We propose that the Miocene Gatun Formation represents the first documented paleo-nursery area for C. megalodon from the Neotropics, and one of the few recorded in the fossil record for an extinct selachian. We therefore show that sharks have used nursery areas at least for 10 millions of years as an adaptive strategy during their life histories.

We collected and measured fossil shark teeth of C. megalodon, within the highly productive, shallow marine Gatun Formation from the Miocene of Panama. Surprisingly, and in contrast to other fossil accumulations, the majority of the teeth from Gatun are very small. Here we compare the tooth sizes from the Gatun with specimens from different, but analogous localities. In addition we calculate the total length of the individuals found in Gatun. These comparisons and estimates suggest that the small size of Gatun's C. megalodon is neither related to a small population of this species nor the tooth position within the jaw. Thus, the individuals from Gatun were mostly juveniles and neonates, with estimated body lengths between 2 and 10.5 meters.

As we know from modern species, nursery areas are essential shark habitats for vulnerable young. Nurseries are typically highly productive, shallow-water habitats that are characterized by the presence of juveniles and neonates. It has been suggested that in these areas, sharks can find ample food resources and protection from predators. Based on the fossil record, we know that the extinct Carcharocles megalodon was the biggest shark that ever lived. Previous proposed paleo-nursery areas for this species were based on the anecdotal presence of juvenile fossil teeth accompanied by fossil marine mammals. We now present the first definitive evidence of ancient nurseries for C. megalodon from the late Miocene of Panama, about 10 million years ago.

Funding: This project was funded by NSF EAR 0418042 ( http://www.nsf.gov/funding ), Sigma Xi G2009100426 ( http://www.sigmaxi.org/programs/giar/index.shtml ), The Florida Museum of Natural History ( www.flmnh.ufl.edu ), The Smithsonian Tropical Research Institute ( www.stri.org ), The Mitchell Hope Scholarship ( http://www.southwestfloridafossilclub.com/ ) and the Ken Ericson Scholarship ( http://www.flmnh.ufl.edu/vertpaleo/kenericsonscholarship.htm ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Sharks, especially large species, are highly mobile organisms with a complex life history and wide distribution. During their lifetime they generally utilize three types of areas: adult feeding, reproduction and nurseries [1]. In modern species, nursery areas are historically defined by the presence of gravid females and free-swimming neonates. It is also an area that can be shared by several shark species, where young sharks spend their first weeks, months or years [2]. More recent studies have defined nursery areas as geographically discrete essential zones for shark survival [3] that provides them with two types of benefits: protection from predation (mainly larger sharks [2]) and abundant food resources. Productive, shallow-water ecosystems thus provide sharks significant protection from larger predators and/or abundant food resources, both of which are essential to survival [4].

The Gatun is a highly fossiliferous Neogene formation located in the Isthmus of Panama (Figure 1) with a diverse fauna of sharks [5]–[7]. It was located within a marine strait that connected the Pacific Ocean and the Caribbean Sea during the late Miocene (∼10 Ma) [8]. Studies of different taxa, including the exceedingly diverse molluscan fauna, indicate that it was a shallow-water ecosystem (∼25 m depth) with higher salinity, mean annual temperature variations, seasonality and productivity relative to modern systems in this region [7], [9]–[13]. Over the past 20 years, the Gatun Formation localities have been extensively used to extract sediment for construction. During the more recent years, these extraction activities have increased substantially. Based on our observations made during the two past years of fieldwork, we predict that these outcrops will soon likely be excavated completely. Therefore it is timely and urgent to study the fossils occurring in these outcrops before they are no longer available to science.

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larger image TIFF original image Download: Figure 1. Study area. A. Location of Panama and the Gatun Formation. The shaded box represents the general study area in northern Panama. B. Expanded geological map (from “See Below” shaded box in Fig. A). This map shows the exposures of the Gatun Formation and surrounding rock units (modified from Coates et al., 1992). The two fossil localities collected from the Gatun Formation during this study include: (1) Las Lomas and (2) Isla Payardi. https://doi.org/10.1371/journal.pone.0010552.g001

Fossil sharks were first reported from Panama in 1862 [5]. In 1984, the first description of the elasmobranchs from the Gatun Formation was published [6]. More recently, in 2010 the biodiversity of the fossil sharks from the Gatun has been documented from large new collections, and comprise 16 recognizable taxa. This work also included paleoecological and paleodepth analyses that supported the interpretation of the paleoecology of the Gatun Formation as shallow-water habitat in a productive environment [7].

Although it is not very common, the extinct Carcharocles megalodon (Agassiz 1843) is one of the species that occurs in the Gatun Formation. The taxonomic assignment of this species has been debated for nearly a century, and there are three possible interpretations: (1) Some authors place C. megalodon and other megatoothed sharks with the extant white shark (Carcharodon carcharias) in the same genus (Carcharodon) and therefore the same family (Lamnidae) [14]–[16]. (2) Other authors place C. megalodon and megatoothed sharks in a different genus (Carcharocles) and family (Otodontidae) [17]–[23]. Although a minority point of view, some workers recognize (3) megatoothed sharks as a series of chronospecies of the genus Otodus, and place all megatoothed sharks except C. megalodon in this genus. Furthermore, C. megalodon is assigned to the genus Megaselachus, based on the loss of lateral cusplets [24]. We follow the second hypothesis; that Carcharocles megalodon and Carcharodon carcharias belong to separate genera in different families. However, both species belong to the order Lamniformes, and in the absence of living members of the Otodontidae, C. carcharias should be regarded as ecologically analogous species to C. megalodon. We base this analogy on the fact that both species share similar ecological niches with presumed similarities in body shape, feeding habits, and overall tooth and vertebral centrum morphology. Even though these species are not direct relatives, no other extant lamniform species share as many characteristics with C. megalodon as does C. carcharias.

C. megalodon is widely regarded as the largest shark to have ever lived. Based on tooth crown height (CH), this giant reached a total length (TL) of more than 16 m. One single tooth can exceed more than 168 mm of total height [14]. The diagnostic characters of C. megalodon teeth include: large size, triangular shape, fine serrations on the cutting edges, a convex lingual face, a slightly convex to flat labial face, and a large v-shaped neck [7]. Juvenile specimens of C. megalodon can have lateral cusplets [15], or not [22]. The size and shape of the teeth vary within the jaw: anterior teeth are large and symmetrical whereas the latero-posterior teeth are asymmetrical with slanted crowns. Moving antero-posteriorly through the jaw, there is a slight initial increase in size on either side of the mid-line, followed by a progressive decrease that continues to the last tooth, e.g. [25] (Figure S1). Fossil teeth of C. megalodon range in age from 17 to 2 Ma (middle Miocene to Pleistocene) and have a cosmopolitan distribution [7], [14], [16].

Of relevance of this study, two shark paleo-nursery areas have previously been proposed: the Paleocene Williamsburg Formation of South Carolina, based on the presence of juvenile teeth of four lamnoid taxa [26]; and the late Oligocene Chandler Bridge Formation of South Carolina, based on the abundance of juvenile Carcharocles teeth, accompanied by small odontocete and mysticete skulls, which are assumed to be their prey species [16]. However, neither of the collections from these two localities have been rigorously analyzed and thus the presence of paleo-nurseries remained anecdotal until the present report.

The presence of mammals as potential prey does not represent evidence of a shark nursery area. As known from modern studies of sharks, the main purpose of the nursery areas is not feeding [1]–[4]. Studies have shown that some shark species do not consume large quantities of food during their juvenile stages [27]–[28]. Even when high-productivity nursery areas provide ample food resources for juvenile sharks, some species select these habitats more for predator avoidance and not food consumption [3]–[4]. Furthermore, some shark species present an ontogenetic shift in feeding patterns [29]–[32]. For example, the lamnoid white shark (C. carcharias) feeds mostly on fishes (including other sharks) during their juvenile stage and on mammals during their adult stage [33]–[35]. Marine mammals are not commonly found in the Gatun Formation. On the other hand, bony fish otoliths [36] and other shark species [7] are abundant, representing a food source for the marine fauna that lived in this diverse environment.

In this study C. megalodon teeth were collected and measured from two localities within the Gatun Formation of Panama (Figure 1). Surprisingly, large teeth are uncommon with specimens recovered having CH ranging between 16 to 72 mm (Figure 2). The objective of this work is to determine if the late Miocene Gatun Formation was used as a nursery area by young C. megalodon. Accordingly, we compared the tooth sizes from the Gatun Formation with those found in older and younger formations to determine if the smaller size distribution observed is unique to the species during the late Miocene. In addition, we compared these sizes with tooth sets from individuals of different life stages to determine if the small size observed is related to age, or position within the jaw. Finally, we calculated the TL of all C. megalodon individuals from the Gatun Formation to estimate their life stage. The results obtained in this study from tooth measurement comparisons and individual total length estimates allowed us to determine the age class/size of individuals that inhabited the shallow-water habitats of the late Miocene Gatun Formation, ∼10 million years ago.