Abstract

Light-dependent behavior of the abundant zooplankton species inhabiting the White Sea were studied experimentally during: (i) the spring equinox (March); (ii) the polar day (late May to June), (iii) August, 17/7 h day–night light cycle, (iv) the fall equinox (October). Behavioral patterns were investigated for eight species of Copepoda (Metridia longa, Calanus glacialis, Pseudocalanus minutus, Oithona similis, Oncaea borealis, Temora longicornis, Centropages hamatus, Acartia spp.), one Cladocera species (Evadne nordmanni) and Polychaeta larvae. The hypothesis was tested that attraction to (or repulsion from) light is the primary mechanism involved in the vertical migration of zooplankton with different trophic characteristics in relation to phytoplankton-rich upper water layer. The impact of red (680 nm), yellow (560 nm) and UV (280 nm) light was tested. The animals were acclimated to two food conditions: natural seawater (satiated) and filtered (1 µm) seawater (hungry). The positive light response of predominantly herbivorous and omnivorous copepods and cladocerans inhabiting the photic water layer corresponds with their distribution and their food vertical distribution. Hungry animals display the strongest responses to light. Light effects on behavior were weak in deep-dwelling O. borealis. We suggest that red and yellow light is an indicator of the photic layer (high food concentration) to zooplankton groups that feed on phytoplankton. In contrast, diapausing (e.g. non-feeding) copepods totally avoid light, especially when they hibernate in the aphotic layer. We hypothesize that there is a relationship between the light response of the zooplankton, their trophic characteristics, migration behavior (diel and ontogenetic) and the water layer occupied.

INTRODUCTION

It is widely accepted that light plays an important role in the behavior of pelagic animals (Forward, 1988). Numerous plankton species, particularly copepods and cladocerans, have both diel and ontogenetic vertical migrations (Leech and Johnsen, 2003). Diel vertical migrations involve daily changes in vertical distribution of plankton. Ontogenetic vertical migrations involve seasonal and life history specific changes in their distribution. The latter are characteristic of many high-latitude species, especially the genus Calanus. These animals actively feed and reproduce in the surface water layers in spring but move down to deeper layers to hibernate during the long winter period (Conover and Huntley, 1991). Ontogenetic migrations are thought to be governed by factors other than light. However, light is a major trigger of diel vertical migrations.

It has long been known that light may regulate animal behavior, and many zooplankton are light-dependent (Clarke, 1934; Duval and Geen, 1974; Pagano et al., 1993; Atkinson et al., 1996). Ultraviolet (UV) radiation, especially with a wavelength of 280 to 315 nm, negatively affects many zooplankton species (Hunter et al., 1981; Kouwenberg et al., 1999). Some animals, for example, larvae of Coregonidае fishes, use skin pigmentation and avoidance behavior to protect themselves against UV radiation (Yloёnen et al., 2005). Larvae of some marine benthic animals and deep-dwelling shrimp species escape the negative impact of UV radiation by migrations (Frank and Widder, 1994; Adams, 2001). Copepod (Martin et al., 2000; Rhode et al., 2001) and cladoceran (Johnsen and Widder, 2001) species avoid UV stress by vertical migrations. Some crustaceans have evolved biochemical methods of avoiding the UV-induced stress, including pigmentation (Rhode et al., 2001); more colored shrimps tend to occur in deeper water layers (Vestheim and Kaartvedt, 2009). Different responses of Cladoceran species to UV exposure in various freshwater lakes have been documented (Leech and Williamson, 2000; Leech et al., 2005).

Unfortunately, most publications on light-dependent behavior of zooplankton involve freshwater species. Almost nothing is known about the effect of visible light on marine zooplankton. Because most of these animals are transparent, a significant impact of UV-induced stress may be expected. There are currently few publications on behavioral responses of zooplankton to different light wavelengths. Evidence for color vision has been found in some Crustaceans (Stomatopoda) (Marshall et al., 1996). However, it is still unknown if other groups can distinguish different wavelengths (Menzel, 1979; Frank and Case, 1988), except for a single publication by Forward and Cronin (Forward and Cronin, 1979).

On the other hand, many investigators discuss vertical migration of zooplankton in close relationships with their diel feeding rhythms. Possible interrelations between the diel feeding patterns, the light dynamics and the migrations for these animals have been analyzed, but only in the field (Bautista et al., 1988; Atkinson et al., 1992, 1996; Pagano et al., 1993; Øresland, 2000). The most recent publications involve experiments on freshwater organisms, usually Cladocera (Stutzman, 2000; Leech and Williamson, 2001; Boeing et al., 2004; Fischer et al., 2006), and almost nothing is known about the response of marine copepods, maintained in various food environments, to different light conditions (Karanas et al., 1979). The intensity of UV light is assumed to decrease in a very upper layer of the water column, whereas red and yellow light may penetrate deeper down to 20 m depth (Jerlov, 1976; Burenkov et al., 2004). We assume that these two wavelengths may become a sign of the 'upper' and 'lower' borders of the photic layer for the organisms. Thus, it is interesting to compare the impact of these wavelengths separately on the zooplankton behavior, because UV light is proposed to have damaging effect, and visible light does not.

It is known that the feeding rhythmicity of zooplankton is intimately linked with the diurnal distribution of their populations, with some minor exceptions (Pasternak, 1995; Wang et al., 1998; Torgersen, 2003). The diurnal feeding rhythms are also pronounced at the physiological level. For example, the tissue morphology of the gut in Acartia tonsa changes during the day (Hassett and Blades-Eckelbarger, 1995). Also chemical factors may affect the diurnal vertical migrations of zooplankton: for example, daphnids exhibit a clear avoidance of kairomones from some predatory fish (Loose et al., 1993). Other chemical factors of migrations also include the destructive effects of reactive oxygen species caused by UV light (Holm-Hansen et al., 1993). Furthermore, many species of phytoplankton synthesize both attractive and repellent substances for the zooplankton (Chaudron et al., 1996; Dutz, 1998; Ianora et al., 1999; Miralto et al., 1999). Some authors suggest visual predator pressure as one of the major factors controlling downwards migrations of zooplankton during daylight (Gliwicz and Pijanowska, 1988; Bollens and Frost, 1989; Neill, 1990; Bollens et al., 1993; Loose and Dawidowicz, 1994). However, diel vertical migrations may be observed in the high latitudes during polar day independently of the light regime (Fortier et al., 2001), or the copepods may stop migrating altogether (Blachowiak-Samolyk et al., 2006). It is obvious that the diurnal distribution patterns are crucial for many of the crustaceans that inhabit the upper water layers and are susceptible to light, predators and various chemical factors.

The White Sea, situated near to the North Polar Circle, shares many characteristics with other polar seas but is unique in a number of features (Berger et al., 2001). In the summertime, it has two pronounced water layers, separated by the thermocline. The upper layer, extending 15–50 m in depth, is the productive area, and can warm up to 18°C on the surface. The water masses situated under the thermocline are characterized by low productivity and temperatures below 0 Celsius. The UVB radiation in the White Sea does not penetrate to a depth of more than 3 m, whereas yellow light of 560 nm has relatively low extinction coefficient comparing to UVB light and goes down to 15–20 m depth (Burenkov et al., 2004). Diel patterns of vertical distribution of certain copepod species have been described previously (Bogorov, 1946; Pertzova, 1997), but these authors did not arrive at the same conclusions. All the data on vertical distribution and diel vertical migrations of calanoids inhabiting the White Sea are predominantly published in Russian and are extremely outdated. There are no data on the effects of light on the behavior of White Sea zooplankton, and the driving factors of the diel vertical migrations are still open. This study is the first to distinguish experimentally the differences in the behavioral responses to specific light wavelengths for major White Sea zooplankton species in relation to their feeding, vertical distribution, biogeography and life cycle. Our main approach involved the choice between darkness and light (UV or visible, red and yellow) of the intensity close to natural. Thus, it was possible to test the hypothesis that these wavelengths indicate the layer of optimal food availability especially for herbivorous and migrating animals.

METHOD

Sampling

Fifty-two experiments were performed to investigate the light-dependent behavior of the abundant zooplankton species in different seasons during 2005–2006: (i) the spring equinox, 12/12 h day–night light pattern (ice coverage, end of March); and three times through the ice free season; (ii) the polar day, 22/2 h day–night (late May–June), (iii) 17/7 h day–night (middle August), (iv) the fall equinox, 11/13 h day–night (beginning of October). The day length was defined as a period between the sunrise and sunset according to the ephemeris. Zooplankton sampling was performed close to the Cape Kartesh (Kandalaksha Bay, the White Sea, 66°20.2 N; 33°38.9 E, 65 m depth) and in the innermost part of Chupa Bay (Kandalaksha Bay, the White Sea, 66°20.0 N; 33°37.7 E, 30 m depth). Zooplankton was sampled by means of a Juday net (37 cm diameter, 100 µm mesh) using standard techniques (Harris et al., 2000). The water column was divided into two sampling layers: (i) photic, 0–15 m, (ii) aphotic, 15 m to bottom, according to Burenkov et al. (Burenkov et al., 2004). The animals were collected during the day (about midday in the period of maximum light intensity), because the light impact (vertical distribution) is more pronounced during the daylight (see review, Mauchline, 1998). Temperature measurements were performed with a MIDAS CTD with 0.1°C accuracy through the 0–15 m water layer at the vicinity of zooplankton sampling sites. Light intensity measurements were performed simultaneously in the water column at 0, 5, 10 and 15 m depth by means of illuminometer U-116 (Russian analog to FX-200 Illuminometer). We have chosen the light intensity of 5 m depth (about 30 lux) as experimental, because it constituted about 10% of light intensity for the red light observed at the surface (Jerlov, 1976), and varied as 300 to 600 lux. Sampled zooplankton were gently diluted with seawater, placed in a dark container and immediately transported to the shore laboratory.

Acclimation of zooplankton

Live animals were sorted by species and developmental stages under the dissecting microscope (total magnification ×40) and then acclimated to either total darkness or visible 'scattered sunlight' (UV and IR radiation reduced, 30 lux intensity, LED white lamps), during 24, 48, 72 or 96 h in temperature conditions similar to natural. The animals were also kept under two different food conditions: (i) natural seawater was collected according to the zooplankton sampling by 5-l Niskin bottle close to surface and (ii) filtered seawater (GF/C fiber glass filters, 1 µm). We tested if the length of the light/food acclimation period might increase/decrease the light response of the animals and also tried to find the 'critical' time period for such increase/decrease. The acclimation of animals and further experiments were conducted at the temperature similar to natural (the temperature of zooplankton sampling depth) to avoid temperature-induced stress. The light-dependent behavior of 10 zooplankton species was investigated (eight species of Copepoda (Metridia longa, Calanus glacialis, Pseudocalanus minutus, Oithona similis, Oncaea borealis, Temora longicornis, Centropages hamatus, Acartia spp.), one Cladocera species (Evadne nordmanni) and Polychaeta larvae. The number of specimens used in each experiment ranged from 28 to 500 individuals and was size-dependent.

Experimental chamber

The experimental chamber was made of transparent plastic, 50 × 250 × 50 (W:L:H) mm, the central part (50 × 50 mm) could be isolated by means of sliding 'doors' (Fig. 1). The experimental chamber was filled with natural seawater of specific temperature. The depth of the water layer was 5 to 7 mm, and as the animals ranged in body length from 0.1 to 2.2 mm, vertical movements were impossible. Therefore, gravitation-induced movements were excluded. All the experiments were performed during the daytime from 10.00 to 16.00, to exclude the diurnal rhythm factor. We used small fluorescent UVB lamps UF-19 (Russian analog to PHILIPS 9 Watt Short Compact Fluorescent UVB Narrowband PL-S9W/01) and red and yellow LED lamps as a light source in the experiment. The UV light is scattered in the very upper water layers of 1–2 m, and the red and yellow light penetrates deeper down to 20 m depth (Ahlquist, 1965, cited under Jerlov, 1976), so we assume these two wavelengths may indicate the upper and lower boundaries of the photic layer for the plankton. The light intensity was regulated by a dimmer and set up accordingly to illuminometer values.

Fig. 1.

Scheme of the experimental chamber (plan view).

Fig. 1.

Scheme of the experimental chamber (plan view).

Experiments

The light patch of 15 mm diameter and of about 30 lux intensity (similar to 5 m depth at midday) was created by an iris aperture and was applied evenly to the left and the right part of the experimental chamber, 10 replicates each, to exclude any factor of chamber position. Animals, using a new sub-sample each time, were gently placed via Pasteur pipette in the center of the experimental chamber with open 'doors'. The duration of the experiment was 10 min, then the 'doors' were closed, animals were taken from each part ('light', 'center' and 'dark’) separately by Pasteur pipette and counted under a dissection microscope (magnification ×40). A minimum of 20 replications with new animals each time was performed for each experimental series.

Analysis

The Student t-test was used to assess the significance of the differences between means. The differences between the animal responses to red and yellow light were not significant and therefore they were combined (red and yellow). Primary data were normalized via arc tg root transformation (Sokal and Rohlf, 1995). These values were used later in ANOVA to analyze the effects of such factors as acclimation duration, light wavelength, sampling depth and food conditions. If the animals distributed evenly in the experimental chamber and no significant differences were found in their relative abundance in the chamber parts, we assumed that no phototaxis occurred. All the zooplankton sampling and thus experiments for each season were conducted within a 7–10 days period. The datasets were combined on each species for certain season, water layer occupied, light wavelength and acclimation period and food/light acclimation pattern. Animals were divided by (i) trophic characteristic into 'herbivorous' and 'non-herbivorous' and (ii) biogeographical distribution as arctic, boreal and eurybiont species (Table I). The designation 'herbivorous' in this study includes those animals with algae in their diet, so this group united herbivorous, as well as predominantly herbivorous and omnivorous. Others were treated as non-herbivorous. Heterogeneity of the variances was tested with the Levene test.

Table I:

Light-induced (red and yellow visible light, 560–680 nm) behavioral responses of investigated zooplankton species inhabiting the White Sea

        Significance of duration of light acclimation to light response intensification, P
 
Species and their biogeographical characteristic Season Feeding preferences Developmental stage Water layer Light response Significance of light response, P Significance of starvation acclimation to light response intensification, P Darkness Light 
Acartia spp., boreal August Omnivore CI-CV Photic ** 0.051 
 −/− CVI −/− ** 0.06 
October −/− CI-CVI −/− ** 0.14 0.64 0.10 
Centropages hamatus, boreal August −/− CI-CV −/− ** ** 0.75 0.65 
 −/− CVI −/− − ** 0.07 0.79 0.23 
October −/− CVI −/− − ** 0.17 0.42 0.14 
 −/− CI-CV −/− ** 0.34 0.55 0.17 
Temora longicornis, boreal May −/− CI-CIII −/− ** No data 0.15 
August Predominantly herbivore Np −/− ** 0.08 0.25 
 Omnivore CVI −/− − ** ** ** 0.25 
 −/− CI-CV −/− ** ** ** 0.15 
October −/− CIV-CV −/− ** 0.23 0.65 0.12 
 −/− CIV-CV −/− − ** 0.43 0.77 0.23 
Calanus glacialis, arctic May Predominantly herbivore Np −/− ** No data ** 0.15 
August −/− CIV aphotic − ** 0.35 0.41 0.50 
Metridia longa, arctic October Omnivore CIV-CV −/− − ** 0.65 0.12 0.16 
Oncaea borealis, arctic March CI-CV photic ** 0.23 0.46 0.67 
 CI-CV aphotic ** 0.44 0.89 0.88 
August CVI −/− ** 0.56 0.45 0.33 
October CVI photic 0.55 0.45 0.53 
Evadne nordmanni, boreal August Predominantly herbivore? CI-CVI −/− ** 0.78 0.32 0.98 
Polychaeta, various May larvae −/− ** No data 0.93 0.82 
Oithona similis, eurybiont March CI-CVI −/− ** No data 0.83 0.70 
 CI-CVI aphotic ** No data 0.96 0.98 
May CI-CV photic ** No data ** 0.34 
August CI-CV −/− ** ** ** 0.55 
 CVI aphotic ** No data 0.21 0.46 
 CI-CV −/− ** No data 0.44 
October CI-CVI photic No data 0.66 0.52 
Pseudоcalanus minutus, arctic March Predominantly herbivore CV-CVI photic + aphotic ** ** No data No data 
May Herbivore Np photic ** No data ** 0.34 
 −/− CI-CII −/− ** No data ** 0.36 
 −/− CIII aphotic − ** No data 0.14 0.12 
 −/− CIII −/− ** No data 0.34 0.78 
 Predominantly herbivore CIV −/− ** 0.87 0.45 
 −/− CIV −/− − ** 0.12 0.42 0.76 
 −/− CV −/− ** 0.45 0.24 0.46 
 −/− CV −/− − ** 0.77 0.54 0.44 
August Herbivore CIII −/− ** ** ** 0.15 
 −/− CIII −/− − ** 0.50 0.17 
 Predominantly herbivore CIV −/− ** ** ** 0.17 
 −/− CIV −/− − 0.57 0.65 0.34 
 −/− CV −/− ** ** ** 0.33 
 −/− CV −/− − ** 0.35 0.41 0.20 
October −/− CIV −/− − 0.10 0.32 0.42 
 −/− CV −/− − ** 0.73 0.55 0.09 
        Significance of duration of light acclimation to light response intensification, P
 
Species and their biogeographical characteristic Season Feeding preferences Developmental stage Water layer Light response Significance of light response, P Significance of starvation acclimation to light response intensification, P Darkness Light 
Acartia spp., boreal August Omnivore CI-CV Photic ** 0.051 
 −/− CVI −/− ** 0.06 
October −/− CI-CVI −/− ** 0.14 0.64 0.10 
Centropages hamatus, boreal August −/− CI-CV −/− ** ** 0.75 0.65 
 −/− CVI −/− − ** 0.07 0.79 0.23 
October −/− CVI −/− − ** 0.17 0.42 0.14 
 −/− CI-CV −/− ** 0.34 0.55 0.17 
Temora longicornis, boreal May −/− CI-CIII −/− ** No data 0.15 
August Predominantly herbivore Np −/− ** 0.08 0.25 
 Omnivore CVI −/− − ** ** ** 0.25 
 −/− CI-CV −/− ** ** ** 0.15 
October −/− CIV-CV −/− ** 0.23 0.65 0.12 
 −/− CIV-CV −/− − ** 0.43 0.77 0.23 
Calanus glacialis, arctic May Predominantly herbivore Np −/− ** No data ** 0.15 
August −/− CIV aphotic − ** 0.35 0.41 0.50 
Metridia longa, arctic October Omnivore CIV-CV −/− − ** 0.65 0.12 0.16 
Oncaea borealis, arctic March CI-CV photic ** 0.23 0.46 0.67 
 CI-CV aphotic ** 0.44 0.89 0.88 
August CVI −/− ** 0.56 0.45 0.33 
October CVI photic 0.55 0.45 0.53 
Evadne nordmanni, boreal August Predominantly herbivore? CI-CVI −/− ** 0.78 0.32 0.98 
Polychaeta, various May larvae −/− ** No data 0.93 0.82 
Oithona similis, eurybiont March CI-CVI −/− ** No data 0.83 0.70 
 CI-CVI aphotic ** No data 0.96 0.98 
May CI-CV photic ** No data ** 0.34 
August CI-CV −/− ** ** ** 0.55 
 CVI aphotic ** No data 0.21 0.46 
 CI-CV −/− ** No data 0.44 
October CI-CVI photic No data 0.66 0.52 
Pseudоcalanus minutus, arctic March Predominantly herbivore CV-CVI photic + aphotic ** ** No data No data 
May Herbivore Np photic ** No data ** 0.34 
 −/− CI-CII −/− ** No data ** 0.36 
 −/− CIII aphotic − ** No data 0.14 0.12 
 −/− CIII −/− ** No data 0.34 0.78 
 Predominantly herbivore CIV −/− ** 0.87 0.45 
 −/− CIV −/− − ** 0.12 0.42 0.76 
 −/− CV −/− ** 0.45 0.24 0.46 
 −/− CV −/− − ** 0.77 0.54 0.44 
August Herbivore CIII −/− ** ** ** 0.15 
 −/− CIII −/− − ** 0.50 0.17 
 Predominantly herbivore CIV −/− ** ** ** 0.17 
 −/− CIV −/− − 0.57 0.65 0.34 
 −/− CV −/− ** ** ** 0.33 
 −/− CV −/− − ** 0.35 0.41 0.20 
October −/− CIV −/− − 0.10 0.32 0.42 
 −/− CV −/− − ** 0.73 0.55 0.09 

**P < 0.01; *P < 0.05. Np, naupliar stages; СI-CV, young and pre-mature copepodites; CVI, mature copepodites. Phototaxis (light response) pattern: +, positive; −, negative; 0, indifferent.

RESULTS

Vertical distribution of zooplankton species: temperature preferences

The distribution of the species in the photic layer differs from season to season (Fig. 2). We treated the spring and autumn equinoxes and the polar day as the season of both cold photic and aphotic layers according to the temperature profiles (Fig. 2). No pronounced thermocline was observed in this period and the temperature in the whole water column was only several degrees above 0 Celsius (autumn equinox) or even below (the spring equinox and polar day). The summer period (August) was characterized by a well-pronounced thermocline, and thus we treated this as a period with warm photic and cold aphotic layers. Vertical species distribution significantly differs depending on the temperature of the water layer (Fig. 2). The minor impact of boreal species in the period of cold photic layer is the result of their decreasing presence in the autumn.

Fig. 2.

The vertical distribution pattern of the species and temperature profiles. The pie charts indicate the contribution of each biogeographical group to total species numbers.

Fig. 2.

The vertical distribution pattern of the species and temperature profiles. The pie charts indicate the contribution of each biogeographical group to total species numbers.

Responses of zooplankton species to red and yellow (560–680 nm, RY) light

Various acclimation designs did not affect the phototactic reaction. Zooplankton response either stayed unchanged or become more intense. Thus, we further refer to either significant intensification or no effect of acclimation on light response.

Eurybiont species

Polychaeta larvae representing different biogeographical groups were combined since they displayed no significant differences in light response [ANOVA: F(1, 60) = 0.53; P = 0.45]. Polychaete larvae were abundant only in the spring (May) in the photic layer soon after the ice melting and all showed positive phototaxis (Fig. 3a). However, their light response was not affected significantly by the duration or light conditions of acclimation (Table I).

Fig. 3.

The distribution pattern of the animals in the experimental chamber: (a) Polychaeta larvae, May; (b) non-mature copepodites of Oithona similis, August; (c) naupliar and young (CI-CIII) copepodite stages of Temora longicornis, early June; (d) CIV-CV copepodites of T. longicornis, October; (e) naupliar stages of Calanus glacialis, May; (f) CIV copepodites of Мetridia longa, October; (g) Pseudocalanus minutus naupliar stages, May; (h) P. minutus CI-CII copepodite stages, early June; (i) P. minutus CIII copepodite stages, early June. Vertical bars represent the standard deviation (σ, P < 0.05).

Fig. 3.

The distribution pattern of the animals in the experimental chamber: (a) Polychaeta larvae, May; (b) non-mature copepodites of Oithona similis, August; (c) naupliar and young (CI-CIII) copepodite stages of Temora longicornis, early June; (d) CIV-CV copepodites of T. longicornis, October; (e) naupliar stages of Calanus glacialis, May; (f) CIV copepodites of Мetridia longa, October; (g) Pseudocalanus minutus naupliar stages, May; (h) P. minutus CI-CII copepodite stages, early June; (i) P. minutus CIII copepodite stages, early June. Vertical bars represent the standard deviation (σ, P < 0.05).

The eurybiont cosmopolitan species O. similis, inhabiting the whole water column in the White Sea, displayed a clear, positive response to light, which was more pronounced after prolonged acclimation of these animals in darkness in May and August (Fig. 3b and Table I). The specimens, sampled in the periods of spring and autumn equinox, were also positively phototactic, but were indifferent to any of the acclimation factors applied. Mature copepodites, sampled in the aphotic layer in August, showed no significant intensification of the phototactic reaction after acclimation in both light and dark conditions (Table I).

Boreal species

Positive phototaxis was characteristic of the cladoceran E. nordmanni, inhabiting the surface layer during the summer. Meantime, there were no significant effects of the duration or light conditions of acclimation on the responses of the animals to light (Table I), as was observed for Polychaeta larvae. Keeping animals without food also did not intensify the light response.

Neritic copepod species (Acartia spp., T. longicornis, C. hamatus), which also dominated in the photic layer in summer time, had a different response pattern to RY light. Pre-mature developmental stages of Acartia spp. tended to increase their positive light responses after 48 h of acclimation both in total darkness and in light in August. Individuals of the last generation (October) also had positive phototaxis, but their behavioral responses to the RY light were not significantly different after being kept under various acclimation environments. In contrast to Acartia, immature copepods (August) and mature females (October) of C. hamatus displayed pronounced negative phototaxis after 48 h acclimation in different light conditions (Table I). At the end of September to the beginning of October, immature individuals of this species were characterized by positive phototaxis, but the effects of the duration and light conditions of acclimation were not significant. Temora longicornis also had a different pattern of response. During the polar day period (May–June) naupliar and immature copepods had strong positive phototaxis (Fig. 3c), which increased significantly in agreement suggest with the acclimation duration. Maintaining the animals in darkness increased the positive light response, but this tendency was much less pronounced after a 48 h acclimation period. In October, different conspecifics either preferred or avoided light, while few individuals were left in the middle chamber (Fig. 3d). Significant differences in light responses were also found between mature and immature specimens (Table I). However, effects of various acclimation factors were insignificant.

Arctic species

Mature O. borealis did not display any significant responses to the RY during spring and autumn equinox and polar day period (early June). This was true for copepods from both photic and aphotic layers (Table I).

Naupliar stages of a large Arctic copepod species C. glacialis inhabiting the upper water layer in May exhibited strong positive response to light (Fig. 3e), which increased after the animals were kept in darkness for 48 h. In contrast, CIV copepodites, inhabiting the aphotic layer in August, avoided light during the experiment, even after 48 h acclimation in light. The same developmental stages of another Arctic species M. longa, inhabiting the aphotic layer, had almost identical light behavior in October (Fig. 3f and Table I).

Pseudocalanus minutus was characterized by the most pronounced variability of light-dependent behavior. Their naupliar stages, inhabiting the photic layer in May, showed strong positive phototaxis (Fig. 3g), which increased after animals were kept in darkness. The same was observed for CI and CII copepodites that dominated in the upper water layer in June (Fig. 3h). CIII copepodites of the studied species, sampled from the aphotic layer, formed two distinct groups by their photobehavior (Fig. 3i). The most numerous group was characterized by positive phototaxis, the other individuals displayed negative phototaxis. The same pattern was observed in August (Table I). CIV copepodites inhabiting the deep (aphotic) water layer in early June also divided into two groups, but the 48 h acclimation period without food supply increased the number of individuals with positive phototaxis. In October, this developmental stage showed negative light-dependent behavior, and no significant effect of the acclimation environment was found. The CV copepodites from the aphotic water layer had the same pattern of photobehavior as CIII and CIV, both in early June and August, divided into two groups. Additionally, as in CIV copepodites, the acclimation environment did not significantly affect their responses to light for the group of negative phototaxis. In the spring equinox, CV copepodites and adults were equally distributed in through the water column. They exhibited positive phototaxis, which was more pronounced after 24 h of starvation (Table I).

Combining all the data, we tried to find a regular pattern in the relationships between trophic and biogeographical status, vertical distribution and light response of the studied species. As can be seen in Fig. 4a, more than a half of all the studied species were quite sensitive to the RY light. Moreover, most of them are herbivorous species. Almost all boreal herbivorous species present in the photic layer during the warm period have positive phototaxis (Fig. 4b). However, this pattern changes slightly for the Arctic herbivores, which could include up to 40% indifferent to and light avoiding.

Fig. 4.

The vertical distribution of the species, % of total species number, of different food, temperature and light preferences in the photic and aphotic layers: (a) all the species; (b) only herbivorous. Phototaxis (light response) pattern: +, positive; −, negative; 0, indifferent.

Fig. 4.

The vertical distribution of the species, % of total species number, of different food, temperature and light preferences in the photic and aphotic layers: (a) all the species; (b) only herbivorous. Phototaxis (light response) pattern: +, positive; −, negative; 0, indifferent.

The UV effect on the light response

Three species were tested, Acartia spp. (boreal, omnivorous), P. minutus (arctic, predominantly herbivorous) and O. borealis (arctic, with unknown food preferences). Acartia spp. (photic layer) and P. minutus (aphotic layer) showed positive phototaxis in August (Table II). Mature and older copepodites (CIV-CV) of P. minutus increased their positive response to the UV light after 24 h acclimation to red light. The same was observed for mature females of Acartia spp.

Table II:

Light-induced (UV, 280 nm) behavioral responses of investigated zooplankton species inhabiting the White Sea

        Significance of duration of light acclimation to light response intensification, P
 
Species and their biogeographical characteristic Season Feeding preferences Developmental stage Water layer Light response Significance of light response, P Significance of starvation acclimation to light response intensification, P Darkness Light 
Acartia spp., boreal August Omnivore CI-CVI Photic ** No data ** 
Pseudоcalanus minutus, arctic March Predominantly herbivore CIII-CV −/− ** 0.38 0.52 
 −/− CIII-CV Aphotic ** 0.34 0.23 
August −/− CIV-CVI −/− ** No data ** 
Oncaea borealis, arctic March CI-CVI −/− ** 0.54 0.62 0.45 
        Significance of duration of light acclimation to light response intensification, P
 
Species and their biogeographical characteristic Season Feeding preferences Developmental stage Water layer Light response Significance of light response, P Significance of starvation acclimation to light response intensification, P Darkness Light 
Acartia spp., boreal August Omnivore CI-CVI Photic ** No data ** 
Pseudоcalanus minutus, arctic March Predominantly herbivore CIII-CV −/− ** 0.38 0.52 
 −/− CIII-CV Aphotic ** 0.34 0.23 
August −/− CIV-CVI −/− ** No data ** 
Oncaea borealis, arctic March CI-CVI −/− ** 0.54 0.62 0.45 

**P < 0.01; *P < 0.05. Np, naupliar stages; СI-CV, young and pre-mature copepodites; CVI, mature copepodites. Phototaxis (light response) pattern: +, positive; −, negative; 0, indifferent.

In March, P. minutus copepods also showed positive UV phototaxis. Furthermore, 24 h and longer periods of starvation (keeping animals in filtered water) increased their light responses. However, animals sampled from different water layers or acclimated at different light conditions did not significantly change their behavior. The interaction between the 'light' and 'food' factors was not significant, ANOVA: F(1, 128) = 0.001; P = 0.97. Oncaea borealis was indifferent to UV light, during the same season and the effects of all the acclimation factors were not significant (Table II).

DISCUSSION

Almost all the studied species, such as Acartia spp., C. hamatus, E. nordmanni, C. glacialis, M. longa, T. longicornis, P. minutus, O. similis, and Polychaeta larvae, were light-sensitive. However, they showed different responses to light. For example, some species were characterized by positive response to RY light during the whole life cycle, whereas others changed their behavior depending on the season and developmental stage. Light did not affect the behavior of O. borealis. We hypothesize that the species inhabiting the upper water layers or feeding close to the surface should depend on light more than deep-dwelling or eurybiont forms. Generally, marine copepods can be divided into several trophic groups inhabiting specific depth horizons. For example, predominantly herbivorous species tend to occupy the upper (photic) water layer, detritus consumers are linked with bottom layers, whereas predatory and omnivorous crustaceans have an intermediate position (Vinogradov, 1968). However, such division is not observed clearly in the relatively shallow White Sea, (average depth 60 m, maximum depth up to 340 m). Nevertheless, certain species exhibit seasonal ontogenetic migrations (Prygunkova, 1974). The White Sea copepods may be clearly divided into several groups depending on their feeding patterns. All stages of C. glacialis and P. minutus, and younger copepodite stages of the superfamily Centropagоidае (T. longicornis, C. hamatus, Acartia spp.) are herbivorous or predominantly herbivorous (Martynova, 2004; Martynova et al., unpublished results) and depend on phytoplankton availability (Martynova et al., submitted for publication). Omnivorous species are represented by younger stages of M. longa and elder copepodite stages of Centropagoids, whereas predation is characteristic of elder M. longa copepodites (Perueva, 1982; Martynova, 2004). Trophic characteristics of O. borealis and O. similis are still unclear; however, there is evidence that Onceidae are suctorial predators, whereas cyclopoids (O. similis) feed on faecal pellets of other copepods (Nielsen and Sabatini, 1996). In addition to grouping based on feeding patterns, all studied species may be divided into migrating and non-migrating. We hypothesize that migrating forms may have higher light sensitivity than non-migrating. The diurnal patterns of distribution of different copepod species in the White Sea are different. For example, Bogorov (1974) considered migrating females of C. glacialis and P. minutus, younger copepodites of M. longa and older copepodites of O. borealis. Kosobokova (1989) also distinguished the White Sea M. longa, O. borealis and C. glacialis as species characterized by pronounced diurnal migrations. Beare and McKenzie (Beare and McKenzie, 1999) documented diel vertical migration in a related species Calanus finmarchicus. Diurnal vertical migrations are characteristic of T. longicornis, M. longa and P. minutus (Kutcheva, personal communication). All the above-mentioned species tend to occupy water layers with specific illumination levels, rising into upper layers during the dark period and descending deeper during the day. At the same time, in summer (the end of July) Acartia is characterized by a bimodal distribution pattern, and animals of all age groups migrate to the water surface (0–3 m) twice, first, around midnight (illumination minimum) and secondly, near midday (illumination maximum). The dynamics of food consumption by these crustaceans also have two maxima associated with morning (8.30) and evening (20.20) hours, when the proportion of feeding individuals in the population in the surface water layer reaches the maximum value of 85% (Vakatov and Martynova, submitted for publication). It is also possible to divide the animals by biogeographical groups into Arctic (C. glacialis, P. minutus, M. longa, O. borealis) and boreal (T. longicornis, C. hamatus, Acartia spp., E. nordmanni). Oithona similis is a eurybiont species (Prygunkova, 1974).

The light responses of predominantly herbivorous and omnivorous copepods and cladocerans, such as C. glacialis (May), Acartia spp., E. nordmanni and young copepodites of C. hamatus and T. longicornis agree with the patterns of the vertical distribution of their populations (Prygunkova, 1974) and their potential food in the White Sea. These species tend to inhabit the upper water layers with sufficient food availability. Feeding rates of T. longicornis, C. hamatus, Acartia spp., inhabiting the surface (photic) layer in the White Sea during the whole summer, depend significantly on the illumination level (Martynova, 2005). For example, in Acartia spp., this parameter is significantly higher at high illumination. The significant differences in the light responses between hungry and fed animals indicate that light is a signal of food availability for these species. As it was shown earlier, hungry animals increase their positive reaction to light, which agrees with data on hungry and non-hungry Daphnia behavior (Stutzman, 2000). The hungry animals tend to respond strongly to light than more fed. Thus, RY light could provide a signal of food availability for animals, inhabiting the upper (photic) water layer, especially hungry. In addition, the water layer with illumination optimal for boreal species E. nordmanni and Acartia spp. (the most intensely feeding in the light) may also be optimal with respect to temperature. It is known that the White Sea is characterized by pronounced vertical water stratification (Babkov, 1998). The upper 15–20 m layer inhabited by boreal crustaceans has the highest temperature in summer. Furthermore, the rate of feeding in all crustaceans of the superfamily Centropagoidea is significantly higher at +15/+16°С than at +10°С (Martynova, 2005), usually observed in the uppermost 0–5 m layer in July–August, which is the reproductive period in these species (Prygunkova, 1974). This temperature dependence was also shown for Daphnia longispina (boreal species). The range of vertical diurnal migrations was higher at lower water temperatures, close to those critical for normal development of this species (Young and Watt, 1996). Moreover, daphnids migrate to the upper layers not only for feeding, but also to experience optimal temperature for ovarian development even when the upper water layer is low in seston (Winder et al., 2003). Low temperatures could also slow the light behavioral response in several limnoplankton species (Persaud and Williamson, 2005).

Two groups, arctic and boreal, significantly depend on the temperature. From this perspective, positive phototaxis of boreal ('warm water’) species (Acartia spp., C. hamatus, T. longicornis, E. nordmanni) must be essential for their survival in the harsh White Sea environment (Martynova et al., 2009). On the other hand, Hansson et al. (Hansson et al., 2007) showed that nearly continuous daylight at high latitudes relaxes the diel migratory behavior in zooplankton making it independent of the predation risk. At lower latitudes, however, such nearly continuous daylight leads to pronounced diel rhythms in migration.

Zooplankton may show local behavioral adaptations in their circadian rhythm. They are also able to assess potential benefits of diel migration and completely suppress diel migration at constant daylight irrespective of the predator risk (Hansson et al., 2007). However, the behavior of mature C. hamatus (boreal species) remains difficult to understand. These copepodites are characterized by negative phototaxis that corresponds well with data, indicating that they feed intensely in darkness (Martynova, 2005). The maximum ingestion rate for a related crustacean species Centropages typicus was noted in twilight and at night (Saiz et al., 1992; Calbet et al., 1999). In contrast, adult individuals of a different crustacean, T. longicornis divided into two groups with opposite patterns of phototaxis in the autumn period, when the changes in night and day light regime are pronounced. Most of them were still characterized by a negative light response, which is supported by the data indicating that feeding was more active in darkness (Martynova, 2005). Furthermore, mature C. hamatus and T. longicornis inhabit the upper 0–10 m water layer in the White Sea. During the day, they prefer the 5–10 m depth layer, whereas at night, migrate to the surface (0–5 m) (Kutcheva, personal communication). We explain this pattern by dividing the population of these two species into two groups depending on the developmental stage which would help to reduce intraspecific food competition. The separation of predominantly herbivorous Arctic P. minutus into two groups with different light responses throughout the year is difficult to explain. However, the vertical distribution of this species in the White Sea has two maxima, especially in summer (Martynova and Kutcheva, unpublished results): first, in upper water layers (10–25 m) and the second, below the thermocline (60–100 m). Also, P. minutus has pronounced ontogenetic vertical migrations. This species tended to diapause as CIII-CV copepodites in deep water layers through summer, autumn and winter periods, when it has stored significant amount of lipids for wintering during the spring time and then became inactive (Prygunkova, 1974). We assume that diapausing copepodites may avoid the light, trying to 'migrate in deeper layers', while those, which still have to store lipids, may exhibit the opposite response by 'migrating to food-rich layer'.

Obviously, the absence of a light response is more likely in such species as O. borealis, whose life cycle occurs almost completely in darkness (Prygunkova, 1974).

The light responses of polychaete larvae agree with their life cycle. The vertical distribution of meroplanktonic polychaete larvae differs between age groups (Shuvalov, 1978). Younger stages presumably feed on phytoplankton and obviously inhabit the upper near-surface water layer with optimal feeding conditions. When these animals reach a certain stage, they settle to the bottom substrate and the sign of phototaxis probably reverses.

The positive response of the eurybiont O. similis to light may also be accounted for by their feeding pattern. Oithona is known to actively destroy faecal pellets of calanoids (Svensen and Nejstgaard, 2003). The peak concentration of suspended organic materials (including pellets) in the White Sea is observed in the upper water layers (Lukashin et al., 2003; Martynova, 2003). The maximum of the vertical distribution of O. similis is also usually observed in the upper 25 m (Prygunkova, 1974; original data).

The relationships between zooplankton vertical distribution and visible light differ across species. The most surprising results were obtained for the phototactic response to UV radiation, which in some cases was positive. As it was stated by many of authors, UV light deters most of hydrobionts due to its harmful effect (Frank and Widder, 1994; Martin et al., 2000; Adams, 2001; Johnsen and Widder, 2001; Rhode et al., 2001). However, we tend to explain such unexpected behavior in the White Sea species by the low UV dose the animals are typically exposed to. We hypothesize that low-intensity UV light may signal the upper food-rich layer for herbivores (Acartia and Pseudocalanus). This is consistent with the increasing positive effect of UV on starved herbivores (Table II). As it was shown by Forward and Cronin (1979), intertidal plankton species had different sensitivity to UV and green/blue light with respect to their preferable depth, whereas deep-dwelling animals had no reaction to UV light. We suppose that low UV intensity may not be harmful for the animals, but can provide certain biologically relevant signal.

The role of visual predators in diel vertical migration behavior has been widely discussed (Gliwicz and Pijanowska, 1988; Bollens and Frost, 1989; Neill, 1990; Bollens et al., 1993; Loose and Dawidowicz, 1994). The role of predator pressure as a factor inducing DVM overlaps with the focus of the present research; however, some assumptions may be made. The herring Clupea pallasi maris-albi is the most abundant planktivorous fish, which may represent up to 95% of all visual predator abundance in the White Sea (Berger et al., 2001). The adult specimens are the most active in May during reproduction period, consuming mostly the large calanoid copepod C. glacialis. In summer and autumn period, herring larvae, and various coelenterate and chaetognath species ('non-visual predators’) feed on many small plankton species (e.g. Oithona, Acartia, Temora, Centropages and some others). Young copepodite stages are most affected by predation (Soloviov and Kosobokova, 2003; Kosobokova et al., 2005). Data on chemical cues inducing migrations in the White Sea are totally absent.

Analyzing phototactic behavior in different life history stages of zooplankton species, we found no evidence that young stages are more vulnerable than elder copepodites, even in ecologically similar species. Thus, we hypothesize a relationship between light responses of crustaceans and such ecological features as trophic characteristics and the inhabited water layer. Light is considered one of the most important factors inducing diurnal vertical migrations of zooplankton in upper water layer (Williamson et al., 1994; Ringelberg, 1999; Hansson et al., 2007). However, biological processes, which determine behavioral responses, are still far from being understood.

To summarize, we documented significant differences in responses of the species studied to light of different wavelengths. Positive phototaxis to red and yellow light is associated with the tendency of herbivorous crustaceans to keep within the layer with the highest food availability (photic layer, where 95% of all phytoplankton is aggregated). Animals may also avoid this layer. Avoidance of the photic layer may be linked with the ontogenetic diapause, which in Arctic species occurs in the aphotic layer. Positive responses to light in predominantly herbivorous P. minutus and omnivorous Acartia spp. to extreme, but low dose UVB, especially after starvation, may also be accounted for by their tendency to migrate to upper water layers with higher food availability. In addition, we speculate that migrations of older copepodite stages of predatory crustaceans Metridia are associated with prey search. Thus, we hypothesize a relationship between light sensitivity, on the one hand, and trophic characteristics, migration behavior (including its changes during the life cycle) and the water layer occupied by the species, on the other. Further studies should include detailed analysis of the effects of UV and visible light on the behavior of copepods with different feeding strategies after their acclimation to specific food availability. Thus, light plays an important role in the behavior of copepods; however, it may also depend on their ecological characteristics, feeding strategy and condition.

FUNDING

The present investigation was supported by Russian Foundation for Basic Research (RFBR grants 05-04-49316-a; 07-04-10165-k and 08-04-01691-а).

ACKNOWLEDGEMENTS

We are grateful to Prof. Alexander P. Savitsky and July A. Labas (INBI RAS) for useful advice; Dr Sergey Budaev (University of Sussex) and Dr Elizabeth Sweet (AWI) for their help in English text editing.

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Author notes

Corresponding editor: Roger Harris