Evidence of a specialized feeding niche in a Late Triassic ray-finned fish: evolution of multidenticulate teeth and benthic scraping in †Hemicalypterus
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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.
KeywordsHerbivory Trophic specialization Dentition Neopterygii Mesozoic
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.
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
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).
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.
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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