RESEARCH ARTICLE The effect of food properties on grasping and manipulation in the aquatic frog Xenopus laevis Aude Anzeraey, Madeleine Aumont, Thierry Decamps, Anthony Herrel* and Emmanuelle Pouydebat* , ‡ ABSTRACT The ability to grasp an object is fundamental from an evolutionary perspective. Involved in many daily activities, grasping has been extensively studied in primates and other mammals. Yet other groups of tetrapods, including anurans, have also evolved significant forelimb prehensile capacities that are often thought to have originated in an arboreal context. In addition, grasping is also observed in aquatic species. But how aquatic frogs use their forelimbs to capture and manipulate prey remains largely unknown. The aim of this study is to explore how the grasping and manipulation of food items in aquatic frogs is impacted by food properties such as size and mobility. To do so, we uses the aquatic frog Xenopus laevis and quantified the use of the hands and fingers while processing mobile and stationary prey of different sizes (small, intermediate and large). Our results show that X. laevis is able to individualize the digits and that the mobility and the length of the prey significantly influence the kind of grasping pattern used. Grasping abilities are thus not specific to terrestrial or arboreal species. These results illustrate how prey properties impact grasping and manipulation strategies in an aquatic frog and shed further light on the ecological contexts that may have given rise to the origin of grasping in frogs. KEY WORDS: Prehension, Manipulation, Prey properties, Anurans, Digits, Dexterity, Hand INTRODUCTION The ability to grasp an object with an appendage is fundamental from an evolutionary perspective (Sustaita et al., 2013). It can be accomplished by the hand, foot, tail, trunk, tongue, teeth or other parts of the body (Mackenzie and Iberall, 1994). Involved in many daily activities, hand grasping has been extensively studied in primates, which are characterized by the ability to individualize their fingers and thus able to perform complex grasping and manipulation tasks (e.g. Christel, 1993; Jones-Engel and Bard, 1996; Christel et al., 1998; Christel and Billard, 2002; Crast et al., 2009; Pouydebat et al., 2008, 2009, 2011; Peckre et al., 2016). Anurans have also evolved significant prehensile abilities that in some cases involve individualization of the fingers (e.g. Manzano et al., 2008; Abdala and Diogo, 2010). Whereas frogs typically transfer small prey to the esophagus with the tongue or jaws, the hands play an important role in the manipulation of larger prey (Anderson and Nishikawa, 1996; Valdez and Nishikawa, 1997). However, in contrast to studies on the role of the tongue and jaws during prey capture (Nishikawa, 1999, 2000; Monroy and Nishikawa, 2011), studies on the use of the forelimbs during feeding are rather scarce (Gray et al., 1997). Previous studies on anurans have identified five distinct behavioral patterns that involve the use of the forelimbs: (1) scooping, involving the use of the back of the hand to push prey into the mouth as observed for Xenopus laevis Daudin 1802 and Rana pipiens (Avila and Frye, 1977, 1978; Comer and Grobstein, 1981; Gray et al., 1997); (2) wiping, involving the use of the palm of the hand to push prey protruding laterally from the mouth as observed in X. laevis, R. pipiens and Hymenochirus boettgeri (Sokol, 1969; Avila and Frye, 1978; Comer and Grobstein, 1981; Gray et al., 1997); (3) prey stretching, involving the grasping of one end of the prey by the hands while the other end is pulled upward by the jaws (Gray et al., 1997); (4) grasping, involving the wrapping of the fingers around the prey (Gray et al., 1997); and (5) finally, hand grasping was observed for several species, involving grasping motions by the hands instead of the tongue to capture and transport prey from the external environment into the mouth (Gray et al., 1997). The goal of the present study is to quantify the use of the hands during prey grasping and manipulation in the aquatic frog X. laevis. Moreover, we test whether and how food properties modify the use of the hands. As has been described for primates (Pouydebat et al., 2009, 2014; Toussaint et al., 2013, 2015), the mobility and the size of a prey item may affect the grasping and manipulation strategies used (e.g. the use of two hands versus one hand, and which fingers are involved in grasping). Specifically, we predict that larger prey will involve an increased used of the hands during grasping as observed in many other taxa (Sustaita et al., 2013). We also predict that mobile prey will induce the use of the hands more as observed in mouse lemurs, for example (Toussaint et al., 2013). Finally, we also explore whether this species is able to individualize the fingers as observed in some marsupials, carnivores and primates (Sustaita et al., 2013). MATERIALS AND METHODS Animals Xenopus laevis were housed at the laboratory [UMR 7179, Muséum National d’Histoire Naturelle (MNHN), Paris, France] in groups of three to eight individuals in aquaria (60×30×30 cm) with the temperature set at 23°C, which is close to the preferred and optimal temperature of Xenopus frogs (Casterlin and Reynolds, 1980; Miller, 1982). Frogs were fed every other day with beef heart, earthworms or mosquito larvae ad libitum. All individuals were pit- tagged (NONATEC, Rodange, Luxembourg) before the onset of the experiments, allowing unambiguous identification of each individual. A total of 10 individuals (five males: snout–vent length 70.3±3.5 mm, hand+finger length: 16.1±1.7 mm; five females: snout–vent length 83.9±9.3 mm, hand+finger length: 17.1± 2.1 mm) were included in the present study. All experiments were Received 14 March 2017; Accepted 3 October 2017 UMR 7179 CNRS/MNHN, Dé partement Adaptations du Vivant, 75005, Paris Cedex 5, France. *These authors contributed equally to this work ‡ Author for correspondence (emmanuelle.pouydebat@mnhn.fr) E.P., 0000-0002-0542-975X 4486 © 2017. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2017) 220, 4486-4491 doi:10.1242/jeb.159442 Journal of Experimental Biology