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LOCOMOTION ENERGETICS of LEEDSICHTHYS PROBLEMATICUS (ACTINOPTERYGII, PACHYCORMIFORMES) by HUMBERTO G

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LOCOMOTION ENERGETICS of LEEDSICHTHYS PROBLEMATICUS (ACTINOPTERYGII, PACHYCORMIFORMES) by HUMBERTO G [Palaeontology, Vol. 61, Part 5, 2018, pp. 775–783] ASSESSING METABOLIC CONSTRAINTS ON THE MAXIMUM BODY SIZE OF ACTINOPTERYGIANS: LOCOMOTION ENERGETICS OF LEEDSICHTHYS PROBLEMATICUS (ACTINOPTERYGII, PACHYCORMIFORMES) by HUMBERTO G. FERRON 1,* ,BORJAHOLGADO2,* , JEFFREY J. LISTON3,4,5,6,CARLOSMARTINEZ-PEREZ 1,6 and HECTOR BOTELLA1 1Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de Valencia, C/Catedratic Jose Beltran Martınez 2, 46980, Paterna, Valencia Spain; [email protected], [email protected], [email protected] 2Laboratory of Systematics & Taphonomy of Fossil Vertebrates, Departamento de Geologia e Paleontologia, Museu Nacional/Universidade Federal do Riode Janeiro (UFRJ), Quinta da Boa Vista, s/n, S~ao Cristov ~ao, 20940-040, Rio de Janeiro, RJ Brazil; [email protected] 3Bayerische Staatssammlung fur€ Pal€aontologie und Geologie, Richard-Wagner-Straße 10, 80333, Munchen,€ Germany; [email protected], [email protected] 4National Museums Scotland, Chambers Street, Edinburgh, EH1 1JF, UK; [email protected] 5Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK; [email protected] 6School of Earth Sciences, University of Bristol, Bristol, BS8 1TQ, UK; [email protected], [email protected] *Corresponding authors Typescript received 21 October 2017; accepted in revised form 5 April 2018 Abstract: Maximum sizes attained by living actinoptery- weighing up to 44.9 tonnes would have been energetically gians are much smaller than those reached by chon- viable and suggests that similar body sizes could also be possi- drichthyans. Several factors, including the high metabolic ble among living taxa, discarding metabolic factors as likely requirements of bony fishes, have been proposed as possible body size constraints in actinopterygians. Other aspects, such body-size constraints but no empirical approaches exist. as the high degree of endoskeletal ossification, oviparity, indi- Remarkably, fossil evidence has rarely been considered despite rect development or the establishment of other large suspen- some extinct actinopterygians reaching sizes comparable to sion-feeders, could have hindered the evolution of gigantism those of the largest living sharks. Here, we have assessed the among post-Mesozoic ray-finned fish groups. From this per- locomotion energetics of Leedsichthys problematicus, an extinct spective, the evolution of anatomical innovations that allowed gigantic suspension-feeder and the largest actinopterygian ever the transition towards a suspension-feeding lifestyle in med- known, shedding light on the metabolic limits of body size in ium-sized pachycormiforms and the emergence of ecological actinopterygians and the possible underlying factors that opportunity during the Mesozoic are proposed as the most drove the gigantism in pachycormiforms. Phylogenetic gener- likely factors for promoting the acquisition of gigantism in alized least squares analyses and power performance curves this successful lineage of actinopterygians. established in living fishes were used to infer the metabolic budget and locomotion cost of L. problematicus in a wide Key words: metabolic constraints, body size, gigantism, range of scenarios. Our approach predicts that specimens actinopterygians, Pachycormiformes, Leedsichthys problematicus. Giant animals have intrigued both popular culture and throughout the Cenozoic, the first unequivocal gigantic the scientific community for many centuries. The largest suspension-feeders were representatives of a Mesozoic living vertebrates occur in the oceans as massive suspen- group of actinopterygians called pachycormiforms (Fried- sion-feeders, reaching more than 50 tonnes in weight man et al. 2010). The largest representative by far of this (Ferron et al. 2017), closely linked to areas of high plank- extinct lineage is Leedsichthys problematicus, a Middle–Late tonic productivity (Vermeij 2016 and references therein). Jurassic species known from the Callovian of England Although this ecological role has exclusively been occupied (Peterborough, Christian Malford), France (Normandy), by mysticete cetaceans and some chondrichthyans northern Germany (Wiehengebirge), the Oxfordian of © The Palaeontological Association doi: 10.1111/pala.12369 775 776 PALAEONTOLOGY, VOLUME 61 Chile (east of Antofagasta) and the Kimmeridgian of with independent inferences of its locomotion energy France (Cap de la Heve) (Liston 2010), being considerably requirements (i.e. net cost of swimming). larger than the contemporary and subsequent Cretaceous Routine metabolic rate (RMR), defined as the mean suspension-feeding pachycormiforms (Liston 2008, 2013; metabolic rate measured in an animal performing random Schumacher et al. 2016). Leedsichthys is preserved in the physical activity over a given period (Dowd 2003), can be fossil record as isolated, poorly ossified (Liston 2004) and considered in a broad sense to be equivalent to its ener- fragmentary skeletal remains, leading to its frequent getic budget (Willmer et al. 2009; Clarke 2013). The scal- misidentification as organisms other than fish (Liston ing of RMR with mass has been established in living 2010; Liston & Gendry 2015), and most frequently as a ste- ectothermic fishes by means of phylogenetic generalized gosaurian dinosaur (Liston 2016). The most complete least squares (PGLS) analysis and is used here to infer specimen ever recorded still represents only a partial indi- RMR of L. problematicus. PGLS is a phylogenetic regres- vidual (Liston 2006), but some remains have served to sion method in which the covariance among specimens as indicate the large size of this taxon with great clarity (Lis- a result of their shared evolutionary history (i.e. phy- ton & Noe 2004; Liston 2008). As such, body size estimates logeny) is incorporated in the regression error term, thus of L. problematicus have been based on allometric relation- being accounted for during the analysis (see Symonds & ships established in the most closely related large bony fish Blomberg 2014 for a general introduction to PGLS analy- which is likely to have the most comparable form: the sis). Records of RMR and body mass have been compiled pachycormiform Saurostomus esocinus (Liston 2007; Liston for more than 100 fish species from Froese & Pauly (2017) et al. 2013). The dimensions of preopercular remains and Ferron (2017) (data in Ferron et al. 2018). A super- found with a ventral gill basket (Liston 2008) suggest that tree containing all the considered species was constructed L. problematicus reached body lengths of up to 16.5 m. based on the phylogenies provided by Betancur et al. (Liston et al. 2013), which would make it the largest bony (2013) and Velez-Zuazo & Agnarsson (2011) using Mes- fish known among both living and fossil species, and is quite software version 3.2 (Maddison & Maddison 2017). approximately the size of the largest chondrichthyan. RMR data were temperature adjusted to 20, 25 and 30°C Recently, some metabolic aspects have been proposed with a Q10 of 2 (factor by which the oxygen consumption as constraining factors of both body size and activity level increases for every 10° rise in the temperature), covering in animals. Makarieva et al. (2006) suggested that the the presumed range of temperatures inhabited by L. prob- physiological viability of all organisms is limited by a lematicus (Anderson et al. 1994; Jenkyns et al. 2012). minimum critical value of mass-specific metabolic rate. RMR and body mass data were log-transformed and PGLS Thus, since mass-specific metabolic rate decreases as the analysis was conducted, at each temperature, by means of size of organisms increases, larger sizes are not physiologi- R software version 3.4.0 (R Core Team 2017) using the cally viable once this limit has been reached. Similarly, ape package version 4.1 (Paradis et al. 2004) and the this implies that cost of locomotion at certain swimming caper package version 0.5.2 (Orme 2013) with the maxi- speeds or highly energetic activities is not affordable over mum likelihood transformation of branch lengths opti- particular size thresholds (Ferron et al. 2017). Ferron mized for the data (‘lambda = ML’). Estimated values of (2017) established a methodology for assessing the ener- lambda were used and kappa and delta were fixed at 1. getic budget and cost of locomotion in extinct aquatic L. problematicus body mass was calculated following Webb vertebrates, allowing the determination of the range of (mass = 0.01 L3; Webb 1975, following Bainbridge 1961) sizes within which a given activity (e.g. active predation using the previously-derived estimate of L. problematicus or suspension-feeding) can be sustained on a long-term maximum body length (i.e. 16.5 m according to Liston basis. Based on this idea, we here establish a similar et al. 2013; this was also used as the basis for depicting the framework to evaluate the swimming energetics of body mass of Leedsichthys in Ferron 2017 and Ferron et al. L. problematicus, shedding light on the metabolic limits of 2017) and cross-checked with a scale model as per Motani body size in actinopterygians, and discuss the possible (2001) (see Liston 2007 for full description). RMR of underlying factors that drove the gigantism and success of L. problematicus was then inferred from its body mass in Mesozoic suspension feeding pachycormiform fishes. all three scenarios by interpolation in the established models.
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