Thermal correlates of foraging-site selection by Chinese pit-vipers (Gloydius shedaoensis, Viperidae)

Abstract

• Do thermal factors influence foraging-site selection by ectothermic predators? Snake species that obtain their prey from ambush must remain immobile for long periods, precluding overt behavioural thermoregulation; and some “ambush” snakes use thermal cues to detect endothermic prey. Plausibly, alternative ambush sites might differ either in equilibrial body temperatures available to snakes, or in the thermal “background” against which prey items must be detected.

• We examined this topic with field data on pit-vipers (Gloydius shedaoensis) on a small island in northeastern China. Adult snakes feed only on migrating passerine birds. The snakes ambush birds both from arboreal perches (branches of small trees) and from the ground.

• Arboreal versus terrestrial ambush sites differed both in operative temperatures and thermal “backgrounds” available to the snakes. Operative temperatures inside copper models were lower in trees than on the ground (because of wind), and snakes in arboreal ambush sites were cooler than those in terrestrial sites. Thermal backgrounds from arboreal perches were cooler (and thus, provided more contrast against prey items) than did backgrounds available from terrestrial ambush-sites.

• Thermal factors thus modify the suitability of alternative ambush locations for these pit-vipers, but with a trade-off: a snake in a tree can “see” its prey more clearly, but may not be warm enough (and hence, able to strike fast enough) to capture it. Further work is required to determine whether or not snakes actually use such thermal differences as criteria for the selection of ambush sites.

Introduction

Many natural environments display substantial thermal heterogeneity. Especially when ambient temperatures are low but solar radiation is intense, an ectothermic animal can choose between adjacent sites with very different operative temperatures (e.g. Huey and Slatkin, 1976; Huey, 1991; Peterson et al., 1993). Such sites may also differ in other ways relevant to the organism's biology: for example, an exposed site may offer better basking opportunities, but simultaneously increase vulnerability to predators and reduce rates of encounter with prey (Huey, 1974). Presumably, patterns of habitat selection reflect a compromise among these conflicting optima. The selection of an appropriate site is most important for sedentary animals, and especially for ambush (“sit-and-wait”) predators. Because they rely upon immobility for effective concealment, such animals cannot move about to track temporal shifts in weather conditions. They may thus need to forego precise thermoregulation (Hertz et al., 1993; Webb and Shine, 1998). In keeping with these ideas, previous studies have reported lower, more variable body temperatures in free-ranging pit-vipers than in sympatric active-foraging snakes (Secor and Nagy, 1994). Rattlesnakes selected higher, more stable temperatures after feeding (Beck, 1996), suggesting that they had tolerated lower more variable temperatures while waiting in ambush for prey.

The significance of this potential conflict between foraging and thermoregulation will depend upon the degree to which alternative potential ambush-sites do indeed constrain body temperatures in different ways. In a closed-canopy forest, for example, spatial heterogeneity in operative temperatures will usually be low, and hence most potential ambush-sites may be equivalent thermally. However, predators in many other habitat types may have to choose between alternative ambush sites that differ profoundly in their thermal consequences. We have studied such a system in insular pit-vipers on a small island in northeastern China.

The pit-vipers of Shedao are well-suited to analyse this topic for several reasons. First, the climate is cool. The snakes feed only at the beginning of spring and the end of autumn, immediately after and before the hibernation period respectively. Their prey—migrating passerine birds—also visit the island earlier in spring and later in autumn, but the snakes are inactive at these times (Sun et al., 1990; Li, 1995). Because ambient temperatures constrain the seasonal timing of feeding, we might expect thermal factors to play some role in foraging success. Laboratory trials confirm that hotter Shedao pit-vipers strike faster and further (Shine et al., 2002). Second, the snakes are sedentary and capture their prey from ambush (Li, 1995; Sun et al., 2000). Because the snake cannot move about to thermoregulate, its body temperature will be determined by its selection of an ambush site. Third, the two main alternative types of ambush site are in trees versus on the ground (Fig. 1), and biophysical modelling suggests that these alternatives may provide very different operative temperatures (Bakken and Gates, 1975). Fourth, pit-vipers localize prey items using specialized infrared detectors (loreal pits) that rely on thermal contrast between the prey item and the background (de Cock Buning et al., 1981; de Cock Buning, 1983). Hence, ambush sites may also differ in the ease with which snakes can detect prey using their loreal pits. To maximize the thermal contrast of prey versus background, a snake might forage in sites where a warm bird would stand out against a relatively cool background.

We visited Shedao for most of one spring feeding season to quantify the thermal attributes of arboreal versus terrestrial ambush sites, in terms of operative temperature regimes as well as thermal “backgrounds” for prey detection. We also measured body temperatures of snakes both in ambush positions in the field and when provided with a thermal gradient in captivity.