For 400 million years, shark-like fishes have prowled the oceans as predators, but now humans kill 100 million sharks per year, radically disrupting ocean food chains. Based on microscopic shark scales found on fossil- and modern coral reefs in Caribbean Panama, Smithsonian scientists reveal the changing roles of sharks during the last 7000 years, both before and after sharks in this region were hunted. They hope this new use for dermal denticles will provide context for innovative reef conservation strategies.

Microscopic scales covering a shark’s body—dermal denticles—reduce drag as sharks swim and protect from abrasion with hard substrates and ectoparasite attachment.

“If you have ever petted a shark in an aquarium touch tank,” said Erin Dillon, who began this study as an intern at the Smithsonian Tropical Research Institute (STRI) and is now wrapping up her doctoral work at the University of California, Santa Barbara, “denticles are the reason why shark skin is rough like sandpaper if you rub it in one direction yet smooth in the other direction. Sharks are essentially covered by millions of tiny teeth.”

Just as humans shed dry skin and dandruff, sharks shed their denticles, which accumulate in marine sediments. The oldest denticles found so far, in the Harding Sandstone of Colorado, are about 455 million years old.

STRI paleobiologist, Aaron O’Dea, pieces together clues from fossil- and modern coral reefs to reconstruct baseline conditions before human colonization, and to understand how ecological and evolutionary processes change through time.

“Placoderms in the Paleozoic, and then marine reptiles in the Mesozoic, were larger and ate sharks.” O’Dea explained. “Placoderms ruled the oceans for around 70 million years and marine reptiles of the Mesozoic ruled for more than 100 million years. Sharks are only top predators now because extinction events preferentially took out other groups but allowed sharks to survive. Sharks seem to have remarkable evolutionary resilience and I was fascinated to work on a technique that would help us explore how sharks have fared more recently when humans step into the picture.”

His team sampled material from a 7000-year-old fossilized reef in Bocas del Toro, Panama and nearby modern Caribbean reefs. O’Dea asked Erin Dillon to see if she could find shark denticles in the samples.

“What started as a three-month-long internship turned into a two-year stay in Panama and then expanded into part of my PhD thesis,” Dillon said. “I’ve grown with this project as my role shifted from first exploring and processing the samples as an intern to leading the project, analyzing and interpreting the data, and spearheading the writing.”

For each week or so of collecting samples from fossil reefs and modern coral rubble, it took about a year of lab work to recover and identify the denticles. In total, Dillon and colleagues had to sift through around 300 kilograms of reef sediments, enough to fill two bathtubs, to find the denticles they needed to know how many and what kind of sharks were in Bocas del Toro in the past. First, they used acetic acid to dissolve away the chalky sediments and then they sorted the residue under a microscope using a paintbrush to isolate the denticles.

“Finding the first denticles was thrilling,” exclaimed Dillon. “They were beautifully preserved and abundant enough to provide insights into millennia-old shark communities.”

But before using these fossils to uncover past shark communities, Dillon wanted to better understand the relationship between shark numbers and denticle abundances, how denticles fossilize in reef sediments, and which sharks possess which types of denticles. After publishing these studies, she could finally return to the fossil record.

She found that denticle accumulation rates, and therefore, shark abundances, were over three times higher before humans began using marine resources in the region. All denticle types declined over time, but those found on commercially valuable, fished species declined the most. The oldest samples contained a higher proportion of denticles from fast swimming, pelagic sharks like hammerheads and requiem sharks. In contrast, Dillon found that nurse shark denticles are relatively more common today than they were in the past.

To complement this evidence from the fossil record, Dillon combed through archaeological studies and historical narratives to better understand the forces that might have caused these declines. She found that the steepest decline in shark abundance occurred in the late 20th century according to these historical records. This timing coincided with the development of a shark fishery in Panama, which selectively targeted pelagic sharks. Yet, the decline in denticles belonging to nurse sharks, which are infrequently harvested both today and historically, suggested that indirect factors like the loss of coral reef habitat or prey items were also to blame.

“When the Spanish arrived in the Americas, they wrote fantastic accounts of seas swarming with sharks,” Dillon said. “But these days we see very few sharks: we are lucky to see the occasional nurse shark. Our data show that sharks in Bocas del Toro have been depleted both by long-term harvesting, which accelerated in the second half of the 20th century, and by habitat degradation, which began even earlier with the expansion of banana cultivation and coastal development. There is so much land-based runoff from the coast today that in some locations it’s like swimming through limeade.”

“Taken together, Erin’s body of work shows that denticle assemblages can be used with care to help reconstruct past shark communities through time,” O’Dea said. “Sharks are an integral part of ocean health and play important roles in the great diversity and functioning of coral reefs. Having empirical estimates of past shark abundances and community composition helps us frame our understanding of what is natural in the seas.”

“We hope to extend this method to other locations to examine broader geographic patterns of change in reef shark communities over long ecological timescales,” Dillon said. “For example, we’re currently reconstructing trends in denticle accumulation along Panama’s Pacific coast over the last several thousand years using sediment cores. These baseline data will help us explore the causes and consequences of changes in shark abundance and functional diversity. Our work can also help tailor shark management goals to this local region.”

This study was made possible due to generous support from Panama’s Secretariat for Science and Technology (SENACYT), SNI, STRI, the Association of Marine Laboratories of the Caribbean, the Save Our Seas Foundation, the International Coral Reef Society, the Schmidt Family Foundation, the Alfred P. Sloan Foundation, M. Selin, J. Bilyk, V. and B. Anders and J. and M. Bytnar.

Reference:  Erin M. Dillon el al., "Fossil dermal denticles reveal the preexploitation baseline of a Caribbean coral reef shark community," PNAS (2021). www.pnas.org/cgi/doi/10.1073/pnas.2017735118