ABSTRACT
The Arizona State University (ASU) Tempe campus is inhabited by some 55,000 enrolled students as well as several mosquito species that can transmit West Nile virus, dengue, Zika, chikungunya, and yellow fever. The time of host-seeking of these vectors has not been quantified on the ASU Tempe campus, but this information is important to inform ground and/or truck-mount fogging operations targeting mosquitoes to prevent or control disease outbreaks. We quantified the time of host-seeking of the predominant mosquito vector species at the ASU Tempe campus during the post-monsoon season in 2021, using collection bottle rotators with encephalitis vector survey traps that were baited with CO2, at 3 h intervals during a full day. Culex quinquefasciatus, Aedes aegypti, and Culex tarsalis were the most abundant species captured. Pre-midnight host-seeking (18:00–00:00) accounted for 52% of all captures, whereas post-midnight host-seeking (00:00–06:00) accounted for 35% of all captures. Peak activity times were between 21:00 and 00:00 for Cx. quinquefasciatus and Cx. tarsalis, and between 15:00 and 18:00 for Ae. aegypti. Data can be used to inform local mosquito surveillance and control programs.
Tempe, Arizona, a city east of Phoenix, has an estimated population of 185,000, and contains several mosquito vector species that are well established and capable of transmitting arboviral diseases such as dengue, Zika, chikungunya, yellow fever (primarily vectored by Aedes aegypti [Linnaeus], and Aedes vexans [Meigen]), West Nile virus (WNV) (primarily vectored by Culex tarsalis [Coquillett] and Culex quinquefasciatus [Say]). West Nile virus is endemic in Maricopa County, in which Tempe resides (Kretschmer et al. 2023b). This may partially be contributable to the numerous wetland and riparian areas embedded in the city, as these locations are simultaneously suitable habitats for Culex mosquitoes and bird reservoirs (Dimenna et al. 2006; DeGroote et al. 2008; Komar et al. 2013). Tempe also houses the vast Arizona State University (ASU) campus, encompassing an estimated 2.7 km2 in size. In 2021, 54,866 students were enrolled (ASU, 2021), including an estimated 15,000 international students. Arboviral transmission from travel-associated cases may threaten the establishment of arboviruses such as dengue and Zika in Arizona, as vector populations are already well established (Kretschmer et al. 2023a).
Although human movement on campus is not quantified, classes, sporting events, recreational activities, and student events take place during the morning, afternoon, and evening, bringing potential human hosts to campus. Vector species are also expected to be active during those times, e.g., Aedes spp. during daytime (Smith et al. 2018; Mutebi et al. 2022) and Culex spp. during nighttime (Wilke et al. 2023). However, there is currently no campus-specific vector surveillance in place, and host-seeking activity has never been quantified for mosquitoes on campus. The aim of this study was to identify local principal vector species and their time of host-seeking activity in the Tempe campus following the monsoon season in 2021.
Collection Bottle Rotators (John W. Hock Company, FL, USA) were placed in two locations on the Tempe campus adjacent to 1) the ASU Farmer Education building (105 S Forest Mall, Tempe, AZ, hereafter referred to as “location 1”), and 2) the Social Sciences building (951 Cady Mall, Tempe, AZ, hereafter referred to as “location 2”). Each rotator, equipped with 8 collection nets, was set to rotate every 3 h to evaluate mosquito host-seeking activity across a full 24-h cycle (i.e., 09:00–12:00, 12:00–15:00, etc.). An Encephalitis Vector Survey (EVS) (BioQuip Products Inc., CA, USA) trap was placed on top of the rotator and was baited with CO2 (∼5 cm above the EVS trap, 0.5 kg/day). Each rotator was run for 5 days/wk during the study period (October–November 2021, 23 days of sampling), starting each day at 09:00. Identification of captured mosquitoes was done through stereomicroscopy by Maricopa County Environmental Services personnel. Per species, trap-specific mean number of female mosquitoes captured per 3 h period were analyzed using analysis of variance (ANOVA) with a Tukey’s HSD test in R v. 4.2.1. (The R Foundation 2023).
A total of 376 female mosquitoes were captured, consisting of 341 Cx. quinquefasciatus, 18 Cx. tarsalis, and 17 Aedes aegypti (Fig. 1). Location 1 captured a total of 127 females (118 Cx. quinquefasciatus, 2 Cx. tarsalis, and 7 Ae. aegypti); location 2 captured a total of 249 females (223 Cx. quinquefasciatus, 16 Cx. tarsalis, and 10 Ae. aegypti). Time of day was significant for Cx. quinquefasciatus activity (ANOVA: alpha = 0.05, F(7) = 12.6713, P < 0.001; Fig. 1).
Pre-midnight nighttime host-seeking (18:00–00:00) accounted for 195 captures (52%) consisting of 183 Cx. quinquefasciatus (54% of all Cx. quinquefasciatus captures); 10 Cx. tarsalis (56% of Cx. tarsalis); and 2 Ae. aegypti (12% of Ae. aegypti). Post-midnight nighttime host-seeking (00:00–06:00, when truck-mount fogging typically takes place in areas outside the Tempe campus) accounted for 132 captures (35%) consisting of 123 Cx. quinquefasciatus (36% of Cx. quinquefasciatus captures); 8 Cx. tarsalis (44% of Cx. tarsalis captures); 1 Ae. aegypti (6% of Ae. aegypti captures). Peak activity times were between 21:00 and 00:00 for Cx. quinquefasciatus and Cx. tarsalis, and between 15:00 and 18:00 for Ae. aegypti.
The aim of this study was to quantify the time of host-seeking of mosquito vectors present on ASU Tempe during the post-monsoon season. Culex spp. are known to be nighttime biters (Breidenbaugh et al. 2009; Wilke et al. 2023), which was confirmed in our study: 94% of Cx. quinquefasciatus and 100% of Cx. tarsalis were collected between 18:00 and 06:00. The time at which Ae. aegypti was most active (15:00–18:00) is also in line with their known peak activity patterns during daytime and dusk/dawn (Breidenbaugh et al. 2009; Smith et al. 2018).
However, the majority of Cx. quinquefasciatus and Cx. tarsalis were collected between 21:00 and 00:00, which differed from the post-midnight peak observed for vector species (Cx. tarsalis, Ae. vexans, and Cx. quinquefasciatus) during a similar study earlier that year (Spring, 2021) at the Salt River Pima Maricopa Indian Community (Kalmouni et al., unpublished data). However, in that same study, a majority in Cx. tarsalis and Cx. quinquefasciatus were captured during pre-midnight hours (18:00–00:00) at the end of the study, when mosquito activity monitoring was switched to 1-h periods. Diurnal rhythms of insects assist in the synchronization of host-seeking behaviors. Ae. aegypti are typically considered daytime biters and have been observed to have bimodal peaks in activity (morning and evening) (Mutebi et al. 2022), a trend also observed in this study, though increased crepuscular activity compared to nocturnal activity has also been observed (Ndenga et al. 2022). Differences in host-seeking patterns observed in summer months compared to autumnal months can in part be potentially explained through diel daylight variation associated with seasonality (i.e., longer or shorter durations of daylight, shifted times of twilight hours, etc.). Other related factors include temperature (e.g., daytime temperatures are warmer in the summer than in the autumn) and circadian rhythm variability.
As such, time of host-seeking appears to vary temporally and spatially (Ryan et al. 2017; Smith et al. 2018; Wilke et al. 2023), and although general trends were observed in this study, the study was limited by 1) its short duration and 2) two sampling locations. Overall capture rates were low, which limits our interpretation of host-seeking trends in this area. Future studies should assess mosquito host-seeking across seasons and in several locations, as confounding factors (such as climate, human population densities, and water availability) are known to affect mosquito abundance. In addition, implementing additional traps, each specializing in distinctive baiting methods (i.e., effective in Culex spp. captures, such as the Centers for Diseases Control and Prevention [CDC] Light Trap); gravid mosquitoes, such as the CDC Gravid Trap; resting traps; etc.) would improve our overall understanding of the vector presence on ASU’s Tempe campus.
Human activity (from students, staff, faculty, visitors, etc.) is present throughout the day (e.g., during classes) and extends into the evening such as through large sports events and late-night events that are regularly hosted by the Memorial Union (the campus community center) throughout the year. Mosquito host-seeking in this study was observed in the morning, afternoon, and evening, and thus there are potentially human-vector interactions throughout all time intervals during the day.
Given the fact that we have human (including a large proportion of international students, which may have potential for travel-associated cases), mosquito, and bird populations present on our Tempe campus, vector surveillance (including monitoring the time of host-seeking) should be considered by the university or its partners at least during peak seasons of abundance and disease transmission risk. A better understanding of how and when human hosts move across campus could better inform vector control efforts and public health outreach on how to reduce vector-borne disease transmission.
We thank Brook M. Jensen for her assistance with this study’s logistics and data visualization. Krijn P. Paaijmans was supported by National Science Foundation (award number 2052363), a grant from ASU’s Women and Philanthropy, and acknowledges funding support from the Pacific Southwest Regional Center of Excellence for Vector-Borne Diseases funded by the CDC (Cooperative Agreement 1U01CK000649). This study’s contents are solely the responsibility of the authors and do not necessarily represent the official views of the CDC.
REFERENCES CITED
Author notes
The Center for Evolution & Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85281
Vector Control Division, Maricopa County Environmental Services Department, Phoenix, AZ 85009
Simon A. Levin Mathematical, Computational and Modeling Sciences Center, Arizona State University, Tempe, AZ 85281
Wits Research Institute for Malaria, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa