Seduction Below the Surface: Learning from a Small Marine Fish That Seduction Is an Ever-Changing Game

This blog post is provided by Ivain Martinossi and tells the #StoryBehindThePaper for the paper A test of operational sex-ratio theory across latitudes reveals temporal variation in sex-specific behavioural reaction norms, which was recently published in the Journal of Animal Ecology. In their study, Martinossi and colleagues shine a light on the nuanced seduction strategies of a small marine fish, the two-spotted goby, which has a lot to tell us about courtship in the animal kingdom.  

From popular science documentaries, we all have an idea of what courtship in animals can look like. We may have seen the ritual dance of the male birds of paradise, male deer fighting head-to-head, or perhaps even male giraffes, which engage in impressive contests of neck fencing. There are two important misconceptions carried by this popular science picture that I would like to challenge, and that my work below the surface challenges.

It’s not always the males!

The first one is straightforward, so let us get it out of the way: it’s not always the males! It is getting more and more obvious to biologists that females are also playing the game of seduction, are also fighting hard to get the mate that they want and fending off competing females. In fish, female courtship is in fact relatively common because males are often the ones doing the job of looking after the babies (Figure 1). This means that males represent a valuable resource that females want to control; this is particularly obvious in seahorses and pipefish, where the males carry developing eggs on their belly, and even feed them in the case of seahorses. Females fight for the privilege of giving their eggs in custody to the best father. Unfortunately, birds and mammals are by far the favorite taxa of biologists. This means that our knowledge of seduction in animals has long been based on the behavior of these species, which mostly follow the pattern of female looking after babies and males competing for females. Exploring seduction below the surface has completely changed our point of view.

Figure 1. Male goby oxygenating eggs in Southern Norway.  What you see here is not a fish running on a treadmill. It is a male goby in his nest, which happens to be a PVC tube that we set out at sea for an experiment. By swimming on the spot, the male creates a current of fresh water that is bringing oxygen to the eggs. Without this, the eggs would never be able to develop. Watch the video here!

In the next figure (Figure 2), you can see a female of my study species (the two-spotted goby, Pomatoschistus flavescens) chasing a male that at first does not want to breed. In this species, males defend a nest that is usually a natural cavity in an empty mussel shell or a fold in a leaf of kelp. Males look after the eggs alone, protecting them against predators, oxygenating them with their fins (as in Figure 1), and cleaning them from fungus and algae that might grow on them. This means that a good male is very valuable to females, and so females are often seen chasing and courting males or fending off each other.

Figure 2. Female courting a male in Southern Norway. A female, identifiable by her orange belly, is courting a male who is swimming away. You can see the female is courting by her posture, slightly arched back, belly forward (as much as a swimming position allows), and by her color, where the belly is very visible, but the rest of the body is more transparent than usual (compare her to the male color). Changing color is a trick that fish can pull easily with specialized pigmented cells in their skin. If you watch the video here, you will see the female courting and the male responding by his own courtship display later.
Seduction in animals is an ever-changing game

The interesting thing is that in the two-spotted goby, males are also often seen courting. This brings me to the second misconception, which is more subtle. In my view, popular science gives the impression that seduction in animals is a very ritualized, very rigid behavior- that both sexes have fixed roles they always follow. This is not true! Of course, there are very specific behaviors associated with courtship, but individuals are constantly adapting what they do to the context. By context, I mean who the animals are trying to seduce, and who else is available for mating, and what are the prospects for successful reproduction.

The fact that seduction behaviors are ever-changing is easy to prove, you just have to observe animals long enough. For example, in our little fish, studying behavior at different locations along the coast, or in the same location but at different times of the year, gives completely different results. In the Northern Sea off the Swedish coast, where we have done a lot of our work, males court females a lot early in the spring, while females court males a lot in the summer. At the same time, if we go further North all the way up to the Lofoten in Norway, we don’t see females courting males at all!

The tricky part is to demonstrate what is causing these changes in behavior, and this is exactly what we do in our most recent study published in the Journal of Animal Ecology. We spent many hours diving and observing the fish at different places along the Swedish and Norwegian coast. By recording the frequency of different behaviors and important elements of the context in which these behaviors happen, we have been able to figure out some interesting trends. For example, males court more often when males are more abundant on the mating market, and inversely females court more when they are more abundant. This makes perfect sense, because the more abundant sex will always have a harder time finding a mate. Still, it is pretty amazing to see that these little creatures are capable of sensing their social environment and responding to it immediately!

Climate matters

One important aspect of our latest work was to show that climate also has a great influence on the two-spotted goby’s seduction tactics. Because we worked in so many different places, we were able to compare the seduction behaviors of the fish under different climatic conditions. In the north of Norway, the water is much colder, and the warm season during which reproduction can happen each year is much shorter than in Sweden. This means that in Sweden, males have to look after babies over and over again, which leaves them exhausted and, after a while, unable to reproduce anymore. The Swedish mating market becomes empty of males and females are seen courting desperately. On the contrary, in Northern Norway the reproductive season is short and so females never run out of males: we don’t see females courting there at all!

Showing how climate affects seduction tactics is very important. With ongoing climate change, animal mating behaviors are often disrupted and the consequences of this are not well understood yet. In the ocean, we already see a global rising of temperatures and increased noise pollution, which is more problematic that we think. We imagine the ocean as a silent world, but this is far from true. Not only is the ocean full of human sounds, caused by propellers and echosounders, but it is also full of the songs of life. In fact, our little gobies themselves are part of this choir, and singing is part of their seduction arsenal. Yes, fish sing love songs to each other. And if we want these songs to keep echoing in the deep, we need to understand, love, and protect our oceans. We certainly hope that our scientific work will contribute to this endeavor.

Read the paper

Read the full paper here: https://doi.org/10.1111/1365-2656.14250

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