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Acta Tropica 110 (2009) 187199

Contents lists available at ScienceDirect

Acta Tropica

journa l homepage: www.e lsev ier .com/ locate /ac ta t ropica

n the genus Panstrongylus Berg 1879: Evolution, ecologynd epidemiological significance

ames S. Pattersona,b,1, Silvia E. Barbosac, M. Dora Feliciangelid,

Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UKSchool of Life Sciences, University of Sussex, Brighton, East Sussex BN1 9QG, UKLaboratrio de Triatomneos e Epidemiologia da Doenca de Chagas, Centro de Pesquisa Ren Rachou-FIOCRUZ, Av. Augusto de Lima, Barro Preto,715, 30190-002 Belo Horizonte, Minas Gerais, BrazilInstituto de Investigaciones Biomdicas, Universidad de Carabobo (CNRFV-BIOMED) Apartado 4873, Venezuela

r t i c l e i n f o

rticle history:eceived 14 April 2008eceived in revised form 7 August 2008ccepted 1 September 2008vailable online 20 September 2008

eywords:anstrongylushagas diseasehylogenyeographical distributioncologyiologyedical 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 trans-mission of Trypanosoma cruzi to humans in South and Central America. Some species exhibit minormorphological differences possibly associated with adaptation to different silvatic ecotopes or domes-tic environments. We present a distillation of past and recent literature pertaining to the biology ofthis group. In particular, we summarise the current status of the genus according to systematic andrecent phylogenetic studies. In light of recent evidence suggesting polyphyly/paraphyly of the genuswe have investigated the possible mechanisms of morphological convergence/divergence. By assessingpostembryonic ontogeny we reveal that the distinctive head shape of Panstrongylus can be derived froma Triatoma-like head late in development. A comprehensive phylogenetic study is therefore required toelucidate their relationshipwith Triatoma spp., and other genera of the tribe Triatomini.We also present acomparative summary of biology, ecology and epidemiological significance 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]), impor-tant vectors of Chagas disease in Brazil and Peru, the majority are sylvatic species, associated with a widevariety 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 inthe genus (P. geniculatus, P. rufotuberculatus, P. lutzi, P. chinai), while others are opportunistic species (e.g.P. lignarius in the Amazon basin flying 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 thegenus Panstrongylus requires some focus on investigating the natural ecology of these species. This knowl-edge would add to our understanding of their evolutionary potential and may assist in predicting new

, for w

omp

epidemiological scenarios

. Introduction

Following the comprehensive revision of the subfamily Triatom-

nae (Hemiptera: Reduviidae) by Lent and Wygodzinsky (1979),hree publications in the last decade (Carcavallo et al., 1997a;ujardin et al., 2002; Galvo et al., 2003) have provided usefulpdates and compendia on the scientific investigation of this group

Corresponding author. Tel.: +58 243 242 58 22.E-mail addresses: mdora@movistar.net.ve, spinicrassa@yahoo.com

M.D. Feliciangeli).1 Current address: South African National Bioinformatics Institute, University of

he Western Cape, Private Bag X17, Bellville 7535, South Africa.

tptttts

pri

001-706X/$ see front matter 2008 Elsevier B.V. All rights reserved.oi:10.1016/j.actatropica.2008.09.008hich new control strategies need to be devised. 2008 Elsevier B.V. All rights reserved.

f insects. Triatomine bugs are responsible for the most commonode of transmission of Trypanosoma cruzi (Kinetoplastida: Try-anosomatidae), the etiological agent of Chagas disease, endemichroughout Latin America where an estimated 810 million peo-le have Chagas Disease (OPS, 2006; Remme et al., 2006). Effortso control Chagas disease have been successful in several coun-ries. However, this goal has not been wholly achieved. One ofhe possible factors that holds back progress towards interruptingransmission in many areas, is triatomine species considered to be

econdary or occasional vectors.

In this review we have comprehensively gathered informationublished on the genus Panstrongylus. This group of species cur-ently deserves special attention, as several appear to be involvedn a process of domiciliation. This trend poses new complex epi-

http://www.sciencedirect.com/science/journal/0001706Xhttp://www.elsevier.com/locate/actatropicamailto:mdora@movistar.net.vemailto:spinicrassa@yahoo.comdx.doi.org/10.1016/j.actatropica.2008.09.008

1 Tropica 110 (2009) 187199

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

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

2. Panstrongylus diasi Pinto and Lent, 1946

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

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

5. Panstrongylus howardi (Neiva, 1911)Triatoma howardi Neiva, 1911

6. Panstrongylus humeralis (Usinger, 1939)7. Panstrongylus lenti Galvo and Palma, 1968

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

9. Panstrongylus lutzi (Neiva and Pinto, 1923)Triatoma lutzi Neiva and Pinto, 1923Panstrongylus sherlocki Jurberg, Carcavallo and Lent, 2001 (cf.

Barbosa et al., 2005)

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

11. Panstrongylus mitarakaensis Brenger and Blanchet (2007)

12. Panstrongylus rufotuberculatus (Champion, 1899)Lamus rufotuberculatus Champion, 1899Triatoma rufotuberculata Neiva, 1914Triatoma coxo-rufra Campos, 1932

1

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88 J.S. Patterson et al. / Acta

emiological settings and new challenges for the control of Chagasisease in the Americas (Schofield et al., 1999).

. Systematics and phylogeny

Currently there are 140 species within the subfamily Triatomi-ae, arranged in 6 tribes and19genera. Galvo (2003) discussed theontroversies in the application of different concepts and new toolsor the classification of this subfamily (see also in this issue). Heree update the list of Panstrongylus species and summarise the cur-ent status of the genus in terms of phylogenetics and systematics.e go on to present somenewdata exploring the processes ofmor-hological evolution as evidence for a close relationship between ateast some Panstrongylus and Triatoma, and demonstrate a possibleoute to morphological convergence.

ThegenusPanstrongylusBerg, 1879 isgroupedwithTriatomaandother genera within the Tribe Triatomini. It was established withhe description of the type species; P. guentheri Berg 1879, havingormerly been described as the genus Lamus Stal 1859 within theamily Pentatomidae. After Triatoma and Rhodnius, Panstrongylus ishe third most speciose genus of the Triatominae subfamily. It isresently composed of 13 species with a wide geographical distri-ution throughout the Neotropical region, extending from Mexicoo Argentina (Curto de Casas et al., 1999) (Table 1, Fig. 1).

The most recently described species, P. mitarakaensis, was dis-overed in French Guiana last year and by our assessment looks toe closely related to P. geniculatus, rather than P. lignarius as sug-ested by the authors. In recent literature (Marcilla et al., 2002;rossa et al., 2002; Galvo et al., 2003; dos Santos et al., 2003) P.erreri and P. lignarius have been synonymised on the basis of iden-ity at the level of ITS-2 rDNA sequences (Marcilla et al., 2002) andytogenetic similarity (Crossa et al., 2002). As for other close rela-ionships, two species; P. chinai and P. sherlocki have been recentlyther species on the basis that they may only represent melanicorms of P. howardi and P. lutzi respectively. In the case of sher-ocki/lutzi, evidence for conspecificity was shown by Barbosa et al.2005). They studiedP. lutzi captured inMinasGerais and found thatt may show intraspecific variations in its phallic structures com-atible with the description of P. sherlocki (Jurberg et al., 2001). Theelationship between P. chinai and P. howardi remains to be eluci-ated, and subsequently, for the time being, both are counted as aalid species.

.1. Intrageneric relationships

Intrageneric relationships among specieswere explored by Lentnd Wygodzinsky (1979) by constructing a dendrogram based on1 character states (Fig. 2). The species groupings suggested by thisentatively cladistic treatment more or less correlate with patternsf geographical distribution, giving northern and southern cladesFig. 2), and are on the whole supported by molecular and cytoge-etic studies. Only the placement of P. megistus is discordant, in soar that it is largely southern in its distribution and is unusual cyto-enetically, having only 18 autosomal chromosomes compared tohe 20 autosomes of other Panstrongylus (andmost other Triatomi-ae) so far analysed (Crossa et al., 2002). Similar species groupingsor the genus were also reported by Lent and Jurberg (1975) onhe basis of a comparative analysis of male and female genitalia,nd tentatively by traditional morphometrics of head shape (dosantos et al., 2003)..2. Intergeneric relationships and paraphyly

Molecular genetic studies conducted fairly recently (Marcillat al., 2002; Hypsa et al., 2002) have addressed intergeneric

Pi(mt

Mestor rufotuberculatus Usinger, 1939

3. Panstrongylus tupynambai Lent, 1942

elationships and suggest that the genus may in fact representpolyphyletic assemblage of converged species. Hypsa et al.

2002) were more reserved in their inferences. Notwithstanding,hey demonstrate paraphyly in their analysis, showing a closeelationship between P. herreri/lignarius and the Caribbean Neso-riatoma (formerly Triatoma flavida and relatives) and between. megistus and T. tibiamaculata (the latter two species hav-

ng, to some extent, overlapping distributions). Marcilla et al.2002) clearly show that North American Triatoma lineages areore closely related to northern Panstrongylus spp. (in par-

icular 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 institutionwhere held (as applicable andwhere known), for each specimenshown, 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 deJaneiro, Brazil; LSHTM=London School of Hygiene and Tropical Medicine, UK; NHM=Natural History Museum London, UK. Attributions: * J.S. Patterson C. Galvo J.M.B

Tcclot

2

renger and B. Blanchet (2007) Y. Basmadjin. # S.E. Barbosa.

riatoma. These studies lack representatives of the southern

lade Panstrongylus species, and there is now a clear need toonduct a comprehensive phylogenetic analysis of Panstrongy-us with representatives of the various Triatoma lineages andther genera of the Triatomini to elucidate the phylogeny ofhe tribe.

lrd

.3. Head shape convergenceIn light of molecular evidence suggesting that some Panstrongy-us share theirmost recent commonancestorswith certainTriatomaather than other Panstrongylus specieswehave scrutinised the tra-itionalmorphological trait that characterises thegenus: Thegenus

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

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ig. 2. Cladogramof hypothesised relationshipswithin the genus Panstrongylus. Redach with two states. Northern and Southern geographical distributions correspond

s traditionally thought tobemonophyletic, and isprimarilydefinedy autapomorphic characterisation of head patterning, specificallyhat the anteniferous tubercules are situated close to the anteriorargin of the eye (Lent and Wygodzinsky, 1979). A comprehen-ive morphometric comparison of head shape differences amonganstrongylus species (dos Santos et al., 2003) tentatively supportshe aforementioned division between the northern and southernpecies. To explore the suggestedparaphyly/polyphyly of the genus,rom themorphological perspective,wehave examined the relativeifferences in head shape between Triatoma and Panstrongylus.Other than having their antennae inserted close to their eyes,

anstrongylus heads are often considered to be relatively short. Fur-her to this, on inspection it seems that inmany cases Panstrongyluspecies have large eyes relative to their head size and overall body

ize (e.g. P. megistus and many of the northern clade species) inomparison to many other triatomines. A functional interpretations that large eyes with more numerous and/or larger ommatidiare considered to be an adaptation to dim illumination (Bauert al., 1998; Olof Bjrn, 2002). When considered in the context

t(sPi

ig. 3. Comparative proportions of head shape between (a) Triatoma (T. vitticeps) and (broportions i and iii are similar across a and b, whereas proportion ii differs between a anrom Lent andWygodzinsky (1979). Constructed using 21morphological characters,nably well with the two main clades, with the exception of P. megistus**.

f the common general ecological specialisation of Panstrongyluspecies, i.e. terrestrial, arboreal, and subterranean habitats (albeithat details of specific habitats are scant formany species), it seemseasonable to assign large relative eye size as an adaptation tohe dim illumination associated with such habitats. A corollaryf this is that relatively large eye size, and restricted head lengthould account for a shorter distance between eye and antennalnsertion. From this perspective the character can be consideredpossible homoplasy contributing to morphological convergencemong some Panstrongylus with large eyes to those with smallerelative eye size (northern and southern species groups). Inomparison to Triatoma (characterised as having their antennaenserted intermediately between anterior edge of eye and ante-lypeus) an enlargement of eye size without otherwise modifying

he head plan could result in a Panstrongylus-like head (Fig. 3a)see Schofield and Galvo this issue, where they comment on theimilarity between certain North American Triatoma species andanstrongylus head configuration). Conversely, we can imagine thatf certain Panstrongylus species had smaller eyes, their headswould

) Panstrongylus (P. megistus). Images are scaled to the same length revealing thatd b in relation to the relative eye size (e).

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ave a more Triatoma-like appearance (Fig. 3b). Indeed, duringevelopment, nymphs of Panstrongylus have proportionately smalleveloping eyes and consequently their heads are Triatoma-like.Credence of a link between eye size, relative head shape and

cology can be found in observed patterns of natural variation:t has been recorded that two widely dispersed species P. rufotu-erculatus and P. geniculatus demonstrate notable morphologicalariation across their ranges, including some clear reductions inye size (Lent and Wygodzinsky, 1979; dos Santos et al., 2003).n illustration of such an example for P. rufotuberculatus (Lent andygodzinsky, 1979) does indeed show that the small eyed formas a more Triatoma-like head shape.

.4. Comparative ontogeny of head shape

Working on the hypothesis that in some cases if not all,anstrongylus species have arisen from lineages with Triatoma-ike heads by adaptation to a common ecology, we conducted areliminary analysis of comparative head shape changes duringevelopment (ontogeny). We conducted a geometric morphome-ric analysis of post-embryonic head shape changes through theve nymphal stages and compared them to adult head shape (seeocha et al., 2005 for details of methodology). We used specimensf P. megistus in comparison to two Triatoma species (T. lecticulariand T. infestans) and included Rhodnius prolixus as an outgroup. Allpecimens were laboratory reared under common conditions and0 specimens of each of the five stadia and each sex of adults were

ncluded.

Geometric morphometry was conducted as follows: The dorsalurface of the heads were imaged by microscopy and digital pho-ography and digitised to acquire a suite of seven landmarks (seeig. 4). Procrustes superimposition algorithmswere used to extract

astmf

ig. 4. Comparative geometric morphometric investigation of head shape ontogeny. The p. infestans, R. prolixus and P. megistus. Procrustes superimposition was used to extract isoottom left shows the set of landmarks recorded from each specimen). Subsequently, prinifferences among all specimens. This gave the two axis used in the plot (PC1 and PC2). End female (10 specimens per stage, i.e. 70 specimens per species). Lines are draw to fit thre enclosed by ellipses). Transformation grids correspond to the shape changes associateca 110 (2009) 187199 191

sometry-free shape variables from the two dimensional landmarkonfigurations. Subsequently, multivariate statistics, i.e. principalomponent (PC) analysis was used to extract themain componentsf shape differences among all specimens. The first two principalomponents cumulatively account for 92.8% of the shape varia-ion (PC1 72.2% and PC2 20.6%). A plot of these two axes (Fig. 4)learly shows an overlap in head shape among Triatoma nymphsT. lecticularia in particular) and P. megistus nymphs. Notably, the P.egistus ontogenetic trajectory is remarkably discontinuous com-ared to the other species, with all P. megistus nymphs occupyingsimilar area of the shape space. The huge jump from juvenile

o adult head shape is attributable to PC2 and relates primarily tohe relative enlargement of the eyes (Fig. 4). This reinforces ourssertion above that the Panstrongylus-like head is derived fromTriatoma-like head plan and demonstrates that it is derived byodification in late post-embryonic development. All the species

ncluded in the analysis can be seen to do this to a certain extent,hich accounts for the clear distinction in head shape betweenymphs and adults intraspecifically (Fig. 4). Invoking Gould (1977),e postulated that amongK-strategistsmacroevolutionary changesccur by one of two heterochronic (change of timing) events: eithery hypermorphosis: extended differentiation and an increase inpecialised complexity accompanying delayed maturation; or byeoteny; delayedmaturation linked to retarded differentiation andetention of flexible juvenile morphology. It is the latter that Gouldtates as being less common but with greater macroevolutionaryotential. Applying this, it seems that in our analysis of ontogenic

llometry all the species includedexhibit adegreeofhypermorpho-is; with specialised head shapes as adults with long trajectorieshrough the shape space. In addition to this, we observe that P.egistus, in comparison to the other species varies little along PC1

rom 1st instar to adult, and in this respect seems to be relatively

lot shows shape differences among nymphs and adults of four species T. lecticulariametry-free shape variables from two dimensional landmark configurations (imagecipal component (PC) analysis was used to extract the main components of shapeach data point represents a single specimen from samples of instars 15 plus malee ontogenic trajectories from 1st instars to adults (adult specimens of each speciesd with the extremes of the principal component axes, as indicated by dashed lines.

192J.S.Patterson

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

Species Distributiona Life cycleb (d =days) Natural infection byTrypanosoma cruzi

Feeding sourcesc Ecology and evolution

Panstrongylus chinai (Del Ponte,1929)

Venezuela, Ecuador, Peru 236 d at 29 C; 70% RH (Guillnet al., 1991)

(Arrarte Ovalle, 1955) Wild sources unknown.Chickens and domesticmammals

Tropical and subtropical forestsand dry forest (Curto de Casaset al., 1999)

(Herrer, 1955) Wild habitats in Peru (Vasquez,2005; Vargas, 2005) and SEEcuador (Abad-Franch et al.,2001)

(Daz-Limay et al., 2004) (allrecords from Peru)

Peridomestic ecotopes (goatpens; chicken coops) and stonebuilt structures, occasionallydomestic (Vasquez, 2005;Abad-Franch et al., 2001;Cceres et al., 2002; Grijalva etal., 2005)

Panstrongylus diasi Pinto &Lent, 1946

Bolivia, Brazil No data No data Wild sources unknown.Domestic animals (?) humans

Forest species; adult specimenshave been found in humandwellings (Silveira, 2000;Oliveira and Silva, 2007)

Panstrongylus geniculatus(Latreille, 1811)

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

(Chagas, 1912 in Brazil, Silvrieet al., 1964) in French Guiana,Omah-Maharaj, 1992 inTrinidad (42.5%)

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

Tropical dry or very dry forestand savannah to humid tropicalforest (Carcavallo et al., 1999)

531 d (Lent and Jurberg, 1969);1st instar nymphs to adults:269297 d (Galndez, 1990);274.8 d (Cabello and Galndez,1998)

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, sometimescaptured in domestic ecotopesin Argentina, Brazil, Colombia,Ecuador, French Guyana,Venezuela and Peru

Humans (60.2%), domesticanimals (52.27) rats (3.8%);chickens (1.4%) (Carrasco et al.,2005)

Incipient domesticationobserved in Colombia (Wolffand Castillo, 2000) andVenezuela (Feliciangeli et al.,2004; Carrasco et al., 2005)

Panstrongylus guentheri Berg,1879

Bolivia, Paraguay, Uruguay,Argentina, Brazil (Almeida etal., 2008)

264 d (Carcavallo et al., 1994) Mazza and Reyes Oribe (1939)in Argentina

Marsupials, rodents, birds.Possibly edentates

Savannahs, dry tropical andsubtropical xerophytic forestsas well as semi-arid plains andplateau. (Curto de Casas et al.,1999)Wild species, with adultsseldom found in dwellings, butit does not establish colonies

Panstrongylus howardi (Neiva,1911)

Ecuador No data Len (1962) Wild sources unknown.Possibly domestic animals orhumans

Unknown ecology, adultsseldom found in dwellings.Few records of presence inartificial habitats, Defran(1982) reported finding a smallperidomestic colony.Abad-Franch et al. (2001)found specimens indoors

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193

Panstrongylus humeralis(Usinger, 1939)

Panama, Colombia (Guhl, 1999) 149.4151 days (Turner andSousa, 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

Panstrongylus lenti Galvo andPalma, 1968

Brazil No data No data Unknown The only adults found wereinside dwellings (Barata et al.,1997)

Panstrongylus lignarius (Walker,1873)=Panstrongylus herreriWygodzinsky, 1948

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

165 d (2530 C) (Silva andSilva, 1991)

Lumbreras Cruz et al. (1955) (inPeru)

Marsupials, spiny rats,anteaters, bats, toucans,chickens, rabbits, pigeons

Tropical and subtropical forestsas well as tropical andsubtropical dry forests (Curtode Casas et al., 1999). Domesticand peridomestic in Peru (CubaCuba et al., 2002), Silvatic inthe Amazon basin

1st instar nymphs to adults:173 days at 25 C and 155 at30 C (Canale et al., 1999)

Deane and Damasceno (1949),Teixeira et al. (2001) (27%) bothin Brazil; Guhl et al. (2007) inColombia

Guinea pigs, domestic animals,humans

(Teixeira et al., 2001; Guhl etal., 2007)

Panstrongylus lutzi (Neiva andPinto, 1923)

Brazil 1st instar nymphs to adults:664 days (Dias, 1955)

Silveira et al. (1984), Garca etal. (2005, 1%-5%), Caranha et al.(2006, 29.1%). All data fromBrazil, 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 andWygodzinsky, 1979, Carcavalloet al., 1999) and native toregions of caatinga. Speciesmainly wild; peridomestic anddomestic colonies found inCear, 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 Barbosaet al. (2001)

Chagas (1909), Steindel et al.,1994: 55.3% in Santa Catarina;Litvoc 1990: 44.0% in SoPaulo; Koop, 2002: 32.0% inParan; Pinho et al., 2000: 3.6%in Rio Grande do Sul; Silva etal., 2006: 5.3% in Gois (1990s);Oliveira and Silva (2007): 0.49%in Gois (20022003)

Humans, birds opossumrodents, dogs, bats (Barretto,1968)

In Brazil the distribution of P.megistus coincides with theoriginal Atlantic Forest and itsremnants, now included in thedryer regions of caatinga andcerrado (Forattini, 1980;Barbosa et al., 2001, 2003)

Humans (80.8%) from insectscaught indoors in Bahia(Minter, 1975)

Species found in sylvatic andartificial ecotopes withfrequent domestic colonies(Silveira, 2000, WHO, 2002)

Opossums (62.9%) in StaCatarina Island (Steindel et al.,1994)

Panstrongylus mitarakaensisBrenger and Blanchet(2007)

French Guiana (Brenger andBlanchet, 2007)

No data Brenger and Blanchet (2007) Unknown Unknown

Panstrongylus rufotuberculatus(Champion, 1899)

Mexico,Costa Rica, Panama,Colombia, Venezuela, Ecuador,Peru, Bolvia, Brazil, Argentina

138.8251.42 d (242 C;RH=944%) (Wolff et al.(2004)

Lent and Pifano, 1940: inVenezuela. Len and Len,1953): Lazo, 1985: 14.% inEcuador, 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 andsubtropical forest (Curto deCasas et al., 1999)

194 J.S. Patterson et al. / Acta TropiTa

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ca 110 (2009) 187199

eotenic. In turn, this retention of flexible juvenile morphologyay be the factor that has allowed P. megistus, and perhaps otheranstrongylus to accommodate an enlargement in eye size. Thisegion of the shape space also coincides with the other juvenileriatoma and may represent the ancestral head shape of the tribe.

. Geographical distribution, ecology and behaviour

A large amount of information on the geographical distributionnd ecology of triatomine bugs is available in the literature. Weave summarised the essential data in Table 2 (mainly extractedrom Lent and Wygodzinsky (1979), Dujardin et al. (2002), Galvot al. (2003), Carcavallo et al. (1997a), Curto de Casas et al. (1999),arata et al. (1997) and Almeida et al. (2008). In the original papersore detailed information (e.g. distribution by State in each coun-

ry, description of habitats and microhabitats, etc.) can be found.ata published after the references cited above have been addednd additional comments are in the text.Among the 13 species of the genus, P. geniculatus has the widest

istribution, being currently known in 18 Latin American coun-ries, fromMexico to Argentina, including several of the Caribbeanslands. It is followedbyP. rufotuberculatus,which also extends fromentral to South America occupying 10 countries. The third mostidely dispersed species is P. lignarius found in 7 scattered Southmerican countries, while P. megistuss geographical distribution isainly restricted to eastern South America. The remaining speciesave more limited or undefined distributions and, as we will see,ess ecological data are available, with several species completelynigmatic. However, although some Panstrongylus species, such as. megistus, can be found in palm crowns, all species are predomi-antly associatedwith terrestrial burrows, tree root cavities and/orrboreal tree holes (Gaunt andMiles, 2000). Based on its ecologicalharacteristics, P. geniculatus has been considered an eurythermicpecies, adapted to several dry as well as humid ecotopes where its found in a great variety of sylvatic habitats including the burrowsr resting places of armadillos, opossums, rodents, bats and birds,s well as hollow trees or under bark, in bromeliads and amonghe fronds of various species of palm (Carcavallo et al., 1998a). Thispecies is frequently captured inperidomestic environments and itsccurrence inside houses has been cited in several countries. Sea-onal domiciliation of P. geniculatus with pigs has been reportedn the Amazon Basin (Valente et al., 1998), who also stressed theotential for domiciliation of this species in Maraj Island, State ofar, Brazil (Valente, 1999). Evidence for the domiciliation of thispecies inAmalfi, Colombia, has been reportedbyWolff andCastillo2000) who demonstrated that domestic invasion by P. geniculatusoes not seem to be exclusively due to attraction to electric light,swas commonly accepted previously.We observedmixed domes-ic infestation of nymphs of P. geniculatus and Rhodnius prolixus in aural area ofVenezuelawhich also ledus to suspect apossible incip-ent process of domiciliation (Feliciangeli et al., 2004). Domestic P.eniculatus has also been caught repeatedly by the inhabitants ofaracas, Venezuela in their dwellings. This led us to investigate theotential role of these bugs as vectors of Chagas disease in an urbanetting (Carrasco et al., 2005) (see Section 5).

Panstrongylus rufotuberculatus is generally considered to be aylvatic species ranging from Mexico to Argentina. It has beenound in palms, hollow trees and the refuges of wild mammalsLent andWygodzinsky, 1979;DAlessandro et al., 1981;Miles et al.,

981). Adult insects frequently invade human dwellings, attractedy electric light (Lent and Wygodzinsky, 1979; Salomn et al.,999). However, the presence of stable domestic colonies has beeneported recently in 2/15 houses in the region of Piura, Peru (Marnt al., 2007). This species tends to be more abundant during the

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rst 6 months of the year (dry season and onset of rainy season)lthough it is easily found throughout the year (Zelednet al., 2001;olff and Castillo, 2002). Based on records of diffuse distribution

n Venezuela, Guyana, Suriname, Brazil, Colombia and Ecuador, P.ignariuswas previously considered to be mainly a sylvatic species.t has been found in palms, birds nests and Didelphis nests, rodenturrows, toucan nests and hollow trees (Carcavallo et al., 1998a).he unique record of P. lignarius in Venezuelawas a female found inpalm (Otero et al., 1975). Gaunt andMiles (2000) observed that inhe Amazon basin in Brazil, adults move freely over the trees pro-ected by their coloration that matches beautifully the bark, whileymphs lacking this exquisite camouflage, rest in tree holes. In themazonbasin in Ecuador P. lignariuswas found in adwelling (Abad-ranchet al., 2001) and it hadoccasionallybeen reported indoors, orn chicken coops, sometimes attracted by light, in Brazil andColom-ia (DeaneandDamasceno, 1949;Miles et al., 1981;DAlessandroetl., 1984; Guhl et al., 2007). However, P. lignarius domestic popula-ions in Peru (formerly P. herreri) show strong synanthropic habitsnown in Peru since 1948, where its phototropism has also beenepeatedly observed (Herrer, 1960; Caldern et al., 1985).

Panstrongylus megistus is a triatomine with a wide geographicalistribution, ecological valence and great potential of colonisationf the artificial ecotopes. According to Forattini (1980), in tropicaltlantic region, this species is associated with habitats charac-erised by high levels of humidity. However, except those of themazon, P. megistus occurs in all types of Brazilian forests whichnclude dry and moist humid forest in the cerrado and caatinga.he occurrence of P. megistus in the dryer regions of the cerradothe Brazilian savanna) has been reported by Barretto (1979) andherlock (1979). It was found in palm crowns, other trees, rodentnd marsupials shelters, terrestrial burrows and hollow trees withats. Miles et al. (1982) reported occurrences in arboreal tree holesith Didelphis in Rio de Janeiro Brazil. However, the species issually associated with humid forests, from which adults invadeouses (Forattini et al., 1977), especially during the rainy seasonDias and Dias, 1968). P. megistus may have begun to invade theomestic environment during the post-colonial period; followinghe destruction of its natural habitat and consequent agriculturalevelopments, this species presumably invaded and adapted toxploit domestic environments (Litvoc et al., 1990).Barbosa et al. (2006) observed great diversity in populations of

. megistus, this was considered in the context of paleovegetationeconstruction. The local paleovegetation record shows a clear pro-ess of expansion and retraction of humid forest during the last18,000 years, and can account for the observed fragmented pop-lation structure. The autochthonous status of P. megistus in theerrado is reinforced by control program data that shows the rein-asion of houses after control with insecticide, with bugs thoughto be originating from silvatic foci.

In other countries (Bolivia, Paraguay, Uruguay, Argentina) P.egistus is almost entirely sylvatic (Salvatella, 1986a; CarpinteirondViana, 2008), and on the occasionswhen it is found in domesticabitats it is usually associatedwith synanthropics hosts, especiallypossums (Steindel et al., 1994).The ecology of P. chinai is known mainly from Peru (Vargas,

005; Vasquez, 2005), where adults have been occasionallyeported in houses, with similar observations in Ecuador (Abad-ranch et al., 2001; Grijalva et al., 2005) (Table 2), but not fromenezuela where it was reported only from the locality El CarrizalMrida State) as P. turpiali (Valderrama et al., 1996) (cf. Lent, 1997).Although frequently collected in artificial environments inrazil, the wild habitats of P. diasi remain unknown as well asspects of its biology, ecology and genetics; P. humeralis waseported in Colombia by Guhl (1999) and it constituted 0.5% ofriatomines caught in the eastern region of this country (Angulo,

acatm

ca 110 (2009) 187199 195

000). The incipient process of colonisation by P. lutzi was firstoted in 1984 by Silveira. The few reports of this species fromild ecotopes refer to nymphs and adults in armadillo burrows

Dias-Lima et al., 2003) and adult females under the bark of pauranco (Auxemma oncocalyx) trees (Garcia et al., 2005). Althought remains a predominantly wild species, its presence in peri- andntradomestic habitats is currently being noted with increasingrequency (Vinhaes and Dias, 2000; Freitas et al., 2004; Garciat al., 2005). Colonies have also been observed in the Braziliantate of Cear where an infestation rate of 4.6% was reported byarcia et al. (2005). Panstrongylus tupynambai is strictly sylvatic,nhabiting rupestrian and subterranean ecotopes, such as rockpilesemi-buried in humid soil, as well as rodent and reptile burrowsSalvatella, 1986a,b; Martins et al., 2006).

To conclude, from the knowledge so far available, according tourto de Casas et al. (1999), excluding P. lenti, P. mitarakaensis and. sherlocki (amelanic specimen of P. lutzi) (because only one or twopecimens have been caught of each), based on Holdriges climatearameters, of the Panstrongylus genus, P. geniculatus occupies theidest range of life zones; very dry forests or savannahs, dry, wet,oist and rainy forests; P. rufotuberculatus and P. megistus inhabitsry, wet and moist forests; P. howardi and P. humeralis are found inet forest; P. lutzi seems to be restricted to moist forest; P. lignar-

us is found in wet as well as in dry habitats; P. chinai occupiesesert, desertic brushwood or steppe and thorny brushwood; P.iasi is found in desertic brushwood or steppe and thorny brush-oods; P. guentheri and P. tupynambai are found in very dry forestsr savannah and thorny brushwood.In relation to the synanthropichabits of these species,P.megistus

n Brazil is one of the main domiciliated species along with P. lig-arius domestic populations (formerly P. herreri) in northern Peru;. geniculatus, P. lutzi and P. rufotuberculatus are all able to developeridomestic and domestic colonies in certain areas, while P. chi-ai, P. diasi, P. guentheri, P. howardi, P. humeralis, and P. tupynambaire wild species with occasional records of specimens in humanwellings.

. Biology

There is relatively little information on the biology of theanstrongylus species. Historically, little attention has been paido these species because the majority of them are sylvatic andherefore often regarded solely as a potential threat, not typi-ally involved in human transmission. In Table 2 we report thevailable data on the life cycles of 9 species. There is the obviousaveat that different geographical origins, different laboratory con-itions, feeding sources and rhythms of feeding may undermineny inferences made from any comparison of life cycles. Despitehis, measurements of life cycles, as well as population parametersnd demographic strategies, constitute useful biological informa-ion, which might assist in estimating the potential a species hasor colonisation and also their vector potential.

. Medical importance

We have already reported on and discussed several factors,hich may predispose triatomine species to be potential vectors;uch as geographical distribution, capacity for establishing peri-nd domestic colonies, frequency of invading domestic ecotopes,

daptability to different habitats and hosts, and finally biologicalharacteristics. In this section we will focus on other variables thatre more strictly related to the parasitevector relationship andhe vectorhuman contact, which are clearly the ultimate deter-inants for vectorial transmission of T. cruzi. The primary factor is

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96 J.S. Patterson et al. / Acta

he susceptibility of a triatomine species to T. cruzi, secondary ishe efficiency in the process of feeding in terms of T. cruzi trans-ission, i.e. a successful human-vector contact, and thirdly the

iming of defaecation of the bug during blood meal uptake whichould facilitate deposition of the parasite on or near the hostefore departing. These three parameters have been well studiedor domestic species, but have only been recorded for a few syl-atic species. Nevertheless, gathering all the available information,e have inferred the vector potential of each species in the genusanstrongylus.Natural infection with T. cruzi has been detected in 12 out of 13

anstrongylus species (see Table 2). High infection rates might ben indicator of close proximity to reservoir hosts and high suscep-ibility to T. cruzi, as seems to be the case for P.megistus in Brasil, P.ignarius in Peru and P. geniculatus in several countries. On the otherand, information on the source of blood-meals (Table 2) is of epi-emiological importance because it indicates potential reservoirsf T. cruzi and vectorhuman contact, revealing the presence of pos-ible synanthropic transmission cycles. Six species, P. megistus, P.eniculatus,P. lignarius,P. rufotuberculatus,P. lutzi, andP. tupynambaiuccessfully feed on humans (Table 2), while other species (P. diasi,. howardi) are strongly suspected to feed on humans (Carcavallo etl., 1998b).Panstrongylus megistus was the first species of triatomine to be

ncriminatedasavectorofChagas disease (Chagas, 1909) and itwasonsidered as the main domestic vector in Brazil until the decadef 1930 when it started to be progressively replaced by Triatomanfestans (Dias and Dias, 1968; Dias, 1982). Decreased infectionates for Brazil overall (3.50% for 197783 and 2.72% for 1997) wereeported during that period (Silveira and Vinhaes, 1998). However,ollowing the success of the southern cone Chagas disease controlrogramme that achieved the elimination of T. infestans in manyreas (Dias and Schofield, 1999), P. megistus initiated a new processf invasion and domiciliation in several states of Brazil. In 46/54unicipalities of Minas Gerais under epidemiological surveillanceetween 2000 and 2003, P. megistus was 94.1% of the total bugsaught, with a colonisation index of 32.3% and a rate of infection of.3% (Villelas et al., 2005). In Goias where 201 out of 246 munic-palities were infested by triatomine bugs, Triatoma sordida andhodnius neglectus predominated, but P. megistus was also caughtn the peridomestic as well in the domestic ecotopes (Oliveira andilva, 2007). Thus, P.megistus is currently considered to be themainutochthonous vector of Chagas disease in the central, eastern andoutheastern regions of Brazil.

Reported high incidence of P. geniculatus blood-fed on humansnd concomitantly infectedwith T. cruzi I (ZI) in Caracas, VenezuelaCarrasco et al., 2005), highlighted the epidemiological impor-ance of this species classically considered a visitor species, andn accidental human feeder. Wolff and Castillos study (2000)emonstrated that P. geniculatus defecates during feeding, suggest-ng that this species is likely to be a competent vector. Subsequentlyt was implicated in fatal cases of acute Chagas myocarditis innfants in Caracas (Losada et al., 2000). Further to this, a recentutbreak of infections occurred in Caracas, possibly via oral trans-ission, in aprimary school, November2007 (ProMED-mail, 2007).he ingestion of fruit juice accidentally contaminated by P. genic-latus, is thought to have been the cause. This highlights oralransmission as a possible emerging epidemiological scenario inenezuela.Infection by T. cruzi I (ZI) was also reported in P. geniculatusnfesting pigsties in the community Furo do Rio Grande in themazon Basin, where it was also isolated from the pigs and Didel-his marsupialis, although no human infections were registeredValente et al., 1998). Elsewhere (Amazonias and Rondonia States). geniculatus was frequently associated with the armadillo Dasy-

cGItm

ca 110 (2009) 187199

us novemcinctus, infesting its burrows and transmitting T. cruzi,ymodeme3 (Z3) (Povoa et al., 1984). This reveals that transmissionycles are possibly partitioned according to host and ecology. Fur-her studies along these lines are vital to elucidating the aetiologyf human infections.P. rufotuberculatus has been incriminated as a vector of Chagas

isease in Andean and coastal foci of Ecuador, with domestic pop-lations reported in Santo Domingo de los Colorados. The deathf a child from Chagas disease has been attributed to a bite fromhis species (Abad-Franch and Aguilar, 2003). In themunicipality ofmalfi in Antioquia, Colombia, the presence of P. rufotuberculatusthe second most common triatomine caught inside buildings) isonsidered to be a major epidemiological risk factor (Wolff et al.,001). Several characteristics that could be linked to high vectorialapacity were observed for this species, including longevity, rapidesponse to the presence of a host, large volume of blood ingestednd frequent defecation during the feeding process (Wolff et al.,004).The most strongly synanthropic species P. lignarius (formerly

. herreri) is considered the principal vector of Chagas disease iner (Cuba Cuba et al., 2002). It was the predominant species4721/5008 indoors and 534/559 in the peridomestic habitat) col-ected by active search in urban and rural areas in the departmentsf Cajamarcas and Amazonas, endemic for Chagas disease (Ccerest al., 2002). Transmission of sylvatic T. cruzi to humans has alsoeen associated with P. lignarius. In the Amazon basin this speciesas observed to fly from palm trees (Attalaea phalerata) to housesTeixeira et al., 2001). In Colombia, this species has been found inird nests and it is not considered of epidemiological importanceGuhl et al., 2007).

P. lutzi is one of the most important secondary vectors in Brazil.ogether with its great capacity for invading houses through flight,t showshigh ratesofnatural infectionwithT. cruzi,probably relatedo its intimate association with armadillos (Dias-Lima et al., 2003).hiswas confirmed by a study on its feeding sourceswhich showedhat P. lutzi appears to be an eclectic species that takes bloodmealsrom at least eight different hosts species (Caranha et al., 2006).. chinai probably acts as the vector of T. cruzi in sylvatic cycles inrid areas of north and eastern Peru (Vasquez, 2005) as well asn SE Ecuador (Abad-Franch and Aguilar, 2003). Finally, P. howardis considered to be as potential vector of T. cruzi in the coastalegion of Ecuador (Abad-Franch and Aguilar, 2003). The remain-ng Panstrongylus species; P. diasi, P. guenteri, P. humeralis, P. lenti, P.itarakaensis and P. tupynambai have not so far been incriminateds vectors of T. cruzi to humans but are most probably involved inylvatic T. cruzi cycles.

To conclude, we have demonstrated here that there is a cleareed to know more about the genus Panstrongylus, from a phy-ogenetic/evolutionary point of view, and in regard to ecology,iogeographyandvectorhosts/parasite interactions. Research intohese areas would shed more light on the complex and changingpidemiological settings of Chagas disease in the Americas, withhe aim of achieving further progress in reducing the burden ofhis neglected disease.

cknowledgements

Many thanks to Lileia Diotaiuti and Michael A. Miles for theirrudite comments on the manuscript and to the referees for their

onstructive criticism. We are also extremely grateful to Cleberalvo, Dayse da Silva-Rocha et al. of the Laboratrio Nacional enternacional de Referncia em Taxonomia de Triatomneos, Insti-uto Oswaldo Cruz, Rio de Janeiro for rearing the insects used in theorphometric investigation. Many thanks to Roberto Salvatella for

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is kind assistance in locating a picture of P. tupynambai. Part of thisork was funded by the Sir Halley Stewart Trust and the Welcomerust.

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On the genus Panstrongylus Berg 1879: Evolution, ecology and epidemiological significanceIntroductionSystematics and phylogenyIntrageneric relationshipsIntergeneric relationships and paraphylyHead shape convergenceComparative ontogeny of head shape

Geographical distribution, ecology and behaviourBiologyMedical importanceAcknowledgementsReferences