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Marine biorhythms, bridging chronobiology and ecology part I by Martin Bulla et alii

tempo di lettura: 10 minuti


livello medio


parole chiave: Cronobiologia, ecologia


Marine biorhythms: bridging chronobiology and ecology
authors: Martin Bulla, Thomas Oudman, Allert I. Bijleveld, TheunisPiersma, Charalambos P. Kyriacou
Published 9 October 2017  DOI: 10.1098/rstb.2016.0253

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’.

1. Introduction
As the Earth rotates around its axis every 24 h, it generates relentless rhythms of light and dark, heat and cold. In addition, the tilt of the Earth’s axis produces the annual seasonal rhythms that so dramatically modulate the light and dark cycles as we move towards the polar extremes [1,2]. The rotation of the Earth and the gravitational pull of the Sun and the Moon deform the mass of the oceans, producing the rise and fall of sea levels every 12.4 h. When the Earth, Moon and Sun are in alignment during new and full moon every 15 days, the gravitational pull on the Earth’s oceans is at its maximum, producing the high-amplitude spring tides (figure 1a). When the Sun and Moon are at right angles when viewed from the Earth (Moon’s first or third quarter), the gravitational pull on the oceans is reduced, generating the low-amplitude neap tides (figure 1a). Furthermore, when the Moon orbits off the equatorial plane the tide is higher at night than during the day, a phenomenon termed ‘diurnal inequality’ ([3] and figure 1b). Finally, there is the waxing and waning of the Moon itself with its 14.8 day semi-lunar and 29.6 day lunar cycles.

Questa immagine ha l'attributo alt vuoto; il nome del file è bulla-cronobiologia.jpg

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). da Marine biorhythms: bridging chronobiology and ecology – PubMed (nih.gov)

For hundreds of millions of years these geophysical cycles have shaped the behaviour and physiology of organisms. Not surprisingly, nearly all terrestrial and marine species (including some bacteria) show circadian phenotypes [4]. In addition, organisms living in intertidal zones also show tidal, semi-lunar and lunar cycles [5]. However, marine biorhythms are rarely studied in higher vertebrates [6]. Also, whereas genetic studies of circadian rhythms have a 45-year history, particularly in the model organisms of mouse and Drosophila, until recently a similar approach to studying rhythms in intertidal (non-model) organisms was not feasible. However, in the past few years, the advent of genomic technologies that are applicable to any species has initiated the mechanistic study of tidal and lunar cycles of behaviour and physiology [7].

Here, our aims are threefold. We first address the scarcity of data on intertidal higher vertebrates by investigating the interactions between tidal and daily cycles in the foraging movements and incubation rhythms of shorebirds. We then discuss some fresh studies that have illuminated the role of circadian clock genes in the intertidal behaviour and physiology of arthropods and worms. Finally, we use our findings and the reported examples to highlight how collaborations between field ecologists and chronobiologists may uncover fundamental adaptive principles about biorhythms in the wild.

2. Tidal rhythms in shorebirds
Substantial numbers of shorebird species live and feed, at least for part of the year, in tidal habitats [8,9]. Some of these tidal populations are sedentary in tidal environments, and face day–night fluctuations of illumination throughout the year (e.g. several species of oystercatcher, Haematopus; [10]). Other populations are migratory and live in the coastal nonbreeding areas during 8–10 months of the year, where they cope with a combination of tidal and day–night environmental rhythms (e.g. bar-tailed godwit, Limosa lapponica; sanderling, Calidris alba; and red knot, Calidris canutus), and breed in Arctic non-tidal environments for two months of the year, where day–night environmental rhythms are damped [8,9]. Shorebirds manage the interplay between circadian and tidal environmental, but how they schedule their behaviour to the interacting environmental rhythms is unclear [11]. Indeed, the behavioural rhythms of shorebirds under such circumstances are relatively unexplored (but see [12,13]). To anticipate tidal foraging opportunities, it is assumed that these species have activity patterns with a period length resembling the tidal period. We might expect shorebirds that use tides throughout the whole year to exhibit incubation rhythms with tidal periods [14] more readily than shorebirds that only use tides away from their breeding grounds. Nevertheless, as changing to a different rhythm may be costly [15], the tidal activity patterns could carry over to incubation even for shorebirds that are tidal only when away from their breeding grounds. The aims of our shorebird study are twofold. We used novel automated-tracking technology [16] to first describe the foraging rhythms of red knots at Banc d’Arguin, their coastal Mauritanian wintering ground—an environment with both tidal rhythms and strong diel fluctuations in light intensity (see [17]. Second, we analyse data from a recent comparative study on shorebirds that incubate biparentally [14,18], to reveal whether shorebirds with tidal life-histories keep tidal rhythms also during incubation [14].

(a) The tidal rhythm of red knots
Red knots, C. canutus, are long-distance migratory shorebirds that breed in the High Arctic and live in coastal intertidal environments during the rest of the year [19,20], where they almost exclusively eat hard-shelled molluscs ingested whole and crushed in their large muscular gizzards [21]. When the tide goes out and the intertidal mudflats become available they take the opportunity to feed, being forced to retreat to shoreline high-tide roost during the high-water periods [22]. However, the individual variation in foraging rhythm of knots (and of any other intertidal bird) is unknown. We found that the distance of red knots to their roosting site followed the tidal as well as the day–night rhythm (tidal = 88% of individuals, daily = 57%, both rhythms = 52%; N = 42 individuals with more than 50 h of observation; median [range] = 19 [2–34] days of observation per individual; for methods see Supplementary Information [16]). At high tide, the birds were generally close to the roost and as the tide retreated, birds moved away from it (figure 2a). How far the birds moved was modulated by time of day, but in a bird-specific manner (figure 2b). For example, one bird usually roamed between 400 and 600 m from its roost when the low tide occurred during the day (figure 3a, light blue), but often went to mudflats further than 1 km from its roost when the low tide occurred at night (figure 3a, dark blue). In this particular bird it seems that an approximately 15 day semi-lunar pattern also emerges where the distance travelled at night is greater and is particularly consolidated when the low tide is at its lowest ebb.

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. Marine biorhythms: bridging chronobiology and ecology – PubMed (nih.gov)

The reported tidal rhythms (figure 2a) reflect red knots’ feeding on molluscs that are only available during low tide. However, why red knots varied so much in how far they travelled during the night and during the day remains unclear. Such daily rhythms (superimposed on the tidal rhythm) can be partly a consequence of the slightly higher tide during the night (figure 3b), reducing the maximal extent of the available foraging area. However, why some individuals foraged further from the roost during the night is unclear and unlikely a consequence of dynamics in searching efficiency or food availability. That is, red knots forage by touch rather than by sight [23] and the burying depths of their main prey are not expected to differ between day and night. An alternative explanation for the individual differences may be individual experience with predators. During the day, red knots are predated mainly by large falcons [24,25], and during the night by owls [26–28] . Thus, depending on the local distributions of these two kinds of predators and individual experiences with these predators, the red knot’s perceived ‘landscape of fear’ [29], and hence its movement choices, may differ between individuals and between day and night, something worthy of future investigations.
The individuality of red knot tidal movements and hence the investigation of among-individual variation in behavioural rhythms in the wild contrast starkly with laboratory studies where individual subjects, for methodological reasons, are often chosen to be as similar as possible. Although foraging rhythms of red knots appear related to both tidal and daily environmental fluctuations, quantitative studies from different locations are required to validate the generality of these behavioural rhythms, as well as to explore (albeit in a correlative manner) the hypotheses about possible ecological causes of such biorhythms. Also, to demonstrate whether individuals will free-run with circatidal or circadian rhythm or with both of these rhythms, and hence to demonstrate whether these rhythms are truly endogenous, we would need to keep red knots under constant conditions. Such observations will also reveal whether the among-individual differences are endogenous.

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. Marine biorhythms: bridging chronobiology and ecology – PubMed (nih.gov)

(b) Do tidal shorebirds maintain a tidal incubation rhythm?
In a recent study of 32 species of shorebirds with biparental care, only in 5% of 584 nests did the shorebird pairs display an incubation period length that might have been entrained by the tide [14]. This is surprising, given that half of the studied species live in intertidal habitats away from their breeding grounds [14]. Interestingly, from populations known to forage on intertidal habitats at their breeding grounds (N = 10), pairs in only 3 out of 74 nests displayed a period length entrained by the tide. In contrast, incubation rhythms with periods that do not follow the 24 h light–dark cycle were more common and the deviations from 24 h increased in shorebirds breeding at high latitudes.

Although these findings support the existence of a latitudinal cline in incubation rhythms, a substantial number of rhythms defied the 24 h day even at low and mid latitudes. These results might reflect an underestimation of tidal and circadian patterns in incubating shorebirds because the method used depicted only the dominant period of the incubation rhythm, yet other less-dominant periodicities were rare [14]. Importantly, the study suggests that other factors (such as risk of predation and synchronization of the clock between the two parents) might be much more important than any geophysically imposed variable, hence the extremely variable and generally non-daily/tidal rhythmicity in incubation [14].

In summary, these findings suggest that tidal life-history seems to play, at best, a negligible role in determining incubation rhythms, even in shorebirds that forage with the tide during breeding. They corroborate the observations on pre-incubation activities of shorebirds on their Arctic breeding grounds; birds were active around the clock without significant tidal periodicity [30]. Chronobiologists might ask whether these variable cycles of incubation mask an otherwise endogenous circatidal rhythm. Unfortunately, to study any such tidal cycle, birds would have to be removed from the entraining stimuli, conspecifics and any potential predators and placed in free-running constant conditions for several days, something that is impractical during breeding.

end part I 


1. Alerstam T. 1990. Bird migration. Cambridge, UK: Cambridge University Press.
2. Hut RA, Paolucci S, Dor R, Kyriacou CP, Daan S. 2013. Latitudinal clines: an evolutionary view on biological rhythmsProc. R. Soc. B 280, 20130433 (doi:10.1098/rspb.2013.0433[PMC free article][PubMed]
3. de la Iglesia HO, Johnson CH. 2013. Biological clocks: riding the tidesCurr. Biol. 23, R921–R923. (doi:10.1016/j.cub.2013.09.006[PMC free article] [PubMed]
4. Dunlap J. 2004. Chronobiology. Sunderland, MA: Sinauer Associates.
5. Naylor E. 2010. Chronobiology of marine organisms. Cambridge, UK: Cambridge University Press.
6. Palmer JD. 2000. The clocks controlling the tide-associated rhythms of intertidal animalsBioessays 22, 32–37. (doi:10.1002/(SICI)1521-1878(200001)22:1<32::AID-BIES7>3.0.CO;2-U[PubMed]
7. Kaiser TS, et al. 2016. The genomic basis of circadian and circalunar timing adaptations in a midgeNature 540, 69–73. (doi:10.1038/nature20151[PMC free article] [PubMed]
8. del Hoyo J, Elliott A, Sargatal J. 1996. Handbook of the birds of the world. Barcelona: Lynx Edicions.
9. van de Kam J, Ens B, Piersma T, Zwart L. 2004. Shorebirds: an illustrated behavioural ecology. Zeist, The Netherlands: KNNV Publishing.
10. Ens BJ, Underhill LG. 2014. Synthesis of oystercatcher conservation assessments: general lessons and recommendationsInt. Wader Stud. 20, 5–22.
11. Helm B, Gwinner E, Koolhaas A, Battley P, Schwalb I, Dekinga A, Piersma T. 2012. Avian migration: temporal multitasking and a case study of melatonin cycles in waders. In The neurobiology of circadian timing (eds A Kalsbeek, M Merrow, T Roenneberg, RG Foster), pp. 457–479. Amsterdam: Elsevier.[PubMed]
12. Daan S, Koene P. 1981. On the timing of foraging flights by oystercatchers, Haematopus ostralegus, on tidal mudflatsNeth. J. Sea Res. 15, 1–22. (doi:10.1016/0077-7579(81)90002-8)
13. Hötker H. 1995. [Activity rhythms of shelducks (Tadorna tadorna) and waders (Charadrii) on the North Sea coast]J. Ornithol. 136, 105–126 (in German with English abstract) (doi:10.1007/BF01651234)
14. Bulla M, et al. 2016. Defying the 24-h day: unexpected diversity in socially synchronized rhythms of shorebirds Nature 540, 109–113. (doi:10.1038/nature20563[PubMed]
15. Foster RG, Wulff K. 2005. The rhythm of rest and excessNat. Rev. Neurosci. 6, 407–414. (doi:10.1038/nrn1670[PubMed]
16. Bulla M, Oudman T, Bijleveld AI. 2017. Supporting information for ‘Marine biorhythms: bridging chronobiology and ecology’ Open Sci. Framework. (doi:10.17605/OSF.IO/XBY9T[PMC free article][PubMed]
17. Zwarts L, Blomert A, Hupkes R. 1990. Increase of feeding time in waders preparing for spring migration from the Banc d’Arguin, MauritaniaArdea 78, 237–256. 

see also II Part at
30. Steiger SS, Valcu M, Spoelstra K, Helm B, Wikelski M, Kempenaers B. 2013. When the sun never sets: diverse activity rhythms under continuous daylight in free-living arctic-breeding birdsProc. R. Soc. B 280, 20131016 (doi:10.1098/rspb.2013.1016[PMC free article] [PubMed]


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