ABSTRACT

In recent years, Aedes albopictus has become the most important invasive mosquito species worldwide. In 2018, Ae. albopictus was found in a suburban area of Merida, one of the cities with the highest number of arbovirus cases in Mexico in the last 10 years. As Ae. albopictus continues its range expansion, there is a need to monitor its susceptibility to existing insecticide classes, since countries like Mexico currently do not consider Ae. albopictus in its insecticide management programs. In order to determine its susceptibility to the insecticides usually applied by the vector control program in Mexico, the Centers for Disease Control and Prevention bottle bioassays were performed on individuals from established population of Ae. albopictus from Merida, Yucatan, Mexico. Results suggested that the population recently found in the suburban area of Merida is susceptible to permethrin, deltamethrin, chlorpyrifos, malathion, bendiocarb, and propoxur. Further studies of insecticide resistance using biochemical and molecular tools together with more knowledge of the biology and ecology of this species are necessary to generate specific and efficient control strategies in Mexico.

Aedes aegypti (L.) and Ae. albopictus (Skuse) are vectors of emerging arboviruses, which represent a significant threat to public health and economic burden worldwide (Lwande et al. 2020). The presence of Ae. albopictus was recently reported in the suburban area of the city of Mérida, capital of the state of Yucatan, Mexico (Contreras-Perera et al. 2019). The Yucatan Health Services (SSY) immediately applied focal adulticide-based control and enhanced Ae. albopictus–specific entomological surveillance in response to the 1st detection of this invasive species in the periphery of Merida, one of the largest demographic centers of great epidemiological importance for the transmission of dengue, chikungunya, and Zika viruses at the national level (Rojas et al. 2018). Local assessment of the insecticide susceptibility status of Ae. aegypti populations is one of the components of enhanced entomological surveillance in Mexico (Kuri-Morales et al. 2018). Eggs collected from the ovitrap network surveillance (Hernández-á vila et al. 2013, Secretaria de Salud 2018) set in the most important dengue-prone urban areas of Mexico are tested at least once a year with the bottle bioassay protocol developed by the US Centers for Disease Control and Prevention (CDC) (Brogdon and Chan 2010) to assess the effect of different chemical groups usually employed for vector control (Secretaria de Salud 2019). However, there is no systematic monitoring of the susceptibility/resistance of Ae. albopictus in Mexico. Here, we report the status of insecticide susceptibility of the Ae. albopictus population recently found in the suburban area of Merida city (Contreras-Perera et al. 2019) against pyrethroids (deltamethrin, permethrin), carbamates (bendiocarb and propoxur), and organophosphates (chlorpyrifos and malathion).

An entomological survey with collection of larvae, pupae, and adults was performed during October 15–19, 2018, in the locality of San Pedro Nohpat (20.951514°N, −89.564964°W), a suburban area 500 m away from Merida's beltway where Ae. albopictus population was reported (Contreras-Perera et al. 2019). Larvae, pupae, and adults were transferred to the Collaborative Unit for Entomological Bioassays (UCBE)—Universidad Autonoma de Yucatan. Larvae and pupae were reared under laboratory standard conditions (Zhang et al. 2018). Emerging adults (parental generation, F0) were maintained under insectary conditions (26 ± 1°C, 75 ± 5% relative humidity, and a 12:12 (light:dark) with 10% glucose solution soaked in cotton pads. Female mosquitoes were reared (bovine blood for egg production) up to F1 generation and used for bioassays.

The susceptibility of Ae. albopictus to insecticides was evaluated using the CDC bottle bioassay protocol (Brogdon and Chan 2010). Briefly, bioassays were carried out with 4 replicates and 3 repetitions exposing 20–25 unfed 3–5 day old females against diagnostic doses suggested for Aedes by CDC guidelines (Brogdon and Chan 2010): (>90% purity; Sigma-Aldrich, St. Louis, MO): permethrin (15 μg/bottle), deltamethrin (10 μg/bottle), malathion (50 μg/bottle), bendiocarb (12.5/bottle μg), chlorpyrifos (85 μg/bottle), and propoxur (12.5 μg/bottle). One bottle precoated with acetone was used as control. A susceptible field strain of Ae. albopictus from Atlanta, GA (donated by Emory University), was used as a susceptible strain. Mosquito responses were evaluated by knockdown and recorded every 10 min until the diagnostic time (30 min) for all insecticides; mortality was recorded 24 h postexposure. Mosquito collections were classified as resistant or susceptible according to the World Health Organization criteria (WHO 2016) as follows: 98 ± 100% mortality indicates susceptibility, 90 ± 97% mortality suggests that resistance may be developing, and mortality less than 90% indicates resistance.

Results of the study indicated that the Ae. albopictus population recently found in the suburban area of Merida (Contreras-Perera et al. 2019) was susceptible to permethrin, deltamethrin, chlorpyrifos, malathion, bendiocarb, and propoxur. The knockdowns were above >98%, 10 min for all insecticides except deltamethrin, which took 20 min (Fig. 1). Mortality was 100% for all insecticides after 24 h.

Fig. 1.

Knockdown (%) of susceptible and wild Ae. albopictus strains by insecticides (dose and diagnosis time) tested: Susceptible strain (A) permethrin, (B) deltamethrin, (C) propoxur, (D) bendiocarb, (E) chlorpyrifos, and (F) malathion; wild strain (A) permethrin, (B) deltamethrin, (C) propoxur, (D) bendiocarb, (E) chlorpyrifos, and (F) malathion and control.

Fig. 1.

Knockdown (%) of susceptible and wild Ae. albopictus strains by insecticides (dose and diagnosis time) tested: Susceptible strain (A) permethrin, (B) deltamethrin, (C) propoxur, (D) bendiocarb, (E) chlorpyrifos, and (F) malathion; wild strain (A) permethrin, (B) deltamethrin, (C) propoxur, (D) bendiocarb, (E) chlorpyrifos, and (F) malathion and control.

Fig. 1.

Continued.

Fig. 1.

Continued.

This report contributes to the understanding of the susceptibility status of Ae. albopictus as it continues its range expansion into the Mexican territory. Sames et al. (1996) reported the susceptibility of Ae. albopictus to permethrin, resmethrin, and malathion from north Mexico. In Chiapas (South Mexico), López-Solís (2016) reported considerable resistance levels to temephos, malathion, chlorpyrifos, and deltamethrin. Enzymes such as monooxygenase, glutathione-S-transferase, esterase-mediated metabolism, and altered acetylcholinesterase are resistance mechanisms likely involved in these populations (Ponce-García et al. 2009, López-Solís 2016). It is known that Ae. albopictus presents an unexpectedly low level of resistance to pesticides (Hemingway et al. 2004, Kasai et al. 2019), very likely due to its spreading capacity, bringing susceptible populations that contribute to low levels of resistance (Gratz 2004). However, Ae. aegypti requires systematic monitoring because of the increased pattern of resistance observed to major classes of chemical insecticides (Vontas et al. 2012, Moyes et al. 2017, Richards et al. 2019).

Our results showed that Ae. albopictus currently found in suburban areas of Merida are susceptible to most common chemical insecticides recommended by Mexican health authorities. As with Ae. aegypti, a systematic monitoring of insecticide resistance of Ae. albopictus, with bioassays as well as biochemical and molecular studies, is essential to implement specific and effective vector control strategies throughout the Mexican territory.

This study received support from Mexico's CONACYT (Project No. 255141) and Fondo Mixto CONACyT (Mexico)–Gobierno del Estado de Yucatan (Project YUC-2017-03-01-556). Abdiel Martin-Park was supported by the Catedras CONACYT program. We thank Gonzalo Vazquez-Prokopec (Emory University) for donating the susceptible strain of Ae. albopictus. Thanks are also due to the UCBE team: Silvia Perez-Carrillo and Daniel Chan Espinoza for field work, and for Ana García-Moreno Malcolm for grammatical corrections.

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Author notes

1

Collaborative Unit for Entomological Bioassays, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán. Mérida, Yucatán, México.

2

Servicios de Salud de Yucatán. Mérida, Yucatán, México.

3

Secretaría de Salud de Quintana Roo, Chetumal, Quintana Roo, México.