The survival of coral reefs and their menagerie of rainbowed residents relies on seldom seen and historically overlooked tiny fish — the smallest of marine vertebrates. No larger than two inches in length, these tiny fish maintain the productivity and diversity of coral reef communities, which exist as oases of life in what would otherwise be an oceanic desert.

A study published in the May 24 issue of Science sheds light on the "dark productivity" of these cryptobenthic reef fishes, a group that includes gobies, blennies and cardinalfish. According to the results, tiny cryptobenthic fish make up almost half of the total reef-fish biodiversity as well as nearly two-thirds of the fish larvae that reside near the reef.

Critically, this abundance provides the lion's-share — 57% — of consumable reef biomass and provides the foundational food source for larger reef fish, organisms on which the livelihoods of millions of people worldwide depend.

"For any diver or snorkeler on a reef, these tiny fish will only ever be flashes of red, white, orange or yellow, scurrying to safety," said Simon Brandl, the study's lead author and researcher at Simon Fraser University — that is, if the inconspicuous species are ever seen at all.

However, Brandl and his colleagues show that this group of small-bodied, short-lived fish underpin the high productivity of coral reefs by supplying larger reef species with a limitless buffet of fresh fish flesh to devour — and perhaps solve a long-standing ecological mystery.

When we imagine tropical oceans, our minds evoke vivid images of crystal clear, cobalt-blue waters teeming with a kaleidoscopic array of colorful life of all shapes and forms. However, vast expanses of Earth's tropical oceans are barren places largely bereft of productivity or life. In fact, it is these absences which give tropical seas their characteristic color and clarity.

Despite the oceans' lack of life-sustaining nutrients, coral reefs punctuate these regions with dense pockets of exceptional biological diversity. The counterintuitive occurrence of highly-productive reef environments separated by bleak stretches of open ocean was not lost on naturalist Charles Darwin, who commented on the observations as he voyaged amidst the islands and atolls of the tropical Pacific.

Yet Darwin was never able to resolve how these isolated reef communities managed to survive and flourish in low-productivity oceans. This ecological quandary — often termed "Darwin's Paradox" — has baffled scientists for nearly 200 years.

"While our work certainly isn't the sole puzzle piece that solves this paradox," said Brandl, "the unique role for tiny [cryptobenthic] fish we have discovered highlights an interesting and thus far unknown quirk of coral reefs that may permit them to support such a rich fish life."

Notoriously shy cryptobenthic fish often live their lives hidden in the dark grottos, crevasses, canyons and other protected nooks and crannies found among coral heads and lumps of reef rock, which has made the lives of the tiny fish difficult to understand, despite decades of effort.



The bluebelly blenny fish avoid predation with a careful lookout. | Tane Sinclair-Taylor

What is known about these mysterious fish, however, is how remarkably short their lives are. For example, one species of reef goby — the shortest living vertebrate on Earth — has a lifespan of just 59 days, 25 of which are spent as an adult. Considering their rapid growth, extreme mortality and vulnerability to virtually any of the hungry predators living around them, it is unknown how cryptobenthic fish populations can toe such a thin demographic line and maintain their populations.

Brandl and the research team developed an analytical model based on a comprehensive global dataset of near-reef larval communities and adult reef-fish dynamics to evaluate the hidden complexities of cryptobenthic fish populations.

"I was floored when I weeded through decades of data on the abundances of larvae near reefs and found that consistently and pretty much across the globe, these tiny, cryptobenthic larvae absolutely dominate the larval communities," said Brandl.

The key to cryptobenthic abundance and productivity in the near-shore reefs may be because of an evolutionary shift away from the long-range open-ocean drifting that larger reef fish larvae normally do, with cryptobenthic fish remaining instead in the immediate vicinity of their home reefs. Furthermore, as parents, these little fish show exceptional skill in ensuring the survival of their offspring, the results show.

By creating "a giant reservoir of new recruits ready to replace adults on the reef," Brandl said, the overwhelming presence of cryptobenthic larvae in the reef, despite the limited number of reproducing adults, not only helps to explain how their populations persist, but also reveals their previously hidden functional role in fueling reef productivity by providing a large and continuous supply of fish food.

According to co-author Isabelle Côté, a Simon Fraser University researcher, the larger reef creatures — well-known and commercially important species like sharks, barracuda and groupers — completely depend on the food chains that start with the smallest fishes on the reef. As such, one might expect to observe a traditional ecological pyramid where lots of little fish feed fewer medium-sized species, which in turn feed even fewer larger species.

However, the study shows that on the reef, predation at the lowest levels can occur so rapidly it can make the ecological pyramid appear inverted.

"These [cryptobenthic] larvae settle onto the reef and turn into tiny fish and are eaten by larger fish and invertebrates virtually as fast as they settle," said Côté



The Spotted Dwarfgoby plays a key role in reef productivity. | Tane Sinclair-Taylor

Côté likens it to a sushi train restaurant where plates of fish larvae, placed at breakneck speed on a conveyor belt, are taken off and consumed equally fast by hungry, predatory patrons.

"A snapshot would suggest that the conveyor belt is mostly empty, but this would belie the intense feeding and eating activity that's happening," said Côté.

Côté suggested that in order to preserve the world's large reef fishes, we must better understand — and target for conservation — those at the bottom of the reef food web.

The study offers a clear example of how the smallest of fishes can be critically important and have massive yet barely perceived influences on the survival of coral reef ecosystems. Now that the dark productivity provided by this "hidden half" of reef-fish has been illuminated, the researchers want to understand exactly how these tiny reef fishes have managed to survive so well compared to other fish groups, despite their abridged and predator-oppressed lives.

"These fishes are such an incredibly diverse and intriguing group that I think we all knew had a big secret to tell, as it turns out that their secret was being an important group for coral reefs as a whole," said Brandl. "I would argue that our results make a really compelling case for why we should start looking at these fish in more detail, especially given the dramatic changes that coral reefs are currently undergoing."