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Body-Size Trends of the Extinct Giant Shark Carcharocles Megalodon: a Deep-Time Perspective on Marine Apex Predators

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Body-Size Trends of the Extinct Giant Shark Carcharocles Megalodon: a Deep-Time Perspective on Marine Apex Predators Paleobiology, 41(3), 2015, pp. 479–490 DOI: 10.1017/pab.2015.16 Body-size trends of the extinct giant shark Carcharocles megalodon: a deep-time perspective on marine apex predators Catalina Pimiento and Meghan A. Balk Abstract.—The extinct shark Carcharocles megalodon is one of the largest marine apex predators ever to exist. Nonetheless, little is known about its body-size variations through time and space. Here, we studied the body- size trends of C. megalodon through its temporal and geographic range to better understand its ecology and evolution. Given that this species was the last of the megatooth lineage, a group of species that shows a purportedsizeincreasethroughtime,wehypothesizedthatC. megalodon also displayed this trend, increasing in size over time and reaching its largest size prior to extinction. We found that C. megalodon body-size distribution was left-skewed (suggesting a long-term selective pressure favoring larger individuals), and presented significant geographic variation (possibly as a result of the heterogeneous ecological constraints of this cosmopolitan species) over geologic time. Finally, we found that stasis was the general mode of size evolution of C. megalodon (i.e., no net changes over time), contrasting with the trends of the megatooth lineage and our hypothesis. Given that C. megalodon is a relatively long-lived species with a widely distributed fossil record, we further used this study system to provide a deep-time perspective to the understanding of the body- size trends of marine apex predators. For instance, our results suggest that (1) a selective pressure in predatory sharks for consuming a broader range of prey may favor larger individuals and produce left-skewed dis- tributions on a geologic time scale; (2) body-size variations in cosmopolitan apex marine predators may depend on their interactions with geographically discrete communities; and (3) the inherent characteristics of shark species can produce stable sizes over geologic time, regardless of the size trends of their lineages. Catalina Pimiento. Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, U.S.A.; Department of Biology, University of Florida, Gainesville, Florida, U.S.A. and Smithsonian Tropical Research Institute, Box 2072, Balboa, Panama. E-mail: pimientoc@ufl.edu Meghan A. Balk. University of New Mexico, Albuquerque, New Mexico 87131, U.S.A. Accepted: 24 March 2015 Supplemental materials deposited at Dryad: doi:10.5061/dryad.6q5t4 Introduction importantly, apex predators are pivotal in maintaining ecosystem stability, and their elim- The extinct megatooth shark Carcharocles ination can produce cascading effects through- megalodon is the largest shark ever to exist out entire food webs (Myers et al. 2007; (Gottfried et al. 1996). From its tooth size and Terborgh et al. 2010; Estes et al. 2011). Accord- morphology, it was inferred to have been an ingly, the extinction of C. megalodon potentially apex predator that reached up to ~ 18 m of total affected the structure and function of ancient length (TL) (Gottfried et al. 1996; Pimiento et al. ecosystems (Pimiento and Clements 2014). The 2010; Pimiento et al. 2013a). Furthermore, causes of its extinction are still unknown. given the nearly global distribution of its fossil The phylogenetic relationships of C. megalodon record, C. megalodon is considered to have been have mainly been studied on the basis of its a cosmopolitan species that lived from relatedness to the great white shark, Carcharodon ca. 15.9 Ma (middle Miocene) to ca. 2.6 Ma carcharias (e.g., Long and Waggoner 1996; (Pliocene/Pleistocene boundary) (Applegate Martin 1996). To our knowledge, no phylogenies and Espinosa-Arrubarrena 1996; Gottfried for this species have ever taken into considera- et al. 1996; Purdy 1996; Purdy et al. 2001; tion all its ancestors. Thus, the taxonomy of Cappetta 2012; Pimiento and Clements 2014). C. megalodon has long been debated, with a Apex predators are animals with no preda- number of possible interpretations. For instance, tory pressures. Usually they are large-bodied some authors place it in the genus Carcharodon vertebrates that can move over large areas, thus (family Lamnidae) (e.g., Applegate and Espinosa- interacting with different communities. Most Arrubarrena 1996; Gottfried et al. 1996; Purdy © 2015 The Paleontological Society. All rights reserved. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. 0094-8373/15 480 CATALINA PIMIENTO AND MEGHAN A. BALK 1996), whereas others place it in the genus Pliocene Carcharocles (Family Otodontidae) (e.g., Ward and Bonavia 2001; Nyberg et al. 2006; Ehret Late et al. 2009; Ehret 2010; Pimiento et al. 2010; Miocene Cappetta 2012). Using the most recent morpho- Middle logical evidence (e.g., Nyberg et al. 2006; Ehret Miocene et al. 2009), we follow the second interpretation. Early Carcharocles Regardless of its taxonomic assignment, it is Miocene megalodon widely accepted that C. megalodon is the largest member of the megatooth lineage, an extinct Late group of large predatory sharks. It has been Oligocene Carcharocles proposed that the megatooth sharks comprise chubutensis a series of chronospecies (i.e., a group of Early Oligocene species that evolve via anagenesis and that gradually replace each other in a evolutionary Carcharocles Late angustidens scale [Benton and Pearson 2001]) that are Eocene distinguished from each other in the fossil Early record by the morphological changes of their Eocene Carcharocles auriculatus teeth (Ward and Bonavia 2001). These changes include the loss of lateral cusplets (Ward and Bonavia 2001; Ehret 2010; Pimiento et al. 2010; Otodus Pimiento et al. 2013b); broadening of tooth obliquus crowns; and, of most relevance to this study, FIGURE 1. Schematic representation of the changes in size increase through geologic time (Ehret tooth morphology within the megatooth lineage: cusplet 2010). Because tooth size has been demon- loss, broadening of tooth crowns, and size increase. Scheme based on the work of Ehret (2010). strated to be a good proxy of body size in lamnoid sharks (Gottfried et al. 1996; Shimada 2003; Pimiento et al. 2010), we can infer that the observed chronoclinal tooth size trend of the body-size distribution pattern, where the megatooth linage (Fig. 1) translates into a majority of species are small and a few are macroevolutionary body-size increase over large (Kozlowski and Gawelczyk 2002; geologic time. O’Gorman and Hone 2013). This pattern has Body size has long been of interest to scientists, been demonstrated in mammals, birds, rep- not only because it is a relatively easy trait to tiles, amphibians, and fish, but not in dinosaurs quantify in both living and fossil organisms (left-skewed) or snakes (not skewed) (Boback (Peters 1983; Maurer et al. 1992; Kingsolver and and Guyer 2003; Lyons and Smith 2010; Pfennig 2004; Smith et al. 2008), but also because O’Gorman and Hone 2013). Moreover, body- it correlates with many ecological and evolu- size patterns are driven by clade- or region- tionary patterns (Peters 1983; Calder 1996; Smith specific mechanisms, which produce both et al. 2008). For example, body-size distributions positive and negative correlations between are an important component of community body size and latitude (Cushman et al. 1993; structure and thus are often studied to infer Atkinson 1994). It has also been argued that selection pressures (Peters 1983; Werner and body-size distributions are invariant along Gilliam 1984; Bell et al. 2006). Furthermore, body latitudinal gradients (Roy et al. 2000). To our size is highly correlated with geographic dis- knowledge, there have been no studies tribution, making it the most common and investigating body-size trends (either body- repeatable relationship studied in macroecology size distributions or body-size geographic (Lyons and Smith 2010). patterns) at the species level of any marine Body size has important implications for apex predator over a geologic time scale. a species’ ecology. Many clades have a log- Little is known about the body-size trends of skewed (right-skewed on logarithmic axes) the extinct apex predatory shark C. megalodon MEGALODON BODY-SIZE TRENDS 481 over geologic time. Because body size predic- their specimens for signs of abrasion (as an tably scales with many aspects of species’ indicator of redeposition; e.g., Boessenecker biology, here we study body-size trends of et al. 2014), we selected only well-preserved, C. megalodon across time and space as a means relatively complete specimens with adequate to better understand the ecology and evolution stratigraphic information for inclusion in of this species. Given that C. megalodon was the our study. largest of a lineage with a purported body-size Tooth Measurements.—We measured tooth increase over time, we hypothesize that this crown height (CH) and width (CW) of a total species increased in size through time, reach- of 544 C. megalodon specimens from 32 ing its largest size prior to extinction. In order localities, 26 formations, and nine countries to reach our research objectives and test our (Fig. 2). Another 51 specimens were measured; hypothesis, we estimated the body size of however, they either showed signs of individuals from a large sample across regions redeposition or lacked sufficient stratigraphic and time periods, compared trends through information to be included in our analyses. the species’ temporal and geographic range, These include 30 teeth from the Red Crag and tested its general mode of size evolution. Formation (U.K.) that were clearly eroded, and Our results provide novel information on the 21 specimens from the Middle Globigerina macroecological patterns of this extinct giant Limestone (Malta) that did not have accurate shark. Moreover, because C. megalodon is a stratigraphic information. These teeth are all long-lived species (~14 Myr) with a widely deposited in the NHM collection.
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