Research Article |
Corresponding author: Wanzhi Cai ( caiwz@cau.edu.cn ) Academic editor: Laurence Livermore
© 2021 Yisheng Zhao, Cleber Galvão, Wanzhi Cai.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Zhao Y, Galvão C, Cai W (2021) Rhodnius micki, a new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. ZooKeys 1012: 71-93. https://doi.org/10.3897/zookeys.1012.54779
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Rhodnius Stål, 1859 is the second largest genus of Triatominae after Triatoma Laporte, 1832, and includes several important Chagas vectors. Genitalia in Reduviidae are frequently used for species identification, but the current use of terminology for it is inconsistent in Triatominae. Here, Rhodnius micki sp. nov., is described from Bolivia and considered as belonging to the pictipes group based on its morphological characters and distribution. Detailed documentation of the genitalia of Rhodnius micki sp. nov. is provided with emphasis on its everted phallus, especially the endosomal sclerites, which are potentially useful as species-level diagnostic features in Rhodnius. To further verify the validity of this species, the head shapes and wing venation patterns of five species in Rhodnius are compared with morphometric analysis. After reviewing taxonomic and comparative morphology papers of assassin bugs, a vocabulary with a terminology of morphological characters, especially of external male genitalic characters, is assembled with the preferred terms and the synonyms listed. Establishing a consistent terminological framework will greatly facilitate future research on the homology of these structures across Triatominae and will ultimately contribute to our understanding of the evolution of these groups.
Comparative terminology, genitalia, geometric morphology, kissing bug, taxonomy
Triatominae are a subfamily within Reduviidae that is known for its hematophagous feeding habit (
The tribe Rhodniini currently contains two genera, Rhodnius Stål, 1859 (with 20 species) and Psammolestes Bergroth, 1911 (with three species) (Justi and Galvão et al. 2017;
The latest taxonomic revision of the entire genus was published approximately 40 years ago in the monograph on Triatominae by
Rhodnius is relatively easy to distinguish from other Triatominae genera because of its long head and coloration pattern but shows low non-genitalic morphological variability between species in the genus, which may account for the difficulties in species identification. The female external genitalia was described for most species of the subfamily (
When examining the specimens of Rhodnius, two specimens from Bolivia were distinctly different from any other species found. In this study, they are named Rhodnius micki sp. nov. and described. Male genitalia are important in identifying assassin bugs, especially for Rhodnius which has low non-genitalic morphological variability between species. Therefore, special emphasis is put on their everted phallus, allowing for detailed photographic documentation of the phallus, particularly the sclerites of the endosoma. The diagnosis of the new species takes advantage of qualitative morphological features including genitalic features, and of geometric morphometric approaches to better characterize head and forewing shapes. Combining morphometric characters with distribution, we propose that this new species should be classified in the pictipes group. We also provide a synopsis of genitalic terminology applied to Triatominae and offer preferred terms to facilitate future investigations into the homology of these structures across Triatominae and even Heteroptera.
Type specimens and an additional male specimen of R. robustus Larrousse, 1927 are deposited in The Natural History Museum (
Specimens of R. stali, R. pictipes, R. pallescens, and R. ecuadoriensis which were used for the geometric analysis came from colonies reared at Fundação Oswaldo Cruz (
After softening the abdomens of dried specimens with wet tissue, the pygophores were removed and soaked in 100% lactic acid overnight (Fig.
Process of dissection 1 soaking genitalia in 100% lactic acid overnight 2 boiling genitalia in 20% lactic acid solution for ~ 30 minutes 3–6 dissecting genitalia under microscope with forceps and blunted insect pin 4, 5 inserting the insect pin along the membrane of the endosoma and agitate the pin 6 using forceps to stretch the endosoma.
Because of the inconsistent use of terminology in Triatominae, after reviewing many taxonomic and comparative morphology papers of assassin bugs, the terminology adopted in this paper are listed in Table
Habitus images were obtained using a Canon EOS 7D and 60mm macro lens. Detail images of heads, pronota, and wings were obtained using a Microscope (Nikon SMZ18) with a Canon EOS 600D. Genital images were taken using an Olympus BX51 with a Canon EOS 450D. Images were stacked using the EOS Utility 2, and Helicon focus 5.3. Photographs were edited with Adobe Photoshop CS4, including adjustment of background color and cropping without modifying any characters. All the images were taken in the laboratory by the authors. The plate of male genitalia is that of the paratype.
In total, 42 specimens of five species, R. ecuadoriensis (ten specimens), R. pallescens (ten specimens), R. pictipes (ten specimens), R. stali (ten specimens), and R. micki sp. nov. (two specimens), were used in the analysis. and nine anatomical landmarks were extracted respectively on the heads and forewings. Thirteen landmarks of head (type II points, which combine geometric and biological or histological descriptions) (
Rhodnius prolixus Stål, 1859.
Bolivia: Santa Cruz, Saavedra, C.J. Pruett [leg.], 1 male holotype, 10.v.1989, 1 male paratype, 1.iii.1989 (NMHUK).
General coloration dark brown. Head relatively short, only slightly longer than the pronotum. Eyes small, width of the eye shorter than the synthlipsis. Central area of the anterior lobe of the pronotum conspicuously dark and its humeral angle of the posterior lobe relatively sharply curved. Legs brown. The median process of the pygophore long and bifid on the tip. The medial basal sclerite of the phallosoma with two straight and flat projections. One distal dorsal sclerite of the endosoma bifurcated, and its tip rounded and curved slightly inward.
Coloration. Body generally dark brown. Head with light median longitudinal stripe extending from the apex of clypeus to the posterior portion of ocelli; eyes blackish; middle of third segment and posterior half of forth segment yellow; a pair of black stripes on the dorsal surface of neck, half of lateral side and ventral side dark. Pronotum with a pair of submedian carinae and lateral margin yellow; concave areas on anterior lobe, especially the central area darkened; posterior lobe dark with scattered irregular small yellow spots. Scutellum dark with a yellow “Y”-shaped ridge; the tip of scutellar process white. Hemelytra generally brown and mottled; corium with small lightly colored spots; membrane with narrowly rimmed pale-yellow veins, area between veins with scattered light color spots. Legs mottled with yellow spots; tarsi yellowish (Fig.
Head. Elongated and granulose, almost 2.5 × as long as width across eyes (1:2.6–2.59), slightly longer than length of pronotum (1:1.17–1.21); apex of maxillary plate surpassing clypeus; anteocular region ~ 3 × as long as postocular region in length (1: 2.84–3.15); eyes small, width of eye in dorsal view shorter than synthlipsis (1:0.60); in lateral view, eyes far away from upper surface of head and approaching to lower surface; ratio of antennal segments 1:5.11–6.29:4.66–5.14:3.55–4.43; first labial segment proceeding toward antenniferous tubercle and second labial segment approaching to posterior margin of head. Ratio of labial segments 1:2.78–3.13:0.61–0.83. Thorax. Anterolateral angles triangle-like. Surface of pronotum granulose, length of posterior pronotal lobe ~ 2 × as that of anterior lobe (1:1.89–1.93); posterior pronotal lobe ~ 1.5 ×as wide as anterior lobe (1:1.52–1.74); median longitudinal furrow of anterior lobe deep on the median transverse furrow; humeral angles sharply curved relatively to other species of Rhodnius (Fig.
Pygophore and paramere of paratype of Rhodnius micki sp. nov. 12–14 pygophore 12 dorsal view 13 lateral view 14 ventral view 15, 16 paramere: 15 dorsal view 16 lateral view. Scale bars: 1.00 mm. Abbreviations: DSPr dorsal sclerites of pygophore MPPy Median process of pygophore TBPy Transverse bridge of pygophore.
Pallus 17–24 Rhodnius micki sp. nov. 25, 26 Rhodnius robustus 17–19 non-everted phallus 20–26 everted phallus 17, 20 dorsal side 18, 21 lateral side 19, 22 ventral side 23, 25 distal ventral sclerite of endosoma 24, 26 distal dorsal sclerite of endosoma. Scale bars: 1.00 mm (11–16); 0.50 mm (17–20). Abbreviations: BP basal plate TBBP transverse bridge of basal plate DPS dorsal phallothecal sclerite MBSPh medial basal sclerite of phallosoma LFPPh lateral flat-like prolongation of phallosoma VSPh ventral sclerite of phallosoma BPE basal plate extension DDSEn distal dorsal sclerite of endosoma DVSEn distal ventral sclerite of the endosoma AA articulatory apparatus Ph phallosoma En endosoma.
The species epithet is named in honor of Mr. Mick Webb (
[in mm, ♂ (n = 2)] Total length to tip of abdomen 17.20–17.33. Length of head (exclude neck) 3.21–3.55; width of head 1.40–1.43; length of anteocular 2.27–2.30; length of postocular 0.73–0.80; width of eye 0.40–0.44; length of synthlipsis 0.67–0.73. Length of antennal segments I–IV=0.35–0.45/2.20–2.30/1.80–2.10/1.55–1.60; length of visible labial segments I–III=0.80–0.90/2.50/0.60. Length of anterior lobe of pronotum 0.90–0.93; length of posterior pronotal lobe 1.70–1.93; width of anterior pronotal lobe 2.30–2.33; width of posterior pronotal lobe 4.00–4.15. Length of scutellum 1.70–1.75; width of scutellum 1.80–1.90; length of hemelytron 10.40–10.50. Width of abdomen 5.35–5.40. (all the former numbers are for holotype, except length of total, anteocular, second and fourth segment, and width of abdomen).
Rhodnius robustus Larrousse, 1927 (1♂, Brazil: Belém, Instituto Evandro Chagas, reared in lab, 20.II.1992) (
(Figs
Morphological variations of five Rhodnius species based on Principal Component Analysis. The 90% equal frequency ellipses containing approximately 90% of the data points are shown. The thin-plate splines show the average shape for each species, corresponding to the deformation of the landmarks compared with the origin (the average shape of all species) 27 head 28 fore wing.
It is relatively easy to distinguish this species from other Rhodnius species because of its relatively sharply curved humeral angles and unique color pattern. Rhodnius stali and R. pictipes are similar to R. micki sp. nov. because their heads are all relatively short, only slightly longer than their pronota, and their pronota have a defined transverse sulcus. However, the tibiae of R. micki sp. nov. are uniformly dark brown, the humeral angle is sharply curved (Fig.
Rhodnius micki sp nov. is known from Santa Cruz, Bolivia, where some species of pictipes group and prolixus group, i.e., R. stali, R. pictipes, and R. robustus are distributed (
Historically, the terminology of Triatominae, especially male genitalic terms, has developed at least partially in isolation from that of Reduviidae. A plethora of terms have been used for homologous genitalic structures, and in some cases different structures have used the same name. This inconsistency results in incompatible and sometimes misleading terminology for taxonomic descriptions and diagnoses. For example, some researchers have variously used the terms aedeagus, phallus, phallosoma, conjunctiva and phallothecal plate when describing the apical apart of the intromittent organ, and the sclerotized plate beneath the basal plate (
Preferred term (abbreviation) | Definition | Previously used terms | References |
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Articulatory apparatus (AA) | System of plates and apodemes for suspension of phallus and attachment of its motor muscles | Articulatory apparatus (Apb) (apt) |
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Phallobase |
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Basal plate (BP) | Paired major plates of articulatory apparatus | Basal plate (Plb) |
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Basal plate arm (bpa) |
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Basal arm |
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Basal plate extension (BPE) | Ventral sclerite arising from the basal plate | Basal plate extension (bpe) |
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Pedicel (ped) (pd) |
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Median (Medium) extension of the basal plate (EPlb) (MeBp) |
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Median basal plate |
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Plate extension (pext) |
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Distal dorsal sclerite of endosoma (DDSEn) | Paired or single sclerite on the tip of endosoma which is on the dorsal side of the distal ventral sclerite | Process of endosoma |
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Processes of endosoma 1 (PrEn 1) |
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Processes of endosoma 2 (PrEn 2) |
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Distal ventral sclerite of endosoma (DVSEn) | A single sclerite on the tip of endosoma which is on the ventral side of the distal ventral sclerite | Processes of endosoma |
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Processes of endosoma 1 (PrEn 1) |
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Processes of endosoma 2 (PrEn 2) |
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Dorsal phallothecal sclerite (DPS) | Sclerotized proximal part of phallosoma | Dorsal phallothecal sclerite (dps) |
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Phallosoma (Ph) |
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Dorsal phallotheca plate |
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Phallotheca plate |
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Dorsal sclerites of pygophore (DSPr) | Posterior dorsal sclerotization of pygophore | Dorsal sclerotization of genital opening, tergite 9 (t9) |
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Endosoma (En) | Distal portion of phallus which can be reverted | Endosoma |
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Lateral flap-like prolongation of phallosoma (LFPPh) | Paired of sclerite on the lateral side of phallosoma | Lateral flat-like prolongation of the phallosoma |
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Processes of the conjunctiva 1 (PrCj 1) |
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Processes of the conjunctiva |
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Mandibular plate | Laterad of clypeus and dorsad of maxillary plate | Mandibular plate |
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Jugum |
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Maxillary pate | Ventral to mandibular plate | Maxillary plate |
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Gena (ge) |
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Medial basal sclerite of phallosoma (MBSPh) | Basal part of a phallosoma, often sclerotized | Vesica (V) |
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Median distal process |
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Median process of endosoma |
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Central sclerite of endosoma (cs) |
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Median basal sclerotization (mbs) |
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Processes of conjunctiva 2 |
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Dorsobasal large sclerite |
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Median process of pygophore (MPPy) | Median process of (the) pygophore (PrP) |
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Median pygophore process |
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Phallosoma (Ph) | Proximal portion of phallus, between basal plate and endosoma. | Phallosoma |
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Conjunctive |
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Phallus (P) | Intromittent organ inside the pygophore | Phallus (Ph) (P) |
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Aedeagus |
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Struts | Paired sclerites on the ventral side of dorsal phallothecal sclerite | Struts (str) |
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Phallosoma support (Sph) |
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Struts of phallus |
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Synthlipsis | Minimum interocular distance | Synthlipsis |
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Interocular space |
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Interocular region |
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Transverse bridge of basal plate (TBBP) | Connection between two basal plate | Basal plate; Bridge (bpb) |
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Basal bridge (PB) |
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Transverse bridge of pygophore (TBPy) | Anterior dorsal sclerotization of pygophore | Transverse bridge of the pygophore (br) |
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Ventral sclerite of phallosoma (VSPh) | Paired of sclerites on the ventral side of phallosoma | Processes of the conjunctiva 2 (PrCj 2) |
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Processes of the conjunctiva (PrCj) |
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Processes of the conjunctiva 3 (PrCj 3) |
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We are grateful to Christiane Weirauch, her lab members, and Dimitri Forero for kindly reviewing the manuscript and greatly improving the final version. Special thanks to Carolina Dale for offering photos and kindly reviewing the manuscript. This research is financially supported by the National Natural Science Foundation of China (Nos. 31730086, 31772498).
TPS file of landmarks of R. ecuadoriensis
Data type: measurement
Explanation note: This TPS file contains the landmark cordinates of R. ecuadoriensis.
TPS file of landmarks of R. micki
Data type: measurement
Explanation note: This TPS file contains the landmark cordinates of R. micki.
TPS file of landmarks of R. pallescens
Data type: measurement
Explanation note: This TPS file contains the landmark cordinates of R. pallescens.
TPS file of landmarks of R. pictipes
Data type: measurement
Explanation note: This TPS file contains the landmark cordinates of R. pictipes.
TPS file of landmarks of R. stali
Data type: measurement
Explanation note: This TPS file contains the landmark cordinates of R. stali.