Topic: Durophagy (hard prey-eating) in fish
Plenty of animals have an extraordinary capacity to crush hard prey and this has evolved independently many times in the vertebrates. If you suspect it is a durophage, watch your fingers!
One of the minor distresses of life is to bite unexpectedly on a small stone, say lurking amongst the lentils. Surprising, sometimes costly, as the dentist will tell you. But plenty of animals, whilst certainly not chewing stones, have an extraordinary capacity to crush hard prey and this has evolved independently many times in the vertebrates. Here we will look at the fish.
Durophagous fish are able to take advantage of a food source that, because it is encased in protective armour, is not readily available to other fish. To achieve this they use a suite of morphological and functional adaptations that enable them to exert the large forces needed to break open animals such as crabs, mussels and sea urchins. These features may include strong, flattened (molariform) teeth, robust jaws and enlarged jaw adductor muscles, but the functional patterns and modifications in dental and jaw morphology vary between different durophagous taxa.
Durophagy has evolved several times in the chondrichthyans, the group of “primitive” cartilaginous fish that includes elasmobranchs (sharks, rays and skates) and the rather poorly known holocephalans (chimaeras or ratfish). This is a particularly intriguing achievement as these fish lack bone and thus need to crush prey that it significantly harder than their jaws. Or as Henry Gee put it: “Crushing clams with cartilaginous jaws is like trying to fell a tree with a sock full of custard.” (in: Summers 2000, Journal of Morphology, vol. 243, pp. 113-126) So how do they do it?
Eagle rays (Myliobatidae)
The widely distributed myliobatids are the cartilaginous masters of durophagy. Five of the seven genera in the family have specialised on hard prey (Rhinoptera, Myliobatis, Pteromylaeus, Aetomylaeus and Aetobatus), whereas the other two (Manta and Mobula) feed on plankton. It is generally assumed that durophagy evolved at the base of the
myliobatid clade and has been lost in the planktivores.
While the typical ray jaw is particularly poorly designed for crushing, with its left and right sides not well joined and small, sharply pointed teeth, the durophagous rays have evolved several morphological novelties enabling them to grind hard prey: They possess hard, flat, usually hexagonal pavement teeth that interlock to form continuous tooth plates, which flex relative to one another during crushing. Their cartilaginous jaws are strengthened by calcification, calcified struts (trabeculae) and fusion of the palatoquadrate and mandibular symphyses. Strong ligaments connect upper and lower jaw, restricting the gape. Similar to a nutcracker, this lever system acts to amplify the force of the jaw adductor muscles, which are asynchronously activated.
Cownose rays (Rhinoptera bonasus) are of particular interest, because their jaw ligaments show striking morphological and ultrastructural convergent similarities to some of the tendons found in mammals. When feeding, the cownose ray evidently blows water into the sediment and sucks its prey into its mouth, where it is then crushed between the tooth plates. Essential for prey excavation and handling are the cephalic lobes, modified extensions of the pectoral fins, which are highly sensitive (including tactility). Their use is somewhat reminiscent of how dugongs manipulate food with their facial bristles.
Bullhead sharks (Heterodontidae)
The heterodontids are the only elasmobranch family, in which every species shows ecological and functional adaptations for durophagy. Best studied is the horn shark (Heterodontus francisci). Here we see very robust and powerful, mineralised jaws and enlarged jaw adductor muscles, but unlike the eagle rays, the two sides of the jaw are not solidly fused. Furthermore, the dentition is less specialised, as only the teeth at the back of the mouth are molariform and used for crushing, while the cuspidate teeth at the front are employed for grasping. After capturing its prey, the horn shark applies several processing bites to reduce it before swallowing, with the greatest bite force probably generated in the region of the molariform teeth.
Bonnethead shark (Sphyrna tiburo)
Unlike the other hammerhead sharks (Sphyrnidae), which capture fish with rows of sharp teeth, the bonnethead is a specialised crab-eater that possesses molariform teeth at the back of the mouth. Its crushing mechanism is quite similar to that of the heterodontid sharks, although the jaws are not particularly robust and the upper jaw is firmly connected with the cranium, so reducing its mobility. Prey is captured by ram feeding, then processed by crushing it between the molariform teeth and finally swallowed by suction. During processing, the jaw adductor muscles show prolonged activity and jaw kinematics is modified in such a way that biting does not cease at jaw closure but continues well afterwards (so there is a second jaw-closing phase), thus distinguishing prey crushing from simple bite capture. While this mechanism allows for specialisation on crabs, it seems to limit the bonnethead’s ability to alter its feeding behaviour when occasionally taking other prey.
Not much is known about this enigmatic group of cartilaginous fish, also referred to as ratfish. Their dietary habits remain largely elusive, but the possession of fused symphyses and massive hypermineralised, pavement-like tooth plates suggests that they specialise on hard prey. The largest tooth plates were found in some fossil chimaeroids (e.g. Edaphodon and Ischyodus), indicating these extinct ratfish might have consumed larger and harder prey than their extant relatives. However, holocephalan jaws are only poorly mineralised and their jaw adductor muscles not particularly large, implying a feeding mechanism different from that used by elasmobranchs.
Support for this notion comes from an analysis of the feeding biomechanics of the reasonably well-studied spotted ratfish (Hydrolagus colliei). This holocephalan, which mainly eats hard prey (particularly gastropod molluscs), can generate mass-specific bite forces similar to those of durophagous elasmobranchs. In fact, its jaw leverage is the highest of all cartilaginous fishes studied so far. This high-performance crushing capability seems to be accomplished by mechanically advantageous geometries of the feeding mechanism. Stabilisation against dorsoventral flexion is probably achieved by a vaulted cranial region to which the upper jaw is fused, while the expanded tooth plates distribute the forces equally across the jaw surface.
In addition to these derived crushing mechanisms in cartilaginous fish, more ancestral, less specialised ones are found in smoothhound sharks (Mustelus spp.) in the family Triakidae, the zebra shark (Stegostoma fasciatum) and some skates and guitarfish (such as Raja spp. and Rhinobatos spp.). They are less well studied, but likely to involve slightly modified teeth and alterations in the motor pattern of the jaw muscles.
Durophagy has also evolved independently several times amongst the teleosts. Here are some examples:
The Pycnodontiformes, an extinct order of bony fish that evolved during the Late Triassic and lasted for more than 150 million years, are often considered to be the top durophages among the bony fish, rivalled only by the most derived extant species. They had specialised jaws with flattened, round teeth that were well suited to crush hard-bodied prey. Pycnodont dentition is furthermore interesting because of two chisel-shaped front teeth that are, together with similar tooth forms in extant fish (e.g. in Xyrichthys razorfish and the red porgy Pagrus pagrus), structurally and functionally analogous to the sharp beaks of some reptiles and the incisors of mammals, mammal-like reptiles and even some theropod-like dinosaurs.
Fish in the order Tetraodontiformes, a highly derived group that includes pufferfish (famous for the fugu and its lethal dose of the toxin tetrodotoxin), triggerfish and boxfish, show a variety of feeding mechanisms, but durophagy is the dominant one. The jaws of durophagous tetraodontiforms are specialised for powerful biting and, unusually, it is the oral teeth that serve as the crushers. The mechanism of crushing prey in the oral jaws has been studied most extensively in the queen triggerfish (Balistes vetula). It possesses long, sharp, strong teeth on short, robust jawbones and the upper jaw is tightly connected with the cranium, which reduces its mobility. The jaw adductor muscles are greatly enlarged and active for longer when feeding on hard compared with soft prey. Fish in the family Sparidae, such as porgies and the Atlantic sheepshead (Archosargus probatocephalus), also use their oral teeth as crushers.
A number of durophagous teleosts have modified their pharyngeal jaws as crushing tooth plates. Hard prey is usually transported hydraulically to these tooth plates, where it is then crushed with the aid of enlarged pharyngeal muscles (as in bonnethead sharks). This method of feeding has arisen several times and is found in the Haemulidae (including the black margate Anisotremus surinamensis), the Sciaenidae (including the black drum Pogonias cromis) and the Carangidae (including the African pompano Alectis ciliaris). Amongst these, the convergences between the last two groups are particularly noticeable. A fourth independent employment of durophagy is found in the freshwater cichlids, notably in the Neotropical heroines, where the ability to crush molluscs may have evolved several times.
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Map of Life - "Durophagy (hard prey-eating) in fish"
April 3, 2020