Proximate control of diel vertical migration in Phyllosoma larvae of the Caribbean spiny lobster Panulirus argus

Phyllosoma larvae of the spiny lobster Panulirus argus undergo diel vertical migration (DVM), in which they are at depth during the day and nearer the surface at night. This study determined the visual spectral sensitivity of Stage I larvae and investigated whether light plays a proximate role in DVM as an exogenous cue and as an entrainment cue for an endogenous rhythm in vertical migration. Under constant conditions, larvae have a circadian rhythm (24.5-h period) in vertical swimming that resulted in a twilight DVM pattern. The behavioral response spectrum and electroretinogram recording indicated two photoreceptor spectral classes with maxima at 360 and 486 nm. When stimulated in an apparatus that simulated the underwater angular light distribution, dark-adapted larvae showed only positive phototaxis, with a threshold intensity of 1.8 × 10(13) photons m(-2) s(-1) (3.0 × 10(-5) μmoles photons m(-2) s(-1)). They have an avoidance response to predator shadows in which they descend upon sudden decreases in light intensity of more than 69%. When stimulated with relative rates of decrease in light intensity as occur at sunset they ascended, whereas they descended upon relative rates of light intensity increase as occur at sunrise. Thus, the DVM pattern is controlled by both an endogenous circadian rhythm in swimming and behavioral responses to light at sunrise and sunset.     

A laboratory method for studying zooplankton swimming behaviors

A laboratory method is presented for studying zooplankton swimming behaviors such as phototaxis and photokinesis. The method attempts to standardize laboratory conditions and to minimize the effects of several phenomena which modify zooplankton behavior. The role of angular light distribution in zooplankton behavior is discussed, and an apparatus which simulates a natural underwater light environment is described. The procedure minimizes the fluctuations in zooplankton swimming speed and vertical distribution that are caused by large light stimuli, noise, food deprivation, endogenous rhythms, and other factors. The experimental animals were viewed remotely with the aid of a light amplifier and video camera. A mathematical equation and computer program for calculating three-dimensional swimming speeds of zooplankton from video recordings are described in detail.     

Diel vertical migration and endogenous swimming rhythm in Asterope mariae (Baird) and Philomedes interpuncta (Baird) (Crustacea Ostracoda Cypridinidae)

Among the benthic ostracods Asterope mariae and Philomedes interpuncta, the adult males emerge at dusk from the benthos and swim straight up to the surface, where they soon concentrate in the neustonic realm. The migration starts when the irradiance is almost 1 W cm^-2 and the maximal density occurs at the surface when the light has reached 0.005 W cm^-2, before it is completely dark. The migration ends <1 h later and very few animals are observed in the water column later in the night. Upward migration does not result from a positive phototaxis to dim light, but rather from a strong negative geotaxis and an increase in kinesis or swimming activity which occur at around 1 W cm^-2. This activity is induced both by the end of the diurnal period of photoinhibition and by an endogenous circadian rhythm. This rhythm could be clearly observed in both species from the recordings made during up to 2 weeks in constant darkness. The length of the period was roughly 24 h (24 h 3 min in Asterope, 23 h 10 min i Philomedes). The timing of the activity phase in total darkness varied depending on the post-capture history of the experimental animals, especially on the time of onset of the experiment. The adaptive advantage of this rapid diel vertical migration may be a question of feeding, but this may also increase the nocturnal dispersal of the reproductive males, and thus promote the reproduction of the species.      

Phototaxis by the Dinoflagellate Gymnodinium splendens Lebour*

A microscope-television system was used to monitor quantitatively the behavior of Gymnodinium splendens Lebour in response to light. The predominant behavioral sequence upon stimulation is (a) an initial 2–5 sec cessation of movement (stop-response) followed by (b) positive phototaxis. The action spectra for each response are identical, having maxima at 450 and 280 nm. Upon measuring the percent response to a range of stimulus intensities, it is apparent that a stop-response is not a behavioral prerequisite for phototaxis. An identical circadian rhythm in photoresponsiveness is observed for phototaxis and for the stop-response with greatest light sensitivity occurring during the first 4 hr of the entrained light period. The implication of phototactic sensitivity and the phototactic circadian rhythm in diurnal vertical migration is discussed.     

The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton

Many pelagic animal species in the marine environment and in lakes migrate to deeper water layers before sunrise and return around sunset. The amplitude of these diel vertical migrations (DVM) varies from several hundreds of metres in the oceans to approx. 5–20 m in lakes. DVM can be studied from a proximate and an ultimate point of view. A proximate analysis is intended to reveal the underlying behavioural mechanism and the factors that cause the daily displacements. The ultimate analysis deals with the adaptive significance of DVM and the driving forces that were responsible for the selection of the traits essential to the behavioural mechanism. The freshwater cladoceran Daphnia is the best studied species and results can be used to model migration behaviour in general. Phototaxis in Daphnia spp., which is defined as a light-oriented swimming towards (positive phototaxis) or away (negative phototaxis) from a light source, is considered the most important mechanism basic to DVM. A distinction has been made between primary phototaxis which occurs when light intensity is constant, and secondary phototaxis which is caused by changes in light intensity. Both types of reaction are superimposed on normal swimming. This swimming of Daphnia spp. consists of alternating upwards and downwards displacements over small distances. An internal oscillator seems to be at the base of these alternations. Primary phototaxis is the result of a dominance of either the upwards or the downwards oscillator phase, and the direction depends on internal and external factors: for example, fish-mediated chemicals or kairomones induce a downwards drift. Adverse environmental factors may produce a persistent primary phototaxis. Rare clones of D. magna have been found that show also persistent positive or negative primary phototaxis and interbreeding of the two types produces intermediate progeny: thus a genetic component seems to be involved. Also secondary phototaxis is superimposed on normal swimming: a continuous increase in light intensity amplifies the downwards oscillator phase and decreases the upwards phase. A threshold must be succeeded which depends on the rate and the duration of the relative change in light intensity. The relation between both is given by the stimulus strength versus stimulus duration curve. An absolute threshold or rheobase exists, defined as the minimum rate of change causing a response if continued for an infinitely long time. DVM in a lake takes place during a period of 1-5-2 h when light changes are higher than the rheobase threshold. Accelerations in the rate of relative increase in light intensity strongly enhance downwards swimming in Daphnia spp. and this enhancement increases with increasing fish kairomone and food concentration. This phenomenon may represent a ‘decision-making mechanism’ to realize the adaptive goal of DVM: at high fish predator densities, thus high kairomone concentrations, and sufficiently high food concentrations, DVM is profitable but not so at low concentrations. Body axis orientation in Daphnia spp. is controlled with regard to light-dark boundaries or contrasts. Under water, contrasts are present at the boundaries of the illuminated circular window which results from the maximum angle of refraction at 48–9° with the normal (Snell's window). Contrasts are fixed by the compound eye and appropriate turning of the body axis orients the daphnid in an upwards or an obliquely downwards direction. A predisposition for a positively or negatively phototactic orientation seems to be the result of a disturbed balance of the two oscillators governing normal swimming. Some investigators have tried to study DVM at a laboratory scale during a 24 h cycle. To imitate nature, properties of a natural water column, such as a large temperature gradient, were compressed into a few cm. With appropriate light intensity changes, vertical distributions looking like DVM were obtained. The results can be explained by phototactic reactions and the artificial nature of the compressed environmental factors but do not compare with DVM in the field. A mechanistic model of DVM based on phototaxis is presented. Both, primary and secondary phototaxis is considered an extension of normal swimming. Using the light intensity changes of dawn and the differential enhancement of kairomones and food concentrations, amplitudes of DVM could be simulated comparable to those in a lake. The most important adaptive significance of DVM is avoidance of visual predators such as juvenile fish. However, in the absence of fish kairomones, small-scale DVMs are often present, which were probably evolved for UV-protection, and are realized by not enhanced phototaxis. In addition, the ‘decision-making mechanism’ was probably evolved as based on the enhanced phototactic reaction to accelerations in the rate of relative changes in light intensity and the presence of fish kairomones.     

Ultrastructure of the epidermis of Meara stichopi (Platyhelminthes,Nemertodermatida) and associated extra-epidermal bacteria

This preliminary mechanistic model of normal swimming and phototactic behaviour in individual Daphnia was constructed using data and assumptions based on experiments and observations. Swimming under constant light intensity is characterized by short periods of upward movements alternating with equal periods of downward movements. Two oscillators are proposed that generate these phases in swimming. Unexpected shifts in depth, as observed in D. magna and D. longispina, are also present in the swimming of the computer daphnid and thus seem to be inherent to the underlying mechanism. As in real daphnids, during relative decreases in light intensity of low velocity, positive phototactic upward swimming is stepwise. With increasing velocity in the change in light, these steps disappear. When the model is triggered by a natural increase in light at dawn, a small downward movement results. Migration distance can be increased to commonly found depths of migrating Daphnia by the introduction of a fish exudate factor into the model, which enhances the phototactic response. Since attenuation of light in the water affects the phototactic swimming response, it also influences migration distance. The results of model calculations agree quite well with an empirical relationship between Secchi disc depth and amplitude of diel vertical migration in a number of lakes.     

Photoresponses of Chaoborus larvae

The diel vertical migration of Chaoborus larvae is a well known phenomenon. In order to quantify the ability of larvae to utilize underwater light cues in their migration, we measured photoresponses of fourth-instar Chaoborus punctipennis larvae in the laboratory. The action spectrum for these larvae was characterized by a maximum in sensitivity at 400 nm, a plateau at a lower sensitivity from 480 to 560 nm, and a region of much lower sensitivity at wavelengths longer than 620 nm. Dark-adapted larvae exhibited a positive phototaxis at low light intensity which shifted to a negative phototaxix as light intensity increased. At 540 nm the threshold intensity was 1.5 × 10^?9 W/m² for positive phototaxis and about 10^?6 W/m² for negative phototaxis. Light adaptation decreased sensitivity and altered the phototactic pattern. Larvae have a clear circadian rhythm in negative phototaxis, in which greatest responsiveness occurs early in the day. We suggest that the rhythm in photoresponsiveness primarily controls the timing of the downward migration at dawn.     

Light-induced swimming of Daphnia: can laboratory experiments predict diel vertical migration?

Vertical displacement velocity of a Daphniagaleata × hyalina clone was quantified inrelation to changes in the relative rate of lightchange. An increase in the latter variable triggers anenhanced swimming response, and this response is againelicited when a second increase in the rate ofrelative light increase is applied. Decreases in therate of light increase affect phototactic swimming ina similar way. The acceleration/deceleration assistedstimulus-response system is an extension of the ideaof phototaxis as the underlying behavioural mechanismfor vertical migration, and suggests that continuousaccelerations in light change also affect verticaldisplacements observed in the field. A simple dielvertical migration simulation model was used tocalculate the vertical displacement of Daphniain relation to the natural light change at sunrise.The calculated vertical displacement fits nicely inthe temporal range of the observed averaged downwardmigration of adult Daphnia in Lake Maarsseveen.The calculated migration amplitude, however, islarger than the change in mean population depthobserved in nature.     

Photoresponses of the copepod Mesocyclops edax

The predatory copepod Mesocyclops edax is an important componentof many zooplankton communities where it typically makes extensivedid vertical migrations. To describe the effect of light onadults we measured their photoresponses in the laboratory. Theresponse spectrum is characterized by a wide plateau of greatestsensitivity from about 480 – 580 nm. These animals areadapted to perceive light during the day since their regionof maximum sensitivity overlaps the spectral region of highestquantal intensity underwater (575 – 700 nm). The thresholdintensity for positive phototaxis by dark adapted animals wasabout 5 x 10^–1 Wm^–2 at 540 nm, and they were positivelyphototactic up to an intensity of 5 x 10^–1 Wm^–2.Above this intensity phototaxis is no longer observed. Light-adaptedanimals were less sensitive than dark-adapted, but their generalpattern of response to light intensity did not differ. Thereis no rhythm in phototaxis. Their photoresponses may providea mechanism for controlling vertical migration so as to minimizeexposure to planktivorous fish. ¹Contribution No. 1375-AEL from UM-CEES, Appalachian EnvironmentalLaboratory.     

Factors affecting the circatidal rhythm in vertical swimming of ovigerous blue crabs, Callinectes sapidus, involved in the spawning migration

Ovigerous blue crabs, Callinectes sapidus, are observed to undergo nocturnal ebb-tide transport (ETT) during their seaward spawning migration. A previous study found that females undergoing the spawning migration have a circatidal rhythm in vertical swimming, which serves as the biological basis for ETT. The present study asked three questions about this endogenous rhythm. First, does the rhythm occur in females with mature embryos regardless of whether they are undergoing ETT? Second, when exposed to a light/dark cycle in the laboratory, do ovigerous females only swim vertically at the time of ebb tide during the dark phase? Third, do attachments to the backs of ovigerous crabs affect the circatidal rhythm? The circatidal rhythm occurred in all crabs with mid-stage embryos that were prevented from undergoing ETT. The rhythm was unaffected by the light/dark cycle, which implies that migration can occur at lower light levels at depth during the day. Finally, attachments did not affect the rhythm, which suggests that tags and transmitters will not affect the spawning migration.     

Polarotaxis,gravitaxis and vertical phototaxis in the green flagellate,Euglena gracilis

A fully automatic computer-controlled video analysis system has been used to study the movement of the green unicellular flagellate, Euglena gracilis in a horizontal or vertical cuvette. In darkness, in the absence of gaseous gradients, most cells swim straight upwards. While in a horizontal cuvette the transition between positive and negative phototaxis is found at about 1.5 W m^-2, an excess of 30 W m^-2 is required to reverse the upward swimming (due to the combined stimulus of negative gravitaxis and positive phototaxis) in a vertical cuvette. By studying the swimming direction in horizontal and vertical cuvettes in polarized light irradiated from above or from the side, respectively, the dichroic orientation of the photoreceptor molecules can be determined in three dimensions with respect to the axes of the cell: In a horizontal cuvette, in a linearly polarized beam from above, the cells orient predominantly at an angle of about 30° clockwise off the electric dipole transition moment as seen from above. The behavior in a vertical cuvette with polarized light entering from above indicates that the photoreceptor pigments are dichroically oriented 60° counterclockwise from the flagellar plane (seen from the front end of the cell). Experiments with horizontal polarized light indicate that the photoreceptor transition moment deviates 25° clockwise off the long axis of the cell.Abbreviation PFB paraflagellar body Dedicated to Prof. Dr. W. Nultsch on the occasion of his 60th birthday     

A mechanism of predator-mediated induction of diel vertical migration in Daphnia hyalina

Predator avoidance is generally thought to be the most importantultimate reason for diel vertical migration in zooplankton.Combining field observations and experimental results, it isshown, first, that a phototactic reaction to relative changesin light intensity is at the base of a diel vertical migrationand, secondly, how this phototaxis is enhanced by a chemicalmediated by juvenile perch.     

Phototaxis in water fleas (Daphnia magna) is differently influenced by visible and UV light

The effects of vertical illumination with monochromatic lights on phototaxis of Daphnia magna in a test chamber were determined at five levels of equal quantal flux density (between 188 and 6.42 · 10⁻⁵ nEinstein). Visible adaptation light (500 nm) and subsequent spectral test light had the same quantal flux density. The animals reacted to ultraviolet light (260–380 nm) with negative phototaxis, whereas visible light (420–600 nm) caused positive phototaxis. Action spectra were determined, based on the evaluation of different parameters of phototactic behavior. The maximum spectral sensitivity in the ultraviolet was found at 340 nm. The maximum spectral efficiency in the visible varied in dependence on light intensity. Ecological consequences of the results are discussed. Accepted: 3 August 1998     

Light-induced chemotactic responses of the colorless flagellate,Polytomella magna,in the presence of photodynamic dyes

The colorless flagellate,Polytomella magna, does not show natural reactions toward light like phototaxis, photophobic response or photokinesis. However, if photosensitizers (e.g. riboflavin) are added to the culture an avoidance response toward a light field is induced. The photodynamic reaction depends on the presence of O₂. The action spectra are in good agreement with the absorption spectra of the tested dyes. The photobehavioral response in the presence of riboflavin seems to be based on a negative chemotaxis toward H₂O₂ which is produced when the dye is irradiated.     

Action spectra for phototaxis in zoospores of the brown algaPseudochorda gracilis

Summary Action spectra for phototaxis in zoospores of brown alga,Pseudochorda gracilis (Laminariales), were examined in the wavelength range between 300 and 600 nm using the Okazaki Large Spectrograph and a video tracking system. The direction of swimming (both in percent cells swimming in parallel with the stimulating light, and in mean angle of cell movement) was dependent on the wavelength. The action spectra had two peaks at 420 and 460 nm, while light above 500 nm was not effective in changing the swimming direction of the cells.Abbreviations TCMA tracker-cell movement analyzer system - CMA cell movement analyzer program     

Negative Phototaxis in Blepharisma japonicum

The protozoan Blepharisma japonicum showed negative phototaxis caused by transient reversal of the direction of ciliary beat and changes of swimming velocity induced with varying intensities of light. The ciliary reversal occurred at 1–2 sec after a sudden increase in light intensity. When light intensity was decreased, no response was observed. Moreover, the ciliates swam fast in light areas but slowly in dark areas; the mean velocity of swimming was 80 μ m/sec at 5 × 10² lux but reached about 400 μMm/sec at 5 × 10³ lux. In addition, the cell body elongated in response to light application; the mean length of the body was 308 μm at 5 × 10² lux, which increased to 397 μ m at 10⁴ lux. Such body elongation seems to contribute to rapid swimming. Negative phototaxis may be an important behavior in B. japonicum because the organisms are killed by exposure to strong light.     

What goes down must come up: symmetry in light-induced migration behaviour of Daphnia

During a short period of the year, Daphnia may perform a phenotypically induced diel vertical migration. For this to happen, light-induced swimming reactions must be enhanced both at dawn and at dusk. Enhanced swimming in response to light intensity increase can be elicited by fish-associated kairomone in the laboratory, if food is sufficiently available. However, during the light change at dusk the Daphnia are still in the hypolimnion, where no fish kairomone is present and both temperature and food availability is low. Still, what goes down must come up. This raises questions about how Daphnia tunes its light-induced swimming behaviour to prevailing conditions such that a normal diel vertical migration can be performed. We investigated the symmetry in behavioural mechanism underlying these diel vertical migrations in the hybrid Daphnia galeata × hyalina (Cladocera; Crustacea), with special interest for the environmental cues that are known to affect swimming in response to light increase. That is, we tested whether fish- associated kairomone, food availability, and temperature affected both swimming in response to light intensity increase and decrease similarly. We quantified swimming behaviour during a sequentially increased rate of light change. Vertical displacement velocity was measured and proved to be linearly related to the rate of the light change. The slope (PC) of the function depends on the value of the factors kairomone concentration, food availability, and temperature. The changes of the PC with kairomone concentration and with temperature were similar both at light intensity increases and decreases. The PC also increased with food concentration, although during light increases in a different way from during light intensity decreases. Low food availability inhibited swimming in response to light intensity increase, but enhanced swimming in response to light intensity decrease. Hence, ascent from the deep water layers with low food concentration at dusk is facilitated. These causal relations are part of a proximate decision-making mechanism which may help the individual Daphnia to tune migration to predation intensity and food availability.     

Diel vertical migration: modelling light-mediated mechanisms

Light is generally regarded as the most likely cue used by zooplanktonto regulate their vertical movements through the water column.However, the way in which light is used by zooplankton as acue is not well understood. In this paper we present a mathematicalmodel of diel vertical migration which produces vertical distributionsof zooplankton that vary in space and time. The model is usedto predict the patterns of vertical distribution which resultwhen animals are assumed to adopt one of three commonly proposedmechanisms for vertical swimming. First, we assume zooplanktontend to swim towards a preferred intensity of light. We thenassume zooplankton swim in response to either the rate of changein light intensity or the relative rate of change in light intensity.The model predicts that for all three mechanisms movement isfastest at sunset and sunrise and populations are primarilyinfluenced by eddy diffusion at night in the absence of a lightstimulus. Daytime patterns of vertical distribution differ betweenthe three mechanisms and the reasons for the predicted differencesare discussed. Swimming responses to properties of the lightfield are shown to be adequate for describing did vertical migrationwhere animals congregate in near surface waters during the eveningand reside at deeper depths during the day. However, the modelis unable to explain how some populations halt their ascentbefore reaching surface waters or how populations re-congregatein surface waters a few hours before sunrise, a phenomenon whichis sometimes observed in the field. The model results indicatethat other exogenous or endogenous factors besides light mayplay important roles in regulating vertical movement.     

Top-down control of natural phyto- and bacterioplankton prey communities by Daphnia magna and by the natural zooplankton community of the hypertrophic Lake Blankaart

Biomanipulation, through the reduction of fish abundance resulting in an increase of large filter feeders and a stronger top-down control on algae, is commonly used as a lake restoration tool in eutrophic lakes. However, cyanobacteria, often found in eutrophic ponds, can influence the grazing capacity of filter feeding zooplankton. We performed grazing experiments in hypertrophic Lake Blankaart during two consecutive summers (1998, with and 1999, without cyanobacteria) to elucidate the influence of cyanobacteria on the grazing pressure of zooplankton communities. We compared the grazing pressure of the natural macrozooplankton community (mainly small to medium-sized cladocerans and copepods) with that of large Daphnia magna on the natural bacterioplankton and phytoplankton prey communities. Our results showed that in the absence of cyanobacteria, Daphnia magna grazing pressure on bacteria was higher compared to the grazing pressure of the natural zooplankton community. However, Daphnia grazing rates on phytoplankton were not significantly different compared to the grazing rates of the natural zooplankton community. When cyanobacteria were abundant, grazing pressure of Daphnia magnaseemed to be inhibited, and the grazing pressure on bacteria and phytoplankton was similar to that of the natural macrozooplankton community. Our results suggest that biomanipulation may not always result in a more effective top-down control of the algal biomass.