Bottom Feeding and Beyond: How the Premaxillary Protrusion of Cypriniforms Allowed for a Novel Kind of Suction Feeding

Abstract

While much of the functional work on suction feeding has involved members of Acanthopterygii, an earlier cypriniform radiation led to over 3200 species filling nearly every freshwater trophic niche. Within the great majority of acanthomorph clades that have been investigated suction feeding and the underlying morphology responsible for the generation of rapid suction have been largely conserved. This conserved feeding-apparatus is often associated with increasing the force experienced by the prey item, thus making a strike on elusive prey more effective. Cypriniforms' trophic anatomy is comprised of a number of novelties used for benthic feeding, which characterized early members of this clade. The modified cypriniform structure of the oral jaws represents a situation in which a particular type of suction feeding allowed for probing the benthos with a more functionally maneuverable anatomy. Requisite evolutionary modifications included origin and elongation of a median kinethmoid, duplications of certain divisions of the muscles of the adductor mandibulae, and origin of a dorsal, intra-buccal muscular palatal organ used in winnowing detritus. The elongated kinethmoid (coupled with modified adductor muscles) allowed for a type of premaxillary protrusion that decoupled the upper and lower jaws, enabled premaxillary protrusions with a closed mouth, and facilitated benthic feeding by increasing functional flexibility. The resultant flow of fluid generated by cypriniforms is also quite flexible, with multiple instances of peak flow in a single feeding event. This greatly modified morphology allowed for a degree of kinematic maneuverability not seen within most acanthomorphs. Later cypriniform radiations into piscivorous, insectivorous, or planktivorous feeding guilds were associated with shortening of the kinethmoid and with simplified morphology of the adductor, likely involving an emphasis on ram feeding. Although this suite of morphological novelties seemingly originated within the context of benthic feeding, with minimal modifications these anatomical features were later coopted during radiations into different functional niches.

The evolution of jaw protrusion mechanics has been tightly coupled to bentho-pelagic divergence in damselfishes (Pomacentridae)

“…Two of the most successful vertebrate lineages, the Acanthomorpha (∼17,000 species) and Cypriniformes (∼3200 species), are composed of fish species that have rapidly transitioned between forms with highly protrusile upper jaws and those that exhibit little to no jaw protrusion (Hernandez and Staab, 2015;Hulsey et al, 2010;Staab et al, 2012;Wainwright et al, 2015;Bellwood et al, 2015). Both acanthomorphs and cypriniforms possess jaw arrangements that allow simple shape changes to either enhance or reduce jaw protrusion, with changes in the length of the ascending arm of the premaxilla having particular importance (Hernandez and Staab, 2015;McGee et al, 2015b;Rice et al, 2008;Staab et al, 2012). Both clades also occupy an extremely large number of feeding niches (Hernandez and Staab, 2015;Wainwright et al, 2015).…”

“…Both acanthomorphs and cypriniforms possess jaw arrangements that allow simple shape changes to either enhance or reduce jaw protrusion, with changes in the length of the ascending arm of the premaxilla having particular importance (Hernandez and Staab, 2015;McGee et al, 2015b;Rice et al, 2008;Staab et al, 2012). Both clades also occupy an extremely large number of feeding niches (Hernandez and Staab, 2015;Wainwright et al, 2015). If this diversity is largely a product of having protrusion mechanisms in which small morphological changes produce adaptive functional shifts, then these jaw mechanisms can be regarded as highly evolvable biomechanical systems (Pigliucci, 2008).…”

“…Furthermore, the use of phylogenetic comparative methods to analyse functional data has been limited, and this impairs the validity of many of the statistical methods that have been used to examine functional diversification. Although it has been demonstrated that differences in jaw protrusion mechanics between closely related species are associated with differences in trophic ecology (Hernandez and Staab, 2015;Holzman et al, 2008a;McGee et al, 2015b;Rice et al, 2008), we know of only a single study that corrected for relatedness in order to identify which aspects of functional morphology have evolved in correlation with jaw protrusion (Hulsey et al, 2010). No previous studies have used phylogenetic comparative methods to: (1) determine whether fishes in different trophic guilds possess different protrusion abilities, or (2) characterize which evolutionary models best fit patterns of divergence in protrusion ability among the members of a lineage.…”

The complex trophic anatomy of silver carp, Hypophthalmichthys molitrix, highlighting a novel type of epibranchial organ

“…Cypriniformes, the largest order within Otocephala, is characterized by multiple trophic modifications including loss of several structures (oral jaw teeth, upper pharyngeal jaws, and stomach) as well as the addition of a kinethmoid and palatal organ (Finger, 2008;Hernandez, Bird, & Staab, 2007;Sibbing, 1982). The palatal organ is present at the base of Cypriniformes (Hernandez & Staab, 2015) and is a thick cushion of muscle located on the roof of the buccal cavity shown to play a large role in prey manipulation in common carp (Sibbing, Osse, & Terlouw, 1986). There is significant morphological variation in the palatal organ of cypriniforms (Doosey & Bart, 2011).…”

Anatomical Assessment of the Adult Skeleton of Zebrafish Reared Under Different Thyroid Hormone Profiles

“…Ostariophysi, the larger group that includes Cypriniformes, has a number of evolutionary novelties including the Weberian apparatus (bony ossicles that connect the swim bladder to the inner ear, making species within this group hearing specialists) (Bird and Hernandez, ; Hernandez et al, ). Cypriniformes in particular possess the kinethmoid, a sesamoid bone that mediates premaxillary protrusion (Hernandez et al, ; Hernandez and Staab, ).…”