T r e n d s i n

Entomology
Vol. 14, 2018

Eco-epidemiological aspects of mosquitoes of the genus

Haemagogus and Sabethes involved in sylvatic yellow fever
transmission in Brazil
Marli do Carmo Cupertino1,2, Taciana de Souza Bayão2, Andréia Patrícia Gomes2,
Nicholas Mayers2,3 and Rodrigo Siqueira-Batista1,2,*
1
Medical School, Faculdade Dinâmica do Vale do Piranga, Ponte Nova;
2
Laboratory of Epidemiological and Computational Methods in Health,
Department of Medicine and Nursing, 3Department of Veterinary Medicine,
Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.

ABSTRACT transvaginal and transestadial transmission from

Brazil, Angola, Democratic Republic of Congo
and Nigeria recorded significant yellow fever
(YF) outbreaks during 2016, 2017 and 2018,
attributing to several deaths. YF is caused by a
virus (Flavivirus) which is transmitted to humans
through infected mosquito bites. The sylvatic YF
reemergence, despite the availability of an effective
vaccine, requires more research to identify the
geographical distribution and eco-epidemiological
aspects of the sylvatic mosquito species consociated
with the yellow fever disease sustention and
consequent dissemination. According to the World
Health Organization, these recent outbreaks are
forewarnings of worse to come, if no action
is taken. Understanding mosquitoes’ biology
facilitates the control and prevention of YF,
and is vital in situations where the vaccination
coverage is low or the vaccine is not readily
available. The aim of this study is to review
and describe the biological and ecological aspects
of the mosquito genera Haemagogus and Sabethes,
being the two most prevalent vectors and
repositories of this virus type, and their role in
the preservation and transmission of sylvatic YF
in Brazil, imperatively noting the probability of
*Corresponding author: rsiqueirabatista@yahoo.com.br
female mosquitoes to their eggs and resultant
larvae, which further perpetuates the disease. This
transmittal adaptation may explain the isolated
outbreaks in previously uninfected areas. Another
contributing factor to recent outbreaks is the
change in human lifestyles, ingenuously invading
forest areas triggering inadvertent infections.
This circumstance would be efficiently controlled
if population growth did not invade these
vector-infested & virus-infected forest ecosystems.
Moreover, the degradation of these sylvatic
mosquito habitats and their propensity to explore
instigates their permeation throughout urban
areas, enhancing mosquito-human interactions.
The results contributed to the formation of an
environmental surveillance, incorporating the
analysis of the influence of geographical locations
of the mosquitoes within YF outbreak regions,
capacitating the creation of prevention alternatives
for new cases.
KEYWORDS: arboviruses, Culicidae, Diptera,
yellow fever.
INTRODUCTION
Yellow fever (YF) is a disease whose etiological
agent is an arbovirus of the family Flaviviridae
and genus Flavivirus, the yellow fever virus
2 Marli do Carmo Cupertino et al.
(YFV), which is transmitted to vertebrates by
arthropod vectors [1]. In general, YFVs have
a common single stranded RNA aspect; they
geographically inhabit the tropical regions of
Africa and South America and can trigger a
wide spectrum of clinical manifestations, from
asymptomatic cases to more ominous situations,
with an inexorable evolution towards death [1, 2].
The initial epidemiological focus of YF in
America remains controversial. Recent research -
based on calculating the number of mutations in
the viral genome - has generated consistent data
confirming that it was “imported” from Africa.
The most likely hypothesis is that the mosquito
eggs traveled in the water tanks brought by slave
ships [3], which is corroborated by the fact that
the disease disseminated throughout the slave
trade route and reached the Caribbean and Latin
America. There were reports of yellow fever-like
signs and symptoms amongst Christopher Columbus’
crew members while traveling to Haiti in the late
fifteenth century [4]. In Brazil, the first yellow
fever epidemic erupted in the 16th century, in
Recife. Thereafter, the disease became a health
and, also, a commercial problem for the country,
which gained worldwide notoriety - negative - as
a dangerous place for travelers, due to the fear
of acquiring the disease.
YF presents two distinct epidemiologically
transmission cycles: sylvatic and urban. From
aetiological, clinical, immunological and
pathophysiological points of view, the disease
is similar in both. In the sylvatic cycle, non-
human primates (in the Americas, monkeys
of the genera Alouatta, Callithrix, Saimiri) [5]
are the main protagonists of the virus, with
Haemagogus (Haemagogus janthinomys,
Haemagogus leucocelaenus and Haemagogus
albomaculatus), Sabethes (Sabethes chloropterus,
Sabethes cyaneus and Sabethes glaucodaemon)
and Aedes (Africa) being the most prevalent
mosquito-vector genera with sylvatic tendencies
[6]. In this cycle, humans involuntarily participate
as fortuitous hosts, when encountering infested
areas of forest, which could be adeptly controlled
if the obstinate population density refrained
from the exploration of virus-infected forest areas.
In addition, the degradation of the primates’
habitat and the aptness of these vertebrates to
prospect new environments cause them to invade
parks and urban areas [3]. In the urban cycle,
humans are the only host with epidemiological
importance and transmission mainly occurs through
the Aedes aegypti species - implicated in the
transmission of other diseases, such as Chikungunya,
Dengue and Zika [7] - which are strongly associated
with the human environment [6, 8].
Outbreaks of YF have occurred sporadically in
Africa and America, although the disease has
a highly effective vaccine, nevertheless, it should
be noted that such events are mainly due to the
ineffectiveness of vaccination campaigns. Current
focal points are those recent occurrences in Brazil,
Angola and the Democratic Republic of Congo,
in 2016, 2017 and 2018 respectively [9, 10].
The previous cases that had occurred in Brazil
(1942) were documented in sylvatic, rural and
forest areas, as being transmitted by the genera
Haemagogus and Sabethes mosquitoes [10].
According to the World Health Organization
(WHO), these are only warnings of major outbreaks
that will come if no action is taken [10, 11].
Based on these preliminary considerations, the
objective of this article is to present a brief review
of the main morphological and ecological aspects
of the genera involved in the YF sylvatic cycle
in Latin America, with emphasis on their contact
and proximity relationship with Homo sapiens
sapiens.
Genus Haemagogus
Mosquitoes, of the genus Haemagogus (Table 1,
Figure 1), described by Williston (1896) [12],
are disseminated throughout the tropical rainforests
of North and South America, where they have
been characterized and studied [13]. They portray
pertinency in human health studies, given
the vector potential of the H. janthinomys,
H. leucocelaenus and H. albomaculatus species
in the propagation of YF, Mayaro, Dengue and
other arbovirus viruses [14, 15].
Representatives of the genus Haemagogus have
an average size of five millimeters, a life
expectancy of around 30 days and possess viral
repositories in their bodies, facilitating infections.
The name Haemagogus comes from the Greek -
haemo = blood; agogus = conduction -, meaning,
therefore, “blood conductor” [12]. This genre
Eco-epidemiological aspects of sylvatic YF vector mosquitoes 3

Table 1. Taxonomy of the genus Haemagogus.

Kingdom Animalia
Phylum Arthropoda
Class Insecta
Subclass Pterygota
Infraclass Neoptera
Superorder Holometabola
Order Diptera
Suborder Nematocera
Infraorder Culicomorpha
Family Culicidae
Genus Haemagogus
Haemagogus janthinomys (Dyar, 1921)
Species Haemagogus leucocelaenus (Dyar & Shannon, 1924)
Haemagogus albomaculatus (Theobald, 1903)

Source: http://www.ncbi.nlm.nih.gov/taxonomy

Figure 1. Mosquito Haemagogus. Sources: Paula Carolina Andrade Mariano

and Ademir Nunes Ribeiro Júnior.

inhabits forests, savannas and similar regions.
It has a special preference for the tree canopies,
considering it is the abode of mosquito food
sources, especially monkeys of the genus Alouatta
[5, 13, 16]. Specimens of this genre manage
to sustain flight for more than five kilometers,
preferably at dusk, taking advantage of the
evening breeze. The female Haemagogus are
particularly selective, always looking for fresh
food and new places to spawn. This is a complex
task, even for insects, like Haemagogus, although
capable of long distance travel. In this pursuit,
they can travel from one closed forest area to
another or fly along the forest edges. This ease
of movement and aptitude to fly long distances
is correlated with the amplification of sylvatic
yellow fever [17].
A distinctive morphological observation of this
genus can be depicted by the presence of silver
scales on the thorax, extending from the shield
to lower limbs. Haemagogus can be differentiated
from other mosquitoes by the absence of
4 Marli do Carmo Cupertino et al.
mesonotums. The palps of the females are small,
whereas the palps of the males may vary in
length [18]. Although there are three divisions
(Albomaculatus, Splendens and Tropicalis), this
genus is visibly quite homogeneous in its physical
presentation [13].
The time between generations of H. janthinomys
is approximately 35 days, its gonotrophic cycle
varies from 10 to 12 days, and 1 in every 100
mosquitoes persist after two months [14]. In order
to reproduce, these insects lay their eggs in the
hollows of the trees, in fallen branches and in
bamboos (in the latter case in regions where there
is accumulation of water formed in the internodes:
the connections between stretches of the stem).
Thus, Haemagogus do not lay their eggs directly
on the aquatic surface, but on the inner wall of the
breeding site near the waters’ edge. When the
eggs are submerged, the larvae hatch and begin to
develop, feeding on the organic matter present
in the water, until they become pupae. About
seven to ten days after egg hatching, Haemagogus
species reach adult mosquito stage [17, 19].
The eating habits of mosquitoes are quite varied.
Only the females bite targeted blood hosts - in
search of the blood that is necessary for the
process of maturing eggs - while the males feed
on nectar. Birds, oxen, non-human primates and
humans are examples of vertebrate targets of
females of this species [12]. The preferred time
to feed is between 11 am and 3 pm (i.e. the
daytime interval when the heat and brightness are
higher). There is no preference for specific body
parts for the blood repast; and it must be
emphasized that the insect can drill fine and fair
clothes [17].
Many Haemagogus species inhabit the treetops
in the forests. Although there are regional and
seasonal variations, the circadian habits of this
genre involve the accomplishment of the sanguine
repast at diurnal periods during the high temperature
hours. Alencar et al. (2008) investigated the
influence of ecological and climatic factors
throughout the days and months, and the ecological
relationships amidst H. capricornii, H. janthinomys
and H. leucocelaenus, in different regions of
Brazil. The results evinced a strong interference
of the climate on the repast schedule. The
“humidity” factor seems to influence the location
of each species, with variable preferences of
humidification in the treetops. On the other hand,
Galvão (1974) analyzed another aspect: how the
proximity of Homo sapiens sapiens to the forests
would influence the displacement of Haemagogus
to the soil [20]. It was perceived that the exit
of the mammalian primates would incite the
mosquitoes to look for other food sources below
the trees, a more significant event as opposed
to deforestation. The significant presence of
H. janthinomys at the soil level would even
represent a bioindicator of forest felling [21].
To assess the infection risk in humans, it is
important to verify the parameters of daily
survival rate, sting index and infection rate of this
species, which, according to some studies [14],
manifest favorable vector-human contact indices
(i.e. between H. janthinomys and H. sapiens
sapiens). It is estimated that the bites on the
humans occur at ground level and are predominant
in the lower limbs [13]. The urban invasion of
these mosquitoes, although rare, has been evinced
by the species H. albomaculatus, whose flight
amplitude is extensive [14]. In this way, civil
constructions near the woods are forewarnings
for possible contact of Haemagogus mosquitoes
with humans.
As aforementioned, the maturation of the larval
phases of Haemagogus often occurs in hollows
of trees and bamboos. However, there are reports
of evolutionary development of the species
H. equinus and H. leucocelaenus in places such
as rock puddles, raising the possibility of the
adaptation in urban environments [22, 23].
Moreover, the H. janthinomys lays its eggs in
accordance with the climatic conditions (e.g.
humidity levels), which can induce the gradual
hatching of the immersions. Such a mechanism
would be an intelligent evolutionary strategy
in the production of mosquitoes at different times
of the year [24]. However, as organisms involved
in the YF cycle, they represent an imminent threat,
considering they substantiate the hypothesis that
these species act not only as potential vectors but
also as feasible reservoirs.
A study carried out by Alencar et al. (2008)
verified the biodiversity of sylvatic mosquito
populations (Culicidae) as a potential arbovirus
transmissibility factor in urban areas, accentuating
Eco-epidemiological aspects of sylvatic YF vector mosquitoes 5

two species of mosquitoes with higher population Genus Sabethes

density (H. janthinomys and H. leucocelaenus)
in the investigated region. The authors emphasized
that although there is no evidence of YF
transmissibility by these vectors in the urban
region, they represent potential vectors: they
inhabit deforested lands and acclimatize themselves
to breeding in urban areas, suggesting constant
epidemiological surveillance [24].
The morphological study, described by Robineau-
Desvoidy (1827), of the Sabethes (seen in Table 2,
Figure 2), illustrates this species as having shields,
thorax and abdomens covered by metallic scales.
Other common characteristics of this species
include having well-developed antepronuts, antennae,
similar palps (between sexes) and missing superior
poliepisternals. The species of the subgenus

Table 2. Taxonomy of the genus Sabethes.

Kingdom Animalia
Phylum Arthropoda
Class Insecta
Subclass Pterygota
Infraclass Neoptera
Superorder Holometabola
Order Diptera
Suborder Nematocera
Infraorder Culicomorpha
Family Culicidae
Genus Sabethes
Sabethes chloropterus (Humboldt, 1819)
Species Sabethes cyaneus (Fabricius, 1805)
Sabethes glaucodaemon (Dyar & Shannon, 1925)
Source: http://www.ncbi.nlm.nih.gov/taxonomy

Figure 2. Mosquito Sabethes. Sources: Paula Carolina Andrade Mariano and

Ademir Nunes Ribeiro Júnior.
6 Marli do Carmo Cupertino et al.
Sabethoides [25] have medium tarsi with clear
markings [12], with S. chloropterus, S. cyaneus
and S. glaucodaemon being the main transmitters
of sylvatic yellow fever [19].
This group encompasses biologically and
structurally diverse invertebrates, whose geographical
distribution extends close to Ecuador, and manifest
a greater biodiversity in the Americas [26]. They
are sylvatic invertebrates, diurnal, and often
acrodendrophilics. Ecological observations of the
species of Sabethes in the National Forest of
Caxiunã-Pará-Brazil attested the presence of these
insects at heights of approximately 15 m to 30 m
above soil level [19]. Pregnant females are adapted
to spawn in limited orifices with reproductive
proliferation in tree trunks and bamboos, dispatching
their eggs directly onto the surface of the water.
These arthropods reach the adult stage almost
a month later [19]. In the last decade, research
on the species Sabethes cyaneusas, using scanning
electron microscopy, distinguished thick eggs
with smooth surfaces [27]. Additionally, the action
of how hydrophobic structures facilitate their free
flotation on the water surface was observed.
These eggs are sensitive to desiccation, with their
population incidence favoring high humidity.
Their breeding sites rarely dry out during the year
[12]. A study carried out in epizootic areas
for the YFV in Rio Grande do Sul, Brazil,
indicated that the species Sabethes albiprivus
and Sabethes quasycianus had constant reproductive
and hematophagous activity during the seasons
[17].
Although sylvatic, such insects feed on human
blood relatively often. Sabethes chloropterus [28],
subgenus Sabethoides, have greater applicability
in the YF cycle. The first reported instances
of sylvatic YF transmission occurred in Central
America. Adults of this species are characterized
by superior proepisternal setae, vertex of violaceous
tonality, anterpronuts, scaly shields and clear
sternites. The geographical coverage extends
throughout the Americas, with emphasis on
the dense, hot and humid forests in the tropical
zones of Brazil. Open and less humid forests
are detrimental to acrodendrophilia, since
S. chloropterus descends from the upper storeys
to search for other food sources. The mannerism
of frequently flying over the victim before
landing, in face regions (especially the nasal
protuberance), is characteristic of the Sabethes
[12].
Yellow fever propagation cycle: Hypothesis
of “double function vector-reservoir” of the
species Haemagogus and Sabethes
Arbovirus diseases are infections that are sustained
in the environment by ecological relationships
between susceptible hosts and invertebrate
vectors/hosts, where hematophageal females
are responsible for the stinging and propagation
of the virus in vertebrates [10, 29, 30, 31].
Insects of the genera Haemagogus and Sabethes
have a long life span for mosquitoes, which may
favor the propagation of YF. Observations in
the laboratory indicate that their survival rate
perpetuates months after the insects reach
adulthood. This factor is important because, once
infected, the mosquito remains the carrier and
is able to transmit the YFV throughout its
lifespan, supplementary to being able to infect
its eggs and other generations at varying stages
of life (Figure 3). Studies accredit the probability
of transvaginal and transestadial transmission
of a female mosquito to its eggs and then to the
larvae, promoting the continuation of the disease
[32, 33, 34]. This mode of YF transmission,
without the need for a vertebrate host, can explain
isolated outbreaks in areas previously free of the
disease [35, 36].
As shown in Figure 3, after the insect sucks the
blood of a primate - during this period the victim
is within the first three or four days of the fever -
the blood virus passes into the stomach of
the mosquito. Over the next twelve days, if the
concentration is high enough, viruses can infect
epithelial cells and reproduce before they are
passed into the circulatory system of the
mosquito. Thenceforth, the virus will enter the
salivary glands, being injected into the victim
the next time the mosquito feeds. Once human
and viral cells make contact, the receptor-
mediated endocytosis process begins [37]. Inside
the cell, the virus uses the cellular components
to replicate the viral proteins and nucleic acids
(RNA), forming new viral particles which are
released from the host cell membrane. Duplicated
millions of times, the virus fills the body of the
Eco-epidemiological aspects of sylvatic YF vector mosquitoes
Figure 3. The propagation cycle of sylvatic yellow fever in humans and its relation with vectors and
hosts. Source: Ademir Nunes Ribeiro Júnior.
host, inducing fever as the most significant
etiopathogenic result. However, some characteristics
of the virus prevent its dissemination, such as, its
incapacity to survive outside the body for more
than a few hours, cannot infect through air or
contact, has a low mutation rate and fundamentally
its dependency on vector transmission. In Homo
sapiens sapiens, after introduction of the virus
into the circulation from the mosquito bite, a few
hours later the virus reaches the regional lymph
nodes, where it silently multiplies in the cells
of the reticuloendothelial system. Subsequently,
with the release of the viral particles by the cells,
viremia occurs, which corresponds clinically to
prodromes of the disease and, in particular, fever.
Through the bloodstream, the virus reaches and
allocates itself in the liver, kidneys, heart, central
nervous system, pancreas, spleen and lymphoid
structures [37, 38].
Invertebrate hosts of the species H. janthinomys,
H. leucocelaenus, H. albomaculatus and S. cyaneus
possibly propagate YF through the transovarian
and sexual pathways. Hence, a single insect, once
infected, does not lose its viremic ability. For this
reason, they are called vectors, reservoirs and
disseminators of arboviruses [32, 33, 34].
Human contact near forests provides a greater
risk of infection [39], presuming that the human
species - usually - has the role of YF amplifying
host [14]. The sylvatic transmission to Homo
sapiens sapiens has an adventitious attribute,
which was not identified as being directly
responsible for the maintenance of viruses
circulating in nature [38].
7
Final considerations
The tropical areas, vulnerable to the spread of YF,
contain the highest insect biodiversity [30] and
favor the larval abundance of vectors/reservoirs
of the genus Haemagogus and Sabethes [13] in
rural and sylvatic areas. For the spread of the
disease, the virus must also be circulating in
the susceptible population, which is why YF in
humans in sylvatic areas has been occurring in
outbreaks with intervals of more than four years
[10].
Haemagogus and Sabethes are strictly sylvatic,
with the latter being even more selective in their
dispersion. In fact, although the vectors are
concentrated in the sites of preserved vegetation,
Haemagogus can also be found on the fringes
of the forests, and it is in these so-called areas
that Sabethes usually do not venture. In addition,
Haemagogus leucocelaenus can fly a few kilometers
through the open air to reach portions of forest
isolated by the action of man [17, 19]. It should
also be noted that the seasons with high
temperatures and relative humidity favor the
propagation of larvae and adult forms of these
genera, given the highest rainfall indices. Such
rainy periods may corroborate with possible
epizootics or even arbovirus epidemics for Homo
sapiens sapiens, since virus circulation becomes
more effective. This places emphasis on the
employment of preventive and prophylactic
actions - such as vaccination [40] - in areas of
possible transmission, as well as effective
epidemiological surveillance and due systematic
investigation of insects.
8 Marli do Carmo Cupertino et al.
Understanding the ecological aspects of the
Haemagogus and Sabethes mosquitoes - with an
emphasis on the double vector-reservoir function -
is an essential tool to combat the dissemination of
arboviruses. Parameters such as climate changes,
habitats, circadian, behavioral and alimentary
habits of the mosquito are all variables of analysis
that can potentiate or reduce the spread of YF.
The study of physical factors (such as luminosity
in closed forests or woods) and biological factors
(such as mosquito habits as hosts during rest
periods) could be beneficial. Consequently, the
inevitable systematization of these species,
through, for example, the classification of apex
moments in their blood suction, could indeed limit
the contact and the transmission of the disease
to humans.
ACKNOWLEDGMENTS
This study was supported by the Conselho
Nacional de Desenvolvimento Científico e
Tecnológico (CNPq - National Council for Scientific
and Technological Development) and the Research
Program of the Faculdade Dinâmica do Vale do
Piranga (PROAPP/FADIP). The authors are grateful
to Paula Carolina Andrade Mariano and Ademir
Nunes Ribeiro Júnior for their work on the
figures.
CONFLICT OF INTEREST STATEMENT
The authors declare that there are no conflicts
of interest regarding the publication of this article.
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