Mechanisms of the jaws of some atheriniform fish

The Atheriniformes is an order of teleost fish which consists of the Atherinoidei (sand smelts etc.), Cyprinodontoidei (tooth-carps) and Exocoetoidei (halfbeaks etc.). Some of its members have protrusible upper jaws and some do not. Photographs have been taken of two species of Cyprinodontoidei feeding, to discover how they use their jaws, which are protrusible. The anatomy and mechanisms of the jaws of these and of various other Atheriniformes have been studied. The terminology of the kinematics of machines is used in a general discussion of the mechanisms of teleost jaws. Anatomical similarities between the jaws of Acanthopterygii, Cyprinoidei and Atheriniformes are noted and discussed.     

A comparison of the mouth morphology of three co-occurring species of atherinid

The mouth morphology of three species of atherinids, which feed at different levels in the water column (benthos, plankton and water surface) were compared. These three species, which all grow to less than 100 mm in length, inhabit the shallows (<2m) of Wilson Inlet, a temperate south-western Australian estuary. The species could be distinguished primarily on the basis of the extent to which they can protrude their jaws. Thus, whereas Leptatherina presbyteroides feeds highest in the water column, including at the water surface on terrestrial insects, and has the most protrusible jaws, Atherinosonia elongata feeds predominantly at or near the benthos and has the least protrusible jaws. Leptatherina wallacei , which ingests prey from the plankton and near the benthos, is intermediate in the degree to which it can protrude its jaws. Other characters of the three species which are associated with feeding, such as the number of gill rakers and the size of teeth, show consistent trends with the degree of jaw protrusion in relation to the type of prey consumed.     

A forceful upper jaw facilitates picking-based prey capture: biomechanics of feeding in a butterflyfish,Chaetodon trichrous

Biomechanical models of feeding mechanisms elucidate how animals capture food in the wild, which, in turn, expands our understanding of their fundamental trophic niche. However, little attention has been given to modeling the protrusible upper jaw apparatus that characterizes many teleost species. We expanded existing biomechanical models to include upper jaw forces using a generalist butterflyfish, Chaetodon trichrous (Chaetodontidae) that produces substantial upper jaw protrusion when feeding on midwater and benthic prey. Laboratory feeding trials for C. trichrous were recorded using high-speed digital imaging; from these sequences we quantified feeding performance parameters to use as inputs for the biomechanical model. According to the model outputs, the upper jaw makes a substantial contribution to the overall forces produced during mouth closing in C. trichrous. Thus, biomechanical models that only consider lower jaw closing forces will underestimate total bite force for this and likely other teleost species. We also quantified and subsequently modeled feeding events for C. trichrous consuming prey from the water column versus picking attached prey from the substrate to investigate whether there is a functional trade-off between prey capture modes. We found that individuals of C. trichrous alter their feeding behavior when consuming different prey types by changing the timing and magnitude of upper and lower jaw movements and that this behavioral modification will affect the forces produced by the jaws during prey capture by dynamically altering the lever mechanics of the jaws. In fact, the slower, lower magnitude movements produced during picking-based prey capture should produce a more forceful bite, which will facilitate feeding on benthic attached prey items, such as corals. Similarities between butterflyfishes and other teleost lineages that also employ picking-based prey capture suggest that a suite of key behavioral and morphological innovations enhances feeding success for benthic attached prey items.     

Ontogeny of the jaw apparatus and suspensorium of the Tetraodontiformes

Konstantinidis, P. and Johnson, G. David 2012. Ontogeny of the jaw apparatus and suspensorium of the Tetraodontiformes. —Acta Zoologica (Stockholm) 93 : 351–366. The jaw apparatus and suspensorium of adult Tetraodontiformes are well adapted to a durophagous feeding habit. Anatomical indicators are the short, stout jaws and a suspensorium in which the quadrate lies in the same vertical plane as the autopalatine. In contrast, the palatoquadrate of larval Tetraodontiformes generally resembles that of larval percomorphs – a more posteriorly positioned quadrate and a slender and long Meckelian cartilage. Among Tetraodontiformes, the Triacanthodidae retain a protrusible upper jaw and a versatile suspensorium. The jaws of the Balistoidei have greater mobility achieved by a reduced autopalatine that has lost its bony contact with the suspensorium. In contrast to the Balistoidei, the beak‐like jaws of the Tetraodontoidei lack individual teeth in the biting part of the jaws. The autopalatine is enlarged, which results in immobilization of the ethmopalatine articulation. The Ostraciidae are exceptional in having the distal part of the autopalatine reduced, while the proximal part remains attached to the suspensorium.     

A catalogue of skulls and jaws of eastern tropical Pacific blennioid fishes (Blennioidei: Teleostei): A proposed evolutionary sequence of morphological change

Skulls and jaws are compared in 35 species of tropical eastern Pacific (mainly Gulf of California) blennioid fishes (5 species of Tripterygiidae, 13 Labrisomidae, 12 Chaenopsidae, 5 Blenniidae). Morphotypes are arranged in a series from relatively large-mouthed fishes (tripterygiids and a few labrisomids) with protrusible jaws and conical teeth to species with small, non-protrusible jaws and a single row of incisiform teeth. This polarity of arrangement probably reflects the direction of phylogenetic development, as suggested by outgroup comparison with other perciform fishes. Distribution patterns of morphotypes in a simple morphospace, obtained by combining dentition, shape of the jaw arch and jaw protrusibility, are discussed within an adaptive context.     

Trophic ecomorphology in eastern Pacific blennioid fishes: character transformation of oral jaws and associated change of their biological roles

Synopsis The ecomorphological relationships between the oral jaws and food spectra were highlighted in 34 species of Gulf of California blennioid fishes (5 Tripterygiidae, 13 Labrisomidae, 11 Chaenopsidae and 5 Blenniidae). Twenty-nine species are microcarnivorous, two are omnivorous browsers, two are algae grazers and one was an ‘ectoparasite’ feeder. The spectrum of oral (as opposed to pharyngeal) jaw (OJA) morphology ranges from plesiomorphic, suction-feeding (relatively large, protrusible jaws, with many coniform-caniniform teeth) to apomorphic, biting (relatively small, non protrusible jaws, with a single row of incisiform teeth). As species with similar morphology may widely differ in food, it is concluded, that morphology is not a reliable predictor for ecology in this case. With the exception of a few specialists, species with apomorphic, biting OJA utilize sessile items in addition to mobile categories and thus show a higher food diversity as compared to species with plesiomorphic OJA. Thus in the present case morphological differentiation goes along with ecological generalization. Only three blenniid species with the most apomorphic OJA may be considered as specialized also with regard to food resource utilization. Transformation of morphological characters and the ecological role of the OJA of blennioids may serve as a model to illustrate the steps required to achieve a biting-browsing and grazing feeding apparatus in many taxa of modern acanthopterygian reef fishes.     

It's a family matter: molecular phylogenetics of Atheriniformes and the polyphyly of the surf silversides (family: Notocheiridae)

Phylogenetic relationships among families of Atheriniformes have long been problematic. The affinities of one of the most enigmatic lineages, surf silversides (Notocheiridae), have proven particularly elusive due to this taxon's unique morphology and rarity in museum collections. In this study, we use mitochondrial and nuclear sequence data to generate a phylogeny for seven of the eight families of Atheriniformes. Our results reveal that four families within Atheriniformes (Atherinopsidae, Notocheiridae, Atherinidae, Melanotaeniidae) are not monophyletic. Most notably, Notocheiridae is polyphyletic, with Notocheirus hubbsi nested within New World silversides (Atherinopsidae), while members of Iso are sister to all other Old World Atheriniforms. These data suggest that the unique morphology of Notocheirus and Iso is a result of adaptive convergent evolution to the high-energy surf habitat where these species live.     

Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea)

Protrusion of the jaws during feeding is common in Batoidea (rays, skates, sawfishes, and guitarfishes), members of which possess a highly modified jaw suspension. The lesser electric ray, Narcine brasiliensis, preys primarily on polychaete annelids using a peculiar and highly derived mechanism for jaw protraction. The ray captures its prey by protruding its jaws beneath the substrate and generating subambient buccal pressure to suck worms into its mouth. Initiation of this protrusion is similar to that proposed for other batoids, in that the swing of the distal ends of the hyomandibulae is transmitted to Meckel's cartilage. A "scissor-jack" model of jaw protrusion is proposed for Narcine, in which the coupling of the upper and lower jaws, and extremely flexible symphyses, allow medial compression of the entire jaw complex. This results in a shortening of the distance between the right and left sides of the jaw arch and ventral extension of the jaws. Motion of the skeletal elements involved in this extreme jaw protrusion is convergent with that described for the wobbegong shark, Orectolobus maculatus. Narcine also exhibits asymmetrical protrusion of the jaws from the midline during processing, accomplished by unequal depression of the hyomandibulae. Lower jaw versatility is a functional motif in the batoid feeding mechanism. The pronounced jaw kinesis of N. brasiliensis is partly a function of common batoid characteristics: euhyostylic jaw suspension (decoupling the jaws from the hyoid arch) and complex and subdivided cranial musculature, affording fine motor control. However, this mechanism would not be possible without the loss of the basihyal in narcinid electric rays. The highly protrusible jaw of N. brasiliensis is a versatile and maneuverable feeding apparatus well-suited for the animal's benthic feeding lifestyle.     

Development of the cypriniform protrusible jaw complex in Danio rerio: Constructional insights for evolution

Studies on the evolution of complex biological systems are difficult because the construction of these traits cannot be observed during the course of evolution. Complex traits are defined as consisting of multiple elements, often of differing embryological origins, with multiple linkages integrated to form a single functional unit. An example of a complex system is the cypriniform oral jaw apparatus. Cypriniform fishes possess an upper jaw characterized by premaxillary protrusion during feeding. Cypriniforms effect protrusion via the kinethmoid, a synapomorphy for the order. The kinethmoid is a sesamoid ossification suspended by ligaments attaching to the premaxillae, maxillae, palatines, and neurocranium. Upon mouth opening, the kinethmoid rotates as the premaxillae move anteriorly. Along with bony and ligamentous elements, there are three divisions of the adductor mandibulae that render this system functional. It is unclear how cypriniform jaws evolved because although the evolution of sesamoid elements is common, the incorporation of the kinethmoid into the protrusible jaw results in a function that is atypical for sesamoids. Developmental studies can show how biological systems are assembled within individuals and offer clues about how traits might have been constructed during evolution. We investigated the development of the protrusible upper jaw in zebrafish to generate hypotheses regarding the evolution of this character. Early in development, the adductor mandibulae arises as a single unit. The muscle divides after ossification of the maxillae, on which the A1 division will ultimately insert. A cartilaginous kinethmoid first develops within the intermaxillary ligament; it later ossifies at points of ligamentous attachment. We combine our structural developmental data with published kinematic data at key developmental stages and discuss potential functional advantages in possessing even the earliest stages of a system for protrusion. J. Morphol. 2010. © 2010 Wiley‐Liss, Inc.     

Trophic apparatus in cyprinodontiform fishes: Functional specializations for picking and scraping behaviors

Cyprinodontiforms are a diverse and speciose order that includes topminnows, pupfishes, swordtails, mosquitofishes, guppies, and mollies. Sister group to the Beloniformes and Atheriniformes, Cyprinodontiformes contains approximately twice the number of species of these other two orders combined. Recent studies suggest that this group is well suited to capturing prey by “picking” small items from the water surface, water column, and the substrate. Because picking places unusual performance demands on the feeding apparatus, this mode of prey capture may rely upon novel morphological modifications not found in more widespread ram‐ or suction‐based feeding mechanisms. To assess this evolutionary hypothesis, we describe the trophic anatomy of 16 cyprinodontiform species, selected to broadly represent the order as well as capture intrageneric variation. The group appears to have undergone gradual morphological changes to become increasingly specialized for picking and scraping behaviors. We also identify a suite of functional characters related to the acquisition of a novel and previously undescribed mechanism of premaxillary protrusion and retraction, including: modification of the “premaxillomandibular” ligament (which connects each side of the premaxilla to the ipsilateral mandible, or lower jaw), a novel architecture of the ligaments and bony elements that unite the premaxillae, maxillae and palatine bones, and novel insertions of the adductor muscles onto the jaws. These morphological changes to both the upper and lower jaws suggest an evolutionary trend within this group toward increased reliance on picking individual prey from the water column/substrate or for scraping encrusting material from the substrate. We propose that the suite of morphological characters described here enable a functional innovation, “picking,” which leads to novel trophic habits. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Adaptation in the jaws of flatfish (Pleuronectiformes)

The structure and mechanisms of the jaws of 18 species of flatfish have been investigated. Clear adaptations to different modes of feeding were found. The mechanisms of the jaws of Soleidae, Cynoglossidae, and Rhombosoleinae are highly specialized and the representatives of the two latter groups have some interesting jaw muscles of doubtful homology.     

Osteoclasts in teleost fish: Light-and electron-microscopical observations

Summary This paper reports the common occurrence of osteoclasts during normal and experimental bone resorption in a number of teleost fishes. Light-microscopical observations on osteoclasts are presented in resorption areas on perichondral bone (mandibula and pharyngeal jaws of cichlids and vertebrae of gymnotids), on dermal bone (mandibula of salmonids and characoids and frontal bone of cichlids), on chondroid bone (pharyngeal jaws of cichlids), and on elasmoid body scales (eichlids and gymnotids). Osteoclasts acting along the bone surface usually lie in a Howship's lacuna whereas others are wrapped around bone extremities. Electronmicroscopical observations reveal that teleost osteoclasts show features similar to those of higher vertebrate osteoclasts, c.g., the presence of a ruffled border and the occurrence of numerous vacuoles, lysosomes and mitochondria. The multinucleated aspect that characterizes osteoclasts in other vertebrate groups is not a distinct feature of teleost osteoclasts since some are possibly mononucleated. Teleost osteoclasts are also able to resorb uncalcified tissues adjoining bone resorption areas, either as a primary process directed toward the tissue (basal plate of elasmoid scale) or as a secondary phenomenon (cartilage).     

A Systematic Survey of the Occurrence of the Hypothalamic Saccus Vasculosus in Teleost Fish

The saccus vasculosus (SV) was examined histologically in more than 200 species of teleosts. The Atherinomorpha (Cyprinodontiformes and Atheriniformes) completely lack the SV. Many primary freshwater teleosts (Osteoglossiformes, Cypriniformes, Characiformes, Siluriformes, Gymnotiformes, and Synbranchiformes) possess none or a reduced SV. Some secondary freshwater teleosts also possess a reduced SV, but other secondary freshwater teleosts have a well-developed SV. Some marine teleosts swimming in the surface water, for example, the Clupeiformes and Scombridae, possess a somewhat reduced SV. Bathypelagic teleosts also possess a rather reduced SV. On the other hand, most marine teleosts, benthic or nektonic in the subsurface water, have a well-developed SV. The examples are the Anguilliformes, Scorpaeniformes, Perciformes, Pleuronectiformes, and Tetraodontiformes. Since all non-teleostean actinopterygians possess a well-deveoped SV, it is assumed that the earliest teleosts also possessed a SV. In the course of adaptive radiation, some teleost groups certainly have reduced or lost the SV while others developed it to various degrees. Reduction or development of the SV might be influenced more easily by environments in certain groups and might be constrained more strongly by phylogenetic lineages in other groups.     

An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws

Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.     

FUNCTIONAL INNOVATIONS AND MORPHOLOGICAL DIVERSIFICATION IN PARROTFISH

The association between diversification and evolutionary innovations has been well documented and tested in studies of taxonomic richness but the impact that such innovations have on the diversity of form and function is less well understood. Using phylogenetically rigorous techniques, we investigated the association between morphological diversity and two design breakthroughs within the jaws of parrotfish. Similar intramandibular joints and other modifications of the pharyngeal jaws have evolved repeatedly in teleost fish and are frequently hypothesized to promote diversity. We quantified morphological diversity within six functionally important oral jaw traits using the Brownian motion rate of evolution to correct for phylogenetic and time‐related biases and compared these rates across clades that did and did not possess the intramandibular joint and the parrotfish pharyngeal jaw. No change in morphological diversity was associated with the pharyngeal jaw modification alone but rates of oral jaw diversification were up to 8× faster in parrotfish species that possessed both innovations. Interestingly, this morphological diversity may not have led to differential resource uses as available data suggest that members of this clade show remarkable homogeneity of diet.     

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.     

Influence of Trophic Relations on Form and Behavior Among Fishes and Benthic Invertebrates in Some California Marine Communities

Study of interactions among fishes and benthic invertebrates off southern California's Santa Catalina Island showed the great extent to which taxa are defined by trophic relations. The dominant fishes there are acanthopterygian teleosts, with the serranine serranid Paralabrax clathratus morphologically nearest the evolutionary mainstream. Because mainstream species have morphologies similar to their progenitors, marine communities have a long history of adaptations to threats from generalized predators like P. clathratus. Species examined at Santa Catalina indicate this experience has produced four basic defenses: smallness, which presents difficulties for predators with large and simply constructed feeding mechanisms; dissemblance, as through camouflage, which makes detection by visual hunters difficult; inedibility, which is attained by incorporating materials that an unspecialized digestive system cannot accommodate; and nocturnality, which results in avoiding diurnal predators altogether. Examination of trophic relations among the major fishes in Santa Catalina communities shows each with specialized ways to counter these defenses. Prey smallness has been met by reducing size of mouth relative to size of prey, either by evolving as smaller fishes or through structural changes in head and jaws. Prey dissemblance has been accommodated through enhanced visual acuity and varied means to remain an unrecognized threat while waiting for prey to move. Inedibility has been countered by developing specialized features of the alimentary tract, including dentition, while adjustments to nocturnality have included enhanced sensory capabilities that detect prey in low light. These adaptations to prey defenses define varied lines of divergence from the teleost mainstream as represented atbreak Santa Catalina.     

Functional morphology of the feeding system in the ruff — Gymnocephalus cernua (L. 1758) — (Teleostei,Percidae)

The ruff, Gymnocephalus cernua, is a European freshwater fish that feeds by sucking up small invertebrates from the bottom of ponds and slow flowing rivers. The feeding movements have been studied by simultaneous electromyography of seventeen muscles of the head and cinematographic techniques. A theoretical model of movements imposes the functional demands of suction upon an abstraction of the form of a teleost head. Three phases in the feeding act, a preparatory phase, a suction phase and a transport phase, could be correlated with the observed movements and EMGs. Differences between the predicted and the actual movement are discussed. Two different types of feeding occur. The direction, magnitude and duration of the suction forces during feeding are modified, according to the position of the prey. A mechanism preventing early mandibular depression allows sudden and strong suction. Retardation of the suspensorial abduction during the overall expansion of the buccal cavity is ascribed to kinetic interrelations with the hyoid arch. Protrusion of the upper jaws also permits an earlier closure of the mouth and directs the food-containing waterflow posteriorly. When the fish is feeding on sinking prey, protrusion occurs later in the sequence of movements than when it is feeding from the bottom. As the protruded jaws produce a downwardly pointed mouth this retardation aims the suction force.     

Epural bones in teleost fishes: a problem of phylogenetic homology

Ichthyological Research - In the past, epural bones of teleost fishes have been labeled sequentially from anterior to posterior (e.g., epural 1, epural 2, etc.) without regard to their position...     

The oldest Gondwanan cephalopod mandibles (Hangenberg Black Shale,Late Devonian) and the mid‐Palaeozoic rise of jaws

It is widely accepted that the effects of global sea‐level changes at the transition from the Devonian to the Carboniferous are recorded in deposits on the shelf of northern Gondwana. These latest Devonian strata had been thought to be poor in fossils due to the Hangenberg mass extinction. In the Ma'der (eastern Anti‐Atlas), however, the Hangenberg Black Shale claystones (latest Famennian) are rich in exceptionally preserved fossils displaying the remains of non‐mineralized structures. The diversity in animal species of these strata is, however, low. Remarkably, the organic‐rich claystones have yielded abundant remains of Ammonoidea preserved with their jaws, both in situ and isolated. This is important because previously, the jaws of only one of the main Devonian ammonoid clades had been found (Frasnian Gephuroceratina). Here, we describe four types of jaws of which two could be assigned confidently to the Order Clymeniida and to the Suborder Tornoceratina. These findings imply that chitinous normal‐type jaws were likely to have already been present at the origin of the whole clade Ammonoidea, i.e. in the early Emsian (or earlier). Vertebrate jaws evolved prior to the Early Devonian origin of ammonoids. The temporal succession of evolutionary events suggests that it could have been the indirect positive selection pressure towards strong (and thus preservable) jaws since defensive structures of potential prey animals would otherwise have made them inaccessible to jawless predators in the course of the mid‐Palaeozoic marine revolution. In this respect, our findings reflect the macroecological changes that occurred in the Devonian. [Correction added on 28 July 2016 after first online publication: In the Abstract, the sentence “Vertebrate jaws probably … in the Early Devonian” was amended]