Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

Daniel Schwarz,Egon Heiss,Nicolai Konow,Laura B Porro

doi:10.1186/s12983-020-00373-x

Abstract

BackgroundThe feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region. The morphology of the feeding apparatus in turn determines the boundary conditions for possible food processing (i.e., intraoral mechanical reduction) mechanisms. However, the morphology of the feeding apparatus changes substantially during metamorphosis, prompting the hypothesis that larvae might use a different food processing mechanism than post-metamorphic adults. Salamandrid newts with facultative metamorphosis are suitable for testing this hypothesis as adults with divergent feeding apparatus morphologies often coexist in the same population, share similar body sizes, and feed on overlapping prey spectra.MethodsWe use high-speed videography to quantify the in vivo movements of key anatomical elements during food processing in paedomorphic and metamorphic Alpine newts (Ichthyosaura alpestris). Additionally, we use micro-computed tomography (μCT) to analyze morphological differences in the feeding apparatus of paedomorphic and metamorphic Alpine newts and sort them into late-larval, mid-metamorphic and post-metamorphic morphotypes.ResultsLate-larval, mid-metamorphic and post-metamorphic individuals exhibited clear morphological differences in their feeding apparatus. Regardless of the paedomorphic state being externally evident, paedomorphic specimens can conceal different morphotypes (i.e., late-larval and mid-metamorphic morphotypes). Though feeding on the same prey under the same (aquatic) condition, food processing kinematics differed between late-larval, mid-metamorphic and post-metamorphic morphotypes.ConclusionsThe food processing mechanism in the Alpine newt changes along with morphology of the feeding apparatus during ontogeny, from a mandible-based to a tongue-based processing mechanism as the changing morphology of the mandible prevents chewing and the tongue allows enhanced protraction. These results could indicate that early tetrapods, in analogy to salamanders, may have developed new feeding mechanisms in their aquatic environment and that these functional innovations may have later paved the way for terrestrial feeding mechanisms.

Highlights

The feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region
The food processing mechanism in the Alpine newt changes along with morphology of the feeding apparatus during ontogeny, from a mandible-based to a tongue-based processing mechanism as the changing morphology of the mandible prevents chewing and the tongue allows enhanced protraction. These results could indicate that early tetrapods, in analogy to salamanders, may have developed new feeding mechanisms in their aquatic environment and that these functional innovations may have later paved the way for terrestrial feeding mechanisms
Functional morphology of the feeding apparatus Detailed descriptions of the cranial anatomy of Ichthyosaura alpestris and other salamandrids can be found elsewhere [26, 32, 46,47,48,49,50,51,52] and we focus on structures relevant for processing and on specific differences between morphotypes

Summary

Introduction

The feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region. The morphology of the feeding apparatus changes substantially during metamorphosis, prompting the hypothesis that larvae might use a different food processing mechanism than post-metamorphic adults. A recent study suggests that in species undergoing metamorphosis, parts of the skull associated with feeding develop faster and more independently from the rest [4]. This in turn suggests that the form and function of skeletal elements associated with feeding may be more flexible. Individuals can either undergo or skip metamorphosis (i.e., facultative paedomorphosis) [8, 11], resulting in paedomorphic and metamorphosed adults co-populating similar niches of a habitat whilst differing in morphology (i.e., heterochronic morphotypes). Behavioral studies have shown that paedomorphs tend to have greater aquatic prey capture performance [12, 14], but surprisingly, despite diverging prey capture performance and major differences in head morphology, there are only minor differences in prey capture kinematics between heterochronic morphotypes [13,14,15,16]

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