All About Changes: colour and sex change in aquatic creatures – Dr Chiara Benvenuto

It is all about changes

I am an evolutionary behavioural ecologist, a generalist, not a specialist. I get excited about many different topics and fast; but most of all, I enjoy working with aquatic organisms (mainly fish and crustaceans, marine and freshwater, in temperate and tropical environments: yes, I do not have one favoured study organism, but many). I am fascinated by behavioural adaptations and the evolution of animal mating systems and convinced that a deep knowledge of behavioural ecology and mating strategies in animals is fundamental in any program of conservation and management of biodiversity.  
In the last few years, I focused on two projects, both involving changes – of different magnitudes and for different reasons. 

Colour change in the brown shrimp Crangon crangon 

Many animals play hide and seek with their predators and preys; often they are hidden in plain sight, as they blend with their background, concealing themselves. But camouflage is not the only reason to change colour: communication, thermoregulation (1) and even stress (2) can also play a role. The brown shrimp, Crangon crangon uses chromatophores (cells containing pigments) to physiologically modulate its colour. Moving shrimp from black to white sediment, we were able to observe dark individuals (with the pigment expanded to cover their bodies) turn pale (contracted pigments occupy little space and show the lighter tissues underneath), in just one hour (2). We discovered that the overall colour of the shrimp follows a clear rhythm (darker at night, lighter during the day) and shrimp are able to match their background, consistently overall but with great variation among individuals and even in the same individual tested multiple times. This suggests a balance between environmental adaptation (matching the background) and behavioural plasticity (variation is good) possibly enhancing change in heterogeneous and dynamic environments. Did I mention that when we prevented the shrimp from burrowing using a transparent plastic layer (shrimp spend most of the time buried into the sediment, with only the eyes sticking out), animals became darker, regardless the colour of the sand? This could represent a “visual stress sign” to unfavourable conditions.  


Two individuals of Crangon crangon (top picture) kept in dark (top left) and white (bottom right) substrates; one individual photographed after a 2 hours permanence in dark substrate (bottom left) and white substrate (bottom right): note the correspondence in number and position of chromatophore, but difference in sizes (expanded vs contracted). Photos by A. Siegenthaler

Sex change in fish (and other organisms)

If you think colour change is remarkable, let me tell you about a more drastic change. Many animals (and plants!) can change sex (3). Among vertebrates, fish are the only animals presenting sequential hermaphrodites (sex changers). Hermaphrodites are individuals capable of producing both male and female gametes: they are simultaneous (or synchronous) if they produce both gametes at the same time, and sequential if they produce gametes of the two sexes consecutively (acting first as a male and then as a female or vice versa: i.e., they change sex). We are also aware of “intersexes” (4); individuals with abnormal presence of both gonadal cells due to exogenous hormones and chemicals in the water (endocrine disruptors), but sequential hermaphroditism is not an environmental issue: it is a strategy to maximise fitness (how many offspring are produced in a lifetime): as the size advantage model (5) tells us, sex change is expected when fecundity (fertility) is correlated with size, much more so for one sex than the other. It all depends on the mating system: in haremic species (where one male dominates a group of females) it is better to be a small female first (as they can reproduce with the dominant male) and a large dominant male later (small males are not successful, as they are easily dislodged by the dominant male). So here a female-first sex change (called protogyny) is favoured. But if mating is random it is better to be a small male first (small males are still very successful in fertilizing females) and a large female later (as larger females can produce more eggs than smaller ones). So, sex change is important – it has many implications, for fisheries, management, conservation, effective population size (6,7) – AND the direction of sex change (from male to female or from female to male) is crucial (6). Not to forget that some species can change sex in both directions (bi-directional sex changers). Fascinating topic! And we still have a lot to learn. 


Sex changers in the Mediterranean Sea. left) Thalassoma pavo: a protogynous species (female-to-male sex changer); right) Sarpa salpa: a protandrous species (male-to-female sex changer). Photos by C. Benvenuto.

Should we change perspective?

The changes I showed you here are examples of adaptations: to survive (colour change allows successful adaptive camouflage) or to increase fitness (the second sex is the largest and more fecund). Want to know more? Contact me at the University of Salford or @cbenvenuto73 or visit: https://sites.google.com/view/benvenutoresearchgroup/home
Possibly, a successful strategy in the Anthropocene will be to change perspective and revisit our place, impact and role on Earth’s ecosystems. After all, changes are powerful. 

References:

1. Stuart-Fox D., Moussalli A., 2009. Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philosophical Transactions of the Royal Society B: Biological Sciences 364:463–470.  

2. Siegenthaler A., Mastin A., Dufaut C., Mondal D., Benvenuto C., 2018. Background matching in the brown shrimp Crangon crangon: adaptive camouflage and behavioural-plasticity. Scientific Reports 8:3292.  

3. Policansky D., 1982. Sex change in plants and animals. Annual Review of Ecology and Systematics 13:471–495.  

4. Abdel-moneim A., Coulter D.P., Mahapatra C.T., Sepúlveda M.S., 2015. Intersex in fishes and amphibians: population implications, prevalence, mechanisms and molecular biomarkers. Journal of Applied Toxicology35(11):1228-1240. 

5. Warner R.R., 1975 The adaptive significance of sequential hermaphroditism in animals. American Naturalist 109: 61–82. 

6. Benvenuto C., Coscia I., Chopelet J., Sala-Bozano M., Mariani S., 2017. Ecological and evolutionary 

7. Waples R.S., Mariani S., Benvenuto C., 2018. Consequences of sex change for effective population size. Proceedings of the Royal Society B. 285:20181702.