Saturday, January 13, 2024

Some recent advances in late Cenozoic shark paleontology

When I first started out in paleontology as an undergraduate in the mid 2000s, I had a background in fossil sharks. I collected shark teeth in high school and they ultimately got me hooked on marine mammals. However, it seemed like most of the publishing effort on fossil sharks at the time, and up until 2014-2015, had focused chiefly on Mesozoic through Eocene sharks and the study of Neogene (Miocene, Pliocene; 23-2.6 Ma) sharks was quite stagnant. One major exception at the time was the hallmark publication by Purdy et al. 2001 in Lee Creek Volume III, on the fossil sharks, rays, and fish from the Pungo River Limestone and Yorktown Formation. However, it feels that recently - since the start of the pandemic - the publishing rate on Neogene sharks has exploded - especially as regards the megatoothed sharks. There are more papers on Carcharocles megalodon in the past five years than the prior thirty (estimate, I'm too lazy to actually count - though I suspect that's actually going to be a conservative figure). So, I figure it's about time to cover some of this territory.

Lamniform sharks (plus Squatina, Hexanchus, and Pristiophorus) from the latest Miocene-late Pliocene aged Purisima Formation in California - from Boessenecker (2011), the first paper I ever wrote, and one of the first ones I ever published.

I started working on my first paper reporting fossil sharks in fall 2006 - eventually submitted sometime in 2010 and published, of all days, on the day of my wedding to Sarah in 2011 (only about an hour before we left for the venue). This paper (Boessenecker, 2011) in Palarch's Journal of Vertebrate Paleontology reported fossil sharks, skates, bony fish, and some sea bird remains from a formely unstudied locality in the Purisima Formation, and focused on a bunch of fossils I had collected. I had a firmer grasp of the identifications and morphology of the non-mammals, and the marine mammal remains would have to wait. 

While I was in college, not much was published on mid-late Cenozoic sharks - but I'll briefly list some of the more salient articles. Sylvain Adnet et al. (2006) published an interesting study documenting body size changes in the cow shark Hexanchus through geologic time. Somewhat later, Adnet et al. (2010) reported an unusually large fossil great white shark tooth from Spain suggestive of larger body size in the past. The tired argument regarding whether or not C. megalodon was related to great whites was finally addressed in a morphometric analysis by Nyberg et al. (2006), who found that it is not very similar to Carcharodon carcharias. Catalina Pimiento et al. (2010) reported a Carcharocles megalodon nursery assemblage from the Miocene of Panama and followed it up with a pretty impressive study of the entire shark fauna from the same locality (Pimiento et al., 2013). The infamous "transitional" great white shark dentition from the Pisco Formation of Peru was finally described by Dana Ehret et al. (2009) and shortly thereafter formally named Carcharodon hubbelli (Ehret et al., 2012). Christy Visaggi and Stephen Godfrey (2010) published a survey of shark teeth from Calvert Cliffs in Maryland, comparing ex-situ teeth found on the beach with teeth found in situ from the cliffs and examining issues like collections bias. 

Research seemed to pick up a bit during my Ph.D. program (2011-2015). Bruce Welton returned to publishing after his retirement and published some papers on fossil basking sharks, including naming the archaic genus Keasius (Welton, 2013). The extinct megamouth shark from the Oligocene of Pyramid Hill, California, was finally named as Megachasma applegatei (Shimada et al., 2014). A number of shark assemblages from South America, Central America, and the Caribbean were reported (Aguilera et al., 2017; Carillo-Briceno et al., 2016; Carillo-Briceno et al., 2016; Carillo-Briceno et al., 2015; Carillo-Briceno et al., 2015; Staig et al., 2015; Carrilo-Briceno et al., 2014). Jurgen Kriwet et al. (2014) named a new genus for Isurus/Cosmopolitodus escheri, placing it in Carcharomodus. Perhaps the most important study published in the interim was by Kent (2018), who reported the shark and ray fauna of Calvert Cliffs in Calvert Cliffs Volume I. Most critically, and perhaps preceding the recent flourishing of research on Neogene sharks, was a flurry of articles on megatoothed sharks including a statistical analysis supporting a relatively recent extinction for Carcharocles megalodon (Pimiento and Clements, 2014), a study of body size change in Carcharocles (Pimiento and Balk, 2015), the naming of a new dwarf megatoothed shark Megalolamna (Shimada et al., 2016), a study of paleogeographic distribution of Carcharocles megalodon (Pimiento et al., 2016), and a report of long-forgotten C. megalodon teeth from California and a comprehensive reanalysis of its extinction (supporting a much older, "mid" Pliocene extinction) by yours truly (Boessenecker et al., 2019).

This blog post will focus on summarizing some of (but certainly not all) of the papers since the Covid-19 pandemic started that report new occurrences, assemblages, and findings on Neogene sharks - and Oligocene sharks as well (since Oligocene assemblages have more in common with Miocene than Eocene assemblages). If I've missed something you'd like me to include, please let me know in the comments and I'll consider updating the article!

Examples of fossil sharks and the rarefaction analysis from Chavez-Hoffmeister and Villafana (2022).

Shark Assemblages

Chavez-Hoffmeister and Villafana (2022) report an aggregate fossil assemblage of sharks and rays from three different formations along the northern coast of Chile - the Coquimbo Formation, La Portada Formation, and the famous Bahia Inglesa Formation (near Caldera, Chile). The study is more of a checklist and identification guide than a formal description of a chondrichthyan assemblage - but that's actually the goal of the study. The study acknowledges the extractive role of illegal fossil digging in Chile that led to large numbers of shark teeth being sold, without provenience, on the black market. Fortunately, this has slowed considerably and permitted Chilean researchers to actually collect specimens with stratigraphic data. For context - there is considerable confusion as to the stratigraphic record of Carcharodon carcharias within the Bahia Inglesa Formation, no doubt a cause of the 1) poor stratigraphic control over the years and 2) poor collection of stratigraphic data by illegal fossil diggers. This study also used a rarefaction analysis to estimate how many additional species may await discovery, suggesting that only 3/4 of the fauna had been detected.

Oligo-Miocene sharks from Ecuador, reported by Carillo-Briceno et al. (2020).

An assemblage from the Oligocene-Miocene boundary (~23 Ma; Montanita-Olon) of Ecuador was reported by Carillo-Briceno et al. (2020). Like other Pacific assemblages covered elsewhere in this post, there's much more in the way of deep water sharks present, including Heptranchias, Centrophorus, Echinorhinus, Mitsukurina, and Pristiophorus. Some of the regular suspects are present as well - Carcharocles chubutensis/angustidens, Carcharias, Odontaspis, Parotodus, Carcharhinus, Galeocerdo, Alopias, Hemipristis, etc. This study reports many new records for the Tropical east Pacific and South America.

The sample of Carcharocles angustidens teeth from the original Chandler Bridge excavation, along with our reconstructed body length curves - clearly dominated by juvenile sharks. From Miller et al. (2021).

In 2021 my student Addie Miller, Matt Gibson (natural history curator at Charleston Museum), and I published a paper reporting an assemblage of Carcharocles angustidens teeth from the Chandler Bridge Formation here in South Carolina. The teeth are from a location where only we had access (and given my frequent visits, there were very few if any folks who snuck onto the property). Mostly all we found were small teeth. Addie reconstructed the body sizes from each tooth by identifying the likely tooth position, plugging each measurement into a different tooth-by-tooth set of equations developed earlier by Kenshu Shimada for great white sharks. Then, she generated a size distribution curve - and determined that nearly all of the specimens were from individuals that were only half grown in body size or smaller. She also did the same for a larger assemblage of teeth from the original Chandler Bridge excavation, briefly mentioned in a 1996 book chapter by Bob Purdy - and duplicated the results. Two different localities in the same rock unit, a couple of miles apart, collected nearly 50 years apart by different researchers! These results indicate that the Charleston Embayment was likely used as a nursery area by megatoothed sharks in the Oligocene. 

 Analysis of body size distribution in Carcharodon carcharias teeth from  three different localities in the Pliocene of South America: Pisco Formation of Peru, Coquimbo and Caldera in Chile - from Villafana et al. (2020).

Another nursery area was reported by Villafana et al. (2020) for the extant great white shark (Carcharodon carcharias) from the Coquimbo Formation of Chile. Teeth from the Pisco Formation of Peru and the Bahia Inglesa Formation further north at Caldera (Chile) are dominated by subadults and adults. This is the first well-documented nursery area for Carcharodon carcharias in the fossil record, and I suspect many more have yet to be identified and studied.

Fossil sharks from the lower Miocene molasse of Switzerland, reported by Villafana et al. (2020).

A diverse assemblage of sharks from the early Miocene aged Achen Formation in the Molasse of Switzerland was reported by Villafana et al. (2020). This assemblage includes 37 taxa, some of which are deep water species like Chlamydoselachus, Notorhynchus, Squalus, Deania, Isistius, Mitsukurina, Scyliorhinus, Pachyscyllium, Paragaleus, and Chaenogaleus. Other more typical shelf-inhabiting (or otherwise shallow water) sharks like Alopias, Carcharias, Carcharhinus, Squatina, Galeocerdo, Physogaleus, Sphyrna, Rhizoprionodon, Myliobatis, Rhinoptera, Dasyatis, and others.

Fossil sharks from the Liuchungchi Formation of Taiwan, from Lin et al. (2022).

Lin et al. (2022) report a rare example of a shark assemblage from the early Pleistocene - and better yet, from an unusual location: Taiwan. Owing to low sea level in general and the repeated and rapid changes in sea level, Pleistocene marine vertebrate-bearing fossil assemblages are quite rare because they are either underwater, never deposited, or have been completely eroded away. In this case, there are abundant specimens of Carcharodon carcharias, and some of the first Pleistocene records of Hemipristis serra from the Pacific basin - now completely extinct.

 Sharks from the Duho Formation of South Korea - reported by Malyshkina et al. (2023).

A somewhat older shark assemblage from another unusual western North Pacific location - the Duho Formation of South Korea - was reported by Malyshkina et al. (2023). They report a mixed pelagic and deep marine assemblage including kitefin sharks (Dalatias), cow sharks (Hexanchus), basking sharks (Cetorhinus), makos (Isurus sp. 1 and 2, Cosmopolitodus hastalis and "Isurus" planus), megatoothed sharks C. megalodon and Parotodus benedeni, a bunch of reef sharks (Carcharhinus spp.) and a tiger shark (Galeocerdo aduncas). 

Shark and ray teeth found ex situ on beaches of the northeastern Gulf coast (MI/FL) - from Clinton et al. (2023).

An ex-situ assemblage was reported from the coastline of Mississippi and the panhandle of Florida by Clinton et al. (2023). These fossils are likely from Pliocene and Pleistocene marine strata - several different formations are possible sources. These teeth were all collected by beachcombing - picking up fossil teeth on beaches on the Atlantic and Gulf coasts is a very popular hobby. I've found a single tooth this way on the Pacific coast, and thousands here in South Carolina alone; about 700 such teeth were reported from this survey. Taxa include the usual suspects for the southeast: Carcharhinus, Negaprion, Galeocerdo, Rhinoptera, Aetobatus, and others.

New specimens of the tiny megatoothed shark Megalolamna paradoxodon from the Miocene Maryland (A-H) and Oligocene of South Carolina (I-M), from Shimada et al. (2023).

More on Carcharocles megalodon and friends

Just last week, Kenshu Shimada, Victor Perez, Bretton Kent, and I published a new article reporting new records of the tiny megatoothed shark Megalolamna paradoxodon from the Miocene Calvert Formation of Maryland and the Oligocene Chandler Bridge Formation of South Carolina. The first is a first record for the state of Maryland, but the second extends the range of Megalolamna well into the Oligocene epoch (though I'll note that one specimen from the Jewett Sand at Pyramid Hill is from right around the Oligocene-Miocene boundary, and the locality has been considered to be of Oligocene age in the past and only recently revised).

Growth lines in the vertebra of C. megalodon - from Shimada et al. (2020).

A couple of papers from 2020 dove into the life history and body size of C. megalodon. The first of these by Shimada et al. (2020) studied the growth of C. megalodon using growth lines in a vertebra from an associated set of vertebrae from the Miocene of Belgium. The first growth band was laid down at a relatively large size, indicating a size at birth of about two meters! Enormous babies like this indicate that C. megalodon likely achieved such large fetal sizes through intrauterine cannibalism - one fetal shark swimming around inside the uterus for quite some time and eating successive rounds of eggs - such in some extant mackerel sharks. Another study by Shimada et al. (2020) evaluated recent hypotheses of 'regional endothermy' from prior studies of body size modeling. Shimada et al. reconstructed the maximum body length of C. megalodon at about 14.5 meters (~48 feet). Endothermy has previously been hypothesized for explaining gigantism in C. megalodon and other lamiform sharks - but Shimada et al. point out that this may have been in turn driven by live birth and intrauterine cannibalism.

Possible life reconstruction of Carcharocles megalodon based on the allometry of modern lamniform sharks - from Cooper et al. (2020).

A recent study by doctoral student Jack Cooper and colleagues (2020) produced a new two dimensional reconstruction of the body proportions of C. megalodon. They studied the proportions of the fins and tail throughout growth (allometry: change in proportions during growth) of five modern mackerel sharks including great whites (Carcharodon), both species of makos (Isurus), and two species of Lamna, in order to predict what the proportions would be in such a gigantic shark. Based on these predictions, they hypothesized that C. megalodon was a rapid, active swimmer. However, this was recently criticized by Sternes et al. (2022) given that none of this was based on actual fossil data. Sternes et al. further highlighted a lack of correlation between body form in lamniform sharks and their thermophysiology, suggesting a limited implication of these models on understanding the life history and behavior of C. megalodon. Modeling is great, but in this case I feel like it was pretty far divorced from what we can actually know from the fossils.

Nursery assemblage of juvenile C. megalodon teeth from Spain and other assemblages from around the world - from Herraiz et al. (2020).

A short paper by Herraiz et al. (2020) reported several nursery assemblages of C. megalodon from around the world, including a new assemblage from Spain - but also the Calvert Formation of Maryland, Bone Valley Formation of Florida, and the Chucunaque Formation of Panama. Each of these assemblages was found to be dominated by juvenile sized teeth. This study generated a response by Shimada et al. (2021), who indicated that some degree of this might be influenced by latitude, with larger individuals possibly inhabiting higher latitudes, and smaller individuals at lower latitudes - an example of Bergmann's Rule.

3D modeling of the body form of C. megalodon by Cooper et al. (2022).

This was shortly thereafter revisited by Cooper et al. (2022), who did a somewhat more data-based approach and attempted to reconstruct the 3D body form of C. megalodon based on a known set of associated vertebrae from the Miocene of Belgium and also an attempted reconstruction of the cranium and jaws based on a fossil tooth set of C. megalodon from the USA and scaling up the cartilaginous chondrocranium of a great white shark. The results surprisingly differ quite a bit from the reconstruction by Cooper et al. (2020), as the pectoral and tail fins seem quite a bit smaller than the prior reconstruction. Again, acknowledging that there is an enormous amount of wiggle room here is being overly modest: we don't know what the body of C. megalodon looked like and likely never will, and I'm not certain how repeatable this is. However, another study did report new fossils that can actually test this...

Representative examples of placoid scales from the Japanese C. megalodon specimen, from Shimada et al. (2023).

Another recent study by Kenshu Shimada et al. (2023) weighed in on the recent controversy over the ecology of C. megalodon by reporting the first assemblage of placoid scales (denticles) from the species. One of the few specimens of C. megalodon consisting of associated teeth that had been competently collected is an associated tooth set reported in the late 1980s from the Miocene of Japan. One of the preparators of the specimen had the foresight to save large samples of matrix from the specimen. Kenshu asked for the matrix and screened through it - revealing a spectacular assemblage of 589 (!!!) scales, from only about 30 cubic centimeters of matrix. They also report a number of cartilage fragments. The individual carilaginous tesserae (prisms of prismatic cartilage) are the same size and structure of regular-sized modern sharks, indicating that gigantism in sharks does not require an increase in the size of the tesserae. The placoid scales of this specimen are noteworthy because they give us some unprecedented information about the swimming speed of C. megalodon - scale morphology in sharks is generally linked to their life habits. Scales are generally similar in morphology to mako sharks, but large in size and comparable to some pelagic carcharhiniforms like blue sharks (Prionace) and reef sharks (Carcharhinus). Analysis of the distance between keels on the scales suggests that C. megalodon was actually a somewhat slow cruising swimmer with the occasional burst of speed.

A manganese oxide-encrusted C. megalodon tooth from the deep sea floor reported by Pollerspock et al. (2023).

A new study by Pollerspock et al. (2023) reports the first discovery of a C. megalodon tooth found in situ on the seafloor. Many such specimens have been reported over the past 150 years, including specimens found on the expedition by the HMS Challenger - but all previous examples were dredged from their context. This specimen was found by an ROV on the top of a seamount at a depth of three kilometers (still quite deep!). These authors point out that the coastal ecology of C. megalodon inferred from the fossil record may be biased towards deposits above sea level, and that future discoveries from the deep sea might adjust these hypotheses somewhat.

Mediterranean specimens of the "false mako" Parotodus benedeni from Collareta et al. (2023).

A more obscure paper on "the other megatooth" - Parotodus (aka false mako) - was published just a few months ago by Alberto Collareta et al. (2023)* - this study reports new specimens of Parotodus benedeni from the Pliocene of Italy and took the opportunity to review the state of knowledge of the paleobiology of this species. They indicate a maximum body size of around 7 meters (roughly 20-22 feet), support a pelagic (open ocean) lifestyle for this shark owing to its rarity in shallow marine deposits, and likely very different feeding ecology as compared to its bigger cousin C. megalodon given the stouter unserrated teeth and relatively limited pattern of tooth breakage/chipping - perhaps suggesting feeding on soft prey such as rotting whale carcasses (a very Hornerian style hypothesis, a la scavenging T. rex).

*funny story, I've been talking with Kenshu Shimada about some proposed research on this shark, and when I ran into him the first day of the Society of Vertebrate Paleontology conference he asked me if I had read the most recent paper on it. "No?", I responded. He said "Wait, I've got a paper copy, I just finished reading it" and handed me a printout. I did not recognize the title and so I looked for the publication date - "Kenshu, this was published yesterday! There's no way I would have seen it!" We had a good laugh about it and he gave me the copy, which I read on the elliptical after I got home to Charleston.

Noteworthy studies reporting one or two taxa

 Late Miocene sharks from South Korea reported in various papers by Yun (2020, 2021).

A number of fossil occurrences of sharks from South Korea were recently reported by Yun (2020), Yun (2021), and Yun (2021) including the ancestral great white Carcharodon hastalis, "hooktooth mako" Cosmopolitodus planus, goblin shark Mitsukurina lineata, and kitefin shark Dalatias licha. In one of these papers, Yun formally transferred the species Isurus planus to Cosmopolitodus, a genus that was originally designated for the species Isurus hastalis. Yun disagreed with the placement of 'hastalis' within Carcharodon (e.g. Ehret et al., 2009), and stuck it back in Cosmopolitodus - the genus for the broad toothed makos. Owing to the similarity with C. hastalis, 'planus' was also transferred to this genus. Additionally, see Malyshkina et al. (2022) above.

The oldest known Cosmopolitodus planus specimen, early Miocene, Sakhalin, Russia - from Malyshkina et al. (2023).

Malyshkina et al. (2023) report the oldest known specimen of Cosmopolitodus planus, the extinct and poorly understood "hooktooth mako" as it's called in California. This species is widely known from the Pacific coast of North America, particularly from Sharktooth Hill; I've collected many such specimens from there and the Santa Margarita Sandstone near Santa Cruz. Additional records are known from Japan and Australia (and New Zealand; sea below!). Unfortunately, whether this occurrences is from the earliest or late early Miocene is unclear as the deposits in Sakhalin and Kamtchatka require considerable further stratigraphic study.

The first records of Carcharodon hubbelli and Carcharodon planus from New Zealand - from Ehret et al. (2023).

A recent paper (that actually came out shortly before Malyshkina et al., 2023) by Dana Ehret, Marcus Richards, Alan Tennyson, and myself reported some specimens of sharks including the first records of Carcharodon hubbelli and Cosmopolitodus planus from New Zealand. The record of C. hubbelli is noteworthy as it has previously been reported from Peru, California, Japan, and perhaps Australia - further suggesting a Pacific-only transition for the great white, followed by a dispersal to other ocean basins like the Atlantic, Mediterranean, and Indian oceans. The new records of C. planus further illustrate a similar Pacific basin distribution - though we note the lack of this species from the Pacific coast of South America. In this paper, we further acknowledged the similarities between "planus" and "hastalis", and formally transferred "planus" to Carcharodon, forming the new combination Carcharodon planus. We also reported the oldest known specimen of this species that is well-dated, and very possibly older than the Sakhalin specimen above - one specimen from the Kaipuke Siltstone has an age determination of lower Waitakian, corresponding to Aquitanian and a likely age of 22.7 Ma (earliest Miocene).

Thresher sharks (Alopias, left) and mackerel sharks (Lamna, right) reported from Bahia Inglesa, Chile by Villafana et al. (2023).

Another similar paper by Villafana et al. (2023) reports the first fossil records of the porbeagle shark Lamna nasus and thresher shark Alopias vulpinus from the Neogene of South America. These specimens were collected from the Bahia Inglesa Formation near Caldera in Chile. This is the first report of the genus Lamna in the fossil record of the Americas, and one of only a few records - period.

Mediterranean Pliocene specimens of Carcharodon carcharias and presumed changes in food webs since the Pliocene, from Collareta et al. (2023).
A short paper by Collareta et al. (2023) reviews the record of Pliocene great white sharks (Carcharodon carcharias) from the Mediterranean. This study synthesizes fossil and molecular data, highlighting an arrival of the species sometime in the earliest Pliocene and more recent dispersal (~3 Ma) from an ancestral Australian/Pacific stock for the current population. A review of tooth size in Pliocene Italian specimens suggests considerably larger body lengths in the past versus modern shark specimens. The loss of many 'medium sized' whales in the Mediterranean during the Pliocene-Pleistocene transition suggests that great whites have weathered some major trophic changes - perhaps corresponding to a decrease in body size.

Comparison of teeth of Isurus subserratus (A-D), Carcharodon carcharias (E), and Carcharocles megalodon (F), from De Schutter et al. (2021).
In addition to the transitional great white Carcharodon hubbelli from the upper Miocene of the Pacific, there is also "Isurus" escheri from the mid-upper Miocene of the eastern North Atlantic - a narrow-toothed mako-like form with faintly serrated teeth. This species was recombined as Carcharomodus escheri a few years ago by Kriwet et al. (2014). A new study by De Schutter et al. (2021) reports new specimens of this taxon from the mid-upper Miocene of the Netherlands. However, they point out that Isurus subserratus and Isurus escheri were named on the same page of Agassiz (1843 - page 260), but subserratus was named earlier on the page - and therefore technically has priority over escheri. So, they sweep both Carcharomodus and escheri under the rug and synonymize everything with Isurus subserratus. Teeth of Isurus subserratus have much finer serrations than anything in the Carcharodon lineage, and start out narrow like shortfin mako teeth, and become gradually broader and more similar to Carcharodon in successively younger strata - and the authors group these from different horizons into Type 1, 2, 3, and 4. Unfortunately, many of the specimens (plates 5-6) reside in a private collectin (and, IMO, should not have been published upon).

Geologic range of "valid" (bold) and "invalid" species of Galeocerdo, and a comparison of Galeocerdo aduncas (A-B) and Physogaleus contortus (C) - from Turtscher et al. (2021).
A new morphometric study by Turtscher et al. (2021) evaluated the taxonomy of different species of fossil tiger sharks in the genus Galeocerdo. This study resulted in the synonymy of many species, recognizing the following as diagnosable and senior synonyms: the extant Galeocerdo cuvier of course, Galeocerdo eaglesomei (Eocene), Galeocerdo clarkensis (Eocene), Galeocerdo mayumbensis (Miocene), Galeocerdo aduncas (Oligocene-Miocene), Galeocerdo capellinii (Pliocene). This study also resurrects Physogaleus contortus, formerly considered a synonym of Galeocerdo aduncas, through careful attention to the serrations: the teeth of Physogaleus contortus and probable lower teeth of Galeocerdo aduncas both have long narrow crowns, but the crown heel (behind the distal notch) is coarsely serrated in Galeocerdo aduncas but very finely serrated in Physogaleus - requiring some careful observations before an identification can be made.

No comments: