Crown-of-Thorns and Favorable Disturbance

For millions of years, crown-of-thorns starfish (COTS) have devoured coral colonies, leaving behind white calcium-carbonate bones.

Slowly, silently an elastic arm armored with sharp, toxin-covered spines reaches up over the edge of a large table coral. One by one, delicate tube feet stretch down from the underside of the arm and grip the coral with suction cups. Before long more spiked arms come into view, and the entire body of a large, flexible starfish clamors atop the colony of delicate polyps. Underneath the starfish, the soft tissue of its stomach gradually everts (turns inside out), covering a swath of defenseless coral. Digestive enzymes immediately begin to dissolve the living polyps. The starfish's stomach absorbs the liquefied nutrients, eventually leaving the underlying calcium-carbonate bones of the coral clean of every scrap of animal tissue. Over the next day or two the ravenous starfish will devour the entire coral colony in this manner, leaving behind a bright white skeleton, and then crawl on to the next colony.

This is the peculiar but typical behavior of one of the most influential invertebrate predators found on Pacific coral reefs, the crown-of-thorns starfish (Acanthaster planci). The starfish is doing what its ancestors did for millennia — eating the corals with which they evolved millions of years ago. Like many other species that aren't widely accepted as aesthetically pleasing or don't fit neatly into popular concepts of a healthy ocean, crown-of-thorns starfish (COTS) are subject to vilification. Their recent history has been tarnished by some massively destructive population outbreaks. These days the large, coral-eating echinoderms are familiar inhabitants of tropical Pacific reefs, and virtually every diver and snorkeler knows what they are. At the same time, however, few people appreciate the species' functionality and its role in the overwhelmingly complex coral reef ecosystem.

The hungry starfish on top of the Acropora coral is a mature female and will soon spawn. Unlike some other echinoderms, COTS are not known to reproduce asexually via arm autonomy; sexual reproduction through synchronized spawning usually coincides with seasonal spikes in water temperatures. This female, being large and therefore quite fecund, can release close to 60 million eggs per spawning season. Broadcasting her eggs into the current while nearby males release sperm at the same time should produce fertilized eggs that rapidly metamorphose into planktonic larvae. Widely distributed, COTS larvae normally spend three to four weeks drifting at the whim of ocean currents before settling on a reef.

By way of this long larval period the species has been able to spread eastward from the western Pacific to the Gulf of California and westward all the way to the Red Sea. Environmental conditions such as temperature, salinity and food availability influence the settlement of larvae on reefs and subsequent metamorphosis. Juvenile COTS are cryptic and begin their lives feeding on encrusting coralline algae commonly found on reefs. At this young age their growth rate is exponential; they add arms, and after about six months their diet changes. They go from seemingly harmless herbivores grazing on algae to predators that seek out and prey upon live coral.

The evolutionary history of COTS is still something of a mystery, but the speciation from herbivorous ancestors undoubtedly coincided with the success of reef-building corals sometime between 1 million and 3.7 million years ago in the southwestern Pacific. Recent genetic studies have indicated that the species is still diverging, and A. planci is, in fact, a complex of four sibling species, or clades. Similar to all starfish, COTS are pliable and have no rigid skeleton. But uniquely shaped calcium-carbonate spicules provide some structural support and are the only evidence of COTSs that can be found in fossil records. Interestingly, COTS spicules have been discovered in ancient soil strata, which indicates that large numbers of COTS existed at one time and then died off quickly. These layers of spicules suggest natural boom and bust cycles on coral reefs that occurred well before humans ever reached many Pacific islands.

Crown-of-thorns starfish have apparently acquired their sinister name within the last 50 years. Understandably, divers and snorkelers who explore and appreciate coral reefs for their aesthetic value aren't happy to watch their underwater playgrounds being decimated by starfish outbreaks. Under ordinary circumstances, COTS are found on the order of 1-15 per 100 square meters of reef. During outbreaks, abundances can be 400-600 percent higher than normal, and coral mortality on a given reef may range from 50-100 percent. Though the effects of the outbreaks are well known, the triggers remain somewhat mysterious.
An outbreak occurs when the number of COTS on a reef rapidly increases so that they consume coral faster than the corals can grow. They prefer particular coral species such as table and staghorn corals, but in general they simply act like a living, slow-moving and devastating wildfire. Outbreaks radically modify reefs; duration and severity vary greatly, which means some reefs and regions are affected much more significantly than others. After COTS devour all of the edible corals in an area, algae swiftly colonize most of the newly available space. The fish community changes, and sessile invertebrates such as sponges and soft corals grow over areas once covered by hard corals. In the aftermath of an outbreak it may take decades for a reef to recover its original biodiversity, and some reefs never fully recover.

Over the past several decades researchers have posed a number of hypotheses about how and why COTS outbreaks happen. The hypotheses are split into two basic categories: those that consider outbreaks natural and recurring, and those that presume outbreaks are recent, novel events. The two categories are not necessarily mutually exclusive; while the roots underlying outbreaks are still debated, it is likely that they are caused by an ever-changing amalgamation of natural and anthropogenic factors.

Though the first scientifically documented COTS outbreak was in Japan in 1957, there is substantial evidence for outbreaks having occurred previously. Skeletal elements (ossicles) of COTS have periodically been found in abundance in reef sediments from the past 7,000 years. Population explosions appear to be driven by both coral abundance and the success of COTS larvae at settling and surviving the juvenile stages. For a species that produces tens of millions of eggs every spawning season, just a small percentage increase in larval survival could lead to huge numbers of adults within a year's time. COTS larvae have been shown to survive better in conditions of low salinity and warm temperatures, and this is evident in the fact that the majority of outbreaks have occurred on reefs surrounding high islands or near continents where freshwater runoff occurs seasonally.

In the early 1980s Charles Birkeland, now professor of biology at the University of Hawaii, proposed the terrestrial runoff hypothesis, stating that nutrients in freshwater runoff, especially from large storms, cause phytoplankton blooms that boost the food supply for COTS larvae. Assuming that under normal conditions most COTS larvae starve from lack of food, increased larval survival and recruitment leads to subsequent outbreaks. With increases in human populations throughout the Pacific and more nutrient input, often from agricultural sources, phytoplankton blooms are occurring more often than in previous decades and creating optimal conditions for COTS larvae.

One of the popular hypotheses for why outbreaks have become more common is the reduction of COTS predators. At least 12 different species, including crabs, shrimp, a polychaete, gastropods and fish, are known to prey on juvenile and/or adult COTS. But most predators will not feed on COTS larvae or adults if given a choice of other food options. COTS eggs and larvae are protected by toxins, and the spine-laden adults can resist all but the most effective predators; the cryptic juveniles are probably the most vulnerable, but there is virtually no evidence that predation controls COTS population sizes.
The Intermediate Disturbance Hypothesis

Whatever the origins and consequences of outbreaks, COTS generally contribute to the maintenance of reef diversity outlined in the intermediate disturbance hypothesis (IDH). Disturbances clear habitat and lead to species immigration into newly cleared space, such as dead coral colonies. The IDH states that species diversity is maximized when ecological disturbance occurs at a rate for both fast-growing and slow-growing species to coexist.

When disturbance is removed, species richness decreases as competitive exclusion increases. In other words, species competing for the same resources cannot coexist in the same niche. By feeding on fast-growing corals, COTS in normal abundance help maintain robust reef systems. Fast-growing corals, if not kept in check, have the potential to overgrow a reef, creating a monotypic habitat that is susceptible to collapse under any number of environmental stresses. The more diverse a reef system is, the more capable it is of withstanding various environmental pressures and changes. On the other hand, all species on a reef are at risk of going extinct when there is too much disturbance. Therefore COTS, in ordinary conditions, play a vital role in Pacific reef ecosystems.

While the underlying causes of COTS outbreaks are still debated, it is likely they are caused by an ever-changing amalgamation of natural and anthropogenic factors.

The female starfish has finished its meal, and as the morning brightens the animal begins to move all of its tube feet in unison, crawling toward the dark underside of the coral. Behind the starfish is a white scar devoid of life. But that scar will soon serve as substrate for new life to colonize and compete and contribute to the energy transfers continually occurring in the reef ecosystem. For now, the starfish rests. In a matter of hours it will mindlessly continue the business of helping keep the whole reef ecosystem diverse and healthy.

Outbreaks appear to be natural reset buttons as well as recurring anthropogenic sources of devastation. It is time for a paradigm shift, or maybe a reality check, with regard to how we think about COTS and their influence on reefs. We must begin looking at the ways in which humans are involved in the outbreak process: nutrient input along coastal regions and sea surface temperature rises caused by anthropogenic climate change. Let's look at COTS not as a cancer on Pacific reefs but as a naturally evolved and integral player in healthy reef environments. It is time to focus less on managing COTS and more on managing human activities, human populations and human ignorance.

© Alert Diver — Q1 Winter 2015