Occurrences of Ornithocoris toledoi (Cimicidae) on a free-range chicken farm in the state of Rio de Janeiro, Brazil

Ocorrência de Ornithocoris toledoi (Cimicidae) em uma fazenda com criação rústica de galinhas no estado do Rio de Janeiro, Brasil

Marcus Sandes Pires Hermes Ribeiro Luz Maristela Peckle Claudia Bezerra da Silva Gabriela Lopes Vivas Vitari Renata Lins da Costa Mariana Guimarães Graciosa Huarrisson Azevedo Santos João Luiz Horacio Faccini Carlos Luiz Massard About the authors

Abstract

Ornithocoris toledoi is a hematophagous insect that parasites birds, particularly, galliformes. Although the occurrence of this arthropod is relatively low in Brazil, this is an important ectoparasite associated with backyarding poultry. The objective of this study was to report the occurrence of O. toledoi in a free-range chicken farm in the state of Rio de Janeiro, Brazil, including aspects of its taxonomic identification, biology and epidemiology.

Keywords:
Bed bugs; chicken bugs; ectoparasite; Gallus gallus; poultry

Resumo

Ornithocoris toledoi é um inseto hematófago que parasita aves, particularmente os galiformes. Embora a ocorrência deste artrópode seja relativamente baixa no país, este é um ectoparasito importante relacionado à criação rústica de galinhas. O objetivo estudo foi relatar a ocorrência de O. toledoi em uma criação rústica de galinhas no estado do Rio de Janeiro, incluindo aspectos sobre a sua identificação taxonômica, biologia e epidemiologia.

Palavras-chave:
Percevejos; percevejos-de-galinha; ectoparasita; Gallus gallus; produção avícola

Cimicids are hematophagous insects of small size, ranging from 4.5 mm to 7 mm ( FREITAS et al., 1978 Freitas MG, Costa HMA, Costa JO, Lide P. Ordem Hemiptera: Famílias Reduviidae e Cimicidae. In: Freitas MG, Costa HMA, Costa JO, Lide P, editors. Entomologia e acarologia médica e veterinária. 4th ed. Belo Horizonte: Precisa; 1978. p. 175-191. ). The original description ( PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ) was based on absence of wings, pronotum with rounded edges and anterior margins presenting little depth, narrower than the rear margin, with a trapezoidal appearance and body covered with small short bristles. The Cimicidae include six subfamilies, 24 genera and 110 species ( HENRY, 2009 Henry TJ. Biodiversity of Heteroptera. In: Foottit RG, Adler PH, editors. Insect biodiversity: science and society. Oxford: Wiley-Blackwell Publishing; 2009. p. 223-263. http://dx.doi.org/10.1002/9781444308211.ch10.
http://dx.doi.org/10.1002/9781444308211...
) and are mainly distributed in the Neotropical region. “Bed bug” is the popular name given to the members of this family for which the life cycle includes egg, nymph and adult stages. These insects are temporary ectoparasites and, between blood meals, they remain in their hosts’ nests or in the cracks or crevices of their hosts’ shelters ( USINGER, 1966 Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). ). Most cimicid species are parasites of birds and bats, but some are parasites of humans and are therefore of public health concern ( COSTA LIMA, 1940 Costa Lima AMC. Superfamília Cimicoidea. In: Costa Lima AMC, editor. Insetos do Brasil. 3th ed. Rio de Janeiro: Escola Nacional Agronomia; 1940. p. 242-292. (Série Didática). ; FORATTINI, 1990 Forattini OP. Os Cimicídeos e sua importância em Saúde Pública (Hemiptera-Heteroptera; Cimicidae). Rev Saúde Pública 1990; 24(Suppl): 1-37. http://dx.doi.org/10.1590/S0034-89101990000700001. PMid:2218370.
http://dx.doi.org/10.1590/S0034-8910199...
).

Some species of the genera Cimex Linnaeus, 1758, Ornithocoris Pinto, 1927; Propicimex Barber, 1941; and Latrocimex Lent, 1941, have been found in Brazil ( RYCKMAN et al., 1981 Ryckman RE, Bentley DG, Archbold EF. The Cimicidae of the Americas and Oceanic islands, a checklist and bibliography. Bull Soc Vec Ecol 1981; 6: 93-142. ). The genus Ornithocoris currently has two valid species: O. toledoi and Ornithocoris pallidus Usinger, 1959. Both species are apparently rare in Brazil. Ornithodoros toledoi has been reported twice on poultry farms in the states of São Paulo ( PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ) and Minas Gerais ( CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ). It has also been found infesting chickens in other South American countries, such as Bolivia and Argentina ( RYCKMAN et al., 1981 Ryckman RE, Bentley DG, Archbold EF. The Cimicidae of the Americas and Oceanic islands, a checklist and bibliography. Bull Soc Vec Ecol 1981; 6: 93-142. ). Although there is one report of the genus Ornithocoris in the state of Rio Grande do Sul ( OTTO et al., 2008 Otto MA, Silva AS, Zanette RA, Schmitt L, Monteiro SG. Infestação por Ornithocoris sp. em residências do Município de Santa Maria, Rio Grande do Sul, Brasil. Rev Bras Parasitol Vet 2008;17(Suppl 1): 99-101. PMid:20059826. ), its identification was questioned by Di Iorio et al. (2010) Di Iorio O, Turienzo P, Masello J, Carpintero DL. Insects found in birds’nests from Argentina. Cyanoliseus patagonus (Vieillot, 1818) [Aves: Psittacidae], with the description of Cyanolicimex patagonicus, gen. n., sp. n., and a key to the genera of Haematosiphoninae (Hemiptera: Cimicidae). Zootaxa 2010; 2728: 1-22. . The species O. pallidus was described from the nests of Pygochelidon cyanoleuca (Vielliot, 1817) (Aves: Passeriformes) in Viçosa, state of Minas Gerais, Brazil. Later on, it was reported in the states of Florida and Georgia, USA, associated with chickens and Passeriform birds: Progne subis Linnaeus, 1758, and Passer domesticus Linnaeus, 1758 ( USINGER, 1966 Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). ; WILSON et al., 1986 Wilson N, Smith GC, Sykes DL. An additional record of Ornithocoris pallidus (Hemiptera: Cimicidae) for the United States. J Med Entomol 1986; 23(5): 575. http://dx.doi.org/10.1093/jmedent/23.5.575. PMid:3772958.
http://dx.doi.org/10.1093/jmedent/23.5....
). In relation to the distribution of O. toledoi in chicken farms in Brazil, few reports have been observed so far ( PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ; MORAES, 1939 Moraes RG. Breve nota sobre o Ornithocoris toledoi Pinto,1927. Rev Med Cirurg Brasil 1939; 47(2): 250-255. ; CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ). However, their presence may lead to a decrease in egg production and increase in susceptibility to diseases ( CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ; SNIPES et al., 1940 Snipes BT, Carvalho JCM, Tauber OE. Biological studies of Ornithocoris toledoi Pinto, the Brazilian chicken bedbug. Iowa State Coll J Sci 1940; 15: 27-36. ). This aspect related to a free-range chicken breeding can cause losses up to the abandon of this activity. Another important aspect is related to its biology, as this parasite was observed in nests of wild birds ( CARPINTERO et al., 2011 Carpintero D, Berkunsky I, Aramburú R. Primer registro del Calancate Común Aratinga a. acuticaudata (Aves: Psittacidae) como huésped nativo primario de Ornithocoris toledoi Pinto (Hemiptera: Heteroptera: Cimicidae). Rev Mus Argent Cienc Nat 2011; 13(2): 205-212. http://dx.doi.org/10.22179/REVMACN.13.223.
http://dx.doi.org/10.22179/REVMACN.13.2...
), which demonstrates it has a greater potential of dissemination to other localities.

This study aimed to report the occurrence of O. toledoi to a farm located in the municipality of Valença (22º 14' 44” S; 43º 42' 01” W), state of Rio de Janeiro, Brazil ( Figure 1 ) and to add biological, morphologic and epidemiological information about this hematophagous species which is of importance to free-range chicken farms and wild birds.” This farm was primarily set up for milk production, but also raises backyarding poultry such as Gallus gallus, Meleagris gallopavo, Coturnix coturnix and Numida meleagris ( Figures 2 2B). During a technical visit in March 2012, high levels of infestation with small dark wingless insects were observed in the nests inside the chicken coops, in cracks in the walls and roof, and on the birds’ food and fecal waste ( Figure 2 D). Some chickens were also inspected for signs of parasitism ( Figure 2 C).

Figure 1
Geographical location of the area where specimens of Ornithocoris toledoi were observed in free-range chicken farm, in March 2012, in the state of Rio de Janeiro, Brazil.
Figure 2
View of the chicken coops (A and B). Examination of chickens (C). Ornithocoris toledoi seen on the ground in the coop (D).

Some specimens were collected and placed in polypropylene tubes containing 70% alcohol. These were then transported to the Multiuser Microscopy and Bioimaging Laboratory of the Federal Rural University of Rio de Janeiro (UFRRJ). Eight specimens were cleared in lactophenol at 37 °C and mounted in Hoyer’s medium. An optical microscope was used at 1800s, 400x and 1000x to make the following measurements of body parts: pronotum length(PL); pronotum width (PW); second and third bristles of the posterior pronotum angle (Lb2 and Lb3); first, second, third and fourth antennal flagella (A1, A2, A3 and A4); head width with eyes (HW); PW/HW ratio; interocular space (IS); length of the male genitalia (GL); abdomen length (AL) and width (AW); hemelytra length (HmL) and width (HmW); length of the femur (FL) and tibia (TiL) of the third leg; and total length (TL) of the specimen ( Figure 3 A).

Figure 3
Morphology of Ornithocoris toledoi collected on the farm. Parameter scheme measurements of the O. toledoi specimens (A); O. toledoi observed under stereomicroscope, showing dark brown color (B); Pronotum of O. toledoi wider than long (C); Details pointed with an arrow: pronotum bristles (D); Bristle tufts in the final third of the tibia (E); Sexual organ of the male (F) and female (G).

All of the measurements were made using the CellD software, version 5.1, under an OLYMPUS BX51 microscope. We compared our specimens with two reference specimens of O. toledoi in the Costa Lima Entomological Collection of the Oswaldo Cruz Institute (IOC/FIOCRUZ; accession numbers CCL 5475, slide 4730, female specimen, and CCL 5476, slide 4731, male specimen). Two voucher specimens (female and male) were deposited in the “Angelo Moreira da Costa Lima” Entomological Collection (CECL) of the Biology Institute, Federal Rural University of Rio de Janeiro (accession numbers 12501 and 12502, respectively). We identified our specimens in accordance with Pinto (1927) Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. , Carvalho (1939) Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. , Moraes (1939) Moraes RG. Breve nota sobre o Ornithocoris toledoi Pinto,1927. Rev Med Cirurg Brasil 1939; 47(2): 250-255. , Usinger (1959 Usinger RL. New species of Cimicidae (Hemiptera). Entomol 1959; 92: 218-222. , 1966 Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). ), Jansen (1979) Jansen AM. Estudos biológicos e biométricos de Ornithocoris toledoi Pinto, 1927 (Cimicidae: Hemiptera) [dissertation]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1979. , Jurberg & Azevedo (1982) Jurberg J, Azevedo EMVM. Contribuição para o estudo da morfologia de Ornithocoris toledoi Pinto, 1927 (Hemiptera, Cimicidae). Rev Bras Biol 1982; 42(1): 255-262. and Di Iorio et al. (2010) Di Iorio O, Turienzo P, Masello J, Carpintero DL. Insects found in birds’nests from Argentina. Cyanoliseus patagonus (Vieillot, 1818) [Aves: Psittacidae], with the description of Cyanolicimex patagonicus, gen. n., sp. n., and a key to the genera of Haematosiphoninae (Hemiptera: Cimicidae). Zootaxa 2010; 2728: 1-22. .

During the technical visit, we observed that these insects moved quickly to hidden in dark crevices and cracks of buildings. Regarding to the chickens, some of them showed signs of weakness, which can be directly related to the high infestation level that was observed in the flock. The presence of this ectoparasite in chicken coops can decrease egg production and increase susceptibility to other diseases ( CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ). Although some studies have indicated that pathogen transmission by other Cimicidae species occurs ( BURTON, 1963 Burton GJ. Bedbugs in relation to transmission of human diseases. Public Health Rep 1963; 78(6): 513-524. http://dx.doi.org/10.2307/4591852. PMid:14017240.
http://dx.doi.org/10.2307/4591852 ...
; DELAUNAY, 2012 Delaunay P. Human travel and traveling bedbugs. J Travel Med 2012; 19(6): 373-379. http://dx.doi.org/10.1111/j.1708-8305.2012.00653.x. PMid:23379708.
http://dx.doi.org/10.1111/j.1708-8305.2...
; LEULMI et al., 2015 Leulmi H, Bitam I, Berenger JM, Lepidi H, Rolain JM, Almeras L, et al. Competence of Cimex lectularius Bed bugs for the transmission of Bartonella quintana , the Agent of Trench Fever. PLoS Negl Trop Dis 2015; 9(5): e0003789. http://dx.doi.org/10.1371/journal.pntd.0003789. PMid:26000974.
http://dx.doi.org/10.1371/journal.pntd....
), the role of O. toledoi as a vector of pathogens to chickens is unknown.

Also during the technical visit to the farm, we did not see any evidence of the presence of insects in the bodies of chickens, or any lesions suggestive of parasitism by these insects. However, Carvalho (1939) Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. and Snipes et al. (1940) Snipes BT, Carvalho JCM, Tauber OE. Biological studies of Ornithocoris toledoi Pinto, the Brazilian chicken bedbug. Iowa State Coll J Sci 1940; 15: 27-36. reported that the signs caused by the bites of O. toledoi in G. gallus consisted of punctiform hemorrhage and hyperemia at the bite sites, and that they disappeared almost entirely within 12 hours. This may have the cause of the lack of signs in the birds during our visit. In addition, the owner of the farm reported deaths of young chickens, probably due to blood loss resulting from the high of infestation by these insects, which feed during all phases of their life cycle ( USINGER, 1966 Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). ).

Accordingly, identification of O. toledoi was based on the following characters: pronotum wider than long ( Figure 3 C); second segment, of the antenna wider than the third and fourth ones; presence of two pairs of bristles in the posterior prothoracic angles (Lb2 and Lb3) ( Figure 3 D); presence of two tufts in the final thirds of tibia I and II in males, and only in tibia II in females ( Figure 3 E); presence of spicule in males; presence of Ribaga’s organ in the dorsal region of in females ( Figure 3 3G). These external characters of the genitalia are typical of O. toledoi ( JANSEN, 1979 Jansen AM. Estudos biológicos e biométricos de Ornithocoris toledoi Pinto, 1927 (Cimicidae: Hemiptera) [dissertation]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1979. ; JURBERG & AZEVEDO, 1982 Jurberg J, Azevedo EMVM. Contribuição para o estudo da morfologia de Ornithocoris toledoi Pinto, 1927 (Hemiptera, Cimicidae). Rev Bras Biol 1982; 42(1): 255-262. ). As expected, these measurements varied between the specimens collected ( Table 1 ) and among specimens of O. toledoi from other regions ( PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ; CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ; MORAES, 1939 Moraes RG. Breve nota sobre o Ornithocoris toledoi Pinto,1927. Rev Med Cirurg Brasil 1939; 47(2): 250-255. ; USINGER, 1966 Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). ; JANSEN, 1979 Jansen AM. Estudos biológicos e biométricos de Ornithocoris toledoi Pinto, 1927 (Cimicidae: Hemiptera) [dissertation]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1979. ; DI IORIO et al. 2010 Di Iorio O, Turienzo P, Masello J, Carpintero DL. Insects found in birds’nests from Argentina. Cyanoliseus patagonus (Vieillot, 1818) [Aves: Psittacidae], with the description of Cyanolicimex patagonicus, gen. n., sp. n., and a key to the genera of Haematosiphoninae (Hemiptera: Cimicidae). Zootaxa 2010; 2728: 1-22. ). Morphometric variations may be influenced by the specimen’s physiological status, adaptive changes, genetic differences ( DUJARDIN & SLICE, 2007 Dujardin JP, Slice DE. Contributions of morphometrics to medical entomology. In: Tibayrenc M, editor. Encyclopedia of infectious diseases: modern methodologies . New York: Wiley & Sons; 2007. p. 435-447. http://dx.doi.org/10.1002/9780470114209.ch25.
http://dx.doi.org/10.1002/9780470114209...
), feeding or climatic conditions ( JANSEN, 1979 Jansen AM. Estudos biológicos e biométricos de Ornithocoris toledoi Pinto, 1927 (Cimicidae: Hemiptera) [dissertation]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1979. ).

Table 1
Mean values obtained from morphometry on Ornithocoris toledoi in this study.

Despite the morphological similarities between O. toledoi and O. pallidus, they can be separated by the dark-brown body ( Figure 3 B), which is typical of O. toledoi ( CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ; JANSEN, 1979 Jansen AM. Estudos biológicos e biométricos de Ornithocoris toledoi Pinto, 1927 (Cimicidae: Hemiptera) [dissertation]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1979. ; MORAES, 1939 Moraes RG. Breve nota sobre o Ornithocoris toledoi Pinto,1927. Rev Med Cirurg Brasil 1939; 47(2): 250-255. ; PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ), and the ratio between the width and pronotum head width (PW/HW) proposed by Usinger (1966) Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). . In the specimens collected by us, this ratio (PW/HW) was approximately 1.8, matching the diagnosis of O. toledoi by Usinger (1966) Usinger RL. Monograph of Cimicidae (Hemiptera - Heteroptera). Maryland: Entomological Society of America, College Park; 1966. (Serie Thomas Say Foundation ). and Di Iorio et al. (2010) Di Iorio O, Turienzo P, Masello J, Carpintero DL. Insects found in birds’nests from Argentina. Cyanoliseus patagonus (Vieillot, 1818) [Aves: Psittacidae], with the description of Cyanolicimex patagonicus, gen. n., sp. n., and a key to the genera of Haematosiphoninae (Hemiptera: Cimicidae). Zootaxa 2010; 2728: 1-22. .

Regarding insect/host relationships, specimens were collected from chickens, thus confirming the association of this species with this typical host ( CARVALHO, 1939 Carvalho JCM. Sobre a biologia do Ornithocoris toledoi Pinto 1927, percevejo dos galinheiros em Minas Gerais (Hemíptera: Cimicidae). Ceres 1939; 1: 128-140. ; MORAES, 1939 Moraes RG. Breve nota sobre o Ornithocoris toledoi Pinto,1927. Rev Med Cirurg Brasil 1939; 47(2): 250-255. ; PINTO, 1927 Pinto C. Ornithocoris toledoi, novo gênero e nova espécie de percevejo de ave (Hemiptera – Fam. Cimicidae). Rev Biol Hyg 1927; 1: 17-22. ). Recently, the species O. toledoi was also described from nests of birds Psittacidae ( CARPINTERO et al., 2011 Carpintero D, Berkunsky I, Aramburú R. Primer registro del Calancate Común Aratinga a. acuticaudata (Aves: Psittacidae) como huésped nativo primario de Ornithocoris toledoi Pinto (Hemiptera: Heteroptera: Cimicidae). Rev Mus Argent Cienc Nat 2011; 13(2): 205-212. http://dx.doi.org/10.22179/REVMACN.13.223.
http://dx.doi.org/10.22179/REVMACN.13.2...
), which suggests that this species may use wild birds as hosts, but further research is needed to clarify this issue.

Two years after the first technical visit, these ectoparasites were no longer observed in the chicken coops, probably due to the effective chemical control recommended to the farmer.

Acknowledgements

Dra. Jane Costa, curator of the Entomological Collection of the Oswaldo Cruz Institute (FIOCRUZ) and Msca. Claudia Leal Rodrigues, assistant curator (FIOCRUZ), and Dra. Teresa Cristina Gonçalves, Department of Entomology (FIOCRUZ), for the technical assistance. The CNPq and FAPERJ, for research scholarships granted to João Luiz Horácio Faccini and Carlos Luiz Massard.

References

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    » http://dx.doi.org/10.1093/jmedent/23.5.575

Publication Dates

  • Publication in this collection
    11 June 2018
  • Date of issue
    Jul-Sep 2018

History

  • Received
    27 Nov 2017
  • Accepted
    06 Apr 2018
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