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Exceptionally Preserved Tadpoles from the Miocene of Libros, Spain: Ecomorphological Reconstruction and the Impact of Ontogeny Upon Taphonomy

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Exceptionally Preserved Tadpoles from the Miocene of Libros, Spain: Ecomorphological Reconstruction and the Impact of Ontogeny Upon Taphonomy Exceptionally preserved tadpoles from the Miocene of Libros, Spain: ecomorphological reconstruction and the impact of ontogeny upon taphonomy MARIA E. MCNAMARA, PATRICK J. ORR, STUART L. KEARNS, LUIS ALCALA´ , PERE ANADO´ N AND ENRIQUE PEN˜ ALVER-MOLLA´ McNamara, M.E., Orr, P.J., Kearns, S.L., Alcala´, L., Anado´n, P. & Pen˜alver-Molla´,E. 2010: Exceptionally preserved tadpoles from the Miocene of Libros, Spain: ecomorpho- logical reconstruction and the impact of ontogeny upon taphonomy. Lethaia,Vol.43, pp. 290–306. The Libros exceptional biota from the Upper Miocene of NE Spain includes abundant frog tadpoles (Rana pueyoi) preserved in finely laminated lacustrine mudstones. The tad- poles exhibit a depressed body, short tail, low tail fins, dorso-laterally directed eyes and jaw sheaths; these features identify the Libros tadpoles as members of the benthic lentic ecomorphological guild. This, the first ecomorphological reconstruction of a fossil tad- pole, supports phylogenetic evidence that this ecology is a conserved ranid feature. The soft-tissue features of the Libros tadpoles are characterized by several modes of preserva- tion. The space occupied previously by the brain is defined by calcium carbonate, the nerve cord is defined by calcium phosphate, and jaw sheaths and bone marrow are pre- served as organic remains. Gut contents (and coprolites adjacent to specimens) comprise ingested fine-grained sedimentary detritus and epiphyton. The body outline and the eye- spots, nares, abdominal cavity, notochord, caudal myotomes and fins are defined by a carbonaceous bacterial biofilm. A similar biofilm in adult specimens of R. pueyoi from Libros defines only the body outline, not any internal anatomical features. In the adult frogs, but not in the tadpoles, calcium phosphate and calcium sulphate precipitated in association with integumentary tissues. These differences in the mode of preservation between the adult frogs and tadpoles reflect ontogenetic factors. h Anuran, ecology, soft- tissue, tadpoles, taphonomy. Maria E. McNamara [[email protected]], Patrick J. Orr [[email protected]], UCD School of Geological Sciences, University College Dublin, Belfield, Dublin 4, Ireland; Stuart L. Kearns [[email protected]], Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Rd, Bristol BS8 1RJ, UK; Luis Alcala´ [alcala@ dinopolis.com], Fundacio´nConjuntoPaleontolo´gico de Teruel-Dino´polis, Avda. Sagunto s ⁄ n, 44002 Teruel, Arago´n, Spain; Pere Anado´n [[email protected]], Consejo Superior de Investigaciones Cientı´ficas, Institut de Cie`ncies de la Terra ‘Jaume Almera’, Lluı´s Sole´ iSab- arı´ss⁄ n 08028, Barcelona, Spain; Enrique Pen˜alver-Molla´ [[email protected]], Museo Geominero, Instituto Geolo´gico y Minero de Espan˜a, C ⁄ Rı´os Rosas 23, E-28003 Madrid, Spain; manuscript received on 30 ⁄ 12 ⁄ 2008; manuscript accepted on 24 ⁄ 06 ⁄ 2009. Exceptionally preserved anurans (Rana pueyoi)from morphologyoftheLibrostadpolescouldtherefore the lacustrine-hosted Miocene Libros biota (Spain) constrain hypotheses of their palaeoecology. These comprise both larvae (representing a range of develop- results would have significant wider implications. mental stages) (n = 72) (Figs 1, 2) and adults Soft tissues are preserved in larval anurans from (n = 73). The taphonomy of the non-biomineralized numerous Late Cretaceous and Cenozoic localities (soft) tissues of the adult frogs has been studied com- (Young 1936; Nevo 1968; Sˇpinar 1972; Estes et al. prehensively (McNamara et al. 2006, 2009). Previous 1978; Wassersug & Wake 1995; Maus & Wuttke observations of the larval frogs comprise only brief 2002; Toporski et al. 2002; Rocˇek & Van Dijk 2006). references to a brown carbonaceous bacterial biofilm Collectively, this material has improved our under- that defines the general body outline and, in a single standing of anuran phylogeny, most importantly via specimen, the presence of organically preserved bone the construction of ontogenetic series (e.g. Maus & marrow (McNamara et al. 2006). This paper therefore Wuttke 2002; Rocˇek & Van Dijk 2006). Complemen- considers in detail the taphonomy of the larval frogs tary studies of larval anuran taphonomy and ecology, from Libros. however, are rare (but see Maus & Wuttke 2002; Notably, the soft-tissue morphology of modern Toporski et al. 2002). anuran larvae varies strongly with ecology and habi- This paper also considers how biological factors tat (Table 1). Reconstruction of the soft-tissue control exceptional fossil preservation. Exceptional DOI 10.1111/j.1502-3931.2009.00192.x Ó 2009 The Authors, Journal compilation Ó 2009 The Lethaia Foundation LETHAIA 43 (2010) Miocene fossil tadpoles 291 faunas often include various developmental stages of specimens were recovered during commercial exploi- the same taxon: the preservation potential and the tation of the sulphur and oil shales of the Libros mode of preservation of each should not be assumed Gypsum Unit in the early 20th century; the original to be constant. Different developmental stages can field context and way up of specimens is unknown. vary in their ecology, and thus different biostratinom- The precise fossiliferous horizons are unknown and ic processes may affect carcasses. Factors that influence it is therefore impossible to determine to what decay and mineralization, such as physiology and tis- extent the curated specimens are an unbiased sample sue chemistry, can also vary during ontogeny. The of the fossil assemblage. All developmental stages occurrence of both adult and larval stages of R. pueyoi that were preserved may not be represented. Intui- in the Libros biota is therefore an opportunity to elu- tively, smaller specimens, broadly synonymous with cidate the extent to which differences in the mode, earlier developmental stages, are more likely to be and fidelity, of soft-tissue preservation of the same absent. Similarly, all states of preservation may not taxon have been influenced by factors relating to their be represented; disarticulated specimens and those ontogeny. lacking obvious soft-tissue outlines are more likely to be under-represented. Not all of the soft-tissue features discussed below Geological background could be identified in each specimen, e.g. if a speci- men was incomplete, truncated by the edge of the The Libros lacustrine system developed within the slab, or if soft tissues were obscured in part by sedi- Early Miocene–Late Pliocene Teruel Basin in NE ment. The number of specimens in which a particular Spain (Ortı´ et al. 2003). The Teruel basin-fill in the feature is present is therefore indicated in the text in Libros region comprises up to 500 m of alluvial parentheses. terrigenous facies, lacustrine carbonates and evaporites. The deepest water facies of the Libros Ontogeny sequence is the 150-m-thick late Miocene (Vallesian) Libros Gypsum Unit. The lowest part of this unit, The general categories of larval anuran development the bituminous–calcareous subunit, comprises inter- sensu Gosner (1960) are: (1) embryo (stages 1–20); (2) calated charophytic limestones and laminated hatchling (stages 21–25); (3) tadpole (stages 26–41) mudstones (including oil shales) with deposits of and (4) metamorph (stages 42–46). Twelve incom- native sulphur and rare primary gypsum (Ortı´ et al. plete R. pueyoi larvae could not be staged. The remain- 2003). The exceptional biota comprises salamanders, ing 60 specimens fall within a narrow range of frogs, birds, snakes, insects, arachnids and leaves developmental stages (Gosner stages 30–41) and (Nava´s 1922a,b; Olson 1995; Pen˜alver 1996) and is represent fossil tadpoles. hosted within the laminated mudstones. This facies More detailed resolution of the data is difficult. The represents deposition within the profundal regions Gosner (1960) staging system (and also the Shumway of a permanently stratified bench-type lake, in which 1940; Taylor & Kollros 1946 systems) for modern laterally extensive shallow-water zones (<10 m ranid larvae is based primarily upon the presence of depth) were separated from deeper waters by steep specific soft-tissue morphological features and cannot slopes. The monimolimnion was anoxic and sulphi- be applied easily to fossil anuran larvae. The skeletal dic, and there was intense bacterial sulphate reduc- ossification sequence has been described for Rana tion in the uppermost sediment column (Anado´n pipiens (Kemp & Hoyt 1969); however, the relative et al. 1992; de las Heras et al. 2003; Ortı´ et al. timing of ossification of skeletal elements, and the 2003). order in which they ossify, varies considerably among ranids (Sheil 1999), making extrapolation to other taxa difficult. For example, certain cranial elements Material and methods begin to ossify 11 stages earlier in R. temporaria (de Jongh 1968) than in R. pipiens (Kemp & Hoyt 1969). A total of 72 specimens were examined from the The Libros specimens present additional difficulties. collections of the following institutions: Forschungs- The skeleton is often obscured in part by sediment, institut und Naturmuseum Senckenberg, Frankfurt, gut contents or diagenetic minerals; the ossified parts Germany (FNS), Museu de Geologia de Barcelona, of elements diagnostic of certain stages (e.g. the max- Barcelona (MGB), Museo Nacional de Ciencias illa, femur, humerus and ischium) are less than 1 mm Naturales, Madrid (MNCN) and the Natural History long initially and therefore difficult to identify. Museum, London (NHM). Specimens occur mainly It is not possible to assign any tadpole of
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