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J Vector Borne Dis 53, March 2016, pp. 70–76
Phlebotomine sandflies (Diptera: Psychodidae) in a sub-Andean forest from
the Norte de Santander, Colombia
Richard Hoyos-López1, Rafael Bolaños2, María Contreras-Gutierrez3 & Diego Carrero-Sarmiento2
de Resistencia Bacteriana y Enfermedades Tropicales, Universidad del Sinú, Facultad de Ciencias de la Salud, Montería, Córdoba;
Laboratory-Ecology and Biogeography Research Group, Basic Sciences Faculty, Universidad de Pamplona, Pamplona;
3Molecular Systematics Group, Bioscience School, Universidad Nacional de Colombia, Medellín, Antioquia, Colombia
Background & objectives: The recognition of communities of arthropods with medical importance in natural
systems constitutes an important step in the prediction of possible epidemic events and/or emergence of infectious
diseases in the human population. This is due to anthropogenic impact in natural areas and landscape modification,
which changes the dynamics of pathogenic agents, reservoirs, and vector insects. In this study, an inventory was
compiled of species of the genus Lutzomyia present in sub-Andean forest from the confluence of the Pamplonita
River basin.
Methods: CDC-light and Shannon traps were used for collecting adult phlebotomine sandflies during the month
of October 2013 in a sub-Andean forest from river basin Pamplonita. All specimens were identified using
morphological keys. The epidemiological relevance of each species was reported using a literature review about
natural infection or vector incrimination with Leishmania species or other pathogens microorganism.
Results: A total of 2755 specimens belonging to eight species of the genus Lutzomyia were collected. Out of the
eight species, seven belonged to the group verrucarum (Lutzomyia sp — townsendi series, L. ovallesi, L. spinicrassa,
L. serrana, L. townsendi, L. nuneztovari and L. pia), while one belonged to the subgenus Helcocyrtomyia
(L. hartmanni). A new registry of L. townsendi was observed for the Norte de Santander department.
Interpretation & conclusion: The appreciable diversity of the verrucarum group observed in this area suggest
further investigation on the biogeography and evolution of this group, and epidemiological risk for human
populations around this area, as there are reports of Leishmania natural infection and favourable conditions for
domestication of phlebotomines in rural towns.
Key words Leishmaniasis, Lutzomyia; Norte de Santander; Phlebotominae; sub-Andean forest
The genus Lutzomyia (Franca 1924) (Diptera: Psychodidae), include species with hematophagous and anthropophilic habits, responsible for the transmission of
microorganisms pathogenic to humans1–5. These act as
biological vectors of protozoans of the Leishmania
genus, which are responsible for the tropical disease
leishmaniasis in its cutaneous, mucosal, and visceral
For this reason, knowledge of the presence and geographic distribution of arthropods of the genus Lutzomyia
might play a major role in the estimation of basic aspects
of epidemiological risk for human populations, vector
incrimination, and establishment of schemas focused on
their prevention and/or control7–9. These aspects require
the taxonomical identification of species of the genus
Lutzomyia, as well as knowledge of the composition of
species in natural and fragmented ecosystems, where hu-
man dynamics favour the emergence of cycles of active
transmission in habitats where human-vector contact
occurs7–8, 10.
Norte de Santander is a zone in northeast Colombia
which has registered significant increase in the cases of
leishmaniasis in 2014, documenting 275 cases (273 cutaneous, 2 mucosal, and 1 visceral)11. From an epidemiological perspective, this is a consequence of the increase
in diversity of the Lutzomyia genus in this department to
37 species12–13, and an appreciable percentage of the fauna
incriminated as a vector for cutaneous and visceral forms
of leishmaniasis in Colombia14. Sub-Andean forest at the
confluence of the Pamplonita River constitutes a natural
stage with potential for human ecotourism, farming, and
mining activities; which might result in fragmentation of
natural habitats. The probable consequences are displacement and change in the communities of reservoirs and
pathogenic vector insects and the emergence of infectious
zoonotic diseases15. Some species of the genus Lutzomyia
Hoyos et al: Sandflies of sub-Andean forest
have been able to adapt to degraded habitats and urbanized area; contributing to increased dispersion and prevalence of cases associated with the clinical forms of leishmaniasis8, 16–19. This study registers, for the first time,
the phlebotomine fauna of the Lutzomyia genus present
in a sub-Andean forest located in the Cucalina Valley associated with the Pamplonita River confluence in Norte
de Santander, for its economic potential for human activities and the presence of Lutzomyia species with epidemiological relevance involved in the active transmission of leishmaniasis and other emerging pathogens of
bacterial or arboviral origin.
Study area
The sampling area corresponded to the La Cucalina
Valley (7° 27' 52.3'' N, 72° 36' 49.9" W) which belongs
to the village of San Antonio; under the municipality of
Pamplonita, Norte de Santander department, located in
the sub-Andean forest biome and representing 33.2% of
the total area of the mountainous zone at the confluence
of the Pamplonita River surrounded by the municipalities of Pamplona, Pamplonita, Bochalema, and Chinácota;
with an altitudinal range between 1000 and 2000 m above
sea level (masl), average temperature between 6 and 22°C;
and annual precipitation between 800 and 2000 mm
(Fig. 1)20. The predominant vegetation is characterized
by an abundance of the family Lauraceae, with Aniba
cinnamomiflora, Phoebe triplinervia, and Ocotea species
being most common20.
Collection and identification of phlebotomines
Entomological sampling was done during the month
of October 2013, and was directed toward places suitable
for the development of immature stages, potential humanvector contact, dispersion range, and distance from human dwellings8, 21. For the collection of adult sandflies,
three white light CDC traps, installed at a height of 1.30
m from the ground and connected to a 6 V power source
and a Shannon trap were utilized from 1800 until 0600
hrs. Exemplars collected were dry-preserved in Eppendorf
1.5 ml vials, deliberately rotated, and transported to the
Entomology Laboratory at Pamplona University for their
taxonomic identification.
Insects of the genus Lutzomyia were separated from
the other dipterans by external morphological characteristics and later cleared with a 1:1 lacto-phenol solution
for 24 h in order to see the internal structures of females
(spermathecae, common and individual ducts, cibaria) and
males (ejaculatory apparatus, sperm pump, aedeagus).
Fig. 1: Location of sub-Andean forest, the sampling site for sandflies
of the genus Lutzomyia at the confluence of the Pamplonita
River (Norte de Santander, Colombia).
Later, individuals were mounted on stickers for taxonomic
identification based on the Young and Duncan22, IbáñezBernal23; and Galati24 keys.
Data analysis
Abundance of the identified species is described in
percentage frequencies, tables, and graphs using R-project
3.0.2. The epidemiological relevance of each species was
argued based on prior instances of natural infection with
Leishmania species or other pathogens, behaviour, and
biting habits.
A total of 2755 specimens (196 males and 2559 females) belonging to eight species of the genus Lutzomyia
were collected, namely Lutzomyia sp (townsendi series),
L. ovallesi (Ortiz 1952), L. spinicrassa (Morales, Osorno,
Osorno & Muñoz 1969), L. townsendi (Ortiz 1959), L.
serrana (Damasceno & Arouck 1949), L. nuneztovari
(Ortiz 1954), L. pia (Fairchild & Hertig 1961), and L.
hartmanni (Fairchild & Hertig 1957); the first seven corresponding to the group Verrucarum (Theodor 1965), and
the last to the subgenus Helcocyrtomyia (Barreto 1962).
The richness of the collected species did not vary significantly with respect to the type of trap used, except for
L. pia, which was collected with Shannon trap. This
J Vector Borne Dis 53, March 2016
method was more efficient (requiring least effort) in registering the abundance of the species identified (80.98%),
as compared to CDC traps (19.01%) (Table 1). Lutzomyia
sp (townsendi series) was the most abundant taxon; however, its taxonomical identification was not possible due
to the absence of males in the collection. The verrucarum
group was amply found in the study area, with a new
registry for Norte de Santander of the species L. townsendi,
increasing the diversity of the verrucarum group to 11
species for this region, making it the most representative
group of this department, thus totaling the species to 38
for the Lutzomyia genus. The L. ovallesi was second-highest abundant species, showing a significant difference
between males and females collected (1:48), a phenomenon that was also observed in L. serrana (1:12), but not
in L. spinicrassa (2:1).
The identified species showed both experimental and
natural records of infection for protozoans of the genus
Leishmania, or are suspected to be implicated in the transmission of cutaneous leishmaniasis and bartonelosis in
active zones (Table 2). The literature review carried out
in this study did not show records of natural infection of
arbovirus of medical importance.
The registry of seven species of the group verrucarum,
genus Lutzomyia in an altitudinal range from 1800–2300
masl is an interesting observation for this group from both
phylogeographic and biogeographic perspective, as it is
highly diverse in the northwest of South America, with
an Andean distribution of endemic species described in
Colombia, Ecuador, Peru, and Bolivia22, 25–26.
The speciation of the group verrucarum was considered a consequence of climatic changes characterized by
cyclic periods of glaciation and recession during the past
2.4 million year, which resulted in the isolation of
phlebotomines in refuges of humid forest since the quaternary period25. Other factors responsible for their speciation/geographical separation include the limited capacity of flight dispersion; restriction of gene flow and
population migration27–29 and allopatric fragmentation25.
Paleontological evidence shows the altitudinal fluctuation of Andean forests between 3300–3600 masl and
2000 masl30. In this sense, the sub-Andean forest at the
confluence of the Pamplonita River constitutes an ideal
location for the study of the evolutionary diversification
and ecological niche of the L. townsendi group
verrucarum, with increasing altitudinal range to 2150 m
in comparison to the reports in the Cordillera Occidental
where this species inhabits between 1450 and 1799 masl26.
L. townsendi is a probable vector for Le. brazilliensis in
the Valle del Cauca department22, 25–26, due to experimental evidence of vector competence for this pathogen31–33.
A considerable number of identified species showed
an association with diverse habitats within the Andean
region and an appreciable concentration of diversity related to coffee ecosystems14, 25–27, 34. Additionally, the
significant epidemiological evidence of their vectorial potential in the transmission of cutaneous leishmaniasis
(Table 1) constitutes a risk factor in agricultural ecosystems. Also, species such as L. ovallesi and L. spinicrassa
showed a high capacity for adaptation to anthropogenic,
peri-urban, and urban ecosystems; and contribute to the
appearance of urban cases of cutaneous leishmaniasis17, 19.
In dry forests of the Atlantic Coast, the presence of one or
two species of the group verrucarum has been described16,
35–36 and in Andean humid forests, the presence of up to six
or more species has been registered14, 26, similar to that in
our study (Table 2), with an appreciable morphological
Table 1. Species of Phlebotomine sandflies collected in a sub-Andean forest from River La Cocalina in the
river basin Rio Pamplonita (Norte de Santander, Colombia)
CDC trap
Shannon trap
Lutzomyia sp (series townsendi)
Lutzomyia ovallesi
Lutzomyia spinicrassa
Lutzomyia townsendi*
Lutzomyia serrana
Lutzomyia nuneztovari
Lutzomyia hartmanni
Lutzomyia pia
*New record for Norte de Santander (Colombia); Figures in parentheses indicate percentages.
1323 (48.02)
1166 (42.32)
122 (4.42)
67 (2.43)
51 (1.85)
18 (0.65)
6 (0.21)
2 (0.07)
Hoyos et al: Sandflies of sub-Andean forest
Table 2. Registers of natural infection by pathogenic microorganisms and bitebehaviour for species identified in a sub-Andean
forest of the Pamplonita River confluence in Norte de Santander, Colombia
Infection — genus Leishmania
Biting behaviour
Flagellates not identified
Leishmania amazonensis (Experimental)
Leishmania mexicana (Natural)
Leishmania braziliensis (Natural and experimental)
Leishmania panamensis (Suspected)
Williams et al37; Christensen et al38; Young
et al39; Bonfante et al40; Rownton et al41;
Alexander et al34; Barrios et al42; Feliciangeli
et al43; Santamaría et al44; Nieves et al45;
Nieves and Rondon46
Leishmania braziliensis (Natural)
Leishmania mexicana (Natural)
Leishmania spp
Young et al39; Alexander et al34; Maingon
et al47; Young and Duncan22; Perruolo et al48
Carnevali and Scorza31; Carnevali and Scorza32;
Scorza and Delgado49; Young and Duncan22
Bartonella spp
and Leishmania spp (Suspected)
Leishmania braziliensis
Young and Duncan22; Santamaría et al44;
Dujardin et al50
Leishmania sp (Natural)
Young and Duncan22
Leishmania colombiensis (Natural)
Leishmania panamensis (Suspected)
Leishmania equatorensis (Natural)
Kreutzer et al56; Young and Duncan22;
Furuya et al51
Lutzomyia pia
Leishmania braziliensis (Experimental)
Warburg et al52
braziliensis (Suspected and natural)
garnhami (Natural)
spp (Experimental)
mexicana (Experimental)
similarities that make their identification difficult, and
consequentially, determine the epidemiological importance
of similar species with sympatric distribution25.
In this sense, the development of alternative taxonomic tools that permit the discrimination of females with
high abundance in the collection area, without the presence of males, in order to successfully determine up to
the species category, as in the case of Lutzomyia sp
(townsendi series); a solution is the use of molecular
markers such as tRNA-SER53, cytochrome B54 and cytochrome oxidase I (DNA barcode)9, 55–57, the use of which
presents notable advances in the identification and differentiation of species, vector incrimination, evolution in
species complexes, and identification of immatures58–62.
The high abundance of L. ovallesi in sub-Andean forest may reflect the availability of favourable microclimates for the development and care of immatures. Recently, the isolation of larvae of this species has been
described in leaf litter of areas relatively exposed to the
direct light, dessication, and precipitation in a transitional
forest (humid-dry) in Colosó (Sucre) 36, considering
that anthropophilic species show a preference for leaf lit-
ter as nursery sites in wild environments due to their external composition, texture, and stability; as these areas
permit the development of abundant populations of
This ecological feature acquires notable transcendence
when it is observed that one of the principal consequences
of deforestation and areas conserved for the construction
of hydroelectric dams, roads, aqueducts, and agricultural
development favour nursery areas with abundant substrates
and decomposed organic material, the presence of domestic animals with abundant food supplies, and species such
as L. evansi and L. ovallesi, with shorter life cycle (39–42/
49–64 days, respectively)65–66 in comparison with life cycle
of other members of the verrucarum group (94–97 days)67.
All these factors suggest a rapid adaptive tendency
for the colonization and invasion of new habitats in
anthropically modified ecosystems18, 68, in which the inadequate management of organic wastes and precarious
sanitary conditions create attractive environment for rodents and marsupials, which are natural reservoirs for
Leishmania species69, thus initiating emergencies and epidemic outbreaks of Leishmaniasis68 and urbanizing the
J Vector Borne Dis 53, March 2016
disease17, 19. Several studies indicate the importance of
the peri-domicile in new human settlements, for the presence of farms with chicken coops, dairy cattle, swine,
and horses8; and the communities of phlebotomines inhabiting in fragments of forest close by influence the dynamics of parasitic transmission for Leishmania species
due to changes in the differential access to reservoirs and
hosts communities70.
L. hartmanni was the only registry that was different
from verrucarum belonging to the subgenus
Helcocyrtomyia—sanguinaria series24, with a significant
presence in the coffee ecosystems and wild forests
associated with animal burrows and trees of great
bearing14, 71. It was implicated in the transmission of
Leptodactylus colombiensis, an etiological agent of cutaneous leishmaniasis72.
The presence of a community represented by the
group verrucarum of the genus Lutzomyia with a history
of the transmission of protozoa responsible for the cutaneous form of leishmaniasis constitutes a pattern that is
interesting for the biogeography and phylogeny of this
group of species at the confluence of the Pamplonita River,
and allows for the planting of questions with reference to
the variation in structure and composition of the species
present in the altitudinal range of the confluence (2400–
800 m) to the city of Cúcuta (capital of the department of
Norte de Santander). The possible ecology of the transmission of leishmaniasis in this zone, adaptation to artificial human ecosystems, and the influence of the modifications to the landscape are the aspects that favour the
domestication of populations of phlebotomines compatible with Leishmania species. The invasion of reservoirs,
and the presence of domestic animals and susceptible
hosts; might favour the ecology of the disease in human
ecosystems, contributed to the emergence of outbreaks
and epidemics of leishmaniasis. In conclusion, it is necessary to identify patterns of diversity of the Lutzomyia
genus, rates of natural infection of Leishmania, biting
behaviour, and nursery sites in order to identify the areas
of most probable emergence and to generate a prevention
strategy for this disease.
The authors are grateful to Convocatory 528–
Colciencias for providing Ph.D scholarship to Richard
Hoyos-López and University of Pamplona-research
vice-rectory (Intern convocatory).
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Correspondence to: Dr Diego Carrero-Sarmiento, Entomology Laboratory-Ecology and Biogeography Research Group, Basic Sciences
Faculty, Universidad de Pamplona, Pamplona, Colombia.
E-mail: [email protected]
Received: 14 December 2015
Accepted in revised form: 2 January 2016