Acta Tropica 237 (2023) 106734
Available online 29 October 2022
0001-706X/© 2022 Published by Elsevier B.V.
Tabanidae (Diptera) captured on horses in Amazon Forest fragments of the state of Rond onia, Brazil ˆ
Tallita Beatriz de Oliveira Zamarchi
a,*, Augusto Loureiro Henriques
b, Tiago Kütter Krolow
c, Rodrigo Ferreira Krüger
d, Gratchela Dutra Rodrigues
d, Amanda Munari
e,
Felipe Arley Costa Pessoa
a, e Luís Marcelo Aranha Camargo
a,f,g,h,iaFundaç˜ao Oswaldo Cruz, Instituto Leˆonidas e Maria Deane, Manaus, AM, Brasil
bInstituto Nacional de Pesquisa da Amazˆonia, Coordenaç˜ao de Biodiversidade, Manaus, AM, Brazil
cUniversidade Federal do Tocantins, Programa de P´os-Graduaç˜ao em Biodiversidade, Ecologia e Conservaç˜ao, Porto Nacional, TO, Brazil
dUniversidade Federal de Pelotas, Departamento de Microbiologia e Parasitologia, Laborat´orio de Ecologia de Parasitos e Vetores, Pelotas, RS, Brazil
eUniversidade Federal de Pelotas, Centro de Desenvolvimento Tecnol´ogico, Programa de P´os-Graduaç˜ao em Biotecnologia, Pelotas, RS, Brazil
fUniversidade de S˜ao Paulo, Instituto de Ciˆencias Biom´edicas 5, Monte Negro, RO, Brasil
gCentro Universit´ario S˜ao Lucas, Porto Velho, RO, Brazil
hInstituto Nacional de Epidemiologia da Amazˆonia Ocidental, Porto Velho, RO, Brazil
iCentro de Pesquisa em Medicina Tropical, Porto Velho, RO, Brazil
A R T I C L E I N F O Keywords:
Horse flies Animal bait Amazon Seasonality
A B S T R A C T
Tabanidae is one of the most diverse families of hematophagous dipterans. Tabanids, in general, are mechanical vectors of some pathogens. Given the vector importance and the lack of knowledge of the tabanid fauna in horses in Amazon Forest fragments of the state of Rondˆonia, this work aimed to determine the season that the different species of horse flies prefer to carryout hematophagy on horses and verify whether the horse fly community remains the same throughout the year. The sampling areas for tabanid captures were in the municipality of Monte Negro, Western Amazon, Brazil. Four new occurrences were recorded for the state of Rondˆonia: Sten- otabanus albilinearis, Tabanus fuscofasciatus, T. macquarti and T. restrepoensis, which increases the number of species for the state to 109. The horse flies were most frequently collected on the hind leg (43.15%) and front leg (31.11%), followed by the belly (7.41%) and the ear (5.18%). In the other anatomical regions, the collection frequency was 13.15% of the remaining individuals.
1. Introduction
Tabanidae is one of the most diverse families of hematophagous dipterans and has about 4500 species in 144 genera, with a high occurrence in the tropics and in humid and temperate regions (Fairchild 1969; Coscar´on and Papavero 2009; Baldacchino et al., 2014; Mullens 2019). The Neotropical region possesses the greatest biodiversity, with 1205 species, of which 475 species occur in Brazil and, before this study, 105 species had been recorded in the state of Rondonia (Henriques and ˆ Gorayeb 1993; Henriques 1997; Coscar´on and Papavero 2009; Henri- ques et al. 2012; Krolow et al., 2015; Krolow et al., 2017; Carmo and Henriques 2019; Gualdr´on-Díaz and Gorayeb 2020; Henriques et al., 2022).
The female horse flies of most of the species are hematophagous and
noxious to their hosts and, due to their painful, irritating and insistent biting, are therefore considered uncomfortable pests for humans, wild animals and livestock. In places where the abundance of horse flies is high, outdoor activities and tourism are hampered, although such losses are difficult to quantify (Baldacchino et al., 2014; Mullens 2019).
Tabanids, in general, are important mechanical vectors of some pathogens, since the vertebrate host makes some movements to try to avoid or interrupt their painful bites. The transmission of diseases can occur if the host is infected, the flies immediately bite another host with their infected mouthparts to finish the blood meal and subsequently infect the next host (Foil 1989; Barros & Foil 2007; Desquesnes et al., 2009).
In equines, one of the most important diseases occurring in the Amazon basin is equine infectious anemia, which is caused by a
* Corresponding author.
E-mail address: tallitazamarchi@gmail.com (T.B.O. Zamarchi).
Contents lists available at ScienceDirect
Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica
https://doi.org/10.1016/j.actatropica.2022.106734
Received 16 July 2022; Received in revised form 26 October 2022; Accepted 27 October 2022
retrovirus, and its transmission in nature can occur by the infected mouthparts of tabanids. The disease can remain asymptomatic in some animals, however, the symptomatic ones present fever, anemia, pete- chial hemorrhages, and lack of appetite, and the outcome can be death.
In Brazil, putting down animals sick with equine infectious anemia is mandatory, since the disease has no cure (Issel and Coggins 1979; Issel et al., 1988; Carpenter and Chesebro 1989). Tabanids are also incrimi- nated as mechanical and biological vectors of Trypanosoma theileri (Baldacchino et al., 2014) and, in Rondˆonia, the species Chrysops laetus and Dichelacera tetradelta have been detected with these pathogens (Bilheiro et al., 2019).
The state of Rondˆonia is an important area for cattle production, with more than 15 million bovines. Horses are important to farm manage- ment and Rondˆonia possesses the main herd of horses in the Brazilian Amazon, with over than 150 thousand animals, which in 2014 was approximately 3% of the national total (MAPA 2016). The municipality of Monte Negro possesses more than 300 thousand head, and In addi- tion, has 3635 horses and 357,104 cattle registered in 2021 (IDARON 2022a; IDARON 2022b).
Given the importance of the vector and the lack of knowledge of the tabanid fauna in the region, this work aimed to determine the season in which different species of horse flies prefer to perform hematophagy on horses and verify whether the horse fly community remains the same throughout the year. When determining the compositions of the tabanid fauna, it was verified whether the horse flies species prefered certain periods of the day or night to perform hematophagy. In addition, it was assessed whether, throughout the day, species of horse flies prefer a specific area of the host.
2. Materials and methods
Study areas for tabanid captures were located in the municipality of Monte Negro (10◦15′33.0′′S; 63◦17′56.5′′W) in the central region of Rondˆonia, Western Brazilian Amazon. Two points within the munici- pality were selected for captures on horses (Fig. 1), named point 1 (10◦ 28′26.9′′S; 63◦15′18.1′′W) and point 2 (10◦06′21.4′′S; 63◦16′55.7′′
W). Points were chosen for convenience of uniformity and five locations were designated. All selected locations have forest fragments, water- courses, as well as pasture areas with cattle and horses.
The specimens were captured close to the riverbank at both points.
The captures took place during two days at each point from 06:00 h to 18:00 h in the months August 2019, November 2019, February 2020 and May 2020 (the amazon summer tends to occur between the months of june to november, with the months of july to september being the driest). One male horse was used at each point and the animals had similar characteristics, such as, horses were sorrels and males. The horse flies were captured manually, with the aid of an aerial collecting net (35 cm in diameter, 73 cm in depth and 74 cm in rodlength). Horse flies were identified and associated with the anatomical regions of the horses and the hourly period of collection. The identification of horse flies was via direct comparison with previously identified specimens from the Na- tional Institute of Amazonian Research’s (INPA) reference collection and pertinent literature. The vouchers were deposited in the INPA entomology collection.
2.1. Statistical analysis
An exploratory analysis of the collected data was first carried out to verify possible patterns in the collections, such as the frequency of
Fig. 1.Sampling sites for captures of the tabanids collected on horses A) Location of the Brazilian state of Rondˆonia. B) Location of the municipality of Monte Negro in the state of Rondˆonia. C) Sampling sites in the municipality of Monte Negro. D) Location of horses at each sampling site. Source: Google Earth™ Software.
Accessed: 07/09/2020.
species and the distribution throughout the year, hours, and months. In addition, from the database that was built, it was also possible to observe possible trends in relation to the abiotic variables used.
To compare the methods and treatments in terms of abundance, richness, and efficiency (species accumulation curve), rarefaction/
extrapolation curves of Hill numbers (Magurran, 2009) were drawn using the iNEXT package (Hsieh et al., 2016) based on the methodology proposed by Colwell et al. (2012) and Chao et al. (2014).
Another analysis performed was non-metric multidimensional scaling (nMDS), which consists of a particular analysis in which the number of dimensions that should compose all the data variation is established in advance using the Bray-Curtis distance. The nMDS ana- lyses were followed by PERMANOVA considering p<0.05. To perform all the analyses, the R language was used with the iNext and vegan packages, available in the Comprehensive R Archive Network (CRAN).
3. Results
Four new occurrences were recorded for the state of Rondˆonia:
Stenotabanus albilinearis, Tabanus fuscofasciatus, T. macquarti and T. restrepoensis, which increases the number of species for the state to 109.
In two seasons in the two localities, 540 female individuals were captured, which were distributed in 13 genera and 41 species (Table 1).
In the rainy season, 72% of individuals and 73% of the species (S =30) were captured and, in the dry season, 28% of the individuals and 51% of the species (S = 21) were captured. Only 11 species (24%) were captured both seasons (Table 1).
The PERMANOVA did not allow us to verify significant differences between the communities of horse flies in the dry and rainy seasons (F = 0.815, P =0.667). There seems to be a separation of both communities based on the rare species, which are unique to each season (Table 1), but the similarity based on the Bray-Curtis distance was 60%, considering the abundance of species.
The estimated values of Chao for the richness of horse flies were 43.465 ±12.429 and 36.025 ±12.392 for the rainy and dry seasons, respectively, with no trend towards stabilization of the collector curve to the q =0 (red one in the Fig. 2). This is the opposite of the tendency of the stabilization to the q =1 (green one in the Fig. 2) and q =2 (blue one in the Fig. 2).
The lower and upper values of the variation interval of the richness estimator were 32,891 and 92,725, respectively, for the rainy season, and 24,662 and 82,659, respectively, for the dry season. About three and four species above the observed richness in the lower values and 62 and Table 1
Abundance and relative abundance (%) of Tabanidae (Diptera) that landed on the horses in forest fragments of the municipality of Monte Negro, Rondˆonia, Western Brazilian Amazon.
Season
Rainy Dry
Species Point 1 Point 2 Point 1 Point 2 Relative Abundance Abundance
Acanthocera fairchildi Henriques & Rafael, 1992 5 0.93 5
Catachlorops difficilis (Kr¨ober), 1931 5 0.93 5
Catachlorops halteratus Kr¨ober, 1931 1 0.19 1
Chrysops varians Wiedemann, 1828 1 1 0.37 2
Chrysops variegatus (De Geer), 1776 1 3 3 1 1.48 8
Diachlorus curvipes (Fabricius), 1805 1 0.19 1
Dichelacera cervicornis (Fabricius), 1805 2 0.37 2
Dichelacera tetradelta Henriques, 1995 12 1 2.41 13
Leucotabanus albovarius (Walker), 1854 1 1 0.37 2
Leucotabanus exaestuans (Linnaeus), 1758 2 3 2 1.30 7
Leucotabanus pauculus Fairchild, 1951 1 0.19 1
Phaeotabanus nigriflavus (Kr¨ober), 1930 1 0.19 1
Philipotabanus pictus Gorayeb & Rafael, 1984 2 0.37 2
Pityocera cervus (Wiedemann), 1828 43 11 10.00 54
Pityocera pernaquila Gorayeb & Krolow, 20,015 13 2.41 13
Poeciloderas quadripunctatus (Fabricius), 1805 1 0.19 1
Stenotabanus albilinearis Philip, 1960 2 12 2.59 14
Stenotabanus incipiens (Walker), 1860 7 1 1.48 8
Stypommisa apicalis Fairchild & Wilkerson, 1986 4 0.74 4
Stypommisa aripuana Fairchild & Wilkerson, 1986 66 10 14.07 76
Stypommisa captiroptera (Kr¨ober), 1930 1 0.19 1
Stypommisa modica (Hine), 1920 2 1 0.56 3
Tabanus antarcticus Linnaeus, 1758 67 99 10 5 33.52 181
Tabanus discifer Walker, 1850 1 0.19 1
Tabanus discus Wiedemann, 1828 4 0.74 4
Tabanus dorsorufus Carmo and Henriques, 2019 1 0.19 1
Tabanus fuscofasciatus Macquart, 1838 2 0.37 2
Tabanus humboldti Fairchild, 1984 1 0.19 1
Tabanus macquarti Schiner, 1868 1 0.19 1
Tabanus mucronatus Fairchild, 1961 3 10 1 2.59 14
Tabanus nebulosus De Geer, 1776 1 0.19 1
Tabanus occidentalis Linnaeus, 1758 14 8 3 15 7.41 40
Tabanus occidentalis var. dorsovittatus Macquart, 1855 3 2 4 3 2.22 12
Tabanus occidentalis var. modestus Wiedemann, 1828 15 5 6 7 6.11 33
Tabanus piceiventris Rondani, 1848 2 0.37 2
Tabanus pungens Wiedemann, 1828 1 0.19 1
Tabanus restrepoensis Fairchild, 1942 1 0.19 1
Tabanus rondoniensis Henriques, Krolow, Zamarchi & Camargo, 2022 1 0.19 1
Tabanus rubripes Macquart, 1838 7 9 2 3.33 18
Tabanus sorbillans Wiedemann, 1828 1 0.19 1
Tabanus trivittatus Fabricius, 1805 1 0.19 1
Abundance 204 184 107 45 540
Relative Abundance 37.78 34.07 19.82 8.33 100.00
61 species for the upper values for the rainy and dry seasons, respec- tively (30 for rainy and 21 for dry, Table 1).
In the dry season, Stypommisa aripuana was the most abundant spe- cies (14%) while in the rainy season the most abundant species were Tabanus antarcticus (43%) and Pityocera cervus (10%). The most abun- dant species under the horses in both seasons was Tabanus antarcticus (33%), which occurs in both seasons with the highest abundance (~90%
of total population) during the dry season. The other species shared by both seasons was Tabanus occidentalis, with intermediate abundance (~15%), considering the three varieties (Table 1).
The peaks of abundance, with more than 20 individuals collected, shows that T. antarcticus begins to appear on horses in November and highest abundance occurs in February, though it remains in the envi- ronment and on the hosts until May. P. cervus has a peak of abundance only in February (rainy season), and S. aripuana was only captured in
August (dry season) (Fig. 3. Sectorial Graphics).
Fig. 4 shows the occurrence of tabanid species according to the anatomical region of the horses. The horse flies were most frequently captured on the hind leg (43.15%) and front leg (31.11%), followed by the belly (7.41%) and the ears (5.18%). In the other anatomical regions, the collection frequency was 13.15% of the remaining individuals.
The Fig. 5 (per hour) for the four dominant tabanid species showed a preference for landing on the horses at the end of the day, between 5 pm and 6 pm, with an exception for S. aripuana, which occurred between 1 pm and 4 pm.
4. Discussion
The use of the horses as bait for the manual capture resulted in 41 horse flies species and it is the first systematic capture of this Diptera Fig. 2. Species accumulation curve based on the abundance of tabanids captured on horses in forest fragments of the municipality of Monte Negro, Rondˆonia, Western Brazilian Amazon. The solid line represents the observed richness of the collection and the dashed line the richness estimated by Chao 1 with q-values: q = 0 (red), q =1 (green) and q =2 (blue).
Fig. 3. Sectorial representation of the abundance of Pityocera cervus, Stypommisa aripuana and Tabanus antarcticus per month in forest fragments of the mu- nicipality of Monte Negro, Rondˆonia, Western Brazilian Amazon. The shaded areas correspond to peaks of abundance greater than 20 individuals.
family in the Brazilian state of Rondˆonia. The richness represented 38%
of tabanid fauna for Rondˆonia and, according to the collector curve, it seems to agree with the estimated richness for the rainy and dry seasons, which predicts a richness that is much greater than those observed. In general, studies that use horses as attractants and manual collection (Lee et al., 1969; Bassi et al., 2000; Luz-Alves et al., 2007; Parra-Henao et al., 2008; Lima et al., 2015) tend to not have as great a sampling effort as those works that use flight interception traps or use chemical at- tractants, such as octenol (Fairchild 1942; Gorayeb 2000; Man- rique-Saide et al., 2001; Barbosa et al., 2005; Ferreira-Kepler et al.
2010). Therefore, there is a clear tendency for the communities observed in horses to be a subset of the richness of a region that includes species that were not attracted to horses. For this reason, the capture curve and the richness estimates do not predict a stabilization of the curve and, according to Colwell & Coddington (1994), require more collectors and animals as baits to achieve an adequate effort.
The number of horse flies species and abundance reduces from the rainy to the dry season and this is a rather confusing pattern when considering the seasons in the Neotropical region and especially the Brazilian biomes. For example, in the central Amazon, around Manaus, the seasonality patterns of tabanids in relation to the presence of high precipitation and humidity are different from those observed in this study. In the Adolpho Ducke Forest Reserve, the richness of species and abundance of Tabanidae were higher when precipitation and humidity were lower (Oliveira et al., 2007). The same pattern was observed by Ferreira-Keppler et al. (2010), who recorded greater abundance and richness of species from July to December, the driest and hottest period, with peaks of occurrence in October. While in the eastern part of the northern Brazilian Amazon, in the municipalities of Benevides and
Bel´em, Gorayeb (1993) also observed a greater activity of horse flies between October and December, with an inversely proportional rela- tionship with precipitation and humidity, as is observed in the region of Manaus. In the Pantanal, horse fly abundance tends to increase at the beginning of the rainy season in September, with peaks in October, gradually declining until the beginning of the dry season (Barros and Foil 1999; Barros 2001), as observed in this work in Rondˆonia. Clearly, the chronological similarity often does not correspond to the climatic or even ecological similarity in different places, as argued by Ferreir- a-Keppler et al. (2010) and some other factor is predominant in this temporal window of abundance peaks between October and December in the southern hemisphere.
Another consistent pattern shared with other works is the occurrence of three or four species of Tabanidae with high abundance on the horses in different biomes such as the Amazon (Gorayeb 2000), Cerrado (Lima et al., 2015), Pantanal (Barros 2001), Atlantic Forest (Bassi et al., 2000) and Araucaria Forest (Miletti et al. 2011), which normally have different species dominating the community.
In Rondˆonia, of the most abundant species, T. antarcticus was the dominant species as also occurred in the eastern Amazonia (Gorayeb 2000). This species has a peak of abundance in February and may also occur at the beginning of the dry season in Rondˆonia, with a preference for visiting the horses between 5:00 pm and 6:00 pm (dusk). Unlike the abundance pattern in Rondonia, T. antarcticus has two abundance peaks ˆ in the eastern Amazon, one in mid-September to October and the other in April (Gorayeb et al. 1999). Both in Rondˆonia and in the eastern Amazon, T. antarcticus prefers to land on horses at the same time of day (Gorayeb 2000).
Another species that occurred in both seasons with intermediate Fig. 4. Distribution of tabanid species captured in forest fragments of the municipality of Monte Negro, Rondˆonia, Western Brazilian Amazon, according to the anatomical region where they landed on horses.
abundance was T. occidentalis. Three varieties were identified in the captured specimens: T. occidentalis, T. occidentalis var. modestus and T. occidentalis var. dosovittatus. The species had a wide distribution, as does the “dorsovittatus” variety, ranging from southern South America to Mexico (Coscar´on and Papavero 2009). The “modestus” variety occurs in northern Brazil (Gorayeb et al. 1999; Gorayeb 2000; Lima et al., 2015) and occurs in the Atlantic Forest (Bassi et al., 2000). It is also a species identified in the detection of bacteria in the eastern Amazon. In both the eastern Amazon (Gorayeb 2000) and in Mexico (Manrique-Saide et al., 2001), the variety “dorsovittatus” is one of the dominant species in horse fly communities. In Rondˆonia, like T. antarcticus, it prefers to land on horses between 5 pm and 6 pm. In the eastern Amazon, the visitation period for horses ranges from 1 pm to 5 pm and with high abundance (Gorayeb 2000).
On Marambaia Island, in the southeastern region of Brazil, specimens of T. occidentalis preferred to bite on the legs and lower parts of the body (Guimar˜aes et al. 2016). Herein, the most part of them were collected also on the lower parts of the body of the horse.
Pityocera cervus is a species that occurs with low abundance in forest areas and clearings in the central Amazon (Barbosa et al., 2005; Fer- reira-Keppler et al., 2010) and Colombia (Pisciotti and Miranda 2011).
Even in horses in the eastern Amazon, it also occurs in low abundance (Gorayeb 2000), which is a pattern that is quite different from that observed in horses in Rondˆonia, where it was one of the three most abundant species, mainly in February.
Stypommisa aripuana was the most abundant species in the dry sea- son, and occurred more frequently in August. This species was also very abundant on horses in the Cerrado of the state of Tocantins in Brazil (Lima et al., 2015), and did not occur in any other diversity study. Other species are observed with intermediate abundances, such as Stypommisa captyroptera in the eastern Amazon (Gorayeb 2000), S. glandicolor in the central Amazon (Ferreira-Keppler et al., 2010) and in the Cerrado of Tocantins (Lima et al., 2015), with the exception occurring in the work of Barbosa et al. (2005), in which S. glandicolor was one of the dominant
species.
Tabanus are not very selective about the preferred anatomical region, since it was possible to observe that it landed in most of the analyzed areas.
During the capture on the horses, it was observed that the tabanids were generally not able to perform the blood meal on the first attempt, since the horses performed involuntary movements during the onslaught. This attitude was observed by França (1975) and very well explored by Barros and Foil (2007), who observed in detail the behavior of horses in relation to the feeding behavior of horse flies. These authors found that when disturbed by the host’s reaction, some horse flies (4.5–7%) tend to move to new hosts that are between 5 and 25 m away, while approximately 36% return to the same animal. Because of this behavior and the results observed, Barros and Foil (2007) recommend that in areas of high abundance of horse flies, there should be a mini- mum distance of 50 m between horses to reduce discomfort and me- chanical transmission of pathogens.
Finally, Bassi et al. (2000) also point out that anatomical preferences must be associated with the height of flight of tabanids, which would explain the high species richness and abundance of horse flies on the forelegs and hindlegs of horses.
The results obtained by this work allow us to conclude that the species T. antarcticus, P. cervus, S. aripuana and T. occidentalis can be very important in the transmission of pathogens to horses. The importance of these species is due to their high abundance, with emphasis on the first two in the rainy season, mainly in February, and the third in the dry season, mainly in August. The care with the horses must be redoubled in the hours close to the end of the day when the two most abundant species in the rainy season prefer to land on the animals. In the dry season, S. aripuana actively seeks animals throughout the afternoon. All the most abundant species prefer feeding on the forelegs and hindlegs of horses.
Fig. 5. Diurnal activity of the most abundant species Pityocera cervus, Stypommisa aripuana, Tabanus antarcticus and Tabanus occidentalis in forest fragments of the municipality of Monte Negro, Rondonia, Western Brazilian Amazon. The shaded areas correspond to peaks of abundance (Nˆ >8 specimens).
Author agreement statement
Tabanidae (Diptera) captured on horses in Amazon Forest fragments of the State of Rondˆonia, Brazil. We the undersigned declare that this manuscript is original, has not been published before and is not currently being considered for publication elsewhere. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. We understand that the Corresponding Author is the sole contact for the Editorial process. She is responsible for communicating with the other authors about progress, submissions of revisions and final approval of proofs.
Declaration of Competing Interest
Tabanidae (Diptera) captured on horses in Amazon Forest fragments of the State of Rondonia, Brazil. The authors whose names are listed ˆ immediately below certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bu- reaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing ar- rangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.
Data Availability
No data was used for the research described in the article.
Acknowledgements
To Fundaçao de Amparo ˜ `a Pesquisa do Estado de S˜ao Paulo (Fapesp) for financial resources, “Auxílios `a Pesquisa” (grant 2018/09293–4) and Marlon Ferreira de Freitas for the worthy help in the fieldwork. This study was financed in part by the Coordenaç˜ao de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and National Institute of Science, Technology and Epidemiology of the Occidental Amazon Region (INCT-EpiAmo/CNPq). TKK thanks to the Conselho Nacional de Desenvolvimento Científico e Tecnologico for the ´ research grant (CNPq, process number 310214/2021–1).
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