COMMENTARY

Shifting paradigms: Herbivory and body size in lizards

Laurie J. Vitt* Sam Noble Oklahoma Museum of Natural History and Zoology Department, University of Oklahoma, Norman, OK 73072

any lizards frequently eat fruits and flowers, but few are strictly herbivorous (1, 2). For Ͼ30 years, biolo- gistsM have perpetuated the notion that herbivory in lizards required large body size, based largely on a set of physiologi- cal arguments centered on thermal re- quirements for digestion of plants and the observation that the few studied herbivorous lizards were relatively large in body size (3). From the outset, the argument was fundamentally flawed, because most known large-bodied her- bivorous lizards are members of a strictly herbivorous clade, the Iguanidae. Consequently, a single origin of her- bivory from a large-bodied ancestor accounts for much of the association between herbivory and large size in liz- ards. Within other lizard clades, herbivo- rous species are not among the largest (e.g., Teiidae, Cnemidophorus murinus, Cnemidophorus arubensis, and Dicrodon guttulatum; and Varanidae, Varanus oli- vaceus). Even when the few noniguanian origins of herbivory are added, the num- ber of origins pales in comparison with those identified in this issue of PNAS by Espinoza et al. (4) in a single iguanian Fig. 1. Evolution of prey detection, prey prehension, and herbivory in squamate reptiles. Numbers of clade, the Liolaemidae. More impor- origins for herbivory are taken from Espinoza et al. [ref. 4; at least two more are known in Autarchoglossa; tantly, the multiple origins identified by one in the family Teiidae (Dicrodon) and at least one in Varanidae (V. olivaceus)]. Nevertheless, the Espinoza et al. derive from small-bodied number of origins (at least 18) in the Liolaemidae (a subclade of the Iguania) far exceeds those in all other ancestors in relatively cool environ- lizards combined. The traditional phylogeny is shown (2, 5, 6). ments, running counter to the notion that herbivory in ectotherms requires large body size and warm environments. diverged, with one clade, Gekkota, using orthopterans, spiders, and insect larvae Why is this such an important finding, the tongue to clean its facial scales and, (6). Increases in activity levels and, in and how does it change the way we in some cases, the spectacle over the some autarcholglossans, activity at ele- think about the evolution of feeding and eye. These lizards developed an olfac- vated body temperatures were associated diets in lizards? tory chemical discrimination system (8– with changes in foraging and possibly 10). Members of the other clade, Autar- the kinds of prey eaten (11). Several Squamate Feeding Strategies choglossa, used the tongue to carry autarchoglossan clades specialized on chemical cues from the environment to vertebrates, termites, snails, and other To fully appreciate the significance of prey not frequently eaten by iguanians. this finding, it is necessary to recount their highly developed vomeronasal or- gans (5, 8). For ancestral iguanians, prey New opportunities opened up, and a the evolution of feeding strategies in remarkable diversification followed. The that moved were the primary targets. squamate reptiles (Fig. 1). Squamate evolution of several limbless lizard For ancestral gekkotans and autar- ancestors used visual cues to detect and clades, including one frequently referred discriminate prey, the tongue to capture choglossans, moving prey were detected to as ‘‘snakes’’ (12), is but one of many and manipulate prey (lingual prehen- visually, but nonmoving and hidden prey examples. Success of this diversification sion), and an ambush foraging mode (2, were detected chemically. Moreover, becomes obvious when comparing num- 5–7). During late Triassic or early Juras- chemosensory systems allowed members bers of species in each major clade. sic, the most important divergence in of these clades to discriminate prey Iguania contains Ϸ1,230, Gekkota con- the history of squamates produced one based on quality and production of de- tains Ϸ975, and Autarchoglossa con- clade, Iguania, which retained ancestral fensive chemicals (6). Comparisons be- tains Ϸ5,000 species. Snakes comprise traits, and another, Scleroglossa, which, tween these clades clearly reveal a major Ϸ2,900 of autarchoglossans, none of rather than using the tongue for prey dietary shift deep in squamate history. which is herbivorous. capture, used the jaws (jaw prehension). Although most carnivorous and omnivo- The scleroglossan skull was much more rous lizards eat a diversity of prey (1), kinetic, facilitating prey capture, and the iguanians (excluding herbivores) primar- See companion article on page 16819. tongue was freed from involvement in ily eat ants, other hymenopterans, and *E-mail: [email protected]. prey prehension (5). Scleroglossa soon beetles, whereas scleroglossans eat more © 2004 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0407439101 PNAS ͉ November 30, 2004 ͉ vol. 101 ͉ no. 48 ͉ 16713–16714 Downloaded by guest on September 23, 2021 Traits related to feeding in iguanian pothesis explaining the high diversity and possibly releasing them from competi- ancestors (visual prey detection, lingual frequent evolution of herbivory. tion and predation by autarchoglossans. prehension, and ambush foraging) render Even though herbivorous liolaemids may it even more remarkable that herbivory Many Paths to Herbivory have slightly higher body temperatures evolved repeatedly in the Liolaemidae. A recent study posits that diversification than their carnivorous or omnivorous relatives (4), high body temperature Most prior known origins of herbivory and the ability of autarchoglossans to alone may not be sufficient for digestion occurred in the Autarchoglossa, in which harvest prey unavailable to iguanians provided them with a competitive ad- of plant materials. Increased activity typical behavior includes moving about in periods may be necessary as well. The search of prey, discriminating prey chemi- vantage and enabled them to dominate terrestrial environments throughout the herbivorous teiid lizard C. murinus (an cally, and grasping prey with the jaws. The autarchoglossan) maintains body tem- world (6). Iguanians tend to use ele- shift from digesting arthropods, verte- peratures similar to other teiid lizards vated perches, and many species are brates, and other animals to digesting but remains active much longer to facili- arboreal in environments containing plants is not a small one but should have tate digestion of plants (19). Risk associ- autarchoglossans. Gekkotans, for the ated with extended activity is reduced been more easily attained in lizard clades most part, are nocturnal, thus avoiding living primarily in tropical and desert hab- because the island on which it lives (Bo- itats, where thermal conditions facilitating naire) contains few predators. The high elevation and high latitude habitat of gut fermentation abound. Autarchoglos- High body temperature most liolaemids may have provided an san diversity is greatest in such regions environment with few competitors and (2, 6). Nevertheless, it now appears that may not be sufficient predators (in particular, a lack of autar- origins of herbivory are much more fre- choglossans) throughout much of their quent in an iguanian clade than among for digestion of plants; evolutionary history; thus, diversification autarchoglossans. into terrestrial microhabitats and ex- Within Iguania, two subclades diversi- increased activity tended activity times with reduced risk fied more than all others: Polychrotidae may have set the stage for repeated evo- (mostly the genus Anolis) and Liolaemi- periods may be lution of herbivory. The ability of small dae. Anolis have proven to be excellent liolaemid lizards to heat rapidly if com- bined with extended activity may be models for evolutionary studies, partially necessary as well. sufficient to select for herbivory, partic- because ecomorphs have evolved indepen- ularly in environments in which arthro- dently on different Caribbean islands. interactions with autarchoglossans as pod food resources are limited. Some Studies of these lizards have revealed that iguanians developed the ability to dis- morphology responds to changes in micro- well as iguanians. Autarchoglossans reach their greatest diversity in warm criminate plant chemicals by using habitat use (13, 14). Liolaemid lizards vomerofaction, even though insectivo- environments (tropical rainforests, tropi- have been long overlooked as models for rous iguanians have not (20). High fre- cal savannas, deserts), likely because quency of evolutionary events leading to ecological and evolutionary studies, even they can attain body temperatures nec- though they diversified at high elevations herbivory, coupled with a background of essary to support their relatively high ecological diversity among liolaemid liz- in southern South America, producing activity levels. Their diversity drops off species that occupy nearly every imagin- ards, makes them ideal models for evo- rapidly with increased elevation and lati- lutionary, ecological, physiological, and able terrestrial microhabitat (15–18). The tude. Although portions of the history behavioral studies aimed at understand- high diversity of liolaemids in southern of iguanians and autarchoglossans may ing adaptive radiation. Thus, in a more South America (168 species, with 157 in have been independent, much of it was general context, the discovery of multi- the genus Liolaemus) suggests an evolu- not (2, 6). However, liolaemids diversi- ple origins of herbivory in liolaemids is tionary history quite different from that of fied at high elevations at high latitudes, a starting point for what promises to be other iguanians, and herein may lie a hy- largely in the absence of autarchoglossans, exciting new directions in lizard ecology.

1. Cooper, W. E., Jr., & Vitt, L. J. (2002) J. Zool. 257, 7. Cooper, W. E., Jr. (1997) Behav. Ecol. Sociobiol. 15. Cei, J. M., ed. (1986) Mus. Reg. Sci. Nat. Torino 487–517. 41, 257–265. Monogr. 4. 2. Pianka, E. R. & Vitt, L. J. (2003) Lizards: Windows 8. Cooper, W. E., Jr. (1995) Anim. Behav. 50, 973–985. 16. Cei, J. M., ed. (1993) Mus. Reg. Sci. Nat. Torino to the Evolution of Diversity (Univ. of California 9. Schwenk, K. (1993) J. Zool. 229, 289–302. Monogr. 14. Press, Berkeley). 10. Schwenk, K. (1993) Brain Behav. Evol. 41, 124–137. 17. Fuentes, E. R. (1976) Ecology 57, 3–17. 3. Pough, F. H. (1973) Ecology 54, 837–844. 11. Huey, R. B. & Pianka, E. R. (1981) Ecology 62, 991–999. 18. Fuentes, E. R. & Jaksı´c, J. M. (1980) Oecologia 46, 4. Espinoza, R. E., Wiens, J. J. & Tracy, C. R. (2004) 12. Greene, H. W. (1997) Snakes: The Evolution of 45–48. Proc. Natl. Acad. Sci. USA 101, 16819–16824. Mystery in Nature (Univ. of California Press, 19. Vitt, L. J., Caldwell, J. P., Sartorius, S. S., Cooper, 5. Schwenk, K. (2000) in Feeding, ed. Schwenk, K. Berkeley). W. E., Jr., Baird, T. A., Baird, T. D. & Pere´z- (Academic, San Diego), pp. 175–291. 13. Losos, J. B. (1992) Syst. Biol. 41, 403–420. Mellado, V. (2004) Funct. Ecol., in press. 6. Vitt, L. J., Pianka, E. R., Cooper, W. E., Jr., & 14. Losos, J. B., Warheit, K. I. & Schoener, T. W. 20. Cooper, W. E., Jr., & Alberts, A. C. (1991) Schwenk, K. (2003) Am. Nat. 162, 44–60. (1997) Nature 387, 70–73. J. Chem. Ecol. 17, 135–146.

16714 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0407439101 Vitt Downloaded by guest on September 23, 2021