Wade C. Sherbrooke

Functional morphology of scale hinges used to transport water: convergent drinking adaptations in desert lizards ( Moloch horridus and Phrynosoma cornutum )

The Australian thorny devil, Moloch horridus Gray, 1841, and the Texas horned lizard, Phrynosoma cornutum Harlan, 1825, have the remarkable ability to rapidly move water through interscalar spaces on their skin’s surface to their mouth for drinking. The morphology of these scale hinges has not been studied. We used histological and SEM techniques to examine and compare the scale hinges of both species. Additional taxa in their respective lineages were examined in order to evaluate the potential that convergent evolution has occurred. In the two species that transport water, each scale hinge has a basally expanded and semi-enclosed channel formed by the hinge joint that is interconnected with all scale hinges on the body. We hypothesize that it is within this semi-tubular channel system of hinge joints, where the β-layer keratin of the integument is very thin, that water is transported. Hinge joint walls are covered by a complex topography of fractured surfaces that greatly expand the channel’s surface area and probably enhance capillary transport of water. In addition, we note differing morphology of scale surfaces at the rear of the jaws of both species. We hypothesize that capillary forces fill the scale-hinge system and additional forces, generated within the mouth by observed motions during drinking, depress local water-pressure to pull water through the channels of the hinge-joint system. We conclude that the combined features in the two species, semi-tubular hinge-joint channels with convoluted walls and a jaw-buccal cavity pumping-mechanism, have convergently evolved for capture, transport, and drinking of water from sporadic rainfall.

Temperature Effects on in vitro Skin Darkening in the Mountain Spiny Lizard, Sceloporus jarrovi: A Thermoregulatory Adaptation?

The in vitro sensitivity of integumental pigment cells (melanophores) to darkening hormones was studied in a winter-active montane lizard (Sceloporus jarrovii) that rapidly changes color. The darkening responses, shown by dose-response curves, of skin samples to melanophore-stimulating hormone (α-MSH) were slightly higher at 15° than at 25°C, but not significantly so. At 35°C, as compared to 25°C, the darkening responses were dramatically and unexpectedly reduced, a sevenfold higher concentration of α-MSH being needed to elicit equivalent responses. Darkening responses to isoproterenol, a β-adrenoceptor agonist, applied to skins in the presence of the a-adrenoceptor blocker Dibenamine, were significantly diminished at both 15° and 35°C, as compared to 25°C The similarity of the dose-response curves for α-MSH at 15° and 29°C (no reduction in sensitivity at the lower temperature) and the marked decrease of response to α-MSH and isoproterenol at 35°C are consistent with the thermoregulatory chromatic behavior of the animal: dark color at low temperatures in order to maximize heat gain, and light color once high, activity body temperature is achieved. These in vitro results suggest a direct, temperature-dependent, cellular response of S. jarrovii chromatophores to hormones. The temperature pattern suggests that the cellular response may be adaptive. Parallel experiments performed with Anolis carolinensis, a species that displays physiological color changes for crypsis rather than thermoregulation, demonstrated that the sensitivities to both a-MSH and isoproterenol were significantly lower at 15° and 35°C, compared to 25°C Our results suggest that reptile pigment cell sensitivity to hormones at varying temperatures may be regulated at the cellular level.

Antipredator Responses by Texas Horned Lizards to Two Snake Taxa with Different Foraging and Subjugation Strategies

Abstract The discrimination ability of Texas Horned Lizards (Phrynosoma cornutum) during antipredator responses was tested with snakes of two genera having distinctly different prey foraging and subjugation strategies; Western Diamondback Rattlesnakes (Crotalus atrox) are “sit-and-wait” predators with a venomous strike from ambush, whereas whipsnakes (Masticophis spp.) are nonvenomous, rapid pursuit-and-grasp predators. Neither snake constricts prey; both ingest prey whole. Lizards were watched for reactions during close approaches by moving snakes. All unapproached and some approached lizards remained alert and motionless. Approached lizards that reacted either (1) ran rapidly to a distant point in the large enclosure, or (2) maintained their position but dorsoventrally flattened their body and tilted their stance, orienting a “dorsal shield” posture toward the snake. The distinctly contrasting responses of the lizards to the two snakes were significantly different, relocation running from rattlesnakes and stationary-body reorientation toward whipsnakes. For slow-running, broad-bodied Texas Horned Lizards, running is an appropriate escape response to a nonpursuing venomous predator, whereas the nonrunning body-conformation/orientation change is an appropriate defensive response, advertising size and spiny defenses, to a rapid-pursuit snake that must grasp prey with its jaws to effect capture and subjugation. Apparently horned lizards visually recognized, probably innately, the two snake taxa as different categories of predator threat.

Responses of Kit Foxes (Vulpes macrotis) to Antipredator Blood-Squirting and Blood of Texas Horned Lizards (Phrynosoma cornutum)

Abstract Six related studies were conducted with four captive juvenile Kit Foxes (Vulpes macrotis) to test the hypothesis that blood-squirting from eye-socket tissues by Texas Horned Lizards (Phrynosoma cornutum) is a canid antipredator defense. In 16 trials, naive “hungry” foxes killed and ate adult Yarrows Spiny Lizards (Sceloporus jarrovii; eight of eight trials) slightly more frequently than adult P. cornutum (six of eight trials). Adverse responses by foxes (head shaking) were seen in five of six trials in which Phrynosoma squirted blood. Later these experienced foxes, fed ad libitum, killed and ate mice (eight of eight trials) while largely ignoring P. cornutum (one killed and eaten in eight trials), suggesting a learned aversion to horned lizards as prey. During attacks on mice smeared with horned-lizard blood, foxes displayed behaviors typical of predatory encounters with horned lizard prey (head shaking and prey tearing). These prey-handling behaviors were in striking contrast to those elicited by untreated mice and by mice treated with mouse blood, demonstrating that horned-lizard blood (and its chemical constituents) altered normal behaviors toward mouse prey. Prey-handling times for mice treated with horned lizard blood were significantly longer than mouse-only treatments. Responses of foxes to mice coated with horned lizard Harderian- and lacrimal-gland tissues coupled with responses to mice coated with systemic horned-lizard blood, mouse blood, and untreated mice suggest that (1) no defensive chemicals are added to the blood by orbital glands before blood ejection, and (2) active antipredator chemicals are carried in the circulating blood as well as in squirted blood. In four trials, foxes attacked “de-horned” horned lizards; a role for cranial horns in facilitating predator hesitancy prior to blood squirting is proposed. Evidence is presented that horned lizards visually identify and categorize foxes as appropriate predators for a blood-squirting defense. We conclude that, in many predator-prey encounters with wild canids, blood-squirting by Texas Horned Lizards is an effective chemical defense. We propose a scenario for the evolution of this unique defense and suggest that the defensive compounds found in the blood may be sequestered from the seed-harvester ant prey of horned lizards.

Rain-drinking behaviors of the Australian thorny devil (Sauria: Agamidae)

During natural and simulated rainfall, Moloch horridus used the cutaneous surface of its integument as a water-harvesting system to capture rain water for drinking. Circumstantial behavioral evidence, in combination with experimental studies (Withers, 1993), suggests that the capillary, interscalar, water-transport system of Moloch is also used to absorb water for drinking from rain-moistened substrates. Lizards rub their venters against wet substrates and dig sand onto their backs. This is a previously unreported behavior for water acquisition by lizards inhabiting arid regions. No stereotypic behavioral stance for rain harvesting, as seen in Phrynocephalus helioscopus and Phrynosoma cornutum, was observed in Moloch horridus

Horned lizards (Phrynosoma) incapacitate dangerous ant prey with mucus

Horned lizards (Iguanidae, Phrynosomatinae, Phrynosoma) are morphologically specialized reptiles characterized by squat, tank-like bodies, short limbs, blunt snouts, spines and cranial horns, among other traits. They are unusual among lizards in the degree to which they specialize on a diet of ants, but exceptional in the number of pugnacious, highly venomous, stinging ants they consume, especially harvester ants (genus Pogonomyrmex). Like other iguanian lizards, they capture insect prey on the tongue, but unlike other lizards, they neither bite nor chew dangerous prey before swallowing. Instead, they employ a unique kinematic pattern in which prey capture, transport and swallowing are combined. Nevertheless, horned lizards consume dozens of harvester ants without harm. We show that their derived feeding kinematics are associated with unique, mucus-secreting pharyngeal papillae that apparently serve to immobilize and incapacitate dangerous ants as they are swallowed by compacting them and binding them in mucus strands. Radially branched esophageal folds provide additional mucus-secreting surfaces the ants pass through as they are swallowed. Ants extracted from fresh-killed horned lizard stomachs are curled ventrally into balls and bound in mucus. We conclude that the pharyngeal papillae, in association with a unique form of hyolingual prey transport and swallowing, are horned lizard adaptations related to a diet of dangerous prey. Harvester ant defensive weapons, along with horned lizard adaptations against such weapons, suggest a long-term, predator-prey, co-evolutionary arms race between Phrynosoma and Pogonomyrmex.

Effects of recent movement, starting distance and other risk factors on escape behaviour by two phrynosomatid lizards

Cost–benefit models of escape behaviour predict that flight initiation distance (FID, predator-prey distance when the prey starts to flee from an approaching predator) increases as the cost of not fleeing (risk) increases. This prediction has been verified for many risk factors and prey species. The same predictions may apply to other aspects of escape, but testing has been much less extensive. For the lizards Callisaurus draconoides and Sceloporus magister, we tested several such predictions and examined the effect of a previously unstudied risk factor, recent movement by prey. Starting distance (predator-prey distance when approach begins) was unrelated to FID in C. draconoides, as in previously studied ambush foragers. Because movement increases probability of being detected, we predicted that FID would be greater for prey that had moved immediately before being approached than those that had been immobile. FID and distance fled (DF) were longer for lizards that had moved recently. In C. draconoides DF and probability of entering refuge were greater for the second of two approaches, as predicted from greater threat posed by a persistent predator. Callisaurus draconoides had shorter FID and shorter DF, and fewer entered refuge where lizards were habituated than unhabituated to human presence. In S. magister FID increased as distance to refuge increased, FID and DF were longer for fast than slow approaches; probability of fleeing and FID were larger for direct than indirect approach. Effects of these risk factors on FID are consistent across studies, but approach speed has affected DF in only half of studies, perhaps due to constraints by refuge entry and variable distance to refuge. Similarities in effects of risk factors across escape variables, types of predator-prey encounters, and latency to emerge from refuge suggest that similar risk assessment mechanism are used for all variables and settings.

SENSORY MODALITY USED BY COYOTES IN RESPONDING TO ANTIPREDATOR COMPOUNDS IN THE BLOOD OF TEXAS HORNED LIZARDS

Abstract We investigated the hypothesis that the squirting of blood from orbital sinuses by Texas horned lizards (Phrynosoma cornutum) is an antipredator defense against some mammalian species. Coyotes (Canis latrans) were tested for the first time. As expected, Texas horned lizards squirted blood in response to coyote attacks, and coyotes exhibited startle response, avoidance response, or both as a result of these events. Whereas lizard carcasses mixed into normal food-mash elicited regurgitation by coyotes, possibly due to physical effects, blood of horned lizards similarly mixed into food did not. Coyote responses to simulated squirts of 5 compounds, including blood of horned lizards, into 3 potential sensory target areas (eyes, nose, and mouth) strongly suggested that aversive effects were mediated by receptors in the oral or nasal cavities. Coyote responses were more frequent to delivery of blood plasma and whole blood of Phrynosoma to buccal and nasal membranes than to delivery of plasma and blood from spiny lizards (Sceloporus jarrovii) or to delivery of a saline control to these membranes. We concluded that Texas horned lizards squirt blood from sinuses surrounding the eyes during attacks by canids, such as coyotes, and that this blood affects oral receptors, causing a negative response in coyote attack behavior that potentially increases survival of the lizards.

Risk and cost of immobility in the presence of an immobile predator

Escape latency theory models the tradeoff between maintaining crypsis by remaining immobile near an immobile predator versus moving to flee or engage in fitness-enhancing activities. The model predicts that latency to flee increases as cost of fleeing increases and decreases as cost of remaining immobile increases. As predation risk increases, cost of fleeing, primarily due to abandoning crypsis due to immobility, decreases. Predictions have been tested for few risks and a single cost of immobility factor in only two species of active foragers. To gauge the breadth of applicability of the model, we tested effects of four risk factors and two cost of immobility factors in ambush-foraging phrynosomatid lizards, which we selected for testing because foraging mode strongly affects many aspects of ecology and behavior of lizards. Latency to flee decreased as standing distance (predator–prey distance before fleeing) decreased, predator approach speed increased, directness of approach increased, and predator persistence increased. Latency to move was shorter in the presence of food and shorter for males in the presence of females. Lizards often moved toward food or females instead of fleeing. Latency was affected as predicted by all risk and by cost of remaining immobile factors. Our findings agree with previous results for the same four risk factors and the foraging cost of immobility. That social cost of immobility affects latency as predicted is a novel finding. The model is robust, applying to ecologically diverse prey and to a wide range of factors affecting costs of fleeing and of immobility.

Physiological (rapid) change of color in horned lizards

Rapid color-change in three congeneric desert lizards of diverse size was studied and compared. Using in vitro skins, the highest % skin-darkening values (15-19%) of dose-response curves for α-melanophore stimulating hormone (α-MSH) were determined for each species. In the smallest species, Phrynosoma modestum, melanophores responded to α-MSH over the broadest range, 2.5 x 10 -10 - 6.5 10 -8 M. Isoproterenol, a β-adrenoceptor agonist, was less effective than α-MSH at darkening skins, 5% in P. cornutum. Norepinephrine (NE), an α-adrenoceptor agonist, dramatically lightened α-MSH darkened skins of P solare and P modestum. Catecholamine responses were further investigated with the α-adrenoceptor blocker Dibenamine and the β-adrenoceptor blocker oxprenolol. Phrynosoma cornutum did not respond to NE. The effects of temperature on α-MSH activity were studied in vitro and in vivo. Skins in vitro darkened most rapidly in response to α-MSH at 41°, to an intermediate degree at 22°, and least at 6°C. Lizards in vivo exhibited the darkest color at 22°, lightest at 41°, and intermediate color at 6°C. A potent α-MSH receptor agonist, [Nle 4 , D-Phe 7 ]-α-MSH, was used to further study the significance of temperature on in vivo α-MSH regulation of color. Both P. cornutum and P. modestum placed on black-and-white backgrounds for twenty-four hours failed to show background matching. Diel color changes associated with thermoregulatory needs are apparently consistent with crypsis, an antipredator strategy; cool lizards darken (to increase solar thermal gain) in early morning and late afternoon when background shadows are prominent, and warm lizards lighten (to reduce solar thermal gain) at midday when the albedo of the environment is high.