Ecology

Fairy circles (FCs) are remarkably circular and regular vegetation patterns covering an area of thousands of square kilometres in hyper-arid grasslands in Southern Africa (e.g. Namibia)1,2,3. They are typically made up of perennial tufts of Stipagrostis grass growing around barren circular patches roughly 2–10 m in diameter, with annual or perennial grasses in the area between circles, the matrix1,2. The edges of FCs are about 5–10 m apart and when dense they have a regular hexagonal arrangement3. Similar vegetation rings also occur in arid lands in Australia, Israel and elsewhere1,2,3,4,5,6,7. The processes leading to the formation of FCs have been the subject of debate for several decades8,9,10,11,12,13.
Aspects of FCs that require explanation include how and why individual circles form, how they persist and how the similar size and regular pattern is established at the landscape scale. The bare centres of individual FCs persist in situ almost permanently, although the peripheral plants delimiting the circles are much shorter-lived. Van Rooyen et al.8 noted no change in the position of five marked FCs over 22 years, despite intervening droughts8. Tschinkel14 analysed pairs of aerial photographs taken 4 years apart, and on the basis of how many FC positions were unchanged, died or emerged, estimated that average sized FCs persist in situ for an average of 75 years, implying some circles remain in situ for a century14. Similarly, using aerial photographs, Juergens2 noted a high survival (97%) of FCs in situ over a 50-year period (=0.06% pa mortality), implying an age of millennia for some FCs2.
Many alternative hypotheses have been proposed for FC spatial and temporal patterns, but without agreement. The first hypothesis is based on ecosystem engineering by termites that remove plants from the centres of circles2, facilitating localized underground water accumulation in circle centres. This moisture maintains the termites and the band of perennial grass on which termites feed year-round. The spatial patterning of the FCs is considered to result from competition between termite colonies2. However, the poor correlation of FCs with the presence of specific termites is an important concern with this hypothesis13.
The second hypothesis is based on the clonal mode of growth of individuals of many arid-land species that create vegetation rings4,6,7,15. For example, rings are formed by one of the Namibian FC species, Stipagrostis ciliata in the Negev desert. Here individual plants of this species send out underground rhizomes, which, with increasing age, results in a ring of ramets (i.e. sprouts from the same clonal colony or genet) around a barren central patch, which forms as the plant centre dies4. Such vegetation rings form and enlarge centrifugally due to competition between ramets, and as this process continues over time new ramets establish successfully only towards the periphery4,7. Globally, all of the many plant species that form circles do so by this type of clonal growth15. As the pattern of FCs is virtually fixed in situ for centuries, this suggests that the plants that indicate the pattern may also be long-lived. Individual clonal plants can be extremely long-lived15,16, which could then match longevities between the plants and the FCs they delimit. The clonality hypothesis could thus explain how circular shapes form (by self-thinning of ramets spreading from source plant), why bare centres occur (resource depletion and source plant death) and how they can persist over long periods of time (by continuous production of short-lived ramets). However, clonality has been disputed8 as an explanation for FCs for two reasons. Firstly, van Rooyen et al. suggested that the FCs referred to by Danin and Orshan are considerably smaller (about 2 m) than most FCs in Namibia4,8. Although this is correct that FCs tend to be much larger in Namibia, the mean size of FCs can be as small as 2.5 m in some areas2. Secondly, van Rooyen and colleagues suggested that clonality cannot explain why FC centres are bare8. Bare centres are now well known in rings and are commonly explained as being due to inter-ramet competition and resource depletion7.
The third hypothesis for FC spatial patterns is that it emerges through vegetation self-organization (the VSO hypothesis)1,5,12,17,18. Grasses in the peripheral band outcompete grasses in the FC centre and keep it bare and moist at depth1. The plants in the peripheral bands also compete with the matrix grasses and with the peripheral bands on adjacent FCs to maintain the regular pattern1. Mathematical vegetation models based on partial differential equations represent the theoretical basis of the VSO hypothesis17,18. These partial differential equations do not operate at the scale of individual-plant interactions, but at the level of local processes (largely rates of lateral water movement due to plant evapo-transpiration) in comparison to rates of lateral biomass spread. For these current VSO models, lateral water flow needs to be about 100 times faster than lateral biomass spread18. Thus, the mode and rate of how biomass spreads, whether via clonal growth or seed dispersal and population growth18, has an impact on the viability of vegetation-patterning models. In the absence of such information for FCs, the most recent VSO modelling study18 assumed a rate of biomass dispersal (1.2 m2 yr−1) derived from the Canadian woodlands19, for clonal spread or seed dispersal. These literature values may be unrealistic for FCs. For example, 1.2 m2 yr−1 is likely to be too high for clonal growth in the arid circumstances in which FCs occur. Stipagrostis individual plants across the landscape are typically only 0.005–0.13 m2 in canopy area with a mean area of 0.05 m2 (ref. 20). Similarly, clonal spread in other systems can also be lower than 1.2 m2 yr−1 by orders of magnitude (ref. 19). Alternatively, if Stipagrostis plants are not clones, their highly awned seeds will disperse much further than 1.2 m2 yr−1. Finally, if the assumed 1.2 m2 yr−1 biomass spread18 is due to the total growth of new recruits per parent individual, then this implies unrealistically high population growth rates ( >20 new recruits, each with 0.05 m2 in canopy volume20 required per parent individual). Getzin et al.3 acknowledge that in the context of their VSO model it needs to be further investigated whether grass tufts experience a central dieback due to self‐thinning, i.e. the role of clonality33. Thus, clonality may be relevant to some VSO models.
Juergens has argued that there is a spatial mismatch in the root length and inter-FC distances10 and therefore that FCs cannot directly interact with each other to produce the regular spatial pattern. An extreme example of this mismatch is a study by Ravi et al. reporting that the roots of peripheral plants in FCs had a mean length of 5.9 cm, which is more than two orders of magnitude shorter than inter-circle distances (10–20 m)12. These short root lengths would make competition for water and other resources over long distances crucial for explaining FC patterning1. Most recently, Ravi et al.12 rejected the termite hypothesis due to an absence of termites and partially invoked clonal dynamics as well as the VSO to explain their FC patterning12.
In summary, there are critical issues with all the hypotheses explaining the formation of FCs and the role of clonality appears to be relevant to two of the hypotheses. Here, we use ddRAD-seq as a genetic test of clonality of peripheral grasses. Our analysis indicates that most individual grasses surrounding FCs are genetically distinct and does not support the clonality hypothesis. More

The spatiotemporal characteristics analysis
The temporal characteristics
As seen in Fig. 2a, the climate tendency rate of the annual mean temperature series is 0.337 °C per decade, and its correlation coefficient is 0.7674 ( > r0.01 = 0.3357). In conjunction with the result of the M–K trend test, this finding demonstrates that the annual mean temperature has significantly increased in the past 56 years. In addition, the climate tendency rates of the annual mean temperature in the LARHR, YERHR and YARHR are 0.352 °C per decade, 0.34 °C per decade and 0.319 °C per decade, respectively (except for the climate tendency rate of the annual temperature in the YARHR, the correlation coefficients of the annual temperature series exceeded the significance level of 0.01). These rates exceed the mean rising rate of annual mean temperature in China (0.21–0.25 °C per decade) and that of the global annual mean temperature (0.07℃ per decade) in the past 56 years. The climate tendency rates of the annual mean temperature in the LARHR and YERHR were higher than those in Northwest China (0.32 °C/10a)1,27, and the climate tendency rate of the annual mean temperature in the YARHR was similar to that in Northwest China. The higher annual climate tendency rate of the THRHR is related to the increase in the lowest night temperature in the study area28 and the large amount of solar radiation in the lower altitude area of the THRHR13; furthermore, it may also be related to the decrease in total cloud cover and the increase in snow cover in the study area29. In addition, as seen in Fig. 2a,b, the annual mean temperature of the THRHR has increased significantly since the late1990s.
Figure 2

The change in annual mean temperature in the THRHR from 1960 to 2015.

Full size image

As seen in Fig. 3, the annual and seasonal mean temperatures in the THRHR and its three subregions have been increasing in fluctuations since the 1960s, and the fluctuations in winter and spring are greater than those of summer and autumn. Due to the higher climate tendency rate of the summer, autumn and winter in LARHR than in the other two subregions, the orders of the climate tendency rate of seasonal mean temperature in the THRHR are completely consistent with that of LARHR (autumn, summer, winter, and spring mean temperatures), which are different from that in Northwest China (winter, autumn, spring and summer mean temperatures). In the three subregions, the spring climate tendency rate is lowest, and the orders of the climate tendency rate of autumn and winter are higher than that of spring, while that of summer varies greatly, it is highest in the YARHR, and that of autumn in the LARHR and the YERHR are highest. The high temperature rise rate in autumn and winter in the THRHR is related to the increase in the lowest temperature at night, the climate high tendency rate of winter in three subregions corresponds with the positive phase of the Arctic Oscillation (AO), and namely, the high climate tendency rate of winter corresponds with the high value of the AO. In addition, the annual and seasonal mean temperatures in the LARHR are ≥ 0 °C, respectively; meanwhile, the increasing range of the seasonal mean temperature climate tendency rate is significantly higher than that in the YERHR and YARHR, respectively. The decadal mean temperatures, the decadal minimum and maximum temperatures and their extreme values in the YERHR are lower than those in the LARHR, while they are higher than those in the YARHR (the value of decadal mean temperature is  More

1.
Laidre, K. L., Heide-Jørgensen, M. P., Nielsen, T. G. & Gissel Nielsen, T. Role of the bowhead whale as a predator in West Greenland. Mar. Ecol. Prog. Ser. 346, 285–297 (2007).
ADS  Article  Google Scholar 
2.
Pomerleau, C., Ferguson, S. H. & Walkusz, W. Stomach contents of bowhead whales (Balaena mysticetus) from four locations in the Canadian Arctic. Polar Biol. 34, 615–620 (2011).
Article  Google Scholar 

3.
Pomerleau, C. et al. Prey assemblage isotopic variability as a tool for assessing diet and the spatial distribution of bowhead whale Balaena mysticetus foraging in the Canadian eastern Arctic. Mar. Ecol. Prog. Ser. 469, 161–174 (2012).
ADS  Article  Google Scholar 

4.
Kenney, R. D., Hyman, M. A. M., Owen, R. E., Scott, G. P. & Winn, H. E. Estimation of prey densities required by western North Atlantic right whales. Mar. Mamm. Sci. 2, 1–13 (1986).
Article  Google Scholar 

5.
Baumgartner, M. F. & Tarrant, A. M. The physiology and ecology of diapause in marine copepods. Ann. Rev. Mar. Sci. 9, 387–411 (2017).
PubMed  Article  Google Scholar 

6.
Fortune, S. M., Trites, A. W., Mayo, C. A., Rosen, D. A. S. & Hamilton, P. K. Energetic requirements of North Atlantic right whales and the implications for species recovery. Mar. Ecol. Prog. Ser. 478, 253–272 (2013).
ADS  Article  Google Scholar 

7.
Hays, G. C., Richardson, A. J. & Robinson, C. Climate change and marine plankton. Trends Ecol. Evol. 20, 337–344 (2005).
PubMed  Article  PubMed Central  Google Scholar 

8.
Beaugrand, G., Mackas, D. & Goberville, E. Applying the concept of the ecological niche and a macroecological approach to understand how climate influences zooplankton: advantages, assumptions, limitations and requirements. Prog. Oceanogr. 111, 75–90 (2013).
ADS  Article  Google Scholar 

9.
Beaugrand, G., Reid, P. C., Ibañez, F., Lindley, J. A. & Edwards, M. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296, 1692–1694 (2002).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

10.
Beaugrand, G. Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas. Deep Res. Part II Top. Stud. Oceanogr. 56, 656–673 (2009).
ADS  Article  Google Scholar 

11.
Chust, G. et al. Are Calanus spp. shifting poleward in the North Atlantic? A habitat modelling approach. ICES J. Mar. Sci. 71, 241–253 (2014).
Article  Google Scholar 

12.
Grieve, B. D., Hare, J. A. & Saba, V. S. Projecting the effects of climate change on Calanus finmarchicus distribution within the U.S. Northeast Continental Shelf. Sci. Rep. 7, 6264 (2017).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

13.
Feng, Z., Ji, R., Campbell, R. G., Ashjian, C. J. & Zhang, J. Early ice retreat and ocean warming may induce copepod biogeographic boundary shifts in the Arctic Ocean. J. Geophys. Res. Ocean. 121, 6137–6158 (2016).
ADS  Article  Google Scholar 

14.
Feng, Z., Ji, R., Ashjian, C., Campbell, R. & Zhang, J. Biogeographic responses of the copepod Calanus glacialis to a changing Arctic marine environment. Glob. Chang. Biol. 24, e159–e170 (2018).
ADS  PubMed  Article  PubMed Central  Google Scholar 

15.
Kwok, R. et al. Thinning and volume loss of the Arctic Ocean sea ice cover: 2003–2008. J. Geophys. Res. Ocean. 114, 1–16 (2009).
Article  Google Scholar 

16.
Stroeve, J., Holland, M. M., Meier, W., Scambos, T. & Serreze, M. Arctic sea ice decline: Faster than forecast. Geophys. Res. Lett. 34, 1–5 (2007).
Article  Google Scholar 

17.
Notz, D. & Stroeve, J. Observed Arctic sea-ice loss directly follows anthropogenic CO2 emission. Science 354, 747–750 (2016).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

18.
Pomerleau, C. et al. Spatial patterns in zooplankton communities across the eastern Canadian sub-Arctic and Arctic waters: insights from stable carbon (delta C-13) and nitrogen (delta N-15) isotope ratios. J. Plankton Res. 33, 1779–1792 (2011).
CAS  Article  Google Scholar 

19.
Pomerleau, C., Lesage, V., Winkler, G., Rosenberg, B. & Ferguson, S. H. Contemporary diet of bowhead whales (Balaena mysticetus) from the eastern Canadian Arctic inferred from fatty acid biomarkers. Arctic 67, 84–92 (2014).
Article  Google Scholar 

20.
Heide-Jørgensen, M. P. et al. Large scale sexual segregation of bowhead whales. Endang. Species Res. 13, 73–78 (2010).
Article  Google Scholar 

21.
Heide-Jørgensen, M. P. et al. Winter and spring diving behavior of bowhead whales relative to prey. Anim. Biotelemetry 1, 1–15 (2013).
Article  Google Scholar 

22.
Curry, B., Lee, C. M., Petrie, B., Moritz, R. E. & Kwok, R. Multiyear volume, liquid freshwater, and sea ice transports through Davis Strait, 2004–10. J. Phys. Oceanogr. 44, 1244–1266 (2014).
ADS  Article  Google Scholar 

23.
Pomerleau, C. et al. Mercury and stable isotope cycles in baleen plates are consistent with year-round feeding in two bowhead whale (Balaena mysticetus) populations. Polar Biol. 41, 1881–1893 (2018).
Article  Google Scholar 

24.
Doniol-Valcroze, T. et al. Abundance estimate of the Eastern Canada-West Greenland bowhead whale population based on the 2013 High Arctic Cetacean Survey. (2015).

25.
Frasier, T. et al. Abundance estimates of the Eastern Canada-West Greenland bowhead whale (Balaena mysticetus) population based on genetic capture-mark-recapture analyses. (2015).

26.
Frasier, T. R. et al. Abundance estimation from genetic mark-recapture data when not all sites are sampled: an example with the bowhead whale. Glob. Ecol. Conserv. 22, e00903 (2020).
Article  Google Scholar 

27.
Dunbar, M. J. Physical oceanographic results of the ‘Calanus’ expeditions in Ungava Bay, Frobisher Bay, Cumberland Sound, Hudson Strait and Northern Hudson Bay, 1949–1955. J. Fish. Res. Board Canada 15, 155–201 (1958).
Article  Google Scholar 

28.
Aitken, A. & Gilbert, R. Holocene nearshore environments and sea-level history in Pangnirtung fjord, Baffin Island, NWT, Canada. Arct. Alp. Res. 21, 34–44 (1989).
Article  Google Scholar 

29.
McMeans, B. C. et al. Seasonal patterns in fatty acids of Calanus hyperboreus (Copepoda, Calanoida) from Cumberland Sound, Baffin Island, Nunavut. Mar. Biol. 159, 1095–1105 (2012).
CAS  Article  Google Scholar 

30.
Bedard, J. M. et al. Outside influences on the water column of Cumberland Sound, Baffin Island. J. Geophys. Res. C Ocean. 120, 5000–5018 (2015).
ADS  Article  Google Scholar 

31.
Tang, C. C. L. et al. The circulation, water masses and sea-ice of Baffin Bay. Prog. Oceanogr. 63, 183–228 (2004).
ADS  Article  Google Scholar 

32.
Falk-Petersen, S., Mayzaud, P., Kattner, G. & Sargent, J. R. Lipids and life strategy of Arctic Calanus. Mar. Biol. Res. 5, 18–39 (2009).
Article  Google Scholar 

33.
Davies, K. T. A., Ryan, A. & Taggart, C. T. Measured and inferred gross energy content in diapausing Calanus spp. in a Scotian shelf basin. J. Plankton Res. 34, 614–625 (2012).
Article  Google Scholar 

34.
Koski, W. R., Davis, R. A., Miller, G. W. & Withrow, D. E. Reproduction. in The bowhead whale (eds. Burns, J. J., Montague, J. J. & Cowles, C. J.) 239–274 (Special Publication Number 2. The Society of Marine Mammalogy, Lawrence, KS, 1993).

35.
George, J. C. et al. Inferences from bowhead whale ovarian and pregnancy data: age estimates, length at sexual maturity and ovulation rates. International Whaling Commission Scientific Paper 56 (2004).

36.
Higdon, J. W. & Ferguson, S. H. Past, present, and future for bowhead whales (Balaena mysticetus) in northwest Hudson Bay. In A Little Less Arctic: Top Predators in the World’s Largest Northern Inland Sea, Hudson Bay (eds Ferguson, S. H. et al.) 159–177 (Springer, New York, 2010).
Google Scholar 

37.
Liu, H. & Hopcroft, R. R. Growth and development of Pseudocalanus spp. in the northern Gulf of Alaska. J. Plankton Res. 30, 923–935 (2008).
Article  Google Scholar 

38.
DeLorenzo Costa, A., Durbin, E. G. & Mayo, C. A. Variability in the nutritional value of the major copepods in Cape Cod Bay (Massachusetts, USA) with implications for right whales. Mar. Ecol. 27, 109–123 (2006).
ADS  Article  CAS  Google Scholar 

39.
Madsen, S. D., Nielsen, T. G. & Hansen, B. W. Annual population development and production by Calanus finmarchicus, C. glacialisand C. hyperboreus in Disko Bay, western Greenland. Mar. Biol. 139, 75–93 (2001).
Article  Google Scholar 

40.
Reeves, R., Mitchell, E., Mansfield, A. & McLaughlin, M. Distribution and migration of the bowhead whale, Balaena mysticetus, in the Eastern North American. Arctic 36, 60 (1983).
Article  Google Scholar 

41.
Holland, C. A. William penny, 1809–92: Arctic whaling master. Polar Rec. 15, 25–43 (1970).
Article  Google Scholar 

42.
Higdon, J. W. Commercial and subsistence harvests of bowhead whales (Balaena mysticetus) in eastern Canada and West Greenland. J. Cetacean Res. Manag. 11, 185–216 (2010).
Google Scholar 

43.
Diemer, K. M. et al. Marine mammal and seabird summer distribution and abundance in the fjords of northeast Cumberland Sound of Baffin Island, Nunavut, Canada. Polar Biol. 34, 41–48 (2011).
Article  Google Scholar 

44.
Matthews, C. et al. Boat-based surveys for marine mammals and seabirds in Cumberland Sound. Field report. (2012).

45.
Baumgartner, M. F., Wenzel, F. W., Lysiak, N. S. J. & Patrician, M. R. North Atlantic right whale foraging ecology and its role in human-caused mortality. Mar. Ecol. Prog. Ser. 581, 165–181 (2017).
ADS  Article  Google Scholar 

46.
Fortune, S. et al. Seasonal diving and foraging behaviour of Eastern Canada-West Greenland bowhead whales. Mar. Ecol. Prog. Ser. 643, 197–217 (2020).
ADS  Article  Google Scholar 

47.
Block, B. A. Physiological ecology in the 21st century: Advancements in biologging science. Integr. Comp. Biol. 45, 305–320 (2005).
PubMed  Article  PubMed Central  Google Scholar 

48.
Hays, G. C. New insights: animal-borne cameras and accelerometers reveal the secret lives of cryptic species. J. Anim. Ecol. 84, 587–589 (2015).
PubMed  Article  PubMed Central  Google Scholar 

49.
Bograd, S. J., Block, B. A., Costa, D. P. & Godley, B. J. Biologging technologies: new tools for conservation. Introduction. Endanger. Species Res. 10, 1–7 (2010).
Article  Google Scholar 

50.
Unstad, K. H. & Tande, K. S. Depth distribution of Calanus finmarchicus and C. glacialis in relation to environmental conditions in the Barents Sea. Polar Res. 10, 409–420 (1991).
Article  Google Scholar 

51.
Hirche, H. J. & Niehoff, B. Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea-field and laboratory observations. Polar Biol. 16, 209–219 (1996).
Article  Google Scholar 

52.
Madsen, S. J., Nielsen, T. G., Tervo, O. M. & Söderkvist, J. Importance of feeding for egg production in Calanus finmarchicus and C. glacialis during the Arctic spring. Mar. Ecol. Prog. Ser. 353, 177–190 (2008).
ADS  CAS  Article  Google Scholar 

53.
Darnis, G. & Fortier, L. Temperature, food and the seasonal vertical migration of key arctic copepods in the thermally stratified Amundsen Gulf (Beaufort Sea, Arctic Ocean) GE. J. Plankton Res. 36, 1092–1108 (2014).
CAS  Article  Google Scholar 

54.
Parent, G. J., Plourde, S. & Turgeon, J. Overlapping size ranges of Calanus spp. off the Canadian Arctic and Atlantic Coasts: impact on species abundances. J. Plankton Res. 33, 1654–1665 (2011).
CAS  Article  Google Scholar 

55.
Hyslop, E. J. Stomach contents analysis—a review of methods and their application. J. Fish Biol. 17, 411–429 (1980).
Article  Google Scholar 

56.
Dunweber, M. et al. Succession and fate of the spring diatom bloom in Disko Bay, western Greenland. Mar. Ecol. Prog. Ser. 419, 11–29 (2010).
ADS  Article  CAS  Google Scholar 

57.
Swalethorp, R. et al. Grazing, egg production, and biochemical evidence of differences in the life strategies of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, Western Greenland. Mar. Ecol. Prog. Ser. 429, 125–144 (2011).
ADS  Article  Google Scholar 

58.
Baumgartner, M. F. & Mate, B. R. Summertime foraging ecology of North Atlantic right whales. Mar. Ecol. Prog. Ser. 264, 123–135 (2003).
ADS  Article  Google Scholar 

59.
Hirche, H. J. Long-term experiments on lifespan, reproductive activity and timing of reproduction in the Arctic copepod Calanus hyperboreus. Mar. Biol. 160, 2469–2481 (2013).
Article  Google Scholar 

60.
Visser, A. W. & Jónasdóttir, S. H. Lipids, buoyancy and the seasonal vertical migration of Calanus finmarchicus. Fish. Oceanogr. 8, 100–106 (1999).
Article  Google Scholar 

61.
Scott, C. L., Kwasniewski, S., Falk-Petersen, S. & Sargent, J. R. Lipids and life strategies of Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus in late autumn, Kongsfjorden, Svalbrad. Polar Biol. 23, 510–516 (2000).
Article  Google Scholar 

62.
Heide-Jørgensen, M. P., Laidre, K. L., Logsdon, M. L. & Nielsen, T. G. Springtime coupling between chlorophyll a, sea ice and sea surface temperature in Disko Bay, West Greenland. Prog. Oceanogr. 73, 79–95 (2007).
ADS  Article  Google Scholar 

63.
Baumgartner, M. F. Comparisons of Calanus finmarchicus fifth copepodite abundance estimates from nets and an optical plankton counter. J. Plankton Res. 25, 855–868 (2003).
Article  Google Scholar 

64.
Herman, A. W. Design and calibration of a new optical plankton counter capable of sizing small zooplankton. Deep Sea Res. A 39, 395–415 (1992).
ADS  Article  Google Scholar 

65.
Falk-Petersen, S. et al. Vertical migration in high Arctic waters during autumn 2004. Deep Sea Res. II(55), 2275–2284 (2008).
ADS  Article  Google Scholar 

66.
Baumgartner, M. F., Lysiak, N. S. J., Schuman, C., Urban-Rich, J. & Wenzel, F. W. Diel vertical migration behavior of Calanus finmarchicus and its influence on right and sei whale occurrence. Mar. Ecol. Prog. Ser. 423, 167–184 (2011).
ADS  Article  Google Scholar 

67.
Bollens, S. M. & Frost, B. W. Predator-induced diet vertical migration in a planktonic copepod. J. Plankton Res. 11, 1047–1065 (1989).
Article  Google Scholar 

68.
Hays, G. C. Ontogenetic and seasonal variation in the diel vertical migration of the copepods Metridia lucens and Metridia longa. Limnol. Oceanogr. 40, 1461–1465 (1995).
ADS  Article  Google Scholar 

69.
Huntley, M. & Brooks, E. R. Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar. Biol. 71, 23–31 (1982).
Article  Google Scholar 

70.
Simon, M., Johnson, M. J., Tyack, P. & Madsen, P. T. Behavior and kinematics of continous ram filtration in bowhead wahles (Balaena mysticetus). Proc. R. Soc. Lond. B. 276, 3819–3828 (2009).
Article  Google Scholar 

71.
van der Hoop, J. M. et al. Foraging rates of ram-filtering North Atlantic right whales. Funct. Ecol. 33, 1290–1306 (2019).
Article  Google Scholar 

72.
Goldbogen, J. A. et al. Prey density and distribution drive the three-dimensional foraging strategies of the largest filter feeder. Funct. Ecol. 29, 951–961 (2015).
Article  Google Scholar 

73.
Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. & Sinnett, E. E. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemsitry and behavior. J. Comp. Physiol. B 138, 335–346 (1980).
CAS  Article  Google Scholar 

74.
Kooyman, G. L., Castellini, M. A., Davis, R. W. & Maue, R. A. Aerobic diving limits of immature Weddell seals. J. Comp. Physiol. B 151, 171–174 (1983).
Article  Google Scholar 

75.
Dyke, A. S., Hooper, J. & Savelle, J. M. A history of sea ice in the Canadian Arctic archipelago based on postglacial remains of the bowhead whale (Balaena mysticetus). Arctic 49, 235–255 (1996).
Article  Google Scholar 

76.
Baumgartner, M. F., Hammar, T. & Robbins, J. Development and assessment of a new dermal attachment for short-term tagging studies of baleen whales. Methods Ecol. Evol. 6, 289–297 (2015).
Article  Google Scholar 

77.
Reinhart, N. R. et al. Occurrence of killer whale Orcinus orca rake marks on Eastern Canada-West Greenland bowhead whales Balaena mysticetus. Polar Biol. 36, 1133–1146 (2013).
Article  Google Scholar 

78.
Fortune, S. M. E. et al. Evidence of molting and the function of “rock-nosing” behavior in bowhead whales in the eastern Canadian Arctic. PLoS ONE 12, 1–15 (2017).
MathSciNet  Article  CAS  Google Scholar 

79.
Silva, M. A. et al. Assessing performance of Bayesian state-space models fit to argos satellite telemetry locations processed with kalman filtering. PLoS ONE 9, e92277 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

80.
Lowther, A. D., Lydersen, C., Fedak, M. A., Lovell, P. & Kovacs, K. M. The argos-CLS kalman filter: Error structures and state-space modelling relative to fastloc GPS data. PLoS ONE 10, e0124754 (2015).
PubMed  PubMed Central  Article  CAS  Google Scholar 

81.
R Development Core Team. R: A Language and Environment for Statistical Computing. R Development Core Team, Vienna (2016). https://doi.org/10.1038/sj.hdy.6800737.

82.
Jonsen, I. D., Flemming, J. M. & Myers, R. A. Robust state-space modeling of animal movement data. Ecology 86, 2874–2880 (2005).
Article  Google Scholar 

83.
Jonsen, I. D. et al. State-space models for bio-loggers: a methodological road map. Deep. Res. II(88–89), 34–46 (2013).
ADS  Google Scholar 

84.
Tinbergen, N., Impekoven, M. & Franck, D. An experiment on spacing-out as a defence against predation. Behaviour 28, 307–320 (1967).
Article  Google Scholar 

85.
Kareiva, P. & Odell, G. Swarms of predators exhibit ‘preytaxis’ if individual predators use area-restricted search. Am. Nat. 130, 233–270 (1987).
Article  Google Scholar 

86.
Haskell, D. G. Experiments and a model examining learning in the area-restricted search behavior of ferrets (Mustela putorius furo). Behav. Ecol. 8, 448–455 (1997).
Article  Google Scholar 

87.
Fauchald, P. & Tveraa, T. Using first-passage time in the analysis of area-restricted search and habitat selection. Ecology 84, 282–288 (2003).
Article  Google Scholar 

88.
Anderwald, P. et al. Spatial scale and environmental determinants in minke whale habitat use and foraging. Mar. Ecol. Prog. Ser. 450, 259–274 (2012).
ADS  Article  Google Scholar 

89.
Jonsen, I. D., Myers, R. A. & James, M. C. Identifying leatherback turtle foraging behaviour from satellite telemetry using a switching state-space model. Mar. Ecol. Prog. Ser. 337, 255–264 (2007).
ADS  Article  Google Scholar 

90.
Pinheiro, J. C. & Bates, D. M. Linear mixed-effects models. in Mixed-effects models in S and S-Plus 1–56 (Springer, New York, 2000). https://doi.org/10.1198/tech.2001.s574.

91.
Sverdrup, H. U. On conditions for the vernal blooming of phytoplankton. ICES J. Mar. Sci. 18, 287–295 (1953).
Article  Google Scholar 

92.
Thomson, R. E. & Fine, I. V. Estimating mixed layer depth from oceanic profile data. J. Atmos. Ocean. Technol. 20, 319–329 (2003).
ADS  Article  Google Scholar 

93.
Smith, W. O. & Jones, R. M. Vertical mixing, critical depths, and phytoplankton growth in the Ross Sea. ICES J. Mar. Sci. 72, 1952–1960 (2015).
Article  Google Scholar 

94.
Suthers, I. M., Taggart, C. T., Rissik, D. & Baird, M. E. Day and night ichthyoplankton assemblages and zooplankton biomass size spectrum in a deep ocean island wake. Mar. Ecol. Prog. Ser. 322, 225–238 (2006).
ADS  CAS  Article  Google Scholar 

95.
Grainger, E. H. The copepods Calanus glacial is Jaschnov and Calanus finmarchicus (Gunnerus) in Canadian Arctic-Subarctic waters. J. Fish. Res. Board Can. 18, 663–678 (1961).
Article  Google Scholar 

96.
Jaschnov, W. A. Distribution of Calanus Species in the Seas of the Northern Hemisphere. Int. Rev. Hydrobiol. Hydrogr. 55, 197–212 (1970).
Article  Google Scholar 

97.
Hirche, H. J. & Mumm, N. Distribution of dominant copepods in the Nansen Basin, Arctic Ocean, in summer. Deep Sea Res. A 39, 485–505 (1992).
ADS  Article  Google Scholar 

98.
Breteler, W. C. M. K., Fransz, H. G. & Gonzalez, S. R. Growth and development of four calanoid copepod species under experimental and natural conditions. Neth. J. Sea Res. 16, 195–207 (1982).
Article  Google Scholar  More