Using the whole body as a sucker: Combining respiration and feeding with an attached lifestyle in hill stream loaches (Balitoridae, Cypriniformes)

Abstract

Small fishes living in fast-flowing rivers face a harsh environment as they can easily be swept away by the rapid currents. To survive such circumstances, teleosts evolved a wide variety of attachment mechanisms, based on friction, negative pressure or both. Balitorinae (Balitoridae, Cypriniformes) are exceptional in using their whole body as an adhesive apparatus. We investigated the morphological adaptations of Balitorinae by studying the osteology and myology of four species (Beaufortia leveretti, Sewellia lineolata, Pseudogastromyzon myersi, and Gastromyzon punctulatus) using clearing and staining, serial cross-sections and CT-scanning. A kinematic analysis was performed to study the respiration and feeding mechanisms and to identify key structures in these mechanisms. Our research showed that the whole body of Balitorinae acts as a suction disc, with friction-enhancing structures (unculi) on the thickened anterior rays of the paired fins. The abruptly rising head profile, supported by the extremely enlarged lacrimal bone and the flat ventral body surface facilitate effective substrate attachment. During attachment, the pelvic girdle is pulled anterodorsally, suggesting the formation of a negative pressure underneath the body. Detachment by water inflow underneath the body is prevented by three mechanisms. 1) Barbels control the water inflow by detachment and reattachment to the substrate. 2) Most water present underneath the body is removed during inspiration. 3) Excess water is regularly removed by movements of the posterior pectoral fin rays. The balitorine body is thus modified as such that it allows effective attachment, while not impairing respiration. Comparison with other teleosts living in similar environments shows that most species use more locally concentrated modifications of the paired fins and/or the mouth for attachment. The high diversity in teleostean adhesive apparatuses and associated myological modifications suggest a substantial functional convergent evolution, without necessarily highly convergent anatomical adaptations.

The Adhesive System and Anisotropic Shear Force of Guizhou Gastromyzontidae

“…In some published works, the unculi were supposed to be a key factor to prevent slipping171819. However as reviewed by Conway et al 16,.…”

“…In previous works, the unculi were supposed to be a key factor to prevent slipping171819, and the hypothesis (D) above was applied to explain the mechanism. However, Fig.…”

“…The structure and adhesive mechanism of gastromyzontine loaches have been reported since the 1930s161718. The fishes depend on a suction disc to attach to rocks, and the small keratinous structures covering the surface of the fins and body, unculi18, are important to increase friction.…”

Evolutionary optimization of an anatomical suction cup: Lip collagen content and its correlation with flow and substrate in Neotropical suckermouth catfishes (Loricarioidei)

“…Suction cups that have evolved in fishes fit three broad categories: Whole body, modified fins, and modified mouths. Due to their flexible, highly depressed bodies, hillstream loaches (Balitoridae) are able to use their entire body as a sucker (De Meyer & Geerinckx, 2014). Clingfishes (Gobiosocidae), lumpsuckers (Cyclopteridae), and gobies (Gobiidae) have independently derived pelvic‐fin modifications that allow them to act as a suction cup (Blob et al, 2019; Blob, Rai, Julius, & Schoenfuss, 2006; Davenport & Thorsteinsson, 1990; Ditsche, Wainwright, & Summers, 2014; Maie, Schoenfuss, & Blob, 2012; Schoenfuss & Blob, 2003; Wainwright, Kleinteich, Kleinteich, Gorb, & Summers, 2013), whereas remoras have a highly modified spiny dorsal fin that serves the same function (Beckert, Flammang, & Nadler, 2015; Fulcher & Motta, 2006; Nadler et al, 2013).…”

“…Clingfishes (Gobiosocidae), lumpsuckers (Cyclopteridae), and gobies (Gobiidae) have independently derived pelvic‐fin modifications that allow them to act as a suction cup (Blob et al, 2019; Blob, Rai, Julius, & Schoenfuss, 2006; Davenport & Thorsteinsson, 1990; Ditsche, Wainwright, & Summers, 2014; Maie, Schoenfuss, & Blob, 2012; Schoenfuss & Blob, 2003; Wainwright, Kleinteich, Kleinteich, Gorb, & Summers, 2013), whereas remoras have a highly modified spiny dorsal fin that serves the same function (Beckert, Flammang, & Nadler, 2015; Fulcher & Motta, 2006; Nadler et al, 2013). Cypriniform algae‐eaters (Gyrinocheilidae), some gobies, and suckermouth catfishes in both Africa (Mochokidae) and South America (Astroblepidae, Loricariidae) have mouths that are modified to act as oral suckers, allowing them to adhere to surfaces, often while simultaneously feeding and respiring (De Meyer & Geerinckx, 2014; Geerinckx, Brunain, Herrel, Aerts, & Adriaens, 2007; Gerstner, 2007; Macdonnell, 1990; MacDonnell & Blake, 1990; Maie et al, 2012; Schoenfuss & Blob, 2003). Such anatomical suction cups not only help fishes resist displacement in flowing water, but also aid some species in terrestrial locomotion.…”