A machine vision system for tracking population behavior of zooplankton in small-scale experiments: a case study on salmon lice (Lepeophtheirus salmonis Krøyer, 1838) copepodite population responses to different light stimuli.

To achieve efficient and preventive measures against salmon lice (Lepeophtheirus salmonis Krøyer, 1838) infestation, a better understanding of behavioral patterns of the planktonic life stages is key. To investigate light responses in L. salmonis copepodites, a non-intrusive experimental system was designed to measure behavioral responses in a 12.5-l volume using machine vision technology and methodology. The experimental system successfully tracked the collective movement patterns of the sea lice population during exposure to different light stimuli emitted from alternating zones in the system. This system could further be used to study behavioral responses to different physical cues of various developmental stages of sea lice or other zooplankton.

Artificial light during the polar night disrupts Arctic fish and zooplankton behaviour down to 200 m depth.

For organisms that remain active in one of the last undisturbed and pristine dark environments on the planet-the Arctic Polar Night-the moon, stars and aurora borealis may provide important cues to guide distribution and behaviours, including predator-prey interactions. With a changing climate and increased human activities in the Arctic, such natural light sources will in many places be masked by the much stronger illumination from artificial light. Here we show that normal working-light from a ship may disrupt fish and zooplankton behaviour down to at least 200 m depth across an area of >0.125 km2 around the ship. Both the quantitative and qualitative nature of the disturbance differed between the examined regions. We conclude that biological surveys in the dark from illuminated ships may introduce biases on biological sampling, bioacoustic surveys, and possibly stock assessments of commercial and non-commercial species.

Mycosporine-Like Amino Acids (MAAs) in Zooplankton.

Organisms have different adaptations to avoid damage from ultraviolet radiation and one such adaptation is the accumulation of mycosporine-like amino acids (MAAs). These compounds are common in aquatic taxa but a comprehensive review is lacking on their distribution and function in zooplankton. This paper shows that zooplankton MAA concentrations range from non-detectable to ~13 µg mgDW-1. Copepods, rotifers, and krill display a large range of concentrations, whereas cladocerans generally do not contain MAAs. The proposed mechanisms to gain MAAs are via ingestion of MAA-rich food or via symbiotic bacteria providing zooplankton with MAAs. Exposure to UV-radiation increases the concentrations in zooplankton both via increasing MAA concentrations in the phytoplankton food and due to active accumulation. Concentrations are generally low during winter and higher in summer and females seem to deposit MAAs in their eggs. The concentrations of MAAs in zooplankton tend to increase with altitude but only up to a certain altitude suggesting some limitation for the uptake. Shallow and UV-transparent systems tend to have copepods with higher concentrations of MAAs but this has only been shown in a few species. A high MAA concentration has also been shown to lead to lower UV-induced mortality and an overall increased fitness. While there is a lot of information on MAAs in zooplankton we still lack understanding of the potential costs and constraints for accumulation. There is also scarce information in some taxa such as rotifers as well as from systems in tropical, sub(polar) areas as well as in marine systems in general.

A machine vision system for zooplankton behavioural studies: a case study on the phototactic behaviour of sea lice (Lepeophtheirus salmonis) during sound and ultrasound stimuli.

Machine vision represents an accurate and easily verifiable method for observing live organisms and this technology is constantly evolving in terms of accessibility and cost. Motivated by the complexity of observing small-sized aquatic organisms in experimental systems, and the difficulties related to real-time observation, sampling and counting without interfering with the organisms, we here present a new method for observing behaviour and dispersion of non-sessile zooplankton organisms using a custom-made tank with an associated machine vision system. The system was used in an experiment where the aim was to assess the effect of sound and ultrasound on the phototactic behaviour of copepodite stages of the salmon louse (Lepeophtheirus salmonis). The experimental set-up is described, including a triangular test tank designed to create a sound pressure gradient, a mechanized camera movement system and a vision system with dedicated image processing software.

Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton.

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor-cell evolution in animals. The two cell types coexist in some animals, however how these cells functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming in non-directional UV light, a behavior absent in ciliary-opsin knockout larvae. UV avoidance overrides positive phototaxis mediated by the rhabdomeric eyes such that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during vertical migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptor cells in a zooplankton larva.

Distribution and UV protection strategies of zooplankton in clear and glacier-fed alpine lakes.

Zooplankton, a group of aquatic animals important as trophic link in the food web, are exposed to high levels of UV radiation (UVR) in clear alpine lakes, while in turbid glacier-fed lakes they are more protected. To study the interplay between behavioral and physiological protection responses in zooplankton from those lakes, we sampled six lakes of different UVR transparency and glacial turbidity. Copepods were absent in the upper water layers of the clearest lake, while in glacier-fed lakes they were more evenly distributed in the water column. Across all lakes, the weighted copepod mean depth was strongly related to food resources (chlorophyll a and rotifers), whereas in the fishless lakes, glacial turbidity largely explained the vertical daytime distribution of these organisms. Up to ~11-times (mean 3.5) higher concentrations of photo-protective compounds (mycosporine-like amino acids, MAAs) were found in the copepods from the clear than from the glacier-fed lakes. In contrast to carotenoid concentrations and antioxidant capacities, MAA levels were strongly related to the lake transparency. Copepods from alpine lakes rely on a combination of behavioral and physiological strategies adapted to the change in environmental conditions taking place when lakes shift from glacially turbid to clear conditions, as glacier retreat proceeds.

A ciliary opsin in the brain of a marine annelid zooplankton is ultraviolet-sensitive, and the sensitivity is tuned by a single amino acid residue.

Ciliary opsins were classically thought to function only in vertebrates for vision, but they have also been identified recently in invertebrates for non-visual photoreception. Larvae of the annelid Platynereis dumerilii are used as a zooplankton model, and this zooplankton species possesses a "vertebrate-type" ciliary opsin (named c-opsin) in the brain. Platynereis c-opsin is suggested to relay light signals for melatonin production and circadian behaviors. Thus, the spectral and biochemical characteristics of this c-opsin would be directly related to non-visual photoreception in this zooplankton model. Here we demonstrate that the c-opsin can sense UV to activate intracellular signaling cascades and that it can directly bind exogenous all-trans-retinal. These results suggest that this c-opsin regulates circadian signaling in a UV-dependent manner and that it does not require a supply of 11-cis-retinal for photoreception. Avoidance of damaging UV irradiation is a major cause of large-scale daily zooplankton movement, and the observed capability of the c-opsin to transmit UV signals and bind all-trans-retinal is ideally suited for sensing UV radiation in the brain, which presumably lacks enzymes producing 11-cis-retinal. Mutagenesis analyses indicated that a unique amino acid residue (Lys-94) is responsible for c-opsin-mediated UV sensing in the Platynereis brain. We therefore propose that acquisition of the lysine residue in the c-opsin would be a critical event in the evolution of Platynereis to enable detection of ambient UV light. In summary, our findings indicate that the c-opsin possesses spectral and biochemical properties suitable for UV sensing by the zooplankton model.

Direct and indirect effects of ionizing radiation on grazer-phytoplankton interactions.

Risk assessment of exposure to radionuclides and radiation does not usually take into account the role of species interactions. We investigated how the transfer of carbon between a primary producer, Raphidocelis subcapitata, and a consumer, Daphnia magna, was affected by acute exposure to gamma radiation. In addition to unexposed controls, different treatments were used where: a) only D. magna (Z treatment); b) only R. subcapitata (P treatment) and c) both D. magna and R. subcapitata (ZP treatment) were exposed to one of three acute doses of gamma radiation (5, 50 and 100 Gy). We then compared differences among treatments for three endpoints: incorporation of carbon by D. magna, D. magna growth and R. subcapitata densities. Carbon incorporation was affected by which combination of species was irradiated and by the radiation dose. Densities of R. subcapitata at the end of the experiment were also affected by which species had been exposed to radiation. Carbon incorporation by D. magna was significantly lower in the Z treatment, indicating reduced grazing, an effect stronger with higher radiation doses, possibly due to direct effects of gamma radiation. Top-down indirect effects of this reduced grazing were also seen as R. subcapitata densities increased in the Z treatment due to decreased herbivory. The opposite pattern was observed in the P treatment where only R. subcapitata was exposed to gamma radiation, while the ZP treatment showed intermediate results for both endpoints. In the P treatments, carbon incorporation by D. magna was significantly higher than in the other treatments, suggesting a higher grazing pressure. This, together with direct effects of gamma radiation on R. subcapitata, probably significantly decreased phytoplankton densities in the P treatment. Our results highlight the importance of taking into account the role of species interactions when assessing the effects of exposure to gamma radiation in aquatic ecosystems.

Joint Toxicity of Cadmium and Ionizing Radiation on Zooplankton Carbon Incorporation, Growth and Mobility.

The risk of exposure to radioactive elements is seldom assessed considering mixture toxicity, potentially over- or underestimating biological and ecological effects on ecosystems. This study investigated how three end points, carbon transfer between phytoplankton and Daphnia magna, D. magna mobility and growth, responded to exposure to γ-radiation in combination with the heavy metal cadmium (Cd), using the MIXTOX approach. Observed effects were compared with mixture effects predicted by concentration addition (CA) and independent action (IA) models and with deviations for synergistic/antagonistic (S/A), dose-level (DL), and dose-ratio (DR) dependency interactions. Several patterns of response were observed depending on the end point tested. DL-dependent deviation from the IA model was observed for carbon incorporation with antagonism switching to synergism at higher doses, while the CA model indicated synergism, mainly driven by effects at high doses of γ-radiation. CA detected antagonism regarding acute immobilization, while IA predicted DR-dependency. Both CA and IA also identified antagonism for daphnid growth. In general, effects of combinations of γ-radiation and Cd seem to be antagonistic at lower doses, but synergistic at the higher range of the doses tested. Our results highlight the importance of investigating the effects of exposure to γ-radiation in a multistressor context.

Combined Effects from γ Radiation and Fluoranthene Exposure on Carbon Transfer from Phytoplankton to Zooplankton.

Risk assessment does not usually take into account mixtures of contaminants, thus potentially under- or overestimating environmental effects. We investigated how the transfer of carbon between a primary producer, Pseudokirchneriella subcapitata, and a consumer, Daphnia magna, is affected by acute exposure of γ radiation (GR) in combination with the polycyclic aromatic hydrocarbon fluoranthene (FA). We exposed D. magna to five concentrations of FA and five acute doses of GR as single contaminants and in nine binary combinations. We compared the observed data for three end points (incorporation of carbon by D. magna, D. magna ingestion rates, and growth) to the predicted joint effects of the mixed stressors based on the independent action (IA) concept. There were deviations from the IA predictions, especially for ingestion rates and carbon incorporation by D. magna, where antagonistic effects were observed at the lower doses, while synergism was seen at the highest doses. Our results highlight the importance of investigating the effects of exposure to GR in a multistressor context. In mixtures of GR and FA, the IA-predicted effects seem to be conservative as antagonism between the two stressors was the dominant pattern, possibly due to stimulation of cellular antioxidative stress mechanisms.

Diel vertical migration.

In this Quick Guide, Brierley provides a brief overview of a pervasive aspect of aquatic ecosystems, the daily movement of organisms up and down the water column.

High mortality of Red Sea zooplankton under ambient solar radiation.

High solar radiation along with extreme transparency leads to high penetration of solar radiation in the Red Sea, potentially harmful to biota inhabiting the upper water column, including zooplankton. Here we show, based on experimental assessments of solar radiation dose-mortality curves on eight common taxa, the mortality of zooplankton in the oligotrophic waters of the Red Sea to increase steeply with ambient levels of solar radiation in the Red Sea. Responses curves linking solar radiation doses with zooplankton mortality were evaluated by exposing organisms, enclosed in quartz bottles, allowing all the wavelengths of solar radiation to penetrate, to five different levels of ambient solar radiation (100%, 21.6%, 7.2%, 3.2% and 0% of solar radiation). The maximum mortality rates under ambient solar radiation levels averaged (±standard error of the mean, SEM) 18.4±5.8% h(-1), five-fold greater than the average mortality in the dark for the eight taxa tested. The UV-B radiation required for mortality rates to reach ½ of maximum values averaged (±SEM) 12±5.6 h(-1)% of incident UVB radiation, equivalent to the UV-B dose at 19.2±2.7 m depth in open coastal Red Sea waters. These results confirm that Red Sea zooplankton are highly vulnerable to ambient solar radiation, as a consequence of the combination of high incident radiation and high water transparency allowing deep penetration of damaging UV-B radiation. These results provide evidence of the significance of ambient solar radiation levels as a stressor of marine zooplankton communities in tropical, oligotrophic waters. Because the oligotrophic ocean extends across 70% of the ocean surface, solar radiation can be a globally-significant stressor for the ocean ecosystem, by constraining zooplankton use of the upper levels of the water column and, therefore, the efficiency of food transfer up the food web in the oligotrophic ocean.

Induced tolerance expressed as relaxed behavioural threat response in millimetre-sized aquatic organisms.

Natural selection shapes behaviour in all organisms, but this is difficult to study in small, millimetre-sized, organisms. With novel labelling and tracking techniques, based on nanotechnology, we here show how behaviour in zooplankton (Daphnia magna) is affected by size, morphology and previous exposure to detrimental ultraviolet radiation (UVR). All individuals responded with immediate downward swimming to UVR exposure, but when released from the threat they rapidly returned to the surface. Large individuals swam faster and generally travelled longer distances than small individuals. Interestingly, individuals previously exposed to UVR (during several generations) showed a more relaxed response to UVR and travelled shorter total distances than those that were naive to UVR, suggesting induced tolerance to the threat. In addition, animals previously exposed to UVR also had smaller eyes than the naive ones, whereas UVR-protective melanin pigmentation of the animals was similar between populations. Finally, we show that smaller individuals have lower capacity to avoid UVR which could explain patterns in natural systems of lower migration amplitudes in small individuals. The ability to change behavioural patterns in response to a threat, in this case UVR, adds to our understanding of how organisms navigate in the 'landscape of fear', and this has important implications for individual fitness and for interaction strengths in biotic interactions.

Effects of temperature on type approval testing of ballast water treatment systems.

To limit the risk associated with invasion of habitats by exogenous species, the International Convention for the Control and Management of the Ships' Ballast Water and Sediments was adopted in February 2004 and may soon enter into force. The International Maritime Organization (IMO) has produced guidelines to assess the efficacy and reliability of Ballast Water Treatment Systems (BWTS), but no guidance on how to take temperature into account during test cycles has been provided yet. Temperature is one of the main factors influencing the distribution and ecology of organisms along latitudes. Its increase results in higher grazing, growth, and reproduction rates of zooplankton. Under dark conditions, phytoplankton loss is also increased due to faster natural decay as well as enhanced top down control from zooplankton. Increased temperatures also improve the efficacy of chemical treatment, whereas the decay rates of disinfectants and their byproducts are potentially accelerated. The IMO guidelines for the type approval of BWTS should be amended to include recommendations on how to take temperature into account. Failing to ensure comparability and reliability between tests may pose a threat to the environment and may create problems for those attempting to apply BWTS. We propose to use a fixed Q10 value and a temperature of reference to adjust the retention time in ballast water tanks during testing.

[Phytoplankton and zooplankton of the industrial reservoir R-9 (Lake Karachay)].

Planktonic communities of the Reservoir-9 (Lake Karachay, storage reservoir of liquid medium-level radioactive waste of the Mayak Production Association) are exposed to the severe radioactive forcing (in 2010 the total beta-activity of the water was 1.8 x 10(7) Bq/L, total alpha-activity was 1.1 x 10(4) Bq/L), aswell as to the chemical contamination (level of nitrates in water 4.1 g/L). The calculated values of the absorbed dose rate were 130 Gy/day for phytoplankton and 4.0 Gy/day for zooplankton. Extremely low species diversity, the overwhelming dominance of one species (phytoplankton is close to a monoculture of ubiquitous cyanobacteria Geitlerinema amphibium, zooplankton--to a monoculture of rotifers Hexarthrafennica), wide fluctuations in numbers of algae, a low number of zooplankton were the most substantial characteristics of the plankton communities in Lake Karachay. So, plankton communities status is a sign of environmental retrogress in this ecosystem.

[Assessment of radiation exposure level for hydrobionts in some special industrial ponds at the "Mayak" PA].

Evaluation of the radionuclide content in the ecosystem components (water, sediments, aquatic organisms) of industrial reservoirs-storages of liquid radioactive waste of the "Mayak" PA (reservoirs R-4, R-10, R-11, R-17, R-9) and the estimation of the absorbed dose rate in aquatic organisms of these reservoirs using the software package ERICA Assessment Tool 1.0 May 2009 have been performed. Gradient of the absorbed dose rate for the detected taxonomic groups of hydrobionts in the series of the studied reservoirs R-11 --> R-10 --> R-4 --> R-17 --> R-9 was almost equal to one order of magnitude. The estimated absorbed dose rate for phytoplankton ranged from 5.4 x 10(0) mGy/day (R-11) to 4.0 x 10(4) mGy/day (R-9), for zooplankton--from 6.4 x 10(-1) mGy/day (R-11) to 3.8 x 10(3) mGy/day (R-9), for zoobenthos (chironomids)--from 5.6 x 10(0) mGy/day (R-11) to 1.1 x 10(3) mGy/day (R-17), for fish (roach)--from 8.0 x 10(-1) mGy/day (R-11) to 1.9 x 10(1) mGy/day (R-4).

Stability of complex food webs: resilience, resistance and the average interaction strength.

In the face of stochastic climatic perturbations, the overall stability of an ecosystem will be determined by the balance between its resilience and its resistance, but their relative importance is still unknown. Using aquatic food web models we study ecosystem stability as a function of food web complexity. We measured three dynamical stability properties: resilience, resistance, and variability. Specifically, we evaluate how a decrease in the strength of predator-prey interactions with food web complexity, reflecting a decrease in predation efficiency with the number of prey per predator, affects the overall stability of the ecosystem. We find that in mass conservative ecosystems, a lower interaction strength slows down the mass cycling rate in the system and this increases its resistance to perturbations of the growth rate of primary producers. Furthermore, we show that the overall stability of the food webs is mostly given by their resistance, and not by their resilience. Resilience and resistance display opposite trends, although they are shown not to be simply opposite concepts but rather independent properties. The ecological implication is that weaker predator-prey interactions in closed ecosystems can stabilize food web dynamics by increasing its resistance to climatic perturbations.

Horizontal migration of Acartia pacifica Steuer (copepoda) in response to UV-radiation.

It is known that zooplankton migrate vertically to avoid UV-radiation (UVR, 280-400nm), but little is known if such avoidance happens horizontally. Here, we showed that the copepod Acartia pacifica avoided UV irradiated fields horizontally. Exposure of A. pacifica to PAR or PAR+UV-A for 30min did not make any difference in the horizontal distribution of the individuals. However, addition of UV-B radiation, that is PAR+UV-A+B, resulted in uneven distributions among the treatments, with significant less individuals compared to the PAR or PAR+UV-A treatments. More carotenoids and UV-absorbing compounds were found in the A. pacifica individuals that chose to stay under the radiation treatments with UV. It is concluded that A. pacifica can migrate horizontally to avoid UV-related harms and those contains more protective compounds were less sensitive to UVR.

An approach for the assessment of risk from chronic radiation to populations of phytoplankton and zooplankton.

A conceptual model of the effects of chronic radiation on a population of phytoplankton and zooplankton in an oceanic nutrient layer is presented. The model shows that there are distinct threshold dose rates at which the different plankton populations become unsustainable. These are 10,400 microGy h(-1) for phytoplankton and 125 microGy h(-1) for zooplankton. Both these values are considerably greater than the current screening values for protection of 10 microGy h(-1). The model highlights the effects of predator-prey dynamics in predicting that when the zooplankton is affected by the radiation dose, the phytoplankton population can increase. In addition, the model was altered to replicate the dose rates to the plankton of a previous ERICA Irish Sea assessment (24 microGy h(-1) for zooplankton and 430 microGy h(-1) to phytoplankton). The results showed only a 10% decrease in the zooplankton population and a 15% increase in the phytoplankton population. Therefore, at this level of dose, the model predicts that although the dose rate exceeds the guideline value, populations are not significantly affected. This result highlights the limitations of a single screening value for different groups of organisms.

Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton.

In this report, we provide a perspective on how zooplankton are able to respond to present and future levels of ultraviolet (UV) radiation, a threat that has been present throughout evolutionary time. To cope with this threat, zooplankton have evolved several adaptations including behavioral responses, repair systems, and accumulation of photoprotective compounds. Common photoprotective compounds include melanins and carotenoids, which are true pigments, but also mycosporine-like amino acids (MAAs) and several other substances, and different taxa use different blends of these compounds. It is not only the level of UV radiation, however, that determines the amount of photoprotective compounds incorporated by the zooplankton, but also other environmental factors, such as predation and supply rate of the compounds. Furthermore, compared to taxa that are less pigmented, those taxa with ample pigmentation are generally less likely to exhibit diel migration. The photoenzymatic repair of UV damages seems to be more efficient at intermediate temperature than at low and high temperatures, suggesting that it is less useful at high and low latitudes, where UV radiation is often extremely high. While predicted future increases in UV radiation are expected to substantially affect many processes, recent studies show that most zooplankton taxa are well adapted to cope with such increases, either by UV avoidance behavior or by incorporation of photoprotective compounds. Hence, we conclude that future increase in UV radiation will have only moderate direct effects on zooplankton biomass and community dynamics.