Abstract

Transitions between aquatic and terrestrial habitats are significant steps in vertebrate evolution. Due to the different biophysical demands on the whole organism in water and air, such transitions require major changes of many physiological functions, including feeding. Accordingly, the capability to modulate the pre-programmed chain of prey-capture movements might be essential to maintain performance in a new environment. Newts are of special interest in this regard as they show a multiphasic lifestyle where adults change seasonally between an aquatic and a terrestrial stage. For instance, the Alpine newt is capable of using tongue prehension to feed on land only when in the terrestrial stage, but still manages to suction feed if immersed whilst in terrestrial stage. During the aquatic stage, terrestrial feeding always involved grasping prey by the jaws. Here, we show that this seasonal shift in feeding behavior is also present in a species with a shorter terrestrial stage, the smooth newt Lissotriton vulgaris. Behavioral variability increases when animals change from aquatic to terrestrial strikes in the aquatic stage, but prey-capture movements seem to be generally well-coordinated across the feeding modes. Only suction feeding in the terrestrial stage was seldom performed and appeared uncoordinated. Our results indicate that newts exhibit a high degree of seasonal flexibility of the prey-capture behavior. The similarity between movement patterns of suction feeding and terrestrial feeding suggests that only relatively subtle neuromotoric adjustments to the ancestral, suction-feeding motor program are required to successfully feed in the new environment.

Highlights

  • Transitions from an aquatic to a terrestrial lifestyle require changes in form and function of almost every organ system (Denny 1993; Vogel 1994; Carroll 2009; Stayton 2011; Clack 2012)

  • Regarding timings of gape and hyoid movements, we found significant correlations between the time to peak gape and the time to peak magnitude of hyoid depression in suction feeding in the aquatic stage (r25=0.78; P

  • We further tested for correlations between peak magnitudes of the above listed kinematic variables of gape and hyoid excursions and found significant correlations between magnitudes of maximum gape opening and maximum hyoid depression in suction feeding in the aquatic stage (r25=0.64; P=0.001), jaw prehension (r25=0.56; P=0.004), and tongue prehension (r25=0.76; P

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Summary

Introduction

Transitions from an aquatic to a terrestrial lifestyle require changes in form and function of almost every organ system (Denny 1993; Vogel 1994; Carroll 2009; Stayton 2011; Clack 2012). The ability to capture and transport food both in aquatic and terrestrial environments is most challenging for the organism as the mechanical demands on the whole feeding biology are different (Deban 2003). Most aquatic predators use a prey-capture mechanism referred to as suction feeding where a fast oropharyngeal volume expansion generates a suction flow that drives prey and surrounding water to flow into the gaping mouth (Alexander 1967; Muller and Osse 1984; van Leeuwen and Muller 1984; Lauder 1985). Terrestrial prey-capture strategies rely on grasping by the jaws (i.e., jaw prehension) or by the tongue (i.e., tongue prehension; Bramble and Wake 1985; Larsen et al 1996; Schwenk 2000)

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