Downloaded from https://academic.oup.com/iob/article-abstract/1/1/obz011/5512359 by guest on 31 July 2019 Integrative OrganismalA Journal of the Society Biology for Integrative and Comparative Biology academic.oup.com/icb Integrative Organismal Biology Integrative Organismal Biology,pp.1–13 doi:10.1093/iob/obz011 A Journal of the Society for Integrative and Comparative Biology RESEARCH ARTICLE Eye Movements in Frogs and Salamanders—Testing the Palatal Buccal Pump Hypothesis F. Witzmann,1* E.L. Brainerd† and N. Konow‡ Downloaded from https://academic.oup.com/iob/article-abstract/1/1/obz011/5512359 by guest on 31 July 2019 *Museum fu¨r Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrasse 43, 10115 Berlin, Germany; †Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912 USA; ‡Department of Biological Sciences, UMass Lowell, Lowell MA 01854 USA 1E-mail: [email protected] Synopsis In frogs and salamanders, movements of the Synopsis Augenbewegungen bei Fro¨schen und Salamandern- eyeballs in association with an open palate have often Pru¨fung der ‘‘palatalen Bukkalpumpen’’-Hypothese been proposed to play a functional role in lung breathing. Bei Fro¨schen und Salamandern wurde oft vorgeschlagen, dass In this ‘‘palatal buccal pump,’’ the eyeballs are elevated Bewegungen der Auga¨pfel in Verbindung mit einem offenen during the lowering of the buccal floor to suck air in Gaumen eine funktionale Rolle bei der Lungenatmung spie- through the nares, and the eyeballs are lowered during len. Bei dieser ‘‘palatalen Bukkalpumpe’’ werden die Auga¨pfel elevation of the buccal floor to help press air into the wa¨hrend des Absenkens des Mundbodens angehoben, um lungs. Here, we used X-Ray Reconstruction of Moving Luft durch die Nasenlo¨cher anzusaugen, und die Auga¨pfel Morphology to investigate eye movements during lung werden wa¨hrend des Anhebens des Mundbodens abgesenkt, breathing and feeding in bullfrogs and axolotls. Our data um Luft in die Lungen zu dru¨cken. Hier verwendeten wir do not show eye movements that would be in accordance Ro¨ntgenrekonstruktionen der Bewegungsmorphologie, um with the palatal buccal pump. On the contrary, there is a Augenbewegungen wa¨hrend der Lungenatmung und bei der small passive elevation of the eyeballs when the buccal Erna¨hrung von Ochsenfro¨schen und Axolotl zu untersuchen. floor is raised. Inward drawing of the eyeballs occurs Unsere Daten zeigen keine Augenbewegungen, die der pala- only during body motion and for prey transport in bull- talen Bukkalpumpe entsprechen wu¨rden. Im Gegenteil, es frogs, but this was not observed in axolotls. Each eye gibt eine kleine passive Anhebung der Auga¨pfel, wenn der movement in bullfrogs has a vertical, a mediolateral, and Mundboden angehoben wird. Ein nach innen Ziehen der an anteroposterior component. Considering the surpris- Auga¨pfel tritt nur wa¨hrend der Ko¨rperbewegung und fu¨r ingly weak posterior motion component of the eyeballs, den Beutetransport in Ochsenfro¨schen auf, bei Axolotl wurde their main role in prey transport might be fixing the dies jedoch nicht beobachtet. Jede Augenbewegung in prey by pressing it against the buccal floor. The retraction Ochsenfro¨schen hat eine vertikale, eine mediolaterale und of the buccal floor would then contribute to the posterior eine anteroposteriore Komponente. Angesichts der u¨berra- push of the prey. Because our study provides no evidence schend schwachen posterioren Bewegungskomponente der for a palatal buccal pump in frogs and salamanders, there Auga¨pfel ko¨nnte ihre Hauptaufgabe beim Beutetransport is also no experimental support for the idea of a palatal die Fixierung der Beute sein, indem sie gegen den bukkalen buccal pump in extinct temnospondyl amphibians, in con- Mundboden Boden gedru¨ckt wird. Das Zuru¨ckziehen des trast to earlier suggestions. Mundbodens wu¨rde dann zum nach hinten gerichteten Schub der Beute beitragen. Da unsere Studie keine Belege fu¨r eine palatale Bukkalpumpe in Fro¨schen und Salamandern liefert, gibt es im Gegensatz zu fru¨heren Vorschla¨gen auch keine experimentelle Unterstu¨tzung fu¨r die Idee einer palatalen Bukkalpumpe in ausgestorbenen tem- nospondylen Amphibien. translated to German by F. Klimm (frederike.klimm@neptun. uni-freiburg.de) VC The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/ 4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 F. Witzmann et al. Introduction also held the view that movements of the eyeballs assist in lung ventilation and regarded the expansion A diagnostic feature of lissamphibians (frogs, sala- of the buccal cavity for breathing as a principal func- manders, and caecilians) is a palate with widely sep- tion of the m. levator bulbi in salamanders. arated pterygoids (Parsons and Williams 1963). The More recently, the hypothesis that the eyeballs and resulting fenestrations between pterygoids and para- the interpterygoid vacuities in frogs and salamanders sphenoid, the interpterygoid vacuities, are consider- may contribute to lung ventilation has attracted the ably enlarged especially in the ‘‘open palate’’ of frogs attention of paleontologists studying early tetrapods. and salamanders (Duellman and Trueb 1994; Schoch Among early tetrapods, the largest and most diverse 2014). This trait facilitates movements of the eyeballs group, the temnospondyls (known from the Early into the buccal cavity (usually termed eye retraction Carboniferous to the Early Cretaceous), have open pal- Downloaded from https://academic.oup.com/iob/article-abstract/1/1/obz011/5512359 by guest on 31 July 2019 in the literature, e.g., Schwenk 2000; Deban and ates with large interpterygoid vacuities similar to extant Wake 2000; Levine et al. 2004). Thereby the eyes frogs and salamanders. Lissamphibians are derived are (1) pulled in by action of the m. retractor bulbi, from temnospondyls (Ruta and Coates 2007; which originates on the ventral surface of the para- Sigurdsen and Green 2011; Schoch 2014; but see sphenoid and is attached to the eyeball and (2) ele- Marjanovic´and Laurin 2019 for a different view) and vated by action of the m. levator bulbi that spans therefore, the enlarged interpterygoid vacuities of frogs most of the interpterygoid vacuities and forms the and salamanders on the one hand and temnospondyls elastic floor of the orbit (Gaupp 1904; Luther 1914; on the other hand can be regarded as a common derived Francis 1934)(Fig. 1). Apart from frogs and sala- character (Fig. 2)(Lautenschlager et al. 2016; manders, inwards drawing of the eyeballs has been Witzmann and Werneburg 2017; Witzmann and Ruta described in batoids (Tomita et al. 2015) and ceta- 2019). Clack (1992) was the first to propose a breathing ceans (Zhu et al. 2001; Bjergager et al. 2003), where function of the open palate in temnospondyls, while it may serve mainly as protection of the eyeballs. In noting that the assistance of the interpterygoid vacuities mudskippers, eye retraction helps the eyeballs to get in buccal pumping of extant frogs and salamanders remoistened (Schwab 2003; Al-Behbehani and ‘‘needs to be corroborated using modern techniques’’ Ebrahim 2010). Frogs and salamanders may similarly (Clack 1992, 416–417). Laurin (2010) similarly sug- pull their eyeballs in for protection, for example, gested a breathing function of the palate in temno- during prey capture (Nishikawa 2000) or while the spondyls, and Clack (2012) presumed both a animals are moving (F. Witzmann and E.L. Brainerd, swallowing and a breathing function of the interpter- personal observations). However, frogs and salaman- ygoid vacuities and eyeball movements in temno- ders are unique among extant tetrapods in pulling spondyls. Schoch (2014,142)introducedtheterm the eyeballs down through the interpterygoid vacui- ‘‘palatalbuccalpump’’forthispresumedmodeof ties into the buccal cavity to force the prey toward lung ventilation in temnospondyls and lissamphi- the esophagus or to help to fixate it (Larsen and bians. The presence of the palatal buccal pump in Guthrie 1975; Deban and Wake 2000; Schwenk temnospondyls would indeed correspond with their 2000; Levine et al. 2004). proportionally large, broad heads and their rather For a long time, a further function of the large immobile ribs, which suggest that they were buccal interpterygoid vacuities and the associated eye pumpers like lissamphibians rather than aspiration muscles in frogs and salamanders has been hypoth- breathers (Janis and Keller 2001). Costal aspiration esized for breathing. Panizza (1845) and Gaupp by contrast probably evolved in stem amniotes with a (1896) proposed that movements of the eyeballs in moveable ribcage and comparatively smaller heads frogs help to ventilate the lungs by buccal pumping. (Janis and Keller 2001), and most of them possess a According to their view, the eyeballs are elevated closed palate or small, slit-like interpterygoid vacui- during the lowering of the buccal floor to increase ties (Fig. 2). the buccal volume and to suck air in through the The present study aims to test the hypothesis of nares, and the eyeballs are lowered during elevation the palatal buccal pump experimentally. Prior studies of the buccal floor to help press air from the buccal have described