The Triatominae species of French Guiana (Heteroptera: Reduviidae)

Abstract

An annotated list of the triatomine species present in French Guiana is given. It is based on field collections carried out between 1993-2008, museum collections and a literature review. Fourteen species, representing four tribes and six genera, are now known in this country and are illustrated (habitus). Three species are recorded from French Guiana for the first time: Cavernicola pilosa, Microtriatoma trinidadensis and Rhodnius paraensis. The two most common and widely distributed species are Panstrongylus geniculatus and Rhodnius pictipes. The presence of two species (Panstrongylus megistus and Triatoma maculata) could be fortuitous and requires confirmation. Also, the presence of Rhodnius prolixus is doubtful; while it was previously recorded in French Guiana, it was probably mistaken for R. robustus. A key for French Guiana's triatomine species is provided.

Full text

Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(8): 1111-1116, December 2009 1111
online | memorias.ioc.fiocruz.br
The triatominae species of French Guiana (Heteroptera: Reduviidae)
Jean-Michel Bérenger1, 2/+, Dominique Pluot-Sigwalt1, Frédéric Pagès2,
Denis Blanchet3, Christine Aznar3
1Muséum National d’Histoire Naturelle, Département Systématique & Evolution (Entomologie), 45 rue Buffon, 75005 Paris, France
2Institut de Médecine Tropicale du Service de Santé des Armées, Allée du Médecin Colonel Jamot, Marseille, France 3Laboratoire Hospitalier
Universitaire de Parasitologie et Mycologie, UFR de Médecine, Université des Antilles et de la Guyane, Cayenne, Guyane Française
An annotated list of the triatomine species present in French Guiana is given. It is based on field collections
carried out between 1993-2008, museum collections and a literature review. Fourteen species, representing four
tribes and six genera, are now known in this country and are illustrated (habitus). Three species are recorded from
French Guiana for the first time: Cavernicola pilosa, Microtriatoma trinidadensis and Rhodnius paraensis. The two
most common and widely distributed species are Panstrongylus geniculatus and Rhodnius pictipes. The presence of
two species (Panstrongylus megistus and Triatoma maculata) could be fortuitous and requires confirmation. Also,
the presence of Rhodnius prolixus is doubtful; while it was previously recorded in French Guiana, it was probably
mistaken for R. robustus. A key for French Guiana’s triatomine species is provided.
Key words: Heteroptera - Reduviidae - Triatominae - French Guiana
Financial support: CPER/DocUP 2000-2006 (2364, Convention
421), Bioécologie et taux d’infestation des triatomes en Guyane,
agents vecteurs de la maladie de Chagas
+ Corresponding author: jmberenger@free.fr
Received 17 June 2009
Accepted 7 October 2009
Within the large family of Reduviidae, comprising
more than 6,000 known species (Maldonado Capriles
1990), one subfamily, the hematophagous Triatominae
is of great importance for human health because many
of them are vectors of the Trypanosoma cruzi parasite
responsible for Chagas disease. This fact explains why
more than 80% of scientific publications about reduvids
concern only triatomines, which comprise no more than
140 valid species (Costa & Lorenzo 2009, Schofield &
Galvão 2009). The group is mainly diversified in the
New World and roughly 20 species have been recorded
in the Amazonian Region (Lent & Wygodzinsky 1979,
Barret & Arias 1985, Serra et al. 1987, Lent et al. 1995,
Coura et al. 2002, Costa & Lorenzo 2009).
However, relatively few investigations have been con-
ducted regarding the triatomine fauna of French Guiana.
The first lists given by Floch and Abonnenc (1941, 1943)
reported five species in 1941 and six in 1943. In their revi-
sion, Lent and Wygodzinsky (1979) mentioned six spe-
cies in French Guiana, chiefly based on a Floch’s publica-
tion (1947). In 1983, Chippaux et al. listed eight species
belonging to four genera, but this data was omitted by
Ryckman (1986), who noted only six species from French
Guiana. In 2003, Galvão et al. mentioned seven species.
Finally, considering a larger area called “humid Guyana”
(comprising French Guiana, Guyana and Surinam), Abad-
Franch and Monteiro (2007) compiled a list of 14 species,
including four species considered as “possibly present”.
Thus, during the last few decades, no precise investi-
gation has been conducted of the French Guiana’s triatom-
ine fauna [apart from the studies of Chippaux (1984) and
Chippaux et al. (1985), which provide interesting data]
and the group remains to be thoroughly investigated.
After a first assessment on this subject (Aznar et al.
2000), we summarise here the results of many searches,
mainly from field sampling, carried out between 1993-
2008. Concerning the medical aspect of these species,
studies devoted to their infection by T. cruzi in French
Guiana have been led by Aznar (since 1997) using mo-
lecular biology. Relevant recent data from these investi-
gations will be published separately (D Blanchet et al.,
unpublished observations).
MATERIALS AND METHODS
From 1993-2008, we have undertaken regular col-
lections of reduvid specimens in French Guiana, main-
ly during 10 or so field trips to the country and also
through permanent collaborations with several resident
colleagues and friends. Each collecting stay lasted from
2-4 weeks, usually during the dry season, except for two
stays made during the rainy season. The aim for one of
us (JMB) was to compile a faunistic list of the reduvid
fauna in this country, a plan that is still in progress. The
triatomine fauna has been studied specifically. Several
museum collections, in particular those of the Muséum
National d’Histoire Naturelle (MNHN, Paris) and the
Institut Pasteur (Paris), were also examined. In addition,
two recent prospecting trips (2007, 2008) made around
three military bases provided complementary data; these
trips were particularly devoted to the triatomine and to
the study of Chagas disease in French Guiana.
Insects were mainly caught using a light source;
roughly 100 light trap sessions were conducted. During
the two last prospecting trips, 15 light trap sessions were
carried out from 7 pm to midnight and for each triatom-
ine specimen, the time of the catch was noted. The light

Triatominae of French Guiana • Jean-Michel Bérenger et al.
1112
trap was composed of a white sheet vertically stretched
and lit on each side by two 125-W ballast bulbs, with or
without a calling light and a white sheet on the ground.
On some occasions, a vertical sheet was extended on
each side, using a 5 m longer sheet to create a brightness
gradient. Bugs were also actively searched for at night by
sight, mainly around public or residential lighting. In to-
tal, several hundred triatomine specimens were captured
and examined between 1993-2008. Identified triatomine
specimens were deposited in the first author’s collection
(JMB), in the MNHN collection and in the collection of
the Faculty of Medicine in Cayenne.
The prospecting sites (Fig. 16) included (i) a large
area along the coast (Kaw, Patawa, Regina, Cacao, Cay-
enne and the area around, Sinnamary, Kourou, Iracou-
bo, Mana), (ii) various places along several rivers (the
Maroni River: St-Laurent, St-Jean, Grand-Santi, Mari-
pasoula and the Oyapock River: St-Georges, Camopi),
(iii) the vicinity of Saül, located in the centre of French
Guiana and in some places not easily accessible (Mi-
taraka Mountains) with the assistance of entomological
associations (Alabama, Guyanentomo, Société Ento-
mologique Antilles-Guyane) and (iv) around military
bases (the centre for entertainment in the tropical for-
est, CEFE Régina, GSMA of St-Jean du Maroni and the
Spatial Base of Kourou).
Sampling was performed in different environments:
domestic and peridomestic, urban, rural and sylvan.
Over the last 30 years, French Guiana’s population has
increased from 70,000 to 200,000 people (illegal work-
ers not included) [Institut National de la Statistique et
des Etudes Economique - INSEE 2009 (www.insee.fr/
guyane)]. This large increase induced the quick devel-
opment of human dwellings, residential areas and un-
planned urbanisation near forests or incorporating forest
islands. This particular environment is referred to below
as the “urban forest island.”
The climate of French Guiana is equatorial, warm
and humid, with little change in temperature during the
year. The average annual temperature is 27°C and the
annual precipitation measures more than 2.500 mm.
RE SULTS
Attracting only adult specimens, light traps cannot
divulge any information on the biology of the collected
triatomine species. However, this method does give in-
formation on the period of activity of the species. Our
experience during several years shows that after mid-
night, the total catch of triatomine specimens is scarce
(this is the same for all reduvids species). A maximum of
individuals was collected between 9-11 pm.
During our investigation, 14 triatomine species were
recorded in French Guiana (Table). Among these, the
presence of 11 species has been confirmed; three other
species require confirmation, not having been collected
by us. Two additional species, at first considered as pos-
sibly present, were subsequently dismissed.
Confirmed species - From the 11 species collected
by us, six were historically known to be present in
French Guiana (i.e., prior to our 1993 investigation):
Panstrongylus geniculatus (L atreill e), Panstrongylus
rufotuberculatus (Champion), Panstrongylus lignarius
(Walker), Rh odnius pictipe s Stål, Rhodnius robustus La r-
rousse and Eratyrus mucronatus Stål. Five species were
not previously known in this country (see catch localities
in Fig. 16): Cavernicola pilosa Barber, Microtriatoma
trinidadensis (Lent) and Rhodnius paraensis Sherlock
et al. were not recorded previously in French Guiana.
Rhodnius amazonicus Almeida et al. was recently re-
stored as a valid species (Bérenger & Pluot-Sigwalt 2002).
Panstrongylus mitarakaensis Bérenger and Blanchet is a
newly described species (Bérenger & Blanchet 2007).
Of these 11 species, only two appear to be very com-
mon in French Guiana, P. geniculatus and R. pictipes,
which are widely distributed in the Amazonian Region.
Species requiring confirmation - The presence of four
triatomine species not collected by us during our inves-
tigation requires confirmation. These species seem very
rare, accidental, or possibly now missing in the country.
Triatoma maculata (Erichson) and Triatoma rubrofasciata
(De Geer) are cited in the literature from French Guiana.
The presence of the former is probable because this spe-
cies occurs in Surinam; we found four specimens of the
latter in museum collections, but the species could have
disappeared from French Guiana. Panstrongylus megis-
tus (Burmeister) has been found, only as poorly labelled
specimens, preserved in museum collections.
Potential species - It is very likely that species oth-
er than those listed in the present paper are present in
French Guiana, particularly six species described in Bra-
zil [Pará (PA), principally]: Cavernicola lenti Barret and
TABLE
List of the triatomine species recorded from French
Guiana - literature data and present investigations (1993-2008)
Literature data Present study 1993-2008
- Microtriatoma trinidadensis
- Cavernicola pilosa
-Rhodnius amazonicus
-Rhodnius paraensis
Rhodnius pictipes Rhodnius pictipes
Rhodnius prolixusa -
Rhodnius robustus Rhodnius robustus
Eratyrus mucronatus Eratyrus mucronatus
Panstrongylus geniculatus Panstrongylus geniculatus
Panstrongylus lignarius Panstrongylus lignarius
-Panstrongulus mitarakaensis
-Panstrongylus megistusc
Panstrongylus rufotuberculatus Panstrongylus rufotuberculatus
Triatoma maculatab -
Triatoma rubrofasciata Triatoma rubrofasciatac
a: probable misidentification; b: need confirmation; c: from
museum specimens.

1113
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(8), December 2009
Arias, Rhodnius brethesi Matta, Belminus herreri Lent
and Wygodzinsky, Belminus laportei Lent et al., Psam-
molestes tertius Lent and Jurberg and Alberprosenia
malheiroi Serra et al.
Excluded species - The presence of Rhodnius prolixus
is likely a mistake. Although cited from French Guiana
by Floch and Abonnenc (1941), Lent and Wygodzinsky
(1979), Chippaux et al. (1985), Maldonado Capriles (1990),
Carcavallo et al. (1999) and Galvão et al. (2003), we have
excluded R. prolixus from our list. Several facts lead us to
think that the species does not occur in French Guiana.
Misidentification is strongly suspected. R. prolixus
and R. robustus are extremely similar and difficult
to separate morphologically (Miles et al. 1981, Harry
1993a, b). R. prolixus is cited from French Guiana by
Floch and Abonnenc (1941) based on a single female
collected on the Comté River. In order to identify the
specimen, Floch used the works of Larrousse (1927) and
Neiva and Lent (1941), which did not allow for a rig-
orous distinction between R. prolixus and R. robustus.
Later, Chippaux et al. (1985) again listed R. prolixus
in French Guiana, despite Miles’ opinion (Miles et al.
1983); Miles had doubts as to the presence of the species
in French Guiana and he assigned the specimens iden-
tified by Chippaux to R. robustus [Miles in litt. cited
by Chippaux et al. (1985)]. Unfortunately, we could not
find and examine the specimens in question.
Other data seem to exclude R. prolixus from French
Guiana. Recent studies in molecular biology and phy-
logeography (Monteiro et al. 2003, Pavan & Monteiro
2007) show that the Guyana Shield is located out of the
distribution area of R. prolixus. According to these stud-
ies, the species is present north of the Amazonian Basin,
in Central America and in the non-Amazonian zone of
Colombia and Venezuela. Records of R. p rol ixus in Brazil
may be due to confusion with R. robustus and Rhodnius
neglectus Lent, 1954 (Gurgel-Gonçalves et al. 2008).
The case of Triatoma brasiliensis Neiva, 1911 is also
in dispute. We have found only a single male specimen in
the MNHN collection (Fig. 14), simply labelled “Guyane
française”. Considering that the geographical distribu-
tion of T. brasiliensis is restricted to the semiarid areas of
North-eastern Brazil (Lent & Wygodzinsky 1979, Cos-
ta et al. 2003) we consider the species as not present in
French Guiana until further information is available.
Annotated list of French Guiana’s triatomines
Bolboderini Usinger, 1944
M. trinidadensis (Lent, 1951)
(Fig. 7)
One specimen of this arboreal species was captured
in the primary forest area. It was found on the extension
of the sheet of the light trap (brightness gradient).
Distribution - Montagne des Singes (near Kourou).
Cavernicolini Usinger, 1944
C. pilosa Barber, 1937
(Fig. 6)
Three specimens have been collected, each time in
forested areas. The bug does not stay on the sheet of the
light trap; it escapes very quickly requires vigilance to
catch it. This fleetness could explain why the species is
so rare in the museum collections.
Distribution - Piste changement (near Kourou), mon-
tagne de Kaw (PK 37).
Rhodniini Pinto, 1926
R. amazonicus Almeida, Santos & Sposina, 1973
(Fig. 11)
We have collected and studied five specimens, which
allowed the rehabilitation of R. amazonicus as a valid
species (Bérenger & Pluot-Sigwalt 2002). It is a sylvatic
species, captured by light and apparently very rare.
Distribution – Saül, degrad Kwata (near Cacao), Bé-
lizon, Tibourou.
R. paraensis Sherlock, Guitton & Miles, 1977
(Fig. 9)
Three specimens were collected by light trap, each
time on the sheet on the ground.
Distribution - Degrad Kwata (near Cacao), CEFE
(Regina), Bélizon.
R. pictipes Stål, 1872
(Fig. 10)
It is the most common triatomine species in French
Guiana, after P. geniculatus. It is often captured by
light in forest areas, but we also found it near human
dwellings in forested areas. More than 50 specimens
were collected.
R. robustus Larrousse, 1927
(Fig. 12)
This species is usually caught in urban areas and
urban forest island areas (Cayenne, Montjoly, Matoury,
Macouria (near Tonate); some specimens were also col-
lected around Grand-Santi village. We found it more
scarcely in forested areas (Kaw mountain). About 20
specimens were collected.
Triatomini Jeannel, 1919
E. mucronatus Stål, 1859
(Fig. 5)
This species is common in forest areas, present near
human dwellings in forest areas and rarely present in ur-
ban areas. About 40 specimens were collected.
Distribution - Kaw Mountain, Kaw village, Petit-
Saut dam, Saül, Grand-Santi, Kourou, Sinnamary, Nan-
cibo, Cacao, Roura. Villiers (1971) found it on the Oy-
apock River (Saut Maripa, Alicoto).
P. geniculatus (Latreille, 1811)
(Fig. 1)
Clearly the most common and the most widely distrib-
uted French Guiana’s triatomine species, it was found in all
parts of the country and in all environments (urban areas,

Triatominae of French Guiana • Jean-Michel Bérenger et al.
1114
urban forest island areas and sylvan areas). It was collected
mainly by light trap and according to Chippaux et al. (1983)
and our own experience, it represents 80% of the triatomine
species collected in sylvan areas and near human dwellings.
We have collected more than 100 specimens.
P. lignarius (Walker, 1873)
(Fig. 2)
This species is uncommon; about 20 specimens were
collected by light in sylvan areas and near urban forest
island areas.
Distribution - Cayenne (Mt Saint-Martin), Kaw, Be-
lizon, Saül, Kourou, Cacao, Bélizon, Petit Saut dam.
P. megistus (Burmeister, 1835)
(Fig. 13)
We never collected P. megistus. We found only one
male specimen labelled French Guiana (without further
indication) in the MNHN collection. We consider that
the species could be present in French Guiana, being
widely distributed in the Northeastern Brazil, in par-
ticular in PA (Lent & Wygodzinsky 1979, Galvão et al.
2003). Chippaux (1984) hypothesised that P. megistus
might have arrived in PA using merchandise transport
and he thought that the species may have arrived in
French Guiana in the same way.
P. mitarakaensis Bérenger & Blanchet, 2007
(Fig. 4)
A single specimen was collected in the Mitaraka
Mountains, South-West of French Guiana on the Brazil
frontier, an arid zone with granite outcrops (inselberg).
P. rufotuberculatus (Champion, 1899)
(Fig. 3)
This uncommon species was collected by light in for-
est areas. About 20 specimens were collected.
Distribution - Awala-Yalimapo (near Mana), Kaw,
Belizon, Saül, Cacao, Kourou.
T. maculata (Erichson, 1848)
(Fig. 15)
T. maculata was recorded in French Guiana and
borderlands by Carcavallo et al. (1999), Galvão et al.
(2003) and Jurberg and Galvão (2006). However, we
never collected it and cannot confirm its presence. If
present, it may be rare.
T. rubrofasciata (De Geer, 1773)
(Fig. 8)
We never collected any specimens of T. rubro-
fasciata. The species seems to have disappeared. A
possible reason could be a successful fight against ro-
dents that has eliminated both the bugs and its hosts.
If T. rubrofasciata is still present in Cayenne, it is cer-
tainly not abundant.
After the Second World War, the species seemed to
be relatively common in French Guiana. This can be de-
duced from the great number of specimens collected in
1945 (Floch & Abonnenc 1941, Floch & Lajudie 1945,
Floch 1947) in Cayenne and around human dwellings.
Although Chippaux et al. (1985) did not collect any
specimens of this species, they recorded T. rubrofasciata
with the notation - not very abundant -.
In the MNHN collection, we found a female speci-
men labelled “coll. Bar Oberthur, 1899, Guyane Fran-
çaise” and three more recent specimens labelled “1975,
trouvé dans habitations à Cayenne”.
Fig 1-12: triatomine habitus. 1: Panstrongylus geniculatus; 2: Pan-
strongylus lignarius; 3: Panstrongylus rufotuberculatus; 4: Pan-
strongylus mitarakaensis; 5: Eratyrus mucronatus; 6: Cavernicola
pilosa; 7: Microtriatoma trinidadensis; 8: Triatoma rubrofasciata; 9:
Rhodnius paraensis; 10: Rhodnius pictipes; 11: Rhodnius amazoni-
cus; 12: Rhodnius robustus (photos: JMB).
Fig 13-15: triatomine habitus. 13: Panstrongylus megistus; 14: Tria-
toma brasiliensis (Muséum National d’Histoire Naturelle collection);
15: Triatoma maculata (Venezuela, coll. JMB).

1115
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(8), December 2009
Key to the triatomine species from French Guiana
1. Genae conspicuously surpassing apex of clypeus .
................................................................M. trinidadensis
- Genae not surpassing apex of clypeus .................. 2
2. Head ovoid and convex in lateral view ....C. pilosa
- Head never ovoid or convex .................................. 3
3. Antennae inserted near the apex of the head. Pos-
tocular region with callus and setigerous tubercles ......4
- Antennae inserted far from the apex of the head.
Postocular region without lateral callus ........................ 7
4. Meso and metatibiae at least with a black median
annulus ........................................................................... 5
- Tibiae without black annulus .................R. robustus
5. Length < 12 mm; protibiae without black annuli ..
......................................................................R. paraensis
- Length > 15 mm; all tibiae annulate .....................6
6. Brown colour of femora and corium uniform .......
.................................................................. R. amazonicus
- Femora and corium brown with irregular yellowish
spots ................................................................R. pictipes
7. Humeral angle of pronotum and process of scutel-
lum spinose .............................................. E. mucronatus
- Humeral angle of pronotum and process of scutel-
lum without spine .......................................................... 8
8. Antennae insertion close to the eyes ................... 9
- Antennae insertion situated about the middle of
preocular region of head .............................................. 13
9. Femora light with a black median annulus ............
...............................................................P. mitarakaensis
- Femora without black annulus ............................. 10
10. Anterior lobe of pronotum with lateral and discal
tubercles reduced or erased; posterior margin of prono-
tum with a black strip ...............................P. geniculatus
- Anterior lobe of pronotum with lateral and dis-
cal tubercles prominent; posterior margin of pronotum
without black strip ........................................................11
11. Posterior lobe of pronotum yellowish with seven
black longitudinal strips ...............................P. lignarius
- Posterior lobe of pronotum blackish or reddish with
three black longitudinal strips ..................................... 12
12. Pronotum blackish with three yellowish spots on
posterior margin ...............................P. rufotuberculatus
- Pronotum black with four reddish spots more or
less spread ..................................................... P. megistus
13. Membrane of hemelytra blackish; vein of mem-
brane inconspicuous ..............................T. rubrofasciata
- Membrane of hemelytra light brown; vein of mem-
brane black and conspicuous ........................ T. maculata
ACKNOWLEDGEMENTS
To our colleagues and friends who kindly collected for us
triatomine specimens during their field collections: B Hermier,
J Cerda, O Morvan, I Curtet, M Thouvenot, JJ Briswalter,
JC Streito (LNPV Montpellier), R Rougerie, HP Aberlenc
(CIRAD), R Garrouste (MNHN), P Cerdan (Labo Hydreco),
P Causse, Y Hauray, D et L Rignon, H de Toulgoët, G Tavaki-
lian (IRD), JP Vesco, Alabama Association, JP Champenois
(Guyanentomo), PH Dalens (SEAG), to Dr Delesquen, chief of
the French Army Health Service in French Guiana, to Sandy
Jones, for her comments, and to the anonymous referees, for
the relevant suggestions.
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