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Biological Control 42 (2007) 288–299

Survey of brown soft scale Coccus hesperidum L. parasitoidsin southern California citrus

Apostolos Kapranas, J.G. Morse, P. Pacheco, L.D. Forster, R.F. Luck *

Department of Entomology, University of California, Riverside CA 92521, USA

Received 18 December 2006; accepted 22 May 2007Available online 31 May 2007

Abstract

The parasitoid complex of brown soft scale, Coccus hesperidum L., a multivoltine soft scale, was determined in southern Californiacitrus over the period February 2004–March 2006. The survey was conducted by placing brown soft scale-infested yucca leaves in thecanopy of citrus trees and subsequently rearing individually isolated parasitized scales in the laboratory. A total of 14 species parasitizedbrown soft scale in the field, the most abundant ones belonging to the genus Metaphycus Mercet (75%). The most abundant parasitoidspecies was Metaphycus angustifrons Compere (38% parasitism), and this is a new record of establishment for this species in California.Coccophagus species accounted for only 11% parasitism. There were important spatio-temporal differences across the parasitoid complexsurvey locations. We also found that the five most abundant encyrtid parasitoid species showed preferences for scales of different sizes.Our results have implications for biological control of citricola scale, Coccus pseudomagnoliarum (Kuwana), an important pest of citrusin the San Joaquin Valley of central California. Notably, this species is nearly absent in southern California. Brown soft scale is consid-ered to be an alternate host for parasitoids of citricola scale, a univoltine soft scale, at times when the latter species is unavailable forparasitism.� 2007 Elsevier Inc. All rights reserved.

Keywords: Citrus; Coccus hesperidum; Coccus pseudomagnoliarum; Parasitoids; Metaphycus; Biological control

1. Introduction

Brown soft scale, Coccus hesperidum L. (Homoptera:Coccidae), is a cosmopolitan and polyphagous pest speciesthat utilizes some 90 families of host plants (Ben-Dov,1993). Its area of origin is hypothesized to be either theAfro-Ethiopian, Oriental, and/or Austro-Oriental regions(Kozar and Ben-Dov, 1997). It is seldom considered a seri-ous pest, except on ornamental plants used in interiorscapes,greenhouses, gardens, arboretums, zoos, and parks (Quayle,1938; Bodenheimer, 1951; Ben-Dov and Hodgson, 1997).The damage that it causes in such situations is mostlycosmetic and is related to the sooty mold fungi that developon the scale’s honeydew excretions. Occasionally, brownsoft scale has been a serious citrus pest in California and

1049-9644/$ - see front matter � 2007 Elsevier Inc. All rights reserved.

doi:10.1016/j.biocontrol.2007.05.012

* Corresponding author. Fax: +1 951 827 3086.E-mail address: robert.luck@ucr.edu (R.F. Luck).

Texas (Bartlett, 1978), the Middle East and South Africa(Stapley and Gayner, 1969), and Zimbabwe (Hodgson,1970). Economic damage associated with this scale has alsooccurred on mango, Mangifera indica L. (Anacardiaceae), inPakistan (Mahmood and Mohyuddin, 1986) and the CanaryIslands (Perez-Guerra, 1986); on guava, Psidium guajava L.(Myrtaceae), in South Africa (De Villiers and Van den Berg,1987); on lychee, Litchi chinesis Sonn. cv. Brewster (Sapind-aceae) in Australia (Waite, 1986); and on tea, Camellia

sinensis (L.) O. Kuntze (Theaceae), in India (Das and Gang-uli, 1961). In most cases, it is economic only when denseaggregations form as a result of it being tended by ants(Hymenoptera: Formicidae). This relationship between antsand brown soft scale is thought to be mutualistic, in that theants obtain honeydew, a rich carbohydrate resource, fromthe scale while in return, they protect the scale from its nat-ural enemies (predators and parasitoids) (Gullan, 1997).However, in the absence of ants, brown soft scale is

A. Kapranas et al. / Biological Control 42 (2007) 288–299 289

normally under natural control and only achieves pest statuswhen its natural enemies are disrupted by broad-spectrumpesticide use, by dust from nearby roadsides, or after coldwinters (Flint et al., 1991). In California, brown soft scaleis an ovoviviparous, parthenogenetic, and multivoltine spe-cies with as many as seven overlapping generations annuallyin greenhouse crops and three to four overlapping genera-tions annually on outdoor crops; in such cases, all of itsdevelopmental stages are usually found concurrently (Gill,1988).

Brown soft scale is rarely a pest of citrus because it isunder effective natural control (Quayle, 1938; Ebeling,1959; Bartlett, 1978). Ecologically, however, its presenceis likely to be important because it is multivoltine and,thus, can serve as an alternate host for parasitoids thatattack other economically important, univoltine soft scalepests, such as citricola scale, Coccus pseudomagnoliarum

(Kuwana). Many parasitoid species that attack citricolascale in California have also been recovered from brownsoft scale, e.g., Coccophagus lycimnia (Walker) and C. semi-

circularis (Forster) (Hymenoptera: Aphelinidae), andMetaphycus helvolus (Compere), M. luteolus (Timberlake),and M. stanleyi (Compere) (Hymenoptera: Encyrtidae)(Bernal et al., 1998, 2001). Whereas brown soft scale isnot an important citrus pest in the absence of ants, its pres-ence or absence in citrus or adjacent vegetation may pro-vide a reservoir for the parasitoids exerting biologicalcontrol on citricola scale.

In contrast to brown soft scale, its congener, citricolascale, is an important pest of citrus and ornamental treesin the San Joaquin Valley of central California where70% of the state’s citrus currently is grown (Grafton-Car-dwell, 2002, 2003; Grafton-Cardwell and O’Connell,2006). Interestingly, it is effectively controlled by naturalenemies in southern California where it was once a seriouspest (Quayle, 1938). Its decrease in southern California wascoincident with the introduction of several parasitoidsreleased for control of black scale, Saissetia oleae (Olivier)(Hemiptera: Coccidae) in the 1930s. These species alsoattacked citricola scale (Bartlett, 1953, 1978) but the speciesmost responsible for its control remains unknown. Citrico-la scale’s reemergence as a pest in San Joaquin Valley citruscoincides with a decline in broad-spectrum insecticide usefor the suppression of three citrus pests: citrus thrips, Scirt-

othrips citri (Moulton) (Thysanoptera: Thripidae) (Imma-raju et al., 1989), and two armored scales, California redscale, Aonidiella aurantii (Maskell), and yellow scale,A. citrina (Coquillet) (Hemiptera: Diaspididae) (Grafton-Cardwell and Vehrs, 1995), which evolved resistance tothese broad-spectrum materials. Prior use of these pesticidessuppressed citricola scale coincidentally. More recently,experiments have shown that augmentative biologicalcontrol of citricola scale with parasitoids is a potentialsolution to its current re-emergence as a pest in California’sSan Joaquin Valley, if such releases can be shown to beeconomic (Bernal et al., 1999, 2001; Schweizer et al., 2002;Schweizer et al., 2003).

A determination of brown soft scale parasitoids insouthern California could improve biological control ofcitricola scale in the San Joaquin Valley because it wouldallow us to identify a set of candidate parasitoid speciesthat probably exploit both scale species and, most impor-tantly, likely regulate citricola scale populations in south-ern California. This in turn will point to one or moreparasitoid species that can be mass reared in brown softscale and later tested for augmentative releases to controlcitricola scale in the San Joaquin Valley. It is also impor-tant to elucidate whether brown soft scale size influencesparasitoid preference because it has been shown that differ-ent parasitoid species exploit different sizes/developmentalstages of citricola scale more effectively than others (Bernalet al., 1999, 2001). Therefore, knowledge of host-size pref-erence by the different parasitoids in southern Californiacan have important implications for implementing aug-mentative biological control against citricola scale in theSan Joaquin Valley (Schweizer et al., 2003).

Thus, this study has three objectives: (i) to determine theparasitoid complex associated with brown soft scale insouthern California, (ii) to evaluate whether this complexshows seasonal or temporal patterns in the use of brownsoft scale, and (iii) to assess host-size dependent parasitismof brown soft by members of the parasitoid species com-plex using this scale as a host.

2. Materials and methods

2.1. Survey of parasitoids in the field

A survey of the parasitoid species exploiting brown softscale in southern California citrus groves was conductedfrom February 2004 to March 2006 using excised leavesof Yucca recurvifolia Salisbury (Agavaceae) infested withbrown soft scale. We maintained a culture of brown softscale on excised yucca leaves hydroponically at the UCR(University of California, Riverside, CA) insectary. Theplants from which the leaves were taken for this culturewere grown in a small field plot at Agricultural Operations,UCR.

Eleven citrus groves distributed in inland southern Cali-fornia were chosen as locations to assess the parasitoid spe-cies exploiting brown soft scale (Riverside, San Bernardino,and San Diego counties) (Fig. 1). Surveys of brown softscale parasitoids in the San Diego area occurred only duringthe second year of our study. At each grove, we chose threecitrus trees distributed through each grove and used thesesample sites continuously from February 2004 to March2006. Our sample unit in each grove consisted of an excisedyucca leaf with 200–300, 20–28 day old scales obtained fromour hydroponic rearing system. The leaf was inserted into a5 · 8.5 cm plastic vial filled three-quarters full with waterand the leaf and vial opening were wrapped tightly with a3 cm wide strip of Parafilm� (Structure Probe, Inc., WestChester, PA) to secure the leaf in the vial. The wrapping alsoretarded the evaporation of water from the vial. Each leaf

Kapranas et al. Brown soft scale parasitoid survey

Riverside Co.

San Bernardino Co.

San Diego

Los Angeles

100 miles

1a, b, c, d, e

2a, b

3a, b

4a, b

San Diego Co.

Fig. 1. Locations of the eleven inland southern California citrus sample groves used to survey the soft scale parasitoid complex present in inland southernCalifornia: 1a–d = Riverside, Riverside County; 2a and b = San Bernardino County; 3a and b = Hemet, Riverside County; and 4a and b = San Diego,County.

290 A. Kapranas et al. / Biological Control 42 (2007) 288–299

was replaced at the sampling sites every 2 weeks. The unithosting the leaf was located under the canopy on the northside of each of the three sample trees (sample site). An insec-ticidal tape (14% chlorpyrifos, Suscon Ribbon Insecticide�,Crop Care Australasia Pty., Ltd.) was strapped halfway tothe unit bearing each leaf to prevent access by ants. Weexcluded ants because citricola scale is not tended by ants,especially the argentine ant, Linepithema humile (Mayr)(Formicidae; Hymenoptera) contrary to brown soft scale,and thus our survey results would be more realistic in lightof the purpose of our study (Ewart and Metcalf, 1956)(see also Section 4 below). Climatic information wasobtained during our sampling period from four weather sta-tions, representative of the areas of survey (source: UCStatewide IPM Project, Davis, CA; http://www.ipm.ucda-vis.edu/WEATHER/wxretrieve.html). Generally during2005, monthly mean temperatures were higher than thoseduring 2004, especially during fall and early spring(Fig. 2). Also, more precipitation was observed on averagein 2004 relative to that in 2005 (52.31 vs. 29.48 cm over eachyear, respectively).

Each scale-infested yucca leaf was placed in a 7.5 cmdiam by 45.5 cm long clear plastic mailing tube (S&W Plas-tics Inc., Riverside, CA), which was capped on each end,during transportation to field sites and also during ‘‘batchrearing’’ of parasitoids. Upon returning to the laboratoryat UCR, each leaf was inspected for foraging adult wasps,which were removed with an aspirator and killed. We theninspected the leaf for the presence of recognizably parasit-

ized scales (i.e. after parasitoids had reached the pupalstage, resulting in a ‘‘mummified’’ scale). Scale mummieswere removed from the leaf with a fine paint brush andwere placed individually in a 3.0 · 0.8 mm glass vial provi-sioned with a streak of honey on its inside wall and the vialwas stoppered with a cotton plug. The leaf was then iso-lated in its mailing tube and was hung from a wire strungalong a laboratory bench between inspections. Each sam-ple leaf was re-inspected for parasitized scales two to threetimes during the subsequent 15 days. The period betweeninspections allowed the young, immature parasitoids todevelop within the parasitized scales to a stage easily recog-nized visually (= a mummy). We only collected mummiedscales from the yucca leaves within 15 days of their arrivalin the laboratory to eliminate scales potentially parasitizedduring the laboratory rearings. In addition, we collected‘‘batch-reared’’ parasitoids that emerged after the 15-dayinspection period, in case a rare species was not recoveredin the rearing of the isolated parasitized scale specimens.These batch-reared specimens were collected for 50 daysafter the yucca leaves had arrived in the laboratory. Theywere placed in a screw top vial containing 95% alcoholfor cold storage and future identification. The room inwhich the immature parasitoids were reared was main-tained at �25–28 �C (subject to occasional fluctuationsof ± 4 �C) with a photoperiod dictated by the light enteringthe rearing room through the laboratory windows.

We inspected the vials with the developing parasitoidsevery 1–2 days for parasitoid emergence. The emerged

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Fig. 2. Mean monthly (a) temperatures and (b) precipitation from foursouthern California climate stations near the four clusters of sampledcitrus groves: San Bernardino (CIMIS #44, University of California,Riverside, UCR); Riverside (NCDC #7473, UCR Citrus ExperimentStation); San Diego (CIMIS #62, Temecula); and Hemet (Touchtone #25,Hemet) obtained from http://www.ipm.ucdavis.edu/WEATHER/wxretrieve.html.

A. Kapranas et al. / Biological Control 42 (2007) 288–299 291

adult wasps were then killed by placing the vial containingthem in a freezer and, when dead, the group of wasps (=brood) into a screw top vial containing 95% alcohol forcold storage was transferred and subsequent processing.The species and sex of each wasp comprising the broodwas identified and recorded along with the host scale’slength and width to the nearest 0.01 mm. An ocularmicrometer mounted in the eyepiece of a dissecting micro-scope was used to measure scale size.

2.2. Specimen identification

Identification of specimens to genus level was based onkeys of Prinsloo (1997), whereas identification to the spe-cies level was based on keys provided as follows: Metaphy-

cus spp. (Annecke and Mynhardt, 1971, 1972, 1981) andCoccophagus spp. (Compere, 1931). We also comparedthe emerged parasitoids with specimens from the Entomol-ogy Research Museum at UCR. However, we were unableto distinguish Metaphycus angustifrons (Compere) malesfrom those of M. stanleyi. If females of a single speciesemerged from an isolated scale along with males ofM. angustifrons/stanleyi, then the males were assumed tobe conspecific with the female(s) that were present. Thus,

the remaining problem was to assign males to species whenthey developed solitarily within a scale. We labeled thesesolitary specimens as Metaphycus sp. males. It was onlyduring the end of the second year of our survey (April2005) that we developed the ability to identify the solitarymales based on the color of the mummified scales fromwhich they emerged. M. angustifrons males emerged fromscales with a more yellow-golden color than those fromwhich M. stanleyi emerged. Thus, after April 2005, scaleswith solitary males of either species lacking females weredetermined to be M. angustifrons or M. stanleyi based onthe mummified scale color if they could be determined withrelative certainty. If not, they were designated as Metaphy-

cus sp.

2.3. Statistical analyses

Contingency tables were used to test the hypothesis thateach encyrtid species develops in a different range of hostsizes (Sokal and Rohlf, 1995). The same analysis was usedto assess whether male versus female Coccophagus speciesemerged from different scale sizes. For this analysis, wetreated host size as a categorical parameter and created10 host-size classes. We calculated the elliptical surface areaof each parasitized scale as an index of host size using thewidth and length of each host scale (mm2) [(p · width ·length)/4] as an index for host size because it explainedmore of the variation in the emerging brood size thanlength or width only (Kapranas, 2006).

3. Results

3.1. Parasitoid species complex

Overall, 921 soft scale-infested yucca leaves weredeployed at the 11 citrus groves throughout inland south-ern California, and leaves with host scale were continu-ously available to the resident soft scale parasitoidsduring our 2-year survey. The survey yielded 30,326 para-sitoid specimens, 5861 of which were reared as broods ofone or more parasitoids per scale from 2758 individuallyisolated scales. The remaining 24,465 specimens werereared from the leaves isolated in the mailing tubes(batch-reared specimens). All of the parasitoids we col-lected were brown soft scale parasitoids because no otherscale species occurred on the yucca leaves we placed inthe field.

Fourteen parasitoid species were reared from the scaleswe isolated (Table 1) and all 14 were also recovered fromthe scales that we batch-reared. The most abundant para-sitoid species were Metaphycus spp. accounting for 75%of the emerging parasitoids (Fig. 3). This complex com-prised M. angustifrons (38% of 2758 isolated parasitizedscales) followed by M. luteolus (18%), M. stanleyi (13%),and M. helvolus (6%). We also recovered four Coccophagusspp. (11%) consisting of C. cowperi (Girault), C. lycimnia

(Walker), C. rusti (Compere), and C. semicircularis

Table 1Parasitoids known to attack Coccus hesperidum and C. pseudomagnoliarum infesting citrus in California

Species Habit Referencesa Recovery in this study Known occurrence in Citricola scalec

SJV So. Cal.

EncyrtidaeDiversinervus elegans (Silvestri) PP 4 Yes (2%) � �Encyrtus lecaniorum (Mayr) PP 3, 11 Yes (1%) + �Metaphycus alberti (Howard) 8, 11 No + +M. angustifrons (Compere) PP 2 Yes (38%) � �M. helvolus (Compere) PP 3, 8, 9, 11 Yes (6%) + +M. luteolus (Timberlake) PP 5, 11 Yes (18%) + +M. stanleyi (Compere) PP 3, 8, 11 Yes (13%) + +Microterys nietneri (Motschulsky) (= flavus) PP 3, 8, 11 Yes (7%) + +

AphelinidaeCoccophagous ceroplastae (Howard) ALP 7 No � �C. cowperi (Girault) FAP 7, 8 Yesb + �C. eritreansis (Compere) FAP 7 No � +C. lycimnia (Walker) FAP 7 Yesb + +C. pulvinariae (Walker) FAP 3, 8 No � �C. rusti (Compere) FAP 3, 7 Yesb � +C. semicircularis (Forster) (= scutellaris) OAP 7, 8 Yesb + +Marietta mexicana (Howard) HP 1, 10, 6 Yes (1%) + �

SigniphoridaeChartocerus sp. HP 12 Yes (0.5%) � �

EulophidaeAprostocetus minutus (Howard) HP 12 Yes (0.5%) + �

Notes: Habit: PP, primary parasitoid; ALP, alloparasitoid; FAP, facultative autoparasitoid; OAP, obligate autoparasitoid; HP, hyperparasitoid. SeeWalter (1983a) for definitions of ALP, FAP, and OAP.

a References regarding the biology of these parasitoids are 1, Smith and Compere (1928); 2, Compere (1957); 3, Annecke (1964); 4, Bartlett and Medved(1966); 5, Saakyan-Baranova (1966); 6, Yanosh (1980); 7, Walter (1983a); 8, Prinsloo, (1984); 9, Lampson et al. (1996); 10, Hayat (1997); 11, Prinsloo(1997); and 12, Viggiani (1997).

b Absolute abundance for each species of Coccophagus was not determined because identification to the species level took place after the survey wascomplete.

c After Timberlake (1913), Compere (1924), Flanders (1942b), Bartlett (1953), and Bernal et al. (2001).

292 A. Kapranas et al. / Biological Control 42 (2007) 288–299

(Forster). Lastly, we recovered the encyrtid, Microterys

nietneri (Motschulsky) (7%). Four rare parasitoid speciesalso appeared in both individually parasitized scale andbatch rearings and consisted of Diversinervus elegans

(Silvestri), Encyrtus lecaniorum (Mayr), Marietta mexicana

(Howard), Chartocerus sp., and Aprostocetus minutus

(Howard). Collectively these four species accounted for only7% of the parasitoids emerging from the isolated scales.

3.2. Regional and seasonal dynamics of the parasitoid

complex on brown soft scale

Parasitoid recovery from the scale-infested yucca leavesbegan in March each year of our 2-year survey with peakemergence occurring during the summer months and thenleveling off as fall progressed (Fig. 4). However, the onsetand termination of parasitoid recovery occurred earlier inthe first year (2004) than during the second year (2005).Also, the species complex differed quantitatively over thetwo years. A greater fraction of parasitoids that emergedfrom isolated scales in the first year were M. angustifrons

(29% vs. 44%) (Fig. 3a and b); more M. nietneri (2% vs.11%) emerged from isolated scales during the second(2005) than the first year; and more M. luteolus (27% vs.10%) and M. stanleyi (17% vs. 10%) emerged the first

(2004) than the second year (Fig. 3a and b). Eighty-ninescales yielded only male M. angustifrons/ M. stanleyi inthe first year (= Metaphycus sp.), whereas 106 isolatedscales yielded only males the second year. Based onmummy color, 58, 15, and 33 were categorized as scalesparasitized by M. angustifrons, M. stanleyi, and Metaphy-

cus sp., respectively, during the second year of the survey.We also noted that the parasitoid complex exhibited a

regional pattern among the four southern Californiaregions we sampled (Fig. 5). Metaphycus luteolus was thedominant parasitoid (63.7% parasitism) in the Hemet area,a more interior area (see Fig. 1) whereas M. angustifrons

was less abundant (2.9% parasitism) in this region relativeto the other three regions. Also, more scales were parasit-ized by Coccophagus species in the Riverside area (19.1%parasitism) than in the other three areas. Finally most ofthe scales parasitized by M. nietneri were recovered fromthe San Diego area (9.7% parasitism) (Fig. 5). We alsonoted a difference in parasitoid phenology among the fourregions. Metaphycus angustifrons was present throughoutthe period when the parasitoids were active. In contrast,M. helvolus was recovered mostly during the early springand the late fall-winter seasons (Fig. 5), i.e. during thecooler months of the year. Microterys nietneri occurredonly during the summer months of the year.

Fig. 3. Percent parasitism of brown soft scale by seven parasitoid species at eleven citrus groves scattered though inland southern California. (a) For 2004,and (b) for 2005. Data shown are from individual parasitized scales only. Hosts parasitized by Metaphycus sp. are those from which a single male ofM. angustifrons or M. stanleyi emerged (see the text for further explanation).

A. Kapranas et al. / Biological Control 42 (2007) 288–299 293

3.3. Brown soft scale size and parasitism by different species

The five most abundant encyrtid species utilized differ-ent sizes and/or stages of brown soft scale on the infestedyucca leaves (Fig. 6) (G = 624, df = 32, p < 0.001). Eachspecies emerged from a different size range of scales (M.helvolus vs. M. luteolus: G = 122, df = 7, p < 0.001 [thetenth size class was excluded because only one scale of this

size was parasitized by M. stanleyi]; M. luteolus vs.M. angustifrons: G = 50.9, df = 8, p < 0.001; M. angusti-

frons vs. M. stanleyi: G = 19.9, df = 8, p < 0.05; M. stanleyi

vs. M. nietneri: G = 19.9, df = 8, p < 0.05). Metaphycus

helvolus developed predominantly in small scales,M. luteolus and M. angustifrons developed mostly inmedium sized scales, and M. stanleyi and M. nietneri devel-oped in progressively larger hosts (Fig. 6).

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Fig. 4. The cumulative monthly abundance of soft scale parasitoids recovered from a survey of eleven inland southern California citrus groves usingbrown soft scale-infested yucca leaves during 2004 and 2005 (data combined from individual and batch-reared scales).

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Fig. 5. Spatio-temporal dynamics of the parasitoid complex of brown soft scale-infested yucca leaves in southern California. Stacked bars represent datafrom individually isolated parasitized scales during 2004–2005 at (a) Riverside, (b) San Bernardino Co., (c) Hemet, and (d) San Diego Co. (2005 only)citrus groves.

294 A. Kapranas et al. / Biological Control 42 (2007) 288–299

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Fig. 6. The size distribution of brown soft scales parasitized byMetaphycus helvolus, n = 153; M. luteolus, n = 483; M. angustifrons,

n = 1054; M. stanleyi, n = 349; and Microterys nietneri, n = 20; at eleveninland southern California citrus groves during 2004–2005 combined.Each species utilized a significantly different range of brown soft scale sizesas a host (G = 624, df = 32, p < 0.001).

A. Kapranas et al. / Biological Control 42 (2007) 288–299 295

Coccophagus spp. parasitoids were recovered mostlyfrom hosts that ranged in size from 1.0 to 7.0 mm2. How-ever, the size distribution of hosts yielding only female Coc-

cophagus differed from those yielding only maleCoccophagus (G = 56.72, df = 7, p < 0.001 [the first and lastsize classes were excluded from analysis as no Coccophagus

emerged from them]) (Fig. 7a). Also, Coccophagus sexratios followed the same trend in both years of the survey,being extremely female biased in the early in spring andduring the fall, but male biased during the summer(Fig. 7b).

4. Discussion

4.1. Parasitoids of brown soft scale in southern California

Metaphycus species dominated the parasitoid complexexploiting brown soft scale in southern California. Thesespecies are all facultatively gregarious endoparasitoids ofsoft scales. Most of them are exotic (all except M. luteolus)and were imported into California as part of a multiyearbiological control effort targeting several soft scale pests(Bartlett 1978). M. angustifrons was the most abundantbrown soft scale parasitoid in our survey. It was introducedfrom Taiwan into California in 1952 and again in 1954 andwas released repeatedly in California during this periodfrom insectary rearings using brown soft scale as a host(Compere, 1957). Records show that this parasitoid wasintroduced specifically for the control of black scale, Sai-

ssetia oleae Olivier (Hemiptera: Coccidae), but it has notestablished on black scale in California (Bartlett, 1978;Lampson and Morse, 1992). Moreover, no records existdocumenting its establishment on other soft scale speciesduring this period, including brown soft scale. Thus, ourrecoveries of this species are the first recorded for Califor-nia. The fact that it is so abundant and yet has gone unre-corded is surprising, especially given that it was rearedinitially on brown soft scale in the UCR insectary beforebeing released in California. M. angustifrons was also intro-duced into Texas from California for biological control ofbrown soft scale (Dean and Bailey, 1960), but its impact onbrown soft scale in that state has not been evaluated. Itsbiology has not been studied in detail but it is a faculta-tively gregarious species that develops in a range of scalesizes, and can occur as very large broods per host relativeto those of other encyrtid parasitoids. As many as 14 indi-viduals of this species emerged from a single host in ourstudy (Kapranas, 2006).

Metaphycus helvolus is endemic to South Africa, wasimported into California in 1937 for control of black scaleand has been recovered from this species (Flanders, 1942a;Lampson and Morse, 1992). Subsequently, it was intro-duced into other countries for black scale control (Guerri-eri and Noyes, 2000). Metaphycus helvolus attacks mostlysecond instar (small) black scales (Lampson et al., 1996;Weppler et al., 2003). Details of its biology are given byBartlett (1978) and Lampson et al. (1996). In our survey,we recovered M. helvolus mostly during the cooler monthsof the year and from very small brown soft scales in whichit developed as a solitary parasitoid. However, it also devel-

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Fig. 7. (a) Size distribution of soft scale yielding only female or male Coccophagus species and (b) cumulative monthly sex ratios for Coccophagus speciesemerging from brown soft scale during 2004–2005.

296 A. Kapranas et al. / Biological Control 42 (2007) 288–299

oped gregariously in a few larger brown soft scales in ouryucca leaf outplants. Its occurrence on brown soft scalecan likely be explained by the lower encapsulation ratesoccurring in the smaller hosts especially when temperaturesare cool (Blumberg, 1997). Metaphycus helvolus occuredinfrequently in our survey suggesting that its impact onbrown soft scale is limited. When we reared isolated scalesin the laboratory yielding M. helvolus adults, we repeatedlyobserved that many of the scales on the same yucca leafhad only encapsulated eggs, with an absence of developingparasitoids. It is likely these encapsulated eggs were M.

helvolus eggs because we only obtained M. helvolus fromthese isolated scales.

Metaphycus luteolus is native to California (Timber-lake, 1913) and attacks soft scales in the genera Coccus,Lecanium, and Saissetia (Hemiptera: Coccidae) (Bartlett,1978). It is a solitary parasitoid of small scales and a fac-ultatively gregarious parasitoid in larger scales. Detailson its biology are given by Saakyan-Baranova (1966)and Bartlett (1978). Timberlake (1913), Flanders

(1942b), Bartlett and Ball (1964), and Bartlett (1978)all claim that M. luteolus is the most important parasit-oid of brown soft scale in California citrus although oursurveys suggest that its role as a natural enemy of brownsoft scale has been overestimated, at least in southernCalifornia.

Metaphycus stanleyi was imported from South Africafor release against black scale in 1937 (Bartlett, 1978;Lampson and Morse, 1992; Bernal et al., 1998). This para-sitoid was recovered from larger scales than M. helvolus,M. luteolus, or M. angustifrons (Fig. 7). This finding is con-sistent with previous studies (Bernal et al., 1999, 2001). Incontrast to the other Metaphycus species in this study, M.

stanleyi does not host-feed (Flanders, 1953; Bernal et al.,1998).

Microterys nietneri is native either to Southeast Asia andwas accidentally introduced into California or it wasimported from Pakistan in the 1950s (Bartlett andLagace, 1961). This species occurs (or apparently occurs)as two races (Bartlett and Lagace, 1961). It is not

A. Kapranas et al. / Biological Control 42 (2007) 288–299 297

known which race parasitizes brown soft scale in southernCalifornia because both races are reported to be equallysuccessful in parasitizing this species (Bartlett and Lagace,1961).

Microterys nietneri has been recorded as parasitizingsoft scales belonging to 11 genera (Prinsloo, 1997) andattacks larger scales than the Metaphycus species (Fig. 6).Bartlett and Ball (1964) reported that its larvae are at a dis-advantage when competing with M. luteolus larvae, when-ever they share the same host. To what degree this can begeneralized to the other Metaphycus species remains to bedetermined. However, this observation, when coupled withthe fact that M. nietneri attacked larger scales than theMetaphycus species in our samples, probably explains itslow abundance. It is an intrinsically inferior parasitoid rel-ative to Metaphycus spp.

The Coccophagus species we recovered are facultative orobligate, heteronomous hyperparasitoids of coccids,including brown soft, citricola, and black scales (Annecke,1964; Walter, 1983a,b; Bernal et al., 2001). FemaleCoccophagus are endoparasitoids of soft scales, whereasmales are secondary ectoparasitoids on conspecific orheterospecific female parasitoids. Additional details oftheir biology are given by Prinsloo (1984), Walter(1983a,b), and Muegge and Lambdin (1989a,b). Duringour survey, we observed one to several Coccophagus spp.males emerging from a scale along with males of eitherM. helvolus, M. luteolus, M. angustifrons, or M. stanleyi,suggesting that the Coccophagus males are indeedhyperparasitic on the Metaphycus species attacking brownsoft scale.

4.2. Spatio-temporal dynamics of the parasitoid complex

Our survey suggests that important differencesoccurred in the seasonal and spatial parasitism ratesamong the various parasitoid species exploiting brownsoft scale. Parasitoid species composition appeared tomirror temperature and precipitation patterns which dif-fered during the two years of our survey. These differ-ences were manifested as a difference in the onset ofparasitism over the two years. Microterys nietneri, whichdevelops in larger hosts than Metaphycus species,increased five-fold in abundance during the second yearfollowing a cooler, moister first year. The colder tem-peratures that prevailed during the first year of our sur-vey likely caused the scales to grow larger, as wasobserved with California red scale, Aonidiella aurantii

Maskell, Hemiptera: Diaspididae (Yu and Luck, 1988).However, this hypothesis requires experimental confir-mation. Furthermore, temperature patterns are poten-tially important in host–parasitoid interactions becausethey affect rates of parasitoid egg encapsulation (Blum-berg, 1997). Thus, individual species abundance at eachof the sample locations may mirror such complicatedhost–parasitoid interactions via variation in abioticfactors.

4.3. Parasitoids in southern California vs. the San Joaquin

Valley—Implications for biological control of soft scales

Citricola and brown soft scale are the only two citrus-inhabiting Coccus species in California (Gill, 1988). Withthe recent reduction in organophosphate and carbamatepesticide use in San Joaquin Valley citrus, citricola scalehas re-emerged as a primary pest, whereas it remainsrare or absent in southern California citrus (Schweizeret al., 2002, 2003; Grafton-Cardwell and O’Connell,2006). Some of the parasitoid species utilizing brown softscale in southern California are also part of a parasitoidcomplex that can exploit citricola scale, at least in theSan Joaquin Valley (Bernal et al., 2001). However, oursurvey showed that significant differences exist betweenthe parasitoid complexes attacking brown soft scale inthe two citrus regions. The most significant of these dif-ferences is the presence of M. angustifrons in southernCalifornia, where it is the most abundant parasitoidattacking brown soft scale. A recent survey of brownsoft and citricola scale parasitoids in the San JoaquinValley failed to detect this species (Bernal et al., 2001).Nor was it recovered recently from ant-tended brownsoft scale during a limited survey in southern California(Bernal et al., 1998) or from brown soft scale-infestedyucca leaves set out in a San Joaquin Valley citrus grove(A.K., unpublished data). Thus, understanding the basisfor these differences between regions may explain whycitricola scale is not under effective biological control inthe San Joaquin Valley.

Another interesting result from our survey was theidentity of the complex currently extant on the soft scalesutilizing citrus. In the early 1950s, the complex parasitiz-ing citricola scale in southern California consisted mostlyof M. luteolus, M. helvolus, M. stanleyi, and C. semicirc-

ularis (Bartlett, 1953). At that time, citricola scale wasstill detectable in southern California’s citrus groves(Bartlett, 1953). However, it has not been detected dur-ing the past 20 years in this region (R.F.L., personalobservation). Whether M. angustifrons can be creditedwith suppressing this scale to extremely low levels insouthern California is uncertain. Bartlett (1978) reportedthis parasitoid as attacking citricola scale in the labora-tory and Kapranas (personal observation) recentlyobserved that it recognized citricola scale in the labora-tory and host-fed on it, particularly when the scale wasvery small. It remains unclear whether M. angustifrons

can develop successfully in citricola scale.A second influence on the parasitoid complex exploiting

brown soft scale and other coccid species in southern Cal-ifornia citrus is the presence of ants. As argued by Staufferand Rose (1997), the presence of ants, especially Argentineants (Hymenoptera: Formicidae), may decrease the efficacyof the parasitoid fauna. In California (Flanders, 1945) andIsrael (Rosen, 1967), Metaphycus flavus (Howard), M. lute-

olus, and M. nietneri tend to be displaced by C. lycimnia

and C. scutellaris (Dalman) in ant-tended, brown soft scale

298 A. Kapranas et al. / Biological Control 42 (2007) 288–299

infestations (Flanders, 1945; Rosen, 1967). Coccophagus

spp. have shorter handling times than Metaphycus or Mic-

roterys spp. when parasitizing a soft scale; thus, Coccopha-

gus spp. may exploit such patches because they are lessfrequently disturbed by ants (Bartlett, 1961). That Coc-

cophagus spp. parasitized >99% of the ant-tended brownsoft scales collected by Bernal et al. (2001) in the San Joa-quin Valley, supports this hypothesis. We did not assessthis in our parasitoid survey because we used individualyucca leaves in units that excluded ants.

Coccophagus species appear to be ecologically importantin the biological control of soft scales. Hyperparasitism ofMetaphycus species, manifested as an increase in male Coc-

cophagus later in the season, was suggested as a reason forthe unsatisfactory biological control of citricola scale inSan Joaquin Valley citrus groves (Bernal et al., 2001). How-ever, this contrasted with a similar increase in Coccophagus

males later in the season in our survey (Fig. 7b) without aconcurrent reduction in parasitism by Metaphycus spp.

Our survey of the parasitoid species attacking brownsoft scale in southern California leads us to conclude thatthey are likely to be responsible for suppressing citricolascale at extremely low densities in this region. Our resultsalso suggest that some of these parasitoids can be releasedagainst citricola scale in the San Joaquin Valley, eitherinoculatively or augmentatively by mass rearing them usingbrown soft scale as an insectary host.

Acknowledgments

We thank J. Barcinas, D. Holcomb, and A. Washburnfor grove access; Dr. J.G. Millar and A. Tena for criticalreview of the manuscript; and Drs. E. Guerrieri (Istitutoper la Protezione delle Piante, CNR, Portici Napoli, Italy),and J.M. Heraty and S. Triapitsyn (University of Califor-nia, Riverside) for providing taxonomic advice. This studywas supported in part by grants from the California CitrusResearch Board (CRB 5500-159) and USDA National Re-search Initiative (USDA-NRI 2005-01006). A.K. alsoacknowledges support provided by the Van den BoschScholarship in Biological Control from the Center for Bio-logical Control at the University of California, Berkeley.

References

Annecke, D.P., 1964. The encyrtid and aphelinid parasites (Hymenoptera:Chalcidoidea) of soft brown scale, Coccus hesperidium Linnaeus(Hemiptera: Coccidae) in South Africa. Entomol. Mem. Rep. S. Afr.Dep. Agric. Tech. Serv. 7, 1–74.

Annecke, D.P., Mynhardt, M.J., 1971. The species of the zebratus -groupof Metaphycus Mercet (Hym., Encyrtidae) from South Africa, withnotes on some extra-limital species. Rev. Zool. Bot. Afr. 83, 322–360.

Annecke, D.P., Mynhardt, M.J., 1972. The species of the insidiosus -groupof Metaphycus Mercet in South Africa with notes on some extra-limitalspecies (Hymenoptera Encyrtidae). Rev. Zool. Bot. Afr. 85, 227–274.

Annecke, D.P., Mynhardt, M.J., 1981. The species of the asterolecanii -group of Metaphycus Mercet (Hymenoptera: Encyrtidae) from SouthAfrica with notes on some extralimital species. J. Entomol. Soc. SouthAfr. 44, 1–68.

Bartlett, B.R., 1953. Natural control of citricola scale in California. J.Econ. Entomol. 46, 25–28.

Bartlett, B.R., 1961. The influence of ants upon parasites, predators, andscale insects. Ann. Entomol. Soc. Am. 54, 543–551.

Bartlett, B.R., 1978. Coccidae. In: Clausen, C.P. (Ed.), IntroducedParasites and Predators of Arthropod Pests and Weeds: A WorldReview. Agriculture Handbook, 480. U.S. Dept. Agric., Washington,DC, pp. 57–74.

Bartlett, B.R., Ball, J.C., 1964. The developmental biologies of twoencyrtid parasites of Coccus hesperidium and their intrinsic competi-tion. Ann. Entomol. Soc. Am. 57, 496–503.

Bartlett, B.R., Lagace, C.F., 1961. A new biological race of Microterys

flavus introduced into California for the control of lecaniine coccids,with an analysis of its behavior in host selection. Ann. Entomol. Soc.Am. 54, 222–227.

Bartlett, B.R., Medved, R.A., 1966. The biology and effectiveness ofDiversinervus elegans (Encyrtidae: Hymenoptera), an imported para-sites of lecaniine scale insects in California. Ann. Entomol. Soc. Am.59, 974–976.

Ben-Dov, Y., 1993. A Systematic Catalogue of the Soft Scale Insects of theWorld (Homoptera: Coccoidea: Coccidae) with Data on GeographicalDistribution, Host Plants, Biology and Economic Importance. Flora &Fauna Handbook, vol. 9. Sandhill Crane Press, Gainesville, FL.

Ben-Dov, Y., Hodgson, C.J., 1997. Soft Scale Insects: Their Biology,Natural Enemies and Control, vol. 7B. Elsevier, Amsterdam.

Bernal, J.S., Luck, R.F., Morse, J.G., 1998. Sex ratios in field populationsof two parasitoids (Hymenoptera: Chalcidoidea) of Coccus hesperidum

L. (Homoptera: Coccidae). Oecologia 116, 510–518.Bernal, J.S., Luck, R.F., Morse, J.G., 1999. Augmentative release trials

with Metaphycus spp. (Hymenoptera: Encyrtidae) against citricolascale (Homoptera: Coccidae) in California’s San Joaquin Valley. J.Econ. Entomol. 92, 1099–1107.

Bernal, J.S., Luck, R.F., Morse, J.G., Drury, M.S., 2001. Seasonal andscale size relationships between citricola scale (Homoptera: Coccidae)and its parasitoid complex (Hymenoptera: Chalcidoidea) on SanJoaquin Valley citrus. Biol. Control 20, 210–221.

Blumberg, D., 1997. Encapsulation of parasitoids. In: Ben-Dov, Y.,Hodgson, C.J. (Eds.), Soft Scale Insects Their Biology NaturalEnemies and Control, vol. 7A. Elsevier, Amsterdam, pp. 375–387.

Bodenheimer, F.S., 1951. Citrus Entomology in the Middle East. Dr. W.Junk, Dordrecht, The Netherlands.

Compere, H., 1924. A preliminary report on the parasitic enemies ofthe citricola scale (Coccus pseudomagnoliarum [Kuwana]) withdescriptions of two new chalcidoid parasites. Bull. S. Calif. Acad.Sci. 23, 113–123.

Compere, H., 1931. A revision of the species of Coccophagus, a genus ofhymenopterous, coccid-inhabiting parasites. Proc. U.S. Nat. Mus. 78,1–132.

Compere, H., 1957. Descriptions of species of Metaphycus recentlyintroduced into California and some corrections. Bollettino delLaboratorio di Entomologia Agraria ‘Filippo Silvestri’. Portici 15,227–229.

Das, G.M., Ganguli, R.N., 1961. Coccoids on tea in North-east India.Indian J. Entomol. 23, 245–256.

Dean, H.A., Bailey, J.C., 1960. Introduction of beneficial insects for thecontrol of Citrus scale insects and mites. J. Rio Grande Valley Hortic.Soc. 14, 40–46.

De Villiers, E.A., Van den Berg, M.A., 1987. Soft and wax scales. In:Myburgh, A.C. (Ed.), Crop Pests in Southern Africa, vol. 2. Citrusand Other Subtropicals. Plant Protection Research Institute, Pretoria,pp. 33–37.

Ebeling, W., 1959. Subtropical Fruit Pests. Univ. Calif. Div. Agric. Nat.Sci., Oakland, CA.

Ewart, W.H., Metcalf, R.L., 1956. Preliminary studies of sugars andamino acids in the honeydews of five species of coccids feeding oncitrus in California. Ann. Entomol. Soc. Am. 49, 441–447.

Flanders, S.E., 1942a. Metaphycus helvolus, an encyrtid parasite of theblack scale. J. Econ. Entomol. 35, 690–698.

A. Kapranas et al. / Biological Control 42 (2007) 288–299 299

Flanders, S.E., 1942b. Biological observations on the citricola scale and itsparasites. J. Econ. Entomol. 35, 830–833.

Flanders, S.E., 1945. The complete interdependence of an ant and acoccid. Ecology 38, 535–536.

Flanders, S.E., 1953. Variations in susceptibility of citrus infesting coccidsto parasitization. J. Econ. Entomol. 46, 266–269.

Flint, M.L., Kobbe, B., Clark, J.K., Dreistadt, S.H., Pehrson, J.E., Jr.,Flaherty, D.L., O’Connell, N.V., Phillips, P.A., Morse, J.G., 1991.Integrated Pest Management for Citrus. 2nd ed. Univ. Calif. Div. Ag.& Nat. Res. Publ. 3303, Oakland, CA.

Gill, R.J., 1988. The Scale Insects of California. Part I. The Soft Scales(Homoptera: Coccoidea: Coccidae). Calif. Dep. Food & Agric.,Sacramento, CA.

Grafton-Cardwell, E.E., 2002. Can reduced risk pesticides upset biologicalcontrol of citrus pests? In: Hoddle, M.S. (Ed.), Proc. III Calif. Conf.Biol. Control, Univ. Calif., Riverside, CA, pp. 107–113.

Grafton-Cardwell, E.E., 2003. Citrus IPM in California: Regionaldifferences and their effects on arthropod management in the millen-nium.In: Proc. IX Intern. Citrus Cong., Intern. Soc. Citriculture,Orlando, FL, pp. 729–732.

Grafton-Cardwell, E.E., O’Connell, N.V., 2006. The status of biologicalcontrol in San Joaquin Valley citrus. In: Hoddle, M.S. (Ed.), Proc. VCalif. Conf. Biol. Control, Univ. Calif., Riverside, CA, pp. 8–15.

Grafton-Cardwell, E.E., Vehrs, S.L.C., 1995. Monitoring for organo-phosphate- and carbamate-resistant armored scale (Homoptera:Diaspididae) in San Joaquin Valley citrus. J. Econ. Entomol. 88,495–504.

Guerrieri, E., Noyes, J.S., 2000. Revision of the European species of genusMetaphycus Mercet (Hymenoptera, Chalcidoidea: Encyrtidae), para-sitoids of scale insects (Homoptera: Coccoidea). Syst. Entomol. 25,147–222.

Gullan, P.J., 1997. Relationships with ants. In: Ben-Dov, Y., Hodgson,C.J. (Eds.), Soft Scale Insects, Their Biology, Natural Enemies andControl, vol. 7A. Elsevier, Amsterdam, pp. 351–373.

Hayat, M., 1997. Aphelinidae. In: Ben-Dov, Y., Hodgson, C.J. (Eds.),Soft Scale Insects, Their Biology, Natural Enemies and Control, vol.7B. Elsevier, Amsterdam, pp. 111–145.

Hodgson, C.J., 1970. Pests of citrus and their control. PANS Trop. Pestic.Res. Headq. Inf. Unit 16, 647–666.

Immaraju, J.A., Morse, J.G., Kersten, D.J., 1989. Citrus thrips (Thysa-noptera: Thripidae) pesticide resistance in the Coachella and SanJoaquin Valleys of California. J. Econ. Entomol. 82, 374–380.

Kapranas, A., 2006. Parasitoids of Brown Soft Scale Coccus hesperidum L.in Southern California and Their Reproductive Strategies. Ph.D.Dissertation. Department of Entomology, University of California,Riverside, 162 pp.

Kozar, F., Ben-Dov, Y., 1997. Zoogeographical considerations and statusof knowledge of the family. In: Ben-Dov, Y., Hodgson, C.J. (Eds.),Soft Scale Insects, Their Biology, Natural Enemies and Control, vol.7A. Elsevier, Amsterdam, pp. 213–228.

Lampson, L.J., Morse, J.G., 1992. A survey of black scale, Saissetia oleae

(Hom., Coccidae) parasitoids (Hym. Chalcidoidea) in southern Cal-ifornia. Entomophaga 37, 373–390.

Lampson, L.J., Morse, J.G., Luck, R.F., 1996. Host selection, sexallocation, and host feeding by Metaphycus helvolus (Hymenoptera:Encyrtidae) on Saissetia oleae (Homoptera: Coccidae) and its effect onparasitoid size, sex, and quality. Environ. Entomol. 25, 283–294.

Mahmood, R., Mohyuddin, A.I., 1986. Integrated control of mango pests.Commonwealth Institute of Biological Control, Pakistan AgriculturalResearch Council, Islamabad, 11 pp.

Muegge, M.A., Lambdin, P.L., 1989a. Optimal length of Coccus hesperi-

dum (Homoptera: Coccidae) for parasitism by Coccophagus lycimnia

(Walker) (Hymenoptera: Aphelinidae). J. Entomol. Sci. 24, 96–100.Muegge, M.A., Lambdin, P.L., 1989b. Longevity and fecundity of

Coccophagus lycimnia (Walker) (Hymenoptera: Aphelinidae), a

primary parasitoid of Coccus hesperidum (Homoptera: Coccidae). J.Agric. Entomol. 6, 169–174.

Quayle, H.J., 1938. Insects of Citrus and Other Subtropical Fruits.Comstock Press, New York, NY.

Perez-Guerra, G., 1986. Coccids of holticultural crops in Canary Islands.Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’,Portici 43 (Suppl.), 227–229.

Prinsloo, G.L., 1984. An illustrated guide to the parasitic wasps associatedwith citrus pests in the Republic of South Africa. Sci. Bull. Dep. Agric.Rep. S. Afr. 402, 1–119.

Prinsloo, G.L., 1997. Encyrtidae. In: Ben-Dov, Y., Hodgson, C.J. (Eds.),Soft Scale Insects, Their Biology, Natural Enemies and Control, vol.7B. Elsevier, Amsterdam, pp. 69–109.

Rosen, D., 1967. On the relationships between ants and parasites ofcoccids and aphids on citrus. Beitr. Entomol. 17, 281–286.

Saakyan-Baranova, A.A., 1966. The life cycle of Metaphycus luteolus

Timb. (Hymenoptera, Encyrtidae), parasite of Coccus hesperidum L.(Homoptera, Coccoidea), and the attempt of its introduction into theUSSR. Entomol. Rev. 45, 414–423.

Schweizer, H., Luck, R.F., Morse, J.G., 2003. Augmentative releases ofMetaphycus sp. nr. flavus against citricola scale on oranges in the SanJoaquin Valley of California: are early releases better than late ones? J.Econ. Entomol. 96, 1375–1387.

Schweizer, H., Morse, J.G., Luck, R.F., Forster, L.D., 2002. Augmenta-tive releases of a parasitoid (Metaphycussp. nr. flavus) against citricolascale (Coccus pseudomagnoliarum) on oranges in the San JoaquinValley of California. Biol. Control 24, 153–166.

Smith, H.S., Compere, H., 1928. A preliminary report on the insectparasites of the black scale Saissetia oleae (Bernard). Univ. Calif. Publ.Entomol. 4, 231–334.

Sokal, R., Rohlf, F.J., 1995. Biometry. W.H. Freeman, New York, NY.Stapley, J.G., Gayner, F.C.H., 1969. World Crop Protection. Pests and

Diseases, vol. 1. Life Books Limited, England and Chemical RubberCo., Cleveland, OH.

Stauffer, S., Rose, M., 1997. Biological control of soft scale insects ininterior plantscapes in the USA. In: Ben-Dov, Y., Hodgson, C.J.(Eds.), . Soft Scale Insects, Their Biology, Natural Enemies andControl, vol. 7B. Elsevier, Amsterdam, pp. 183–205.

Timberlake, P.H., 1913. Preliminary report on the parasites of Coccus

heperidum in California. J. Econ. Entomol. 6, 293–303.Viggiani, G., 1997. Eulophidae, Pteromalidae, Eupelmidae and Signi-

phoridae. In: Ben-Dov, Y., Hodgson, C.J. (Eds.), Soft Scale Insects,Their Biology, Natural Enemies and Control, vol. 7B. Elsevier,Amsterdam, pp. 147–158.

Waite, G.K., 1986. Pests of lychees in Australia. In: Menzel, M., Greer,G.N. (Eds.), The Potential of Lychee in Australia, Proc. First Nat.Lychee Sem, Queensland, AU, pp. 41–50.

Walter, G.H., 1983a. ‘‘Divergent male ontogenies’’ in Aphelinidae(Hymenoptera: Chalcidoidea): A simplified classification and asuggested evolutionary sequence. Biol. J. Linn. Soc. 19, 63–82.

Walter, G.H., 1983b. Differences in host relationships between male andfemale heteronomous hyperparasitoids (Aphelinidae: Chalcidoidea): Areview of host location, oviposition, and pre-imaginal morphology andphysiology. J. Entomol. Soc. South Afr. 46, 261–282.

Weppler, R.A., Morse, J.G., Luck, R.F., 2003. Studies on rearingMetaphycus helvolus (Hymenoptera: Encyrtidae) for augmentativerelease against black scale (Homoptera: Coccidae) on citrus inCalifornia. Biol. Control 28, 118–128.

Yanosh, V.A., 1980. Food specialization in the family Aphelinidae(Hymenoptera, Chalcidoidea). Entomol. Rev. 58, 61–70.

Yu, D.S., Luck, R.F., 1988. Temperature-dependent size and devel-opment of California red scale (Homoptera: Diaspididae) and itseffect on host availability for the ectoparasitoid, Aphytis melinus

DeBach (Hymenoptera: Aphelinidae). Environ. Entomol. 17, 154–161.