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All issues Volume 32 (2025) Parasite, 32 (2025) 57 Full HTML
Open Access
Review
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Parasite
Volume 32, 2025
Article Number 57
Number of page(s) 17
DOI https://doi.org/10.1051/parasite/2025039
Published online 08 September 2025

© J. Shaw et al., published by EDP Sciences, 2025

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Anthropophily in dipteran biology signifies an attraction or preference for humans, feeding on humans, breeding in anthropogenic environments, and a habitat preference for these same biomes. Because of the feral origin of blood-sucking Diptera, it is unwise to consider that they are preferentially attracted to humans, as their main food sources are non-human vertebrates. However, attraction to anthropogenic biomes can enhance breeding and this closeness to humans, in the absence of other mammals, means that humans become the principal food source, confirmed by blood meal identifications.

In the literature, there are phrases such as “At least 15 Lutzomyia spp. are known to be anthropophilic and are strongly suspected as vectors”, but the criteria for such assertions are not mentioned nor what species they are. In others, there are statements such as “biting rates”, but they refer to catches in traps. These records may refer to species found to be biting humans, taken when landing on a protected individual or captured in Shannon traps. Sometimes, Shannon trap catches are equated to anthropophily. However, this may be problematic because there is sometimes a light source in this type of trap. Photophilia varies between species. In one study [56], the proportion of Nyssomyia yuilli and Lutzomyia tortura captured landing on humans was 1/3.3 and taken in a Shannon trap was 1/0.005. This indicates that Shannon trap catches reflected Ny. yuilli’s attraction for humans, but not Lu. tortura’s, and results with CDC traps showed that Ny. yuilli is attracted to light but Lu. tortura is not. This study emphasized that one trapping method may be useful for evaluating attraction of one species to humans, but for others, it is not. Also, it cannot be assumed that being attracted to humans is synonymous with “feeding on humans”, sometimes referred to a human-biting. I only use the term human-biting when it refers to observations of flies physically biting humans. Given the antiquity of sand flies and their co-evolution with mammalian orders, it is difficult to accept the evolution of specific attraction to humans. As a result, we need to reset the idea of sand fly “anthropophily” in a more realistic manner that relates to these insects’ feeding preferences, which have guaranteed their survival, and considering that the species evolved together with vertebrate groups, including mammals. Based on the records of Leishmaniinae infections, this research questions the usefulness of “anthropophily” to describe the feeding habits of American sand flies, as well as confusing derivatives, such as “anthropo-zoophilic” and “zoo-anthropophilic” that appear in the literature. Other researchers have replaced anthropophilic with terms such as human-feeding tendency, opportunistic feeder, or eclectic feeder. These are improvements but they do not dissect the biological complexity that is associated with different feeding habits.

In relation to the above, I am introducing the use of the “Generalist” and “Specialist” concepts to describe host preferences, how they differ, and their epidemiological implications:

Generalists and Specialists:

1. Host range:

Generalist sand flies: feed on a wide range of hosts and are adaptable and readily switch between available hosts for blood meals.

Specialist sand flies: have more restricted host ranges and are highly adapted to specific hosts or host groups and environments.

2. Adaptations:

Generalist sand flies: have adaptations that allow them to exploit a variety of hosts. They may have specialized mouthparts that can pierce the skin of different types of animals, as well as mechanisms to detect hosts and avoid host defences.

Specialist sand flies: are often highly adapted to feed on specific hosts. Their mouthparts may be specialized to penetrate the skin of particular animals, and they may possess sensory organs that help them locate their preferred hosts.

3. Transmission:

Generalist sand flies: may support the multiplication and transmission of different parasites that results in the spread of diseases to various host species. Some have been considered “permissive” vectors. This has occurred with visceral leishmaniasis in the Americas.

Specialist sand flies: transmission is often more focused on specific hosts or host groups, potentially playing key roles in transmitting pathogens and parasites within certain ecosystems, such as diseases affecting livestock or wildlife.

4. Ecological role:

Generalist sand flies: can have a significant impact on the health of both human and animal populations by being able to breed in anthropogenic environments. Their presence can influence disease transmission dynamics and affect the behavior and potentially the distribution of their hosts.

Specialist sand flies: may have a more localized impact on specific host populations or ecosystems. They may be important vectors of diseases within their specialized host groups and can influence the health and behavior of those hosts.

5. Evolution:

Generalist sand flies: their evolution is linked to environments where there are multiple blood sources.

Specialist sand flies: their evolution is linked to more specific environments that favor close relationships with specific hosts.

Additionally, I propose three subdivisions within the above categories of generalists and specialists that are orientated towards their behavior in seeking humans as a food source. These subdivisions are anthropportunistic, anthroaccidentalistic, and zoophilic. The first two are new terms and the other is widely used in biology. Evaluating these categories is complex and is based on many parameters that range from how flies were collected to molecular identification of blood meals. Species considered to belong to any one of these categories can be generalists or specialists. Some generalists, when feeding, transmit Leishmaniinae parasites to a wide of hosts belonging to different mammalian orders and on occasions opportunistically feed on humans. Feeding on what is available is an excellent survival strategy and for those that are known to bite humans, I use the term anthropportunists. They are attracted to humans, may or may not be the dominant species in light and Shannon traps, and are associated with the dominant Leishmania species found in humans. There are others with more focused ecological roles within ecosystems and only under unusual circumstances bite people. I refer to these as anthroaccidentalists. They contribute minimally to zoonotic transmission of Leishmania species that are less common in humans. The categorization of species as zoophilic is based on absence of any information of their contact with people. They may be either generalists or specialists and may or may not play a role in the enzootic cycle. Generalists and specialists may belong to any one of these three categories. Assignment to these different categories was based on host preferences, trapping methods, feeding behavior, leishmanial infections, ecological adaptability, and epidemiological importance. The use of anthropophily and anthrophilic is limited to being found in anthropogenic biomes.

In 1940, Pessôa and Pestana [93] recorded the first flagellate infection in Migonemyia migonei. The earlier records between 1940 and 1965, as well as similar more recent ones, are not cited in this paper because there were no specific parasite identifications. However, infections in species mentioned in these publications have subsequently been identified, confirming identifications based on circumstantial epidemiological evidence. A review of the literature between 1965 and 2024 identified Leishmania infections in 91 sand fly species. These are listed in Table 1 together with their different behavioral character categories mentioned above, and the method of detection. These infections were reported over a period of 59 years using a variety of methods ranging from identifying parasites isolated from dissected flies to indirect molecular detection. However, they do not relate to vectorial capacity nor to the number of times that a species has been found to be infected. The literature citation refers to the first time the infections were published. At the time of writing, there are approximately 550 named phlebotomine species (Galati personal communication) in the Americas. This means that so far Leishmania have only been found in 16.4% of the American sand fly species. Of the 91 mentioned above, 75 were considered to be generalists or 16 as specialists and 51 as anthropportunists, 15 as anthroaccidentalists, 24 as zoophilic and one as phytophagous. This potentially suggests that if such infections were transmissible, 42.2% of the species would not represent a serious threat of zoonotic transmission. Older works refer to in vivo dissections coupled with biochemical identifications and even experimental transmissions. As a result, they more accurately indicate transmissibility and vectorial status, but in the absence of such observations, many recent molecular identifications merely indicate possible roles and nothing more. A method identifying metacyclics would add weight to the potential importance of infections detected by molecular techniques. The data also showed that 56.7% of infected species belonged to the genera Lutzomyia, Nyssomyia, Pintomyia, and Psychodopygus. This emphasizes the epidemiological importance of species belonging to these genera, especially as some species of the first three-genera breed in anthropogenic biomes.

Table 1

The feeding habits and Leishmania infections of American Phlebotomine species.

The species mentioned below have been found to be infected with Leishmania during American cutaneous leishmaniasis (ACL) and American visceral leishmaniasis (AVL) epidemiological studies. Based on the available data, they are categorized as generalist or specialists and then anthropportunists, anthroaccidentalists, or zoophilic. The major difference between the last two is the absence of evidence indicating humans as a source of food.

Genus Bichromomyia and Leishmania (Leishmania) mexicana complex parasite vectors

Members of this genus are found throughout Central and South America and transmit parasites of the L. (L.) mexicana clade [11, 45, 62], but evidence of their anthropophily under certain situations is based more on the fact that these parasites are found in humans. In Yucatan state, Mexico, Bichromomyia olmeca is considered to be the vector, but the low number of cases suggests that it is anthroaccidentalist. Other species may transmit L. (L.) mexicana, as human infections occur outside Bi. olmeca’s distribution. It has been suggested [44] that Lutzomyia cruciata and Psathyromyia shannoni would be the most suitable candidates as both are distributed broadly and have been found to be infected with L. (L.) mexicana. All three species have been considered as being “highly anthropophilic” [18], but the reasons for this statement are not given. This could be because they were the dominant species in Shannon traps [88], but it does not mean that they would feed on people. A series of chemicals such as carbon dioxide and semiochemicals [14] attract sand flies. Nonetheless, there is a lack of data on the molecules emitted by vertebrates, sand flies, and plants that affect phlebotomine behavior. If these molecular signatures were compatible, the females would feed on either plants or animals. A species may be attracted, but if its chemoreceptors were not tuned to the host’s semiochemicals, it would not feed. This is very important in host specificity. Leishmania (L.) amazonensis’s vector is Bi. flaviscutellata and given a choice of hosts, the majority feed on rodents. That said, the species has been collected from humans in small numbers [124], while large numbers were collected from rodents. However, in ecotopes where the populations were high, the human-biting index was 1.25 flies per hour [125]. The available evidence indicates that Bi. flaviscutellata can be considered an anthroaccidentalist species [17], but its biting index is dependent on the population density in specific biomes. Bichromomyia species are strongly attracted to rodents and given their importance as reservoirs [74] of L. (Viannia) braziliensis, it is very surprising that this parasite has only been recorded in this genus on one occasion [140]. It has been shown experimentally that Bi. flaviscutellata does not support the development of L. (Viannia) species [30, 101]. The single recorded infection [140] was a molecular identification and was probably a dead-end infection that would subsequently be excreted. This is a good example of how laboratory experimental infections can help to interpret field results.

In other regions such as Texas, United States the vector of L. (L.) mexicana is considered to be a rodent loving species, Dampfomyia anthophora [78], and human cases are extremely rare. It has been suggested that other species such as Lutzomyia diabolica or Psathyromyia shannoni may be responsible for the human infections. There are no records of this species seeking humans as a food source, so it has been considered zoophilic.

The genus Evandromyia

Species of this genus are not considered to feed on humans, but have been found to be infected with L. (V.) braziliensis [3, 20, 112] and L. (L.) infantum [19, 20, 121]. Their importance in leishmanial enzootic cycles has yet to be determined. They are generally taken in light traps. An infection of L. (V.) braziliensis has been recorded on one occasion [24] in Ev. infraspinosa. This species has been collected in small numbers in Shannon traps, while 97% were captured in light traps [27]. It is not considered to be attracted to humans [17]. An isolate from Ev. infraspinosa captured in Rondônia, Brazil was identified [34] as a trypanosome of anurans. There are records of L. (L.) infantum and L. (V.) braziliensis [131] in several Evandromyia species that have been captured in light traps. The available evidence strongly suggests that Evandromyia species are zoophilic generalists, indicating that they could play a role in enzootic but not zoonotic cycles. Attempts to infect laboratory reared Ev. carmolinoi with different Leishmania have failed [115]. Alternatively, the recorded infections in Evandromyia species might be ones that die out. These questions could be answered by dissections of wild caught flies and experimental infections in laboratory reared females.

The genus Lutzomyia

Species of this subgenus are vectors of cutaneous and visceral leishmaniasis-causing parasites. Lutzomyia longipalpis is a complex of genetically distinct species [143, 146] responsible for the transmission of L. (L) infantum throughout Central and South America. It was first associated with visceral leishmaniasis in 1934 by Penna [90], and similar observations by other Latin American workers cemented it as the vector of American visceral leishmaniasis. However, it was only shown to experimentally transmit L. (L) infantum in 1977 [65]. Finally, isolates from naturally infected flies were shown to have the same enzymatic profiles in 1986 [13] as those isolated from humans. The degree of attraction to humans was uncertain in Amazonia, but studies have shown that in the peri-domestic environment, attractiveness for this species is largely related to the host’s size and accessibility [97]. It appears to feed on what is most readily available, in many cases large animals such as pigs and cows, but in houses it feeds predominantly on humans [84], indicating that it is an anthropportunist. However, given the choice, it is attracted preferentially to dogs and chickens instead of humans [17]. It has been found to be infected with L. (L) amazonensis [122] and L. (V.) braziliensis [87], but its preference for the known reservoirs of these two species suggests that it may play a minimal role, if any, in their transmission.

In some Andean regions of Ecuador and Peru, Lu. ayacuchensis is the dominant species collected from humans, where it has been captured in large numbers [41]. In both countries [48, 58], it has been found infected with a parasite that was identified as belonging to the L. (L) mexicana complex. Epidemiological studies have shown that this species is the vector [50] of Andean cutaneous leishmaniasis in Ecuador’s Chimborazo province. It has also been found to be infected with L. (V.) peruensis in Ayacucho, Peru [15] and should be considered an anthropportunist generalist.

In Mato Grosso do Sul, Brazil Lu. almerioi and Lu. forattinii are closely related to Lu. longipalpis and are a “highly anthropophilic species” [122]. Both have been found to be infected with L. (L) infantum as has Lu. cruzi [25], and are considered AVL vectors in Mato Grosso do Sul, indicating that these three species are anthropportunists.

Lutzomyia cruciata is an anthropportunistic species, as shown by collection from humans [31, 104] and in Shannon traps [88] in Mexico. It has been found to be infected with L. (L) mexicana in Mexico’s Yucatan peninsula [88, 116]. This sand fly occurs in southern Texas and Central America, and it has been reported as far south as Panama [36].

Lutzomyia gaminarai was described from Uruguay and also occurs in Paraguay, as well as in the southern Brazilian states of Rio Grande do Sul and Parana [36]. It was the dominant species captured in light traps set in anthropogenic environments during an outbreak of visceral leishmaniasis in Porto Alegre, Brazil and was found to be infected with both L. (L) infantum and L. (V.) braziliensis [107].

Lutzomyia gomezi has a very extensive geographical distribution throughout Central and South America [36] and can be considered to be anthropportunistic [31, 41]. In Amazonia, its attraction to humans was like that of Ny. whitmani [17]. It has been found to be infected with L. (V.) braziliensis [111], L. (V.) naiffi [8], L. (V.) panamensis [118], L. (V.) shawi [27], and Endotrypanum [59]. The fact that it is infected with so many different parasites fully supports the view that it is a generalist. Given its parasitological background, this species is clearly an anthropportunist. Although it occurs in many countries, its density varies, which impacts its epidemiological importance as an ACL vector.

Lutzomyia hartmanni has been recorded as being attracted to humans in Ecuador [41], and has been found to be infected with Endotrypanum species but not any Leishmania species. Sloths are hosts to both parasites, leading to the question of why no Leishmania infections have been recorded in this species. It could be refractory to Leishmania infection, but this seems unlikely given leishmanial susceptibility of Lutzomyia species. To date, the available data indicate that this is an anthropportunistic species of no leishmanial vectorial importance. An unknown Leishmania has been recorded in Lu. sherlocki in the Peruvian Amazon [150]. This species occurs in Bolivia, Brazil, Colombia, Ecuador, and Peru [36].

Lutzomyia peruensis occurs in the Andean highlands of Bolivia and Peru and has been found to be infected [91] with L. (V.) peruviana in a number of Peruvian localities above 2,000 m above sea level [49]. It is an anthropportunistic species [91], is distributed on the western side of the Andes [82], and is the principal vector of uta due to its endophilic habit [144].

Lutzomyia tortura is a species with limited geographical distribution in Bolivia, Ecuador, and Colombia [36] and, so far, the evidence indicates that it is an anthropportunist species in Ecuador [41]. In this country, it has been found to be infected with L. (V.) naiffi [57] and was considered the vector of this parasite to humans.

Lutzomyia tejadai was captured in CDC and Shannon traps in and around houses in a Peruvian endemic ACL focus situated approximately 3,000 m above sea level. A single infection was found in one of these sand flies that was identified as a hybrid L. (V.) braziliensis/L. (V.) peruviana [55]. Human infections of this hybrid have been reported in the area, strongly supporting Lu. tejadai’s vectorial role and it being considered an anthropportunist.

The genus Migonemyia

The only species of this genus associated with leishmanial parasites is Mi. migonei. It is found in most Brazilian States as well as Argentina, Bolivia, Colombia, Venezuela, and Peru [36]. It is attracted to humans and has been found to be infected with both L. (V.) braziliensis [7] and L. (L.) infantum [85]. Interest in this species’ epidemiological importance is linked to it being anthropportunistic and being found in anthropogenic environments.

The genus Nyssomyia

Species of this genus are among the most important ACL vectors throughout the Americas and are found in both sylvatic and anthropogenic environments. Among the 21 Nyssomyia species, Leishmania infections have been found in ten (Ny. anduzei, Ny. antunesi, Ny. intermedia, Ny. neivai, Ny. shawi, Ny. trapidoi, Ny. umbratilis, Ny. whitmani, Ny. ylephilator, and Ny. yuilli). For some, there are records of individual infections with up to three Leishmania species. The available evidence of their biology and infections indicates that these ten species are anthropportunistic generalists.

Leishmania (V.) guyanensis have been recorded in Ny. anduzei and Ny. umbratilis and both are anthropportunists [28, 103]. Additionally, L. (V.) naiffi has been found in Ny. anduzei [28] and L. (L.) amazonensis in [127] Ny. umbratilis. This suggests that besides being the vectors of zoonotic L. (V.) guyanensis, they may play a vectorial role for other Leishmania. Nyssomyia antunesi occurs in more open areas [141] and has been found to be infected with L (V.) braziliensis [24], L (V.) naiffi [126], and L (V.) panamensis [142]. Its presence in houses makes it a potential anthropportunistic generalist ACL vector.

Nyssomyia intermedia and Ny. neivai are closely related species [2, 86] and both occur in anthropogenic environments. They are accepted as ACL vectors and are found in the drier eastern regions of the South American continent from Rio Grande do Norte to Argentina and Paraguay [36]. It is considered that older southerly records of Ny. intermedia refer to Ny. neivai but in São Paulo state they are sympatric. There are records of L. (V.) braziliensis [72, 94, 105, 110] in both species and Ny. intermedia blood meal analyses indicate that it is an eclectic feeder [10], showing that it is an anthropportunistic generalist. In a rural area of Minas Gerais, Ny. intermedia has been found to be infected [105] with L. (V.) braziliensis, L. (L.) infantum, and L. (L.) amazonensis. The earliest 1922 records [2] of Ny. intermedia presence in the homes of infected people indicated its anthropophily, and subsequent studies [130] have confirmed this.

The first indication of Ny. shawi’s anthropophily was in Bolivia [38] where it was found inside human dwellings and collected in Shannon traps in large numbers. In this study where L. (V.) braziliensis ACL was endemic, it was found to be infected with L. (V.) braziliensis and L. (V.) guyanensis, strongly indicating that it is an anthropportunistic generalist.

Nyssomyia trapidoi is a Central American species that is also found in Colombia and Ecuador [36]. It feeds on humans [32] and occurs in anthropogenic environments [80]. It has been found to be infected with L. (V.) panamensis [68, 77] and more recently with L. (V.) naiffi [8, 109] and Endotrypanum [41]. With changing environments, this species is responsible for L. (V.) panamensis [109] ACL. It has been shown to feed on a wide range of wild mammals, particularly primates [135], suggesting that it is an anthropportunistic generalist and an important ACL vector.

Nyssomyia whitmani has a long history of anthropophily [40] and is considered to be an important vector of L. (V.) braziliensis ACL throughout its extensive distribution in practically all Brazilian States, as well as in Argentina, Bolivia, Paraguay, Surinam, and the Guyanas [36]. In some areas, in overlaps with another important ACL vector, Ny. intermedia. Molecular studies [99] have shown distinct geographical populations and that there are some behavioral differences [17]. In different regions, it has been found to be infected with L. (V.) braziliensis [6], L. (V.) guyanensis [28], L. (V.) shawi [61], L. (L.) amazonensis [132], and L. (L.) infantum [120]. The evidence clearly shows that this is an anthropportunistic species and an important ACL vector of the first two parasite species. However, its participation in a cycle involving visceral parasite is uncertain.

Nyssomyia ylephilator is a Central American species that has been found to bite humans predominantly in forest environments, but also inside houses [32] and can be considered an anthropportunistic vector. It has been found to be infected with L. (V.) braziliensis [113], L. (V.) panamensis [77], and L. (L.) mexicana [95]. In Guatemala it was considered an L. (V.) braziliensis ACL vector together with Pintomyia ovallesi and Psychodopygus panamensis [113].

In the Amazon region of Ecuador, Ny. yuilli yuilli is anthropophilic because it is found in domestic settings. It has been found to be infected with L. (L.) amazonensis in the Brazilian Amazon [127], L. (V.) panamensis [118] in a domestic location in Colombia, and Endotrypanum sp., [41] and a possible L. (Mundinia) sp., [98] in Ecuador. This variety of parasites reflects eclectic feeding, but so far it has not been implicated as an ACL vector. Studies of vertical distribution showed this species to be more common in canopy catches [69]. Given these different characters, this species appears potentially to be an anthroaccidental generalist.

The genus Pintomyia

Species of this genus feed on humans, are found in anthropogenic biomes, and are considered to be important vectors of L. (Viannia) and L. (Leishmania) parasites. Infections of L. (L.) infantum have been found in Pi. evansi in Colombia [137]. This species extends from Mexico throughout Central America down into Peru and Venezuela [36]. In Honduras, it is considered a sympatric vector of VL, preferentially feeding on dogs and pigs [79]. A less well-known species, Pi. longiflocosa has so far only been found in Colombia [36]. Pintomyia fischeri has a long history of being a suspected leishmaniasis vector in Brazil. It has been found to be infected with L. (L.) braziliensis [110] and L. (L.) infantum [37]. In an ACL epidemic in Chaparral, Colombia [35] it was the dominant species, highly attracted to humans and endophilic. Infections with L. (V.) guyanensis were identified in patients and Pi. longiflocosa. An outbreak of L (L.) amazonensis ACL occurred in Inquisivi Province, La Paz [76] and infections with this parasite were later found in Pi. nuneztovari [75]. Infections with L. (V.) braziliensis [136] and L. (V.) lainsoni [9] have also been found in this same sand fly species. An infection with L. (V.) panamensis has been recorded [71] in Pi. pia captured in Colombian montane forest. The parasitological and epidemiological evidence indicates that the six species mentioned in this paragraph are anthropportunistic generalists.

Pintomyia ovallesi has an extensive geographical distribution that stretches from Mexico to Colombia, and then easterly across Venezuela to Trinidad [36]. It is attracted to humans in Central America [114] and in Venezuela, where it is endophilic [33]. It has been found to be infected with L. (L.) infantum [117], L. (L.) mexicana [53], L. (V.) braziliensis [114], and L (V.) panamensis [117], indicating that it is an anthropportunistic generalist. Given its endophilic habits, it is considered an L. (V.) braziliensis ACL vector and has potential vectorial roles for other parasites. Pintomyia robusta was shown to be attracted to humans, but so far has only been found to be infected with Endotrypanum [41], and because of this, it is not included in Table 1.

Pintomyia spinicrassa has a limited distribution in Colombia and Venezuela [36], is anthrophilic, and has been collected from humans in Colombia [1, 149]. It has been found to be infected with L. (V.) braziliensis in the mountainous area of Arboledas [149], in the Santander region with L. (L.) amazonensis, L. (V.) braziliensis, and L. (V.) panamensis [117], and in the Venezuelan Andean region with L. (V.) braziliensis [92]. It is considered one of the main L. (V.) braziliensis ACL vectors in these three regions and is characteristic of an anthropportunistic generalist.

Three Pintomyia species, Pi. columbiana, Pi. townsendi, and Pi. verrucarum have limited distributions in Peru, Columbia, and Venezuela [36]. All are considered as occurring in anthropogenic biomes and are attracted to humans [23, 145]. Leishmania (V.) peruviana has been recorded [23] in Pi. verrucarum and it was shown to transmit the same parasite experimentally. Leishmania (L.) amazonensis has been recorded in Pi. townsendi [52]. The available evidence indicates that these three species are anthropportunistic generalists.

The genus Psathyromyia

Of the species belonging to this genus, Psa. shannoni has the greatest geographical distribution from the United States down to southern Brazil [36]. In many situations, it is collected in small numbers [41] and in Amazonia, ten different species were captured in CDCs, but only one female in a Shannon trap [28]. However, in Mexican villages where ACL was endemic, it was the only species found to be infected with L. (L.) mexicana and was attracted to humans in Shannon traps [88]. Leishmania (V.) braziliensis has been found in Psa. aragoi [87], L. (L.) amazonensis in Psa. barrettoi majuscule [5], L. (L.) mexicana in Psa. cratifer [81], and an unidentified Leishmania in Psa. naftalekatzi [47]. In another endemic Mexican ACL region, Psa. cratifer was the dominant species collected in Shannon traps, but not in CDC traps [81]. The overall evidence indicates that Psathyromyia species are anthroaccidental generalists, but in specific environments that favor large populations, they may be the main species attracted to humans and therefore ACL vectors.

The genus Psychodopygus

The greatest number of Psychodopygus species is found in Amazonia, but few have been recorded in the Atlantic forest and Central America. To date, L. (Viannia) infections have been recorded in 13 Psychodopygus species. Of these, L. (V.) braziliensis was recorded in ten species and L. (V.) naiffi in seven species. There is conclusive evidence [64] that Ps. wellcomei bites humans in areas such as the Carajás mountains of Pará State, Brazil. There may be five times more Ps. wellcomei than Ps. davisi collected from humans. However, in regions such as Rondônia, where Ps. wellcomei does not occur, Ps. davisi was dominant in Shannon traps [39] and has been found to be infected with L. (V.) braziliensis. In the Paragominus region of Pará State, Brazil Ps. complexus was infected with L. (V.) braziliensis and attracted to humans [26]. This is a sympatric morphospecies with Ps. wellcomei and their females can only be differentiated by molecular methods [102].

The above are examples of the changing dominance of Psychodopygus species in different regions, where all are considered ACL vectors. There are records of 12 different Psychodopygus species in Rondônia [39] and 11 in the Tapajós FLONA (FLOresta NAcional), Pará State [27]. In both regions, Ps. davisi was dominant and there was a noticeable absence of Ps. complexus/Ps. wellcomei. Leishmania (L.) amazonensis [108] as well as L. (V.) braziliensis and L. (V.) naiffi [39] have been record in Ps. davisi from Rondônia. This suggests that the same species transmit the latter two ACL parasites. Parasites of the subgenus L. (Leishmania) are rarely found in Psychodopygus species, suggesting the existence of biological or environmental barriers preventing them from being infected and of being involved in their transmission.

Leishmania (V.) braziliensis has been recorded in Ps. amazonensis [108], Ps. ayrozai [24], Ps. carrerai [45], Ps. chagasi [108], Ps. clausterei [87], Ps. hirsutus [22], Ps. llanosmartinsi [24], Ps. lloydi [132], Ps. panamensis [113], Ps. squamiventris [45], and Ps. yucumensis [67]. Leishmania (V.) naiffi has been recorded in Ps. amazonensis [46], Ps. ayrozai [4], Ps. carrerai [98], Ps. hirsutus [27], Ps. maripaensis [28], Ps. paraensis [4], and Ps. squamiventris [45]. Seven leishmanial parasites have been recorded in Ps. panamensis: L. (L.) amazonensis [71], L. (L.) mexicana [89], L. (V.) braziliensis [113], L. (V.) naiffi [109], L. (V.) panamensis [118], L. (Mundinia) sp., [98], and a major-like parasite [98]. Only once has L. (L.) infantum been found in a Psychodopygus species, Ps. lloydi [66], reflecting the predominantly sylvatic habits of the species in this genus. The variety of parasites reflects captures in different regions and biomes, but reflects the generalist habits of these species given the wide variety of animals that host them.

There are bona fide records that Ps. amazonensis, Ps. davisi, Ps. carrerai, and Ps. paraensis bite humans [147]. In the original description, Ps. panamensis was recorded as biting humans [31] as well as being taken in human landing captures [41]. Taken together, these records, along with the different associated Leishmaniinae infections, strongly indicate that Psychodopygus species are anthropportunistic generalists.

The genus Trichophoromyia

Trichophoromyia ubiquitalis is the vector [129] of L. (V.) lainsoni. Records of flies do not appear in captures taken from human bait [147], but it is captured in light traps [28, 39, 129, 138] and in smaller numbers in Shannon traps [28]. However, on a single occasion, one female was captured biting a man [63] and there are human infections of L. (V.) lainsoni [128]. From this, it appears that under exceptional conditions, Th. ubiquitalis will bite humans, and as such, it is an anthropportunistic ACL vector. In the Belém metropolitan region, ten L. (V.) lainsoni ACL cases were seen over a 23-year period that represented 0.4 cases per year [42]. In an entomological survey in the same region, 23% of the phlebotomines captured in light traps were Th. ubiquitalis. This is an example of how an anthroaccidentalist can be responsible for a constant low level of ACL transmission. There is a single record of L. (L.) amazonensis in this same sand fly captured in Amazonas [127].

Leishmania (V.) naiffi is recorded in Th. triramula captured in Panama [109]. Infections with L. (V.) braziliensis have been found in Th. aurensis from Acre, Brazil [24, 133], L. (V.) guyanensis [133] and L. (V.) lainsoni [139] captured in Madre de Dios, Peru [139]. In both regions, L. (V.) lainsoni has been found in humans. Leishmania (V.) braziliensis has been recorded in Th. reburra from Ecuador [5] and Th. ininii from Brazil [140]. Infections with L. (V.) braziliensis and L. (V.) guyanensis have been found in Th. ruifreitasi captured in Acre, Brazil [133]. A recent review [119] of the vectorial importance of this sand fly genus concluded that there was increasing evidence of their putative role as vectors. I agree with this and consider that the available evidence suggests that Trichophoromyia species are anthroaccidental specialist ACL vectors. In Peruvian regions where over 60% of the sand flies were Th. aurensis [139], its ACL vectorial potential is greatly increased.

There are 57 named Trichophoromyia species [36]. So far only one, Th. triramula, has been found in Central America and they are absent in the southern regions of South America, including southern Brazil. The coincidental geographical distribution of Th. ubiquitalis [148] and L. (V.) lainsoni, but not with that of the paca (Agouti paca), its proven reservoir, strongly suggests a specific vector/parasite relationship between Trichophoromyia species and L. (V.) lainsoni.

Genus Warileya

Eight Warileya species have been described. In an endemic L. (V.) panamensis ACL locality of Colombia, W. rotundipennis represented 98% of the sand flies captured inside houses. It was found to be infected with a L. (Viannia) species and blood meal analysis was positive for human, sloth, cow, and marsupial blood [83]. Of the blood meals, 95% were human. This is not surprising as catches were performed with CDCs inside houses. These data indicate that W. rotundipennis is an anthropportunistic generalist. Warileya species can be found in different biomes ranging from caves and crevices to tree trunks. This is the first time that a species of this genus has been found inside houses, suggesting that some new environmental event may have occurred.

Zoophilic and nectar-feeding genera

Leishmania have been recorded in species of the following genera: Brumptomyia [98], Expapillata [29], Martinsmyia [105], Micropygomyia [43, 87, 98, 105, 106, 110], Pressatia [98, 109], Sciopemyia [20, 126], and Viannamyia [12]. It is unknown whether these represent chance infections due to a fortuitous encounter with an infected host, are involved in the maintenance of an enzootic cycle, or are transient infections that do not lead to transmission. All of the recorded parasites, except L. (V.) utingensis, found in L. (V.) tuberculata, have been found in humans. The identification of a L. (Mundinia) species in Br. leopoldoi is surprising as, so far, Brumptomyia species are considered nectar feeders. Also, the vectors of L. (Mundinia) species are midges. Could these parasites be trypanosomatids of plants being transmitted by phlebotomines?

The feeding habits of the species classified as zoophilic are poorly understood, and further ecological studies are needed to clarify their role in transmission and host interactions. Species of these genera are considered to be nectar feeders or hematophagous.

Discussion

Given phlebotomine sand flies’ antiquity and their feral life cycles, it is unlikely that their human seeking and anthropogenic biomes (anthropophily) are the result of evolutionary selection. This is more likely related to pre-existing behavioral traits. However, insects adapt rapidly to selective pressures, such as the dominance of melanisms of the peppered moth [21] and insecticide resistance [70]. There is evidence that sand fly populations that have been exposed to insecticides for many years become resistant [54]. As a result, it is possible that there could be behavioral selection for anthropogenic biomes that would bring them into greater contact with humans. One possibility would be gene flow or introgression between species found in the same biome that could potentially contribute to adaptation and evolution. Introgression has been found between two anthropportunistic species, Ny. intermedia and Ny. whitmani [73]. The former is well adapted to anthropogenic biomes. In areas where they are sympatric, Ny. whitmani lineages thrive in peri-domestic environments, but where they are not sympatric, they do not. This suggests that gene flow may have been responsible for this and other behavioral changes of Ny. whitmani.

The available evidence indicates that species that bite humans are generalists that evolved in environments where they feed opportunistically on a wide range of animals. For instance, in Colombia [43], Lu. gomezi was found to have fed on chickens, pigs, dogs and humans, confirming its generalist and anthropportunistic habits. Epidemiologically important anthropportunistic species belong to the genera Lutzomyia, Nyssomyia, Pintomyia, and Psychodopygus. However, there are biological distinctions between them. All occur in natural biomes, but so far, Psychodopygus species have not adapted to anthropogenic environments as have some species of the other three genera. Such behavior increases their chance of feeding on humans and consequently being the main ACL vectors. It has been shown that Ny. whitmani preferentially returns to a site [16] where a particular food source is located. This would clearly favor contact with that host. In southern Brazil, Ny. whitmani is found in greater numbers in anthropogenic sites [134], which enhances its contact with humans and chances of feeding on them.

To date, Ny. whitmani has been shown to consist of at least three mitochondrial lineages [99], one in Amazonia and two in eastern Brazil. Studies on their attractiveness [17] indicated that the most southeastern lineage had a greater preference for humans than the other two and that the greatest numbers of individuals in the southern lineage occurred in peri-domestic environments. Previously Amazonian Ny. whitmani populations were recorded as not being attracted to human-based ground level catches in forested regions [60]. A possible explanation for these conflicting conclusions is that population densities of this species are lower at ground level and higher in the canopy. Additionally, Ny. whitmani was considered to be the vector of L. (V.) shawi and an outbreak of this parasite occurred in southeast Amazonia [123]. Subsequently, peri-domestic populations of the Amazonian lineage were found in the region of the outbreak [100]. It is quite remarkable that a species that in its sylvatic habitat is a canopy dweller adapts to anthropogenic biomes. This probably occurred because the females found suitable oviposition sites that were rich in organic material in these biomes, resulting in the production of adult flies that subsequently increased the chances of their feeding on humans. The migration from sylvatic to anthropogenic biomes is well documented for Lutzomyia species such as Lu. longipalpis.

Determining the role of a sand fly in ACL and AVL epidemiology is complex. Over the years, various criteria have been used. Evidence of infection is primordial together with being attracted to humans. A recent publication evaluated the vectorial status of sand flies found infected in Colombia [96]. The authors created five vectorial levels that graduated from 1, based on just detecting parasite DNA, to 5 which was a proven vector. The vectorial statuses of the flies with infections reviewed in this paper fall within these five categories. However, the problem is that there are records in different countries where a species may be a vector in one but not in the other. Because of this difficulty, irrespective of the country, certain species have been highlighted as being proven vectors in Table 1. The vectorial situation of a sand fly species is further complicated when more than one species has been found to be infected with the same parasite in the same biome.

A study of Ecuadorian [41] sand flies using human landing collections showed marked differences in the dominance of different species collected from humans. In a coastal region, Ps. maripaensis represented 0.1% of the total, yet in a mountainous region, it was 9.7%. A more marked example was Lu. ayacuchensis that was 47.5% of the catch in the Andean region, and merely 1.4% in the Amazon region. At higher altitudes, Lu. ayacuchensis is an anthropportunist species, but if studies had been limited to the Amazonian lowlands, it could be categorized as an anthroaccidentalists due to the low numbers captured from humans. This indicates that relative attraction of phlebotomine species to humans can only be accurately assessed when their population dynamics are known. To do this, population densities must be evaluated simultaneously using different methods in different biomes.

Under the present-day ethical environment, the definitive solution of knowing whether a species feeds on humans is blood meal analysis using molecular methods. Beyond this, there is circumstantial evidence when the same parasite is found in both a sand fly and human in the same biome, but it is not definitive proof of it feeding on humans as other species could transmit the same parasite.

Conclusion

Sand fly generalist or specialist status is related to the parasite species found in them and the hosts that they feed on. Of the 75 generalist species, 52 were considered anthropportunists, 5 anthroaccidentalists, and 18 zoophilic. The anthropportunists included important ACL and AVL vectors. Zoophilic species may participate in the maintenance of the leishmanial enzootic cycle. The Leishmania species associated with the 12 anthroaccidentalist species of the genera Bichromomyia, Psathyromyia, and Trichophoromyia are less common in humans, but under specific environmental circumstances may become ACL vectors. The majority of records are based on molecular parasite identifications, so it is impossible to say whether they represent transmissible or dead-end infections. Importantly, finding a parasite in a sand fly solely indicates a potential vectorial role that needs to be investigated in greater detail.

As more precise information on the biology of sand fly species becomes available, it will be possible to fine tune these categories. Finding the same parasite in sand flies belonging to different categories poses many questions. Combinations of 157 individual Leishmania infections were recorded in 91 sand fly species (Table 1). These varied from infections of one Leishmania species to seven in a single sand fly species. There are records of L. (V.) braziliensis in 43 different sand fly species, of which 29 are anthropportunists, one is an anthroaccidentalist, and 12 are zoophilic species. Concerning the epidemiological significance of this, one possibility is that it generates the extensive genetic diversity of this species [51] and that the relative epidemiological importance of a particular sand fly species is associated with a specific biome. Also, mere records of parasites in a species do not indicate its vectorial or epidemiological importance, and zoophilic species of interest may be playing a part in the maintenance of the enzootic cycle. Infections of L. (V.) naiffi continue to be found [46] and it has now been recorded in 18 species belonging to the three different categories. Anecdotally, Ps. ayrozai has sometimes been selected as the main vector, as it was detected feeding on armadillos, but presumably the other infections were acquired feeding on armadillos or perhaps other animals. Similarly for L. (V.) braziliensis, it is likely that the extensive genetic diversity of the armadillo Leishmania is linked to its presence in many vectors. Such questions are associated with the species in which L. (V.) guyanensis, L. (V.) panamensis, and L. (L.) infantum have been found.

The problem with the terms “anthropophily” and “anthropophilic” is that they are overgeneralizations that unfortunately promote misleading simplifications of sand fly behavior. In relation to feeding, they falsely suggest a deliberate preference for humans when sand flies are opportunistic feeders, biting humans only when other hosts are unavailable. Such anthropocentric biases obscure the true ecological dynamics of vector-host interactions, ultimately weakening our understanding of disease transmission. The use of the generalist and specialist concept, and the introduction of the terms anthropportunist and anthroaccidentalist, are aimed at diminishing these distortions, fostering a more precise, evidence-based approach to evaluating sand fly behavior and its role in the intricate epidemiology web of leishmaniasis in the Americas.

Acknowledgments

I wish to thank Jérôme Depaquit and Luigi Gradoni for their encouragement in finishing this paper and to the anonymous reviewers for their helpful and pertinent comments.

Funding

Brazilian Research São Paulo Research Foundation grant 307937/2021-6 [Fundação de Amparo à Pesquisa do Estado de São Paulo] grants 2012/05388-4; 2022/08550-9.

Conflicts of interest

The author declares no conflicts of interest.

★

This paper is based on a talk given in 2024 at the 11th International Phlebotomine Symposium on Sandflies (ISOPS XI) held in Portorož, Slovenia.

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Cite this article as: Shaw JJ. 2025. A review of Leishmania infections in American Phlebotomine sand flies – Are those that transmit leishmaniasis anthropophilic or anthropportunists?. Parasite 32, 57. https://doi.org/10.1051/parasite/2025039

All Tables

Table 1

The feeding habits and Leishmania infections of American Phlebotomine species.

In the text

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