Infestation of arboreal nests of coatis by triatomine species, vectors of Trypanosoma cruzi, in a large Neotropical wetland

Vol. 40, no. 2 Journal of Vector Ecology 379 nfestation of arboreal nests of coatis by triatomine species, vectors of Trypanosoma cruzi, in a large Neotropical wetland Juliane Saab de Lima ¹, Fabiana Lopes Rocha²,3, Fernanda oreira Alves 3, Elias Seixas Lorosa 4, Ana aria Jansen 3, and Guilherme de iranda ourão 5 ¹Programa de Pós-graduação em Ecologia e Conservação, Universidade Federal de ato Grosso do Sul, Campo Grande S, Brazil 2 Programa de Pós-graduação em Ecologia e onitoramento Ambiental - PPGEA Universidade Federal da Paraíba. Campus V - Litoral Norte. Rua da angueira s/n. Centro. Rio Tinto, PB, 58.297-000, Brazil 3 Laboratório de Biologia de Tripanosomatídeos, Fundação Oswaldo Cruz, FOCRUZ. Av. Brasil 4365. Pav. Rocha Lima 518. Rio de Janeiro, RJ, 21045-900, Brazil 4 Laboratório Nacional e nternacional de Referência em Taxonomia de Triatomíneos, Departamento de Entomologia, Fundação Oswaldo Cruz. Av. Brasil 4365, Rio de Janeiro, RJ, 21045-900, Brazil 5 Laboratório de Vida Selvagem, Embrapa Pantanal, Rua 21 de Setembro, 1880, Corumbá, S, 79320-900, Brazil, guilherme.mourao@embrapa.br Received 1 June 2015; Accepted 10 August 2015 ABSTRACT: The coati (Nasua nasua, Carnivora) is a medium-sized mammal common in the Pantanal of Brazil. Unlike most mammals, coatis construct arboreal nests used for resting and reproduction. n this region, the coati is an important host of Trypanosoma cruzi, the causative agent of Chagas disease. There are two possible routes through coatis can be infected by T. cruzi: the oral route or the vectorial route. However, the relative importance of each of these routes in the infection of coatis and its role in the sylvatic cycle of the parasite are unknown. Our objectives were to investigate: (i) whether coati nests were infested by triatomine bugs, (ii) what species were frequent in the nests, (iii) whether the triatomines in nests were infected by T. cruzi, and (iv) what were the food resources of these triatomines. Eight of the 24 nests sampled were infested with triatomines, a total of 37 specimens of at least two species ( stali and sordida). n one nest, R. stali and T. sordida co-occurred and both fed on multiple resources, including coatis. This is the first report of triatomines occurring in arboreal nests of coatis. The co-occurrence of two different genera of triatomine vectors and coatis within the limited space of the coati nests provide multiple opportunities for the exchange of the protozoan parasite through both the vectorial and oral transmission routes. Journal of Vector Ecology 40 (2): 379-385. 2015. Keyword ndex: Brown-nosed coati,,, Pantanal, neglected diseases, Trypanosoma. NTRODUCTON The flagellate protozoan Trypanosoma cruzi is the etiological agent of Chagas disease, a neglected tropical disease that represents a serious public health problem in Latin America. The T. cruzi transmission cycle is a complex system that involves different components comprising the protozoan parasite, many mammalian host species, and dozens of triatomine species, the insect vectors (Noireau et al. 2009). There are several recent reports pointing to the colonization of houses by sylvatic triatomine species, which limits the effectiveness of control programs based on insecticides (Almeida et al. 2009, Guhl et al. 2009, Grijalva et al. ). Observations on the ecology and behavior of triatomine sylvatic populations and their interactions with mammalian hosts are fundamental to understanding the ecological factors involved in the maintenance of the enzootic cycle of the T. cruzi in nature and the dynamics of triatomine species. However, natural ecotopes for some triatomine species are widely acknowledged (Gaunt and iles 2000) and few studies have focused on the specific relationship with mammalian hosts. n the Chaco region, and species are T. cruzi vectors with a large distribution and they are the main species responsible for parasite transmission in domestic, peridomestic, and sylvatic environments (atias et al. 2003, Justi et al. 2010, Rolón et al. 2011). are usually associated with palm species (Abad-Franch and onteiro 2007, Dias et al. 2010, 2014, Gaunt and iles 2000, Justi et al. 2010), while are more related to terrestrial rocky habitats, rodent burrows, or bird nests (iles et al. 1981, Noireau et al. 2005). The extent of niche overlap between triatomine species is well documented. Although infrequent observations have found mixed infestation of triatomines in domestic and peridomestic environments (Feliciangeli et al. 2004), only one single species is generally present in one type of ecotope (Canale et al. 2000). The recognized T. cruzi sylvatic mammalian hosts include species of eight orders: Artiodactyla, Carnivora, Chiroptera, Cingulata, Didelphimorphia, Pilosa, Primates, and Rodentia (Noireau et al. 2009, Jansen and Roque

380 Journal of Vector Ecology December 2015 2010). nfections of mammals can occur either through the vectorial contaminative route or through the oral route. The vectorial contaminative route is believed to be inefficient, and in humans it could take about 1,700 (95% C=900-4,000) contacts between the bug and the person for an infection to occur (Nouvellet et al. 2013). The oral route is highly efficient and might occur by the ingestion of infected bug feces, food contaminated with the parasite or by preying on infected bugs or mammals (Jansen and Roque 2010, Gürtler and Cardinal 2015). Taking into account the efficiency of the oral route, carnivoran mammals such as coatis (Nasua nasua) may occupy the top of the T. cruzi transmission chain. This is especially true for the omnivorous coatis, whose diet includes both insects and small mammals, resulting in several paths for infection by T. cruzi (Rocha et al. 2013). The coati is a diurnal and scansorial species that is organized in a complex social structure with adult females and immature individuals and some adult males forming social groups (Hirsch and aldonado 2011). ts diet is omnivorous, including fruits, small vertebrates, and invertebrates, with a high ingestion of insects (Bianchi et al. 2014). The coatis build arboreal nests (Figure 1), which are all bird-like, that is, open nests having a semi-spherical shape with leaves and branches used from the tree within which the nest is situated (Olifiers et al. 2009). The nests are constructed in larger trees with well-formed canopy, sites where there is a higher density of older trees (taller trees with a large diameter) and higher canopy density. Both males and females use the nests to rest overnight. n some cases, coatis can reuse resting-nests after a period of days. The nests can be individual, especially in the case of males, or communal, with more than one group member using them. Also, females build larger nests to give birth to up to seven cubs and remain in birthing nests for about 25 days, when the pups climb down to the forest floor for the first time (Emmons 1997, Gompper and Decker 1998, Hirsch 2007). n the Pantanal of Brazil, the coati is considered the main reservoir host of T. cruzi due to its high potential to infect vectors, since it has consistently high prevalence of infection and high parasitemias. Furthermore, this species was pointed as a T. cruzi bioaccumulator, given the reports of infection with the main T. cruzi lineages both in single and mixed infections (Herrera et al. 2008, 2011, Alves et al. 2011, Rocha et al. 2013). Taken together, the coati s high reservoir competence and its ecological characteristics of using both arboreal and terrestrial strata suggest this species may be considered as a network hub in the T. cruzi transmission cycle (Rocha et al. 2013). Oral infection is suggested as the main T. cruzi infection route for coatis due to its omnivore diet, which includes insects and also small mammals (Rocha et al. 2013). Considering the importance of coatis in the T. cruzi transmission network in the Pantanal, investigating whether coati nests are suitable ecotopes for triatomines can aid in understanding T. cruzi transmission dynamics, as well as extending the knowledge of the ecology of sylvatic triatomine populations and the element features that may influence their occurrence and distribution. The purpose of this study was to investigate whether the nests built by coatis indeed represent a suitable ecotope for triatomine bug populations in the Brazilian Pantanal and to discuss the potential implications for the T. cruzi enzootic cycle. Specific objectives were to determine (i) the rate of infestation by triatomine bugs in the coatis nests, (ii) which triatomine species were most frequent in these nests, (iii) how many triatomines found were infected by T. cruzi, and (iv) the triatomine blood meal sources in the nests. ATERALS AND ETHODS Figure 1. Figure 1. (a) Female coati (Nasua nasua) climbing a tree to reach her arboreal nest; (b) coati birthing nest; October 2011, Pantanal of Brazil. Study site This study was carried out at the Nhumirim Ranch (18º 59 S and 56º 39 W), in the Central Pantanal of Brazil, located about 160 km east from Corumbá. The landscape is a mosaic composed of fresh water and saline lakes, forest patches, savannah, and scrub savannah corridors. During the wet season (November - April), many parts of open grassland change from terrestrial habitats into aquatic ones and during the dry season (ay - October) the land dries out and only scarce pools, creeks, and some lakes remain. The flooding regime is classified as low height (30 to 40 cm) with an average duration of three to four months (Soriano et al. 1997).

Vol. 40, no. 2 Journal of Vector Ecology 381 Field survey To localize coati nests, we tracked coatis equipped with radio collars during the nights from ay, to September,. When we detected that the radio signal was coming from the top of a tree, we approached it in silence to locate the nest without disturbing the coatis. The following morning, when the coatis had left the nest, we collected the nests in boxes or plastic bags. We also collected coatis nests found occasionally while monitoring radio collared coatis. We found and monitored one birthing nest until the young climbed down the tree and we then collected the nest. We brought the nests to the laboratory, where we carefully dismantled them to search for triatomine bugs, which were placed alive and individually in falcon tubes with an individual nest number. All procedures employed in this study were in accordance with the license obtained by BAA, the Brazilian Government nstitute (first license No. 28772-1/2011 and last license No. 28772-4/) and sanctioned by the Comitê de Ética e Utilização de Animais (Universidade Federal de ato Grosso do Sul; CEUA; protocol No. 350/2011). dentification of triatomine species and laboratory analyses Triatomines were in the National and nternational Laboratory of Reference on Taxonomy of Triatominae of Oswaldo Cruz Foundation (FOCRUZ), by their external morphological conformations, following Carcavallo et al. (1997) and Lent and Wygodzinsky (1979) taxonomic references. All triatomines collected in the nests were dissected for examination of T. cruzi infection. A rectal puncture were diluted in saline solution and analyzed by direct observation under a light microscope. Positive flagellated protozoa samples were posteriorly confirmed as T. cruzi (Alves 2013) by multiplex PCR amplification of the non-transcribed spacer of the mini-exon gene (PCR) following the conditions described by Fernandes et al. (2001). We determined the blood feeding sources for triatomines based on the precipitin test. The precipitin test was applied to the intestinal contents of the engorged triatomines. The stomach content was triturated in 0.85% saline and left for 12 h at -4º to 8º C. t was then centrifuged for 5 min at 1,500 rpm, and the supernatant was mixed with the antisera of bird, coati, opossum, armadillo, rodent, lizard, dog, cat, goat, cow, human, horse, and pig (Lorosa et al. 1998). RESULTS We sampled 24 coati nests; 12 of them were communal nests, nine were individual nests from males, and one was a birthing nest used by a female and its offspring for 25 days. We have no information about the remaining two nests, because the coatis were present when we found them. n total, 37 triatomines were collected from eight of the sampled nests (33.3%) and the number of triatomines per nest varied from one to 21, averaging 4.5 bugs per infested nest. The species collected were adults of sordida (29.7%, n=11) and stali (8.1%, n=3). Also, we collected (35.1%, n=13) and (16.2%, n=6) that were nymphs of different instars (Table 1). We were able to identify the genera of four specimens, because they were 1 st instars nymphs. Additionally, in two nests we found T. sordida and R. stali concurrently, both of them showing different developmental stages. Flagellated protozoan infection was detected in 23 (67.6%) of 34 triatomines examined, including individuals from all species and genera analyzed (Table 1). These flagellates were later as T. cruzi (Alves 2013). nfected individuals belonged to five out of eight nests. The infection rate was 65.3% of all examined triatomines and, although the sample size was marginally small to detect differences between genera, it was significantly different (χ2 = 1.06, p = 0.30). We performed the precipitin test in seven triatomine specimens collected from two different nests. The specimens fed on coati, bird, rodent and marsupial. Also, one R. stali and two T. sordida from these two infested nests fed simultaneously on multiple sources, including the coatis (Table 2). DSCUSSON The determination of triatomine natural ecotopes and putative hosts may provide key information on the wild cycle of T. cruzi. However, this kind of investigation is time consuming and expensive, particularly in dense forests in remote sites. For this reason, some ecotopes of triatomine species remain poorly known, such as T. vitticeps in the Atlantic Forest (Souza et al. 2011). The ecotope used for R. stali and T. sordida has been widely addressed (see below), though without precise information regarding the host in the Brazilian Pantanal. We investigated coati shelters, represented by arboreal nests, and suggest it is an important sylvatic ecotope for both species in the study area. Ferriolli- Filho and Barretto (1968) had already found Panstrongylus megistus triatomine infected in the hollow tree used as shelter by coatis in the state of São Paulo, Brazil. As such, this is the first report of occurrence and description of infestation rate of triatomines in arboreal nests of coatis. sordida is known for occupying a large variety of ecotopes (Lent and Wygodzinsky 1979), including palms (see Gurgel-Gonçalves et al. ) and the finding of this species in coati nests reinforces its ecotope eclecticism. On the other hand, is known to be closely associated with palm trees (Gaunt and iles, 2000, Abad-Franch and onteiro 2007, Abad-Franch et al. 2010, 2015, Escalante et al. 2015), especially with acuri palms (Attalea phalerata; Justi et al. 2010), which are very common in the Pantanal. atias et al. (2003) found R. stali inhabiting dwellings constructed with A. phalerata leaves in Alto Beni, Bolivia, and stated that this palm would be the original sylvatic habitat of R. stali. However, in this study we found inhabiting coati nests built in angiosperm trees, indicating a larger ecotope use than acknowledged. Also, we found well established colonies of both triatomines occurring in the same coati nests. Species sharing the feeding resources and microhabitat at the same time seems to be unusual in nature,

382 Journal of Vector Ecology December 2015 Table 1. nfested coati nests and the triatomines collected between ay and September,, in the Pantanal of Brazil. Nest Date Sex i Type ii Species n stages iii nfected iv 1 24-AY- F C stali 1 A 2 1/1 N u,u 1/2 2 7-JUL- F C 3 N 4,4,5 0/3 3 8-JUL- F C sordida 2 A 1/2 1/1 4 2-AUG- 4 N 3,4,4,4 3/4 5 2-AUG- - 6 4-AUG- sordida 1 A 1/1 sordida 8 A 5/8 stali 2 A 1/1 7 7-AUG- 6 N 3,3,4,4,5,5 6/6 3 N 1,5,u 2/2 1/1 8 13-SEP- - 1 N 3 0/1 0/1 Total 37 23/34 i Sex refers to the coati (Nasua nasua) using the nest; ii Type refers to nest type and was classified as: C=communal resting, =individual resting, - = information available; iii A=adult, N U =nymph of un instars, N 1-5 =nymph of 1 st to 5 th instars, - = information available; iv Trypanosoma cruzi-positive/examined.

Vol. 40, no. 2 Journal of Vector Ecology 383 Table 2. Triatomines collected in arboreal nests of coatis (Nasua nasua) and origin of the blood they ingested (precipitin test). The study was carried out in the Brazilian Pantanal, between the months of ay and September,. Nest i Sex ii Date Triatomine Preciptin test 1 Female 24-AY- Bird 1 Female 24-AY- stali Coati and marsupial 6 ale 07-AUG- Rodent 6 ale 07-AUG- sordida Coati and bird 6 ale 07-AUG- sordida Coati 6 ale 07-AUG- sordida Coati and rodent 6 ale 07-AUG- Not Rodent i Nest= nest D (same of Table1). ii Sex refers to the coati that used the nest. although it was reported even with triatomines. For example, three members of T. rubrovaria species complex have been collected concomitantly under the same rock (Almeida et al. 2009), and T. dimidiata was found co-occurring with R. pallecens within the bracts of a A. butyracea palm-tree (Parra et al. 2009, Escalante et al. 2015). Yet, such larger niche overlap is indicative of competition, and co-occurrence of the two species inhabiting the same shelters in the Pantanal should be investigated just under the ecological perspective, but also from an epidemiological point of view. After all, both species were infected by T. cruzi and this situation would allow the parasite exchange. Triatomines can feed on a wide variety of vertebrate hosts and some authors have suggested it is a result of an opportunistic character, rather than choice, which may be driven by the proximity and availability of animals (Rabinovich et al. 2011). The precipitin test showed that triatomines inhabiting the coati nests fed in taxa as varied as bird, rodent, and marsupial, beside coati. n fact, we have some opportunistic observations of the spiny rat (Thrichomys fosteri), as well as of some birds, visiting an abandoned coati nest, and the presence of this visitors could explain how colonies of triatomines, including non-volant nymphs, could be maintained in nests so infrequently used by coatis. ultiple feeding sources have already been evidenced by molecular techniques (Stevens et al. ) and these results evidence the opportunistic theory of feeding by triatomines. Although the oral route has been suggested as an important mechanism for T. cruzi transmission and perpetuation in free-ranging coatis (Herrera et al. 2008, 2011), the preciptin test indicates that triatomines present in the coati nests have effectively fed on coatis. Females and their brood remain in close contact with the triatomines in the nest for about one month after birth (Saab, unpublished data). ost Reduviidae have several exocrine glands that produce chemicals that may have defense and other functions (anrique et al. 2006). Also, many triatomines, including some and, emit stridulations that have been interpreted as a signal indicating unpalatability (Schilman et al. 2001), although at least some bats do feed on triatomines (Thomas et al. 2007). f the triatomines are palatable to the coatis, their presence in the nests would propitiate the opportunity of occurrence of both routes, with triatomines feeding on coati blood and coatis feeding on infected triatomines. n any case, the presence of triatomines in coati nests may be the primary cause of occurrence of high seroprevalence of T. cruzi in coatis (Herrera et al. 2008, 2011, Rocha et al. 2013). Acknowledgments We are grateful to smael Verrastro, Rafael Penedo, and Carlos Zucco for assistance with field work. Funds were provided by dea Wild, Neotropical Grassland Conservancy, ChagasEpiNet (grant 223034), and Embrapa Pantanal (Project 02.10.06.007.00.02). J.S.L., F.L.R., and F..A. received scholarships from CNPq, Capes, and CNPq-Faperj, respectively. athews Gompper and one anonymous referee improved the draft manuscript. REFERENCES CTED Abad-Franch, F. and F.A. onteiro. 2007. Biogeography and evolution of Amazonian triatomines (Heteroptera: Reduviidae): implications for Chagas disease surveillance in humid forest ecoregions. em. nst. Oswaldo Cruz 102: 57-70. Abad-Franch, F., G. Ferraz, C. Campos, F.S. Palomeque,.J. Grijalva, H.. Aguilar, and. iles. 2010. odeling disease vector occurrence when detection is imperfect: infestation of Amazonian palm trees by triatomine bugs at three spatial scales. PLoS Negl. Trop. Dis. 4, e620. Abad-Franch, F.,.. Lima, O. Sarquis, R. Gurgel- Gonçalves,. Sánchez-artín, J. Calzada, A. Saldaña, F.A. onteiro, F.S. Palomeque, W.S. Santos, V.. Angulo, L. Esteban, F.B.S. Dias, L. Diotaiuti,.E. Bar, and N.L. Gottdenker. 2015. On palms, bugs, and Chagas disease in the Americas. Acta Trop. doi:10.1016/j. actatropica.2015.07.005. Almeida, C.E., P.L. arcet,. Gumiel, D.. Takiya,. Cardozo de Almeida, R.S. Pacheco, C.. Lopes, E.. Dotson, and J. Costa. 2009. Phylogenetic and pheypic relationships among carcavalloi (Hemiptera:

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