Suckermouth armored catfish resolve the paradox of simultaneous respiration and suction attachment: a kinematic study of Pterygoplichthys disjunctivus

Abstract

Suckermouth armored catfishes (Loricariidae) use their suckermouth for inspiration, feeding, and attachment to substrates. The sucker consists of a pre-valvular cavity, formed by a modified lip disc, and is separated from the larger post-valvular buccal cavity by a muscular oral valve. The combination of respiration and suction attachment seems paradoxal, as a properly functioning suction device would need a sucker without leakage (yet inspiration must occur via the sucker), and continuous subambient pressure in the sucker cavity (even during expiratory mouth floor elevation). In the loricariid Pterygoplichthys disjunctivus, the anatomy of the suckermouth structures was examined, and a kinematic analysis was performed to acquire insights into how respiration and attachment are combined. High-speed external and X-ray recordings show that suckermouth attachment influences respiratory parameters such as decreasing excursion amplitudes of mouth floor elements, and the way water enters the mouth via furrows in the lip disc. Respiration, however, continues during attachment and is not blocked. Our data show that the muscular oral valve actively separates the post-valvular buccal cavity from the pre-valvular sucker cavity. Volume changes of this pre-valvular cavity are opposite to those of the post-valvular cavity and assure sucker function even during expiration. These volume changes are caused by movements of the lower lip, the lower jaws, and the oral valve. The lateral inflow furrow openings, controlled by the maxillary barbels, can occur unilaterally. Morphological and kinematic data also show that the opercle is anatomically and functionally decoupled from the gill opening.

Functional morphology of the Andean climbing catfishes (Astroblepidae, Siluriformes): Alternative ways of respiration, adhesion, and locomotion using the mouth

“…Astroblepidae do not share the loss of the involvement of the pectoral girdle in respiration, as has been observed in sister family Loricariidae, where the pectoral girdle is virtually immobile (Geerinckx et al, ). Compared to the hyoid and pectoral girdle, the contribution of the lower jaws is low in astroblepids, and higher in loricariids (Geerinckx et al, ). Apart from the pectoral girdle, the opercular of Loricariidae also has been decoupled from respiration, leaving them with a prominent role for the lower jaws and hyoid.…”

“…This is quite different from the mechanism found in Loricariidae. During respiration with suckermouth attachment, loricariids sustain adhesion via the mouth while allowing water inflow through a furrow created in the lateral lip tissue by slightly elevating the maxillary barbel (Alexander, 1965; Geerinckx et al, ). This action has been ascribed to the levator tentaculi muscle (Geerinckx et al, ).…”

The liver transcriptome of suckermouth armoured catfish (Pterygoplichthys anisitsi, Loricariidae): Identification of expansions in defensome gene families

“…are known to have several distinctive features that might aid their rapid establishment in non-native habitats (Douglas et al, 2002; Ebenstein et al, 2015; Geerinckx et al, 2011; German and Bittong, 2009; Harter et al, 2014; Jumawan and Herrera, 2015; Villalba-Villalba et al, 2013). Among these features, the modified stomach of loricariid catfishes allows the absorption of oxygen through a well documented air-breathing behavior, making these species highly resistant to hypoxia (da Cruz et al, 2013).…”

Underwater attachment using hairs: the functioning of spatula and sucker setae from male diving beetles

“…Cephalopods use arm and tentacle suckers for prey capture or manipulation by varying the pressure differential through active muscle control [18 -21]. Muscular suckers also evolved in some fishes as oral discs to maintain position [22,23] or at modified dorsal fins to attach to a host's skin [24]. Despite the growing knowledge of dry adhesion in biological fibrillar systems, little is known about their underwater attachment except for a few demonstrations of bioinspired fibrillar adhesives with chemical coatings [9] or through a suction effect [25,26].…”

“…However, less is known about the biomechanics of their specialized attachment devices, either in the primitive spatula form or the derived sucker form. Spatula setae found in insects are mostly used for dry adhesion involving a van der Waals interaction or wet adhesion using capillary force [12], whereas biological suckers mostly require muscular control for sealing and generating pressure differences [18,19,[22][23][24]. Therefore, members of the Dytiscinae provide us with a great opportunity to explore and compare the functional mechanisms of spatula setae and 'passive' suckers for underwater adhesion.…”