SPIDER MITE MANAGEMENT IN WALNUTS N.J. Mills, E.E. Grafton-Cardwell, and C. Cois ABSTRACT Over the last 10 years new classes of insecticides have been introduced as tools for the management of codling moth, as the key insect pest, to replace the more traditional use of organophosphates. It is not always clear that these ‘reduced risk’ products are selective in the context of the natural enemies that provide effective control of secondary pests such as web-spinning spider mites. The goal of this project is to gain a sufficient understanding of spider mites and their predators in walnuts to be able to enhance the existing biological control for management of spider mites. The main focus during this first year of the project was on conducting surveys of spider mites and spider mite predators in orchards throughout the main walnut growing regions. A series of 21 orchards were surveyed regularly through the growing season to document seasonal and geographic patterns of abundance and species representation. Three web-spinning spider mites were found with twospotted spider mite being the most widespread and abundant species. A set of 11 phytoseiid mite predators were found with Euseius spp., Amblyseius similoides, Typhlodromus caudiglans and Galendromus occidentalis being the most widespread and abundant species. There were distinct geographical differences in the complexes of phytoseiid predators, with Euseius species being numerically dominant in orchards on the eastern side of the Sacramento Valley, whereas Amblyseius similoides was the dominant species in the San Joaquin Valley. In general, G. occidentalis, as a specialist predator of web-spinning spider mites, was found throughout the Central Valley, but appeared in most orchards only late in the season. Insect predators, such as the six-spotted thrips and spider mite destroyer, were generally uncommon. The survey of spider mites and associated predators suggest that the twospotted spider mite is the most important species present in walnuts, that insect predators are generally absent from the orchards, and that there is a large complex of phytoseiid mite predators that vary in relative abundance both regionally and between orchards in the same region. The western predatory mite, G. occidentalis, does not appear to be present in orchards early enough in the season to be effective in providing biological control of the web-spinning mites. In the absence of detailed previous studies of mites in walnuts, additional surveys will be needed to determine how consistent the observed patterns will be between years and the factors that may be compromising the reliability of biological control. OBJECTIVES The overall objective of this project is to gain a sufficient understanding of spider mites and their predators in walnuts to be able to enhance the existing biological control for management of spider mites. The specific objectives are:

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1. Surveys of factors influencing the abundance of spider mites and their predators throughout the major walnut growing regions

2. Early-season releases of Galendromus occidentalis to test the potential to change the dominance of species in the predator mite complex

3. Bioassays to determine the laboratory toxicity and effect of field-aged residues of pesticides on predatory mites

In this first year of the project, the focus of our activities has been on the first of these three objectives. SIGNIFICANT FINDINGS From the regular sampling of spider mites and their predators in 21 walnut orchards throughout the Central Valley in 2013 the following significant findings emerged: • What spider mite species occur in walnut orchards? Four spider mite species were found:

European red mite was widespread and low in abundance; twospotted spider mite was numerically dominant in all orchards sampled; Pacific spider mite was present in orchards in the Sacramento Valley, absent from the northern San Joaquin, and abundant in the southern San Joaquin; and strawberry spider mite was found in the southern San Joaquin only at low abundance.

• How abundant were the insect predators of spider mites? Only 2 of 21 orchards sampled had significant number of six-spotted thrips and spider mite destroyer. In general insect predators where either absent or in very low numbers.

• How abundant were the phytoseiid mite predators of spider mites? A total of 11 different

predator species were found and their abundance varied with walnut growing region. Ineffective Euseius species dominated the eastern Sacramento Valley and Amblyseius similoides a species with low efficiency against web-spinning mites dominated the San Joaquin Valley, and the web-spinning spider mite specialist Galendromus occidentalis was generally found only late in the season in significant numbers.

• In the southern San Joaquin Valley, where miticides were routinely applied to manage spider

mites, predatory mite populations were severely reduced by Omite, Fujimite, but to a lesser extent Zeal, Agri-Mek, Epi-Mek, Temprano. The negative effect was longer lasting if full label rates of the miticides were applied.

• Are these patterns typical for walnuts or the result of changing materials used for codling

moth and husk fly? In the absence of any detailed studies of spider mites and predators in walnuts, it is unclear how typical these patterns are. A second year of survey will be needed to determine if the pattern is consistent between years, and to better identify whether pesticides are having an influence.

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PROCEDURES 1. Objective 1. Surveys of factors influencing the abundance of spider mites and their predators

throughout the major walnut growing regions Surveys of spider mites, predatory mites and other mite predators were made in 10 pairs of orchards spanning the major walnut growing regions of the central Valley in 2013 (Fig. 1). Five pairs of orchards were selected in the Sacramento Valley; one pair of orchards in Red Bluff and a second in the Winters area were designated as western Sacramento Valley, and paired orchards in Gridley, Wheatland and Nicolaus were designated as eastern Sacramento Valley. An additional five pairs of orchards spanned the San Joaquin Valley: two pairs of orchards in Farmington and a single orchard in Linden constituted the northern San Joaquin Valley sites, while pairs of orchards in Hanford, Farmersville and Porterville were sampled in the southern San Joaquin Valley. The pairing of orchards was to allow spider mite and predator populations to be compared between walnut cultivars in the same locations. For most locations Chandler, as the most widely planted cultivar, was compared with another dominant cultivar (Hartley, Howard, Serr, Tulare or Vina). Two exceptions were the Winters area, where a block initially thought to be Chandler turned out to be Tulare and so was matched with Hartley, and in Linden where a Chandler block was not available for sampling. For each orchard, the cultivar, age, ground cover, surrounding landscape, and pesticide treatments were also documented. For each of the orchards sampling for spider mites and predators was conducted from June through October, either every two weeks (Sacramento Valley locations) or every month (San Joaquin Valley locations). Ten trees were randomly sampled in each orchard on each sample date, collecting the three terminal leaflets from four leaves from both the lower and mid canopies of each tree to give a total of 80 sets of terminal leaflets on each occasion. The leaflets from each tree were collected into separate paper sandwich bags and placed into coolers for return to the laboratory where the spider mites and predators were removed from the leaflets using a mite-brushing machine. Mites and predators from the 24 leaflets (8 leaves x 3 terminal leaflets) of each sample tree were combined onto a single plate and motile stages only (excluding eggs) were counted to provide estimates of densities per leaflet for the following categories: web spinning mites (Tetranychus species), European red mite (Panonychus ulmi), phytoseiid predators (all species combined), and insect predators (six-spotted thrips Scolothrips sexmaculatus, spider mite destroyers Stethorus punctipes, and minute pirate bugs Orius minutus). While European red mite is not an important pest species in walnuts it can be an important food source for mite predators. Samples from all 10 trees combined were used for identification of the spider mite and phytoseiid mite species present in each orchard on each sample date. Identification of the spider mites was based on random sub-samples (up to 15 individuals from each orchard on each sample date) after slide mounting individuals in Hoyer’s medium under cover slips and warming at 45 °C for 3-5 days to clear the body contents. Identifications were based on mature males for locations in the San Joaquin Valley and on mature females for Sacramento Valley locations. All adult females of the phytoseiid mites collected from each orchard on each sample date were slide mounted for identification.

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RESULTS Objective 1. Surveys of factors influencing the abundance of spider mites and their predators throughout the major walnut growing regions Web-spinning spider mites (Tetranychus species) were generally more abundant than European red mite in all orchards sampled (Table 1). Three different species of web-spinners were found in our surveys; twospotted spider mite (T. urticae), Pacific spider mite (T. pacificus) and strawberry spider mite (T. turkestani). Twospotted spider mite was the most abundant species in all growing regions (Fig. 2). Pacific spider mite was found occasionally throughout the Sacramento valley locations, was absent from the northern San Joaquin locations, and was almost as abundant as twospotted spider mite at the southern San Joaquin locations. Strawberry spider mites were found only in small numbers and only at the southern San Joaquin locations. The average abundance of web-spinning spider mites was generally greater in the Sacramento Valley than in the San Joaquin Valley (Table 1) and this was largely due to a difference in the use of mid-season miticides such as Abamectin, Fujimite and Zeal. Consequently, there were generally higher populations of phytoseiid predators in the Sacramento Valley, but there was little evidence of a greater abundance of the insect predators of spider mites. The latter were present at significant densities in only 2 of the 21 orchards sampled, the Hartley orchard in Winters and the Serr orchard in Porterville (Table 1). The pattern of abundance of web-spinning spider mites and the phytoseiid predators varied considerably between orchards. In the Sacramento Valley web-spinning spider mite populations were very low in early June, but in several cases populations grew to peak levels of abundance in August or September (Fig. 4). Bronzing of the walnut foliage was apparent when densities of web-spinning mites reached approximately 5 motile stages per leaflet, but there was little evidence of premature leaf drop even when densities exceeded 100 motile stages per leaflet. In contrast, populations of web-spinning spider mites in the San Joaquin Valley were either naturally low throughout the season (Porterville, Chandler) or were kept at low levels of abundance through applications of miticides (Fig. 5). Applications of Fujimite and Omite reduced web-spinning mites to undetectable levels for longer periods, whereas abamectin and Zeal appeared to reduce mite abundance for only 1-2 months. In general, phytoseiid predator populations tracked the patterns of abundance of the web-spinning spider mites in all orchards and were seldom less than 10-fold lower in abundance, providing a favorable ratio of predators to prey. However, there was little indication that the predatory mites were providing effective biological control of the web-spinning mites, and certainly did not prevent the latter from reaching high levels of abundance in some of the Sacramento Valley orchards. Closer examination of the phytoseiid predators present in the orchards revealed a complex of 11 different species. Three species, Metaseius sp., Metaseiulus smithi, and Neoseilulus barkeri were represented by only 1-2 individuals and so can be considered incidental, but the remaining 8 species (Table 2) were found more consistently in several different locations. Of these, only two species Galendromus occidentalis and Neoseiulus californicus are type 2 phytoseiid predators that specialize on web-spinning mites as prey. The remaining species are classified either as type

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3 predators (Amblyseius similoides, Metaseiulus citri, and Typhlodromus caudiglans) or as type 4 predators (Euseius quetzali, E. stipulatus, and E. tularensis). The type 3 species feed on tetranychid mites other than web-spinning mites and can also feed on other small insects and pollen. The type 4 predators feed on the same food sources as the type 3 predators, but can also feed on leaf exudates. For orchards in the western region of the Sacramento Valley type 4 predators were present, but poorly represented, and type 3 predators present earlier in the season were largely replaced by G. occidentalis in August and September (Fig. 4a,b). In contrast, orchards in the eastern region of the Sacramento Valley the predatory mite complex was dominated by type 4 species, particularly E. stipulatus, throughout the season, with G. occidentalis appearing only after mid-August (Fig. 4c,d). Type 3 phytoseiid species were the dominant members of the predator complex in the San Joaquin Valley, with A. similoides being abundant in orchards in both the northern and southern regions (Fig. 5). In addition, T. caudiglans was abundant in orchards in the Farmington area while M. citri was better represented in the southern part of the valley (Fig. 5). Type 4 predators were less frequent in the San Joaquin Valley, but as was found in the Sacramento Valley, G. occidentalis was typically represented in the orchards only late in the season (Fig. 5). These differences in representation of the phytoseiid predator species in the four regions of the Central Valley are shown more clearly from their mean relative abundance for the season for orchards within each region (Fig. 6). DISCUSSION Spider mites are consistent secondary pests on tree fruit and nut crops worldwide. For many of these crops, spider mites are of marginal concern as their abundance is suppressed through natural biological control by phytoseiid mite predators. In some cases, such as almonds in California, spider mites are of particular concern as the trees are unusually susceptible to premature leaf drop in response to spider mite feeding damage. Most other tree fruit and nut crops are not as sensitive to spider mite feeding damage and natural biological control by resident predators provides consistent and sufficient suppression of damage, unless the predators are disrupted by pesticide used for the management of other pests and diseases. The well documented cases of spider mite outbreaks in apples in Washington state in the 1960s and in almonds in California in the 1980s were mitigated by the use of lower doses of more selective pesticides, and the introduction of pesticide-resistant western predatory mites. From our survey of spider mite and predator species in walnuts in 2013, initial results suggest that twospotted spider mite is more abundant in walnuts than Pacific spider mite, with the exception of orchards in the southern San Joaquin, where both species are equally abundant. European red mites were widespread, but were low in abundance and are far less damaging that the web-spinning spider mites. Web-spinning spider mites were more abundant in orchards in the Sacramento Valley, where populations tended to peak in August and September. Populations were much lower in the San Joaquin Valley due to more consistent use of mid-season (June/July) miticide sprays. While Fujimite and Omite generally suppressed both web-spinning spider mites and associated predators for long periods, Abamectin and Zeal had a more limited impact that lasted for 1-2 months only.

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The resident predators of spider mites included insects (six-spotted thrips, spider mite destroyer, and minute pirate bug) and phytoseiid mites. The insect predators were notable for their absence from most orchards, and their occurrence late in the season in the two orchards where they occurred in greater number. In contrast, the phytoseiid mites were notable for their presence in all orchards and for the diversity of species present. It has been helpful to categorize phytoseiid predator species into one of four different lifestyles according to the types of food sources that they can use for successful completion of development and reproduction and their role in biological control. Type 1 and 2 lifestyles include specialist predators of web-spinning spider mites that are able to cut their way through the webbing produced by their prey, have a high reproductive potential and are known to be effective in the biological control of their prey. In walnuts, these lifestyles are represented by G. occidentalis and N. californicus, with only the former species being widespread in walnut orchards throughout the Central Valley. Type 3 predators have a broader range of foods including pollen and honeydew, are unable hampered in their movement by webbing, have a moderate reproductive potential, and have proved to be more effective in the biological control of non-webbing spider mites such as European red mite. Among the type 3 predators, A. similoides, was the dominant species in the predator complexes found in the San Joaquin Valley, with T. caudiglans and M. citri also represented. It is generally believed that these type 3 predators are unable to control web-spinning mites effectively, but that they have the ability to competitively displace type 2 predators when web-spinning mites become scarce. It was more of a surprise to find a good representation of Euseius species as type 4 predators in walnuts and of their abundance in orchards on the eastern side of the Sacramento Valley. These predators are typically pollen feeders, although they do also feed on non-webbing mites and other insects as well as leaf exudates, but reproduce only when they have access to pollen. Their populations tend to be highest during bloom or new shoot growth, but surprisingly were abundant all through the cropping season in walnuts. Their competitive ability with respect to type 2 predators is less well known, but their broad range of food sources suggests that they may be similar to type 3 predators in this regard, and a recent study in Spanish satsuma orchards lends some support to this possibility. The representation of phytoseiid predator species varied between the different growing regions, with type 2 predators dominant in the western Sacramento Valley, type 3 predators being most abundant in the San Joaquin Valley, and type 4 species best represented on the eastern side of the Sacramento Valley. Whether the greater use of mid-season miticide sprays and absence of walnut blight sprays in the San Joaquin is associated with the dominance of the type 3 predators in this region is unclear. There were no clear associations between the pesticide programs used in each orchard and either the densities or the species representation of phytoseiid predators. This doesn’t mean that there are no linkages between the two, as it is well known that insecticides can trigger spider mite outbreaks, but rather that the programs used in the orchards surveyed were not similar enough for clear patterns to emerge. In addition, there were no clear associations between either spider mite species or phytoseiid predator species and the crops that immediately surrounded the orchards that were surveyed. However, mites can disperse over considerable distances and thus crops grown in a 2-5 mile radius of an orchard may have a greater influence than those grown around the perimeter.

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Two other points that arose from these initial surveys of spider mites and their predators in walnuts is whether we have a clear picture of action thresholds for spider mite management, and whether G. occidentalis as the key type 2 predator is able to effectively re-establish populations in walnuts in the spring. Walnuts appear able to tolerate higher levels of abundance of spider mites than are typically accepted by growers, but perhaps are treated more consistently in the San Joaquin Valley due to earlier population build up than occurred in the Sacramento Valley in 2013. Thus a greater understanding of action thresholds and simpler monitoring protocols for spider mites in walnuts might be of value to walnut growers and PCAs. Our observation that G. occidentalis typically occurred in walnut orchards only later in the season suggests that even though it does overwinter in walnuts it may experience some difficulty in re-establishing populations successfully in the spring, due either to the late bud burst and availability of prey or to competition and displaced by more generalist type 3 and 4 phytoseiid species. A failure to re-establish in spring might then account for the apparent late season arrival of G. occidentalis following dispersal from other crops. CONCLUSIONS The survey of spider mites and predators in 2013 suggests that twospotted mite is the dominant web-spinning spider mite in walnuts and that the key insect and type 2 phytoseiid mite predators were not as well represented as would be expected. While the reasons for this are not yet clear, it is also too early to know whether these patterns are typical for walnuts in other years or not. The only other survey of mites in walnuts was conducted by Jim McMurtry in Tulare County (1972-74) who also found two-spotted spider mite to be the dominant web-spinner and that type 3 phytoseiid predators were more common than G. occidentalis. However, additional surveys will be needed to determine the consistency of these observations between years, and to determine the influence of pesticide programs and competition from generalist phytoseiid predators on the occurrence and abundance of G. occidentalis and the potential to restore biological control of spider mites in walnuts.

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Table 1. Seasonal abundance of the spider mites and predators found at different walnut locations in the Central Valley in 2013. Location Cultivar Mean (±SE) web-

spinning spider mites per leaflet

Mean (±SE) European red mites per leaflet

Mean (±SE) predatory mites per leaflet

Mean (±SE) predatory insects per leaflet

Sacramento Valley

Red Bluff Chandler 2.770 ± 2.655 0.033 ± 0.033 0.079 ± 0.060 0.007 ± 0.005

Hartley 1.024 ± 1.010 0.001 ± 0.001 0.063 ± 0.022 0.004 ± 0.003

Winters Tulare 3.037 ± 2.800 0.029 ± 0.017 0.285 ± 0.074 0.035 ± 0.013

Hartley 13.879 ± 9.227 0.000 ± 0.000 0.256 ± 0.164 0.176 ± 0.149

Gridley Chandler 0.065 ± 0.035 0.000 ± 0.000 0.124 ± 0.047 0.002 ± 0.002

Hartley 0.133 ± 0.062 0.000 ± 0.000 0.128 ± 0.059 0.002 ± 0.001

Wheatland Chandler 16.925 ± 7.998 0.009 ± 0.004 1.663 ± 0.648 0.010 ± 0.008

Hartley 21.470 ± 14.714 0.004 ± 0.002 1.161 ± 0.459 0.002 ± 0.001

Nicolaus Chandler 4.014 ± 1.547 0.397 ± 0.233 3.165 ± 1.430 0.036 ± 0.018

Howard 2.955 ± 1.079 0.247 ± 0.115 0.857 ± 0.386 0.022 ± 0.020

San Joaquin Valley

Linden Hartley 0.484 ± 0.280 0.183 ± 0.117 0.594 ± 0.230 0.001 ± 0.001

Farmington 1 Chandler 0.117 ± 0.050 0.000 ± 0.000 0.033 ± 0.009 0.000 ± 0.000

Vina 0.017 ± 0.013 0.017 ± 0.017 0.028 ± 0.009 0.006 ± 0.005

Farmington 2 Chandler 0.047 ± 0.024 0.067 ± 0.049 0.019 ± 0.009 0.003 ± 0.002

Tulare 0.509 ± 0.278 0.103 ± 0.038 0.026 ± 0.010 0.012 ± 0.007

Hanford Chandler 0.040 ± 0.036 0.000 ± 0.000 0.074 ± 0.031 0.002 ± 0.002

Vina 0.195 ± 0.153 0.006 ± 0.004 0.036 ± 0.021 0.195 ± 0.153

Farmersville Chandler 0.032 ± 0.014 0.071 ± 0.042 0.079 ± 0.039 0.005 ± 0.004

Tulare 0.002 ± 0.002 0.000 ± 0.000 0.006 ± 0.005 0.000 ± 0.000

Porterville Chandler 0.011 ± 0.005 0.000 ± 0.000 0.017 ± 0.006 0.009 ± 0.008

Serr 3.234 ± 2.764 0.029 ± 0.029 0.051 ± 0.033 0.073 ± 0.057

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Table 2. The food sources and lifestyles (type 2, 3, and 4) of the main phytoseiid predator species found in walnuts Fig. 1. Location of the walnut orchards used in the spider mites and predator surveys in 2013.

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Fig. 2. Relative abundance of the different web-spinning Tetranychus species found in orchards in different walnut growing regions in 2013 a) Sacramento Valley

b) Northern San Joaquin Valley c) Southern San Joaquin Valley

Fig 3. Color code for the phytoseiid predator species represented in the bar charts in Figs 4 and 5

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Fig. 4. Seasonal abundance of web-spinning spider mites and the relative abundance of phytoseiid predator species in example walnut orchards in the Sacramento Valley in 2013

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Fig. 5. Seasonal abundance of web-spinning spider mites and the relative abundance of phytoseiid predator species in example walnut orchards in the San Joaquin Valley in 2013

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Fig. 6. Relative abundance of the phytoseiid predator species in orchards in the different walnut growing regions in 2013

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