Joachim Christiaens

Musculoskeletal structure of the feeding system and implications of snout elongation in Hippocampus reidi and Dunckerocampus dactyliophorus

A thorough morphological description of the feeding apparatus in Hippocampus reidi, a long-snouted seahorse, and Dunckerocampus dactyliophorus, an extremely long-snouted pipefish, revealed specialized features that might be associated with the fast and powerful suction feeding, like the two ligamentous connections between the lower jaw and the hyoid, the saddle joint of the latter with the suspensorium and the vertebro-pectoral fusion that articulates on three points with the cranium. Despite the conserved morphology of the feeding apparatus, it was found that in H. reidi the orientation of the occipital joint is ventrocaudal, the sternohyoideus and epaxial muscles are more bulky and both have a short tendon. In D. dactyliophorus, on the other hand, the protractor hyoidei muscle is enclosed by the mandibulo-hyoid ligament, the sternohyoideus and epaxial tendons are long and a sesamoid bone is present in the latter. These features were compared to other syngnathid species with different snout lengths to evaluate the implications of snout elongation on the musculoskeletal structure of the cranium. The arched path of the adductor mandibulae and the greater rigidity of the lower jaw might be related to elongation of the snout, as it yields an increased mechanical advantage of the lower jaw system and a reduced torque between the elements of the lower jaw during protractor hyoidei muscle contraction, respectively. Nevertheless, most observed features did not seem to be related to snout length, but might be associated with different force-generating strategies.

Cranial architecture of tube-snouted gasterosteiformes (Syngnathus rostellatus and Hippocampus capensis).

The long snout of pipefishes and seahorses (Syngnathidae, Gasterosteiformes) is formed as an elongation of the ethmoid region. This is in contrast to many other teleosts with elongate snouts (e.g., butterflyfishes) in which the snout is formed as an extension of the jaws. Syngnathid fishes perform very fast suction feeding, accomplished by powerful neurocranial elevation and hyoid retraction. Clearly, suction through a long and narrow tube and its hydrodynamic implications can be expected to require certain adaptations in the cranium, especially in musculoskeletal elements of the feeding apparatus. Not much is known about which skeletal elements actually support the snout and what the effect of elongation is on related structures. Here, we give a detailed morphological description of the cartilaginous and bony feeding apparatus in both juvenile and adult Syngnathus rostellatus and Hippocampus capensis. Our results are compared with previous morphological studies of a generalized teleost, Gasterosteus aculeatus. We found that the ethmoid region is elongated early during development, with the ethmoid plate, the hyosymplectic, and the basihyal cartilage being extended in the chondrocranium. In the juveniles of both species almost all bones are forming, although only as a very thin layer. The elongation of the vomeral, mesethmoid, quadrate, metapterygoid, symplectic, and preopercular bones is already present. Probably, because of the long and specialized parental care which releases advanced developmental stages from the brooding pouch, morphology of the feeding apparatus of juveniles is already very similar to that of the adults. We describe morphological features related to snout elongation that may be considered adaptations for suction feeding; e.g. the peculiar shape of the interhyal bone and its saddle‐shaped articulation with the posterior ceratohyal bone might aid in explosive hyoid retraction by reducing the risk of hyoid dislocation. J. Morphol., 2010.

Grasping convergent evolution in syngnathids: a unique tale of tails

Seahorses and pipehorses both possess a prehensile tail, a unique characteristic among teleost fishes, allowing them to grasp and hold onto substrates such as sea grasses. Although studies have focused on tail grasping, the pattern of evolutionary transformations that made this possible is poorly understood. Recent phylogenetic studies show that the prehensile tail evolved independently in different syngnathid lineages, including seahorses, Haliichthys taeniophorus and several types of so‐called pipehorses. This study explores the pattern that characterizes this convergent evolution towards a prehensile tail, by comparing the caudal musculoskeletal organization, as well as passive bending capacities in pipefish (representing the ancestral state), pipehorse, seahorse and H. taeniophorus. To study the complex musculoskeletal morphology, histological sectioning, μCT‐scanning and phase contrast synchrotron scanning were combined with virtual 3D‐reconstructions. Results suggest that the independent evolution towards tail grasping in syngnathids reflects at least two quite different strategies in which the ancestral condition of a heavy plated and rigid system became modified into a highly flexible one. Intermediate skeletal morphologies (between the ancestral condition and seahorses) could be found in the pygmy pipehorses and H. taeniophorus, which are phylogenetically closely affiliated with seahorses. This study suggests that the characteristic parallel myoseptal organization as already described in seahorse (compared with a conical organization in pipefish and pipehorse) may not be a necessity for grasping, but represents an apomorphy for seahorses, as this pattern is not found in other syngnathid species possessing a prehensile tail. One could suggest that the functionality of grasping evolved before the specialized, parallel myoseptal organization seen in seahorses. However, as the grasping system in pipehorses is a totally different one, this cannot be concluded from this study.

Diet-induced phenotypic plasticity in European eel (Anguilla anguilla).

ABSTRACT Two phenotypes are present within the European eel population: broad-heads and narrow-heads. The expression of these phenotypes has been linked to several factors, such as diet and differential growth. The exact factors causing this dimorphism, however, are still unknown. In this study, we performed a feeding experiment on glass eels from the moment they start to feed. Eels were either fed a hard diet, which required biting and spinning behavior, or a soft diet, which required suction feeding. We found that the hard feeders develop a broader head and a larger adductor mandibulae region than eels that were fed a soft diet, implying that the hard feeders are capable of larger bite forces. Next to this, soft feeders develop a sharper and narrower head, which could reduce hydrodynamic drag, allowing more rapid strikes towards their prey. Both phenotypes were found in a control group, which were given a combination of both diets. These phenotypes were, however, not as extreme as the hard or the soft feeding group, indicating that some specimens are more likely to consume hard prey and others soft prey, but that they do not selectively eat one of both diets. In conclusion, we found that diet is a major factor influencing head shape in European eel and this ability to specialize in feeding on hard or soft prey could decrease intra-specific competition in European eel populations. Highlighted Article: Diet differences lead to head shape dimorphism in European eel; this occurs at a much earlier stage than was originally thought.

Functional Morphology of the Feeding Apparatus in Simenchelys parasitica (Simenchelyinae: Synaphobranchidae), an Alleged Parasitic Eel

The Pugnose Eel, Simenchelys parasitica (family Synaphobranchidae, subfamily Simenchelyinae), is a deep-water species described as both being a parasite and a scavenger that can bite off large chunks of flesh. Little, however, is known about its cranial morphology, including to what degree its feeding apparatus is modified to allow feeding specializations. We provide a detailed description of the cranial morphology of S. parasitica, comparing it with that of more closely related synaphobranchid species, for which no parasitic behavior has been reported, i.e., Ilyophis brunneus (Ilyophinae) and Synaphobranchus brevidorsalis (Synaphobranchinae). Pugnose Eels have stretchable skin around a small, terminal mouth, as well as teeth with a clear cutting edge, a mouth-closing apparatus equipped with large jaw muscles, a large tongue-like secretory structure, and well-developed hyoid and branchial arches to facilitate the transport of large food items in the buccal cavity. A comparison with other species provides several lines of evidence supporting the hypothesis that Pugnose Eels have a feeding apparatus that is equipped for biting off chunks of flesh from prey (irrespective of whether prey is dead or alive), most likely by using rotational feeding.

Broader head, stronger bite : in vivo bite forces in European eel Anguilla anguilla

This work examined three different phenotypes of the yellow-eel stage of the European eel Anguilla anguilla, broad-heads, narrow-heads and eels with an intermediate head shape. The aim was to see whether broad-headed A. anguilla, which generally consume harder, larger prey, such as crustaceans and fish, exerted greater bite force than the narrow-headed variant, which mainly consume soft, small prey such as chironomid larvae. It was found that in 99 yellow A. anguilla, in vivo bite force of broad-heads are higher compared with narrow-heads and intermediates.

Ontogenesis of opercular deformities in gilthead sea bream Sparus aurata : a histological description: opercular deformities in sparus aurata

The aim of this study was to characterize histological changes during opercular osteogenesis in farmed gilthead sea bream Sparus aurata larvae from 7 to 69 days post hatching (dph) and compare normal osteogenesis with that of deformed opercles. Mild opercular deformities were first detected in 19 dph larvae by folding of the opercles distal edge into the gill chamber. Here, the variation in the phenotype and the irregular bone structure at the curled part of the opercles is described and compared with the histology of normal opercles. Results indicated that deformed opercles still undergo bone growth with the addition of new matrix by osteoblasts at the opercular surface, especially at its edges. No significant difference was found in bone thickness between deformed and normal opercles. In addition to differences in bone architecture, differences in collagen fibre thickness between normal and deformed opercles were also found.

Diet-induced phenotypic plasticity in head morphology in European eel elvers (Anguilla anguilla): the effects of hard vs soft food

By bone remodeling and changing of muscle volume, fish can adapt to changes in mechanical loads they are confronted with, including dietary changes such as prey hardness. This capability of a genotype to develop different phenotypes in response to varying environment is known as phenotypic plasticity. Differences in prey type being consumed might trigger such a phenotypic plasticity in fish. In European eel, two morphotypes exist: broadheads and narrowheads. Studies based on gut content have shown that broadheads consume larger and harder prey, such as fish, whereas narrowheads feed on smaller prey, such as benthic invertebrates. These studies, however, are performed on yellow eels with a minimum length of 30 cm, and only provide indirect evidence that head shape is affected by diet differences. Here, we performed a feeding experiment on glass eels that just swam up the European rivers to start feeding. These glass eels were captured and separated in three groups: one group was given hard feed requiring biting, the second group got soft feed that could be sucked in and the final group, which acted as a control group, was given a mixture of both. We found that hard feeders developed a broader general head width and postorbital region than soft feeders. This region is associated with the location of the jaw muscles, indicating that hard feeders develop larger muscles to cope with the harder prey. Hard feeders, however, also grew more slowly than soft feeders, suggesting that net energy uptake of hard feeders was lower as prey handling required more energy and time. Specimens of the control group, finally, developed intermediate head widths, implying that they are not fully adapted to feed on either hard or soft prey. In conclusion, this study provides the first direct evidence that diet influences the head shape of European eel.