Acta Tropica 110 (2009) 187199

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

On the genus Panstrongylus Berg 1879: Evolution, ecology

and epidemiological signicance
James S. Patterson a,b,1 , Silvia E. Barbosa c , M. Dora Feliciangeli d,
a

Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
School of Life Sciences, University of Sussex, Brighton, East Sussex BN1 9QG, UK
c
Laboratrio de Triatomneos e Epidemiologia da Doenca de Chagas, Centro de Pesquisa Ren Rachou-FIOCRUZ, Av. Augusto de Lima, Barro Preto,
1715, 30190-002 Belo Horizonte, Minas Gerais, Brazil
d
Instituto de Investigaciones Biomdicas, Universidad de Carabobo (CNRFV-BIOMED) Apartado 4873, Venezuela
b

a r t i c l e

i n f o

Article history:
Received 14 April 2008
Received in revised form 7 August 2008
Accepted 1 September 2008
Available online 20 September 2008
Keywords:
Panstrongylus
Chagas disease
Phylogeny
Geographical distribution
Ecology
Biology
Medical importance

a b s t r a c t
The genus Panstrongylus is currently composed of 13 species, several of which are involved in the transmission of Trypanosoma cruzi to humans in South and Central America. Some species exhibit minor
morphological differences possibly associated with adaptation to different silvatic ecotopes or domestic environments. We present a distillation of past and recent literature pertaining to the biology of
this group. In particular, we summarise the current status of the genus according to systematic and
recent phylogenetic studies. In light of recent evidence suggesting polyphyly/paraphyly of the genus
we have investigated the possible mechanisms of morphological convergence/divergence. By assessing
postembryonic ontogeny we reveal that the distinctive head shape of Panstrongylus can be derived from
a Triatoma-like head late in development. A comprehensive phylogenetic study is therefore required to
elucidate their relationship with Triatoma spp., and other genera of the tribe Triatomini. We also present a
comparative summary of biology, ecology and epidemiological signicance for each species in the genus.
This reveals that knowledge of many species is fragmentary or lacking. This is mainly due to the fact that,
except for few species with synanthropic traits (P. megistus and P. lignarius [formerly P. herreri]), important vectors of Chagas disease in Brazil and Peru, the majority are sylvatic species, associated with a wide
variety of habitats and wild animals (many of them reservoirs of Trypanosoma cruzi). However, trends
to invade human dwellings and to establish domestic colonies have been observed in several species in
the genus (P. geniculatus, P. rufotuberculatus, P. lutzi, P. chinai), while others are opportunistic species (e.g.
P. lignarius in the Amazon basin ying from wild ecotopes to houses on occasion without colonizing).
Nevertheless, they can play some role in the transmission of sylvatic T. cruzi to humans. Research on the
genus Panstrongylus requires some focus on investigating the natural ecology of these species. This knowledge would add to our understanding of their evolutionary potential and may assist in predicting new
epidemiological scenarios, for which new control strategies need to be devised.
2008 Elsevier B.V. All rights reserved.

1. Introduction
Following the comprehensive revision of the subfamily Triatominae (Hemiptera: Reduviidae) by Lent and Wygodzinsky (1979),
three publications in the last decade (Carcavallo et al., 1997a;
Dujardin et al., 2002; Galvo et al., 2003) have provided useful
updates and compendia on the scientic investigation of this group

Corresponding author. Tel.: +58 243 242 58 22.

E-mail addresses: [email protected], [email protected]
(M.D. Feliciangeli).
1
Current address: South African National Bioinformatics Institute, University of
the Western Cape, Private Bag X17, Bellville 7535, South Africa.
0001-706X/$ see front matter 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.actatropica.2008.09.008

of insects. Triatomine bugs are responsible for the most common

mode of transmission of Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae), the etiological agent of Chagas disease, endemic
throughout Latin America where an estimated 810 million people have Chagas Disease (OPS, 2006; Remme et al., 2006). Efforts
to control Chagas disease have been successful in several countries. However, this goal has not been wholly achieved. One of
the possible factors that holds back progress towards interrupting
transmission in many areas, is triatomine species considered to be
secondary or occasional vectors.
In this review we have comprehensively gathered information
published on the genus Panstrongylus. This group of species currently deserves special attention, as several appear to be involved
in a process of domiciliation. This trend poses new complex epi-

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J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

demiological settings and new challenges for the control of Chagas

disease in the Americas (Schoeld et al., 1999).

Table 1
List of valid species and synonymies in the genus Panstrongylus Berg 1879.
1.

Panstrongylus chinai (Del Ponte, 1929)

Triatoma chinai Del Ponte, 1929
Panstrongylus turpiali Valderrama et al. (1996) (cf. Lent, 1997)

2.

Panstrongylus diasi Pinto and Lent, 1946

2. Systematics and phylogeny

Currently there are 140 species within the subfamily Triatominae, arranged in 6 tribes and 19 genera. Galvo (2003) discussed the
controversies in the application of different concepts and new tools
for the classication of this subfamily (see also in this issue). Here
we update the list of Panstrongylus species and summarise the current status of the genus in terms of phylogenetics and systematics.
We go on to present some new data exploring the processes of morphological evolution as evidence for a close relationship between at
least some Panstrongylus and Triatoma, and demonstrate a possible
route to morphological convergence.
The genus Panstrongylus Berg, 1879 is grouped with Triatoma and
7 other genera within the Tribe Triatomini. It was established with
the description of the type species; P. guentheri Berg 1879, having
formerly been described as the genus Lamus Stal 1859 within the
family Pentatomidae. After Triatoma and Rhodnius, Panstrongylus is
the third most speciose genus of the Triatominae subfamily. It is
presently composed of 13 species with a wide geographical distribution throughout the Neotropical region, extending from Mexico
to Argentina (Curto de Casas et al., 1999) (Table 1, Fig. 1).
The most recently described species, P. mitarakaensis, was discovered in French Guiana last year and by our assessment looks to
be closely related to P. geniculatus, rather than P. lignarius as suggested by the authors. In recent literature (Marcilla et al., 2002;
Crossa et al., 2002; Galvo et al., 2003; dos Santos et al., 2003) P.
herreri and P. lignarius have been synonymised on the basis of identity at the level of ITS-2 rDNA sequences (Marcilla et al., 2002) and
cytogenetic similarity (Crossa et al., 2002). As for other close relationships, two species; P. chinai and P. sherlocki have been recently
other species on the basis that they may only represent melanic
forms of P. howardi and P. lutzi respectively. In the case of sherlocki/lutzi, evidence for conspecicity was shown by Barbosa et al.
(2005). They studied P. lutzi captured in Minas Gerais and found that
it may show intraspecic variations in its phallic structures compatible with the description of P. sherlocki (Jurberg et al., 2001). The
relationship between P. chinai and P. howardi remains to be elucidated, and subsequently, for the time being, both are counted as a
valid species.

3.

4.

Panstrongylus guentheri Berg, 1879

Triatoma guentheri Neiva, 1914
Panstrongylus gntheri Berg, 1879
Panstrongylus larroussei Pinto, 1931
Panstrongylus seai Pinto, 1931
Triatoma larroussei Pinto, 1925
Triatoma seai Del Ponte, 1929

5.

Panstrongylus howardi (Neiva, 1911)

Triatoma howardi Neiva, 1911

6.
7.

Panstrongylus humeralis (Usinger, 1939)

Panstrongylus lenti Galvo and Palma, 1968

8.

Panstrongylus lignarius (Walker, 1873)

Triatoma lignarius Walker, 1873
Panstrongylus herreri Wygodzinsky, 1948
(cf. Marcilla et al., 2002; Crossa et al., 2002)

9.

Panstrongylus lutzi (Neiva and Pinto, 1923)

Triatoma lutzi Neiva and Pinto, 1923
Panstrongylus sherlocki Jurberg, Carcavallo and Lent, 2001 (cf.
Barbosa et al., 2005)

10.

Panstrongylus megistus (Burmeister, 1835)

Conorhinus megistus Burmeister, 1835
Lamus megistus Stal, 1859
Conorhinus gigas Burmeister, 1861
Conorhinus porrigens Walker, 1873
Triatoma africana Neiva, 1911
Triatoma megista Neiva, 1911
Triatoma wernickei Del Ponte, 1923
Triatoma megista var. wernickei Del Ponte, 1930
Panstrongylus africanus Pinto, 1931
Mestor megistus Usinger, 1944
Panstrongylus megistus leucofasciatus Lucena, 1959

11.

Panstrongylus mitarakaensis Brenger and Blanchet (2007)

12.

Panstrongylus rufotuberculatus (Champion, 1899)

Lamus rufotuberculatus Champion, 1899
Triatoma rufotuberculata Neiva, 1914
Triatoma coxo-rufra Campos, 1932
Mestor rufotuberculatus Usinger, 1939

13.

Panstrongylus tupynambai Lent, 1942

2.1. Intrageneric relationships

Intrageneric relationships among species were explored by Lent
and Wygodzinsky (1979) by constructing a dendrogram based on
21 character states (Fig. 2). The species groupings suggested by this
tentatively cladistic treatment more or less correlate with patterns
of geographical distribution, giving northern and southern clades
(Fig. 2), and are on the whole supported by molecular and cytogenetic studies. Only the placement of P. megistus is discordant, in so
far that it is largely southern in its distribution and is unusual cytogenetically, having only 18 autosomal chromosomes compared to
the 20 autosomes of other Panstrongylus (and most other Triatominae) so far analysed (Crossa et al., 2002). Similar species groupings
for the genus were also reported by Lent and Jurberg (1975) on
the basis of a comparative analysis of male and female genitalia,
and tentatively by traditional morphometrics of head shape (dos
Santos et al., 2003).
2.2. Intergeneric relationships and paraphyly
Molecular genetic studies conducted fairly recently (Marcilla
et al., 2002; Hypsa et al., 2002) have addressed intergeneric

Panstrongylus geniculatus (Latreille, 1811)

Reduvius geniculatus Latreille, 1811
Conorrhinus lutulentus Erichson, 1848
Conorhinus geniculatus Walker, 1873
Lamus geniculatus Stal, 1859
Mestor geniculatus Brindley, 1931
Triatoma geniculata Chagas (1912)
Conorhinus lutulentes Erichson, 1848
Conorhinus corticalis Walker, 1873
Triatoma tenuis Neiva, 1914
Triatoma uminensis Neiva and Pinto, 1922
Panstrongylus parageniculatus Ortiz, 1971

relationships and suggest that the genus may in fact represent

a polyphyletic assemblage of converged species. Hypsa et al.
(2002) were more reserved in their inferences. Notwithstanding,
they demonstrate paraphyly in their analysis, showing a close
relationship between P. herreri/lignarius and the Caribbean Nesotriatoma (formerly Triatoma avida and relatives) and between
P. megistus and T. tibiamaculata (the latter two species having, to some extent, overlapping distributions). Marcilla et al.
(2002) clearly show that North American Triatoma lineages are
more closely related to northern Panstrongylus spp. (in particular P. rufotuberculatus) than to a sample of South American

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

189

Fig. 1. Photographs of Panstrongylus species. Specimen details; date and location of collection and institution where held (as applicable and where known), for each specimen
shown, ordered from left to right, top to bottom: P. chinai (Northern Peru, 1959, FIOCRUZ); P. howardi (Ecuador, 2000); P. rufotuberculatus (Panama, 1954, LSHTM); P. geniculatus
(Panama, 1954, LSHTM); P. mitarakaensis (French Guiana, 2007); P. lignarius (Guyana, 1938, NHM); P. humeralis (FIOCRUZ); P. megistus (lab colony Fundaco Oswaldo Cruz,
Minas Gerais, Brazil, 2008); P. lutzi (Bahia, FIOCRUZ); P. diasi (Minas Gerais, Brazil, Holotype, FIOCRUZ); P. tupynambai; P. guentheri (Argentina, 1948, NHM); P. lenti (Goias,
Brazil, allotype, 1988, FIOCRUZ). (Institutions FIOCRUZ = Laboratrio Nacional e Internacional de Referncia em Taxonomia de Triatomneos, Instituto Oswaldo Cruz, Rio de
Janeiro, Brazil; LSHTM = London School of Hygiene and Tropical Medicine, UK; NHM = Natural History Museum London, UK. Attributions: * J.S. Patterson C. Galvo J.M.
Brenger and B. Blanchet (2007) Y. Basmadjin. # S.E. Barbosa.

Triatoma. These studies lack representatives of the southern

clade Panstrongylus species, and there is now a clear need to
conduct a comprehensive phylogenetic analysis of Panstrongylus with representatives of the various Triatoma lineages and
other genera of the Triatomini to elucidate the phylogeny of
the tribe.

2.3. Head shape convergence

In light of molecular evidence suggesting that some Panstrongylus share their most recent common ancestors with certain Triatoma
rather than other Panstrongylus species we have scrutinised the traditional morphological trait that characterises the genus: The genus

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J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

Fig. 2. Cladogram of hypothesised relationships within the genus Panstrongylus. Redrawn from Lent and Wygodzinsky (1979). Constructed using 21 morphological characters,
each with two states. Northern and Southern geographical distributions correspond reasonably well with the two main clades, with the exception of P. megistus**.

is traditionally thought to be monophyletic, and is primarily dened

by autapomorphic characterisation of head patterning, specically
that the anteniferous tubercules are situated close to the anterior
margin of the eye (Lent and Wygodzinsky, 1979). A comprehensive morphometric comparison of head shape differences among
Panstrongylus species (dos Santos et al., 2003) tentatively supports
the aforementioned division between the northern and southern
species. To explore the suggested paraphyly/polyphyly of the genus,
from the morphological perspective, we have examined the relative
differences in head shape between Triatoma and Panstrongylus.
Other than having their antennae inserted close to their eyes,
Panstrongylus heads are often considered to be relatively short. Further to this, on inspection it seems that in many cases Panstrongylus
species have large eyes relative to their head size and overall body
size (e.g. P. megistus and many of the northern clade species) in
comparison to many other triatomines. A functional interpretation
is that large eyes with more numerous and/or larger ommatidia
are considered to be an adaptation to dim illumination (Bauer
et al., 1998; Olof Bjrn, 2002). When considered in the context

of the common general ecological specialisation of Panstrongylus

species, i.e. terrestrial, arboreal, and subterranean habitats (albeit
that details of specic habitats are scant for many species), it seems
reasonable to assign large relative eye size as an adaptation to
the dim illumination associated with such habitats. A corollary
of this is that relatively large eye size, and restricted head length
could account for a shorter distance between eye and antennal
insertion. From this perspective the character can be considered
a possible homoplasy contributing to morphological convergence
among some Panstrongylus with large eyes to those with smaller
relative eye size (northern and southern species groups). In
comparison to Triatoma (characterised as having their antennae
inserted intermediately between anterior edge of eye and anteclypeus) an enlargement of eye size without otherwise modifying
the head plan could result in a Panstrongylus-like head (Fig. 3a)
(see Schoeld and Galvo this issue, where they comment on the
similarity between certain North American Triatoma species and
Panstrongylus head conguration). Conversely, we can imagine that
if certain Panstrongylus species had smaller eyes, their heads would

Fig. 3. Comparative proportions of head shape between (a) Triatoma (T. vitticeps) and (b) Panstrongylus (P. megistus). Images are scaled to the same length revealing that
proportions i and iii are similar across a and b, whereas proportion ii differs between a and b in relation to the relative eye size (e).

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

have a more Triatoma-like appearance (Fig. 3b). Indeed, during

development, nymphs of Panstrongylus have proportionately small
developing eyes and consequently their heads are Triatoma-like.
Credence of a link between eye size, relative head shape and
ecology can be found in observed patterns of natural variation:
It has been recorded that two widely dispersed species P. rufotuberculatus and P. geniculatus demonstrate notable morphological
variation across their ranges, including some clear reductions in
eye size (Lent and Wygodzinsky, 1979; dos Santos et al., 2003).
An illustration of such an example for P. rufotuberculatus (Lent and
Wygodzinsky, 1979) does indeed show that the small eyed form
has a more Triatoma-like head shape.
2.4. Comparative ontogeny of head shape
Working on the hypothesis that in some cases if not all,
Panstrongylus species have arisen from lineages with Triatomalike heads by adaptation to a common ecology, we conducted a
preliminary analysis of comparative head shape changes during
development (ontogeny). We conducted a geometric morphometric analysis of post-embryonic head shape changes through the
ve nymphal stages and compared them to adult head shape (see
Rocha et al., 2005 for details of methodology). We used specimens
of P. megistus in comparison to two Triatoma species (T. lecticularia
and T. infestans) and included Rhodnius prolixus as an outgroup. All
specimens were laboratory reared under common conditions and
10 specimens of each of the ve stadia and each sex of adults were
included.
Geometric morphometry was conducted as follows: The dorsal
surface of the heads were imaged by microscopy and digital photography and digitised to acquire a suite of seven landmarks (see
Fig. 4). Procrustes superimposition algorithms were used to extract

191

isometry-free shape variables from the two dimensional landmark

congurations. Subsequently, multivariate statistics, i.e. principal
component (PC) analysis was used to extract the main components
of shape differences among all specimens. The rst two principal
components cumulatively account for 92.8% of the shape variation (PC1 72.2% and PC2 20.6%). A plot of these two axes (Fig. 4)
clearly shows an overlap in head shape among Triatoma nymphs
(T. lecticularia in particular) and P. megistus nymphs. Notably, the P.
megistus ontogenetic trajectory is remarkably discontinuous compared to the other species, with all P. megistus nymphs occupying
a similar area of the shape space. The huge jump from juvenile
to adult head shape is attributable to PC2 and relates primarily to
the relative enlargement of the eyes (Fig. 4). This reinforces our
assertion above that the Panstrongylus-like head is derived from
a Triatoma-like head plan and demonstrates that it is derived by
modication in late post-embryonic development. All the species
included in the analysis can be seen to do this to a certain extent,
which accounts for the clear distinction in head shape between
nymphs and adults intraspecically (Fig. 4). Invoking Gould (1977),
he postulated that among K-strategists macroevolutionary changes
occur by one of two heterochronic (change of timing) events: either
by hypermorphosis: extended differentiation and an increase in
specialised complexity accompanying delayed maturation; or by
neoteny; delayed maturation linked to retarded differentiation and
retention of exible juvenile morphology. It is the latter that Gould
states as being less common but with greater macroevolutionary
potential. Applying this, it seems that in our analysis of ontogenic
allometry all the species included exhibit a degree of hypermorphosis; with specialised head shapes as adults with long trajectories
through the shape space. In addition to this, we observe that P.
megistus, in comparison to the other species varies little along PC1
from 1st instar to adult, and in this respect seems to be relatively

Fig. 4. Comparative geometric morphometric investigation of head shape ontogeny. The plot shows shape differences among nymphs and adults of four species T. lecticularia
T. infestans, R. prolixus and P. megistus. Procrustes superimposition was used to extract isometry-free shape variables from two dimensional landmark congurations (image
bottom left shows the set of landmarks recorded from each specimen). Subsequently, principal component (PC) analysis was used to extract the main components of shape
differences among all specimens. This gave the two axis used in the plot (PC1 and PC2). Each data point represents a single specimen from samples of instars 15 plus male
and female (10 specimens per stage, i.e. 70 specimens per species). Lines are draw to t the ontogenic trajectories from 1st instars to adults (adult specimens of each species
are enclosed by ellipses). Transformation grids correspond to the shape changes associated with the extremes of the principal component axes, as indicated by dashed lines.

192

Table 2
Distribution, bionomics and ecology of the Panstrongylus species.
Distributiona

Life cycleb (d = days)

Natural infection by
Trypanosoma cruzi

Feeding sourcesc

Ecology and evolution

Panstrongylus chinai (Del Ponte,

1929)

Venezuela, Ecuador, Peru

236 d at 29 C; 70% RH (Guilln

et al., 1991)

(Arrarte Ovalle, 1955)

Wild sources unknown.

Chickens and domestic
mammals

Tropical and subtropical forests

and dry forest (Curto de Casas
et al., 1999)
Wild habitats in Peru (Vasquez,
2005; Vargas, 2005) and SE
Ecuador (Abad-Franch et al.,
2001)
Peridomestic ecotopes (goat
pens; chicken coops) and stone
built structures, occasionally
domestic (Vasquez, 2005;
Abad-Franch et al., 2001;
Cceres et al., 2002; Grijalva et
al., 2005)

No data

Wild sources unknown.

Domestic animals (?) humans

Forest species; adult specimens

have been found in human
dwellings (Silveira, 2000;
Oliveira and Silva, 2007)

(Chagas, 1912 in Brazil, Silvrie

et al., 1964) in French Guiana,
Omah-Maharaj, 1992 in
Trinidad (42.5%)

Marsupials, opossums,
anteaters, armadillos, bats,
cats, birds, chicken

Tropical dry or very dry forest

and savannah to humid tropical
forest (Carcavallo et al., 1999)

Valente, 1999 in Brazil;

(16.46%), Wolff and Castillo
(2000) (50%) and Guhl et al.
(2007) in Colombia);
(Feliciangeli et al., 2004) (20%)
and (Carrasco et al., 2005)
(76.1%), in Venezuela

Edentata (81-93%), opossum

(4-11%), rodents (4-8%)
(Barretto, 1967, 1968, 1971)

Wild species, sometimes

captured in domestic ecotopes
in Argentina, Brazil, Colombia,
Ecuador, French Guyana,
Venezuela and Peru

Humans (60.2%), domestic

animals (52.27) rats (3.8%);
chickens (1.4%) (Carrasco et al.,
2005)

Incipient domestication
observed in Colombia (Wolff
and Castillo, 2000) and
Venezuela (Feliciangeli et al.,
2004; Carrasco et al., 2005)

(Herrer, 1955)

(Daz-Limay et al., 2004) (all

records from Peru)

Panstrongylus diasi Pinto &

Lent, 1946

Bolivia, Brazil

Panstrongylus geniculatus
(Latreille, 1811)

Mexico, Guatemala, Nicaragua,

Costa Rica, Panama, Colombia,
Venezuela, Trinidad, Guyana,
Surinam, French Guyana,
Brazil, Ecuador, Peru, Bolivia,
Paraguay, Uruguay, Argentina

No data

531 d (Lent and Jurberg, 1969);

1st instar nymphs to adults:
269297 d (Galndez, 1990);
274.8 d (Cabello and Galndez,
1998)

Panstrongylus guentheri Berg,

1879

Bolivia, Paraguay, Uruguay,

Argentina, Brazil (Almeida et
al., 2008)

264 d (Carcavallo et al., 1994)

Mazza and Reyes Oribe (1939)

in Argentina

Marsupials, rodents, birds.

Possibly edentates

Savannahs, dry tropical and

subtropical xerophytic forests
as well as semi-arid plains and
plateau. (Curto de Casas et al.,
1999)
Wild species, with adults
seldom found in dwellings, but
it does not establish colonies

Panstrongylus howardi (Neiva,

1911)

Ecuador

No data

Len (1962)

Wild sources unknown.

Possibly domestic animals or
humans

Unknown ecology, adults

seldom found in dwellings.
Few records of presence in
articial habitats, Defran
(1982) reported nding a small
peridomestic colony.
Abad-Franch et al. (2001)
found specimens indoors

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

Species

Panstrongylus humeralis
(Usinger, 1939)

Panama, Colombia (Guhl, 1999)

149.4151 days (Turner and

Sousa, 1988)

Sousa and Adames (1977)

Wild sources unknown.

Probably wild mammals
(Cedillos et al., 1985)

Tropical and subtropical forest

(Curto de Casas et al., 1999)
Natural habitat unknown,
occasionally invades houses

Brazil

No data

No data

Unknown

Panstrongylus lignarius (Walker,

1873) = Panstrongylus herreri
Wygodzinsky, 1948

Venezuela, Guyana, Suriname,

Brazil, Colombia (DAlessandro
et al., 1984); Peru, Ecuador
(Aguilar et al., 1999;
Abad-Franch et al., 2001;
Abad-Franch and Aguilar,
2003)

165 d (2530 C) (Silva and

Silva, 1991)

Lumbreras Cruz et al. (1955) (in

Peru)

Marsupials, spiny rats,

anteaters, bats, toucans,
chickens, rabbits, pigeons

1st instar nymphs to adults:

173 days at 25 C and 155 at
30 C (Canale et al., 1999)

Deane and Damasceno (1949),

Teixeira et al. (2001) (27%) both
in Brazil; Guhl et al. (2007) in
Colombia

Guinea pigs, domestic animals,

humans

The only adults found were

inside dwellings (Barata et al.,
1997)
Tropical and subtropical forests
as well as tropical and
subtropical dry forests (Curto
de Casas et al., 1999). Domestic
and peridomestic in Peru (Cuba
Cuba et al., 2002), Silvatic in
the Amazon basin
(Teixeira et al., 2001; Guhl et
al., 2007)

Panstrongylus lutzi (Neiva and

Pinto, 1923)

Brazil

1st instar nymphs to adults:

664 days (Dias, 1955)

Silveira et al. (1984), Garca et

al. (2005, 1%-5%), Caranha et al.
(2006, 29.1%). All data from
Brazil, Cear

Birds, rodents (10.1%), opossum

(8.8%), armadillo, ox (6.3%)
humans (3.8%) horses (2.5%)
cats (1.3%) (Caranha et al.,
2006)

Indigenous to Brazil (Lent and

Wygodzinsky, 1979, Carcavallo
et al., 1999) and native to
regions of caatinga. Species
mainly wild; peridomestic and
domestic colonies found in
Cear, Brazil (Freitas et al.,
2004; Garcia et al., 2005)

Panstrongylus megistus
(Burmeister, 1835)

Brazil, Bolivia, Paraguay,

Uruguay, Argentina

260324 d (Neiva, 1910);

100159 d
(Perlowagora-Szumlewicz,
1976); see the text for Barbosa
et al. (2001)

Chagas (1909), Steindel et al.,

1994: 55.3% in Santa Catarina;
Litvoc 1990: 44.0% in So
Paulo; Koop, 2002: 32.0% in
Paran; Pinho et al., 2000: 3.6%
in Rio Grande do Sul; Silva et
al., 2006: 5.3% in Gois (1990s);
Oliveira and Silva (2007): 0.49%
in Gois (20022003)

Humans, birds opossum

rodents, dogs, bats (Barretto,
1968)

In Brazil the distribution of P.

megistus coincides with the
original Atlantic Forest and its
remnants, now included in the
dryer regions of caatinga and
cerrado (Forattini, 1980;
Barbosa et al., 2001, 2003)

Humans (80.8%) from insects

caught indoors in Bahia
(Minter, 1975)

Species found in sylvatic and

articial ecotopes with
frequent domestic colonies
(Silveira, 2000, WHO, 2002)

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

Panstrongylus lenti Galvo and

Palma, 1968

Opossums (62.9%) in Sta

Catarina Island (Steindel et al.,
1994)
Panstrongylus mitarakaensis
Brenger and Blanchet
(2007)

French Guiana (Brenger and

Blanchet, 2007)

No data

Brenger and Blanchet (2007)

Unknown

Unknown

Panstrongylus rufotuberculatus
(Champion, 1899)

Mexico,Costa Rica, Panama,

Colombia, Venezuela, Ecuador,
Peru, Bolvia, Brazil, Argentina

138.82 51.42 d (24 2 C;

RH = 94 4%) (Wolff et al.
(2004)

Lent and Pifano, 1940: in

Venezuela. Len and Len,
1953): Lazo, 1985: 14.% in
Ecuador, Noireau et al. (1994)
in Bolivia; Wolff and Castillo,
2002: 4.6%; and Guhl et al.
(2007) in Colombia

Kinkajous, vampire bats,

armadillos, opossums.
Domestic animals, humans

Tropical, humid and

subtropical forest (Curto de
Casas et al., 1999)

193

Sylvatic; adults occasionally

found in dwellings, but
colonisation of the domestic
environment has not been
conrmed (Lent and
Wygodzinsky, 1979; Ruas-Neto
and Corseuil, 2002)

neotenic. In turn, this retention of exible juvenile morphology

may be the factor that has allowed P. megistus, and perhaps other
Panstrongylus to accommodate an enlargement in eye size. This
region of the shape space also coincides with the other juvenile
Triatoma and may represent the ancestral head shape of the tribe.

3. Geographical distribution, ecology and behaviour

Unless citations are given, data are from Lent and Wygodzinsky (1979), Carcavallo et al. (1997b), Dujardin et al. (2002) and Galvo et al. (2003).
Unless specied, time is referred to the cycle egg-adult.
Unless citations are given, data are from Carcavallo et al. (1998b).

Cricetidae, Didelphidae birds,

reptile (Uruguay) Salvatella
(1986a,b) humans, birds, dogs
rodents (Brazil) Lorosa et al.,
2000), lizards (Martins et al.,
2006)
Lorosa et al. (2000): 14.3%;
(Ruas-Neto and Corseuil,
2002): 5.1% (both records from
Brazil)
Brazil, Uruguay
Panstrongylus tupynambai Lent,
1942

455 days (Salvatella, 1986b)

Feeding sourcesc
Natural infection by
Trypanosoma cruzi
Life cycleb (d = days)
Distributiona
Species

Table 2 (Continued )

Species generally wild, but

domestic colonies have been
reported from southern
Ecuador (Avils et al., 1995,
Abad-Franch, 2000), Peru
(Lizaraso, 1955; Caldern et al.,
1985); Bolivia (Noireau et al.,
1994; Dujardin et al., 1998),
Colombia (Wolff and Castillo,
2002) and Peru (Marn et al.,
2007)

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

Ecology and evolution

194

A large amount of information on the geographical distribution

and ecology of triatomine bugs is available in the literature. We
have summarised the essential data in Table 2 (mainly extracted
from Lent and Wygodzinsky (1979), Dujardin et al. (2002), Galvo
et al. (2003), Carcavallo et al. (1997a), Curto de Casas et al. (1999),
Barata et al. (1997) and Almeida et al. (2008). In the original papers
more detailed information (e.g. distribution by State in each country, description of habitats and microhabitats, etc.) can be found.
Data published after the references cited above have been added
and additional comments are in the text.
Among the 13 species of the genus, P. geniculatus has the widest
distribution, being currently known in 18 Latin American countries, from Mexico to Argentina, including several of the Caribbean
islands. It is followed by P. rufotuberculatus, which also extends from
Central to South America occupying 10 countries. The third most
widely dispersed species is P. lignarius found in 7 scattered South
American countries, while P. megistuss geographical distribution is
mainly restricted to eastern South America. The remaining species
have more limited or undened distributions and, as we will see,
less ecological data are available, with several species completely
enigmatic. However, although some Panstrongylus species, such as
P. megistus, can be found in palm crowns, all species are predominantly associated with terrestrial burrows, tree root cavities and/or
arboreal tree holes (Gaunt and Miles, 2000). Based on its ecological
characteristics, P. geniculatus has been considered an eurythermic
species, adapted to several dry as well as humid ecotopes where it
is found in a great variety of sylvatic habitats including the burrows
or resting places of armadillos, opossums, rodents, bats and birds,
as well as hollow trees or under bark, in bromeliads and among
the fronds of various species of palm (Carcavallo et al., 1998a). This
species is frequently captured in peridomestic environments and its
occurrence inside houses has been cited in several countries. Seasonal domiciliation of P. geniculatus with pigs has been reported
in the Amazon Basin (Valente et al., 1998), who also stressed the
potential for domiciliation of this species in Maraj Island, State of
Par, Brazil (Valente, 1999). Evidence for the domiciliation of this
species in Amal, Colombia, has been reported by Wolff and Castillo
(2000) who demonstrated that domestic invasion by P. geniculatus
does not seem to be exclusively due to attraction to electric light,
as was commonly accepted previously. We observed mixed domestic infestation of nymphs of P. geniculatus and Rhodnius prolixus in a
rural area of Venezuela which also led us to suspect a possible incipient process of domiciliation (Feliciangeli et al., 2004). Domestic P.
geniculatus has also been caught repeatedly by the inhabitants of
Caracas, Venezuela in their dwellings. This led us to investigate the
potential role of these bugs as vectors of Chagas disease in an urban
setting (Carrasco et al., 2005) (see Section 5).
Panstrongylus rufotuberculatus is generally considered to be a
sylvatic species ranging from Mexico to Argentina. It has been
found in palms, hollow trees and the refuges of wild mammals
(Lent and Wygodzinsky, 1979; DAlessandro et al., 1981; Miles et al.,
1981). Adult insects frequently invade human dwellings, attracted
by electric light (Lent and Wygodzinsky, 1979; Salomn et al.,
1999). However, the presence of stable domestic colonies has been
reported recently in 2/15 houses in the region of Piura, Peru (Marn
et al., 2007). This species tends to be more abundant during the

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

rst 6 months of the year (dry season and onset of rainy season)
although it is easily found throughout the year (Zeledn et al., 2001;
Wolff and Castillo, 2002). Based on records of diffuse distribution
in Venezuela, Guyana, Suriname, Brazil, Colombia and Ecuador, P.
lignarius was previously considered to be mainly a sylvatic species.
It has been found in palms, birds nests and Didelphis nests, rodent
burrows, toucan nests and hollow trees (Carcavallo et al., 1998a).
The unique record of P. lignarius in Venezuela was a female found in
a palm (Otero et al., 1975). Gaunt and Miles (2000) observed that in
the Amazon basin in Brazil, adults move freely over the trees protected by their coloration that matches beautifully the bark, while
nymphs lacking this exquisite camouage, rest in tree holes. In the
Amazon basin in Ecuador P. lignarius was found in a dwelling (AbadFranch et al., 2001) and it had occasionally been reported indoors, or
in chicken coops, sometimes attracted by light, in Brazil and Colombia (Deane and Damasceno, 1949; Miles et al., 1981; DAlessandro et
al., 1984; Guhl et al., 2007). However, P. lignarius domestic populations in Peru (formerly P. herreri) show strong synanthropic habits
known in Peru since 1948, where its phototropism has also been
repeatedly observed (Herrer, 1960; Caldern et al., 1985).
Panstrongylus megistus is a triatomine with a wide geographical
distribution, ecological valence and great potential of colonisation
of the articial ecotopes. According to Forattini (1980), in tropical
Atlantic region, this species is associated with habitats characterised by high levels of humidity. However, except those of the
Amazon, P. megistus occurs in all types of Brazilian forests which
include dry and moist humid forest in the cerrado and caatinga.
The occurrence of P. megistus in the dryer regions of the cerrado
(the Brazilian savanna) has been reported by Barretto (1979) and
Sherlock (1979). It was found in palm crowns, other trees, rodent
and marsupials shelters, terrestrial burrows and hollow trees with
bats. Miles et al. (1982) reported occurrences in arboreal tree holes
with Didelphis in Rio de Janeiro Brazil. However, the species is
usually associated with humid forests, from which adults invade
houses (Forattini et al., 1977), especially during the rainy season
(Dias and Dias, 1968). P. megistus may have begun to invade the
domestic environment during the post-colonial period; following
the destruction of its natural habitat and consequent agricultural
developments, this species presumably invaded and adapted to
exploit domestic environments (Litvoc et al., 1990).
Barbosa et al. (2006) observed great diversity in populations of
P. megistus, this was considered in the context of paleovegetation
reconstruction. The local paleovegetation record shows a clear process of expansion and retraction of humid forest during the last
18,000 years, and can account for the observed fragmented population structure. The autochthonous status of P. megistus in the
cerrado is reinforced by control program data that shows the reinvasion of houses after control with insecticide, with bugs thought
to be originating from silvatic foci.
In other countries (Bolivia, Paraguay, Uruguay, Argentina) P.
megistus is almost entirely sylvatic (Salvatella, 1986a; Carpinteiro
and Viana, 2008), and on the occasions when it is found in domestic
habitats it is usually associated with synanthropics hosts, especially
opossums (Steindel et al., 1994).
The ecology of P. chinai is known mainly from Peru (Vargas,
2005; Vasquez, 2005), where adults have been occasionally
reported in houses, with similar observations in Ecuador (AbadFranch et al., 2001; Grijalva et al., 2005) (Table 2), but not from
Venezuela where it was reported only from the locality El Carrizal
(Mrida State) as P. turpiali (Valderrama et al., 1996) (cf. Lent, 1997).
Although frequently collected in articial environments in
Brazil, the wild habitats of P. diasi remain unknown as well as
aspects of its biology, ecology and genetics; P. humeralis was
reported in Colombia by Guhl (1999) and it constituted 0.5% of
triatomines caught in the eastern region of this country (Angulo,

195

2000). The incipient process of colonisation by P. lutzi was rst

noted in 1984 by Silveira. The few reports of this species from
wild ecotopes refer to nymphs and adults in armadillo burrows
(Dias-Lima et al., 2003) and adult females under the bark of pau
branco (Auxemma oncocalyx) trees (Garcia et al., 2005). Although
it remains a predominantly wild species, its presence in peri- and
intradomestic habitats is currently being noted with increasing
frequency (Vinhaes and Dias, 2000; Freitas et al., 2004; Garcia
et al., 2005). Colonies have also been observed in the Brazilian
state of Cear where an infestation rate of 4.6% was reported by
Garcia et al. (2005). Panstrongylus tupynambai is strictly sylvatic,
inhabiting rupestrian and subterranean ecotopes, such as rockpiles
semi-buried in humid soil, as well as rodent and reptile burrows
(Salvatella, 1986a,b; Martins et al., 2006).
To conclude, from the knowledge so far available, according to
Curto de Casas et al. (1999), excluding P. lenti, P. mitarakaensis and
P. sherlocki (a melanic specimen of P. lutzi) (because only one or two
specimens have been caught of each), based on Holdriges climate
parameters, of the Panstrongylus genus, P. geniculatus occupies the
widest range of life zones; very dry forests or savannahs, dry, wet,
moist and rainy forests; P. rufotuberculatus and P. megistus inhabits
dry, wet and moist forests; P. howardi and P. humeralis are found in
wet forest; P. lutzi seems to be restricted to moist forest; P. lignarius is found in wet as well as in dry habitats; P. chinai occupies
desert, desertic brushwood or steppe and thorny brushwood; P.
diasi is found in desertic brushwood or steppe and thorny brushwoods; P. guentheri and P. tupynambai are found in very dry forests
or savannah and thorny brushwood.
In relation to the synanthropic habits of these species, P. megistus
in Brazil is one of the main domiciliated species along with P. lignarius domestic populations (formerly P. herreri) in northern Peru;
P. geniculatus, P. lutzi and P. rufotuberculatus are all able to develop
peridomestic and domestic colonies in certain areas, while P. chinai, P. diasi, P. guentheri, P. howardi, P. humeralis, and P. tupynambai
are wild species with occasional records of specimens in human
dwellings.
4. Biology
There is relatively little information on the biology of the
Panstrongylus species. Historically, little attention has been paid
to these species because the majority of them are sylvatic and
therefore often regarded solely as a potential threat, not typically involved in human transmission. In Table 2 we report the
available data on the life cycles of 9 species. There is the obvious
caveat that different geographical origins, different laboratory conditions, feeding sources and rhythms of feeding may undermine
any inferences made from any comparison of life cycles. Despite
this, measurements of life cycles, as well as population parameters
and demographic strategies, constitute useful biological information, which might assist in estimating the potential a species has
for colonisation and also their vector potential.
5. Medical importance
We have already reported on and discussed several factors,
which may predispose triatomine species to be potential vectors;
such as geographical distribution, capacity for establishing periand domestic colonies, frequency of invading domestic ecotopes,
adaptability to different habitats and hosts, and nally biological
characteristics. In this section we will focus on other variables that
are more strictly related to the parasitevector relationship and
the vectorhuman contact, which are clearly the ultimate determinants for vectorial transmission of T. cruzi. The primary factor is

196

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

the susceptibility of a triatomine species to T. cruzi, secondary is

the efciency in the process of feeding in terms of T. cruzi transmission, i.e. a successful human-vector contact, and thirdly the
timing of defaecation of the bug during blood meal uptake which
would facilitate deposition of the parasite on or near the host
before departing. These three parameters have been well studied
for domestic species, but have only been recorded for a few sylvatic species. Nevertheless, gathering all the available information,
we have inferred the vector potential of each species in the genus
Panstrongylus.
Natural infection with T. cruzi has been detected in 12 out of 13
Panstrongylus species (see Table 2). High infection rates might be
an indicator of close proximity to reservoir hosts and high susceptibility to T. cruzi, as seems to be the case for P. megistus in Brasil, P.
lignarius in Peru and P. geniculatus in several countries. On the other
hand, information on the source of blood-meals (Table 2) is of epidemiological importance because it indicates potential reservoirs
of T. cruzi and vectorhuman contact, revealing the presence of possible synanthropic transmission cycles. Six species, P. megistus, P.
geniculatus, P. lignarius, P. rufotuberculatus, P. lutzi, and P. tupynambai
successfully feed on humans (Table 2), while other species (P. diasi,
P. howardi) are strongly suspected to feed on humans (Carcavallo et
al., 1998b).
Panstrongylus megistus was the rst species of triatomine to be
incriminated as a vector of Chagas disease (Chagas, 1909) and it was
considered as the main domestic vector in Brazil until the decade
of 1930 when it started to be progressively replaced by Triatoma
infestans (Dias and Dias, 1968; Dias, 1982). Decreased infection
rates for Brazil overall (3.50% for 197783 and 2.72% for 1997) were
reported during that period (Silveira and Vinhaes, 1998). However,
following the success of the southern cone Chagas disease control
programme that achieved the elimination of T. infestans in many
areas (Dias and Schoeld, 1999), P. megistus initiated a new process
of invasion and domiciliation in several states of Brazil. In 46/54
municipalities of Minas Gerais under epidemiological surveillance
between 2000 and 2003, P. megistus was 94.1% of the total bugs
caught, with a colonisation index of 32.3% and a rate of infection of
1.3% (Villelas et al., 2005). In Goias where 201 out of 246 municipalities were infested by triatomine bugs, Triatoma sordida and
Rhodnius neglectus predominated, but P. megistus was also caught
in the peridomestic as well in the domestic ecotopes (Oliveira and
Silva, 2007). Thus, P. megistus is currently considered to be the main
autochthonous vector of Chagas disease in the central, eastern and
southeastern regions of Brazil.
Reported high incidence of P. geniculatus blood-fed on humans
and concomitantly infected with T. cruzi I (ZI) in Caracas, Venezuela
(Carrasco et al., 2005), highlighted the epidemiological importance of this species classically considered a visitor species, and
an accidental human feeder. Wolff and Castillos study (2000)
demonstrated that P. geniculatus defecates during feeding, suggesting that this species is likely to be a competent vector. Subsequently
it was implicated in fatal cases of acute Chagas myocarditis in
infants in Caracas (Losada et al., 2000). Further to this, a recent
outbreak of infections occurred in Caracas, possibly via oral transmission, in a primary school, November 2007 (ProMED-mail, 2007).
The ingestion of fruit juice accidentally contaminated by P. geniculatus, is thought to have been the cause. This highlights oral
transmission as a possible emerging epidemiological scenario in
Venezuela.
Infection by T. cruzi I (ZI) was also reported in P. geniculatus
infesting pigsties in the community Furo do Rio Grande in the
Amazon Basin, where it was also isolated from the pigs and Didelphis marsupialis, although no human infections were registered
(Valente et al., 1998). Elsewhere (Amazonias and Rondonia States)
P. geniculatus was frequently associated with the armadillo Dasy-

pus novemcinctus, infesting its burrows and transmitting T. cruzi,

zymodeme 3 (Z3) (Povoa et al., 1984). This reveals that transmission
cycles are possibly partitioned according to host and ecology. Further studies along these lines are vital to elucidating the aetiology
of human infections.
P. rufotuberculatus has been incriminated as a vector of Chagas
disease in Andean and coastal foci of Ecuador, with domestic populations reported in Santo Domingo de los Colorados. The death
of a child from Chagas disease has been attributed to a bite from
this species (Abad-Franch and Aguilar, 2003). In the municipality of
Amal in Antioquia, Colombia, the presence of P. rufotuberculatus
(the second most common triatomine caught inside buildings) is
considered to be a major epidemiological risk factor (Wolff et al.,
2001). Several characteristics that could be linked to high vectorial
capacity were observed for this species, including longevity, rapid
response to the presence of a host, large volume of blood ingested
and frequent defecation during the feeding process (Wolff et al.,
2004).
The most strongly synanthropic species P. lignarius (formerly
P. herreri) is considered the principal vector of Chagas disease in
Per (Cuba Cuba et al., 2002). It was the predominant species
(4721/5008 indoors and 534/559 in the peridomestic habitat) collected by active search in urban and rural areas in the departments
of Cajamarcas and Amazonas, endemic for Chagas disease (Cceres
et al., 2002). Transmission of sylvatic T. cruzi to humans has also
been associated with P. lignarius. In the Amazon basin this species
was observed to y from palm trees (Attalaea phalerata) to houses
(Teixeira et al., 2001). In Colombia, this species has been found in
bird nests and it is not considered of epidemiological importance
(Guhl et al., 2007).
P. lutzi is one of the most important secondary vectors in Brazil.
Together with its great capacity for invading houses through ight,
it shows high rates of natural infection with T. cruzi, probably related
to its intimate association with armadillos (Dias-Lima et al., 2003).
This was conrmed by a study on its feeding sources which showed
that P. lutzi appears to be an eclectic species that takes blood meals
from at least eight different hosts species (Caranha et al., 2006).
P. chinai probably acts as the vector of T. cruzi in sylvatic cycles in
arid areas of north and eastern Peru (Vasquez, 2005) as well as
in SE Ecuador (Abad-Franch and Aguilar, 2003). Finally, P. howardi
is considered to be as potential vector of T. cruzi in the coastal
region of Ecuador (Abad-Franch and Aguilar, 2003). The remaining Panstrongylus species; P. diasi, P. guenteri, P. humeralis, P. lenti, P.
mitarakaensis and P. tupynambai have not so far been incriminated
as vectors of T. cruzi to humans but are most probably involved in
sylvatic T. cruzi cycles.
To conclude, we have demonstrated here that there is a clear
need to know more about the genus Panstrongylus, from a phylogenetic/evolutionary point of view, and in regard to ecology,
biogeography and vectorhosts/parasite interactions. Research into
these areas would shed more light on the complex and changing
epidemiological settings of Chagas disease in the Americas, with
the aim of achieving further progress in reducing the burden of
this neglected disease.

Acknowledgements
Many thanks to Lileia Diotaiuti and Michael A. Miles for their
erudite comments on the manuscript and to the referees for their
constructive criticism. We are also extremely grateful to Cleber
Galvo, Dayse da Silva-Rocha et al. of the Laboratrio Nacional e
Internacional de Referncia em Taxonomia de Triatomneos, Instituto Oswaldo Cruz, Rio de Janeiro for rearing the insects used in the
morphometric investigation. Many thanks to Roberto Salvatella for

J.S. Patterson et al. / Acta Tropica 110 (2009) 187199

his kind assistance in locating a picture of P. tupynambai. Part of this

work was funded by the Sir Halley Stewart Trust and the Welcome
Trust.
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