Belminus santosmalletae (Hemiptera: Heteroptera: Reduviidae): New Species from Panama, with an Updated Key for Belminus Stål, 1859 Species

Simple Summary A new species of Belminus, discovered during the study of unidentified Triatominae specimens from the Hemiptera collection of the National Museum of Natural History, Smithsonian Institution, Washington DC, USA is described here. After comparison with previously described species, significant morphological and morphometric differences were observed, confirming the discovery of a new triatomine species, Belminus santosmalletae. Abstract Belminus santosmalletae, a new triatomine species, is described based on a specimen from Panama, deposited in the collection of the National Museum of Natural History (NMNH), Smithsonian Institution, Washington, DC, USA. Attempts failed to identify this specimen using the keys by Lent and Wygodzinsky (1979) and Sandoval et al. (2007). A comparison was made with specimens of Belminus Stål, 1859 specimens deposited at the Triatominae collection at the Oswaldo Cruz Institute (CTIOC), Rio de Janeiro, Brazil; and with previous descriptions of Belminus species. These comparisons showed the specimen represents a new species, described in the present paper. It differs from other species of the genus mainly by the grainy tegument, scarce pilosity along the body, and the number of tubercles observed on the pronotum.


Introduction
The subfamily Triatominae (Hemiptera: Reduviidae) comprises 153 extant and three fossil species assigned to five tribes [1][2][3][4] with all the extant species being considered potential Chagas disease vectors. The tribe Bolboderini has been considered a monophyletic group, and includes the genera Bolbodera Valdés, 1910; Belminus Stål, 1859; Parabelminus Lent, 1943; Microtriatoma Prosen and Martínez, 1952 [4] (Figure 1). The genus Belminus was described by Stål [5] based on a single species, Belminus rugulosus, from Colombia [6]. The group is well characterized and can be easily differentiated from other triatomines by the small total body length (8.5-12 mm); elongate and fusiform head; dorsoventrally compressed labium, with the first and second visible segments elongate and subequal in length and longer than the third segment; the presence of 6-7 small discal tubercles on the anterior lobe of pronotum and connexivum with a dorsal longitudinal ridge [7,8]. It is the most diverse genus of Bolboderini, with eight previously described valid species: Belminus corredori Galvão (Figure 2A-H).
During a study of the Hemiptera collection at National Museum of Natural History, Smithsonian Institution (NMNH), Smithsonian Institution, Washington DC, USA, a specimen belonging to the genus Belminus was found. Upon comparison with other specimens of the genus deposited in the Triatominae collection of the Oswaldo Cruz Institute (CTIOC), and with the descriptions of the other Belminus species, it was clear that such specimen represents a new species. Here, we describe Belminus santosmalletae sp. n. (Figure 3) based on this single female specimen.

Materials and Methods
Measurements and observations were made using a Dino-Lite Edge digital microscope. Dorsal habitus images and detailed photos were taken using the wide zoom microscope OlympusDSX100 camera. The following characters and terminology used for description based on Lent and Wygodzinsky [8] and Sandoval et al. [9].

Coloration
Overall color brown to yellowish-brown, with light and dark brown areas on the pronotum, hemelytra, connexivum, legs, and abdomen; with a few spots paler than the integument. Visible labial segments brown to yellowish-brown. Pronotum predominantly yellow with brown stripes and spots. Scutellum brown with the apex of scutellar process yellow. Femora with a subapical yellow ring. Corium yellow with three dark brown areas, one external, almost straight, the other internal. Membrane of hemelytron dark brown, veins darker with secondary venation within cells visible but not conspicuous. Connexival segments with transverse marks, anterior dark brown marks wider than posterior dark yellow marks ( Figure 3A,B).

Morphological Features
Female. Total length 11.45 mm, width of pronotum 2.75 mm, and width of abdomen 4.63 mm. The integument of the entire body was very grainy with short pilosity, except for the hemelytra.
Head. Elongated, fusiform, very granulose, three times as long as wide (1:0.31), slightly longer than pronotum (1:0.84). Clypeus truncated on the apex. The anteocular region was more than twice as long as postocular region (1:0.41). The postocular region was sub-circular, with sides which were convex and convergent posteriorly. The genae was compressed laterally, with the apices, considerably, surpassing anteclypeus. The external spinelike projection of the antenniferous tubercle was short, and barely extending beyond the base of the first antennal segment. Antennae were inserted apically, a third of the way through the anteocular, towards the postocular region. Antennal segments were missing, except in segment I. Eyes in the lateral view reached the level of the lower but not the upper surface of the head (Figure 4). The ratio between eye width and synthlipsis was 1:2.1. Ocelli were very small, not elevated, laterally oriented, and situated at the level of the integument. The visible labial segments of the first segment was longer than second, not reaching the anterior border of the eyes, while the third visible segment barely reached the anterior portion of the stridulatory sulcus; the length ratio of visible labial segments was 1:0.8:0.4 ( Figure 4). Pronotum. The width of the pronotum was slightly bigger than the length (1:0.83). The anterior lobe was narrow, granulose, with 7 + 7 conspicuous discal tubercles and 2 + 2 conspicuous lateral tubercles ( Figure 5), sides forming a conspicuous angle at the junction of the posterior lobe sides. The anterolateral processes were short, subtriangular, and rounded apically. Th posterior lobe was granulose with submedian carinae almost attaining the posterior border of the pronotum. The scutellum was triangular, with the apex of the scutellar process being long, subcylindrical, and not pointed apically. Further scutellum characters are not available for this specimen, as it was primarily pinned through the scutellum. Prosternum with 1 + 1 projections, lateral to the stridulatory sulcus. Legs. Short and stout. Femora were sulcate at the venter, and with 2 + 2 subapical denticles, one being distinctively larger ( Figure 6). Tibiae were slender and compressed laterally with short pilosity. The specimen was without tarsi. The hemelytra fell distinctly short of the apex of abdomen, with venations consistent with the genus description. Abdomen. Abdominal venter was flattened, and the connexivum was wide dorsally with a dorsal ridge. The spiracles were close but not adjacent to the connexival suture ( Figure 7). Remarks on the conditions of the specimen. The specimen was found without the last three antennal segments, without tarsi, and with scutellum damaged by the pin.
Diagnosis. According to the comparative morphology of the genus, Belminus, B. santosmalletae, it seems to be closer to the species B. ferroae and B. pittieri, and can be distinguished by the yellow rings on all femora (these rings can be found in B. herreri and B. laportei, but the morphology of the wing is distinct), grainer integument, scarce pilosity, lighter and larger yellow spots on the pronotum, 7 + 7 discal tubercles on the pronotum, rather than 6 + 6 and darker membrane, with little color contrast between the cells and veins.

Etymology
This species is dedicated to Dr. Jacenir dos Santos-Mallet, a Brazilian researcher at the Fundação Oswaldo Cruz, in Rio de Janeiro, Brazil. She has dedicated over 30 years to the research of tropical disease vectors.

Discussion and Conclusions
The genus Belminus currently comprises nine valid species, with distribution ranging through Central America, Colombia, Peru, Venezuela, and northern Brazil. The genus, previously thought to be exclusively sylvatic (arboreal), was recently found inside human dwellings in some locations in Colombia and Peru [10]. To this date, however, there has been no report of infection by Trypanosoma cruzi (Chagas 1909), the etiological agent of Chagas disease.
A unique feature within Triatominae is also the fact that Belminus species have been found feeding on other insects, especially cockroaches, showing a broader host preference. Wheeler and Pennak [11] considered Belminus corredori one of the 100 most interesting species discovered in this century, and according to Gil-Santana [4] this fact launched "an unprecedented focus on the uniqueness of the representatives of this tribe".
Belminus santosmalletae is the ninth species described to this understudied genus, and the second from Panama. In addition to the original descriptions [8,12,13], taxonomic knowledge on the genus is restricted to a few morphological papers reflecting the fact that this is the one of the least known triatomine genera. Herrer et al. [7] made the first descriptions of eggs and nymphs of first and fifth instars of B. peruvianus, and only after 31 years, Rocha et al. [14] described all instars of one Belminus species: B. herreri. They provide a complete description, as well as ontogenetic morphometrics of post-embryonic head development. Gil-Santana and Galvão [15] described the male genitalia of B. rugulosus and B. corredori and provided a discussion on previous data in the literature on male genitalia of other species. It is impossible to make inferences on the biology of B. santosmalletae because, like B. pittieri, the description is based on a single female specimen. Additionally, a search on GenBank shows a single sequence (GenBank access AJ421964) from this group, highlighting the lack of data available to further studies on integrative taxonomic approaches for the genus.