Marine biorhythms: bridging chronobiology and ecology

Abstract

Marine organisms adapt to complex temporal environments that include daily, tidal, semi-lunar, lunar and seasonal cycles. However, our understanding of marine biological rhythms and their underlying molecular basis is mainly confined to a few model organisms in rather simplistic laboratory settings. Here, we use new empirical data and recent examples of marine biorhythms to highlight how field ecologists and laboratory chronobiologists can complement each other's efforts. First, with continuous tracking of intertidal shorebirds in the field, we reveal individual differences in tidal and circadian foraging rhythms. Second, we demonstrate that shorebird species that spend 8-10 months in tidal environments rarely maintain such tidal or circadian rhythms during breeding, likely because of other, more pertinent, temporally structured, local ecological pressures such as predation or social environment. Finally, we use examples of initial findings from invertebrates (arthropods and polychaete worms) that are being developed as model species to study the molecular bases of lunar-related rhythms. These examples indicate that canonical circadian clock genes (i.e. the homologous clock genes identified in many higher organisms) may not be involved in lunar/tidal phenotypes. Together, our results and the examples we describe emphasize that linking field and laboratory studies is likely to generate a better ecological appreciation of lunar-related rhythms in the wild.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Keywords: circadian; invertebrates; lunar; molecular; shorebirds; tidal.

Figure 1.

Variation in high-tide levels. (a) When the Sun, Moon and Earth are in alignment during new or full moon (i.e. twice a month) the gravitational pull on the oceans is strongest, producing the high-amplitude spring tides, i.e. lunar tide (dark blue) and sun tide (light blue) combine. In contrast, when the Moon is in its first or third quarter the gravitational pull on the oceans is reduced, leading to the low amplitude neap tides. (b) If the Moon orbits directly over the Equator, the day and night tides are similar, whereas when the Moon orbits at high declination the night tides are higher than the day tides (diurnal inequality; indicated by red dots).

Figure 2.

Distance of redknots to their to the closest roost relative to high tide (a) and time of day (b). Each line depicts the model prediction for a single individual (N = 42 individuals; see [16] for details.

Figure 3.

The distance of a radio-tagged red knot to its roost. (a) The distance to the main roost (the darker the blue, the farther the knot travelled). Sunrise and sunset are given by the solid vertical lines and the day and night are indicated above the actogram. The low tide times are given by the dashed lines. For actograms see [16]. (b) Differences in low-tide water height between day (open circles) and night (filled circles) and during the neap–spring lunar cycle.

Figure 4.

Examples of lunar-related rhythms of invertebrates. (a) Eurydice adult with chromatophores (black dots on the dorsal surface of cuticle) and swimming activity of a single individual over 9 days in constant darkness). The animal was taken during a spring tide from Bangor, Wales, UK and placed immediately in constant darkness (DD). The approximate natural light (grey)/dark (black) cycle on the day the animal was harvested is shown as a bar above the actogram and each day's activity is double plotted on a horizontal 48 h scale so that so that each row represents two consecutive days. Note that the movement to the right on every successive day reveals a tidal period longer than 12 h and the night-time activity is greater than that of the daytime (diurnal inequality). Adapted from [30]. (b) Mangrove cricket and an actogram for single individual placed in 12 L: 12 D for 8 days then allowed to free run in DD, during which there is more intense activity in the dark phase compared with the light phase (see the histogram) which drifts towards the right reflecting the predominantly 24.8–25.5 h rhythm which is about twice the tidal period of approximately 12.4 h. The histogram shows the night-time burst of activity (filled columns) being greater than the daytime burst (unfilled columns) for a few cycles but as this is modulated by the circadian clock, it drifts out of phase with the tidal cycle; so after many cycles, the daytime tidal episode is greater than the night-time (adapted from [33]). The cricket image is taken from http://mangrove.nus.edu.sg/guidebooks/text/2010.htm. (c) Midge C. marinus and five natural populations (i) with different phases of emergence (ii) and semi-lunar or lunar frequency during day of emergence (iii). Image is taken from https://www.flickr.com/photos/davidh-j/6270311922 and figure was adapted from [34]. (d) Premature adult, and adult male and female Platynereis dumerilii. Lunar maturation cycle of single individual over several months. FM, full moon simulated by dim light. NM, new moon. Lunar month in days plotted as horizontal yellow bar. Adapted from [35].