Host biology and environmental variables differentially predict flea abundances for two rodent hosts in a plague-relevant system

Abstract

While rodents frequently host ectoparasites that can vector zoonotic diseases, often little is known about their ectoparasite communities, even in places where hosts frequently interact with humans. Yosemite National Park is an area of high human-wildlife interaction and high potential zoonotic disease transfer. Nonetheless, relatively few studies have surveyed the flea communities on mammalian hosts in this area, and even fewer have characterized the environmental and host factors that predict infestation. We focused on two species, the alpine chipmunk (Tamias alpinus) and the lodgepole chipmunk (T. speciosus), which inhabit Yosemite and surrounding areas and can host fleas that vector plague. Because these hosts are exhibiting differential responses to environmental change, it is valuable to establish baselines for their flea communities before further changes occur. We surveyed fleas on these chipmunk hosts during three years (2013-2015), including in the year of a plague epizootic (2015), and documented significant inter-host differences in flea communities and changes across years. Flea abundance was associated with host traits including sex and fecal glucocorticoid metabolite levels. The average number of fleas per individual and the proportion of individuals carrying fleas increased across years for T. speciosus but not for T. alpinus. To better understand these patterns, we constructed models to identify environmental predictors of flea abundance for the two most common flea species, Ceratophyllus ciliatus mononis and Eumolpianus eumolpi. Results showed host-dependent differences in environmental predictors of flea abundance for E. eumolpi and C. ciliatus mononis, with notable ties to ambient temperature variation and elevation. These results provide insight into factors affecting flea abundance on two chipmunk species, which may be linked to changing climate and possible future plague epizootics.

Keywords: Climate change; Host-parasite interactions; Sex-biased parasitism; Siphonaptera; Vector-borne disease; Yersinia pestis.

Graphical abstract

Fig. 1

Map showing study sites. Sites (see Supplementary Data S1 for more information) located in and around Yosemite National Park (green) were visited either in all three years (2013, 2014, and 2015; black), in two of the years (yellow), or in only one year (red). Yellow and black lines show significant roadways in the area. Lakes are shown in blue, including Mono Lake at top right. Inset shows Yosemite National Park (green) on a map of California. Site codes: AL: Arrowhead Lake; CL: Cathedral Lake (upper); GA: Glen Aulin; GL: Gaylor Lakes; HC: Hoffmann Creek; MA: Mammoth Lakes; ML: May Lake; PC: Porcupine Creek; SL: Saddlebag Lake; SLN: Saddlebag Lake, north-side (Greenstone and Steelhead Lakes); TM: Tuolumne Meadows. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2

Patterns of flea abundance across years, hosts, and flea species. Overall average flea abundances (A–B) and abundances of each flea species (C–D) in each year for T. alpinus (A, C) and T. speciosus (B, D). Abundances of each flea species on hosts of each sex (Males: closed circles, Females: open circles) on T. alpinus (E) and T. speciosus (F).

Fig. 3

Cumulative distribution plots divided by year for (A) T. alpinus and (B) T. speciosus. For each species 2013 is shown in red, 2014 in teal, 2015 in pink. The x-axis represents each host individual, ordered from least to most flea infested, and the y-axis shows the cumulative proportion of total flea counts. The dotted line indicates individuals in the 90^th percentile of flea abundances, illustrating that the top 10% most infected chipmunks usually account for close to 50% of all counted fleas. The proportion of individuals without fleas in each year is represented graphically as the proportion at which each colored line departs from the x-axis. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4

Relationships between fecal glucocorticoid metabolite levels, sex, and flea abundance for (A) T. alpinus and (B) T. speciosus. Points show the mean±S.E. number of fleas counted for female (white) and male (black) individuals within FGM categories (FGM values were rounded to the nearest 10). Lines of best fit (based on all raw data points) ±95% confidence intervals are overlaid for each sex.

Fig. 5

Relationships between flea abundances and (A) the second principal component of temperature data; or (B) elevation for T. alpinus (white) and T. speciosus (black). Points show the mean±S.E. number of fleas counted for a given study site in a given year. For each study site in each year, a mean±S.E. temperature or elevation value is shown. Lines of best fit (based on all raw data points) ±95% confidence intervals are overlaid for each species.