1 What do we know about Plant Parasitic nematodes?

TARG.jpgWhat do we know about Plant Parasitic nematodes?

Before we take a look at where we are today and what the future may hold with regard to plant parasitic nematodes, it's worth taking a quick look back at what we have learned over the past few years about what is, arguably, one of the most significant changes in modern turfgrass management.

I have been looking at disease problems for the past 18 years and, for the first ten of them, the potential for plant parasitic nematodes to cause problems in cool-season grasses was dismissed out of hand. During that time I remember occasionally seeing problems of reoccurring fungal disease and symptoms that could not be associated with specific diseases and these had to be reported as 'stress'. I had definitely seen the Root-gall nematode, Subanguina radicicola, causing what I call 'peanut-like' galls on the roots of Poa annua but none of the advice available at that time suggested that this nematode could have any detrimental effect on turfgrass growth.

When I started to work for myself in 2000, I was able to make time to investigate things more closely and to question all of the unusual things that I had been finding. One of the first investigations that I was asked to help with, by Headland Amenity, was to identify the cause of a patch 'disease' that, for several years, had been affecting creeping bentgrass greens on USGA rootzones. After a lengthy investigation which confirmed no evidence of any fungal disease, the cause was identified as the Root-knot nematode Meloidogyne minor (new species), something that was confirmed through extensive research by Dr Colin Fleming at AFBI Northern Ireland (AFBI NI), contracted by Headland Amenity.

This plant parasitic nematode disease has been well documented over recent years and since that initial confirmation of a plant parasitic nematode causing disease in amenity turfgrasses, we have been actively looking at turfgrass roots and rootzones to determine which plant parasitic nematodes are present and which are associated with symptoms of turfgrass disease.

All rootzones are likely to possess some plant parasitic nematodes and, during any one year, but the species diversity and individual species populations will fluctuate in response to rootzone and environmental conditions. Therefore, as with fungal pathogens, the presence of these nematodes does not necessarily mean that they are causing (or likely to cause) any problem. Compared to weaker turf, a stronger turf area can tolerate higher nematode populations without significant symptoms developing on the turf.

However, since plant parasitic nematodes feed on, or within, the root (and occasionally in the leaf) tissues, they adversely affect the function of the roots such that water and nutrient uptake is compromised. In addition, these nematodes can introduce certain compounds in to the plant whilst they are feeding, or the plant can respond to their feeding by producing certain metabolic products which may directly and adversely change the physiology of the plant.

Plant parasitic nematodes feed by repeatedly forcing their spear-like stylet in to the plant cells until they puncture the cell wall and gain access to the cell content. Some nematodes, like the Root-knot nematode Meloidogyne, induce changes in the root development which result in the formation of so-call giant cells which act as a sink for photosynthetic materials and serve as a constant food source for the parasite.

There are two main groups of plant parasitic nematodes, the endo- and the ecto-parasites which have their body inside or outside of the plant tissues whilst feeding. To further complicate things, some nematodes are classed as semiendo- and these have the front part of their body inside the plant tissues whilst keeping their rear end in the rootzone.

lant parasitic nematodes can be sedentary whilst feeding (staying in the same location) or migratory, moving through the rootzone or the plant tissues where, in the latter case, they will destroy the structural integrity of the plant tissues by their physical movement.

Although there will be slight difference between nematode species, their life cycles are fairly straightforward. The juveniles emerge from the egg after they have passed through the first moult. After a total of four moults, during which time the nematodes increase in size, the adult male and female nematodes will emerge, the female will lay a number of eggs and the life cycle will begin again.

n some species, e.g. the Root-knot nematode, only the emerging juveniles are the infective stage and can enter the plant to cause initial infection. In others, e.g. the Lesion nematode, all stages from emerging juvenile to adult can enter the plant root and initiate infection. A recent article in the Institute of Biology magazine (Fleming, et al, 2008), comprehensively details the problem of plant parasitic nematodes in amenity situations. A copy of this article in PDF format is available, via email, on request.

We are now aware that the endo-parasitic Root-knot nematodes, initially seen to be a problem on creeping bentgrass, can also cause damage to the roots of ryegrass and annual meadowgrass sward alike. There are two main species of Meloidogyne that are frequently recorded, but both appear to go through several life cycles each year under the ideal conditions provided by modern amenity constructions.

The Root-gall nematode, Subanguina radicicola has been found extensively causing problems on golf course putting greens, bowling greens, soccer pitches and racecourses but always on Poa species in the turf. It is a relatively easy nematode to identify due to the development of characteristic swellings on the roots that contain the entire life cycle of the nematode.

Perhaps one of the most frequently recorded nematodes is the Spiral nematode, Helicotylenchus, and this can build to massive populations both in the rootzone and within the root tissues themselves. This is an endo- ecto-parasite that can cause severe deformity to root development, adversely affecting plant growth and development. Although all grasses can be affected by the feeding activity of this nematode, I am frequently recording high populations in Poa annua dominated, close-mown turf in which the sward has developed small (10-20mm diameter) chlorotic patches that progressively develop into decaying, bleached turf.

Often, these small patches will appear to coalesce and, in most cases, no fungal mycelium has been seen to develop across the affected areas. Occasionally, fungal mycelium may be seen around the perimeter of the affected plants but, in all cases that have so far been analysed, this mycelium has been found not to be that of any known fungal pathogen. The fungus appears to be related to a secondary infection that develops on the weakened and dying leaf tissues of these nematode-infected plans. These symptoms tend to appear as if the problem was dollar spot but on these Poa swards, the dollar spot fungus has not been conclusively identified.

The ecto-parasitic Stunt nematode Tylenchorhynchus is also commonly identified in amenity rootzones that are showing symptoms of discolouration and decline. The affected area of individual patches can range from 100mm to 1500mm or more and the plants appear to show a tan/chlorosis and, again, no evidence of any fungal mycelium.

During May and June, I recorded an increase in the frequency and general population size of the Stunt nematode in samples received from across the UK, with some nematode populations over fifteen times the current proposed threshold for damage to amenity turfgrasses. The Stunt nematode is most often identified in the rootzones of fine turfgrass areas rather than soccer pitches but other nematodes, notably the Cyst nematode, Heterodera, can be found in both.

he Cyst nematode is another sedentary parasite like the Root-knot nematode, but unlike the Root-knot nematode, the Cyst is a semi-endoparasite in which the maturing female is embedded in the plant tissues but with her body exposed on the outside of the plant. As the female matures, her body becomes brown in colour and hardens to form a cyst. Within the cyst, the juveniles develop inside the eggs and, when they have developed sufficiently, the cyst breaks open and the juveniles are released in to the rootzone.

The Lesion nematode is an example of an endo-parasite that migrates through the root tissues whilst feeding on the cell contents. It causes the outer cortical cells of the root to be separated from the inner stele (xylem and phloem) and thereby, renders the root unable to take up water and nutrient from the rootzone.

o date, the Lesion nematode has been found on ryegrasses and on close-mown bentgrass swards causing significant decline in turf quality.
Since 2001, when we initially reported that plant parasitic nematodes have the ability to cause disease in cool-season turfgrasses, there has gradual reduction of perceived scepticism towards the idea that the nematodes should be considered as a potential problem in amenity areas.

However, over recent years, there has, unfortunately, been an increase in the number of confirmed problems that have been associated with high populations of one or more nematode species.

Is this because nematodes are becoming more of a problem or because we are now aware of their potential and are looking for them in rootzones that are supporting a weak and unresponsive sward? I believe that these nematodes have always been present but our recently acquired knowledge has encouraged us to be more vigilant and to look more closely for them in turf that we may have otherwise reported as 'stressed'.

It is also true that their populations will be strongly affected by environmental conditions and, that the recent shift towards milder winters and wetter summers, can only encourage the development of their populations. We also know that nematodes tend to thrive in a sandier rootzone and therefore our tendency to construct and to topdress with high sand content materials, is further facilitating the development of ideal growing conditions.

Nematodes don't only cause damage in isolation. High populations can certainly cause disease, as we have seen all too often with the Root-knot nematode. However, for the past couple of years, I have been looking at turf samples that come in to my lab with fungal diseases like Take-all patch, Microdochium patch and Anthracnose, to see if their rootzones also show the presence of plant parasitic nematodes. Quite unsurprisingly, most rootzones do but, more interestingly, what I have seen is a large number of instances where reoccurring fungal disease problems (what I call 'niggling' disease developments) are present on the sward above a rootzone containing high nematode populations.

There is a lot of research to support the association of fungal disease and plant parasitic nematode activity in agricultural situations but, not surprisingly, none to support this observation in amenity turf. From my experience, I have little doubt that there is a correlation between the two and, if asked to speculate, I would suggest that, in many cases, the nematodes are more likely to cause the initial infection and damage to the roots, initiate a decline in plant strength and adverse changes in plant physiology, which eventually allows the weakened plant tissues to be colonised by fungal disease. It is only then that we recognise a problem in the turf.

So, what do we know?

• We know that plant parasitic nematodes certainly can, and do, cause damage and disease to cool-season turfgrasses. There is much debate still, even amongst researchers, as to what populations are necessary to cause disease but, as I mentioned above, these populations will be affected by turf composition, strength and environmental conditions. There can be no clear-cut answer to this question.

• We know that there is potentially a strong, but currently only theoretical, link between the activity of plant parasitic nematodes and fungal disease. We know this from the research published in agricultural systems and I have seen evidence to support this in turf samples that pass through my lab.

• We can be certain that we still have a lot to learn about which nematodes are present and what type of problems they can cause. New nematodes continue to be identified in amenity situations, like the Gracilacus sp. that we have recently found on four golf courses in Portugal in putting green that are showing symptoms of severe stress. In agriculture, Gracilacus can cause serious damage to cereals but we need to confirm the problems that it can cause to fine turf.

Perhaps the most important question regarding plant parasitic nematode damage is what can be done to manage the nematode populations and the symptoms that develop as a result of their activity on and within the plant?

Research is currently underway to investigate the potential of several products that could hopefully be of benefit to affected turf. Already, research has shown that both a mustard bran product (tested at the request of Headland Amenity) and a product called BioMass Sugar (tested at the request of Barenbrug UK) can produce a significant improvement to turf quality following application.

t present, only the BioMass Sugar is generally available for application to turf but independent research has confirmed that this natural solution can effectively minimise the symptoms of stress and, most importantly, promote recovery in a weakened sward. Research has also shown that the use of cold-extracted seaweed products is particularly effective in alleviating stress and reducing visible symptoms on the sward that result from nematode activity.

Furthermore the use of plant elicitors to 'condition' the grass plant to grow better under the effect of the pathogenic nematode has also shown promise in the field. According to Mark Hunt of Headland Amenity, "Successful nematode management comes down to a combined strategy involving correct identification and assessment, effective control, revised cultural practices and the use of products to provide stress reduction and enhanced growth under the effects of the plant parasitic nematodes". Field work over the last four years has shown that employing such a combination strategy provides turf managers with an effective and environmentally acceptable approach to nematode management.

As for the future, times are changing, the environment is changing (as we are constantly being told) and so too are the potential problems that we face in day to day turfgrass maintenance. I have little doubt that with new grass types being introduced for amenity use, we will see new disease problems developing and, if we decide to look more closely to determine the cause of these diseases, nematodes will be up there as important turfgrass pathogens.

That doesn't mean the future for turf quality is on a downward spiral but that, when they occur, our turf disease problems may not be the same as those we have managed in the past. We need to be looking harder today for the potential problems of the future, to fully understand their causes and to work towards identifying feasible and effective management options. Hopefully, disease problems will be few and far between on the turf areas that you manage but should the symptoms develop, try to keep an open mind as to their likely cause.

Acknowledgement: I would like to extend my sincere thanks to Dr Colin Fleming and his team at AFBI Northern Ireland for their invaluable support and assistance in my work on plant parasitic nematodes.

Dr. Kate Entwistle, The Turf Disease Centre
Email: kate@theturfdiseasecentre.co.uk

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