Actinopterygians, Ray-finned Fish, are the most successful group of Vertebrates on our planet. They have colonised almost every aquatic ecosystem around the world (with the exception of hypersaline lakes). Most Fish are predators exploiting multiple niches, from large apex predators to tiny plankton eaters. However, in some groups, bizarre, multidenticulate, specialised teeth have evolved, which are interpreted as an adaptation to herbivorous feeding, mainly benthic scraping of Plants. Herbivores constitute only 8–20% of Actinopterygian diversity in freshwater biota and 16–18% on coral reefs. Nowadays, two groups of derived Actinopterygians, the Cyprinidae, and Cichlidae, dominate among herbivores in freshwater ecosystems, while the Siganidae, Acanthuridae, and Scaridae dominate in the marine realm.
In a paper published in the journal Acta Palaeontologica Polonica on 27 January 2020, Maciej Pindakiewicz of the Institute of Paleobiology of the Polish Academy of Sciences, Mateusz Tałanda of the Department of Palaeobiology and Evolution at the University of Warsaw, Tomasz Sulej, also of the Institute of Paleobiology of the Polish Academy of Sciences, Grzegorz Niedźwiedzki of the Department of Organismal Biology at Uppsala University, Andrey Sennikov of the Borissiak Paleontological Institute of the Russian Academy of Sciences, and the Institute of Geology and Petroleum Technologies at the Kazan Federal University, Alexandr Bakaev, also of the Borissiak Paleontological Institute of the Russian Academy of Sciences, Valeriy Bulanov and Valeriy Golubev, again of the Borissiak Paleontological Institute of the Russian Academy of Sciences,
and the Institute of Geology and Petroleum Technologies at the Kazan
Federal University, and Alla Minikh of the Saratov State University, present evidence for the herbivory in Actinopterygians from the latest Permian of the East European Platform of Russia.
There are conflicting claims about the first appearance of Fish herbivory. The first herbivorous Fish may have evolved from marine durophagous forms as Perciformes, Anguiliformes, and Syngnathiformes, as suggested by the Cainozoic fossil record of the shallow marine sediments. Alternatively, adaptation to herbivory in Actinopterygians may have evolved much earlier and in more basal forms, represented by the Late Triassic Holostean Hemicalypterus from the Chinle Formation of Utah. Other research has claimed that freshwater herbivorous Fish already existed in the Permian.
The teeth of most Ray-finned Fish are morphologically simple, but some Fish have more complex, multidenticulate teeth for scrapping algae from the surface of hard objects. The Late Triassic Hemicalypterus had such multicuspid teeth resembling those of modern Scat, Scatophagus argus, implying similar feeding behavior, grazing Algae from the surface of rocks. It has been suggested that Hemicalypterus represents one of the oldest known Ray-finned Fish to have possibly exploited an herbivorous trophic feeding niche.
However, some palaeoichthyologists claimed in the 1990s that herbivory evolved even earlier in Actinopterygians. The Middle to Upper Permian deposits in East-European Russia yielded numerous and diverse Fish remains, including those of possible herbivores. According to these findings the earliest herbivorous Actinopterygians appear in the middle Permian, and diversified in the late Permian.
Pindakiewicz et al.'s study focuses on material collected from uppermost Permian strata of the East European Platform (Russia). Many, probably endemic Actinopterygians lived there in Middle–Late Permian times. These are still poorly-known groups of late Palaeozoic Ray-finned Fish, and among them Eurynotoidiformes are especially characteristic and widespread in the Permian deposits of East European Russia. These spindle-shaped forms with blunt snout and heterocercal caudal fin were morphologically very similar to Holosteans like some members of Ospiida and Amiida. First report on herbivory adaptations in the late Permian genus Isadia were made in the 1990s. This interpretation of trophic specialisation of Eurynotoidiidae was additionally supported by similarity of teeth of Isadia and the modern Tangs, Acanthuridae, (two types of teeth were mentioned, for scrapping and filter feeding). It was later suggested that herbivory in Eurynotoidiidae evolved parallely to specialised aquatic and probably algae feeding, herbivorous Kotlassiid Seymouriamorphs.
Pindakiewicz et al. employed scanning electron microscope imaging to examine collected Permian Fish teeth and compare them to modern herbivores. They confirm that herbivory was the most probable diet of Eurynotoidiidae, and the late Permian record from East European Russia provides the oldest potential evidence for key functional innovations in feeding that would become repeated motifs over the subsequent evolutionary history of Ry-finned Fish.
The studied material was collected at the Sokovka site at Vyazniki in the Vladimir Region. The fossil bearing deposits were examined during fieldworks in 2008, 2010, and 2013 organised by the Institute of Paleobiology of the Polish Academy of Sciences, the Faculty of Biology at the University of Warsaw, Poland; and the Borissiak Paleontological Institute of the Russian Academy of Sciences. The fossiliferous Sokovka outcrop exposes a section of the uppermost Permian Zhukov Member of the Vokhma Formation. The sediments are mostly unconsolidated alluvial sand and subordinate conglomerate and claystone layers. Conglomerate beds occur within the sandstone sequence in the Sokovka section. These deposits have unique and rich fossil content of terrestrial and aquatic Vertebrates. Altogether they are part of the Vyazniki Biotic Assemblage, which represents the latest Permian fauna living there just before faunal turnover associated with the Permian–Triassic transition.
Location of the Fish-bearing site and details of the exposed section. (A) Map of the Eastern Europe with position of Vyazniki (BY, Belarus, LV, Latvia; EST, Estonia; LT, Lithuania). (B) The area around the town of Vyazniki with position of Sokovka site (star). (C) Photograph of the Sokovka section from 2013 and exposure of the Fish-bearing deposits. (D) The simplified section from Sokovka site showing the Fish-bearing layers. Pindakiewicz et al. (2020).
The Vyazniki fauna includes various Amphibians, Dicynodonts, specialised Therocephalians, and the earliest large Proterosuchid, Archosaurus rossicus. The well characterized changes in the Vertebrate assemblages through time are the main base for biostratigraphy in that region. The highly diversified ichthyofauna of the Sokovka outcrop is represented by the Hybodont Shark, Lissodus sp., predatory Discordichthyiform Palaeoniscids, such as Mutovinia sennikovi, smaller predators such as the Actinopterygian Saurichthys, the Coelacanths Strelnia sp. and Evenkia sp., and the huge Dipnoan Permoceratodus gentilis. Abundant remains of the Eurynotoidiform Actinopterygian, Isadia, mainly isolated teeth, is thought to represent herbivores.
The collection housed, at the Institute of Paleobiology of the Polish Academy of Sciences, was sieved in the field into three fractions: large (more than 3 mm), medium (1–3 mm) and small (under 1 mm). The residue was separated from grains by additional strains and three other methods of separation: electromagnetic (for small fraction), manual (for large fraction) and density (for medium fraction). A heavy liquid, lithium heteropolytungstate, was used for the density separation. Scanning electron microscope imaging of the specimens was conducted in the Institute of Paleobiology. Three species of Isadia are reported by Pindakiewicz et al.
Isadia aristoviensis is represented by the isolated tooth specimens ZPAL V.51/1–9, as well as 208 unnumbered teeth: 124 maxillary and 84 mandibular. The maxillary teeth have 3 cusplets of the crown with acrodine. The crown is flat and labially convex and lingually concave. The internal canal starts at the beginning of the root and ends in the base of crown. Morphotypes differ in size, length of base and shape of crown. The smaller morphotype is more straight, has short base and has slightly flat and labiolingually curved cusps. The acrodine tips are wider than in large morphotype. Length of the maxillary teeth estimates between 2.1–4.7 mm and 5.6–10 mm (with the crown). The width of the crown is placed between 0.6–1 mm (small morphotype) and 1.2–1.6 mm (large morphotype).
Isolated teeth of actinopterygian fish Isadia aristoviensis from the Sokovka outcrop, Vyazniki, Russia, late Permian (Upper Vyatkian). (A)–(D) Mandibulary teeth. (A) ZPAL V.51/1, lingual view. (B) ZPAL V.51/2, labial view. (C) ZPAL V.51/3, lingual view. (D) ZPAL V.51/4, labial view. (E)–(I) Maxillary teeth. (E) ZPAL V.51/6, lingual view. (F) ZPAL V.51/7, labial view. (G) ZPAL V.51/5, lingual view. (H) ZPAL V.51/8, lingual view. (I) ZPAL V.51/9, labial view. Scale bars 1 mm. Pindakiewicz et al. (2020).
Isadia arefievi is represented by an isolated tooth (ZPAL V.51/10) and two unnumbered mandibular teeth. The base of the crown is labio-lingually curved, short and thick. These are characters unique for Isadia arefievi teeth. In the collected teeth the whole crown is very wide and has three cusps (the cusp number of Isadia arefievi reaches up to five in specimens from the Eleonora locality). The middle cusp is especially wide, making the crown shovel-shaped. Flat crown is lightly labiolingually curved. The two outer cusplets are very small, thin, and occur on different heights of the tooth. The distal half of the crown is made of acrodine. Width of the crown is between 1.2–2 mm, teeth are smaller than in Isadia aristoviensis. The length is unknown because collected specimens are not well preserved. They represent mandibular teeth according to the number of cusplets in this species.
The isolated tooth of Actinopterygian Fish Isadia arefievi from the Sokovka outcrop, Vyazniki, Russia, late Permian (Upper Vyatkian). ZPAL V.51/10, mandibular tooth, ?lingual view. Scale bar 1 mm, Pindakiewicz et al. (2020).
The teeth of Isadia arefievi are rare in material from Sokovka. The same morphotype was found at the Eleonora site in the Vologda Region, and the Lagernyi Ovrag-3 site in the Nizhny Novgorog Region, dated to the Mutovinia sennikovi–Gnathorhiza otschevi ichthyozone of the lower part of the uppermost Permian. This species of Isadia could have only one row of teeth, forming a tool for scrapping Algae. Enlargement of the medium cusp suggests an adaptation to reduce pressure for each tooth while scrapping Algae, creating a large abrasive surface. The same trend might be seen in durophagous Hybodont teeth. The lack of wide, triangular labial roots on the base is probably caused by some taphonomic factors. The teeth described by Pindakiewicz et al. suggest that Isadia arefievi survived to the terminal part of the late Permian in East European Platform.
Isadia suchonensis is represented by the iosolated teeth (ZPAL V.51/11–13) and 25 unnumbered teeth: 14 maxillary and 11 mandibular. The teeth are curved in anterior view, with tips directed slightly lingually. A shallow row in the middle of the crown is visible on the labial side in some specimens. It is oriented parallel to the tooth axis. Teeth are small and have interior passage larger than Isadia aristoviensis and it ends close to the tips of the crown. The crown of the collected teeth has 4–7 cusps (in some specimens of this species collected from other outcrops show 3–9 cusps on the crown). The tips of the cusps are not covered by acrodine (in Pindakiewicz et al.'s investigations, the acrodine tips in discussed species are developed and clearly distinct from tooth bases in absence of tubercle microstructure of the external surface). The length of the teeth is 1.16–1.47 mm. Two morphotypes of these teeth were found. One with 4–5 cusps, and second with 6–7 smaller cusps. The mandibular teeth have straight base of the crown with less cusplets than crowns of the maxillary teeth.
The isolated teeth of Actinopterygian Fish Isadia suchonensis from the Sokovka outcrop, Vyazniki, Russia, late Permian (Upper Vyatkian). (K) ZPAL V.51/11, lingual (K₁) and lateral (K₂) views. (L) ZPAL V.51/12, labial view. (M) ZPAL V.51/13, maxillary tooth, ?labial view. Scale bars 0.5 mm (J, K, M), 0.2 mm (L). Pindakiewicz et al. (2020).
The species of Isadia had unique dentition among early Actinopterygians. The crown of their teeth is multicuspid. Marginal teeth of Isadia are not capable of durophagus diet, because they are too thin and delicate to crush shells, also the number and morphology of the crown cusps are not adapted for filtrating. They are too large and wide to filter microflora and microfauna from water. Cusplets are small and wide similar to Hemicalypterus and herbivorous Cichlids and Characids. Comparison with teeth of African Cichlids and Scats showed that Hemicalypterus was already a specialised herbivore. Isadia also shares this similarity and most likely diet. The teeth of different species of Isadia are similar to modern herbivorous Fish from different ecological niches.
Comparison of teeth of Actinopterygian Fish Isadia spp. from the Late Permian of Sokovka, Russia with their Recent equivalents. (A), (B) Isadia aristoviensis. (C)–(E) Labeotropheus fuelleborni. (F), (G) Isadia suchonensis. (H), (J) Monotocheirodon kontos. (I) Bryconamericus lethostigmus. (K), (L) Isadia arefievi. (M)–(O) Eretmodus cyanosticus. Not to scale. Pindakiewicz et al. (2020).
Cichlids possess homodont dentition. Adult individuals of the East African cichlid Labeotropheus fuelleborni, have three cusplets on each maxillary tooth and two on each mandibular tooth. The dentition of Isadia aristoviensis (ZPAL V.51/2) is similar to Labeotropheus fuelleborni. Labeotropheus fuelleborni and Isadia aristoviensis have teeth with their base rooted deeply in the jaws and multicuspid crown. Labeotropheus fuelleborni is a highly specialised Algae biter and scraper. This Cichlid lives only in shallow water of the litoral zone. Young Fish have one to two cusplets on each tooth and narrower jaws. The number of cusps of each tooth strongly depends on width of the jaw. Probably this expression suggests heterodentical stage in evolution of their ancestor. Young Fish live in extremely shallow waters where they scrape surfaces of rocks, and when they grew older they swim to deeper but still shallow waters. Pindakiewicz et al. suggest that similar ontogeny in Isadia aristoviensis. They found many maxillary teeth of different sizes and the degree of development of the third cusp. The cheek teeth were shorter, while the longer teeth with bases rooted deeply in the bone were located in the posterior side of the jaw. Mandibular teeth are similar to the maxillary, but they have only two apical cusps on the crown. This could suggest that the maxilla of Isadia aristoviensis in its ontogeny had a tendency to grow wider reflecting change in diet from scraping to biting Algae, as in some modern Fish.
Isadia arefievi has a more derived dentition compared to other members of the Eurynotoidiidae. In its teeth the middle cusp is the largest in comparison to small, short lateral cusps. The shape of the middle cusp suggests that this species of Isadia was scrapping small fragments of Algae from rocks as in modern African Cichlids of the Eretmodini, and especially Eretmodus cyanostictus. This Cichlid is specialised in scrapping Algae from the surface of rocks in deeper parts of rivers. There is, however, one difference; Eretmodus has monocuspid teeth, while those of Isadia arefievi are multicuspid. This difference has explanation in evolution of these Fish. In both the mechanism of developing spatula-shaped teeth from conical teeth could be very similar. The difference lies in the ancestors of the two species of Fish. Eretmodus' ancestors had monocuspid, conical teeth, while those of Isadia had multicuspid teeth. In both lineages the development of shovel like teeth is a result of lateral enlargement and labiolingual flattening.
The teeth of Isadia suchonensis are morphologically similar to teeth of South American Characid Monotocheirodon kontos. Monotocheirodon kontos has a cutting bite. Species of this genus are algivorous Fish that live near the bottom and pick Algae from the sediment. The same situation is observed in some closely related genera, such as Bryconamericus. The jaws of Monotocheirodon kontos bear only 7–9 teeth in one row. In Monotocheirodon kontos as in Isadia suchonensis the maxillary and premaxillary teeth have more cusps (6–7, up to 9), than mandibulary ones (3–5 cusps). In both species the medium cusps of the mandibular teeth are slightly larger than others. In Monotocheirodon kontos and Isadia suchonensis teeth have more antero-posteriorly compressed crown than their base. Isadia suchonensis probably occupied similar niche like Monotocheirodon kontos. Like Monotocheirodon kontos it could live in deeper parts of river and specialise in cutting and filtrating Algae from sediment.
Acrodine on the cusp of teeth appeared early in the evolution of Actinopterygians, and might be plesiomorphic for the whole group. Teleostei had teeth covered by acrodine. The lack of acrodine appeared independently in many Fish lineages. Lack of acrodine in Isadia suchonensis (ZPAL V.51/11–13) might suggests that it belongs to Teleosteomorpha. But more likely this feature is autapomorphic (a unique derived trait) for this species and it is a feeding adaptation as acrodine generates difference in compression between itself and rest of teeth. In the holotype of Isadia suchonensis the acrodine is still visible, although to lesser degree than in other species of Isadia.
The multicuspid teeth of Isadia could have evolved from monocuspid, carnivorous ancestors as in the case of Cichlids. Carnivorous Actinopterygian teeth more closely resemble Isadia teeth than teeth of typical durophagous forms because they have distinct acrodine cap and recognisable crown from its base. Carnivorous teeth are long and also labiolingually curved. Durophagous teeth are very short and rounded. In the latter group the acrodine cap becomes just a thin layer on upper part of teeth. It is an adaptation to crush invertebrates. Usually these teeth form tooth plates. Evolution from durophagy to herbivory would require much greater morphological transition in this case. Therefore Pindakiewicz et al. consider it more probable that Isadia's ancestors were carnivorous with long, conical teeth.
The tooth morphologies of herbivorous Cichlids and Characids are unique and very characteristic. Long multicuspid teeth or short monocuspid spatula-shaped teeth are only a few examples of their diversity. Studying these morphologies shows how |Fish adapt to their environments. The teeth described by Pindakiewicz et al. are not identical to Cichlids but the differences are very small and probably their way of functioning was nearly the same. Analogies to Characidae and Cichlidae suggest that these multicuspid Eurynotoidiids were diverse and specialised herbivores. The convergence of modern Cichlids and Characids with Isadia is very strong, showing that most of their adaptations have mechanical nature. This suggests that herbivory is even older than Hemicalypterus, and make Isadia and other Eurynotoidiidae potentially the oldest known herbivorous Actinopterygians in the fossil record. Species of Isadia were freshwater Fish, which suggests that herbivory first appeared not in the marine, but rather in freshwater ecosystems.
Isadia dentition reveals considerable new anatomical data on the feeding apparatus of one of the earliest herbivorous Actinopterygians. Their morphology shows that some Late Permian Actinopterygians were highly specialised Fish. Pindakiewicz et al. recognised three species of Isadia in the microvertebrate material collected from the uppermost Permian deposits from the Sokovka site at Vyazniki. All of them have specialised dentition for herbivory. Thus far, they are known only from freshwater sediments of the late Permian of Cis-Ural Foredeep and East European Platform. Some possibly herbivorous genera of Eurynotoidiidae have also been found in the Middle Permian (upper Urzhumian) of Russia. Isadia shares many distinctive tooth specialisations with the stratigraphically younger Holostean Hemicalypterus and Recent Characiforms and Cichlids. This suggests that herbivory in Actinopterygians first appeared in the freshwater environment instead of marine realm.
Along with the results presented by Pindakiewicz et al. for Isadia from Sokovka, emerging results for middle and Late Permian Fish fossils from Russia point to unanticipated and phylogenetically informative characters that might help to clarify the Late Paleozoic Actinopterygian evolution in the freshwater ecosystems of northern Pangea. This record from Late Permian of Russia indicates that Ray-finned Fish were diversifying into different trophic niches and exploring different modes of feeding as early as the latest Paleozoic, thus altering our perception of the ecological roles of Fish during the late Paleozoic.
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