Hayhurstia atriplicis (Linnaeus, 1761)

Kondo, Takumasa, Rosero, Robert & Gaviria, Jackeline, 2024, First record of the invasive chenopodium aphid, Hayhurstia atriplicis (Linnaeus, 1761) (Hemiptera: Aphididae), in Colombia, Insecta Mundi 2024 (48), pp. 1-7 : 3-5

Hayhurstia atriplicis (Linnaeus, 1761)

Diagnosis

Insects in life ( Fig. 1A–B ). Individual of H. atriplicis feed on young leaves which become folded along the midvein and distorted, forming pseudogalls ( Fig. 1C–D ), probably due to the injection of toxins in the aphids’ saliva. Females: Alate with dark head and thorax, abdomen light brown in color; adult apterae dark green, covered with white waxy powder; siphunculi very small, ca. 1.5 to 3.0 mm long, inconspicuous, distinctly shorter than cauda ( Blackman and Eastop 2008), oviparous ( Hayhurst 1909). Males: Apterous or alate ( Blackman and Eastop 2008), small, elongated, wingless males yellowish, with blackish appendages ( Hayhurst 1909).

Mounted specimens (Not illustrated, but good photographs available in Pruna et al. 2023). Hayhurstia Del Guercio, 1917 ( Aphidinae : Macrosiphini ) is a monotypic genus, with its type species, H. atriplicis , defined by the presence of slightly clavate siphunculi with a small flange distinctly shorter than the finger-like cauda ( Blackman and Eastop 2008).

Biology. The species is monoecious, holocyclic, ovipositing in October [in temperate regions of the Northern Hemisphere] ( Blackman and Eastop 2008). In Colombia, the species is multivoltine and is found throughout the year; only females were observed in the present study. Aphids are commonly found living inside yellowish pod-like pseudogalls which are formed by leaves rolling upwards ( Blackman and Eastop 2008). During the present study, inside some of the pseudogalls of H. atriplicis , numerous specimens of the thrips, Frankliniella sp. ( Thysanoptera : Thripidae ), were found, probably taking advantage of the protection provided by the pseudogalls (T. Kondo, personal observation). Earwigs and syrphid fly larvae were also found inside the pseudogalls (see below under natural enemies). Quinoa plants of the Blanca de Jerico variety which were heavily infested by H. atriplicis had most of the leaves deformed into pseudogalls, showed stunted growth, and did not develop panicles (T. Kondo, personal observation). During the present study, H. atriplicis was found affecting various cultivars, including Blanca de Jericó, Tunkahuan and Aurora, however, the levels of susceptibility and resistance of these varieties to this aphid species remains to be studied.

Host plants. Hayhurstia atriplicis is found on host plants of the family Amaranthaceae (as Chenopodiaceae ), usually on Atriplex spp. [hence its specific epithet “ atriplicis ”] and Chenopodium spp. [hence its common name “ Chenopodium aphid”] ( Blackman and Eastop 2008). Ellis (2024) reported H. atriplicis as oligophagous on Amaranthaceae and provided a detailed list of plant hosts as follows: Atriplex calotheca (Rafn) Fr. , A. glabriuscula Edmondston , A. halimus L., A. hortensis L., A. laciniata L., A. littoralis L., A. patula L., A. prostrata Boucher ex DC. , A. sagittata Borkh. ; Bassia scoparia (L.) A.J. Scott; Chenopodiastrum hybridum (L.) S. Fuentes-B., Uotila & Borsch, Chenopodiastrum murale (L.) S. Fuentes-B., Uotila & Borsch; Chenopodium album L., Ch. bonus-henricus L., Ch. ficifolium Sm. , Ch. foliosum (Moench) Asch. , Ch. glaucum L., Ch. opulifolium Schrad. ex W.D.J. Koch & Ziz , Ch. quinoa , Ch. rubrum L., Ch. strictum Roth , Ch. urbicum L., Ch. vulvaria L.; Dysphania ambrosioides (L.) Mosyakin & Clemants, D. botrys (L.) Mosyakin & Clemants; Einadia nutans (R. Br.) A.J. Scott ; Halimione pedunculata (L.) Aellen, H. portulacoides Aellen ; Haloxylon tamariscifolium (L.) Pau (as “ Hammada tamariscifolia ”); and Lipandra polysperma (L.) S. Fuentes-B., Uotila & Borsch. Additionally, it is rarely found on Beta vulgaris L. and Spinacia oleracea L. ( Ellis 2024).

Natural enemies. A study conducted in the Czech Republic reported that H. atriplicis is commonly parasitized by two braconid parasitoids, namely, Diaeretiella rapae (McIntosh, 1855) and Ephedrus nacheri Quilis, 1934 ( Hymenoptera : Braconidae ) ( Starý and González 1991). Furthermore, the Universal Chalcidoidea Database ( UCD Community 2023), lists five wasp parasitoids of H. atriplicis , namely Aphelinus atriplicis Kurdjumov, 1913 ( Hymenoptera : Aphelinidae ), Asaphes rufipes Brues, 1909 , A. suspensus (Nees, 1834) , A. vulgaris Walker, 1834 and Pachyneuron siphonophorae (Ashmead, 1886) ( Hymenoptera : Pteromalidae ). During the present study, numerous natural enemies were found inside the pseudogalls of H. atriplicis , including an undetermined species of parasitoid wasp ( Hymenoptera ) (based on the presence of mummies of both alate and apterous aphid individuals), an unidentified earwig ( Dermaptera : Forficulidae ), and the larvae of at least two unidentified species of syrphid flies ( Diptera : Syrphidae ). Other generalist predators were found on infested plants (outside the pseudogalls), including the invasive ladybird beetles, Harmonia axiridis (Pallas, 1773) and Cheilomenes sexmaculata (Fabricius, 1781) , and New World species, Coleomegilla maculata (DeGeer, 1775) , Cycloneda emarginata (Mulsant, 1850) , and Neda sp. ( Coleoptera : Coccinellidae ), as well as an undescribed species of green lacewing ( Neuroptera : Chrysopidae ) and a brown lacewing ( Neuroptera : Hemerobiidae ); all of the latter are possible predators of H. atriplicis , however, further studies are needed to confirm their role as predators of this aphid species. Specimens of the natural enemies are deposited in CTNI.

Material examined. Hayhurstia atriplicis (Linnaeus, 1761) . Colombia: Cauca, Bolivar, Vereda La Zanja , 01°46′ 28″N, 76°53′38″W, 1.777 m.s.n.m., ex Chenopodium quinoa , 5.x.2023, coll. Takumasa Kondo, 5 slides, 5 specimens ( CTNI) ; same data except, 28.viii.2023, coll. Robert Rosero, 5 slides, 5 specimens ( CTNI) ; Cauca, Totoró, vereda La Palma , Finca La Palma , 02°33′45″N, 76°26′14″W, 2.600 m.s.n.m., 11.iv.2023, coll. Robert Rosero, 5 slides, 5 specimens ( CTNI). Ecuador: Hayhurstia atriplicis / (Linnaeus) / ECUADOR / ex Chenopodium sp. / April 20, 2006 / K. Ahuja / Elizabeth 210904 / 0608240 / Balsam, 1 slide, 2 specimens ( USNM) .

Other material studied. Frankliniella sp. ( Thysanoptera : Thripidae ). Colombia: Cauca, Totoró, vereda La Palma, Finca La Palma, 02°33′45″N, 76°26′14″W, 2.600 m a.s.l., 11.iv.2023, coll. Robert Rosero, 4 slides, 4 specimens ( CTNI). Cycloneda emarginata (Mulsant) ( Coleoptera : Coccinellidae ), Colombia: Cauca, Bolívar, La Zanja, Finca La Zanja, 01°46′27.9″N, 76°53′37.5″W, 1777 m a.s.l., ex panicle of quinoa Chenopodium quinoa , 28.iii.2023, coll. Jackeline Gaviria, 1 specimen ( CTNI); same data, except Neda sp. , 1 specimen ( CTNI); Cheilomenes sexmaculata Fabricius ( Coleoptera : Coccinellidae ), Colombia: Cauca, Totoró, La Palma, Finca La Palma, 02°33′45″N, 76°26′14″W, 2.600 m a.s.l., 11.ix.2023, coll. Robert Rosero, 1 specimen ( CTNI); same data, except Harmonia axyridis (Pallas) ( Coleoptera : Coccinellidae ); same data except 10.vii.2023, Coleomegilla maculata De Geer ( Coleoptera : Coccinellidae ), 1 specimen ( CTNI).

Figures

Figure 1. Hayhurstia atriplicis (Linnaeus). A) Adult alate and apterae. B) An aggregation of adults and immature apterae inside a curled infested quinoa leaf. C) A quinoa plant with many leaves being infested by the aphid. D) Close-up of two pseudogalls on quinoa plant of the Blanca de Jerico variety. Notice the reddish color of the pseudogalls which contrasts with the healthy green leaves. Photos: A and B by Y. Campos Patiño; C and D by T. Kondo.