Abstract
INTRODUCTION:
The Culicoides transmit a variety of pathogens. Our aim was to survey the Culicoides species occurring in an Amazonian rural settlement, comparing abundance, richness, and diversity in different environments.
METHODS:
Culicoides were captured using CDC light traps. The Shannon-Wiener (H’) and Rényi indices were used to compare species diversity and evenness between environments, the equitability (J’) index was used to calculate the uniformity of distribution among species, and similarity was estimated using the Jaccard similarity index. A permutational multivariate analysis of variance was applied to assess the influence of environment on species composition. A non-metric dimensional scale was used to represent the diversity profiles of each environment in a multidimensional space.
RESULTS:
6.078 Culicoides were captured, representing 84 species (45 valid species/39 morphotypes). H’ values showed the following gradient: forest > capoeira > peridomicile > forest edge. The equitability J’ was greater in capoeira and forests compared to peridomiciles and the forest edge. The population compositions of each environment differed statistically, but rarefaction estimates indicate that environments of the same type possessed similar levels of richness. Species of medical and veterinary importance were found primarily in peridomiciles: C. paraensis, vector of Oropouche virus; C. insignis and C. pusillus, vectors of Bluetongue virus; C. filariferus, C. flavivenula, C. foxi, and C. ignacioi, found carrying Leishmania DNA.
CONCLUSIONS:
This study indicates that diversity was higher in natural environments than in anthropized environments, while abundance and richness were highest in the most anthropized environment. These findings suggest that strictly wild Culicoides can adapt to anthropized environments.
Keywords:
Culicoides; Diversity; Abundance; Anthropized environments
INTRODUCTION
Tropical forest ecosystems host two thirds of the Earth’s terrestrial biodiversity and provide significant benefits to the biosphere and the global economy11. Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS. Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett. 2009;12(6):561-82. doi:10.1111/j.1461-0248.2009.01294.x
https://doi.org/10.1111/j.1461-0248.2009...
. According to Steege et al. (2015)22. Steege H, Pitman NCA, Killeen TJ, Laurance WF, Peres CA, Guevara JE, et al. Estimating the global conservation status of more than 15,000 Amazonian tree species. Sci Adv. 2015;1(10):e1500936. doi: 10.1126/sciadv.1500936.
https://doi.org/10.1126/sciadv.1500936...
, approximately 40% of the original Amazon forest will be lost by 2050 if historical rates of deforestation continue. Anthropization is the primary cause of environmental change and the degradation of tropical ecosystems.
Environmental changes caused by anthropogenic interference are associated with increased health risks. Vectors and pathogens previously found only in forests have been observed in human settlements. According to Gottdenker et al. (2014)33. Gottdenker NL, Streicker DG, Faust CL, Carroll CR. Anthropogenic land use change and infectious diseases: a review of the evidence. Eco Health. 2014;11(4):619-32. doi: 10.1007/s10393-014-0941-z
https://doi.org/10.1007/s10393-014-0941-...
, disease transmission is affected land-use changes that include: deforestation, forest and habitat fragmentation, agricultural development, irrigation, urbanization, and suburbanization. In the Amazon, these changes may be responsible for the increased incidence of endemic diseases such as Malaria, Yellow fever, Dengue, Zika, Mayaro, Oropouche, Chikungunya, and several other arboviruses and protozoa that cause leishmaniasis.
Hematophagous biting midge populations are affected by anthropogenic interference. In the Brazilian Amazon, Castellón (1990)44. Castellón EG. Culicoides (Diptera: Ceratopogonidae) na Amazônia Brasileira. II. Espécies coletadas na Reserva Florestal Ducke, aspectos ecológicos e distribuição geográfica. Act Amaz. 1990;20:83-93. http://dx.doi.org/10.1590/1809-43921990201093
https://doi.org/http://dx.doi.org/10.159...
observed a greater abundance of biting midges in capoeira and clearings than in primary forest. In urban and rural areas in Maranhão State, Silva and Carvalho (2013)55. Silva FS, Carvalho LPC. A Population Study of the Culicoides Biting Midges (Diptera: Ceratopogonidae) in Urban, Rural, and Forested Sites in a Cerrado Area of Northeastern Brazil. Ann Entomol Soc Am. 2013;106(4):463-70. doi: 10.1603/AN12047
https://doi.org/10.1603/AN12047...
found both a greater richness and abundance of biting midges in peridomiciles. According to Cazorla and Campos (2018)66. Cazorla CG, Campos RE. Synanthropy and Community Structure of Ceratopogonidae from the Northeast of Buenos Aires Province, Argentina. J Med Entomol. 2018;56(1):129-36. doi.org/10.1093/jme/tjy165
https://doi.org/10.1093/jme/tjy165...
, anthropization impacts ceratopogonid communities by decreasing biodiversity and favoring species that best adapt to altered environments.
This study was conducted in the settlement of Rio Pardo, Presidente Figueiredo Municipality, Amazonas State, Brazil. Until recently, human activity in Rio Pardo was limited to subsistence farming, raising livestock, hunting, fishing, and gathering wood for local use, but newly expanded branches of forestry and fish farming have had a significant impact on the natural environment. Disease transmission dynamics in the region may have been altered by the degradation of natural habitats causing increased human exposure to forests, and to disease vectors and their hosts. The increased supply of blood meal sources around peridomiciles and a lack of basic sanitation offer favorable conditions for insect vectors to flourish.
The genus Culicoides is comprised of 1.368 species worldwide; 299 of these species occur in the Neotropics and 122 species occur in the Brazilian Amazon Basin77. Borkent A. Numbers of Extant and Fossil Species of Ceratopogonidae. 2016. Available from: http://wwx.inhs.illinois.edu/files/8514/2385/5053/CulicoidesSubgenera.pdf
http://wwx.inhs.illinois.edu/files/8514/...
-88. Santarém M, Felippe-Bauer M. Brazilian species of biting midges. Fundação Oswaldo Cruz. 2019. Available from: https://portal.fiocruz.br/sites/portal.fiocruz.br/files/documentos/brazilian_species_of_biting_midges_2019.pdf
https://portal.fiocruz.br/sites/portal.f...
. Certain Culicoides species transmit viruses such as African horse sickness virus (AHSV), Bluetongue virus (BTV) which infects domestic and wild ruminants, and Oropouche virus (OROV) which infect humans99. Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol. 2000;45:307-40. doi: 10.1146/annurev.ento.45.1.307
https://doi.org/10.1146/annurev.ento.45....
. Oropouche virus is one of the most common arboviruses in Brazil; it has affected an estimated 500,000 people since it was first isolated in 19551010. Travassos da Rosa JF, Souza WM, Pinheiro FP, Figueiredo ML, Cardoso JF, Acrani GO, et al. Oropouche Virus: Clinical, Epidemiological, and Molecular Aspects of a Neglected Orthobunyavirus. Am J Trop Med Hyg. 2017;96(5):1019-30. doi:10.4269/ajtmh.16-0672
https://doi.org/10.4269/ajtmh.16-0672...
. Biting midges and simulids have been implicated in the transmission of some species of filariae to humans, including: Mansonella ozzardi, M. perstans and M. streptocerca1111. Linley JR, Hoch AL, Pinheiro FP. Biting midges (Diptera: Ceratopogonidae) and human health. J Med Entomol . 1983;20(4):347-64. doi: 10.1093/jmedent/20.4.347. Culicoides may also be involved in the transmission of Leishmania1212. Seblova V, Sadlova J, Vojtkova B, Votypka J, Carpenter S, Bates PA, et al. The Biting Midge Culicoides sonorensis (Diptera: Ceratopogonidae) is Capable of Developing Late Stage Infections of Leishmania enriettii. PLoS Negl Trop Dis. 2015;9(9),e0004060. https://doi.org/10.1371/journal.pntd.0004060
https://doi.org/https://doi.org/10.1371/...
.
Identifying possible disease vectors is therefore of significant epidemiological importance. The aim of this study was to survey the Culicoides species that occur in a typical Amazonian rural settlement, and to compare the abundance, richness, and diversity of Culicoides populations present in different environments.
METHODS
The rural settlement of Rio Pardo (1°49’02.3’’S 60°19’03.5’’W), Presidente Figueiredo Municipality, Amazonas State, Brazil (Figure 1), was founded in 1996 and has approximately 700 inhabitants (ILMD/FIOCRUZ). In 2002, approximately 95% of its total area, about 28,000 hectares, was composed of preserved forest. From 1996-2002, the rate of deforestation was estimated to be about 150 ha/year, while land was developed for agricultural and community use at a rate of about 220 ha/year1313. Ramos WR, Medeiros JF, Julião GR, Ríos-Velásquez CM, Marialva EF, Desmouliére SJM, Luz SL, Pessoa FA. Anthropic effects on sand fly (Diptera: Psychodidae) abundance and diversity in an Amazonian rural settlement, Brazil. Acta Trop. 2014;139:44-52. doi: 10.1016 / j.actatropica.2014.06.017
https://doi.org/10.1016 / j.actatropica....
.
Location of the study area where Culicoides were captured: (A) Brazil; (B) Location of Presidente Figueiredo Municipality in the Central Amazon; (C) The rural settlement of Rio Pardo, numbers indicate specific dwellings where collections were made; (D) Diagram of a single collection area, a collection area was defined as the area within 300 m of a dwelling (Adapted by Ramos et al. 20151313. Ramos WR, Medeiros JF, Julião GR, Ríos-Velásquez CM, Marialva EF, Desmouliére SJM, Luz SL, Pessoa FA. Anthropic effects on sand fly (Diptera: Psychodidae) abundance and diversity in an Amazonian rural settlement, Brazil. Acta Trop. 2014;139:44-52. doi: 10.1016 / j.actatropica.2014.06.017
https://doi.org/10.1016 / j.actatropica.... ).
Culicoides capture was performed in June, July, and August 2010 on four consecutive nights per month. Four different environments within the household buffer zone were sampled: peridomicile, areas with enclosures for livestock; capoeira, successional areas that have regenerated naturally from both functioning and abandoned agroecosystems; forest edge, areas of transition between capoeira and forest; and forest, comprised primarily of ombrophilous forest or “terra firme” (upland Amazonian forest that never floods) and river margins. Twenty-four household buffers were sampled. Four Centers for Disease Control (CDC) light traps per household were used to capture Culicoides, totaling 96 traps. These were installed 1.5 m above the ground and remained in the field from 6:00 p.m. to 6:00 a.m.
Biting midges were transported in 70% ethanol and slide-mounted in phenol-balsam, as described by Wirth and Marston (1968)1414. Wirth W, Marston N. A Method for Mounting Small Insects on Microscope Slides in Canada Balsam. Ann Entomol Soc Am . 1968; 61(3);783-784. https://doi.org/10.1093/aesa/61.3.783
https://doi.org/https://doi.org/10.1093/...
. Species identification was performed following: Wirth and Blanton (1959)1515. Wirth WW, Blanton FS. Biting Midges of the Genus Culicoides from Panama (Diptera: Heleidae). Proc US Nat Mus. 1959;109(3415):237-482. https://doi.org/10.5479/si.00963801.109-3415.237
https://doi.org/https://doi.org/10.5479/...
, Spinelli et al. (1993)1616. Spinelli GR, Wirth WW, Greiner EC. The neotropical bloodsucking midges of the Culicoides guttatus group of the subgenus Hoffmania (Diptera: Ceratopogonidae). Contrib Amer Entomol Inst. 1993;27:1-91., and Santarém et al. (2015)1717. Santarém MCA, Farias ES, Felippe-Bauer ML. Culicoides castelloni sp. nov. from the Brazilian Amazon Region with a revision of the reticulatus species group (Diptera, Ceratopogonidae). An Acad Bras Cienc. 2015;87(2):955-72. http://dx.doi.org/10.1590/0001-3765201520140517
https://doi.org/http://dx.doi.org/10.159...
; subgeneric classifications were based on Borkent (2015)1818. Borkent A. The subgeneric classification of species of Culicoides - thoughts and a warning. 2015. Available from: http://wwx.inhs.illinois.edu/files/8514/2385/5053/CulicoidesSubgenera.pdf
http://wwx.inhs.illinois.edu/files/8514/...
. Voucher specimens were deposited at the Laboratório de Doenças Transmissíveis na Amazônia (ILMD/FIOCRUZ, Amazônia).
Many specimens had morphological variations in common. Unidentified specimens were therefore grouped into morphotypes and treated as valid species in the diversity and richness analyses. The Shannon-Wiener (H’) and Rényi indexes were used to compare species diversity and evenness between the four environments. The Pielou equitability index (J') was used to calculate the uniformity of distribution of individuals among species, and similarity was calculated using the Jaccard similarity index (Cj), which qualitatively compares species similarity along an environmental gradient1919. Magurran AE. Species abundance distributions: pattern or process? Funct Ecol. 2005;19(1):177-81. https://doi.org/10.1111/j.0269-8463.2005.00930.x
https://doi.org/https://doi.org/10.1111/...
. A permutational multivariate analysis of variance (PERMANOVA) was applied to assess the influence of each environment on species composition. A non-metric dimensional scale (NMDS) was used to represent the diversity profiles of each environment in a multidimensional space. All analyses were carried using the statistical package R version 3.4.22020. R Core Team. R: A Language and Environment for Statistical Computing 2017.. The level of significance considered for all tests was 95%.
RESULTS
A total of 6.078 Culicoides (96.38% females and 3.62% males) were collected, representing 84 species, comprised of 45 valid species and 39 morphotypes.
Culicoides fusipalpis exhibited the highest abundance (2.178-35.84%), followed by C. dasyophrus (919-15.12%), C. pseudodiabolicus (459-7.55%), C. diabolicus (426-7.01%), C. filarifer (319-5.25%), C. ocumarensi (290-4.77%), C. foxi (231-3.80%), and C. insignis (229-3.77%). The remaining species represented less than 3% of the collected specimens (Table 1). The most abundant species in peridomiciles were C. fusipalpis (1.641-44.05%) and C. diabolicus (416-11.17%); the most abundant species in capoeira were C. pseudodiabolicus (27-31.77%) and C. fusipalpis (20-23.53%); the most abundant species at the forest edge were C. dasyophrus (745-47.79%) and C. fusipalpis (430-27.59%); and the most abundant species in forests were C. pseudiabolicus (246-34.75%) and C. fusipalpis (87-12.29%) (Table 1).
Of the incriminated and putative vectors recorded (Table 1): C. paraensis was found primarily in peridomiciles; C. insignis was most abundant in peridomiciles near corrals and chicken coops; a single specimen of C. pusillus was collected in a peridomicile near a corral; C. filariferus was found in all environments except capoeira; C. flavivenula exhibited low abundance in forests and peridomiciles; C. foxi occurred in all environments; and C. ignacioi occurred in all environments except forests.
Richness between environments varied from 22 to 58 species/morphotypes. Abundance varied significantly between environments, with values ranging from 85 to 3.725 individuals (Table 1). Species diversity was highest in forests (H’= 2.55) and lowest at the forest edge (H’=1.71). H’ values showed the following gradient: forest > capoeira > peridomicile > forest edge. The equitability (J’) index was greater in capoeira and forest than in peridomicile and the forest edge (Table 1), which indicates that Culicoides individuals are more equitably distributed among different species in capoeira and forest environments.
Similarity was greater between the forest and capoeira than between capoeira and peridomiciles. The population compositions of each environment differed statistically (PERMANOVA S.S=1.61, PSEUDO-F=1.96, p=0.04) (Figure 2 and Figure 3). Richness differed between environments, but rarefaction estimates indicate that environments of the same type possessed similar levels of richness (Table 1 and Figure 4).
Rényi diversity profiles of Culicoides for the four environments investigated: capoeira (successional vegetation), forest, forest edge, and peridomicile in the rural settlement of Rio Pardo, Presidente Figueiredo Municipality, Amazonas, Brazil. Circles show the values for each site, and dashed lines show the median and extreme values.
Non-metric multidimensional scaling (NMDS) showing Culicoides diversity profiles in capoeira, forest, forest edge, and peridomicile environments in the rural settlement of Rio Pardo, Presidente Figueiredo Municipality, Amazonas, Brazil.
Rarefaction curves representing the species richness of Culicoides in capoeira, forest, forest edge, and peridomicile environments in the rural settlement of Rio Pardo, Presidente Figueiredo Municipality, Amazonas, Brazil (95% CI).
DISCUSSION
Eighty-four Culicoides species/morphotypes were collected in the rural settlement of Rio Pardo, representing 69% of the known Culicoides species found in the Brazilian Amazon Basin88. Santarém M, Felippe-Bauer M. Brazilian species of biting midges. Fundação Oswaldo Cruz. 2019. Available from: https://portal.fiocruz.br/sites/portal.fiocruz.br/files/documentos/brazilian_species_of_biting_midges_2019.pdf
https://portal.fiocruz.br/sites/portal.f...
. Previous studies conducted in Rio Pardo recorded five new species of Culicoides and nine new occurrences1717. Santarém MCA, Farias ES, Felippe-Bauer ML. Culicoides castelloni sp. nov. from the Brazilian Amazon Region with a revision of the reticulatus species group (Diptera, Ceratopogonidae). An Acad Bras Cienc. 2015;87(2):955-72. http://dx.doi.org/10.1590/0001-3765201520140517
https://doi.org/http://dx.doi.org/10.159...
,2121. Santarém MCA, Trindade RLD, Silva TDND, Castellón EG, Patiu CADM, Felippe-Bauer ML. New Neotropical Culicoides and redescription of Culicoides reticulatus Lutz (Diptera: Ceratopogonidae). Zoot. 2014;3795(3):255-74. http://dx.doi.org/10.11646/zootaxa.3795.3.2
https://doi.org/http://dx.doi.org/10.116...
-2222. Farias ES, Almeida JF, Pessoa FAC. List of Culicoides biting midges (Diptera: Ceratopogonidae) from the state of Amazonas, Brazil, including new records. Check List. 2016;12(6):2002. doi: 10.15560/12.6.2002.
https://doi.org/10.15560/12.6.2002...
. Until now, the highest levels of richness in Brazil have been recorded in the municipality of Belém in Pará State, with 50 species; followed by Porto Velho in Rondônia, with 40 species; Alto Alegre in Roraima, with 38 species; and Manaus and Tefé in Amazonas, with 35 species and 19 species, respectively2323. Aparício AS, Castellón GE, Fonseca FO. Distribution of Culicoides (Diptera: Ceratopogonidae) in the Amazon region using geoprocess technics. Rev Colomb Cienc Anim. 2011;3(2):283-99.
24. Farias ES, Júnior AMP, Almeida JF, Pessoa FAC, Medeiros JF. Hematophagous biting midges (Diptera: Ceratopogonidae) from Tefé municipality, Amazonas state, Brazil. Check List . 2015;11(4):1676p. doi: http://dx.doi.org/10.15560/11.4.1676
https://doi.org/http://dx.doi.org/10.155...
-2525. Carvalho LPC, Farias ES, Gil LHS, Pessoa FAC, Medeiros JF. New species records of Culicoides biting midges (Diptera: Ceratopogonidae) for the state of Rondônia in Brazilian Amazon. Biodiv Dat J. 2017;(5):e13075. doi: 10.3897 / BDJ.5.e13075. eCollection 2017
https://doi.org/10.3897 / BDJ.5.e13075...
.
Species of medical and veterinary importance were found primarily in peridomiciles, these include: Culicoides paraensis, which is a vector of OROV in humans; C. insignis and C. pusillus, which are vectors of BTV in domestic and wild ruminants; C. filariferus and C. flavivenula, which have been found carrying Leishmania amazonensis DNA; and C. foxi and C. ignacioi which have been found carrying Le. braziliensis DNA99. Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol. 2000;45:307-40. doi: 10.1146/annurev.ento.45.1.307
https://doi.org/10.1146/annurev.ento.45....
,2626. Rebêlo JMM, Rodrigues BL, Bandeira MCA, Moraes JLP, Fonteles RS, Pereira SRF. Detection of Leishmania amazonensis and Leishmania braziliensis in Culicoides (Diptera, Ceratopogonidae) in an endemic area of cutaneous leishmaniasis in the Brazilian Amazonia. J Vector Ecol. 2016;41(2):303-8. doi: 10.1111 / jvec.12227
https://doi.org/10.1111 / jvec.12227...
. All of these species were found in this study, but some in low abundance. This is probably due to the collection method. In entomological inventories, it is common for some species to appear with low frequency because bait type, capture effort, collection environment, and the presence of animals favors the capture of other species2727. Costa JC, Lorosa ES, Moraes JLP, Rebêlo JMM. Espécies de Culicoides (Diptera; Ceratopogonidae) e hospedeiros potenciais em área de ecoturismo do Parque Nacional dos Lençóis Maranhenses, Brasil. Rev Pan-amaz Saúde. 2013;4(3):11-8. doi.org/10.5123/S2176-62232013000300002
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. This low frequency may also be related to the fact that some species are diurnal while others are nocturnal2828. Hoch AL, Roberts DR, Pinheiro FP. Host-seeking behavior and seasonal abundance of Culicoides paraensis (Diptera: Ceratopogonidae) in Brazil. J Am Mosq Control Assoc. 1990;6(1):110-4.-2929. Koch HG, Axtell RC. Attraction of Culicoides furens and C. hollensis (Diptera: Ceratopogonidae) to animal hosts in a salt marsh habitat. J Med Entomol . 1979;15(5-6):494-9. https://doi.org/10.1093/jmedent/15.5-6.494
https://doi.org/https://doi.org/10.1093/...
.
Few studies conducted in the Amazon have examined Culicoides anthropophily. Of the species identified in this study, the following are known to exhibit anthropophilic behavior: Culicoides batesi; C. benarrochei; C. debilipalpis; C. flavivenula; C. fluviatilis; C. foxi; C. fusipalpis; C. glabellus; C. ignacioi; C. insignis; C. leopondoi; C. limai; C. lutzi; C. paraensis; C. paraignacioi; C. paramaruim; C. pseudodiabolicus and C. pusillus44. Castellón EG. Culicoides (Diptera: Ceratopogonidae) na Amazônia Brasileira. II. Espécies coletadas na Reserva Florestal Ducke, aspectos ecológicos e distribuição geográfica. Act Amaz. 1990;20:83-93. http://dx.doi.org/10.1590/1809-43921990201093
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,3030. Aitken THG, Wirth WW, Williams RW, Davies JB, Tikasingh ES. A review of the bloodsucking midges of Trinidad and Tobago, West Indies (Diptera: Ceratopogonidae). J Entomol Ser B Taxon. 1975;44(2):101-44. doi:10.1111/j.1365-3113.1975.tb00007.x
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31. Trindade RL, Gorayeb IS. Maruins (Ceratopogonidae: Diptera) do estuário do Rio Pará e do litoral do Estado do Pará, Brasil. Entomol Vect. 2005;12(1):61-74. http://dx.doi.org/10.1590/S0328-03812005000100005.
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-3232. Trindade RL, Gorayeb IS. Maruins (Diptera: Ceratopogonidae: Culicoides), após a estação chuvosa, na Reserva de Desenvolvimento Sustentável Itatupã-Baquiá, Gurupá, Pará, Brasil. Rev Pan-Amaz Saúde. 2010;1(2):121-30. http://dx.doi.org/10.5123/S2176-62232010000200015
https://doi.org/http://dx.doi.org/10.512...
. Of these, all except C. glabellus were found in peridomiciles. Santiago-Alarcon et al. (2013)3333. Santiago-Alarcon D, Havelka P, Pineda E, Segelbacher G, Schaefer HM. Urban florests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians. Parasitol. 2013;140(14):1799-810. doi: 10.1017/S0031182013001285
https://doi.org/10.1017/S003118201300128...
argue that humans may serve as blood meal sources for dominant Culicoides species in peridomicile environments.
Abundance was greatest in peridomiciles, followed by the forest edge, forest, and capoeira. Culicoides fusipalpis has been observed in high abundance in anthropic environments where it feeds on a variety of blood meal sources, including humans, other mammals and birds3434. Santarém MCA, Confalonieri UEC, Felippe-Bauer ML. Diversity of Culicoides (Diptera: Ceratopogonidae) in the National Forest of Caxiuanã, Melgaço, Pará State, Brazil. Rev Pan-Amaz Saúde . 2010;1(4):29-33. http://dx.doi.org/10.5123/S2176-62232010000400005.t
https://doi.org/http://dx.doi.org/10.512...
. Species richness was greatest in peridomiciles, followed by forest, forest edge, and capoeira. The concentration of a variety of blood meal sources and the presence of suitable breeding sites may be attracting Culicoides to peridomiciles. Santiago-Alarcon et al. (2013)3333. Santiago-Alarcon D, Havelka P, Pineda E, Segelbacher G, Schaefer HM. Urban florests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians. Parasitol. 2013;140(14):1799-810. doi: 10.1017/S0031182013001285
https://doi.org/10.1017/S003118201300128...
surveyed Culicoides feeding behavior in households near an urban forest in Germany where the dominant Culicoides species were known to be ornithophilous and found that blood ingested by these midges contained the mitochondrial DNA of mammals such as cows and humans. Generalist species are able to tolerate a broad set of environmental conditions and make use of a wide range of resources, which allows them to become both widespread and locally abundant (Brown, 1984)3535. Brown JH. On the Relationship between Abundance and Distribution of Species. Am Nat. 1984;124(2):255-79. doi: 10.1086/284267
https://doi.org/10.1086/284267...
.
In Rio Pardo, species diversity was highest in forests, while richness and abundance was highest in peridomiciles. In a study conducted in Rondônia, Carvalho et al. (2016)3636. Carvalho LPC, Pereira Júnior AM, Farias ES, Almeida JF, Rodrigues MS, Resadore F, Pessoa FAC, Medeiro JF. A study of Culicoides in Rondônia, in the Brazilian Amazon: species composition, relative abundance and potential vectors. Med Vet Entomol. 2016;31(1):117-22. doi.org/10.1111/mve.12208.
https://doi.org/10.1111/mve.12208...
found that species diversity was higher in forests than in pasture. In a study conducted in rural and urban areas in Maranhão, Silva and Carvalho (2013)55. Silva FS, Carvalho LPC. A Population Study of the Culicoides Biting Midges (Diptera: Ceratopogonidae) in Urban, Rural, and Forested Sites in a Cerrado Area of Northeastern Brazil. Ann Entomol Soc Am. 2013;106(4):463-70. doi: 10.1603/AN12047
https://doi.org/10.1603/AN12047...
found that species diversity was highest in the Cerrado (savanna) and in gallery forests, while richness and abundance were highest in peridomiciles.
Equitability was highest in capoeira environments, where the number of individuals per species ranged from 1 to 27, and equitability was lowest in the forest edge environments, where the number of individuals per species ranged from 1 to 745 (Table 1). The high equitability observed in capoeira environments is the result of low abundance and a relatively homogeneous distribution of species. The low equitability observed in forest edge environments is likely due to an uneven distribution of species abundance caused by the predominance of C. dasyophrus, which comprised 47.76% of all individuals collected at the forest edge. These findings demonstrate that the local diversity index may decrease in environments where one species is highly dominant.
Species similarity between environments was low (> 50%), which is likely due to the different degrees of anthropic interference present in each environment. Capoeira-forest edge and forest-forest edge exhibited the highest similarity. These findings suggest that strictly wild Culicoides fauna tends to adapt to anthropized environments.
We observed that richness differed between environments, but rarefaction estimates indicate that environments of the same type possessed similar levels of richness. This is probably due to the three-month capture effort occurring during the dry season, a period that the abundance of general hematophagous dipteria are low1313. Ramos WR, Medeiros JF, Julião GR, Ríos-Velásquez CM, Marialva EF, Desmouliére SJM, Luz SL, Pessoa FA. Anthropic effects on sand fly (Diptera: Psychodidae) abundance and diversity in an Amazonian rural settlement, Brazil. Acta Trop. 2014;139:44-52. doi: 10.1016 / j.actatropica.2014.06.017
https://doi.org/10.1016 / j.actatropica....
, which may have interfered with the results, indicating the need for more captures and in different seasons.
The data obtained in this study indicate that diversity was higher in natural environments (forest) than in anthropized environments (capoeira), while abundance and richness were both highest in the most anthropized environment (peridomiciles). It is likely that the concentration of a variety of food sources and the presence of suitable breeding grounds in peridomiciles favors the establishment of certain species.
In settled areas, the presence of domestic and wild animals provides vectors with a rich variety of food sources and this fosters their adaptation to new environments. This behavior may alter pathogen transmission dynamics and increase the risk of disease transmission by Culicoides.
ACKNOWLEDGMENTS
To the CT-Amazônia CNPq/FAPEAM project, “Risk of vector-borne diseases in the central Amazon: effect of deforestation and human population density”. To the Brazilian Council for Scientific and Technological Development (CNPq) for FAC Pessoa research scholarship, and JA Feijó research scholarship number 141323/2019-1. To Dr. Maria Luiza Felippe Bauer-FIOCRUZ/IOC, for the Culicoides taxonomy training.
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Financial Support: Fundação de Amparo à Pesquisa do Estado do Amazonas-FAPEAM-Project number 062.01844/2014 and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES-process number 001.
Publication Dates
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Publication in this collection
18 May 2020 -
Date of issue
2020
History
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Received
19 Feb 2020 -
Accepted
24 Mar 2020