The latest Paper of the Month for Parasitology is Restless nights when sick: ectoparasite infections alter rest–activity cycles of diurnal fish hosts and is freely available for one month.

Circadian rhythms are timekeeping mechanisms responsible for the cyclic repetition of metabolic, behavioural and psychological processes in all living organisms, typically over a 24-hour period. They are generated by self-sustaining biological clocks, encoded by “clock genes” and entrained by environmental cues such as light and temperature. Circadian rhythms have been observed in fish of economic importance and seem to govern functional activities ranging from reproduction and maturation to immune responses and disease susceptibility.  Disruption of the biological clocks can adversely impact animal health. Such disruption can affect rest-activity cycles and immunity, as shown in humans if natural circadian cues are ignored due to shift work, jet-lag and general sleep deprivation.

Circadian rhythms are also critical in the co-evolution of host-parasite systems, as synchronisation of parasite rhythms to the host can influence infection dynamics and transmission. Parasites can directly impact host rest-activity cycles, which are associated with activation of immune defences. In turn, host individuals are most at risk of acquiring parasitic infections when sleep deprived. Thus, the reciprocal interaction between rest-activity cycles and immune functioning is complex. Given our increasing understanding of the intricate link between fish body clocks and their immune systems, harnessing knowledge of circadian rhythms may be hugely beneficial in tackling infectious diseases. In this study, we examined the circadian rhythms in behaviour and activity of guppies (Poecilia reticulata) individually and in shoals, both when uninfected and infected with a helminth parasite (Gyrodactylus turnbulli). Additionally, we explored the rhythmicity in activity and transmissibility of the parasite itself.

Interestingly, our results showed that the circadian rhythm detected in guppy activity was disturbed by infection, resulting in increased nocturnal restlessness both individually and in shoals. Even though parasite behaviour and activity did not exhibit diurnal variance, parasite activity peaked at night, coinciding with the increase in host activity. A possible explanation for this host rest deprivation could be the increased activity of gyrodactylids. Whilst migration of gyrodactylids across the host’s skin may have caused irritation resulting in nocturnal restlessness, altered expression of host immunity might also have caused disruption in guppy activity rhythm.

Evidence of complex interactions between molecular clocks and immunity demonstrate that dysregulation of certain proteins may lead to immunodeficiency and disease. For example, inflammatory responses to infection significantly contribute to sleep disturbances, as the production and release of cytokines has been associated with the secretion of melatonin: a regulatory hormone essential for enhancing propensity to sleep. Perturbances in natural oscillations of a protein like melatonin can promote restlessness. While clock gene expression drives daily cycles in immunity, immune activation caused by infection can itself alter clock gene expression.

Regarding parasite activity, even though no ‘true’ circadian rhythmicity was detected, host seeking behaviour and activity were greater in the dark. This could potentially facilitate transmission between hosts, as fish are closely aggregated during shoaling, enabling infected fish to directly contact resting conspecifics potentially diluting their parasite burdens, a behaviour also known as ‘vaccination’. 

Better understanding of both guppy and gyrodactylid patterns, provides a greater insight in host-parasite dynamics. Using this knowledge of circadian rhythms may be helpful in tackling infectious diseases, which negatively impact fish productivity, health and welfare and can even lead to mortality. As parasites pose a significant threat to aquaculture, the use and application of chronotherapy could be a potential solution to this problem.

The paper Restless nights when sick: ectoparasite infections alter rest–activity cycles of diurnal fish hosts by Elissavet A. Arapi, Michael Reynolds, Amy R. Ellison and Jo Cable, published in Parasitology, is available free for a month.