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Parasitoids of obscure mealybug, Pseudococcusviburni (Hem.: Pseudococcidae) in California:establishment of Pseudaphycus flavidulus (Hym.:Encyrtidae) and discussion of related parasitoid speciesKent M. Daane a; Monica L. Cooper a; Serguei V. Triapitsyn b; John W. AndrewsJr c; Renato Ripa da Department of Environmental Science, Policy and Management, University ofCalifornia, Berkeley, CA, USAb Department of Entomology, University of California, Riverside, CA, USAc College of Natural Resources, University of California, Berkeley, CA, USAd Instituto de Investigaciones Agropecurias, Centro Regional de Investigación, LaCruz, Chile

Online Publication Date: 01 January 2008To cite this Article: Daane, Kent M., Cooper, Monica L., Triapitsyn, Serguei V., Andrews Jr, John W. and Ripa, Renato(2008) 'Parasitoids of obscure mealybug, Pseudococcus viburni (Hem.: Pseudococcidae) in California: establishment ofPseudaphycus flavidulus (Hym.: Encyrtidae) and discussion of related parasitoid species', Biocontrol Science andTechnology, 18:1, 43 - 57To link to this article: DOI: 10.1080/09583150701729906URL: http://dx.doi.org/10.1080/09583150701729906

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Parasitoids of obscure mealybug, Pseudococcus viburni(Hem.: Pseudococcidae) in California: establishment of Pseudaphycus

flavidulus (Hym.: Encyrtidae) and discussion of related parasitoidspecies

Kent M. Daanea*, Monica L. Coopera, Serguei V. Triapitsynb,

John W. Andrews Jrc and Renato Ripad

aDepartment of Environmental Science, Policy and Management, University of California,

Berkeley, CA, USA; bDepartment of Entomology, University of California, Riverside, CA, USA;cCollege of Natural Resources, University of California, Berkeley, CA, USA; dInstituto de

Investigaciones Agropecurias, Centro Regional de Investigacion, La Cruz, Chile

(Received 4 August 2007; returned 5 October 2007)

To improve natural suppression of the obscure mealybug, Pseudococcus viburni

(Signoret), the parasitoids Pseudaphycus flavidulus (Brethes) and Leptomastix

epona (Walker) (Hymenoptera: Encyrtidae) of Chilean origin were released in

California’s Central Coast vineyards from 1997 to 1999. A survey for parasitoids

of P. viburni was conducted in the Edna Valley appellation wine grape region from

2005 to 2007, 6�8 years after classical biological control releases were discon-

tinued. Two survey methods were used. First, field collections of obscure

mealybugs from commercial vineyard blocks (2005�2007) and, second, placement

of ‘‘sentinel mealybugs’’ on potted (1 L) grape vines (2006 only). From both

survey methods, P. flavidulus was recovered, albeit levels of parasitism were low

(less than 0.6%). We also placed longtailed mealybug, Pseudococcus longispinus

(Targioni Tozzetti), on potted plants concurrent with placement of sentinel

obscure mealybugs in the vineyard in order to measure parasitoid activity on this

closely-related mealybug species. No P. flavidulus were recovered from

P. longispinus. Other encyrtid parasitoids reared from either P. viburni or

P. longispinus were Anagyrus pseudococci (Girault), Leptomastix dactylopii

Howard, Leptomastidea abnormis (Girault), Coccidoxenoides perminutus Girault,

and Tetracnemoidea peregrina (Compere). A hyperparasitoid, Chaetocerus sp.,

was also reared. The data are discussed with respect to biological control of

vineyard mealybugs and newly developed controls for the Argentine ant,

Linepithema humile (Mayr) (Hymenoptera: Formicidae). Because Pseudaphycus

species reared from mealybugs are superficially very similar a taxonomic key and

discussion of host relationships for selected Pseudaphycus species are provided.

Keywords: vineyards; Pseudaphycus; Pseudococcus viburni; Pseudococcus

longispinus; Linepithema humile

*Corresponding author. Email: daane@uckac.edu

ISSN 0958-3157 print/ISSN 1360-0478 online

# 2008 Taylor & Francis

DOI: 10.1080/09583150701729906

http://www.informaworld.com

Biocontrol Science and Technology,

Vol. 18, No. 1, 2008, 43�57

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Introduction

Mealybug species in the Pseudococcus ‘‘maritimus-malacearum’’ (Hemiptera: Pseu-

dococcidae) complex include the grape mealybug, Pseudococcus maritimus (Ehr-

horn), obscure mealybug, P. viburni (Signoret), and longtailed mealybug,

P. longispinus (Targioni Tozzetti) (Wilkey and McKenzie 1961). The taxonomic

descriptions of these mealybug species were quite confused until the 1960s, leading to

frequent misidentifications, especially for P. maritimus and P. viburni. Nevertheless,

these mealybug species have distinct biological characteristics that result in different

geographic ranges, host plant preferences, and economic damage to agricultural

crops. Key amongst their differences is the parasitoid species that provide effective

control. Without effective natural enemies present to suppress their populations

these Pseudococcus species have caused economic damage in vineyards and/or pome

fruit orchards in North and South America, Australia, and New Zealand (Ben-Dov

1994). Crop loss occurs when mealybugs infest fruit or excrete honeydew that covers

fruit and leaves and serves as a medium for sooty mold fungi (Charles 1982;

Grasswitz and Burts 1995; Walton and Pringle 2004b). Species of Pseudococcus

Westwood have also been shown to transmit closteroviruses such as grapevine

leafroll (Golino, Sim, Gill and Rowhani 2002; Charles et al. 2006). Here, we describe

efforts to improve the natural enemy complex of P. viburni in California coastal

vineyards where this mealybug is an invasive and damaging pest (Phillips and Sherk

1991). We begin with a brief description that contrasts the parasitoid complex of

P. viburni with those of P. maritimus and P. longispinus in California vineyards.

Pseudococcus maritimus (grape mealybug) was first described by Ehrhorn in 1900

from specimens collected on coastal buckwheat (Eriogonum latifolium J. E. Sm.) in

California, and was then termed the ocean mealybug (Miller, Gill and Williams

1984). This species has long been known to infest vineyards in North America (Essig

1914) where it is considered native (Ben-Dov 1994). Pseudococcus longispinus

(longtailed mealybug) is thought to be native to South America (Ben-Dov 1994).

Although it has been long resident in North America, its pest status in California

vineyards has been limited to cooler regions of the Central Coast. A complex of

natural enemies is often credited with providing effective P. maritimus and

P. longispinus suppression (Smith 1916; Clausen 1924; Flaherty, Phillips, Legner,

Peacock and Bentley 1992). Currently, Acerophagus notativentris (Girault) and

Pseudaphycus angelicus (Howard) (Hymenoptera: Encyrtidae) are the dominant

parasitoid species of P. maritimus in California and Washington vineyards (Grimes

and Cone 1985; Flaherty et al. 1992) and Washington pears (Hill and Burts 1982).

Both parasitoid species also attack P. longispinus. Other encyrtid parasitoid species

reared from these mealybugs include Zarhopalus corvinus (Girault), Anagyrus yuccae

(Coquillet) [�A. subalbicornis (Girault)], Pseudleptomastix squammulata Girault,

and Anagyrus clauseni Timberlake (Noyes and Hayat 1994). Note that it is quite

common for individual parasitoid species to attack both P. maritimus and

P. longispinus.

Pseudococcus viburni (obscure mealybug) is thought to be Australian or South

American in origin. Its history in North America is not clear, due in part to earlier

taxonomic confusion. Prior to 1960, P. maritimus, P. longispinus, P. obscurus Essig,

P. capensis Brain, P. malacearum Ferris, and P. affinis (Maskell) were all synonyms

or misidentifications of P. viburni (Ferris 1918; McKenzie 1967; Miller et al. 1984;

44 K.M. Daane et al.

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Ben-Dov and Matile-Ferrero 1995). In North America, P. viburni is primarily a pest

of ornamental plants (Laflin, Gullan and Parella 2004). However, since proper

taxonomic descriptions were produced, P. viburni has been verified as a pest in pear

and apple orchards and coastal vineyards especially in association with the

Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae) (Phillips

and Sherk 1991; Daane, Sime, Fallon and Cooper 2007). Pre-release surveys of

P. viburni in California’s coastal vineyards, including vineyards used in this study,

found no parasitoid species attacking P. viburni (Daane et al. 1996).

To improve natural suppression of P. viburni, Pseudaphycus flavidulus (Brethes),

and Leptomastix epona (Walker) (Hymenoptera: Encyrtidae) were imported from

insectary colonies maintained at Centro Regional de Investigacion, La Cruz, Chile,

and released in Central Coast vineyards from 1997 to 2000 (USDA APHIS permit

number 32875). The Chilean material of P. flavidulus was originally collected in Chile

and is believed to be South American in origin; the Chilean material of L. epona

originated from a stock culture in England, provided by Dr M.J.W. Copland (Wye

Campus, Imperial College London). At two of the release sites, ant exclusion trials

were concurrently conducted in small five-vine plots and at these sites only

P. flavidulus and L. epona were recovered in 1998 (Daane et al. 2007). In 1999, the

ant exclusion barriers were removed, resulting in an increase in both ant and P.

viburni densities and a return of the annual insecticide applications to control these

pests. Later studies on the impact of novel ant controls on ant and P. viburni

densities, conducted from 2002 to 2004, reported parasitised mealybugs as indicated

by a mummy with a parasitoid emergence hole (Daane et al. 2006b). However, no

parasitoids were reared and it could not be determined if the mummies were of

P. maritimus, P. longispinus, or P. viburni, as all three mealybug species are found in

Central Coast vineyards. Therefore, it was unknown if either P. flavidulus or L. epona

had established in California. Here, we report on post-release surveys, conducted

from 2005 to 2007, which show P. flavidulus has established on P. viburni. We include

information on the initial parasitoid releases that has not yet been published in

detail. We also include a key to the species of the genus Pseudaphycus Clausen that

could potentially be reared from mealybugs found in North American vineyards and

tree fruit orchards.

Materials and methods

Parasitoid release

From June 1997 to December 1999, �194 000 P. flavidulus and �5500 L. epona

were released, spread amongst six Central Coast vineyards, located in the Edna

Valley appellation and California Polytechnic University Farm (San Luis Obispo

County), and Santa Maria appellation (Santa Barbara County) (Table 1). (An

appellation is a geographical-based term used to identify where wine grapes are

grown and has set boundaries.) The Edna Valley appellation release sites were heavily

infested with both obscure mealybug and Argentine ants. The two Santa Maria

appellation sites were infested with both P. viburni and P. longispinus, as well as

Argentine ants.

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Post-release sampling

From 2005 to 2007, vineyard blocks in a portion of the Edna Valley appellation were

surveyed for P. flavidulus and L. epona, reared from P. viburni. Vineyard blocks were

targeted for surveys after vineyard managers reported the presence of mummified

mealybugs; some of these blocks were concurrently being used to test liquid baits for

Argentine ant control (Daane et al. 2006b). The vineyard blocks surveyed were

located southeast of the San Luis Obispo County airport where there are

approximately 650 ha of mostly contiguous wine grapes (Figure 1). The region is

surrounded by residential homes, a golf course, and natural oak-grassland chaparral.

Two types of surveys were conducted: a visual search and collection of mealybugs

and the placement of sentinel mealybugs. Release site 3 in the Edna Valley

appellation is located 11 km southeast from sites 1 and 2, and the California

Polytechnic University Farm is located within the Edna Valley appellation. Both sites

Table 1. Classical biological control release of Pseudaphycus flavidulus and Leptomastix

epona for the obscure mealybug (Pseudococcus viburni) showing release location, numbers, and

schedule.

Release location

Edna Valley

appellation Cal Poly1Santa Maria

appellation

Release date Site 1 Site 2 Site 3 Site 1 Site 1 Site 2 Total per date

(A) Leptomastix epona releases

July 1997 300 300 0 0 0 0 600

Aug 1997 450 450 0 0 0 0 900

June 1998 500 500 0 0 0 0 1000

July 1998 500 500 0 0 0 0 1000

Aug 1998 750 750 0 0 500 0 2000

Total per site 2500 2500 0 0 500 0 5500

(B) Pseudaphycus flavidulus releases

July 1997 200 200 0 0 0 0 400

Aug 1997 400 400 0 0 0 0 800

Sept 1997 1000 1000 0 0 0 0 2000

June 1998 500 500 0 0 0 0 1000

July 1998 1000 1000 0 0 0 0 2000

Aug 1998 4000 4000 0 0 1000 0 9000

Sept 1998 3000 3000 0 0 2000 0 8000

Mar 1999 500 500 0 0 0 0 1000

May 1999 500 500 0 0 0 0 1000

June 1999 4800 0 0 0 0 0 4800

July 1999 3000 0 0 0 0 0 3000

Aug 1999 12 100 12 700 0 0 0 0 24 800

Sept 1999 0 4000 0 0 14 700 0 18 700

Nov 1999 0 0 8000 6500 0 11 500 26 000

Dec 1999 19 000 17 000 10 500 19 500 12 000 10 500 88 500

Total per site 50 000 44 800 18 500 26 000 29 700 22 000 191 000

1California Polytechnic University, San Luis Obispo, Department of Crop Protection, University Farm.

46 K.M. Daane et al.

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received less than 25,000 P. flavidulus and no L. epona over two late-season releases

(Table 1); neither field was sampled as vineyard mangers attempted localised

P. viburni eradication with multiple annual insecticide applications soon after

parasitoid releases were discontinued.

For the visual search and collection, approximately 0.4 ha (500 vines set as 10�20

rows by 25�50 vines) sections of each block were selected for sampling during the

summer and fall when second instar to adult stage P. viburni are present (Daane et al.

2007). We utilised a timed count previously validated to provide information on

mealybug age structure and density, as described by Geiger and Daane (2001).

Approximately 10% of the vines were randomly selected and searched for a 2.5-min

period. Mealybug density was recorded and all live mealybugs between the second

instar to adult stages were collected and categorised by their location on the vine as

either exposed (located on the canes, leaves or fruit) or protected (located under the

bark of the trunk or canes). The collected mealybugs were placed individually in

gelatin capsules when their density on the vine was low or moderate and they could

be easily separated. At higher densities, individuals were not easily separated and

these bulk collections were placed into larger emergence containers. Samples were

taken on 23 June 2005, 15 July 2006, 24 August 2006, 3 and 16 October 2006, and

3 May 2007.

Figure 1. Release sites (k) for Pseudaphycus flavidulus and Leptomastix epona from 1997 to

1999 in a portion of the Edna Valley appellation, as described in Table 1 for ‘‘site 1 and site 2’’,

and recovery sites of P. flavidulus, in this same region, from 2005 to 2007 ( ). The shaded area

is commercial wine grapes, approximately 650 ha.

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For sentinel mealybugs, potted (1 L) grape vines were infested with either

P. viburni or P. longispinus. Each potted vine was inoculated with approximately 100

mealybugs (second and third instars). Five vines with each mealybug species were

placed in the field for a 2-week period in each of two vineyard blocks. After the

exposure period, the potted vines were returned to the laboratory and all mealybugs

were collected and isolated individually in gelatin capsules. The experiment was

conducted on 28 August, 11 September, and 9 October 2006, during the period when

parasitism is typically at its seasonal peak (Daane et al. 2007).

All collected mealybugs were held at room temperature for 4 weeks and then

examined for parasitoid emergence. All adult parasitoids were identified to species

and gender. There were few unemerged mummies, and these were not dissected or

assigned to a specific parasitoid species.

Results and discussion

From the visual search and collection, across all years and vineyard blocks, we

collected 4532 mealybugs (identified as P. viburni), from which 40 adult parasitoids

were reared (Table 2). From individuals isolated in gelatin capsules, 17 P. flavidulus

were reared from four mealybugs. Pseudaphycus flavidulus can be gregarious and

multiple parasitoids from individual P. viburni are common, especially with larger

mealybugs (Karamaouna and Copland 2000). From field-collected P. viburni that

were placed in emergence containers there were 13 P. flavidulus reared (Table 2).

Other parasitoids reared from these field-collections were Anagyrus pseudococci

(Girault), Leptomastix dactylopii Howard, and Leptomastidea abnormis (Girault).

Few parasitoids were collected and no discernable pattern could be determined for

parasitoid species seasonal occurrence, host stage preference, or location on the vine.

From the sentinel plants, we isolated 283 P. viburni from which we reared a single

P. flavidulus female. We also recovered 604 P. longispinus from which we reared 11

adult parasitoids: A. pseudococci, L. dactylopii, L. abnormis, Tetracnemoidea

peregrina (Compere), and Coccidoxenoides perminutus Girault. As with the field

collections, there were so few parasitoids reared that there can be no meaningful

comparison of parasitoid levels or species recovered with respect to the seasonal

period when the sentinel plants were placed in the vineyard (28 August, 11 September

and 9 October 2006).

Results from both survey methods provide evidence that P. flavidulus has

established in California on P. viburni. However, the level of parasitism was quite low.

From mealybugs isolated in gelatin capsules there was only 0.54% parasitism.

Percentage parasitism can not be exactly determined from mealybugs placed in the

emergence containers because the 13 P. flavidulus collected may have emerged from

one to 13 mealybugs. The other parasitoid species reared are either exclusively or

commonly solitary. Therefore, parasitism levels would have ranged from 0.25 to

0.49%. Similar results were obtained from the sentinel plants where there was 0.35%

parasitism of P. viburni and 1.82% parasitism of P. longispinus. Although parasitism

levels are low, P. flavidulus has become established in these blocks and has been able

to expand its range from the initial release sites to other areas of the vineyard where

P. viburni populations are present.

The low level of parasitoid activity for both P. viburni and P. longispinus is probably

due to the presence of the Argentine ant in these vineyard blocks (Daane et al. 2007).

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Ants have long been associated with outbreaks of honeydew-producing homopterans

(Buckley 1987) and the Argentine ant is a particularly aggressive species (Buckley and

Gullan 1991) whose invasion into California vineyards has been implicated in

outbreaks of mealybugs in North Coast and Central Coast appellations (Phillips

and Sherk 1991; Daane et al. 2006b). Some Californiavineyard managers are currently

using liquid baits rather than barrier sprays for Argentine ant control (Cooper et al.,

unpublished data) and we suspect that as ant populations are suppressed, without the

use of organophosphates, parasitism levels of P. viburni and P. longispinus will increase

as was shown in the earlier ant exclusion experiments (Daane et al. 2007). Note that

L. epona was not recovered in our surveys. There is some observational evidence that

L. epona is even less successful in the presence of foraging ants than P. flavidulus

(Daane et al. 2007) due in part to its slower oviposition behaviors.

Of interest is that a number of well-known mealybug parasitoid species were

reared from P. viburni and P. longispinus, which have not previously been reported

from California field-collections. These are A. pseudococci, L. dactylopii, L. abnormis,

and C. perminutus. Data from the visual search and collection provide the first report

of A. pseudococci reared from field-collected P. viburni, although the parasitoid has

often been reported as reared in the laboratory on P. viburni (Berlinger 1977; Islam

Table 2. The number and species of parasitoids reared from obscure mealybug (OMB),

Pseudococcus viburni, collected in Californian Central Coast wine grape (Edna Valley

appellation) vineyards.

Adult parasitoid reared1

Date Block Location No. OMB P.f.

(�)

P.f.

(�)

A.p. L.a. L.d. C.sp. Unk2 Total

23 Jun 05 1 Protected 252 1 0 0 0 0 0 0 1

15 Jul 06 2 Protected 252 5 4 0 0 0 0 0 9

24 Aug 06 3 Exposed 12163 3 0 0 1 1 0 2 7

24 Aug 06 3 Protected 1352 2 1 0 0 0 0 0 3

24 Aug 06 4 Exposed 982 0 0 0 0 0 0 0 0

24 Aug 06 4 Protected 72 0 0 0 0 0 0 0 0

3 Oct 06 3 Exposed 8313 0 0 1 0 0 0 0 1

3 Oct 06 3 Protected 22 0 0 0 0 0 0 0 0

3 Oct 06 4 Exposed 10043 0 0 1 0 0 0 0 1

3 Oct 06 4 Protected 1002 1 0 0 0 0 0 0 1

16 Oct 06 3 Exposed 202 0 0 0 0 0 0 0 0

16 Oct 06 3 Protected 62 0 0 0 0 0 0 0 0

16 Oct 06 4 Exposed 122 1 0 0 0 0 0 0 1

16 Oct 06 4 Protected 32 1 0 0 0 0 0 0 1

3 May 07 5 Exposed 10003 0 10 0 0 0 0 0 10

10 Jun 07 6 Protected 502 1 0 0 0 0 4 0 5

TOTALS 4532 15 15 2 1 1 4 2 40

1Insect codes are: P.f.�Pseudaphycus flavidulus (female), A.p.�Anagyrus pseudococci, L.d.�Leptomas-tix dactylopii, L.a.�Leptomastidea abnormis, C.sp.�Chaetocerus sp. 2All mealybugs were identified as P.viburni and then placed individually in gelatin capsules. 3Includes mealybugs in mass collections that wereplaced in emergence containers. While mealybugs infesting the vine were identified as P. viburni, not allmealybugs on the collected plant material could be clearly seen and be positively identified. We estimatethe ‘‘unknown’’ mealybugs to be B10% of the sample.

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1992) and P. longispinus (Bartlett and Lloyd 1958; Wakgari and Giliomee 2004).

Similarly, L. abnormis is here first reported as being field-collected from P. viburni.

Earlier studies reported this parasitoid was previously reared from the closely related

P. maritimus (Smith and Armitage 1920) and the citrophilus mealybug Pseudococcus

calceolariae (Maskell) (Bartlett and Lloyd 1958). We also reared a single L. dactylopii

from P. viburni. This parasitoid species has been reported reared from P. viburni in

field-collections in South African vineyards (Wakgari and Giliomee 2004; Walton

and Pringle 2004a) and laboratory-based studies of parasitoid biology (Blumberg and

Van Driesche 2001; Chong and Oetting 2007). We must note here that both A.

pseudococci and L. abnormis were collected from the emergence containers and while

we believe all material placed into these containers were P. viburni, both P. longispinus

and Planococcus ficus (Signoret) are present in the Edna Valley appellation. These

mealybug species rather than P. viburni could be the host of A. pseudococci and L.

abnormis reared from the emergence containers. We estimate the maximum likelihood

of either P. longispinus or P. ficus coming from collected material was B1%, noting

that neither species was found in the sampled blocks during the survey period and the

material placed into the containers was identified as P. viburni.

The widest array of parasitoid species was reared from the P. longispinus that

were placed in the field as sentinel mealybugs (Table 3). Anagyrus pseudococci has

been reared from P. longispinus in the laboratory (Bartlett and Lloyd 1958) but is not

considered an important P. longispinus parasitoid in the field. Leptomastix dactylopii

has been reared from field-collected P. longispinus and, in fact, the holotype of one of

its synonyms, Leptomastix bifasciatus (Compere), was reared from a Pseudococcus

Table 3. The number and species of mealybug (MB) parasitoids reared from obscure

mealybug, Pseudococcus viburni, and longtailed mealybug, P. longispinus, placed on potted

grape and exposed to parasitoids in two Californian Central Coast wine grape (Edna Valley

appellation) vineyards on three sample dates in 2006.

Adult parasitoid reared1

Date Block MB species MB collected P.f. A.p. T.p. C.p. L.d. L.a

28 Aug 1 Obscure 24 0 0 0 0 0 0

28 Aug 2 Obscure 37 1 0 0 0 0 0

11 Sep 1 Obscure 59 0 0 0 0 0 0

11 Sep 2 Obscure 71 0 0 0 0 0 0

9 Oct 1 Obscure 70 0 0 0 0 0 0

9 Oct 2 Obscure 22 0 0 0 0 0 0

28 Aug 1 Longtailed 258 0 0 2 0 0 0

28 Aug 2 Longtailed 112 0 1 0 1 0 0

11 Sep 1 Longtailed 23 0 1 0 0 0 0

11 Sep 2 Longtailed 86 0 0 0 0 0 0

9 Oct 1 Longtailed 21 0 0 0 0 0 0

9 Oct 2 Longtailed 104 0 0 0 0 0 0

1Insect codes are: P.f.�Pseudaphycus flavidulus (female), A.p.�Anagyrus pseudococci, T.p.�Tetracne-moidea peregrina, C.p.�Coccidoxenoides perminutus (female), L.d.�Leptomastix dactylopii, L.a.�Leptomastidea abnormis.

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species (Compere 1938). While L. dactylopii has been widely used for biological

control of the citrus mealybug, Planococcus citri (Risso) (Noyes and Hayat 1994)

and in laboratory studies with P. longispinus (e.g. Blumberg and Van Driesche 2001),

this is a first report of its presence on P. longispinus in California vineyards. Similarly,

C. perminutus has been commonly reported as a parasitoid of P. ficus in vineyards

(Wakgari and Giliomee 2004; Walton and Pringle 2004) but this is the first report of

C. perminutus reared from P. longispinus in field collected material that we couldlocate in the literature (Noyes 2003). We also collected T. peregrina, which has long

been reported as both present in California vineyards and as a parasitoid of

P. longispinus (Noyes and Hayat 1994).

We believe the presence of these common mealybug parasitoids (A. pseudococci,

L. dactylopii, L. abnormis, and C. perminutus) results from the recent invasion of the

vine mealybug (P. ficus) in the Central Coast wine grape region as well as other

California vineyard regions. In the 1990s, P. ficus was found in vineyards in Mexico

(Castillo, Hernandez and Daane 2005) and California (Daane et al. 2006a). As part

of biological control efforts against this pest, resident parasitoids of the closely

related P. citri and imported parasitoids of P. ficus were released in vineyards in the

Edna Valley appellation. These included A. pseudococci (resident and material newly

imported from Europe), L. dactylopii, L. abnormis (purchased from Novartis BCM

North America), and C. perminutus (newly imported from South Africa) (Daane

et al., unpublished data). We will continue to closely monitor the geographic

expansion of P. ficus and whether the presence of this damaging Planococcus speciescreates improved biological control for Pseudococcus species or creates more

disruptive conditions as vineyard managers select broad-spectrum insecticides to

reduce its densities and economic damage.

Currently, a second Pseudaphycus species, P. maculipennis Mercet, has been

imported from New Zealand (HortResearch, Auckland, New Zealand) for P. viburni

control and is currently under evaluation in the University of California Berkeley

Quarantine for possible non-target impacts. This Pseudaphycus species has been used

successfully to control P. viburni in New Zealand tree fruit (Charles et al. 2004). We

also expect to find P. angelicus in vineyard and orchard systems where either

P. maritimus or P. longispinus are common.

Similarly, there are a number of less common mealybugs in North America that

could be found in vineyards and tree fruit; these include the citrophilus mealybug,

citrus mealybug, Gill’s mealybug (Ferrisia gilli Gullan), striped mealybug (Ferrisia

virgata (Cockerell)), Comstock mealybug (Pseudococcus comstocki (Kuwana)), pink

hibiscus mealybug (Maconellicoccus hirsutus (Green)), and ground mealybugs(Rhizoecus falcifer Kunckel d’Herculais and R. kondonis Kuwana). Because

Pseudaphycus species reared from mealybugs are superficially very similar, we

provide the following summary of key characteristics to separate Pseudaphycus

species reared from mealybugs found in North American vineyards and tree fruit

orchards. As presently understood the genus Pseudaphycus includes 26 valid species

(Noyes 2003), distributed in Europe, North and South America, the Caribbean, the

Far East, and Africa. Most of the known species are primary parasitoids of

mealybugs. Although there are some references for Pseudaphycus reared from non-

mealybug hosts such as coccids (Hemiptera: Coccidae), these reports are rare and

likely are misidentifications. Several Pseudaphycus species have been used success-

fully in the biological control of serious mealybug pests (Bartlett et al. 1978; Noyes

Biocontrol Science and Technology 51

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and Hayat 1994). According to Rosen (1981), Pseudaphycus differs from most other

members of the encrytid tribe Aphycini in having a five-segmented funicle in the

antennae of both sexes and is most similar to Bothriocraera Timberlake and

Acerophagus Smith, differing from the former only in details of sculpture and

coloration, and from the latter mainly in the narrower frontovertex and bicolorous

antennae with a contrastingly white clava. Earlier reported differences in the palpal

formula among the species of Acerophagus and Pseudaphycus are not reliable to

separate these two genera (S. Triapitsyn, unpublished data). According to Noyes

(1980), Pseudaphycus is also very close to Timberlakia Mercet.

A flaw in the provided key is that it is based on the few published keys and

descriptions by Bennett (1955), De Santis (1964), Gahan (1946), and Rosen (1981).

Unfortunately, Gahan (1946) based his taxonomic work on Pseudaphycus on very

poorly preserved and mounted dry specimens and a few poor, uncleared slides (S.V.

Triapitsyn, personal observation). Thus, the palpal formula is currently known for

just a few of the described species of Pseudaphycus. What is critically needed is a

combined molecular and morphological separation of at least the already described

Pseudaphycus species. Currently, we have well-preserved specimens of P. angelicus,

P. flavidulus, P. maculipennis, and also a Pseudaphycus sp. near meritorious Gahan or

meracus Gahan, which are undergoing molecular separation. Other Pseudaphycus

and Acerophagus species are needed to complete this work but that, however, is

beyond the goals of this communication and will be reported elsewhere.

Key to female Pseudaphycus species, reared or potentially reared from mealybugs

in North American vineyards and tree fruit orchards [for practical reasons, it also

includes the common parasitoid of P. maritimus in California, Acerophagus

notativentris (Girault), which can be confused with the Pseudaphycus spp.]. The

common mealybug host associations of Pseudaphycus spp. are provided in Table 4.

1. Antennal flagellum uniformly orange�yellow or light brown . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acerophagus notativentris (Girault)

Antennal flagellum with a white or pale yellow (at most blackish basally) clava and a

contrastingly darker (brown, dark brown, or black) funicle (Pseudaphycus spp.) . . . . . 2

2. Pedicel of antenna not longer than first two funicular segments combined, first funicular

segment small, transverse, narrower than pedicel; segments 2 to 5 of funicle subquadrate,

subequal, and a little broader than pedicel . . . . . . . . . . . . . . . . . . P. meritorius Gahan

Pedicel of antenna as long as or longer than first three funicular segments combined,

funicular segments from first to last successively increasing in width and all more or less

transverse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

3. Forewing fuscous with more or less distinct paler hyaline or subhyaline transverse streak

beyond apex of stigmal vein; scape obviously a little thickened or broadened . . . . . . . 4

Forewing either uniformly fuscous or subfuscous, without a paler transverse streak, or

almost hyaline; scape usually slightly thickened or cylindrical . . . . . . . . . . . . . . . . . . 9

4. Anterior ocellus at the center of frontovertex; speculum of forewing not interrupted . . 5

Anterior ocellus distinctly above center of frontovertex; speculum of forewing interrupted

a little behind the middle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

5. Mesocutum, axillae, and scutellum bright orange�yellow, with a conspicuous narrow

transverse band of black at anterior margin of mesoscutum, gaster blackish; antennal

scape mostly black except basally, pedicel and funicle uniformly black. . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. websteri Timberlake

52 K.M. Daane et al.

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General color brown, sometimes with a purplish tinge; antennal scape lightly infuscated

on outer surface, pale on inner and dorsal surfaces; pedicel fuscous, funicle black . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. ferrisianae Bennett

6. Mesocutum, axillae, scutellum, and gaster blackish�yellow; lateral borders of mesoscutum

white; posterior ocelli as far from anterior ocellus as from occipital margin; inner eye

orbits parallel for the whole length of frontovortex . . . . . . . . . . P. maculipennis Mercet

Mesocutum, axillae, and scutellum dusky orange; lateral borders of mesoscutum not

white; posterior ocelli a little more distant from anterior ocellus than from occipital

margin; inner eye orbits diverging very slightly below . . . . . . . . . . . . . . . . . . . . . . . 7

7. Reticulation on 3rd gastral tergite distinctly transverse; dorsum of gaster with a distinctive

pattern of black transverse stripes on a white background (anterior stripes separated by

white stripes, posterior stripes united medially by a narrow blackish blotch) . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. debachi Rosen

Reticulation on 3rd gastral tergite rectangular; dorsum of gaster black (black transverse

stripes united medially by a wide blackish blotch) . . . . . . . . . . . . . . . . . . . . . . . . . . 8

8. Frontovertex about two and one-half times as long as broad; head and mesosoma dorsally

rather pale orange�yellow, axillary sutures of metanotum usually not blackish . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. angelicus (Howard)

Frontovertex fully three time as long as broad; head and mesosoma dorsally a deeper

shade of orange�yellow mixed with blackish, and axillary sutures brownish�black . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .P. abstrusus Gahan

9. Middle and hind tibiae with two fuscous or blackish bands . . . . . . . . P. malinus Gahan

Middle and hind tibiae without fuscous or blackish bands . . . . . . . . . . . . . . . . . . . 10

10. Mesoscutum, scutellum, and axillae weakly sculptured, distinctly shining; mesosomal

dorsum dirty yellowish or grayish; scape a little thickened or expanded beneath; ovipositor

exserted one-third length of gaster; speculum of forewing uninterrupted . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. mundus Gahan

Mesoscutum, scutellum, and axillae finely and densely sculptured, dull; dorsum of

mesosoma orange�yellow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

11. Anterior margin of face narrowly dark brown or blackish, forming a dark transverse line

between bases of mandibles; occiput except around margins blackish, anterior part of

pronotum mostly black; suture between pronotum and mesoscutum blackish; tegula pale

at base, blackish apically; gaster dorsally mostly blackish . . . . . . . . . . P. malinus Gahan

Anterior margin of face without dark line between bases of mandibles; head yellow or

bright orange�yellow. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

12. Pedicel almost as long as first four funicular segments combined; clava entirely white . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. meracus Gahan

Pedicel about as long as entire funicle combined; clava blackish basally . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .P. flavidulus (Brethes)

Table 4. Common host associations for Pseudaphycus species present in North American

vineyards and orchards.1

Pseudaphycus spp. Mealybug host Common name

P. abstrusus Gahan Pseudococcus comstocki

(Kuwana)

Comstock mealybug

P. angelicus (Howard) Pseudococcus calceolariae

(Maskell)

Citrophilis mealybug

Pseudococcus longispinus

(Targioni-Tozzetti)

Longtailed mealybug

Pseudococcus maritimus (Ehrhorn) Grape mealybug

Planococcus citri (Risso) Citrus mealybug

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Acknowledgements

The America Vineyard Foundation, California Competitive Grants Program for Enology and

Viticulture, Viticulture Consortium, Central Coast Vineyard Team, and the California Table

Grape Commission funded research on Argentine ant invasions in vineyards. We thank the

Domaine Chandon, Paragon, and Wolff vineyards for use of their land and their vineyard

managers for help with collections; Emily Smith for assistance in the laboratory, field and

insectary; and Robert Zuparko with help identifying specimens.

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P. debachi Rosen Ferrisia virgata (Cockerell) Striped mealybug

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