Gert Roos

Suction is kid's play: extremely fast suction in newborn seahorses

Ongoing anatomical development typically results in a gradual maturation of the feeding movements from larval to adult fishes. Adult seahorses are known to capture prey by rotating their long-snouted head extremely quickly towards prey, followed by powerful suction. This type of suction is powered by elastic recoil and requires very precise coordination of the movements of the associated feeding structures, making it an all-or-none phenomenon. Here, we show that newborn Hippocampus reidi are able to successfully feed using an extremely rapid and powerful snout rotation combined with a high-volume suction, surpassing that observed in adult seahorses. An inverse dynamic analysis shows that an elastic recoil mechanism is also used to power head rotation in newborn H. reidi. This illustrates how extreme levels of performance in highly complex musculoskeletal systems can be present at birth given a delayed birth and rapid development of functionally important structures. The fact that the head skeleton of newborn seahorses is still largely cartilaginous may not be problematic because the hydrodynamic stress on the rotating snout appeared considerably lower than in adult syngnathids.

Kinematics of suction feeding in the seahorse Hippocampus reidi

SUMMARY Fish typically use a rostro-caudal wave of head expansion to generate suction, which is assumed to cause a uni-directional, anterior-to-posterior flow of water in the expanding head. However, compared with typical fish, syngnathid fishes have a remarkably different morphology (elongated snout, small hyoid, immobile pectoral girdle) and feeding strategy (pivot feeding: bringing the small mouth rapidly close to the prey by neurocranial dorsorotation). As a result, it is unclear how suction is generated in Syngnathidae. In this study, lateral and ventral expansions of the head were quantified in Hippocampus reidi and linked to the kinematics of the mouth, hyoid and neurocranium. In addition, the flow velocities inside the bucco-pharyngeal cavity and in front of the mouth were calculated. Our data suggest that the volume changes caused by lateral expansion are dominant over ventral expansion. Maximum gape, neurocranium rotation and hyoid depression are all reached before actual volume increase and before visible prey movement. This implies that, unlike previously studied teleosts, hyoid rotation does not contribute to ventral expansion by lowering the floor of the mouth during prey capture in H. reidi. The lateral volume changes show a rostro-caudal expansion, but the maximal flow velocity is not near the mouth aperture (as has been demonstrated for example in catfish) but at the narrow region of the buccal cavity, dorsal to the hyoid.

Linking morphology and motion: a test of a four-bar mechanism in seahorses.

Syngnathid fishes (seahorses, pipefish, and sea dragons) possess a highly modified cranium characterized by a long and tubular snout with minute jaws at its end. Previous studies indicated that these species are extremely fast suction feeders with their feeding strike characterized by a rapid elevation of the head accompanied by rotation of the hyoid. A planar four‐bar model is proposed to explain the coupled motion of the neurocranium and the hyoid. Because neurocranial elevation as well as hyoid rotation are crucial for the feeding mechanism in previously studied Syngnathidae, a detailed evaluation of this model is needed. In this study, we present kinematic data of the feeding strike in the seahorse Hippocampus reidi. We combined these data with a detailed morphological analysis of the important linkages and joints involved in rotation of the neurocranium and the hyoid, and we compared the kinematic measurements with output of a theoretical four‐bar model. The kinematic analysis shows that neurocranial rotation never preceded hyoid rotation, thus indicating that hyoid rotation triggers the explosive feeding strike. Our data suggest that while neurocranium and hyoid initially (first 1.5 ms) behave as predicted by the four‐bar model, eventually, the hyoid rotation is underestimated by the model. Shortening, or a posterior displacement of the sternohyoid muscle (of which the posterior end is confluent with the hypaxial muscles in H. reidi), probably explains the discrepancy between the model and our kinematic measurements. As a result, while four‐bar modeling indicates a clear coupling between hyoid rotation and neurocranial elevation, the detailed morphological determination of the linkages and joints of this four‐bar model remain crucial in order to fully understand this mechanism in seahorse feeding.

Snout allometry in seahorses: insights on optimisation of pivot feeding performance during ontogeny

SUMMARY As juvenile life-history stages are subjected to strong selection, these stages often show levels of performance approaching those of adults, or show a disproportionately rapid increase of performance with age. Although testing performance capacity in aquatic suction feeders is often problematic, in pivot feeders such as seahorses models have been proposed to estimate whether snout length is optimal to minimise the time needed to reach the prey. Here, we investigate whether the same model can also explain the snout lengths in an ontogenetic series of seahorses, explore how pivot feeding kinematics change during ontogeny, and test whether juveniles show disproportionate levels of performance. Our analysis shows that the dimensions of the snout change during ontogeny from short and broad to long and narrow. Model calculations show that the snout lengths of newborn and juvenile seahorses are nearly optimal for minimising prey reach time. However, in juveniles the centre of head rotation in the earth-bound frame of reference is located near the posterior end of the head, whereas in adults it is shifted forward and is located approximately above the eye. Modelling shows that this forward shift in the centre of rotation has the advantage of decreasing the moment of inertia and the torque required to rotate the head, but has the disadvantage of slightly increasing the time needed to reach the prey. Thus, the snout lengths of juvenile seahorses appear to be close to optimal, suggesting that they reach levels of performance close to adult levels, which illustrates the pervasive nature of selection on performance in juveniles.

Effects of snout dimensions on the hydrodynamics of suction feeding in juvenile and adult seahorses

Seahorses give birth to juveniles having a fully functional feeding apparatus, and juvenile feeding behaviour shows striking similarities to that of adults. However, a significant allometric growth of the snout is observed during which the snout shape changes from relatively short and broad in juveniles to relatively long and slender in adults. Since the shape of the buccal cavity is a critical determinant of the suction performance, this snout allometry will inevitably affect the suction feeding ability. To test whether the snout is optimised for suction feeding throughout an ontogeny, we simulated the expansion of different snout shapes varying from extremely long and slender to short and broad for juvenile and adult snout sizes, using computational fluid dynamic models. Our results showed that the snout diameter at the start of the simulations is involved in a trade-off between the realizable suction volume and expansion time on the one hand (improving with larger initial diameters), and maximal flow velocity on the other hand (improving with smaller initial diameters). Moreover suction performance (suction volume as well as maximal attainable flow velocity) increased with decreasing snout length. However, an increase in snout length decreases the time to reach the prey by the cranial rotation, which may explain the prevalence of long snouts among syngnathid fishes despite the reduced suction performance. Thus, the design of the seahorse snout revolves around a trade-off between the ability to generate high-volume suction versus minimisation of the time needed to reach the prey by the cranial rotation.

Why the long face? A comparative study of feeding kinematics of two pipefishes with different snout lengths.

This study showed that the mouth of Doryrhamphus dactyliophorus, a species with a relatively long snout, travels a greater distance compared with Doryrhamphus melanopleura, a species with a considerably shorter snout, allowing it to strike at prey that are farther away from the mouth. The long-snouted species also tended to reach significantly higher linear velocities of the mouth approaching the prey. On the other hand, D. melanopleura needed less time to capture its prey. A striking difference in prey-capture success was observed between species: D. melanopleura and D. dactyliophorus had a prey-capture success of 91 and 31%, respectively. The small prey size and the relatively large distance between eyes and prey are potential reasons why directing the mouth accurately to the prey is difficult in D. dactyliophorus, hence possibly explaining the lower prey-capture success in this long-snouted species.

Morphological variation in head shape of pipefishes and seahorses in relation to snout length and developmental growth

The feeding apparatus of Syngnathidae, with its elongate tubular snout and tiny, toothless jaws, is highly specialized for performing fast and powerful pivot feeding. In addition, the prolonged syngnathid parental care probably enables the juveniles to be provided with a feeding apparatus that resembles the one in adults, both in morphology and function. In this study, a landmark‐based geometric morphometric analysis was carried out on the head of syngnathid representatives in order to (1) examine to what degree pipefish shape variation is different from that of seahorses; (2) determine whether the high level of specialization reduces the amount of intraspecific morphological variation found within the family; and (3) elucidate whether or not important shape changes occur in the seahorse head during postrelease ontogeny. We found that (1) there is a significant shape difference between head shape of pipefish and seahorse: the main differences concern snout length and height, position and orientation of the pectoral fin base, and height of the head and opercular bone. We hypothesize that this might be related to different prey capture kinematics (long snout with little head rotation versus short snout with large head rotation) and to different body postures (in line with the head versus vertical with a tilted head) in pipefishes and seahorses; (2) both pipefishes and seahorses showed an inverse relation between relative snout length and intraspecific variation and although pipefishes show a large diversity in relative snout elongation, they are more constrained in terms of head shape; and (3) the head of juvenile Hippocampus reidi specimens still undergoes gradual shape changes after being expelled from the brood pouch. Ontogenetic changes include lowering of the snout and head but also differences in orientation of the preopercular bone and lowering of the snout tip. J. Morphol. 2011.