the effect of temperature on the behaviour and development of triatoma brasiliensis

The effect of temperature on the behaviour anddevelopment of Triatoma brasiliensis

AL E S S ANDRA A . GUARNER I , C L AUD I O LA Z ZAR I * ,

ANA AM E L I A P . X AV I E R , L I L E I A D I O TA I U T I and MARCE LO

G . L OR ENZOCentro de Pesquisas Rene Rachou, FIOCRUZ, Belo Horizonte, MG, Brazil and *Departamento de Biodiversidad y Biologıa

Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

Abstract. The effects of temperature on the development of early stages and thethermopreference of nymphs and adults were analysed in the haematophagousbug Triatoma brasiliensis Neiva, 1911 (Hemiptera, Reduviidae). Egg hatching,mortality of nymphs, feeding and moulting success of the early stages ofT. brasiliensis were all affected by temperature. While high rates of egg hatchingwere observed between 25 and 27 �C, no hatching occurred at 12, 19 and 38 �C.The mortality of first-instar nymphs was highest at 38 �C, at which no insectssurvived after 10 days of exposure. Feeding success was only affected at the lowesttemperature (12 �C). No ecdysis was observed in the groups exposed to 12, 19 and21 �C. Recently fed fourth-instar nymphs preferred to stay at a temperature ofapproximately 30 �C. The preferred temperature began to decline gradually toapproximately 27 �C during ecdysis, reaching 26 �C at 30 days after ecdysis. Aftera second blood meal, the insects’ preferred temperature was again approximately30 �C. The thermopreference pattern of females was similar to that of nymphs.Nymphs and females showed a daily fluctuation in their preferred temperature,moving towards higher values at the beginning of the dark phase, and choosinglower ones after this time interval, at which they remained until the end of the lightphase. The females laid their eggs in all sectors of the arena, although the largestnumbers of eggs were found between 28 and 32 �C.

Key words. Behaviour, Chagas vectors, microclimate, temperature, Triatoma.

Introduction

After the elimination of Triatoma infestans from many

Brazilian states through spraying campaigns, Triatoma

brasiliensis Neiva, 1911 (Hemiptera, Reduviidae) is now

considered the main vector of Trypanosoma cruzi in north-

eastern Brazil. T. cruzi is the aetiological agent of Chagas

disease, which affects approximately 17 million people in

Latin America, where another 100 million people are at risk

of contracting it (Schofield & Dias, 1999).

T. brasiliensis is distributed widely in the north-eastern

region (Silveira et al., 1984), a characteristically hot and dry

area with absence of rain along 8–9months of the year. This

triatomine species lives in wild habitats, where it is mainly

found in rock piles associated with rodents, marsupials and

bats. It is also able to colonize houses and peridomicilary

areas, where it feeds on man and domestic animals

(Alencar, 1987).

Studies on the influence of climatic factors on the biology

of triatomines are relevant because the distribution of many

species of this group, as well as other species of insects, is

affected by environmental factors. The shelters where

T. brasiliensis is found in both sylvatic and domestic habi-

tats show similar temperature and relative humidity (RH)

values, with little variation in magnitude when compared

with the broader oscillations of the external environment

Correspondence: Dr Alessandra A. Guarneri, Centro de Pesquisas

Rene Rachou, FIOCRUZ, Avenue Augusto de Lima, 1715, CEP

30190-002,BeloHorizonte,MG,Brazil.Tel:þ553132953566, fax:þ55

31 3295 3115; e-mail: [email protected]

Physiological Entomology (2003) 28, 185–191

# 2003 The Royal Entomological Society 185

(Lorenzo et al., 2000). This suggests that this species,

although living in an area with fluctuating high temperature

and low RH, chooses to live in more stable microenviron-

ments (Lorenzo et al., 2000). In the laboratory, the egg

hatching of T. brasiliensis is lower under low RH condi-

tions, whereas feeding and ecdysis of first-instar nymphs are

only affected by high RH values (Guarneri et al., 2002). In

addition, T. brasiliensis chooses low RHs when recently fed,

changing its preference to more humid sites with extreme

starvation (Guarneri et al., 2002).

The triatomine bugs studied to date modulate their

thermopreference following a similar pattern, according to

their physiological state. However, the rate of variation in

preferred temperatures with increasing starvation is differ-

ent among species (Lazzari, 1991; Schilman, 1998; Pires

et al., 2002). To characterize the influence of climatic effects

on the physiology and behaviour of triatomines, the effect

of temperature on egg hatching, nymph mortality and

moulting success of T. brasiliensis was studied. In addition,

the temperature preference of this species in relation to

resting, moulting and laying eggs was also characterized.

Finally, the effect of starvation on thermopreference in this

species was analysed.

Materials and methods

Insects

The colony used for all assays was started with insects

collected in Piauı and Ceara states, Brazil, and reared in the

insectary of the Laboratorio de Triatomıneos e Epidemio-

logia da Doenca de Chagas, Centro de Pesquisas Rene

Rachou, FIOCRUZ, Brazil. Insects were reared under a

natural regime of temperature (27� 3 �C), RH (65� 10%)

and illumination, and fed weekly on chicken.

Control of temperature

A temperature gradient was established through an

aluminium plate that had one end heated by an electrical

resistance and the other end cooled by a cool plate. The

temperature at both ends was controlled by electronic

thermostatic devices to within 0.1 �C. This system generated

a linear temperature gradient ranging from 12 to 41 �C. Thetemperatures were measured using a thermohygrometer

(Testo 625, Lenzkirch, Germany, accuracy � 0.4 �C).

The effect of temperature on T. brasiliensis

Batches of eggs laid over a 3-day period were randomly

assigned to eight groups, each exposed to a different tem-

perature. Each group of eggs was placed in a Petri dish

surrounded by a saturated solution of Ca(NO3)2 which

was kept in a larger, hermetically sealed Petri dish. This

solution provided RHs that ranged from 48 to 60%,

depending on the temperature to which the plate was

exposed. This variation in RH does not affect egg hatching

in this species, as already established by Guarneri et al.

(2002). The Petri dishes were placed on the aluminium

plate described above. The resulting temperatures inside

Petri dishes were 12, 19, 21, 25, 27, 31, 33 and 38 �C. Theeggs were exposed to an illumination cycle of LD 12 : 12 h.

During the light phase, diffuse illumination was provided by

a fluorescent lamp (7V), which rendered an intensity of

10 lux. The eggs were maintained under these conditions

until eclosion finished, when the percentage of eggs hatched

was calculated. If none of the eggs hatched at a certain

temperature within a period of 30 days, they were trans-

ferred to 28 �C for an additional 30-day period to determine

if eclosion would still take place. The number of eggs per

plate varied between 33 and 65.

In another experiment, batches of first-instar nymphs

ecloded over a 3-day period were randomly assigned to

eight groups. They were exposed to the same temperatures

defined above for the eggs during a period of 10 days and,

subsequently, their mortality was determined. The surviving

nymphs were fed on Swiss mice previously anaesthetized

with thionembutal injected intraperitonially. The percen-

tage of insects fed to repletion was then determined for

each group. Subsequently, the insects were put back in the

dish under the same conditions until ecdysis occurred. The

moulting success was then determined for each of the eight

temperatures tested. If no ecdysis was observed within

a period of 30 days, the nymphs were submitted to 28 �Cfor an additional 10-day period, after which they received a

second blood meal and were maintained in the same condi-

tions until moulting. Two replications of the complete assay

were conducted for each group. The number of nymphs per

plate (n) varied between 33 and 50.

The thermopreference of T. brasiliensis

Two groups of 50 fourth-instar nymphs were fed on live

chicken 15 days after ecdysis and released the following day

in the centre of a closed arena placed on the aluminium

plate described above (Fig. 1). The arena made of

glass (40� 20� 5 cm) was divided in two sections

(40� 10� 5 cm each), which enabled to carry out two

simultaneous assays. The sides and the bottom of the

arena were covered with filter paper that acted as substrate

for the bugs and isolated the arena’s lateral view from the

outside. This was carried out to prevent dark backgrounds

that could affect the distribution of the bugs along the

arena. In this experiment, the device generated a linear

temperature gradient inside the arena ranging from 22 to

41 �C. The RH measured in this chamber ranged from 21 to

53% from the warmer to the colder end, respectively. The

insects were maintained under a LD 12 : 12 h regime of

illumination. An infrared-sensitive video camera, with its

own illumination system composed of six infrared light-

emitting diodes (LED) (900 nm) and 28 extra infrared-

LEDs, were located above the arena providing a uniform

186 A. A. Guarneri et al.

# 2003 The Royal Entomological Society, Physiological Entomology, 28, 185–191

illumination for video recording. This device allowed record-

ing the position of the bugs even during complete functional

darkness for the insects. This kind of infrared illumination is

not perceivedby triatominebugs (Reisenman et al., 1998).The

position of the bugs was recorded every 3 h over a period of

42 days. The position of the exuviae along the gradient was

also recorded. After this period, the insects were fed again,

returned back to the arena and their position was recorded for

an additional 5-day interval. The activity of the nymphs was

measured by counting the number of insects that moved

during each single record (i.e. for 1min every 3h). The values

used to depict the thermopreference of the insects were

obtained from the calculation of the mean temperatures

chosen by the group of bugs. We determined the position of

each individual in every sample over the experiment and, for

each position, a temperature was assigned. Therefore, the

values depicted aremeans of 50 individual choices for every 3h.

Additionally, a group of 12 females was fed on live chicken

and released the following day in the same arena described

before, where they were kept during a period of 37days.

Subsequently, the insects were offered a second blood meal

and were replaced in the arena for an additional 24-day inter-

val. The position of the bugs was recorded every hour. To

analyse the thermopreference of the females to oviposit, two

groups of 12 and 11 females were fed on live chicken and

released in the arena the following day. A plastic net was

placed on the bottom of the arena to prevent eggs from rolling

away from the site where they had been laid. The two groups

of females were maintained in the arena for 17 and 24days,

respectively, when the eggs in each sector were counted.

Statistical analysis

Analysis of variance (ANOVA) and post hoc comparisons

(Scheffe test) were made to test the null hypothesis of a lack

of effect of temperature on the different variables assessed.

Results

The effect of temperature on egg hatching, mortality of

nymphs, feeding and moulting success in T. brasiliensis

Egg hatching, mortality of nymphs, feeding and moulting

success of early stages of T. brasiliensis were all affected by

temperature (in all cases, ANOVA P < 0.05) (Table 1). None

Fig. 1. Experimental arena in which a

temperature gradient was established to

test the thermopreference of Triatoma

brasiliensis.

Table 1. Influence of temperature (mean�SE) on the development of Triatoma brasiliensis.

Temperature (�C) Eclosion success (%) Mortality (%) Fed insects (%) Ecdysis (%)

12 0 47.1� 19.6 1.7� 1.7 0

19 0 1.8� 1.2 92.3� 0.0 0

21 65.0� 25.0 0 100.0 0

25 96.9� 1.5 2.5� 2.5 100.0 89.4� 10.5

27 96.2� 1.2 0 100.0 85.4� 7.9

31 64.6� 0.0 0 98.7� 1.2 80.7� 11.5

33 27.5� 2.5 0 97.3� 3.8 66.3� 12.0

38 0 100.0 – –

*All assays were performed in duplicate. The number of eggs or insects per assay varied between 33 and 65.

Temperature, behaviour and development of Triatoma brasiliensis 187


of the eggs hatched at 12, 19 or 38 �C and the highest

hatching success occurred in the groups tested between 21

and 31 �C (Scheffe, not significant). After submitting those

batches of eggs that did not eclode to 28 �C, only those that

had been previously maintained at 19.1 �C showed

10.4� 4.1% of successful hatching.

The mortality of first-instar nymphs was highest at 38 �C;at this temperature none of the insects survived after 10 days

of exposure (for all comparisons, Scheffe, P< 0.05). On the

other hand, feeding was only affected at 12 �C (Scheffe,

P< 0.05). No ecdysis was observed in the groups exposed

to 12, 19 and 21 �C during a period of 30 days. These insects

were subsequently exposed to 28 �C for 10 days. After-

wards, 5.71� 0.1% and 3.12% of the insects moulted that

had previously been exposed to 19 and 21 �C, respectively.Nymphs that did not moult were offered a second blood

meal and subsequently maintained at 28 �C. After approxi-

mately 12 days, 98.6� 1.3% and 100% of the insects

exposed to 19 and 21 �C, respectively, ecdysed.

Thermopreference of T. brasiliensis

Recently fed fourth-instar nymphs preferred to stay at a

temperature of approximately 30 �C. After nearly 15 days,

when most had ecdysed, the preferred temperature values

declined abruptly to approximately 27 �C, reaching 26 �C at

30 days after ecdysis (Fig. 2). After feeding the insects for a

second time, their thermopreference returned to approxi-

mately 30 �C. Nymphs showed a daily fluctuation in their

preferred temperature, this behaviour being more evident in

starved insects (Fig. 3). They moved to higher temperatures

at the beginning of the dark phase, and chose lower ones

after the third hour of the night, keeping this choice until

the end of the light phase.

The activity of the nymphs increased with starvation

(Fig. 4). The maximum activity was observed at the begin-

ning of the dark phase (Fig. 4, insert). The exuviae left by

moulted insects were found distributed along all sectors of

the arena, but mostly between 24 and 26 �C.The thermopreference pattern of females was similar to

that shown by nymphs (Fig. 5). Recently fed insects

remained at approximately 29 �C and gradually moved to

26 �C with increasing starvation. They also presented a daily

fluctuation on their thermopreference, preferring higher

temperatures at the beginning of the dark phase (Fig. 6).

The daily fluctuation observed in the females was, however,

broader than that observed in nymphs (two-way ANOVA,

P< 0.05). A larger number of eggs was found between 28

and 32 �C, although they were laid in all sectors of the arena

(Fig. 7).

Discussion

Several studies have shown the influence of temperature on

the development of triatomines (Juarez & Silva, 1982; Silva,

1988; Cabelo, 1999; Luz et al., 1999). The environmental

temperature affects the fecundity and the maturity rate of

T. infestans (Jorg, 1960, 1989) and Mepraia spinolai

(Ehrenfeld et al., 1998). The dispersion of T. infestans is

also affected by temperature. When the environmental tem-

perature increases over 25 �C, the proportion of individuals

that begin to fly also increases (Lehane et al., 1992). In the

present study, both egg hatching and development of early

stages of T. brasiliensis were significantly affected by

temperature. Temperatures of 12 and 38 �C were lethal to

Fig. 2. Thermopreference of nymphs of Triatoma brasiliensis as a

function of nutritional status. The data depicted are the mean

temperature values preferred by a group of 50 fourth-instar

nymphs for every 3 h over 45 days.

Fig. 3. Daily pattern of thermopreference in nymphs of Triatoma

brasiliensis. Data from this experiment were depicted separatedly

for three different time intervals: (a) recently fed: from the start of

the assay to the beginning of ecdysis (approximately 10 days); (b)

ecdysis: whereas exuviae continued to appear in the gradient

(approximately 10 days); and (c) after ecdysys (approximately

20 days). The data depicted are the mean� SE thermopreference of

the group for each hour at which the positions of the insects were

registered.



this species because neither eggs nor nymphs developed

when exposed to them, even if they were later transferred

to 28 �C. The temperature of 19 �C was not completely

deleterious for the insects. Despite the fact that no egg

hatching occurred at this temperature, once the eggs were

exposed to 28 �C, a small percentage of eclosion was

observed. In addition, when the nymphs that had not

moulted at 19 �C were fed again, and subsequently exposed

to 28 �C, the ecdysis rate was similar to that obtained for the

groups exposed to 27 �C. Similar results on the influence of

temperature on the biology of Rhodnius prolixus were

obtained by Clark (1935) and Luz et al. (1999).

According to the results presented in this study, early

stages of T. brasiliensis showed a better development at

temperatures between 25 and 31 �C. Environmental meas-

urements taken in natural refuges of T. brasiliensis showed

mean temperatures of 31, 31 and 33 �C for shelters inside

houses, peridomiciles and inside rock piles in wild environ-

ments, respectively (Lorenzo et al., 2000). However, there

are some important differences between the assays used here

and the conditions in the field. In the laboratory experi-

ments, insects were submitted to a constant temperature, in

contrast to what happens in the field, where the shelter

temperatures fluctuate during the day, even though at

lower amplitudes than the external environment (Lorenzo

et al., 2000). This temperature oscillation in natural shelters

Fig. 4. Locomotor activity pattern in

nymphs of Triatoma brasiliensis. Insert:

Daily pattern of activity. The data are the

mean�SE of the number of insects that

moved over the assay for each hour in

which the position of the insects was

registered.

Fig. 5. Thermopreference in females of Triatoma brasiliensis as a

function of nutritional status. The data depicted are the mean

temperature values preferred by a group of 12 females for every

hour over the assay. Mean thermopreference values were calculated

using the same method as those for nymphs.

Fig. 6. Daily pattern of thermopreference in females of Triatoma

brasiliensis. The data depicted are the mean�SE thermopreference

of the group of 12 females for each hour at which their position was

registered.



may allow the insects to bear temperatures, daily and over

several hours, that were not tolerated in constant experi-

mental conditions. In addition, and as demonstrated in the

gradient assays, T. brasiliensis searches actively for its pre-

ferred temperature. These insects show a behaviour that can

be related to the avoidance of high temperatures in the field.

According to our field observations, during sunset, when

the surface temperature of the rocks is at least 5 �C higher

than the air temperature, nymphs and adults of T. brasiliensis

leave the shelters inside the rock piles, and reach the outer

surface of rocks. Moreover, insects of this species adopt a

characteristic stance, maintaining the abdomen at a high

distance from the substrate, unlike other triatomine bugs.

The insects display this behaviour for approximately 3 h,

after which they return to their shelters. Maintaining the

body distant from the ground can be a strategy to avoid

harmful temperatures. In the Sahara desert, ants from the

genus Cataglyphis possess long legs that keep their body at a

height of approximnately 4mm above ground, where tem-

peratures may be >10 �C lower than on the sand surface

(Gehring & Wehner, 1995).

Within the normal range of temperatures at which they

are active and can survive, insects express a thermoprefer-

ence when given the choice. The tendency to remain still at

the preferred range may be a behavioural mechanism to

maintain the insects within optimal temperature limits for

most metabolic processes (Chapman, 1998).

In the present study, both nymphs and adults showed a

thermopreference with a pattern similar to that recorded for

other triatomine species studied to date (Lazzari, 1991;

Schilman, 1998; Pires et al., 2002). Of note, we also

observed a decrease in the preferred temperature as the

length of starvation increased. However, although the pre-

ferred temperature of T. infestans changes from 29 to

25–26 �C after 10 days of starvation (Lazzari, 1991), this

change takes 18days in Panstrongylus megistus (Pires et al.,

2002). Rhodnius prolixus, which is tolerant to starvation,

prefers to stay at lower temperatures, approximately

24 �C, and this preference only changed with prolonged

food deprivation (Schilman, 1998). Trypanosoma brasiliensis,

which is also tolerant to starvation, shows a decrease in its

preferred temperature only after 25–30 days of starvation.

However, it prefers significantly higher temperatures than

R. prolixus during the whole process.

These results support the previous idea that this behav-

iour may reflect a common mechanism for regulating

metabolism or water balance in triatomines. Elimination

of large amounts of water through diuresis takes place

during a few hours after the intake of a blood meal

(Wigglesworth, 1931). At this stage, triatomines show a

preference for higher temperatures, which probably increase

their metabolic rate, and therefore the speed of digestion

and moulting processes. However, when starvation ensues,

the preference changes to lower temperatures, decreasing

the insects’ metabolic rate to a level that would avoid unne-

cessary waste of water and nutrients (Pires et al., 2002). In a

previous study, it was demonstrated that T. brasiliensis

regulates the amount of cuticular and breathing water loss

by actively searching for appropriate environmental RH

values that vary depending on its nutritional status

(Guarneri et al., 2002). The long-term variation in thermo-

preference would tend toward the same direction.

Again, the daily variation in temperature preferences of

T. brasiliensis show the same pattern depicted for the other

triatomine species studied. The insects demonstrate a pre-

ference for higher temperatures at the beginning of the dark

phase. Thus, staying at lower temperatures during resting

hours would decrease their metabolic rate during that

period. At the time when the host seeking occurs, they expose

themselves to higher temperatures, thus increasing their

metabolic rate and, consequently, their locomotor activity

(Pires et al., 2002). However, T. brasiliensis and T. infestans

(Lazzari, 1991) show a broader daily variation compared to

R. prolixus (Schilman, 1998) and P. megistus (Pires et al.,

2002). This daily variation also differs between nymphs and

adults of T. brasiliensis, with adults showing a higher varia-

tion than nymphs. The daily variation changed according to

the physiological status of the insects, being more evident as

starvation increased. A similar change was observed in the

locomotor activity pattern of nymphs, which increased

significantly with a prolonged food deprivation.

The eggs of T. brasiliensis were found distributed

throughout the gradient with a peak at 28–32 �C. In the

two assays where the preferred temperature for oviposition

was studied, the eggs were collected at the 17th and 24th

days post feeding, respectively. During this period, the

females stayed preferentially at higher temperatures. There-

fore, it is not possible to affirm that females prefer to lay

their eggs at those temperatures because they could have

simply laid their eggs at the temperature where they pre-

ferred to stay. Apparently, this is the case for the oviposi-

tion of this species in relation to relative humidity (Guarneri

et al., 2002).

The results concerning thermopreference and the way in

which temperature affects the development of T. brasiliensis,

Fig. 7. Thermopreference for oviposition in females of Triatoma

brasiliensis. The data are the mean� SE of the eggs laid by two

groups of 12 and 11 females over a period of 17 and 24 days,

respectively.



together with the analysis of temperature measurements

taken in the field (Lorenzo et al., 2000), indicate that this

environmental parameter represents a limiting factor both

for the geographical distribution of this species and for the

microenvironment that these insects require. In this way,

T. brasiliensis appears to be an insect not only adapted to

hot and dry environments, but also very sensitive to low

temperatures because it does not develop at temperatures

below 20 �C, and it slightly decreases its thermopreference

to 29 �C only after a prolonged food deprivation.

Acknowledgements

We thank Dr Graciela Flores for correcting the English in

this manuscript. This work is a collaborative effort

supported by grants from the UNDP/World Bank/WHO

Special Program for Training in Tropical Diseases (TDR)

and from the CAPES (Brazil)� SETCIP (Argentina)

exchange programme. Experiments were also supported

by grants from CPqRR/FIOCRUZ, CNPq, CONICET

and the Universidad de Buenos Aires. This study is part of

a thesis to be submitted to the Instituto Oswaldo Cruz,

FIOCRUZ, Rio de Janeiro, Brazil, in partial fulfilment of

the requirements for a Doctoral degree.

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Accepted 13 March 2003



the effect of temperature on the behaviour and development of triatoma brasiliensis

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