François-Gaël Michalec

Changes in the swimming behavior of Eurytemora affinis (Copepoda, Calanoida) in response to a sub-lethal exposure to nonylphenols.

Estuarine waters are continuously loaded with chemicals which affect the physiology of aquatic organisms to various extents. They also have adverse effects on a wide range of behaviors. Nonylphenols and related compounds are biodegradation products of the nonionic surfactants nonylphenol polyethoxylates. They are commonly found in the aquatic environment. We observed immediate alterations of the free swimming activity of the calanoid copepod Eurytemora affinis from the Seine estuary in response to a sub-lethal concentration of nonylphenols (4-NP and NP1EC) at environmentally realistic concentrations (2 μg/L). Swimming speed and activity increased for both males and females. The use of copepod kinematic proved to be a sensitive indicator of sub-lethal exposure to pollutants.

Effects of animal density, volume, and the use of 2D/3D recording on behavioral studies of copepods

Studies on the behavior of copepods require both an appropriate experimental design and the means to perform objectively verifiable numerical analysis. Despite the growing number of publications on copepod behavior, it has been difficult to compare these studies. In this study, we studied two species of copepods, Eurytemora affinis and Pseudodiaptomus annandalei, and employed recently developed scaling and non-scaling methodology to investigate the effects of density and volume on the swimming behavior of individual organisms in still water. We also compared the results of two- and three-dimensional projections of the swimming tracks. A combination of scale-dependent and scale-independent analysis was found to characterize a number of behavioral observations very effectively. We discovered that (i) density has no effect except to increase the time spent in the swimming state of “breaking”, (ii) smaller volumes resulted in more complex trajectories, and larger volumes, like density, increased the time spent in the swimming state “breaking”, and (iii) three-dimensional projections gave a more accurate estimation of speed and the time spent cruising. When only a vertical 2D projection was used, “cruising” could be confused with “sinking”. These results indicate that both experimental conditions and the selection of 2D or 3D projection have important implications regarding the study of copepod behavior. The development of standardized procedures with which to compare the observations made in different studies is an issue of particular urgency.

Turbulence triggers vigorous swimming but hinders motion strategy in planktonic copepods

Calanoid copepods represent a major component of the plankton community. These small animals reside in constantly flowing environments. Given the fundamental role of behaviour in their ecology, it is especially relevant to know how copepods perform in turbulent flows. By means of three-dimensional particle tracking velocimetry, we reconstructed the trajectories of hundreds of adult Eurytemora affinis swimming freely under realistic intensities of homogeneous turbulence. We demonstrate that swimming contributes substantially to the dynamics of copepods even when turbulence is significant. We show that the contribution of behaviour to the overall dynamics gradually reduces with turbulence intensity but regains significance at moderate intensity, allowing copepods to maintain a certain velocity relative to the flow. These results suggest that E. affinis has evolved an adaptive behavioural mechanism to retain swimming efficiency in turbulent flows. They suggest the ability of some copepods to respond to the hydrodynamic features of the surrounding flow. Such ability may improve survival and mating performance in complex and dynamic environments. However, moderate levels of turbulence cancelled gender-specific differences in the degree of space occupation and innate movement strategies. Our results suggest that the broadly accepted mate-searching strategies based on trajectory complexity and movement patterns are inefficient in energetic environments.

Lipid nanocapsules for behavioural testing in aquatic toxicology: Time–response of Eurytemora affinis to environmental concentrations of PAHs and PCB

The increasing interest for behavioural investigations in aquatic toxicology has heightened the need for developing tools that allow realistic exposure conditions and provide robust quantitative data. Calanoid copepods dominate the zooplankton community in marine and brackish environments. These small organisms have emerged as attractive models because of the sensitivity of their behaviour to important environmental parameters and the significance of self-induced motion in their ecology. Estuarine copepods are particularly relevant in this context because of their incessant exposure to high levels of pollution. We used lipid nanocapsules to deliver sub-lethal concentrations of PAHs (pyrene, phenanthrene and fluoranthene) and PCB 153 into the digestive track of males and females Eurytemora affinis. This novel approach enabled us to achieve both contact and trophic exposure without using phytoplankton, and to expose copepods to small hydrophobic molecules without using organic solvent. We reconstructed the motion of many copepods swimming simultaneously by means of three-dimensional particle tracking velocimetry. We quantified the combined effects of contact and trophic toxicity by comparing the kinematic and diffusive properties of their motion immediately and after 3h and 24h of exposure. Despite the lack of toxicity of their excipients, both empty and loaded capsules increased swimming activity and velocity immediately after exposure. Laser microscopy imaging shows adhesion of nanocapsules on the exoskeleton of the animals, suggesting contact toxicity. The behavioural response resembles an escape reaction allowing copepods to escape stressful conditions. The contact toxicity of empty capsules and pollutants appeared to be additive and nanocapsules loaded with PCB caused the greatest effects. We observed a progressive accumulation of capsules in the digestive track of the animals after 3h and 24h of exposure, which suggests an increasing contribution of systemic toxicity. Nanocapsules filled with PAHs caused a smaller response compared to empty capsules, which we attribute to the narcotic properties of these toxicants. The sharp decrease in velocity after 24h of exposure to capsules loaded with PCB suggests physiological incapacitation following systemic toxicity. Clear differences are visible between genders in their response to empty and loaded capsules, for all exposure durations. Females appear to be less sensitive than males, suggesting different tolerance to stress conditions. Our results confirm the feasibility of using lipid nanocapsules to identify pollutant-induced behavioural alteration in the plankton. They also add new insights into the contact and systemic toxicity of common pollutants. We expect that our results will assist and evoke further research to develop suitable nanocarrier systems for behavioural testing.

Characterization of intermittency in zooplankton behaviour in turbulence.

We consider Lagrangian velocity differences of zooplankters swimming in still water and in turbulence. Using cumulants, we quantify the intermittency properties of their motion recorded using three-dimensional particle tracking velocimetry. Copepods swimming in still water display an intermittent behaviour characterized by a high probability of small velocity increments, and by stretched exponential tails. Low values arise from their steady cruising behaviour while heavy tails result from frequent relocation jumps. In turbulence, we show that at short time scales, the intermittency signature of active copepods clearly differs from that of the underlying flow, and reflects the frequent relocation jumps displayed by these small animals. Despite these differences, we show that copepods swimming in still and turbulent flow belong to the same intermittency class that can be modelled by a log-stable model with non-analytical cumulant generating function. Intermittency in swimming behaviour and relocation jumps may enable copepods to display oriented, collective motion under strong hydrodynamic conditions and thus, may contribute to the formation of zooplankton patches in energetic environments.Graphical abstract

Zooplankton can actively adjust their motility to turbulent flow

Significance Zooplankton possess narrow swimming capabilities, yet are capable of active locomotion amid turbulence. By decoupling the relative velocity of swimming zooplankton from that of the underlying flow, we provide evidence for an active adaptation that allows these small organisms to modulate their swimming effort in response to background flow. This behavioral response results in reduced diffusion at substantial turbulence intensity. Adjusting motility provides fitness advantage because it enables zooplankton to retain the benefits of self-locomotion despite the constraints enforced by turbulence transport. Vigorous swimming and reduced diffusion oppose turbulence advection, can directly affect the dispersal of zooplankton populations, and may help these organisms to actively control their distribution in dynamic environments. Calanoid copepods are among the most abundant metazoans in the ocean and constitute a vital trophic link within marine food webs. They possess relatively narrow swimming capabilities, yet are capable of significant self-locomotion under strong hydrodynamic conditions. Here we provide evidence for an active adaptation that allows these small organisms to adjust their motility in response to background flow. We track simultaneously and in three dimensions the motion of flow tracers and planktonic copepods swimming freely at several intensities of quasi-homogeneous, isotropic turbulence. We show that copepods synchronize the frequency of their relocation jumps with the frequency of small-scale turbulence by performing frequent relocation jumps of low amplitude that seem unrelated to localized hydrodynamic signals. We develop a model of plankton motion in turbulence that shows excellent quantitative agreement with our measurements when turbulence is significant. We find that, compared with passive tracers, active motion enhances the diffusion of organisms at low turbulence intensity whereas it dampens diffusion at higher turbulence levels. The existence of frequent jumps in a motion that is otherwise dominated by turbulent transport allows for the possibility of active locomotion and hence to transition from being passively advected to being capable of controlling diffusion. This behavioral response provides zooplankton with the capability to retain the benefits of self-locomotion despite turbulence advection and may help these organisms to actively control their distribution in dynamic environments. Our study reveals an active adaptation that carries strong fitness advantages and provides a realistic model of plankton motion in turbulence.

Behavioral response of the freshwater cyclopoid copepod Eucyclops serrulatus to hydropeaking and thermopeaking in a laboratory flume

ABSTRACT The generation of electricity by hydropower plants meets the requirements for intermittent energy demand and for the production of renewable energy. However, the hydropower plant operation has important consequences for the biotic compartment of the river reaches downstream. Intermittent release of water causes sudden variations in discharge that increase bed shear stress and dislodge benthic organisms. Release from high-elevation reservoir can also affect the thermal regime of the river by causing sharp variations in water temperature. Because the hydrodynamic and thermal waves separate while propagating downstream, the benthic community is exposed to two distinct stressors that affect taxa differently based on their sensitivity and adaptations. We investigated separately the effects of a sudden variation in discharge or in water temperature on the small-scale swimming behavior of a widespread species of cyclopoid copepod in a laboratory flume that allows the tracking of organisms both in the water column and in a transparent sediment bed. We gradually varied the discharge or the temperature of the water to mimic the artificial changes caused by hydropower plants. We tracked copepods in three dimensions and quantified the kinematics of their motion. Copepods increased substantially their counter-current swimming effort in response to increasing flow velocity. This behavioral response seems to occur above a threshold in flow velocity of approx. 40 mm/s. It results in a substantial reduction in their downstream transport and hence opposes drift. Copepods reacted differently to warm and cold variations in temperature. Decreasing temperature resulted in a substantially lower counter-current swimming effort, which may therefore increase drift. Rising temperature had no clear effect on their behavior. Our study highlights the importance of understanding the behavioral traits that mediate the response of stream invertebrates to disturbances in the hydraulic and thermal regimes of their environment.

Counter-current swimming of lotic copepods as a possible mechanism for drift avoidance: Benthic copepods swim actively to reduce downstream drift

Ecohydrology. 2018;11:e1992. https://doi.org/10.1002/eco.1992 Abstract Benthic invertebrates in streams and rivers face a dominant downstream flow that may impose drift. The mechanisms that allow organisms to maintain their position instead of being swept downstream are not well known. One possible strategy involves active behaviour: Organisms perform small‐scale counter‐current displacements along the streambed. Because these fine‐scale processes are difficult to approach in field studies, evidence for behavioural mechanisms against flow advection has remained scarce. We reconstruct the three‐dimensional trajectories of the widespread cyclopoid copepod Eucyclops serrulatus moving freely in the water column and in the transparent sediment bed of a laboratory flume. In the different experiments, the average flow velocity is 12, 35, and 67 mm/s. We isolate the behavioural component of their motion by subtracting the local flow velocity. We show that copepods stay preferentially within the interstitial space of the sediment bed or close to its surface from which they perform frequent excursions in the water column. We also show that copepods perform active counter‐current swimming to limit downstream drift. The counter‐current swimming effort increases with flow velocity, and therefore, downstream drift remains moderate and does not vary strongly for the different flow rates tested. This active behavioural response to changing flow conditions, combined with frequent stops in the substratum where flow velocity is negligible, may confer lotic copepods the ability to reduce downstream transport. Our results confirm the importance of behaviour in drift avoidance and may evoke further research on taxon‐specific responses to varying hydraulic conditions.