Polar Biology

, Volume 38, Issue 1, pp 51–65 | Cite as

Quantifying the light sensitivity of Calanus spp. during the polar night: potential for orchestrated migrations conducted by ambient light from the sun, moon, or aurora borealis?

  • Anna S. Båtnes
  • Cecilie Miljeteig
  • Jørgen Berge
  • Michael Greenacre
  • Geir Johnsen
Original Paper

Abstract

Recent studies have shown that the biological activity during the Arctic polar night is higher than previously thought. Zooplankton perform diel vertical migration during the dark period/winter, with the calanoid copepods Calanus spp. being one of the main taxa assumed to contribute to the observed diel vertical migration. We investigated the sensitivity of field-collected Calanus spp. to irradiance by keeping individuals in an aquarium and exposing them to gradually increasing irradiance in white, blue, green, and red wavebands, recording their phototactic response with a near-infrared-sensitive video camera. Experiments were performed with the two oldest copepodite stages as well as adult males and females. The copepods were negatively phototactic, and the lowest irradiance eliciting a significant phototactic response was of the order of 10−8–10−6 μmol photons m−2 s−1 for white, green, and blue wavebands, whereas the comparative irradiance for red wavebands was up to three orders of magnitudes higher. The different copepod developmental stages displayed different sensitivities to irradiance. During the darkest part of the polar night, the lowest irradiance for significant response corresponded to 0.0005–0.5 % of the ambient surface irradiance, depending on light source. Accordingly, Calanus spp. may respond to irradiance from the night sky down to 70–80 m, moonlight to 120–170 m, and aurora borealis down to 80–120 m depth. The high sensitivity to blue and green light may explain the Calanus’ ability to perform diel vertical migration during the polar night when intensity and diurnal variation of ambient irradiance is low.

Keywords

Phototaxis Light response Spectral sensitivity Copepods Arctic 

Introduction

Diel vertical migration (DVM) of zooplankton is found in all the world’s oceans and is considered the largest synchronised movement of biomass on the planet (Hays 2003). It is thus an important factor in structuring the pelagic community. The most common type is nocturnal DVM, where the plankton ascend to surface waters at sunset to feed in the darkness, hiding from visual predators, and descend to deeper waters at sunrise. The ultimate cause for DVM is considered to be the optimisation of feeding at the same time as minimising the risk of being predated (the predator evasion hypothesis; e.g. Lampert 1989; Hays 2003). The primary proximate cause of DVM is considered to be the use of light as an exogenous cue (e.g. reviewed in Cohen and Forward 2009). There are three main hypotheses to explain this. The isolume hypothesis states that the zooplankton will follow a preferred light level during migration. The rate of change hypothesis describes the relative rate and direction of change in light from the ambient level as the cue for migration, while the absolute intensity threshold hypothesis states that migration is initiated when light increases above or decreases below a certain threshold intensity (Lampert 1989; Ringelberg 1995, 1999; Hays 2003; Ringelberg and Van Gool 2003; Cohen and Forward 2009). The spectral sensitivity of the zooplankton is also of importance, as it influences the light available to the individuals. The peak spectral sensitivity tends to be clustered in the blue–green wavebands (460–530 nm), matching the ambient light at the time of migration, which commonly is twilight (Forward 1988; Cohen and Forward 2009). In this paper, we define light as irradiance at 400–700 nm, henceforth abbreviated as E.

Copepods are major contributors to DVM and may perform diel migrations down to 200–300 m (e.g. Tande 1988; Dale and Kaartvedt 2000; Fortier et al. 2001; Baumgartner et al. 2003; Yamagutchi et al. 2004; Cottier et al. 2006). Assuming that E is the proximate factor triggering the migratory behaviour, copepods must have high sensitivity to light to be able to detect and respond to E at great depths. A few studies have investigated the phototactic response of copepods related to the rate of change and absolute intensity threshold as well as spectral sensitivity. Cohen and Forward (2005) studied responses of Calanopia americana to absolute E changes as well as relative rates of change and found that both factors affected DVM. Stearns and Forward (1984) investigated both E thresholds for phototactic response as well as the spectral sensitivity of Acartia tonsa and found that the peak spectral sensitivity was broad and matched the E available for the copepods during daytime. Cohen and Forward (2002) found that the spectral sensitivities of copepod species varied between species and were closely connected to different patterns of DVM, the peak spectral sensitivity of species performing DVM in coastal waters matching the E during twilight, and that of a non-migrating species being broader and corresponding to a shallower habitat. The spectral sensitivity of Calanus finmarchicus as well as Metridia longa has been investigated by simulating bioluminescent flashes of different wavelengths, and the strongest responses were found in blue–green wavebands (Buskey and Swift 1985). Miljeteig et al. (submitted) established the absolute E threshold for phototactic response of C. finmarchicus from a laboratory culture and concluded that it matched the E available in the depth range reported for natural C. finmarchicus populations.

In the Arctic, DVM has mostly been studied during the time of year when there is a distinct photoperiod (daylight), and a clear DVM signal has been described (Fortier et al. 2001; Cottier et al. 2006; Falk-Petersen et al. 2008; Wallace et al. 2010; Rabindranath et al. 2011). Over the last few years, researchers have also taken interest in the dark winter period, the polar night, and recent studies have described biological activity far higher than previously thought during this time of year (Sato et al. 2002; Berge et al. 2009, 2012; Fort et al. 2010). It has been shown that zooplankton perform DVM during the polar night despite the low-light conditions (Berge et al. 2009, 2012). The E in the polar night originates from different sources and has varying periodicity. The night sky and scattered E from the sun has a 24-h cycle, and the latter varies with the time of year, the daytime E increasing/decreasing with the solar elevation angle (e.g. Simmons et al. 1996). The moonlight has an approximate 25-h daily cycle as well as the 29-day lunar cycle. The aurora borealis also has a 24-h cycle due to the Earth’s rotation under the aurora oval, and in Svalbard, the green aurora (emission line 557.7 nm) outbreaks are most frequent between 19:00 and 00:00 (e.g. Myrabø 1985; Simmons et al. 1996). In the Arctic, the frequency of active aurora borealis varies depending on location and the solar activity. Furthermore, all E varies according to cloud cover. Thus, although variable, there is a periodicity in all polar night E, which in theory could influence high-latitude ecosystems.

The calanoid copepod genus Calanus is one of the major taxa performing DVM in the Arctic (e.g. Dale and Kaartvedt 2000; Fortier et al. 2001; Cottier et al. 2006; Rabindranath et al. 2011). The genus constitutes a major part of the zooplankton biomass in the Arctic shelf seas (e.g. Hassel 1986; Mumm et al. 1998; Blachowiak-Samolyk et al. 2008) and is a highly important food source for amphipods and other zooplankton, as well as fishes, seabirds, and whales (e.g. Falk-Petersen et al. 1990; Auel and Werner 2003; Baumgartner and Mate 2003; Karnovsky et al. 2003). Calanus spp. are considered to be primarily herbivores, but may also switch to heterotrophic prey (Søreide et al. 2008; Falk-Petersen et al. 2009; Vadstein 2009). In the Arctic, the most dominant Calanus species are C. glacialis, which is an Arctic shelf species, C. finmarchicus, which is dominant in areas influenced by water masses with Atlantic origin, and C. hyperboreus, which is associated with the deeper parts of the polar ocean (e.g. Conover 1988; Falk-Petersen et al. 2009). As C. hyperboreus mainly is a polar basin species, overwintering at large depths (500–2000 m; Falk-Petersen et al. 2009), C. glacialis and C. finmarchicus are the dominant species in West Spitsbergen fjords during winter (Arnkværn et al. 2005; Berge et al. 2012). The main overwintering stages of C. glacialis and C. finmarchicus are copepodite stages IV and V (CIV and CV) as well as adults (e.g. Tande 1982; Hirche 1991; Falk-Petersen et al. 2009).

Due to the ecological importance of Calanus spp., as well as the reported DVM during polar night (Berge et al. 2009, 2012), the genus was used in this study. The E in the polar night has low intensity, but still a certain periodicity, and given a sufficient sensitivity to E, zooplankton could be influenced by it. To our knowledge, the only study investigating the E threshold for response of Calanus spp. was performed with laboratory cultured C. finmarchicus, using a white light stimulus (Miljeteig et al. submitted). We aimed to investigate the absolute E needed to elicit a phototactic response in an Arctic population of Calanus spp. by sampling in the field during the polar night, and using a laboratory experimental setup designed to test phototactic response in low-light conditions. We performed experiments with the developmental stages of Calanus spp. present in the polar night (CIV, CV, and adults), investigating the sensitivity to different wavebands of visible light. We also compared the Calanus spp. response and sensitivity to E during daytime and nighttime, and finally, we related our findings to the ambient E in the polar night.

Materials and methods

Zooplankton collection

Calanus spp. were collected using a WP3 net (mesh size 500 μm, diameter 1 m) in Adventfjorden, close to Longyearbyen, Svalbard (78.228 N, 15.604 E), through a hole in the ice. Samples were collected in 7–8, 11, and 17 January 2011. Several net hauls were taken during the four sampling days to collect the sufficient amount of zooplankton. The samples were stored in 10–20-L buckets and transported to a seawater laboratory at the University Centre in Svalbard, Longyearbyen. The Calanus spp. were immediately sorted by developmental stage; stages CIV and CV, and sex; adult females and males (AF and AM), and incubated according to stage in 3-L buckets with lids at 1–2 °C (20–25 individuals per bucket). Due to sampling in shallow waters, there was some sediment in the samples. During sorting, the Calanus spp. were inspected visually for sediment particles and only individuals appearing healthy were selected for experiments. To minimise light exposure, only dim room light (no microscope lights) was used during the sorting. Buckets were covered in three layers of black plastic bin liners and stored in the dark seawater laboratory for at least 24 h to ensure the zooplankton were acclimated to darkness before the experiments.

The experimental setup

The experimental setup was the same as described in Miljeteig et al. (submitted), with a few modifications (the aquarium and the near-infrared (N-IR) lamps; see details below), see Online Resource 1 for a photograph of the experimental setup. An acrylic glass aquarium with 18 cm width, 48 cm length, 8 cm height (internal dimensions), and 1 cm thick walls was used to keep the zooplankton (sampled in January 2011) during experiments. Inside the aquarium was a 48 × 8 cm wall, which was used to adjust the width to fit the light stimulus (13 cm), limiting the projection area available to the copepods to 48 × 13 cm. The water depth was 6 cm during all experiments. Experiments were performed in the horizontal plane to avoid possible effect of gravitation and buoyancy, thus investigating the active, directional phototactic response only. A light emitting diode (LED) was fitted to a filter wheel with integrated controller (Tofra, Inc., Palo Alto, California, USA). The filter wheel was attached to a 14 × 10 × 12 cm light tight box with a Fresnel lens (95 × 135 mm, optical PVC, 3Dlens.com, Taiwan) in front, making the light path collimated. To adjust the E, the filter wheel contained neutral optical density (OD) filters (CVI Melles Griot, The Netherlands) with increasing OD (absorbance, dimensionless). Optical density is logarithmic, decreasing the E to 10 % of the previous level for each increasing OD number. Filters with OD from 4 to 9 were used in the experiments, called OD4 to OD9, respectively. The LED and filter wheel assembled in the light tight box made up the light stimulus unit. WheelTool v1.0 software (Tofra Inc., Palo Alto, California, USA) controlled the position of the filter wheel. In addition, LabView 8.2.1 software was used to further adjust the E of the LEDs by pulsing the light. It was used to reduce the E at each OD level by 50 % (for simplicity named OD4.5, OD5.5 and so on), providing a higher resolution to the E levels the zooplankton were exposed to. Experiments were performed with white (LXHL-PW01), blue (LXHL-PR03; emission peak at 455 nm), green (LXHL-PM01; peak at 525 nm; called green525), and red (LXHL-PD01; peak at 640 nm) LEDs (Fig. 1). In addition, the white LED was used with a green transmission filter with peak at 550 nm (hereafter called aurora green550), to more closely simulate the green aurora borealis (emission line at 557.7 nm), which is a common light source in the polar night.
Fig. 1

Relative spectral irradiance (E) for the different wavebands used in experiments. Based on the measurements of OD5 for all wavebands, full width at half maximum was 23 nm for blue, 37 nm for green525, 27 nm for auroragreen550, and 20 nm for red. (Color figure online)

To record the responses of the zooplankton, the aquarium was placed on a table with a 48 × 18 cm hole and illuminated from below by four inclined N-IR lamps (IR30, SmartProdukter Norge AS, emission peak at 850 nm). The experiments were recorded from above using a N-IR-sensitive video camera (Sony Handycam HDR-XR550) in NightShot mode standing on a quadrapod (Quadrapod Elite Copy Stand, Forensic Imaging, Inc., USA). The N-IR lamps were covered with filters to remove the visible part of the spectrum (Kodak Wratten Infrared filters, #87C, Edmund Optics Ltd, York, UK; 0 % transmission up to ~790 nm). The experimental setup was covered in black fabric during experiments to avoid possible stray light from entering and to minimise the effect of air currents on the aquarium.

A spectroradiometer (ORIEL Fixed Imaging Compact Spectrograph; FICS SN 7743) was used to obtain the spectral E used in experiments. The detector of the instrument was placed in front of the aquarium, on the opposite side of the light stimulus unit, and the highest E levels for all LEDs (OD4 through OD6 for white, blue, green525, and red and OD3 through OD5.5 for the aurora green550) were measured. The lower E levels were outside the linear response area of the instrument and were instead calculated, extrapolating from the measured E levels. As the detector was not waterproof, the measurements were done outside of the aquarium, including both aquarium walls as well as the water. Thus, the E measured was lower than that experienced by the copepods. To correct for this, measurements were also done (white LED, OD5) with only one aquarium wall as well as through both walls of the aquarium without water, and the fraction of E absorbed by one aquarium wall was calculated. This factor was then used to correct the E for all wavebands and OD levels used. The spectroradiometer was calibrated with a Quartz Tungsten Halogen lamp (Oriel Instruments, Model no. 63358, 45 W, 6.5 A) to convert the data from the original output in counts s−1–μW m−2 nm−1. To convert to photons m−2 s−1 nm−1, the equation by Baker and Romick (1976) was used:
$$1\,{\text{photon}}/{\text{s}} = 1. 9 8 6 4 7 5( 1/\lambda ) \times 10^{ - 1 9}\,{\text{W}},$$
where λ is wavelength in μm. The output was further converted into μmol photons m−2 s−1 nm−1 and then integrated over 400–700 nm to obtain the E values for each waveband and OD level.

Light response experiments

All experiments were performed in a temperature-controlled seawater laboratory at the University Centre in Svalbard. Room and water temperatures were 1–2 °C. To make the laboratory completely dark and prevent stray light, all openings were covered with three layers of aluminium foil. The computer controlling the light stimulus was placed outside the laboratory, so that the experiments could be performed without entering the room. Freshly collected Calanus spp. (20 individuals for stages CIV and AM, 25 individuals for stages CV and AF; acclimated in dark for at least 24 h prior to experiments) were transferred from the storing buckets to the aquarium as quickly as possible, using only red light to minimise light exposure (Cohen and Forward 2005). A small touch by a pair of tweezers was used as a simple fitness test; only individuals performing immediate escape response were considered healthy and used in experiments. The Calanus spp. were acclimated in the aquarium for at least 1 h in darkness before experiments started. The location of the light stimulus was alternated from one side of the aquarium to the other between replicates to control for room effects, e.g. air currents produced by the cooling system.

24-hour experiments

Twenty-four-hour experiments (two replicates with different sets of Calanus spp. individuals) were performed to test whether the Calanus spp. responded differently during daytime than nighttime. The light stimulus was a white LED. A sample of 25 specimens of Calanus spp. CV was transferred to the aquarium at 11:00 and dark acclimated, and at 12:00 (noon), the camera was turned on to record the starting distribution (darkness). After 10 min, the LED was turned on, starting with OD8 (0.099 × 10−6 μmol photons m−2 s−1; Table 1). The E range used in the experiment was determined by preliminary experiments (not shown), to ensure a starting E well below the threshold for phototactic response. Every 10 min, the filter wheel was turned so that the OD decreased by 1, thus increasing the E. The highest E used for this experiment was OD4 (860 × 10−6 μmol photons m−2 s−1), giving a total of 6 E levels including the dark initial period. The light stimulus was then turned off, and the Calanus spp. were left in the aquarium. This procedure (trial) was repeated every 3 h for 24 h (at 12:00, 15:00, 18:00, 21:00, 00:00, 03:00, 06:00, 09:00) and then one last time at 12:00; making a total of 9 trials for each replicate.
Table 1

Irradiance (400–700 nm) for the different wavebands and optical density (OD) levels used in experiments

 

White

Blue

Green525

Aurora green550

Red

OD4

860

OD4.5

52

1,800

OD5

79

8.1

310

OD5.5

42

39

4.6

150

OD6

9.4

8.7

4.3

0.85

28

OD6.5

4.7

4.3

2.1

0.43

14

OD7

0.94

0.62

0.34

0.083

2.6

OD7.5

0.47

0.31

0.17

0.041

1.3

OD8

0.099

0.050

0.030

OD8.5

0.025

0.015

OD9

0.0040

0.0026

Values are in μmol photons m−2 s−1 × 10−6

Threshold value experiments (white, blue, green525, aurora green550, and red wavebands)

A sample of 20 (for stages CIV and AM) or 25 (for stages CV and AF) specimens of Calanus spp. was transferred to the aquarium and dark acclimated. The camera was turned on, and the first 10-min period of the experiment was recorded as distribution in darkness. The light stimulus was then turned on, the starting E level varying from OD7.5 to OD9 depending on the waveband (Table 2; Fig. 1). The E range used for each waveband was determined by preliminary experiments (not shown), to ensure a starting E well below the threshold for phototactic response. Every 10 min, the E was increased by decrementing the OD by 0.5. The Calanus spp. were left in the dark for at least 1 h to acclimate, the LED was then changed to a different waveband, and a corresponding experiment was performed. The order of the wavebands was randomized. Experiments with the aurora green light stimulus were run with stage CV only.
Table 2

Overview of threshold value experiments performed with different Calanus spp. developmental stages and sexes

 

CIV

2 replicates, 20 ind

OD range (duration)

CV

3 replicates, 25 ind

OD range (duration)

AF

2 replicates, 25 ind

OD range (duration)

AM

3 replicates, 20 ind

OD range (duration)

White

5.5–8 (70)

5–8 (80)

5.5–8 (70)

5–8 (80)

Blue

6–9 (80)

6–9 (80)

6–9 (80)

5.5–9 (90)

Green525

6–9 (80)

6–9 (80)

6–9 (80)

6–9 (80)

Aurora green550

 

4.5–7.5 (80)

  

Red

4.5–7.5 (80)

4.5–7.5 (80)

4.5–7.5 (80)

4.5–7.5 (80)

Number of replicates, number of individuals per replicate, the range of light intensities (range of optical densities OD), and duration of experiments (min) for each waveband. White, blue, green525, and red are LEDs, aurora green550 is the white LED with a green transmission filter, emission peak 550 nm

Image analysis

Using Picture Motion Browser video software (v 4.2, Sony Corporation), we extracted one still image per minute (including minute 0) from the video of the experiments, amounting to 11 min representing the initial dark period and ten images representing the subsequent E level. Images were analysed in stacks (one stack per replicate), using the image analysing software ImageJ (1.43u; Rasband 1997–2012). The images were cropped, and contrast was improved. Using the whole image stack, the median image was calculated and then subtracted from the stack, removing air bubbles, aquarium edges, and debris (all stationary objects). Colour threshold was adjusted (saturation and brightness) to create binary images for particle analysis. The particle analyses were performed by defining thresholds for minimum size and circularity and provided the particles’ distances from the light stimulus (in cm; the total length of the aquarium was 48 cm), as well as their size (area in square pixels). Due to some floating debris particles in the aquarium, the number of particles was larger than the number of copepods. We assumed that the copepods were the largest particles observed and used the R environment (R Development Core Team 2012) to extract the position of the 20 or 25 (depending on stage) copepods for further analyses.

Statistical analyses

Statistical modelling of the experimental data was performed using linear mixed-effects modelling, computed with the package lme4 in the R environment (Bates et al. 2011; R Development Core Team 2012).

24-hour experiments

The trials performed at 18:00, 21:00, 00:00, 03:00, and 06:00 from both replicates (10 trials altogether) were defined as nighttime, and the remaining (12:00, 15:00, 09:00, and 12:00 second time; 8 trials altogether) were defined as daytime. The phototactic response was tested with linear mixed-effects modelling, with trial as random factor to account for the repeated measurements nature of the design. For the initial dark period, the copepods’ median positions (distance from light stimulus) over the entire period (11 min) were used in the analysis. For the subsequent E levels, only the single last minute of each level was used, to capture the developed phototactic response. Firstly, for nighttime, the distribution of copepods at the end of each E level was compared to the distribution of copepods in the initial dark period. Then, the distribution of copepods during daytime trials as a whole was compared to that of nighttime to investigate whether the response was different during day compared to night. The conventional significance level of 0.05 was lowered to 0.01, to reduce the false discovery rate when conducting multiple tests.

Threshold value experiments (white, blue, green525, aurora green550, and red wavebands)

The phototactic response in each experiment (developmental stage and waveband; Table 2) was investigated using linear mixed-effects modelling, with replicate as random factor to account for the repeated measurements nature of the design. For the initial dark period, the copepods’ median positions (distance from light stimulus) over the entire period (11 min) were used in the analysis. For the subsequent E levels, only the single last minute of each level was used. The distribution of copepods at the end of each E level was compared to the distribution of copepods in the initial dark period. The overall significance of effects in the model was tested by the ANOVA F statistic, with the significance level set at 0.05. The significance level was again lowered to 0.01 for testing individual effects, due to the problem of multiple testing. For all the experiments, there is strong autocorrelation in the original minute-by-minute data, but this autocorrelation becomes much lower, and statistically insignificant, in our analysis of the last minute of each E level.

Irradiance from natural light sources in the polar night

There was no light metre or spectroradiometer available that was sensitive enough to measure ambient polar night E, hence values for background (night sky) E, moonlight, and aurora borealis at sea surface, as well as data on cloud cover, could only be derived from literature (Clarke 1971; Myrabø 1985; Simmons et al. 1996; Jensen et al. 2001; Müller et al. 2011). Neither was there an attenuation coefficient available for the water masses on West Spitsbergen during winter, but we assumed that the inherent optical properties of the water and its constituents (Johnsen et al. 2009) resembled those of Arctic water masses at a time of year when there are low concentrations of chlorophyll a (“winter concentration”), coloured dissolved organic matter, and total suspended matter (Case 1 waters; Jerlov 1968). Water masses with these characteristics were sampled in the Barents Sea during August by Hovland et al. (2012), and this spectral attenuation coefficient was used to model the E from the different light sources with increasing depth. Due to lack of good spectral data, the spectral distributions of surface moonlight, night sky E, and cloudy conditions were for simplicity assumed to be horizontally linear over 400–700 nm. As the E during polar night varies greatly, we are operating with E at an orders of magnitude level, and thus, we assume our results are relevant despite these approximations. The E with increasing depth was compared to the lowest E for significant response in Calanus spp. to investigate how deep the copepods may be influenced by E during the polar night. The E eliciting a significant response in Calanus spp. was also compared (in %) to the surface E from moonlight, night sky, and aurora borealis. The effect of sea ice has not been taken into consideration here, as the albedo and E attenuation of sea ice have so large variations that taking this into account would add additional variation (over several orders of magnitude) to our results. Thus, the estimated depths where E may influence the copepods must be considered as maximum depths. However, ice-free areas throughout the winter are relatively common, particularly on West Spitsbergen, so these results are relevant for at least parts of the Arctic.

Results

24-hour experiments

The median distance to the light stimulus increased with increasing E through the trials; thus, the Calanus spp. CV were consistently negatively phototactic throughout the 24-h period (Fig. 2; Online Resource 2). The response to the white LED used was significant from 9.4 × 10−6 μmol photons m−2 s−1 (OD6; Tables 1, 3). There was no overall change in response to the light stimulus during day compared to night (p = 0.739; Table 3).
Fig. 2

Median distance from light (cm; each black dot representing 1 min) with interquartile range (grey bars) over the duration of the experiment. Each irradiance level lasted 10 min. Dark is the initial dark period; subsequent OD levels are indicated (see Table 1 for the irradiance values used). Night represents the nighttime trials combined (18:00, 21:00, 00:00, 03:00, and 06:00); Day represents the daytime trials combined (12:00, 15:00, 09:00, and 12:00 second time). See Table 1 for the irradiance range used in each experiment

Table 3

Output from mixed modelling of phototactic response in 24-h experiment

 

Distance

p value

Dark

19.5

 

OD8

−2.1

0.247

OD7

4.2

0.023

OD6

15.9

<0.001

OD5

21.9

<0.001

OD4

23.2

<0.001

Day

−0.3

0.739

“Dark” refers to the estimated baseline value during the initial dark period, to which the last timepoint of each subsequent irradiance level is tested. “Distance” is the estimated median distance from the light stimulus (cm) for the initial dark period (Dark) and the changes in median distance for the subsequent E levels. p values denote the significance of comparison to the initial dark period. Dark through OD4 represents the results from nighttime trials, showing a significant response from OD6. Day is daytime; the effect needed to add to the results from nighttime to get those of daytime, showing that day-time trials were not significantly different from the nighttime trials

Threshold values experiments

Calanus spp. were negatively phototactic for all wavebands (Fig. 3; Table 4; see Online Resource 2 for viewing the replicates separately). For all experiments, there was a phototactic response throughout the experiment (almost all ANOVAs have p < 0.001, the least significant being p = 0.012), and a threshold value for response was identified (Table 4). The threshold E level for response differed depending on waveband as well as copepod developmental stage (summarised in Table 5). For the white waveband, the threshold for significant phototactic response was 0.47–4.7 × 10−6 μmol photons m−2 s−1 (Tables 4, 5). For the blue waveband, the threshold for response was 0.05–4.3 × 10−6 μmol photons m−2 s−1, and for the green525 waveband, the threshold for response was 0.17–4.3 × 10−6 μmol photons m−2 s−1. For aurora green550 (experiments performed with stage CV only), the threshold was 0.43 × 10−6 μmol photons m−2 s−1, which was in the same range as the significant response of stage CV to green525 LED (0.34 × 10−6 μmol photons m−2 s−1). For the red waveband, the threshold for significant response was 28–1,800 × 10−6 μmol photons m−2 s−1. Thus, the sensitivity of each developmental stage to red light was about three orders of magnitude lower compared to other wavebands. AF showed the highest sensitivity to light, while AM were the least sensitive.
Fig. 3

Median distance from light (cm; each black dot representing 1 min) with interquartile range (grey bars) over the duration of each experiment (2–3 replicates per experiment, see Table 2) for A stage CIV, B stage CV, C AF, and D AM. Waveband is indicated above the top panel. Each irradiance level lasted 10 min. Dark is the initial dark period; subsequent OD levels are indicated (see Table 1 for the irradiance range used in each experiment)

Table 4

Output from mixed modelling of phototactic response in threshold value experiments for all Calanus spp. stages and wavebands, comparing distance from the light source at each irradiance level to the distance from light source in the initial dark period

White

CIV

F = 8.91, p < 0.001

CV

F = 31.34, p < 0.001

AF

F = 63.02, p < 0.001

AM

F = 7.54, p < 0.001

ANOVA

 

Distance

p value

Distance

p value

Distance

p value

Distance

p value

Dark

37.3

 

20.7

 

16.0

 

16.7

 

OD8

−3.6

0.064

0.2

0.925

−0.7

0.800

−0.8

0.783

OD7.5

1.4

0.470

4.1

0.072

16.8

<0.001

−2.0

0.489

OD7

6.1

0.003

9.6

<0.001

24.4

<0.001

−5.1

0.074

OD6.5

7.1

<0.001

17.9

<0.001

28.5

<0.001

8.3

0.005

OD6

7.4

<0.001

21.2

<0.001

28.4

<0.001

7.6

<0.001

OD5.5

7.6

<0.001

15.1

<0.001

28.2

<0.001

13.1

<0.001

OD5

16.9

<0.001

10.6

<0.001

Blue

CIV

F = 22.02, p < 0.001

CV

F = 14.78, p < 0.001

AF

F = 7.50, p < 0.001

AM

F = 3.32, p = 0.009

ANOVA

Distance

p value

Distance

p value

Distance

p value

Distance

p value

Dark

15.4

 

28.1

 

23.3

 

15.1

 

OD9

0.1

0.963

−6.9

0.015

4.6

0.359

0.3

0.930

OD8.5

0.3

0.911

−8.4

0.003

−2.9

0.556

4.6

0.131

OD8

−0.6

0.847

−5.7

0.042

13.5

<0.001

1.9

0.542

OD7.5

3.4

0.211

5.8

0.040

13.1

0.011

4.7

0.126

OD7

11.2

<0.001

9.8

<0.001

19.2

<0.001

7.4

0.017

OD6.5

22.2

<0.001

15.0

<0.001

20.4

<0.001

9.9

0.002

OD6

29.2

<0.001

15.7

<0.001

20.8

<0.001

8.4

0.007

OD5.5

7.5

0.016

Green525

CIV

F = 4.01, p = 0.005

CV

F = 16.06, p < 0.001

AF

F = 17.44, p < 0.001

AM

F = 3.54, p = 0.007

Aurora green550

CV

F = 17.74, p < 0.001

ANOVA

Distance

p value

Distance

p value

Distance

p value

Distance

p value

Distance

p value

Dark

35.6

 

20.2

 

17.3

 

19.2

 

Dark

19.3

 

OD9

−0.1

0.970

0.9

0.783

−0.5

0.910

3.5

0.392

OD7.5

2.1

0.602

OD8.5

−0.9

0.708

−5.2

0.122

1.2

0.758

6.0

0.146

OD7

8.0

0.323

OD8

0.2

0.946

−2.7

0.419

5.3

0.198

9.8

0.020

OD6.5

16.1

0.004

OD7.5

3.9

0.124

2.1

0.525

17.1

<0.001

8.1

0.053

OD6

14.6

0.005

OD7

5.3

0.040

9.1

0.008

25.3

<0.001

10.6

0.012

OD5.5

19.0

<0.001

OD6.5

8.6

0.001

24.1

<0.001

26.7

<0.001

6.8

0.103

OD5

22.9

<0.001

OD6

8.6

0.001

24.2

<0.001

26.6

<0.001

14.3

<0.001

OD4.5

17.5

<0.001

Red

CIV

F = 12.37, p < 0.001

CV

F = 8.37, p < 0.001

AF

F = 13.50, p < 0.001

AM

F = 3.28, p = 0.012

ANOVA

Distance

p value

Distance

p value

Distance

p value

Distance

p value

Dark

21.5

 

14.9

 

18.2

 

15.0

 

OD7.5

−0.3

0.941

5.0

0.181

1.7

0.646

−4.6

0.288

OD7

5.4

0.138

4.2

0.266

1.6

0.668

1.0

0.808

OD6.5

2.7

0.451

5.6

0.135

7.7

0.044

5.1

0.236

OD6

9.3

0.014

5.5

0.142

12.8

0.001

5.9

0.172

OD5.5

19.3

<0.001

11.4

0.003

21.2

<0.001

7.3

0.092

OD5

20.9

<0.001

13.9

<0.001

20.1

<0.001

8.8

0.044

OD4.5

20.3

<0.001

24.0

<0.001

22.6

<0.001

16.0

<0.001

The ANOVA F statistic was used as an overall test of the models (significant values in bold, using a significance level of 0.05). “Distance” is the median distance from the light stimulus (cm) for the initial dark period (Dark) and change in median distance for the subsequent light levels (OD4.5-9) (significant values in bold, using a stricter significance level of 0.01)

Table 5

Threshold values (×10−6 μmol photons m−2 s−1) for phototactic response are given for all developmental stages and wavebands, as well as the fraction (%) of surface irradiance for each light source for the specific threshold value

 

CIV

CV

AF

AM

White

    

 Threshold

0.94

0.94

0.47

4.7

 Moon

0.01–0.2

0.01–0.2

0.005–0.09

0.05–0.9

 Night sky

3.1–9.4

3.1–9.4

1.6–4.7

16–47

 Aurora borealis

0.02–0.9

0.02–0.9

0.005–0.09

0.1–4.7

Blue

    

 Threshold

0.62

0.62

0.05

4.3

 Moon

0.007–0.1

0.007–0.1

0.0005–0.01

0.05–0.8

 Night sky

2.1–6.2

2.1–6.2

0.2–0.5

14–43

 Aurora borealis

0.02–0.6

0.02–0.6

0.001–0.05

0.1–4.3

Green525

    

 Threshold

2.1

0.34

0.17

4.3

 Moon

0.02–0.4

0.004–0.07

0.002–0.03

0.05–0.8

 Night sky

7.0–21

1.1–3.4

0.6–1.7

14–43

 Aurora borealis

0.05–2.1

0.009–0.3

0.002–0.03

0.1–4.3

Aurora green550

    

 Threshold

 

0.43

  

 Moon

 

0.005–0.09

  

 Night sky

 

1.4–4.3

  

 Aurora borealis

 

0.01–0.4

  

Red

    

 Threshold

150

150

28

1,800

 Moon

1.7–30

1.7–30

0.3–5.6

>20

 Night sky

>100

>100

>93

>100

 Aurora borealis

>3.8

>3.8

0.7–28

>45

For the CV blue waveband experiment, there was a significant result with positive phototaxis at OD8.5. As the copepod position shifted slowly towards the light stimulus already from the dark period through OD8.5 and the response was negative later in this experiment, in addition to that in no other experiment there was a response at this low E level, we attributed this result to “room effects” and chose to ignore this in the further treatment of the results (see “Discussion”).

Comparison to polar night irradiance

For blue and green wavebands, the threshold E for response corresponded to <0.8 % of surface moonlight and 0.2–43 % of surface night sky E (Table 5). The threshold level for phototaxis for green525 and aurora green550 corresponded to <4.3 % of surface aurora borealis E. For the red waveband, the threshold level for response corresponded to >0.3 % of the surface moonlight and >93 % of the night sky E. When applying an E threshold value of 0.05 × 10−6 μmol photons m−2 s−1 as well as an attenuation coefficient of light in water assumed to correspond to the ambient (winter) conditions, Calanus spp. may respond to E from the clear night sky down to about 70–80 m, from aurora borealis down to 80–120 m, and moonlight to 120–170 m depth (Fig. 4).
Fig. 4

Irradiance in the polar night from the moon, night sky, and aurora borealis with depth, the shaded areas representing an approximate range of irradiance from each source. The vertical dotted line (0.05 × 10−6 μmol photons m−2 s−1) represents the lowest irradiance value for phototactic response in Calanus spp.

Discussion

Threshold values for response and their ecological relevance

All developmental stages and both sexes of Calanus spp. displayed negative phototaxis and were highly sensitive to E. The negative phototaxis is in accordance with what would be expected for species displaying nocturnal (normal) DVM, which has been documented for Calanus spp. (e.g. Nicholls 1933; Huntley and Brooks 1982; Frost 1988; Lampert 1989; Fortier et al. 2001; Falk-Petersen et al. 2008; Baumgartner et al. 2011). The lowest E eliciting a significant phototactic response in this study was 0.05 and 0.17 × 10−6 μmol photons m−2 s−1, displayed by AF (blue and green525 wavebands, respectively; see Tables 3, 4 and 5), and 0.34 and 0.43 × 10−6 μmol photons m−2 s−1, displayed by CV (green525 and aurora green550, respectively, the latter simulating aurora borealis emission line). These are ecologically relevant E values, corresponding to <0.09 % of the surface moon E, <4 % of the night sky E, and <0.4 % of the Aurora borealis E. This clearly indicates that a phototactic response to ambient E is indeed possible for Calanus spp. in the polar night.

When comparing the lowest E threshold value to polar night irradiance with depth, Calanus spp. may respond to E from the clear night sky down to about 80 m, from aurora borealis down to 120 m and moonlight to 170 m depth. Berge et al. (2009) found that DVM with significant rhythmicity occurred within a 30–60 m depth range during the darkest time of the polar night (mid-December to early January). This is within our estimated depth range of night sky E detection of Calanus spp. As the solar elevation angle increases after winter solstice, the E (solar background) during midday will increase, as will the depth for E detection. This is reflected in the data of Berge et al. (2009), showing that the greatest depth of DVM increased to around 70 m in late January and beyond 90 m in February. Berge et al. (2012) also detected a DVM signal down to 80–90 m in late January. The E from aurora and moonlight will probably be detected deeper into the water column than night sky/solar background during mid-winter. This is supported by the study of Berge et al. (2009), who found that during the 3 days prior to and after full moon, there was a shift in DVM signal from a 24-h cycle towards a 25-h lunar cycle. Zooplankton performing reverse DVM during full moon, the moon rising during night and setting during day, has also been described in Svalbard in January (Webster et al. in press). The DVM signal has to our knowledge not been investigated in relation to the aurora borealis, but the intensity of auroras is probably high enough to affect DVM. The frequency of winter nights with clear or partially clear skies has been reported to be 68 % for Longyearbyen, Svalbard (1986–1995; Simmons et al. 1996). Looking at the frequency of auroras, the average occurrence was approximately 65 % for the same location (varying between 55 and 95 % from 2000 through 2012; Pulkkinen et al. 2011; with additional data at www.space.fmi.fi/MIRACLE/ASC/AuroralOccurrence.html). Thus, the frequency of nights with aurora visible at sea surface level may be about 44 % (0.68 × 0.65 = 0.44). The intensity of the aurora varies, as will the depth the aurora can be perceived by the zooplankton, so the frequency of 44 % may be seen as a maximum estimate. Still, the aurora may, at least in periods, affect the zooplankton during the polar night.

The high sensitivity to E is also relevant for Calanus spp. in deeper waters at lower latitudes. Light has been proposed as one of the factors governing the termination of the winter resting phase of Calanus spp. in the North Atlantic, possibly by the change in photoperiod in late winter (Miller et al. 1991). In addition, water clarity, and thus the irradiance with depth, has been found to affect the vertical distribution of Calanus spp. (Daase et al. 2008; Dupont and Aksnes 2012).

Light is considered the primary cue for DVM, but the DVM behaviour may be altered by factors such as gravity and lipid content (e.g. Forward 1988, Ringelberg 1995). To start elucidating the DVM behaviour of Calanus spp., we wanted to investigate the directional phototactic behaviour only, and by performing the experiments in the horizontal plane, we limited the influence from buoyancy and gravity. The results from this kind of experiments (this study, Miljeteig et al. submitted) appear to match well with findings for natural populations, e.g. with regard to depth distributions. Thus, the results may be related to the DVM of Calanus spp.

The Calanus species

The Calanus spp. specimens used in our experiments were probably a mix of C. glacialis and C. finmarchicus, as these are species described to be common in West Spitsbergen fjords (e.g. Kwasniewski et al. 2003, Arnkværn et al. 2005, Hop et al. 2006, Gabrielsen et al. 2012). The third common Calanus species, C. hyperboreus, would have been recognised by its size as well as morphological traits during sorting. We chose not to attempt identification of the specimens to species, due to that recent investigations have described large rates of misidentification using prosome length, which is the conventional and least time-consuming way of separating C. glacialis and C. finmarchicus (Kwasniewski et al. 2003; Lindeque et al. 2004; Parent et al. 2011; Gabrielsen et al. 2012). In addition, these species have recently been found to have a high frequency of hybridisation (Parent et al. 2012). We thus treated our sets of individuals as Calanus spp. As the specimens were sampled from the population in Adventfjorden during January, they were ecologically relevant for our study.

Between-stage sensitivity variations

The different developmental stages and sexes showed different sensitivities to E. Adult females were the most sensitive, with thresholds of e.g. 0.05 and 0.17 × 10−6 μmol photons m−2 s−1 (Table 5). The lowest E thresholds for stage CV were 0.34 and 0.43 × 10−6 μmol photons m−2 s−1 and for stage CIV 0.62 × 10−6 μmol photons m−2 s−1. AM displayed the lowest sensitivity, with a lowest threshold value of 4.3 × 10−6 μmol photons m−2 s−1 for blue and green525 wavebands. Related to DVM, this would correspond to greatest migration depths for AF, followed by CV, CIV, and shallowest for AM, which is in accordance with field studies of stage-specific migration depth of Calanus spp. copepodite stages and AF. Huntley and Brooks (1982) found that for C. pacificus, the amplitude of DVM increased with increasing age/stage, the night depths remaining constant while daytime depths increased. Nicholls (1933) reported that C. finmarchicus AF inhabited the deepest parts and that migration depth increased with increasing stage, and Unstad and Tande (1991) reported the same for both C. finmarchicus and C. glacialis. During summer in Kongsfjorden, West Spitsbergen, the younger stages (CI-CIV) of C. finmarchicus and C. glacialis have been reported to inhabit surface and intermediate water layers, while older stages stayed in bottom layers; however, the latter had probably descended for overwintering (Kwasniewski et al. 2003). An explanation to the deeper migration of larger stages may be that larger and more pigmented individuals are more susceptible to predators and must thus, according to the predator evasion hypothesis, migrate deeper to get the same protection (Hays 2003). The need of high sensitivity to light is thus expected to be more pronounced in larger and older individuals, which is generally supported in this study. Larger individuals also tend to have larger lipid reserves, which decreases the need of migrating to surface waters to feed (e.g. Hays et al. 2001; Hays 2003). This may be part of the explanation to the deeper distribution and higher light sensitivity of older individuals. In this study, AM displayed lower sensitivity to light than the other stages investigated, as well as higher variability in response, and did thus not follow the general rule of higher sensitivity to light in older stages. Copepod AM generally display higher swimming activity than AF and CV, spend little time feeding, and are mainly focused on mate-finding (e.g. Irigoien et al. 2000; Kiørboe and Bagøien 2005), which may lead to the weaker and less uniform response to E. In contrast to this study, Miljeteig et al. (submitted) found that C. finmarchicus AM from a laboratory culture had a strong, uniform positive phototaxis. The reason for these differences is not known, but the cultured animals may be acclimated differently both regarding nutritional and mating status compared to the polar night acclimated, field-collected specimens.

The eye of Calanus spp. is called a nauplius eye and is situated in front of the brain close to the ventral surface of the animal (Elofsson 1966). Three cups, one ventral and two lateral, make up the eye. The eye contains three small, thin pigment cells, and light sensitivity is enhanced by two tapetal (light-reflecting) cells in each cup. Elofsson (1966) described the eye of adult specimens, and to our knowledge, ontogenetic changes in eye structure have not been investigated. Thus, we do not know if the variations in sensitivity with stage may be caused by structural differences or by other factors.

Threshold levels in other taxa

The threshold E values we found for Calanus spp. are highly comparable to those of other zooplankton. For Crustacea in general, the threshold was stated to be about 5 × 10−5 μW cm−2 (Clarke 1971), corresponding to about 2.3 × 10−6 μmol photons m−2 s−1, which is approximately two orders of magnitude higher than the lowest threshold detected in this study. Cohen and Forward (2005) found that using the blue–green waveband, the copepod C. americana responded to E > 1 × 1011–1 × 1014 photons m−2 s−1 during day and night, respectively, which corresponds to 0.17–170 × 10−6 μmol photons m−2 s−1. The copepod A. tonsa displayed positive phototaxis and responded to E down to 2.8 × 1011 photons m−2 s−1, corresponding to 0.46 × 10−6 μmol photons m−2 s−1 (Stearns and Forward 1984). For Calanus spp., a few studies have looked at the response to ultraviolet radiation stress and PAR in C. finmarchicus (Aarseth and Schram 1999; Wold and Norrbin 2004), but the E levels used in these studies were relatively high (14–75 μmol photons m−2 s−1) and thus not relevant for detecting a threshold level for response. Buskey and Swift (1985) investigated the response of C. finmarchicus to simulated bioluminescent flashes of different intensity, but also here the lowest E level used was too high (200 × 10−6 μmol photons m−2 s−1) for detecting a threshold level. Miljeteig et al. (submitted) detected threshold levels of 0.99–9.8 × 10−6 μmol photons m−2 s−1 (white waveband) for C. finmarchicus CV, AM, and AF from a laboratory culture acclimated to a light–dark cycle corresponding to spring at 63° N. The threshold E for response of field-collected Calanus spp. in this study to the white waveband was lower for CV and AF, but higher for AM. Based on that the threshold levels for laboratory cultured (spring acclimated) and polar night acclimated Calanus spp. are within the same range, there seems to be only small seasonal changes in E sensitivity (if any, as the observed differences may have other causes). Even though the surface daytime E levels are many orders of magnitude higher during spring in Norway than during the polar night, the attenuation of light in sea water is correspondingly higher, particularly during spring bloom. Miljeteig et al. (submitted) showed that the threshold levels of C. finmarchicus corresponded to depths of only 50 m during peak spring bloom conditions in Trondheimsfjorden, Mid-Norway. Thus, the high sensitivity to light may be relevant during all times of year due to the varying attenuation of light in the sea.

Spectral sensitivity

The E required to elicit a significant phototactic response was lowest in the blue and green wavebands (0.05 and 0.17 × 10−6 μmol photons m−2 s−1, respectively; Table 5) and slightly higher in white (0.94 × 10−6 μmol photons m−2 s−1). For stage CV, the E for significant response was relatively similar for green525 aurora green550 (0.34 and 0.43 × 10−6 μmol photons m−2 s−1, respectively). The Calanus spp. were, looking at each developmental stage and sex, about 3 orders of magnitude less sensitive to red (28–1,800 × 10−6 μmol photons m−2 s−1). Thus, the highest spectral sensitivity seems to be broad, from blue through the green part of the visible spectrum, as we could not detect clear differences between the different blue and green wavebands used. The low sensitivity to red is probably related to the ecology of these copepods and is also commonly observed in other studies investigating the spectral sensitivity of pelagic copepods (e.g. Stearns and Forward 1984; Buskey and Swift 1985; Cohen and Forward 2002). The attenuation coefficient of light in water is higher in the red waveband (600–700 nm) than in the rest of the visible spectrum (Sakshaug et al. 2009), and the blue or green light penetrates deepest depending on the constituents of the water (blue in Case I water, green in Case II water; Jerlov 1968; Sakshaug et al. 2009). Calanus finmarchicus and C. glacialis are pelagic species, inhabiting depths down to hundreds of metres (e.g. Tande 1988; Fortier et al. 2001; Cottier et al. 2006; Falk-Petersen et al. 2009; Bergvik et al. 2012), and benefit from being more sensitive to the predominant blue–green wavebands than to red. This pattern has also been confirmed by hyperspectral imaging of Calanus spp. eyes, showing high reflectance and thus low absorbance in the red waveband and lower reflectance/higher absorption in blue and green wavebands (Båtnes et al. unpublished data). Buskey and Swift (1985) investigated the behavioural response of C. finmarchicus to simulated bioluminescent flashes at different wavelengths and found that the peak response was from approximately 460–540 nm, which corresponds well to the range of the blue and green525 used in the present study. Buskey and Swift (1985) detected a weaker response in the waveband of the aurora green550, which differs from our results. However, the response to bioluminescent flashes may differ from the response to ambient diffuse light. Cohen and Forward (2002) investigated the spectral sensitivities of four copepod species displaying different migration patterns and found that the species Centropages typicus and C.americana, both performing nocturnal DVM, had spectral sensitivity peaks from 480 to 520 nm, which is in the range of the blue and green525 used in this study. Species inhabiting shallow/estuarine waters with broad spectral E have broader spectral sensitivities, e.g. A. tonsa (Stearns and Forward 1984) and Labidocera aestiva (Cohen and Forward 2002).

Phototactic response during day and night

The phototactic response of Calanus spp. was not significantly different during day compared to night. In contrast, the copepod C. americana had an E threshold of response three orders of magnitude lower during day than during night (Cohen and Forward 2005). C. americana undergoes twilight DVM, which involves a descent after sunset (the “midnight sink”) and an ascent before sunrise (the “early morning rise”) in addition to the sunset ascent and sunrise descent also involved in nocturnal DVM. The additional descent and ascent is under endogenous control, and the endogenous rhythms of C. americana were thought to suppress the phototactic response during night (Cohen and Forward 2005). Calanus spp. is known to perform nocturnal DVM, which may explain the uniform phototactic response over 24 h.

Variability in the experiments

For some of the experiments, there were variable results for the different replicates (Online Resource 2), and the response seemed to be gradual, ranging over at least three E levels (Table 4; Fig. 3). This may indicate variability within the group of copepods, some of the individuals starting the response earlier than others, and some not responding at all. As we did not track the position of the individuals, only of the group, we could not detect this in detail, but the variability may be explained by species differences (C. glacialis and C. finmarchicus) and individual variation in nutritional status and age/development within the stage (e.g. Nicholls 1933, Huntley and Brooks 1982; Hays et al. 2001; Bergvik et al. 2012). In addition, due to sampling difficulties, the number of replicates (2–3 replicates with 20–25 individuals in each) was low, which makes the analyses vulnerable to variability among replicates. Some of the Calanus spp. may have been in poor condition after sampling and storage in buckets over time (24 h–18 days). Particularly, AM are vulnerable to handling and keeping in small containers (D. Altin, personal comment), which is reflected in highly variable results with replicates 2 and 3 (Online Resource 2). Variability among replicates may also appear because of “room effects” (air currents from the cooling system and other, unidentified causes). We believe that these “room effects” also may explain that CV first appeared to perform positive phototaxis towards blue (OD8.5; Table 4). In this experiment, the position of the copepods started to gradually shift towards the light stimulus already in the dark period and continued through OD8.5 (Fig. 3C). As the phototaxis is negative and more rapid and pronounced later in the experiment, in a similar manner as for the other stages, we assume that air currents or other “room effects” led to a drift towards the light stimulus during the first 30 min and that the negative phototaxis is the true, active response (significant from OD7).

In darkness in some of the replicates, there was a partial accumulation of copepods in one end of the projection area, but we could not find any connection between the starting distribution in one experiment and the end distribution of the previous. We thus believe that 1-h dark acclimation was sufficient and that the accumulation probably was due to the observed “room effects.” The accumulation alternated between aquarium ends and could only be limited and not eliminated by randomising the order of wavebands and by alternating the light stimulus between aquarium ends. As we analysed the copepods’ position compared to the distribution in darkness in each particular experiment, we captured the phototactic response despite the differences in starting position.

Concluding remarks

Knowledge about the spectral sensitivities as well as the E levels triggering phototactic response is crucial to understanding the migrations of Calanus spp. and their role in the polar night ecosystem. In this study, we show that both copepodite stages and both sexes (CIV, CV, AF, and AM) responded with negative phototaxis to all the wavebands used in the experiments. The lowest E eliciting a significant response (0.05 × 10−6 μmol photons m−2 s−1) corresponds to 0.0005–0.5 % of the polar night surface E. Modelling the E from different light sources with depth, the Calanus spp. may respond down to approximately 70–80 m depth to clear night sky E, 120–170 m to moonlight, and 80–120 m to aurora borealis. This supports that the ambient E, including the aurora borealis, may be a proximate cue for DVM also during the polar night. Further investigations on the rhythmicity of migrations in relation to ambient E, as well as the ultimate reasons for undergoing diel migrations in “complete darkness,” would further increase the understanding of marine pelagic ecosystem in the polar night.

Notes

Acknowledgements

Funding for the Ph.D. Project of A. S. Båtnes was provided by the Faculty of Natural Sciences and Technology (SO funding), NTNU, and the field work was funded by the Arctic Field Grant (Svalbard Science Forum, Norwegian Polar institute). The Ph.D. Project of C. Miljeteig was funded by VISTA—a basic research programme funded by Statoil, conducted in close collaboration with The Norwegian Academy of Science and Letters (Project No. 6156). J. Berge is supported by the Norwegian Research Council project Circa (Project No. 214271). M. Greenacre’s research is partially supported by the BBVA Foundation in Madrid and grant MTM2012-37195 of the Spanish Ministry of Education and Competitiveness.

Supplementary material

300_2013_1415_MOESM1_ESM.docx (3.4 mb)
Supplementary material 1 (DOCX 3523 kb)
300_2013_1415_MOESM2_ESM.tif (3.1 mb)
Supplementary material 2 (TIFF 3174 kb)

References

  1. Aarseth KA, Schram TA (1999) Wavelength-specific behaviour in Lepeophtheirus salmonis and Calanus finmarchicus to ultraviolet and visible light in laboratory experiments (Crustacea: Copepoda). Mar Ecol Prog Ser 186:211–217CrossRefGoogle Scholar
  2. Arnkværn G, Daase M, Eiane K (2005) Dynamics of coexisting Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus populations in a high-Arctic fjord. Polar Biol 28:528–538CrossRefGoogle Scholar
  3. Auel H, Werner I (2003) Feeding, respiration and life history of the hyperiid amphipod Themisto libellula in the Arctic marginal ice zone of the Greenland Sea. J Exp Mar Biol Ecol 296:183–197CrossRefGoogle Scholar
  4. Baker DJ, Romick GJ (1976) The rayleigh: interpretation of the unit in terms of column emission rate or apparent radiance expressed in SI units. Appl Opt 15:1966–1968PubMedCrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4
  6. Baumgartner MF, Mate BR (2003) Summertime foraging ecology of North Atlantic right whales. Mar Ecol Prog Ser 264:123–135CrossRefGoogle Scholar
  7. Baumgartner MF, Cole TVN, Campbell RG, Teegarden GJ, Durbin EG (2003) Associations between North Atlantic right whales and their prey, Calanus finmarchicus, over diel and tidal time scales. Mar Ecol Prog Ser 264:155–166CrossRefGoogle Scholar
  8. Baumgartner MF, Lysiak NSJ, Schuman C, Urban-Rich J, Wenzel FW (2011) Diel vertical migration behavior of Calanus finmarchicus and its influence on right and sei whale occurrence. Mar Ecol Prog Ser 423:167–184CrossRefGoogle Scholar
  9. Berge J, Cottier F, Last KS, Varpe Ø, Leu E, Søreide J, Eiane K, Falk-Petersen S, Willis K, Nygård H, Vogedes D, Griffiths C, Johnsen G, Lorentzen D, Brierley AS (2009) Diel vertical migration of Arctic zooplankton during the polar night. Biol Lett 5:69–72PubMedCentralPubMedCrossRefGoogle Scholar
  10. Berge J, Båtnes AS, Johnsen G, Blackwell SM, Moline MA (2012) Bioluminescence in the high Arctic during the polar night. Mar Biol 159:231–237PubMedCentralPubMedCrossRefGoogle Scholar
  11. Bergvik M, Leiknes Ø, Altin D, Dahl KR, Olsen Y (2012) Dynamics of the lipid content and biomass of Calanus finmarchicus (copepodite V) in a Norwegian fjord. Lipids 47:881–895PubMedCrossRefGoogle Scholar
  12. Blachowiak-Samolyk K, Søreide JE, Kwasniewski S, Sundfjord A, Hop H, Falk-Petersen S, Hegseth EN (2008) Hydrodynamic control of mesozooplankton abundance and biomass in northern Svalbard waters (79-81°N). Deep-Sea Res II 55:2210–2224CrossRefGoogle Scholar
  13. Clarke GL (1971) Light conditions in the sea in relation to the diurnal vertical migration of animals. In: Farquhar GB (ed) Proceedings of the International Symposium on Biological Sound Scattering in Ocean. Maury Center for Ocean Science, Washington, pp 41–50Google Scholar
  14. Cohen JH, Forward RB Jr (2002) Spectral sensitivity of vertically migrating marine copepods. Biol Bull (Woods Hole) 203:307–314CrossRefGoogle Scholar
  15. Cohen JH, Forward RB Jr (2005) Diel vertical migration of the marine copepod Calanopia americana. II. Proximate role of exogenous light cues and endogenous rhythms. Mar Biol 147:399–410CrossRefGoogle Scholar
  16. Cohen JH, Forward RB Jr (2009) Zooplankton diel vertical migration—a review of proximate control. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review, vol 47. CRC Press, Boca Raton, pp 77–109CrossRefGoogle Scholar
  17. Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiol 167(168):127–142CrossRefGoogle Scholar
  18. Cottier FR, Tarling GA, Wold A, Falk-Petersen S (2006) Unsynchronized and synchronized vertical migration of zooplankton in a high arctic fjord. Limnol Oceanogr 51:2586–2599CrossRefGoogle Scholar
  19. Daase M, Eiane K, Aksnes DL, Vogedes D (2008) Vertical distribution of Calanus spp. and Metridia longa at four Arctic locations. Mar Biol Res 4:193–207CrossRefGoogle Scholar
  20. Dale T, Kaartvedt S (2000) Diel patterns in stage-specific vertical migration of Calanus finmarchicus in habitats with midnight sun. ICES J Mar Sci 57:1800–1818CrossRefGoogle Scholar
  21. Dupont N, Aksnes DL (2012) Effects of bottom depth and water clarity on the vertical distribution of Calanus spp. J Plankton Res 34:263–266CrossRefGoogle Scholar
  22. Falk-Petersen S, Hopkins CCE, Sargent JR (1990) Trophic relationships in the pelagic, Arctic food web. In: Barnes M, Gibson RN (eds) Trophic relationships in the marine environment. Aberdeen University Press, Aberdeen, pp 315–333Google Scholar
  23. Falk-Petersen S, Leu E, Berge J, Kwaśniewski S, Nygård H, Røstad A, Keskinen E, Thormar J, von Quillfeldt C, Wold A, Gulliksen B (2008) Vertical migration in high Arctic waters during Autumn 2004. Deep Sea Res II 55:2275–2284CrossRefGoogle Scholar
  24. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39CrossRefGoogle Scholar
  25. Fort J, Cherel Y, Harding AMA, Egevang E, Steen H, Kuntz G (2010) The feeding ecology of little auks raises questions about winter zooplankton stocks in North Atlantic surface waters. Biol Lett 6:682–684PubMedCentralPubMedCrossRefGoogle Scholar
  26. Fortier M, Fortier L, Hattori H, Saito H, Legendre L (2001) Visual predators and the diel vertical migration of copepods under Arctic sea ice during the midnight sun. J Plankton Res 23:1263–1278CrossRefGoogle Scholar
  27. Forward RB (1988) Diel vertical migration: zooplankton photobiology and behaviour. Oceanogr Mar Biol Annu Rev 26:361–393Google Scholar
  28. Frost BW (1988) Variability and possible significance of diel vertical migration in Calanus pacificus, a planktonic marine copepod. Bull Mar Sci 43:675–694Google Scholar
  29. Gabrielsen TM, Merkel B, Søreide JE, Johansson-Karlsson E, Bailey A, Vogedes D, Nygård H, Varpe Ø, Berge J (2012) Potential misidentifications of two climate indicator species of the marine arctic ecosystem: Calanus glacialis and C. finmarchicus. Polar Biol 35:1621–1628CrossRefGoogle Scholar
  30. Hassel A (1986) Seasonal changes in zooplankton composition in the Barents Sea, with special attention to Calanus spp. (Copepoda). J Plankton Res 8:329–339CrossRefGoogle Scholar
  31. Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiol 503:163–170CrossRefGoogle Scholar
  32. Hays GC, Kennedy H, Frost BW (2001) Individual variability in diel vertical migration of a marine copepod: why some individuals remain at depth when others migrate. Limnol Oceanogr 46:2050–2054CrossRefGoogle Scholar
  33. Hirche H-J (1991) Distribution of dominant calanoid copepod species in the Greenland Sea during late fall. Polar Biol 11:351–362CrossRefGoogle Scholar
  34. Hop H, Falk-Petersen S, Svendsen H, Kwasniewski S, Pavlov V, Pavlova O, Søreide JE (2006) Physical and biological characteristics of the pelagic system across Fram Strait to Kongsfjorden. Prog Oceanogr 71:182–231CrossRefGoogle Scholar
  35. Hovland EK, Hancke K, Alver MO, Drinkwater K, Høkedal J, Johnsen G, Moline M, Sakshaug E (2012) Optical impact of an Emiliania huxleyi bloom in the frontal region of the Barents Sea. J Mar Syst. doi:10.1016/j.jmarsys.2012.07.002 Google Scholar
  36. Huntley M, Brooks ER (1982) Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar Biol 71:23–31CrossRefGoogle Scholar
  37. Irigoien X, Obermuller B, Head RN, Harris RP, Rey C, Hansen BW, Hygum BH, Heath MR, Durbin EG (2000) The effect of food on the determination of sex ratio in Calanus spp.: evidence from experimental studies and field data. ICES J Mar Sci 57:1752–1763CrossRefGoogle Scholar
  38. Jensen HW, Durand F, Stark M, Premoze S, Dorsey J, Shirley P (2001) A physically-based night sky model. Proc SIGGRAPH. doi:10.1145/383259.383306
  39. Jerlov NG (1968) Optical oceanography. Elsevier, AmsterdamGoogle Scholar
  40. Johnsen G, Volent Z, Sakshaug E, Sigernes F, Pettersson LH (2009) Remote sensing in the Barens Sea. In: Sakshaug E, Johnsen G, Kovacs K (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 139–168Google Scholar
  41. Karnovsky NJ, Kwaśniewski S, Weşławski JM, Walkusz W, Beszczynska-Möller A (2003) Foraging behavior of little auks in a heterogeneous environment. Mar Ecol Prog Ser 253:289–303CrossRefGoogle Scholar
  42. Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007CrossRefGoogle Scholar
  43. Kwasniewski S, Hop H, Falk-Petersen S, Pedersen G (2003) Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard. J Plankton Res 25:1–20CrossRefGoogle Scholar
  44. Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3:21–27CrossRefGoogle Scholar
  45. Lindeque PK, Harris RP, Jones MB, Smerdon GR (2004) Distribution of Calanus spp as determined using a genetic identification system. Sci Mar 68:121–128CrossRefGoogle Scholar
  46. Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H (1991) Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar Ecol Prog Ser 72:79–91CrossRefGoogle Scholar
  47. Müller A, Wuchterl G, Sarazin M (2011) Measuring the night sky brightness with the lightmeter. RevMexAA (Serie de Conferencias) 41:46–49Google Scholar
  48. Mumm N, Auel H, Hanssen H, Hagen W, Richter C, Hirche HJ (1998) Breaking the ice: large-scale distribution of mesozooplankton after a decade of Arctic and transpolar cruises. Polar Biol 20:189–197CrossRefGoogle Scholar
  49. Myrabø HK (1985) Nocturnal ground irradiance at high latitudes. Appl Optics 24:3908–3913CrossRefGoogle Scholar
  50. Nicholls AG (1933) On the biology of Calanus finmarchicus. III. Vertical distribution and diurnal migration in the Clyde-Sea area. J Mar Biol Assoc UK 19:139–164CrossRefGoogle Scholar
  51. Parent GJ, Plourde S, Turgeon J (2011) Overlapping size ranges of Calanus spp. off the Canadian Arctic and Atlantic coasts: impact on species’ abundances. J Plankton Res 33:1654–1665CrossRefGoogle Scholar
  52. Parent GJ, Plourde S, Turgeon J (2012) Natural hybridization between Calanus finmarchicus and C. glacialis (Copepoda) in the Arctic and Northwest Atlantic. Limnol Oceanogr 57:1057–1066CrossRefGoogle Scholar
  53. Pulkkinen TI, Tanskanen EI, Viljanen A, Partamies N, Kauristie K (2011) Auroral electrojets during deep solar minimum at the end of solar cycle 23. J Geophys Res. doi:10.1029/2010JA016098 Google Scholar
  54. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0Google Scholar
  55. Rabindranath A, Daase M, Falk-Petersen S, Wold A, Wallace MI, Berge J, Brierley AS (2011) Seasonal and diel vertical migration of zooplankton in the High Arctic during the autumn midnight sun of 2008. Mar Biodivers 41:365–382CrossRefGoogle Scholar
  56. Rasband WS (1997–2012) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/
  57. Ringelberg J (1995) Changes in light-intensity and diel vertical migration—a comparison of marine and freshwater environments. J Mar Biol Assoc UK 75:15–25CrossRefGoogle Scholar
  58. Ringelberg J (1999) The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biol Rev Cambridge Philos Soc 74:397–423CrossRefGoogle Scholar
  59. Ringelberg J, Van Gool E (2003) On the combined analysis of proximate and ultimate aspects in diel vertical migration (DVM) research. Hydrobiol 491:85–90CrossRefGoogle Scholar
  60. Sakshaug E, Johnsen G, Zsolt V (2009) Light. In: Sakshaug E, Johnsen G, Kovacs K (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 117–138Google Scholar
  61. Sato M, Sasaki H, Fukuchi M (2002) Stable isotopic compositions of overwintering copepods in the arctic and subarctic waters and implications to the feeding history. J Mar Syst 38:165–174CrossRefGoogle Scholar
  62. Simmons DAR, Sigernes F, Henriksen K (1996) Weather, twilight, and auroral observing from Spitsbergen in the polar winter. Polar Rec 32:217–228CrossRefGoogle Scholar
  63. Søreide JE, Falk-Petersen S, Hegseth EN, Hop H, Carroll ML, Hobson KA, Blachowiak-Samolyk K (2008) Seasonal feeding strategies of Calanus in the high-Arctic Svalbard region. Deep-Sea Res II 55:2225–2244CrossRefGoogle Scholar
  64. Stearns DE, Forward RB (1984) Photosensitivity of the calanoid copepod Acartia tonsa. Mar Biol 82:85–89CrossRefGoogle Scholar
  65. Tande KS (1982) Ecological investigations on the zooplankton community in Balsfjorden, northern Norway: generation cycles, and variations in body weight and body content of carbon and nitrogen related to overwintering and reproduction in the copepod Calanus finmarchicus (Gunnerus). J Exp Mar Biol Ecol 62:129–142CrossRefGoogle Scholar
  66. Tande KS (1988) An evaluation of factors affecting vertical distribution among recruits of Calanus finmarchicus in three adjacent high-latitude localities. Hydrobiol 167–168:115–126CrossRefGoogle Scholar
  67. Unstad KH, Tande KS (1991) Depth distribution of Calanus finmarchicus and Calanus glacialis in relation to environmental conditions in the Barents Sea. Polar Res 10:409–420CrossRefGoogle Scholar
  68. Vadstein (2009) Interactions the planktonic food web. In: Sakshaug E, Johnsen G, Kovacs KM (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 251–266Google Scholar
  69. Wallace MI, Cottier FR, Berge J, Tarling GA, Griffiths C, Brierley AS (2010) Comparison of zooplankton vertical migration in an ice-free and a seasonally ice-covered Arctic fjord: an insight into the influence of sea ice cover on zooplankton behavior. Limnol Oceanogr 55:831–845CrossRefGoogle Scholar
  70. Webster CN, Varpe Ø, Falk-Petersen S, Berge J, Stübner E, Brierley AS (in press) Moonlit swimming: vertical distributions of macrozooplankton and nekton during the polar night. Polar BiolGoogle Scholar
  71. Wold A, Norrbin F (2004) Vertical migration as a response to UVR stress in Calanus finmarchicus females and nauplii. Polar Res 23:27–34CrossRefGoogle Scholar
  72. Yamagutchi A, Ikeda T, Watanabe Y, Ishizaka J (2004) Vertical distribution patterns of pelagic copepods as viewed from the predation pressure hypothesis. Zool Stud 43:475–485Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Anna S. Båtnes
    • 1
    • 2
  • Cecilie Miljeteig
    • 1
  • Jørgen Berge
    • 3
    • 2
  • Michael Greenacre
    • 3
    • 4
  • Geir Johnsen
    • 1
    • 2
  1. 1.Department of BiologyNorwegian University of Science and TechnologyTrondheimNorway
  2. 2.The University Centre in SvalbardLongyearbyenNorway
  3. 3.Faculty of Biosciences, Fisheries and EconomicsThe Arctic University of NorwayTromsøNorway
  4. 4.Department of Economics and Business, Barcelona Graduate School of EconomicsUniversitat Pompeu FabraBarcelonaSpain

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