Metaphycus Mercet 1917

Zuparko, Robert L., 2015, Annotated Checklist of California Encyrtidae (Hymenoptera), Zootaxa 4017 (1), pp. 1-126 : 35-41

Metaphycus Mercet 1917

Hosts. Hemiptera : Coccidae , Diaspididae , Eriococcidae , Kermesidae , Pseudococcidae , Triozidae

alberti ( Howard 1898a: 247) (Aphycus)

Type. USNM

Distribution. W (Los Angeles, Riverside, San Diego, Santa Barbara)

Host/habitat. Ceroplastes sp., Coccus hesperidum , Parthenolecanium persicae

Remarks. Originally described from Australia, this species has also been recorded from Hawaii and South Africa. Stauffer & Rose (1997) reported this species from Riverside county on C. hesperidum , while Bernal et al. (2001) reported it on citrus from the southern San Joaquin Valley (Fresno, Kern and Tulare counties) without specifying exactly which county it occurred in. They also reared this species from a batch of Coccus pseudomagnoliarum , noting that the exact host still needs to be confirmed. Kapranas et al. (2007) failed to find this species in their survey of Coccus hesperidum in southern California citrus. A single specimen from Solano County (UCDC) may belong to this species as well.

angustifrons Compere 1957: 227

Type. USNM

Distribution. E (Riverside, San Bernardino, San Diego)

Host/habitat. Coccus hesperidum

Remarks. In the 1950s, this species was repeatedly imported into California from the Orient against Coccus hesperidium and Saissetia oleae , but it was never considered established here ( Bartlett 1978a; Lampson & Morse 1992) until Kapranas et al. (2007) found it 50 years later in a survey of C. hesperidum parasitoids. Three scale species ( Coccus pseudomagnoliarum , Pulvinaria psidii and S. oleae ) have been reported as hosts of M. angustipennis ( Noyes & Hayat 1994; Noyes 2001), based upon citations from Bartlett (1978a) and Cock (1985) but I consider these records dubious, at best. For C. pseudomagnoliarum, Barlett (page 61) noted that M. angustipennis (among other species) reportedly “showed some interest in this scale in the laboratory”, and for S. oleae, Bartlett (page 69) simply reported that the parasitoid was imported in a biocontrol program, without any evidence that the scale was actually an acceptable host. The record of P. psidii is traceable to its importation into Bermuda in the 1950s, when Bennett & Hughes (1959) reported that many parasites from California of “unknown value” against the scale were imported, and among these was M. angustifrons , which did not become permanently established there. This species is very close to M. stanleyi , and Rugman-Jones et al. (2011), suggest that records of the former may be applicable to the latter.

anneckei Guerrieri & Noyes 2000

Type. PPRI

Distribution. E (Alameda, Los Angeles, Riverside, San Diego, Santa Clara, Ventura, San Francisco Bay area, Central Valley)

Host/habitat. Coccus hesperidum , Saissetia miranda , S. oleae , Waxiella mimosae ; NEW: Parasaissetia nigra (UCRC)

Remarks. Early in the 20th century, the South African species Metaphycus lounsburyi was exported to several countries (including Australia) in biocontrol programs directed against Saissetia oleae . However, Guerrieri & Noyes (2000) realized that two parasitoid species were involved, and described the second one as M. anneckei , noting that much of the literature about M. lounsburyi may refer to M. anneckei . In 1916, “ M. lounsburyi ” was imported from Australia and became established in southern California ( Smith & Compere 1928), but Noyes (in litt.) thinks this was likely M. anneckei . Bartlett (1978a) reported that M. lounsburyi (presumably M. anneckei ) may be the second most effective parasitoid of the black scale in the State, while Kennett (1986) and Lampson & Morse (1992) found it to be much less important. Specimens labelled as this species are recorded from “ Lecanium viridis ” (=? Coccus viridis Green ) and Parthenolecanium corni (both UCRC), but I suspect these are misidentifications.

argyrocomus ( Compere 1947: 10) (Erythraphycus) Type. USNM

Distribution. C (Lassen, Marin, Monterey, Riverside) Host/habitat. Eriococcus sp.

armitagei ( Compere 1926a: 30) (Aenasioidea)

Type. USNM

Distribution. C (Los Angeles, Marin)

Host/habitat. The original description was based on a specimen collected on a Quercus sp. in Los Angeles, which led Compere to opine that the host was likely to be a Kermes sp., but such an association has never been established. A single specimen (RLZC) was collected on Quercus agrifolia in Marin County, indicating that the species extends throughout California’s central coast area.

californicus ( Howard 1898a: 245) (Aphycus)

Type. USNM

Distribution. N (Butte, Calaveras, Contra Costa, El Dorado, Lassen, Los Angeles, Madera, Marin, Monterey, Nevada, Plumas, Riverside, San Benito, San Bernardino, San Joaquin, San Luis Obispo, Santa Barbara, Santa Clara, Sonoma, Stanislaus, Tulare, Yolo)

Host/habitat. Eulecanium sp., Mesolecanium nigrofasciatum , Parthenolecanium corni , P. pruinosum

Remarks. Timberlake (1916) thought that M. oregonensis ( Howard 1898a) was probably the male of M.

californicus , and later suggested that M. pulvinariae ( Howard 1881) might be synonymous as well ( Compere & Annecke 1961). This same paper noted that M. californicus was indistinguishable from the imported Palearctic M. insidiosus ( Mercet 1921) , although there is no evidence that the latter ever established in California. They also reported that M. californicus is likely to be confused with M. stanleyi Compere morphologically, although these two species can be separated based on host species. Two specimens from Santa Barbara County (USNM) that seems to be referable to this species were reared from Physokermis insignicola .

calvus ( Compere 1947: 11) (Erythraphycus)

Type. USNM

Distribution. C (Contra Costa, Marin, Riverside, San Benito, San Bernardino, Santa Clara, Solano, Stanislaus)

Host/habitat. Collected on an Eriogonum sp. ( Polygonaceae )

Remarks. Compere described this species with only the first two funicular segments darkened, but here I include a series of specimens which have the 3rd and 4th segments darkened as well.

clauseni ( Timberlake 1918: 358) (Pseudococcobius)

Type. USNM

Distribution. C (Alameda, Calaveras, Contra Costa, Imperial, Kern, Los Angeles, Marin, Napa, Riverside, San Benito, San Bernardino, San Diego, Santa Clara, Sonoma, Stanislaus)

Host/habitat. Amonostherium lichtensioides , Eriococcus adenostomae , E. palustris , E. sp.; NEW: Eriococcus coccineus (UCRC)

Remarks. Timberlake (1918) recorded this species from an “ Erium sp.” on cactus, which Peck (1951) considered possibly an Amonostherium species. Essig (1926) reported the association with E. palustris on Spartina foliosa (Poaceae) , which is limited to the high tide zone in the San Francisco Bay area. I have collected specimens over a range of ecological habitats, including the Sierra foothills, inland chapparal, and the coastal plain.

coquilletti ( Howard 1898a: 244) (Aphycus) Type. USNM

Distribution. N (Los Angeles) Host/habitat. Pulvinaria bigeloviae

eriococci ( Timberlake 1916: 631) (Aphycus)

Type. USNM

Distribution. N (Contra Costa)

Host/habitat. Coccus hesperidum , Eriococcus quercus

Remarks. Originally described from Utah, Essig (1926) reported this species from California, without providing a more specific location. I’ve found only one specimen from California, from Mt. Diablo State Park.

eruptor ( Howard 1881: 364) [New state record] (CSCA, RLZC) Type. USNM

Distribution. W (Marin, San Diego)

Host/habitat. Ceroplastes cirridpediformis , C. floridensis , C. sp., “ Lecanium sp.”

flammeus Compere 1947:13

Type. USNM

Distribution. C (Alameda, Calaveras, Contra Costa, Kern, Los Angeles, Marin, Mendocino, Plumas, Santa Clara, Sierra, Solano, Tehama)

Host/habitat. Parthenolecanium quercitronis

fumipennis ( Timberlake 1918: 356) (Pseudococcobius) Type. USNM

Distribution. N (Riverside, San Bernardino) Host/habitat. Eriococcus sp., Phenacoccus solani Remarks. Timberlake (1918) reported this species was reared from Pseudococcus solani (Cockerell) in southern California (San Bernardino County). However, it is likely that Timberlake’s identification of the host was based on Essig’s (1909 or 1914) characterization, which was a misidentification of Phenacoccus solani ( Ben-Dov 2006b). Certainly, in a later work Essig (1926: 833) reported the parasitoid (as Pseudococcobius fumipennis ) “Reared from Phenacoccus solani Ferris in southern California” and did not include any mention of Pseudococcus solani , suggesting that he recognized the initial record of this species to be a mistake. Further, while Phenacoccus solani is known from throughout California ( McKenzie 1967), Pseudococcus solani is known only from New Mexico ( Ben-Dov 2006b).

funicularis Annecke 1965: 227

Type. SANC

Distribution. E (Alameda, Marin, Monterey, Santa Cruz, Yolo)

Host/habitat. Pulvinaria delottoi , Pulvinariella mesembryanthemi , P. sp.

Remarks. This species was introduced from South Africa with M. stramineus in a biocontrol program against P. delottoi and P. mesembryanthemi from 1978–1983, and along with Encyrtus saliens , is credited with successfully controlling both scale species ( Tassan & Hagen 1995). The record of M. funicularis being used in a biocontrol program against Saissetia oleae ( Lampson & Morse 1992) appears to be in error.

fuscipennis ( Howard 1898a: 241) (Aphycus)

Type. USNM

Distribution. C (Alameda, Amador, Calaveras, Contra Costa, El Dorado, Kern, Marin, Monterey, San Benito, San Bernardino, Santa Barbara, Santa Clara, Sonoma, Stanislaus)

Host/habitat. Eulecanium sp. on Arctostaphylos pungens (Ericaceae)

Remarks. Both Howard (1898a) and Compere (1947) reported this species from undetermined “ Lecanium ” species, but this generic name has since been suppressed under Eulecanium Cockerell. Essig (1926) ascribed the original host record from Arctostaphylos in Sonoma County to Parthenolecanium corni , but this conclusion is questionable since P. corni has not otherwise been associated with any Arctostaphylos species.

hageni Daane & Caltagirone 1999: 14

Type. EMEC

Distribution. E (Tehama)

Host/habitat. Saissetia oleae

Remarks. This is a European species, imported from Spain in 1985 during a biocontrol program against Saissetia oleae ( Daane & Caltagirone 1999) and has been confused with both M. anneckei and M. lounsburyi ( Guerrieri & Noyes 2000) .

helvolus ( Compere 1926a:25) (Aphycus)

Type. USNM

Distribution. E (Alameda, Contra Costa, Kern, Los Angeles, Marin, Merced, Modoc, Monterey, Orange, Placer, Riverside, San Bernardino, San Diego, San Francisco, San Mateo, Santa Clara, Stanislaus, Tulare, Ventura)

Host/habitat. Ceroplastes destructor , C. helichrysi , C. sp., Coccus hesperidum , C. pseudomagnoliarum , Coccus viridis , Eucalymnatus tessellatus , Marsipococcus proteae , Parasaissetia litorea , P . nigra, P. sp., Parthenolecanium corni , P. persicae , Protopulvinaria pyriformis , Pulvinaria aethiopica , P. psidii , P. urbicola , Pulvinariella mesembryanthemi , Saissetia coffeae , S. nigrella , S. oleae , S. somereni , S. sp.; NEW: Coccus africanus , Parlatoria pergandii (both UCRC)

Remarks. This is a south African species which was established in California in 1937 in a biocontrol program for Saissetia oleae , and is one of its most effective imported natural enemies ( Bartlett 1978a; Kennett 1986; Daane et al. 1991; Lampson & Morse 1992). Noyes (2001) listed M. helvolus as a biocontrol agent of Aonidiella aurantii , but this is misleading—the paper he cited ( Bellows & Morse 1988) merely noted the effect of pesticides (applied for A. aurantii control) on parasitoids of other species. Guerrieri & Noyes (2000) note that Aspidiotus sp. (Homoptera: Diaspididae ) and Rastrococcus mangiferae (Green) (Homoptera: Pseudococcidae ), have been reported as hosts, but they consider these records questionable.

howardi ( Cockerell 1898: 276) (Aphycus)

Type. USNM

Distribution. N (Lassen, Riverside)

Host/habitat. Eriococcus tinsleyi , E. sp.

Remarks. Two specimens (UCDC) from Imperial County may belong to this species as well.

immaculatus (Howard 1894: 235) (Aphycus) [New combination]

Type. USNM

Distribution. C (Los Angeles)

Host/habitat. Aonidiella aurantii

Remarks. The species was described in Aphycus , based on a single male. Timberlake (1916) was unable to locate the type, and opined that if it was a true Aphycus , then the host record of A. aurantii was “undoubtedly erroneous”. The holotype is slide type #1474 at the USNM, and belongs in Metaphycus , which means the original host record may be correct.

inviscus Compere 1940a: 20

Type. BMNH

Distribution. E (Contra Costa, Fresno, Marin, Santa Cruz, Sonoma, Tulare)

Host/habitat. Saissetia oleae , S. sp.

Remarks. Native to South Africa, this species was imported into California at least twice. A specimen mentioned in the original description was reared from the Riverside Insectary in 1924—probably imported in one of the shipments of parasitoids made by E.W. Rust in the 1920s ( Compere 1940b)—but there is no record of this species being released then. A second importation was made in 1979, and the species was recovered soon thereafter in the Central Valley ( Kennett 1986). Bartlett (1978a) reported a third importation of this species in1958, which apparently failed to establish. However, Annecke & Mynhardt (1972) considered this effort involved a species that is distinct from M. inviscus and described it as M. bartletti (now a junior synonym of M. lounsburyi ).

kermicola ( Timberlake 1916: 583) (Aenasioidea)

Type. USNM

Distribution. N (Los Angeles)

Host/habitat. Allokermes essigi , A. galliformis

Remarks. The host record of Allokermes (= Kermes ) nigropunctatus (Ehrhorn & Cockerell) cited in Essig (1926) is a misidentification of A. essigi (Miller & Gimpel) .

lecanii ( Howard 1898a: 242) (Aphycus)

Type. USNM

Distribution. C (Alameda, Los Angeles, Santa Barbara) Host/habitat. Eulecanium pubescens , E. sp., Parthenolecanium corni , P. quercifex , Physokermes insignicola

lounsburyi ( Howard 1898a: 244) (Aphycus)

Type. USNM

Distribution. E (Alameda, Marin, Riverside, San Diego, San Mateo, Santa Barbara, Santa Clara, Solano, Tulare, Ventura, Yolo)

Host/habitat. Ceroplastes floridensis , Coccus capparidis , C. hesperidum , C. pseudomagnoliarum , Lichtensia viburni , Parthenolecanium corni , Saissetia coffeae , S . oleae

Remarks. This species is native to South Africa, and has been exported as a parasitoid of Saissetia oleae to several countries. However, Guerrieri and Noyes (2000) discovered that material identified as M. lounsburyi included a second species, which they described as M. anneckei , noting that previous literature references to M. lounsburyi may be referrable to M. anneckei . One such reference includes Smith and Compere’s (1928) report of material imported from Australia into California in 1916, which Noyes (in litt.) thinks was likely M. anneckei . In 1958, a species identified as M. inviscus was imported from South Africa into California ( Bartlett 1978a), but Annecke & Mynhardt (1972) considered this material represented a new species, which they described as Metaphycus bartletti . Based on a comparison of types, Guerrieri & Noyes (2000) synonymized M. bartletti under M. lounsburyi . This makes M. lounsburyi represents one of the most widespread and important natural enemies of S. oleae in California ( Smith & Compere 1928; Bartlett 1978a; Kennett 1986, Daane et al. 1991; Lampson & Morse 1992). In his report on the parasitoids of S. oleae in central and northern California, Kennett (1986) reported distinct biological differences between the taxa he identified as M. lounsburyi and M. bartletti : the latter was one of the most common species found (in both the interior valley as well as the coastal and subcoastal areas), while the former appeared to be largely limited to the more temperate coastal area. Noyes (in litt.) suspects Kennett’s M. lounsburyi was really M. anneckei , and his M. bartletti was M. lounsburyi . Two specimens that appear close to M. lounsburyi were taken in Contra Costa and Kern counties (RLZC).

luteolus ( Timberlake 1916: 636) (Aphycus)

Type. USNM

Distribution. W (Butte, Fresno, Kern, Los Angeles, Orange, Riverside, San Bernardino, San Diego, Tulare, Ventura, Yolo, Yuba)

Host/habitat. Coccus hesperidum , C. pseudomagnoliarum , Parthenolecanium corni , Pulvinaria psidii , Pulvinariella mesembryanthemi , Saissetia coffeae , S. oleae

Remarks. This species may prove to be a junior synonym of M. flavus (Howard) ( Guerrieri & Noyes 2000) . These authors also note that the host record of Saissetia coffeae was incorrect, based upon an error in Herting (1972). However, S. coffeae is now considered the senior synonym of S. hemisphaerica ( Ben-Dov 2006a), and there are several records of that species serving as a host for M. luteolus . Coccus viridis has been noted as host of M. luteolus ( Noyes & Hayat 1994: 398) , based on its use in biocontrol programs against the scale in Bermuda and Hawaii. However, M. luteolus failed to establish in both cases, and there is no record of it successfully attacking this host ( Bennett & Hughes 1959; Bartlett 1978a). Specimens (UCRC) have been reportedly reared from Aonidiella aurantii and Parlatoria pergandii (both Hemiptera : Diaspididae ), but these records need to be confirmed.

matteolus ( Compere 1947: 11) (Erythraphycus)

Type. USNM

Distribution. C (Contra Costa, Imperial, Kern, Los Angeles, Marin, Merced, Napa, Riverside, San Bernardino, Solano, Stanislaus)

Host/habitat. Host unknown, but this species is common in chaparral, collected off Adenostoma fasciculatum , Chilopsis linearis arcuata (Bignoniaceae) , Juniperus californicus (Cupressaceae) and Larrea tridentata (Zygophyllaceae) .

Remarks. This species was described based on a single male specimen ( Compere, 1947). There are a series of females (EMEC, RLZC) that match the original description exactly, except for the color of the fore- and hind tibiae. Given the propensity for sexual dimorphism in the Encyrtidae , I have no hesitation in considering these females conspecific with M. matteolus . The specimen from Merced County (EMEC) was labeled “ex Desmia on wild grape”, but I think it likely this simply indicates the specimen was collected on grape ( Vitaceae ) infested with a Desmia species, and does not reflect an actual rearing record.

physokermis ( Timberlake 1916: 606) (Aphycus) Type. USNM

Distribution. C (Alameda, Contra Costa, Humboldt, Plumas, Santa Barbara) Host/habitat. Physokermis insignicola

psyllidis Compere 1943: 72

Type. USNM

Distribution. C (Los Angeles, Orange, Santa Barbara, Santa Clara, Ventura)

Host/habitat. Bactericera cockerelli

Remarks. This is one of only three species in the genus recorded as psyllid parasitoids ( Guerrieri & Noyes 2000).

stanleyi Compere 1940a: 20

Type. Lost

Distribution. E (Los Angeles, Orange, Riverside, San Bernardino, San Diego, Santa Barbara, Tulare, Ventura )

Host/habitat. Ceroplastes brevicauda , C. sp., Coccus alpinus , C. celatus , C. hesperidum , C. pseudomagnoliarum , C. viridis , Eucalymnatus tessellatus , Lichtensia chilianthi , Parasaissetia nigra , P. sp., Protopulvinaria pyriformis , Pulvinariella mesembryanthemi , Pulvinaria psidii , Saissetia coffeae , S. nigrella , S. oleae , Saissetia somereni , S. sp.; NEW: Pulvinarisca jacksoni (UCRC)

Remarks. Although the name is properly ascribable to Compere 1940a, the full description is found in Compere 1940b. Native to Africa, this species was imported into California in 1937 in a biocontrol program against Saissetia oleae , and immediately became established ( Compere 1940a, 1940b; Bartlett 1978a). This species was recovered in southern California over 55 years later at very low levels ( Lampson & Morse 1992), but was not found in central or northern California ( Kennett 1986; Daane et al. 1991). Bernal et al. (2001) reported this species on citrus from the southern San Joaquin Valley (Fresno, Kern and Tulare counties) without specifying exactly in which county this species occurred. This species is very similar to M. californicus , separable only by differences in hosts ( Compere & Annecke 1961). A host record of Coccus subhemisphaericus (Newstead) is doubtfully referred to M. stanleyi ( Compere 1940a) .

stramineus Compere 1940a: 28

Type. BMNH

Distribution. E (Alameda, Monterey, San Mateo)

Host/habitat. Pulvinaria delottoi , Pulvinariella mesembryanthemi

Remarks. Imported from South Africa from 1978–1983 in a biocontrol program against iceplant scales, this species, along with Encyrtus saliens and Metaphycus funicularis , established immediately and are credited with the successful control of those species ( Tassan & Hagen 1995).

trimblei ( Dozier 1936: 183) (Aenasioidea)

Type. USNM

Distribution. N (San Bernardino)

Host/habitat. Parthenolecanium quercifex

Remarks. The only primary literature record of this species is the original description, based on specimens from Caledonia, Pennsylvania. Noyes (2001) noted the type was from California, but I suspect this was a misreading of “ Caledonia ”. However, there is a single specimen of this species collected from San Bernardino County (UCRC).

zebratus ( Mercet 1917: 138) (Aphycus)

Type. MNMS

Distribution. E

Host/habitat. Ceroplastes floridensis , Drepanococcus cajani , Eriopeltis festucae , E. lichtensteini , Lecanopsis formicarum , Luzulaspis luzulae , Parthenolecanium corni , P. persicae , P. pomeranicum , P. rufulum , Pulvinaria vitis , Saissetia oleae

Remarks. This is a Palearctic species, imported into California in 1986 in a biocontrol program against Saissetia oleae . The species was released in northern and central California (Alameda, Contra Costa, Fresno, Glenn, Madera & Tehama counties), recovered and considered established, although the exact localities were not specified ( Lampson & Morse 1992). Questionable host records for this species include Aonidiella orientalis , Planchonia arabidis , Nipaecoccus sp., Phenacoccus aceris and Trionymus perrisi .

spp.

Remarks. In addition to the described species listed above, I have seen specimens that appear to represent up to 31 undescribed morphospecies from the state (LACM, RLZC, SBMN, UCDC, UCFC, UCRC).