Euschistus taurulus Berg, 1878

Hickmann, Frederico, Moraes, Tamara, Bianchi, Filipe Michels, Corrêa, Alberto Soares & Schwertner, Cristiano Feldens, 2019, Integrating data to redescribe Euschistus taurulus Berg (Hemiptera: Pentatomidae), Zootaxa 4688 (1), pp. 119-134 : 122-128

Euschistus taurulus Berg, 1878

( Figs. 1–6 )

Euschistus taurulus Berg, 1878: 44-45 ; Kirkaldy, 1909: 66; Pennington, 1920: 8; Rufinelli & Pirán, 1959: 15; Rolston, 1984:

353. Euchistus bifibulus var. guayaquilinus Kuhlgatz & Melichar, 1903: 247 ; Rolston, 1984: 353. Euschistus (Mitripus) taurulus ; Grazia & Schwertner, 2008: 234. Euschistus (Euschistus) taurulus ; Grazia & Schwertner, 2011: 715; Dellapé, Rider & Dellapé, 2015: 171; Grazia, Schwertner & Coscarón, 2017: 224; Da Silva, Santos & Fernandes, 2018: 429.

Coloration. Dorsal surface light to dark brown with black punctures ( Fig. 2 A–B), with sexual dimorphism: dorsal surface of females often lighter than males. Antennae light to dark brown, becoming darker toward the apex of the antennomeres IV and V. Humeral angles sometimes reddish. Scutellum bearing a small pale spot apically. Connexivum dark brown to black, bearing a median semicircular light spot. Ventral surface: green in alive females and yellow in males; pale yellow to light brown in dry-pinned specimens, with no distinction between female and male. Thorax ventrally with punctures darker than the surrounding area; thoracic pleura bearing black spots at supracoxal cleft of each pleurite. Legs darker than abdomen with small black spots at the distal apex of femur and the tibia. Abdomen may present irregular light brown spots mesial and mesolaterally.

General body structure. Median size (7–10 mm), with males smaller than females ( Tab. 1 ). Body dorsally flattened, anterior portion of pronotum declivent. Abdomen more convex ventrally.

Head. Clypeus slightly longer than mandibular plates (juga), both rounded apically. Antenomeres proportion in both sexes: I<II<III<V=IV. Anterior margin of bucculae truncated, posterior margin evanescent. Rostrum reaching the metacoxae.

Thorax. Anterolateral margin of pronotum denticulated from anterior onto humeri; humeral angles produced anterolaterally in a stout spine. Foveas present, and basal angles of scutellum unpunctured or at least less punctured than the disc. Mesocorium opaque, membrane of hemelytra light brown translucent. Evaporatorium surface unpunctuated, extending onto posterior margin of mesopleuron, on the metapleuron extending no more than halfway from ostiole to metapleural lateral margin; spout-like peritreme.

Abdomen. Urosternite III presenting a slight tumescent area mesially. Posterolateral angles of urosternite VII slightly projected in a spine. Spiracles concolors.

Male genitalia ( Figs. 3 & 4 ). Pygophore quadrangular; genital cup well exposed dorsally ( Fig. 3A ); posterolateral angles of pygophore slightly acute produced. Inferior layer of ventral rim (vr) concave, bearing an acute projection mesially; superior layer of ventral rim (slvr) (inferior ridge sensu Rolston 1974) produced dorsally, excavated mesially in a shallow U-shape notch; dorsal rim (dr) concave, slightly notched mesially, but not projected over the segment X. Lateral margin stout, blackened ( Fig. 3A and C ). Superior process of dorsal rim (spdr) toothlike ( Fig. 3B ). Segment X presenting a pair of small tubercles pointing laterally, located at ⅔ to the apex, apical third of seg- ment X smooth, presenting setae.

Paramere ( Fig. 4 D–G) with basal apodeme smaller than the base of the crown. Stem longer than the crown, enlarged apically. Crown geniculate, bent laterally, surface connecting basal and apical processes deeply concave ( Fig. 4E and F ); apical process (app) rounded and stout at apex, bearing a crenulated region; middle process not developed; basal process (bpp) rounded at apex projected laterally, outer surface with long sensilla.

Phalloteca pyriform ( Fig. 4 A–C), short; posterodorsal margin concave, posterolateral angles with rounded projections; short dorsal processes of phallotheca (prph), digitiform, tapering towards the apex ( Fig. 4A ), slightly bent ventrally, not surpassing the conjunctiva when it is expanded ( Fig. 4A and B ). Vesica process (vp) gutter-like ( Fig. 4A and 4C ). Ductus seminis distalis (dsd) coiled, twice longer than phallotheca. Lobes of conjunctiva (cj) sclerotized apically forming a black spike.

Female genitalia ( Figs. 5 & 6 ). In posterior view ( Fig. 5B ): sutural margins of gonocoxites VIII straight at the base, not overlapped, slightly concave at the middle toward the apex; posterior margin of gonocoxites VIII concave, posterolateral margins projected posteriorly, but not reaching the middle of gonocoxites IX (gcIX). Gonocoxites IX wider than long, somewhat triangular; lateral and posterior margins rounded, anterior margin straight. In pos- teroventral view ( Fig. 5A ): posterior margin of gonocoxites VIII sinuous, rounded laterally and acute mesially; conspicuously elevated mesially related to lateral half. Laterotergites VIII acute, sometimes developed as a black spine. Laterotergites IX (laIX) rounded at apex, margin posterolateral convergent, almost reaching each other at apex of gonocoxites IX. Segment X not surpassing the dorsal band that unites laterotergite VIII, almost obliterated by laterotergites IX.

Internal genitalia ( Fig. 6 ): Ring sclerites (rs) oblong, transversally oriented ( Fig. 6B ). Ductus receptaculi proximalis (drp) as long as vesicular area ( Fig. 6A ). Median wall of vesicular area enlargerd at apex; porterior margin of ductus receptaculis distalis (drd) conical ( Fig. 6A ); anterior (aaf) and posterior (paf) annular flanges projected anteriorly, the last covering a membranous portion of the pars intermedialis (pi); pars intermedialis 2/3 sclerotized and cup-like; capsula seminalis (cs) oval ( Fig. 6C ).

Type material. Holotype ♂, Argentina, Misiones (near San Ignácio). [not examined]

Material examined. VENEZUELA. Amazonas: Mavaca , 15.Apr.1965, F. Fernandes coll. ( IZAV, 1♂) ; Mona- gas: Jusepín , 09.Sep.1965, C. J. Rosales & F. Fernandez coll. ( IZAV, 3♀) . BRAZIL. Amapá: Macapá , 11.Jan.1980 ( UFRG, 1♂) . Amazonas: Barcelos , 18-22.Feb.1963, J. Bechyné coll. ( MZUSP, 1♀) ; Benjamin Constant , Nov.1962, A. Silva coll. ( MZUSP, 2♀ 2♂) ; Benjamin Constant, Rio Javari , Nov.1961, Coll. Dirings ( MZUSP, 2♀) ; São Paulo de Olivença, Nov.1960, Coll. Dirings ( MZUSP, 1♀ 1♂) ; Tabatinga , Apr.1950, J. C. M. Carvalho coll. ( MNRJ, 1♀) . Acre: Cruzeiro do Sul, 20.Feb.1973 ( UFRG, 1♂) . Paraíba: Santa Luzia , Sep.1956, C. Gonçalves coll. ( MNRJ, 1♀ 1♂) . Mato Grosso: Pôrto Velho, Rio Tapirapé , 30.Dec.1964, R. T. Lima coll. ( MZUSP, 2♂) . Minas Gerais: Paracatu , Jul.1960 ( MNRJ, 1♀) . São Paulo: Araçatuba , Oct.1961, Lane & Rabello coll. ( MZUSP, 1♀ 1♂) ; Pal- mital, 29.Nov.2001, J.J. Silva coll. ( UFRG, 1♀ 1♂) ; Morro Agudo , 20.Mar.1996, A.M. de Faria coll. ( MZUSP, 1♂) ; Piracicaba , Fev.2018, E. Martins coll. ( ESALQ, 3♀ 3♂) ; Ribeirão Preto , 29.Jan.1993, A.M. de Faria coll. ( MZUSP, 1♂) ; Jan.2006, A.M. de Faria coll. ( MZUSP, 1♀) ; Rio Grande do Sul: Porto Alegre , 11.Oct.1983, A. Mohr coll. ( UFRG, 1♀) ; Santa Maria , 10.May.1973, O. J. Lopes coll. ( UFRG, 1♂) ; 20.Nov.1973, N. Tresoldi coll. ( UFRG, 1♂) ; 16.Oct.1980, J. Mario coll. ( UFRG, 1♂) ; 26.Nov.1980, E. C. Costa coll. ( UFRG, 1♀) ; 10.Dec.1980, E. C. Costa coll. ( UFRG, 1♀) ; 01.Oct.1981, D. Link coll. ( UFRG, 1♂) ; Nov.1981, D. Link coll. ( UFRG, 1♂) ; 07.Dec.1981, D. Link & E. Costa coll. ( UFRG, 1♂) ; Oct.1982, D. Link coll. ( UFRG, 1♂) ; Nov. 1982, D. Link coll. ( UFRG, 1♀) ; 15.Oct.1984, D. Link & E. Costa coll. ( UFRG, 1♀) ; 18.Oct.1984, D. Link & E. Costa coll. ( UFRG, 1♂) ; Oct.1984, D. Link coll. ( UFRG, 1♀ 1♂) ; 15.Oct.1984, D. Link coll. ( UFRG, 1♂) ; 20.Apr.1987, D. Link coll. ( UFRG, 1♀ 1♂) ; Santa Vitória do Palmar, Estação Ecológica do Taim , 05.Feb.1981, J. Grazia coll. ( UFRG, 1♀) ; 23.Mar.-03.Apr.1981, J. Grazia coll. ( UFRG, 1♀) . PERU. Junín: Satipo , Dec.1936, P. Paprzyck coll. ( FIOC, 1♀) . BOLIVIA. Cochabamba: Cochabamba, 1949, Coll. Dirings ( MZUSP, 1♂) .

Distribution ( Fig. 7 ). Widely distributed in South America, with recorded localities including Venezuela, Brazil, Ecuador, Peru, Bolivia, Argentina and Uruguay. VENEZUELA. Amazonas: Mavaca, new record; Monagas: Jusepín, new record. BRAZIL. Acre: Cruzeiro do Sul, new record. Amapá: Porto Platon [ Da Silva et al. 2018]; Macapá, new record. Amazonas: Barcelos, new record; Benjamin Constant, new record; Presidente Figueiredo, [ Silva et al. 2012]; São Paulo de Olivença, new record; Tabatinga, new record. Pará: Belém, [ Da Silva et al. 2018]. Paraíba: Santa Luzia, new record. Mato Grosso: Pôrto Velho, Rio Tapirapé, new record. Minas Gerais: Paracatu, new record. São Paulo:Araçatuba, new record; Palmital, new record; Morro Agudo, new record; Piracicaba, new record; Ribeirão Preto, new record. Rio Grande do Sul: Porto Alegre, new record; Santa Maria, [ Link & Grazia 1987]; Santa Vitória do Palmar [Estação Ecológica do Taim], new record. ECUADOR. Guayas: Guayaquil, [ Kuhlgatz & Melichar 1903 — mentioned as Euschistus bifibulus var. guayaqulinus Kuhlgatz ]. PERU. Junín: Satipo, new record. ARGENTINA. Misiones: San Ignácio [ Berg 1878]; Chaco: National Park of Chaco, [ Dellapé et al. 2015]; Formosa: Formosa, [ Dellapé et al. 2015]. BOLIVIA. Cochabamba: Cochabamba, new record. URUGUAY (unknown locality) [ Ruffinelli & Pirán 1959].

Host plants. E. taurulus was recorded in fourteen species from seven plant families, including literature and new records from museum specimen label data: Apiaceae : Foeniculum vulgare (sweet fennel) [ Link & Grazia 1987]. Brassicaceae : Brassica napus (rapeseed) [ Link & Grazia 1987]; Brassica oleracea var. botrytis botrytis (cauliflower) new record; B. oleracea var. botrytis italica (broccoli) [ Silva et al. 2012]; Brassica oleracea var. acephala (kale) [ Link & Grazia 1987]. Fabaceae : L. culinaris (lentil) new record; Lupinus albus (white lupine) [considered natural host, since allows egg to adult development, Link & Grazia 1987]; Lupinus luteus (yellow lupine) new record; Lupinus perennis (sundial lupine) [ Link & Grazia 1987]; G. max (soybean), new record; Linaceae : Linum usitatissimum (common flax) [ Link & Grazia 1987]. Malvaceae : Sida sp. ( sida ), new record. Polygonaceae : Polygonum spp. (smartweed), new record. Solanaceae : N. tabacum (tobacco), new record.

DNA barcoding. We successfully obtained 658 bp region of COI for E. taurulus and for the species D. melacanthus as wel as D. furcatus . For E. heros , the first 39 bp were discarded due to low quality of the chromatogram, resulting in 619 bp fragment of COI. The sequences obtained were deposited in NCBI-GenBank database with the accession numbers: MN257051 – MN257054 . The genetic distance of COI barcode region of E. taurulus was from 0.2309 to D. furcatus , 0.2499 to D. melacanthus , and 0.2220 to E. heros .

Bionomics. Individuals of E. taurulus were able to complete development and reproduce under laboratory conditions, feeding on the natural diet offered ( Tab. 2 and 3 ). Most of the females were able to lay eggs, with preoviposition period (ca. 9 days) and fecundity of 132.25 eggs/female ( Tab. 2 ). Longevity of males was higher than females ( Tab. 2 ). Immature stages reached adulthood in about 35 days, with low viability/high mortality during egg stage and initial instars ( Tab. 3 ). Total mortality and development time for the 2 nd instar to adult was 54.72 % and 24.67 days, respectively ( Tab. 3 ). Sex ratio was 0.67 (females).

Figures

FIGURE 1 Stink bugs found in legume crops in Brazil, alive specimens. A: Adults of Euschistus taurulus, male (left) and female (right) in ventral view, showing color polymorphism; B: Similarity of adult females of Euschistus heros (left) and Dichelops melacanthus (right) to E. taurulus (middle); C and D: Adult female of E. taurulus; E: Adult female of E. heros; F: Adult male of D. melacanthus; G: Adult female of E. taurulus; H: Adult males of E. heros (left) and D. melacanthus (right). Photos: Fernando H. Iost Filho.

FIGURE 2. Adults of Euschistus taurulus Berg. A & C: Male in dorsal and ventral views, respectively; B & D: Female in dorsal and ventral views, respectively. Scale bar: 5 mm.

FIGURE 3. Pygophore of adult male Euschistus taurulus Berg. in dorsal (A), posterior (B), and ventral (C) view. dr, dorsal rim; par, paramere; slvr, superior layer of ventral rim; spdr, superior process of dorsal rim; vr, ventral rim. Scale bar: 1.0 mm.

FIGURE 4. Phallus (A–C) and paramere (D–G) of adult male Euschistus taurulus Berg. Dorsal (A), lateral (B), and ventral view (C) of phallus; Lateral inner (D), dorsal (E), ventral (F), and lateral outer (G) views of paramere. app, apical process of paramere; ba, basal apodeme; bpp, basal process of paramere; cj, conjunctiva; dsd, ductus seminis distalis; prph, processus phallotheca; vp, vesica process.

FIGURE 5. External genital plates of adult female Euschistus taurulus Berg. A & B: posteroventral and posterior views, respectively.

FIGURE 6. A–C. Internal genitalia of adult female Euschistus taurulus Berg. A: general aspect; B: magnification of genital plates region; C: magnification of spermatheca. aaf, anterior anular flange; cs, capsula seminalis; drd, ductus receptaculi distalis; drp, ductus receptaculi proximalis; gcIX, gonocoxite IX; laIX, laterotergite IX; paf, posterior anular flange; pi, pars intermedia- lis; rs, ring sclerites.

FIGURE 7. Occurrence of Euschistus taurulus Berg in South America (white dots: old records; black diamonds: new records). Dashed area: record with unknown locality. Arrows show the recorded hosts in the localities. Shades of grey show the Neotropical sub regions. BRS: Brazilian subregion; CSR: Chaco subregion; SATZ: South America transition zone. Biogeographical classification follows Morrone (2017).