Climate-driven variation in the phenology of juvenile Ixodes pacificus on lizard hosts.

Abstract

Background: Ectothermic arthropods, like ticks, are sensitive indicators of environmental changes, and their seasonality plays a critical role in the dynamics of tick-borne disease in a warming world. Juvenile tick phenology, which influences pathogen transmission, may vary across climates, with longer tick seasons in cooler climates potentially amplifying transmission. However, assessing juvenile tick phenology is challenging in arid climates because ticks spend less time seeking for blood meals (i.e. questing) due to desiccation pressures. As a result, traditional collection methods like dragging or flagging are less effective. To improve our understanding of juvenile tick seasonality across a latitudinal gradient, we examined Ixodes pacificus phenology on lizards, the primary juvenile tick host in California, and explored how climate factors influence phenological patterns.

Methods: Between 2013 and 2022, ticks were removed from 1527 lizards at 45 locations during peak tick season (March-June). Tick counts were categorized by life stage (larvae and nymphs) and linked with remotely sensed climate data, including monthly maximum temperature, specific humidity and Palmer Drought Severity Index (PDSI). Juvenile phenology metrics, including tick abundances on lizards, Julian date of peak mean abundance and temporal overlap between larval and nymphal populations, were analyzed along a latitudinal gradient. Generalized additive models (GAMs) were applied to assess climate-associated variation in juvenile abundance on lizards.

Results: Mean tick abundance per lizard ranged from 0.17 to 47.21 across locations, with the highest abundance in the San Francisco Bay Area and lowest in Los Angeles, where more lizards had zero ticks attached. In the San Francisco Bay Area, peak nymphal abundance occurred 25 days earlier than peak larval abundance. Temporal overlap between larval and nymphal stages at a given location varied regionally, with northern areas showing higher overlap, possibly due to the bimodal seasonality of nymphs. We found that locations with higher temperatures and increased drought stress were linked to lower tick abundances, although the magnitude of these effects depended on regional location.

Conclusions: Our study, which compiled 10 years of data, reveals significant regional variation in juvenile I. pacificus phenology across California, including differences in abundance, peak timing, and temporal overlap. These findings highlight the influence of local climate on tick seasonality, with implications for tick-borne disease dynamics in a changing climate.