Temporal Variation of the Presence of Rhodnius prolixus (Hemiptera: Reduviidae) Into Rural Dwellings in the Department of Casanare, Eastern Colombia

Abstract

Rhodnius prolixus (Stål, 1859) is the major vector of Trypanosoma cruzi in Colombia and Venezuela. The species is strongly associated with high-altitude ecotopes, such as sylvatic palms (Attalea butyracea), where spatially and temporally stable infestations are established. We investigated temporal variation in regards to the presence of R. prolixus in rural dwellings in the department of Casanare (eastern Colombia) over a period of 12 mo. Thirty houses were sampled from January to December 2017 by installing Maria sensors, collecting triatomines through community entomological surveillance, and conducting a monthly search in each house. The collection of specimens from the houses varied significantly by month with the higher number of collections occurring in the low-rainfall season and the lower number of collections occurring in the months of increased precipitation. The proportions of males, females, and nymphs also varied significantly throughout the time period: nymphs (fifth instar only) were reported only during May, July, and September and significantly greater numbers of females than males were reported in the inspected dwellings in all months. Density, crowding, and colonization indices varied according to the season. A bloodmeal analysis revealed 17 different hosts. A total of 42 randomly selected R. prolixus specimens were subjected to molecular analyses for detection of T. cruzi DNA with 22 found positive (infection prevalence of 52%). In conclusion, we observed a high presence of R. prolixus (infected with T. cruzi) in dwellings close to native palm plantations. These findings indicate a high risk of vector transmission of T. cruzi for people in the study areas and challenges for the current vector control schemes in the region.

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Sampling, Distribution, Dispersal
Temporal Variation of the Presence of Rhodnius prolixus
(Hemiptera: Reduviidae) Into Rural Dwellings in the
Department of Casanare, Eastern Colombia
HelenJineth Rincón-Galvis,1 Plutarco Urbano,1,2 Carolina Hernández,2,3 and
JuanDavid Ramírez2,3,4,
1Grupo de Investigaciones Biológicas de la Orinoquia (GINBIO), Fundación Universitaria Internacional del Trópico Americano
(Unitrópico), Yopal, Colombia, 2Centro de Investigaciones en Microbiología y Parasitología Tropical (CIMPAT), Facultad de
Ciencias, Universidad de los Andes, Bogotá, Colombia, 3Grupo de Investigaciones Microbiológicas-UR (GIMUR), Departamento de
Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia, and4Corresponding author,
e-mail: juand.ramirez@urosario.edu.co
Subject Editor: David Florin
Received 13 May 2019; Editorial decision 25 August 2019
Abstract
Rhodnius prolixus (Stål, 1859)is the major vector of Trypanosoma cruzi in Colombia and Venezuela. The spe-
cies is strongly associated with high-altitude ecotopes, such as sylvatic palms (Attalea butyracea), where spa-
tially and temporally stable infestations are established. We investigated temporal variation in regards to the
presence of R.prolixus in rural dwellings in the department of Casanare (eastern Colombia) over a period of
12 mo. Thirty houses were sampled from January to December 2017 by installing Maria sensors, collecting
triatomines through community entomological surveillance, and conducting a monthly search in each house.
The collection of specimens from the houses varied significantly by month with the higher number of col-
lections occurring in the low-rainfall season and the lower number of collections occurring in the months of
increased precipitation. The proportions of males, females, and nymphs also varied significantly throughout
the time period: nymphs (fifth instar only) were reported only during May, July, and September and signifi-
cantly greater numbers of females than males were reported in the inspected dwellings in all months. Density,
crowding, and colonization indices varied according to the season. Abloodmeal analysis revealed 17 different
hosts. Atotal of 42 randomly selected R.prolixus specimens were subjected to molecular analyses for detec-
tion of T.cruzi DNA with 22 found positive (infection prevalence of 52%). In conclusion, we observed a high
presence of R.prolixus (infected with T.cruzi) in dwellings close to native palm plantations. These findings in-
dicate a high risk of vector transmission of T.cruzi for people in the study areas and challenges for the current
vector control schemes in the region.
Key words: Colombia, temporal variation, Rhodnius prolixus, density, dispersion
American trypanosomiasis, Chagas disease, is a parasitic infection
caused by the protozoan Trypanosoma cruzi (Cortés and Suárez
2005, Montilla et al. 2011, Llano et al. 2014). This parasite is
transmitted by insects of the subfamily Triatominae, when mucous
membranes or wounded skin comes into contact with the parasite-
infected feces of the bug (Guhl etal. 2007, Becerril et al. 2010). In
Colombia, the department of Casanare (eastern Colombia) has the
second highest reported prevalence of T. cruzi infection in humans
(10%), after Arauca (21.1%) (Cortés and Suárez 2005, Guhl etal.
2007, Parra-Henao etal. 2009). Casanare is recognized as a focus of
vector and oral transmission of Chagas disease as well (Angulo etal.
2012, Zuleta etal. 2017, Hernández etal. 2016).
This disease is endemic on the American continent (Dias etal.
2002), where millions of people are affected. In Colombia, it has
been estimated that 5% of the population are infected and 23% live
in areas with high risk of transmission (Hoyos etal. 2007, Llano
etal. 2014). Vector transmission can occur through the domestic,
peri-domestic, and sylvatic cycles (Montilla etal. 2011, Angulo etal.
2012, Guhl and Ramírez 2013). In a process of domicilation that is
dened as sylvatic triatomines entering dwellings and then propa-
gating as evidenced by the presence of at least three developmental
stages (Guhl etal. 2007, Esteban etal. 2017) sylvatic triatomines
can enter dwellings where both shelter and blood of humans and/
or domestic animals can be obtained. This capacity of triatomines
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Journal of Medical Entomology, XX(X), 2019, 1–8
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Research
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2Journal of Medical Entomology, 2019, Vol. XX, No. XX
to disperse from sylvatic ecotopes to human habitations represents
a critical factor in the population dynamics of triatomines and the
epidemiology of Chagas disease as previously reported in Brazil and
Argentina (Zeledon and Rabinovich 1981, Pizarro and Romaña
1998, Canale etal. 1999, Dias-Lima and Sherlock 2000).
The distribution of the 149 known species of triatomines varies
according to their ecological requirements (Justi and Galvão 2017).
In Colombia, 27 species have been recorded, of which 17 have been
found infected with T. cruzi (Parra-Henao etal. 2015, Ayala etal.
2019, Velásquez-Ortiz etal. 2019). In the eastern plains of Colombia
(extending into Venezuela), Triatoma dimidiata (Latreille, 1811),
Triatoma. maculata (Erichson, 1848)and Rhodnius prolixus (Stål,
1859)have been recorded as the main vectors of T.cruzi. Of these,
R.prolixus is the most important in Colombia and Venezuela be-
cause of occurrence in sylvatic, domestic, and peri-domestic ecotopes
(Dias et al. 2002, Angulo and Esteban 2011, Angulo et al. 2012,
Urbano etal. 2015, Esteban etal. 2017, Urbano etal. 2018).
Forests of Attalea butyracea (wine palm) are considered the
main ecological entities for sustaining and establishing colonies
of triatomines, particularly R. prolixus in the eastern plains of
Colombia (Teixeira etal. 2001, Abad-Franch et al. 2005, Angulo
etal. 2012, Urbano etal. 2018). Rueda etal. (2014), observed higher
densities of triatomines in palms located near houses, banana plan-
tations, and fruit trees, than in palms located in secondary forests,
possibly because the former provide conditions (food resource in the
blood of humans and domestic animals) that facilitate domiciliation
of the vector (Guhl etal. 2007, Angulo et al. 2013, Urbano et al.
2015, Urbano etal. 2018). Consequently, humans play an important
role in altering the cycle of transmission of the trypanosome parasite
and the vector, increasing the probability of transmission of the par-
asite (Guhl etal., 2007). It is important to clarify the capacity of this
vector to adapt to different ecotopes and to intrude into homes under
different environmental conditions. Precipitation is one of the most
relevant factors involved in the presence of triatomines in human
dwellings; a higher population density was found in wild popula-
tions of R.prolixus (Urbano etal. 2018), Rhodnius neglectus (Lent,
1954), and Rhodnius robustus (Larouse, 1927)during periods of
low rainfall (Gurgel-Gonçalves etal. 2004, Longa and Scorza 2005).
Such information is required to dene rational surveillance
interventions and to implement control programs in areas where
sylvatic populations of triatomines are potentially involved in the
transmission of Chagas disease (Abad-Franch et al. 2005). Most
rural dwellings in the department of Casanare are immersed in land-
scape matrices whose main structural component consists of sylvatic
palms. This area provides biological, ecological, and environmental
conditions, which favor the eco-epidemiological cycles of the para-
site. The aim of this study was to determine the temporal variation
of R.prolixus in rural dwellings of the Casanare department over a
12-mo period. We also identied the T.cruzi infection and the blood
feeding sources of a random subsample of collected R.prolixus.
Materials and Methods
StudyArea
The study was carried out in the villages of Agualinda in the mu-
nicipality of Pore (5.66278°N, −71.9908°W) and Sabanetas in the
municipality of Paz de Ariporo (5.872663°N, −71.84714°W) of the
department of Casanare (Fig. 1). The area comprises forest matrices
composed of grazing and silvo-pastoral areas (trees, forage, and
the grazing of domesticated animals), in addition to natural and
introduced pastures currently used for extensive cattle ranching.
Plantain, cassava, corn, and cacao crops are the most important
economic activities in these municipalities (Bejarano 2012). These
areas have an average annual temperature of 28± 8°C and average
annual rainfall of 2,000–2,700mm. According to the climatic clas-
sication of Kӧppen (Köppen 1918), a tropical climate is repre-
sented with a marked unimodal seasonality having a period of high
rainfall that extends from May to November with average monthly
precipitation of 329mm, and a period of low rainfall during the re-
maining 5 mo with average monthly precipitation of 89mm, and an
altitude range of 280± 10 m above sea level. The dwellings selected
for monitoring were typically located in grazing areas surrounded
by small cultivated areas and scattered palms near riverine forests,
where the main structural component was sylvatic palms. Ahigh
index of infestation by R.prolixus (3.3%) and cases of infection
in humans (7.2%) had previously been reported for the area (Guhl
etal. 2007, Zuleta etal. 2017).
Sampling
Sampling and monitoring were carried out on a total of 30 houses,
12 selected from the village of Sabanetas (Paz de Ariporo) and 18
from the village of Agualinda (Pore). Maria sensors were installed in
these houses, according to the methodology proposed by Wisnivesky-
Colli etal. (1992) and triatomines were collected through commu-
nity entomological surveillance by families trained in recognition of,
searching for, and collection of the triatomine insects. The ‘María
Sensors’ (in-house made) are cardboard boxes with absorbent paper
folded inside that, xed to the walls of the house, can passively de-
tect the presence of triatomines. Direct collection of the insects from
the Maria Sensors occurred when periodic monitoring of the boxes
was carried out, or by evidence of the triatomines such as feces, eggs,
or exuvia. Visits were made monthly during 2017, when the num-
bers of triatomines recorded by the installed sensors was checked
and specimens captured by the families were collected. In addition,
an active-man-hour search was carried out inside each house, with
a sampling effort of 16h per month, and triatomines that were at-
tracted by light during 2 d per month from 1,800 to 2,200 were
collected (Jácome-Pinilla etal. 2015). Triatomines were placed in la-
beled plastic containers, with lter paper folded inside, covered with
a tulle cloth and fastened with rubber band, allowing movement and
absorbing excess moisture, for later identication and processing
in the laboratory. Specimens were identied using the keys of Lent
and Wygodzinsky (1979). In addition, a subsample (42 randomly
selected individuals) was selected to carry out molecular analysis
for identication of the infective agent; these specimens were placed
in absolute ethanol and labeled with the household and the month
sampled.
Statistical Analysis
Shapiro–Wilk tests were performed to analyze data normality as-
sumptions and Levene tests to determine the homoscedasticity of
the variables. Subsequently, Kruskal–Wallis nonparametric tests
were applied to determine signicant differences in the popula-
tion densities of R.prolixus among sampling months, and among
nymphs, females, and males. Trends in the density of individuals cap-
tured per month were analyzed using a multiple Dunn test (P > 0.05).
The relationships between the density of R.prolixus and the average
monthly precipitation and temperature in the inspected dwellings
were examined using the Spearman correlation coefcient (P<0.05).
Density (number of triatomines collected/number of houses exam-
ined), crowding (number of triatomines collected/number of positive
houses), infestation (number of positive houses/number of houses
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3Journal of Medical Entomology, 2019, Vol. XX, No. XX
examined × 100), and colonization (number of houses with nymphs/
number of positive houses × 100)were quantied using the meth-
odological parameters proposed by Suarez-Davalos et al. (2010).
Statistical analyses were performed using RStudio software and the
graphics were made with the Origin 5.0 program.
Detection of T.cruzi DNA, Parasite Genotyping, and
Determination of Feeding Sources
A total of 42 randomly selected R.prolixus were subjected to mo-
lecular analyses for detection of T.cruzi DNA, parasite genotyping,
and identication of feeding sources. All specimens were stored and
conserved in ethanol until processing. DNA extraction of the in-
sects’ guts was conducted using a Qiagen Dneasy Blood & Tissue
kit (Qiagen, Berlin, Germany). Detection of T.cruzi was conducted
by end-point quantitative polymerase chain reaction (qPCR) using
TaqMan Fast Advanced Master Mix 2× (Roche Diagnostics GmbH,
Mannheim, Germany), water and the primers cruzi1 (10µM) (5′-
AST CGG CTG ATC GTT TTC-3′), cruzi2 (10µM) (5′-AAT TCC
TCC AAG CAG CGG ATA-3′), and a cruzi3 probe (5µM) (FAM-
CAC ACA CTG GAC ACC AA-NFQ-MGB) to detect the satellite
tandem repeat DNA of the parasite (166bp), following the proce-
dure previously reported (Hernández etal. 2016). A Ct value <38
was considered as positive amplication. For insects with a positive
qPCR result, a conventional PCR for kinetoplast DNA amplication
was conducted using Buffer Taq 10×, MgCl2 50mM, dNTPs 25mM,
Taq Platinum 5 U/µl, water and the primers 121 (50 pmol/µl) (5′-
AAA TAA TGT ACG GGK GAG ATG CAT GA-3′) and 122 (50
Fig. 1. Geographic location of the villages of Agualinda and Sabanetas in the municipalities of Pore and Paz de Ariporo, respectively (Casanare). Symbols in
the form of houses represent the locations of the villages and stars indicate the urban centers of the two municipalities. Asterisks represent houses that were
monitored in each municipality.
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4Journal of Medical Entomology, 2019, Vol. XX, No. XX
pmol/µl) (5′-GGT TCG ATT GGG GTT GGT GTA ATA TA-3′) to
discriminate between T.cruzi (330bp) and T.rangeli (400–450bp),
as reported elsewhere (Ramírez etal. 2009). Parasite genotyping was
accomplished by amplication of the spliced leader intergenic region
of the miniexon gene (SL-IR), dividing discrete typing units into two
groups: TcI (350bp) and TcII–T cVI (300bp) as reported elsewhere
(Ramírez etal. 2010).
To determine the blood feeding sources, a 215-bp fragment of the
12S gene fragment was amplied using Go Taq Green Master Mix,
water and primers L1085 (10nM) (5′-CCC AAA CTG GGA TTA
GAT ACC C-3′) and H1259 (10nM) (5′-GTT TGC TGA AGA TGG
CGG TA-3′), as reported by Dumonteil et al. (2018). PCR prod-
ucts were cleaned using ExoSAP-IT Express PCR Product Cleanup
75001/75002 (Affymetrix, Thermo Fisher Scientic Inc., Waltham,
MA) and then submitted to Sanger sequencing. Resulting sequences
were edited in MEGA X software and submitted to BLASTn for
similarity search.
Results
A total of 2,240 specimens of R.prolixus were collected with density
variation recorded according to the month sampled. Despite the use
of Maria sensors to ensure the maximum collection of insects, these
sensors did not collect or detect any specimens. Triatomines were
detected only in each of the inspected homes by communitarian sur-
veillance and active-man-hour search. The months, organized from
lowest to highest with respect to the numbers of individuals col-
lected, were: 125 in July, 130 in September, 132 in August, 136 in
June, 141 in October, 149 in November, 185 in May, 205 in March,
210 in April, 223 in December, 289 in January, and 316 in February.
Presence
The population density of captured R.prolixus varied signicantly
among months (Kruskal–Wallis, χ2=51.12, P< 0.05). The highest
densities of presence of triatomines into homes were observed in
February, January, December, April, and March, and the lowest
densities were observed in May, November, October, June, August,
September, and July (Dunn test, P<0.05). The density of individuals
captured per dwelling was signicantly higher in the period of low
rainfall than during high rainfall (Dunn test, P< 0.05). However,
the period of transition from low to high rainfall (April and May)
also recorded high densities of individuals in the dwellings (Fig. 2).
In the case of temperature, this variable was homogenous across the
year with an average temperature of 26.4°C. Therefore, we were not
able to nd an association between insect’s density and temperature.
Statistically signicant differences were found among the monthly
samples in the densities of males, females, and nymphs (fth instar)
of R.prolixus (Kruskal–Wallis, χ2=9,573.12, P<0.05). The propor-
tion of females recorded in the inspected houses was higher than that
of males in all months. The highest presence densities of females rel-
ative to males were recorded in February, January, December, April,
and March. Nymphs were reported only in the months of May, July,
and September (Fig. 3).
Entomological Indexes
The months of low rainfall had higher density and crowding indexes.
The colonization index estimates the number of micro-habitats in
which immature stages of development are found with respect to the
number of habitats in which an individual is collected. There was ev-
idence of possible colonization only in the months of May, July, and
September (Table 1). In contrast, the index of infestation was rela-
tively high throughout the year; although the number of individuals
arriving per dwelling uctuated according to the season, there was
continuous presence of individuals throughout theyear.
Presence and Precipitation
As the average monthly precipitation levels increased, the number
of individuals arriving at the dwellings decreased (Spearman coef-
cient=−0.6643) indicating greater presence into dwellings during
the months of low rainfall (P= 0.0021) (Fig. 4). During the 7 mo
from May to November with the greatest precipitation, the detection
of triatomines was low as evidenced by only 998 specimens (44.5%
of the total for the year) collected, while the 5 mo of lower rainfall
from December to April recorded 1,243 insects (55.4%). In the case
of temperature, detections did not vary signicantly.
Detection of T.cruzi Infection, Parasite Genotyping,
and Determination of Blood Sources
We analyzed 20 R.prolixus individuals from Paz de Ariporo. Eight
(40%) were found infected with T.cruzi and subsequently four were
Fig. 2. Numbers of Rhodnius prolixus specimens (adults and nymphs) col-
lected per dwelling during the sampling months in the villages of Agualinda
(Pore) and Sabaneta (Paz de Ariporo) in the department of Casanare. Error
bars are shown during each month of sampling.
Fig. 3. Numbers of Rhodnius prolixus males (Green), females (Blue), and
nymphs (red) collected per dwellings of the villages of Agualinda (Pore) and
Sabaneta (Paz de Ariporo) in the department of Casanare. Error bars are
shown during each month of sampling.
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5Journal of Medical Entomology, 2019, Vol. XX, No. XX
typed as TcI, and two with mixed infections (TcI/TcII–T cVI). At
Pore, we analyzed 22 R. prolixus individuals of which 14 (64%)
were found infected with T.cruzi, of which six were typed as TcI and
four as mixed infections (TcI/T cII–TcVI). In terms of blood sources,
we identied the following BLAST hits: Coendou melanurus (por-
cupine) (seven hits), Homo sapiens (Human) (eight hits), Alouatta
caraya (Howler monkey) (seven hits), Ovis candensis (Sheep) (one
hit), Equus caballus (Horse) (seven hits), Sus scrofa (Pig) (seven
hits), Oryctolagus cuniculus (Rabbit) (two hits), Felis catus (Cat)
(ve hits), Rattus norvegicus (Rat) (one hit), Monodelphis domestica
(Opposum) (four hits), Canis lupus familiaris (Dog) (seven hits),
Didelphis marsupialis (Opposum) (seven hits), Mus musculus
(Mouse) (three hits), Ochotona koslowi (Kozlov’s Pika) (one hit),
Myrmecophaga tridactyla (Giant anteater) (six hits), Xenothrix
mcgregori (The Jamaican monkey) (four hits), and Talpa occidentalis
(Iberian Mole) (two hits). No individuals were positive for T.rangeli.
Discussion
Human habitations provide suitable environments for some
triatomines to easily establish infestations (Gurgel-Gonçalves etal.
2004). Once triatomines establish in dwellings, or in adjacent loca-
tions, they are able to feed on animals and/or people, increasing the
transmission risk of T.cruzi, which in turn would be reected in the
incidence of Chagas disease and the maintenance of triatomines in
the home and peri-domiciliary areas (Rueda etal. 2014, Hernández
etal. 2016). This could explain the high indexes of infestation and
crowding found in this investigation (Table 1). However, the colo-
nization index found was very low and in only a small proportion
of dwellings, which suggests that the species was not establishing
populations within the dwellings. Rather, there were continuous
events of presence throughout the year (Fig. 2), with an index of
home infestation higher than previously recorded for R. prolixus
in other areas of the department (Angulo etal. 2012, Zuleta etal.
2017), and also higher than reported for other species: Rhodnius
ecuadoriensis (Lent & León, 1958)in Ecuador (47.4%) (Grijalva
et al. 2017) and Triatoma infestans (Klug, 1834) in Argentina
(2.9–14.4%) (Espinoza et al. 2017, Cavallo et al. 2018). This is
consistent with the high prevalences of T. cruzi infection (40% in
Paz de Ariporo and 64% in Pore), which were higher than those re-
ported for intradomiciliary triatomines in Brazil (1.8–24.7%) (Ferro
e Silva etal. 2018), Venezuela (0.06%) (Carrasco etal. 2014), and
the Colombian Orinoco (15.78%) (Angulo etal. 2012).
The understanding regarding the feeding sources and T. cruzi
infection in triatomines found in human dwellings has relevance
in terms of transmission dynamics and vector control programs.
For example, in Mexico, the feeding sources conrmed a signi-
cant dispersal of T. dimidiata between habitats (domestic and syl-
vatic) (Torres-Montero 2012). In addition, this has been reported in
T.brasiliensis from Brazil where the authors could hypothesize with
the mammal feeding source information previous concerns about
the potential of several animals to link the sylvatic and domiciliary
T.cruzi cycles (Almeida etal. 2016). Recent work in the Colombian
Orinoco region concluded that A.butyracea palms found in altered
areas provide a similar quality habitat for R.prolixus populations in
terms of bloodmeal availability. Both habitats showed similarities in
vector infection prevalence and potential host species, representing a
single T.cruzi transmission scenario at the introduced oil palm plan-
tation and native Attalea palm interface (Erazo etal. 2019). These
studies augment our ndings of 17 feeding sources and high T.cruzi
infection indicating high risk for Chagas disease transmission in the
studyarea.
Although a high frequency of presence in houses was observed
throughout the year (12-mo period of sampling) (Fig. 2), there was
no evidence of colonization, because the presence of immature stages
was sporadic (Fig. 3, Table 1). This could perhaps be explained by
the rst to fourth instars not having the capacity to disperse the dis-
tance from the palms to the houses. Nevertheless, a study conducted
in Venezuela showed the presence of rst to fourth instar infesting
houses but in the absence of palm surroundings (Feliciangeli etal.
2004). Future studies should consider the sampling of the palms
and houses to unveil the true entomological indexes. In addition,
this highlights one limitation of our study as R.prolixus individuals
were removed from the environment each month, reducing the ef-
fective sample size of the population. In certain houses, the monthly
surveys may have reduced the presence of R.prolixus to near zero.
Thus the next month survey would have been new individuals that
moved in since the previous survey, representing a sample bias. As
we are aware of this possible limitation, the collection of new indi-
viduals each month supports our hypothesis of strong dispersion of
R.prolixus into the houses, which poses a challenge for the vector
control programs in the region.
Table 1. Monthly changes of density, crowding indexes, infestation, and colonization indexes of Rhodnius prolixus in dwellings in the
department of Casanare, during the year 2017
Index Jan. Feb. Mar. Apr. May June July Aug. Sep. Oct. Nov. Dec.
Density 9.6 10.6 6.8 7.0 6.2 4.5 4.2 4.4 4.3 4.7 5.0 7.4
Crowding 10.3 10.9 7.6 8.1 7.4 5.7 5.0 4.7 5.0 5.2 5.3 8.0
Infestation (%) 93.3 96.7 96.7 86.7 83.3 80.0 83.3 93.3 86.7 90.0 93.3 93.3
Colonization (%) 0.0 0.0 0.0 0.0 16.7 0.0 10.7 0.0 15.4 0.0 0.0 0.0
Fig. 4. Changes in the density of R. prolixus (adults and nymphs) in rural
dwellings in the municipalities of Pore and Paz de Ariporo Casanare, and in
the average monthly rainfall reported at the Paz de Ariporo meteorological
station (36011501 of 2017).
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6Journal of Medical Entomology, 2019, Vol. XX, No. XX
In the case of the adults collected, Ayala etal. (2019) recorded the
highest number of triatomine presences into houses in the months of
April and May, and lower densities in the months of higher rainfall.
These observations are consistent with ours, in which we recorded
the largest numbers of R.prolixus individuals reaching homes in the
months of lower average rainfall (Fig. 4), and higher frequency of
arrival at homes in the months of April and May (Fig. 2). This re-
inforces the importance of precipitation in terms of triatomine inva-
sion and entomological indexes. In our case, temperature was not an
important factor as this was constant during the year. In the present
study, an inverse relationship was noted between the number of indi-
viduals per dwelling and the average monthly rainfall (Fig. 4), corrob-
orating earlier studies (Pizarro and Romaña 1998, Longa and Scorza
2005, Vásquez etal. 2013, Esteban etal. 2017, Ayala etal. 2019).
These changes represent a response of the species to environmental
changes, habitat disturbances, and inter- and intraspecic competi-
tion. However, triatomines mitigate exposure of their populations
to these adverse conditions by developing adaptive physiological
and ethological responses to seasons, which may also be reected
in variations in the incidence of developmental stages (Schowalter
2006). The difference noted in the proportions of nymphs and adults
collected in the dwellings could be determined, in the rst instance,
by forced dispersion from wild and peri-domiciliary ecotopes and,
secondly, by physiological adaptations of Triatominae, consisting
of variations of nymphal periods, molting and hatching rates of
eggs, longevity of adults, and the numbers of instars and periods of
starvation (Zeledon and Rabinovich 1981, Arévalo etal. 2007). In
addition, R. prolixus tends to migrate from its original ecotope in
search of food or shelter in some seasons (Noireau and Dujardin
2001), and the immature stages have smaller dispersion distances
than adults (Zeledon and Rabinovich 1981). Likewise, other au-
thors have suggested that the density of triatomines captured in the
months of low rainfall is signicantly higher than during the high
rainfall season (Noireau and Dujardin 2001, Hernández etal. 2010,
Vásquez etal. 2013, Reyes et al. 2017), possibly because the dis-
persion of triatomines is related to their nutritional status during
the dry season. When their wild food sources are reduced, adult
triatomines may migrate toward articial ecotopes in search of alter-
natives sources of blood. This is consistent with our observations of
an inverse relationship between the density of triatomines that reach
dwellings and the average monthly precipitation in the study area,
giving rise to a higher density of triatomines in dwellings in the dry
season (Fig. 4). Similarly, higher population densities were found in
wild populations of R.prolixus (Urbano etal. 2018), R. neglectus,
and R. robustus during periods of low rainfall (Gurgel-Gonçalves
etal. 2004, Longa and Scorza 2005).
Rhodnius prolixus is a species with a wide climatic and alti-
tudinal range. It is frequently found in houses in localities where
the opportunity to colonize domestic structures is present (Noireau
et al. 1994, Esteban etal. 2017). However, according to Esteban
etal. (2017), adaptation of this vector to ecotopes such as palms
means that the presence of immature stages in dwellings could result
from displacement from nearby wild habitats rather than a coloniza-
tion event. The presence of the species in homes has been associated
with decrease in vegetation coverage, the distance to the forest, and
lights from houses at night (Angulo etal. 2012, Erazo and Cordovez
2016). This could explain the low colonization frequency, which was
observed in only three months (Table 1). These results differed from
those found for R.ecuadoriensis and Panstrongylus rufotuberculatus
(Latreille, 1811), which exhibited rates of intradomiciliary coloni-
zation up to 77% (Grijalva etal. 2017). Interestingly, the average
densities of males, females, and nymphs within dwellings showed
the opposite trend to those reported by Esteban etal. (2017) for the
department of Santander (eastern Colombia), where a greater pro-
portion of males were reported to reach homes. Asignicant differ-
ence between collections of females and males (Fig. 3) was detected,
suggesting the composition of populations that enter dwellings is
variable due to previous reports that demonstrate that the male/fe-
male ratio in sylvatic populations is similar (Grijalva et al. 2012,
Urbano etal. 2015).
The high dispersal capacity of R. prolixus is linked to a high
adaptability to invade and colonize different micro-habitats in par-
ticular areas (Heger etal. 2006, Feliciangeli etal. 2007). This was
evidenced in the present investigation by the observation that 100%
of the homes inspected contained triatomines in at least 1 mo, and
that the index of infestation throughout the hydrological period was
relatively constant (Table 1). Conversely, since 100% of the houses
contained triatomines, the presence of the triatomines may also have
been the result of propagation within the houses. Rhodnius prolixus
was recorded in houses of the municipalities of both Pore and Paz de
Ariporo, suggesting that the wide geographical distribution of this
species in Casanare results from its successful colonization of many
species of palm and types of housing. Dispersion of R.prolixus may
occur toward anthropogenic environments where some vertebrate
refuges are present or relict palm species occur (Urbano etal. 2015);
later they behave as intruders in homes in search of food. These fac-
tors have been evaluated for several species of triatomines in other
countries (Fitzpatrick etal. 2008, Grijalva etal. 2014, Ferro e Silva
etal. 2018). An understanding of the mammals that inhabit the palm
forests is important to unveil the blood sources for the triatomines.
However, we do not have information about the diversity of ani-
mals in these palms and therefore cannot formulate a hypothesis in
this regard. The only available information was the high diversity
of blood sources demonstrating that despite having food available,
R.prolixus is attracted to human dwellings, possibly due to light at-
traction (Jácome-Pinilla etal. 2015).
Finally, control strategies for vector transmission of Chagas di-
sease in the department of Casanare have been directed towards
housing interventions with insecticides (Palomino etal. 2007, Silva
etal. 2007, Rendón etal. 2015, Zuleta etal. 2017). However, our
data show that the months in which the probability of dispersion
and presence of insects into houses is greatest corresponds to the
low rainfall period. It is important to keep this in mind in the imple-
mentation of control strategies and epidemiological surveillance in
the department.
Conclusion
The high values of the indices and trends in the presence frequencies
of triatomines in rural dwellings in the department of Casanare indi-
cate a high risk of T.cruzi vectorial transmission in the study areas.
However, the low colonization indexes recorded for R.prolixus in-
dicate that this species is unlikely to exhibit domiciliation. This does
not rule out this process in the future, given that the largest propor-
tion of individuals entering the houses in an intrusive or sporadic
manner were females.
Acknowledgments
The authors wish to express their gratitude to the owners of the homes where the
samplings were made. We thank Harry Taylor, Ph.D., from Edanz Group (www.
edanzediting.com/ac) for editing a draft of this manuscript. This work was funded
by Dirección de Investigación e Innovación from Universidad del Rosario and by
Fundación Universitaria Internacional del Trópico Americano (Unitrópico).
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7Journal of Medical Entomology, 2019, Vol. XX, No. XX
Competing Interests
The authors assert no conict of interest. All authors have read and
approved the manuscript and its analyses.
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