What’s the cause of your disease?
Identifying the primary cause of turfgrass diseases has, arguably, become more difficult over recent years as we have become better able to identify differences between certain closely-related organisms and to recognise the potential of previously unconsidered pests.
Dr. Kate Entwistle asks ...What's the cause of your disease?
During the past 5 years, research from the USA has confirmed the identification of new fungal turf diseases, for example Dead Spot (Ophiosphaerella agrostis) and Waitea Patch (Waitea circinata var. circinata) and a disease caused by a fungal-like organism, namely Rapid Blight (Labyrinthula terrestris). Here in Europe, we have seen the diseases of Waitea Patch and Rapid Blight but, as far as I am aware, we have not yet had confirmed reports of Dead Spot disease. Is that because the pathogen is not present across Europe, the conditions favourable to disease development are not encountered here, or because we have not looked for it?
It is not only fungi and fungal-like organisms that are being reported as causing new problems on amenity turf. Other plant parasites are being recognised with increasing frequency and the time has come to ask the question - have these problems always been here, but been overlooked, or are they really new problems that we are now having to deal with?
If we consider the cool-season turfgrass diseases that were recognised prior to 2000, we could no doubt list several fungal problems including Fusarium Patch (now called Microdochium Patch), Red Thread, Anthracnose Basal Rot, Dollar Spot, Take-all Patch, Leaf Spots, Rust and Brown Patch (though never that much of a problem in the UK). By looking at each of these diseases in turn and considering how our understanding of the causal organisms has changed over recent years, you may be more than a little surprised with what you find. With regard to Fusarium Patch, its name change to Microdochium Patch reflects the fact that for some considerable time we have been aware that the causal fungus was not a Fusarium species.
Microdochium Patch has historically been thought of as a winter disease and one that was controlled to a large degree by severe winters. It may, therefore, be a surprise to learn that frosts don't kill the fungus, they merely slow its growth and some isolates of the fungus are still capable of growth at temperatures below freezing.
Although it is true that the ideal conditions for the development of the disease are cool, wet weather and a weakened sward, Microdochium Patch can occur on any sward throughout the year as long as conditions are conducive. Different known strains of this fungus may account for differences in disease development and variation in the expression of symptoms between locations or under different local conditions. 
Red Thread disease was always regarded as an indicator of low nutrition, but this disease is increasingly seen on areas receiving adequate amounts of balanced nutrition. During 2007, Red Thread was a common sight on amenity areas and its incidence was probably affected by the leaching effect of the heavy rainfall experienced in many areas of the UK. Right picture of Fusarium
Anthracnose diseases are true stress diseases and Anthracnose Basal Rot is a disease that frequently affects weakened Poa annua swards during cool, wet conditions. However, this disease is not restricted to Poa annua and has been seen in Agrostis sp. in the UK although, as far as I am aware, its relative incidence is comparatively low.
What is increasing, however, is the incidence of Anthracnose Foliar Blight, a disease that can develop on all turfgrasses and which is caused by the same pathogen. It may be worth mentioning here that Anthracnose diseases are no longer caused by the fungus Colletotrichum graminicola but the causal fungus has recently been re-named C. cereale. In the near future, the old name is likely to remain commonplace in publications but as with Microdochium nivale and Microdochium Patch, the new name will become increasingly used and accepted.
In addition to the name change, research has shown that the fungus appears to be relatively host specific and, although it can infect grass types other than the one from which it has been isolated, it is less aggressive in the other grasses. Therefore, in a mixed Agrostis and Poa sward, an isolate from Poa will be able to infect the Agrostis but the severity of the infection will be lower than that seen in the Poa.
As for Dollar Spot - where do we start!? Previously known as a disease of fescues in the UK and caused by the fungus Sclerotinia homoeocarpa, both of these facts are now considered incorrect. We have long known that the causal pathogen is not S. homoeocarpa but its identity remains somewhat uncertain (if indeed the disease is caused by one pathogen alone).
Generally now accepted as a Rutstroemia sp. of fungus, it has apparently now been seen on Poa annua in the UK. However, a recent molecular analysis of two known isolates of the Dollar Spot fungus taken from fescue in the UK and several isolates of a fungus isolated from suggested Dollar Spot on Poa annua has confirmed that the fungi from the Poa annua is '…a totally different organism', (personal communication).
Is it a pathogen causing Dollar Spot-like symptoms or is it a secondary infection that is developing on weakened Poa plants? Further work is currently under way, but I'm certain that the 'is it or is it not Dollar Spot' debate will run and run. We need to find the answer but, as you read on, you will hopefully appreciate that the answer may not be that straightforward to find. Right picture of Waitea Patch
Back to our pre-2000 disease list and we have Take-all Patch which, according to all texts of the time, suggested that this was a disease that only affects bentgrasses. We have always known that the fungus can infect other grasses and we are now recording an increasing number of cases of Take-all Patch on pure Poa annua swards.
Many fungi that cause disease are capable of living as both pathogens (causing disease) and saprophytes (on dead and decaying material), but exceptions to this include the Rust fungi and the fungus that causes Yellow Tuft disease which need to live on living tissues. Of those fungi capable of both parasitic and saprophytic lifestyles, some spend more time as saprophytes and can invariably be found on the older leaf tissues at the base of the sward.
Does that mean that disease is always present? That depends on your definition. I believe it means that the potential for disease development in these cases is always present and one thing that remains unchanged over time is that a weakened sward is more susceptible to infection by these fungi or to increased disease severity.
We have generally considered a weakened sward to be the result of maintenance or environmental stress - unbalanced nutrition, reduced nutrient or water availability, compaction etc. and, clearly, these and other environmental factors will stress the turf and increase its propensity to disease. But, we are becoming increasingly aware that they are not the only factors that cause stress.
Over the past two or three years I have received an increasing number of calls relating to reoccurring disease problems, primarily those of Microdochium Patch, Take-all Patch and Anthracnose diseases, where cultural management options and the correct application of plant protection products have apparently failed to relieve the problems. In effect, what was developing over a period of several months was a continuous, niggling infection that didn't develop fully and never really went away.
In all of the samples received for analysis from these situations, root depth was minimal, turf strength was reduced and root development was to varying degrees, deformed. High populations of plant parasitic nematodes were recorded in all of these situations and, with the mounting volume of data to support their possible involvement, it is becoming increasingly difficult to say that plant parasitic nematodes have no adverse effect on cool-season turfgrass development. In fact, in addition to being recognised as causing 'extensive losses in turfgrasses in warm temperate and subtropical regions', plant parasitic nematodes are now generally considered to cause a 'chronic debilitation of grasses' in cooler regions too.
Fact: Plant parasitic nematodes have long been known to cause significant problems on warm-season turfgrasses and they are one of the major causes of agricultural losses worldwide, estimated to be around $78 billion a year, according to the University of California.
Fact: Plant parasitic nematodes can be present in virtually all soils but it is only at high populations (or populations above their threshold values) that they are likely to cause problems in turf.
Fact: The Root-knot nematode Meloidogyne is now recognised as a serious problem on both fine turf and coarse turfgrass swards. The Root-gall nematode Subanguina is a significant and widespread problem on Poa. The Lesion nematodes Pratylenchus and Pratylenchoides are increasingly being recorded as damaging both coarse and fine turfgrass swards.
The Spiral nematode Helicotylenchus and the Stunt nematode Tylenchorhynchus are both regularly identified as being present in high populations in fine turf that is showing symptoms typically considered to have a fungal disease.
Fact: Although we are working towards improving our knowledge and understanding of these nematodes in amenity situations and to determine more robust threshold values in different turf situations, there is still a vast amount to learn about these organisms.
One thing that we know is that the majority of plant parasitic nematodes feed on root tissues, piercing the root cells with their stylet and removing the cell content for nutrition. The length of time that the nematode spends feeding at any given site depends on the nematode species but they will all inject chemicals in to the root tissues that facilitate their feeding and cause adverse changes to the physiology of the plant.
Some species of nematode keep most of their body in the rootzone whilst they are feeding, but others venture in to or remain permanently inside the root tissues as they feed. Not only do they impart chemical damage via their secretions but they also cause mechanical damage to the root structure.
Plants affected by the activity of nematodes, weakened by reduced water and nutrient uptake and damaged physically by the passage of the nematodes through the plant cells, would surely be more susceptible to fungal infection. It could also be argued that plants affected by fungal disease would be an easier source of nutrition for the nematode.
So, in cases where both a nematode and a fungus occur in the same area of turf, which was first to attack the plant? Although research has been done to look at this situation in agriculture, similar studies have not been done in amenity situations. However, I would argue that the situation that makes most sense is most likely.
Considering that plant parasitic nematodes need a steady source of nutrition and that dying or decaying plants that have succumbed to a fungal infection are less likely than unaffected plants to provide this, the nematodes are more likely to infect newly produced and growing root tissues and initiate weakness in the plant.
Most fungi, as we saw earlier, have the ability to live as parasites or saprophytes and they have the capacity to colonise weakened plants, causing increasingly severe disease problems. I would argue that it is possible that where a rootzone supports a high population of plant parasitic nematodes, and where there is root deformity or reduced rooting depth, it is more likely that the nematodes are weakening the plant and enabling fungal disease to develop or allowing a niggling, reoccurring fungal infection that never really goes away. Plants that are dying as a result of fungal infection would, in my opinion, not be preferentially targeted as a feeding site by nematodes.
Work is needed to confirm this theory in amenity situations, but there is evidence to support the general theory that nematode infected plants can show increased levels of fungal infection caused either by increased entry of the fungus through the wounds inflicted by the nematode, or entry in to a weakened plant whose physiology has been altered by the secretions pumped in to the plant during nematode feeding.
In the past, it seemed as if turf diseases just needed a name in order for us to be satisfied and for a management programme to be implemented. Now, with our increased abilities and awareness of potential and emerging problems, we are quite rightly called upon to identify all potential contributory factors in disease development and to suggest which is the most important. But, how can we make an informed assessment of relative importance when so much is still to be learned about the organisms themselves?
We need to keep a close eye on the published research that is increasingly available to us and recognise that there is still so much that we have yet to learn about something which only a couple of decades ago seemed 'all sewn up' and to remember to employ a modicum of common sense.
What else is waiting to be discovered as we look closer at the turf with the improved tools that are available to researchers around the world?
Dr. Kate Entwistle
The Turf Disease Centre
Email: kate@theturfdiseasecentre.co.uk