Editor's Note: this post introduces Dr. Neale Monks, who should be no stranger to anyone in our community with his many excellent aquatics book and magazine publications!
I have read with interest Robert Wintner's piece on the possible overfishing of reef fish by the aquarium industry as well as Bob Fenner's response on the Coral Magazine web site. Although both gentlemen make valid points, both have oversimplified the situation in terms of biology, and in doing so, some of the shades of grey between their positions may be lost.
Most fish are different, as are virtually all non-cnidarian invertebrates. They instead form a group known as r-selected organisms: they are small, grow rapidly, produce huge numbers of offspring, and those offspring individually have a low probability of reaching sexual maturity. Unlike K-selected organisms that exhibit steady populations, populations of r-selected organisms fluctuate up and down all the time, booming in some years, and crashing in others. So the letter r stands for "rate of reproduction" since these organisms rely on being able to rapidly exploit resources when they're available, and then being able to bounce back quickly should resources fail and their population crash.
Mr. Wintner and the Sea Shepherd foundation have been doing their best to limit commercial whaling. That's a laudable aim precisely because whales are K-selected organisms. It may take a whale decades to reach sexual maturity, mothers produce just a single calf at a time, and that calf may remain with the mother for several years, effectively taking its mother out of the population for the duration so far as reproduction goes. In other words, over a 60-year lifespan, a female whale might only produce half a dozen offspring. Obviously, killing even a small number of adults will have a huge impact on whale populations because the ability of survivors to make good any losses is extremely limited. An extreme example is the Atlantic Right Whale, which hasn't been hunted commercially for more than 100 years, and yet there's little sign that the population is growing at all, simply because the surviving adults produce no more offspring than natural mortality and accidents with large ships remove from the population.
A fish like a yellow tang is completely different. Individual fish will reach sexual maturity within a year, and females will produce thousands if not tens of thousands of eggs every time they mate. The eggs and sperm mix in the seawater, and the fertilised eggs drift off in the plankton where they can potentially develop into juvenile fish within a relatively short space of time. However, mortality during this phase is immense. In fact hardly any juveniles survive this process. Some aspects of mortality will be familiar to aquarists, for example predation by predators feeding on the plankton: arrow worms, pteropods, filter-feeding fish, and so on. But others are less familiar, in particular the importance of synchronicity between when fish breed and the cycles of other planktonic organisms. I don't know much about tangs, but certainly for fish like the Atlantic herring there's a narrow window of opportunity bounced by starvation on the one side and predators and toxins on the other. If the herrings breed too early in the year, there isn't enough algae for the developing fry to eat; if they breed too late, dinoflagellate populations are so high their toxins can kill the fry. In some years the herrings mis-time their breeding and virtually no offspring survive. Other years they get it right and so many offspring survive they make up the failures of previous years. While the details surely vary between fish species, this basic pattern is probably significant in most cases.
Another factor aquarists are less familiar with comes after the planktonic stage, the stage that biologists refer to as recruitment in the sense that these organisms are being recruited by a given habitat or location. Older fry or for that matter metamorphosed invertebrates like hermit crabs don't just magically settle down on the reef and then go on to live happy lives! Finding the right place to live, and then finding the resources they need to successfully settle down, are both very difficult challenges. Many, perhaps most late-stage planktonic juveniles don't arrive where they need to be. Ocean currents carry them to hostile environments, for example the open ocean, or places that are too hot or too cold for them. In the big picture that's fine; these animals cannot cover long distances as adults, and the species rely on planktonic currents to carry their juveniles into new habitats. It wasn't adult yellow tangs that swam across the Pacific Ocean from Indonesia to Hawaii! It was their offspring that drifted there, and as the volcanoes produced new islands, so the planktonic offspring of corals, crustaceans, molluscs and fish arrived on those islands, settled down, and created the coral reefs we know so well. But even larger numbers probably ended up in places where they were doomed. Some simply ran out of time, halfway across the Pacific they metamorphosed into something that needed solid ground, and consequently they starved or otherwise died. The fact you find sessile organisms like barnacles and mussels on floating debris is a reminder of how many of these organisms there are thousands of miles from the nearest coastline.
Even if they arrive on a coral reef, there's no guarantees they'll find ecological space. Remember, the stiffest threat any species faces is competition from its own kind. Empty but intact shells are rare, and hermit crabs have to fight one another to secure them. Territorial reef fish that need caves (such as groupers) or cultivate patches of algae (such as damselfish) have no guarantees at all that they will find such resources or be able to hold onto them. Since bigger individuals are stronger than smaller ones, newcomers to the reef, i.e., the juveniles, are the ones most likely to lose out. In other words, there are many hermit crabs and reef fish that settle out from the plankton onto the reef after metamorphosis, but die for one reason or another because they can't find or secure the resources they need.
A parallel might be drawn with mariculture of mussels. There's plenty of food for them, but intertidal hard grounds where they can live are limited. Mussel farmers use a variety of techniques to attract juvenile mussels (known as spat) from the plankton onto their farms. Once there, they can maintain commercially significant populations of mussels that may be harvested annually, without any harm to the wild mussels. Why? Because the spat the farmers are collecting would have died if they hadn't been captured and farmed! Mussels produce far more offspring than their habitat can normally sustain, so all the farmers are doing is removing natural "wastage". It would not be difficult to extrapolate this to, for example, the farming of clean-up crew hermit crabs by using shells, perhaps even artificial ones, that would house hermit crabs that in the wild would not have survived to sexual maturity.
The upside to r-selected organisms is that they undo human carelessness quite quickly. It may well be that poorly managed collecting has reduced tubeworm or hermit crab populations on certain reefs. But provided those habitats remain in good shape, and if exploitation is suspended for a period of time, there's no reason at all not to expect them to be back within a few years. Parallels can be drawn from commercial fisheries for species like herring and lobster, where multi-year bans have allowed populations to bounce back. Once recovered, sensible management of a new fishery can ensure its long-term viability.
So far, much of what I've said concurs with Mr. Fenner's point of view. Just as he points out, if in fact 99% of the marine fish captured do indeed die within a year, that's not very different to the proportion that die anyway. However, there is complexity to this, and going by the maximum sustainable yield alone doesn't paint the full picture. Indeed, what I've stated above only looks at things from the perspective of a single species. Where Mr. Wintner may have a point is once entire ecosystems are examined.
Simply because you can remove a certain number of yellow tangs without harming the long-term security of that species tells you nothing about what removal of yellow tangs does to the coral reef. Depressed populations of yellow tangs may remain viable, but the algae the removed tangs used to eat is now no longer being eaten by them. It may be consumed by other species that, for one reason or another, couldn't compete with the yellow tangs. Many aquarists will be familiar with the tensions between those species that farm algae, like damselfish, and those that bulldoze into those algae farms and eat everything they can find, like schooling surgeonfish. Energy always flows through ecosystems, and if doesn't go through a yellow tang, it'll go through something else. Fewer yellow tangs could mean more damselfish, more sea urchins, more snails. Who knows? It's very, very difficult to predict. But there are well-studied examples of what happens in situations like this. One example from the Mediterranean involves mackerel and squid; heavy mackerel fishing didn't exterminate them, but it did allow the squid populations to increase dramatically. There's some suggestion that overfishing sharks (classic K-selected animals) in the Pacific has allowed Humboldt squid (r-selected animals) to become far more numerous.
The bottom line is that the maximum sustainable yield metric is a very crude one, and without a better understanding of coral reef ecosystems, determining the optimal size for a given fishery will be very difficult.
Mr. Fenner's argument than wild fish populations may experience 99% turnover rates is also somewhat misleading. So far as planktonic and recruitment-stage individuals go, that's probably not far off the mark. Suppose a yellow tang female produces 10,000 eggs, even if 99% of those offspring fail in the first year, there will still be 100 of her descendants left, a pretty good rate of return. In all probability, she'd be very lucky if even that proportion survived. However, mortality after recruitment tends to drop dramatically, and continues to decline with age, at least up to the point where a fish or invertebrate gets so old it stops working properly. Yearling tangs probably have mortality rates far below 99%, and these are the ones that are breeding. So where Mr. Wintner does have a point is that because ornamental fish fisheries are targeting subadult and adult specimens rather than planktonic fish or recruits, the effects of a 99% mortality are in fact very serious. As aquarists buy new fish to replace those that died during the preceding year, more subadults and adults have to be removed from the reef. Put another way, while r-selected species can tolerate quite heavy mortality rates, in the wild this will be strongest on the juveniles, and less so on the adults. Aquarium collectors are operating the other way, taking the subadult and adult fish, which are the ones r-selected species are most dependent on for long-term survival. For a species like the yellow tang to do well, there needs to be a certain number of adults spawning each year.
There is an insidious aspect to this overlooked by aquarists. By targeting big or colourful specimens, the gene pool changes. Here we might examine the Atlantic cod, which in times past typically reached adult lengths of around 6 feet. Modern specimens are barely half that size. Over the last century, there's been a clear trend towards cod that reach sexual maturity at smaller sizes. Those are the ones that fisheries don't target so much, and those are the ones that get to breed at least a few times before they die or are caught by fishermen. By contrast, those cod that needed to reach a large size before the became sexually mature never had a chance to breed, so their "big" genes weren't passed on. Gradual changes to the size of a fish species like this will have follow-on effects in terms of its relationships with both prey and predator; smaller fish can consume smaller prey profitably, but smaller fish will also be easier targets for predators that couldn't handle larger fish of the same species. In terms of colouration, we simply don't understand why coral reef fish are so colourful, but where we see species that occur in a range of colours, targeting one particular morph may make that species less able to adapt to the range of habitats it exploits, or perhaps alter the social or behavioural interactions between individuals, symbiotes, or whatever.
Of course Mr. Fenner is quite right to point out that ornamental fish collection is a fairly trivial threat to coral reefs, though at a local level there may very well be a real threat to particular species. Human activities of various sorts do far more harm, from coastal development through to climate change. The recent oil spill in the Gulf of Mexico highlighted this perfectly. Damage from oil spills is relatively short-term and while obviously not beneficial, within a few decades even the worst oil spills seem to fade away with no long-term damage to the ecosystem affected. Yet the people most vociferously complaining about the oil spill included fishermen and hoteliers. The long-term damage caused by draining a mangrove or salt marsh to create a marina or a beachfront hotel is immense and for all practical purposes permanent. Habitat vital to coastal fish and the juvenile stages of many offshore species is gone for good. Without the natural shore defences provided by mangroves especially, coastal erosion and the damage done by freak storms increases. Shrimp fisheries are notoriously damaging, year after year catching immense quantities of so-called bycatch that is returned to the sea either dead or dying; the Gulf of Mexico fishery has been described by the Sustainable Fisheries Partnership as "unsustainable" thanks in part to "high levels of bycatch" and "impacts on threatened species". According to the FAO, out of what a typical Gulf of Mexico trawl hauls aboard, only 26% is shrimp; the rest is a variety of fish and invertebrates of no commercial value to the shrimp fishermen, and so it's thrown overboard, dead. The human species has an astonishing ability to focus on the trivial while ignoring the urgent.
Even if you allow Mr. Wintner's basic point to stand, that ornamental fish collecting is broadly bad, it may well be the price you have to pay for the security of the coral reefs. An analogy might be drawn with foxhunting. Many ecologists have pointed out that while chasing and then killing this little dog-like animal isn't very nice, the upside is that farmers and other landowners set aside woodland and hedgerow to "cultivate" foxes. Without that incentive, such preserves may be ripped up to provide farmland or property developments, with a net loss of not just foxes but all sorts of other wildlife as well. Sure, people could fly out to Hawaii and spend time with Mr. Wintner enjoying his excellent tours and availing themselves of his fine SCUBA equipment. But the carbon footprint of me flying across to Hawaii is a good deal greater than me buying a yellow tang. If a tankful of marine fish is what it takes to monetise the Hawaii reef, then that at least places a dollar value on the long-term maintenance of that reef and careful regulation of its fisheries. Without that incentive, there's a tendency to minimise the importance of natural resources where more obviously commercial ones, like beachfront property and tourism, can be promoted.
My intention here was to stress as clearly as I could that there are uncertainties within the arguments put forward by both Mr. Wintner and Mr. Fenner, both of whom I'm sure have the best of intentions as well as demonstrable concern for coral reefs generally. To try to simplify things down to "collecting bad" or "collecting good" overlooks the need for a better understanding of how populations work and the knock-on effects between species populations. Without making an effort to quantify the value of a pristine or managed coral reef, getting lawmakers to preserve them will be all but impossible.
More information about collection, aquaculture, and larval survival rates is available in this interview with Matt Wittenrich.