Marine megafauna, the largest animals in the oceans, serve key roles in ecosystem functioning. Yet, one-third of these animals are at risk of extinction. To better understand the potential consequences of megafaunal loss, here we quantify their current functional diversity, predict future changes under different extinction scenarios, and introduce a new metric [functionally unique, specialized and endangered (FUSE)] that identifies threatened species of particular importance for functional diversity. Simulated extinction scenarios forecast marked declines in functional richness if current trajectories are maintained during the next century (11% globally; up to 24% regionally), with more marked reductions (48% globally; up to 70% at the poles) beyond random expectations if all threatened species eventually go extinct. Among the megafaunal groups, sharks will incur a disproportionate loss of functional richness. We identify top FUSE species and suggest a renewed focus on these species to preserve the ecosystem functions provided by marine megafauna.
BackgroundAs 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.Methodology/Principal FindingsWe 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.Conclusions/SignificanceWe 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.
The end of the Pliocene marked the beginning of a period of great climatic variability and sea-level oscillations. Here, based on a new analysis of the fossil record, we identify a previously unrecognized extinction event among marine megafauna (mammals, seabirds, turtles and sharks) during this time, with extinction rates three times higher than in the rest of the Cenozoic, and with 36% of Pliocene genera failing to survive into the Pleistocene. To gauge the potential consequences of this event for ecosystem functioning, we evaluate its impacts on functional diversity, focusing on the 86% of the megafauna genera that are associated with coastal habitats. Seven (14%) coastal functional entities (unique trait combinations) disappeared, along with 17% of functional richness (volume of the functional space). The origination of new genera during the Pleistocene created new functional entities and contributed to a functional shift of 21%, but minimally compensated for the functional space lost. Reconstructions show that from the late Pliocene onwards, the global area of the neritic zone significantly diminished and exhibited amplified fluctuations. We hypothesize that the abrupt loss of productive coastal habitats, potentially acting alongside oceanographic alterations, was a key extinction driver. The importance of area loss is supported by model analyses showing that animals with high energy requirements (homeotherms) were more susceptible to extinction. The extinction event we uncover here demonstrates that marine megafauna were more vulnerable to global environmental changes in the recent geological past than previously thought.
The late Miocene Gatun Formation of northern Panama contains a highly diverse and well sampled fossil marine assemblage that occupied a shallow-water embayment close to a purported connection between the Pacific and Atlantic (Caribbean) oceans. However, the diverse chondrichthyan fauna has been poorly documented. Based on recent field discoveries and further analysis of existing collections, the chondrichthyan fauna from this unit comprises at least 26 taxa, of which four species are extinct today. The remaining portion of the total chondrichthyan biodiversity has affinities with modern taxa and is therefore comprised of long-lived species. Based on known records of the modern geographic distribution range of the Gatun chondrichthyans, the fauna has mixed biogeographic affinities suggesting that around 10 million yr ago, a connection likely occurred between the Pacific Ocean and the Caribbean Sea. Given the known habitat preferences for modern chondrichthyans, the Gatun fauna was primarily adapted to shallow waters within the neritic zone. Finally, comparisons of Gatun dental measurements with other faunas suggest that many of the taxa have an abundance of small individuals, in agreement with previous studies that proposed this area as a paleonursery habitat for the species Carcharocles megalodon.
Carcharocles megalodon (“Megalodon”) is the largest shark that ever lived. Based on its distribution, dental morphology, and associated fauna, it has been suggested that this species was a cosmopolitan apex predator that fed on marine mammals from the middle Miocene to the Pliocene (15.9–2.6 Ma). Prevailing theory suggests that the extinction of apex predators affects ecosystem dynamics. Accordingly, knowing the time of extinction of C. megalodon is a fundamental step towards understanding the effects of such an event in ancient communities. However, the time of extinction of this important species has never been quantitatively assessed. Here, we synthesize the most recent records of C. megalodon from the literature and scientific collections and infer the date of its extinction by making a novel use of the Optimal Linear Estimation (OLE) model. Our results suggest that C. megalodon went extinct around 2.6 Ma. Furthermore, when contrasting our results with known ecological and macroevolutionary trends in marine mammals, it became evident that the modern composition and function of modern gigantic filter-feeding whales was established after the extinction of C. megalodon. Consequently, the study of the time of extinction of C. megalodon provides the basis to improve our understanding of the responses of marine species to the removal of apex predators, presenting a deep-time perspective for the conservation of modern ecosystems.
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 purported size increase through time, we hypothesized that C. 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 distributions 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.
Through elasmobranch (sharks and rays) evolutionary history, gigantism evolved multiple times in phylogenetically distant species, some of which are now extinct. Interestingly, the world's largest elasmobranchs display two specializations found never to overlap: filter feeding and mesothermy. The contrasting lifestyles of elasmobranch giants provide an ideal case study to elucidate the evolutionary pathways leading to gigantism in the oceans. Here, we applied a phylogenetic approach to a global dataset of 459 taxa to study the evolution of elasmobranch gigantism. We found that filter feeders and mesotherms deviate from general relationships between trophic level and body size, and exhibit significantly larger sizes than ectothermic‐macropredators. We confirm that filter feeding arose multiple times during the Paleogene, and suggest the possibility of a single origin of mesothermy in the Cretaceous. Together, our results elucidate two main evolutionary pathways that enable gigantism: mesothermic and filter feeding. These pathways were followed by ancestrally large clades and facilitated extreme sizes through specializations for enhancing prey intake. Although a negligible percentage of ectothermic‐macropredators reach gigantic sizes, these species lack such specializations and are correspondingly constrained to the lower limits of gigantism. Importantly, the very adaptive strategies that enabled the evolution of the largest sharks can also confer high extinction susceptibility.
Aim Given its catastrophic consequences, the extinction of apex predators has long been of interest to modern ecology. Despite major declines, no presentday species of marine apex predator has yet become extinct. Because of their vulnerability, understanding the mechanisms leading to their extinction in the past could provide insight into the natural factors that interact with human threats to drive their loss. We studied the geographical distribution patterns of the extinct macro-predatory shark Carcharocles megalodon in order to elucidate its pathway to extinction.Location World-wide from the Miocene to the Pliocene (c. 23-2.6 Ma).Methods A meta-analysis of C. megalodon occurrence records was performed using the Paleobiology Database as a platform. The data were binned into geological time slices, and the circular home range around each data point was mapped in reconstructions made in GPlates. We then quantitatively assessed the species' geographical range and global abundance over time, and the relationship between distribution and climate.Results The pathway to extinction of C. megalodon probably started in the late Miocene with a decrease in its global abundance. This decrease was then followed by a decline in its geographical range during the Pliocene. Although the extinction of C. megalodon has been attributed to climate change, we found no evidence of direct effects of global temperature. Instead, we found that the collapse in geographical distribution coincided mainly with a drop in the diversity of filter-feeding whales and the appearance of new competitors (large predatory whales and the great white shark).Main conclusions This research represents the first study of the distributional trends of an extinct, cosmopolitan apex predator in deep-time. Our results suggest that biotic factors, and not direct temperature limitations, were probably the primary drivers of the extinction of the largest marine apex predators that ever lived.
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