Written by Charlie Gregory

Cueva del Azufre is a complex cave system in southern Mexico with incredibly harsh conditions which make it seem almost impossible for any form of life to survive there. But despite waters filled with over 50 times the lethal dose of toxic hydrogen sulphide, a near complete absence of light and a religious ritual where natives further poison the waters, one species of fish is not just surviving there but thriving. That species is the Atlantic molly (Poecilia mexicana) that have become so well adapted to their dangerous environment they are starting to evolve into a brand-new species. But what makes Cueva del Azufre so dangerous and how are the cave mollies able to survive there?

Environmental pressures

Hydrogen sulphide is a respiratory toxicant that is lethal to most organisms, even in micromolar amounts. H 2 S originates either in hypoxic environments where organic matter is decaying due to microbial activity, such as lakes or marshes, or from volcanic activity within some freshwater systems. Regardless, sustained high levels of H 2 S transforms aquatic habitats like Cueva del Azufre into extreme systems, making life difficult or even impossible for many organisms. Another inhibiting factor is the absence of a light source within the cave system meaning its inhabitants must adapt to perpetual darkness.

Consequently, life within cave systems often entails complex evolutionary distinctive life history traits. Within a small geographical range, there are distinct reproductively isolated populations of P. mexicana inhabiting environments ranging from a toxic cave, a nontoxic cave, a toxic surface stream and an array of nontoxic surface waters. Due to the spatiality and geographically distinct parameters of the cave system, it is theorised that the P. Mexicana inhabiting the inner reaches of the system are becoming distinct species from their freshwater cousins that are present at nontoxic environments surrounding the cave system.

Physiological adaptations

A principal adaptation to the concentrations of H 2 S is thought to originate in the respiratory system, whereby P. mexicana minimise uptake of H 2 S by respiring at the water’s surface utilising a compensatory behaviour known as aquatic surface respiration. Another distinct variation between the cave-dwelling P. mexicana and their nontoxic adaptive counterparts is in gill morphology. Due to the toxicity of the surrounding waters these organisms have developed an increase in gill size so as to extract the maximum available oxygen from the water columns.

Similarly, to minimise the uptake of H 2 S, these fish have also developed the ability to detoxify the chemical from within their own physiology. They do this by switching to anaerobic metabolism over aerobic, despite it being a much less efficient form of energy production. It has also been observed that there is an increased gene expression for proteins that break down H 2 S into nontoxic forms which can then be excreted. While increasing their resilience to the toxin, the fish have also found a method of neutralising and processing it from within their physiology.

Another problem for the cave mollies is that the inner reaches of the cave system have become such an epitome of extremity that few other organisms have followed them into their dark world. This has resulted in a loss of nutritional sources meaning they have become energetically limited. To adapt to this pressure, they have evolved to reduce their overall energy expenditure. To do this they have changed their diets preferring to feed on bacterial films and invertebrates rather than algae and detritus which has also led to a shorter and less energetically expensive intestinal tract. An interesting observation also notes how P. Mexicana have a smaller brain size, its theorised that this is related to the lack of food sources and is an attempt at further conservation of energy.

The fact that they live with a complete absence of light has also led to adaptations which conserve energy. In comparison to their counterparts outside the cave mouth, cave mollies have lost their colourful pigmentation, an unnecessary waste of resources in an unlit environment where visibility is poor. They have also evolved to have smaller, desensitised eyes, instead relying on a system of sense organs, known as the lateral line system, that detect movement, vibration and pressure gradients in the surrounding water.

Behavioural changes

Beside the evolutionary genetic adaptations observed in this extremophile, there are also a variety of behavioural changes which are paramount to their survival. Cave mollies are significantly less aggressive than their adjacent non-toxic cousins, this is likely due to the energy expenditure of aggressive behaviour, when resources are limited this is unadvisable. It has also been observed that cave mollies are less likely to shoal and are generally solitary.

Life in perpetual darkness has also had an influence on mate selection within cave dwelling species of Poeciliidae. Female mollies are observed to selectively choose larger males, relying upon their lateral line system rather than visual cues. A greater disturbance of pressure within the water column will indicate a larger male, offering an assessment of body size and physiological condition of a potential mating partner. Related to this, the live bearing mollies exhibit a lower fecundity rate, producing larger but less offspring, an advantage against the extreme conditions of the cave system.

It is observed that cave mollies within the labyrinth of the cave system are genetically different from surface water mollies, however, it has recently been noted that fish in varying chambers within the cave system are also genetically different to each other. This is likely due to the isolated populations having adapted to their own unique environment that each vary in levels of darkness and H 2 S. It makes cave mollies one of the most fascinating examples of how quickly and effectively life can evolve to cope with even the smallest of environmental differences.

Human pressures

Despite having to contend with high levels of H 2 S, perpetual darkness, and a limited amount of resources, the population of P. mexicana must also resist an annual religious ceremony by the local natives. This ceremony is thought to bring rain from the Gods and so each year the Zoque natives of Southern Mexico throw leaves containing a paste of ground barbasco root into the water column. Unfortunately the barbasco root contains rotenone, a powerful anaesthetic, and although not all fish are affected it can be very dangerous. Over time cave mollies have become much more resistant to the anaesthetic than their surface cousins, although males were significantly more susceptible than females.

To sum up

This is yet another example of how cave mollies have quickly adapted to their extreme environment via natural selection despite overwhelming odds against them. Not only have the cave mollies started to diverge from the rest of their species outside their caves but they are also evolving between different parts of them. They are a fantastic example of how extreme environments can re-shape and change and organism, but also how quickly and effectively those organisms are able to change. Despite the array of environmental stressors and anthropogenic impacts these hardy fish are insistent on surviving and thriving in their dark, toxic world.

Charlie is a third-year student studying Marine Biology at Bangor University, Wales. Alongside his studies he works under a research grant studying phenotypic plasticity in African Cichlids. You can email him directly at osub4a@bangor.ac.uk with any questions or comments.

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