Kurt Schwenk

History and the Global Ecology of Squamate Reptiles

The structure of communities may be largely a result of evolutionary changes that occurred many millions of years ago. We explore the historical ecology of squamates (lizards and snakes), identify historically derived differences among clades, and examine how this history has affected present‐day squamate assemblages globally. A dietary shift occurred in the evolutionary history of squamates. Iguanian diets contain large proportions of ants, other hymenopterans, and beetles, whereas these are minor prey in scleroglossan lizards. A preponderance of termites, grasshoppers, spiders, and insect larvae in their diets suggests that scleroglossan lizards harvest higher energy prey or avoid prey containing noxious chemicals. The success of this dietary shift is suggested by dominance of scleroglossans in lizard assemblages throughout the world. One scleroglossan clade, Autarchoglossa, combined an advanced vomeronasal chemosensory system with jaw prehension and increased activity levels. We suggest these traits provided them a competitive advantage during the day in terrestrial habitats. Iguanians and gekkotans shifted to elevated microhabitats historically, and gekkotans shifted activity to nighttime. These historically derived niche differences are apparent in extant lizard assemblages and account for some observed structure. These patterns occur in a variety of habitats at both regional and local levels throughout the world.

Of tongues and noses: chemoreception in lizards and snakes

Lizards and snakes inhabit a world so richly textured in chemical information that, as primates, we can only imagine it. Subtle nuances of chemical shading underline nearly every fundamental activity of their lives, from finding foot to finding mates. Recent work examines the nature of these chemical messages, mechanisms for their perception, the interplay of the chemical senses in the sociobiology of the group, and patterns of chemosensory evolution. Emerging is a new sense of lizard and snake behavioral complexity that belies the common notion of these animals as simple automata and points to a surprising capacity for plasticity and learning.

Evolutionarily Stable Configurations: Functional Integration and the Evolution of Phenotypic Stability

Phenotypic evolution has been studied since Darwin established the fact of evolution. In contrast, molecular evolution has been a subject of study since the mid-1960s. Nevertheless, our understanding of the mechanisms of phenotypic evolution is far less developed than our knowledge of molecular evolution. This fact is often attributed to the greater “complexity” of phenotypic characters, although it is not always clear what complexity means. More specifically, there are two features of phenotypic evolution that make molecular and phenotypic evolution quite distinct problems. First, molecular evolution is a continuing process, often occurring over long periods of time at a nearly constant rate, even if there are variations in rate among lineages. In contrast, phenotypic evolution is perceived as a highly irregular process with long periods of stasis interrupted by short bursts of change (Gould and Eldredge, 1977; Kimura, 1983). Second, most phenotypic characters comprise many levels of organization from the molecular to the behavioral and the population level, and the rate of change is nonuniform across these levels of organization. Some attributes of the phenotype, such as color and size, vary widely and evolve rapidly whereas other aspects of the phenotype, such as mode of food acquisition, are remarkably stable. Furthermore, even the conservative elements of the phenotype are not immutable because they have evolved in ancestral lineages and may become variable in a descendant lineage. Molecular evolution, on the other hand, pertains to evolutionary change on only one level of organization.

Occurrence, Distribution and Functional Significance of Taste Buds in Lizards

The tongue and oral epithelium beneath and lateral to the tongue have been examined in 37 species of lizard representing all families except the Helodermatidae and Lanthonotidae. Taste buds occur in all species examined except Varanus indicus (Varanidae). They are found on the tongues of all remaining species except Gonatodes antillensis (Gekkonidae) and in the oral epithelia of all species except Chamaeleo jacksoni (Chamaeleonidae). Taste buds may be abundant, particularly in the Iguanidae, in which densities greater than 104/mm2 occur. These observations are contrary to statements in the literature which have assumed taste buds to be rare or absent in lizards.

Why Snakes Have Forked Tongues

The serpents forked tongue has intrigued humankind for millennia, but its function has remained obscure. Theory, anatomy, neural circuitry, function, and behavior now support a hypothesis of the forked tongue as a chemosensory edge detector used to follow pheromone trails of prey and conspecifics. The ability to sample simultaneously two points along a chemical gradient provides the basis for instantaneous assessment of trail location. Forked tongues have evolved at least twice, possibly four times, among squamate reptiles, and at higher taxonomic levels, forked tongues are always associated with a wide searching mode of foraging. The evolutionary success of advanced snakes might be due, in part, to perfection of this mechanism and its role in reproduction.

Function and the Evolution of Phenotypic Stability: Connecting Pattern to Process

SYNOPSIS. Phenotypes manifest a balance between the inherited tendency to remain the same (phenotypic stability) and the tendency to change in response to current environmental conditions (adaptation). This paper explores the role of functional integration and functional trade-offs in generating phenotypic stability by limiting the responses of individual characters to environmental selection. Evolutionarily stable configurations (ESCs) are systems of functionally interacting characters within which characters are ‘‘judged’’ by their contribution to systemlevel functionality. This ‘‘internal’’ component of selection differs from traditional ‘‘external’’ selection in that it travels with the organism wherever it goes and is maintained across a wide range of environments. External selection, in contrast, is by definition environment-dependent. The temporal and geographic constancy of internal selection therefore acts to maintain phenotypic stability even as environments change. Functional trade-offs occur when one character participates in more than one function, but can only be optimized for one. Participation of certain (‘‘keystone’’) characters in a trade-off potentially causes stabilization of an entire system owing to a cascade of functional dependencies on that character. Phylogenetic character analysis is an essential part of elucidating these processes, but patterns cannot be used as prima facie evidence of particular processes.

CHAPTER 2 – An Introduction to Tetrapod Feeding

This chapter highlights the diversity of the tetrapod feeding apparatus that is remarkable for its exploitation of a common set of parts. Perhaps the most important underlying theme to tetrapod feeding is the evolution of the tongue and its integration with the hyobranchial apparatus in feeding function. Modification and adaptation of the hyolingual apparatus are prominent features of tetrapod feeding evolution. It should be expected that the kind of phenotypic remodeling necessary to create a novel feeding system is to be a relatively rare evolutionary event associated phylogenetically with the origin of new clades and adaptive radiations. From this, it can be predicted that local adaptation to transient ecological conditions is not a general feature of tetrapod feeding evolution. Rather, feeding systems seem to reflect more fundamental aspects of phenotypic organization and adaptation. It is a challenge, therefore, to discern commonalities among the related but divergent types of feeding systems among tetrapods. Individual taxon-specific chapters address the issues of feeding system form, function, and evolution on a finer and more tractable scale.

A cryptic intermediate in the evolution of chameleon tongue projection

An incipient form of tongue projection occurs inPhrynocephalus helioscopus, a generalized agamid lizard. We argue that this condition represents a functional intermediate between typical lingual prehension and chamaeleontid tongue projection, and that tongue projection evolved in chameleons by augmentation of ancestral mechanisms still operating in related, generalized lizards.

The Mechanism of Chemical Delivery to the Vomeronasal Organs in Squamate Reptiles: A Comparative Morphological Approach

Vomeronasal chemoreception, an important chemical sense in squamate reptiles (lizards and snakes), is mediated by paired vomeronasal organs (VNOs), which are only accessible via ducts opening through the palate anteriorly. We comparatively examined the morphology of the oral cavity in lizards with unforked tongues to elucidate the mechanism of stage I delivery (transport of chemical-laden fluid from the tongue tips to the VNO fenestrae) and to test the generality of the Gillingham and Clark (1981. Can J Zool 59:1651-1657) hypothesis (based on derived snakes), which suggests that the sublingual plicae act as the direct conveyors of chemicals to the VNOs. At rest, the foretongue lies within a chamber formed by the sublingual plicae ventrally and the palate dorsally, with little or no space around the anterior foretongue when the mouth is closed. There is a remarkable conformity between the shape of this chamber and the shape of the foretongue. We propose a hydraulic mechanism for stage I chemical transport in squamates: during mouth closure, the compliant tongue is compressed within this cavity and the floor of the mouth is elevated, expressing fluid from the sublingual glands within the plicae. Chemical-laden fluid covering the tongue tips is forced dorsally and posteriorly toward the VNO fenestrae. In effect, the tongue acts as a piston, pressurizing the fluid surrounding the foretongue so that chemical transport to the VNO ducts is effected almost instantaneously. Our findings falsify the Gillingham and Clark (1981. Can J Zool 59:1651-1657) hypothesis for lizards lacking forked, retractile tongues.

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.