phlebotomine sandflies and leishmaniasis risks in colombian coffee plantations under two systems of...

Phlebotomine sand¯ies and leishmaniasis risksin Colombian coffee plantations under two systemsof cultivation

B , A L E X A N D E R * , L . A . A G U D E L O ² , F . N A V A R R O ² , F . R U I Z ² ,

J . M O L I N A ³ , G . A G U I L E R A ³ and M . L . Q U I NÄ O N E S ²

*Centro de Pesquisas Rene Rachou, Ministerio de SauÂde/FundacËaÄo Instituto Oswaldo Cruz, Avenida Augusto de Lima 1715,

Belo Horizonte, Minas Gerais 30190-002, Brazil, ²Programa de Estudio y Control de Enfermedades Tropicales (PECET)

Universidad de Antioquia, Apartado Aereo 1226, Medellin and ³Centro de Investigaciones en Microbiologia y Parasitologia

Tropical, Universidad de los Andes, Carrera 1A no. 18 A-70 BogotaÂ D.C., Colombia

Abstract. The phlebotomine sand¯y fauna of traditional (shaded) and intensi®ed

(unshaded) coffee plantations in Colombia was sampled by a variety of methods

and the species composition and density under the two systems compared. Twenty

species of Lutzomyia sand¯ies (Diptera: Psychodidae: Phlebotominae) were

collected, of which eight were found only in the `Coffee Axis' (`Eje Cafetero') of

the departments of Caldas, Risaralda and Quindio, six were exclusive to the

department of Norte de Santander and six occurred in both regions. Four species

were collected only in traditional plantations and two exclusively in intensi®ed

ones. At least 13 species occurred in both plantation types. Fifteen species are

opportunistic man-biters and eight are suspected vectors of leishmaniasis caused by

Le. braziliensis, Le. panamensis or Le. mexicana. Seven species were collected

inside houses and may be involved in intradomiciliary transmission of Leishmania.

The dominant species in Norte de Santander was Lu. spinicrassa, which made up

93.8% of all the sand¯ies collected in this department. This species was absent

from the Eje Cafetero and a number of others among the 15 recorded there might

be responsible for Leishmania transmission in this region, including Lu. trapidoi,

Lu. yuilli, Lu. gomezi, L. hartmanni and Lu. ovallesi. Sand¯y population densities

were signi®cantly higher in traditional plantations than in intensi®ed ones.

Residents of traditional plantations were able to describe sand¯ies in signi®cantly

more detail than those of intensi®ed plantations, based on seven basic

characteristics related to the appearance and biting behaviour of the insects.

Key words. Leishmania, Lutzomyia, Psychodidae, coffee, leishmaniasis, risk

analysis, Colombia.

Introduction

The relationship between coffee cultivation and Leishmania

transmission by phlebotomine sand¯ies was ®rst noted by

Scorza & Rojas (1988) in Venezuela and Warburg et al. (1991)

in Colombia. In both countries optimum conditions for coffee

growing occur in mountainous areas at 1000±2100 m a.s.l.,

where the tegumentary leishmaniases caused by members of

the Le. (Viannia) braziliensis and Le. (Leishmania) mexicana

species complexes are the most important vector-borne

diseases (Montoya et al., 1990; Montoya-Lerma, 1990).

Although autochthonous cases of tegumentary leishmaniasis

have been recorded from all but three of the 32 departments of

Colombia, at least 1700 (29.7%) of the 5716 cases of

leishmaniasis reported to the Ministry of Health in 1994

were from coffee-growing muncipalities.

The arrival of coffee rust fungus Hemileia vastatrix in 1984

was the principal motive for the intensi®cation of Colombian

plantations, a process by which so-called `traditional' planta-

tions in which coffee of the `arabica borboÂn' and `tõÂpica'Correspondence: B. Alexander. E-mail: bruce@cpqrr.®ocruz.br

364 ã 2001 Blackwell Science Ltd

Medical and Veterinary Entomology (2001) 15, 364±373Medical and Veterinary Entomology (2001) 15, 364±373

varieties grown under the shade of large trees were replaced by

the fungus-resistant `colombia' variety, which can be grown

under full sunlight in more extensive monocultures

(Valenzuela Samper, 1990). Although relatively small in area

(1.61 ha being the average in Colombia), traditional planta-

tions often represent the only remnants of forest in a particular

area and support a rich diversity of plant and animal species,

including phlebotomine sand¯ies (Diptera: Psychodidae),

some of which transmit Leishmania to man. The insects have

a limited ¯ight range of a few hundred metres (Alexander,

1987; Alexander & Young, 1992) but are able to encounter all

their vital requirements within this small area. These include

(i) terrestrial breeding sites rich in organic matter, (ii) diurnal

resting sites, including leaf litter and the trunks of shade trees,

many of which shed their leaves completely during the dry

season, (iii) sources of sugar meals, probably obtained by

piercing the tissues of plants (Alexander & Usma, 1994) and

from deposits of insect honeydew (Moore et al., 1987), and

(iv) sources of bloodmeals, including wild animals and birds,

domestic livestock and the human residents of the plantation,

who live adjacent to or within the coffee crop. As the wild

mammals bitten by sand¯ies may include reservoirs of

Leishmania such as rodents and opossums (Alexander et al.,

1998), all the factors necessary for transmission of leishma-

niasis may be concentrated within a relatively small area.

Some idea of the man-biting activity of sand¯ies in coffee

plantations can be obtained by the ability of growers to identify

the insects, this being an important prerequisite for any

leishmaniasis control measure that depends on community

participation (Alexander et al., 1995; Koirala et al., 1998).

Phlebotomine sand¯ies are known in Colombia by a variety of

common names that demonstrate the ability of people in

Leishmania-endemic areas to distinguish them from other

biting ¯ies. These names include `manta blanca' (`white

mantle') and `palomilla' (`little dove'), referring to the whitish

colour imparted by the water-repellent oil that covers the hairy

bodies of these insects, as well as `quemador' (`burner') and

`pringador' (`stinger') referring to the pain of their bites. The

name `aguilita' (`little eagle') may refer to the erect, V-shaped

posture of the wings at rest.

Coffee leaves contain high levels of protective alkaloids

(P. Mazzaferra, personal communication). There were apparently

no native species in the New World that had evolved mechanisms

to overcome these defences, a common phenomenon in plant

introductions (Frischknecht et al., 1966). Colombian coffee thus

had no serious insect pests until the arrival in 1988 of the coffee

berry borer or `broca' (Hypothenema hampei), a scolytid beetle

native to Africa. Agrochemicals taint the subtle ¯avour and

aroma of the mild coffee produced in Colombia and the

Colombian coffee grower's federation FEDERACAFE discour-

ages insecticide use. Nevertheless, many growers use chemicals

such as the organophosphate Thiodanã (endosulphan) against

H. hampei, often at doses much higher than those recommended

by the manufacturers and/or mixed with other chemicals. The

effect of these sprayings on sand¯y populations in coffee

plantations is unknown, although diurnal resting sites, breeding

sites and human habitations (in which sand¯ies take blood-

meals) are not targeted.

A number of other methods of controlling H. hampei have

been employed, including mass release of parasitic wasps,

spraying with the entomopathogenic fungus Beauveria bassa-

nia and removal and collection of all infected coffee cherries

by hand (`reÂ-reÂ'). None of these methods is likely to affect

sand¯y populations in coffee plantations, although a strain of

B. bassiana pathogenic to sand¯ies has been produced in the

laboratory (Warburg, 1991). Commercially available strains

tested against sand¯ies under laboratory and ®eld conditions

were found to be innocuous (Reithinger et al., 1997).

Although no information was available prior to the present

study on the suitability of intensi®ed plantations as habitats for

sand¯y vectors and mammalian reservoirs of Leishmania,

several of the changes associated with intensi®cation would

seem to reduce the likelihood of transmission to man. Removal

of shade trees results in a reduced production of leaf litter and

destruction of sand¯y diurnal resting sites, as well as removal

of potential food sources for frugivorous mammals. Intensi®ed

plantations are also larger, with a smaller human population

density, the grower, his family and workers generally living at

the edge of the crop rather than within it. Sand¯ies living in an

intensi®ed plantation would be exposed to higher levels of

sunlight by day and less protected from wind when active at

night. Reduced transmission of Leishmania, however, could

therefore be seen as a collateral bene®t of intensi®cation and

that should be taken into account by coffee-growing and health

authorities. With this in mind, the objectives of the present

study were to sample the phlebotomine sand¯y fauna of both

traditional and intensi®ed coffee plantations and compare the

species composition and density under the two systems.

Information on awareness of the insects by coffee growers

was also collected.

Materials and methods

Study area

There are four main coffee-growing regions in Colombia: (i)

the Cordillera Central, including the departments of Risaralda,

Quindio, Tolima, Cundinamarca, Huila and NarinÄo, as well as

parts of Caldas, Antioquia and Valle; (ii) the Cordillera

Occidental, including parts of the latter three departments as

well as Cauca; (iii) the Cordillera Oriental, consisting of the

departments of Santander, Norte de Santander and Boyaca; and

(iv) the Sierra Nevada, a mountain range geologically distinct

from the three Andean ranges, located in the departments of

Magdalena, Cesar and Guajira. Sand¯y collections were made

in coffee plantations in 10 municipalities (Fig. 1), representing

two of the above regions (Cordillera Central and Cordillera

Oriental).

Sand¯y sampling

A combination of sampling methods was used to obtain the

best pro®le of the phlebotomine sand¯y fauna in the limited

time available. Insects were collected in two traditional and

ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 364±373

Phlebotomine sand¯ies and leishmaniasis risks 365Phlebotomine sand¯ies and leishmaniasis risks 365

two intensi®ed plantations of each municipality by the

following methods.

Diurnal resting site collections. Insects were aspirated

during daylight hours directly from the trunks of 20 shade

trees (traditional plantations only) and/or by disturbing the leaf

litter under a mesh-covered wooden frame of triangular cross-

section (Alexander, 2000) placed on the ground in 100 spots

within each plantation and collecting ¯ies that ¯ew up onto the

sides of the trap (traditional and intensi®ed plantations). These

collections comprised sand¯ies that had not been attracted

from marginal wooded areas by light or host-produced stimuli.

Insects collected from leaf litter included gravid females and

recently emerged adults, indicating the presence of breeding

sites. Resting site collections are an important supplement to

those made by light traps and/or human bait, as they also

sample non-phototropic species that do not bite man, including

those involved in Leishmania transmission between wild

mammals. They also generally include large numbers of

males, whose presence permits distinction among species

whose females are morphologically identical, such as members

of the medically important Lu. verrucarum group.

Illuminated Shannon trap collections. Sand¯ies attracted to

illuminated Shannon traps manned by two volunteers were

collected between 18.00 and 20.00 hours, i.e. within 2 h of

sunset. Collections were made simultaneously in traditional

and intensi®ed plantations and represented the most ef®cient

way of collecting large numbers of sand¯ies, principally those

belonging to man-biting species.

Sticky trap collections. Twenty sticky traps (half sheets of

A4 paper impregnated with castor oil) were hung in two houses

of each plantation type, 10 each at ground and ceiling levels.

The traps were left in place for ®ve nights and then revisited,

sand¯ies that had adhered to the traps being removed carefully

with a mounted needle and rinsed in detergent solution prior to

clearing in lactophenol and identi®cation to species. As this

method involves the interception of ¯ying insects rather than

attraction to light or host-produced stimuli, relatively few

sand¯ies could be collected in the short time available.

However, the specimens caught allowed the identi®cation of

species that might be involved in intradomiciliary transmission

of Leishmania.

All specimens were preserved dry for transportation to the

laboratory, where they were cleared in lactophenol and

identi®ed to species (Young & Duncan, 1994).

Comparison of sand¯y faunae of traditional and intensi®ed

plantations

The proportion of species known to be opportunistic man-

biters among the sand¯y fauna of each plantation was noted

and the species composition of each plantation compared based

on calculation of Jaccard's (1908) coef®cient of similarity

(CJ = j(a + b ± j) where j is the number of species common to

both samples and a and b are, respectively, the total numbers

of species in each sample. These coef®cients give equal weight

to all species, irrespective of their relative abundance

Marsella

Montenegro

PensilvaniaAguadas

Salamina

Filadelfia

Gramalote

Bochalema

Labateca

Toledo

Norte de Santander

Caldas

Quindio

Risaralda

N

50 km

scale

Fig. 1. Outline maps showing locations of 10 municipalities with study sites in four administrative Departments (names in italics) of Colombia:

Caldas, Norte de Santander, Quindio and Risaralda. Central map (103 reduced scale) shows areas and positions of these four Departments in

Colombia.


366 B. Alexander et al.366 B. Alexander et al.

(Southwood, 1978). A value of 1.00 indicates that the

species compositions of two plantations are identical, and 0

means that they are completely dissimilar. The values obtained

were then analysed using the NTSys program (J. NTSys ± PC),

numerical taxonomy and multivariate analysis system, version

2.02i, Exeter Software, NY) and a dendrogram constructed

based on unweighted pair-group method analysis (UPGMA)

(Fig. 2).

Geometric means were calculated of the total numbers of

sand¯ies collected in each plantation type. The results were

analysed by paired t-test after log transformation of the totals

(n + 1) to compare the densities of different Lutzomyia species

in each plantation type and municipality.

Awareness of sand¯ies

Fifty-six residents of coffee plantations (25 male, 31 female)

aged between 7 and 67 (median age 37) were asked whether

biting insects ever bothered them and, if so, asked to describe

them. Inclusion of one or more of the following seven

characteristics in each response was noted:

d Small (2±3 mm);

d Whitish (¯uorescent at night);

d Wings at rest held in a `V' shape;

d Silent;

d Weak but direct ¯ight (do not hover),

hop between biting sites;

d Nocturnal;

d Painful bite.

Taken together, these characteristics describe no other type

of biting ¯y than phlebotomine sand¯ies and indicate the

ability of local people to distinguish these insects from other

Diptera such as mosquitoes and simuliids.

Results

Comparison of sand¯y faunae of traditional and intensi®ed

plantations

Entomological data are summarized in Tables 1 and 2. A

total of 20 species of sand¯y was collected during the study, of

which eight were found only in the Eje Cafetero, six were

exclusive to Norte de Santander and six occurred in both

regions. Five species, i.e. Lu. cayennensis (Floch &

Abonnenc), Lu. shannoni (Dyar), Lu. trapidoi (Fairchild &

Hertig), Lu. yuilli Young & Porter and an unidenti®ed Lu.

(Helcocyrtomyia), were collected only in traditional planta-

tions, compared with two, i.e. Lu. bifoliata (Osorno-Mesa

et al.) and Lu. sordellii (Shannon & Del Ponte), exclusively in

intensi®ed ones. At least 13 species occurred in both plantation

types. With regard to the transmission of Leishmania, 15

species were opportunistic man-biters and eight are suspected

vectors of: Le. braziliensis, i.e. Lu. spinicrassa (Morales et al.),

Lu. nunÄeztovari (Ortiz), Lu. ovallesi (Ortiz) and Lu. youngi

Feliciangeli & Murillo; Le. panamensis, i.e. Lu. hartmanni

(Fairchild & Hertig), Lu. trapidoi and Lu. gomezi (Nitzulescu);

or Le. mexicana i.e. Lu. columbiana (Ristorcelli & Van Ty)

(Young & Duncan, 1994). Seven species, including six

opportunistic man-biters, were collected on sticky traps inside

houses and could be involved in intradomiciliary transmission

of Leishmania. Shade trees are used as resting sites by at least

10 species, and three were taken among leaf litter.

A total of 12 species were collected in Norte de Santander.

The dominant species was clearly Lu. spinicrassa, which made

up 93.8% of all the sand¯ies collected in the four municipal-

ities of this department. It was the only sand¯y found in all

four municipalities, other important species being Lu.

nunÄeztovari, Lu. serrana (Damasceno & Arouck) and Lu.

Arma Trad.

Arma Int.

Filadelfia Trad.

Marsella Trad.

Marsella Int.

Filadelfia Int.

Salamina Trad.

Salamina Int.

Bochalema Trad.

Gramalote Trad.

Gramalote Int.

Labateca Trad.

Labateca Int.Toledo Trad.Toledo Int. Pensilvania Trad.

Pensilvania Int.

0.02 0.26 0.51 0.75 1.00

Fig. 2. Dendrogram based on unweighted pair group method analysis (UPGMA)and Jaccard's index Cj = j(a + b ± j) showing the degrees of

similarity with respect to the sand¯y fauna among plantations under the traditional (trad) and intensi®ed (int) systems in nine municipalities:

Arma (Aguadas), Bochalema, Filadel®a, Gramalote, Labateca, Marsella, Pensilvania, Salamina and Toledo. One other municipality (Montenegro)

was not included in this analysis because only a single specimen was collected there.



ovallesi, all of which occurred in at least two. The greatest

diversity was seen in Gramalote (11 species), considerably

more than the number collected in Bochalema (four), Toledo

(three) and Labateca (one). All but two species (Lu.

cayennensis and Lu. shannoni) were collected in both types

of plantation and none were exclusive to intensi®ed planta-

tions. Nine of the 12 species are opportunistic man-biters, and

®ve (including Lu. walkeri (Newstead) and the non-anthro-

pophilic Lu. ferroae Young & Morales) were collected on

sticky traps inside houses. With respect to diurnal resting sites,

eight were collected on tree trunks and one (Lu. spinicrassa)

taken among leaf litter in both types of plantation. Collections

of Lu. erwindonaldoi (Ortiz), the remaining man-biting

species, were restricted to Shannon traps in both types of

plantation.

The man-biting species Lu. spinicrassa was absent from the

Eje Cafetero and a number of others among the 15 recorded

might be responsible for Leishmania transmission in this

region, including Lu. trapidoi, Lu. yuilli, Lu. gomezi, Lu.

hartmanni and Lu. ovallesi. Seven species were collected in

both types of plantation, ®ve were exclusive to traditional

plantations and three were only collected in intensi®ed ones.

None of the species was collected in all six municipalities,

although Lu. lichyi (Floch & Abonnenc) occurred in at least

four and Lu. columbiana, Lu. youngi and Lu. pia (Fairchild &

Hertig) in at least three. The numbers of species collected in

each municipality were seven (Filadel®a), six (Arma/

Aguadas), four (Pensilvania and Salamina), three (Marsella)

and one (Lu. lichyi) in Montenegro. All 11 species collected in

traditional plantations were opportunistic man-biters, although

none were taken inside houses on sticky traps. At least four

(Lu. columbiana, Lu. lichyi, Lu. pia and Lu. shannoni) were

found resting during the day on shade trees, with Lu. lichyi also

being collected among leaf litter. With respect to intensi®ed

plantations, eight of the 10 species were collected were man-

biters, the exceptions being Lu. bifoliata and Lu. sordellii.

Table 1. Summary of entomological data for collections made in six municipalities of the Eje Cafetero (Departments of Caldas, Risaralda and

Quindio), Colombia

Lutzomyia sp. Municipality

Collection type

Diurnal resting sites Intradomiciliary Nocturnal

Trees Leaf litter Sticky traps Shannon trap Totals

TR TR IN TR IN TR IN TR IN

L. bifoliata Arma/Aguadas 0 0 0 0 0 0 2 0 2

L. columbiana Pensilvania 0 0 0 0 0 11 0 1 0

Marsella 6 0 0 0 0 0 1 6 1

Filadel®a 2 0 0 0 0 0 0 2 0

L. gomezi Filadel®a 0 0 4 0 2 0 8 0 14

L. hartmanni Pensilvania 0 0 0 0 0 22 1 22 1

Filadel®a 0 0 0 0 1 0 0 0 1

L. (Helcocyrtomyia) sp. Aguadas 0 0 0 0 0 1 0 1 0

L. lichyi Montenegro 1 0 0 0 0 0 0 1 0

Marsella 21 0 0 0 0 0 0 21 0

Filadel®a 10 1 0 0 0 1 0 12 0

Salamina 2 0 0 0 0 0 0 2 0

L. nunÄeztovari Salamina 0 0 0 0 0 8 3 8 3

L. ovallesi Aguadas 0 0 0 0 0 1 4 1 4

L. pia Marsella 82 0 0 0 0 24 22 106 22

Filadel®a 5 0 0 0 0 116 0 121 0

Salamina 15 0 0 0 1 102 31 117 32

L. shannoni Filadel®a 3 0 0 0 0 0 0 3 0

L. sordellii Aguadas 0 0 0 0 0 0 1 1 0

L. trapidoi Pensilvania 0 0 0 0 0 5 0 5 0

L. youngi Aguadas 0 0 0 0 0 50 7 50 7

Filadel®a 0 0 0 0 0 0 3 0 3

Salamina 0 0 0 0 0 51 18 51 18

L. yuilli Pensilvania 0 0 0 0 0 24 0 24 0

Totals 555 108

Geometric mean 6.12 1.50

TR ± traditional; IN ± intensi®ed **Statistically signi®cant at P <0.01

Paired t-test t = ± 3.15, d.f. = 23; P = 0.004**



Only one species (Lu. gomezi) was collected among leaf litter

during the day. This species was taken inside houses on sticky

traps, as were Lu. hartmanni and Lu. pia.

The only medically important species not found in both

types of coffee plantation were Lu. trapidoi and Lu. yuilli, both

highly anthropophilic species of the subgenus Lutzomyia

(Nyssomyia). Both species were only recorded in Pensilvania

and assuming that they truly are absent from intensi®ed

plantations, the most likely candidates as Leishmania vectors

in the latter habitat are Lu. hartmanni and Lu. columbiana,

both of which readily bite man.

The fact that collections were made over short periods

means that several species may not have been collected from

each municipality. However, members of the Lu. verrucarum

species group, such as Lu. columbiana, Lu. nunÄeztovari, Lu.

ovallesi, Lu. serrana, Lu. youngi and Lu. spinicrassa, are

clearly well adapted to coffee plantations of both types,

particularly in Norte de Santander. Although some species are

found in both regions, the vectors and parasites involved in

Leishmania transmission in the Eje Cafetero and Norte de

Santander are likely to be different. In order to determine

whether differences between the faunae of traditional and

intensi®ed plantations were consistent, comparisons were

made between all plantations surveyed, using Jaccard's index

of similarity (Fig. 2) The greatest degree of similarity

(j = 1.00) was seen between traditional and intensi®ed plan-

tations in Toledo and Labateca, in which the species recorded

were identical in both types of cultivation system. However,

this is undoubtedly a re¯ection of incomplete sampling, only

two species (both anthropophilic) having been collected.

Collections from the two types of plantation were, however,

also very similar in Gramalote (j = 0.90) and Salamina

(j = 0.75). The former was the municipality in which most

species were collected and provides more conclusive evidence

of the ability of sand¯y species to adapt to intensi®ed

plantations. The greatest differences between traditional and

intensi®ed plantations of the same municipality were seen in

Filadel®a (j = 0.27) and Pensilvania (j = 0.25).

The two regions visited could be separated at a very low

level (j = 0.05) so that the higher prevalence of tegumentary

leishmaniasis seen in Norte de Santander (Alexander et al.,

unpublished data) could be a function of different behaviour

patterns of the vectors involved (including greater degree of

anthropophilicity or propensity to enter houses or greater

susceptibility to infection by Leishmania), as well as differ-

ences that in¯uence man±vector contact arising from human

activities (such as coffee-growing practices and construction

materials of houses).

Table 2. Summary of entomological data for collections made in four municipalities of Norte de Santander, Colombia

Lutzomyia sp. Municipality

Collection type

Diurnal resting sites Intradomiciliary Nocturnal

Trees Leaf litter Sticky traps Shannon trap Totals

TR TR IN TR IN TR IN TR IN

L. cayennensis Bochalema 4 0 ± 0 ± 0 ± 4 ±

L. erwindonaldoi Gramalote 0 0 0 0 0 5 3 5 3

L. ferroae Gramalote 0 0 0 0 1 1 1 1 2

L. gomezi Gramalote 0 0 0 1 0 0 2 1 2

L. lichyi Gramalote 10 0 0 0 0 11 11 21 11

L. nunÄeztovari Gramalote 0 0 0 0 0 89 14 89 14

Toledo 16 0 0 0 1 57 38 73 39

L. ovallesi Gramalote 0 0 0 0 0 2 1 2 1

Bochalema 41 0 ± 2 ± 0 ± 43 ±

L. pia Gramalote 0 0 0 0 0 6 1 6 1

L. serrana Gramalote 1 0 0 0 0 119 83 120 83

Toledo 0 0 0 0 0 36 8 36 8

L. shannoni Gramalote 0 0 0 0 0 9 0 9 0

Bochalema 41 0 ± 0 ± 0 ± 41 ±

L. spinicrassa Gramalote 0 1 6 28 1 4785 2427 4814 2433

Bochalema 94 0 ± 3 ± 2 ± 99 ±

Toledo 47 6 0 0 0 882 396 929 402

Labateca 0 0 0 74 19 196 396 270 415

L. walkeri Gramalote 1 0 0 0 1 4 2 5 3

Totals 6568 3417

Geometric mean 30.0 15.1

TR ± traditional; IN ± intensi®ed **Statistically signi®cant at P <0.01.

Paired t-test t = ± 3.23, d.f. = 14; P = 0.006**



A signi®cant difference was observed between the number

of specimens collected in each type of plantation. The density

of sand¯ies in traditional plantations was signi®cantly higher

than that in intensi®ed ones in both the Eje Cafetero and Norte

de Santander. Although the number of sampling nights in each

municipality was limited to four, collections were made

simultaneously in both types of plantations. The differences

in density were consistent for all the municipalities and for

most of the species of Lutzomyia (Tables 1 and 2).

Insecticide use

As insecticides sprayed on coffee to control H. hampei could

also affect sand¯y populations, a survey was made of their use

on 36 farms in the 10 municipalities visited. In all, 29 growers

reported the presence of H. hampei, which had arrived between

1989 and 1997. Only two of these farms were in Norte de

Santander, although the beetle was present on all plantations

visited in the remaining three departments. According to the

1997 coffee census, the beetle infested 50.53% of plantations

in Risaralda, 33.48% in Caldas, 21.22% in QuindõÂo and only

0.09% in Norte de Santander. Control methods used included

reÂ-reÂ alone (seven farms), Beauveria alone (three farms) and

use of one or more pesticides, with or without the above

methods, on 16 farms. The chemicals most frequently used

were the organophosphates Thiodanã (nine farms), Lorsbanã

(six farms), Sumithionã (two farms) and Actellicã (one farm).

ReÂ-reÂ was practised at weekly or twice-weekly intervals,

whereas frequency of Beauveria and chemical insecticide use

varied widely. Although endosulphan use is permitted to

control broca on coffee by Ministry of Health resolutions

00483±00486 (March 29, 1999) and 01669 (May 25, 1999),

chemical insecticide application is discouraged by

FEDERACAFE for reasons of safety, contamination of the

crop and the fact that they are only ineffective against insects

on the surface or foliage rather than within the fruit.

Nevertheless, their use continues to be practised in an arbitrary

and uncontrolled manner.

Phlebotomine sand¯ies of seven species (Lu. columbiana,

Lu. hartmanni, Lu. lichyi, Lu. ovallesi, Lu. pia, Lu. shannoni

and Lu. youngi), were collected on 13 of the plantations where

insecticide use had been practised, including two treated with

Lorsbanã and Thiodanã shortly before sampling. Sand¯ies

belonging to ®ve species (Lu. columbiana, Lu. gomezi, Lu.

lichyi, Lu. pia and Lu. youngi) were also collected on ®ve of

the plantations treated with Beauveria.

Awareness of sand¯ies

Results of this survey are shown in Table 3. Five of the

people interviewed were able to cite six of the seven

characteristics, 20 were able to give at least ®ve characteristics

Table 3. Characteristics of sand¯ies recognized by residents of coffee plantations

Municipality Type n

% of respondents able to cite characteristic

Mean no.

recognized

Common

name(s)Small Nocturnal Whitish

Painful

bite Silent

V-shaped

wings

Direct

¯ight

Arma TR 5 100 100 40.0 100 60.0 50.0 0 3.83 Palomilla

IN 4 80.0 100 50.0 100 100 0 0 4.00 Pito/

Palomilla

Filadel®a TR 2 50.0 50.0 83.3 50.0 50.0 50.0 0 3.00 Palomilla

IN 2 100 100 33.3 100 100 0 0 5.00 Paloma

Pensilvania TR 6 83.3 83.3 50.0 33.3 83.3 0 66.7 5.20 Palomilla

IN 3 33.3 33.3 75.0 0 33.3 0 0 1.33 Palomilla

Salamina TR 2 100 0 50 100 0 50.0 0 3.00 Palomilla

IN 4 75.0 25.0 100 25.0 0 0 0 2.00 Paloma

Marsella TR 2 100 100 100 50.0 100 50.0 50.0 5.50 Palomilla

IN 1 100 100 100 100 100 0 0 5.00 Palomilla

Montenegro TR 2 0 0 0 0 0 0 0 0 ±

IN 2 50.0 50.0 50.0 50.0 50.0 0 0 2.50 ±

Bochalema TR 4 75.0 75.0 75.0 100 0 50.0 25.0 4.00 Chire/Quemador

Gramalote TR 3 100 100 100 66.7 66.7 33.3 0 4.6 Quemador/Aliblanco

IN 2 50.0 50.0 0 50.0 50.0 0 50.0 2.50 Quemador/Pito

Labateca TR 5 100 100 80.0 0 0 50.0 0 3.20 Chire

IN 2 100 50.0 0 0 100 0 0 2.50 Chire

Toledo TR 3 66.7 50.0 0 100 0 100 66.7 3.67 Chire

IN 2 50.0 100 50.0 50.0 0 50.0 0 3.00 Chire

Overall TR 34 79.4 73.5 61.8 61.8 41.1 38.2 23.5 4.00 ±

IN 22 68.2 63.7 45.4 13.6 31.8 4.5 4.5 2.67 ±

Both 56 75.0 69.7 55.3 42.8 37.5 25.0 16.1 3.43 ±

t-test comparing means of traditional and intensi®ed plantations, t = 3.47, P = 0.004**

**Statistically signi®cant at P <0.01.



and 28 persons at least four. Seven of the people questioned

had no knowledge of the insects and three gave only one of the

characteristics. The four most frequently cited characteristics

were that the insects were small (75.0% of respondents),

nocturnal (69.6%), whitish in colour (57.1%) and gave a

painful bite (55.3%). Twenty-®ve people (44.6%) described

the insects as silent and 16 people (25.0%) mentioned the habit

of holding the wings at rest in an erect `V' shape. The least

frequently cited characteristic was that of the direct (non-

hovering) ¯ight, mentioned by only nine respondents. The

common names given for the sand¯y differed between the two

different regions. In Norte de Santander the insect is known as

`quemador' in Gramalote and `chire' in Bochalema, Labateca

and Toledo. The latter term presumably refers to the insect's

small size, perhaps a corruption of the word `chiriquitico'

(tiny). One person in Bochalema cited both these names, others

used less frequently being `aliblanco' (white wing) and `pito'

(the latter term, meaning `bug' is also used to refer to

leishmaniasis). The name `pito' was also given by two people

in Caldas (both in Aguadas), although `palomilla' or `paloma'

were cited by all respondents from the Eje Cafetero (including

the two mentioned) able to identify the insects. The mean

number of characteristics cited by residents of traditional

plantations was 4.00, signi®cantly greater than that given by

people living on intensi®ed ones (2.59) (t = 3.47; P = 0.004),

suggesting that awareness of the insects is greater in the

former, presumably due to greater biting activity.

Discussion

Coffee plantations, particularly those still under the traditional

system of cultivation, represent the only signi®cant forest

cover in many areas of Colombia. Traditional plantations

harbour a greater diversity of plants, insects, spiders, reptiles,

mammals and birds (Perfecto et al., 1996) and also provide

important refuges for bird species migrating from North

America (Tangley, 1996; Greenberg et al., 1997). Many

species of phlebotomine sand¯y have adapted to living within

their con®nes. Alexander et al. (1992) recorded 17 species

within one small (2 ha) traditional coffee plantation in

Arboledas, Norte de Santander, of which 15 belonged to the

genus Lutzomyia, including ®ve members of the medically

important Lu.verrucarum species group. Eleven of these

species (64.6%) were opportunistic man-biters (Alexander

et al., 1992) and natural infections with Le. (V.) braziliensis

were found in Lu. spinicrassa (Young et al., 1987). At least

two other species (Lu. ovallesi and Lu. gomezi) are suspected

vectors of Leishmania in other parts of their ranges (Killick-

Kendrick, 1990; Young & Duncan, 1994).

Colombia is the world's second biggest coffee producer, the

558 000 tons harvested in 1998 (10.1% of the world total)

being exceeded only by Brazil and far greater than the

production of any other country. Coffee provides 37% of

Colombia's agricultural employment, involving 3.3 million

people on 566 000 farms in 590 municipalities (Anon, 1999).

Although the importance of coffee to the Colombian economy

has steadily fallen from 84% of exports in 1954 to only 12% in

1998, as a legitimate source of export earnings it is still

exceeded only by petroleum. The population at risk of

acquiring tegumentary leishmaniasis is therefore considerable

and although treatment is provided free of charge to patients

this is a strain on the economic resources of the health

authorities. In addition, chemotherapy is not always available

and many patients seek a variety of alternative remedies, most

of which have no effect and may allow mucocutaneous lesions

to develop at a later date (WHO, 1990).

Many cases could be prevented by better understanding the

transmission cycle of leishmaniasis in coffee plantations and

providing susceptible individuals with information on how to

avoid being bitten by sand¯ies. Intradomiciliary transmission

of Leishmania is probably the most important type of contact

between man and vector in coffee plantations. Extradomi-

ciliary and peridomiciliary transmission of Leishmania is

likely to be less important for three reasons: (a) the disease

occurs in both sexes and all age groups, including very young

children, (b) coffee plantations do not support large game

animals suitable for hunting at night, (c) although sand¯ies

may bite during the day this is relatively rare, and (d) the cool

nocturnal temperatures of the Colombian Andes tend to force

people indoors after dark (Alexander et al., 1995).

Insecticidal treatment of sand¯y resting and breeding sites in

coffee plantations would be costly, impractical and unaccept-

able because of the risk of tainting the crop. Residual spraying

of human habitations would be also be logistically impractical,

because farms are widely dispersed over mountainous terrain

and often inaccessible by road. Impregnated mosquito nets

may offer the most practical solution, provided that the

insecticidal formulations involved were available in quantities

that could be used by families rather than at the community

level, at low cost and with minimal risk of accidental

intoxication through lack of supervision. The ef®cacy of

bednets impregnated with the synthetic pyrethroid deltame-

thrin in reducing sand¯y biting rate was demonstrated in a

coffee-growing community of Valle del Cauca, Colombia by

Alexander et al. (1995), although whether or not impregnated

bednet use could also reduce the incidence of Leishmania

infection remains to be demonstrated. Impregnated bednets are

unlikely to have a signi®cant effect on sand¯y populations in

the plantations themselves, as the insects entering houses to

bite probably represent a relatively small fraction of the total

number. This has been demonstrated for Anopheles mosquitoes

in areas of Africa where bednets are used for malaria control

(QuinÄones et al., 1998).

The degree of protection from the sun provided by certain

trees could modulate sand¯y biting activity. With respect to

resting sites/lekking sites, the most suitable species are those

with rough bark and/or buttress roots such as Albizzia

carbonaria, Anacardium rhinocarpus, Cordia alliodora,

Erythrina edulis and Ficus glabrata. Several of these species

lose all their leaves during the dry season, increasing the

covering of leaf litter on the plantation ¯oor and impeding the

growth of other species (Acero Duarte, 1985). Slender, quick-

growing and smooth-trunked trees such as Inga spp. are less

favourable as resting sites (Alexander et al., 1992), although



they are widely grown and often predominate in Colombian

plantations.

Thus, although the intensi®cation of coffee plantations

might be expected to affect Leishmania transmission by

creating less favourable conditions for vectors and reservoirs

as well as reducing man-vector contact, several sand¯y species

have adapted to the new conditions and the disease still occurs

(Alexander et al., unpublished data). This and the environ-

mental problems associated with removing shade trees may be

used to argue against the continued intensi®cation of

Colombian plantations, despite the increased productivity of

the new system. The production of `ecological coffee' has been

suggested as a solution to this dilemma, biodiversity and soil

quality being as important in rating plantations as non-use of

insecticides (Perfecto et al., 1996). Several groups of insects

have been proposed as indicators of biodiversity and habitat

quality, including ants, butter¯ies (Osborn et al., 1999) and

mosquitoes (DorvilleÂ, 1996). Phlebotomine sand¯ies are

themselves particularly suitable as indicators, being a well-

studied group of medical importance whose members are easy

to transport and identify. They are directly dependent on the

vertebrate fauna of the areas they inhabit and harbour parasites

that are themselves of phylogenetic interest (Barrett et al.,

1996). They also have a relatively long life cycle (4±6 weeks),

which precludes them from colonizing ephemeral micro-

habitats, and have a limited ¯ight capacity. As such, they can

be considered true residents of a particular habitat rather than

transient opportunists (Alexander, 1999).

Acknowledgements

The logistic support provided by the following people is

gratefully acknowledged: Idelfonso Cepeda of the MinisteÂrio

de Salud, Fiorentino CeÂlis and Hector Anaya of the Servicio

Seccional de Salud de Norte de Santander, Humberto Bedoya

and Julian Montoya of the Servicio Seccional de Salud de

Caldas, Pablo Ruiz and Alba Nidia Salazar of the Servicio

Seccional de Salud de Risaralda, Cesar Augusto Pineda

CastanÄo of the ComiteÂ Departamental de Cafeteros de

Marsella and Ivan Dario Velez of the University of

Antioquia. The study was funded by a grant no. 9403334 of

the WHO/TDR.

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Accepted 25 June 2001



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