Aquatic feeding in a terrestrial turtle: a functional-morphological study of the feeding apparatus in the Indochinese box turtle Cuora galbinifrons (Testudines, Geoemydidae)

Abstract

The Indochinese box turtle Cuora galbinifrons is regarded as a purely terrestrial species, but our results demonstrate that it can feed both on land and in water. The inverse relationship between the relative development of the hyoid apparatus and the tongue found in the most investigated chelonians is not valid in the Indochinese box turtle. Our morphological analysis of the feeding apparatus reveals that the palate shape and the design of the tongue are consistent with terrestrial feeders, but the construction of the hyoid complex is more characteristic of aquatic feeders. Previous studies have demonstrated that tongue enlargement negatively impacts the capacity of the turtles to suction feed. The present study focuses on the aquatic intraoral prey transport kinematic patterns. Our analysis is based on high-speed Wlms with 250 fr/s and high-speed cineradiography with 50 fr/s. The aquatic intraoral food transport mechanisms diVer depending on prey size: small items are transported predominantly by "inertial suction", whereas larger items are moved by the tongue-normally a clear terrestrial strategy. As the genus Cuora is ancestrally aquatic, the use of lingual food transport in the aquatic environment is presumably an aberrant modus typical only for the most terrestrial among the Asian box turtles.

Avaliação da cavidade orofaríngea da tartaruga da Amazônia, Podocnemis expansa (Schweigger, 1812)

“…Observa-se uma grande semelhança entre a língua de Podocnemis expansa com as espécies Manouria emys emys, Cuora galbinifrons e Mesoclemmys vanderhaegei, pois todas são alongadas, bem desenvolvidas, com seu ápice em formato rombo (triangular) e caudalmente encontra-se o frê-nulo proeminente, que permite uma grande aderência ao assoalho (Natchev et al 2010, Pinheiro et al 2010 acrescenta ainda que a retração do alimento pela língua começa a partir do momento que o alimento é liberado da ranfoteca durante a abertura da mandíbula, porém, antes de que o alimento flutue da cavidade oral. As características do epitélio da língua descritas por nós se assemelham às descritas por Aughey & Frye (2001), Heiss (2010) e Samuelson (2007.…”

Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue

“…The system as a whole, however, may be less adapted for terrestrial feeding in semiaquatic forms. Such amphibious turtles are able to feed underwater, an ability lost in all testudinids (Bels et al,2008; Natchev et al,2010). Fully aquatic turtles (at least those few studied so far) seem to show all major lingual muscle components as well (for an overview see Werneburg,2010), but the usually very small and weak tongues in these forms seem to play a subordinate role in their feeding mechanism, and tongue movements may therefore be limited (see Bramble and Wake,1985; Iwasaki et al,1996b; Lemell et al,2000, Beisser et al,2001; Heiss et al,2010).…”

Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newtIchthyosaura alpestris(Salamandridae)

“…In fact, only a few species have evolved mechanisms that allow them to exploit food sources in both environments. Such amphibious feeders are mainly known within lower tetrapods, especially within salamanders and turtles (Reilly and Lauder, 1989;Miller and Larsen, 1989;Miller and Larsen, 1990;Summers et al, 1998;Deban and Wake, 2000;Deban, 2003;Heiss et al, 2008;Natchev et al, 2009;Natchev et al, 2010;Stayton, 2011). Recent studies have shown that the capability to feed in both media is mainly due to behavioral plasticity, where modulatory behavior compensates for morphological constraints (Stayton, 2011).…”