When less means more: dehydration improves innate immunity in rattlesnakes

Abstract

Immune function can vary based on availability of resources, and most studies of such influences have focused on the co-investment of energy into immune and other physiological functions. When energy resources are limited, trade-offs exist, which can compromise immunity for other functions. As with energy, water limitation can also alter various physiological processes, yet water has received little consideration for its possible role in modulating immune functions. We examined the relationship between immunocompetence and hydration state using the western diamond-backed rattlesnake (). This species is known to undergo substantial seasonal fluctuations in water availability with extreme limitations during the hot-dry season. We collected blood samples from free-ranging to compare osmolality and innate immune function (lysis, agglutination and bacterial growth inhibition) during the milder and relatively moister early spring season, the hot-dry season and the hot-wet season. To isolate effects of dehydration from other possible seasonal influences, we complemented this field study with a laboratory study in which we withheld food and water from individually housed adult for up to 16 weeks. We collected blood samples from each snake as it dehydrated and collected a final sample after the snake was given water at the end of the experiment. Our results demonstrate that experience significant dehydration during the hot-dry season, and that, in general, innate immune function is highly correlated with osmolality, whether natural or artificially manipulated.

Dehydration enhances innate immunity in a semiaquatic snake from the wet‐dry tropics

“…We did not detect any significant increases in agglutination, however. These results are consistent with findings of a positive relationship between hyperosmolality and innate immune performance in other squamates (Gila monsters; Moeller, Butler, & DeNardo, ; rattlesnakes; Brusch & DeNardo, ; Children's pythons; Brusch et al, ). As in those studies, we found that rehydration rapidly returned immune metrics to baseline values (Figure ), suggesting that the innate molecules responsible for the positive influence of dehydration on immune function rapidly disassociate or become ineffective upon rehydration.…”

“…Comparing our data (pooled from our field and laboratory studies) with similarly pooled data from other experiments that used analogous methods on a sympatric species (Children's pythons; Brusch et al, ) and a xeric‐adapted species (western diamond‐backed rattlesnake; Brusch & DeNardo, ), reveal some interesting comparisons (Figure ). Water pythons have the smallest range of plasma osmolality of the three species (279–343 mOsm/kg), Children's pythons are intermediate (279–354 mOsm/kg), and rattlesnakes have the largest range (277–436 mOsm/kg).…”

“…Relationships between plasma osmolality (mOsm/kg) and immune scores. (a–c) lysis (CH 50 ), (d–f) percent bacteria ( Escherichia coli ) killed in pooled data from free‐ranging and laboratory held water pythons ( Liasis fuscus ; a,d; this study), Children's pythons ( Antaresia childreni ; b,e; Brusch et al, ), and western diamond‐backed rattlesnakes ( Crotalus atrox ; c,f; Brusch & DeNardo, ) . Gray circles represent individual blood samples, and the line of best fit is in black.…”

“…Children's pythons occur in the same area as water pythons (the study by Brusch et al, was conducted at Beatrice Hill) but are typically found in dry woodlands and rocky outcrops (Wilson & Swan, ) and may be adapted to longer periods without access to water (compared to semiaquatic water pythons). Similarly, the study by Brusch and DeNardo () used rattlesnakes from the Sonoran Desert, where the snakes often experience no rainfall for >3 months during annual seasonal droughts (and can survive for 16 weeks without water before showing signs of clinical dehydration). This variation in dehydration tolerance among species and the coinciding variable osmolalities at which immune scores are all elevated suggest that enhanced immune abilities are triggered by species‐specific physiological set points rather than absolute osmolality values per se.…”

“…In early June 2016, we collected 15 adult water pythons (male = 8, female = 7) from Beatrice Hill Farm and Harrison Dam, and transported them to the nearby University of Sydney's Tropical Ecology Research Facility, Middle Point, NT. Mass, sex, and SVL of each snake were recorded, and females were abdominally palpated to confirm they were not gravid as gravidity can affect both hydration and immune function in a sympatric python species (Brusch et al, ). Snakes were housed individually in translucent containers (87 × 60 × 29.5 cm) with lids and held at ambient temperature with natural light from rooftop windows.…”