Abstract
It has long been known that the waterflea Daphnia hyalina exhibits diel vertical migration in the water column, but the chemical that triggers this behaviour has not been identified. We find that trimethylamine (TMA), which is a major component of the odour produced by decaying fish, induces Daphnia to migrate to greater depths during the day, presumably to avoid predation by fish1,2. We observed a gradual increase in average depth of Daphnia with increasing TMA concentration. Changes in light intensity are known to trigger migration3, and chemicals produced by their predators must also be present4. Because migration has demographic and physiological costs, this chemical cue ensures that zooplankton migration occurs only when fish are present.
Main
It has been shown that, whatever the migration trigger substance may be, it is produced only by fish in the presence of bacteria. This led to the hypothesis that trimethylamine-N -oxide (TMAO), which is important for cell volume regulation5 and protein stabilization6 in marine and freshwater fish, could be a precursor of the kairomone. Surplus TMAO is deposited in fish scales7, and bacteria of the skin mucus layer are known to reduce TMAO to TMA8.
We tested the hypothesis that TMA induces vertical migration in Daphnia by using a range of different concentrations, from 0 to 500 μM TMA, in autoclaved lake water9 (Fig. 1). Five individuals of a single Daphnia hyalina clone were put into each of four Perspex tubes (1 m long and 1.5 cm in diameter) per treatment. The tubes were then placed in a water bath with a temperature gradient from top to bottom of 20 to 10 °C. We used a spectrophometric assay procedure10 to establish the TMA concentration in 10 litres of the medium that had previously contained four fish (ides, Leuciscus idus, 10 cm long), and recorded the resulting vertical migration behaviour of daphnids exposed to this medium. TMA concentration in this ‘fish’ water was between 10 and 25 μM.
We found that even low concentrations of TMA induce Daphnia to migrate to deeper waters during the day in our test system. At night, they migrate back to the surface when exposed to small amounts of TMA, and stay near the bottom when TMA levels are high (more than 100 μM). When the lowest TMA concentration that induces vertical migration is compared with the activity in the fish water, it is clear that the reaction of Daphnia to fish water is stronger than just to TMA alone. This indicates that, although TMA is an active component of the ‘fish factor’, it is likely to be part of a cocktail of substances that deter Daphnia. The other substances probably help to reduce the chemical threshold that induces migration. It is not clear whether the TMA concentrations used in this study represent realistic values for aquatic systems, as we could find no published details of TMA concentrations in aquatic systems.
It has been shown9 that the fish kairomone is broken down by bacteria. We therefore compared the average day depth of daphnids exposed to 75 μM TMA in autoclaved water, and with the antibiotic ampicillin added and the TMA dissolved in non-autoclaved lake water. The migration activity of the Daphnia in non-sterile water slowly decreased over time (Fig. 2). After 72 hours, the average day depth of the animals in non-sterile conditions was no longer significantly different from the average day depth of animals in sterile control medium.
To investigate whether simply adding any substance to the water induces vertical migration, we added the same amount of TMAO and triethylamine to sterile water (both at 75 μM). As with the control Daphnia, there was no significant increase in day depth. We therefore conclude that the reaction to TMA is a specific one, and not simply a response to a change in conductivity or ionic strength of the medium.
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Boriss, H., Boersma, M. & Wiltshire, K. Trimethylamine induces migration of waterfleas. Nature 398, 382 (1999). https://doi.org/10.1038/18796
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DOI: https://doi.org/10.1038/18796
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