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Evidence of a specialized feeding niche in a Late Triassic ray-finned fish: evolution of multidenticulate teeth and benthic scraping in †Hemicalypterus

Original Paper

Abstract

Fishes have evolved to exploit multiple ecological niches. Extant fishes in both marine (e.g., rabbitfishes, surgeonfishes) and freshwater systems (e.g., haplochromine cichlids, characiforms) have evolved specialized, scoop-like, multidenticulate teeth for benthic scraping, feeding primarily on algae. Here, I report evidence of the oldest example of specialized multidenticulate dentition in a ray-finned fish, †Hemicalypterus weiri, from the Upper Triassic Chinle Formation of southeastern Utah (∼210–205 Ma), USA. †H. weiri is a lower actinopterygian species that is phylogenetically remote from modern fishes, and has evolved specialized teeth that converge with those of several living teleost fishes (e.g., characiforms, cichlids, acanthurids, siganids), with a likely function of these teeth being to scrape algae off a rock substrate. This finding contradicts previously held notions that fishes with multicuspid, scoop-like dentition were restricted to teleosts, and indicates that ray-finned fishes were diversifying into different trophic niches and exploring different modes of feeding earlier in their history than previously thought, fundamentally altering our perceptions of the ecological roles of fishes during the Mesozoic.

Keywords

Herbivory Trophic specialization Dentition Neopterygii Mesozoic 

Introduction

Ray-finned fishes (Actinopterygii) are one of the largest and most successful groups of vertebrates on the planet, with over 30,000 species in both marine and freshwater environments (Near et al. 2012), and display a dazzling array of morphological variation associated with behavior, habitat, ecology, and preferred diet. Fishes have occupied carnivorous niches in both marine and freshwater systems for 450 million years (Long 2011). Studies have indicated that the fossil record for herbivorous ray-finned fishes (Actinopterygii) extends only to the Eocene (∼50 Ma; Bellwood 2003). There is no evidence of herbivory among fishes prior to the Cenozoic, whereas herbivorous tetrapods date back to the Carboniferous (∼305 Ma; Sues and Reisz 1998). To exploit various food sources, specialized dentition often associated with herbivory has evolved in teleosts in both marine and freshwater environments, and the morphology of herbivorous dentition varies among different groups: including rasping, needle-like teeth (loricarioid armored catfishes; Delariva and Agostinho 2001); densely packed, bristle teeth (coral-reef butterflyfishes, combtooth blennies, and bristletooth surgeonfishes; Bellwood et al. 2014a); and compressed, scoop-like, scraping incisors with multidenticulate edges (coral-reef rabbitfishes, tangs, surgeonfishes and freshwater characiforms, and lacustrine algae-scraping haplochromine cichlids; Blot and Tyler 1990; Fishelson and Delarea 2013; Purcell and Bellwood 1993; Tyler and Bannikov 1997; Teixeira et al. 2013; Fryer and Isles 1972). The fossil record for teleosts expressing herbivory extends to the Eocene (∼50 Ma; Bellwood 1996), including fossil representatives of many extant marine and brackish inhabitants (e.g., rabbitfishes, scats; Tyler and Sorbini 1990; Blot 1969). Without previous fossil anatomical evidence to indicate a herbivorous diet, it has been assumed that Paleozoic and Mesozoic fishes were carnivorous or omnivorous as they possess generalized caniniform or styliform teeth, associated with carnivory (Schaeffer and Rosen 1961) or specialized durophagous dentition for crushing invertebrates (e.g., Nursall 1996; Kriwet 1999; Tintori 1983; Choo et al. 2014; Smithwick 2015). Evidence of specialized, multidenticulate, scraping dentition is documented here for the first time in the Mesozoic fish †H. weiri (Fig. 1), a non-teleostean ganoid fish from the Upper Triassic Chinle Formation of Lisbon Valley, San Juan County, southeastern Utah (∼210–205 Ma; Schaeffer 1967). †Hemicalypterus is recovered within the upper part of the Church Rock Member of the Chinle Formation in Lisbon Valley, in a sandy siltstone lenticular bed that represents a fluvial channel (Martz et al. 2014; Gibson 2013a, b). The fluvial channel deposits in this area of Lisbon Valley alternate with conglomerate layers, and these geologic deposits are interpreted as a braided stream system with occasional floodplain deposits (Martz et al. 2014; Blakey and Gubitosa 1983 and others). The environment is interpreted by geologists and paleontologists as a freshwater fluvial to deltaic environment (e.g., Dubiel 1987; Good 1998). Recent fieldwork in southeastern Utah recovered hundreds of ray-finned fish fossils from the Church Rock Member of the Chinle Formation, including multiple species of redfieldiiform fishes, a palaeonisciform (†Turseodus dolorensis), a perleidiform (†Tanaocrossus kalliokoskii), two new species of semionotiform fishes, †Lophionotus sanjuanensis (Gibson 2013a) and †Lophionotus chinleana (Gibson 2013b), as well as multiple complete specimens of †Hemicalypterus.
Fig. 1

Hemicalypterus weiri. a Type specimen USNM 23425, composite image of part and counterpart, shown in left lateral view; b reconstruction of †H. weiri, modified from Schaeffer (1967); c inset showing the reconstruction of the teeth of †Hemicalypterus. Scale bar, 1 cm

Hemicalypterus is a monotypic genus whose evolutionary relationship to other actinopterygians remains unclear, although it has been hypothesized to potentially be a member of either the family Semionotidae (Schaeffer 1967) or Dapediidae (Thies and Hauff 2011) based primarily on body shape and cranial morphology. †Hemicalypterus is a small- to medium-sized fish (average standard length 65 mm), with a deep, disc-shaped body, and thick, ganoid scales covering only the anterior half of the body (Fig. 1a, b). The posterior half of the body, beginning at the anterior margin of the dorsal fin, is scaleless, presumably to aid in locomotive flexibility. Its mouth gape is small, and this, combined with its body morphology, suggests that †Hemicalypterus was a slow, docile swimmer. The original description of †Hemicalypterus was based on specimens lacking complete skulls (Schaeffer 1967). Schaeffer (1967) figured a single, isolated “premaxilla” (plate 25, Fig. 4), and described the teeth of †Hemicalypterus as single and peglike. However, recent fieldwork recovered new specimens of †Hemicalypterus, and preparation of these new specimens revealed complete jaws with unique spatulate teeth (Figs. 1c and 2). The “premaxilla” figured in Schaeffer (1967) is in fact a single tooth of †Hemicalypterus. The specialized dentition observed on these specimens represents a previously unknown multidenticulate tooth morphology among any described species of non-teleostean ray-finned fishes and is unique among the extinct actinopterygian fishes of the Mesozoic.
Fig. 2

The multicuspid, herbivorous-type teeth of †Hemicalypterus, seen under normal light, fluorescent light, and line drawing interpretation. a AMNH 5712A, three premaxillary teeth, center tooth is preserved as an impression only; b fluorescent image of teeth as seen in a, hypermineralized acrodin caps on each toothlet do not fluoresce; c interpretation of the premaxillary teeth in AMNH 5712A, teeth shaded in gray; d UMNH VP 19419, lower jaw with six individual teeth, and one premaxillary tooth; e fluorescent image of lower jaw as seen in d; f interpretation of the teeth seen in UMNH VP 19419, teeth shaded in gray, jaw outline shaded in light gray. ang angular, ant antorbital, d dentary, dt dentary tooth, f frontal, io infraorbital, n nasal, pmx premaxilla, pmxt premaxillary tooth, ? question mark provided when identification of bone is unclear due to poor preservation of the fossil; Scale bars, 1 mm

Materials and methods

Specimens of †Hemicalypterus from the American Museum of Natural History (AMNH), Natural History Museum of Utah (UMNH), and United States National Museum (USNM) were examined. In instances where the teeth and jaws were obscured with rock matrix, fossil specimens were mechanically prepared with pneumatic tools, microjacks, and sharpened carbide needles to remove excess matrix. Specimens were examined with the use of several stereomicroscopes with different resolution power. Photographs of the specimens were taken with a Canon digital SLR camera with macro-style lenses (65 and 100 mm). Fluorescent photographs were taken with a SMZ18 stereomicroscope with a P2-EFL GFP-B Filter. Drawings of specimens were done with a camera lucida arm attachment and a digital drawing tablet over high-resolution photographs.

Extant herbivorous fishes from the University of Kansas (KU) Ichthyology collection were examined as comparative material for †Hemicalypterus. Extant specimens (Fig. 3) are preserved in alcohol.
Fig. 3

Examples of the teeth of extant fishes, some showing similarity to the teeth of Hemicalypterus. aAcanthurus chirurgus, KU 34267, upper jaw teeth; bZebrasoma scopas, KU 32001, upper and lower jaw teeth; cCtenochaetus striatus, KU 32014, upper jaw teeth; dSiganus rivulatus, KU 19959, upper and lower jaw teeth; eLabeotropheus fuelleborni, KU 41343, upper jaw teeth; fMaylandia callainos, KU 41344, lower jaw teeth; Scale bars, 1 mm

Specimens examined

The following specimens were examined:

Acanthurus chirurgus KU 34267

Acanthurus nigrofuscus KU 18235

Chaetodipterus faber KU 14910

Chaetodon semilarvatus KU 41093

Chaetodon striatus KU 34269

Ctenochaetus striatus KU 32014

Cyprinodon variegatus KU 17040

Hyphessobrycon panamaensis KU 17702–17704

Hyphessobrycon savagei KU 20104

H. weiri AMNH 5709–5718; UMNH VP 19419, UMNH VP 22903, UMNH VP 22904; USNM V 23424–23425, 23427–23429

Labeotropheus fulleborni KU 41343

Maylandia callainos KU 41344

Naso literatus KU 41125

Poecilia sphenops KU 18694

Siganus rivulatus KU 19959

Siganus vulpinnis KU 29284

Zebrasoma scopas KU 32001

Results

The tooth-bearing premaxillary bones of †Hemicalypterus are not large, lack long ascending processes attaching them to the skull roof, and each premaxilla bears three individual teeth (Fig. 2a–c). The teeth on the premaxillae are long and cylindrical at the base, each broadening at the crown to a flat, spatulate surface with four individual styliform cusps at the edge of the spatulate crown (Fig. 2a–c). These broader tips are in contact with each other, creating a continuous cutting edge (Fig. 2a–c). The lower jaw is short and robust (Fig. 2d–f). The anterior portion of the dentaries contain from 3 to 6 long, spatulate, multicuspid teeth, which are morphologically identical to those seen on the premaxillae. At the broadened, spatulate margin, each tooth contacts its neighbor and is slightly recurved, creating a continuous scraping surface as well as a scoop. The maxilla is either poorly preserved or not preserved on the specimens, but it could potentially be small and edentulous. It appears that this specialized spatulate dentition, while found in both the upper and lower jaws, is restricted to the premaxillae and dentaries (Figs. 1c and 2).

Discussion

Because direct behavior cannot be observed in extinct species, skeletal anatomy becomes crucial for inferring the diet, habit, and potential ecological niche of fossil fishes, and tooth and jaw morphology have been shown to correlate with diet in previous studies (e.g., Clifton and Motta 1998; Bellwood 2003; Purnell et al. 2012). Measurements of the jaw-lever ratio have been correlated with preferences in diet (e.g., Bellwood 2003; Smithwick 2015), but the preservation of specimens of †Hemicalypterus available for this study do not allow for accurate measurements of the jaw-lever ratio. And considering Liem’s paradox, which states that specialized feeding morphologies are not always directly in line with specialized dietary habits (Liem 1980), one cannot definitively deduce the diet of an extinct fish based on specialized tooth morphology alone and can only make general assumptions until more information is available. So in order to infer the potential diet and ecological niche of †Hemicalypterus, the tooth and jaw morphology is compared to the dental morphology of extant taxa. Extant taxa with tooth structures similar to those observed in †Hemicalypterus (i.e., flattened, spatulate, scoop-like incisors with pronounced, multicuspid edges) are found within both marine and freshwater environments, and many of these fishes are known to be benthic feeders scraping the substratum, feeding primarily on algae or attached invertebrates. In marine coral reefs, some surgeonfishes (e.g., Acanthurus, Zebrasoma) have developed large, pronounced, incisiform teeth with multidenticulate edges on the crown, which are successful at sheering algae from a rock substrate (Figs. 3a–c and 4; Fishelson and Delarea 2013; Purcell and Bellwood 1993). Within marine to brackish inhabitants, some fishes, such as the snouted mullet (Chaenomugil proboscideus), have small, recurved teeth with compressed, bifid cusps, and feed primarily on epilithic algae (Ebeling 1957). Rabbitfishes (e.g., Siganus; Figs. 3d and 4) have robust teeth with notched cusps and a sharp edge that shears algal matter off a rocky substrate (Tyler and Bannikov 1997). In freshwater habitats, several species of African rift-lake cichlids have evolved specialized dentition for feeding on epilithic algae (Fryer and Isles 1972). Algae-scraping cichlids, such as Labeotropheus (Figs. 3e and 4) and Maylandia (Figs. 3f and 4), have a jaw margin characterized by rows of long teeth with narrow bases, broadening into a spatulate tip and terminated by a series of two to three cusps upon each tooth. The broadened section of each contacts the neighboring teeth and are slightly recurved (Fryer and Isles 1972), much like what is observed in †Hemicalypterus (Fig. 2). Among non-percomorph teleosts, compressed multidenticulate teeth have also evolved independently in a few characoid lineages (Characiformes: Characoidei; Fink and Fink 1981), such as those observed in the genera Deuterodon and Hyphessobrycon (Fig. 4; Teixeira et al. 2013), which are also known to feed upon algae and macrophytes as well as a small portion of other organisms, such as insect larvae (Teixeira et al. 2013).
Fig. 4

Occurrences of some fishes with multidenticulate dentition through time, with drawings of their individual tooth morphologies. †Hemicalypterus (highlighted in bold) is the oldest occurrence of a fish (within the Late Triassic) with multidenticulate dentition used for scraping the substratum, with the likely function of facultative herbivory. Other fishes with similar, multidenticulate dentition do not occur until the Eocene with fossilized fishes from the Monte Bolca Formation, such as †Pasaichthys and †Ruffoichthys. Many examples of fishes with multidenticulate dentition occur in the Recent, and all of these fishes are at least partially herbivorous

The finding of a specialized, multidenticulate, scoop-like scraping dentition in the Mesozoic in a lower actinopterygian taxon, †Hemicalypterus, is indicative of a novel type of feeding strategy not otherwise observed in ray-finned fishes prior to the Mesozoic. The fine toothlets along the edge of each tooth suggest weak benthic feeding, and these toothlets would likely have broken off if †Hemicalypterus were to attempt feeding upon hard-shelled invertebrates. Invertebrates were more likely the prey of fishes with robust marginal teeth and a pavement of palatal and or vomerine teeth, which is observed in other Mesozoic and Cenozoic deep-bodies fishes, such as pycnodonts (e.g., Nursall 1996; Kriwet 1999), Sargodon (Tintori 1983), and some dapediids (e.g., Thies and Hauff 2011; Smithwick 2015). Based upon the tooth morphology of †Hemicalypterus and its similarity to many extant freshwater and marine herbivorous fishes, it is likely that †Hemicalypterus was herbivorous, at least in part, and exploited a benthic feeding niche by using its fork-like teeth to pull algae or other attached plants and organisms from a rocky substrate in the continental stream systems of the Upper Triassic Chinle Formation. In addition, the deep, disc-shaped body morphology with loss of heavy ganoid scales on its posterior flank imply that †Hemicalypterus was not a fast, open water predatory fish, but instead a slow-moving fish with a more flexible caudal region that could have allowed it to remain still in the water column while feeding and pulling on food sources on the substratum.

Prior to this discovery, the oldest fossil record for herbivorous marine teleosts dates back to the Middle Eocene (50 Ma; Bellwood et al. 2014b). Marine herbivorous fishes with exceptionally preserved fossil taxa are found in the Eocene Monte Bolca Lagerstätte of Italy, which is hypothesized to represent a coral-reef environment (Blot 1969; Bellwood 1996; Bellwood 2003). Most of the fishes found in the Monte Bolca deposits display a more generalized dentition, unlike their extant relatives (Blot and Tyler 1990; Bellwood et al. 2014b). Many species, however, possess a jaw-lever ratio that is consistent with a herbivorous lifestyle as per Bellwood (2003), and some species display similar types of specialized dentition that might indicate a benthic feeding lifestyle, such as the siganid †Ruffoichthys (Fig. 4; Tyler and Sorbini 1990), the monodactylid †Pasaichthys (Fig. 4; Blot 1969), and the scatophagid Eoscatophagus (Tyler and Sorbini 1999). The initial divergence of these closely related families are potentially older than the Eocene, as several representatives from these clades are already present and established in coral-reef environments during the Eocene (Bellwood 2003). Molecular divergence dating of spiny-rayed fishes based on fossil calibration evidence indicates that the origin of most Acanthuriformes and crown percomorphs, that include modern taxa that occupy herbivorous niches, may extend back from the Early Paleocene to the Late Cretaceous (Near et al. 2012). In freshwater habitats, fishes that possess scraping dentition are found in a variety of teleost lineages, such as characiforms, livebearers, and cichlids. The oldest fossil record for a freshwater fish lineage with multiple taxa with compressed multidenticulate teeth (Characiformes) dates back to the Late Cretaceous (97 Ma; Malabarba and Malabarba 2010), although the oldest fossil characiforms have not been hypothesized to be herbivorous. Likewise, African cichlids have a fossil record dating back 45 Ma (Murray 2001; McMahan et al. 2013), but the origin of specialized scraping dentition is thought to have occurred recently in their evolutionary history, with the algae-scraping haplochromine cichlids of Lake Malawi hypothesized to have evolved during the Pleistocene (∼1 Ma; Danley et al. 2012).

The discovery of specialized benthic-scraping dentition in the Late Triassic (∼210 Ma) neopterygian fish †Hemicalypterus changes prior conceptions that this type of specialized multidenticulate dentition evolved recently among teleost fishes. Additionally, the anatomy of its unique dentition is evidence that †Hemicalypterus may have occupied an herbivorous ecological niche that has not been previously associated with any extinct lower actinopterygian or early teleost of the Paleozoic or Mesozoic. Although it is hypothesized that Mesozoic or Paleozoic ray-finned fishes may have been opportunistically feeding on plants or detritus, there is currently no evidence—either via gut contents, ichnological traces, or dentition—to indicate that Paleozoic or Mesozoic actinopterygians had moved into a herbivorous niche that had otherwise been occupied by aquatic invertebrates (Steneck 1983). Instead, it has been inferred that Paleozoic and Mesozoic fishes were carnivorous or omnivorous feeders with generalized teeth either styliform, caniniform, or durophagous in appearance (Schaeffer and Rosen 1961; Tintori 1983; Nursall 1996; Kriwet 1999; Choo et al. 2014; Smithwick 2015). With the evolution of highly specialized tooth morphology for scraping the substrate, †Hemicalypterus likely exploited a new ecological niche that would allow it to feed directly on primary producers in an aquatic ecosystem.

Hemicalypterus is part of an assemblage of aquatic and terrestrial organisms in the Chinle Formation that evolved during a window of time in the Late Triassic that has been associated with significant ecological opportunity, following a faunal turnover event that coincides with a bolide impact (215 Ma; Ramezani et al. 2005; Parker and Martz 2011) that caused ecological upheaval. The only known record of †Hemicalypterus fossils are the uppermost deposits of the Chinle Formation (210–205 Ma) of southern Utah, which falls between two known large catastrophic events that occurred during the Late Triassic (Fig. 4). First is the Manicouagan bolide impact in Quebec Canada (dated at 215.5 Ma; Ramezani et al. 2005) that has been correlated with a terrestrial fauna turnover in the Chinle Formation (Parker and Martz 2011). This event likely opened up ecological opportunity and niche space for aquatic organisms as well, such as †Hemicalypterus and other fishes from the Chinle Formation, to diversify into and exploit. Second, the Triassic Period ended with one of the largest documented mass extinction events in Earth’s history (Benton 1995), and the End-Triassic Extinction event at 201.5 Ma is correlated to a series of volcanic eruptions known as the Central Atlantic Magmatic Province (CAMP; Blackburn et al. 2013). CAMP volcanic eruptions are associated with the breakup of the supercontinent Pangaea, which caused significant climatic changes associated with one of the largest mass extinction events (Blackburn et al. 2013) in Earth’s history. These climatic changes altered the habitat of what is now the Chinle Formation, changing the wetland-like habitat (Dubiel 1987) into extensive sand dunes (Blakey 1989). There is no evidence of †Hemicalypterus fossils following the End-Triassic Extinction Event.

Notes

Acknowledgments

I thank H.-P. Schultze, M. P. Davis, W. L. Smith, G. Arratia, K. R. Smith, and P. A. Selden for their comments on the manuscript, and W. L. Smith for photographic assistance. A. R. C. Milner, J. I. Kirkland, and volunteers from the Utah Friends of Paleontology were instrumental in conducting fieldwork, specimen collection, and fossil preparation. I thank R. Irmis, C. Levitt-Bussian, J. Maisey, A. Gishlik, M. Brett-Surman, W. L. Smith, and A. Bentley for loaning or providing access to fossil and recent specimens from their respective institutions. I acknowledge the University of Kansas Department of Geology and Biodiversity Institute, the University of Utah, the Utah Geological Survey, and the St. George Dinosaur Discovery Site for their support of this research. This research was funded in part by the University of Kansas Biodiversity Institute Panorama Grant, and National Geographic Grant #9071-12. Specimens collected for this study were collected under Utah State Institutional Trust Lands Administration permits 02-334 and 05-347.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Geology and Biodiversity InstituteUniversity of KansasLawrenceUSA

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