Deslocamento Competitivo Triatoma

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Competitive displacement in Triatominae: the Triatoma infestans success Marcos H. Pereira1, Nelder F. Gontijo1, Alessandra A. Guarneri2, Maurı´cio R.V. Sant’Anna3 and Lile´ia Diotaiuti4 1 Departamento de Parasitologia do Instituto de Cieˆncias Biolo´gicas da Universidade Federal de Minas Gerais, Caixa Postal 486, 31270-901, Belo Horizonte, MG, Brazil 2 Departamento de Microbiologia e Parasitologia da Universidade Federal de Santa Catarina, Caixa Postal 476, 88.040-900, Floriano´polis, SC, Brazil 3 Molecular & Biochemical Parasitology Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK 4 Centro de Pesquisas Rene´ Rachou/Fiocruz, Caixa Postal 1743, 30190-901, Belo Horizonte, MG, Brazil

Brazil has just been certificated by Pan American Health Organization as ‘free of Chagas disease transmission due to Triatoma infestans’. During the early 1980s, this species of blood-sucking bug alone was considered responsible for approximately 80% of Chagas disease transmission. But it was not always so. The species originally abundant in houses of central and eastern Brazil was Panstrongylus megistus, which seems to have been progressively displaced from houses by T. infestans during the past century. Indeed, T. infestans seems able to displace other Triatominae in artificial environments. Recent studies suggest that it might simply be because T. infestans feeds more efficiently than its Triatominae competitors. Historic perspective Current theory holds that the blood-sucking bug Triatoma infestans originated from the Andean valleys of Bolivia, where sylvatic populations can still be found among rock piles associated with wild rodents [1]. Its original domestication in that region might have been associated with the hunting and domestication of wild guinea-pigs by preColumbian Andean cultures, but its subsequent dispersal through Argentina and Paraguay into southern Brazil is believed to have been in association with human migrations during the later part of the 19th century [2]. Entomological surveys following the work of Carlos Chagas in the early 1900s give no evidence for the presence of T. infestans in the central Minas Gerais state of Brazil. At that time, in Minas Gerais, T. infestans was present only in the south, near the border with Sa˜o Paulo state [3]. The scale of dispersal of T. infestans became evident following studies carried out in Bambuı´ (a mid-western region of Minas Gerais), where Panstrongylus megistus had previously been described as the main vector of Chagas disease. Although the first record of T. infestans in Bambuı´ was only in 1939, by the early 1940s T. infestans represented >90% of the triatomines collected inside houses Corresponding author: Pereira, M.H. ([email protected]). Available online 12 September 2006. www.sciencedirect.com

(J.C.P. Dias, PhD thesis, Federal University of Minas Gerais, 1982) [4]. Many of the earlier studies reported the co-existence of T. infestans and P. megistus in Minas Gerais [5–8], although in most of these, T. infestans presented greater densities. As T. infestans continued its northern dispersal in Brazil, reaching its greatest dispersion in 1981 [9] (Figure 1), it seemed to displace not only P. megistus but several other Triatominae such as T. sordida in central Brazil [10], and T. brasiliensis and T. pseudomaculata in parts of the northeast of Brazil. [9]. In those states where T. infestans was most abundant, Chagas disease prevalence exceeded the national average of 4.2%: in Minas Gerais (8.8%), Rio Grande do Sul (8.8%), Goia´s (7.4%) and Bahia (5.4%) [11]. Why was T. infestans so successful in displacing other Triatominae in Brazil? Population dynamics and intraspecific competition T. infestans, as well as other triatomine bugs (Hemiptera, Triatominae), are hematophagous insects in both adult and immature (first to fifth instars nymphs) stages and their principal hosts are birds and mammals. Because Triatominae are blood-feeding hemimetabolous insects, their life cycles and population dynamics depend primarily on their interactions with vertebrate hosts. In a domestic habitat, the number of triatomine bugs is related to the number of occupants because the nutritional status of the bugs depends on the number of insects per host [12,13]. The mean amount of blood taken by T. infestans and P. megistus from non-anesthetized hosts is inversely related to insect density [13,14]. Increased insect density causes an increased perception of bites by the host, which probably diminishes blood-meal size because of more frequent interruptions in feeding [15]. Such a reduction in blood intake leads to a prolonged nymphal development time, reduced egg laying and increased dispersal by adults. These factors combine to regulate insect population density [16]. A comparative study using non-anesthetized mice as hosts showed that T. infestans can ingest larger blood meals than P. megistus at different densities (Figure 2). This better

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individuals in a single house. Thus, T. infestans could displace P. megistus in areas where P. megistus already existed in stabilized domestic colonies. The colonization by T. infestans of houses already infested with indigenous triatomines was probably initiated by a few individuals transported passively in human belongings [19]. No direct interference has been observed between the two species when they have been reared together in the laboratory in the same recipient [20]. Peak activity of both species occurs within a few hours of nightfall [21] (H.H.R. Pires, unpublished) so competition between them might involve interactions with the host, as described above for intraspecific competition.

Figure 1. A map of the geographical distribution of Triatoma infestans taken from entomological surveys between 1975 and 1983 by the Chagas Disease Control Program (PCDCh). Sa˜o Paulo state was not included in the entomological surveys. Abbreviations of the Brazilian states: BA, Bahia; MG, Minas Gerais; RS, Rio Grande do Sul; SP, Sa˜o Paulo. Source: PCDCh/Sucan.

exploitation of blood resources might explain why T. infestans reaches greater densities than P. megistus inside human dwellings [17]. Interspecific competition The life cycle of T. infestans is shorter than that of P. megistus, and it needs smaller amounts of blood [18]. Such characteristics could provide T. infestans with a significant competitive advantage over P. megistus if the two species established populations with similar numbers of

Figure 2. The exploitation of the blood resource (weight gain) at different population densities after 24 h contact of third instar nymphs of Triatoma infestans (circles) and Panstrongylus megistus (squares) with non-anesthetized mice. The data were obtained from linear regressions of mean weight gain (mg) versus density from Ref. [17]. Bold lines correspond to experimental data and dotted lines correspond to estimates. www.sciencedirect.com

Feeding behaviour Triatomine bugs are vessel feeders, obtaining their blood meals directly from the blood vessels (venules or arterioles) of their vertebrate hosts. After the bug pierces the host skin, a probing period characterized by rapid whip-like intradermal movements of the maxillae can be observed. Once a suitable vessel is found, probing ceases and the bugs engorge [22]. The ingestion of blood through the food canal is aided by the cibarial pump, the movements of which are regulated by a complex of strong muscles occupying much of the head of the insect [23]. Parameters such as the negative pressures produced by the cibarial pump, the dimensions of the food canal, blood viscosity, and the size of host red cells and their capacity to deform can influence the ingestion rate [24]. Smith and Friend [25] created the standard technique for studying feeding behaviour in triatomines, on the basis of changes in electrical resistance between the insect and its feeding sources. Smith [26] and Guarneri et al. [27] improved this technique to record signals generated by the cibarial pump musculature, similar to an electromyogram. Further modifications of the technique enabled the feeding behaviour of early developmental stages to be recorded because contact involved placing the insect on a metal mesh rather than implanting or fixing electrodes to the thorax [28]. Total ingestion rate On the basis of the electrical signals methodology, several studies have demonstrated total ingestion rate (TI) to be the main parameter that determines contact time between a particular triatomine species and an immobilized host. TI values for fifth instar nymphs of the species studied to date vary from 3.2 mg/min for Rhodnius neglectus feeding on mice to 25.3 mg/min for T. infestans feeding on pigeons [27,29]. The highest TI values for feeding on mice are observed for T. infestans (13.8 mg/min) and R. prolixus (11.9 mg/min), which are the most important vectors of Chagas disease in South and Central America, respectively [27,29]. TI also varies considerably between different nymphal instars of the same species, for example, from 0.4 mg/ min for first instars to 10.6 mg/min for fifth instars of T. brasiliensis feeding on humans [28]. Contact time versus total ingestion rate Contact time with the host for nymphs of T. infestans, T. brasiliensis and T. pseudomaculata is strongly

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correlated (r2 = 0.92) with the ratio between the initial weight after moulting and the total ingestion rate (IW/ TI), which represents the time an insect requires to double its body weight by feeding on a specific type of host (Figure 3). For these species, the initial weight provides a good estimate of the size of the blood meal for the nymphs and is also a good estimate of the insect biomass, regardless of species or nymphal stage. The contact time is strongly correlated with the IW/TI ratio (Figure 3) so triatomines with higher IW/TI values will have more difficulty in maintaining a good nutritional status as population density increases because of their need for a longer contact time to complete the blood meal. The IW/TI values for these three species were lower for feeding on pigeons than on mice. First- and second-instar nymphs of T. brasiliensis fed more efficiently than other instars on human hosts. The same theory could be applied to explain differences between males and females [28]. A lower IW/TI ratio for females (10.8) would enable them to feed more efficiently than males (13.9), which might be an adaptation to increase their fitness in situations of nutritional stress. This theory is in agreement with observations that males have systematically lower qualitative nutritional status than females in T. infestans peridomestic populations from rural northwestern Argentina [30]. The reduced size of insects in high-density situations [10,31] might reflect a selection for individuals with a low IW/TI ratio that can feed more rapidly. Factors affecting total ingestion rate Monitoring the electrical activity of the cibarial pump to study triatomine feeding behaviour has enabled the total ingestion rate (TI) to be correlated with other parameters such as cibarial pump frequency (F), cibarial pump volume (QLC), contact time (CT) and non-ingestive time

Box 1. Parameters of feeding behavior Contact time [CT (min)] is defined as the time during which the mouthparts of the insect are inserted into the host skin. Total ingestion rate [TI (mg min1)] is calculated by dividing the weight gain (mg) by the total contact time (min). Cumulative probing time (PT) is the period from the insertion of the mouthparts into the host to the initiation of the engorgement phase. If the bug ends an initial probing and restarts another elsewhere, the first time is added to the second and so on successively; non-ingestive time [NIT (min)] is defined as the period when insects are not pumping, thus comprising probing time plus any interruption to feeding. The quantity of liquid ingested per cibarial contraction [QLC (ml contraction1)] is obtained by dividing the weight gain by the total number of cibarial pump contractions during the feeding process, considering blood and artificial diet densities (r) as 1 mg ml1. Pump frequency [F (contractions min1)] represents the number of cibarial pump contractions divided by the ingestive time (the time in which the pump is effectively working). These variables are linked by Equation I: TI ¼ QLC  F  r  ½ðCT  NIT Þ=CT 

[Eqn I]

(NIT: probing time plus interruptions during engorgement; see Box 1). The analysis of these parameters during feeding by different triatomine species on pigeons, mice, humans or artificial feeders has provided enough information to know whether differences were because of the vertebrate host, the triatomine species or the developmental stage [27–29]. The QLC and maximum pumping frequency (obtained by using artificial feeders) are related to the intrinsic characteristics of the mouthparts of the insect (morphology). In the triatomine species studied, QLC ranges from
25 nl in T. pseudomaculata to 100 nl in T. infestans. The QLC increases more gradually than the body weight and this asymmetrical growth is responsible for the increase in the

Figure 3. The correlation (r2 = 0.92) between the contact time of Triatominae instar nymphs with their vertebrates hosts and the IW:TI ratio (initial weight: total ingestion rate). Triatoma infestans, circles; Triatoma brasiliensis, squares; Triatoma pseudomaculata, triangles. Each point is labeled with the nymphal instar (1st to 5th) and the vertebrate host used as the blood meal source (human, mouse or pigeon). Adapted, with permission, from Ref. [28]. www.sciencedirect.com

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IW/TI ratio observed during nymphal development (Figure 3). There is a remarkable sexual dimorphism of the QLC, with that of the females being greater than that of males. Parameters such as F and NIT are influenced by the host physiology. Most of the triatomine species feeding on mice have a lower F value than those feeding on pigeons. The NIT values are variable. However, except for R. nasutus, the triatomines feeding on mice usually have a longer NIT. These facts might be related to hemostatic features of birds and mammals. Birds have thrombocytes that perform a similar function to mammalian platelets but are less effective. They also seem to lack some coagulation factors, particularly in the intrinsic system [32]. Experiments using salivarectomized R. prolixus showed that insects had increased difficulty in obtaining a blood meal from rabbits, as well as a prolonged probing time [33]. Although the probing time is reduced (usually < 10% of the contact time), it should be important in triggering the host responses. The insertion of the mouthparts, the movements of the maxillae and saliva deposition within the skin of the host lead to tissue damage, which is responsible for liberating mediators and exposing molecules that trigger hemostasis, inflammation and immunological reactions [34,35]. Saliva is continuously liberated during the feeding process [36] and has an important role in finding blood vessels during probing and keeping blood flowing through the feeding canal [37,34]. Comparative studies showed qualitative and quantitative differences in Triatominae salivary antihemostatic activity [38,39]. Activities of the apyrase enzyme and vasodilator, but not anticlotting agents, correlated with feeding efficiency of triatomines on rat [39]. Besides facilitating blood feeding, triatomine saliva inhibits the generation of nervous impulses, functioning in a similar way to local anaesthetics. This provides further confirmation of the importance of host perception in triatomine feeding success [40]. In summary, the mechanical and salivary characteristics of the insect and the host physiology determine the feeding performance of triatomines. The fact that T. infestans feeds more easily on birds could explain why bugs collected in goat and pig corrals had a lower qualitative nutritional status than those captured in chicken coops in Argentina [30]. The importance of feeding performance (IW/TI) On human hosts, the fifth instar nymph of T. infestans has a lower IW/TI ratio (4.1) than P. megistus (7.6; S.E. Barbosa et al., unpublished) and T. brasiliensis (6.3). A lower IW/TI ratio means a proportionally greater amount of blood ingested in the same contact time with the host. This would explain epidemiological findings in which T. infestans not only succeeds in establishing larger colonies but also displaces P. megistus and T. brasiliensis from human dwellings when it is introduced in areas where the other two species were already established. The existence of competition events among these species is supported by the findings that P. megistus [41] and T. brasiliensis (A.N. Ramos Jr, MSc thesis, Federal University of Rio de Janeiro, 2001) recolonized houses from sylvatic specimens after the elimination of T. infestans (a species only found in domestic and www.sciencedirect.com

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peridomestic environments in Brazil). Studies under laboratory conditions also showed competitive exclusion of T. sordida by T. infestans [42] that probably could be explained by a lower IW/TI ratio characteristic of T. infestans. Another implication of the better exploitation of blood resources by Triatominae is related to the dynamics of defecation and, consequently, the transmission of Trypanosoma cruzi. The defecation timing depends on both the triatomine species and the bloodmeal size because bugs with large blood meals tend to defecate quicker than those that have ingested smaller amounts [43]. Thus, the vectorial capacity of T. infestans might diminish less than that of P. megistus and T. brasiliensis as the population density increases because there is less of a reduction in bloodmeal size for T. infestans. Concluding remarks We propose that the great capacity for exploiting blood resources from available hosts in dwellings enabled T. infestans to spread and become the most important vector of T. cruzi in the south cone of South America. This proposal is in accordance with the central role of the insect–host interactions in the biology and vectorial capacity of Triatominae. Brazil is winning the battle against T. infestans. However, other indigenous species (especially T. brasiliensis and P. megistus) are capable of invading and colonizing houses. These ubiquitous species have been found in natural and artificial sites close to human dwellings and are associated with wild or peridomestic animals. In this scenario, it is important to understand how the features of the hosts (physiology, blood nutritional value and grooming behavior) frequently used as food sources interfere with Triatominae population dynamics to modulate its spatial distribution and predisposition to spread. Acknowledgements We thank C.J. Schofield for reviewing the manuscript. We also thank Bruce Alexander, Ricardo N. Araujo and Adriana Santos for their comments. This work was supported by CNPq, FAPEMIG, CPqRR/ FIOCRUZ and benefited from international collaboration through the ECLAT network.

References 1 Noireau, F. et al. (2005) Can wild Triatoma infestans foci in Bolivia jeopardize Chagas disease control efforts? Trends Parasitol. 21, 7–10 2 Schofield, C.J. (1988) The biosystematics of Triatominae. In Biosystematics of Haematophagus Insects (Service, M.W., ed.), pp. 284–312, Clarendon Press 3 Neiva, A. (1913) Informac¸o˜es sobre a biologia da Vinchuca. Triatoma infestans Klug. Mem. Inst. Oswaldo Cruz 5, 24–31 4 Dias, J.C.P. (1993) Cinqu¨enta anos de Bambuı´. Rev. Soc. Bras. Med. Trop. 26 (Suppl 2), 4–8 5 Martins, A.V. et al. (1951) Distribuic¸a˜o geogra´fica dos triatomı´neos e seus ı´ndices de infecc¸a˜o pelo T. cruzi no Estado de Minas Gerais. Arq. Sau´de Pu´bl. II, 63–79 6 Pellegrino, J. (1950) Novos dados sobre a distribuic¸a˜o de triatomideos e sua infecc¸a˜o pelo Schizotrypanum cruzi no Estado de Minas Gerais. Mem. Inst. Oswaldo Cruz 48, 639–667 7 Dias, E. (1955) Monthly variations of the incidence of developmental forms of Triatoma infestans and Panstrongylus megistus in Bambui. Minas Gerais. Mem. Inst. Oswaldo Cruz 53, 458–472 8 Dias, E. and Zeledo´n, R. (1955) Infestac¸a˜o domiciliaria em grau extremo por Triatoma infestans. Mem. Inst. Oswaldo Cruz 53, 473–486

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9 Silveira, A.C. et al. (1984) Distribuic¸a˜o de triatomı´neos capturados no ambiente domiciliar, no perı´odo 1975/83, no Brasil. Rev. Bras. Malariol. Doencas. Trop. 36, 15–312 10 Schofield, C.J. (1980) Nutritional status of domestic populations of Triatoma infestans. Trans. R. Soc. Trop. Med. Hyg. 74, 770–778 11 Vinhaes, M.C. and Dias, J.C.P. (2000) Doenc¸a de Chagas no Brasil. Cad. Saude Publica 16 (Suppl 2), 7–12 12 Schofield, C.J. (1980) Density regulation of domestic populations of Triatoma infestans in Brasil. Trans. R. Soc. Trop. Med. Hyg. 74, 761–769 13 Schofield, C.J. (1982) The role of blood intake in density regulation of populations of Triatoma infestans (Klug) (Hemiptera: Reduviidae). Bull. Entomol. Res. 72, 617–629 14 Piesman, J. et al. (1983) Host availability limits population density of Panstrongylus megistus. Am. J. Trop. Med. Hyg. 32, 1445–1450 15 Schofield, C.J. et al. (1986) Density dependent perception of triatomine bug bites. Ann. Trop. Med. Parasitol. 80, 351–358 16 Schofield, C.J. (1985) Population dynamics and control of Triatoma infestans. Ann. Soc. Belg. Med. Trop. 65 (Suppl. 1), 149–164 17 Pereira, M.H. et al. (1995) Triatoma infestans is more efficient than Panstrongylus megistus in obtaining blood meals on non anaesthetized mice. Mem. Inst. Oswaldo Cruz 90, 765–767 18 Szumlewicz, A.P. (1975) Laboratory colonies of triatomine, biology and population dynamics. In New Approaches in American Trypanosomiasis Research, International Symposium Proceedings, pp. 63-82, PAHO/WHO 19 Forattini, O.P. (1980) Biografia, origem e distribuic¸a˜o da domiciliac¸a˜o de triatomı´neos no Brasil. Rev. Sau´de Pu´bl. 14, 265–299 20 Dias, E. and Dias, J.C.P. (1968) Variac¸o˜es mensais da incideˆncia das formas evolutivas do Triatoma infestans e do Panstrongylus megistus no municı´pio de Bambuı´, Estado de Minas Gerais (IIa Nota: 1951 a 1964). Mem. Inst. Oswaldo Cruz 66, 209–226 21 Lorenzo, M.G. and Lazzari, C.R. (1998) Activity pattern in relation to refuge exploitation and feeding in Triatoma infestans (Hemiptera: Reduviidae). Acta Trop. 70, 163–170 22 Lavoipierre, M.M.J. et al. (1959) Studies on the methods of feeding of blood sucking arthropods: I. The manner in which triatomine bugs obtain their blood-meal, as observed in the tissues of the living rodent, with some remarks on the effect of the bite on human volunteers. Ann. Trop. Med. Parasit. 53, 235–252 23 Bennett-Clark, H.C. (1963) Negative pressures produced in the cibarial pump of the blood sucking bug, Rhodnius prolixus. J. Exp. Biol. 40, 223–229 24 Kingsolver, J.G. and Daniel, T.L. (1995) Mechanics of food handling by fluid-feeding insects. In Regulatory Mechanisms in Insect Feeding (Chapman, R.F. and De Boer, G., eds), pp. 32–73, Chapman & Hall 25 Smith, J.J.B. and Friend, W.G. (1970) Feeding in Rhodnius prolixus: responses to artificial diets as revealed by changes in electrical resistance. J. Insect Physiol. 16, 1709–1720

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26 Smith, J.J.B. (1979) Effect of diet viscosity on the operation of the pharyngeal pump in the blood-feeding bug Rhodnius prolixus. J. Exp. Biol. 82, 93–104 27 Guarneri, A.A. et al. (2000) Comparison of feeding behaviour of Triatoma infestans, Triatoma brasiliensis and Triatoma pseudomaculata in different hosts by electronic monitoring of the cibarial pump. J. Insect Physiol. 46, 1121–1127 28 Guarneri, A.A. et al. (2003) Blood-feeding performance of nymphs and adults of Triatoma brasiliensis on human hosts. Acta Trop. 87, 361–370 29 Sant’Anna, M.R.V. et al. (2001) Feeding behaviour of morphologically similar Rhodnius species: influence of medical characteristics and salivary function. J. Insect Physiol. 47, 1459–1465 30 Ceballos, L.A. et al. (2005) Feeding rates, nutritional status and flight dispersal potential of peridomestic populations of Triatoma infestans in rural northwestern Argentina. Acta Trop. 95, 149–159 31 Dujardin, J. et al. (1999) Changes in the sexual dimorphism of Triatominae in the transition from natural to artificial habitats. Mem. Inst. Oswaldo Cruz 94, 565–569 32 Lewis, J.H. (1996) Comparative Hemostasis in Vertebrates. Plenum 33 Ribeiro, J.M.C. and Garcia, E.S. (1981) The role of salivary glands in feeding in Rhodnius prolixus. J. Exp. Biol. 94, 219–230 34 Ribeiro, J.M.C. (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect. Agents Dis. 4, 143–152 35 Ribeiro, J.M.C. and Francischetti, I.M. (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu. Rev. Entomol. 48, 73–88 36 Soares, A.C. et al. (2006) Salivation pattern of Rhodnius prolixus (Reduviidae; Triatominae) in mouse skin. J. Insect Physiol. 52, 468–472 37 Law, J. et al. (1992) Biochemical insights, derived from diversity in insects. Annu. Rev. Biochem. 61, 87–112 38 Pereira, M.H. et al. (1996) Anticoagulant activity of Triatoma infestans and Panstrongylus megistus saliva (Hemiptera/Triatominae). Acta Trop. 61, 255–261 39 Ribeiro, J.M.C. et al. (1998) Role of salivary antihemostatic components in blood feeding by triatomine bugs (Heteroptera). J. Med. Entomol. 35, 599–610 40 Dan, A. et al. (1999) Action of the saliva of Triatoma infestans (Heteroptera: Reduviidae) on sodium channels. J. Med. Entomol. 36, 875–879 41 Villela, M.M. et al. (2005) Entomological surveillance for Chagas disease in the mid-western region of Minas Gerais State, Brazil, from 2000 to 2003. Cad. Saude Publica 21, 878–886 42 Oscherov, E.B. et al. (2004) Competition between vectors of Chagas disease, Triatoma infestans and T. sordida: effects on fecundity and mortality. Med. Vet. Entomol. 18, 323–328 43 Trumper, E.V. and Gorla, D.E. (1991) Density dependent timing of defaecation by Triatoma infestans. Trans. R. Soc. Trop. Med. Hyg. 85, 800–802