishment in Europe will be and to be the pathogen more & 2005). the of movement of T. indica from India where it was first described in has been the pathogen has to new from its origin in The between and is to have been & 2005). Thus, it was first reported as being in Mexico during the crop season in Brazil where it has been since at least et al., in the USA in 1996 (Ykema et al., and in South Africa in et al., where being to it spread to new areas in the country between and 2004 2002; Areas of in the prediction of the risk of establishment were in Sansford et al. and in the epiphytic stage of the fungus production and to infection of the host. This has been in a growing wheat crop under conditions and because of quarantine has not been in the Jones (2007b) that T. indica does not for the status of a quarantine pest in the EU or the and Plant Protection This is the view of the EU-PRA and is not the view of the EC or list it as a I/AI and from the and for by The an PRA before any are such as the listing of T. indica as a quarantine pest for the EU and its as a quarantine pest by In Jones (2007b) states (i) there is evidence to that T. indica not even establish in and (ii) yield caused by the pathogen are and disease are high to cause quality This is by the for its as an quarantine pest would to in the for trade should the pathogen be in an The latter is only of several economic effects that are considered in the it is for T. indica as a quarantine pest (Sansford et al., 2006). definition 2006) a quarantine pest pest of potential economic to the area and not or but not and being PRA is as of biological or other and economic evidence to whether a pest should be and the of any to be on the PRA can be found in that the work of the EU the and economic evidence that is for a PRA and the minimal EC that are at or the risk of entry of T. indica to the EU. As indicated Jones (2007b) is evidence to that T. indica not even establish in such evidence or through the of data data and PRA undertaken to produce the EU-PRA. by the author the origin of the quarantine in the USA but this is not relevant to the of risk to the EU and the quarantine status of the pathogen which is based upon a of the risk to the In developing a PRA to needs to be of and pest effects in the area potentially at For T. indica the effects include the effect on yield and quality and the effects include effects on export to or in and cost of and for and as as and other of these have been considered in the EU-PRA, but not fully by Jones Jones (2007b) the economic of by the of disease in In to Sansford et al. of disease incidence and severity are reported only and For example, data from India are the reported in any of the susceptible wheat cultivars have been grown (Gill et al., 1993; Sharma et al., 2004; Sansford et al., 2006) but are not reported by Jones Jones (2007b) states that Karnal bunt causes very yield loss and only small quality in countries where it is The yield are small in but can be high where they occur a large wheat production area (Sansford et al., 2006). The yield are small in countries where the pathogen is because the growing of susceptible wheat cultivars control. Jones (2007b) the of these for is and only can be year (Gill et al., 1993). addition of the for to T. indica in European would be and made a would the of for the of other Jones (2007b) states that yield would for T. indica to warrant quarantine pest status in the EU. this is so in countries growing susceptible the of in European wheat cultivars (Riccioni et al., 2008) suggests yield be than where Karnal bunt is are to of grain and grain and the presence of to the of disease and the Jones (2007b) based upon Warham that grain quality is only more than of grain is by T. in India that susceptible wheat cultivars are grown in areas that disease the of grain infection frequently and grain quality (Gill et al., 1993; Sharma et al., 2004; Sansford et al., 2006). experimental susceptible European wheat cultivars of disease infection (Riccioni et al., 2008). Furthermore, the quality requirements for wheat in European countries are to countries such as India, and in Europe there is of bunt or contaminated grain grown under such as those in the UK 2005). Jones (2007b) that grain infected with T. indica can be to the grain is before it is European grain which is known to be contaminated with T. indica is more to be and to The presence of bunted grain and teliospores of T. indica in European crops would This would a cost in addition to the loss of from wheat to A of the socio-economic impact an outbreak of Karnal bunt occurred in the EU was undertaken to support the EU-PRA (Brennan et al., 2004a,b). Jones (2007b) does not to the only and does not mention that the include the of a to the spread of T. indica from a Furthermore, the author on the that and were estimated to for over of the economic effect of an outbreak in the A of is in those is below and a of these were for is not in these but as would to should T. indica become established in Europe. include yield and wheat to include wheat to and export seed and quality with and and loss from yield from growing cultivars of crops of growing of grain of of grain and A economic unpublished considered a in with spread of the the and This the of on imports as much as any outbreak of disease. Thus, a outbreak with was estimated to cost over 10 years from the of being and the cost was If the spread were the EU the cost would be 10 full over 10 years. Thus, are large but be the T. indica or the EU. However, it is more to the pathogen which is the of the EC Jones (2007b) considers that and are in that they are a result of the international status of the pathogen as a significant quarantine This is not supported by the EU-PRA. The pathogen is a quarantine pest any other quarantine pest by definition such are as significant or The of T. indica as a quarantine pest for Europe was based upon the data available in 1996 and has been by the work to the EU-PRA of Jones (2007b) considers that the EC for T. indica place a on an countries Karnal bunt a over those that have the disease. However, the EC requirements are for T. indica, not Karnal are not in of the by which the requirements are and do not place any more of a than is for any other quarantine pest with EC with T. indica have not been from wheat to the EU under this EC The existing EC are In Jones (2007b) the of other countries in areas that are from the disease Karnal and has not that the EC is for freedom from the T. Jones (2007b) on upon grain for in as being in of grain teliospores of T. indica poses a significant risk since it in than seed wheat and teliospores of T. indica have the potential to into wheat production areas to its destination. Jones (2007b) that general of its quarantine significance to grain to be imported more into countries with where T. indica is to establish would with However, there is no evidence of with trade into Europe, nor are there data to support a view that there are wheat-growing countries in Europe with where T. indica is to Jones (2007b) also trade be restricted for This does not the that there have been no trade to in Europe on wheat or of the other listed from countries where T. indica occurs, nor it is In it is contention that the EU-PRA for T. indica (Sansford et al., 2006) continues to support the view that the pathogen has the potential to enter, establish and cause unacceptable impacts in the wheat-growing areas of Europe. This the status of T. indica as a quarantine pest for Europe and the minimal requirements that are in place in European countries and which are at The collaborative that supported the of a new EU-PRA for Tilletia indica for Europe was in under the European Commission bunt