Two new species of Ta m a r i x i a (Hymenoptera: Eulophidae) from Chile and Australia, established as biological control agents of invasive psyllids (Hemiptera: Calophyidae, Triozidae) in California Author Zuparko, Robert L. Author Queiroz, Dalva Luiz De Author Salle, John La text Zootaxa 2011 2921 13 27 journal article 46635 10.5281/zenodo.277920 134e43ac-a588-4e4b-9a64-7468ce0c7f31 1175-5326 277920 Tamarixia Mercet, 1924 Type species: Tamarixia bicolor Mercet, 1924 (original designation) Diagnostic characters. Tamarixia possesses two apomorphic characters that are unique within the Tetrastichinae : males have exceptionally long genitalia, and the anterior margin of the female hypopygium is almost straight (which may be hidden under the preceding sternite and is not easily visible in undissected specimens). Specimens of Tamarixia can also generally be distinguished by a combination of characters: fore wing with a single seta on the dorsal surface of the submarginal vein, propodeum without a Y-shaped carina as seen in Tetrastichus (although see description of Tamarixia dahlsteni ), midlobe of mesoscutum with 2 pairs of long, semi-erect setae that are about equal in length ( Figs 14, 15 ) (although some specimens of T. dahlsteni have three pairs) ( Graham 1991 ; LaSalle 1994 ). An additional diagnostic character is that the toruli are closer to eye margin than to each other ( Figs 6 , 13 ). Species are generally shiny black, but may have yellow markings on the gaster and/or head. Identification. Tamarixia contains species once treated as belonging to the pubescens group of the genus Tetrastichus ( Graham 1961 ; Domenichini 1966 , 1967 ). The species group was subsequently treated as a subgenus within Tetrastichus by Kostjukov (1977 , 1978 ), but has since been treated as a genus by most authors ( Graham 1987 , 1991 ; Bouček 1988a ; LaSalle 1994 ; Kostjukov, 1995 , 1996 , 2000 ; Schauff et al . 1997 ; Narendran 2007 ). Generic keys that distinguish Tamarixia from other tetrastichine genera are available for Australasia ( Bouček 1988a ), North America ( LaSalle 1994 ; Schauff et al . 1997 ), Europe ( Graham 1987 , 1991 ) and India ( Narendran 2007 ). Keys to Tamarixia species are available for Europe ( Graham 1991 ), European part of the USSR ( Kostjukov 1978: couplets 68–87 in key to Tetrastichus ), Far eastern Russia ( Kostjukov 1995 , 2000 ), India ( Narendran 2007 ) and North America ( Burks 1943, couplet 24 in the key to species of the genus Tetrastichus , treating only the two species ). A list of the 47 described Tamarixia species, with host and distributional information, is given in Table 1 . TABLE 1. Annotated list of species of Tamarixia . See Noyes (2003) for further information on taxonomic history and synonymy. Classification of psyllid hosts follows Burckhardt (2005). Host information mainly taken from Noyes (2003), and in some cases updated following Burckhardt (pers. comm.) and Burckhardt & Lauterer (1997) for Bactericera . actis (Walker 1839) Distribution. Europe: Czech Republic , France , Germany , Hungary , Ireland , England . Macaronesia: Azores, Canary Islands. Hosts. Psyllidae, Strophingiinae : Strophingia cinereae Hodkinson , Strophingia ericae (Curtis) . Host plants. Ericaceae : Calluna vulgaris (Linnaeus) , Erica cinerea Linnaeus , Erica scoparia Linnaeus. akkumica ( Kostjukov 1978 ) Distribution. Asia: Kazakhstan . arboreae (Graham 1979) Distribution. Macaronesia: Madeira Islands. Hosts. Psyllidae, Strophingiinae : Strophingia arborea Loginova , Strophingia fallax Loginova. Host plants. Ericaceae : Erica arborea Linnaeus , Erica scoparia Linnaeus. asiatica Kostjukov 1996 Distribution. Asia: Kazakhstan . atamiensis ( Ashmead 1904 ) . New combination from Tetrastichus Tetrastichus atamiensis Ashmead, 1904 : 162 . Holotype Ƥ, Japan , Atami. USNM Type 7206 [examined, digital image]. Distribution: Asia: Japan . bermius (Walker 1848) = upis bicolor Mercet 1924 Distribution. Europe: Bulgaria , Spain . Asia: Pakistan . Hosts. Triozidae : Trioza chenopodii Reuter. Host plants. Chenopodiaceae : Chenopodium album Linnaeus. brovni Kostjukov 2000 Distribution. Asia: Russia (Primor'ye Kray). caillardiae ( Kostjukov 1978 ) Distribution. Asia: Kazakhstan . Hosts. Psyllidae , Aphalarinae : Caillardia notata Loginova. Host plants. Amaranthaceae : Haloxylon sp. callunae (Erdös 1969) = actis cometes ( Girault 1915 ) Distribution. Australia (Northern Territory). dahlsteni Zuparko , sp. nov. Distribution. Australia (New South Wales , Queensland, Western Australia , Victoria). Hosts. Triozidae : Trioza eugeniae . Host plants. Myrtaceae : Syzygium paniculatum . Biological control. Imported into USA : California for the biological control of Trioza eugeniae . dhetysaicus Kostjukov 1996 Distribution. Asia: Kazakhstan . dryi (Waterston 1922) Distribution. Africa: Kenya , South Africa , Swaziland , Zimbabwe . Hosts. Triozidae : Trioza erytreae (Del Guercio) . Host plants. Rutaceae : Citrus spp. Biological control. Imported into Réunion , Mauritius for the biological control of Trioza erytreae . dwivarnus Narendran 2007 Distribution. Asia: Sri Lanka . dyra ( Burks 1943 ) Distribution. North America : USA (Colorado, Montana, Wyoming). Hosts. Psyllidae , Aphalarinae : Aphalara curta (Caldwell) ; Triozidae : Trioza sp. Host plants. Rutaceae : Citrus spp.; Apiaceae : Angelica sp.; Salicaceae : Salix sp.; Ranunculaceae : Thalictrum sp. flavicoxae Kostjukov 2000 Distribution. Asia: Russia (Primor'ye Kray). flavigaster (Brothers & Moran 1969) Distribution. Africa: South Africa . Hosts. Psyllidae , Rhinocolinae : Moraniella calodendri (Moran) . Host plants. Rutaceae : Calodendrum capense (Linnaeus filius). flaviventris ( Kostjukov 1978 ) Distribution. Asia: Kazakhstan , Tajikistan . girishi Narendran 2007 Distribution. Asia: India (Kerala). hanca Kostjukov 2000 Distribution. Asia: Russia (Primor'ye Kray). klarisae Kostjukov 1996 Distribution. Asia: Kazakhstan . leptothrix Graham 1991 Distribution. Europe: Czechoslovakia , Hungary , Ireland , Italy , England , Yugoslavia . Host plants. Salicaceae : Salix alba Linnaeus , Salix cinerea Linnaeus , Salix fragilis Linnaeus. leucaenae Bou ĕ ek 1988 Distribution. North America : USA (Florida). Central America and Caribbean: Mexico , Trinidad & Tobago . Hosts. Psyllidae, Ciriacreminae : Heteropsylla cubana . Host plants. Rutaceae : Citrus spp.; Fabaceae : Leucaena sp., Leucaena leucocephala (Lamarck) . Biological control. Imported into Africa and Asia for the biological control of Heteropsylla cubana . meteroa ( Girault 1915 ) Distribution. Australia (Queensland). monesus (Walker 1839) Distribution. Europe: Czech Republic , England , France , Germany , Hungary , Ireland , Italy , Slovakia , Slovenia , Sweden , Yugoslavia . Asia: Kazakhstan , Moldova , Russia (Astrakhanskaya Oblast). newelskoyi (Kostjukov 1990) Distribution. Asia: Russia (Yevreyskaya Oblast). nocturna Kostjukov 2000 Distribution. Asia: Russia (Primor'ye Kray). obscuratus (André 1878) = pronomus orientalis Khan, Agnihotri & Sushil 2005 Distribution. Asia: India (Uttaranchal). Hosts. Agromyzidae : Unspecified species. NOTE: This is the only record of a species of Tamarixia from an agromyzid, and indeed from a non-Hemipteran. It should be treated as doubtful without subsequent confirmation. Host plants. Asteraceae : Helianthus sp. orsillus (Walker 1839) = upis pallicornis (Walker 1872) Distribution. Macaronesia: Madeira Islands. pallicornis (Thomson 1878) = monesus pallidicornis (Dalla Torre 1898) = monesus pamyles (Walker 1839) = pronomus poddubnyi ( Kostjukov 1978 ) Distribution. Asia: Moldova , Uzbekistan , China ( new record - NingXia, Yinchuan, Gaojiazha, 22 June 2010 , coll. C.D. Zhu, on Eleagnus angustifolia Linnaeus ). Hosts. Triozidae : Trioza magnisetosa Loginova ; Aphididae : Capitophorus hippophaes (Walker) . Host plants. Elaeagnaceae : Elaeagnus sp., Elaeagnus orientalis Linnaeus , Eleagnus angustifolia ( new record ). pojarkovi (Kostjukov 1990) Distribution. Asia: Russia (Primor'ye Kray). pookodica Narendran 2007 Distribution. Asia: India (Kerala). pronomus (Walker 1839) Distribution. Europe: Czech Republic , England , France , Germany , Greece , Hungary , Ireland , Italy , Norway , Portugal , Sweden . Macaronesia: Canary Islands, Madeira Islands. Hosts. Triozidae : Bactericera kratochvili Vondracek , Trioza apicalis Förster , Trioza centranthi (Vallot) , Trioza urticae (Linnaeus) . Host plants. Valerianaceae : Centranthus angustifolius (Miller) . przewalskii (Kostjukov 1990) Distribution. Asia: Russia (Yevreyskaya Oblast). pubescens (Nees 1834) Distribution. Europe: Czech Republic , England , Germany , Hungary , Italy , Slovakia , Yugoslavia . Hosts: Triozidae . Trioza remota Förster. pygmaea (Erdös 1954) = pygmaeola pygmaeola (Erdös 1958) Distribution. Europe: France , Hungary , Yugoslavia . Hosts. Triozidae : Trioza rumicis Löw. Host plants. Polygonaceae : Rumex scutatus Linnaeus. radiata (Waterston 1922) Distribution. Asia: India , Pakistan . Hosts. Psyllidae, Diaphorininae : Diaphorina citri ; Psyllidae, Aphalaroidinae : Pallipsylla hyalina (Mathur) ; Triozidae : Trioza erytreae , Trioza sp. Host plants. Fabaceae : Albizia lebbeck (Linnaeus) ; Rutaceae : Citrus spp., Murraya paniculata (Linnaeus) . Biological control. Imported into Réunion , India , Saudi Arabia , Mauritius , Nepal , Taiwan , China , Indonesia , Malaysia , Thailand , Vietnam , USA (Florida, Texas), Mexico , Brazil , Argentina , Guadeloupe , Puerto Rico for the biological control of Diaphorina citri . rudolfae ( Kostjukov 1978 ) Distribution. Asia: Kazakhstan . schina Zuparko , sp. nov. Distribution. South America : Chile . Hosts. Calophyidae : Calophya schini . Host plants. Anacardiaceae : Schinus molle . Biological control. Imported into USA (California) for the biological control of Calophya schini . Also present in Mexico , presumably as spread of the California introduction. sheebae Narendran 2005 Distribution. Asia: India (Kerala). Host plants. Combretaceae : Terminalia arjuna Roxburgh. stelleri (Kostjukov 1990) Distribution. Asia: Russia (Primor'ye Kray). tamaricis ( Domenichini 1967 ) = bicolor tremblayi (Domenichini 1965) Distribution. Europe: Czechoslovakia , Italy , United Kingdom . Hosts. Triozidae : Bactericera tremblayi (Wagner) . Host plants. Alliaceae : Allium cepa Linnaeus. triozae ( Burks 1943 ) Distribution. USA (Arizona, California, Colorado, Idaho, Kansas, Montana, Nebraska, New Mexico , Texas, Washington). NOTE: Herting (1972) recorded this species from Italy , and Chazeau (1987) reported it from New Caledonia on Heteropsylla cubana on Leucaena leucocephala . Because T . triozae is otherwise known only from the Nearctic region, we suspect these records are misidentifications. Hosts. Calophyidae : Calophya californica Schwarz , Calophya nigrella Jensen , Calophya nigripennis Riley , Calophya triozomima Schwarz ; Psyllidae : Ceanothia ceanothi (Crawford) , Euglyptoneura minuta (Crawford) , Euphalerus vermiculosus Crawford , Pexopsylla cercocarpi Jensen ; Triozidae : Bactericera cockerelli (Sulc) , Bactericera minuta (Crawford) , Bactericera nigricornis (Förster) , Trioza albifrons Crawford , Trioza beameri Tuthill. Host plants. Rosaceae : Amelanchier sp.; Solanaceae : Solanum tuberosum Linnaeus. tschirikovi (Kostjukov 1990) Distribution. Asia: Russia (Yevreyskaya Oblast). turundaevskayae ( Kostjukov 1978 ) Distribution. Asia: Kazakhstan . upis (Walker 1839) Distribution. Europe: Czech Republic , England , France , Italy , Slovakia , Sweden , Moldova , Russia (Moscow Oblast, St. Petersberg). Macaronesia: Madeira Islands. Hosts. Triozidae : Bactericera femoralis (Förster) , Trioza urticae . Host plants. Rosaceae : Alchemilla vulgaris Linnaeus ; Urticaceae : Urtica sp. vinokurovi Kostjukov 1995 Distribution. Asia: Russia (Primor'ye Kray). yoorica Narendran 2007 Distribution. Asia: India (Kerala). Distribution. Tamarixia is a cosmopolitan genus, with most of its 47 described species from the Palearctic and Oriental regions ( Table 1 ). Because the greatest diversity of Psylloidea occurs in the southern tropics ( Hodkinson 1984 ), the number of known Tamarixia species will undoubtedly increase as the fauna from Africa, Australia and South America becomes better characterized. During the course of this study, specimens have been examined that represent quite a few new species from North America (California, Florida), South America ( Brazil , Chile ), and Australia . It is clear that further collecting and rearing of psyllids will greatly expand the known fauna of this genus. Biology. Species of Tamarixia are primary parasitoids of psyllids ( Graham 1987 , 1991 ; Bouček 1988a , 1988b ; LaSalle 1994 ; Noyes 2003 ). However, aphids can also serve as hosts for Tamarixia species. In his description of T. poddubnyi , Kostjukov (1978) recorded it from the aphid Capitophorus hippophaes (Walker) , and an undescribed Tamarixia species in EMEC has the label data: California: Los Angeles County, Highway 138, 6 miles east of Gorman, 1 June 1961 , J.C. Hall, reared from Aphis gossypii [Glover] on Solanum elaeagnifolium [Cavanilles]. Further collecting will be required to understand just how frequent the use is of non-psyllid hosts. A record of T. orientalis Khan, Agnihotri & Sushil from an agromyzid ( Table 1 ) should be treated as doubtful without subsequent confirmation. Most records list Tamarixia species as ectoparasitoids, however T. upis (Walker) has been recorded as an endoparasitoid ( Noyes 2003 ).