Always chew your food: freshwater stingrays use mastication to process tough insect prey

Abstract

Chewing, characterized by shearing jaw motions and high-crowned molar teeth, is considered an evolutionary innovation that spurred dietary diversification and evolutionary radiation of mammals. Complex prey-processing behaviours have been thought to be lacking in fishes and other vertebrates, despite the fact that many of these animals feed on tough prey, like insects or even grasses. We investigated prey capture and processing in the insect-feeding freshwater stingray Potamotrygon motoro using high-speed videography. We find that Potamotrygon motoro uses asymmetrical motion of the jaws, effectively chewing, to dismantle insect prey. However, CT scanning suggests that this species has simple teeth. These findings suggest that in contrast to mammalian chewing, asymmetrical jaw action is sufficient for mastication in other vertebrates. We also determined that prey capture in these rays occurs through rapid uplift of the pectoral fins, sucking prey beneath the ray's body, thereby dissociating the jaws from a prey capture role. We suggest that the decoupling of prey capture and processing facilitated the evolution of a highly kinetic feeding apparatus in batoid fishes, giving these animals an ability to consume a wide variety of prey, including molluscs, fishes, aquatic insect larvae and crustaceans. We propose Potamotrygon as a model system for understanding evolutionary convergence of prey processing and chewing in vertebrates.

Chewing or not? Intraoral food processing in a salamandrid newt

“…Processing mechanisms differ substantially across vertebrate groups but coordinated rhythmic and cyclic movements of the jaw, skull and hyobranchial (tongue) system are common in cartilaginous and ray-finned fishes, lungfishes and amniotes (Bemis and Lauder, 1986;Dean et al, 2005;Gans et al, 1978;Gans and Vree, 1986;Gintof et al, 2010;Sanford and Lauder, 1989;Schwenk and Rubega, 2005;Schwenk and Wake, 1993;Wainwright et al, 1989). Whereas some cartilaginous fishes, including sharks and rays, use rhythmic chewing to process food within their mandibular jaw systems (Dean et al, 2005;Kolmann et al, 2016), ray-finned fishes exhibit three 'jaw systems' for food processing: (i) raking, using the tongue-bite apparatus (Camp et al, 2009;Hilton, 2001;Konow et al, 2013;Konow and Sanford, 2008;Lauder, 1989, 1990), (ii) grinding, using the pharyngeal jaw apparatus (referred to as 'pharyngognathy') (Gidmark et al, 2014;Liem and Greenwood, 1981;Wainwright, 2002;Wainwright et al, 1989) and (iii) chewing, using the mandibular jaw apparatus (Fernandez and Motta, 1997;Gintof et al, 2010;Konow and Sanford, 2008;Lauder, 1981). While raking and pharyngognathy are derived mechanisms that only occur in some ray-finned fish groups, chewing occurs in both fishes and amniotes (Gans et al, 1978;Gintof et al, 2010;Herring et al, 2001;Hiiemae and Crompton, 1985;Schwenk, 2000a;Schwenk and Rubega, 2005).…”

Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro

“…The batoids (rays, skates, guitarfishes and sawfishes) consume a range of hard and tough prey and are known for their elaborate prey processing strategies (Dean et al, 2005(Dean et al, , 2007Kolmann et al, 2016;Sasko et al, 2006;Wilga and Motta, 1998). Notably, their cranial anatomy differs from that of teleost fishes, as they lack pharyngeal jaws, and from that of other elasmobranchs in that they exhibit a euhyostylic jaw suspension, wherein all skeletal and ligamentous connections between the upper jaw (palatoquadrate) and the cranium have been lost (Maisey, 1980;Wilga, 2002).…”

“…One group of freshwater stingrays, the sub-family Potamotrygoninae, has recently received attention for its complex prey processing kinematics and derived hyomandibular morphology (Kolmann et al, 2016). Potamotrygonins are the neotropical, obligate freshwater members of the family Potamotrygonidae, to which the genus Styracura has recently been added (Carvalho et al, 2016).…”

“…We predict that the elongate morphology of P. motoro's AAC enables the jaws to protrude further and faster from the head than the distal ends of the hyomandibulae, and that the 3D motions of the jaws relative to the hyomandibulae will be limited by the bracing effect of the two cartilages. Kolmann et al (2016) used high-speed video to investigate the processing kinematics of P. motoro. By varying prey type, they found that P. motoro chews with more frequent symphyseal flexion and asymmetrical shearing motions when a prey item is tougher.…”

Dentition of the apron ray Discopyge tschudii (Elasmobranchii: Narcinidae)

“…Discopyge tschudii , like other narcinids such as Narcine brasiliensis (Olfers 1831), use extreme jaw protrusion to capture and process prey (Dean & Motta, ). Posteriorly oriented tooth cusps could facilitate retention of soft‐bodied prey, preventing the prey‐sliding off the jaws as has been suggested for N. brasiliensis (Dean et al ., ) and Potamotrygon motoro (Müller & Henle 1841) (Kolmann et al ., ).…”