Why do wrasse spawn daily throughout the year with different partners while seahorses pair up for life? Why do seabream and an anemonefish change sex from male to female, while many other fish do the exact opposite?
As a diver and marine biologist, I have been fascinated by fish reproduction for over three decades and have devoted thousands of underwater hours to watching fish mate in the hope that we can understand how, when and why they mate the way they do.
There are about 25,000 fish species in the world today and together they display an astonishing variety of lifestyles, and this includes in the range and complexities of their reproductive styles.
But the species of fish that have most captured my attention are those that form massive groupings, known as spawning aggregations, to mate. Some of these aggregating species spawn for just a few hours at exactly the same times and places each year. These special places can be hundreds of kilometres away from their home reefs, to which they promptly return once mating is over. Unravelling the complexities of the behaviours that enable this to happen are questions not just of academic interest. Species that gather predictably in large numbers are very easy to overfish and exploited so aggregations can fast disappear, along with the fisheries they support. There are many good reasons to understand them, and a real need to safeguard them better.
Spawning aggregations are among the most spectacular and least understood events in our seas. To know more about them, I started to work on the largest known aggregation of the camouflage grouper.
Imagine a young male camouflage grouper, less than 1m long. Somehow, he knows exactly the right time of year to begin his migration to a spawning area. How does it tell the time? How does he know where to go on his first journey to mate? When he arrives, how does he select a female partner and successfully compete with the other males to win as many partners as possible during the tiny mating time window each year - little more than an hour over just a few days each year.
These were just some of the questions I had when I travelled to French Polynesia seven years ago during the camouflage grouper spawning period. When you are limited to short dive times (less than an hour or so a day because of the depth of the study site) the chance of actually witnessing this brief spawning period is akin to searching for a needle in a haystack.
You certainly need some clues; time of year, phase of the moon, the state of the tide, the behaviours of the animals and their need to avoid predators could also be important factors.
But which are the most important and what determines that exact brief moment when the fish decide to spawn? I wanted to know.
I vividly remember the first time I dived on a full-blown gathering of camouflage grouper. This was the most important event of their year; the few moments they release their eggs and sperm and create the next generation. Our little group of divers visited the site daily starting about a week before the full moon. Each day there were more fish on the site, about the size of a football field, until there were so many fish that we almost had to nudge them aside to swim through them.
I could feel the energy in the water from the chasing and fighting and movements of thousands of fish. Males shifted their colours between light and dark as if a switch were signaling who was top dog and who was the defeated.
They were fighting for access to females. If neither male backed down, the fighting escalated to mouth snapping, which I could hear, and biting (one reason why many males were scarred and battered and exhausted by the time the spawning was over). The females, every day a little more bloated as their hundreds of thousands of eggs expanded inside their bellies, sheltered uncomfortably in the reef. They seemed to ignore as much as they did the male’s shivering and earnest courtships. All the fish ignored the divers; they were so preoccupied that we could have stroked them had we wanted, but we preferred to watch and to photograph.
As the day of full moon approached, the fighting became more intense. More sharks had gathered for a grouper snack and the fish numbers peaked a little shy of 20,000. It was several years before I actually witnessed the main spawning event. Although we now know the time of month and year of spawning, we still do not know the very last piece of the puzzle, what is the last and immediate trigger of spawning once fish reach the site, so at best we can use informed guesses to plan our dives. At the turn of the tide and when no more fish seemed to be entering the site, when the females were massive and the courtship shivering had intensified, we kitted up and headed for the site of the action: a narrow channel separating the lagoon from the open sea. We back-rolled into the water and settled quietly on sand at about 20m. Just in time. The first mating group, led by a dark-coloured female and followed by several lighter males, suddenly spiraled 4-5m up away from the reef, released a massive white cloud of eggs and sperm. Another group followed and the sharks appeared with lightning speed and occasionally grabbed an unlucky fish
Some fish escaped, often with deep wounds. We were within a couple of feet of the action and were completely ignored. I felt like the invisible spectator of some timeless ritual, one played out yearly for millennia. I was not at all scared, despite being so close. I was blown away by the drama and the abundance; it is a rare experience to be so close to so many large animals.
The next day we returned to the site to find it strangely empty of fish. The yearly event had finished and they were moving back to their homes inside the safety of the lagoon. As we swam out towards the reef passage, we passed lines of straggling fish moving towards us, many with scars, missing fins, some barely able to move. Many would not survive.
I realised another reason for so many injuries on the groupers were the sharks, their semi-circular bite marks clearly outlined on some of the fish.
This aggregation is one of a few of its kind that we know today - large in size and brief and highly predictable for fishing. This one is protected because divers go to watch, but most others are not. Sadly, many are dwindling or even disappearing. Over 60% of documented spawning aggregations have declined because of fishing and some seem to have gone altogether. Once discovered, it is too easy to take too many, or all, of the gathered fish within a few years. If these fish cannot spawn, their populations and the fisheries they support outside of the reproductive period dwindle. A tragic example where this has happened is the case of the Nassau grouper. This fish was once the most important grouper in fisheries of the Caribbean and was fished mainly during its brief annual aggregation time. As a result of unmanaged fishing over the last three to four decades, the species has declined seriously and is now listed as endangered on the IUCN Red List. It is also on the US Endangered Species List and in 2016 was added to the SPAW protocol for regional protection.
Notably, these listings are the first of their kind for tropical commercial marine fishes, a warning for inaction. The Caribbean Nassau grouper shares many biological and fishery features in common with the camouflage grouper which explains the growing concern for its Indo-Pacific cousin. To draw attention to the challenges and implications of exploiting fish spawning aggregations without controls, the Science and Conservation of Fish Aggregations (SCRFA) was formed in 2000 to ensure spawning aggregations are regularly included in fishery management and conservation planning. The aim is that these wonderful aggregations survive into the future as well as the important fisheries they support. We want to have our fish and eat it too!
Refs: Nelson, J. S. 1994. Fishes of the World. Third Edition. John Wiley and Sons, Canada, USA. Pp. 600
Sadovy de Mitcheson. Y. 2016. Mainstreaming fish spawning aggregations into fishery management calls for truly precautionary approach. BioScience 66 (4):295-306.
Sadovy de Mitcheson, Y, Cornish, A., Domeier, M, Colin, P., Russell, M. & Lindeman, K. 2008. A Global Baseline for Spawning Aggregations of Reef Fishes Conservation Biology. 22(5):1233-1244.