This past year the SON Regulatory Committee Pest List Working Group had a project for “Creation of a List of Exotic Nematode Plant Pests of Agricultural Significance to the United States”.  This list was presented at the FINC in Tenerife and has been posted at along with requests for comments from the SON membership and other interested nematologists. Below is a summary of the comments that were received and the actions that have been taken in response to them. The working group is soliciting any comments you may have on the actions that have been taken to date. Action is pending on comments that were received for several nematodes (Anguina funesta, Anguina tritici, and Bursaphelenchus mucronatus) because the working group decided that the questions that have been raised require additional literature review and further evaluation that will include assistance and comments from nematologists who work closely with these pests. 

Below is a summary of the comments and actions for which the SON Pest List Working Group is requesting your evaluation and comments. A good number of SON members sent complimentary comments on the working group’s efforts on the Pest List. Although these comments are not listed here, the working group appreciates very much the encouragement and support we have received from the SON membership. 

Meloidogyne partityla

 Comments by Mike McClure, University of Arizona, Tucson, AZ.

The regulatory committee may want to consider adding Meloidogyne partityla to the list of nemas with limited distribution.  So far as I know, it occurs mainly in Texas, New Mexico, and Arizona where it causes serious losses on pecans.

 Comments by Andrew Nyczepir, USDA/ARS,  Byron, GA. 

….. I would like to amend Mike's message in that M. partityla has now been detected on pecan in Georgia (see my abstract in the FICN program).

Working group action:  This nematode was not included in pest list (See table 3, List of Nematodes considered but not included).

Meloidogyne partityla has been found on pecans in the states of Arizona, Georgia, Texas, and New Mexico and these states do not have adequate regulatory programs to prevent the intra or interstate spread of this pest. International regulatory principles and agreements dictate that if a country does not have internal regulations to prevent the spread a pest that is present within the country, then this country cannot establish external regulations that restrict movement of plants with this same pest from other countries. The working group strongly urges the pecan industry to establish intra and interstate certification regulations to restrict the spread of M. partityla. For a perennial crop such as pecan, excluding nematodes through certification programs is the most cost-effective means for preventing economic damage due to M. partityla

Longidorus diadecturus 

Comment by Roy Neilson, Dundee, Scotland.

Can I draw your attention to a factual error that I noticed in Pest Lists of Plant Nematodes of Regulatory Concern to the United States? …. Longidorus diadecturus is listed as not known to occur in the USA, whereas in fact L. diadecturus has been recorded in the USA.  If you are interested in the distribution of this species in the USA, may I suggest that you contact Prof. Bob Robbins at the University of Arkansas? …

Comments by David McNamara, Assistant Director, European and Mediterranean Plant Protection Organization, Paris, France. 

Longidorus diadecturus was reported as a vector of peach rosette mosaic virus in Ontario, Canada. However, specialists on virus vector relationships have never been satisfied that this transmission was adequately demonstrated; for two reasons. Firstly, the phenomenon of virus specificity has long been recognised, whereby nematodes of one virus-vector genus transmit one group of viruses but never the viruses associated with other genera. For example, at one level, trichodorids transmit viruses of the tobacco rattle group, whereas longidorids transmit nepoviruses, and at a second level, Xiphinema species transmits one sub-group of the nepoviruses (e.g. arabis mosaic, strawberry latent, grapevine fanleaf, tomato ringspot, tobacco ringspot) while Longidorus species transmit a more limited subgroup of the nepovirus (e.g. tomato black ring, raspberry ringspot). Peach rosette mosaic virus belongs to the Xiphinema-transmitted sub-group of viruses (known to be transmitted by X. americanum) and should, theoretically, not be transmitted by a Longidorus species. Secondly, the publications on the transmission of PRMV by L. diadecturus mention that X. americanum was also present in the infected field, so no evidence of field transmission by L. diadecturus was presented. Furthermore, it was not clear from the methods used for laboratory transmission that individuals of X. americanum might not also have been present.
Incidentally, two articles by Weimin Ye and colleagues  (numbered 171 and 358 in the abstracts of the Fourth International Congress of Nematology) suggest that L. diadecturus is present in Arkansas.

Working Group action: Based on the comments received relating to the evidence for widespread distribution of L. diadecturus in central USA (1991 publication of Robbins and Brown) and the nematode’s uncertain virus vector status, the working group has transferred this nematode from table 1 to table 3, which lists nematodes which were considered, but not included in SON Pest List because of their minor economic importance or becausean economically important nematode is present in the U.S. and there are not adequate internal efforts to prevent its dissemination.  International regulatory principles and agreements dictate that if a country does not have internal regulations to prevent the spread a pest that is present within the country, then this country cannot establish external regulations that restrict movement of plants with this same pest from other countries.

Xiphinema italiae

Comments by David McNamara, Assistant Director, European and Mediterranean Plant Protection Organization, Paris, France.

Xiphinema italiae occurs throughout the Mediterranean region, but it is only in Israel that it has been reported to transmit grapevine fanleaf virus. This is, in itself, surprising since the virus and the host plants also occur widely in the same region. Reports from other countries usually mention that X. italiae is a known vector but do not confirm that transmission occurs. Several years ago, I spoke to one of the authors of the original paper, Tanne, who told me that, after publishing the report, the authors had some doubts about their results. Unfortunately, I cannot remember what exactly the doubts concerned - either the virus in the experiments was not confirmed as GFLV or the nematodes may have come from a mixed population with X. index (which also occurs in Israel).

Working Group action: Based on the nematode’s uncertain virus vector status, the working group has transferred this nematode from table 1 to table 3 which lists nematodes which were considered but not included in the SON Pest List.

Pathotypes or races.

Comments by Michael McKenry, Kearney Horticultural Station, Parlier CA 

……Under the descriptors of biotypes, races, pathotypes, aggressive populations, virulent populations, etc. there are some really exotic nematodes, most commonly they are Meloidogyne spp, but they occur among Ditylenchus sp and even Tylenchulus sp. etc.  We don't need to have these populations moving around our agriculture.  My own examples include the highly virulent Senegal population of root knot, the pathotypes of M. arenaria and M. incognita that break resistance to grape rootstocks, the M. arenaria that breaks alfalfa resistance, and the M. hapla pathotype that breaks resistance to alfalfa.  The literature is full of these types of populations, especially literature involved with resistance evaluations.  I am convinced that they really are populations distinct from the normal by man's attempts to control them with inadequate resistance mechanisms.  All these populations that I have worked with have also appeared to be more aggressive on a number of other crops, at least for a few years. I don't have any suggestions as to what to do about them when we can't even identify them except by their cropping history but I wanted you to keep this in mind as you refer to exotic nematodes.
Our current regulatory efforts probably exclude the introduction of most of these exotic populations but it might prove useful to note that they exist as lists of exotic nematodes are compiled.

Working Group action: Although most pathotypes do not meet the criteria for establishing external regulatory action, grower groups (citrus, grape, soybean, etc.) should, whenever practical, limit the spread of pathotypes through certification and field sanitation programs. The following criteria must be met for external regulation of pathotypes: Rapid and reliable diagnostic methods should be available for the pathotypes of the species to be regulated. There should be reliable information on the distribution of the pathotype. If the pathotype is already present in the regulating country, and if this pathotype is regulated externally it should also be regulated internally in the country. The working group has not included most nematode pathotypes on the pest list because it would be very difficult to meet these criteria. One exception that the working group included is the potato pathotype of Nacobbus

Nacobbus aberrans:

Comments by Lynn Carta, USDA, Beltsville, MD

…. I had a few comments and questions on some ratings.  I was surprised that Meloidogyne mayaguensis was not rated highly on the list (and relatively few were high), but Nacobbus aberrans was.  Nacobbus is already in the U.S., has little economic impact, and has not shown great adaptability outside of its limited occurrence in the Midwest. 

Working Group action: Pathotypes of N. aberrans are an exception, because the distribution of the pathotype that damages potatoes is well known and it has not been found in the USA (See fact sheet). The Working Group felt that there was strong evidence that for N. aberrans there are pathotype concerns that should be recognized and addressed. N.aberrans  populations in the United States damage sugarbeet; however, there is no evidence that these populations are able to parasitize potato. Taking into consideration the wide distribution of these populations that parasitize potatoes in South America and Mexico and the increased chance of their introduction into the US due to the increase of the exchange of agricultural commodities between the US and Latin America, a high priority is given for a complete pest risk assessment. At a minimum, N. aberrans found on potato should be excluded.

Ibipora Species

Comments by Lynn Carta, USDA, Beltsville, MD

…. Ibipora, the sister genus of Belonolaimus, has not been found in the U.S. and could be added to the original Exotics list.

Working Group action: Species of Ibipora are not included on the list because evidence that they cause economic damage is lacking. 

Pratylenchus fallax 

Comments by Nicole Viaene, member of the EPPO working group and colleague at the diagnostic laboratory Nancy de Sutter, and Lutgard De Wael, Centrum voor Landbouwkundig Onderzoek, Belgium.

I read your request for comments on the proposed list of quarantine nematodes for the USA and saw your poster in Tenerife. As a member of the EPPO nematode working group, I thought I should make some effort to go through the list with the people of the diagnostic lab at my
institution. Here are our comments:

Table1. Pratylenchus fallax:  this nematode appears quite frequently in soil samples in Belgium. As damage provoked by this nematode has not been shown clearly, we wonder if it should be considered as a quarantine pest.

Working Group action: The priority rating for this nematode was changed from moderate to low, because there are few reports that substantiate that it causes reduced yields, even though this nematode has been widely distributed in Europe on many crops for many years.

Meloidogyne naasi

Comments by Nicole Viaene, member of the EPPO working group and colleague at the diagnostic laboratory Nancy de Sutter, and Lutgard De Wael, Centrum voor Landbouwkundig Onderzoek, Belgium.

….Table 2. Meloidogyne naasi. This nematode is a "common" nematode in Belgian soil samples and we wondered if this is not the case in the US. In other words: can it still be considered as quarantine as it might already be wide spread?

Working Group action: Because this nematode has been reported from five states, and currently there are no regulations to control the interstate movement of this nematode in the USA, this nematode is not included on the pest list and has been transferred to table 3. However, because economic damage caused by this nematode has been reported on spring barley and ryegrasses, growers and state regulatory agencies should consider excluding this nematode from wheat and rye producing states or regions where it does not occur.

Bursaphelenchus mucronatus

Comments by David McNamara, Assistant Director, European and Mediterranean Plant Protection Organization, Paris, France.

Bursaphelenchus mucronatus is widespread throughout Europe and Asia. It has been found virtually everywhere in the Palaearctic region where its vector Monochamus species occur. It has also been recorded in Canada. In many respects, it is similar to B. xylophilus - morphologically, vector relationships, life cycle and host trees. However, the major difference is that B. mucronatus has never been shown to cause the death of trees. Whereas B. xylophilus not only kills trees in Asia but also kills introduced pine species in North America (e.g. P. sylvestris, P. nigra, P. thunbergii), B. mucronatus has had similar opportunities to attack introduced pine species in Europe (where many North American species are grown both commercially and as ornamentals) but no evidence exists to suggest that it does. Certain publications have indicated that B. mucronatus may kill seedling trees when inoculated artificially but such artificial inoculation of seedlings is notoriously unreliable as a means of determining what might happen in the field. To assume that B. mucronatus would behave as B. xylophilus when introduced outside its native range is not, therefore, realistic.

Comments from David Dwinell, U.S. Forest Service, Athens, GA. 

Bursaphelenchus mucronatus and "The List"

1. Of the 55 described species of Bursaphelenchus, only two are generally considered to be pathogens - B. xylophilus (pinewood or pine wilt nematode) and B. cocophilus (red ring nematode). Greenhouse inoculation studies in Japan, Finland, et al have failed to demonstrate that B. mucronatus can kill young seedlings.  In the case of B. xylophilus, greenhouse inoculation studies are not considered to be of high value, but may have some validity in determining avirulence in strains of B. xylophilus or non-pathogenicity in the case of B. mucronatus.

2. Does B. mucronatus occur in the North America?  This topic is still up in the air. An isolate of the so-called "M" form of B. xylophilus from Canada was identified as B. mucronatus by molecular analysis (Harmey and Harmey. 1993. J. Nematol. 25:406-415; Bolla. 1993. J. Nematol. 25:227-238).  At the FICN, Bolla stated that he worked with an isolate of  B. mucronatus from Georgia. I ask him about this and he said he had reported it, but I have not been able to confirm where (Bob is moving and has not responded to my email). In my seventeen years of dealing with the pinewood nematode, I have yet to see a Bursaphelenchus female or larva with a mucronate tail. This includes isolations from pines in Oregon, Colorado, California, and across the southestern U.S. I would not, however, be surprised if B. mucronatus was found in the United States (at the northern limits (boundry with Canada) and/or at high altitudes).

3. Pines native to North America have been planted in several countries in which B. mucronatus is common. For example, lodgepole in Finland and Sweden, and slash and loblolly pines in China. In China they have been planting slash and loblolly pines for some fifty years and these species currently occupy some 1,500,000 ha. I'm not aware of any reports of these native American pines being killed by B. mucronatus in the aforementioned countries. In China, they are reforesting sites of masson pine "killed" by B. xylophilus with loblolly pine. 

4. In China, there appears to be some confusion on the status of B. mucronatus as a pathogen of their native pines. I think this is due to confusion about the phoretic relationship of Monochamus alternatus and B. mucronatus, secondary transmission, et al. The situation in some parts of China may be akin to what it was in the United States from 1978-1982.  At the FICN, the issue of reports of pathogenicity of B. mucronatus in China was brought up during the discussion session. The consensus of those PWN experts present was that B. mucrontaus is not a pathogen of pines.

5. Around 1991, log imports from Siberia were banned largely because of the interception of B. mucronatus in a test shipment of Scots pine logs into California. The "when in doubt, keep it out" principle came into play. The USDA Forest Service's PRA basically plugged B. mucronatus into the pine wilt model. This approach was erroneous (i.e. not based on sound science) and is one of the fatal flaws in the PRA. I would not recommend pointing at this PRA as a sound basis for inclusion of B. mucrontaus on "The List."

6. If B. mucronatus is included on "The List," how do you plan to deal with the other 52 described species of Bursaphlenchus? In Europe, at least 14 species of Bursaphlenchus (i.e., B. leoni, B. tusciae, B. hofmanni, B. hellenicus, et al) have been isolated from conifer wood in the past few years. May be you should just list "Bursaphelenchus spp."?

In conclusion, I fail to see why B. mucronatus was included on The List, much less given a rating of "M."

Working Group response: Action on the rating is pending. The above comments support the view that the evidence for B. mucronatus becoming a strong economic pathogen is weak. The Working Group proposes to remove B. mucronatus  from the list. The working group requests further comment from SON members and other interested scientists before taking this action.

Anguina funesta

Comments by Dr. Ian Riley, University of Adelaide, Australia.

Comments on Anguina funesta and Anguina tritici as quarantine organisms
I would like to make some comments related to the preliminary draft list of nematode pests of regulatory significance developed by the SON Regulatory Committee working group. Although Anguina funesta and Anguina tritici are economic pests in some countries, it is my view that they don’t represent a major risk for the USA. 

In the field A. funesta reproduces in Lolium rigidum (known as annual ryegrass in Australia). Populations of the nematode only increase to problem levels where the host grass is protected from grazing through to maturity and growing seasons are short. This occurs in low rainfall, dry-land cropping areas of southern Australia where L. rigidum is a major component of self-regenerating pastures in the lay cropping system (winter dominant rainfall of 300 to 450 mm pa). Short growing seasons are needed as the nematode invades the plant in early vegetative growth and does not feed until galls are initiated in a reproductive primordia. If the growing season is long the attrition rate between invasion and gall initiation will increase, reducing the reproductive efficiency of the nematode. Invasion and gall initiation are better synchronised in short seasons. A. funesta populations are not found naturally in long season and perennial ryegrass (L. multiflorum and L. perenne) in Australia. They are not found in commercial seed of named ryegrass cultivars as these not L. rigidum and are produced in longer growing season districts. Also, over much of the area prone to high populations of A. funesta, numbers are now kept below an economic level by good pasture management and the naturally occurring antagonist Dilophospora alopecuri. This natural suppression occurs in Victoria, most of South Australian and parts of Western Australia. The fungus is also being actively distributed in other areas. I doubt that the US has significant areas of rangeland or cropping systems that would support problem levels of A. funesta and I question whether it is appropriate to give it a major quarantine pest status.

Working Group action: Action on the rating for this nematode is pending, based on the need for further discussion among SON members and input from other interested scientists. A. funesta is associated the with a yellow slime bacterium, Rathayibacter toxicus which is introduced in the plant tissue during seed gall formation and is fatally toxic to grazing livestock. Does the US have significant areas of rangeland or cropping systems that would support problem levels of A. funesta? Are there short season dry-land rangelands in the Pacific Northwest where A. funesta could become a problem?  These are critical unanswered questions. For this reason the Working Group has given this nematode a high priority rating for a complete pest risk assessment. The working group would like further discussion on this nematode to evaluate if the US has cropping systems that would support problem levels of A. funesta

Anguina tritici

Comments by Dr. Ian Riley, University of Adelaide, Australia

Anguina tritici also occurs in Australia and about 100 years ago economic problems were recorded in the four southern States (South Australia, Victoria, Tasmania and Western Australia). It can now only be found in small pockets of the Western Australian wheatbelt, with particularly short growing seasons, very dry summers and a tendency towards continuous wheat production. It has become locally extinct in the other States. Crop rotation and seed cleaning has either eliminated A. tritici or reduced its significance dramatically. Some markets in the Middle East still require a shipment to be free of A. tritici because of a perception of effect on quality, not for phytosanitary reasons. A.  tritici is found in most of the countries in that region, so without area freedom, this nematode could not be considered quarantine organism. Given that A. tritici is easily controlled in modern commercial agriculture and trade concerns are not phytosanitary in nature, I also question whether it is appropriate that it be given a major quarantine pest. I would be pleased to contribute to further discussion on the ranking of these nematodes, if this would be helpful. Also, I would be willing to contribute to the preparation of fact sheets for Anguina spp., as this is my area of particular interest.

Working Group action: Action on the rating for this nematode is pending, based on the need for further discussion among SON members and input from other interested scientists. Dr. Riley’s comments have identified the dilemma that the Working Group faced in rating this nematode. We agree that A. tritici does not pose a threat to U.S. wheat production through direct economic loss, given that A. tritici is easily controlled in modern commercial agriculture through seed cleaning. There is no evidence that this nematode occurs in the U.S., based on the fact that it was last reported more than 30 years ago and has not been found since that time. If the nematode is reintroduced into the U.S., this could have a significant economic impact on U.S. wheat growers due the indirect losses caused by loss of major export markets. As of February 2003, at least eighteen countries have regulations for this nematode that are phytosanitary in nature. The nematode does not occur in most of these countries. These include major trading partners in South America: Argentina, Brazil, Chile, Colombia, Paraguay, and Uruguay.  Several years ago one of these countries blocked U.S. wheat shipments for some months because A. tritici was possibly detected in a wheat shipment from the U.S. Even though surveys did not confirm this, U.S. wheat growers suffered significant losses when this export market was closed temporarily. Thus although there is no reason to include this nematode on the SON Pest List due to the direct losses, the Working Group gave it high rating because of the indirect losses growers could experience due to this nematode as a consequence of current quarantine regulations in other countries.  The other side of the dilemma is that by acknowledging the reality of the short-term negative impact of this nematode on export markets for cereal growers, the Working Group and indirectly SON may perpetuate regulations that should be changed because they are not based on current management practices and are not justified. One possible solution would be for the Working Group to create a special list or category for nematodes that SON considers candidates for deletion in quarantine regulations, but indicate that the nematodes in this category may be important to growers because current regulations may result in trade restrictions. Examples of nematodes that would be included in this category are A. tritici and Subanguina wevelli. The Working Group will appreciate further comments on this issue