Comparative kinematics of cypriniform premaxillary protrusion

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SUMMARY A protrusible upper jaw has independently evolved multiple times within teleosts and has been implicated in the success of two groups in particular: Acanthomorpha and Cypriniformes. We use digital particle image velocimetry (DPIV) to compare suction feeding flow dynamics in a representative of each of these clades: goldfish and bluegill. Using DPIV, we contrast the spatial pattern of flow, the temporal relationship between flow and head kinematics, and the contribution of jaw protrusion to the forces exerted on prey. As expected, the spatial patterns of flow were similar in the two species. However, goldfish were slower to reach maximal kinematic excursions, and were more flexible in the relative timing of jaw protrusion, other jaw movements and suction flows. Goldfish were also able to sustain flow speeds for a prolonged period of time as compared with bluegill, in part because goldfish generate lower peak flow speeds. In both species, jaw protrusion increased the force exerted on the prey. However, slower jaw protrusion in goldfish resulted in less augmentation of suction forces. This difference in force exerted on prey corresponds with differences in trophic niches and feeding behavior of the two species. The bluegill uses powerful suction to capture insect larvae whereas the goldfish uses winnowing to sort through detritus and sediment. The kinethmoid of goldfish may permit jaw protrusion that is independent of lower jaw movement, which could explain the ability of goldfish to decouple suction flows (due to buccal expansion) from upper jaw protrusion. Nevertheless, our results show that jaw protrusion allows both species to augment the force exerted on prey, suggesting that this is a fundamental benefit of jaw protrusion to suction feeders.

Section: Differences Between Goldfish and Bluegillmentioning

confidence: 88%

Section: Differences Between Goldfish and Bluegillmentioning

confidence: 99%

Independently evolved upper jaw protrusion mechanisms show convergent hydrodynamic function in teleost fishes

Holzman

Hernández

et al. 2012

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“…The amount of body ram also influences initial predator-prey distance, strike speed and strike duration, as well as the shape and volume of ingested water during the strike (Weihs, 1980;Harper et al, 1991;Higham et al, 2005;Tran et al, 2010;Oufiero et al, 2012). Jaw protrusion is the most common mechanism of jaw ram and has been shown to decrease the hydrodynamic disturbance detectable by prey while significantly increasing the suction forces on prey (Holzman et al, 2008;Holzman and Wainwright, 2009;Staab et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…To characterize this diversity, we separated the contributions of suction, body ram and jaw ram to closing the distance between predator and prey. There is a long tradition of quantifying the relative contributions of ram and suction to prey capture (Norton, 1991(Norton, , 1995Norton and Brainerd, 1993;Cook, 1996;Gibb, 1997;Nemeth, 1997;Ferry-Graham et al, 2001a;Kerfoot and Turingan, 2011;Wainwright et al, 2001;Wintzer and Motta, 2005;Wilga et al, 2007;Tran et al, 2010;Ferry et al, 2012;Staab et al, 2012). It is well recognized that fishes vary in the relative amount of ram and suction employed during feeding, and hence the 'ram-suction continuum' is a pervasive framework used to characterize diversity (Norton and Brainerd, 1993).…”

Section: Introductionmentioning

confidence: 99%

Body ram, not suction, is the primary axis of suction feeding diversity in spiny-rayed fishes

Longo

McGee

Oufiero

et al. 2015

Suction-feeding fishes exhibit diverse prey-capture strategies that vary in their relative use of suction and predator approach (ram), which is often referred to as the ram-suction continuum. Previous research has found that ram varies more than suction distance among species, such that ram accounts for most differences in prey-capture behaviors. To determine whether these findings hold at broad evolutionary scales, we collected high-speed videos of 40 species of spiny-rayed fishes (Acanthomorpha) feeding on live prey. For each strike, we calculated the contributions of suction, body ram (swimming) and jaw ram (mouth movement relative to the body) to closing the distance between predator and prey. We confirm that the contribution of suction distance is limited even in this phylogenetically and ecologically broad sample of species, with the extreme suction area of prey-capture space conspicuously unoccupied. Instead of a continuum from suction to ram, we find that variation in body ram is the major factor underlying the diversity of prey-capture strategies among suction-feeding fishes. Independent measurement of the contribution of jaw ram revealed that it is an important component of diversity among spiny-rayed fishes, with a number of ecomorphologies relying heavily on jaw ram, including pivot feeding in syngnathiforms, extreme jaw protruders and benthic sit-and-wait ambush predators. A combination of morphological and behavioral innovations has allowed fish to invade the extreme jaw ram area of prey-capture space. We caution that while two-species comparisons may support a ram-suction trade-off, these patterns do not speak to broader patterns across spiny-rayed fishes.

“…obligate mechanical coupling, between lower jaw depression and upper jaw movements ['mandible depression model' (Motta, 1984)]. Recent work suggests that protrusion in cypriniform fishes involves decoupled movements of the upper and lower jaws (Staab et al, 2012). Cypriniform fishes (minnows, carps and their allies) protrude their premaxillae in two different ways ( Fig.1): open mouth protrusions, in which the mouth opens maximally in concert with buccal expansion during food gathering, and closed mouth protrusions, in which the mouth is minimally opened in concert with buccal expansion and the premaxilla is protruded in a more ventral orientation, during food processing (Sibbing, 1982;Sibbing, 1989).…”

Section: Introductionmentioning

confidence: 99%

Flexibility in starting posture drives flexibility in kinematic behavior of the kinethmoid-mediated premaxillary protrusion mechanism in a cyprinid fish,Cyprinus carpio

Gidmark

Staab

Brainerd

et al. 2012

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SUMMARYPremaxillary protrusion in cypriniform fishes involves rotation of the kinethmoid, an unpaired skeletal element in the dorsal midline of the rostrum. No muscles insert directly onto the kinethmoid, so its rotation must be caused by the movement of other bones. In turn, the kinethmoid is thought to push on the ascending processes of the premaxillae, effecting protrusion. To determine the causes and effects of kinethmoid motion, we used XROMM (x-ray reconstruction of moving morphology) to measure the kinematics of cranial bones in common carp, Cyprinus carpio. Mean kinethmoid rotation was 83deg during premaxillary protrusion (18 events in 3 individuals). The kinethmoid rotates in a coordinated way with ventral translation of the maxillary bridge, and this ventral translation is likely driven primarily by the A1b muscle. Analyses of flexibility (variability between behaviors) and coordination (correlation between bones within a behavior) indicate that motion of the maxillary bridge, not the lower jaw, drives premaxillary protrusion. Thus, upper jaw protrusion is decoupled from lower jaw depression, allowing for two separate modes of protrusion, open mouth and closed mouth. These behaviors serve different functions: to procure food and to sort food, respectively. Variation in starting posture of the maxilla alone dictates which type of protrusion is performed; downstream motions are invariant. For closed mouth protrusion, a ventrally displaced maxillary starting posture causes kinethmoid rotation to produce more ventrally directed premaxillary protrusion. This flexibility, bestowed by the kinethmoid-maxillary bridge-A1b mechanism, one of several evolutionary novelties in the cypriniform feeding mechanism, may have contributed to the impressive trophic diversity that characterizes this speciose lineage.