Dr. Paul Schreiner, Research Plant Physiologist, USDA-ARS
Dr. Inga Zasada, Research Plant Pathologist, USDA-ARS
The ring nematode (Mesocriconema xenoplax) is the most common plant-parasitic nematode found in western Oregon vineyards (Figure 1).
It is an ecto-parasite, as it feeds from outside of the root by inserting a stylet into an individual root cortical cell. Ring nematode does not disrupt the cell membrane during feeding, but alters the sink strength of the punctured cell and those cells surrounding it, allowing for greater metabolic activity (Hussey et al. 1992). The elaborate modification of the feeding site may explain why grape roots show little damage when fed upon by ring nematode (Schreiner and Pinkerton 2008).
A survey conducted in 1994 to 1995 in over 200 blocks from 70 vineyards in the Willamette Valley and southern Oregon (Douglas, Josephine, and Jackson counties) found ring nematode in 81% of vineyards. More than 40% of vineyards had infestation densities of >0.5 ring nematode per gram of soil, and 14% of vineyards had densities of 2.0 per gram of soil (Pinkerton et al. 1999). The suggested damage threshold for ring nematode is 0.5 per gram of soil (McKenry 1992), as this level leads to significant yield loss in California vineyards. Despite the high populations found in the Oregon survey, there was no clear relationship between ring nematode populations and vine vigor or yields based on grower records. The survey work also found ring nematode to be more prevalent on sites that had been planted to orchard crops prior to vineyards (Pinkerton et al. 1999). These findings led to continued research to better understand the impact of ring nematode on vine productivity in Oregon.
An experiment was conducted from 1997 to 2000 to determine vine growth responses to ring nematode. Microplots (similar to a pot-in-pot system) were planted with own-rooted Chardonnay or Pinot noir and inoculated with ring nematode or kept nematode-free (Pinkerton et al. 2004). The pruning weight of both Chardonnay and Pinot noir was reduced by approximately 60% after four years of exposure to ring nematode (Figure 2).
Chardonnay yield was reduced by approximately 30% in year four, but Pinot noir yield was not affected. The reduction in vine growth was associated with ring nematode populations of between 6 to 11 nematodes per gram of soil. In addition to altering above-ground vine growth, ring nematode reduced the fine root density of both Chardonnay and Pinot noir and reduced the extent of fine roots with arbuscules formed by symbiotic, arbuscular mycorrhizal fungi (AMF). Arbuscules are specialized mycorrhiza structures where the plant and fungus exchange nutrients. These results led to the hypothesis that ring nematode competes with AMF for root carbohydrates, thereby reducing the function of mycorrhizal fungi.
This hypothesis was tested and confirmed in a series of experiments conducted in the greenhouse using own-rooted Pinot noir grapevines grown in Jory soil (Schreiner and Pinkerton 2008, Schreiner et al. 2012a). The experiments focused on the impact of ring nematode on overall vine growth, root growth, AMF colonization of roots, and carbohydrate and nutrient status of vines. Results indicated that ring nematode alters vine physiology primarily by reducing carbohydrate reserves in roots and woody tissues needed to support growth, nutrient uptake, and AMF symbionts in future years. However, own-rooted vines had a strong capacity to tolerate feeding by ring nematode, as evidenced by total vine biomass being unaffected after exposure to high ring nematode populations for a single growing season. Some vines used for these experiments had 75% of their leaves removed and others were grown at 15% of full sunlight, as compared to the control with no leaf removal grown at full sun. Only the added stress of growing vines at 15% of full sunlight for three years, which further reduced vine carbohydrate status, resulted in eventual vine death (Schreiner et al. 2012a). The population of ring nematode in these experiments was between 22 to 30 ring nematode per gram of soil. This was 2 to 3 times higher than the populations in the field microplot experiment and about 10 times greater than actual vineyard populations.
Work was also conducted to understand how different rootstocks vary in their susceptibility to ring nematode. Numerous rootstocks were evaluated for resistance to ring nematode in two greenhouse experiments and in a vineyard rootstock experiment at OSU’s Woodhall Research Vineyard. Results indicated that the rootstocks 420A and 101-14 were highly resistant to ring nematode, 110R was moderately resistant, and the highly susceptible list included own rooted Vitis vinifera (numerous cultivars), 3309C, and 1103P rootstocks (Pinkerton et al. 2005). Five rootstocks and own-rooted vines were further evaluated in a second field experiment using a microplot pot-in-pot system to test the durability of resistance to ring nematode and further explore the physiological effects of ring nematode on vines (Schreiner et al. 2012b). The key finding was that the two rootstocks previously classified as resistant, 101-14 and 110R, did not fare well; ring nematode populations skyrocketed on these rootstocks after three to four years of exposure (Figure 3).
Only the rootstock 420A remained resistant to ring nematode over the four-year trial. Nematode populations reached levels of 30 to 40 ring nematode per gram of soil in own-rooted vines and each of the four rootstocks (101-14, 110R, 1103P, 3309C). Ring nematode had differential effects on above-ground vine growth, root growth, and colonization by AMF among the different rootstocks that generally matched their a priori classification of resistant or susceptible to ring nematode. For example, fine root growth and AMF colonization were reduced as early as the second growing season in the ‘susceptible’ group (own-rooted, 3309C, 1103P). Root growth and AMF colonization was not altered by ring nematode in any of the three ‘resistant’ rootstocks (420A, 101-14, 110R), even after four years. However, vesicle formation in roots (indicative of carbon storage by AMF) was reduced in all four rootstocks and own-rooted vines that promoted high ring nematode populations. Vesicles were unaffected in the rootstock 420A. Ring nematode also reduced vine shoot growth and pruning weights by year three or four only in the ‘susceptible’ group. Ring nematode did not alter vine water status (leaf water potential or stomatal conductance) in any year nor did it influence rates of leaf photosynthesis in any rootstock.
These findings led us to wonder if resistance to ring nematode may be overcome in commercial plantings of 101-14 grapevines in the region. Focus was placed on 101-14 because it is widely planted in Oregon vineyards. A survey of the oldest 101-14 plantings in the Willamette Valley was conducted in Fall 2012 to examine ring nematode populations. Populations were also assessed in older 3309C vineyards since 3309C is more susceptible to ring nematode. Fifteen vineyards with either 101-14 or 3309C rootstocks were sampled, including six vineyards that had both rootstocks planted in the same year. The oldest site was planted 18 years ago, and the average age of vines sampled was 14 years. Ring nematode was found in six of the nine vineyards planted to 101-14 and in three of six vineyards planted to 3309C. However, populations of ring nematode were low averaging 0.12 and 0.23 ring nematode per gram of soil in 101-14 and 3309C vineyards, respectively. Ring nematode populations did not differ significantly between 101-14 and 3309C rootstocks in the six vineyards with matching plantings of both. Results from this rather small survey also revealed that prior land cropping history was a key driver of ring nematode presence. Ring nematode was only found if the site was previously planted to orchard crops or grapevines (Figure 4), similar to findings from the prior survey (Pinkerton et al. 1999).
These findings indicate that ring nematode populations in commercial vineyards are not reaching levels known to be damaging based on field microplot and greenhouse experiments. However, own-rooted, 101-14, and 3309C rootstocks are certainly harboring ring nematode in commercial vineyards, similar to our findings from the rootstock experiment in field microplots. At this time, only the rootstock 420A has been shown to have durable resistance to the western Oregon population of ring nematode.
After these studies, we questioned why ring nematode reaches high populations in field microplot or greenhouse trials but not in commercial vineyards. This is important to understand so that appropriate practices to avoid high populations can be identified and used. We suspect that the answer to this question lies in fine root density, which equates to the availability of food for the ring nematode. Grapevines in commercial vineyards do not achieve high fine root densities in the range of what occurs in field microplot or potted vines. The typical fine root length density in commercial vineyards in western Oregon is about 0.5 mm fine root per gram of soil (Schreiner 2005), while fine root length reached 17.0 mm per gram of soil in field microplots (Schreiner et al. 2012b) and over 50 mm per gram of soil in greenhouse trials (Schreiner and Pinkerton 2008, Schreiner et al. 2012a). The ring nematode does not have to spend nearly as much energy foraging for a suitable fine root feeding site in confined conditions of a microplot or greenhouse container as it would need to spend foraging in actual vineyards. Imagine how much more energy you would use if you had to drive 50 miles to the nearest grocery store! Another factor which may contribute to higher populations of ring nematode in microplot or greenhouse studies is the increased frequency of irrigation applied to these systems. Prolonged dry conditions encountered in commercial vineyards may trigger ring nematode to become dormant or quiescent, reduce feeding, and hinder population increase.
After more than a decade of research, we now have a good understanding of the occurrence of ring nematode in Oregon vineyards and its impact on vine productivity. Based upon this knowledge, we provide considerations with respect to risks for ring nematode causing economic damage to grapevines in western Oregon:
The greatest risk is planting on sites with previous vineyard or orchard crops. Testing for ring nematode is recommended in such cases. If high ring nematode populations are found, consider planting to 420A rootstock, as this is the only rootstock we have found to possess durable resistance to high ring nematode pressure.
A small risk may be encountered in vineyards that are planted at high density, require frequent irrigation, or carry a high crop load. High fine root density that increases the food supply for ring nematode will likely result from high density plantings and frequent irrigation, particularly on shallow soils. A higher crop load may reduce vine carbohydrate reserves and increase the potential for ring nematode to cause damage to vines.
At the present time, there is little concern about ring nematode causing significant damage in Oregon vineyards. However, it is possible that ring nematode populations could reach levels observed in our controlled experiments as more acreage is planted, particularly at high vine density. Whether these population increases and/or vine damage occurs or not should be reevaluated with another survey in about ten years. This will be appropriate to gauge whether greater concern about ring nematode is warranted in the future.
Literature Cited
Hussey, R.S., C.W. Mims, and S.W. Westcott III. 1992. Ultrastructure of root cortical cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 167: 55-65.
McKenry, M.V. 1992. Nematodes In Grape Pest Management. 2nd ed. D.L. Flaherty et al. (eds.), pp. 281-285. Publication 3343. University of California, Division of Agriculture and Natural Resources. Oakland.
Pinkerton, J.N., T.A. Forge, K.L. Ivors, and R.E. Ingham. 1999. Plant-parasitic nematode associated with grapevines, Vitis vinifera, in Oregon vineyards. J. Nematol. 31: 624-634.
Pinkerton, J.N., R.P. Schreiner, K.L. Ivors, and M.C. Vasconcelos. 2004. Effects of Mesocriconema xenoplax on Vitis vinifera and associated mycorrhizal fungi. J. Nematol. 36: 193-201.
Pinkerton, J.N., M.C. Vasconcelos, T.L. Sampaio, and R.G. Shaffer. 2005. Reaction of grape rootstocks to ring nematode Mesocriconema xenoplax. Am. J. Enol. Vitic. 56: 377-385.
Schreiner, R.P. 2005. Spatial and temporal variation of roots, arbuscular mycorrhizal fungi, and plant and soil nutrients in a mature Pinot Noir (Vitis vinifera L.) vineyard in Oregon. Plant Soil 276:219–234.
Schreiner, R.P., and J.N. Pinkerton. 2008. Ring nematodes (Mesocriconema xenoplax) alter root colonization and function of arbuscular mycorrhizal fungi in grape roots in a low P soil. Soil Biol. Biochem. 40: 1870-1877.
Schreiner, R.P., J.N. Pinkerton, and I.A. Zasada. 2012a. Delayed response to ring nematode (Mesocriconema xenoplax) feeding on grape roots linked to vine carbohydrate reserves and nematode feeding pressure. Soil Biol. Biochem. 45: 89-97.
Schreiner, R.P., I.A. Zasada, and J.N. Pinkerton. 2012b. Consequences of Mesocriconema xenoplax parasitism on Pinot noir grapevines grafted on rootstocks of varying susceptibility. Am. J. Enol. Vitic. 63: 251-261.
