Athena Review Vol. 5, no. 1
Records of Life: Fossils as Original Sources
10. From Placoderms to bony fish (Osteichthyes)
Placoderms.
Placoderms ("plate-skin", from Greek Plak, "plate" or "tablet", and -derma, "skin") were a class of armored fish that were among the first jawed vertebrates (gnathostomes). They lived in the Early Silurian through Late Devonian periods (443-359 mya). More than 250 genera of placoderms are known, with one genus, Bothriolepis, having nearly 100 species, making Placoderms the most diverse and important of Devonian vertebrates.
Placoderms first appear in the fossil record during the late Llandovery epoch of the early Silurian period (443-433 mya).The first appearance of Silurian placoderm fossils in China show the fishes had already differentiated into the Antiarch and Arthrodire orders, along with other, more primitive groups. Placoderm diversity seems to have originated during the middle Silurian (fig.1).
Fig.1: timeline of Placoderm groups.
Numerous families of placoderms flourished during the Devonian, but became extinct at the end of that period, about 360 million years ago.This extinction may have been due, at least in part, to competition from the bony fish (osteichthyans) and early cartilagenous sharks (chrondichthyes). Placoderms had radiated into a number of body shapes and ecological niches, which were later occupied by other fish lineages after the extinction of the placoderms. It is also thought, however, that they died out as their marine and freshwater environments suffered during massive extinction events at the end of the Devonian, and the start of the early Carboniferous (Mississippian) periods.
The lower jaws of Placoderms likely evolved from the first gill arch of ancestral jawless fishes. Their head and thorax were covered either with fused armored plates, or a mosaic of unfused scales, while the rear part of the body was variably covered or uncovered, depending on the taxa. Their backbone consisted of a cartilaginous notochord (an embryonic feature in higher vertebrates) that persisted throughout life. Their vertebra consisted only of Y-shaped spines, sometimes cartilaginous, located above and below the notochord. Their paired fins and a heterocercal tail suggest that they could swim efficiently (Janvier 1997).
Their body armor was very likely a defense against the giant sea-scorpions that inhabited brackish water environments during this part of the Paleozoic era. It also may have functioned as a kind of exoskeleton, and (as with arthropods and mollusks) as a support for the external organs, supplementing their weak, mainly cartilaginous internal skeleton.
The earliest studies of placoderms were published by Louis Agassiz, in his five pioneering volumes on fossil fishes (1833-1843). Placoderms were then thought to have been shelled jawless fish related to ostracoderms. In the late 1920s, Dr. Erik Stensio of the Swedish Museum of Natural History in Stockholm established more accurate details of placoderm anatomy, and identified them as true jawed fishes; and, as he proposed, related to sharks. With the later discovery of well-preserved placoderm fossils from the Gogo Reef formation in Australia, Stensio's theory of sharks and placoderms as sister groups received considerable support.
This view of the relationship between sharks and placoderms has recently been complicated, however, by the discovery of the Silurian jawed placoderm Entelognathus (Min Zhu et al 2013.) As further described below, the exitence of a jawed placoderm indicates that a group of placoderms were ancestral to all living jawed vertebrates; consequently there is a greater separation between placoderms and ancestral, spiny sharks (acanthodians).
Placoderms do not represent a single descent group; in cladistic terms, they are paraphyletic. Placoderms were also the first vertebrates to have teeth; and the first fish with pelvic fins, the precursor to the lobe fins of acanthostegians, leading, in turn, to the hindlimbs in tetrapods.
Placoderms differ from all other jawed vertebrates in that their nasal capsules were unfused to the rest of the braincase. Furthermore, in 1997, a placoderm fossil from Antarctica was found to contain preserved pigment cells of iridescent silver on the stomach or ventral side, and red on the back or dorsal side. This makes placoderms the oldest vertebrates whose color is at least partly known, and suggests that placoderms may have had color vision.
The main groups of placoderms currently known consist of ten different orders: 1) Arthrodira; 2) Antiarchi; 3) Brindabellaspida; 4) Phyllolepida; 5) Ptyctodontida; 6) Rhenanida; 7) Acanthothoraci; 8) Petalichthyida; 9) Pseudopetalichthyida; and 10) Stensioellida. Of these orders, the affiliations of the last two are considered somewhat problematic, and will not be covered here (Janvier 1997).
Arthrodira.
Arthrodira ("jointed neck") were the most numerous and diverse of the placoderm orders in both their forms and feeding habits, ranging from large predators to bottom feeders. Most arthrodires may have fed on molluscs, crustaceans, and other invertebrates. One of their most diagnostic traits for identification in the fossil
record is a joint between the armor plates of the
head and shoulder or pectoral regions. Early arthrodires, such as the
genus Arctolepis, were well-armored fishes with flattened bodies.
Except for a single genus, all other arthrodires (including Dunkleosteus) lacked teeth, instead using the sharpened edges of a bony
"tooth plate" as a biting surface (the exception, Compagopiscis, had
true teeth in addition to tooth plates). Their eye sockets were
protected by a bony ring, a feature shared by some later diapsids,
including birds.Fig.2: Dunklelosteus (reconstruction).
The largest member of the placoderm order Arthrodira was Dunkleosteus, who grew from 3 to 9 m in length. Dunkleosteus, first found in Devonian stata in Ohio, and whose remains have also been found in Europe, other parts of North America and Morocco, was a major predator of the latest Devonian period. It had a skull measuring about 1.3 m (4 ft) at its widest point, and armor plates up to 5 cm (2 in.) thick. Scars and wounds sometimes preserved on the bony armor of this and other placoderms match the jaws of Dunkleosteus-like fish, showing it probably also attacked its own kind.
Entelognathus primordialisOne of the most significant fossil fish to come to light recently is the advanced arthrodire named Entelognathus primordialis, a placoderm with osteichthyan-like marginal jaw bones (Min Zhu et al. 2013). This well-preserved fossil was found in shale deposits of the Kuanti Formation at Xiaoxiang reservoir in Quijing, Yunnan, China, dating from the Late Ludlow phase of the Silurian (419 mya). The fossil is a mostly intact anterior half of an individual, with the articulating head and trunk armor preserved in three dimensions. Its body length is estimated at slightly over 20 cm (8 in), based on a holotype length of 11 cm (4.3 in).
Fig.3: External form of Entelognathus primordialis (after Min Zhu 2013 ).
E. primordialis represents the earliest known stem gnathostome with dermal marginal jaw bones (premaxilla, maxilla and dentary), features previously restricted to Osteichthyes who are thought to have appeared in the Devonian. It raises important issues about the relative ancestries of osteichthyans (bony fish) versus cartilageneous fishes (sharks and rays) and their presumed ancestor, acanthodians (spiny sharks).
Min Zhu et al. (2013) found that Entelognathus shows a direct link (homology) between the skeletal anatomy of placoderms and osteichthyans. In terms of trait analysis, E. primordialis is grouped with arthrodires and crown gnathostomes (all living jawed vertebrates), whereas all acanthodian (spiny shark) taxa fall on the chondrichthyan (cartiliginous fish) stem. Cladistic analysis suggests that the last common ancestor of Chondrichthyes and Osteichthyes had a macromeric dermal skeleton (macromery is a type of cell division). It shows that micromery (a contrastive type of cell division) is derived in both bony sharks (acanthodians) and cartilaginous sharks and rays (chondrichthyans), and questions acanthodians as stem gnathostomes and stem osteichthyans or bony fish (Min Zhu et al. 2013).
Antiarchi.
Antiarchi ("opposite anus") were another successful order of placoderms. The order's name, curiously, is based on a misidentification by Edward Drinker Cope, who, mistakenly thinking it was an armored tunicate (hemichordate), found the anal opening at the rear of the body, as opposed to having both oral and anal siphons together at one end, as is normal for adult tunicates (although not for fish).
Bothriolepis
canadensis ("pitted scale from Canada"), living from 387-360 mya, was
the most widespread and diverse genus of antiarch placoderms, with 100
or more species known from Middle to Late Devonian strata, found in all
continents. Numerous examples are known from Escuminac Bay, Québec, for
which the species is named. Its wide range appeared to have
corresponded with the Devonian continental coastlines. Bothriolepis
were relatively small, freshwater bottom-feeders, with a heavily
armoured head attached to the thoracic shield. The armored head of
Bothriolepis was only about 10 cm (4 in) across.The body length in most
species was about 30 cm (1 foot), although one species, B. maxima, had
a carapace of about 100 cm (1 m) length. It also had a long pair
of armored pectoral fins, serving as caliper-like, or arthropod-like
limbs, used to raise itself out of the mud. In more
primitive forms of Antiarchi, such as the genus Yunnanolepis from
China, the limbs were thick and short.Fig.4: Bothriolepis canadensis (A: Field Mus.Nat Hist; B: reconstruction.)
Bothriolepis and other antiarchs inhabited both freshwater and marine environments, including lagoons, rivers, deltas, and coastal environments, and probably fed on invertebrates such as crustaceans and molluscs. Bothriolepis had gills in addition to a pair of pouches off the esophagus that may have functioned as lungs. On the front of its head was a keyhole-shaped opening along the midline on the upper side for the eyes and nostrils, and its mouth on the lower side near the front. It also had a separate bone partition or preorbital recess enclosing the nasal capsules.
Brindabellaspida.
Brindabellaspida ("Brindabella's shield") from the early Devonian are characterized by a long rostral projection or snout. Based on comparisons between the brain of Brindabellaspis stensioi and that of a jawless fish, the genus may be related to a line of basal or primitive placoderms (Young 1980; Janvier 1997).
Skull fragments of B. stensioi found in an Early Devonian coral reef setting in New South Wales, Australia have revealed new details on the skull form, rostrum, and endocranial anatomy of this early placoderm (King et al. 2018) Brindabellaspis has some highly unusual morphological traits compared with other placoderms. Among
these are the location of the nasal capsules (n in fig.5 A) and B)), which are
situated within the anterior cavity of the eye orbits. Also the
braincase is unusually deep, and the forward position of the hyoid bone
suggests that the jaws of Brindabellaspis (still unknown) were
situated mainly in front of the eye orbits (King et al. 2018). These
unique forms, due in part to the extended rostrum or snout, may also be primitive features, and contrast
with those of placoderms such as Romundina.Fig.5: Skull of Brindabellapsis stensoi, A) skull fragment from New South Wales B), C) dorsal and lateral reconstructions of skull. D) placement of skull fragment on reconstructed fish. (After King et al.2018, figs. 1 and 4)
Phyllolepida.
Phyllolepida ("leaf scales") were a successful order of flattened placoderms whose fossils have been found around the world. Their head and shoulder armor consisted of whole plates fused together, rather than the numerous tubercles and scales of other orders of placoderms, such as the Petalichthyida.
As is typical for fish with a flattened shape, the Phyllolepida were bottom-dwelling predators that ambushed prey. Also, uniquely for this particular form of placoderm, they were freshwater fish. Overall, however, placoderms included some of the first vertebrates to colonize fresh water; fossils of a number of Devonian placoderms have been found in freshwater habitats. Interestingly, their eyes were located on the sides of the head, unlike most bottom-dwelling predators whose eyes are on the top of the head. Phyllolepida had extremely small eyes, suggesting to some that the eyes may have been vestigial.
Ptyctodontida.
Ptyctodontida ("folded teeth") were lightly armored placoderms with big heads, big eyes and long bodies. They had slender, streamlined forms, and were equipped with crushing tooth plates, inspiring their name. Their armor was reduced to a pattern of small plates around the head and neck. Like fossil acanthothoracids, and living (and unrelated) holocephalians, most of the ptyctodontids are thought to have lived near the sea bottom and preyed on shellfish. Ptyctodontids were sexually dimorphic, with the males having pelvic claspers and possibly claspers on the head as well.
Based on their lack of armor, some paleontologists have suggested that the Ptyctodontida were actually not placoderms, but ancestral holocephalians. Anatomical examinations of well-preserved fossils, however, have largely disproved this. Major differences include skin coloration (holocephalians have shagreen on their skin while ptyctodontids do not); composition of the armoured plates and scales (since those of holocephalians are made of dentine while those of ptyctodontids are made of bone); the form of the cranium (those of holocephalians are similar to sharks while those of ptyctodontids are similar to those of other placoderms); and significantly, that holocephalians have true teeth while ptyctodonts have beak-like, tooth plates (Janvier 1997).
Rhenanida.
Rhenanida ("Rhine fish"; fig 6) were stingray-like forms, living as bottom-dwelling marine predators with large, upturned mouths. This group of placoderms is known only from Europe and North American marine sediments of the early to middle Devonian period (419-385 mya). Their flattened bodies had large wing-like pectoral fins, with their eyes on top of their heads. Unlike modern fishes, their eyes were heavily surrounded with bone, and each eyeball was connected to the brain case by a pedicle of bone or cartilage called the eyestalk, a feature seen in both sharks and placoderms.
The rhenanids were once presumed to be the most primitive placoderm, or at least the closest to the ancestral placoderm, as their armor was made of a mosaic of unfused tubercles, as opposed to the solidified plates of "advanced" placoderms, such as antiarchs and arthrodires. The tail had many bony platelets of varying sizes. Through co
mparisons of
skull anatomy, however, rhenanids are now considered to be the sister
group of the antiarchs.The relatively rare occurance of Rhenanida fossils may be due to sampling error, caused by the fact that, when rhenanids die, their unfused body scale mosaics come apart. This directly limits the sampling possibilities for recovering fossils of this order.
Fig.6: Rhenanida fossil from the Lower Devonian of Bundenbach in the German Rhineland. (after Frickhinger 1995)
Acanthothoraci.
Acanthothoraci ("spine chests") were a group of small, bottom-dwelling placoderms closely related to the rhenanid placoderms. From what can be inferred from the mouthplates of fossil specimens, acanthothoracids were shellfish hunters who were ecologically similar to modern-day chimaeras.
Superficially, acanthoracids resembled scaly chimaeras or small, scaly arthrodires with blunt rostrums. They were distinguished from chimaeras by a pair of large spines that emanate from their chests, the presence of large scales and plates, tooth-like beak plates, and the typical bone-enhanced placoderm eyeball. They were distinguished from other placoderms due to differences in the anatomy of their skulls, and due to patterns on the skull plates and thoracic plates that are unique to this order.
Competition with their relatives, the ptyctodont placoderms, may have been one of the main reasons for the acanthothoracids' extinction prior to the mid-Devonian extinction event.
Petalichthyida.
Petalichthyida ("thin-plated fish") were small, flattened placoderms with long spines, characterized by their splayed fins and by numerous tubercles that decorated all of the plates and scales of their armor. Because they had compressed body forms, it is thought that they were bottom-dwellers who hunted smaller fish. Their diet is not clear, however, as none of the known fossil specimens have preserved mouth parts. Their diversity peaked during the Early Devonian, when they were found throughout the world. Lunaspis and Wijdeaspis are among the best known genera of petalichthyids.
There was an independent diversification event of this order that occurred in what is now Southern China, producing a handful of unique genera that were, at one point, placed in their own order, "Quasipetalichthyida," named after the first discovered species there, Quasipetalichthys haikouensis. Soon after the petalichthids' diversification, they went into decline
Osteichthyes.
Osteichthyes ("bony fish") are a group of fish that have skeletons of bone, as opposed to cartilage (as in sharks and rays). Named by Thomas Huxley in 1880, Osteichthyes is the largest class of vertebrates in existence today. Osteichthyes are divided into ray-finned fish (Actinopterygii) and lobe-finned fish (Sarcopterygii, or "fleshy fin"). The Sarcopterygians are the ancestors of all land vertebrates. Other living sarcopterygians are the coelacanths and lungfish.
The vast majority of present-day fish are osteichthyans, an extremely diverse superclass consisting of 45 orders, and over 435 families and 28,000 species. Most of these are made up of ray-finned fish.
Bony fish are characterized by a relatively stable pattern of cranial bones. The head and pectoral girdles are covered with large dermal bones. The labyrinth in the inner ear contains large otoliths. The braincase, or neurocranium, is frequently divided into anterior and posterior sections divided by a fissure. Bony fish typically have swim bladders, which helps the body float. These bladders have developed into primitive lungs in the lungfishes. All bony fish possess gills. For the majority this is their sole or main means of respiration. Lungfish and other osteichthyan species are capable of respiration through lungs or vascularized swim bladders.
The earliest known bony fish is Guiyu oneiros ("ghost fish"), who lived during the Ludlow epoch of the Late Silurian, 419 million years ago (Zhu et al 2009). It is an exact contemporary of Entelognathus
primordialis, discussed above as a
placoderm with osteichthyan-like marginal jaw bones (Zhu et al.
2013) About 33 cm in length, Guiyu (fig.7) has a combination of both
ray-finned and lobe-finned features, although analysis of the totality
of its features place it closer to lobe-finned fish.Fig.7: Guiyu oneiros (Zhu et al. 2009)
Guiyu oneiros represents an extremely well preserved primitive gnathostome (jawed vertebrate), the oldest articulated sarcopterygian. The postcranial skeleton of this fish includes a primitive pectoral girdle and median fin spine, as in non-osteichthyan gnathostomes, and other traits as found in crown osteichthyans. This substantiates the unexpected mix of postcranial features in basal sarcopterygians, previously restored from the disarticulated remains of Psarolepis.The taxon indicates that the minimum date for the actinopterygian– sarcopterygian split was no later than 419 million years ago (Zhu et al 2009),
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Agassiz, L. 1833-1843. Researches on Fossil Fish, 5 vol.
Benton, M.J. 2005. Vertebrate Paleontology. Blackwell Publishers.
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Janvier, P. 1996. Early Vertebrates. Clarendon Press, Oxford.
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King, Benedict, Gavin C. Young, and John A. Long. 2018. New information on Brindabellaspis stensioi Young, 1980, highlights morphological disparity in Early Devonian placoderms. Royal Society open science 5: 180094.
McCoy 1848
Palaios web pages entitled "Placodermi."
UCMP web page http://www.ucmp.berkeley.edu/vertebrates/basalfish/placodermi.html
Wikipedia, web pages entitled "Placoderms."
Zhu et al. 2009. "The oldest articulated osteichthyan reveals mosaic gnathostome characters." Nature 458, 469-474
Zhu et al. 2013. "A Silurian placoderm with osteichthyan-like marginal jaw bones". Nature 502, pp.188–193.
Glossary