Kraig Adler

EXTRAOCULAR PHOTORECEPTION IN AMPHIBIANS

Abstract— Amphibians possess extraocular photoreceptors (EOPs) which exclusively or together with the lateral eyes perceive light for various physiological and behavioral activities. Several kinds of EOPs are discussed but emphasis is given to the pineal complex: the dermal frontal organ (or stirnorgan) found only in frogs and toads among amphibians and the intracranial pineal body (or epiphysis cerebri) found in all Amphibia. Both structures are derived as dorsal evaginations of the diencephalon and have a retina‐like fine structure. Both are sensitive to visible and UV light but not to IR, mechanical or chemical stimuli. The frontal organ gives chromatic and achromatic responses but in most species only achromatic ones are recorded from the pineal. Photopigments have been identified for some of these responses.

Spatial Orientation by Salamanders Using Plane-Polarized Light

Tiger salamanders (Ambystoma tigrinum) can perceive the plane of polarization in linearly polarized light and can learn to use that e-vector direction for spatial orientation in indoor orientation tests.

True navigation by an amphibian

True navigation, also referred to as map-based homing, is the ability of an organism to return to the origin of a displacement (‘home’) without access to familiar landmarks or goal-emanating cues, and without knowledge of the displacement route. True navigation requires both a ‘map’ or geographical position sense and a compass, and has been demonstrated only in vertebrates (e.g. Walcott & Schmidt-Koenig 1973; Rodda 1984a, b, 1985). In the present study, eastern red-spotted newts, Notophthalmus viridescens, deprived of directional information during long distance displacement from their home pond were able to orient in the homeward direction, indicating that they are capable of true navigation. Homing ability appears to be well developed in the family Salamandridae. Western newts, Taricha rivularis, return to breeding sites along relatively straight paths after displacements of up to 12 km (Twitty et al. 1966). Eastern red-spotted newts exhibit homeward-directed orientation in an enclosed indoor arena after displacements of lo-50 km (Phillips 1986a, 1987; Phillips & Borland 1994). In our earlier homing studies (Phillips 1986a, 1987; Phillips & Borland 1994), male eastern newts were displaced from their home ponds to the testing facility in partially covered plastic buckets which provided access to directional cues en route that could potentially have been used to determine the direction of displacement (Phillips 1987). In the experiments reported here, male newts were deprived of visual, magnetic, olfactory and inertial directional cues during displacement from their

Extraocular perception of polarized light by orienting salamanders

SummarySpatial orientation corresponding to the bearing of thee-vector of linearly polarized light can be demonstrated in sighted and eyeless salamanders (Ambystoma tigrinum) trained under linearly polarized light. However, if opaque polyethylene plastic is inserted over the skull of these animals, whether they are sighted or eyeless, orientation is uniform within the test arena. Bidirectional oriented movement is restored in both groups, however, when transparent plastic is substituted in the same animals. A discussion of the possible mechanism for perception of polarized light by extraocular photoreceptors (EOPs) is given.ZusammenfassungDurch Dressur unter linear polarisiertem Licht wird beiAmbystoma tigrinum sowohl mit als auch ohne Augen eine Orientierung nach deme-Vektor linear polarisierten Lichtes nachgewiesen. Wird jedoch über dem Schädel (unter der Haut) eine opake Polyäthylen-Scheibe eingeschoben, so findet sich weder bei geblendeten noch bei Tieren mit Augen eine Orientierung nach deme-Vektor. Wird die opake Plastikscheibe durch eine transparente ersetzt, so tritt in jedem Fall die Orientierung (± 180 °) wieder auf. Die möglichen Mechanismen der Wahrnehmung polarisierten Lichtes durch extraokulare Rezeptoren werden diskutiert.

Extraoptic phase shifting of circadian locomotor rhythm in salamanders.

Timing of locomotor rhythm in the slimy ralamander, Plethodon glutinosus, can be shifted in phase by the environmental light cycle, whether the animals have eyes or not. Rhythmicity persists at least for the first day when animals are transferred to constant conditions, with a period of about 24 hours, and is therefore circadian in nature. An extraoptic photoreceptor site in the brain is suggested.

Orientation in a desert lizard (Uma notata): time-compensated compass movement and polarotaxis

SummaryThe diurnal escape response of fringetoed lizards (Uma notata) startled by predators demonstrates clear directional orientation not likely to depend on local landmarks in the shifting sands of their desert environment. Evidence that celestial orientation is involved in this behavior has been sought in the present experiments by testing the effects of (1) phase shifting the animals internal clock by 6 h and (2) by training the lizards to seek shelter while exposed to natural polarization patterns. In the first case, 90° shifts in escape direction were demonstrated in outdoor tests, as expected if a time-compensated sun or sky polarized light compass is involved. In the second instance, significant bimodale-vector dependent orientation was found under an overhead polarizing light filter but this was only evident when the response data were transposed to match the zenithe-vector rotation dependent on the suns apparent movement through the sky. This extends to reptiles the capacity to utilize overheade-vector directions as a time-compensated sky compass. The sensory site of this discrimination and the relative roles of sun and sky polarization in nature remain to be discovered.

The Role of Extraoptic Photoreceptors in Amphibian Rhythms and Orientation: A Review

Amphibians possess extraoptic photoreceptors (EOPs) which can be used to perceive light for certain physiological and behavioral activities including pigmentary adaptation, entrainment and phase-shifting of circadian locomotor rhythms, and compass orientation. Several parts of the pineal system seem to be involved in perceiving light: the extracranial pineal end organ (also called frontal organ or stirnorgan) found only in frogs and toads, and the intracranial pineal body (or epiphysis cerebri) found in all Amphibia; both structures possess a retina-like fine structure and have been demonstrated to be functional photoreceptors from neurophysiological studies. Evidence for the use of EOPs and location of specific sites is reviewed drawing upon behavioral, ultrastructural and neurophysiological sources. The existence of non-pineal EOPs in Amphibia and the role of EOPs in other vertebrates are briefly discussed.

The pineal body: Site of extraocular perception of celestial cues for orientation in the tiger salamander (Ambystoma tigrinum)

SummaryTiger salamanders (Ambystoma tigrinum) trained to orient in a particular compass direction under the sun fail to orient in the trained direction if they are (i) eyeless and simultaneously have the brain covered with opaque plastic or are (ii) eyeless and pinealectomized (Fig. 1–2, Table 1). Salamanders with either the eyes or the pineal intact and unobstructed continue to orient in the trained direction. These data strongly support the hypothesis that the pineal body is an effective extraocular photoreceptor (EOP) for compass orientation in tiger salamanders.

Individuality in the use of orientation cues by green frogs

Abstract The common assumption that test groups are motivationally homogeneous and utilize the same orientation reference cues may not be correct. Green frogs ( Rana clamitans ) were trained in a circular arena to seek a goalbox located 90° counterclockwise from a lamp. Most frogs learned the task, but an analysis of the training and testing records showed marked individuality in task learning. Some frogs found the goalbox only with the lamp as a cue; others used the goalbox, the goalbox and lamp, or the goalbox and the lamp separately as cues. One individual learned to orient non-randomly to some still-unknown but geographically fixed cue. These observations show that even though frogs can learn a common task, under supposedly identical training conditions they may utilize a diversity of cues. Larger (thus, older) frogs were significantly more consistent in their patterns of movement. Paths of movement that succeeded in reaching the goal tended to be repeated in later tests. Frogs trained to move around a partition to a goal continued that path even when the obstruction was later removed, suggesting the use of a motor memory or kinaesthesia. Standard orientation tests, in which the group was significantly oriented in the expected direction, were shown on closer inspection to consist of frogs moving according to several individually stereotyped factors. Thus, the heterogeneity of individual experimental animals should be more fully taken into consideration in orientation research.

Directional and Discriminatory Responses of Salamanders to Weak Magnetic Fields

A number of studies now exist pointing to the use of magnetic information in vertebrate orientation especially for birds, but the evidence among lower vertebrates is difficult to interpret. Several studies with fish have demonstrated a response to magnetic fields (e.g., Branover et al., 1971; Ovchinnikov et al., 1973; Andrianov et al., 1974; Tesch, 1974). However, in an aquatic environment electrical events can be induced by a body moving through a magnetic field and, therefore, it is not clear whether magnetic perception is accomplished directly or indirectly through induction. Several fish have been shown to be sensitive enough to electrical stimuli to be able to perceive such induced fields (reviewed in Fessard, 1974) even in some species which lack specialized electroreceptive organs (Rommel and McCleave, 1972, 1973). In studies with the cave salamander Phillips (1977) provided evidence for a learned directional response to the earth’s magnetic field. Since this species is terrestrial, it seems more likely that the magnetic field is perceived directly. The present paper considers an additional source of variation observed in the original data from cave salamanders and also provides supporting evidence for discriminatory responses to weak magnetic fields in a second species of salamander.