Next Article in Journal
A New Sternorrhynchan Genus and Species from the Triassic Period of China That Is Likely Related to Protopsyllidioid (Insecta, Hemiptera)
Next Article in Special Issue
Mitogenomics of Chinch Bugs from China and Implications for Its Coevolutionary Relationship with Grasses
Previous Article in Journal
The Effect of Substrate on the Nutrient Content and Fatty Acid Composition of Edible Insects
Previous Article in Special Issue
The King’s Lace Bug Recaredus rex Distant, 1909 (Hemiptera: Heteroptera: Tingidae): Systematic Position, First Palaearctic and Afrotropical Records, and Ecological Niche Modelling
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 13
Issue 7
10.3390/insects13070591
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Triatoma guazu Lent and Wygodzinsky Is a Junior Synonym of Triatoma williami Galvão, Souza and Lima

by
João Paulo Sales Oliveira Correia
1,
Hélcio Reinaldo Gil-Santana
2,
Carolina Dale
3 and
Cleber Galvão
1,*,†
1
Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil 4365, Rio de Janeiro 21040-900, Brazil
2
Laboratório de Diptera, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil 4365, Rio de Janeiro 21040-360, Brazil
3
Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil 4365, Rio de Janeiro 21040-900, Brazil
*
Author to whom correspondence should be addressed.
†
Zoobank number (synonymization): urn:lsid:zoobank.org:act:4745CE55-7F07-43F7-8AA9-3F0E013AE1BE.
Insects 2022, 13(7), 591; https://0-doi-org.brum.beds.ac.uk/10.3390/insects13070591
Submission received: 3 May 2022 / Revised: 23 June 2022 / Accepted: 24 June 2022 / Published: 28 June 2022
(This article belongs to the Special Issue Systematics, Phylogeny, Evolution and Diversity of True Bugs (Hemiptera: Heteroptera))
Browse Figures
Versions Notes

Abstract

:

Simple Summary

Triatomines are blood-sucking insects, potential vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. Triatoma guazu and Triatoma williami are phylogenetically very close and occur in sympatry. Morphologic, morphometric, and genetic analyses were performed to discuss the taxonomic status of these species. Morphometric and molecular data do not show diagnostic characteristics between species, whereas their different patterns of connexival spots were considered a phenotypic polymorphism, common in triatomines. These results suggest T. guazu as a junior synonym of T. williami. Therefore, the synonym between these species is formally proposed here.

Abstract

Triatoma guazu Lent and Wygodzinsky and Triatoma williami Galvão, Souza, and Lima (Hemiptera: Triatominae) are found in human dwellings and are potential vectors of the protozoan Trypanosoma cruzi, the etiological agent of Chagas disease. Triatoma guazu was described based solely on a single female specimen, from the municipality of Villarica, Guairá Department, Paraguay, and posteriorly, a male from Barra do Garças, Mato Grosso, Brazil was described and designated as the allotype of this species. Triatoma williami is found in the central-west of Brazil between Goiás, Mato Grosso, and Mato Grosso do Sul. However, the taxonomic “status” of these species is questioned. Previous studies indicate the lack of isoenzymatic diagnostic loci, morphometric similarity, low genetic divergence, and close evolutionary relationship of these species. In this study, we compared the morphology, morphometry, and mitochondrial DNA fragments of the populations of the two species. The morphological diagnostic characteristic among these species is the difference in the connexivum spots pattern, which has been recognized as a phenotypic variation that exists among populations resulting from ecological diversity. Furthermore, our analysis also revealed the morphometric similarity and low genetic divergence between these species. Therefore, in the present paper, we formally propose T. guazu as a junior synonym of T. williami.

1. Introduction

The subfamily Triatominae (Jeannel, 1919) includes 155 extant and three fossil species distributed in 18 genera and five tribes [1,2,3,4]. Among the triatomine genera, Triatoma Laporte, 1832 has the highest diversity, with 82 species, of which 39 occur in Brazil [5,6,7,8].
Triatoma williami Galvão, Souza, and Lima, 1965 was described based on specimens from the municipality of Piranhas, Goiás state, in honor of Dr. William Barbosa for his efforts to create a research institute in the region (Instituto de Patologia Tropical) [9]. This species also occurs in other states of the Cerrado, the tropical savanna ecoregion located in central-west Brazil, such as Mato Grosso and Mato Grosso do Sul [7,9,10]. Recently, Martins et al. [10] found, for the first time, domiciliary colonies of T. williami in an urban area of Barra do Garças, Mato Grosso, Brazil. Its original description is short and poorly detailed, highlighting the black spots on intersegmental sutures in the dorsal connexivum, similar to Triatoma sordida (Stål, 1859) and Triatoma guasayana Wygodzinsky and Abalos, 1949 [9,11,12]. According to Lent and Wygodzinsky [13], T. williami differs from these two species in the following characters: pronotum, scutellum, and legs coloration; head length; length of the anteocular region in relation to the post-ocular; eye size; and length and shape of the scutellum.
Triatoma guazu Lent and Wygodzinsky, 1979 was described based on a single female specimen, found in a human dwelling, in the municipality of Villarica, Guairá Department, Paraguay, located in the Humid Chaco ecoregion at ~1000 km from Goiás, Brazil. Male specimens were described only ~20 years later based on bugs collected in the municipality of Barra do Garças, Mato Grosso, Brazil, located 75 km apart from the type locality of T. williami in the Cerrado [7,13,14]. According to Lent and Wygodzinsky [13], T. guazu resembles Triatoma oliveirai (Neiva, Pinto and Lent, 1939), “This species resembles T. oliveirai, but differs from the latter by many characters, such as the short rostral setae, the larger eyes and ocelli, the unicolorous pronotum, the horizontal scutellar process, the no abbreviated hemelytra, and the quite different shape of the ninth urotergite”.
Noireau et al. [15] observed a great similarity between sympatric specimens of T. williami and T. guazu, collected in the male type locality of the latter species, when analyzing 18 isoenzyme loci and four measurements of each, the head and thorax structures through traditional morphometry. In regard to the genitalia of the species studied here, Lent et al. [14] described the male genitalia of T. guazu and Teves et al. [16] described the female genitalia of T. williami. The former authors illustrated their description with drawings, while the latter with Scanning Electron Microscopy images.
Their results were corroborated by subsequent molecular studies with the 12S [17] and 16S [17,18,19,20,21], and 18S and 28S subunits of the mitochondrial and cytoplasmatic ribosomal RNA (SSU rRNA), respectively [20,22], as well as the mitochondrial cytochrome oxidases I (COI) [19,20,21] and II (COII) [20] and Cytochrome B (CytB) [19,20]. All samples analyzed so far were from the municipality of Barra do Garças, Mato Grosso, Brazil, except the specimens used in two studies [18,20], which were from unknown locations. Chromosomal analysis indicated a similar number and the morphology of T. guazu and T. williami chromosomes [23], and fluorescent in situ hybridization (FISH) showed evidence that both species are concentrated in 45S rDNA clusters in an autosomal pair, and not in sexual chromosomes, such as observed in other Triatoma species such as T. maculata and T. matogrossensis [24]. Reis et al. [25], however, observed that the two species can be differentiated by the number of peripheral heteropyknotic filaments during spermiogenesis (a single filament in T. williami and two filaments in T. guazu). In the present study, we review the taxonomic status of T. williami and T. guazu through the analysis of geometric morphometry of head capsules, genetic divergence of publicly available rRNA and mtDNA sequences, and morphological analysis.

2. Materials and Methods

Morphological analysis. We examined 44 individuals (12 Triatoma guazu and 32 T. williami) including the type specimens, deposited in Coleção Entomológica do Instituto Butantan (CEIB), São Paulo, Brazil, and Coleção de Triatomíneos do Instituto Oswaldo Cruz (CTIOC), Fiocruz, Rio de Janeiro, Brazil (see examined material in Supplemental Data S1, Figure 1, Figure 2, Figure 3, Figure 4 and Figure 5). Photographs and morphological analysis were taken with a Leica DMC 2900 camera attached to a Leica M205C stereomicroscope (Figure 1, Figure 4, Figure 5, Figure 6 and Figure 7). Images were edited using Adobe Photoshop 7.0.1. General morphological terminology mainly follows original descriptions of the species [9,12] and previous studies on Triatominae (e.g., Lent and Wygodzinsky [13]).
Geometric morphometrics. The adult head capsule was analyzed from 12 specimens of T. guazu (from Mato Grosso State) and 20 of T. williami (from the States of Goiás, Mato Grosso and Mato Grosso do Sul), in addition to the outgroup consisting of 20 specimens of T. matogrossensis (from Mato Grosso State) and three specimens of T. oliveirai (from the Rio Grande do Sul State) (see examined material in Supplemental Data S1, Figure 1). The head was photographed using a digital camera Nikon coolpix 990, and the landmark coordinates were recorded with TpsDig version v. 2.05 (New York, United States) [26] to achieve a better definition of the head capsule conformation of the specimens [26] (Figure 6). Landmarks were superimposed to Generalized Procrustes Analysis in TPsRelw 1.53 [27,28,29,30]. This method allows the calculation of shape variables among taxa after alignment of the landmarks (to ensure homology). The multivariate differences were evaluated by the Lambda test of Wilks. The scores matrix was examined by Canonical Variate Analysis (CVA) to plot and observe the position of each specimen on the “Shape Discriminant Space”. The observed average distances were used to analyze the relationship among the species through the reconstruction of an UPGMA dendrogram. All analyses were executed in JMP 3.2.6 (SAS Institute, Cary, NC, USA).
Analysis of male genitalia. The dissections of a male genitalia of a specimen identified as T. williami were made by first removing the pygophore from the abdomen with a pair of forceps and then clearing it in 20% NaOH solution for 24 h. The dissected structures were studied and photographed in glycerol (see the label of the analyzed specimen at Data S1). The photographs were obtained using a digital camera (Sony DSC-W830, Budapest, Hungary). Images were edited using Adobe Photoshop CS6.
In relation to the male genitalia portions, the terminology used here follows mostly Lent and Wygodzinsky [13]. However, “vesica” as recognized by Lent and Wygodzinsky [13] and Lent et al. [14] has been considered to be absent in reduviids. The assumed equivalent structure in reduviids is a somewhat sclerotized appendage of the phallosoma or the endosoma [31], but not the homologous vesica that occurs in other heteropterans such as Pentatomomorpha [32]. Thus, this term is not used here for the median process of endosoma, which is named as such.
Scanning Electron Microscopy. The samples of T. guazu examined were obtained from colonies maintained by the Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil (see the label of the analyzed specimens at Data S1). The females were washed with detergent and subsequently metallized. Then, cross-sections were performed between abdominal tergites II and III. The genitals were dehydrated in an alcoholic series on silica and fixed in aluminum stubs. The genitalia were plated on the Rudolf Barth Plataforma de Microscopia Eletrônica de Varredura (IOC) and were photographed using the microscopes JEOL JSM-6390LV.
Molecular analysis. A total of 64 DNA sequences of Triatoma brasiliensis Neiva, 1911 [33], T. guazu, Triatoma jatai Gonçalves, Teves-Neves, Santos-Mallet, Carbajal-de-la-Fuente, and Lopes, 2013 [34], T. matogrossensis and T. williami were retrieved from GenBank [35] for 16S, COI, COII and CytB. Triatoma oliveirai is a rare species and does not have any DNA sequence publicly available. DNA sequence data were aligned separately for each marker using ClustalW [36] implemented in the MEGA-X [37]. MEGA-X was used then to identify the number of variable sites. A pairwise divergence calculation was performed in the MEGA-X program, using the bootstrap method of resampling with 500 replications and the Kimura-2-parameters as the substitution model [38]. Species comparisons were performed by calculating the difference between inter and intraspecific genetic distances. Here, we considered as ‘true’ species those which interspecific divergences were above intraspecific divergences observed for Triatoma species.

3. Results

In the present study, we highlight new diagnostic characters among these species, in addition to those mentioned by Lent and Wygodzinsky [13]: length of the anteocular region in relation to the postocular region; eye position in relation to the ventral surface of the head; length of the submedian carina of the pronotum; and absence of spongy fossa (see Supplemental Table S2). The morphological data did not reveal diagnostic characters to differentiate between T. guazu and T. williami, except for the connexivum spots pattern (see Supplemental Data S2). Based on the original description, both species in the dorsal view have spots on the intersegmental sutures of the connexivum, which are dark and wide in T. guazu, and dark and narrow in T. williami. However, the present analysis evidenced a continuous variation, within the populations of the two species, from narrow to wide dark spots (Figure 7).
The discriminant analysis of the head capsule shape showed that specimens originally designated as T. guazu are not distinct from T. williami specimens (Figure 8A,B).
The male genitalia of a specimen identified as T. williami (Figure 9A–E) revealed the same characteristics as those described to T. guazu [14]. It is noteworthy that the mentioned uniformity was recorded in the structures which are usually more important to diagnosis or to distinguish species of Triatoma, such as the phallic portions (articulatory apparatus, pedicel, phallothecal plate, including the struts and the processes of the endosoma) (Figure 9A–E), which presented the same shape, dimensions, and peculiarities in T. williami as described in T. guazu by Lent et al. [14].
In the same way, the character set of the female genitalia of T. guazu did not reveal differences when compared to T. williami, genitalia described by Teves et al. [17] (Figure 10A–C). It was not possible to compare the genitalia in posterior view, because there is no description for T. williami. However, in posterior view, we observed the following characters for T. guazu: appendix not visible; gonocoxite VIII elongated and slightly wider; abdominal segments IX and X slightly downward and as wide as long; and tergite IX posterior margin clearly separated from tergite X.
A total of 56 sequences were selected and analyzed (Table 1): 16S gene fragments (20 sequences, 356 bp, 48 variable sites); COI (16 sequences, 201 bp, 52 variable sites); COII (eight sequences, 284 bp, and 79 variable sites); and CytB (12 sequences, 313 bp, and 91 variable sites). In general, those markers provide strong evidence that T. guazu and T. williami are the same species. Pairwise comparisons revealed that sequences of these two species diverge less than 2% for all markers analyzed (16S = 0.2%, COI = 1.5%, COII = 1.7%, CytB = 0.9%). These levels of divergence were below some intraspecific comparisons in T. matogrossensis (see Table 2, Table 3, Table 4 and Table 5; see Supplemental Table S2A–D) and T. brasiliensis (see Table 5; Table S2A). A similar pattern was found for COII and CytB pairwise divergences, which T. guazu and T. williami diverged 1.7% and 0.9%, respectively, and intraspecific divergences within T. matogrossensis reached up to 3.2% in COII sequences, and 1.2% in intraspecific divergences within T. brasiliensis CytB sequences.

4. Discussion

Lent and Wygodzinsky [13] considered T. oliveirai to be the closet taxon of T. guazu, because they have connexival spots in a similar pattern. In contrast, our morphological review confirms that T. guazu and T. oliveirai are not a closely related species.
In contrast, the low genetic divergence, lack of morphological diagnostic characters, and low morphometric distinction observed between T. guazu and T. williami corroborate previous studies which stated that they are very similar taxa [14,15,16,17,18,19,20,21,22]. Additionally, the variation in the spots pattern in the connexivum is compatible with phenotypic variations between populations of the same species, possibly a consequence of different ecological characteristics, not standing as a feature to consider them as a separate species [14,39].
The close phylogenetic relationship between T. guazu and T. williami had already been addressed in previous studies [15,19,20,21,22], being confirmed in phylogenetic reconstructions with high node support. Almeida et al. [40] reported low genetic divergence for species from southern Brazil, which may be the result of recent speciation events. Previous studies used 16S, COI, COII, and CytB, with fragments between 200 and 300 bp, to separate species from Triatoma brasiliensis [41], Triatoma matogrossensis [19] and Triatoma rubrovaria subcomplexes [40], highlighting the effectiveness of our approach.
Populations of T. guazu and T. williami occur in the same municipality of Barra do Garças and their biology remains unknown. These sympatric populations show chromatic variations, but chromatic differences provide weak evidence to support distinct species. Triatoma infestans var. melanosoma Lent, Jurberg, Galvão, and Carcavallo, 1994 [42] and Triatoma infestans sensu stricto (Klug, 1834) [43] have sympatric populations, exhibit different color patterns and are the same species [39,44]. Conversely, individuals from different populations of Triatoma rubrovaria (Blanchard, 1843) [45] are polychromatic [13,46,47]. Indeed, Dale et al. [47] observed 16 different chromatic patterns in the collar, pronotum, and connexivum of this species, questioning the validity of these variations as diagnostic characters to designate new species.
Despite the chromatic patterns, which seems to be a continuous variation, the distinct number of heteropyknotic filaments in spermatogenesis is the only character to our knowledge that differentiate T. guazu from T. williami [25,48]. Perhaps both phenotypes are present in the two species and more research involving a better sampling strategy with sympatric and allopatric populations could shed light on this subject. We also emphasize the importance of population genetics studies to identify the presence (or the lack of) barriers to the gene flow of specimens with different chromatic patterns. So far, morphological traits, traditional and geometric morphometry, isozyme and DNA sequencing data prove that T. guazu is a junior synonym of T. williami.

5. Conclusions

Finally, we emphasize the importance of population genetics studies to identify the presence (or the lack of) barriers to the gene flow of specimens with different chromatic patterns. So far, morphological traits, traditional and geometric morphometry, comparison of genitalia in SEM, isozyme and DNA sequencing data prove that T. guazu is a junior synonym of T. williami.
Taxonomy
Order Hemiptera
Suborder Heteroptera
Family Reduviidae
Subfamily Triatominae
Tribe Triatomini
Genus Triatoma Laporte, 1832
Triatoma williami Galvão, Souza, and Lima, 1965
Triatoma guazu Lent and Wygodzinsky, 1979, syn. nov.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/insects13070591/s1, Data S1: Examined material of the studied species; Data S2: T. guazu and T. williami character set; Table S1: Diagnostic character sets between T. guazu and T. oliveirai; Table S2: Estimative of pairwise divergences between sequences of the studied species for 16S, COI, COII and CytB.

Author Contributions

Conceptualization, J.P.S.O.C., H.R.G.-S. and C.G.; methodology, J.P.S.O.C., H.R.G.-S. and C.D.; formal analysis, J.P.S.O.C., H.R.G.-S., C.D. and C.G.; investigation, J.P.S.O.C., H.R.G.-S., C.D. and C.G.; writing—original draft preparation, J.P.S.O.C.; writing—review and editing, J.P.S.O.C., H.R.G.-S., C.D. and C.G.; funding acquisition, C.G. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Grant code 001 and Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brazil (CNPq)—Grant code 305182/2019-6.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analyzed in this study. This data can be found here: [http://0-www-ncbi-nlm-nih-gov.brum.beds.ac.uk/genbank/ (accessed on 20 June 2022) access codes are found in Table 1].

Acknowledgments

We thank Flávia Virgino, curator of the Entomological Collection/Butantan, for support and unrestricted access to the collection, Jader Oliveira for the photographs of the Triatoma williami types of the Entomological Collection/Butantan, Jacenir Reis dos Santos Mallet for the valuable work on the scanning electron microscopy platforms, Lucas Bonato Mosmann for the support in the genetic analysis and Fernanda Firmino for technical support in the Triatomine Collection of the Instituto Oswaldo Cruz.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Jeannel, R. Insectes Hemipteres, iii. Henicocephalidae et Reduviidae. In Voyage Alluaud et R. Jeannel en Afrique orientale (1911–1912); Résultats Scientifiques: Paris, France, 1919; Volume 3, pp. 131–314. [Google Scholar]
  2. Galvão, C. Taxonomia dos Vetores da Doença de Chagas da Forma à Molécula, quase três séculos de história. In Atualidades em Medicina Tropical no Brazil: Vetores, 1st ed.; Oliveira, J., Chaboli, K., Aranha, L., Meneguetti, D., Eds.; Stricto Sensu: Rio Branco, Brazil, 2020; pp. 9–37. Available online: https://sseditora.com.br/wp-content/uploads/Atualidades-em-Medicina-Tropical-no-Brasil-Vetores.pdf (accessed on 6 April 2022).
  3. Zhao, Y.; Galvão, C.; Cai, W. Rhodnius micki, a new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. Zookeys 2021, 93, 71–93. [Google Scholar] [CrossRef] [PubMed]
  4. Gil-Santana, H.R.; Chavez, T.; Pita, S.; Panzera, F.; Galvão, C. Panstrongylus noireaui, a remarkable new species of Triatominae (Hemiptera, Reduviidae) from Bolivia. Zookeys 2022, in press. [Google Scholar] [CrossRef]
  5. Laporte, F.L. Essai d’une classification systematique de l’ordre des Hemipteres (Hemipteres Heteropteres, Latr.). Mag. Zool. 1832, 2, 51–55. [Google Scholar]
  6. Dale, C.; Justi, S.A.; Galvão, C. Belminus santosmalletae (Hemiptera: Heteroptera: Reduviidae): New Species from Panama, with an Updated Key for Belminus Stål, 1859 Species. Insects 2021, 12, 686. [Google Scholar] [CrossRef] [PubMed]
  7. Galvão, C.; Gurgel-Gonçalves, R. Vetores conhecidos no Brasil. In Vetores da Doença de Chagas no Brasil, 1st ed.; Galvão, C., Ed.; Sociedade brasileira de Zoologia: Curitiba, Brasil, 2015; Volume 1, pp. 88–170. [Google Scholar]
  8. Mendonça, V.J.; Alevi, K.C.C.; Pinotti, H.; Gurgel-Gonçalves, R.; Pita, S.; Guerra, A.L.; Panzera, F.; Araújo, R.F.; Azeredo-Oliveira, M.T.V.; Rosa, J.A. Revalidation of Triatoma bahiensis Sherlock & Serafim, 1967 (Hemiptera: Reduviidae) and phylogeny of the T. brasiliensis species complex. Zootaxa 2016, 2, 239–254. [Google Scholar] [CrossRef]
  9. Galvão, A.B.; da Silva e Souza, H.; Lima, R.R. Triatoma williami n. sp. (Hemiptera: Triatominae). Rev. Bras. Malariol. Doenças Trop. 1965, 17, 363–366. [Google Scholar]
  10. Martins, M.F.; Moraes, S.C.; Oliveira, J.; Santos, J.C.; Santos-Silva, L.K.; Galvão, C. Triatoma williami in intradomiciliary environments of urban areas in Mato Grosso State Brazil: Domiciliation process of a wild species? Infect. Dis. Poverty 2022, 11, 18. [Google Scholar] [CrossRef]
  11. Stål, C. Monographie der Gattung Conorhinus und Verwandten. Berl. Entomol. Zeitschriff 1859, 3, 99–117. [Google Scholar] [CrossRef]
  12. Wygodzinsky, P.; Abalos, J.W. Triatoma guasayana sp. n. (Triatominae, Reduviidae, Hemiptera) (Nota previa). Sem. Médica 1949, 56, 2. [Google Scholar]
  13. Lent, H.; Wygodzinsky, P. Revision of the Triatominae (Hemiptera, Reduviidae) and Their Significance as Vectors of Chagas Disease, 1st ed.; American Museum of Natural History: New York, NY, USA, 1979; pp. 1–408. [Google Scholar]
  14. Lent, H.; Jurberg, J.; Galvão, C. Descrição do Alótipo (Macho) de Triatoma guazu Lent & Wygodzinsky, 1979 Proveniente do Estado do Mato Grosso, Brasil (Hemiptera, Reduviidae). Memórias Inst. Oswaldo Cruz 1996, 91, 313–315. [Google Scholar]
  15. Noireau, F.; Santos, S.M.; Gumiel, M.; Dujardin, J.-P.; Soares, M.S.; Carcavallo, R.U.; Galvão, C.; Jurberg, J. Phylogenetic relationships within the oliveirai complex (Hemiptera: Reduviidae: Triatominae). Infect. Genet. Evol. 2002, 2, 11–17. [Google Scholar] [CrossRef]
  16. Teves, S.C.; Gonçalves, T.C.M.; Freitas, S.P.C.; Lopes, C.M.; Carbajal-de-la-Fuente, A.L.; Santos-Mallet, J.R. External female genitalia of Triatoma jatai, Triatoma costalimai and Triatoma williami (Hemiptera: Reduviidae: Triatominae). Parasites Vectors 2020, 13, 538–544. [Google Scholar] [CrossRef]
  17. Sainz, A.C.; Mauro, L.V.; Moriyama, N.E.; García, B. Phylogeny of triatomine vectors of Trypanosoma cruzi suggested by mitochondrial DNA sequences. Genetica 2004, 121, 229–240. [Google Scholar] [CrossRef] [PubMed]
  18. Hypša, V.; Tietz, D.F.; Zrzavý, J.; Rego, R.O.M.; Galvão, C.; Jurberg, J. Phylogeny and biogeography of Triatomine (Hemiptera: Reduviidae): Molecular evidence of a new world origin of the Asiatic clade. Mol. Phylogenetics Evol. 2002, 23, 447–457. [Google Scholar] [CrossRef]
  19. Gardim, S.; Rocha, C.S.; Almeida, C.E.; Takiya, D.M.; Silva, M.T.A.; Ambrósio, D.L.; Cicarelli, R.M.B.; Rosa, J.A. Evolutionary relationships of the Triatoma matogrossensis subcomplex, the endemic Triatoma in Central-Western Brazil, based on mitochondrial DNA sequences. Am. J. Trop. Med. Hyg. 2013, 89, 766–774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Justi, S.A.; Russo, C.A.M.; Santos-Mallet, J.R.; Obara, M.T.; Galvão, C. Molecular phylogeny of Triatomini (Hemiptera: Reduviidae: Triatominae). Parasites Vectors 2014, 7, 149–161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. Teves, S.C.; Gardim, S.; Carbajal de la Fuente, A.L.; Lopes, C.M.; Monte Gonçalves, T.C.; dos Santos Mallet, J.R.; da Rosa, J.A.; Almeida, C.E. Mitochondrial genes reveal Triatoma jatai as a sister to Triatoma costalimai (Reduviidae: Triatominae). Am. J. Trop. Med. Hyg. 2016, 94, 686–688. [Google Scholar] [CrossRef] [Green Version]
  22. Kieran, T.J.; Gordon, E.R.L.; Zaldívar-Riverón, A.; Ibarra-Cerdeña, C.N.; Glenn, T.; Weirauch, C. Ultraconserved elements reconstruct the evolution of Chagas disease vectoring kissing bugs (Reduviidae: Triatominae). Syst. Entomol. 2021, 46, 725–740. [Google Scholar] [CrossRef]
  23. Alevi, K.C.C.; Reis, Y.V.; Mendonça, V.J.; Rosa, J.A.; Azeredo Oliveira, M.T.V. Classical cytotaxonomy the Matogrossensis subcomplex (Hemiptera, Triatominae). Invertebr. Reprod. Dev. 2014, in press. [Google Scholar]
  24. Pita, S.; Lorite, P.; Nattero, J.; Galvão, C.; Alevi, K.C.C.; Teves, S.C.; Azeredo-Oliveira, M.T.V.; Panzera, F. New arrangements on several species subcomplexes of Triatoma genus based on the chromosomal position of ribosomal genes (Hemiptera–Triatominae). Infect. Genet. Evol. 2016, 43, 225–231. [Google Scholar] [CrossRef] [Green Version]
  25. Reis, Y.V.; Alevi, K.C.C.; Rosa, J.A.; Azeredo-Oliveira, M.T.V. Espermiogênese como ferramenta citotaxonômica para diferenciar Triatoma guazu e T. williami, espécies vetoras da doença de Chagas. Rev. Ciências Farm. Básica Apl. 2015, 36, 293–296. [Google Scholar]
  26. Rohlf, F.J. TpsDig, Version 2.1.1. Department of Ecology and Evolution, State University of New York: Stony Brook, NY, USA. Available online: http://en.freedownloadmanager.org/Windows-PC/tpsDig2.html (accessed on 16 January 2022).
  27. Dujardin, J.-P. Morphometrics applied to medical entomology. Infect. Genet. Evol. 2008, 8, 875–890. [Google Scholar] [CrossRef] [PubMed]
  28. Rohlf, F.J. Rotational fit (Procrustes) methods. In Proceedings of the Michigan Morphometrics Workshop, 2nd ed.; Rohlf, F.J., Bookstein, F.L., Eds.; University of Michigan Museum of Zoology: Ann Arbor, MI, USA, 1990; Volume 2, pp. 227–236. [Google Scholar]
  29. Rohlf, F.J.; Marcus, L.F. A revolution morphometrics. Trends Ecol. Evol. 1993, 8, 129–132. [Google Scholar] [CrossRef]
  30. Zelditch, M.L.; Swiderski, D.L.; Sheets, H.D.; Fink, W.L. Geometric Morphometrics for Biologists: A Primer; Elsevier: Amsterdam, The Netherlands, 2004; pp. 1–443. [Google Scholar] [CrossRef]
  31. Forero, D.; Weirauch, C. Comparative genitalic morphology in the New World resin bugs Apiomerini (Hemiptera, Heteroptera, Reduviidae, Harpactorinae). Dtsch. Entomol. Z. 2012, 59, 5–41. [Google Scholar]
  32. Rédei, D.; Tsai, J.-F. The assassin bug subfamilies Centrocnemidinae and Holoptilinae in Taiwan (Hemiptera: Heteroptera: Reduviidae). Acta Entomol. Musei Natl. Pragae 2012, 51, 411–442. [Google Scholar]
  33. Neiva, A. Contribuição para o estudo dos hematophagos brasileiros e descrição de uma nova espécie de Triatoma. IBID 1911, 25, 421–422. [Google Scholar]
  34. Gonçalves, T.C.M.; Teves-Neves, S.C.; Santos-Mallet, J.R.; Carbajal-de-la-Fuente, A.L.; Lopes, C.M. Triatoma jatai sp. nov. in the state of Tocantins, Brazil (Hemiptera: Reduviidae: Triatominae). Memórias Inst. Oswaldo Cruz 2013, 108, 429–437. [Google Scholar] [CrossRef]
  35. GenBank. Available online: http://0-www-ncbi-nlm-nih-gov.brum.beds.ac.uk/genbank/ (accessed on 13 January 2022).
  36. Thompson, D.J.; Higgins, D.G.; Gibson, T.J. CLUSTALW: Improving The Sensitivity of Progressive Multiple Sequence Alignment Through Sequence Weighting, Position-specific Gap Penalties and Weight Matrix Choice. Nucleic Acids Revist. 1994, 22, 4673–4680. [Google Scholar] [CrossRef] [Green Version]
  37. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
  38. Kimura, M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16, 111–120. [Google Scholar] [CrossRef]
  39. Monteiro, F.A.; Perez, R.; Panzera, F.; Dujardin, J.-P.; Galvão, C.; Rocha, D.; Noireau, F.; Schofield, C.; Beard, C.B. Mitochondrial DNA variation of Triatoma infestans populations and its implication on the specific status of T. melanosoma. Memórias Inst. Oswaldo Cruz 1999, 94, 229–238. [Google Scholar] [CrossRef] [PubMed]
  40. Almeida, C.E.; Marcet, P.L.; Gumiel, M.; Takiya, D.M.; Cardozo-de-Almeida, M.; Pacheco, R.S.; Lopes, C.M.; Dotson, E.M.; Costa, J. Phylogenetic and phenotypic relationship among Triatoma carcavalloi (Hemiptera: Reduvidade: Triatominae) and related species collected in domiciles in Rio Grande do Sul State, Brasil. J. Vector Ecol. 2009, 34, 164–174. [Google Scholar] [CrossRef] [PubMed]
  41. Gardim, S.; Almeida, C.E.; Takiya, D.M.; Oliveira, J.; Araújo, R.F.; Cicarelli, R.M.B.; Rosa, J.A. Multiple mitochondrial genes of some sylvatic Brazilian Triatoma: Non-monophyly of the T. brasiliensis subcomplex and the need for a generic revision in the Triatomini. Infect. Genet. Evol. 2014, 23, 74–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Lent, H.; Jurberg, J.; Galvão, C.; Carcavallo, R.U. Triatoma melanosoma, Novo Status para Triatoma infestans melanosoma Martinez, Olmedo & Carcavallo, 1987 (Hemiptera: Reduviidae). Memórias Inst. Oswaldo Cruz 1994, 98, 353–358. [Google Scholar] [CrossRef] [Green Version]
  43. Klug, F. Reise um Die Erde Ausgeführt Auf Dem … Seehandlungs-Schiffe Prinzess Louise, Commandirt von Capitain W. Wendt in … 1830, 1831 und 1832, &c; Sander: Berlin, Germany, 1834; pp. 401–440. [Google Scholar]
  44. Catala, S.; Torres, M. Similarity of the patterns of sensilla on the antennae of Triatoma melanosoma and Triatoma infestans. Ann. Trop. Med. Parasitol. 2001, 95, 287–295. [Google Scholar] [CrossRef]
  45. Blanchard, E. Insectes de I’ Amérique Méridionale. In Voyage Dans I’ Amérique Méridionale Para Alcide d’ Orbigny; Bertrand, P., Ed.; Paris and Strasbourg: Paris, France, 1837; pp. 1–22. [Google Scholar]
  46. Almeida, C.E.; Pacheco, R.S.; Noireau, F.; Costa, J. Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) I: Isoenzymatic and Chromatic Patterns of five populations from the State of Rio Grande do Sul, Brazil. Memórias Inst. Oswaldo Cruz 2002, 97, 829–834. [Google Scholar] [CrossRef] [Green Version]
  47. Dale, C.; Braga, M.V.; Galvão, C. Taxonomia integrada aplicada ao subcomplexo Triatoma rubrovaria no Estado do Rio grande do Sul, Brasil. In Atualidades em Medicina Tropical na America do Sul: Vetores; Oliveira, J., Alevi, K.C.C., Camargo, L.M.A., Meneguetii, D.U.O., Eds.; Stricto Sensu Editora: Rio Branco, Brasil, 2021; pp. 38–68. [Google Scholar]
  48. Succi, M.; Alevi, K.C.C.; Mendonça, O.O.; Bardella, V.B.; Rosa, J.A.; Azeredo-Oliveira, M.T.V. Spermatogenesis in Triatoma williami Galvão, Souza and Lima (1965) (Hemiptera, Triatominae). Invertebr. Reprod. Dev. 2013, 58, 124–127. [Google Scholar] [CrossRef]
Insects 13 00591 g001 550
Figure 1. Species studied, dorsal view: (A) Triatoma guazu; (B) Triatoma williami; (C) Triatoma matogrossensis; (D) Triatoma oliveirai. Scale 5.0 mm.
Figure 1. Species studied, dorsal view: (A) Triatoma guazu; (B) Triatoma williami; (C) Triatoma matogrossensis; (D) Triatoma oliveirai. Scale 5.0 mm.
Insects 13 00591 g001
Insects 13 00591 g002 550
Figure 2. Triatoma williami (paratype, female, deposited in CEIB): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Figure 2. Triatoma williami (paratype, female, deposited in CEIB): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Insects 13 00591 g002
Insects 13 00591 g003 550
Figure 3. Triatoma williami (allotype, male, deposited in CEIB): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Figure 3. Triatoma williami (allotype, male, deposited in CEIB): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Insects 13 00591 g003
Insects 13 00591 g004 550
Figure 4. Triatoma williami (paratype, male, deposited in CTIOC): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Figure 4. Triatoma williami (paratype, male, deposited in CTIOC): (A) Dorsal view; (B) Ventral view; (C) Connexivum, dorsal view; (D) Connexivum, ventral view; (E) Labels. (A–D) Scale 5.0 mm.
Insects 13 00591 g004
Insects 13 00591 g005 550
Figure 5. Triatoma guazu (allotype, male, deposited in CTIOC): (A) Dorsal view; (B) Ventral view; (C) Dorsal view of the connexivum; (D) Ventral view of abdomen, including; (E) Labels. (A–D) Scale 5.0 mm.
Figure 5. Triatoma guazu (allotype, male, deposited in CTIOC): (A) Dorsal view; (B) Ventral view; (C) Dorsal view of the connexivum; (D) Ventral view of abdomen, including; (E) Labels. (A–D) Scale 5.0 mm.
Insects 13 00591 g005
Insects 13 00591 g006 550
Figure 6. Triatoma williami, head, dorsal view of a showing landmarks (target spots) used in morphometric analysis. Scale 5.0 mm.
Figure 6. Triatoma williami, head, dorsal view of a showing landmarks (target spots) used in morphometric analysis. Scale 5.0 mm.
Insects 13 00591 g006
Insects 13 00591 g007 550
Figure 7. Variation of the connexivum spotting pattern. (A–C) Triatoma guazu, wide dark spots, in dorsal and ventral views; (D–F) Triatoma williami, narrow dark spots, in dorsal and ventral views. Scale 5.0 mm.
Figure 7. Variation of the connexivum spotting pattern. (A–C) Triatoma guazu, wide dark spots, in dorsal and ventral views; (D–F) Triatoma williami, narrow dark spots, in dorsal and ventral views. Scale 5.0 mm.
Insects 13 00591 g007
Insects 13 00591 g008 550
Figure 8. Factorial map built with the first two canonical vectors (CV) showing the head shape discrimination. (A) Between Triatoma guazu, Triatoma williami, Triatoma matogrossensis, and Triatoma oliveirai; (B) Without T. oliveirai.
Figure 8. Factorial map built with the first two canonical vectors (CV) showing the head shape discrimination. (A) Between Triatoma guazu, Triatoma williami, Triatoma matogrossensis, and Triatoma oliveirai; (B) Without T. oliveirai.
Insects 13 00591 g008
Insects 13 00591 g009 550
Figure 9. Triatoma williami, male genitalia. (A) Phallus, lateral view, scale bar 0.5 mm. (B,C) Dorsal view, scale bar 0.3 mm. (B) Struts and apical portion of phallothecal plate (pointed by arrows). (C) Articulatory apparatus and pedicel. (D) Lateral process of endosoma, lateral view, scale bar 0.2 mm. (E) Median process of endosoma, superior view, scale bar 0.1 mm. (ba, basal plate arm; bb, basal plate bridge; dp, dorsal phallothecal plate; lp, lateral process of endosoma; mp, median process of endosoma; pd, pedicel).
Figure 9. Triatoma williami, male genitalia. (A) Phallus, lateral view, scale bar 0.5 mm. (B,C) Dorsal view, scale bar 0.3 mm. (B) Struts and apical portion of phallothecal plate (pointed by arrows). (C) Articulatory apparatus and pedicel. (D) Lateral process of endosoma, lateral view, scale bar 0.2 mm. (E) Median process of endosoma, superior view, scale bar 0.1 mm. (ba, basal plate arm; bb, basal plate bridge; dp, dorsal phallothecal plate; lp, lateral process of endosoma; mp, median process of endosoma; pd, pedicel).
Insects 13 00591 g009
Insects 13 00591 g010 550
Figure 10. Female external examined by scanning electron microscopy of Triatoma guazu. (A) Dorsal view (VII and VIII, tergites; IX and X segments). (B) Ventral view (VII, sternite; IX, segment; Gc8, gonocoxite VIII; Gp8, gonapophysis VIII). (C) Posterior view: (Gc8, gonocoxite VIII; Gc9, gonocoxite IX; Gp8, gonapophysis VIII; IX and X, segments).
Figure 10. Female external examined by scanning electron microscopy of Triatoma guazu. (A) Dorsal view (VII and VIII, tergites; IX and X segments). (B) Ventral view (VII, sternite; IX, segment; Gc8, gonocoxite VIII; Gp8, gonapophysis VIII). (C) Posterior view: (Gc8, gonocoxite VIII; Gc9, gonocoxite IX; Gp8, gonapophysis VIII; IX and X, segments).
Insects 13 00591 g010
Table
Table 1. Specimens examined, locality information (when available), ID (unique specimen identifier number), marker and GenBank accession numbers.
Table 1. Specimens examined, locality information (when available), ID (unique specimen identifier number), marker and GenBank accession numbers.
SpeciesIDGeographic OriginMarkers
16S rRNACOICOIICytb
Triatoma brasiliensis40ACuraçá, BA, BrazilKC248986KC249319-KC249240
40BCuraçá, BA, Brazil-KC249320--
- --
172Tauá, CE, Brazil-KC249318--
41Sobral, CE, BrazilKC248987--KC249241
174Tauá, CE, BrazilKC248985-KC249413KC249239
Triatoma guazu -----
Barra do Garças, MT, Brazil--KC249440-
Barra do Garças, MT, Brazil----
Barra do Garças, MT, Brazil----
29 Barra do Garças, MT, BrazilKC249013---
Barra do Garças, MT, Brazil-KC608984-KC608976
Triatoma jatai03Paranã, TO, BrazilKT601153KT601162--
05Paranã, TO, BrazilKT601154KT601163--
16Paranã, TO, BrazilKT601155KT601164--
Triatoma juazeirensis209Uiabi, BA, BrazilKC249026KF826892-KC249263
CTA207Juazeiro, BA, BrazilKF769453---
Triatoma matogrossensis -AF324525---
-AF324526---
-- -
Rio Verde de Mato Grosso, MS, Brazil-KC608985-KC608972
Rio Verde de Mato Grosso, MS, Brazil---KC608978
32Aquidauana, MS, BrazilKC249039--KC249271
33Alegria, MT, BrazilKC249040-KC249460-
191--KC249359KC249456KC249269
192São Gabriel D’oeste, MS, BrazilKC249037KC249360KC249457KC249270
Triatoma melanicaHaplotype G--KJ580492 -
Haplotype H- KJ580493
Haplotype I- KJ580494
Haplotype J- KJ580495
Urandi, BA, BrazilKF769454-
-KC249041-KC249461
Triatoma sherlocki80 KC249068-KC249378
EU489057 EU489058
Triatoma williami04Barra do Garças, MT, BrazilKT601156KT601165--
36-KC249089-KC249493-
Barra do Garças, MT, Brazil----
Barra do Garças, MT, Brazil- KC608981
-----
(-) Uninformative.
Table
Table 2. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for 16S. Interspecific divergence between these two species are in boldface.
Table 2. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for 16S. Interspecific divergence between these two species are in boldface.
12345678
1.Triatoma guazu-
2.Triatoma williami0.0020.000
3.Triatoma matogrossensis0.066 (0.065–0.068)0.063 (0.062–0.065)0.005 (0.000–0.008)
4.Triatoma jatai0.0530.0490.072 (0.071–0.074)0.000
5.Triatoma brasiliensis0.054 (0.052–0.055)0.054 (0.052–0.055)0.084 (0.080–0.090)0.064 (0.061–0.068)0.003 (0.028–0.005)
6.Triatoma juazeirensis0.063 (0.062–0.065)0.060 (0.059–0.062)0.082 (0.077–0.090)0.060 (0.058–0.061)0.021 (0.019–0.025)0.002
7.Triatoma melanica0.057 (0.055–0.059)0.054 (0.052–0.055)0.086 (0.083–0.090)0.054 (0.052–0.055)0.026 (0.022–0.028)0.033 (0.031–0.034)0.002
8. Triatoma sherlocki0.057 (0.056–0.059)0.054 (0.053–0.056)0.084 (0.080–0.089)0.051 (0.049–0.052)0.022 (0.019–0.024)0.030 (0.028–0.031)0.018 (0.017–0.019)0.000
Table
Table 3. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for COI. Interspecific divergence between these two species are in boldface.
Table 3. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for COI. Interspecific divergence between these two species are in boldface.
1234567
1. Triatoma guazu-
2. Triatoma williami0.015 (0.000–0.015)0.015
3. Triatoma matogrossensis0.123 (0.108–0.138)0.126 (0.108–0.145)0.020 (0.000–0.030)
4. Triatoma jatai0.0900.088 (0.085–0.090)0.147 (0.137–0.157)0.000
5. Triatoma brasiliensis0.128 (0.125–0.131)0.137 (0.125–0.151)0.181 (0.161–0.201)0.191 (0.187–0.194)0.005
6. Triatoma melanica0.1490.159 (0.149–0.169)0.191 (0.181–0.202)0.1610.082 (0.079–0.085)0.000
7. Triatoma juazeirensis0.1260.1260.133 (0.124–0.141)0.1670.0490.076 (0.042–0.087)-
Table
Table 4. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for COII. Interspecific divergence between these two species are in boldface.
Table 4. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for COII. Interspecific divergence between these two species are in boldface.
123456
1.Triatoma guazu-
2. Triatoma williami0.017-
3.Triatoma matogrossensis0.165 (0.162–0.167)0.165 (0.162–0.171)0.022 (0.000–0.032)
4. Triatoma brasiliensis0.1560.1430.168 (0.168–0.187)-
5. Triatoma melanica0.1660.1560.245 (0.236–0.254)0.152-
6. Triatoma sherlocki0.1640.1550.206 (0.197–0.212)0.1160.091-
Table
Table 5. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for CytB. Interspecific divergence between these two species are in boldface.
Table 5. Average divergence estimates obtained from pairwise comparisons among sequences of T. guazu and T. williami using the Kimura model 2- Parameter for CytB. Interspecific divergence between these two species are in boldface.
123456
1. Triatoma guazu-
2. Triatoma williami0.009-
3. Triatoma matogrossensis0.1530.1400.006 (0–0.006)
4. Triatoma brasiliensis0.1980.1960.181 (0.178–0.187)0.012 (0–0.012)
5. Triatoma sherlocki0.1980.2040.2130.141 (0.141–0.149)-
6. Triatoma juazeirensis0.1740.1780.1480.0930.012-
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Oliveira Correia, J.P.S.; Gil-Santana, H.R.; Dale, C.; Galvão, C. Triatoma guazu Lent and Wygodzinsky Is a Junior Synonym of Triatoma williami Galvão, Souza and Lima. Insects 2022, 13, 591. https://0-doi-org.brum.beds.ac.uk/10.3390/insects13070591

AMA Style

Oliveira Correia JPS, Gil-Santana HR, Dale C, Galvão C. Triatoma guazu Lent and Wygodzinsky Is a Junior Synonym of Triatoma williami Galvão, Souza and Lima. Insects. 2022; 13(7):591. https://0-doi-org.brum.beds.ac.uk/10.3390/insects13070591

Chicago/Turabian Style

Oliveira Correia, João Paulo Sales, Hélcio Reinaldo Gil-Santana, Carolina Dale, and Cleber Galvão. 2022. "Triatoma guazu Lent and Wygodzinsky Is a Junior Synonym of Triatoma williami Galvão, Souza and Lima" Insects 13, no. 7: 591. https://0-doi-org.brum.beds.ac.uk/10.3390/insects13070591

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop