Development and diversity of the suspensorium of trichomycterids and comparison with loricarioids (Teleostei: Siluriformes)

Studies of ontogenetic series of trichomycterids and other catfishes reveal that the suspensorium of siluroids is highly specialized; several synapomorphies separate siluroids from other teleosts. In siluroids, the palatoquadrate is divided into pars autopalatina and pars pterygoquadrata and both are usually connected by the autopaiatine-metapterygoid ligament. The pterygoquadrate is broadly joined to the dorsal limb of the hyoid arch, forming a cartilaginous hyomandibular-symplectic-pterygoquadrate plate in early ontogeny. This produces a special alignment of the hyomandibula and quadrate which is characteristic of siluroids. A symplectic bone is absent. The interhyal is absent in trichomycterids and astroblepids. Dorsal and ventral limbs of the hyoid arch are connected by a ligament. A rudimentary interhyal and this ligament are present in primitive siluroids such as diplomystids and nematogenyids as well as loricariids. The metapterygoid arises as an anterior ossification of the pars pterygoquadrata in siluroids. The formation and position of the metapterygoid exhibit two patterns: (1) the metapterygoid develops as an ossification of a cartilaginous projection positioned between the future hyomandibula and quadrate in primitive catfishes (e.g., Diplomystes) as well as in Nematogenys, callichthyids, loricariids, and astroblepids; (2) the metapterygoid arises as an ossification of the cartilaginous projection (pterygoid process) positioned just above the articular facet of the quadrate for the lower jaw. An ossified anterior chondral pterygoid process of the complex quadrate is present in trichomycterids, whereas the process is absent (simple quadrate) in catfishes such as diplomystids, nematogenyids, callichthyids, and loricariids. The anterior membranous process of the quadrate of Astroblepus is non-homologous with the chondral pterygoid process of trichomycterids; both structures arose independently within the loricarioids. Despite topological relationships, the origin and development of bones reveal the presence of a chondral hyomandibula which develops a large meinbranous outgrowth during ontogeny and a chondral metapterygoid in trichomycterids. The presence of a compound hyomandibula + metapterygoid or a compound metapterygoid + ectopterygoid + entopterygoid have no developmental support in trichomycterines or other siluroids. The “entopterygoid” of Nematogenys and Diplomystes arises as an ossification of a ligament. The dermal entopterygoid of other ostariophysans and the “entopterygoid” are homologous. An ectopterygoid or tendon bone “ectopterygoid” is absent in loricarioids. The suspensorium is an important structural system which has significant evolutionary transformations which characterize loricarioid subgroups; however, no character, of the suspensorium supports the monophyly of the loricarioids.     

Ontogeny of the chondrocranium in Corydoras aeneus (Gill, 1858) (Callichthyidae, Siluriformes)

Callichthyids take a basal position in the loricarioid evolutionary lineage leading up to an algae scraping feeding mechanism in the loricariid family. Therefore, the study of the morphology and development of a callichthyid representative would contribute to a better knowledge on the differences in cranial morphology and their impact on feeding ecology within this superfamily. Therefore, development in the chondrocranium of Corydoras aeneus was studied based on 22 cleared and stained specimens and 6 series of serial sections. The latter sections were also digitized and used for 3D reconstructions. Development overall follows the typical siluriform trends in chondrocranial development. Even the low complexity of the chondrocranium at hatching fits the trend observed in other siluriforms, although other studies showed loricarioid hatchlings to generally show more complex chondrocrania. In contrast to other catfish, in C. aeneus, the notochord was never found to protrude into the hypophyseal fenestra. In addition, also differing from other siluriforms, a commissura lateralis is present, a state also reported for Ancistrus cf. triradiatus (Geerinckx et al., [2005] J Morphol 266:331-355). The splanchnocranium again has the typical siluriform shape during its ontogeny, with the presence of a compound hyosymplectic-pterygoquadrate plate, although not fused to the neurocranium or interhyal at any time during ontogeny, a state described earlier for Callichthys callichthys (Hoedeman, [1960a] Bull Aquat Biol 1:73-84; Howes and Teugels, [1989] J Zool Lond 219:441-456). The most striking difference found in comparison to other catfishes, however, involves thebranchial basket, which arises as a single element with a further differentiation from the middle arches on in both a rostral and caudal direction.     

Ontogeny of the maxillary barbel muscles in Clarias gariepinus (Siluroidei: Clariidae), with some notes on the palatine-maxillary mechanism

Siluroids are characterized by the presence of a palatine-maxillary mechanism, which enables a controlled mobility of the maxillary barbels. In Clarias gariepinus , the ontogeny of this mechanism is studied and described as well as those muscles related to the maxillary barbel. Two muscles are distinguished: (1) retractor tentaculi , connecting the maxilla to the suspensorium, and (2) extensor tentaculi , running from the ventro-lateral face of the skull to the posterior half of the palatine. These typical catfish muscles are derived from muscles that are present in generalized teleost fishes. The retractor muscle is believed to be derived from the A₃ muscle of the adductor mandibulae complex. The extensor muscle is formed from the anterior fibres of the adductor arcus palatini. The palatine is rod-like in C. gariepinus and articulates with the orbitonasal lamina in larval specimens and with its ossification, the lateral ethmoid, in juvenile and adult specimens. The articulation occurs via a long cartilaginous strip on the dorsal face of the autopalatine, thereby enabling both a rotation and a restricted sliding.     

Comparative trophic morphology in eight species of damselfishes (Pomacentridae)

Damselfishes show significant biodiversity in the coral reefs. To better understand such diversity, an ecomorphological approach was investigated in the trophic morphology of eight species of Pomacentridae (Chromis acares, C. margaritifer, Dascyllus aruanus, D. flavicaudus, Pomacentrus pavo, Plectroglyphidodon johnstonianus, Pl. lacrymatus and Stegastes nigricans) belonging to different trophic guilds (zooplankton, algal, coral polyp feeders and omnivores). Geometric morphometrics were used to quantify size and shape variations in four skeletal units: (1) neurocranium, (2) suspensorium and opercle, (3) mandible and (4) premaxilla. This method allowed us to reveal shape and size differences correlated to functional diversity both within and between trophic guilds. Among zooplanktivores, C. margaritifer, D. aruanus and D. flavicaudus have a high and long supraoccipital crest, short mandibles forming a small mouth and high suspensoria and opercles. These three species can be considered to be suction feeders. In the same guild, C. acares shows opposite characteristics (long and thin mandibles, lengthened neurocranium and suspensorium) and can be considered as a ram feeder. Among herbivores and corallivores, the two species of Plectroglyphidodon and S. nigricans can be considered as grazers. Differences in skeletal shape are mainly related to improving the robustness of some skeletal parts (broad hyomandibular, short and high mandibles). The shapes of P. pavo, which feeds largely on algae, strongly differ from that of the other three grazers exhibiting similar morphological characteristics to C. acares (e.g., long and shallow suspensorium, lengthened neurocranium). This highlights likely differences concerning cutting or scraping method. Finally, no strong correlations exist between size and shapes in the eight studied species. Size difference among species having a very similar shape could be viewed as a factor optimizing resource partitioning.     

Early development of the chondrocranium in Chrysichthys auratus

The inception and development of the cartilaginous cephalis skeleton of Chrysichthys auratus is described from hatching to about 18 days post-hatching. At hatching, no skeletal structure is present. Not until day 3 do clearly delimited cranial primordia become apparent. As in many siluriforms, the neurocranium is platybasic from the start, the suspensorium constitutes, with Meckel's cartilage and the hyoid bar, a single cartilaginous element, and the junction between the front and rear of the neurocranium is complete on day 4. By day 8 the quadratomandibular joint has formed and the tectum posterius has appeared. Cartilage reduction first affects the trabecular bars, then, markedly, the visceral arches. By day 18 the braincase floor has almost disappeared.     

Early development of the chondrocranium in Salmo letnica(Karaman, 1924)(Teleostei: Salmonidae)

The ontogenetic development of the chondrocranium of Ohrid trout Salmo letnica was studied from hatching until 92 days post‐hatching (dph). Most of the samples were in toto trypsin cleared and stained, some specimens were used for serial histological sectioning. The serial histological sections of fish specimens at the age of 92 dph were used for a graphical reconstruction of the cartilaginous neurocranium. A chronological evaluation of the formation of the cartilaginous skull in the early development of S. letnica was performed. In order to investigate to what degree the ontogeny of the Ohrid trout is unique, the results were compared with data of the development of other salmonids, as well as some non‐salmonid teleosts. The development of the cartilaginous structures of the Ohrid trout was found to be similar to that of other salmonids. Most of the cartilage structures of the neurocranium and the viscerocranium are present at the moment of hatching of this species. A fully developed chondrocranium was observed at the age of 92 dph, when the first signs of cartilage resorption could also be observed.     

Ontogenetic shape changes in Pomacentridae (Teleostei,Perciformes) and their relationships with feeding strategies: a geometric morphometric approach

The present study explores the shape changes of cranial structures directly involved in food capturing during growth after reef settlement in two species of Pomacentridae (Dascyllus aruanus and Pomacentrus pavo). Landmark‐based geometric morphometrics were used to study allometric patterns and related shape changes in four skeletal units: neurocranium, suspensorium and opercle, mandible and premaxilla. At settlement, the larvae of both species have a relatively similar morphology, especially with respect to the mandible. Their shapes suggest a feeding mode defined as ram/suction‐feeding. Ontogenetic shape changes show a shift to a suction feeding mode of prey capture. The main transformations involved are an increase in height of the suspensorium and the opercle, an elevation of the supraoccipital crest, a relative shortening of the mandible, and a lengthening of the ascending process of the premaxilla. Shape changes of the mandible in the two studied species also reflect an increase of biting capacities. The high disparity between adult shape results from differences in the rate and in the length of ontogenetic trajectories, from divergence of the ontogenetic trajectories (neurocranium, mandible, and premaxilla) and parallel shifts of the trajectories in the size‐shape space (suspensorium and opercle). In an evolutionary context, allometric heterochronies during ontogeny of different skeletal unit of the head may be considered as a basis for the explanation of the diversity of damselfishes. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 92–105.     

Chondrocranial ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: geometric morphometric and allometric change analysis

Garriga, N. and Llorente, G.A. 2011. Chondrocranial Ontogeny of Pelodytes punctatus (Anura: Pelodytidae). Response to competition: Geometric Morphometric and Allometric Change Analysis. —Acta Zoologica (Stockholm) 93 : 453–464. The chondrocranial development of Pelodytes punctatus is described, from tadpole to froglet, and compared with that of other taxa reported previously, such as species in the Pelobatidae, Pipidae, Ranidae, Hylidae, Bombinatoridae, Leptodactylidae, or Microhylidae families. The comparison leads us to suggest that the ontogeny of the anuran chondrocranium is very conservative, making it difficult to discern phylogenetic or ecologic patterns. Chondrocranial development is also analyzed to quantify shape changes and allometries during ontogeny, using linear and geometric morphometrics. The main shape change observed follows the general pattern of vertebrate postnatal development. The allometric analysis indicates the presence of different functional units in the chondrocranium that could be subjected to different pressures. Finally, tadpoles were raised in two conditions of competition to compare their chondrocranium development. The largest shape differences between the two conditions are located in the anterior region of the cranium and fit the general response to competition stress by increasing growth rate. Comparison of the scaling pattern between Pelodytes and Rana sylvatica and Bufo americanus shows differences, principally in the oral region, that do not fit with the general allometric pattern in larval anurans proposed in previous studies.     

Early development of the skull of Sander lucioperca (L.) (Teleostei: Percidae) relating to growth and mortality

The early osteological development of the skull (chondrocranium and osteocranium) of the pikeperch Sander lucioperca was studied. Specimens were reared at two temperatures, 15·5 and 18·0° C, from hatching until 47 and 43 days after fertilization (DAF), respectively. The skeletal elements characteristic for the different developmental stages were the same at both rearing temperatures, but pikeperch reared at 15·5° C reached the developmental stages later. The formation of the functional complexes, the neurocranium, jaws and suspensorium, branchial basket and hyoid arch, was evaluated chronologically. The focus was on skull development during several functional changes: at hatching, at the shift from endogenous to mixed feeding, the shift to exclusively exogenous feeding and upon reaching the final prey-capture mechanism. Growth in total length differed between fishes reared at the two temperatures, except during a phase of very slow growth from the end of the embryonic stage until the second larval stage. The latter phase, in which most of the bony elements of the viscerocranium started to form, was marked by high mortality. When exogenous feeding began, the growth rates at both temperatures increased distinctly and the first bony elements were formed in the neurocranium. Specimens reared at 18·0° C grew continuously, but those at 15·5° C showed a second period of slow growth and high mortality. Fish reared at 18·0° C reached the successive larval stages distinctly earlier than fish reared at 15·5° C.     

The craniofacial skeleton in anencephalic human fetuses. II. Calvarium.

A detailed study of the calvarium of twelve anencephalic and four normal human fetuses 26 to 40 weeks gestational age using gross dissection, alizarin red S staining, silver nitrate radiography and histology revealed dramatic alterations in the presence, form, location and relationship of the individual bones. In the larger dorsal cranial defects the interparietal portions of the occipital bone were relocated anteriorly to approximate the frontal bone. The occipital components were rotated anterolaterally and inferiorly with lack of fusion of the chondrocranium posterior to the foramen magnum. The squamae of the frontal bone were collapsed horizontally and reduced in size to lie peripheral to the anterior cranial fossa forming most of the orbital roofs. In anencephaly the bones derived from the chondrocranium were not as severely affected morphologically as those derived from the neurocranium. The sutures were narrow and smooth instead of wide and serrated as in the normally developing calvarium. In general the degree of maldevelopment was proportional to the extent of the dorsal cranial defect in anencephaly.     

Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: an example from damselfishes (Pomacentridae)

Background  

Quantitative studies of the variation of disparity during ontogeny exhibited by the radiation of coral reef fishes are lacking. Such studies dealing with the variation of disparity, i.e. the diversity of organic form, over ontogeny could be a first step in detecting evolutionary mechanisms in these fishes. The damselfishes (Pomacentridae) have a bipartite life-cycle, as do the majority of demersal coral reef fishes. During their pelagic dispersion phase, all larvae feed on planktonic prey. On the other hand, juveniles and adults associated with the coral reef environment show a higher diversity of diets. Using geometric morphometrics, we study the ontogenetic dynamic of shape disparity of different head skeletal units (neurocranium, suspensorium and opercle, mandible and premaxilla) in this fish family. We expected that larvae of different species might be relatively similar in shapes. Alternatively, specialization may become notable even in the juvenile and adult phase.     

Development of the nidicolous tadpoles of Eupsophus emiliopugini (Anura: Cycloramphidae) until metamorphosis,with comments on systematic relationships of the species and its endotrophic developmental mode

Vera Candioti, M.F., Nuñez, J.J. and Úbeda, C. 2011. Development of the nidicolous tadpoles of Eupsophus emiliopugini (Anura: Cycloramphidae) until metamorphosis, with comments on systematic relationships of the species and its endotrophic developmental mode. —Acta Zoologica (Stockholm) 92 : 27–45. Species of Eupsophus are unique within Alsodinae in having nidicolous tadpoles. They are characterized by traits typical of generalized exotrophic (e.g., oral disc and spiracular tube) and endotrophic larvae (e.g., scant pigmentation and large hind limbs). The larval morphology and development of E. emiliopugini, including external, buccal, and musculoskeletal features, is described herein. Like the larvae of other alsodines, these larvae have four lingual and four infralabial papillae, quadratoethmoid process, and an m. rectus cervicis with a double insertion. Among the traits exclusive to the genus are: the absence of the pseudopterygoid process and quadrato‐orbital commissure; presence of the m. subarcualis rectus I with two slips; and presence of the m. subarcualis rectus II–IV inserting on Ceratobranchial II. The development and metamorphosis of Eupsophus include some characters that develop later (e.g., degeneration of mouthparts and chondrocranium with minimum calcification), characters that develop earlier (e.g., hind‐limb appearance and jaw and suspensorium ossification), and characters that develop at the same time (e.g., most external features and cranial muscles) than in most exotrophic species. Some distinctive characters (third lower labial ridge absent, general configuration of the hyobranchial skeleton, skeletal development with retention of larval traits) resemble those of other endotrophic species, and the precocious ossification of jaws and suspensorium is shared with several direct‐developing species among recent amphibians.     

Ontogeny of the hyoid musculature in the African catfish, Clarias gariepinus (Burchell, 1822) (Siluroidei: Glariidae)

Three ontogenetic stages of the African catfish Clarias gariepinus have been used to describe and discuss the ontogeny of the hyoid musculature. During ontogeny, an asynchrony in the development of the muscles is observed: the intermandibularis and protractor hyoidei are the first to develop and which bear their insertions, followed by the hyohyoideus inferior and the sternohyoideus. The hyohyoideus abductor and adductor muscles are the last of the hyoid muscles to develop. In the juvenile stage (136.2 mm SL specimen), the intermandibularis is still present. The protractor hyoidei is well developed, as it may play an important role in the opening of the mouth, the elevation of the hyoid bars and, as a typical catfish feature, the displacement of the mandibular barbels. The protractor hyoidei arises as three pairs of muscle bundles (a pars ventralis, a pars lateralis and a pars dorsalis), of which the pars ventralis and the pars lateralis become fused to each other. This fusion gives rise to four different fields of superficial fibres for the manipulation of the mandibular barbels. The pars dorsalis, with its tendinous insertion, may be of more importance for mouth opening and/ or hyoid elevation. The hyohyoid muscle is well differentiated into an inferior, abductor and adductor muscles, acting on the hyoid bars, the branchiostegal rays and the opercular bone.     

Homology and evolution of the opercular series in the loricarioid catfishes (Pisces: Siluroidei)

Aspects of the morphology of the opercular region of siluroids (catfishes) were examined to determine the homologies of the opercular bones of loricarioid catfishes, a diverse monophyletic neotropical group. Homology of the component structures was inferred by examination of three criteria: (1) functional relations to the jaw abduction mechanism of primitive halecostome fishes; (2) positional relations to the bones of the suspensorium and the path of the preopercular laterosensory canal; and (3) pattern of development of the preopercular canal and lateral cheek plates of loricarioid catfishes. The majority of siluroids have lost one or more of the preopercular canal exit branches to the skin surface present in most primitive siluroids. A number of specializations of the canal pathway and components of the opercular series have occurred in loricariids. Trichomycterids have the preopercular canal reduced to a short branch from the pterotic. Callichthyids share the presence of a preopercular canal with primitive siluroids, but have lost the communication of the canal between the preopercle and pterotic bones. Callichthyids and scoloplacids share one additional loss of a preopercle exit. The second of two subopercular elements of astroblepids is homologous with the interhyal. Astroblepids and loricariids have lost one additional preopercle exit, the interoperculo-mandibular ligament and the corresponding biomechanical couple for lower jaw abduction. Loricariids have probably lost the interopercle as well. These derived features of loricariids and astroblepids are viewed as specializations for a particular feeding behaviour: scraping algae and detritus from the substratum.     

Osteology and myology of the cephalic region and pectoral girdle of Plotosus lineatus, with comments on Plotosidae (Teleostei: Siluriformes) autapomorphies

From comparisons of the cephalic and pectoral girdle structures of Plotosus lineatus with those of other plotosid as well as non-plotosid siluriforms, plotosid catfishes can be defined by at least six autapomorphies. These are: (1) the absence of the ventral division of the muscle arrector dorsalis; (2) the double articulation between the neurocranium and the anterior part of the suspensorium; (3) the greatly enlarged utricular otolith, which profoundly inflates the ventral surfaces of both the prootic and the pterotic; (4) the attachment of the muscle extensor tentaculi on the neurocranium lies further anteriorly than its insertion on the autopalatine; (5) the coronoid process of the mandible is linked to the maxillary by means of two thick, long ligaments; (6) the enlarged base of the maxillary barbel.     

Functional morphology of extreme jaw protrusion in Neotropical cichlids

The New World cichlids Petenia splendida and Caquetaia spp. possess extraordinarily protrusible jaws. We investigated the feeding behavior of extreme (here defined as greater than 30% head length) and modest jaw-protruding Neotropical cichlids by comparing feeding kinematics, cranial morphology, and feeding performance. Digital high-speed video (500 fps) of P. splendida, C. spectabile, and Astronotus ocellatus feeding on live guppy prey was analyzed to generate kinematic and performance variables. All three cichlid taxa utilized cranial elevation, lower jaw depression, and rotation of the suspensorium to protrude the jaws during feeding experiments. Extreme anterior jaw protrusion in P. splendida and C. spectabile resulted from augmented lower jaw depression and anterior rotation of the suspensorium. Morphological comparisons among eight cichlid species revealed novel anterior and posterior points of flexion within the suspensorium of P. splendida and Caquetaia spp. The combination of anterior and posterior loosening within the suspensorium in P. splendida and Caquetaia spp. permitted considerable anterior rotation of the suspensorium and contributed to protrusion of the jaws. Petenia splendida and C. spectabile exhibited greater ram distance and higher ram velocities than did A. ocellatus, resulting primarily from increased jaw protrusion. Petenia splendida and C. spectabile exhibited lower suction feeding performance than A. ocellatus, as indicated by lower suction-induced prey movements and velocities. Thus, extreme jaw protrusion in these cichlids may represent an adaptation for capturing elusive prey by enhancing the ram velocity of the predator but does not enhance suction feeding performance.     

Skull ontogeny and modularity in two species of Lagenorhynchus: Morphological and ecological implications

Comparisons of skull shape between closely related species can provide information on the role that phylogeny and function play in cranial evolution. We used 3D‐anatomical landmarks in order to study the skull ontogeny of two closely related species, Lagenorhynchus obscurus and Lagenorhynchus australis , with a total sample of 52 skulls. We found shared trends between species, such as the relative compression of the neurocranium and the enlargement of the rostrum during ontogeny. However, these are common mammalian features, associated with prenatal brain development and sensory capsules. Moreover, we found a posterior displacement of the external nares and infraorbital foramina, and a strong development of the rostrum in an anteroposterior direction. Such trends are associated with the process of telescoping and have been observed in postnatal ontogeny of other odontocetes, suggesting a constraint in the pattern. Interspecific differences related to the deepness of facial region, robustness of the feeding apparatus and rostrum orientation may be related with the specific lifestyles of L. obscurus and L. australis . We also tested the presence of three different modules in the skull (basicranium, neurocranium, rostrum), all of which presented strong integration. Only the rostrum showed a different ontogenetic trajectory between species. Even though we detected directional asymmetry, changes in this feature along ontogeny were not detectable. Because asymmetry may be related to echolocation, our results suggest a functional importance of directional asymmetry from the beginning of postnatal life. J. Morphol. 278:203–214, 2017. © 2016 Wiley Periodicals,Inc.     

Ontogenetic shift in mouth opening mechanisms in a catfish (Clariidae, Siluriformes): a response to increasing functional demands

During ontogeny, larval fish have to deal with increasing nutritional and respiratory demands as they grow. As early ontogeny is characterized by an increasing complexity of moving structural elements composing a fish skull, some constraints will have to be met when developing mechanisms, which enable feeding and respiration, arise at a certain developmental stage. This article focuses on the presence/absence of a possible functional response in mouth opening during ontogeny in Clarias gariepinus. Some reflections are given, based on morphological data, as well as related function-analysis data from the literature. Starting shortly after hatching, a total of up to five different mouth opening mechanisms may become functional. Of these, three may remain functional in the adult. As could be expected, the apparatuses that enable these mechanisms show an increase in complexity, as well as a putative improvement in mouth opening capacity. Initially, two consecutive mechanisms may allow a restricted depression of the lower jaw (both passively and actively). Synchronously, two more mechanisms may arise, which involve the coupling of the hyoid depression to the mouth opening. At about 11 mm SL a fifth mechanism becomes established, better known as the opercular mouth opening mechanism. An overlapping chronology of functionality of the different mechanisms, as well as differences in efficiencies, could be an indication of the absence of a true critical period in C. gariepinus (at least in relation to mouth opening), as well as the possible presence of a shift in feeding type. Finally, the coupling of the chronology of the shift in mouth opening mechanisms and several morphological, behavioral, and physiological changes during ontogeny, related to feeding and respiration, make it possible to distinguish five important phases in the early life history of C. gariepinus.