Arapaima ‘Milk’: Reflections on big fish and a big biological problem

Since the discovery of ‘lactation’ in discus fish, the production of mucus by a number of other species to feed their young has been described. Somewhat different has been the description of what happens in the Giant Arapaima (Arapaima gigas)—an endangered species of the Amazon basin and one that can reach a length of three metres. Locals had observed the gathering of young around the head of the male and the release from the head of a milky fluid into the water. Some work has been done on the phenomenon because these fish are bred and reared for human consumption.

Giant Arapaima (Credit: Citron / CC-BY-SA-3.0)

The fluid comes from the cephalic canals of the lateral line system. The eggs, larvae and young are in close contact with this secretion, even when the male is leading the offspring to water rich in plankton for feeding. Parental care last for three months. There are numerous possibilities for the function of “arapaima milk”. A paper published late last year* describes an attempt to set the ball rolling in this respect by taking a proteomic approach to the composition of the fluid.

The fluids from the cephalic canals breeding and non-breeding males and females were analysed since any additional substances present in the former could indicate a particular adaptation that benefits the young. To cut a long story short, the total protein content of the fluid was low, suggesting that the fluid is not important in nutrition, even if the young were to eat it. There were a number of antimicrobial agents in the vast array of peptides present. Two hormones, prolactin and stanniocalcin were detected in females.

The great problem, as with substances in mammalian milk, is to identify which, if any, substances of the hundreds present have a physiological rôle in the offspring. Fluid from the cephalic canals is bound to reflect cellular and protective systems within that system. They may be in the fluid for no other reason than they are disposable elements and have no function at all in the offspring. But protection for the cephalic canals against infection, which are open to the surrounding water, could simply being extended to provide some degree of protection to the offspring, from contact with the skin and gills and/or by ingestion.

The question of biological signals from parent to offspring through hormones or other biologically active substances has also been raised in discussions of skin or, in this case, cephalic secretions, of fish. For example, it might be tempting to speculate on whether the prolactin detected in female arapaima milk has any effect on the offspring. However, it is a hormone that one would expect to be present given its function in mediating aspects of maternal care in vertebrates and its presence in fluid could simply reflect an action on the tissues of the cephalic canals rather than any significance to the offspring.

Mammalian milk contains a large number of hormones, growth factors and the like which could have an effect on the young. So many people were—and still are—assuming that presence in milk indicates a function in the young mammal ingesting the milk that Peggy Neville and I warned against making such assumptions and published a list of criteria that would need to be met in order to demonstrate that such an effect was taking place:

1. An effect in the offspring must be obtained in response to exposure to the substance in milk.
2. The effect in the offspring must be abolished by removal of the substance from milk and restored when that specific component is restored.
3. Th substance must be shown to be present and active in milk.
4. The substance must be shown to retain its biological activity in the offspring to the point at which it is postulated to act or to be activated by partial digestion within the digestive tract.

Shortly after we wrote that commentary in 1991 only two series of studies satisfied those criteria.

The criteria for demonstrating an effect of a substance in milk on the offspring are tough to fulfil. But they have to be in order to prevent the proliferation of just-so stories masquerading as science. It would be a simple matter to modify those criteria to parental care in fish and any potential chemical communication between parent and offspring through skin or cephalic secretions.

The only clue I have seen so far for the importance of arapaima milk is: ‘Previous work suggested fingerlings raised under parental care condition would have higher survival rates and enhanced growth performance compared to in-door reared ones’*.

I also wondered—and have not seen discussed (although I have not looked that hard)—whether arapaima milk had some chemoattractant function, keeping the offspring concentrated around the head of the male when he finds plankton-rich but possibly murky water in which they can feed. But like every other suggestion that is a just-so story that ‘ain’t necessarily so’.

*Torati LS, Migaud H, Doherty MK, Siwy J, Mullen W, Mesquita PEC, Albalat A. 2017. Comparative proteome and peptidome analysis of the cephalic fluid secreted by Arapaima gigas (Teleostei: Osteoglossidae) during and outside parental care. PLoS ONE 12(10): e0186692. https://doi.org/ 10.1371/journal.pone.0186692

Peaker M, Neville MC. 1991. Hormones in milk: chemical signals to the offspring? Journal of Endocrinology 131, 1-3.