Post provided by Erin Dillon

Close your eyes for a second and imagine a coral reef. What do you think the shark community on that reef looked like historically?

Grey reef sharks on Palmyra Atoll’s forereef. ©Darcy Bradley.

Perhaps you imagined a remote reef with high shark abundance like Fakarava, French Polynesia or Palmyra Atoll, Northern Line Islands. Maybe you thought of a marine protected area such as Jardines de la Reina National Park in Cuba. Or perhaps you relied on your own memories from snorkeling on reefs in the past or photos of reefs taken decades ago.

The answer to this question depends on a reef’s location, given that shark abundances can vary with primary productivity and other oceanographic features. It also depends on which time period you chose as your reference point. Shark abundances can fluctuate over the course of a few hours – as well as over days to years to decades and beyond. Even if you chose the same time and place as the person before you, you might have come up with a slightly different answer. This variation in how we determine baselines – overlaid on a backdrop of natural variation in shark communities over space and time – can contribute to differing perceptions about what’s natural or what a depleted population can possibly be restored to.

This is a relevant yet perplexing question for coral reef conservation and ecology. Sharks play potentially important roles in coral reef ecosystems, from structuring food webs and modifying prey behavior to affecting nutrient cycling. But, many coastal shark populations have declined precipitously over the last several decades at the hands of overfishing and habitat degradation. In many cases, we lack long-term data to define natural variation in the past, assess the ecological consequences of shark declines, and inform realistic recovery targets. One way to fill these knowledge gaps is to go back in time…

A Coral Reef Time Machine

Scanning electron microscope image of a
scalloped hammerhead denticle.
Scale bar = 20 µm. ©Jorge Ceballos and Erin Dillon

When our lab group visits coral reefs for field work, we often don’t see many sharks. But even though sharks can be challenging to directly observe at these sites, their presence is recorded in the sand. Coral reef sand contains a treasure trove of disarticulated skeletal material from coral, sponges, molluscs, urchins, fish, and even sharks. Being cartilaginous, sharks primarily leave behind their teeth and dermal denticles (“skin teeth”), although vertebrae, bits of cartilage, coprolites (fossilized feces), and even articulated remains have been discovered in the deeper fossil record (check out this recent discovery in a Kentucky cave). Sharks have up to hundreds of teeth at any point in time, but their bodies are covered by millions of denticles. These microscopic tooth-like scales are what makes shark skin feel rough like sandpaper if you rub it in one direction yet smooth in the other direction.

It turns out that sharks shed their denticles and they accumulate in marine sediments over time. We can sample these sediments to produce a record of shark occurrences. Surface sediments on coral reefs provide a time-integrated picture of the number and types of sharks that have either lived on or transited through a reef over the last couple years and sometimes even decades. On the other hand, fossil reefs and sediment cores act like time machines, allowing us to reconstruct conditions in the past and look at change over significantly longer periods of time.

Leveraging the Fossil Record for Conservation

This approach is part of a relatively new and growing field called conservation palaeobiology. Conservation palaeobiology applies palaeontology’s theories and methods to generate data over long timescales – often before instrumental and monitoring records or even before human presence altogether – that can address conservation issues. It merges a wealth of information gathered from geochemical (e.g. isotopes), lithological (e.g. sediment characteristics), and biological (e.g. relative abundances) proxies. In doing so, conservation palaeobiology can help:

  • define historical ranges of variation
  • characterize how dynamic an ecosystem or population is naturally
  • examine how and why ecosystems have (or have not) changed over time
  • disentangle human impacts from natural processes that play out over long timescales
  • document geographic range shifts
  • evaluate extinction risk
  • measure recoveries
  • develop management targets based on local expected conditions.

There’s a lot we can learn from the recent and deep-time fossil record that can be applied to conservation today.

Denticles as a Conservation Tool

Dermal denticles and fish teeth have been used in deep time to explore changes in fish communities over millions of years and investigate what drove the dawn of the modern ‘age of fishes’. Our team set out to test whether denticle assemblages could also be used as a proxy of relative shark abundance over the last several thousand years. This timescale is relevant to thinking about how humans have impacted sharks. We found denticles to be well-preserved in low-energy reef environments and that they could be isolated from sediments. But could they be classified in a meaningful way?

Clockwise from upper left: false color scanning electron microscope images of shark denticles belonging to a lemon shark, tiger shark, great hammerhead shark, nurse shark, bull shark, and scalloped hammerhead shark. The ridged denticles with honeycomb-like microstructures belong to fast-swimming species (e.g. great hammerhead shark and scalloped hammerhead shark). The denticle on the lower right belongs to a demersal species (e.g. nurse shark). It is actually several times larger than the other denticles pictured here and is much thicker, creating a protective armor. Denticles are not to scale. © Jorge Ceballos, Aaron O’Dea, and Erin Dillon.

Denticles come in a variety of flavors. Their shape, size, and morphological features differ across shark taxa with different ecologies. Using these morphological features, we can classify them into functional morphotypes and, in some cases, shark families. Isolated denticles recovered from sediments can tell stories about the sharks they came from, both extinct and extant. By building a reference collection of denticles from the ichthyology collection at the Smithsonian National Museum of Natural History, we were able to explore the relationship between shark life mode and denticle morphology across coastal shark species. We used this reference collection to develop a framework for classifying denticles. Confirming what sort of ecological information could be acquired from denticles and what taxonomic resolution was possible when identifying them was the first step in exploring whether denticles could be used as a conservation tool.

For example, thin ridged denticles enhance propulsion by reducing drag and improving thrust. This drag reduction morphotype was a source of inspiration for Speedo’s LZR swimsuit that was banned after the 2008 Beijing Olympics, despite having different surface properties than shark skin. On a shark, the riblets on these denticles influence the way water behaves in the boundary layer, which sits at the interface between a shark’s skin and the surrounding water. Some of the fastest species, such as the shortfin mako, have flexible denticles that reduce flow separation, which can otherwise result in drag. As you might imagine, this denticle morphotype characterizes the bodies of fast-swimming sharks, many of which reach impressive burst speeds to catch their prey.

On the other hand, slower-swimming, demersal species such as nurse sharks have much thicker, pebble-like denticles that act like armor. These abrasion strength denticles provide protection for species that spend much of their time near rocky or hard substrates. Sharks with abrasion strength denticles often eat different prey and occupy different habitats than those with drag reduction denticles.

The bottom line is – given this link between form and function, denticles recovered from sediments can be used to interpret shark life mode even though we can’t classify them to species.

Ground Truthing the Denticle Record

Before we could apply this new approach to reconstruct shark baselines, we needed to test whether denticles accumulating in sediments actually reflect shark abundances. If this were true, we would expect to see more denticles accumulating in surface sediments in areas where there are more sharks today. This finding would give us confidence when interpreting the denticle record in the past. On the other hand, processes that selectively alter the preservation, transport, and temporal context of the denticle record could result in mismatch between denticle abundances and shark abundances. So it was particularly important for us to explicitly test the fidelity of the denticle record.

Collecting surface sediments using SCUBA. ©Sean Mattson.

To do this, we went to a place where there are sharks… lots of sharks. That place was Palmyra Atoll, an unfished atoll in the central Pacific about 1000 miles southwest of Hawaii. Palmyra Atoll National Wildlife Refuge is home to high and well-surveyed shark populations, as it is protected both by its remote location and as part of the Pacific Remote Islands Marine National Monument. Also, it has been studied by a diverse group of institutions via the Palmyra Atoll Research Consortium over the past two decades. This made it an ideal place to ground truth the denticle record using contemporary shark survey data.

The lagoon on Palmyra is a creepy place. Sharks patrol its depths and the water is far from crystal clear. While sampling, I would nervously check over my shoulder from time to time, hoping not to come face to face with a large tiger shark. Fortunately, blacktip reef sharks were our only company. We targeted the lagoon for sampling because it was a low-energy environment where sediment particles (and denticles) would accumulate and not be washed away or broken by waves and currents. We weren’t the first team to survey sharks in the lagoon either, so we selected our sites to overlap with the existing data.

All in all, this study was a highly collaborative effort combining conventional shark survey data collected by multiple research groups, which were compared with denticle accumulation rates at corresponding sites. In ‘Dermal denticle assemblages in coral reef sediments correlate with conventional shark surveys’, we demonstrate that denticle accumulation rates in these low-energy reef environments are positively correlated with shark abundances, with a couple of caveats (read our paper to learn more).

We’ve now shown that time-averaged denticle assemblages in surface sediments can preserve a signal of relative shark abundance in low-energy reef habitats. The next step is to use this approach to characterise historical ranges of variation in shark communities. This will provide context for interpreting modern change and help to inform location-specific management targets.

To find out more, read our Methods in Ecology and Evolution article ‘Dermal denticle assemblages in coral reef sediments correlate with conventional shark surveys