Eye Movements in Frogs and Salamanders—Testing the Palatal Buccal Pump Hypothesis

Abstract

Synopsis In frogs and salamanders, movements of the eyeballs in association with an open palate have often been proposed to play a functional role in lung breathing. In this “palatal buccal pump,” the eyeballs are elevated during the lowering of the buccal floor to suck air in through the nares, and the eyeballs are lowered during elevation of the buccal floor to help press air into the lungs. Here, we used X-Ray Reconstruction of Moving Morphology to investigate eye movements during lung breathing and feeding in bullfrogs and axolotls. Our data do not show eye movements that would be in accordance with the palatal buccal pump. On the contrary, there is a small passive elevation of the eyeballs when the buccal floor is raised. Inward drawing of the eyeballs occurs only during body motion and for prey transport in bullfrogs, but this was not observed in axolotls. Each eye movement in bullfrogs has a vertical, a mediolateral, and an anteroposterior component. Considering the surprisingly weak posterior motion component of the eyeballs, their main role in prey transport might be fixing the prey by pressing it against the buccal floor. The retraction of the buccal floor would then contribute to the posterior push of the prey. Because our study provides no evidence for a palatal buccal pump in frogs and salamanders, there is also no experimental support for the idea of a palatal buccal pump in extinct temnospondyl amphibians, in contrast to earlier suggestions.

XROMM Analysis of Feeding Mechanics in Toads: Interactions of the Tongue, Hyoid, and Pectoral Girdle

“…In previous reports on amphibian feeding mechanics, it has been suggested that eye retraction plays an important role in swallowing prey, either by fixing the prey in place or pushing it backwards into the esophagus ( Larsen and Guthrie 1975 ; Regal and Gans 1976 ; Deban and Wake 2000 ; Nishikawa 2000 ; Schwenk 2000 ; Levine et al 2004 ; Noel et al 2017 ; Witzmann et al 2019 ). Frogs have large interpterygoid vacuities that allow the eyeball to move into the buccal cavity via action of the m. retractor bulbi, which we successfully simulated during our dissections of R. marina .…”

“…The mechanism of the anuran “tongue flip” has been explored by biologists since the 1800s (see Gans and Gorniak 1982a ). Over the past ∼40 years, advancements in experimental techniques such as EMG (electromyography), high speed video, and XROMM (X-ray Reconstruction of Moving Morphology) have led to many new insights in anuran feeding mechanisms ( Emerson 1977 ; Gans and Gorniak 1982a ; Nishikawa 2000 ; Witzmann et al 2019 ).…”

“…However, prey transport and swallowing phases of the feeding cycle are known to be complex and important in vertebrates such as mammals ( Smith 1992 ; Mayerl et al 2021 ). Several studies on frog feeding mechanics have remarked on the swallowing mechanism ( Regal and Gans 1976 ; Ritter and Nishikawa 1995 ; Yoshida 2001 ), but few have examined it specifically ( Levine et al 2004 ; Witzmann et al 2019 ). Some have hypothesized that the tongue is the main functional organ for swallowing prey ( Regal and Gans 1976 ; Duellman and Trueb 1986 ; Gray et al 1997 ; Nishikawa 2000 ) and posited that the hyoglossus muscle and tongue contribute to prey transport and swallowing ( Ritter and Nishikawa 1995 ; Tso et al 1995 ).…”

The orbitalauricular chord of Alligator: The unusual functional linkage between the earflap and eyelid of Crocodylians

“…Less attention has been paid to the coordination between these two sets of anatomically-adjacent epithelial covers; Garrick and Saiff (1974) described a coordinated elevation of the lower eyelid and lower earflap during submergence of Caiman sclerops. Though not as welldeveloped as in some other vertebrates (Witzmann et al, 2019), retraction of the eye has been described in Alligator and other Crocodylians (e.g., Fleming & Fontenor, 2014). Similar medial retraction has not been described in the earflaps of crocodylians.…”

Do salamanders chew? An X-ray reconstruction of moving morphology analysis of ambystomatid intraoral feeding behaviours

“…The idea that amphibians-the closest extant clade of vertebrates to the tetrapod taxa that invaded land in the Devonian [29,30]-are unique among gnathostomes by not processing their food is unparsimonious, particularly when considering that both more basal, as well as more derived taxa process their food. Indeed, recent X-ray-based studies of several salamander species have generated evidence to the contrary [30][31][32][33][34][35] by revealing the presence of cyclic and rhythmic intraoral behaviours following food capture, and before swallowing [36]. However, these studies generally lacked the rigorous hypothesistesting framework required to conclusively disambiguate food processing-chewing-from other intraoral behaviours, particularly intraoral food transport [20,37].…”