Vineyard Managers and Researchers Seek Sustainable Solutions for Mealybugs, a Changing Pest Complex

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Title Vineyard managers and researchers seek sustainable solutions for mealybugs, a changing pest complex

Permalink https://escholarship.org/uc/item/00w2p416

Journal California Agriculture, 62(4)

ISSN 0008-0845

Authors Daane, Kent M Cooper, Monica L Triapitsyn, Serquei V et al.

Publication Date 2008-10-01

Peer reviewed

eScholarship.org Powered by the California Digital Library University of California REVIEW ARTICLE ▼ Vineyard managers and researchers seek sustainable solutions for mealybugs, a changing pest complex ▼ by Kent M. Daane, Monica L. Cooper, In an uncontrolled vine mealybug Serguei V. Triapitsyn, Vaughn M. Walton, infestation in a San Glenn Y. Yokota, David R. Haviland, Joaquin Valley raisin- Walt J. Bentley, Kris E. Godfrey grape vineyard, mealybug and honey- and Lynn R. Wunderlich dew accumulate on the fruit, canes and leaves. Mealybugs have become increasingly important vineyard pests — a result of their direct damage to the vine, their role in transmitting grapevine leafroll viruses, and the costs for their control. Numerous mealybug species are found in vineyards, and each has ▼ An obscure mealy- different biological traits that af- bug infestation fect sustainable control options. We in a Central Coast wine-grape vineyard review the mealybug pests and their shows growth of sooty molds that are natural enemies to provide some often associated with clariﬁ cation about current trends in mealybug excretion (honeydew), espe- biological control tactics and needed cially in cooler grape directions for future work. regions.

ver the past 100 years, a series of different mealybug species have Obeen found in California vineyards, with fi ve species currently causing damage and a sixth posing a threat. Mealybugs have needlelike mouth- specimens collected on coastal buck- Mealybug pests parts that feed on the plant’s phloem, wheat in California in 1900 and was which contains the nutrients needed Most of California’s vineyard mealy- the only vineyard mealybug thought to for mealybug development. As mealybugs are invasive species — although be native to North America (Miller et bugs digest their food, they excrete a some of them have been here for nearly al. 1984) until the arrival of Ferrisia gilli sugar-rich fl uid called “honeydew.” 100 years. For newly invasive species, Gullan. Grape mealybugs can be found All vineyard mealybugs can feed on eradication should be the fi rst response. throughout California’s Central Valley the vine’s trunk, canes, leaves or fruit, If eradication is not feasible, then an and coastal grape regions, as well as and some species feed on vine roots. integrated program that includes clas- in Oregon and Washington vineyards. Crop loss occurs when mealybugs sical biological controls should be con- Typically, there are two generations per infest fruit or excrete honeydew that sidered. For native mealybug species, year (Geiger and Daane 2001). For most covers fruit and leaves, often result- resident natural enemies often provide of the year, grape mealybugs are found ing in sooty mold growth, defoliation substantial control or can be manipu- under the bark, but during the second and sunburned fruit. Continuous high lated to improve their effectiveness. generation (beginning in June) they levels of infestation over successive The history of each mealybug species in move into grape clusters, especially years may also lead to the deteriora- California and its distinctive biological clusters in contact with the trunk or tion of vines. And many mealybug characteristics affect the level of eco- spurs. The population overwinters as species transmit viruses such as grape- nomic damage and potential effective- eggs or small nymphs under the bark, vine leafroll (see sidebar, page 174). ness of biological controls. with a required diapause that helps to However, these mealybug pests can be Pseudococcus. The grape mealybug, synchronize generations each year. controlled, to some extent, by natural Pseudococcus maritimus (Ehrhorn), is one The longtailed mealybug, Pseudo- enemies that are often present in sus- of the oldest California vineyard pests coccus longispinus (Targioni Tozzetti) is tainable management programs. (Essig 1914). It was fi rst described from believed to be of Austro-Oriental origin

http://CaliforniaAgriculture.ucop.edu • OctOBER–DEcEMBER 2008 167 A B Africa, South Africa, Argentina, the Middle East and Mexico. In California, crawlers blown by wind or carried by animals and farm machinery aid its spread. Infested nursery stock (Haviland et al. 2005) and pomace from the wine-grape crush (see sidebar, page 172) can also harbor this pest. Vine mealybug has a number of traits that make it particularly dam- C D aging and difficult to control. Most notably, there are four to seven annual generations in much of California’s grape-growing regions, resulting in rapid population growth. Vine mealybug also feeds on all parts of the vine throughout the season, resulting in a portion of the population protected under the bark. It can feed on a number of plant species; however, while it is common in Europe on fig Ficus( sp.), Common mealybug species in vineyards there are no reports on this host from E are (A) grape mealybug, with orange-to- red ostiolar secretion near the head and California. The closely related citrus anus (the fluid is often a defensive tactic to mealybug, Planococcus citri (Risso), has ward off predators); (B) obscure mealybug; been found on vines but has never been (C) longtailed mealybug; (D) vine mealybug recorded as an economically important approaching a grape berry; and (E) Gill’s mealybug with glasslike rods brushed pest in vineyards. aside to show adult wax pattern. Ferrisia. Ferrisia gilli Gullan is a close relative of the striped mealybug (F. virgata Cockerell), which is probably native to southeastern North America. In fact, until recently the California population was considered to be the (Ben-Dov 1994). This cosmopolitan spe- Biological traits that make obscure striped mealybug, but differences in cies has been resident in California since mealybug more damaging than grape its adult morphology and economic at least 1933 and is best known as a pest mealybug are that it readily feeds on importance in pistachios and almonds of ornamental plants. Longtailed mealy- leaves (causing leaf damage and rain- prompted studies that led to its new bug has been limited to Central Coast ing honeydew down onto grape clus- species description in 2003 (Gullan et vineyards, where it has three generations ters), it can survive on common weeds al. 2003). Damaging vineyard popula- yearly. Unlike the other Pseudococcus spe- such as malva and burclover (Walton tions have only recently been found in cies discussed, longtailed mealybugs give and Pringle 2004b), it has three or four the Sierra foothills. Because F. gilli — birth to live crawlers (1st-instar mealy- overlapping generations per year, and commonly called Gill’s mealybug, after bugs, which disperse before they settle it excretes more honeydew. It is limited, Raymond Gill — is so new to scientists, and feed) rather than depositing eggs. however, to the cooler grape-growing research on its seasonal occurrence The origin of the obscure mealybug, regions, and is most commonly found in has, to date, only been conducted on Pseudococcus viburni (Signoret), is un- Central Coast vineyards. pistachios grown in the Central Valley known, and both Australia and South Planococcus. The vine mealy- (Haviland et al. 2006). There, the mealy- America have been suggested. While bug, Planococcus ficus (Signoret), is bug has three annual generations. In known to be in North America since a relatively new invasive species to fall, adult females produce crawlers that the early 1900s, its history is poorly Californian and Mexican vineyards overwinter in protected crevices of the documented due in part to earlier taxo- (Daane et al. 2006). In 1994, it was trunk and scaffolding branches. During nomic confusion — it is a close relative found in Coachella Valley table grapes, bud-break, the overwintering nymphs of the grape mealybug and was often although it probably entered the state migrate to buds to feed; they become misidentified (Miller et al. 1984). The years before. Vine mealybug has al- adults between late May and mid-June obscure mealybug is primarily a pest of ways been associated with vineyards and give live birth to crawlers, the first ornamental plants but is also found in and was first identified as a new spe- of two in-season generations. Currently, coastal vineyards, especially in associa- cies in the Crimea on grapes in 1868. It studies are ongoing in El Dorado tion with the Argentine ant, Linepithema has since spread and is now a key pest County to determine this mealybug’s humile (Mayr) (Phillips and Sherk 1991). in the vineyards of Europe, northern seasonal occurrence on grapes.

168 CALIFORNIA AGRICULTURE • VOLUME 62, NUMBER 4 Maconellicoccus. The pink hibiscus A B mealybug, Maconellicoccus hirsutus (Green), is an excellent example of an invasive species that presents a significant threat to California grapes but has been limited by a successful classical biological control program (Roltsch et al. 2006). Pink hibiscus mealybug is probably native to Southeast Asia or Australia. It invaded Egypt in 1912, Hawaii in 1984, the Caribbean islands in 1994, Florida in 2002, and reached northern Mexico C D and Southern California in 2003. It has a wide host range of more than 200 plant species. Under optimum temperature conditions, this mealybug can have explosive populations with more than 600 eggs per ovisac and up to 15 generations per year. Natural enemies Hundreds of natural enemies can Common mealybug predators include lady beetles. (A) An adult Scymnus species feeds on a attack mealybugs, making this brief grape mealybug. (B) A large mealybug destroyer larva near the smaller obscure mealybug; review incomplete. Here, we catalog the larvae of many of these lady beetle species have waxy filaments to mimic mealybugs and the more common natural enemies and reduce interference from mealybug-tending ants. (C) A cecidomyiid larva prepares to feed on their potential impact. grape mealybugs. (D) A third-instar green lacewing (Chrysoperla carnea) larva attacks a grape mealybug, prompting it to secrete a ball of red ostiolar fluid in defense. A number of predators contribute to mealybug control; a few specialize on mealybugs, while most are general- Other beetles. Other lady beetle spe- transverse lady beetle (Coccinella trans- ists that prey on any small, soft-bodied cies also attack mealybugs. Many beetle versoguttata [Falderman]). There are no arthropods. For many of these natural larvae in the subfamily Scymninae studies of any of these beetles’ impact on enemies, there are no studies of their are covered with wax, similar to the California mealybugs. impact on mealybug populations. mealybug, and are often mistakenly Lacewings. Lacewings have long Mealybug destroyer. One of the more identified as the mealybug destroyer. been associated with mealybugs. In effective and specialized predators is These include species of Hyperaspis, fact, Doutt and Hagen (1950) first re- the “mealybug destroyer,” Cryptolaemus Nephus (=Scymnobius) and Scymnus, com- ported that the golden-eyed green montrouzieri Mulsant. This lady beetle monly the most abundant mealybug lacewing (Chrysoperla carnea [Stephens]) was imported to California from predators in infested vineyards. Some of suppressed grape mealybugs in pears. Australia in 1891 to help control the these beetles, such as Nephus bineavatus Surveys of coastal vineyards infested citrus mealybug (Bartlett et al. 1978). (Mulsant), were imported for mealybug with mealybugs found C. carnea, Both adults and larvae kill mealybugs. control from South Africa in 1921; oth- Chrysoperla comanche Banks and an The larvae are mealybug mimics. They ers are thought to be native to North unidentified Chrysopa Leach (Daane et have waxlike filaments similar to those America. These species may not be as al. 1996). Lacewing larvae are effective of mealybugs and this “camouflage” dependent on high mealybug pest popu- predators of smaller mealybugs, al- allows beetle larvae to feed amongst lations as the mealybug destroyer and though they have a more difficult time mealybugs without too much distur- therefore, may be more important preda- feeding on eggs in the mealybug ovisac, bance from mealybug-tending ants tors in vineyards with lower mealybug where waxy secretions provide some (Daane et al. 2007). One drawback is population densities. However, because protection from the lacewing larva’s the predator’s poor tolerance to winter the taxonomic keys for these Scymninae mouthparts, or on larger mealybugs, temperatures (Smith and Armitage beetles poorly differentiate among spe- which excrete ostiolar fluid that can act 1920). In 1996, a “cold-hardy” strain of cies, many of the observed beetles are as a defensive mechanism. Often over- the mealybug destroyer was collected never properly identified. Migratory looked, brown lacewings may be im- in southern Australia and released in lady beetles, notably those in the sub- portant mealybug predators in spring California (K.S. Hagen, unpublished family Coccinellinae, are often attracted because they are present and active at data). Material from these releases to large mealybug infestations and their cooler temperatures (Neuenschwander appears to have established and, cur- honeydew; these include some of the and Hagen 1980). Common brown lace- rently, the mealybug destroyer is found large and recognizable species such as wing species are Hemerobius pacificus throughout the coastal wine-grape re- the convergent lady beetle (Hippodamia Banks, Sympherobius californicus Banks gions (Daane, personal observation). convergens Guérin-Méneville) and and S. barberi Banks. No studies docu-

http://CaliforniaAgriculture.ucop.edu • October–December 2008 169 are the largest group, often comprising (fig. 1A). Both Acerophagus species are A. pseudococci Cheiloneurus sp. Zarhopalus sp. more than 90% of arthropod predators gregarious, depositing more eggs in A. angelicus A. notativentris 100 found in vineyards (Costello and Daane larger mealybugs (fig. 1B); these are A 1999). Some spiders, such as Theridion the same key parasitoid species found 80 spp., have been observed feeding on on grape mealybug in Oregon and

60 mealybugs in vineyards. These general- Washington (Grimes and Cone 1985; ist predators are assumed to play a sec- Grasswitz and Burts 1995). In the 1940s, 40 ondary role behind the more specialized a number of parasitoid species were Parasitism (%) predators and parasitoids. imported from Africa to control grape 20 mealybug (Bartlett et al. 1978). The fact Parasitoids — tiny wasps 0 that none of these parasitoids estab- Apr May June July Aug Sept Oct Some of the most important mealy- lished provided further evidence that bug natural enemies are Hymenoptera, the grape mealybug is native to North 30 B or more specifically, tiny encyrtid and America and that the parasitoid species 25 A. angelicus platygastrid wasps (Noyes and Hayat found here may be the most specific to A. notativentris 20 1994). Depending on the species, these this mealybug pest. “internal parasitoids” deposit one (soli- Longtailed mealybug. Soon after 15 tary) or many (gregarious) eggs inside longtailed mealybug was found infest- 10 the mealybug. The parasitoids are clas- ing California citrus in 1933, a number

5 sified as “koinobionts” because the of parasitoid species were imported. Parasitoids/mummy (no.) parasitized mealybug is, initially, active The most important were Tetracnemoidea 0 1 2 3 4 5 (still feeding and moving). As the para- sydneyensis (Timberlake) from Australia, Mealybug (mummy) size (mm) sitoid larva grows internally the mealy- Anagyrus fusciventris (Girault) from bug becomes sluggish and eventually Hawaii and Tetracnemoidea peregrina Fig. 1. (A) Percentage parasitism (●) of grape does not move, producing no new wax (Compere) from Argentina. DeBach mealybug collected in three San Joaquin Valley vineyards, with bar graphs showing filaments and forming a golden-brown et al. (1949) suggested that parasitoids species composition of parasitoids reared “mummified” mealybug. The mummy helped suppress longtailed mealybug on each sample date (Cheiloneurus is a helps protect the developing larval in Southern California, but that preda- hyperparasitoid). (B) Number of Acerophagus parasitoid(s) inside. The larvae pupate tors, especially the mealybug destroyer, angelicus and A. notativentris reared from mealybugs increased with increasing inside the mealybug and the adult were more important. Recent surveys mealybug size. Source: Daane et al. 2001. parasitoid emerges by chewing a hole of longtailed mealybug in coastal vine- through the mummy. Because mealy- yards reared a number of parasitoid ment the impact of green or brown bug parasitoids can be quite special- species including T. sydneyensis, lacewings on mealybugs in California ized, we discuss the complex present in T. peregrina, A. angelicus, Anagyrus vineyards. California for each mealybug group. pseudococci (Girault), Leptomastidea ab- Flies/midges. Cecidomyiid flies — Grape mealybug. Parasitoids thought normis (Girault), Leptomastix dactylopii predaceous midges — are another com- to be native to North America have long Howard and Coccidoxenoides perminu- mon mealybug predator. One midge been credited with grape mealybug tus Girault (Daane et al. 2008). Most of species documented in California control, although the species composi- these were imported to control other vineyards is Dicrodiplosis californica Felt tion has changed over the years. Smith mealybug species, such as the citrophi- (Geiger and Daane 2001). The adult fly, (1916) and Clausen (1924) reported up lus (Pseudococcus calceolariae [Maskell]) which is not predatory, deposits eggs to 80% parasitism of grape mealybugs or citrus mealybugs. Despite a long list in or near the mealybug ovisac and the collected in the Central Valley. In these of natural enemies, outbreaks of long- maggotlike larvae feed, primarily, on pre-1930s surveys, Zarhopalus corvinus tailed mealybug still occur in Central mealybug eggs and small larvae. The fly (Girault) was the dominant parasitoid; Coast vineyards, primarily in the Santa larvae typically pupate in the ground. others were Anagyrus yuccae (Coquillet), Maria appellation. Unfortunately, little is known about Acerophagus notativentris (Girault), Obscure mealybug. Prior to 1993, these predators in California vineyards. Anagyrus clauseni Timberlake and there were no effective parasitoid In New Zealand, Charles (1985) reported Pseudleptomastix squammulata Girault. species of the obscure mealybug in that Diadiplosis koebelei (Koebele) reduced More recent surveys found lower para- California. For this reason, Acerophagus longtailed mealybugs by about 30%. sitism levels and a change in the parasi- flavidulus (Brèthes) and Leptomastix Other predators. Minute pirate bugs toid species complex. epona (Walker) were imported from (Orius spp.), damsel bugs (Nabis ameri- Surveys in the 1970s found that Chile in 1996. Both L. epona and coferus Carayon), big-eyed bugs (Geocoris Acerophagus (=Pseudaphycus) nota- A. flavidulus were initially recovered; pallens Stål), European earwigs (Forficula tiventris was the dominant parasitoid however, foraging ants diminished auricularia Linnaeus) and predaceous (Flaherty et al. 1982), and later surveys the success of these natural enemies mites have all been observed to feed on found Acerophagus angelicus (Howard) (fig. 2A), resulting in higher mealybug mealybugs, but are not commonly found and A. notativentris were common densities (fig. 2B). Currently, only in large numbers in vineyards. Spiders while Z. corvinus was less important A. flavidulus is reported as established

170 CALIFORNIA AGRICULTURE • VOLUME 62, NUMBER 4 A B

600 A 500

400

300

200

100 C D 0

Mealybugs (± SEM) per sampled vine Apr May Jun Jul Aug Sept Oct Nov

Ant-tended Ant-excluded 100 B 80

40 E F Percent parasitism 20 (± SEM) per sampled vine

0 Apr May Jun Jul Aug Sept Oct Nov

Fig. 2. Mealybug and parasitism levels per vine, based on 3 min. timed counts, in ant-tended and ant-excluded treatments for (A) obscure mealybug density and (B) percentage parasitism of obscure mealybug. Source: Daane et al. 2007.

Many parasitoid species attack mealybugs, including: (A) a female Anagyrus pseudococci (ca. 2 mm) near a vine mealybug mummy showing the round parasitoid exit hole; (B) the smaller (ca. 1.3 mm) male A. pseudococci, which has a different color pattern and hairy antennae, feeds on a drop of honeydew; (C) a female Leptomastidea abnormis host-feeds on a vine Mar 15 mealybug crawler; (D) Leptomastix epona was imported for obscure mealybug biological A Outdoors control but did not establish because of Argentine ant interference; (E) the small (ca. 1 Feb 28 Indoors mm) and fast-moving Acerophagus flavidulus closes in on an obscure mealybug; and (F) Coccidoxenoides perminutus (ca. 1 mm) near a vine mealybug first instar. Jan 23 Dec 19 (Daane et al. 2008). Acerophagus maculi- gions. Currently, A. pseudococci, a soli- Nov 15 pennis (Mercet) was recently imported tary parasitoid, is the dominant natural initiation date Trial Oct 18 from New Zealand, where it effectively enemy of vine mealybug throughout Oct Nov Dec Jan Feb Mar Apr May Jun controls obscure mealybug, and is cur- the state, and has a development rate 100 rently undergoing nontarget host evalu- and temperature tolerances that most B ation in the UC Berkeley quarantine. closely match those of the vine mealy- 80 Vine mealybug. The newly invasive bug (Gutierrez et al. 2008). 60 Exposed vine mealybug has become the most However, two biological traits re- Protected serious mealybug pest in California duce levels of natural control. First, 40 vineyards (Daane et al. 2006). From overwintered A. pseudococci remain in 20 1995 to 1999, parasitoids were imported an immature stage inside the mealy-

Parasitized mealybugs (%) 0 from Argentina, Spain, Israel and bug until late April to early May Jun Jul Aug Sept Oct Nov Turkmenistan, and included A. pseudo- (fig. 3A), delaying their period of ac- cocci, L. abnormis, C. perminutus and tivity until after the mealybug is ac- Fig. 3. (A) Average emergence periods for Anagyrus pseudococci on vine mealybug that were exposed to L. dactylopii (González 1998). These spe- tive. Second, the parasitoid does not the parasitoid from October through March, and then cies were already present in California, effectively forage under the vine bark stored either inside at room temperature or outside brought in to control the citrus mealy- (fig. 3B), where the mealybug finds at ambient air temperatures for Fresno County. bug; however, the newly imported refuge. An ongoing program is evalu- Source: Daane et al. 2004. (B) Percent parasitism of vine mealybugs (collected during a timed count) material may have biological charac- ating the biology and molecular iden- separated by location where mealybugs were teristics better suited to environmental tification of A. pseudococci populations collected as exposed (e.g., on leaves) or protected conditions in California vineyard re- collected in Europe and the Middle (e.g., under bark). Source: Daane et al. 2006.

http://CaliforniaAgriculture.ucop.edu • October–December 2008 171 Pomace management reduces spread of vine mealybugs

by Rhonda J. Smith and Lucia G. Varela

fter vine mealybug was first identified in North Coast wine-grape vineyards Ain 2002, growers and wineries needed an- swers to reduce the movement of this pest between vineyards. We investigated the potential for vine mealybugs to survive in one type of winery waste (or pomace) that is often spread over the vineyard floor during the harvest period. The pomace we investigated contains unfermented berry skins, seeds and cluster stems. This fresh material is produced by pressing hand-harvested whole clusters or mechanically harvested berries; the juice is then fermented. Alternatively, clusters are Pomace piles were covered with clear plastic or remained uncovered processed by a destemmer-crusher, after to evaluate vine mealybug survival. which skins and seeds are fermented with the juice, producing sediment also known bug crawlers (the small immature stage) clusters had an average of 1,211 live as pomace. Because insects do not survive per cluster. Afterward, this dropped to vine mealybugs per stem. the fermentation process, we focused on an average of 192 crawlers per cluster Results showed that vine mealybug the survival of vine mealybug in fresh (4.0% survival). mortality was higher when pomace pomace collected from the winery press These trials showed that vine mealy- piles were covered for 1 to 4 weeks with after whole clusters were pressed, as well bugs can survive whole-cluster press- clear plastic than when piles were left as in piles of fresh pomace placed on the ing. As a result, fresh pomace can be a uncovered (table 1). When uncovered, vineyard property. source of vine mealybug contamination more vine mealybugs survived in piles Mealybug survival after whole-cluster for wineries or growers who tradition- consisting of mostly stems discarded press. Two trials were conducted in winer- ally spread this harvest residue directly from the destemming process than in ies located in Sonoma County to determine in the vineyard or who stockpile un- the denser, moister piles composed pri- if vine mealybug survived whole-cluster managed piles of it near the vineyard. marily of berry skins and seeds from pressing. In the first trial, a 6-ton load of in- Controlling mealybugs in pomace. the whole-cluster press. Uncovered fested ‘Grenache’ grapes underwent a press Another experiment evaluated vine piles composed primarily of stems had regime ranging from 0.2 to 1.8 bars of pres- mealybug mortality in static pomace greater survival of vine mealybug over sure. Before pressing, we found an average piles that were either uncovered or time because these piles did not gener- of 47 live vine mealybugs per cluster. After covered with clear plastic. Infested ate high enough temperatures to kill the press was completed, there were an av- cluster stems were placed inside mesh vine mealybugs. erage of 0.04 live vine mealybugs per clus- bags that were then inserted 1-foot In contrast, when pomace piles were ter (0.085% survival). In the second trial, (0.3 meter) and 3-feet (0.9 meter) deep covered, vine mealybugs were reduced single infested clusters were placed inside into pomace piles that were 4 feet by nearly 100% in both “stemmy” and mesh bags and added to a 12-ton load of (1.2 meters) tall and 15 feet (4.5 me- nonstemmy piles. In addition, when ‘Chardonnay’ grapes that underwent a ters) across, approximately the size covered there was no difference in similar press regime. Before pressing, we of piles created by dump trucks com- mortality at different depths in either found an average of over 4,800 vine mealy- monly used by wineries. Initially, the type of pile. Fresh pomace piles gener- ate heat as organic material degrades. TABLE 1. Reduction in vine mealybug on cluster stems after 1 and 4 weeks Temperature loggers recorded sig- in two depths, in covered and uncovered pomace piles nificantly lower fluctuation at higher temperatures of 120°F to 130°F (50°C to Reduction in vine mealybug Infested stem 55°C) in pomace piles with fewer stems Treatment Pile composition position in pile Week 1 Week 4 and more moisture, than at tempera- ...... % ...... tures of 68°F to 130°F (20°C to 55°C) Uncovered piles Mostly stems Top 67.6 89.4 Bottom 60.7 87.5 in piles with a greater mass of cluster Mostly skins and seeds; Top 99.9 > 99.9 stems, which are slower to break down few stems Bottom 99.9 100 (data not shown). Covered piles Mostly stems Top >99.9 100 Recommendations. To reduce the risk Bottom 100 100 of contaminating vineyards with mealy- Mostly skins and seeds; Top 100 100 bugs, growers should avoid spreading few stems Bottom > 99.9 > 99.9 pomace in vineyards unless it has been

172 172CALIFORNIA CALIFORNIA AGRICULTURE AGRICULTURE • VOLUME • VOLUME 62, NUMBER 62, NUMBER 4 4 covered with plastic for at least 1 week. East, noting that this parasitoid is included fumigation with potassium Optimally, pomace piles should be lo- probably a complex of more than one cyanide (Essig 1914), and later materials cated away from vine rows and securely species (Triapitsyn et al. 2007) and included DDT and organophosphates covered as soon as feasible, so heat that other “strains” may be better suited (e.g., parathion) (Stafford and Kido 1955). is generated remains inside the pile. for California. Eventually it became evident that the To help increase temperatures inside Gill’s mealybug. Very little is known insecticidal materials disrupted the stemmy piles and decrease vine mealy- about parasitoids of F. gilli, as this spe- relatively good control provided by bug survival, cluster stems collected cies was only described in 2003. From parasitoids. Flaherty et al. (1982) stated from a winery’s destemmer should be collections of F. gilli in El Dorado County that “extensive use of DDT and other mixed with dense material, such as vineyards, as well as San Joaquin Valley synthetic insecticides used to control pomace from either whole-cluster or me- almonds, it appears that Acerophagus grape leafhopper disrupted natural con- chanically harvested press loads. Front- sp., Chrysoplatycerus sp. and Anagyrus trol of grape mealybug.” Currently, there end loaders, which are commonly used pseudococci will attack F. gilli. High levels are many effective materials, such as in many wineries, may be used to mix of parasitism have been recorded by systemic neonicotinoids, insect growth pomace piles to some degree. Acerophagus sp. nr. meritorius (Gahan) regulators and tetronic acids that inhibit We did not evaluate the survival or A. sp. nr. mundus (Gahan) (the spe- lipid biosynthesis, which can be used of vine mealybug in composted pom- cies cannot be determined because of with reduced impact on natural enemy ace. At facilities required to obtain indecisive species descriptions and poor populations. Use of these more narrow- a Compostable Materials Handling type specimens [Daane et al. 2008]). The spectrum materials may have a less dis- Facility Permit from the California Acerophagus sp. was most likely pres- ruptive effect on biological controls. Integrated Waste Management Board, ent in California as a parasitoid of the Ant controls. Ants can exacerbate regulations require that the windrow closely related striped mealybug, Ferrisia mealybug pest problems by disrupting composting process under aerobic con- virgata. Currently, research is investigat- natural enemy activity in vineyards ditions maintain a temperature of 131°F ing parasitism levels of F. gilli in Sierra (Daane et al. 2007). Unfortunately, (55°C) or higher for 15 days or longer to Foothill vineyards. insecticide controls for ants are often reduce pathogens. During that period, Pink hibiscus mealybug. In India, more disruptive than materials applied the windrow must be turned a mini- the pink hibiscus mealybug is a major for the mealybugs. For that reason, re- mum of five times. Given these rigorous pest of grapes, reducing yields 50% to searchers have developed protein and requirements, this process is likely to 100%. That it is not a pest in California sugar baits for ant control in vineyards, result in similar or increased mortality vineyards may be the direct result of a which can be effective alternative prac- of vine mealybugs compared to static, successful biological control program tices (see page 177). covered pomace piles. that has limited its spread in the state. Augmentation. There are few re- Sanitation practices are recom- After the mealybug was found in the ports of successful augmentation — mended to avoid spreading any spe- Caribbean in 1994, a cooperative clas- when natural enemies are reared in cies of mealybug. Many wineries, sical biological control project was an insectary and released into the tar- regardless of size, find it challenging to established for that region, and later geted habitat — for mealybug control cover pomace with clear plastic as it is extended to California when the pink in vineyards, in part because this has generated. During the harvest period, hibiscus mealybug was found south of not been adequately studied. pomace may be produced daily at a the Coachella Valley table-grape region. In fact, one of the first commercial rate of approximately a ton of pomace The parasitoids Anagyrus kamali Moursi, insectaries in North America was devel- for every 3 to 6 tons of grapes, so the Gyranusoidea indica Shafee, Alam & oped in 1916 to rear the mealybug de- lack of space to store and manage this Agarwal and Allotropa sp. nr. mecrida stroyer for the citrus mealybug (Smith material away from grapevines is a (Walker) were released and, over a and Armitage 1920). Today, this beetle critical problem. Bins and dump trucks 5-year period, mealybug density pro- is commonly released in vineyards, that are used to move pomace during gressively declined to noneconomic lev- but release rates, timing and expected the production process may potentially els (Roltsch et al. 2006). Currently, pink outcomes have not been scientifically contaminate subsequent loads of fresh hibiscus mealybug populations are evaluated. Until those studies are con- grapes with mealybugs. Containers maintained at low levels by these natu- ducted, understanding the biology used to haul grapes and pomace ral enemies, and the pest populations of the mealybug destroyer may help should be cleaned with a high-pressure have been contained in the very south- improve release effectiveness. Beetles sprayer before they are moved offsite. ern portion of the state — currently out are sold as adults and when released of vineyard growing areas. into the vineyard they typically begin searching for mealybug ovisacs, where R.J. Smith is Viticulture Farm Advisor, UC Coop- Manipulating natural enemies they will deposit eggs. If no ovisacs erative Extension (UCCE), Sonoma County; and Insecticides. L.G. Varela is Integrated Pest Management (IPM) Vineyard mealybugs are are found, many of the beetles may Advisor, UC Statewide IPM Program and UCCE often controlled with insecticides. Prior fly away; therefore, releases should be Sonoma County. This study was funded in part to the 1990s, most insecticides were not timed to coincide with the presence of by the USDA Exotic/Invasive Pests and Diseases compatible with biological controls. For ovisacs (or females depositing crawlers Research Program. example, early grape mealybug controls in the case of the longtailed mealybug).

http://CaliforniaAgriculture.ucop.edu • October–December 2008 173 Studies needed of vectors spreading leafroll disease in California vineyards

by Deborah A. Golino and Rodrigo Almeida

eafroll, a common disease of grape- about the biology of leafroll transmission vines caused by a large group of by mealybugs or scales, a research gap we relatedL viruses, reduces the yield and are currently working to fill. quality of fruit from infected vines. Yield Research goals. Control of insect-borne losses of 10% to 20% are fairly typical. plant diseases such as leafroll depends Leafroll damages the phloem of infected upon a solid understanding of pathogen vines, delaying sugar accumulation transmission biology. This knowledge and reducing anthocyanin production. could help explain the efficiency, or lack Fruit from infected vines is low in sugar, thereof, of certain insecticides in reduc- poorly colored and ripens late. In some ing disease spread. It might be the basis Sue Sim varieties, fruit maturity is delayed so that for the development of roguing strategies A leafroll-infected grapevine. fruit on the affected vines may be pale (i.e., the removal of infected vines to pre- or even whitish at harvest, while fruit on vent virus from spreading), and it should Valley is probably driven by another healthy vines is ripe and well colored; late result in improved and vector sampling factor and not the vine mealybug, as this ripening may also expose the fruit to au- practices. The newly invasive vine mealy- insect has a limited spatial distribution tumn rains that cause rot. bug may result in increased rates of in that area. Factors behind the epidemic In the past, researchers observed little leafroll disease in California, a situation may include a large-scale change of root- natural field spread of leafroll disease in similar to the invasive glassy-winged stocks over the last decade or the emer- California vineyards. Unfortunately, this sharpshooter and Pierce’s disease. Our gence of a virus strain that is transmitted situation seems to have changed. In the research groups are working to under- more efficiently by vectors than previ- early 1990s, field spread was observed stand how mealybugs transmit leafroll to ously established isolates. in the UC Davis Foundation vineyard grapes, with the goal of providing grow- Grapevine leafroll viruses are of (Rowhani and Golino 1995). More re- ers with short- and long-term informa- economic importance worldwide. Until cently, the mapping of leafroll distribution that can be incorporated into disease recently this viral disease complex was tion in a ’Cabernet Sauvignon’ vineyard management practices. assumed to be largely graft-transmitted in Napa County documented an increase We have recently determined that under California conditions. The finding in infection rate of approximately 10% per first-instar vine mealybugs are more ef- that mealybugs transmit leafroll was a year over 5 years (see page 156). ficient in transmitting leafroll (GLRaV-3) breakthrough that explained observa- Grapevine leafroll viruses. There are than adult insects. First instars may be tions of disease spread under field condi- currently nine recognized, serologically dispersed by wind, causing them to tions. We are still at the early stages in distinct viruses associated with grape- travel farther than adults. As a result, understanding the most basic aspects of vine leafroll disease. These are unique, virus spread may match these patterns of the biology and ecology of leafroll trans- closely related viruses, not strains of mealybug movement, which in this case mission by mealybugs. the same virus. Taxonomically the nine could be reasonably random. We are now “grapevine leafroll associated viruses” working to identify specific periods of (abbreviated GLRaV-1, and so on) are clas- the year with high risk of disease spread. D.A. Golino is Director, Foundation Plant Services, sified in the virus family Closteroviridae, The rationale is that large numbers of first and Cooperative Extension Specialist, Department which is characterized by large, flexuous, instars are not present in vineyards year- of Plant Pathology, UC Davis; and R. Almeida is As- rod-shaped particles ranging from 1,250 round and spread may be increased when sistant Professor, Department of Environmental Sci- to 2,200 nanometers in length. crawler populations are high; disease ence, Policy and Management, UC Berkeley. Many of these leafroll viruses are control approaches could be developed transmitted by mealybugs and soft scales. to target these times. The incorporation The obscure, longtailed, citrus, grape and of such knowledge, when available, into References vine mealybugs are commonly found in management practices may also reduce Belli G, Fortusini A, Casati P, et al. 1994. Transmission of a grapevine leafroll associated closterovirus by the California vineyards and can transmit the undesirable environmental impacts of scale insect Pulvinaria vitis L. Rivista di Patologia Veg- one or more forms of the virus (Golino certain insect-control strategies. etale 4:105–8. Understanding leafroll transmission. et al. 2002; Martelli 2000). In Europe, soft Golino DA, Sim S, Gill R, Rowhani A. 2002. Grapevine scales such as the vine scale (Pulvinaria We have focused our efforts on the trans- leafroll disease can be spread by California mealy- vitis) have been shown to transmit GLRaVs mission of leafroll by the vine mealybug, bugs. Cal Ag 56:196–201. (Belli et al. 1994); this insect is also found primarily due to its invasiveness and Martelli GP. 2000. Major graft-transmissible diseases in California vineyards, although the more of grapevines: Nature, diagnosis, and sanitation. Proc. present threat to the grape industry. 50th Ann ASEV Mtg. Seattle, Wash. Am J Enol Vitic common soft scale is the European fruit Other mealybugs, however, may be at 51:231–6 lecanium scale (Parthenolecanium corni), least as efficient in transmitting leafroll, Rowhani A, Golino D. 1995. ELISA test reveals new which has been implicated but not yet so they, too, must be assessed. In addi- information about leafroll disease. Cal Ag 49(1):26–9. shown to vector GLRaV. Little is known tion, the current leafroll epidemic in Napa

174 174 CALIFORNIA CALIFORNIA AGRICULTURE AGRICULTURE • VOLUME • VOLUME 62, NUMBER 62, NUMBER 4 4 The beetle is most commonly found in showed that vine mealybug abundance 100 vineyards with many mealybugs and could be reduced by 50% with releases may not be as effective at low mealybug A. pseudococci Control of 10,000 per acre from 80 densities. This suggests the beetle may June to July (fig. 4). Similar success has A. pseudococci be best used by releasing at hot spots been reported in Israel using A. pseudo- 60 where the mealybug density is high. cocci for vine and citrus mealybugs Green lacewings are one of the more (Daane, personal communication). The common commercially produced natu- major limiting factor has been the com- 40 ral enemies. One of their first success- mercial production of parasitoids and ful uses in augmentation was against the cost per acre of release programs. 20 the grape mealybug infesting pears in Because many mealybug parasitoids California (Doutt and Hagen 1950). In are specialists, there is not one parasi- 0 Apr May Jun Jul Aug Sept vineyards, the only published stud- toid species that can be commercially mealybugs per timed count (no.) Average Sample date ies were of green lacewing releases produced and used against all vine- targeting leafhopper pests (Daane and yard mealybugs. Recently, a number Fig. 4. Season-long average density per vine (for timed Yokota 1997), and on the performance of commercial insectaries have shown counts) of vine mealybugs was lower in treatments of mechanically released lacewing eggs an interest in producing A. pseudococci, with Anagyrus pseudococci release, as compared with no-insecticide control plots. Source: Daane et al. 2004. into a vineyard canopy (Wunderlich a particularly good parasitoid for the and Giles 1999). Daane and Yokota’s vine mealybug. Other more specialized work suggested that a critical shortfall species may be good candidates for co- early-harvested varieties are much less of this program was the release meth- operative insectaries. likely to have serious fruit damage than odology, which subjected the lacewing Pheromones. Sexually mature female late-maturing varieties because mealy- eggs and neonate larvae to 60% to 80% mealybugs may emit a sex pheromone bug populations tend to increase with mortality. Wunderlich and Giles (1999) to attract the winged adult male mealy- each new generation. Vigorous vines developed a mechanical technique to bugs. These pheromones can be used to are more likely to be infested than weak safely release eggs in liquid suspen- monitor mealybug populations and den- ones, because mealybug egg production sion; however, adhesion of eggs to the sities. Sex pheromones have been identi- is lower on stressed vines (Daane et al., vineyard canopy was an issue, and fied for the vine (Hinkens et al. 2001), unpublished data). Most infested grape carriers have not yet been developed obscure (Millar et al. 2005), grape (Bruno bunches are those that come in direct that improve “stick” while maintain- et al. 2007) and longtailed (Millar et al., contact with the head or cordons of the ing egg viability. Today, insectaries can unpublished data) mealybugs. Trials vine, because most mealybug species produce lacewing adults, and this may with the vine mealybug found that the find some refuge on the vine trunk for be a more effective stage for release, parasitoid A. pseudococci was also caught oviposition sites. Therefore, remov- especially when combined with an in pheromone- attractant to stimulate the adults to re- baited traps Mealybug pests can be controlled, to some main in the vineyard and deposit eggs (Millar et al. extent, by natural enemies that are often on stalks — where they are not prone to 2002). It was later predation by vineyard ants and spiders. observed that present in sustainable management programs. Most insectaries produce Chrysoperla parasitism levels spp. because the adults are not predatory of vine mealybug were higher in vine- and can be reared on an artificial diet. yards with experimental mating disrup- ing grape bunches in contact with the Other common vineyard species include tion (Walton et al. 2006). Ongoing studies woody portion of the vine will reduce green and brown lacewings, which are are screening the attractiveness of dif- the infestation level. predatory as adults and therefore more ferent parasitoid species to mealybug sex For these reasons, vineyard character- costly to rear. pheromones, to test the hypothesis that istics should be taken into account when Other generalist predators that are some parasitoid species spend more time considering which blocks to transition commercially available for augmenta- searching for mealybugs in vineyards toward more sustainable programs via tion include predaceous mites, minute using a mating disruption program, the enhancement of biological controls. pirate bugs and praying mantis. No thereby increasing parasitism rates. All of these management tools work information on their potential against in concert with biological controls by Role of vineyard characteristics mealybugs is known, and for that rea- lowering mealybug densities or crop son, they are not yet recommended for While we presented information on damage, which can enable the natural mealybug control. biological controls for vineyard mealy- enemies to kill a greater portion of the Parasitoids may be a more effective bugs, other sustainable control tools damaging mealybug population. natural enemy group for augmentative were not highlighted. For example, programs, but there are few studies mealybug infestation levels may de- of their use in California vineyards. pend upon vine growth and fruiting K.M. Daane is Cooperative Extension Special- Experimental release of A. pseudococci characteristics, fruit maturation date ist, and M.L. Cooper is Staff Research Associ- in a San Joaquin Valley raisin vineyard and the type of pruning. Therefore, ate, Department of Environmental Science,

http://CaliforniaAgriculture.ucop.edu • October–December 2008 175 Policy and Management, UC Berkeley; UC Cooperative Extension (UCCE), Kern We thank CDFA for funding this review; and the S.V. Triapitsyn is Principal Museum Scientist, County; W.J. Bentley is Areawide Advisor, UC America Vineyard Foundation, California Table Department of Entomology, UC Riverside; Kearney Agricultural Center; K.E. Godfrey Grape Commission, California Raisin Marketing V.M. Walton is Assistant Professor, Depart- is Research Entomologist, Biological Control Board, Viticulture Consortium, Lodi Winegrape ment of Horticulture, Oregon State University; Program, California Department of Food and Commission (in cooperation with EPA District G.Y. Yokota is Staff Research Associate, Agriculture (CDFA); and L.R. Wunderlich is 9), Central Coast Vineyard Team, UC Statewide Department of Environmental Science, Policy Cooperative Extension Advisor, UCCE El Do- IPM Program, California Department of Pesticide and Management, UC Berkeley; D.R. Haviland rado and Amador counties. Regulation and Western Regional SARE Program is Cooperative Extension Farm Advisor, for funding mealybug research.

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