Rain-harvesting behavior in free-ranging prairie rattlesnakes (Crotalus viridis)

Abstract

Organisms inhabiting arid environments face challenges to obtain dietary water. To prevent desiccation, some organisms possess unique adaptations to harvest water from infrequent and unpredictable rainfall, including several squamates (snakes and lizards). While most squamates consume precipitation as it pools in the environment, a small number engage in behaviors to enhance water collection by capturing precipitation from their own skin, referred to as rain-harvesting behavior (RHB). Details of this behavior remain unclear, particularly the sequence of behaviors associated with RHB. We developed a method to simulate rainfall to observe RHB in prairie rattlesnakes (Crotalus viridis) in situ and recorded 72 events in 94 snakes, the most robust sampling of RHB to date. Using video analysis, we describe the postures and kinematics of RHB and develop the first illustrated ethogram of this behavior for any vertebrate. Our results demonstrate that RHB contains fixed and variable patterns useful in cross-species comparisons and in exploring proximate causes of the behavior. In addition, we describe novel features of RHB including suspended head drinking, body levering, and drinking from neighboring snakes. Our results reveal RHB to be an intricate suite of movements and actions, some of which allude to acute sensory abilities of these animals that warrant further study. Furthermore, observations of RHB at dens and rookeries suggest a potential, novel benefit of snake aggregation is the formation of large, communal surfaces for rain harvesting. We suggest that the extremely elongated body plan of snakes may be well-suited for a rapidly deployed, modular rain-harvesting system effective at capitalizing on fleeting rainstorms characteristic of arid ecosystems of the world.

Keywords: climate; drinking; ethogram; rainfall; reptile; squamate.

Graphical Abstract

Figure 1.

An ethogram of rain-harvesting behavior (RHB) in prairie rattlesnakes (Crotalus viridis). The outer green line encompasses behaviors before drinking occurred, the light blue line encompasses drinking behavior, and the purple line encompasses behaviors after drinking ceases. Typical progression through the behavior is indicated with black arrows. Gray arrows indicate how snakes can bypass the Body Positioning phase and/or briefly re-enter the Exploration phase from the Drinking phase. Phases are defined by several characteristics highlighted in the results. The relative lengths of each phase do not reflect the amount of time snakes spend in each (see text). Rest: Prior to the onset of the simulated rain event (SRE) with little to no tongue-flicking, Initiation: Occurs immediately after the start of the SRE. Tongue flicking and head elevation occurs, Exploration: Increased tongue-flicking continues with greater head movement as the snake probes the surrounding environment for suitable drinking surfaces, Body Positioning: The snake moves its body appropriately to capture and pool water including coiling and dorsoventral flattening its body, Drinking: The snake drinks and adjusts its head angle based on drinking surface, Post-Drinking: Relaxation of body flattening and mimics behaviors in rest or exploration.

Figure 2.

Example of a prairie rattlesnake (Crotalus viridis) before (A) and after (B) a simulated rain event (SRE). Note in (B) the snake is dorsoventral flattening its body and is drinking from a trough created by the junction of one body coil (foreground) with another (beneath snake’s head).

Figure 3.

A barplot representing the number of prairie rattlesnakes (Crotalus viridis) that exhibited tongue flicking behavior before, during, and after simulated rain events (SREs) that ultimately drank (yellow bars) or did not drink water (purple bars).

Figure 4.

Proportional area plot showing the relative proportion of snakes that drank water off different surfaces during simulated rain events (SREs) when drinking off a single surface (left side, N = 20) or more than one surface (right side, N = 21). Circle colors on the right side are blended from those on the left (e.g., Substrate = yellow, Self = teal, thus Self + Substrate = light green).

Figure 5.

Raincloud plots of head angles (A) and drinking durations (B) when prairie rattlesnakes (Crotalus viridis) drank off different surfaces: neighboring snake (purple), non-snake surfaces like rocks and leaves (yellow), and self (teal). Head angles varied based on the surface that the snake was drinking from, but these differences were not significant. Head angles varied between 0 degrees through 180 degrees, with 90 degrees being horizontal to the ground (see Supplementary Figure 1).

Figure 6.

A still image obtained from a video of a prairie rattlesnake (Crotalus viridis) subjected to a simulated rain event (SRE) on a talus slope. Note the snake is exhibiting coiling and dorsoventral flattening despite the uneven surfaces where it is positioned. A body loop (coil) can be seen projecting horizontally (right side of snake) and above the rocks supporting the rest of the snake.