Recurrent evolution of herbivory in small, cold-climate lizards: Breaking the ecophysiological rules of reptilian herbivory

Abstract

Herbivory has evolved in many groups of vertebrates, but it is rare among both extinct and extant nonavian reptiles. Among squamate reptiles, (lizards, snakes, and their relatives), <2% of the >7,800 species are considered to be herbivorous, and herbivory is restricted to lizards. Here, we show that within a group of South American lizards (Liolaemidae, Ϸ170 species), herbivory has evolved more frequently than in all other squamates combined and at a rate estimated to be >65 times faster. Furthermore, in contrast to other herbivorous lizards and to existing theory, most herbivorous liolaemids are small bodied and live in cool climates. Herbivory is generally thought to evolve only in reptile species that are large bodied, live in warm climates, and maintain high body temperatures. These three well known ''rules'' of herbivory are considered to form the bases of physiological constraints that explain the paucity of herbivorous reptile species. We suggest that the recurrent and paradoxical evolution of herbivory in liolaemids is explained by a combination of environmental conditions (promoting independent origins of herbivory in isolated cool-climate regions), ecophysiological constraints (requiring small body size in cool climates, yet high body temperatures for herbivores), and phylogenetic history. More generally, our study demonstrates how integrating information from ecophysiology and phylogeny can help to explain macroevolutionary trends.ecophysiology ͉ macroevolution

Diversity of gut methanogens in herbivorous animals

“…Although 80% of mammalian species are herbivorous (Stevens and Hume, 1995), it is estimated that only 2% of squamate reptiles (snakes and lizards) are herbivores (Espinoza et al, 2004). The existence of active methanogens in the gut of herbivorous lizards has been detected by methane production from fecal material of captive iguanas (Hackstein and Van Alen, 1996).…”

Diet of the lizard Liolaemus occipitalis in the coastal sand dunes of southern Brazil (Squamata-Liolaemidae)

“…Omnivorous Liolaemus species increase their intake of plant material in the adult stage. Several smaller species than those considered by Pough (1973) show an evident tendency to herbivory (Jaksic, 1978;Greene, 1982;Rocha, 1992;Van Sluys, 1993;Espinoza et al, 2004). The genus Liolaemus also shows the same tendency, including L. pictus pictus (DUMÉRIL and BIBRON, 1837) (Ortiz, 1974), L. nigromaculatus kulhmani MÜLLER andHELLMICH, 1933 (Jaksic, 1978) and L. lutzae (Rocha, 1989;1992).…”

“…225 species according to Ávila et al, 2010). Lizards of this genus exhibit ecological variability that is independent of their phylogenetic relationships, which makes these lizards excellent models for vertebrate ecological studies (Espinoza et al, 2004;Tulli et al, 2011). Several studies on the diet of this genus have been published (Ortiz and Riveros, 1976;Fuentes and Ipinza, 1979;Jaksic and Fuentes, 1980;Rocha, 1989;Ávila and Acosta, 1993;Vega, 1999;Belver and Avila, 2001;Halloy et al, 2006;Azócar and Acosta, 2011).…”

“…are excellent representatives of the pattern observed in species of the Iguana group within the foraging models of lizards (Huey and Pianka, 1981). The genus Liolaemus encompasses insectivorous, omnivorous and herbivorous species (Etheridge and Espinoza, 2000;Espinoza et al, 2004). Carnivorous and omnivorous Liolaemus lizards are ambush foragers and present features of the sit-and-wait model for Squamata, such as the prevalence of mobile prey and relatively diverse diets.…”

Ecología trófica, dimorfismo sexual y parámetros reproductivos en el lagarto endémico Andino Liolaemus vallecurensis, Argentina

“…Si el porcentaje de IRI de la categoría queda entre el 100 % y el 75 % se la considerará fundamental, entre el 75% y el 50% secundaria, entre el 50% y el 25% accesoria y si se encuentra en menos del 25% accidental (Aun & Martori, 1998). Se analizó el material vegetal de los estómagos (tallos, hojas, flores, frutos y semillas) siguiendo a Espinoza et al (2004) modificado de acuerdo a Astudillo et al (2015) y Córdoba et al (2015) (0-10% insectívoro, 11-50% omnívoro; 51-100% herbívoro). A cada uno de esos valores porcentuales de materia vegetal se les fue transformado en categorías ordinales de acuerdo Castro et al (2013) y estas categorías fueron analizadas con la prueba no paramétrica de Kruskal-Wallis.…”