Aquatic–terrestrial transitions of feeding systems in vertebrates: a mechanical perspective

Abstract

Transitions to terrestrial environments confront ancestrally aquatic animals with several mechanical and physiological problems owing to the different physical properties of water and air. As aquatic feeders generally make use of flows of water relative to the head to capture, transport and swallow food, it follows that morphological and behavioral changes were inevitably needed for the aquatic animals to successfully perform these functions on land. Here, we summarize the mechanical requirements of successful aquatic-to-terrestrial transitions in food capture, transport and swallowing by vertebrates and review how different taxa managed to fulfill these requirements. Amphibious ray-finned fishes show a variety of strategies to stably lift the anterior trunk, as well as to grab ground-based food with their jaws. However, they still need to return to the water for the intra-oral transport and swallowing process. Using the same mechanical perspective, the potential capabilities of some of the earliest tetrapods to perform terrestrial feeding are evaluated. Within tetrapods, the appearance of a mobile neck and a muscular and movable tongue can safely be regarded as key factors in the colonization of land away from amphibious habitats. Comparative studies on taxa including salamanders, which change from aquatic feeders as larvae to terrestrial feeders as adults, illustrate remodeling patterns in the hyobranchial system that can be linked to its drastic change in function during feeding. Yet, the precise evolutionary history in form and function of the hyolingual system leading to the origin(s) of a muscular and adhesive tongue remains unknown.

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology, development, and vision in the inner ear

“…Feeding mode is a notable trait distinguishing the sensory ecology of surface-dwelling direct developers and permanently aquatic paedomorphic species: the ballistic tongue projection mechanism observed in many direct developing plethodontids requires a robust vestibular capacity to coordinate vision and head posture, which likely plays a less significant role in aquatic suction feeding among paedomorphic species (Roth 1987;Wake and Deban 2000). Additionally, paedomorphic cave and surface species tend to possess dorso-ventrally flattened skulls that may represent morphological homoplasies to support the biomechanical requirements of suction feeding in an aquatic habitat (Heiss et al 2013(Heiss et al , 2018Herrel et al 2019). Although the relationship of cranial depth with inner ear morphology has not been explored in this study, the shape and depth of the salamander skull may further influence the shape of the inner ear and constrain the degree of curvature of the semicircular canals.…”

Introducing the Amphibious Mudskipper Goby as a Unique Model to Evaluate Neuro/Endocrine Regulation of Behaviors Mediated by Buccal Sensation and Corticosteroids

“…Buccal water is also used for sucking food when mudskippers eat on land [37,38]. Water volume accumulation is essential for the intraoral transport of food on land, and eating appears to be a potent stimulus for buccal thirst.…”

Intentional partial beaching in a coral reef fish: a newly recorded hunting behaviour of titan triggerfish, Balistoides viridescens

“…Fish feeding on terrestrial prey has been widely reported and well documented in freshwater systems (see Kelly et al ., 2016; Van Wassenbergh, 2019, and citations within). Several instances also exist in marine and brackish waters including largescale foureyes, Anableps anableps L. (Michel et al ., 2015a), and mudskippers of the family Oxudercinae (Michel et al ., 2015b), though terrestrial prey capture mechanisms and behaviour can differ widely between species (Bressman et al ., 2020; Heiss et al ., 2018). Intentional beaching as a predatory hunting strategy is reported for several fish species and represents the most basal form of transitional feeding between aquatic and terrestrial habitats (Heiss et al ., 2018).…”

“…Several instances also exist in marine and brackish waters including largescale foureyes, Anableps anableps L. (Michel et al ., 2015a), and mudskippers of the family Oxudercinae (Michel et al ., 2015b), though terrestrial prey capture mechanisms and behaviour can differ widely between species (Bressman et al ., 2020; Heiss et al ., 2018). Intentional beaching as a predatory hunting strategy is reported for several fish species and represents the most basal form of transitional feeding between aquatic and terrestrial habitats (Heiss et al ., 2018). Introduced wels catfish, Silurus glanis L., are known to beach while feeding on pigeons in France (Cucherousset et al ., 2012), and snakeheads, Channa spp., may utilize a similar ambush‐beaching strategy to target amphibian prey (N. Bressmen, pers.…”