Phototactic attraction in light trap experiments: A mathematical model

A mathematical model has been developed to evaluate the contribution of phototactic responses in light-induced accumulations. A set of differential equations describes the organism density inside and outside of the light trap as well as on its border.The model predicts that organisms first occupy the rim of the light trap and then gradually fill the interior. This has been substantiated experimentally. Computer simulations of light-induced accumulations in a light trap agree with the measured values. The distance from the trap within which organisms respond phototactically depends on the organism density, which determines the amount of stray light, and on the zero threshold for both phototaxis and photophobic response.     

Evolution of phototaxis

Phototaxis in the broadest sense means positive or negative displacement along a light gradient or vector. Prokaryotes most often use a biased random walk strategy, employing type I sensory rhodopsin photoreceptors and two-component signalling to regulate flagellar reversal. This strategy only allows phototaxis along steep light gradients, as found in microbial mats or sediments. Some filamentous cyanobacteria evolved the ability to steer towards a light vector. Even these cyanobacteria, however, can only navigate in two dimensions, gliding on a surface. In contrast, eukaryotes evolved the capacity to follow a light vector in three dimensions in open water. This strategy requires a polarized organism with a stable form, helical swimming with cilia and a shading or focusing body adjacent to a light sensor to allow for discrimination of light direction. Such arrangement and the ability of three-dimensional phototactic navigation evolved at least eight times independently in eukaryotes. The origin of three-dimensional phototaxis often followed a transition from a benthic to a pelagic lifestyle and the acquisition of chloroplasts either via primary or secondary endosymbiosis. Based on our understanding of the mechanism of phototaxis in single-celled eukaryotes and animal larvae, it is possible to define a series of elementary evolutionary steps, each of potential selective advantage, which can lead to pelagic phototactic navigation. We can conclude that it is relatively easy to evolve phototaxis once cell polarity, ciliary swimming and a stable cell shape are present.     

Effect of external ionic environment on phototaxis of Volvox carteri

The sign of phototaxis in Volvox carteri is temperature-dependent;positive at room temperature and negative at low temperature.Modification of the tactic sign by external ions, pH and chemicalswas studied. The addition of 30 mM potassium ion to the mediumchanged the tactic sign from positive to negative, and a mediumwith a high pH elicited positive phototaxis. An increase inthe potassium or hydrogen ion concentration raised the reversaltemperature of the phototactic sign, and the addition of magnesiumor calcium ion also raised the reversal temperature of the signslightly. Valinomycin, a highly specific ionophore of potassium,raised the reversal temperature. CCCP, DCMU and DCCD, whichdepolarize biological membranes, also raised the reversal temperature.These results show that the sign of phototaxis is determinedby membrane polarization; on depolarization of the membranethe sign of phototaxis changes from positive to negative. Ethanol lowered the reversal temperature, and sodium azide inhibitedboth positive and negative phototaxis. The effects of ethanoland azide indicate that depolarization of the membrane is notthe only factor that induces change in the phototactic sign. (Received July 23, 1979; )     

Collective Motion of Spherical Bacteria

A large variety of motile bacterial species exhibit collective motions while inhabiting liquids or colonizing surfaces. These collective motions are often characterized by coherent dynamic clusters, where hundreds of cells move in correlated whirls and jets. Previously, all species that were known to form such motion had a rod-shaped structure, which enhances the order through steric and hydrodynamic interactions. Here we show that the spherical motile bacteria Serratia marcescens exhibit robust collective dynamics and correlated coherent motion while grown in suspensions. As cells migrate to the upper surface of a drop, they form a monolayer, and move collectively in whirls and jets. At all concentrations, the distribution of the bacterial speed was approximately Rayleigh with an average that depends on concentration in a non-monotonic way. Other dynamical parameters such as vorticity and correlation functions are also analyzed and compared to rod-shaped bacteria from the same strain. Our results demonstrate that self-propelled spherical objects do form complex ordered collective motion. This opens a door for a new perspective on the role of cell aspect ratio and alignment of cells with regards to collective motion in nature.     

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.     

Nutritional state and collective motion: from individuals to mass migration

In order to move effectively in unpredictable or heterogeneous environments animals must make appropriate decisions in response to internal and external cues. Identifying the link between these components remains a challenge for movement ecology and is important in understanding the mechanisms driving both individual and collective motion. One accessible way of examining how internal state influences an individual''s motion is to consider the nutritional state of an animal. Our experimental results reveal that nutritional state exerts a relatively minor influence on the motion of isolated individuals, but large group-level differences emerge from diet affecting inter-individual interactions. This supports the idea that mass movement in locusts may be driven by cannibalism. To estimate how these findings are likely to impact collective migration of locust hopper bands, we create an experimentally parametrized model of locust interactions and motion. Our model supports our hypothesis that nutrient-dependent social interactions can lead to the collective motion seen in our experiments and predicts a transition in the mean speed and the degree of coordination of bands with increasing insect density. Furthermore, increasing the interaction strength (representing greater protein deprivation) dramatically reduces the critical density at which this transition occurs, demonstrating that individuals'' nutritional state could have a major impact on large-scale migration.     

Gametic behavior in a marine green alga, Monostroma angicava: an effect of phototaxis on mating efficiency

The role of phototactic behavior of gametes was tested experimentally in the slightly anisogamous marine green alga Monostroma angicava Kjellman, and the effect of phototaxis on mating efficiency was discovered. Both male and female gametes showed positive phototaxis in response to a white light source. In contrast, they did not respond to a red light source. Their swimming velocity did not differ between these two illuminating light sources. It was, therefore, suggested that the search ability of the gamete itself might not vary between phototactic and non-phototactic conditions. The number of zygotes formed during the mating process may be expressed as the product of the number of encounters between male and female gametes and the fraction of encounters that result in sexual fusion. In this study, with high densities of male and female gametes mixed in test tubes, almost all minor (fewer in number) gametes fused sexually within 10 min. After dilution of the gamete suspensions by half, mating efficiency in test tubes illuminated by white light from above was higher than that in dark controls. This suggests that male and female gametes gathered at the water surface through their positive phototaxis, thus increasing the rate of encounters. Mating efficiency also decreased if the test tubes were illuminated from above by white light and also shaken. Since negative phototaxis is clearly shown in planozygotes, we suggest that positive phototaxis of male and female gametes in M. angicava is an adaptive trait for increasing the rate of gametic encounters rather than for the dispersal of zygotes as previously reported for zoospores of some marine algae. Received: 12 February 1999 / Revision accepted: 24 May 1999     

昆虫趋光性及其机理的研究进展

依据目前已有资料 ,从行为学、生理学及田间应用调查等方面概述了近几十年昆虫趋光性的国内外研究进展。其中 ,行为学与生理学研究较多 ,且两者结果基本一致 ,相互补充 ,为趋光性机制的假说提供了可靠的依据。关于昆虫趋光性机制的假说较多 ,其中报道较多的是光干扰假说、光定向行为假说和生物天线假说 3种 ,现在较为普遍接受的是前两者。光干扰假说是指刺眼作用干扰昆虫的正常活动导致趋光 ,而光定向行为假说则指昆虫趋光是由于光定向行为所致     

How 5000 independent rowers coordinate their strokes in order to row into the sunlight: Phototaxis in the multicellular green alga <Emphasis Type="Italic">Volvox</Emphasis>

Background

The evolution of multicellular motile organisms from unicellular ancestors required the utilization of previously evolved tactic behavior in a multicellular context. Volvocine green algae are uniquely suited for studying tactic responses during the transition to multicellularity because they range in complexity from unicellular to multicellular genera. Phototactic responses are essential for these flagellates because they need to orientate themselves to receive sufficient light for photosynthesis, but how does a multicellular organism accomplish phototaxis without any known direct communication among cells? Several aspects of the photoresponse have previously been analyzed in volvocine algae, particularly in the unicellular alga Chlamydomonas.

Results

In this study, the phototactic behavior in the spheroidal, multicellular volvocine green alga Volvox rousseletii (Volvocales, Chlorophyta) was analyzed. In response to light stimuli, not only did the flagella waveform and beat frequency change, but the effective stroke was reversed. Moreover, there was a photoresponse gradient from the anterior to the posterior pole of the spheroid, and only cells of the anterior hemisphere showed an effective response. The latter caused a reverse of the fluid flow that was confined to the anterior hemisphere. The responsiveness to light is consistent with an anterior-to-posterior size gradient of eyespots. At the posterior pole, the eyespots are tiny or absent, making the corresponding cells appear to be blind. Pulsed light stimulation of an immobilized spheroid was used to simulate the light fluctuation experienced by a rotating spheroid during phototaxis. The results demonstrated that in free-swimming spheroids, only those cells of the anterior hemisphere that face toward the light source reverse the beating direction in the presence of illumination; this behavior results in phototactic turning. Moreover, positive phototaxis is facilitated by gravitational forces. Under our conditions, V. rousseletii spheroids showed no negative phototaxis.

Conclusions

On the basis of our results, we developed a mechanistic model that predicts the phototactic behavior in V. rousseletii. The model involves photoresponses, periodically changing light conditions, morphological polarity, rotation of the spheroid, two modes of flagellar beating, and the impact of gravity. Our results also indicate how recently evolved multicellular organisms adapted the phototactic capabilities of their unicellular ancestors to multicellular life.

     

Ecological consequences of photomovement and photobleaching in the marine flagellate Cryptomonas maculata

Abstract The marine flagellate Cryptomonas maculata is bleached and eventually killed by exposure to even moderate white-light fluence rates. Bleaching affects all of its photosynthetic pigments and the kinetics depend on the fluence rate of the radiation the organisms are exposed to. Nitrogen-deficient cells which show a reduced pigment concentration and impaired photosynthetic efficiency tolerate bleaching white-light exposure far better than the normally colored cells. In their natural environment the organisms escape this situation by a pronounced negative phototaxis at fluence rates above 3.6 klx (= 15 W.m⁻²), while they show positive phototaxis at lower fluence rates. In nitrogen-deficient cells, however, though being less prone to photobleaching, negative phototaxis commences even at a fluence rate of about 830 lx (= 3.5 W.m⁻²). The ecological consequences of the remarkable light sensitivity and the phototactic orientation are being discussed.     

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.     

Sudden reversal of phototaxis during the development of nestling birds

Starling, Sturnus vulgaris, nestlings from about 10 days of age moved away from light, i.e. they were negatively phototactic. However, several days before fledging, they changed to move towards light, probably a necessary prerequisite for fledging. The phototactic reversal was correlated with physical development and the ability to fly. In contrast to most studies or newly acquired behaviour, there was no change in response time associated with the reversal. However, hunger reduced the response time of hand-reared nestlings. It is suggested that a positive phototaxis for strong fliers or negative phototaxis for flightless young is an adaptive escape response. The reversal of phototaxis is probably a general feature of avian development.     

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.     

Ciliary behavior of a negatively phototactic Chlamydomonas reinhardtii

With an instrument that can record the motion of both cilia of the unicellular alga Chlamydomonas reinhardtii for many hours, the behavioral differences of its two cilia have been studied to determine their specific role in phototaxis. The organism was held on a fixed micropipette with the plane of ciliary beating rotated into the imaging plane of a quadrant photodetector. The responses to square-wave light patterns of a wide range of temporal frequencies were used to characterize the responses of each cilium. Eighty-one cells were examined showing an unexpectedly diverse range of responses. Plausible common signals for the linear and nonlinear signals from the cell body are suggested. Three independent ciliary measures--the beat frequency, stroke velocity, and phasing of the two cilia--have been identified. The cell body communicates to the cilia the direction of phototaxis the cell desires to go, the absolute light intensity, and the appropriate graded transient response for tracking the light source. The complexity revealed by each measure of the ciliary response indicates many independent variables are involved in the net phototactic response. In spite of their morphological similarity, the two cilia of Chlamydomonas respond uniquely. Probably the signals from the cell body fan out to independent pathways in the cilia. Each cilium modifies the input in its own way. The change in the pattern of the effective and recovery strokes of each cilium associated with negative phototaxis has been demonstrated and its involvement in phototactic turning is described.     

Functional aspects of secondary carotenoids in Haematococcus lacustris (Girod) Rostafinski (Volvocales). V. Influences on photomovement

Secondary carotenoids are suspected to modulate photomovement in Haematococcus lacustris [Girod] Rostafinski (Volvocales). To investigate the influence of these extrachloroplastic ketocarotenoids on phototactic and photophobic responses in the flagellate stage of the green alga, flagellate suspensions differing in the content of secondary carotenoids were grown from green and red aplanospores. Photo-orientation of these flagellates induced by unilateral irradiation was investigated using a computer-aided system for microscopic image analysis. Results were hypothetically summarized as follows: (1) Diminution of precision of the positive phototaxis was found in red flagellates. This might be due to cellular shading of the blue-light-sensitive photoreceptor by secondary carotenoids. (2) Red flagellates exhibited an increase in the photophobic response. This finding is discussed in relation to an adaptive increase of the photoreceptor sensitivity, thought to be a result of the higher optical density of the corresponding cell suspension in the blue wavelength region.     

Effect of external factors on phototaxis of Chlamydomonas reinhardtii. I. Light.

1. A fully automated phototaxis monitoring device is described for measuring photo-topotactic responses of flagellated organisms. 2. Photokinesis can be demonstrated in Chlamydomonas cells only after a dark period of about 72 hrs. 3. Pre-darkening of a few hours duration raises the phototactic disposition, whereas pre-illumination has no significant effect. 4. Circadian rhythms can be initiated by only one period of darkness or lower light intensity, whereas a period of higher intensity does not induce rhythms. The period length of the circadian rhythms is about 24 hrs.     

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.     

PHOTOTAXIS IN CHLAMYDOMONAS REINHARDTII

Parameters which distinguish phototaxis from random motility in Chlamydomonas reinhardtii have been defined with quantitative assays. The phototactic responses in photosynthetic, mixotrophic, and heterotrophic cultures were highest during exponential growth and declined rapidly as the cultures entered stationary phase. In contrast, random motility was relatively constant throughout growth. Phototaxis and motility also differ in their sensitivity to azide and antimycin A. Both of these drugs inhibited phototaxis within 5 min, but motility was unaffected for at least 30 min. Phototaxis and motility have different ion requirements. Optimum motility was observed in the presence of either Ca⁺⁺ or Mg⁺⁺; phototaxis required Ca⁺⁺ and either K⁺ or NH₄⁺. Photosynthesis is not required for phototaxis, since phototaxis was not inhibited by dichlorophenyldimethyl urea, and a mutant lacking chlorophyll was phototactic.     

Photoresponses of second-instar Chaoborus larvae

The diel vertical migration of Chaoborus larvae varies with larval instar. Although light is involved in the control of vertical migration the contribution of larval photoresponses is unknown. In order to describe ontogenetic changes in larval photoresponses we measured photoresponses of second-instar Chaoborus punctipennis larvae in the laboratory. The response spectrum of these larvae had peaks in sensitivity at 420 and 620 nm with a wide plateau of lower sensitivity from 460 to 600 and 640 to 680 nm. Dark adapted larvae were positively phototactic at intensities from 10^?7 to 10¹ Wm^?2 at 420 nm. The level of response decreased somewhat above 10^?4 Wm^?2, and above 10^?2 Wm^?2 a small proportion of larvae shifted to a negative phototaxis. At 420 nm the threshold intensity was about 10^?7 Wm^?2 for positive phototaxis and 10^?2 Wm^?2 for negative phototaxis. Light adaptation increased the threshold intensity for positive phototaxis. The differences in larval photoresponses between second- and fourth-instar larvae suggests that the young instars are adapted to the photoenvironment of the water column and older larvae are adapted to avoid the water column except at very low light intensities. These predictions match the diel distribution of these larvae.     

Effects of UV-B on motility and photobehavior in the green flagellate,Euglena gracilis

UV-B inhibits the motility of the green flagellate, Euglena gracilis, at fluences rates higher than those expected to occur in the natural sunlight even when the stratospheric ozone layer is partially reduced by manmade pollutants. The phototactic orientation of the cells, however, is drastically impaired by only slightly enhanced levels of UV-B irradiation. Since only negative phototaxis (movement away from a strong light source) is impaired while positive phototaxis (movement toward a weak light source) is not, the delicate balance by which the organisms adjust their position in their habitat is disturbed. Under these conditions the cells are unable to retreat from hazardous levels of radiation and are eventually killed not by the UV-B irradiation but by photobleaching of their photosynthetic pigments in the strong daylight at the surface.