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Home , Araripe Basin, Chanidae, Crato Formation, Dastilbe, Gonorynchidae, Gonorynchiformes

Research 112 (2020) 104454

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Cretaceous Research

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The branchial skeleton in chanid fishes () from the (): 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 fishes with an extensive Received 17 October 2019 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 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 (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 )(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 ranging from the (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 is the epibranchial organ that consists of a blind (), 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 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 . 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 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 osculus (; Eocene, Green formations that belong to the (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 due to the exceptional preservation of or- family 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 , where Dastilbe crandalli is encountered, is known from , with at least eight extinct genera and about 14 a ~90-m-thick succession of meter-scale banks inter- valid species spanning from the Early Cretaceous to the Eocene bedded with equally thick beds of and (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 (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 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 (mostly traces of their meals is much more unlikely. For these cases, to fishes) with preserved soft tissues, constituting the second Kon- recover their behavioral patterns, we must resort to functional servat-Lagerstatte€ of the Araripe Basin (Fara et al., 2005; Martill interpretation of morphology, based on the comparison with et al., 2007). In this portion, the sedimentary and faunal succes- phylogenetically close extant taxa. The elongated rakers supported sion points to a restricted marine influence in the depositional by the epibranchials and ceratobranchials of the aspidorhynchid setting with punctual freshwater input during low sea-level, and comptoni (Crato and Romualdo Formations) provide evi- low-energy and anoxic conditions in the distal portions (Fürsich dence that the species filtered microorganisms suspended in the et al., 2019). water when the mouth was open (Maisey, 1994). Direct data on the trophic characteristics of the Chanidae from the Araripe Basin are 3. Methods very scarce, limited to a few large specimens of Dastible crandalli (Crato Formation) containing fish juveniles presumably of the same Examined specimens are stored in the following institutions: species inside their stomachs, which led to the conclusion that they Academy of Natural Sciences of Drexel University, Philadelphia would be cannibals as adults, and two specimens of Tharrias ara- (ANSP); Coleçao~ de Fosseis da Universidade Federal de Mato ripis (Romualdo Formation) with preserved stomach contents, one Grosso, Mato Grosso, Brazil (CFUFMT); Coleçao~ de Peixes da Uni- with large-eyed decapods and one with unidentified fish remains versidade Federal de Mato Grosso, Mato Grosso, Brazil (CPUFMT); (Maisey, 1994; Davis and Martill, 1999). Virtually nothing is known Departamento Nacional de Produçao~ Mineral, Rio de Janeiro, Brazil about the branchial arches of these species, which might help to (DGM); Instituto de Geociencias,^ Universidade Federal do Rio de infer their eating habits. Janeiro, Brazil (UFRJ); and Laboratorio de Ictiologia de Ribeirao~ In reviewing extensive series of Brazilian fossil gonorynchiforms Preto, Universidade de Sao~ Paulo, Sao~ Paulo, Brazil (LIRP). from Araripe Basin, specimens with preserved elements of the Fossil specimens were acid and mechanically prepared, branchial skeleton came to light for the first time (Fig. 1). Herein we following the methods described by Toombs and Rixon (1959). provide new information regarding the branchial skeleton Some specimens of living species of Gonorynchiformes were morphology, including preserved soft tissue, for the Brazilian fossil cleared and stained (c&s) to observe their skeletons using the chanids Dastilbe crandalli (Crato Formation) and Tharrias araripis technique of Taylor and Van Dyke (1985). Photos were taken with a A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454 3

Fig. 1. Representative specimens of Dastilbe crandalli (Crato Formation) and Tharrhias araripis (Santana Formation) used in this study. A) Dastilbe crandalli, CFUFMT96, 157.0 mm SL, anterior to left; B) Dastilbe crandalli, CFUFMT97, 158.0 mm SL, anterior to left; C) Dastilbe crandalli, CFUFMT98, 99.0 mm SL, anterior to right; D) Dastilbe crandalli, CFUFMT99, 61.0 mm SL, anterior to right; E) Dastilbe crandalli, CFUFMT100, 42.5 mm SL, anterior to left; F) Tharrhias araripis, CFUFMT101, 193.0 mm TFL, anterior to left. Scale in cm. digital camera (Motican 2500) attached to a SMZ 800 Nikon ste- 4. Results reomicroscope. Measures of the gill structures were taken with AxioVision program, version LE4.8.2.0. Drawings were made using A large adult specimen of Dastilbe crandalli (CFUFMT96, a camera lucida attached to a SMZ 800 Nikon stereomicroscope as 157.0 mm SL; Fig. 1A) presents branchial arches with a single row of well as from digital photographs. Anatomical nomenclature follows relatively short, robust, uncinate gill rakers, with no micro- Poyato-Ariza et al. (2010). Standard length (SL) is measured from branchiospines (Figs. 3AeB). This specimen, with the completely snout tip to the posterior end of the hypural plate while total exposed and preserved first arch bears about 30 gill rakers on the fragment length (TFL) corresponds to the maximum measurable first ceratobranchial and at least 20 in the first epibranchial. The gill length of the fossil, when the specimen was incomplete. rakers increase slightly in size from anterior to posterior portion of 4 A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454

Fig. 2. A) Geologic map of the Araripe Basin (modified from Assine et al., 2014). B) The stratigraphic framework of the Aptian Santana Group, with the position of the studied fossil intervals (Crato and Santana Konservat-Lagerstatten€ ). ceratobranchial, ranging from 0.15 to 0.65 mm in length (with a Surprisingly, the observation of even smaller specimens of mean size of 0.45 mm in length). The gill rakers mean length cor- Dastilbe crandalli (CFUFMT 99, 61.0 mm SL; and CFUFMT100, responds to 4.9% of the total ceratobranchial length. The remaining 42.5 mm SL) reveals the presence of the same structures (Figs. 5, 6). branchial arches are not visible in this specimen. Notably, the A camera lucida illustration of main branchial elements including branchial filaments consisting of fragile soft tissue are exceptionally gill arches, gill rakers, branchial filaments and the epibranchial preserved in this specimen. organ is presented in Fig. 7. A second large specimen of Dastilbe crandalli (CFUFMT97, Tharrhias araripis (CFUFMT 101, 193 mm TFL) presents a 158.0 mm SL; Fig. 1B) exhibits several overlapping branchial arches completely different gill raker morphology. Despite being also ar- (Fig. 3CeD) bearing the same kind of relatively short, robust, un- ranged in a single row, the gill rakers are significantly longer and cinate gill rakers, also arranged in a single row. Despite we were not slender (the length of the longer preserved gill raker reaches able to make a precise count of their number in both cerato- and 4.5 mm) than those of Dastilbe crandalli, tapering only slightly. In epibranchials, the arrangement is very similar to that observed in addition, the gill rakers bear distinct microbranchiospines specimen CFUFMT96. Remains of preserved branchial filaments are (Fig. 8AeB). also present. At the postero-dorsal region of the branchial basket in specimen CFUFMT97 we observed the presence of a structure that we interpret as the epibranchial organ (Fig. 3D), which is observed 5. Discussion in fossil chanids for the first time. It consists of a set of imbricated gill rakers just posterior to the posteriormost epibranchial. Gill raker morphology is related to diet and can vary not only In a third medium sized specimen (CFUFMT98, 99.0 mm SL) the between different taxa, but even from one branchial arch to gill rakers are remarkably longer and slender (Fig. 4). Only five gill another within the same species (Vandewalle et al., 2000). Due to rakers are distinctly visible, which range from 0.35 to 0.75 mm in the large opercle, the observation of gill structures in fossil chanids length (mean length of 0.56 mm), corresponding to about 12% of depends on particular preservation situations, in which the bone is the total length of the first ceratobranchial. displaced or is largely fragmented or the gills are moved back during fossilization. The analysis of the branchial skeleton of five A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454 5

Fig. 3. Details of the branchial skeleton on fossil gonorynchiformes from the Early Cretaceous of Brazil. A-B) Dastilbe crandalli, Crato Formation (CFUFMT96, 157.0 mm SL), anterior to left; C-D) Dastilbe crandalli, Crato Formation (CFUFMT97, 158.0 mm SL), anterior to left. Abbreviations: BRF- branchial filaments; CBR-ceratobranchial; EBO- epibranchial organ; EBR- epibranchial; GR-gill rakers; OP-opercle. Scale in mm. specimens of Dastilbe crandalli (Crato Formation) and one specimen limited to a few reports of cannibalism (Maisey, 1994; Davis and of Tharrhias araripis (Romualdo Formation) reveals completely Martill, 1999). The gill raker morphology of Dastilbe crandalli from different feeding habitats as well as evidences of significant onto- the Crato Formation corroborates the assumption that, at least for genetic dietary changes, implying in valuable new paleoecological larger specimens, the species presents a macrophagous or even interpretations. piscivorous diet (Davis and Martill, 1999). The observed variation in length between larger and smaller specimens also suggests an 5.1. Branchial anatomy in Dastilbe crandalli: autecology and ontogenetic variation in feeding habits. Juveniles, with longer gill paleoecological implications rakers and with an epibranchial organ, are expected to eat food items smaller than those consumed by larger specimens, with The absence of teeth in chanids indicates that feeding speciali- short, robust and uncinate rakers. The epibranchial organs, how- zation is reflected directly in the branchial morphology. Direct ev- ever are retained in adult specimens. Ontogenetic dietary shifts, idence of stomach contents in Dastilbe crandalli is scarce, being that is the changes in diet occurring over the life span of an 6 A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454

length, metabolism, and feeding behavior (Sanchez-Hern andez et al., 2019). Based on the presence of small fishes within the guts of only the larger individuals (Maisey, 1994; Davis and Martill, 1999), it has been suggested that Dastilbe crandalli from the Crato Formation was microphagous on soft-bodied organisms, and perhaps algae, until it reached ‘maturity’. Only individuals larger than 150 mm SL appear to have been considered piscivorous (Davis and Martill, 1999). Some larger specimens of Dastilbe crandalli were found with smaller conspecifics in their stomachs, which was interpreted as evidence of cannibalistic behaviour by Maisey (1994) and Davis and Martill (1999). However, the assumption that adults of Dastilbe crandalli were predators may be erroneous. Chanids have a very conservative mouth morphology, with small-sized mouth special- ized to suction feeding of benthos and plankton (Pasleau et al., 2010). Adults of Chanos at sea feed on similar benthic items as do the juveniles, but they add larger planktonic and nektonic items, such as clupeid juveniles, which are probably obtained by swim- ming through the plankton masses and schools of larvae (Kumagai, 1990; Bagarinao, 1991), and not by active hunting. Suction feeding predators typically have large toothed mouths. According to our interpretation the putative predatory behavior of Dastilbe crandalli consists of an atypical behavior due to environmental stress rather than a usual feeding habit, as commented below. Several circumstances may lead to cannibalism (i.e., the act of Fig. 4. Dastilbe crandalli, Crato Formation (CFUFMT98, 99.0 mm SL), anterior to right. fi Abbreviations: BRF- branchial filaments; CBR-ceratobranchial; EBR-epibranchial; GR- eating conspeci cs, recorded for ca. 390 teleost species from 104 gill rakers. Scale in mm. families) in fishes (Pereira et al., 2017). High rates of cannibalism are a natural outcome under some circumstances, such as in hab- itats where certain fish species are resistant to extreme environ- fi individual consumer, are widespread in shes, and their driving mental conditions as well as in some shallow habitats occupied by a mechanisms comprise risk, competition, prey availabil- single fish species (Pereira et al., 2017). Some slabs of the Crato ity, habitat use, morphological constraints, swimming ability, gut limestone display several young specimens of Dastilbe crandalli bearing similar size on the same bedding plane, suggesting mass

Fig. 5. Branchial basket of Dastilbe crandalli, Crato Formation (CFUFMT99, 61.0 mm SL). A) showing the epibranchial organ (greater detail in BeC). Abbreviations: CBR- ceratobranchials; EBO- epibranchial organ; EBR-epibranchials. Scale in mm. A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454 7

Fig. 6. Branchial basket of Dastilbe crandalli, Crato Formation (CFUFMT100, 42.5 mm SL). A), showing the presence of an epibranchial organ (greater detail in B). Abbreviations: BB- branchial basket; EBO- epibranchial organ. Scale in mm.

mortality (Davis and Martill, 1999), which may be due to hypoxia, a common event worldwide in lakes, estuaries and coastal areas (Sagasti et al., 2001). Also, recent analysis on morphological aspects of the Crato Formation's paleoflora indicates adaptations to sazonal, semi-arid conditions, prone to some degree of environmental stress (Bernardes-de-Oliveira et al., 2014). The observed morphological ontogenetic variation on feeding habit of Dastilbe crandalli in the Crato Formation suggests habitat partitioning between juveniles and adults. Juveniles are mostly plankton feeders thriving in shallow habitats exposed to more extreme environmental condi- tions, being susceptible to sporadic mass mortality events, while larger macrophagous specimens may have occurred in deeper channels and lagoons. Cannibalism indicates that, sometimes in- dividuals of very distinct size classes would be in contact to each other under extreme environmental conditions (Fig. 9). Davis and Martill (1999: pl. 1, fig. 4) presented a photograph showing a large specimen of Dastilbe crandalli snapping the head of a fish, pre- sumably of the same species, approximately 60% of its size. Hardly the larger specimen would be able to swallow the smaller specimen completely, in a scene much more consistent with a spasmodic biting behavior caused by a drying environment, for example. Thus, habitat partitioning should be promoted mainly by smaller in- dividuals getting sheltered from large potential predators in shallow-water vegetation instead of in completely separated physical habitats. The presence of an epibranchial organ in Dastilbe crandalli confirms the widespread presence of this specialization for feeding in chanids. Large specimens of Dastilbe crandalli are described herein as being macrophagous, as indicated by their gill raker morphology, but the maintenance of the epibranchial organ rises the assumption that microphagy is also an relevant feeding strategy throughout the entire life cycle of the species. It should be inter- preted as a plastic feeding strategy allowing it to survive on the extreme conditions of the Crato Formation's paleoenvironment.

Fig. 7. Camera lucida illustration of the mains elements of the branchial apparatus observed in Dastilbe crandalli (Crato Formation) of different size classes. A) Dastilbe 5.2. Tharrhias araripis: an open-waters resident crandalli, Crato Formation (CFUFMT99, 61.0 mm SL), anterior to right; B) Dastilbe crandalli, Crato Formation (CFUFMT97, 158.0 mm SL), anterior to left. Abbreviations: BRF- branchial filaments; CBR-ceratobranchials; EBR-epibranchials; EBO- epibranchial Fossil decapods recovered from the stomach contents of Thar- organ; GR-gill rakers. rhias araripis indicate that this taxon was a plankton feeder (Maisey and Carvalho, 1995). Adult individuals of Tharrhias araripis present 8 A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454

Fig. 8. A-B) Tharrhias araripis, Romulado Formation (CFUFMT101, 193.0 mm TFL), anterior to left. Abbreviations: GR-gill rakers; MBS- microbranchiospines. Scale in mm.

associated microbranchiospines are assumed to function in food particle capture and retention (Smith and Sanderson, 2013). Indeed, microbranchiospines are present in suspension-feeding cichlids (Vandewalle et al., 2000), as well as in most extant mem- bers of Gonorynchiformes (except in Gonorynchus and Grass- eichthys)(Pasleau et al., 2010). This is indicative that Tharrhias araripis was a filter feeder, like its extant close relative Chanos chanos. Tharrhias araripis is a very common taxon in the concretion- bearing interval of the Romualdo Formation (Brito and Yabumoto, 2011). Although very rare, specimens of Tharrhias araripis are also recorded in the slightly older Crato Formation (Brito and Yabumoto, 2011). Despite the evidences that the Crato Formation was depos- ited in marginal marine conditions (Goldberg et al., 2019), the Konservat-Lagerstatte€ of this unit seems to have been deposited in lacustrine conditions (Warren et al., 2017; Varejao~ et al., 2019). In this context, Tharrhias araripis apparently had a preference to inhabit more marine settings, as is the case of the Romualdo For- mation (Custodio et al., 2017; Fürsich et al., 2019), explaining its greater abundance in this unit. Chanos chanos (the only extant chanid) fry are most abundant in shore waters feeding mainly on copepods and diatoms. Milkfish fry seek habitats with abundant food in mangrove-vegetated brackish- water coastal wetlands (Bagarinao, 1991, 1994). Juvenile milkfish have been found in such diverse habitats as coral lagoons, mangrove lagoons, estuaries, marsh flats, tidal creeks, and tide pools that share the common characteristics of rich food deposits and protected, relatively shallow waters (Bagarinao, 1991, 1994). They are characterized as being iliophagous, ingesting the top layer of bottom sediments with the associated micro- and meiofauna. Adults are iliophagous, normally feeding on plants and animals of the benthon and planktonic, but also feeding by swimming through plankton masses of larval fish schools (Bagarinao, 1991, 1994). Fig. 9. Dastilbe crandalli of different size classes in association with vegetation in a presumable shallow-water paleoenvironment. CFUFMT102. typical adaptations to filter feeding, which demands a completely 5.3. Evolutionary paleoecological diversity different set of morphological specialization consisting of long gill rakers with microbranchiospines. The diet of a suspension-feeding Tharrhias and Chanos have been considered close relatives, as fish species and the size range of particles ingested should be recent phylogenetic studies includes both genera in the tribe Cha- dependent on the particle capture and retention mechanisms used nini (Poyato-Ariza et al., 2010; Ribeiro et al., 2018). Dastilbe has by the species (Smith and Sanderson, 2013). Gill rakers and the been considered polyphyletic (Amaral and Brito, 2012; Ribeiro A.C. Ribeiro et al. / Cretaceous Research 112 (2020) 104454 9 et al., 2018), with some of the valid species being recognized as Bagarinao, T., 1991. Biology of milkfish (Chanos chanos Forsskal). Southeast Asian distinct genera. Dastilbe elongatus from the Crato Formation has Fisheries Development Center, Aquaculture Department, Tigbauan, Philippines, p. 94. been considered a junior synonym of the type species Dastilbe Bagarinao, T., 1994. Systematics, distribution, genetics and life history of milkfish, crandalli (Davis and Martill, 1999; Dietze, 2007; Brito and Amaral, Chanos chanos. Environmental Biology of 39, 23e41. https://doi.org/ 2008) and all phylogenetic studies including Dastilbe crandalli 10.1007/BF00004752. Bernardes-de-Oliveira, M.E.C., Sucerquia, P.A., Mohr, B., Dino, R., Antonioli, L., were based on material from the Crato Formation instead from the Garcia, M.J., 2014. Indicadores Paleoclimaticos na paleoflora do Crato, final do type locality (Muribeca Formation, Alagoas, Brazil). Dastilbe cran- Aptiano do Gondwana Norocidental. In: Carvalho, I.S., Garcia, M.J., Lana, C.C., dalli from the Crato Formation, according to a recent phylogenetic Strohschoen, O. (Eds.), Paleontologia: cenarios de vida e paleoclimas, vol. 5. Editora Interciencia,^ Rio de Janeiro, pp. 101e119. study (Ribeiro et al., 2018) are not included in the Chanini, but Beveridge, M.C.M., Briggs, M.R.P., Northcott, M.E., Ross, L.G., 1988. The occurrence, consists of a basal Chanidae. structure, and development of microbranchiospines among the tilapias The filter feeding structures of extant gonorynchiforms are (Cichlidae: Tilapiini). Canadian Journal of Zoology 66 (11), 2564e2572. https:// fl doi.org/10.1139/z88-377. morphologically diverse (Pasleau et al., 2010), re ecting a corre- Betancur, R.R., Wiley, E.O., Arratia, G., Acero, A., Bailly, N., Miya, M., Lecointre, G., spondent morphological variation of gill structures (Johnson and Ortí, G., 2017. Phylogenetic classification of bony fishes. BMC Evolutionary Patterson, 1997). Morphologically convergent complex structures Biology 17, 162. https://doi.org/10.1186/s12862-017-0958-3. fi occur even within the order, such as the homoplastic similarities in Brito, P.M., Amaral, C.R.L., 2008. An overview of the speci c problems of Dastilbe Jordan, 1910 (Gonorynchiformes: Chanidae) from the lower cretaceous of the epibranchial organs of kneriids and chanids (Pasleau et al., western Gondwana. In: Arratia, G., Schultze, H.P., Wilson, M.V.H. (Eds.), Meso- 2010), as they are distantly related gonorynchiform families zoic Fishes 4 - Homology and Phylogeny. Dr. Friedrich Pfeil, München, e (Poyato-Ariza et al., 2010). The presence of relatively longer and pp. 279 294. Brito, P.M., Yabumoto, Y., 2011. An updated review of the fish faunas from the Crato slender gill rakers in younger individuals of Dastilbe crandalli is and Santana formations in Brazil, a close relationship to the Tethys fauna. indicative that filtration should be in the early ontogenetic stage. It Bulletin of the Kitakyushu Museum of Natural History and Human History, Ser. e is suggestive that ontogenetic dietary shifts played an important A9,107 136. Custodio, M.A., Quaglio, F., Warren, L.V., Simoes,~ M.G., Fürsich, F.T., Perinotto, J.A.J., role on the evolution of both living and fossil chanids. Assine, M.L., 2017. The transgressive-regressive cycle of the Romualdo Forma- tion (Araripe Basin): sedimentary archive of the Early Cretaceous marine e 6. Conclusions ingression in the interior of Northeast Brazil. Sedimentary Geology 359, 1 15. Davis, S.P., Martill, D.M., 1999. The gonorynchiform fish Dastilbe from the Lower Cretaceous of Brazil. Palaeontology 42 (4), 715e740. https://doi.org/10.1111/ Details of the branchial morphology of Aptian chanids of the 1475-4983.00094. Araripe Basin, Brazil, are described for the first time and provide the Dietze, K., 2007. Redescription of Dastilbe crandalli (Chanidae, Euteleostei) from the Early Cretaceous Crato Formation of North-eastern Brazil. Journal of following conclusions: 27 (1), 8e16. Drenner, R.W., Hambright, K.D., Vinyard, G.L., Gophen, M., 1987. Particle ingestion by 1) Dastilbe crandalli, the most abundant fossil fish from the Crato Tilapia galilaea is not affected by removal of gill rakers and microbranchiospine. 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(Eds.), Gonorynchiformes and Ostar- syntopic habitat partitioning between individuals of different iophysan Relationships. Science Publishers, Enfield, pp. 173e226. https:// size classes under shallow-water extreme (hypoxic) environ- doi.org/10.1201/b10194-7. mental conditions; Fürsich, F.T., et al., 2019. Analysis of a Cretaceous (late Aptian) high-stress 4) Tharrhias araripis, a very common taxon from the nodule level of ecosystem: the Romualdo Formation of the Araripe Basin, northeastern Brazil. Cretaceous Research 95, 268e296. the Romualdo Formation but very rare in the Crato Formation, is Gayet, M., 1985. Gonorhynchiformes nouveau du Cenomanien inferieur marin de a filter-feeding fish that behaved similarly to the adults of living Ramallah (Monts de Judee): Judeichthys haasi nov. gen. nov. sp. (Teleostei, Chanos chanos, inhabiting more marine open-waters conditions. Ostariophysi, Judeichthyidae nov. fam.). Bulletin du Museum national d'histoire naturelle, Section C, Sciences de la terre, paleontologie, geologie, mineralogie 7 (1), 65e85. Acknowledgements Gayet, M., 1986. Ramallichthys Gayet du Cenomanien inferieur de Ramallah (Judee), une introduction aux relations phylogen etiques des Ostariophysi. Memoires du Museum National d'Histoire Naturelle - Serie C: Sciences de la Terre 51, 1e81. We thank Diogenes A. Campos, Ismar S. Carvalho and Mark H. Gayet, M., 1993. Gonorynchoidei du Cretac e superieur marin du Liban et relations Sabaj for allowing us to study material under their care and by phylogen etiques des Charitosomidae nov. fam. Documents des laboratoires de Geologie 126, 1e131. loaning specimens. We thank Fabio Di Dario and Claudio Riccomini Goldberg, K., et al., 2019. Aptian marine ingression in the Araripe Basin: implica- for usefully comments that improved the manuscript. Lionel Cavin tions for paleogeographic reconstruction and evaporite accumulation. 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