Dive deep into the process of aestivation—an evolutionary edge possessed by lungfish that allow them to survive dry river spells. Image credit: Keagan Henman via Unsplash.
Tell-tale ripples of feeding fish decorate the surface of the Bandama River in the Ivory Coast, spreading out from a polka dot pattern of creatures emerging from the murky shallows. But there’s an odd one out: surfacing not to snatch an insect morsel, but instead a gulp of air. This one is a West African Lungfish, but three more Lungfish species can also be found in Africa.
Up to a metre long, eel-like in shape, and with a hint of leopard print against its otherwise olive-brown scales, this fish lives on the tightrope between life underwater and life on land. “Lungfish” is no misnomer. Possessing a pair of lungs, they must surface regularly to take in oxygen, with their gills alone providing insufficient supply. Their air gulping hints at an even more remarkable feature, which takes some effort for a fish that has a lung. Not conforming to the fish rule book, they can withstand their river home receding during the dry season.
Whilst other fish might retreat to inevitably overcrowded pools or migrate away, and others perish (instead relying on their eggs, buried in mud, to make it through the dry season), African Lungfish burrow into the drying riverbed. Here, they encase themselves in a mucus cocoon with just a gap for their mouth, allowing them to breathe air but going without food or water for months (and potentially up to four years). This is aestivation, occurring when animals press the pause button and become physically and metabolically inactive (a state called torpor) to withstand warm and dry conditions: an analogue to hibernation.
Aestivation is largely confined to tropical animals, generally out of reach for the globally northern-biased science community. This, combined with its difficulty to induce artificially in a laboratory, has meant aestivation has remained more enigmatic than hibernation. That hasn’t stopped these fish from being a subject of long-time fascination, however, starting with predictably extravagant attempts by Victorian naturalists to ship African Lungfish halfway around the world to the UK and USA, with the aim of physiological observations. Since then, research technologies have advanced, revealing cellular and genetic processes underpinning African Lungfish’s aestivation.
As we shall see, we are now able to follow the aestivation journey of an African Lungfish, from starting off the process to shutting down the body for months, to the emergence and end of aestivation when the waters return. Understanding how Lungfish sleep through the heat has implications for broad evolutionary theory and specific applications in conservation regarding fisheries management and climate change.
Understanding how Lungfish sleep through the heat has implications for broad evolutionary theory and specific applications in conservation regarding fisheries management and climate change.
Deep dive: decoding the mechanisms of Lungfish slumber
When conditions change, animals face a flight or fight decision at the ecological level: do they move away or stay where they are and fight the change? With no legs to conquer land, and potentially being cut off from other habitats as the water recedes, African Lungfish have taken the second route down into the mud—staying put but existing in a state of inactivity until water returns.
Induction: triggering aestivation
Induction, the first phase of aestivation, lays the behavioural and physiological foundations for spending the coming months underground. In 1986, the aptly named Fishman et al. suggested a range of cues triggering aestivation: dehydration, starvation, increased air-breathing, and stress. There are more recent suggestions of changes in salinity and the composition of dissolved substances (such as calcium and magnesium) in the surrounding water as cues as rivers dry up. As with much in biology, it is likely that a combination of factors gets the ball rolling on aestivation, although it is still unknown exactly how environmental cues are detected. Perhaps gills play a role, given their general importance in sensing water concentration inside the body of fish.
As with much in biology, it is likely that a combination of factors gets the ball rolling on aestivation, although it is still unknown exactly how environmental cues are detected.
With these cues of their surroundings letting them know it’s warming up and drying out, the fish—in a rather undignified fashion—excavate underground chambers in the mud using their mouths for digging and their muscular bodies to burrow into the ground. They then retreat into these chambers, curling up their long bodies and encasing themselves in vast quantities of secreted mucus. Once the mucus has hardened, a watertight cocoon is left, save for a narrow opening to the surface, allowing the fish to breathe air using its lungs. This air-breathing trick reveals the backstory of why African Lungfishes surface for gulps of air during the wet season.
Nevertheless, going underground isn’t enough to get a Lungfish through the warm, dry weather. Their mucosal architectural efforts need to be accompanied by physiological changes. After all, the fish doesn’t have access to food and water for many months, requiring a fundamental metabolic shift.
Analyses at the genetic level have revealed increased expression of hormonal signals in the brain, produced by increased gene activity; this goes against the classical view of genes slowing down and reducing their activity in other systems preparing for summer torpor. Amongst these products of increased gene activity are growth hormone—perhaps not coincidentally associated with sleep in other animals—and prolactin, which has a role in coordinating responses to water concentration throughout the body. In this induction phase, increased metabolic activity occurs, preparing the body for torpor like the final flurry of pre-Christmas preparations.
Maintenance: deep sleep
Sure enough, metabolic shutdown follows during the maintenance phase, beginning once the mucus cocoon has fully dried. Oxygen intake occurs only via the lungs, with O2 consumption dropping to half of that seen in active African Lungfish in the water. These changes are accompanied by a plummet in metabolic activity, a drop in heart rate to around two beats per minute (compared to 25 bpm whilst active in the water), and a stop to ammonia production as a nitrogenous waste product, of which a build-up could be toxic. Parts of the body are remodelled, including the intestine, kidney, and heart, reflecting their functionally reduced role during aestivation, and internal stores are the only source of energy for the fish.
Although these broad patterns have been known since the 1960s and 70s, nuances are becoming clearer. Unlike during induction, prolactin production drops during the maintenance phase. Nevertheless, there is again the broad pattern of genes generally increasing in activity rather than decreasing. Therefore, although much of the body undergoes a drop in activity, the brain remains an important, active coordinating centre.
Yet as successful as this trick is for protection against the elements, with immobility and inactivity comes vulnerability; they need to avoid succumbing to their living enemies. Once again, some early research from 1931 gave a clue as to how they do this.
Large numbers of granulocytes (white blood cells, important in the immune system) deposited in the gut, kidney, and gonads of wet-season African Lungfish hint at a role in aestivation. A 2021 Science publication validated these suggestions and reported the discovery that the mucus cocoon is packed with these granulocytes. These trap pathogens before reaching the aestivating African Lungfish, transforming an earlier paradigm of the cocoon as an inert structure. Granulocytes migrate from their organ storerooms, through the bloodstream to the skin, which enters a state of inflammation, before finishing their journey in the cocoon. Here, granulocytes produce extracellular traps, preventing bacteria from reaching the vulnerable, aestivating Lungfish and making the cocoon an immunological, rather than purely physical, barricade—supplemented by goblet, epithelial, endothelial, and other immune cells also found in the mucus cocoon. Proving the importance of this mucosal biohazard suit, experimentally disabling these granulocytes left Lungfish with increased bacterial presence in the blood and skin infections. Whilst the aestivating African Lungfish lies dormant, the living tissue cocoon remains a hive of activity.
Whilst the aestivating African Lungfish lies dormant, the living tissue cocoon remains a hive of activity.
Arousal: the revival
But eventually, water returns, dragging the African Lungfish out of its summer slumber as its mouth—the only body part not encased by the mucus cocoon—fills with water. This begins the arousal stage of aestivation, the most mysterious phase of the three. Struggling free from its cocoon and rising to the surface sluggishly, presumably like a wearied hotel patron making towards the breakfast buffet, the Lungfish excretes the waste it has accumulated over its aestivation. After around ten days—giving time for internal organ restructuring—the fish begins to feed again. As remarkable as its ability to aestivate in such extreme conditions is its ability to return to a free-living state so quickly, completing the transformation in about the amount of time it has taken me to write this article.
Evolution, environment, and the bigger picture
This transition between water and land offers a glimpse of the evolutionary shift of vertebrates living in water to living on land. As the extant relative to all tetrapods (four-limbed vertebrates and vertebrates descended from four-limbed ancestors), unravelling how the four African Lungfish species (in the Protopterus genus) carry out their Jekyll-and-Hyde routine could shed light on the mechanisms allowing this formative movement onto land. Aided by the recent assembly of the vast West African Lungfish’s genome, genetic innovations could be linked to those physiological adaptations we’ve already seen.
This transition between water and land offers a glimpse of the evolutionary shift of vertebrates living in water to living on land.
Occupying this ringside seat in tetrapod evolution, African Lungfish have remained largely morphologically similar for 390 million years, with fossils of burrowing Lungfish dating back to the Devonian period in Earth’s history. It is poignant, therefore, that this great survivor of millions of years faces destruction by decades of human activity. For instance, Marbled Lungfish have declined in the Lake Victoria Basin by around 11% in just five years, likely due to over-fishing and agricultural sprawl driving wetland degradation and loss. Regarding climate change, this animal is one of the great survivors. Nevertheless, unpredictable rainfall patterns in the future could push drought to unsustainably long periods. Alternatively, African Lungfish are highly plastic and may have the ideal adaptations to persist through climatic unpredictability, a testament to the resilience of life on Earth.
The ability of African Lungfish to sit out the annual drying-up of its habitat by constructing a cocoon underground and entering aestivation is a level of resilience at odds with our mammalian impressions of the world and has fascinated biologists for centuries. Our appreciation for this remarkable persistence should only blossom as science reveals more of the secrets of African Lungfish. Their ability to thrive in conditions that seem inhospitable, in ways that are at odds with our human impressions of summer as a frenzy of activity, demonstrates nature’s resilience and diversity, underpinned by the innovative force of evolution.
