Biology of Triatoma carcavalloi Jurberg, Rocha & Lent, 1998 under laboratory conditions

Margareth Cardozo-de-Almeida Simone Caldas Teves Neves Carlos Eduardo de Almeida Nathanielly Rocha Casado de Lima Maria Luiza Ribeiro de Oliveira Jacenir Reis dos Santos-Mallet Teresa Cristina Monte Gonçalves About the authors

Abstract

Introduction

Triatoma carcavalloi is a wild species that is found in sympatry with Triatoma rubrovaria and Triatoma circummaculata, which are vectors of Trypanosoma cruzi currently found in rural areas of Rio Grande do Sul, Brazil.

Methods

Fertility was assessed and to determine the incubation period, the eggs were observed until hatching. The first meal was offered to 1st stage nymphs. The intermolt period was also determined. The number of blood meals was quantified at each nymphal stage and the resistance to fasting as the period between ecdysis and death. Mortality was assessed and longevity was determined by recording the time that elapsed from molting to the adult stage and until death. The developmental cycle was assessed by recording the length in days of each stage from molting to adult hood.

Results

The average incubation period was 22.7 days. The average first meal occurred 3.1 days after hatching. The 5th stage nymph to adult intermolting period was the longest at 193.4 days. The average number of feedings during nymphal development was 13.4. The resistance to fasting assay indicated that the 3rd, 4th and 5th stage nymphs presented higher resistance than did adults. The highest mortality rate was observed in the 3rd stage nymphs (22.2%). The average length of adult survival was 25.6 weeks, and the average total life cycle lasted 503.4 days.

Conclusions

This study is the first report on the biology of T. carcavalloi that fed on mice. The presented findings expand the bionomic knowledge of these species.

Triatominae; Triatoma carcavalloi ; Biological behavior


INTRODUCTION

The Brazilian State of Rio Grande do Sul harbors eleven species of triatomines, including introduced species with synanthropic habits. These insects are associated with bird nests, mammals and rocky habitats. They are considered autochthonous11. Ruas-Neto AL, Corseuil E. Hábitos, Distribuição Geográfica e Potencialidade dos triatomíneos rupestres como vetores da doença de Chagas no Rio Grande do Sul, Brasil (Hemiptera: Reduviidae: Triatominae). Entomol y Vect 2002; 9: 231-249. and are dispersed in a discontinuous pattern throughout the state, with some species restricted to the central-southern region and others in the northwest and northeast regions. Among the wild species of triatomines, Triatoma rubrovaria (Blanchard, 1843) is the most important in epidemiological terms due to its wide geographic distribution and capacity to transmit Trypanosoma cruzi (Chagas, 1909), followed by Triatoma circummaculata (Stål, 1859) and Triatoma carcavalloi (Jurberg, Rocha & Lent, 1998). These species are sympatric, inhabiting rocky environments and exhibiting feeding habits that are remarkably eclectic, with irregular intervals observed in their biological cycles22. Cardozo-de-Almeida MAR. Estudos morfológicos, morfométricos e ultraestruturais em cinco espécies do gênero Triatoma Laporte, 1832 (Hemiptera: Reduviidae: Triatominae) incluindo a biologia de Triatoma carcavalloi. [Dissertation]. [Rio de Janeiro]: Universidade Federal Rural do Rio de Janeiro 2007; 102 p.. Field data have shown that T. rubrovaria is frequently found in domiciliary and peridomiciliary areas33. Costa J, Lorenzo M. Biology, diversity and strategies for the monitoring and control of triatomines - Chagas disease vectors. Mem Inst Oswaldo Cruz 2009; 104 (supl I): 46-51.. Only T. carcavalloi has been observed in Canguçu, Dom Feliciano, Pinheiro Machado and São Jerônimo44. Bedin C, Mello F, Wilhelms TS, Torres MA, Estima C, Ferreira CF, et al. Vigilância Ambiental: Doença de Chagas no Rio Grande do Sul. Bol Epidemiologico 2009; 11:8. (Source: IPB-LACEN/RS), appearing inside domiciles throughout Rio Grande do Sul55. Martins LP, Castanho RE, Casanova C, Caravelas DT, Frias GT, Ruas-Neto AL, et al. Triatomíneos rupestres infectados por Trypanosomatidae, coletados em Quaraí, Rio Grande do Sul, 2003. Rev Soc Bras Med Trop 2006; 39:198-202.,66. Jurberg J, Rocha DS, Lorosa ES, Vinhaes MC, Lent H. Uma nova espécie de Triatoma do Estado do Rio Grande do Sul, Brasil (Hemiptera, Reduviidae, Triatominae). Entomol y Vect 1998; 5:295-310..

Morphological observations have led T. carcavalloi to be included in the same species complex (infestans complex) and subcomplex (rubrovaria subcomplex) as T. rubrovaria77. Oscherov EB, Bar ME, Damborsky MP, Milano AMF. Estadísticos poblacionales de Triatoma rubrovaria en condiciones de laboratório. Rev Saude Publica 2005; 39:211-216..

Characterizing the biology of wild species is important while evaluating the efficiency of these insects as vectors of T. cruzi, as these species consistently invade environments that are subject to human modification. As a result, knowledge of the biological characteristics of these insects is essential for designing control strategies, mainly in relation to secondary vectors that have the potential to become established in human habitats88. Schofield CJ. Population dynamics and control of Triatoma infestans. Ann Soc Belge Med Trop 1985; 65: 149-164..

The life cycles of triatomines vary according to the species, environmental conditions and the availability of suitable sources of blood99. Carbajal de la Fuente AL, Cunha V, Rocha NL, Lopes CM, Noireau F. Comparative biology of the two sister species of Triatominae (Hemiptera: Reduviidae). Rev Soc Bras Med Trop 2010; 43:15-18.,1010. Moreira CJC, Spata MCD. Dynamics of evolution and resistence to starvation of Triatoma vitticeps (Stål, 1859) (Reduviidae: Triatominae), submitted to two different regimens of food deprivation. Mem Inst Oswaldo Cruz 2002; 97:1049-1055..

Resistance to fasting could be of great importance and might directly affect control campaigns targeting these vectors1111. Cabello DR. Resistance to Starvation of Rhodnius neivai Lent, 1953 (Hemiptera: Reduviidae: Triatominae) under Experimental Conditions. Mem Inst Oswaldo Cruz 2001; 96:587-591.. Tolerance to long periods of fasting helps these insects survive difficult periods when food shortages occur. During these periods, they hide in wall cracks and escape residual insecticides1212. Rocha DS, Galvão C, Jurberg J. Biologia do Rhodnius pictipes Stål, 1872 em condições de laboratório (Hemiptera, Reduviidae, Triatominae). em Inst Oswaldo Cruz 1994; 89:265-270., after which they are able to recolonize the household.

The aim of this study was to examine the bionomic features of Triatoma carcavalloi under laboratory conditions, including incubation time, fertility, first meal of the 1st stage nymphs, intermolt period, number of blood meals, resistance to starvation, mortality, longevity and developmental cycle to better understand its potential capacity as a vector and to use this knowledge to help monitor this species during control activities.

METHODS

Specimens of T. carcavalloi were collected in the State of Rio Grande do Sul, Brazil, in Encruzilhada do Sul City (30°32′38″S; 52°31′19″W), from natural ecotopes and peri-household locations. The insects were maintained at 26°C under 70% RH (relative humidity) in the Laboratory of Transmissores de Leishmanioses, Department of Entomologia Médica e Forense, Oswaldo Cruz Institute, Fundação Oswaldo Cruz.

Fertility

Sixteen females were individually separated into Borrel tubes closed with nylon mesh and observed daily, and the color of their eggs and whether they hatched was recorded.

Incubation period

Sixty eggs from eight females were separated into Borrel tubes closed with nylon mesh (according to the laying date) and then observed daily until they hatched.

First meal

Thirty eggs were individually housed in Borrel tubes. After hatching, a blood meal from a Swiss mouse was offered to each nymph within 10 minutes.

Intermolt period

Fifty nymphs from each stage, as well as 15 males and 15 females, were separated and placed in individual plastic containers (5.5cm in diameter × 10.5cm in height) containing individuals from the same day of hatching or ecdysis. Filter paper was used to cover the inner surface of the container. The specimens were observed daily from ecdysis until the next stage. The intermolt period was noted as the number of days between two consecutive ecdysis events, and the period of nymphal development was recorded as the number of days between the hatching date and ecdysis into the imago stage.

Number of blood meals according to the nymphal stage

The number of blood meals taken during each nymphal stage was quantified. A blood meal was provided once a week until repletion.

Resistance to fasting

The period between ecdysis and the death of the insect was recorded. The insects fed on mice (Mus musculus) weekly for a period of 60-80 minutes. After ecdysis, the specimens were separated into the nymphs of each phase (n = 50) and adults (n = 30) and stored in Borrel tubes with other individuals from the same day of ecdysis. The specimens were observed daily over the period from ecdysis to death.

Mortality

In total, 177 1st stage nymphs were separated, and the mortality was calculated according to the molting of each nymphal stage up to adulthood.

Longevity

The time elapsed from the molting of each individual to the adult stage until its death was recorded.

Developmental cycle

Sixty eggs laid by females of T. carcavalloi obtained from the colony maintained in the laboratory were collected by randomly selection and individually placed in plastic containers that contained filter paper to provide the developing insects with access to a food source. Each container was numbered and examined daily until the egg hatched. The nymphs were observed daily and fed on mice weekly until repletion, and the time required to pass through the various developmental stages and reach adulthood was recorded in days. The development times (total and by stage) were expressed using average values.

RESULTS

Fertility

The first oviposition was observed on day 6. The mean number of eggs/week was 30. The greatest number of eggs/week was observed during the summer. It is important to note that the eggs that did not hatch were also fertile, as the coloring was the same for all eggs. The eggs were initially light pink and then became red, which intensified as the process of embryogenesis progressed. The eggs exhibited an ellipsoid shape and adhered to the substrate. The oviposition of these females began after the first meal.

Incubation period

The mean incubation period of the specimens was 22.7 days, with a minimum of 21 and a maximum of 26 days recorded. Among the 60 eggs observed, only 38.3% hatched.

First meal

The 1st stage nymphs obtained their first meal after a mean of 24 days. The first meal occurred during the other nymphal stages after a mean of 3.1 days, with a recorded minimum value of one day and a maximum of five days, although the majority occurred after two or four days.

Intermolting period

Among the 50 nymphs observed, eight died before reaching adulthood (three 1st stage nymphs, four 2nd stage nymphs and one 3rd stage nymph). Table 1 shows that the shortest intermolting period was observed between the 1st/2nd stages (18.5 days) and the longest between the 5th stage/adulthood (193.4 days). The 5th stage nymphs required several blood meals to molt, which occurred after more than one year.

TABLE 1 -
Intermolting period of Triatoma carcavalloi.

Number of blood meals

The minimum number of blood meals observed in females and males were zero and one meal, respectively, whereas the maximum number (42 meals) was recorded in the 5th stage nymphs. The mean number of feedings throughout all of nymphal development was 13.4 meals (Figure 1).

FIGURE 1 -
The number of blood meals according to the stage of Triatoma carcavalloi.

Resistance to fasting

Observations of all of the nymphal and adult (male and female) stages indicated that the 3rd, 4th and 5th stage nymphs presented greater resistance than did the adults, whereas the males displayed similar resistance to the 1st and 2nd stage nymphs and were less resistant overall than were the females (Table 2). The total observation period was 8 months.

TABLE 2 -
Resistance to fasting in Triatoma carcavalloi (days).

Mortality

From the initial 177 Triatoma carcavalloi nymphs, only 95 reached the adult stage (global mortality rate of 57.2%). The mortality rate for each stage varied from 4.0 to 22.2%. The highest mortality rate was recorded in the 3rd (22.2%) stage nymphs, followed by the 2nd (14%) stage nymphs (Table 3).

TABLE 3 -
Mortality of Triatoma carcavalloi.

Longevity

The mean adult survival was 25.6 weeks (n = 42). Males presented a longer life span, with a mean survival of 25.6 weeks, whereas females presented a life span of 23.1 weeks.

Table 4 shows developmental cycle: The total T. carcavalloi life cycle lasted 503.4 days (72 weeks). Differences were observed for the 5th stage nymphs, whose development lasted a mean of 193.43 days (27 weeks).

TABLE 4 -
Duration of the developmental cycle of Triatoma carcavalloi.

DISCUSSION

Several authors have highlighted the importance of studying the bionomic features of triatomines under laboratory conditions to increase the biological knowledge of these species, improve breeding conditions for the development of laboratory colonies, and provide recommendations to support control measures1313. Galvão C, Jurberg J, Lent H. Resistência ao jejum de Triatoma nitida Usinger, 1939 em laboratório (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz 1996; 91:639-640.1616. Silva IG. Influência da temperatura na biologia de 18 espécies de triatomíneos (Hemiptera: Reduviidae) e no xenodiagnóstico. [Thesis]. [Curitiba]: Universidade Federal do Paraná 1985; 169 p..

Under laboratory conditions, which generally involve more stable abiotic factors, vital cycles are generally shorter1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520.. Nevertheless, certain species may present a longer life cycle. For example, the diapause of 5th stage nymphs has been recorded in several wild species1818. Ruas-Neto AL. Aspectos morfológicos, distribuição geográfica, hábitos e importância vetorial de Triatoma carcavalloi Jurberg, Rocha & Lent, 1998, Triatoma circummaculata (Stål, 1859) e Triatoma rubrovaria (Blanchard, 1843), triatomíneos rupestres do Rio Grande do Sul (Hemiptera:Reduviidae:Triatominae). [Thesis]. [Porto Alegre]: Pontifícia Universidade Católica do Rio Grande do Sul 2002; 108p. and was observed in this study, as fifth-stage nymphs of the examined species require several blood meals to permit molting, which can lengthen this phase up to a year. Similar findings have been reported for T. rubrovaria, T. carcavalloi and T. circummaculata1919. Ruas-Neto AL, Corseuil E, Cavalleri A. Development of rupestrian triatomines (Hemiptera: Reduviidae: Triatominae) following hemolymphagy on blaberids (Blattodea: Blaberidae) in Rio Grande do Sul State, Brazil. Entomol y Vect 2001; 8:205-216..

The first study on the biological cycle of T. carcavalloi under laboratory conditions involved allowing the insects to feed on pigeons, blaberids and lizards2020. Lorosa ES, Jurberg J, Souza ALA, Vinhaes MC, Nunes IM. Hemolinfa de Dictyoptera na manutenção do ciclo biológico silvestre de Triatoma rubrovaria (Blanchard, 1843) e Triatoma circummaculata (Stål, 1859) (Hemiptera, Reduviidae, Triatominae). Entomol y Vect 2000; 7:287-296.. Other authors have studied the biological cycles of T. rubrovaria and T. circummaculata fed the hemolymph of Blattodea (cockroaches) to assess nymphal development2121. Lorosa ES, Nunes IM, Vinhaes MC, Esteves-de-Andrade R, Jurberg J. Preferência alimentar de algumas espécies de Triatomíneos capturados no estado do Rio Grande do Sul, Brasil, com auxílio da técnica de precipitina e grau de infectividade. Entomol y Vect 2000; 7:211-225.. These studies suggested that this type of food may be naturally exploited by these triatomine species and most likely represents a means of surviving under natural conditions. The dependence on hemolymph is obvious in T. circummaculata, as this species does not develop into a 1st stage nymph in the laboratory if this food source is not available11. Ruas-Neto AL, Corseuil E. Hábitos, Distribuição Geográfica e Potencialidade dos triatomíneos rupestres como vetores da doença de Chagas no Rio Grande do Sul, Brasil (Hemiptera: Reduviidae: Triatominae). Entomol y Vect 2002; 9: 231-249.,55. Martins LP, Castanho RE, Casanova C, Caravelas DT, Frias GT, Ruas-Neto AL, et al. Triatomíneos rupestres infectados por Trypanosomatidae, coletados em Quaraí, Rio Grande do Sul, 2003. Rev Soc Bras Med Trop 2006; 39:198-202.. Certain species of triatomines display rather eclectic eating habits under natural conditions2222. Di Primio R. Sobre o Triatoma rubrovaria (Blanchard, 1843) no Rio Grande do Sul. Rev Med Rio Grande do Sul 1953; p. 402-408..

Triatoma rubrovaria develops well under laboratory conditions at temperatures between 20°C and 30°C and a relative humidity maintained at approximately 80%. The various life cycle times were recorded for the two sexes. Males survived for an average of 115.37 days, whereas females survived for an average of 99.6 days1616. Silva IG. Influência da temperatura na biologia de 18 espécies de triatomíneos (Hemiptera: Reduviidae) e no xenodiagnóstico. [Thesis]. [Curitiba]: Universidade Federal do Paraná 1985; 169 p.,2323. Perlowagora-Szumlewicz A. Estudos sobre a biologia do Triatoma infestans, o principal vetor da doença de Chagas no Brasil (importância de algumas de suas características biológicas no planejamento de esquemas de combate a esse vetor). Rev Bras Malariol D Trop 1969; 21:117-159.. The influence of temperature (25°C and 30°C) on T. rubrovaria was studied, and faster development was observed at 30°C1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520.. In the present study, temperatures equal to or higher than 28°C influenced the development of T. carcavalloi, resulting in a shorter life cycle compared to that of T. rubrovaria.

In studies examining the life cycle of T. infestans2424. Feliciangeli D, Rabinovich J, Fernandez E. Resistencia al ayuno em triatominos (Hemiptera, Reduviidae) Venezolanos. I. Rhodnius prolixus Stål. Rev Inst Trop São Paulo 1980; 22:53-61. and the resistance to fasting in Rhodnius prolixus2525. Argüello NV, Mischis CC, Civitta G, Bonino EE. Ciclo biológico de Triatoma rubrovaria (Blanchard, 1843) (Reduviidae, Triatominae) em laboratório. Rev Bras Zool 1988; 5:245-251., the authors suggested that the blood meal represents an essential condition for oviposition in general and fertility in particular. In a study of T. rubrovaria, it is not known whether the low rate of hatching was due to these factors because the experimental specimens were fed once a week for an hour, without establishing the amount of blood ingested by each individual2626. Cabello DR, Lizano E. Biology of Triatoma flavida Neiva, 1911 (Hemiptera:Reduviidae) under Laboratory Conditions. Mem Inst Oswaldo Cruz 2001; 96:879-881.. In the present study, the feeding was standardized, with T. carcavalloi being fed mice once a week until repletion. Therefore, we cannot conclude whether the low rate of hatching recorded was due to food or other factors, such as temperature and humidity, present under the laboratory conditions.

In our experiments, not all of the eggs hatched, indicating that fertility was compromised or that small variations in temperature or humidity (which are known to influence development directly) or some other unknown cause limited hatching.

The hatching incidence varies among species of the Triatoma genus and even within the same species. In T. carcavalloi, the obtained rate of 38.3% is considered low compared to those of Triatoma flavida, in which 93% of eggs have been reported to hatch2727. Gonçalves TCM, Cunha V, Oliveira E, Jurberg J. Alguns aspectos da biologia de Triatoma pseudomaculata Côrrea & Espínola, 1964, em condições de laboratório (Hemiptera: Reduviidae: Triatominae). Mem Inst Oswaldo Cruz 1997; 92:275-280.; T. pseudomaculata, with a rate was 88.3%2828. Damborsky MP, Bar ME, Gorla D. Life cycle and reproductive patterns of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) under constant and fluctuating conditions of temperature and humidity. Rev Soc Bras Med Trop 2005; 38:433-437.; and T. rubrovaria2929. Zeledón R, Guardia VM, Zúñiga A, Swartzwelder JC. Biology and ethology of Triatoma dimidiata (Latreille, 1811). I. Life cycle, amount of blood ingested, resistance to starvation, and size of adults. J Med Entomol 1970; 7:313-319., Triatoma dimidiata3030. Rabinovich JE. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions. I. Triatoma infestans Klug. J Med Ent 1972; 9:351-370., T. infestans3131. Feliciangeli MD, Rabinovich J. Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions. II. Triatoma maculata. J Med Entomol 1985; 22:43-48., T. maculata3232. Braga MV, Pinto ZT, Lima MM. Life cycle and reproductive patterns of Triatoma rubrofasciata (De Geer, 1773) (Hemiptera: Reduviidae), under laboratory conditions. Mem Inst Oswaldo Cruz 1998; 93:539-542., Triatoma rubrofasciata3333. Martínez-Ibarra JA, Katthain-Duchateau G. Biology of Triatoma pallidipennis (Stål, 1872) (Hemiptera: Reduviidae: Triatominae) under laboratory conditions. Mem Inst Oswaldo Cruz 1999; 94:837-840. and Triatoma pallidipennis3434. Rocha DS, Jurberg J, Carcavallo RU, Presgrave OAF, Cunha V, Galvão C. Influência da temperatura e umidade no desenvolvimento ninfal de Rhodnius robustus. Rev Saude Pub 2001; 35:400-406., in which rates range from 60 to 80%. In the Rhodnius genus, temperature was observed to influence not only the incubation period but also the incidence of hatching, as shown for R. robustus3535. Gonçalves TCM, Victorio VNM, Jurberg J, Cunha V. Biologia do Triatoma vitticeps (Stål, 1859) em condições de laboratório (Hemiptera, Reduviidae, Triatominae) I. Ciclo evolutivo. Mem Inst Oswaldo Cruz 1988; 83:519-523..

The average incubation period reported for T. rubrovaria is 24.84 days2626. Cabello DR, Lizano E. Biology of Triatoma flavida Neiva, 1911 (Hemiptera:Reduviidae) under Laboratory Conditions. Mem Inst Oswaldo Cruz 2001; 96:879-881., whereas the incubation period recorded for T. carcavalloi in the present study was 22.7 days.

In this study, the search for the first meals of the 1st stage nymphs of T. carcavalloi showed a higher frequency on days 2 and 4, similar to results reported for T. pseudomaculata2828. Damborsky MP, Bar ME, Gorla D. Life cycle and reproductive patterns of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) under constant and fluctuating conditions of temperature and humidity. Rev Soc Bras Med Trop 2005; 38:433-437. but different from that of Triatoma vitticeps, which shows a preference for days 3, 6 and 103636. Gomes AB, Silva IG. Influência da temperatura na biologia de triatomíneos. XXI. Triatoma jurbergi Carcavallo, Galvão & Lent, 1998 (Hemiptera, Reduviidae). Rev Patol Trop 2000; 29:85-93..

It is important to manage newly fed triatomines carefully because improper handling is a major cause of mortality during their development1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520.,3737. Almeida CE, Folly-Ramos E, Agapito-Souza R, Magno-Esperança G, Pacheco RS, Costa J. Triatoma rubrovaria (Blanchard, 1843) (Hemiptera, Reduviidae, Tiratominae). IV: bionomic aspects on the vector capacity of nymphs. Mem Inst Oswaldo Cruz 2000; 100:231-235..

The T. carcavalloi life cycle requires an average of 13.4 blood meals, which is higher than the values reported for T. rubrovaria (11.1)3838. Soares RP, Evangelista LG, Laranja LS, Diotaiuti L. Population dynamics and feeding behavior of Triatoma brasiliensis and Triatoma pseudomaculata, main vectors of Chagas disease in Northeastern Brazil. Mem Inst Oswaldo Cruz 2000; 95: 151-155., Triatoma vitticeps (8)3636. Gomes AB, Silva IG. Influência da temperatura na biologia de triatomíneos. XXI. Triatoma jurbergi Carcavallo, Galvão & Lent, 1998 (Hemiptera, Reduviidae). Rev Patol Trop 2000; 29:85-93. and Triatoma brasiliensis (11)3939. Gonçalves TCM, Victorio VMN, Jurberg J, Cunha V. Biologia do Triatoma vitticeps (Stål, 1859) em condições de laboratório (Hemiptera, Reduviidae, Triatominae) I. Resistência ao jejum. Mem Inst Oswaldo Cruz 1989; 84:131-134. but lower than the value reported for T. pseudomaculata (14.7)2828. Damborsky MP, Bar ME, Gorla D. Life cycle and reproductive patterns of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) under constant and fluctuating conditions of temperature and humidity. Rev Soc Bras Med Trop 2005; 38:433-437.. However, differences in the experimental conditions used by the various authors must be considered. We also must consider that these species live in distinct habitats and exhibit different feeding habits. Females of T. pseudomaculata make up for the lower amount of blood ingested by seeking out food sources quickly and consuming a larger number of blood meals2828. Damborsky MP, Bar ME, Gorla D. Life cycle and reproductive patterns of Triatoma rubrovaria (Blanchard, 1843) (Hemiptera: Reduviidae) under constant and fluctuating conditions of temperature and humidity. Rev Soc Bras Med Trop 2005; 38:433-437.. The 5th stage nymphs of T. carcavalloi require several feedings to perform ecdysis.

The average intermolt period of the 2nd stage nymphs of T. rubrovaria was longer than that of the 3rd stage nymphs3838. Soares RP, Evangelista LG, Laranja LS, Diotaiuti L. Population dynamics and feeding behavior of Triatoma brasiliensis and Triatoma pseudomaculata, main vectors of Chagas disease in Northeastern Brazil. Mem Inst Oswaldo Cruz 2000; 95: 151-155.. Triatoma brasiliensis, under standard temperature conditions, tends to show a crescent-shaped scale of intermolt periods from the 1st stage to the 5th stage nymphs1515. Rodrigues VLCC, Ferraz Filho AN, Silva EOR. Triatoma rubrovaria (Blanchard, 1843): tábua das ninfas, duração das formas e oviposição das fêmeas. Rev Soc Bras Med Trop 2005; 38:251-254.,1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520., which corroborates our findings.

One of the barriers to successfully combating the vectors of Chagas disease (using insecticides with residual action) is the capacity of these insects to resist fasting4040. Juarez E, Silva EPC. Comportamento do Triatoma sordida em condições de laboratório. Rev Saude Publica 1982; 16 (suppl):1-35.. Nymphs tolerate longer fasting periods than do adults1818. Ruas-Neto AL. Aspectos morfológicos, distribuição geográfica, hábitos e importância vetorial de Triatoma carcavalloi Jurberg, Rocha & Lent, 1998, Triatoma circummaculata (Stål, 1859) e Triatoma rubrovaria (Blanchard, 1843), triatomíneos rupestres do Rio Grande do Sul (Hemiptera:Reduviidae:Triatominae). [Thesis]. [Porto Alegre]: Pontifícia Universidade Católica do Rio Grande do Sul 2002; 108p., confirming that our findings indicate a compensation mechanism for the higher dispersion capacity of adults2525. Argüello NV, Mischis CC, Civitta G, Bonino EE. Ciclo biológico de Triatoma rubrovaria (Blanchard, 1843) (Reduviidae, Triatominae) em laboratório. Rev Bras Zool 1988; 5:245-251..

The ability to resist fasting increased in T. carcavalloi from the 1st to the 5th nymphal stage. During the adult phase, lower resistance was observed in males compared to females, corroborating data obtained at a temperature of 30°C for T. rubrovaria1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520. and T. sordida4141. Almeida CE, Francischetti CN, Pacheco RS, Costa J. Triatoma rubrovaria (Blanchard, 1843) (Hemiptera-Reduviidae-Triatominae). III: Patterns of feeding, defecation and resistance to starvation. Mem Inst Oswaldo Cruz 2003; 98:761-768.. These results contradict results reported for T. vitticeps4040. Juarez E, Silva EPC. Comportamento do Triatoma sordida em condições de laboratório. Rev Saude Publica 1982; 16 (suppl):1-35. and T. rubrovaria4242. Perlowagora-Szumlewicz A. Ciclo evolutivo do Triatoma infestans em condições de laboratório. Rev Bras Malar 1953; 5:35-47., in which males display a higher resistance to fasting.

In the present study the mortality rate was higher in the 3rd stage nymphs of T. carcavalloi (22.2%), corroborating the rate observed in T. rubrovaria88. Schofield CJ. Population dynamics and control of Triatoma infestans. Ann Soc Belge Med Trop 1985; 65: 149-164. When nymphs of T. infestans were fed at longer intervals, their mortality rate increased, indicating the influence of feeding on nymphal mortality2424. Feliciangeli D, Rabinovich J, Fernandez E. Resistencia al ayuno em triatominos (Hemiptera, Reduviidae) Venezolanos. I. Rhodnius prolixus Stål. Rev Inst Trop São Paulo 1980; 22:53-61.,4343. Dias JCP. Observações sobre o comportamento de triatomíneos brasileiros frente ao jejum, em laboratório. Rev Bras Malariol D Trop 1965; 17:55-63..

In this study, the higher longevity was observed in T. carcavalloi males, as was also observed in T. rubrofasciata3333. Martínez-Ibarra JA, Katthain-Duchateau G. Biology of Triatoma pallidipennis (Stål, 1872) (Hemiptera: Reduviidae: Triatominae) under laboratory conditions. Mem Inst Oswaldo Cruz 1999; 94:837-840. and T. rubrovaria88. Schofield CJ. Population dynamics and control of Triatoma infestans. Ann Soc Belge Med Trop 1985; 65: 149-164.,1717. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bull American Mus Nat Hist 1979; 163:125-520.,2626. Cabello DR, Lizano E. Biology of Triatoma flavida Neiva, 1911 (Hemiptera:Reduviidae) under Laboratory Conditions. Mem Inst Oswaldo Cruz 2001; 96:879-881.,2929. Zeledón R, Guardia VM, Zúñiga A, Swartzwelder JC. Biology and ethology of Triatoma dimidiata (Latreille, 1811). I. Life cycle, amount of blood ingested, resistance to starvation, and size of adults. J Med Entomol 1970; 7:313-319.. The longevity of T. carcavalloi females was found to be higher when they were fed pigeons, suggesting a likely influence of feeding1919. Ruas-Neto AL, Corseuil E, Cavalleri A. Development of rupestrian triatomines (Hemiptera: Reduviidae: Triatominae) following hemolymphagy on blaberids (Blattodea: Blaberidae) in Rio Grande do Sul State, Brazil. Entomol y Vect 2001; 8:205-216..

The developmental cycle of the fifth stage nymphs of T. carcavalloi fed with pigeons lasted an average of 259.67 days1919. Ruas-Neto AL, Corseuil E, Cavalleri A. Development of rupestrian triatomines (Hemiptera: Reduviidae: Triatominae) following hemolymphagy on blaberids (Blattodea: Blaberidae) in Rio Grande do Sul State, Brazil. Entomol y Vect 2001; 8:205-216., in contrast to the findings of the present study, in which this species was fed mice and showed an average developmental cycle of 193.43 days. The total life cycle of T. rubrovaria has been reported to be approximately 300 days2929. Zeledón R, Guardia VM, Zúñiga A, Swartzwelder JC. Biology and ethology of Triatoma dimidiata (Latreille, 1811). I. Life cycle, amount of blood ingested, resistance to starvation, and size of adults. J Med Entomol 1970; 7:313-319., whereas a much longer duration was observed in T. carcavalloi in the present study (503.4 days).

Our results suggest that biological traits are important criteria for determining the relationships between the Triatoma carcavalloi, Triatoma circummaculata and Triatoma rubrovaria species in the presence of the same food source and climatization and based on specimens collected in domiciles in State of Rio Grande do Sul, Brazil.

The efficacy of vector control campaigns has been impaired by the resistance to fasting. This resistance allows these animals to remain in their shelters, free from insecticides and sometimes even from their residual effects, thereby increasing the possibility of later recolonization by the remaining individuals[12,14,42,44-47].

The capacity for transmission observed in T. carcavalloi is as high as that of T. rubrovaria, whereas T. circummaculata is infected less often11. Ruas-Neto AL, Corseuil E. Hábitos, Distribuição Geográfica e Potencialidade dos triatomíneos rupestres como vetores da doença de Chagas no Rio Grande do Sul, Brasil (Hemiptera: Reduviidae: Triatominae). Entomol y Vect 2002; 9: 231-249., most likely because it feeds on mammals less frequently. These data together with the results of this study demonstrate the need for constant entomological surveillance of T. carcavalloi.

ACKNOWLEDGMENTS

We thank Dra. Célia Lammerhist and MSc. Cleonara Bedin for support during the field collection of triatomines.

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  • FINANCIAL SUPPORT
    Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Publication Dates

  • Publication in this collection
    May-Jun 2014

History

  • Received
    27 Feb 2014
  • Received
    18 June 2014
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