Introduction
Totally herbivorous lizards are found in three disjunct regions: (1) the New World tropics northward into the Mojave Desert of the SW United States (all the Inguaninae but two species), (2) the Near the Middle East from North Africa to Southwest Asia (spiny tailed agamids Uromastyx); and (3) the tropical Far East in the Fiji Islands (the banded iguanas Brachylophus), the Philippines and Indonesia (water lizards Hydrosaurus) and the Solomon Islands (giant skinks Corusia). They are found on islands as well as continents, in predator-filled to nearly predator-free environments, in xeric (most), mesic, and hydric habitats, and they include both oviparous and viviparous (only Corusia) forms.
Perhaps the most unique characteristic of the lizards of the sub-family Iguaninae is their success at herbivorousness. Unfortunately, complete, reliable data on diet and feeding habits for most of the iguanines are not available; most of the published information is only anecdotal, and, in some cases (see below), clearly misleading. Intrigued by my own observations that the ground iguana, Cyclura carinata, is almost totally herbivorous from hatching through adulthood (a weight range of 15 to 1900 g), I began examining lizard herbivory in terms of diet, feeding habits, feeding strategies, and adaptational correlates (both morphological and physiological). By looking simultaneously at all of these aspects of herbivory, I hoped to better understand the mechanisms involved in its evolution in lizards.
Diet
For purposes of this discussion I consider as "truly herbivorous" (i.e., on the far right of the [carnivory-omnivory-herbivory] continuum) only those species whose diets include essentially only vegetation (whether fruit, flowers, seeds or foliage) throughout the year.
Many species generally called "herbivorous" are probably facultative herbivores at best, and more likely, simple omnivores. Based on the literature and my own dissections of several hundred lizard species, [most] such forms [species names omitted] although often termed herbivorous in the literature are clearly not true herbivores. In fact, by my definition, the only totally herbivorous extant lizards are the iguanines (+/- 30 species among the Iguanidae), the genera Uromastyx, Hydrosaurus among the Agamidae, and Corucia zebrata in the Scincidae.
I have also found no basis for earlier speculations that the iguanines Amblyrhynchus cristatus, Cyclura nubila, Iguana, and Dipsosaurus dorsalis, and the agamid Uromastyx hardwicki exhibit an ontogenetic shift from carnivory to herbivory [eating animal protein as juveniles, adopting an herbivorous diet as adult]. Most of these suggestions were based: (1) on diet information from captive lizards, or (2) on anecdotal field observations. In fact, of all the true herbivores I have dissected, only the iguanine Ctenosaura similis showed any indication of an omnivorous juvenile diet. Further field study will be necessary to establish quantitatively the extent of this omnivory by size and season (for C. similis). I thus conclude that an ontogenic shift from carnivory to herbivory is not usual in lizards truly herbivorous as adults, and further, that the documentation of such a transition (as appears to be the case for C. similis) will at best be the very rare exception rather than the rule.
Feeding Ecology
Other than Auffenberg's work, studies of the ecological aspects of feeding in herbivorous lizards have received little attention. However, it is known that herbivorous lizards spend the majority of their activity cycle resting, not feeding or foraging as do most carnivorous lizards or mammalian herbivores. Moberly estimated that Iguana spends 90% of its time resting, and Beverly Dugan estimated that the same species spent 96% of the day inactive and only 1% feeding.
Despite the apparent abundance of plant food, availability of food resources may be the primary limiting factor for populations of many iguanine lizards species. For example, in Columbia, Mueller has shown that green iguanas inhabiting strongly seasonal habitats are smaller than those in less seasonal habitats.
Rand has suggested that food may be limiting to Iguana iguana in highly seasonal tropical habitats only during part of the year. Further, even during times of maximum primary productivity, i.e., times when high quality foods (e.g., fruits) are most abundant, lizards can only eat and assimilate as much as their digestive machinery can process. Because of the low relative metabolic rats and daily fluctuations in body temperatures, this machinery may well limit energy intake even at maximum efficiency.
Digestive Physiology
Other physiological aspects of lizard herbivory have received some attention. For example, digestive efficiencies of carnivorous lizards are known to vary typically from 70 to 90% and to exceed significantly those of herbivorous lizards, which normally range from 30-70%.
Trophic Adaptations
All true herbivorous lizards, regardless of family, are specialized in that they all share one significant morphological adaptation (and a suite of associated physiological and ecological ones) found in no other living lizards: all have a distinctly enlarged, partitioned colon. All iguanine lizards except Amblyrhynchus cristatus [whose valves differ from the others only in height of the folds with no true valves] possess from one to eleven transverse valves in the proximal colon. Valves are of two kinds, circular or semilunar, and circular valves (if present) always occur proximally to semilunar valves. There is no ontogenetic change in the number or the kind of valves.
Colons of unknown species can nearly always be allocated at least to genus, based solely on morphology of that organ.
Perhaps the most intriguing thing about iguanine colic variation is the significant linear relationship between number of valves and mean body size for interspecific comparisons. The larger the species, the more complex is the colon (i.e., the more colic compartments present).
The partitioned colon surely slows the passage of digesta through the gut, and relative absorptive surface area (for water and nutrients) is certainly increased. But the presence of tremendously dense nematode faunas (and presumably bacterial and protozoan populations) in the normal cecum of all these herbivorous lizards suggest that they provide important microhabitats for colic (cellulytic?) symbionts. These nematodes (families Atracidae and Oxyuridae) have direct life cycle, and eggs are likely ingested during substrate licking, geophagy or coprophagy--behaviors frequently observed in these lizards. Significantly, these heavy worm burdens are typical of herbivorous lizards, where as such burdens are not found in omnivorous or carnivorous lizards.
The tremendous nematode densities in healthy lizards suggest they are not parasitic, but rather commensalistic, or perhaps even mutualistic. Potential roles for these nematodes include (1) the simple mixing and mechanical breakdown of vegetation, effectively increasing the surface area of digesta particles; (2) the production of useable waste products (vitamins, cellulose, volatile fatty acids?); and/or (3) the regulation of the composition and/or abundance of colonic microbes (on which some nematodes are known to feed).
Gastrointestinal tract modification for symbiont culture is also the norm in herbivorous organisms that have previously been studied. Colonic partitioning in herbivorous lizards is thus by no means novel. What is surprising is the lack of attention it has received especially since it appears to be the one adaptation essential for a lizard's completely herbivorous existence.
Body Size
True herbivorous lizards share another obvious character. Excluding the varanids (which are very specialized carnivores), they are the largest extant lizards. [Hypotheses which explain the adaptive significance of body size and herbivory include] the greater mechanical strength [needed] for reducing vegetation for consumption (although there is no mastication); the advantage of reduced predation and competition; the advantage of eating easily obtainable foods of medium to poor quality (i.e., plants) rather than high quality food items (i.e., insects) more energentically costly to obtain (since metabolic rates are relatively lower in large lizards); and the advantage of greater thermal inertia, allowing the maintenance of elevated body temperatures and facilitating the digestion of vegetation. Each of these theories relates selective advantages which no doubt accrue to large, herbivorous lizards, but none appears to fully explain the body size-herbivory relationship in these lizards. I here extend another hypothesis which I think more adequately explains the body size-herbivory correlation and permits speculation on the evolution of these characteristics in lizards. I believe that the anatomical, physiological, and ecological characteristics of the gastrointestinal tract are the most important determinants, not only of herbivorous capabilities, but also of body size in these lizards.
Previous studies on both lizards and turtles have shown that body size may be significantly related to resource availability. Analogously, I believe that the evolutionary increase in colon complexity has increased resource usability (not necessarily availability!), and thereby energetically permitted increased body size. Thus colon modification (and the diversification and increase in the intestinal flora and fauna), these herbivores have been able to grow to larger sizes, and thus more fully gain other selective advantages, such as reduced predation, metabolic and thermoregulatory benefits.
Discussion
I believe that the iguanines, Uromastyx, Hydrosaurus and Corucia are much more specialized that generally realized. Each has a relatively large body size and a modified colon with large nematode and microbe populations--a combination of characters unique among the lizards. In addition, although I have not mentioned them, these lizards all possess dentition modified for herbivory and (apparently) nasal salt glands for extrarenal salt secretion.
These last two characteristics are shared by lizards which are not entirely herbivorous, however they nevertheless facilitate an herbivorous existence: teeth for efficient cropping and salt glands for dealing with the increased potassium load.
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