Components of phototaxis of the nematode Mermis nigrescens

Summary The gravid females of Mermis are positively phototaxic at the time of their migration to egglaying sites in vegetation on which their grasshopper hosts feed. On a horizontal felt surface, segments of the path traced by the tail are oriented approximately towards a source of monochromatic light in the 350–540 nm region, but are not oriented at longer wavelengths and in the dark. The components of this phototaxis include locomotion by the posterior 4/5 of the body, orientational bending of the neck region while the anterior is held above the substrate, and a scanning motion (bending) of the head region (anterior 2 mm). Like other nematodes and snakes, propulsion is associated with posteriorly propagated body waves, but unlike other animals known, the waves tend to lie perpendicular to a felt surface, and unlike other nematodes, contact with the surface is on the female's ventral surface. The body waves are initiated by the motion of the anterior 1/5 (15 mm) of the body, the average orientation of which determines the path of the following 4/5.During phototaxis, the anterior tip is swung both sideways and vertically about the direction towards the light source. The tip motion is a result of a scanning motion of the head and a slower orientational bending of the neck. The base of the head appears to be actively directed towards the source by the bending of the neck. This behavior can resolve two light sources positioned 120° apart but not 90° apart. The scanning motion of the head is independent of neck orientation and appears to enhance the probability of discovering the direction of a new source. Discovery is followed by a directed turn of the base of the head towards the source which is initiated by the bending of the neck. Locomotion of the body follows the path of the anterior through the turn and phototaxis is thus initiated.     

Unique two-photoreceptor scanning eye of the nematode Mermis nigrescens

A single eye is present in females of the nematode Mermis nigrescens. A pigment cup occupies the entire cross section near the anterior tip of the worm, and the curved cuticle at the tip becomes a cornea. The shading pigment is hemoglobin instead of melanin. The eye has been shown to provide a positive phototaxis utilizing a scanning mechanism; however, the eye's structure has not been sufficiently described. Here, we provide a reconstruction of the eye on the basis of light and electron microscopy of serial sections. Hemoglobin crystals are densely packed in the cytoplasm of expanded hypodermal cells, forming the cylindrical shadowing structure. The two putative photoreceptors are found laterally within the transparent conical center of this structure where they would be exposed to light from different anterior fields of view. Each consists of a multilamellar sensory process formed by one of the dendrites in each of the two amphidial sensory nerve bundles that pass through the center. Multilamellar processes are also found in the same location in immature adult females and fourth stage juvenile females, which lack the shadowing pigment and exhibit a weak negative phototaxis. The unique structure of the pigment cup eye is discussed in terms of optical function, phototaxis mechanism, eye nomenclature, and evolution.     

A biased random walk model for the trajectories of swimming micro-organisms

The motion of swimming micro-organisms that have a preferred direction of travel, such as single-celled algae moving upwards (gravitaxis) or towards a light source (phototaxis), is modelled as the continuous limit of a correlated and biased random walk as the time step tends to zero. This model leads to a Fokker-Planck equation for the probability distribution function of the orientation of the cells, from which macroscopic parameters such as the mean cell swimming direction and the diffusion coefficient due to cell swimming can be calculated. The model is tested on experimental data for gravitaxis and phototaxis and used to derive values for the macroscopic parameters for future use in theories of bioconvection, for example.     

External mechanical control of the timing of bend initiation in sea urchin sperm flagella

The movement parameters of a sea urchin sperm flagellum can be manipulated mechanically by applying various modes of periodic vibrations to the sperm head held by suction in the tip of a micropipette. The beat frequency of the flagellum readily synchronizes with the frequency of the externally imposed lateral vibration, and the plane of flagellar bending waves adapts itself to the plane of the pipette vibration (Gibbons et al., J. Cell Biol. 101:270a, 1985; Nature 325: 351-352, 1987). In this study, we observed the particular effects of external asymmetric forces on flagellar beating parameters by vibrating the micropipette holding the sperm head in a transverse sawtooth-like motion composed of a rapid effective stroke and a slower recovery stroke, while keeping the vibration frequency constant. The results demonstrate that the timing of bend initiation within the flagellar beat cycle can be controlled mechanically by changing the time point within the vibration cycle at which the micropipette changes its direction of motion. A switch in the sidedness of the asymmetric movement of the micropipette produces dramatic changes in the profiles of bend growth in the basal 5 microns of the flagellum but has almost no effect on the asymmetry or other parameters of bending in the mid- and distal regions of the flagellum. Our results suggest that elastic strain within the basal region of the flagellar structure may play a more significant role in the process of bend initiation than has been realized heretofore.     

Orientation to shorelines by the supratidal amphipod Talorchestia longicornis: Wavelength specific behavior during sun compass orientation

If released in water or on sand the supratidal amphipod Talorchestia longicornis Say amphipods moves in the onshore direction. The present study was designed to determine whether this species uses the sun as a cue for orientation and if so, which visual pigment in the compound eyes is involved. When tested in an apparatus with a view of only the sun and sky amphipods were disoriented when the sun was obscured by clouds. However, when the sun was visible, they oriented in the onshore direction of their home beach in both water and air during both the morning and afternoon. Resetting the time of their circadian rhythm in activity with either an altered light:dark or diel temperature cycle also reset the chronometric mechanism associated with sun compass. orientation. T. longicornis has two visual pigments with absorption maxima near 420 nm and 520 nm. Only the 420 nm pigment is used for sun compass orientation, which may be an adaptation for increasing the contrast between the sun and background scattered skylight or for detecting the radiance distribution of skylight. Irradiating the 520 nm absorbing pigment alone induced positive phototaxis to the sun but not onshore orientation. Thus, T. longicornis shows wavelength specific behavior by using only one of its visual pigments for sun compass orientation.     

Raman spectroscopic evidence for the microenvironmental change of some tyrosine residues of lens proteins in cold cataract

We found new photochemical intermediate of third rhodopsin-like pigment (tR) or slow cycling rhodopsin-like pigment (sR) in Halobacterium halobium, which was produced by simultaneous illumination with red and blue light. This illumination is employed for measurements of negative phototaxis. The formation of this intermediate is fast. (With the instrument used, it could not be measured.) The half-time of its decay is ca 150 msec in 4 M NaCl, pH 7.0 at 20 degrees C. The maximum of absorbance is located at 510-530 nm.     

PHOTOREACTIONS OF PARTIALLY BLINDED WHIP-TAIL SCORPIONS

The experiments dealt with in this paper were devised to ascertain (1) the relative effectiveness as photoreceptors of the whip-tail scorpion''s median eyes, lateral eye groups, and cutaneous sensitive areas, and (2) the effect on orientation produced by symmetrical and by asymmetrical interference with the photoreceptive mechanism. Each of the receptors was eliminated unilaterally and bilaterally, singly and in combinations with other receptors. In all, sixteen different abnormal conditions of the photoreceptive apparatus were produced. The reactions of animals thus partially blinded were measured in terms of angular deflection from an initial path of locomotion. Measurements obtained under anterior, lateral, and bilaterally balanced illumination were compared with measurements made on normal animals under the same conditions of illumination. The change from the normal reaction induced by covering a photoreceptor was taken as an index of the effectiveness of the receptor prevented from functioning. By comparing the values of the changes from normal reactions produced by the elimination of the several receptors, their relative effectiveness is approximated as median eyes : lateral eyes : cutaneous sensitive areas :: 1:1.6:2.2. All animals in which the receptive mechanism was rendered functionally asymmetrical exhibited, when subJected to bilaterally balanced illumination, deflections toward the side which had been made less sensitive. In a series of measurements made on animals in ten different conditions of asymmetry the amplitudes of the deflections were proportional to the degree of unbalance which had been produced in the photosensitive mechanism. Animals in which the receptive mechanism was reduced but left in a symmetrical condition maintained an undisturbed balance of reaction when subjected to equal, opposed lights. Under lateral or anterior illumination the rate of attaining a new direction of orientation was reduced in proportion to the extent of the interference with the receptive mechanism. The reactions of symmetrically and asymmetrically blinded scorpions indicate that orientation is attained and maintained by a transmission of impulses to the muscles of locomotion which is proportional bilaterally to the excitation of the symmetrically located photoreceptors. In their effect on orientation the three pairs of receptors are completely coordinated. Orientation depends upon bringing the excitation of the receptive mechanism as a whole into bilateral equilibrium.     

A one-instant mechanism of phototaxis in the cyanobacterium Phormidium uncinatum

Abstract The front portion ('head') of a Phormidium uncinatum trichome responds to a step-down in light intensity [10], whereas the rear end ('tail') responds to step-up stimuli [11]. We studied this phenomenon further and found that: (i) illumination of the head caused a reversal within 1 min in only 6% of the trichomes, whereas illumination of the tail produced a reversal in 56% of trichomes; (ii) if a light spot trained on the head of a trichome was moved together with the trichome, there were no reversals for > 20 min, while the normal rate of spontaneous reversals was once per 3–5 min. Shifting the light spot from the head to the tail caused a reversal within 1–2 min; (iii) both the step-up response of the tail and phototaxis were suppressed by an inhibitor of methylation, ethionine, but not by inhibitors of photosynthesis (DCMU, DBMIB); phototaxis and the step-up response of the tail were absent in red light ( λ > 670 nm). It was concluded that trichomes of P. uncinatum possess a one-instant mechanism of phototaxis, which involves a simultaneous comparison of light intensities between two parts of the organism.     

Ultrastructural study of the retinal pigment epithelium during metamorphosis in the sea lamprey (Petromyzon marinus L.)

Summary The sequence of morphological changes in the retinal pigment epithelium during the metamorphic period of the sea lamprey Petromyzon marinus L. has been investigated using electron microscopy. At early metamorphic stages (stages I and II), photoreceptors are present in a small zone of the retina. During these stages, the lateral surface of the epithelial cells shows zonulae occludentes and adhaerentes. The degree of cell differentiation varies throughout the retinal pigment epithelium. Cells covering the differentiated photoreceptors in the central retina have phagosomes, whereas pigment granules appear only in the retinal pigment epithelium dorsal to the optic nerve head. Most epithelial cells have myeloid bodies; their morphology is more complex around the optic nerve head. At stage III, when photoreceptors develop over the whole retina, the distribution of cytoplasmic organelles is almost homogeneous in the retinal pigment epithelium. Subsequently, the basal plasma membrane of the epithelial cells becomes progressively folded and their apical processes enlarged. In addition, extensive gap junctions develop between retinal pigment cells. In late metamorphic stages, noticeable growth of myeloid bodies occurs and consequently the retinal pigment epithelium resembles that of the adult. This study also describes, for the first time, the presence of wandering phagocytes in the retinal pigment epithelium of lampreys; their role in melanosome degradation is discussed.     

Swimming behaviour of the unicellular biflagellate Oxyrrhis marina: in vivo and in vitro movement of the two flagella

The movement of the 2 flagella of Oxyrrhis marina was examined with respect to their individual waveforms and the swimming behavior of the organism. The longitudinal flagella propagated helicoidal waves whose amplitude decreased toward the tip of th flagellum. Their beat frequencies were 50-60 Hz. The transverse flagella beat helicoidally within a furrow. Sudden changes in the direction of the cell trajectories were generated by transient arrests of the longitudinal flagellum beat, which were accompanied by a switch from the backward orientation to a forward one. This sweeping motion generated the rotation of the cell body. Ca2+ ions highly stimulated the frequencies of this arrest response, which compared to the "walking-stick" behavior of sea urchin spermatozoa. Isolated flagella were ATA-reactivated after detergent treatment. They exhibited 2 types of motion within the same experimental conditions. A progressive helicoidal motion was generated upon longitudinal flagellum reactivation, whereas a rolling motion with little progression characterized transverse flagellum reactivation. The differences in motile behavior reflect regulations of flagellar movement which were not destroyed by the isolation procedure and may be indicative of regulation by accessory structures.     

Motion and vision: why animals move their eyes

Nearly all animals with good vision have a repertoire of eye movements. The majority show a pattern of stable fixations with fast saccades that shift the direction of gaze. These movements may be made by the eyes themselves, or the head, or in some insects the whole body. The main reason for keeping gaze still during fixations is the need to avoid the blur that results from the long response time of the photoreceptors. Blur begins to degrade the image at a retinal velocity of about 1 receptor acceptance angle per response time. Some insects (e.g. hoverflies) stabilise their gaze much more rigidly than this rule implies, and it is suggested that the need to see the motion of small objects against a background imposes even more stringent conditions on image motion. A third reason for preventing rotational image motion is to prevent contamination of the translational flow-field, by which a moving animal can judge its heading and the distances of objects. Some animals do let their eyes rotate smoothly, and these include some heteropod molluscs, mantis shrimps and jumping spiders, all of which have narrow linear retinae which scan across the surroundings. Hymenopteran insects also rotate during orientation flights at speeds of 100–200° s⁻¹. This is just consistent with a blur-free image, as are the scanning speeds of the animals with linear retinae. Accepted: 29 April 1999     

Effects of light on pigment development in the echiuran worm, Bonellia viridis

In rhe echiuran Bonellia viridis the green pigment first develops in the gastrula, before the formation of the trochal rings, and the trochophores acquire a deep green pigmentation before hatching. Eggs that were cultured under continuous illumination (2000–4000 lx) did not develop any green pigment, and although the trochophores hatched normally, they lacked pigment entirely. The unpigmented trochophores that were kept under continuous illumination developed into unpigmented males and females. The far-blue (380–400 nm) and red (620–640 nm) regions were more effective in preventing pigment development than the blue, green and yellow regions of the spectrum. Illumination of the eggs before the gastrula stage did not affect the development of pigment when these were subsequently returned to the dark. When unpigmented trochophores, that had been cultured in the light, were placed in the dark they acquired a slight pigmentation, but this was much less intense than that of trochophores that had been cultured in the dark throughout. Pigmented trochophores were more vulnerable to high light intensities than unpigmented ones.     

On the orientation of stripes in fish skin patterning

This paper is focused on the study of the stripes orientation in the fish skin patterns. Based on microscopic observations of the pigment cells behavior at the embryonic stage, the key aspects of the pigmentation process are implemented in an experimental reaction-diffusion system. The experiment consists of a photosensitive Turing pattern of stripes growing directionally in one direction with controlled velocity. Different growth velocities of the system rearrange the stripes in the same three possible orientations observed in the skin of the colored fishes: parallel, oblique, and perpendicular. Our results suggest that the spreading velocity of the pigment cells in the fish dermis selects the orientation in the patterning processes.     

A negative effector of blue light-induced and gravitropic bending in Arabidopsis

Although sessile, plants are able to grow toward or away from an environmental stimulus. Important examples are stem or leaf orientation of higher plants in response to the direction of the incident light. The responsible photoreceptors belong to the phototropin photoreceptor family. Although the mode of phototropin action is quite well understood, much less is known of how the light signal is transformed into a bending response. Several lines of evidence indicate that a lateral auxin gradient is responsible for asymmetric cell elongation along the light gradient within the stem. However, some of the molecular key players leading to this asymmetric auxin distribution are, as yet, unidentified. Previously, it was shown that phototropin gets autophosphorylated upon illumination and binds to a scaffold protein termed NPH3 (for nonphototropic hypocotyl 3). Using a yeast three-hybrid approach with phototropin and NPH3 as a bait complex, we isolated a protein, termed EHB1 (for enhanced bending 1), with a so far unknown function, which binds to this binary complex. This novel interacting factor negatively affects hypocotyl bending under blue light conditions in Arabidopsis (Arabidopsis thaliana) and thus seems to be an important component regulating phototropism. Interestingly, it could be shown that the gravitropic response was also affected. Thus, it cannot be ruled out that this protein might also have a more general role in auxin-mediated bending toward an environmental stimulus.     

Eye Structure and Vision in the Freshwater Pulmonate Mollusc Planorbarius corneus

The structure of the mollusc Planorbarius corneus eye was studied using light and electron microscopy. The eye consists of the cornea, eye lens of non-spherical shape, and the vitreous body tightly bound to it, as well as of a monolayer non-inverted retina composed of photoreceptor and supporting (pigmented) cells. Its inner surface has two invaginations. The apices of several hundreds of photoreceptors directed to the vitreous body have groups of microvilli with a parallel orientation to each other. The eye optic system places the image into the base of the retinal microvillar layer. Its angle resolution provided by density of distribution of photoreceptor cells and the value of the index F = 1.71 is to be about 2.06° with a correction for the light spreading between microvilli of neighbor cells. Under conditions of a V-shaped labyrinth, the P. corneus molluscs show positive phototaxis by moving to the light source. The angular acuity of vision was assessed from differences in the choice by the molluscs of direction of movement to the pattern of vertical black bands with different periods of alternation. The differential threshold obtained is within an interval of 1.43–1.91°, which is close to the calculated value of angular resolution of the retina.     

Phototaxis in the flagellates,Euglena gracilis and Ochromonas danica

Oriented movement with respect to laterally impinging white light of the flagellates Euglena gracilis and Ochromonas danica has been analyzed in an individual cell study with a microvideographic technique. Using the deviation of track segments (in given time intervals of 1 s) from the light direction as raw data allowed a computer based analysis of the direction distribution. A number of statistical methods employed to test the significance of the obtained results demonstrated an obvious phototactic orientation in Ochromonas which was positive (toward the light source) in low illuminance (1.25 lx=5.3×10^-3 Wm^-2) and negative in higher illuminance (>12.5 lx=5.3×10^-2 Wm^-2). Since in this flagellate the threshold for negative phototaxis is much lower than that for the step-up photophobic response, the hypothesis that negative phototaxis may be brought about by repetitive step-up phobic responses can be rejected for at least this organism. In Euglena positive phototaxis was observed in 50 lx (=0.21 Wm^-2), while an illuminance of 500 lx (=2.1 Wm^-2) caused a negative phototaxis.The experiments were carried out in this laboratory     

Pigment migration and illumination of single photoreceptors in a moth

Summary The relation between intensity of illumination of single photoreceptors and position of the screening pigment was studied in the compound eye of the moth Deilephila elpenor. The amplitude of the response to test flashes of white light was measured in 7 dark adapted photoreceptor cells with the screening pigment in the extreme distal and in a proximal position. The experiments demonstrate that the response amplitude of individual photoreceptors varies with the pigment position. The associated variation in screening effect was 1.0 to 1.9 log units.The research reported in this study was supported by Swedish Medical Research Council, Sällskapet för Medicinsk Forskning and Stifteisen Gustaf och Tyra Svenssons Minne.     

PHOTOTROPISM IN YOUNG RATS

Before the eyelids have opened young rats are negatively heliotropic. They behave very much as does the larva of the blow-fly. The angle of orientation by lights opposed at 180° may be calculated by an equation based upon the elementary requirement of phototropism, namely that orientation is attained when the illumination of bilaterally disposed photoreceptors is equal. The precision of orientation decreases very nearly in proportion to the sum of the logarithms of the acting light intensities, due to photokinetic head movements. When the eyelids are opened, the rats move toward a darkened place in the field of vision, usually toward the shaded region immediately to one side of the lamp house. Therefore, when heliotropic, the rat is not "seeking the dark". The phototropism of these animals may be brought into conflict with their pronounced stereotropism, and the resolution of such conflicts may perhaps be utilized for the investigation of central nervous states.     

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.