Characterization of Asian Tiger Mosquito (Aedes albopictus) as Potential Vector of Arboviruses in Non-Human Primates Breeding Facilities Environment

Abstract

Wildlife-originated infectious diseases present a significant threat to global health, security, and economic growth, thus combatting their emergence is a public health priority. Non-human primates (NHPs) frequently act as reservoirs for arboviruses causing diseases in humans. Arboviruses of significant concern in NHPs populations among others are Yellow Fever virus (YFV), Dengue virus (DENV), Zika virus (ZIKV), and Chikungunya virus (CHIKV). The diseases caused by arboviruses usually do not show clinical symptoms but can cause viremia conditions, so the viruses are maintained in nature, include in NHPs’ breeding facilities.

The Primate Research Center (PRC) IPB University is a renowned research center that conducts advanced research on Indonesian primate biology. The PRC IPB University activities encompass various aspects, such as compiling biological data banks, characterizing population genetics within the colony and in the wild, and conducting conservation research. PRC IPB University possesses breeding facilities for NHPs located in urban and peri-urban areas close to human settlements.

Aedes albopictus is reported as a competent vector of more than 20 arboviruses and a significant vector for important pathogenic arboviruses such as CHIKV, ZIKV, and DENV. The presence of Ae. albopictus in NHPs’ breeding facilities can contribute to the transmission of Aedes-borne viral diseases within and between NHPs, as well as between NHPs and humans, or even among humans themselves. There are not yet any previous report on a comprehensive investigation of Ae. albopictus in Indonesia NHPs’ breeding facilities. The presence of Ae. albopictus in both urban and peri-urban regions, where NHPs' breeding facilities are situated, could potentially serve as a contributing factor in the transmission of Aedes-borne viral diseases between NHPs and humans (and vice versa), as well as among human populations.

This research was a comprehensive study regarding Ae. albopictus as a potential arboviruses vector in NHPs’ breeding facilities environments of PRC IPB University. This research consisted of 5 stages as follows (1) biology and life table of the Ae. albopictus populations collected from urban and peri-urban area of NHPs’ breeding facilities under laboratory conditions (2) genetic structure of the Ae. albopictus collected from urban and peri-urban area of NHPs' breeding facilities based on cytochrome oxidase 1 gene (3) Arboviruses circulation and Wolbachia molecular typing of the Ae. albopictus populations collected from urban and peri-urban area of NHPs’ breeding facilities (4) the diversity and composition of gut and larvae microbiota in Ae. albopictus from urban and peri-urban area of NHPs’ breeding facilities (5) characteristic habitat of Ae. albopictus and species distribution model in peri-urban area of NHPs’ breeding facilities.

Ae. albopictus biting behavior in urban and peri-urban area NHPs breeding facilities exhibited distinct bimodal activity patterns, with a peak in the morning around 09:00-10:00 and another peak in the evening around 16:00-17:00. Ae. albopictus mosquitoes from urban area demonstrated greater fecundity, longer lifespan, more gonotrophic cycles, and a higher net reproduction rate (R0) than their counterparts from peri-urban area.

Cytochrome oxidase 1 sequences with 643 base pairs (bp) length were obtained from Ae. albopictus from both populations. Seven bp of nucleotide variation were found with a nucleotide diversity value was 0.00294. Seven haplotypes were formed between Ae. albopictus sample and reference, 1 specific and 6 shared haplotypes, with haplotype diversity’s value was 0.911. There was a change at amino acid position 113 due to a transition mutation at the first codon (site 337 of G>A). An amino acid change was occurred on base 113 (A>T or Alanine to Threonine). The two populations of Ae. albopictus from urban and peri-urban NHPs’ breeding facilities had low genetic distance.

This study also reported a total of 5% pool Ae. albopictus from urban area NHPs’ breeding facility was positive for the Bogor virus, while in peri-urban area NHPs’ breeding facility at as much as 15.38%. The surface protein gene of Wolbachia was detected in both locations with infection rates of 100% and 53.85% in urban and peri-urban area NHPs’ breeding facilities respectively.

Seventy-four bacterial phyla and five hundred and seventy-seven genera were identified in the pool samples analyzed. The phyla Proteobacteria (64.78%), Bacteroides (24.58%), and Firmicutes (3.83%) exhibited high average relative abundances. The number of bacterial species observed was greater in the pool samples of Ae. albopictus collected from peri-urban area compared to those from urban area. At the phylum level, the microbiota of male Ae. albopictus samples showed similarities between the two locations.

Ae. albopictus larvae in peri-urban area NHPs’ breeding facility occupied artificial habitat types that were not turbid, exposed to direct sunlight, and it had no predators. The abundance and occurrence of Ae. albopictus larvae were impacted by pH and total dissolved solids. Larvae of Ae. albopictus were predominantly found in buckets, bromeliads, cans, and artificial ponds. The investigated environment of the peri-urban area of NHPs’ breeding facility in this study was a suitable habitat for breeding site Ae. albopictus larvae. The environmental variable contributing to the species distribution model was the distance to buildings.

This study is the first report that provides a comprehensive molecular and ecological analysis regarding Ae. albopictus as a potential arbovirus vector in NHPs’ breeding facilities. The combination of the results of this analysis can be used as a recommendation or consideration in vector control and prevention of arbovirus transmission in NHPs’ breeding facilities.