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The Branchial Skeleton in Aptian Chanid Fishes

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The Branchial Skeleton in Aptian Chanid Fishes Cretaceous Research 112 (2020) 104454 Contents lists available at ScienceDirect Cretaceous Research journal homepage: www.elsevier.com/locate/CretRes The branchial skeleton in Aptian chanid fishes (Gonorynchiformes) from the Araripe Basin (Brazil): Autecology and paleoecological implications * Alexandre Cunha Ribeiro a, , Francisco Jose Poyato-Ariza b, Filipe Giovanini Varejao~ c, Flavio Alicino Bockmann d a Departamento de Biologia e Zoologia, Universidade Federal de Mato Grosso, Av. Fernando Corr^ea da Costa, 2367, Cuiaba 78060-900, Mato Grosso, Brazil b Centre for Integration on Palaeobiology & Unidad de Paleontología, Departamento de Biología, Universidad Autonoma de Madrid, Cantoblanco, E-28049, Madrid, Spain c Instituto LAMIR, Departamento de Geologia, Universidade Federal do Parana, Av. Cel. Francisco H. dos Santos, 100, Jardim das Americas, Curitiba 81531- 980, Parana, Brazil d Laboratorio de Ictiologia de Ribeirao~ Preto, Departamento de Biologia, FFCLRP, Universidade de Sao~ Paulo, Av. Bandeirantes 3900, Ribeirao~ Preto 14040- 901, Sao~ Paulo, Brazil article info abstract Article history: Gonorynchiformes are a small, but morphologically diverse group of teleost fishes with an extensive Received 17 October 2019 fossil record. Most extant gonorynchiforms are efficient filter feeders, bearing long gill rakers and other Received in revised form morphological specializations, such as microbranchiospines and an epibranchial organ. The analyses of 28 January 2020 the gill arch of the Brazilian gonorynchiform fishes Dastilbe crandalli and Tharrias araripis from the Aptian Accepted in revised form 12 March 2020 of the Araripe Basin, Northeast Brazil, demonstrate significant morphological variation suggestive of Available online 19 March 2020 distinct feeding habitats as well as ontogenetic dietary shifts in these closely related gonorynchiforms. © 2020 Elsevier Ltd. All rights reserved. Keywords: Paleoecology Branchial skeleton Gonorynchiformes Araripe basin 1. Introduction and Poyato-Ariza, 2010). Many anatomical features of visceral arches are informative in identifying the ways in which food is Gonorynchiformes has been traditionally considered as the obtained and processed, as is the case of gonorynchiforms. Indeed, sister group to the Otophysi (i.e., fishes with a functioning Weberian most extant gonorynchiforms are efficient suspension feeders apparatus), together forming the superoder Ostariophysi (Poyato- (Pasleau et al., 2010). The gill rakers of all the branchial arches are Ariza et al., 2010; Betancur et al., 2017). Living gonorynchiforms particularly long and bear microbranchiospines (except in Gonor- are a small, but morphologically diverse group of teleost fishes ynchus and Grasseichthys)(Pasleau et al., 2010). Micro- encompassing only seven extant genera (Johnson and Patterson, branchiospines, sometimes called microgillrakers, are small dermal 1997). The fossil record, however, accounts with additional 20 ossifications situated in the epidermis close to the base of the gill genera and 37 species ranging from the Early Cretaceous (Berria- arches (Greenwood, 1976; Stiassny, 1980; Beveridge et al., 1988). sian-Valanginian) to the Early Neogene (Fara et al., 2010; Amaral These elements are generally considered to take part in the filtra- and Brito, 2012; Taverne et al., 2019). tion process, either by retaining the mucus itself or particle-laden Gonorynchiform fishes are characterized by profound modifi- mucus (Gosse, 1956; Whitehead, 1959), although there are re- cations of the skull, including a small, edentulous mouth (Grande ports of macrophagous fishes bearing microbranchiospines (Beveridge et al., 1988). However, under experimental conditions, gill raker or microbranchiospine ablation does not modify at all the * Corresponding author. ability of a cichlid fish to trap particles when filter feeding (Drenner E-mail addresses: [email protected] (A.C. Ribeiro), francisco. et al., 1987; Vandewalle et al., 2000). Another morphological [email protected] (F.J. Poyato-Ariza), fi[email protected] (F.G. Varejao),~ specialization for filtering present in all gonorynchiforms other [email protected] (F.A. Bockmann). https://doi.org/10.1016/j.cretres.2020.104454 0195-6671/© 2020 Elsevier Ltd. All rights reserved. 2 A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454 than Gonorynchus is the epibranchial organ that consists of a blind (Romualdo Formation), providing new insights on the diversity of sac opening through a canal into the buccopharyngeal cavity just feeding mechanisms in fossil chanids and the paleoecological above and behind the last branchial slit that traps food particles by implications. mucus, transporting it into the esophagus by internal water cur- rents (Pasleau et al., 2010). 2. Geological context Gonorynchiforms are considered to be unique among recent teleosts by presenting an extreme reduction of gill-arch dentition The Aptian evaporitic transitional sequence registers the final (dermal skeleton), which, primitively in teleosts, bears a more or events of the separation between Africa and South America. It less complete covering of autogenous tooth-plates (not fused to consists in complex mixed carbonate-evaporite-siliciclastic suc- endoskeletal elements) (Johnson and Patterson,1997). Gonorynchus cessions deposited in the Brazilian marginal basins as well as in the has a patch of conical teeth (similar to endopterygoid teeth) posi- interior basins of the Northeast Brazil. The Araripe Basin records the tioned on basibranchial 2 (Grande and Poyato-Ariza, 2010). Teeth most complete sedimentary succession among the interior basins have been also reported on the branchial arches of Middle Eastern of NE Brazil, being structurally fitted in a Precambrian shear zone gonorynchids Charitosomus, Judeichthys and Ramallichthys (Gayet, located in the Borborema Province. There, the Aptian transitional 1985, 1986, 1993), supposedly also positioned on basibranchial 2, phase is represented by the Barbalha, Crato, Ipubi and Romualdo and also in Notogoneus osculus (Gonorynchidae; Eocene, Green formations that belong to the Santana Group (Assine et al., 2014) River Formation) (Grande and Poyato-Ariza, 2010). Among (Fig. 2). The Crato and Romualdo formations are among the most remaining fossil gonorynchiforms, details of the branchial skeleton important Cretaceous Konservat-Lagerstatten€ (sensu Seilacher, are virtually unknown. Chanos chanos, the only extant species of the 1990) of the Gondwana due to the exceptional preservation of or- family Chanidae is, as the most extant gonorynchiforms, edentu- ganisms with soft tissues (Fara et al., 2005; Martill et al., 2007; lous and filter feeding, eating a diversity of small-sized items Maldanis et al., 2016; Varejao~ et al., 2019). (Bagarinao, 1994). However, most of the diversity of the Chanidae is The Crato Formation, where Dastilbe crandalli is encountered, is known from fossils, with at least eight extinct genera and about 14 a ~90-m-thick succession of meter-scale limestone banks inter- valid species spanning from the Early Cretaceous to the Eocene bedded with equally thick beds of shales and sandstones (Assine (Fara et al., 2010; Poyato-Ariza et al., 2010; Ribeiro et al., 2018; et al., 2014), and is interpreted as a lacustrine system due to the Taverne et al., 2019). Unfortunately, except for the record of “teeth” apparent absence of true marine fossils (Neumann et al., 2003). on the first ceratobranchial of Tharrhias (Poyato-Ariza et al., 2010; Recently, this interpretation was challenged, as evidence for marine Ribeiro et al., 2018), all characters related to the branchial arches ingressions revealed by occurrence of foraminiferal linings of fossil chanids are coded as indeterminate due to lack of knowl- (Goldberg et al., 2019), dinocysts and marine ichnotaxa (Varejao,~ edge about their states, therefore limiting conclusions regarding 2019) points to marginal marine sedimentation. The Konservat- the origin and evolution of feeding mechanisms in this family. Lagerstatte€ of the Crato Formation is restricted to an ~8-m-thick Trophic structure of the Araripe paleoichthyofauna (Aptian, limestone interval at the lower part of the unit (Martill et al., 2007; Araripe Basin, Northeast Brazil) has been addressed mostly on the Varejao~ et al., 2019). Microbial laminites and stromatolites thrived basis of direct evidences of predator-prey relationships by inven- in this interval (Warren et al., 2017) and favoured the preservation torying their fossilized gastric contents, and functional interpreta- of continental fauna and flora (Varejao~ et al., 2019). tion of morphology (cf. Maisey, 1994; Maisey and Carvalho, 1995). The Romualdo Formation, where Tharrias araripis is found, can Obviously, for fossil fishes, it is much easier to find direct evidence reach 100 m in thickness and is a siliciclastic-dominated and of food items for carnivores that feed on large animals or with hard marine-influenced unit corresponding to a depositional sequence coverings (cf. Maisey, 1994; Maisey and Carvalho, 1995). On the encompassing transgressive-regressive cycles (Custodio et al., other hand, fishes that fed on small and delicate items, such as the 2017; Fürsich et al., 2019). The first transgressive cycle includes case of the filter-feeders, the chance of encountering direct fossil the concretion-bearing black shales containing vertebrates (mostly traces of their meals is much more unlikely. For these cases, to fishes) with preserved soft tissues, constituting the second Kon- recover their
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