Polar Biology

, Volume 37, Issue 5, pp 707–713 | Cite as

Glowing in the dark: discriminating patterns of bioluminescence from different taxa during the Arctic polar night

  • Geir Johnsen
  • Mauro Candeloro
  • Jørgen Berge
  • Mark Moline
Original Paper

Abstract

Research since 2009 has shown that despite almost total darkness during the Arctic polar night, there is much more biological activity than previously assumed, both at the sea surface, water column and sea floor. Here, we describe in situ monitoring of the bioluminescent fraction of the zooplankton community (dinoflagellates, copepods, krill and ctenophores) as a function of time and space. In order to examine the relative contribution of each selected taxon and any diurnal patterns in the relative signals, a time series platform capable of detecting in situ bioluminescent flashes was established in Kongsfjord, Svalbard, during the polar night in January 2013. Combined with laboratory-controlled measurements of animals collected next to the time series platform, we present both taxon-specific and community characteristics of the bioluminescence signal from a location at 79°N and from the middle of the polar night. Based on this 51-h time series, we conclude that the bioluminescent fraction of the zooplankton does not maintain a diurnal signal. Rather, the frequency of bioluminescence flashes from the entire bioluminescent community remained steady throughout the sampling period. Furthermore, we conclude that bioluminescence flash kinetic characteristics have a strong potential for in situ taxa recognition of zooplankton.

Keywords

Arctic Polar night Marine zooplankton Bioluminescence Copepods Krill Ctenophores 

Introduction

During the last few decades, there has been a consistent and strong reduction in the sea ice extent in the Arctic Ocean (Sakshaug et al. 2009; Polyak et al. 2010). For its unique ecosystem, the sea ice is an important habitat for more than one thousand species of algae and invertebrates that have been recorded living in or on the underside of the ice, as well as the marine mammals and seabirds that find their main food there (Bluhm et al. 2011). In addition, the sea ice acts as a key regulator for important processes such as light penetration, water mass formation and temperature regulation. Hence, the Arctic sea ice extent and thickness is a “canary in the coal mine” with respect to global climate change in the high north (Polyak et al. 2010). Today we see an expanding activity and international interest in the marine environment in the Arctic with respect to natural resources such as oil, gas, minerals and fisheries. New activities and sea-transport routes require new knowledge about ecosystem structure and dynamics for sound management and decision making (Sakshaug et al. 2009; Wang and Overland 2009; Hirche and Kosobokova 2011).

There has been a common assumption from the governmental authorities, nature management and the scientific community that during the polar night, there is low biological activity and biomass at all trophic levels throughout the water column and on the sea floor. Lately, however, the use of new underwater technology such as autonomous underwater vehicles (AUVs) and optical sensors have proven to be important for elucidating life and environmental conditions during the polar night (Berge et al. 2009, 2012; Båtnes et al. 2013). Also, we now know that several species of seabirds (Brünnichs guillemot, black guillemot, kittiwake, fulmar, little auk and glaucous gull) are overwintering in Arctic fjords (Weslawski et al. 1991; Berge et al. 2012, own observations) and actively feeding in the upper water column. Their prey comprises of different species of zooplankton (copepods, amphipods, ctenophores, krill) and fish (e.g., polar cod) indicating key trophic linkages persist at these locations.

This study focuses on the bioluminescent fraction of the zooplankton, which may be an important cue for visual predators such as seabirds and fish in their pursuit of prey. Bioluminescence (BL, light generated from an living organism measured as photons s−1) is a characteristic feature of all the world’s oceans, but has been documented to be of special importance in the abyssal zone (Haddock et al. 2010; Moline et al. 2013). In the Arctic, however, during the darkest part of the polar night at 79°N, a distinct and diurnal pattern of depth-dependent bioluminescence associated with zooplankton (diurnal vertical migration, DVM) has been demonstrated to be of particular importance in the upper 50 m of the water column (Berge et al. 2012). In order to investigate which species are actively bioluminescent during the polar night, a high-resolution in situ measurement platform as deployed over a 51-h period in order to measure and count the number of bioluminescence flashes in Kongsfjord, Svalbard, in mid January 2013. Correspondingly, bioluminescent organisms were sampled next to the platform for species-specific bioluminescence characteristics. Documented BL characteristics include maximum, average intensity, duration time until maximum of bioluminescence and BL cumulative sum was reached (see definitions, symbols and units in Table 1). Sampled specimens and bioluminescent taxa were immediately examined in a shipboard aquarium under subdued light. The species-specific bioluminescence characteristics, examined under controlled conditions in the laboratory on board, were related to the in situ measurements and used as an aid to positively identify the species responsible for the in situ bioluminescence.
Table 1

BL kinetic parameters used to discriminate between taxa

Parameter

Explanation

Unit

BLmax

Maximum intensity of BL

×10photons s−1

BLmean

Average BL intensity

×109 photons s−1

Σmax

Cumulative sum of BL0 % until BLmax

×109 photons s−1

Tmax

Time to reach maximum BL

s

Thigh

High intensity duration, BL20 % rise and 20 % decay

s

Tdecay

Time from BL20 % decay to BL0 %

s

The parameters are based on 60 Hz bioluminescence curve kinetics

Materials and methods

Instrumentation

The bathyphotometer (UBAT, Wet Labs, USA) consist of a water inlet and outlet using an impeller to pump the water into a detection chamber equipped with a photon multiplier tube (PMT) counting bioluminescence as photons s−1 after calibration according to Herren et al. (2005). The UBAT flow rate was 0.373 L s−1. The impeller in the detection chamber of the bathyphotometer was used to induce bioluminescence. The controller software (BLINC, Wet Labs) was used as graphic user interface and for control of instrument (inserting calibration coefficient, pump RPM, flow RPM, PMT input/output voltage and raw counts).

The software was used to schedule BL recording times, i.e., schedule for repeating samples and sample length adjusting for battery power needed for 51-h TS at in situ temperatures.

The bathyphotometer provides the measurements as raw 1–60 A/D counts per second that were converted to bioluminescence values (BL, photons s−1) after correction of instrument-specific photomultiplier tube (PMT) calibration coefficient provided by Wet Labs. The BP utilizes an impeller to continuously draw a measured volume of water into a chamber where bioluminescence was measured by the PMT at 60 Hz (see Herren et al. 2005; Berge et al. 2012; Moline et al. 2013 for details). The PMT calibration coefficient was different depending on gain setting.

Taxa-specific bioluminescence: laboratory experiments

The UBAT was used for detecting and characterizing the flash kinetics on living specimens in a laboratory aquarium on board the R/V Helmer Hanssen (University of Tromsø) January 9–21, 2013. The UBAT was connected to the DH4 data handler, logger and power unit (both Wet Labs) with baud rate PC-DH4 set to 115 kHz using the DH4 software. The DH4 was powered with 12 V (input power 12–15 V) and a power cord connection with 12 V was connected from DH4 to UBAT.

In situ collection of zooplankton for onboard laboratory BL work was performed using WP2 zooplankton net (180 μm, 0.25 m2 opening) and Mik-net (1,000 μm, 3 m2 opening) close to the UBAT time series station (in situ temperature ranging from 0.54 to 0.89 °C and salinity 34.62–34.64 (recorded at 1 Hz).

Taxa (still in suspension in net flask) were immediately separated into polyethylene trays and stored in pre-filtered saltwater in a dark cooling room at 2–4 °C before transferred to 50 L aquarium filled with pre-filtered (180 μm) seawater (25 L of pre-washed polyethylene tanks) at in situ temperature. Prior to each specimen examined for BL, new and fresh, pre-filtered seawater at in situ temperature was used. A pre-washed bathyphotometer was submerged into the aquarium and examined species for species.

The bathyphotometer settings were the same for all species. Living specimens were gently put into the aquarium in front of the inlet of the bathyphotometer. The time for each species reaching the detector was noted to relate bioluminescence signal to number and bioluminescence characteristics of specimens. For each species, new and pre-filtered (in situ temperature) saltwater was put into the aquarium prior to experiments. Filtered seawater gave a BLmax (maximum intensity of BL) of 0–2 × 106 photons s−1, indicating BL background signal of in the underwater bathyphotometer (UBAT). For each taxon, the following characteristics according to Table 1 was measured (Figs. 1, 2).
Fig. 1

Species-specific differences in bioluminescence characteristics. a. Graphic presentation of the bioluminescence parameters in Table 1: average BL intensity (BLmean), maximum intensity of BL (BLmax), cumulative sum of BL0 % until BLmaxmax), time to reach maximum BL (Tmax), high intensity duration from 20 % of BL rise and decay level (Thigh), and time from BL20 % decay to BL0 %. Figure modified from Moline et al. (in press). b. Species-specific BL characteristics in M. longa (copepod), the ctenophores M. ovum and B. cucumis, and M. norvegica (krill). Note secondary Y axis for B. cucumis (10–50 X stronger BL intensity than the other species), the others species on primary Y axis. Note X axis include start to end of BL kinetics, numbers indicate BL max intensity

Fig. 2

Interpretation and recognizing in situ BL signatures. a. Indicates BL signature that is produced by more than one taxa (or several individuals of one taxa) shown by several peaks that cannot be recognized as a given taxa. b Represents a clear BL kinetic signature due to one taxa/specimen. The first signature (a) is manually removed from the dataset, while the second one (b) is selected to be recognized to a given taxa

In situ measurements of bioluminescence

An underwater platform consisting of the UBAT and a SBE 49 Fastcat CTD (temperature, salinity and depth, Seabird Electronics, Washington, USA) were deployed 20 m below surface at a location in Kongsfjorden, Svalbard, with a bottom depth of 300 m. The platform was deployed January 15–17, 2013, over a total of 51 h of BL measurements (Figs. 3, 4, 5). The DH4 was used to control the sampling protocol; a programmed warm-up (10 s), a meter flush (20 s), a sampling period of 5 min, with an interval between samples of 10 min, and a low voltage cutoff of 10 V. During the last period of time series, we needed to reduce sampling period and raised the interval between samples to save battery power ensuring that the voltage did not drop below critical voltage (to avoid nonlinear responses in BL measurements). For time series, all BL values are integrated per hour.
Fig. 3

Polar night time series of total species-specific (recognized) BL flashes over 3 days at 20 m depth in Kongsfjorden, Spitsbergen, January 15–17, 2013

Fig. 4

Hourly (integrated values from 3 days) distribution of BL flashes and corresponding recognized fraction of species. From time series presented in Fig. 3

Fig. 5

Sum of measured bioluminescence produced by recognized taxa integrated in 1 h over 3 days (compare with number of flashes in Fig. 3). The total light emitted per recognized taxa indicates that highly bioluminescent species such as B. cucumis and the krill M. norvegica, despite being in low numbers relative to other BL taxa, may contribute significantly to the total bioluminescence produced in the water column during the polar night

In order to assign the BL curves extracted from the time series data to specific taxa, the time series parameters were compared with the taxon-specific parameters (Table 2).
Table 2

Bioluminescence kinetics of the four taxa producing BL in the laboratory using BL kinetic characteristic

BL groups (× 109)

Unit

M. longa

M. norvegica

M. ovum

B. cucumis

Dinoflagellates

BLmax

×109 photons s−1

2.05

10.2

6.64

104

0.32

BLmean

×109 photons s−1

0.25

0.9

0.66

15.5

1.59

Σmax

×109 photons s−1

3.82

19.5

84

1,870

8.39

Tmax

s

0.20

0.27

2.63

1.12

0.051

Thigh

s

0.11

0.12

0.65

1.38

nd

Tdecay

s

0.25

0.48

2.25

3.65

nd

BLmax, maximum intensity of BL; BLmean, average BL intensity; Σmax cumulative sum of BL until maximum intensity is reached; Tmax, time to reach maximum BL; Thigh, high intensity duration, from 20 % rise and 20 % fall; and Tdecay, from 20 % of max to 0 %. Values for dinoflagellates are taken from Moline et al. in press; nd, no data

Taxa-specific BL kinetic signatures

In particular four parameters; maximum bioluminescence (BLmax), time to maximum bioluminescence (Tmax), BL cumulative sum (Σmax) and average bioluminescence (BLmean) provided a BL kinetic signature that could be used to identify the species responsible (Figs. 1, 2; Table 1).

The first step was to automatically identify (see Eqs. 16) and store the BL kinetic signature of the taxa identified in situ (Figs. 3, 4, 5). A manual and visual analysis has been done to eliminate those signatures that were clearly representative of more than one taxa, and therefore difficult to identify and classify (Fig. 2a, b). All the selected data are then further processed and identified. The eliminated data will still take part in the statistical analysis to provide information about the “unidentified data.” The BL kinetic signatures in Fig. 2 has been calculated for all the peaks measured during the time series at 20 m depth (Figs. 3, 4) and compared with the species-specific BL characteristics (Fig. 1; Table 1 elucidated during the laboratory experiments (5 taxa, Table 2). By putting specimens of different taxa into the UBAT, one by one, we detected BL and non-BL zooplankton.

This comparison has been done calculating an error (Eq. 1) that represents an imaginary “distance” between each BL signature and the taxon-specific signatures from the laboratory experiments. The error, \( e_{{{\text{taxa}}_{i} }} \), was calculated as a simple weighted average of the four BL parameters errors:
$$ e_{{{\text{taxa}}_{i} }} = \frac{{w_{1} \cdot e_{{{\text{BL}}_{\hbox{max} } , {\text{taxa}}_{i} }} + w_{2} \cdot e_{{T_{ \hbox{max}} , {\text{taxa}}_{i} }} + w_{3} \cdot e_{{\Sigma_{ \hbox{max} } ,{\text{taxa}}_{i} }}+{w_{4}\cdot e_{{{\text{BL}}_{\text{mean}} ,{\text{taxa}}_{i}}} }}}{{w_{1} + w_{2} + w_{3} + w_{4} }}$$
(1)
where taxai is one of the 5 recognized taxa of interest (Fig. 1; Table 2), w1,…,w4 are the weights of the four parameters errors \( e_{{{\text{BL}}_{ \hbox{max} } , {\text{taxa}}_{i} }} ,e_{{T_{ \hbox{max} } , {\text{taxa}}_{i} }} ,e_{{\Sigma_{ \hbox{max} } , {\text{taxa}}_{i} }} ,e_{{{\text{BL}}_{\text{mean}} , {\text{taxa}}_{i} }} \) defined as (note that the formula is the same for all the parameters):
$$ e_{{{\text{BL}}_{ \hbox{max} } ,{\text{taxa}}_{i} }} = \frac{{\left| {{\text{BL}}_{ \hbox{max} }^{{{\text{in}}\;{\text{situ}}}} - {\text{BL}}_{ \hbox{max} }^{{{\text{lab}},\;{\text{taxa}}_{i} }} } \right|}}{{\left\| {{\text{BL}}_{ \hbox{max} }^{{{\text{in}}\;{\text{situ}}}} ,{\text{BL}}_{ \hbox{max} }^{{{\text{lab}},\;{\text{taxa}}_{i} }} } \right\|_{\infty } }} $$
(2)

Equation 2 is the normalized error between the maximum bioluminescence (BLmax) of the BL kinetic signature of the unknown taxa measured in situ and the parameter of the kinetic BL signature of the taxa measured in laboratory. In this, we considered each parameter to have the same importance (the same weight in Eq. 1), that means: w1,w2,w3,w4 = 1.

After using Eq. 1 (see rewriting of Eq. 1 in Eq. 3 below) together with Eq. 4 for all the 5 taxa (taxai; comprising dinoflagellates, the copepod Metridia longa, the ctenophores Mertensia ovum and Beröe cucumis, and the krill species Meganyctiphanes norvegica), we ended up with five error values for each taxa, each one of them will represent the error recognizing the in situ signature of a specific taxa. Rewriting Eq. 1, we will have (Eq. 3):
$$ e_{{{\text{taxa}}_{i} }} = \frac{{e_{{{\text{BL}}_{ \hbox{max} } ,{\text{taxa}}_{i} }} + e_{{T_{ \hbox{max} } ,{\text{taxa}}_{i} }} + e_{{\Sigma_{ \hbox{max} } ,{\text{taxa}}_{i} }} + e_{{{\text{BL}}_{\text{mean}} ,{\text{taxa}}_{i} }} }}{4} $$
(3)
The taxa providing the minimum recognition value of a given taxa (taxai, Eq. 3) will then recognize the in situ signature as described by Eq. 4:
$$ {\text{taxa}} = {\text{taxa: min}}\left\{ {e_{Metridia} ,\;e_{\text{Beroe}} ,\;e_{\text{Dinoflagellates}} ,\;e_{Mertensia} ,\;e_{\text{krill}} } \right\} $$
(4)

All unclassified flashes have deleted manually (using the approach shown in Fig. 2) from further analysis. The unrecognized BL signatures need further detailed experiments under controlled conditions, but is beyond the scope of this paper.

In the plot, the cumulative sum of BL related to the identified peaks has been integrated over the hours, divided between taxa and compared (Eqs. 56). Unclassified peaks have not been included in Fig. 5, but they will be considered in a further refinement to have a more complete overview about the total amount of light present in a certain hour.

The plotted data in Fig. 5 are the cumulative sum of the whole kinetic signature (from start to end of a BL flash curve defined in Fig. 1a) integrated over 1 h (Eqs. 56; Fig. 5):
$$ \Sigma_{\text{BL}} = \int\limits_{{t : {\text{StartKinSignature}}}}^{{t : {\text{EndKinSignature}}}} {\left( {\text{BL}} \right)\,{\text{d}}t} $$
(5)
$$ \Sigma_{\text{BL, integrated}} = \Sigma_{\text{BL}} \cdot k_{\text{hour}} $$
(6)

The integrating factor khour depends by the amount of sampled minutes over the hour, basically the integrating factor extrapolates the measured data per hour.

Results

Specific-specific characteristics in the laboratory

The four dominant bioluminescent taxa in the laboratory study included (with number of specimens in parentheses) M. longa (12), M. ovum (11), B. cucumis (5) and Meganychtiphanes norvegica (7), all of which were collected and identified from samples taken next to the in situ platform. All bioluminescent species (BL) gave BLmax ranging from 2 to 100 × 109 photons s−1. Bioluminescence characteristics from monocultures of these were measured according to the following BL characteristics by means of BL maximum value, average value, maximum value time and rising time (see Fig. 1a; Table 2 for details).

Seven taxa were found to be non-bioluminescent in this study (number of individuals in parentheses): The pelagic amphipods Themisto libellula (n = 14) and T. abyssorum (n = 8), the arrow worms Parasagitta elegans (n = 15) and Eukrohnia hamata (n = 15), the calanoid copepod Calanus glacialis (n > 100), the krill Thysanoessa sp. (n = 50), and the pteropod Clione limacina (14).

These species gave a BL signal up to 3 × 106 photons s−1, i.e., equivalent to the background signal of filtered water. In contrast, the BLmax values for the true bioluminescent taxa ranged from 2–10 × 109 photons s−1, 1,000 times the background signal.

Identification of in situ bioluminescence peaks

Based upon the taxon-specific bioluminescence characteristics (see Fig. 1; Table 2), five identified taxa were identified as active throughout the period. In total, more than 50 % of the peaks could unequivocally be assigned as being produced by M. longa, whereas dinoflagellates accounted for one-third of all identified peaks. The ctenophore B. cucumis, although numerically the least dominant, had a BL signal one order of magnitude stronger than any of the other taxa (Lapota et al. 1992a, b).

The total BL signal from the zooplankton community was measured in situ during a 51-h deployment of the bathyphotometer at 20 m depth (Figs. 2, 3, 5), covering three noon and two midnight periods. The variation in total number of measured peaks varied throughout the sampling period, no clear diurnal signal could be detected.

Discussion

A total of 2,981 BL flashes were detected during the 51-h time series. Two thousand seven hundred and fifteen different BL peaks were identified, based on the species-specific BL characteristics (see below) comprising M. ovum (20 flashes); M. norvegica (286 flashes), B. cucumis (30 flashes), M. longa (1,344 flashes) and dinoflagellates (1,031 flashes), see Fig. 2. During the second part of the deployment (January 16–17), at total of 266 were identified; M. ovum (10), M. norvegica (44), B. cucumis (6), M. longa (121) and dinoflagellates (81), Fig. 2. The latter group was identified by the bioluminescent characteristics of dinoflagellates (Table 1; Fig. 1).

Identification of biolum taxa based on the laboratory measurements

Time series of taxa-specific bioluminescent zooplankton was identified by means of the laboratory-based measurements of living specimens identified in Table 2. In situ BL zooplankton was dominated by M. longa with about 50 % of total bioluminescent flashes for both January 15–16 and 16–17, 2013. The second dominant BL group was the dinoflagellates with about 25–30 % of BL, followed by bioluminescent krill M. norvegica, and the two ctenophores M. ovum and B. cucumis (Table 3; Figs. 3, 4, 5). In contrast to other bioluminescent organism, B. cucumis gave green–yellow emission in contrast to the other BL species which gave a bright blue emission (seen by eye). All species gave a similar shape bioluminescent curves with smooth rise and decay characteristics, except for a jagged curve from B. cucumis (Fig. 1b). The jagged curvature was caused by pulsating light through the bell-shaped animal giving varying BLmax through the measurements at 60 Hz (Fig. 1). Note that B. cucumis was virtually absent at 20 m depth at midnight, but could be quite numerous around noon (see noon day 3, Fig. 4). If total bioluminescence contribution is taken into consideration, highly BL taxa such as B. cucumis and M. norvegica may be a significant contributor to “light in the dark” (Fig. 5).
Table 3

Major bioluminescent taxa during TS measurements at 20 m depth in Kongsfjorden

Taxa

15–16 January specimens (% of total)a

16–17 January specimens (% of total)b

Dinoflagellates

1,031 (38)

81 (31)

Copepod (M. longa)

1,344 (49)

121 (46)

Krill (M. norvegica)

286 (11)

44 (17)

Ctenophore 1 (M. ovum)

20 (0.7)

10 (3.8)

Ctenophore 2 (B. cucumis)

30 (1.3)

6 (2.2)

Total specimens

2,711 (100)

262 (100)

aJanuary 15–16, 2013, and b January 16–17, 2013. In situ temperature 0.54–0.89 °C

The bioluminescent fraction of the zooplankton community has previously been examined from the same site and at the same time of year, but using a different method deployed herein. Berge et al. (2012) reported on the bioluminescence measured by the same UBAT mounted on an AUV, concluding that bioluminescent dinoflagellates were conducting vertical migrations within the upper 30 m of the water column. Later, Moline et al. (in press) reanalyzed the same dataset and distinguished three main clusters of flashes, arguing that they represented three different groups of bioluminescent taxa. The BL flash kinetics from dinoflagellates (data from Kongsfjorden in January 2010) belongs the low-intensity BLmax group called G1 (Lapota et al. 1992a, b) which was the largest BL group recorded in these waters during polar night. Two other BL groups were recorded (BL group G2 and G3) in Moline et al. (in press), but these groups were not identified. In Table 3, BLmax indicates that B. cucumis can be put into BL G3, and the rest in BL group G2. However, Moline et al. (in press) also identified two other clusters, named group 1 and 2, respectively. Based on the laboratory-controlled bioluminescence characteristics of four other taxa defined herein (Table 2), we conclude that the group 3 in Moline et al. (in press) most likely represent B. cucumis. Especially the BLmax and BLmean correspond with those herein described as characteristic of this large and common ctenophore (Majaneva et al. 2013). The second group (Group 2), however, does not unequivocally correspond to any of the four taxa characterized in Table 2, although the high Σmax might indicate that this group is also a ctenophore—the smaller but more numerous M. ovum

In conclusion, we argue that the flash kinetics of bioluminescent zooplankton is a useful and easy way of characterizing zooplankton communities, particularly so at high latitudes during the otherwise challenging winter conditions. In general, bioluminescence of arctic zooplankton is in itself a poorly studied topic, one that may provide new and vital information concerning both ecological interactions and physical forcing of biological processes during the arctic winter. Specifically, our study demonstrates that the bioluminescence flash kinetics of arctic zooplankton has clear species-specific characteristics that allow for in situ identification of species.

Notes

Acknowledgments

The work is part of the two NFR projects Circa (Project Number 214271/F20) and Marine Night (Project Number 226417/E10). Furthermore, the work was supported by the CoE AMOS at NTNU (NFR 223254). Thanks are given two three anonymous reviewers for constructive comments.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Geir Johnsen
    • 1
    • 2
  • Mauro Candeloro
    • 3
  • Jørgen Berge
    • 2
    • 4
  • Mark Moline
    • 5
  1. 1.Applied Underwater Robotics Laboratory, Department of BiologyNorwegian University of Technology and Science (NTNU)TrondheimNorway
  2. 2.Department of Arctic BiologyUniversity Centre on Svalbard (UNIS)LongyearbyenNorway
  3. 3.Applied Underwater Robotics Laboratory, Department of Marine TechnologyNorwegian University of Technology and Science (NTNU)TrondheimNorway
  4. 4.Faculty of Biosciences, Fisheries and Economy, Institute of Arctic and Marine BiologyUniversity of TromsøTromsøNorway
  5. 5.School of Marine Science and PolicyUniversity of DelawareNewarkUSA

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