Biology, ecology, and systematics of Triatominae (Heteroptera, Reduviidae), vectors of Chagas disease, and implications for human health

2006·1.5 MB·English

by  Jurberg, Jose

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Biology, ecology, and systematics of
Triatominae (Heteroptera, Reduviidae),
vectors of Chagas disease,
and implications for human health1
J. JURBERG & C. GALVÃO
Abstract: The members of the subfamily Triatominae (Heteroptera, Reduviidae) are vectors of Try-
panosoma cruzi (CHAGAS1909), the causative agent of Chagas disease or American trypanosomiasis. As
important vectors, triatomine bugs have attracted ongoing attention, and, thus, various aspects of their
systematics, biology, ecology, biogeography, and evolution have been studied for decades. In the present
paper the authors summarize the current knowledge on the biology, ecology, and systematics of these
vectors and discuss the implications for human health.
Key words: Chagas disease, Hemiptera, Triatominae, Trypanosoma cruzi, vectors.
Historical background (DARWIN 1871; LENT & WYGODZINSKY
1979).
The first triatomine bug species was de-
scribed scientifically by Carl DE GEER American trypanosomiasis or Chagas
(1773), (Fig. 1), but according to LENT & disease was discovered in 1909 under curi-
WYGODZINSKY(1979), the first report on as- ous circumstances. In 1907, the Brazilian
pects and habits dated back to 1590, by physician Carlos Ribeiro Justiniano das
Reginaldo de Lizárraga. While travelling to Chagas (1879-1934) was sent by Oswaldo
inspect convents in Peru and Chile, this Cruz to Lassance, a small village in the state
priest noticed the presence of large of Minas Gerais, Brazil, to conduct an anti-
hematophagous insects that attacked at malaria campaign in the region where a rail-
night. In subsequent reports, various travel- way was being built. The young doctor (28
ers and naturalists also mentioned the pres- years old) stayed in the area for about one
ence of these insects in South America. One year, during which time a railroad engineer,
of the most celebrated reports was by Cantarino Mota, alerted him to the pres-
Charles Darwin, during his trip to South ence of hematophagous insects referred to
America on the H.M.S. Beagle in 1835, locally as “barbeiros“ (the local term for tri-
when he wrote: “One which I caught at atomines) (Fig. 2). Alerted to the presence
Iquique, (for they are found in Chile and of these insects inside the human dwellings,
Peru) was very empty. When placed on a the doctor decided to investigate the possi-
table, and though surrounded by people, if a bility that they might transmit some parasite
finger was presented, the bold insect would to humans, since besides malaria, he had de-
immediately protrude its sucker, make a tected clinical signs that were difficult to in-
charge, and if allowed, draw blood. No pain terpret. The local population complained
was caused by the wound. It was curious to about an uncomfortable feeling referred to
watch its body during the act of sucking, as as “baticum“ (a folk term for palpitation, lit-
in less than ten minutes it changed from be- erally meaning “drumming“ or “pounding“),
ing as flat as a wafer to a globular form...“ and Chagas observed arrhythmia and signs
Denisia 19, zugleich Kataloge
der OÖ. Landesmuseen
1This paper is dedicated to Ernst Heiss on the occasion of his 70thbirthday. Neue Serie 50 (2006), 1096–1116
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of heart failure among local residents, along For more than one century, since the
with reports of unexplained sudden death. first description by De Geer, triatomines
Upon dissecting the triatomines he found were studied merely from a descriptive point
flagellates in their intestinal tract. Believing of view. However, beginning in 1909, when
that they belonged to Trypanosoma mi- Chagas discovered the disease, and due its
nasense, which infected black tufted-ear newly acquired relevance to human health,
marmosets (Callithrix penicillata) in the same studies began on the clinical form of the dis-
region, he sent several triatomine specimens ease, the protozoan, and the vertebrate
to Oswaldo Cruz in Rio de Janeiro to feed hosts, as well as the vector biology and
on uninfected marmosets. Several weeks lat- transmission mechanisms. Advances in vec-
er he returned to Rio de Janeiro to discover tor taxonomy began with Arthur Neiva, one
a new trypanosome in the blood of one of of the most important scientists in this
the animals. As a tribute to his mentor he phase, who, in 1911, began describing vari-
named the species Trypanosoma cruzi. He ous species, culminating with the publica-
then returned to Minas Gerais to attempt to tion of his dissertation “Revisão do gênero
identify the parasite’s vertebrate host. After Triatoma Lap.“ in 1914. Important mono-
numerous negative blood samples, he found graphs were published subsequently by PIN-
an infected cat. Some 30 days later he re- TO (1925) and DEL PONTE (1930), in addi-
turned to the house where he had discov- tion to other extensive studies published by
ered the infected animal and found a little NEIVA & LENT (1936, 1941), USINGER
girl named Berenice, just two years old, who (1944), ABALOS & WYGODZINSKY (1951),
was febrile and presented circulating forms and RYCKMAN (1962), culminating in the
of T. cruziin her bloodstream. grand work by LENT & WYGODZISNKY
(1979).
From 1909 to 1912, Chagas described a
new disease, its causative agent, natural
Trypanosoma cruzi and Chagas disease
Fig. 1: Male of Triatoma rubrofasciata(DE reservoirs, and the vector, a fact unparal-
GEER1773),the first species described. leled in international medicine to this day Chagas disease or American trypanoso-
and a milestone in the history of medicine, miasis was primarily a zoonosis, a parasitic
since the discovery was made in the inverse disease of wild animals transmitted by syl-
order as compared to the usual (where the vatic species of triatomine bugs. The adap-
discovery of a disease generally precedes tation of some triatomine species to human
that of its causative agent). As a result of his dwellings was secondary, as was the para-
work, in 1912 Chagas received the site’s domiciliary cycle. American try-
Schaudinn Award from the Institute of panosomiasis is now an endemic disease af-
Tropical Diseases in Hamburg, Germany fecting mostly Latin America, primarily in
(CHAGAS FILHO 1968). Thus, one and the rural populations of Central and South
same researcher, in inverse order and in a America, where it is an important public
short space of time, discovered a new disease health problem. According to World Health
that would later bear his last name, first rec- Organization, an estimated 100 million peo-
ognizing the vector, next the parasite and ple are at risk of the disease, with 18 million
reservoirs, and finally the clinical disease in currently infected (DIAS & COURA 1997).
humans (CHAGAS1909). Chagas’ discovery Currently there is no vaccine or effective
was overlooked by the Brazilian scientific cure for chronic Chagas disease.
community, as represented by the National
Trypanosoma cruzi, the etiological agent
Academy of Medicine, and was treated with
of the disease, is a flagellate protozoan of the
disbelief for more than 20 years, because
order Kinetoplastida, family Trypanosomati-
some scientists questioned the very exist-
dae. It is some 20-thousandths of a millime-
ence of the disease. It was in Argentina in
ter in length and has an elongated body
1935 that Salvador Mazza submitted studies
with an undulating membrane allowing its
on the disease to the Annual Meeting of the
movement in the bloodstream.
Argentine Society of Tropical Medicine
and, together with Cecílio Romaña, gave a Unlike other diseases transmitted by
new dimension and credibility to the prob- hematophagous insects, in this case infec-
lem (CHAGASFILHO1968). tion does not occur through the insect’s sali-
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va. When the triatomine bug bites, it defe-
cates during or right after bloodsucking,
eliminating infective forms of the parasite in
its feces. These forms can penetrate actively
either through the bite’s orifice, the mucosa,
or small wounds and scratches on the skin.
Vector-borne transmission is the most im-
portant form of transmission, but it can also
take place through transfusion, transplacen-
tally, through organ transplants, accidental
ingestion of triatomines, laboratory acci-
dents, or even inadequate handling of in-
fected animal carcasses.
Animals infected with T. cruzi are al-
ways mammals, as the parasite cannot de-
velop in the blood of birds, reptiles, or am-
phibians. A triatomine bug that has sucked
the blood of a mammal (including a human)
infected with T. cruziacquires the infection
and the protozoan then reproduces, multi-
plying in the insect’s digestive tract and pro-
ducing the infective forms which are ex-
pelled in the feces. Infection remains in the
insect throughout its lifespan and can occur
both in the nymphs and adults. If the insect
sucks infected blood early in life (1st instar
nymph), it acquires the infection and will
remain infected throughout its life. Only
the eggs are not affected, so the second gen-
eration remains uninfected until its first in-
gestion of infected blood (i.e. there is no
transovarian transmission). Therefore tri-
atomine bugs reared in the laboratory with
blood from uninfected animals can be used
safely in experiments. After biting and suck-
ing the blood of humans or animals, the sa-
tiated triatomine bug defecates close to the There are three distinct phases in the Fig. 2: Panstrongylus megistus(BURMEISTER
1835), the triatomine species in which
site of the bite, and these feces can contain disease: acute, indeterminate, and chronic.
Chagas found Trypanosoma cruzi.
the infective form of T. cruzi. The parasites In the acute phase (3-4 weeks), the infec-
quickly penetrate into the bloodstream tion varies from an asymptomatic to a severe
through the triatomine’s bite, some minor and fatal form, the latter mainly in children
wound, or through the mucosa (of the eyes,
or debilitated individuals, characterized by
nose, or mouth). Upon entering the blood-
high fever, while other symptoms like diar-
stream the parasites are transported to the
rhea and vomiting can appear when the di-
muscles or organs (mainly the heart and di-
gestive tract is affected. The indeterminate
gestive tract), where they multiply and
phase is characterized by low parasitemia
cause lesions. Penetration of Trypanosoma
without clinical signs, which can persist or
cruzi through the skin can cause a local re-
evolve into a chronic disease. The chronic
action known as a chagoma, and another
form normally appears 10to 15 years after
important sign is unilateral bipalpebral
swelling, leaving the patient’s eye practical- the acute phase, and Chagasic cardiopathy
ly closed. This is the so-called Romaña’s is the most common manifestation, the di-
sign, named after its discoverer, an Argen- gestive form producing visceromegalies, es-
tine physician. pecially megaesophagus and megacolon.
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When they finish a meal their body
changes appearance, since the volume of
blood ingested is so great that the abdomen
dilates considerably, giving them a globose
appearance by stretching the intersegmental
and connexival membranes. Some species
may defecate while feeding, while others
defecate soon afterwards or even abandon
the food source and defecate far from the
sucking site. This fact characterizes the var-
ious species as either good or bad transmit-
ters of the disease, as the infective forms of
T. cruzi are expelled in the feces of the in-
fected bugs.
These insects generally suck the blood
of their victims at night, while they are
asleep. The bites generally occur on uncov-
ered parts of the body. That is why the pop-
ular name for the triatomine bug in Brazil is
“barbeiro“ (barbeiro being “barber“ in Por-
tuguese). The sleeping persons are unaware
of the bugs, because the bites are generally
painless due to the anesthetic and anti-clot-
ting action of the saliva. Cases of hypersen-
sitivity can occur, but are rare.
Triatomines are vector insects and para-
sites with slow development, whose life-cy-
cle can range from 3-4 months for Rhodnius
prolixusSTÅLup to two years for Panstrongy-
lus megistus (BURMEISTER). They live in pro-
tected environments, the resting places of
their hosts, which can be either sylvatic or
domestic animals or humans. Of the known
species, about a dozen are epidemiologically
important, since they have become domicil-
Fig. 3: Eggs, nymphs and female of
iated due to manmade disequilibria in na-
Panstrongylus megistus(BURMEISTER1835). Chagas disease vectors
ture (LENT& WYGODZINSKY1979).
Members of the Triatominae are
Triatominae external morphology.
hemimetabolous insects whose development
Most triatomine species can be identified on
from egg to adult includes five nymphal
the basis of their external morphology. The
stages (Fig. 3). They are obligatory
general appearance of triatomines is similar
hematophagous insects in all phases of their
to that of other reduviids, and the general
development. The amount of blood ingested
morphology is shown in Fig. 4. Detailed
varies according to the species as well as in
schemata of morphological traits were pub-
relation to the stage, and generally the 4th
lished by LENT& WYGODZINSKY(1979) and
and 5thinstar nymphs are the ones that feed
several scanning electron microscopy illus-
the most. In general most species are noc-
trations were provided by CARCAVALLO et
turnal, and during the day they remain in al. (1998/99). Adults differ from nymphs by
their resting places, although they may the presence of ocelli, and well-developed
sometimes go out to suck blood during the external genitalia and wings (with the ex-
day under adverse conditions. In colonies ception of two species of Mepraia, which dis-
reared in the laboratory, the bugs seek food play wing polymorphism – see JURBERGet al.
sources in broad daylight. 2002). Females have a appointed or trun-
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cate abdominal apex, while in males the
apex is rounded. Females are larger than
males, and the largest triatomine is Dipetalo-
gaster maxima (UHLER), which can reach 44
mm in length. The smallest species is Alber-
prosenia goyovargasi MARTÍNEZ & CARCAV-
ALLO, 5 mm long. The length of most
species usually varies from 20 to 28 mm. The
color pattern (Figs 5-10) varies, with an
overall black or piceous color and spotted
patterns of yellow, brown, orange, or red
(JURBERG et al. 2004). The morphology of
triatomine eggs and nymphs (Fig. 11) has
been the target of several studies, and a sum-
mary of these works was provided by
GALVÃOet al. (2005).
Systematics and current classification
Current classification of this subfamily
is based mainly on the revision by LENT &
WYGODZINSKY (1979), the most important
systematic work on this subfamily. Since
that revision there has been considerable
work, including the descriptions of several
new taxa, and therefore in the present paper
the authors provide a summary of the recent
classification updated from GALVÃO(2003),
GALVÃO et al. (2003) and FORERO et al. Fig. 4: Triatominae general external
(2004) (see Table 1). Although generally morphology.
recognized as a monophyletic subfamily of
the Reduviidae adapted to a blood-feeding
strategy (USINGER 1944; LENT & WYGO-
DZINSKY 1979; CLAYTON 1990; SCHUH &
SLATER 1995), the subfamily Triatominae
still has several serious phylogenetic ques-
tions in regard to its origin and evolution
(SCHAEFER 1998, 2003, 2005). SCHOFIELD
(1988) proposed a concept of polyphyletic
origin of the triatomines, and according to
his view the Asiatic fauna consists of at least
two independent lineages derived from dif-
ferent reduviid stocks. The first Asiatic lin-
eage consists of several species of Triatoma,
which had evolved from what was originally
the New World species Triatoma rubrofascia-
ta(DEGEER)after its introduction into the
Old World. The other lineage is represented
by the genus Linshcosteus, a supposedly au-
tochthonous Asiatic lineage of blood-feed-
ing reduviids. This view was supported by
GORLAet al. (1997) through morphometric
analysis, where all species of Linshcosteus
were shown to be unrelated to the species of
Triatoma recorded from the Old World. On Fig. 5: Color pattern of triatomine bugs: Rhodnius staliLENT, JURBERG& GALVÃO1993.
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Fig. 6: Color pattern of triatomine bugs:Triatoma rubrovaria(BLANCHARD
1843).
Fig. 8: Color pattern of triatomine bugs: Triatoma
dimidiata(LATREILLE1811).
Fig. 7: Color pattern of triatomine bugs: Triatoma sherlockiPAPA, JURBERG,
CARCAVALLO, CERQUEIRA& BARATA2002.
Fig. 9: Color pattern of triatomine bugs: Triatoma
infestans(KLUG1834).
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the other hand, molecular cladistic analysis Fig. 10: Color pattern of
triatomine bugs: Triatoma
of 57 species (HYPSAet al. 2002) showed the
nitidaUSINGER1939.
genus Linshcosteus and Triatoma rubrofasciata
as sister groups. The Linshcosteus-T. rubro-
fasciataclade nests firmly within Triatomini,
supporting a monophyletic origin of Tri-
atominae. According to SCHAEFER (2005)
the most important question about phyloge-
netic relationships of the Triatominae can
be divided in two parts: Is Triatominae actu-
ally a truly independent subfamily at all?
And, if Triatominae is a separate subfamily,
to which other reduviid subfamilies is Tri-
atominae closely related? Attempting to
solve this puzzle, several scientists have used
molecular data to infer phylogenetic rela-
tionships (GARCIA & POWELL 1998;
STOTHARD et al. 1998; LYMAN et al. 1999;
GARCIA1999; MARCILLAet al. 2002; SAINZ
et al. 2004). Unfortunately, most of these
papers are based on limited taxa sampling
and are hence unable to solve the questions
of the (entire) Triatomine subfamily phy-
logeny. A recently published paper (PAULA
et al. 2005) analyzes mitochondrial rDNA
sequences of several triatomine genera and
some representatives of other reduviid sub-
families. This analysis suggests that the Tri-
atominae itself and Rhodnius and Triatoma
genera are polyphyletic. Although this pa-
per is an important contribution, it must be
supported by additional analyses including
morphological characters. In conclusion, all
these studies indicate that we still have in-
sufficient knowledge to answer these ques-
Tab. 1:Current systematic classification of the Triatominae subfamily
tions and that much additional research is (updated from GALVÃO2003;GALVÃOet al. 2003; FOREROet al. 2004).
needed.
Subfamily Tribes Genera Number of
Extensive dichotomous keys for the valid names
Triatominae Alberproseniini Alberprosenia 2
identification of Triatominae species were
Bolboderini Belminus 6
provided by LENT& WYGODZINSKY(1979),
Bolbodera 1
LENT et al. (1994) and CARCAVALLO et al. Microtriatoma 2
(1998/99). Parabelminus 2
Cavernicolini Cavernicola 2
Geographical distribution Linshcosteini Linshcosteus 6
Rhodniini Psammolestes 3
The vast majority of Triatominae species
Rhodnius 16
are found only in the New World; a few
Triatomini Dipetalogaster 1
species are found in East Asia and on the Eratyrus 2
Hermanlentia 1
coast of Australia. In the Neotropical and
Meccus 6
Nearctic regions the species are found be- Mepraia 2
tween 42°N and 46°S. One species, Tri- Nesotriatoma 3
Panstrongylus 13
atoma rubrofasciatais tropicopolitan, and an
Paratriatoma 1
additional seven species of Triatomaoccur in Triatoma 67
southern and southeastern Asia and north- Total 18 136
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Tab. 2: Geographical distribution of triatomine species (updated from GALVÃOet al. 2003). ern Australia. Linshcosteus (Fig. 12) is the
only genus restricted to the Old World,
Species and author Countries
specifically, to the Indian subcontinent
Alberprosenia goyovargasiMARTÍNEZ& CARCAVALLO1977 Venezuela
A. malheiroiSERRA, ATZINGEN& SERRA1980 Brazil (GALVÃO et al. 2003). CARCAVALLO et al.
Belminus costaricencisHERRER, LENT& WYGODZINSKY1954 Costa Rica, Mexico (1999) provided several maps showing the
B. herreriLENT& WYGODZINSKY1979 Colombia, Panama geographical distribution and altitudinal/
B. laporteiLENT, JURBERG& CARCAVALLO1995 Brazil latitudinal dispersion of all American Tri-
B. peruvianusHERRER, LENT& WYGODZINSKY1954 Peru atominae species.
B. pittieriOSUNA& AYALA1993 Venezuela
B. rugulosusSTÅL1859 Colombia, Venezuela Habitats
Bolbodera scabrosaVALDÉS1910 Cuba Knowledge of triatomine species biology
Microtriatoma borbaiLENT& WYGODZINSKY1979 Brazil
in their natural habitats is scarce, and for
M. trinidadensis(LENT1951) Brazil, Bolivia, Colombia,
several species the natural ecotopes have
Peru,Trinidad, Venezuela
not been described. Triatominae species are
Parabelminus cariocaLENT1943 Brazil
P. yurupucuLENT& WYGODZINSKY1979 Brazil found in almost any habitat offering a de-
Cavernicola lentiBARRETT& ARIAS1985 Brazil gree of permanence, climatic shelter, and
C. pilosaBARBER1937 Brazil, Colombia, Panama, Peru, access to a blood source. Most species toler-
Venezuela ate a range of air humidity between 30-80
Linshcosteus carnifexDISTANT1904 India %, and temperatures of 24-28°C are satis-
L. chotaLENT& WYGODZINSKY1979 India factory to them. Their development is usu-
L. confumusGHAURI1976 India
ally slow at temperatures below 16 °C,
L. costalisGHAURI1976 India
whereas temperatures above 40 °C are
L. kaliLENT& WYGODZINSKY1979 India
lethal. Several species have specific habi-
L. karupusGALVÃO, PATTERSON, ROCHA& JURBERG2002 India
tats. For example, Triatoma infestans is found
Psammolestes arthuri(PINTO1926) Colombia, Venezuela
almost exclusively in human dwellings,
P. coreodesBERGROTH1911 Argentina, Bolivia, Brazil, Paraguay
Cavernicolalenti, a sylvatic species, is closely
P. tertiusLENT& JURBERG1965 Brazil
Rhodnius amazonicus ALMEIDA, SANTOS& SPOSINA1973 Brazil, French Guyana related to tree hollows inhabited by bats,
Rhodnius brethesiMATTA1919 Brazil, Colombia, Venezuela and species from of the genus Psammolestes
R. colombiensisMEJIA, GALVÃO& JURBERG1999 Colombia occur only in the nests of certain birds. Most
R. dalessandroiCARCAVALLO& BARRETO1976 Colombia triatomine species are sylvatic, living in bird
R. domesticusNEIVA& PINTO1923 Brazil nests, animal dens, under tree bark or in tree
R. ecuadoriensisLENT& LEÓN1958 Ecuador, Peru hollows, bromeliads, palm trees, and other
R. milesiCARCAVALLO, ROCHA, GALVÃO& JURBERG2001 Brazil ecotopes, feeding on various animals.
R. nasutusSTÅL1859 Brazil GAUNT & MILES (2000) summarize the
R. neglectusLENT1954 Brazil habitats of the triatomine genera Rhodnius
R. neivaiLENT1953 Colombia, Venezuela and Triatoma, showing that most species in
R. pallescensBARBER1932 Belize, Colombia, Costa Rica, Pana- the former genus live in or associated with
ma
palm trees, while most species in the latter
R. paraensisSHERLOCK, GUITTON& MILES1977 Brazil
genus live in or associated with rocky/terres-
R. pictipesSTÅL1872 Belize, Brazil, Colombia, Ecuador,
Guyana, French Guyana, Peru, trial habitats. However, during their evolu-
Suriname, Trinidad, Venezuela tionary process some species acquired the
R. prolixusSTÅL1859 Bolivia, Brazil, Colombia, Costa Rica, capacity to colonize manmade structures
El Salvador, Ecuador, Guatemala,
near human dwellings, like chicken coops,
Guyana, French Guyana, Honduras,
Mexico, Nicaragua, Panama, Suri- pigsties and such species are thus referred to
name, Trinidad, Venezuela
as peridomiciliated. Others can colonize the
R. robustusLARROUSSE1927 Bolivia, Brazil, Colombia, Ecuador, interior of human dwellings and are thus
French Guyana, Peru, Venezuela
called domiciliated. The latter are more im-
R. staliLENT, JURBERG& GALVÃO1993 Bolivia, Brazil
portant, since they account for transmission
Dipetalogaster maxima(UHLER1894) Mexico
Eratyrus cuspidatusSTÅL1859 Colombia, Ecuador, Guatemala, of the disease to humans (CARCAVALLO et
Mexico, Panama, Peru, Venezuela al. 1998/99). Many rural inhabitants live in
E. mucronatusSTÅL1859 Bolivia, Brazil, Colombia, Ecuador, dwellings with straw roofs and mud walls,
Guatemala, Guyana, French Guyana,
and these provide various forms of shelter
Panama, Peru, Suriname, Trinidad,
Venezuela for the triatomines (Fig. 13).
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Behaviour and biological aspects
Species and author Countries
Egg laying and life cycle.In general the Hermanlentia matsunoi(FERNÁNDEZ-LOAYZA1989)Peru
eggs of the majority of triatomine species are Meccus bassolsae(AGUILAR, TORRES, JIMENEZ,
JURBERG, GALVÃO& CARCAVALLO1999) Mexico
deposited free in the environment, although
M. longipennis(USINGER1939) Mexico
some species have an adhesive substance
M. mazzottii(USINGER1941) Mexico
which makes the eggs stick to the substrate
M. pallidipennis(STÅL1872) Mexico
(Fig. 14, 15). Triatoma infestans, a domicili-
M. phyllosomus(BURMEISTER1835) Mexico
ated species that originally inhabited rodent
M. picturatus(USINGER1939) Mexico
nests, is still found in the Bolivian altiplano
Mepraia gajardoiFRIAS, HENRY& GONZALEZ1998 Chile
and lays its eggs loose in the sites it inhabits.
M. spinolai(PORTER1934) Chile
Triatoma platensisand Triatoma delpontei, or- Nesotriatomabruneri USINGER1944 Cuba
nithophilous species, stick their eggs to the N. flavida (NEIVA1911) Cuba
substrate of the bird nests in which they N. obscura MALDONADO& FARR1962 Jamaica
live. Species of Rhodniusalso stick their eggs Paratriatoma hirsutaBARBER1938 Mexico, USA
to the substrate. Rhodnius prolixus, which in- Panstrongylus chinai(DELPONTE1929) Ecuador, Peru, Venezuela
habits the nest of Mycteria americana,a mi- P. diasiPINTO& LENT1946 Bolivia, Brazil
gratory bird, can have its eggs spread when P. geniculatus(LATREILLE1811) Argentina, Bolivia, Brazil, Colombia, Costa Ri-
ca, Ecuador, Guatemala, Guyana, French Guy-
they are adhered to the bird’s feathers.
ana, Mexico, Nicaragua, Panama, Paraguay,
Psammolestes arthuri oviposits in clusters, Peru, Suriname, Uruguay, Trinidad, Venezuela
like members of such reduviid subfamilies as P. guentheriBERG1879 Argentina, Bolivia, Paraguay, Uruguay
Harpactorinae and Apiomerinae (LENT & P. howardi(NEIVA1911) Ecuador
WYGODZINSKY1979). P. humeralis(USINGER1939) Panama
P. lentiGALVÃO& PALMA1968 Brazil
Oviposition normally occurs 10 to 30
P. lignarius(WALKER1873) Brazil, Peru, Guyana, Suriname, Venezuela
days after copulation, which can be repeat-
P. lutzi(NEIVA& PINTO1923) Brazil
ed several times during the adult’s lifespan, P. megistus(BURMEISTER1835) Argentina, Bolivia, Brazil, Paraguay, Uruguay
although a female fecundated just once re- P. rufotuberculatus(CHAMPION1899) Argentina, Bolivia, Brazil, Colombia, Costa Ri-
mains permanently fertilized. Copulation ca, Ecuador, Mexico, Panama, Peru, Venezuela
can last 15 to 30 minutes, and the male fer- P. sherlockiJURBERG, CARCAVALLO& LENT2001 Brazil
tilizes the female by depositing sper- P. tupynambaiLENT1942 Brazil, Uruguay
matophores in the female vagina; these Triatoma amicitiaeLENT1951 Sri Lanka
burst and release the spermatozoa which mi- T. arthurneivai LENT& MARTINS1940 Brazil
grate to the spermathecae, where they re- T. barataiCARCAVALLO& JURBERG2000 Brazil
T. barberiUSINGER1939 Mexico
main protected while awaiting the passage
T. bolivariCARCAVALLO, MARTÍNEZ& PELAEZ1987 Mexico
of the successive ova to fertilize them. The
T. bouvieriLARROUSSE1924 Nicobar Islands, Philippine, Vietnam
number of eggs varies by species and princi-
T. brailovskyiMARTÍNEZ, CARCAVALLO& PELAEZ1984 Mexico
pally as a function the female’s degree of
T. brasiliensisNEIVA1911 Brazil
feeding. Recently laid eggs are whitish or
T. breyeriDELPONTE1929 Argentina
pearly in color and change color over time T. carcavalloiJURBERG, ROCHA& LENT1998 Brazil
until they become pinkish or brownish, near T. carrioniLARROUSSE1926 Ecuador, Peru
the day of hatching. During this phase, with T. cavernicolaELSE& CHEONG1977 Malaysia
the eggs transparent, one can see the black T. circummaculata(STÅL1859) Brazil, Uruguay
ocular spots, as the 1ststage nymphs emerge T. costalimaiVERANO& GALVÃO1958 Brazil
from the egg leaving the exuviae appearing T. deaneorumGALVÃO, SOUZA& LIMA1967 Brazil
(proto-nymph). T. delponteiROMAÑA& ABALOS1947 Argentina, Bolivia, Brazil, Uruguay, Paraguay
T. dimidiata(LATREILLE1811) Belice, Colombia, Costa Rica, El Salvador,
The longevity of nymphs and adults Ecuador, Guatemala, Honduras, Mexico,
varies by species and ambient conditions. Nicaragua, Panama, Peru, Venezuela
Laboratory experiments generally use what T. disparLENT1950 Colombia, Costa Rica, Ecuador, Panama
are considered ideal conditions for most T. eratyrusiformisDELPONTE1929 Argentina
species, with a mean temperature close to 28 T. garciabesiCARCAVALLO, CICHERO, MARTÍNEZ,
PROSEN& RONDEROS1967 Argentina, Bolivia
°C and relative humidity around 70 %,
T. gerstaeckeri(STÅL1859) USA, Mexico
blood feeding on adequate sources for each
T. gomeznuneziMARTÍNEZ,
species, and a photoperiod of 12 hours. Of CARCAVALLO& JURBERG1994 Mexico
course in nature the insect is influenced by T. guasayanaWYGODZINSKY& ABALOS1949 Argentina, Bolivia, Paraguay
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various factors that are difficult to control in
Species and author Countries
T. guazuLENT& WYGODZINSKY1979 Brazil the laboratory. Results obtained in the labo-
T. hegneriMAZZOTTI1940 Mexico ratory are thus merely an approximation of
T. incrassataUSINGER1939 USA, Mexico what occurs in nature, but knowledge of the
T. indictivaNEIVA1912 USA, Mexico biological cycles and population dynamics
T. infestans infestans (KLUG1834) Argentina, Bolivia, Brazil, Chile, Ecuador, allows an estimation of the species’ growth
Paraguay, Peru, Uruguay
and colonization capacity, principally for
T. infestans melanosomaMARTÍNEZ,
anthropophilic species, but also for so-called
OLMEDO& CARCAVALLO1987 Argentina
T. jurbergiCARCAVALLO, GALVÃO& LENT1998 Brazil secondary species with a tendency towards
T. klugiCARCAVALLO, JURBERG, domiciliation (CANALEet al.1999).
LENT& GALVÃO2001 Brazil
Temperature. The importance of tem-
T. lecticularia(STÅL1859) USA, Mexico
perature and humidity for triatomine biolo-
T. lentiSHERLOCK& SERAFIM1967 Brazil
T. leopoldi(SCHOUDETEN1933) Australia, Indonesia gy was studied early by NEIVA (1913) who
T. limaiDELPONTE1929 Argentina observed that high temperatures accelerated
T. maculata(ERICHSON1848) Aruba, Brazil, Bonaire, Curacao, Colombia, the embryonic period of Triatoma infestans.
Guyana, French Guyana, Suriname, Venezuela CARCAVALLO& MARTÍNEZ(1972) obtained
T. matogrossensisLEITE& BARBOSA1953 Brazil shorter cycles in specimens of three species
T. melanocephalaNEIVA& PINTO1923 Brazil of Triatoma reared at high temperatures as
T. mexicana(HERRICH-SCHAEFFER1848) Mexico compared to those reared at variable tem-
T. migransBREDDIN1903 India, Indonesia, (Borneo, Java, Sumatra),
Malaysia, Philippine, Thailand peratures. SILVA(1985, 1988, 1989a, 1989b,
T. neotomaeNEIVA1911 USA, Mexico 1989c, 1990a, 1990b, 1992), SILVA& SILVA
T. nigromaculata(STÅL1872) Colombia, Peru, Venezuela (1988a, 1988b, 1988c, 1988d, 1988e, 1989,
T. nitidaUSINGER1939 Costa Rica, Guatemala, Honduras, Mexico 1990a, 1990b, 1991, 1993) and SILVA et al.
T. oliveirai(NEIVA, PINTO& LENT1939) Brazil (1995) compared the developmental times
T. patagonicaDELPONTE1929 Argentina, Uruguay of several species reared at 25 °C and 30 °C
T. peninsularisUSINGER1940 Mexico showing a reduction of approximately 30
T. petrochiaePINTO& BARRETO1925 Brazil days in three species of Rhodnius and from
T. platensisNEIVA1913 Argentina, Paraguay, Uruguay 40 to 60 days in Triatomaspecies. According
T. protracta(UHLER1894) USA, Mexico to most authors, when associated with low
T. pseudomaculataCORRÊA& ESPÍNOLA1964 Brazil relative humidity the cycle is shortened by
T. pugasiLENT1953 Indonesia (Java)
metabolic alteration and dehydration, in-
T. recurva(STÅL1868) USA, Mexico
creasing the number of blood meals to bal-
T. rubida(UHLER1894) USA, Mexico
ance the energy budget and water loss. Var-
T. rubrofasciata(DEGEER1773) Andaman Islands, Angola, Argentina, Azores, Ba-
hamas, Brazil, Burma, Cambodia, Caroline Islands, ious authors have demonstrated accelera-
China, Comores, Congo, Cuba, Dominican Repub- tion in the developmental period of several
lic, Formosa, French Guyana, Goa, Grenada, Gua-
species submitted to increased temperature
daloupe, Haiti, Hawaii, Hong Kong, India, Indone-
sia (Borneo, Java, Sumatra) Jamaica, Madagascar, (GALVÃO et al. 1995, 1999b; ROCHA et al.
Malaysia, Martinica, Mauritius Islands, New
1994, 2001a, 2001b). These results support
Guinea, Okinawa, Philippine, Saint Croix, Saint
Vincent, Saudi Arabia, Seychelles, Serra Leone, the hypothesis that higher temperatures and
Singapure, South Africa, Sri Lanka, Thailand, lower relative humidity, as possible conse-
USA,Venezuela, Vietnam, Zanzibar
quences of global warming, could accelerate
T. rubrovaria(BLANCHARD1843) Argentina, Brazil, Uruguay
the life cycle. The result is a change in the
T. ryckmaniZELEDÓN& PONCE1972 Costa Rica, Guatemala, Honduras
population dynamics of some Chagas disease
T. sanguisuga(LECONTE1855) USA, Mexico
vectors, extending the geographic distribu-
T. sherlockiPAPA, JURBERG, CARCAVALLO,
CERQUEIRA& BARATA2002 Brazil tion towards more temperate regions as well
T. sinaloensisRYCKMAN1962 Mexico increasing the density of some populations.
T. sinicaHSIAO1965 China The literature shows the results of dozens of
T. sordida(STÅL1859) Argentina, Bolivia, Brazil, Paraguay, Uruguay observations on the life cycles of these in-
T. tibiamaculata(PINTO1926) Brazil sects in the laboratory, a summary of the
T. vandaeCARCAVALLO, JURBERG, ROCHA, GALVÃO, NOIREAU& LENT2002 Brazil principal studies was published by CANALE
T. venosa(STÅL1872) Bolivia, Colombia, Costa Rica,Ecuador, Peru
et al.(1999).
T. vitticeps(STÅL1859) Brazil
T. williamiGALVÃO, SOUZA& LIMA1965 Brazil
T. wygodzinskyiLENT1951 Brazil
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