Phylloxera in the San Joaquin Valley
Karl Lund, UCCE Madera, Merced & Mariposa Counties
Grape phylloxera (Daktulosphaira vitifoliae) are an aphid-like insect parasite of grapes. During a farm visit in western Madera county during the fall of 2019 I observed phylloxera infesting the root system of own-rooted wine grapes. This is a good reminder that phylloxera are present in the San Joaquin Valley (SJV) and can be damaging. Therefore, it is important to have a basic understanding of Phylloxera, their effects on different types of grapevines, and how to identify them. Phylloxera feeding results in three distinctive signs: galls on the leaves, nodosities on young unlignified roots, and tuberosities on mature lignified roots. These different feeding types have a range of effects on the grapevine host. Different grapevine species also succumb to different feeding types.
The first items to understand about phylloxera is their size and basic reproduction (Image 1). While phylloxera are not microscopic, they are very small. Both phylloxera eggs and crawlers start off bright yellow in color before quickly fading and changing color to a dull orange. This color allows them to blend in with lighter colored roots and soils. Adult phylloxera can get to approximately 1 mm (0.04 inch) in length, while eggs are only 0.3 mm (0.01 inch) in length. The nymph stage, commonly called a crawler, start off the same size as an egg, but after a few molts and a couple weeks grows to their adult size. Between their size and color, it is recommended to use a small 10X to 20X hand lens to properly identify phylloxera. Lightly blowing on (living) phylloxera will cause them to wave their antenna around. This is a great final way to distinguish them from oddly shaped sand particles.
Image 1 Phylloxera reproductive cycle. The stages of the phylloxera reproductive cycle are shown from left to right. Starting off as an egg, that hatches to a nymph commonly called a crawler, which matures into a sedentary adult laying asexual (clonal) eggs. The phylloxera life cycle is placed on a one-dollar bill for size comparison.
Image 2 Phylloxera Nodosities. A variety of phylloxera caused nodosities including: A. a hooked gall with little swelling; B. a swollen gall with no hooking; C. a gall with exaggerated hooking with no swelling; D. a hooked and swollen gall.
Nodosities are the most common sign of phylloxera in California. Phylloxera feeding on young unlignified roots causes the roots to swell and often hook (Image 2). These hook galls can look similar to damage caused by the dagger nematode Xiphinema index. Therefore, it is advised to use a small hand lens to try and directly identify the phylloxera. These galls cause the root tip to prematurely die back, but do not affect the remainder of the root system. Unlignified roots are where grapevines uptake most of their water and nutrients from the soil. If phylloxera populations are large enough to drastically reduce the number of unlignified root segments across a whole vine, they can lower the plants ability to uptake water and nutrients, weakening the vine. However, this type of damage would require a very high population of phylloxera. Most grapevines form nodosities, however, there are a few exceptions. Vitis rotundifolia as a species appears to have complete resistance to this type of damage and does not form nodosities. Many selections of V. cinerea and several selections of V. berlandieri also show strong resistance to this type of feeding. When looking at rootstocks, O39-16, and the German rootstock Börner have very strong resistance to this feeding type. The remainder of the common rootstocks allow this feeding type to occur.
Leaf galls are common across phylloxera’s native range in the eastern US. With foliar feeding the phylloxera infest young leaves causing the leaf to produce wart-like galls that surround the phylloxera (Image 3). Erineum mite can produce a similar gall that can be misidentified as a phylloxera gall. The easiest way to tell the difference in galls is that phylloxera galls are closed on the underside of the gall, while Erineum mite galls are open on the underside of the gall. A large number of foliar phylloxera galls cause the leaves to deform their shape. This deformation diminishes the leaves’ photosynthetic ability, and with a large enough infestation can reduce the photosynthetic capacity of the entire canopy. Much like nodosities, if the population is allowed to get big enough it can affect the vigor of the plant but will not kill it. This type of feeding is found universally on American Vitis species (V. riparia, V. rupestris, V. berlandieri, etc.), except for V. rotundifolia which again appears to have species wide resistance. Leaf galls can occur on V. vinifera , but the phylloxera seem to dislike it as a foliar host. During an outbreak at a germplasm repository outside of Davis, foliar galls were observed on pure V. vinifera varieties. However, these galls only formed when heavily infested shoots from regular hosts were found directly above the infested leaves. Young leaves directly up the shoot from infested V. vinifera leaves also showed no infestation, which is commonly how foliar phylloxera infestations progress. As most rootstocks are hybrids of V. riparia, V. rupestris, and V. berlandieri they allow leaf feeding to readily occur. O39-16 does appear to be the only common rootstock to have resistance to this feeding type.
Image 3 Phylloxera Foliar Galls. A series of phylloxera foliar galls going from: A. young crawlers establishing feeding sites on a young leaf; B. a mature phylloxera gall; C. an opened phylloxera gall exposing the feeding adult and her clutch of eggs.
Tuberosity feeding is the most destructive feeding type. In tuberosity feeding the phylloxera infest mature lignified roots. The infestation site swells and cracks (Image 4) allowing for secondary soil fungi to enter the mature root system. These fungi are normally not able to penetrate the lignified root systems, and once inside can cause the roots to start rotting. The infestation site eventually dies off, but not before large numbers of phylloxera eggs have been produced to infect more of the mature root system. As tuberosities can form on lignified roots, it effects all portions of the root system, eventually leading to the collapse of the entire root system and vine death. V. vinifera, as well as all Chinese Vitis species tested, are affected by this type of feeding.
All American Vitis species have resistance to this type of feeding. This is why V. vinifera scions are grafted onto rootstocks that are, or are bred from, American Vitis species. In most cases hybrids of V. vinifera and American Vitis species, such as the rootstock AXR#1, turn out to also be susceptible to tuberosity feeding. The notable exception to this is hybrids between V. vinifera and V. rotundifolia, which seem to segregate 1:1 for susceptibility to tuberosity formation. The rootstock O39-16 owes it breeding to this cross and after many decades of use has no signs of succumbing to phylloxera feeding. While the failed rootstock O43-43 was also from the same cross and was susceptible to tuberosity formation.
Since V. vinifera is susceptible to tuberosity formation, and there are many acres of own rooted grapevine in the SJV, how do they survive? The SJV has a couple natural defenses against phylloxera. The first of these is soil type. For a reason that is still unknown, phylloxera have problems infesting roots in sandy soil. As many soil types within the SJV are sandy, this does give a natural defense to vineyards on sandy soil.
Image 4 Phylloxera Tuberosities. Tuberosities formed on the roots of: A. Chardonnay, and B. Colombard. Red arrows point to callus tissue formation on area were lignified tissue has cracked. These sites are where secondary soil fungi can gain access to root system leading to root death.
Another defense in the SJV is high soil temperature. Phylloxera eggs, and especially crawlers, have a limited range of temperatures in which they can survive (Table 1). The work done by Grannet and Timper (1987) has shown that when crawlers get above 90o F, or below 61o F, their survival drops below the level required to maintain population size. When temperatures are outside of this range phylloxera populations will diminish as the life cycle will be broken.
The work of Grannet and Timper (1987) continued by tracking soil temperature in vineyards within different portions of California. They found that: vineyards in Spreckels (Monterey county) saw 9 continuous months with temperatures permitting phylloxera population growth. And vineyards in Hopland (Mendocino county) saw 7 continuous months with temperatures permitting phylloxera population growth. While Fresno county only had temperatures within the correct range for phylloxera population growth for 3 months in the spring and 3 months in the fall. This would mean that in Fresno county phylloxera have 3 months in the spring that allow population growth before it becomes too hot. The summer heat would then prevent the population from increasing, and possibly reduce it. The cooler fall would then allow population growth again for another 3 months. However, the winter would come and reduce the population.
This gives Fresno, and the rest of the SJV an advantage when controlling phylloxera. The natural temperature extremes in both the summer and winter prevent phylloxera populations from exploding like they can in many other portions of California. It is not a death blow to phylloxera. The temperature readings used in the study were taken at almost 8 inches in depth (for Fresno). Soils deeper down will be exposed to less temperature extremes. Grape roots can penetrate much deeper than 8 inches, and the phylloxera will follow. These deeper depths would give phylloxera a refuge to hide in during the hotter and colder portion of the year. Canopy management practices that lead to nearly full ground shading (overhead raisin trellising) would also decrease soil temperature, although the exact effects of this cooling are unknown.
Table 1 Phylloxera Survival vs Temperature. The survival rate of different stages of phylloxera are plotted against a range of temperature.
*Data from Granett and Timper 1987.
Table 2 Vineyard Soil Temperature. The average monthly soil temperature was collected at 15 cm (5.9 inch) in Spreckels (Monterey county) and Hopland (Mendocino county), and at 20 cm (7.9 inch) for Fresno county. Dashed lines indicate the upper and lower temperature limits of crawler survival.
*Data from Granett and Timper 1987.
Image 5 Phylloxera and Water. A. Phylloxera getting stuck to water drop; B. phylloxera getting surrounded by water drop C. phylloxera drowning in mass within a water drop.
Common practices also help control phylloxera populations within the SJV. The first of these was extremely popular but has faded with time: flood irrigation. During the phylloxera invasion of France in the late 1800’s it was found that flooding a vineyard with 40 cm (15.75 inches) of water for 40 days was effective at reducing phylloxera populations. This is partially due to an interesting combination of biology and physics. For small organisms, the surface tension of water can be stronger than the organisms itself. Due to this many insects evolved a layer on their exoskeleton that repels water. As can be seen in image 5, phylloxera skipped this advantage. Water droplets stick to phylloxera with such strength that as the water droplet grows it easily surround and eventually drowns the phylloxera.
General insecticides are another common practice that helps control phylloxera in the SJV. The UC IPM page lists several insecticides that can help with phylloxera control (http://ipm.ucanr.edu/PMG/r302300811.html). Many of these insecticides are used commonly in grape production to deal with other insect issues. A vineyard in Solano county I was monitoring for phylloxera had a major problem with local sharpshooters and was close to a northern CA hotspot for glassy-winged sharpshooters. As such they would spray to control the sharpshooters, but as a byproduct would control the phylloxera population as well. Systemic insecticides used to control other vineyard pests, such as mealybugs, could also have the same effect.
Overall, the SJV has many natural and cultural practices that limit the extent to which phylloxera will affect local vineyards. While these features do limit their possible effects, it does not eliminate them. Especially as vineyards age the effects that phylloxera have will increase with the declining health of the vineyard. It is a pest that is advantageous to understand and be able to identify.
References:
Granett J. and Timper P. 1987. Demography of grape phylloxera (Daktulosphaira vitifoliae) (Homoptera: Phylloxeridae). Journal of Economic Entomology 80: 327–329.