**3. The main malaria vectors**

#### **3.1.** *Nyssorhynchus darlingi*

The most widespread and dominant malaria vector in the Amazon region is *Nyssorhynchus darlingi* (**Figure 2**) [27, 28, 84, 86]. Localities where *Ny. darlingi* has been formally incriminated by ELISA or other molecular techniques are shown in **Figure 3**, although the full distribution of *Ny. darlingi* extends from southern Mexico through northern Argentina [84]. This species shares several characteristics with invasive species (e.g., *Aedes albopictus*) and other primary malaria vectors such as *An. gambiae* s.s., including fast growth, phenotypic plasticity, rapid reproduction, moderate-high dispersal ability, ecological competence, and association with humans [28, 104–106]. In Loreto Department, Peru, since *Ny. darlingi* reinvaded, or reexpanded its range into the peri-Iquitos area about 1998 [107], it has spread along numerous Peruvian river drainages to the north and west [70, 108]. In Brazil and Peru, it is ranked the number one vector [4, 29, 109]; in Colombia, it is one of three main vectors, the other two being *Ny. albimanus* and *Ny. nuneztovari* [87, 110, 111]; and in Venezuela, it shares top billing with *Ny. albitarsis* s.l. [77, 78, 80]. A recent review highlights the very low insecticide resistance in *Ny. darlingi* detected in the Neotropics, i.e., one population in Choco, western Colombia is resistant to DDT, permethrin, lambda-cyhalothrin, and deltamethrin [23].

The distribution in Brazil includes the lowlands of the Amazonian biome, the Cerrado, and the southern Atlantic forest [84, 112, 113]. *Nyssorhynchus darlingi* is adaptable and flexible in its behavior: exophagic and endophagic; anthropophilic and opportunistic; though generally exophilic [28, 71, 97, 114]. The standard entomological indices range widely across its distribution [71, 80, 96, 97, 103, 114]. One frequently recognized characteristic of *Ny. darlingi* is the speed with which it colonizes deforested Amazonian patches and a variety of anthropogenic water bodies such as gold mining pools, brick-making depressions, wells, cisterns, and fishponds, as well as natural breeding site types linked to rivers or flooded forest [29, 60, 111, 115, 116]. Its adaptation to novel environments may lead to increased vectorial capacity and survival, as well as greater risk of malaria transmission [117, 118]. The most likely drivers of *Ny. darlingi* divergence at a macro-geographic scale, across its broad distribution, are biogeographic or geographic boundaries and Pleistocene environmental changes [113, 119]. At a regional scale, isolation-bydistance has been shown to influence population structure [120], whereas at a micro-geographic scale, current local environmental conditions have a marked effect [113, 119–122].

**Figure 2.** Distribution of *Nyssorhynchus darlingi* (denoted by white dots). Map made in Google Earth Pro [83] using data

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**Figure 3.** Localities (denoted by yellow dots) where the primary malaria vector *Nyssorhynchus darlingi* has been reported infected with *Plasmodium vivax* or *Plasmodium falciparum* incriminated by molecular methods during 2005 to 2017 [8, 35,

from the Malaria Atlas Project [84, 85].

59, 60, 73, 80, 87–103]. Map made in Google Earth Pro [83, 84].

In Colombia, *Ny. darlingi* is distributed on either side of the Andes mountain range in lowland regions characterized by biogeographical and ecological heterogeneity [111]. West of the Andes, in the Urabá-Bajo Cauca and Alto Sinú (UCS) region, *Ny. darlingi* is the most common *Nyssorhynchus* species, exhibits endo and exophagy, is infected with *P. vivax*, and maintains transmission even at low abundance [60, 87, 111]. In most localities included in this study, the peak biting activity of *Ny. darlingi* was after 20:00 or 21:00 h when people conduct indoor and/or outdoor activities increasing the risk of vector-human contact. East of the Andes [111] and in southern Colombia, peak biting activity is at sunset [92] when no one is protected under ITNs. The dominance of *Ny. darlingi* in most of northwestern Colombian localities seems to be favored by ecological perturbations resulting from various human activities, such as alluvial mining, livestock, small-scale rice Malaria Transmission in South America—Present Status and Prospects for Elimination http://dx.doi.org/10.5772/intechopen.69750 291

**3. The main malaria vectors**

290 Towards Malaria Elimination - A Leap Forward

The most widespread and dominant malaria vector in the Amazon region is *Nyssorhynchus darlingi* (**Figure 2**) [27, 28, 84, 86]. Localities where *Ny. darlingi* has been formally incriminated by ELISA or other molecular techniques are shown in **Figure 3**, although the full distribution of *Ny. darlingi* extends from southern Mexico through northern Argentina [84]. This species shares several characteristics with invasive species (e.g., *Aedes albopictus*) and other primary malaria vectors such as *An. gambiae* s.s., including fast growth, phenotypic plasticity, rapid reproduction, moderate-high dispersal ability, ecological competence, and association with humans [28, 104–106]. In Loreto Department, Peru, since *Ny. darlingi* reinvaded, or reexpanded its range into the peri-Iquitos area about 1998 [107], it has spread along numerous Peruvian river drainages to the north and west [70, 108]. In Brazil and Peru, it is ranked the number one vector [4, 29, 109]; in Colombia, it is one of three main vectors, the other two being *Ny. albimanus* and *Ny. nuneztovari* [87, 110, 111]; and in Venezuela, it shares top billing with *Ny. albitarsis* s.l. [77, 78, 80]. A recent review highlights the very low insecticide resistance in *Ny. darlingi* detected in the Neotropics, i.e., one population in Choco, western Colombia is resistant to DDT, permethrin, lambda-cyhalothrin, and deltamethrin [23].

The distribution in Brazil includes the lowlands of the Amazonian biome, the Cerrado, and the southern Atlantic forest [84, 112, 113]. *Nyssorhynchus darlingi* is adaptable and flexible in its behavior: exophagic and endophagic; anthropophilic and opportunistic; though generally exophilic [28, 71, 97, 114]. The standard entomological indices range widely across its distribution [71, 80, 96, 97, 103, 114]. One frequently recognized characteristic of *Ny. darlingi* is the speed with which it colonizes deforested Amazonian patches and a variety of anthropogenic water bodies such as gold mining pools, brick-making depressions, wells, cisterns, and fishponds, as well as natural breeding site types linked to rivers or flooded forest [29, 60, 111, 115, 116]. Its adaptation to novel environments may lead to increased vectorial capacity and survival, as well as greater risk of malaria transmission [117, 118]. The most likely drivers of *Ny. darlingi* divergence at a macro-geographic scale, across its broad distribution, are biogeographic or geographic boundaries and Pleistocene environmental changes [113, 119]. At a regional scale, isolation-bydistance has been shown to influence population structure [120], whereas at a micro-geographic

scale, current local environmental conditions have a marked effect [113, 119–122].

In Colombia, *Ny. darlingi* is distributed on either side of the Andes mountain range in lowland regions characterized by biogeographical and ecological heterogeneity [111]. West of the Andes, in the Urabá-Bajo Cauca and Alto Sinú (UCS) region, *Ny. darlingi* is the most common *Nyssorhynchus* species, exhibits endo and exophagy, is infected with *P. vivax*, and maintains transmission even at low abundance [60, 87, 111]. In most localities included in this study, the peak biting activity of *Ny. darlingi* was after 20:00 or 21:00 h when people conduct indoor and/or outdoor activities increasing the risk of vector-human contact. East of the Andes [111] and in southern Colombia, peak biting activity is at sunset [92] when no one is protected under ITNs. The dominance of *Ny. darlingi* in most of northwestern Colombian localities seems to be favored by ecological perturbations resulting from various human activities, such as alluvial mining, livestock, small-scale rice

**3.1.** *Nyssorhynchus darlingi*

**Figure 2.** Distribution of *Nyssorhynchus darlingi* (denoted by white dots). Map made in Google Earth Pro [83] using data from the Malaria Atlas Project [84, 85].

**Figure 3.** Localities (denoted by yellow dots) where the primary malaria vector *Nyssorhynchus darlingi* has been reported infected with *Plasmodium vivax* or *Plasmodium falciparum* incriminated by molecular methods during 2005 to 2017 [8, 35, 59, 60, 73, 80, 87–103]. Map made in Google Earth Pro [83, 84].

production, and forest fragment landscapes [60]. Vector control strategies that include ITNs are recommended for containment of *Ny. darlingi* populations [60, 87, 111, 123].

Studies on the genetic structure of *Ny. darlingi* in Colombia have shown that at the microgeographic scale, in northwestern Colombia, *Ny. darlingi* is characterized by low genetic differentiation and high gene flow [123, 124]. The environmental heterogeneity that is a hallmark of this malaria endemic region does not reach a threshold to impact the population structure of *Ny. darlingi* [124]. A comprehensive genetic study that evaluated *Ny. darlingi* throughout its distribution in Colombia found that at a macro-geographic scale, differentiation into two main groups, west and east of the Andes, was most likely influenced by the Andes; at a microgeographic scale, differentiation was partly the result of isolation by resistance, probably due to ecological differences, with significant impact on its population structure. In the current malaria scenario in Colombia and considering that Anophelinae mosquitoes adapt to climate and environmental changes, population studies should contribute to the development and implementation of vector control interventions and monitor their effectiveness in important malaria endemic regions of Colombia where *Ny. darlingi* maintains transmission.

Within Peru, only in the peri-Iquitos region of Loreto Department has the genetic structure of *Ny. darlingi* been evaluated, initially using Random Amplified Polymorphic DNA-PCR, that detected substantial homogeneity [125]. When populations from highway and riverine habitats were compared over a decade later using microsatellite markers, two highly admixed subpopulations were detected in each of nine villages [35]. The second major finding was that the 2012–2014 population of *Ny. darlingi* [35] had replaced that of the 2006 [126] and both of these subpopulations had the signature of a recent expansion. The source of the replacement population is unknown, although a broad analysis of microsatellite data across South America suggests that it most likely comes from western Brazil [35].

relation to ENSO patterns and cycles, particularly those transmitted by *Ny. albimanus* along

**Figure 4.** Distribution of *Nyssorhynchus albimanus* (denoted by white dots). Map made in Google Earth Pro [83] using

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The availability of suitable breeding sites determines distribution and abundance of *Ny*. *albimanus* [130], a species that can thrive in fresh and brackish water, natural habitats (animal tracks, lakes, streams, and wells), and anthropogenic ones (rice fields, lagoons, and mining excavations, among others) [130, 135]. Behaviorally, *Ny. albimanus* is mainly zoophilic, exophagic, and exophilic; yet it can be anthropophilic, depending on local circumstances and abundance [130]. It is also known to be endophagic in local malaria hot-spots along the Pacific Coast, i.e., the urban sector of Buenaventura. The main outdoor biting time is 19:00–23:00 h, when many inhabitants are outside, and therefore exposed to biting and *Plasmodium* transmission [130]. As a vector of *P. falciparum* and *P. vivax*, *Ny. albimanus* has been incriminated in the Pacific region [133] and a new species from the southern Pacific Coast, *Ny. albimanus* B, detected by mitochondrial *COI* sequences, was infected with *P. falciparum* [57]. Despite the high abundance

of *Ny. albimanus* in the Caribbean region, no infected specimens were detected [136].

Population genetic studies of *Ny. albimanus* in Colombia confirm its status of a single taxon throughout its distribution, with low population structuring and little genetic differentiation [137]. Two broader studies that included samples from Nicaragua to Ecuador, both nuclear and mitochondrial markers, found evidence for geographic structuring [138] and population contraction across Panama followed by an east-west expansion [139]. Under the hypothesis that malaria vectors are exposed to control pressures and environmental alterations that may lead to genotypic and phenotypic variation, genetic (microsatellite) and phenotypic (wing trait) data

the Pacific Coast of Colombia [61].

data from the Malaria Atlas Project [84, 85].

In Venezuela, *Ny. darlingi* is found in the lowland tropical rainforest, in the southern part of the country (Amazonas and Bolivar States), the piedmont ecoregion characterized by high rainfall and tropical forests in Trujillo State, western Venezuela, and in the llanos in centralwestern Venezuela, a subregion of the savanna ecoregion [127]. There is very little population structure in Venezuelan *Ny. darlingi* based on isozymes, RAPDs, ITS2 sequences [86], but more sensitive molecular markers, or whole genomes, might detect micro-geographic differences among the diverse ecoregions.

#### **3.2.** *Nyssorhynchus albimanus*

*Nyssorhynchus albimanus* is a malaria vector [27] characterized by ecological adaptability and a widespread, mostly coastal lowland, Neotropical distribution (**Figure 4**) [128]. Its presence usually coincides with areas that experience two annual rainy seasons, precipitation greater than 1000 mm, high relative humidity and a monthly variation in temperature between 22° and 29°C [127, 129, 130]. Despite its absence in Brazil, in Colombia, *Ny. albimanus* constitutes one of the main vectors in rural and peri-urban areas below 400–500 m, predominating along the Colombian Caribbean and Pacific Coasts and on the Island of San Andres [130–133]. These regions have different levels of *Plasmodium* transmission and the importance of *Ny. albimanus* also differs [133]. The Pacific is a humid tropical forest and one of the rainiest regions globally; in contrast, the Caribbean tropical forest is drier and hotter [134]. Malaria cases increase in Malaria Transmission in South America—Present Status and Prospects for Elimination http://dx.doi.org/10.5772/intechopen.69750 293

production, and forest fragment landscapes [60]. Vector control strategies that include ITNs are

Studies on the genetic structure of *Ny. darlingi* in Colombia have shown that at the microgeographic scale, in northwestern Colombia, *Ny. darlingi* is characterized by low genetic differentiation and high gene flow [123, 124]. The environmental heterogeneity that is a hallmark of this malaria endemic region does not reach a threshold to impact the population structure of *Ny. darlingi* [124]. A comprehensive genetic study that evaluated *Ny. darlingi* throughout its distribution in Colombia found that at a macro-geographic scale, differentiation into two main groups, west and east of the Andes, was most likely influenced by the Andes; at a microgeographic scale, differentiation was partly the result of isolation by resistance, probably due to ecological differences, with significant impact on its population structure. In the current malaria scenario in Colombia and considering that Anophelinae mosquitoes adapt to climate and environmental changes, population studies should contribute to the development and implementation of vector control interventions and monitor their effectiveness in important

recommended for containment of *Ny. darlingi* populations [60, 87, 111, 123].

malaria endemic regions of Colombia where *Ny. darlingi* maintains transmission.

America suggests that it most likely comes from western Brazil [35].

ences among the diverse ecoregions.

**3.2.** *Nyssorhynchus albimanus*

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Within Peru, only in the peri-Iquitos region of Loreto Department has the genetic structure of *Ny. darlingi* been evaluated, initially using Random Amplified Polymorphic DNA-PCR, that detected substantial homogeneity [125]. When populations from highway and riverine habitats were compared over a decade later using microsatellite markers, two highly admixed subpopulations were detected in each of nine villages [35]. The second major finding was that the 2012–2014 population of *Ny. darlingi* [35] had replaced that of the 2006 [126] and both of these subpopulations had the signature of a recent expansion. The source of the replacement population is unknown, although a broad analysis of microsatellite data across South

In Venezuela, *Ny. darlingi* is found in the lowland tropical rainforest, in the southern part of the country (Amazonas and Bolivar States), the piedmont ecoregion characterized by high rainfall and tropical forests in Trujillo State, western Venezuela, and in the llanos in centralwestern Venezuela, a subregion of the savanna ecoregion [127]. There is very little population structure in Venezuelan *Ny. darlingi* based on isozymes, RAPDs, ITS2 sequences [86], but more sensitive molecular markers, or whole genomes, might detect micro-geographic differ-

*Nyssorhynchus albimanus* is a malaria vector [27] characterized by ecological adaptability and a widespread, mostly coastal lowland, Neotropical distribution (**Figure 4**) [128]. Its presence usually coincides with areas that experience two annual rainy seasons, precipitation greater than 1000 mm, high relative humidity and a monthly variation in temperature between 22° and 29°C [127, 129, 130]. Despite its absence in Brazil, in Colombia, *Ny. albimanus* constitutes one of the main vectors in rural and peri-urban areas below 400–500 m, predominating along the Colombian Caribbean and Pacific Coasts and on the Island of San Andres [130–133]. These regions have different levels of *Plasmodium* transmission and the importance of *Ny. albimanus* also differs [133]. The Pacific is a humid tropical forest and one of the rainiest regions globally; in contrast, the Caribbean tropical forest is drier and hotter [134]. Malaria cases increase in

**Figure 4.** Distribution of *Nyssorhynchus albimanus* (denoted by white dots). Map made in Google Earth Pro [83] using data from the Malaria Atlas Project [84, 85].

relation to ENSO patterns and cycles, particularly those transmitted by *Ny. albimanus* along the Pacific Coast of Colombia [61].

The availability of suitable breeding sites determines distribution and abundance of *Ny*. *albimanus* [130], a species that can thrive in fresh and brackish water, natural habitats (animal tracks, lakes, streams, and wells), and anthropogenic ones (rice fields, lagoons, and mining excavations, among others) [130, 135]. Behaviorally, *Ny. albimanus* is mainly zoophilic, exophagic, and exophilic; yet it can be anthropophilic, depending on local circumstances and abundance [130]. It is also known to be endophagic in local malaria hot-spots along the Pacific Coast, i.e., the urban sector of Buenaventura. The main outdoor biting time is 19:00–23:00 h, when many inhabitants are outside, and therefore exposed to biting and *Plasmodium* transmission [130]. As a vector of *P. falciparum* and *P. vivax*, *Ny. albimanus* has been incriminated in the Pacific region [133] and a new species from the southern Pacific Coast, *Ny. albimanus* B, detected by mitochondrial *COI* sequences, was infected with *P. falciparum* [57]. Despite the high abundance of *Ny. albimanus* in the Caribbean region, no infected specimens were detected [136].

Population genetic studies of *Ny. albimanus* in Colombia confirm its status of a single taxon throughout its distribution, with low population structuring and little genetic differentiation [137]. Two broader studies that included samples from Nicaragua to Ecuador, both nuclear and mitochondrial markers, found evidence for geographic structuring [138] and population contraction across Panama followed by an east-west expansion [139]. Under the hypothesis that malaria vectors are exposed to control pressures and environmental alterations that may lead to genotypic and phenotypic variation, genetic (microsatellite) and phenotypic (wing trait) data in populations of *Ny. albimanus* from the Pacific and Caribbean, despite a significant effect of environmental factors on wing traits, support a regional metapopulation of *Ny. albimanus* [132].

In Peru, *Ny. albimanus* is restricted to the Tumbes region of the northern coast, where it transmits *P. vivax* at the end of the hot rainy season. Local insecticide application, mostly in rice fields, lead to extreme levels of insecticide resistance [23]. A series of meetings and decisions between southern Ecuador and northern Peru health personnel resulted in a highly successful control program that employed a wide array of interventions such that autochthonous malaria was eliminated in El Oro, Ecuador in 2011 and in Tumbes, Peru in 2012 [135].

In Venezuela, *Ny. albimanus* is distributed along the coast and the margins of Valencia Lake, south of Maracay, although it does not appear to contribute to malaria transmission locally [127, 140]. It was found to be as abundant as the known coastal vector *Ny. aquasalis* in Aragua State, northcentral Venezuela, where both species had similar peak biting times during the early evening and were collected biting outdoors [141].

#### **3.3.** *Nyssorhynchus albitarsis* **s.l.**

The *Albitarsis* Complex comprises at least eight species [142] that extend across Central and South America and some Caribbean islands (**Figure 5**). The difficulty of their morphological differentiation complicates recognition of their role(s) in malaria transmission, an important aspect for the implementation of targeted and effective vector control strategies [143]. Three species are known vectors: *Ny. deaneorum*, *Ny. janconnae*, and *Ny. marajoara.* The latter is important regionally in *Plasmodium* transmission in central and eastern Brazil, where its distribution includes Amapá, Mato Grosso, Pará, and Rôndonia [84, 142]. Its role in transmission rivals that of *Ny. darlingi* in some habitat types such as peri-urban Macapá City, Amapá [144] and along the Rio Matapi, Amapá [88]. An entomological survey during an outbreak in western French Guiana, in an illegal gold mining area, detected a high *P. vivax* infectivity rate (6.4%) in specimens of *Ny. marajoara* [99]. An ecological niche model, based on current and future (2070), distributions of *P. falciparum*, *Ny. darlingi*, all species of the *Albitarsis* Complex, climate, biome and topography, projected that, whereas climate change would reduce suitable habitat for *Ny. darlingi,* both *Ny. marajoara* and *Ny. deaneorum* are expected to expand southward, thereby increasing their likely role in *P. falciparum* transmission by the projected date of 2070 [19].

In Colombia, only a few species, in particular *Ny. marajoara,* have been identified morphologically in this complex [90, 145–147] and implicated in urban transmission [145]. This species is thought to be widespread in this country [110]. However, a detailed analysis of many Colombian specimens, identified molecularly, did not detect any individual *Ny. marajoara* [147], in agreement with Ruiz-Lopez et al. [142], whose study indicated that *Ny. marajoara* is restricted to the central-eastern and western regions of Brazil and is most likely absent in Colombia. Further studies need to be done on this vector to better frame its geographic distribution.

*Ny. albitarsis* F in the *Albitarsis* Complex [142], was identified from the Caura Basin, Bolivar State [96]. In the most recent publication from the malaria hot-spot Sifontes, the specimens infected by *Plasmodium* are referred to only as *Ny. albitarsis* s.l. [80]. Hopefully, the correct species identities and distribution will soon be determined in this very crucial Venezuelan hot-spot.

**Figure 5.** Distribution of the *Albitarsis* Complex (denoted by white dots). Map made in Google Earth Pro [83] using data

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The *Nuneztovari* Complex, extending through much of northern South America, includes *Ny. nuneztovari* (**Figure 6**), *Nyssorhynchus dunhami*, and *Nyssorhynchus goeldii* [149]. Like the *Albitarsis* Complex, species in the *Nuneztovari* Complex are similar morphologically and difficult to identify accurately. Scarpassa and collaborators [150] presented strong molecular evidence that additional species exist in Brazil and briefly reviewed the role of *Ny. nuneztovari* as a malaria vector in five Amazonian States. *Nyssorhynchus nuneztovari* is restricted to Colombia and western Venezuela, *Ny. goeldii* to Amazonian Brazil, and *Ny. dunhami* to central-western Brazil, Colombia and Amazonian Peru [71, 150]. It is difficult to evaluate the identification of

**3.4. The** *Nuneztovari* **Complex**

from the Malaria Atlas Project [84, 85].

*Albitarsis* Complex species appear to be uncommon in Peru but this could reflect a general lack of *Nyssorhynchus* taxon sampling and molecular identification, particularly outside the Amazon region of Loreto.

Although there are several published reports of *Ny*. *marajoara* as an important regional malaria vector in Bolivar State, Venezuela, along with *Ny. darlingi* [77, 78, 148], a different species, Malaria Transmission in South America—Present Status and Prospects for Elimination http://dx.doi.org/10.5772/intechopen.69750 295

**Figure 5.** Distribution of the *Albitarsis* Complex (denoted by white dots). Map made in Google Earth Pro [83] using data from the Malaria Atlas Project [84, 85].

*Ny. albitarsis* F in the *Albitarsis* Complex [142], was identified from the Caura Basin, Bolivar State [96]. In the most recent publication from the malaria hot-spot Sifontes, the specimens infected by *Plasmodium* are referred to only as *Ny. albitarsis* s.l. [80]. Hopefully, the correct species identities and distribution will soon be determined in this very crucial Venezuelan hot-spot.

#### **3.4. The** *Nuneztovari* **Complex**

in populations of *Ny. albimanus* from the Pacific and Caribbean, despite a significant effect of environmental factors on wing traits, support a regional metapopulation of *Ny. albimanus* [132]. In Peru, *Ny. albimanus* is restricted to the Tumbes region of the northern coast, where it transmits *P. vivax* at the end of the hot rainy season. Local insecticide application, mostly in rice fields, lead to extreme levels of insecticide resistance [23]. A series of meetings and decisions between southern Ecuador and northern Peru health personnel resulted in a highly successful control program that employed a wide array of interventions such that autochthonous

malaria was eliminated in El Oro, Ecuador in 2011 and in Tumbes, Peru in 2012 [135].

early evening and were collected biting outdoors [141].

**3.3.** *Nyssorhynchus albitarsis* **s.l.**

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Amazon region of Loreto.

In Venezuela, *Ny. albimanus* is distributed along the coast and the margins of Valencia Lake, south of Maracay, although it does not appear to contribute to malaria transmission locally [127, 140]. It was found to be as abundant as the known coastal vector *Ny. aquasalis* in Aragua State, northcentral Venezuela, where both species had similar peak biting times during the

The *Albitarsis* Complex comprises at least eight species [142] that extend across Central and South America and some Caribbean islands (**Figure 5**). The difficulty of their morphological differentiation complicates recognition of their role(s) in malaria transmission, an important aspect for the implementation of targeted and effective vector control strategies [143]. Three species are known vectors: *Ny. deaneorum*, *Ny. janconnae*, and *Ny. marajoara.* The latter is important regionally in *Plasmodium* transmission in central and eastern Brazil, where its distribution includes Amapá, Mato Grosso, Pará, and Rôndonia [84, 142]. Its role in transmission rivals that of *Ny. darlingi* in some habitat types such as peri-urban Macapá City, Amapá [144] and along the Rio Matapi, Amapá [88]. An entomological survey during an outbreak in western French Guiana, in an illegal gold mining area, detected a high *P. vivax* infectivity rate (6.4%) in specimens of *Ny. marajoara* [99]. An ecological niche model, based on current and future (2070), distributions of *P. falciparum*, *Ny. darlingi*, all species of the *Albitarsis* Complex, climate, biome and topography, projected that, whereas climate change would reduce suitable habitat for *Ny. darlingi,* both *Ny. marajoara* and *Ny. deaneorum* are expected to expand southward, thereby increasing their likely role in *P. falciparum* transmission by the projected date of 2070 [19].

In Colombia, only a few species, in particular *Ny. marajoara,* have been identified morphologically in this complex [90, 145–147] and implicated in urban transmission [145]. This species is thought to be widespread in this country [110]. However, a detailed analysis of many Colombian specimens, identified molecularly, did not detect any individual *Ny. marajoara* [147], in agreement with Ruiz-Lopez et al. [142], whose study indicated that *Ny. marajoara* is restricted to the central-eastern and western regions of Brazil and is most likely absent in Colombia. Further

*Albitarsis* Complex species appear to be uncommon in Peru but this could reflect a general lack of *Nyssorhynchus* taxon sampling and molecular identification, particularly outside the

Although there are several published reports of *Ny*. *marajoara* as an important regional malaria vector in Bolivar State, Venezuela, along with *Ny. darlingi* [77, 78, 148], a different species,

studies need to be done on this vector to better frame its geographic distribution.

The *Nuneztovari* Complex, extending through much of northern South America, includes *Ny. nuneztovari* (**Figure 6**), *Nyssorhynchus dunhami*, and *Nyssorhynchus goeldii* [149]. Like the *Albitarsis* Complex, species in the *Nuneztovari* Complex are similar morphologically and difficult to identify accurately. Scarpassa and collaborators [150] presented strong molecular evidence that additional species exist in Brazil and briefly reviewed the role of *Ny. nuneztovari* as a malaria vector in five Amazonian States. *Nyssorhynchus nuneztovari* is restricted to Colombia and western Venezuela, *Ny. goeldii* to Amazonian Brazil, and *Ny. dunhami* to central-western Brazil, Colombia and Amazonian Peru [71, 150]. It is difficult to evaluate the identification of

contiguous with Venezuela, peak biting of *Ny. nuneztovari* was after 21:00 h. This population differed genetically from other Colombian populations and its behavior was similar to *Ny. nuneztovari* from Venezuela. The populations exhibited endo and exophagic behavior in all localities and the results of the study indicated that region-specific interventions on both sides of the Andes would be most effective [152]. EIR values detected for Colombian *Ny. nuneztovari* were 3.5–3.6 in the northwest and 7.2 in the west. The highest value was in Buenaventura, on the Pacific Coast, where *Ny. albimanus* is considered the primary vector [133], but, according to the new study, *Ny. nuneztovari* also has a role in transmission in peri-urban Buenaventura [152].

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In Peru, *Ny. nuneztovari* has been detected in five Departments: Pasco, Junín, Loreto, Ucayali, and Madre de Dios [154] and its presence confirmed in Loreto [155]. It may have a role in local malaria transmission, but remains unexplored. *Nyssorhynchus nuneztovari* is known as an important regional vector in western Venezuela where it occurs in seven States [156]. It was first identified morphologically in Bolivar State by Moreno et al. [157], from the malaria hot-spot of Sifontes municipality and was found infected by *P. vivax* (0.52%) [80]. It has also been found to be as abundant as *Ny. darlingi* in the Lower Caura River Basin, Bolivar State, where it was mostly active at sunset, although biting also throughout the night. Nevertheless, it was not detected infected by *Plasmodium* (although *Ny. darlingi* was), so the latter is more

As discussed by Packard [37], for sustainable malaria control, focusing on decreasing incidence towards elimination, effective measures need to be considered, including those related to human ecology. Examples include a significant improvement in living and housing conditions, redesigning of anthropogenic landscapes from those that favor mosquito vectors to a remodeled landscape that is both adequate for humans and inadequate for vector mosquitoes. The sustainability and success of a malaria control program depends on a combination of diagnosis of human infection, treatment with anti-malarial drugs, and vector control. Moreover, proposed changes will need to be maintained such that the malaria baseline will not be affected by either interruption or disruption of a control program [1]. It would be sensible to include malaria control in the One Health Program, to align it with the elimination

The recent elimination of malaria on the Peru-Ecuador border was a successful strategy and included strengthening surveillance and treatment, resource sharing, the use of operational research to inform policy, and novel interventions [135]. The current program depends on prompt, effective diagnosis and treatment with no charge, community personnel trained to collect blood smears from febrile persons within their communities, case reporting to a national surveillance system that includes a five-category case definition (indigenous, imported, introduced, induced, and cryptic), active foci and case investigations, mapping and elimination of larval habitats, and the use of ITNs and LLINs. This could serve as a model for the current situation along the Venezuelan border with its neighbors, Colombia and Brazil. One very important aspect of this program is that it took 20 years to achieve its goals [135].

important in relation to malaria risk in the Caura River area [96].

of extreme poverty, a goal of the global sustainable development program.

**4. Conclusions and recommendations**

**Figure 6.** Distribution of the Nuneztovari Complex (denoted by white dots). Map made in Google Earth Pro [83] using data from the Malaria Atlas Project [84, 85].

these species in earlier publications, because distributions of *Ny. nuneztovari* and *Ny. goeldii* overlap, as do those of *Ny. goeldii* and *Ny*. *dunhami* [149, 150].

In Colombia, *Ny. nuneztovari* is an important malaria vector on both sides of the Andes presenting morphological, behavioral, and genetic heterogeneity throughout the country [151, 152]. In northwestern Colombia, it was found to be the most prevalent species, confirming an earlier study [58], and showed endo and exophagic behavior [152]. It was naturally infected by *P. vivax* VK247 [60, 87], positive for *P. vivax* VK210, and VK247 in the Pacific Coast [103]. In eastern Colombia, there are no recent reports of *Ny. nuneztovari* infected with *Plasmodium*, but more importantly, there is a lack of investigation of malaria outbreaks along the frontier with Venezuela with no record of species identification and vector incrimination. Because of the humanitarian crisis in Venezuela, the numbers of malaria cases have increased dramatically since 2010 [1, 153]. In the most recent study of Colombian *Ny. nuneztovari*, it was reported to be abundant and dominant in localities where anthropogenic activities such as livestock, fishfarming, and small to medium-scale agriculture were common, attributed to its adaptability to environmentally impacted habitats [152]. Common larval habitats were artificial fishponds and wetlands, particularly in the west and northwest [58, 152].

Regionally, this species shows the highest biting activity after 20:00 h, which suggests high transmission risk when people are at home, but not necessarily under nets. ITNs could be one component of an effective vector control intervention. In a locality in the northeast, Tibú, contiguous with Venezuela, peak biting of *Ny. nuneztovari* was after 21:00 h. This population differed genetically from other Colombian populations and its behavior was similar to *Ny. nuneztovari* from Venezuela. The populations exhibited endo and exophagic behavior in all localities and the results of the study indicated that region-specific interventions on both sides of the Andes would be most effective [152]. EIR values detected for Colombian *Ny. nuneztovari* were 3.5–3.6 in the northwest and 7.2 in the west. The highest value was in Buenaventura, on the Pacific Coast, where *Ny. albimanus* is considered the primary vector [133], but, according to the new study, *Ny. nuneztovari* also has a role in transmission in peri-urban Buenaventura [152].

In Peru, *Ny. nuneztovari* has been detected in five Departments: Pasco, Junín, Loreto, Ucayali, and Madre de Dios [154] and its presence confirmed in Loreto [155]. It may have a role in local malaria transmission, but remains unexplored. *Nyssorhynchus nuneztovari* is known as an important regional vector in western Venezuela where it occurs in seven States [156]. It was first identified morphologically in Bolivar State by Moreno et al. [157], from the malaria hot-spot of Sifontes municipality and was found infected by *P. vivax* (0.52%) [80]. It has also been found to be as abundant as *Ny. darlingi* in the Lower Caura River Basin, Bolivar State, where it was mostly active at sunset, although biting also throughout the night. Nevertheless, it was not detected infected by *Plasmodium* (although *Ny. darlingi* was), so the latter is more important in relation to malaria risk in the Caura River area [96].
