In search of Triatominae (Hemiptera: Reduviidae) using mice-baited traps along the peninsula of Baja California, Mexico

doi:10.21203/rs.3.rs-1743121/v1

During a 3000 kms-exploratory fieldtrip along the peninsula of Baja California, Mexico, we used mice-baited traps in search of Triatominae. Specimens of Paratriatoma hirsuta and Dipetalogaster maxima were collected.

Triatominae

Baja California

Mexico

Paratriatoma hirsuta

Dipetalogaster maxima

Mice-baited traps

Triatominae are the vectors of T. cruzi, the causative agent of Chagas disease. This zoonotic disease is a major public health problem in the Americas, where six to seven million people are estimated to be infected with the parasite (1). In Mexico, transmission of T. cruzi occurs in most of the territory, and it has recently been estimated a national seroprevalence of infection of 3.38%, suggesting that around four million people currently carry the parasite in the country and placing Mexico as the country with the largest number of cases in the world (2). Around 150 species of triatomines are currently recognized (3). Of them, at least 30 occur in Mexico (4), and five, namely Paratriatoma hirsuta, Triatoma rubida, Triatoma protracta, Triatoma peninsularis, and Dipetalogaster maxima, have been reported in the peninsula of Baja California, at the extreme Northwest of Mexico (5). Since the pioneering works performed in the 60’s (5), only a few studies have been dedicated to the vectors of T. cruzi in this region (6–9), and the peninsula of Baja California is among the regions of Mexico where lesser is known regarding T. cruzi transmission and seroprevalence (2). Consequently, our knowledge of T. cruzi transmission in the peninsula of Baja California, as well as of the ecology, distribution and taxonomy of the Triatominae species of this region remains largely unknown.

Table Characteristics of the localities under study, and Triatominae collections using mice-baited traps

Locality Code*	State	Coordinates	Traps placed	Positive traps	Lost traps***	Trap positivity	Caught triatomines	Triatomines / positive trap	Species****	Development stage /sex
Z001	Baja California	31°6.5633'N, 115°38.1383'W	120	0	10	0	-	-
Z002	Baja California	29°45.0617'N, 114°44.6783'W	90	0	0	0	-	-
Z003	Baja California	28°55.7417'N, 113°33.2283'W	1	1	0.8	1	1	P. hirsuta	Male
Z003**	Baja California	28°55.7417'N, 113°33.2283'W	20	1	1	5.3	1	1	P. hirsuta	Male
Z004	Baja California Sur	26°44.027'N, 111°54.466'W	50	0	0	0	-	-
Z005	Baja California Sur	24°00.036'N, 110°10.572'W	48	11	7	26.8	15	1.4	D. maxima	12 N1, 2 N2, 1 Male
Total			433	13	19	3.1	17	1.3

*For health and logistical reasons, half of the team was not able to follow further South of Z003. Consequently, only two sites (Z004 and Z005) were explored in the state of Baja California Sur instead of three as initially planned, and only approx. 50 traps per site were set by the remaining research team

**Because of the detection of a specimen of P. hirsuta during the first night of trapping in Z003, 20 additional traps were set during a second night at the same place where the first specimen was collected

***Unfortunately, some traps were sometime lost, generally because they were taken by wild animals, likely foxes and coyotes

****Species were identified using Triatodex (11) and following taxonomic keys (12)

N1: first instar nymph; N2: second instar nymph

During the first 12 days of May, 2022, we undertook an epic exploratory fieldtrip in search of triatomines following a latitude gradient along the peninsula of Baja California. To this end, we selected different localities, including three localities in the state of Baja California (Z001-Z003), and two localities (Z004 and Z005) in the state of Baja California Sur (Fig. 1) to establish an almost homogenous latitude gradient along the peninsula and where we knew about the presence of rocky ecotopes. In each locality, we installed a varying number of mice-baited traps (10) (see Table). These were set in the afternoon in places that we considered as potential habitats for triatomines (cracks between rocks, rock piles, small burrows, nests, …) and where we noticed signs of animal life (presence of feces, seeds, food residues,…). We preferentially installed the traps in rocky ecotopes, including rocky outcrops, cliffs and screes. Furthermore, inhabitants of each locality were asked about their knowledge on Triatominae, as they could potentially provide valuable assistance in the selection of trapping sites. Traps were operated throughout the night and inspected the next morning. Caught bugs were identified using Triatodex (11) and taxonomic keys (12).

Overall, we placed 433 traps and collected Triatominae in two of the five localities explored (Z003 and Z005). In Z003, two triatomine bugs were collected in a nest containing likely rat and/or squirrel feces. They were identified as male specimens of P. hirsuta (Fig. 2). In Z005, 15 bugs were collected, principally in cracks between rocks in which abundant rodent (likely rats) feces were observed. These were identified as D. maxima (Fig. 2) and included 12 first instar nymphs, two second instar nymphs, and one male. Of the 433 traps installed, 19 were lost, likely taken by foxes or coyotes, and 13 were positive with at least 1 Triatominae specimen, giving an overall positivity of the traps of 3.1%, and an average of 1.3 bugs per positive trap. When considering only the positive localities, trap positivity was 0.8 and 5.3% in Z003 (first and second night of capture, respectively) and 26.8% in Z005. The average number of bugs per positive trap was 1.0 in Z003, and 1.4 in Z005. Noteworthy, an additional 14 specimens of D. maxima, including two males, one fifth instar nymph, one fourth instar nymph, two third instar nymphs, one second instar nymph and three first instar nymphs were manually collected at the time of trap setting in Z005. Indeed, D. maxima appeared very aggressive, and bugs were collected walking on the rocks and/or coming to us. This kind of aggressive behavior was also described by the inhabitants of the area. The same inhabitants also mentioned having frequently observed bugs taking blood upon small reptiles, that seem paralyzed during the blood meal.

Our findings of P. hirsuta and D. maxima are in accordance with the reported distribution of these species (4, 5). To the best of our knowledge, this is the first time that mice-baited traps are used in this area to collect Triatominae bugs. Our results confirm the usefulness of this trapping strategy when standardized protocols are needed, with a positivity approaching 30% in sites with high abundance of triatomines. Nevertheless, effort amount can also sometimes be considerable for no or poor collections. We do not know if the absence of capture in some localities, and if the fact that we did not detect the other previously reported species in the peninsula of Baja California was due to an absence of Triatominae in these localities, a poor efficiency of the traps, a too small number of investigated localities, or if the season was not the best for capture of Triatominae. On some occasions, we were told by inhabitants of the studied areas that they knew about this kind of hematophagous bugs, but that they appeared mostly during the summer. Depending on the research question, mice-baited traps may be very useful, while other trapping techniques, including community participation (13, 14), light traps (15) and the “pick and shovel” technique of (5) or a combination of these may be useful to answer other research questions. At present, further investigation on the ecology, distribution and taxonomy of the Triatominae of the peninsula of Baja California, as well as on the dynamics of T. cruzi transmission in this region is still needed. As for future objectives, our research group plans to return to the sites where Triatominae were detected during this exploratory fieldwork, and to identify the ecological associations of the bugs, as previously proposed (16–18) to enhance our knowledge of Triatominae ecology and T. cruzi transmission cycles in these sites and, more generally, in the peninsula of Baja California.

N1

first instar nymph

N2

second instar nymph

BC

State of Baja California

BCS

State of Baja California Sur

Ethics approval and consent to participate

The use of mice-baited traps for triatomine collection was approved by the bioethics committee of the Dr. Hideyo Noguchi Regional Research Center of the Autonomous University of Yucatan (# CEI-02-2019).

Consent for publication

Not applicable

Availability of data and materials

All data is freely accessible and included in the manuscript.

Competing interests

The authors declare that they have no competing interests

Funding. This work received financial support from the Autonomous University of Baja California (UABC, project ID: 201/2882) and the French National Research Institute for Sustainable Development (IRD) through its program “Ecoles de Formation à la Recherche ».

Authors' contributions

EW and PH designed the study. EW, JJRV and AAR contributed to field collections in BC and BCS. GEMB, GLV, and PH contributed to field collections in BC. EW and AAR performed Triatominae identification, analyzed the data, wrote the main manuscript text, and prepared the table and figures. All the authors read and approved the final manuscript.

Acknowledgements: The research team wants to thank Don Emilio for letting us access to his “rancho” in San Pedro, BCS, and his valuable help in selecting the trapping site for D. maxima collections. We also want to thank the team of the Mastozoology Lab of the Centro de Investigaciones Biologicas (CIB) del Noroeste, for lending us a stereoscope in La Paz to allow for triatomine identification, and Philippe Solano for suggestions and comments.

WHO. Chagas disease (American trypanosomiasis), Fact sheet N°340. 2022. http://www.who.int/mediacentre/factsheets/fs340/en/. Accessed 23 May 2022.
Arnal A, Waleckx E, Rico-Chávez O, Herrera C, Dumonteil E. Estimating the current burden of Chagas disease in Mexico: A systematic review and meta-analysis of epidemiological surveys from 2006 to 2017. PLoS Negl Trop Dis. 2019;13(4):e0006859.
Ceccarelli S, Balsalobre A, Vicente ME, Curtis-Robles R, Hamer SA, Landa JMA, et al. American triatomine species occurrences: updates and novelties in the DataTri database. Gigabyte. 2022
Ramsey JM, Peterson AT, Carmona-Castro O, Moo-Llanes DA, Nakazawa Y, Butrick M, et al. Atlas of Mexican Triatominae (Reduviidae: Hemiptera) and vector transmission of Chagas disease. Mem Inst Oswaldo Cruz. 2015;110(3):339–52.
Ryckman RE, Ryckman AE. Baja California Triatominae (Hemiptera: Reduvvidae) and their hosts (Rodentia: Cricetidae). Ann Entomol Soc Am. 1961;54:142–3.
Bello-Bedoy R, Peiro-Nuno H, Cordoba-Aguilar A, Flores-Lopez CA, Romero-Figueroa G, Arteaga MC, et al. Ontogenetic changes in wild chagasic bugs (Dipetalogaster maxima): exploring morphological adaptations in pre-adult and adult stages. Rev Mex Biodivers. 2019;90.
Flores-Lopez CA, Rivas-Garcia L, Romero-Figueroa G, Guevara-Carrizales A, Peiro-Nuno H, Lopez-Ordonez T, et al. Infection rate of Trypanosoma cruzi (Trypanosomatida: Trypanosomatidae) in Dipetalogaster maxima (Hemiptera: Reduviidae). J Med Entomol. 2022;59(1):394–9.
Jimenez ML, Llinas J, Palacios C. Infection rates in Dipetalogaster maximus (Reduviidae: Triatominae) by Trypanosoma cruzi in the Cape region, Baja California Sur, Mexico. J Med Entomol. 2003;40(1):18–21.
Jimenez ML, Palacios C. Life cycle and reproductive and feeding behavior of Dipetalogaster maximus (Uhler) (Reduviidae: Triatominae) under laboratory conditions in Baja California Sur, Mexico. Southwest Entomol. 2002;27(1):65–72.
Noireau F, Abad-Franch F, Valente SAS, Dias-Lima A, Lopes CM, Cunha V, et al. Trapping Triatominae in sylvatic habitats. Mem Inst Oswaldo Cruz. 2002;97(1):61–3.
Gurgel-Goncalves R, Abad-Franch F, de Almeida MR, Obara MT, de Souza RDM, Batista JAD, et al. TRIATODEX, an electronic identification key to the Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease: Development, description, and performance. PLoS One. 2021;16(4).
Lent H, Wygodzinsky P. Revision of the triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chaga's disease. Bull Am Mus Nat Hist. 1979;163:123–520.
Dumonteil E, Ramirez-Sierra MJ, Ferral J, Euan-Garcia M, Chavez-Nunez L. Usefulness of community participation for the fine Temporal monitoring of house infestation by non-domiciliated triatomines. J Parasitol. 2009;95(2):469–71.
Waleckx E, Pérez-Carrillo S, Chávez-Lazo S, Pasos-Alquicira R, Cámara-Heredia M, Acuña-Lizama J, et al. Non-randomized controlled trial of the long-term efficacy of an Ecohealth intervention against Chagas disease in Yucatan, Mexico. PLoS Negl Tro Dis. 2018;12(7):e0006605.
Rebollar-Tellez EA, Reyes-Villanueva F, Escobedo-Ortegon J, Balam-Briceno P, May-Concha I. Abundance and nightly activity behavior of a sylvan population of Triatoma dimidiata (Hemiptera: Reduviidae: Triatominae) from the Yucatan, Mexico. J Vector Ecol. 2009;34(2):304–10.
Dumonteil E, Ramirez-Sierra MJ, Perez-Carrillo S, Teh-Poot C, Herrera C, Gourbiere S, et al. Detailed ecological associations of triatomines revealed by metabarcoding and next-generation sequencing: implications for triatomine behavior and Trypanosoma cruzi transmission cycles. Sci Rep. 2018;8:4140.
Waleckx E, Arnal A, Dumonteil E. Metabarcoding, un nuevo enfoque para el estudio de los ciclos de transmisión de la enfermedad de Chagas y la ecología de sus vectores. In: Zamora–Bustillos R, Sandoval–Gío JJ, editors. Contribución de la Biotecnología al Desarrollo de la Península de Yucatán. Mérida:TECNM; 2019. P. 1052-65.
Hernandez-Andrade A, Moo-Millan J, Cigarroa-Toledo N, Ramos-Ligonio A, Herrera C, Bucheton B, et al. Metabarcoding, a powerful yet still underestimated approach for the comprehensive study of vector-borne pathogen transmission cycles and their dynamics. In: Clarborn D, editor. Current Topics in the Epidemiology of Vector-Borne Diseases. London: Intech Open; 2019.

No competing interests reported.

In search of Triatominae (Hemiptera: Reduviidae) using mice-baited traps along the peninsula of Baja California, Mexico

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