Vision in chameleons-A model for non-mammalian vertebrates.

Chameleons (Chamaeleonidae, Reptilia) are known for their extreme sensory and motor adaptations to arboreal life and insectivoury. They show most distinct sequences of visuo-motor patterns in threat avoidance and in predation with prey capture being performed by tongue strikes that are unparalleled in vertebrates. Optical adaptations result in retinal image enlargement and the unique capacity to determine target distance by accommodation cues. Ocular adaptations result in complex eye movements that are context dependent, not independent, as observed in threat avoidance and predation. In predation, evidence from the chameleons' capacity to track multiple targets support the view that their eyes are under individual controls. Eye movements and body movements are lateralised, with lateralisation being a function of many factors at the population, individual, and specific-situation levels. Chameleons are considered a potentially important model for vision in non-mammalian vertebrates. They provide exceptional behavioural tools for studying eye movements as well as information gathering and analysis. They open the field of lateralisation, decision making, and context dependence. Finally, chameleons allow a deeper examination of the relationships between their unique visuo-motor capacities and the central nervous system of reptiles and ectotherms, in general, as compared with mammals.

Great cormorants (Phalacrocorax carbo) as potential vectors for the dispersal of Vibrio cholerae.

Vibrio cholerae is the cause of cholera, a devastating epidemic and pandemic disease. Despite its importance, the way of its global dissemination is unknown. V. cholerae is abundant in aquatic habitats and is known to be borne by copepods, chironomids and fishes. Our aim was to determine if fish-eating birds act as vectors in the spread of V. cholerae by consuming infected fish. We determined the existence of V. cholerae in the microbiome of 5/7 wild cormorants' intestine. In three of these V. cholerae-positive wild cormorants, the presence of a gene for cholera toxin (ctxA) was detected. We subsequently tested eight captive, hand-reared cormorants, divided into two equal groups. Prior to the experiment, the feces of the cormorants were V. cholerae-negative. One group was fed exclusively on tilapias, which are naturally infected with V. cholerae, and the other was fed exclusively on goldfish or on koi that were V. cholerae-negative. We detected V. cholerae in the feces of the tilapia-fed, but not in the goldfish/koi-fed, cormorants. Hence, we demonstrate that fish-eating birds can be infected with V. cholerae from their fish prey. The large-scale movements of many fish-eating birds provide a potential mechanism for the global distribution of V. cholerae.

Phylogenetics, biogeography and population genetics of the ascidian Botryllus schlosseri in the Mediterranean Sea and beyond.

The wide distribution of the ascidian Botryllus schlosseri along the Mediterranean coasts has been documented since the eighteenth century. However, despite copious documentation, analyses of dispersal modes and genetic profiles were limited to local populations or restricted regions. In order to get a pan-Mediterranean overview, 288 specimens from 11 populations of B. schlosseri from the western and eastern Mediterranean basins were sampled and analyzed using five microsatellite loci and COI sequences. Both molecular markers revealed high polymorphisms, with 182 microsatellites alleles and 54 COI haplotypes. Overall, Fst, Dest, and COI Фpt values were 0.146, 0.635 and 0.322, respectively, reflecting a high genetic diversity and a significant genetic structure as compared to other B. schlosseri populations worldwide, reflected by substantially higher values for effective number of alleles (Ne) in the Mediterranean. A phylogenetic analysis of the COI sequences resulted in four distinct clades and two molecular operational taxonomic units (OTUs). We recorded a stronger genetic structure among the populations of the eastern basin compared to the western basin (microsatellites Fst=0.217 versus 0.082; COI Фpt=0.416 versus 0.171), suggesting either a restricted connectivity between the basins or a stronger genetic drift in each basin. The occurrence of two OTUs and different ecological conditions may also contribute to this finding. Mean Nei's genetic distance in the eastern Mediterranean populations was more than three times higher compared to the western basin. No correlation was observed between geographic and genetic distances (Mantel test), suggesting that maritime transport is the main dispersal vector of B. schlosseri colonies. The possibility that the Mediterranean is a center of diversity for B. schlosseri, and probably its site of origin, is further discussed.

Avoidance of a moving threat in the common chameleon (Chamaeleo chamaeleon): rapid tracking by body motion and eye use.

A chameleon (Chamaeleo chamaeleon) on a perch responds to a nearby threat by moving to the side of the perch opposite the threat, while bilaterally compressing its abdomen, thus minimizing its exposure to the threat. If the threat moves, the chameleon pivots around the perch to maintain its hidden position. How precise is the body rotation and what are the patterns of eye movement during avoidance? Just-hatched chameleons, placed on a vertical perch, on the side roughly opposite to a visual threat, adjusted their position to precisely opposite the threat. If the threat were moved on a horizontal arc at angular velocities of up to 85°/s, the chameleons co-rotated smoothly so that (1) the angle of the sagittal plane of the head relative to the threat and (2) the direction of monocular gaze, were positively and significantly correlated with threat angular position. Eye movements were role-dependent: the eye toward which the threat moved maintained a stable gaze on it, while the contralateral eye scanned the surroundings. This is the first description, to our knowledge, of such a response in a non-flying terrestrial vertebrate, and it is discussed in terms of possible underlying control systems.

Eye movements in chameleons are not truly independent - evidence from simultaneous monocular tracking of two targets.

Chameleons perform large-amplitude eye movements that are frequently referred to as independent, or disconjugate. When prey (an insect) is detected, the chameleon's eyes converge to view it binocularly and 'lock' in their sockets so that subsequent visual tracking is by head movements. However, the extent of the eyes' independence is unclear. For example, can a chameleon visually track two small targets simultaneously and monocularly, i.e. one with each eye? This is of special interest because eye movements in ectotherms and birds are frequently independent, with optic nerves that are fully decussated and intertectal connections that are not as developed as in mammals. Here, we demonstrate that chameleons presented with two small targets moving in opposite directions can perform simultaneous, smooth, monocular, visual tracking. To our knowledge, this is the first demonstration of such a capacity. The fine patterns of the eye movements in monocular tracking were composed of alternating, longer, 'smooth' phases and abrupt 'step' events, similar to smooth pursuits and saccades. Monocular tracking differed significantly from binocular tracking with respect to both 'smooth' phases and 'step' events. We suggest that in chameleons, eye movements are not simply 'independent'. Rather, at the gross level, eye movements are (i) disconjugate during scanning, (ii) conjugate during binocular tracking and (iii) disconjugate, but coordinated, during monocular tracking. At the fine level, eye movements are disconjugate in all cases. These results support the view that in vertebrates, basic monocular control is under a higher level of regulation that dictates the eyes' level of coordination according to context.

Lateralization of visually guided detour behaviour in the common chameleon, Chamaeleo chameleon, a reptile with highly independent eye movements.

Chameleons (Chamaeleonidae, reptilia), in common with most ectotherms, show full optic nerve decussation and sparse inter-hemispheric commissures. Chameleons are unique in their capacity for highly independent, large-amplitude eye movements. We address the question: Do common chameleons, Chamaeleo chameleon, during detour, show patterns of lateralization of motion and of eye use that differ from those shown by other ectotherms? To reach a target (prey) in passing an obstacle in a Y-maze, chameleons were required to make a left or a right detour. We analyzed the direction of detours and eye use and found that: (i) individuals differed in their preferred detour direction, (ii) eye use was lateralized at the group level, with significantly longer durations of viewing the target with the right eye, compared with the left eye, (iii) during left side, but not during right side, detours the durations of viewing the target with the right eye were significantly longer than the durations with the left eye. Thus, despite the uniqueness of chameleons' visual system, they display patterns of lateralization of motion and of eye use, typical of other ectotherms. These findings are discussed in relation to hemispheric functions.

Relating lateralization of eye use to body motion in the avoidance behavior of the chameleon (Chamaeleo chameleon).

Lateralization is mostly analyzed for single traits, but seldom for two or more traits while performing a given task (e.g. object manipulation). We examined lateralization in eye use and in body motion that co-occur during avoidance behaviour of the common chameleon, Chamaeleo chameleon. A chameleon facing a moving threat smoothly repositions its body on the side of its perch distal to the threat, to minimize its visual exposure. We previously demonstrated that during the response (i) eye use and body motion were, each, lateralized at the tested group level (N = 26), (ii) in body motion, we observed two similar-sized sub-groups, one exhibiting a greater reduction in body exposure to threat approaching from the left and one--to threat approaching from the right (left- and right-biased subgroups), (iii) the left-biased sub-group exhibited weak lateralization of body exposure under binocular threat viewing and none under monocular viewing while the right-biased sub-group exhibited strong lateralization under both monocular and binocular threat viewing. In avoidance, how is eye use related to body motion at the entire group and at the sub-group levels? We demonstrate that (i) in the left-biased sub-group, eye use is not lateralized, (ii) in the right-biased sub-group, eye use is lateralized under binocular, but not monocular viewing of the threat, (iii) the dominance of the right-biased sub-group determines the lateralization of the entire group tested. We conclude that in chameleons, patterns of lateralization of visual function and body motion are inter-related at a subtle level. Presently, the patterns cannot be compared with humans' or related to the unique visual system of chameleons, with highly independent eye movements, complete optic nerve decussation and relatively few inter-hemispheric commissures. We present a model to explain the possible inter-hemispheric differences in dominance in chameleons' visual control of body motion during avoidance.

Visual accommodation and active pursuit of prey underwater in a plunge-diving bird: the Australasian gannet.

Australasian gannets (Morus serrator), like many other seabird species, locate pelagic prey from the air and perform rapid plunge dives for their capture. Prey are captured underwater either in the momentum (M) phase of the dive while descending through the water column, or the wing flapping (WF) phase while moving, using the wings for propulsion. Detection of prey from the air is clearly visually guided, but it remains unknown whether plunge diving birds also use vision in the underwater phase of the dive. Here we address the question of whether gannets are capable of visually accommodating in the transition from aerial to aquatic vision, and analyse underwater video footage for evidence that gannets use vision in the aquatic phases of hunting. Photokeratometry and infrared video photorefraction revealed that, immediately upon submergence of the head, gannet eyes accommodate and overcome the loss of greater than 45 D (dioptres) of corneal refractive power which occurs in the transition between air and water. Analyses of underwater video showed the highest prey capture rates during WF phase when gannets actively pursue individual fish, a behaviour that very likely involves visual guidance, following the transition after the plunge dive's M phase. This is to our knowledge the first demonstration of the capacity for visual accommodation underwater in a plunge diving bird while capturing submerged prey detected from the air.

Visually guided avoidance in the chameleon (Chamaeleo chameleon): response patterns and lateralization.

The common chameleon, Chamaeleo chameleon, is an arboreal lizard with highly independent, large-amplitude eye movements. In response to a moving threat, a chameleon on a perch responds with distinct avoidance movements that are expressed in its continuous positioning on the side of the perch distal to the threat. We analyzed body-exposure patterns during threat avoidance for evidence of lateralization, that is, asymmetry at the functional/behavioral levels. Chameleons were exposed to a threat approaching horizontally from the left or right, as they held onto a vertical pole that was either wider or narrower than the width of their head, providing, respectively, monocular or binocular viewing of the threat. We found two equal-sized sub-groups, each displaying lateralization of motor responses to a given direction of stimulus approach. Such an anti-symmetrical distribution of lateralization in a population may be indicative of situations in which organisms are regularly exposed to crucial stimuli from all spatial directions. This is because a bimodal distribution of responses to threat in a natural population will reduce the spatial advantage of predators.

Threat perception in the chameleon (Chamaeleo chameleon): evidence for lateralized eye use.

Chameleons are arboreal lizards with highly independent, large amplitude eye movements. In response to an approaching threat, a chameleon on a vertical pole moves so as to keep itself away from the threat. In so doing, it shifts between monocular and binocular scanning of the threat and of the environment. We analyzed eye movements in the Common chameleon, Chamaeleo chameleon, during avoidance response for lateralization, that is, asymmetry at the functional/behavioral levels. The chameleons were exposed to a threat, approaching horizontally from clockwise or anti-clockwise directions, and that could be viewed monocularly or binocularly. Our results show three broad patterns of eye use, as determined by durations spent viewing the threat and by frequency of eye shifts. Under binocular viewing, two of the patterns were found to be both side dependent, that is, lateralized and role dependent ("leading" or "following"). However, under monocular viewing, no such lateralization was detected. We discuss these findings in light of the situation not uncommon in vertebrates, of independent eye movements and a high degree of optic nerve decussation and that lateralization may well occur in organisms that are regularly exposed to critical stimuli from all spatial directions. We point to the need of further investigating lateralization at fine behavioral levels.

Rheum palaestinum (desert rhubarb), a self-irrigating desert plant.

The rare plant Rheum palaestinum (Polygonaceae) is a perennial hemicryptophyte that grows during the rainy winter in desert mountainous areas in Israel and Jordan that receive an average annual rainfall of ca. 75 mm. It produces between one and four large round leaves that are tightly attached to the ground and form large rosettes of up to 1 m(2). These leaves differ markedly from the typical small leaves of most desert plants. Moreover, they have a unique 3D morphology resembling a scaled-down mountainous area with well-developed steep drainage systems, raising the question which selective agents were involved in their evolution. We propose that the large leaves collect rainwater that then infiltrates the soil surrounding the root. We measured the seasonal course of leaf growth, examined the area of wet soil surrounding the root after actual and simulated rain, and modeled the water harvesting capacity using the plant leaf area and the weekly precipitation. We show that even in the slightest rains, water flows above the veins to the leaf's base where it irrigates the vertical root. A typical plant harvests more than 4,100 cm(3) of water per year, and enjoys a water regime of about 427 mm/year, equivalent to the water supply in a Mediterranean climate. This is the first example of self-irrigation by large leaves in a desert plant, creating a leaf-made mini oasis.

Prey detection by great cormorant (Phalacrocorax carbo sinensis) in clear and in turbid water.

The scattering and absorption of light by water molecules and by suspended and dissolved matter (turbidity) degrade image transmission and, thus, underwater perception. We tested the effects on visual detection of prey size and distance (affecting apparent prey size) and of low-level water turbidity in hand-reared great cormorants (Phalacrocorax carbo sinensis) diving for natural prey (fish) in a forced-choice situation. The cormorants' detection of underwater prey relied on vision. The minimal tested subtending visual angle of the prey at detection ranged between approximately 34.2' (prey size constant; distance varied) and 9.5' (distance constant; prey size varied). For all tested distances (0.8-3.1 m) the mean detection success was significantly higher than the chance level. The probability of a correct choice declined significantly with increased distance, with Detection success=-0.034D+1.021 (where D is distance, r(2)=0.5, N=70, P<0.001). The combined effect of turbidity and distance on the probability of detection success was significant, with both variables having a negative effect: Detection success=-0.286D-0.224Tu+1.691 (where Tu is turbidity, r(2)=0.68, N=144, P<0.001). At prey detection threshold, the relationship between distance and turbidity was: D=3.79e(-4.55Tu). It is concluded that (i) the subtending angle of natural prey at detection was lower than that of resolution of square-wave, high-contrast grating and (ii) turbidity, at levels significantly lower than commonly used in behavioural experiments, had a pronounced effect on visually mediated behaviour patterns.

Multifocal lenses in coral reef fishes.

The optical properties of crystalline lenses were studied in eleven species of coral reef fish from the Red Sea in Eilat, Israel. Three species each of diurnal planktivores, nocturnal planktivores and diurnal herbivores constituted three groups of animals with little within-group variability. In addition we studied two predators, which differed with respect to body size, prey preference, hunting method and diel activity period. All species studied have multifocal lenses. There were statistically significant differences in the optical properties of the lenses between the first three groups and between the predatory species. The properties of the lenses correlate well with known complements of visual pigments and feeding habits. Lenticular zones focusing ultraviolet light were found in two diurnal planktivores. The optical properties of the lens seem to be specifically adapted to the visual needs of each species.

Hereditary family signature of facial expression.

Although facial expressions of emotion are universal, individual differences create a facial expression "signature" for each person; but, is there a unique family facial expression signature? Only a few family studies on the heredity of facial expressions have been performed, none of which compared the gestalt of movements in various emotional states; they compared only a few movements in one or two emotional states. No studies, to our knowledge, have compared movements of congenitally blind subjects with their relatives to our knowledge. Using two types of analyses, we show a correlation between movements of congenitally blind subjects with those of their relatives in think-concentrate, sadness, anger, disgust, joy, and surprise and provide evidence for a unique family facial expression signature. In the analysis "in-out family test," a particular movement was compared each time across subjects. Results show that the frequency of occurrence of a movement of a congenitally blind subject in his family is significantly higher than that outside of his family in think-concentrate, sadness, and anger. In the analysis "the classification test," in which congenitally blind subjects were classified to their families according to the gestalt of movements, results show 80% correct classification over the entire interview and 75% in anger. Analysis of the movements' frequencies in anger revealed a correlation between the movements' frequencies of congenitally blind individuals and those of their relatives. This study anticipates discovering genes that influence facial expressions, understanding their evolutionary significance, and elucidating repair mechanisms for syndromes lacking facial expression, such as autism.

Changes in the refractive state during prey capture under low light in the nocturnal cardinalfish Apogon annularis.

Many nocturnal and crepuscular fish use vision to feed and function under low light levels. However, little is known about their ability to accommodate or their visual acuity under these light levels. We used Infrared Photoretinoscopy to track the refractive state of the eye during prey capture under low light in Apogon annularis, a nocturnal reef fish. Anatomical measurements of the eyes allowed calculations of visual acuity. Changes in the refractive state were observed in approximately 75% of the prey capturing strikes, preceding the strikes by 30 ms. These changes were rare between strikes or when prey was absent. Anatomical measurements indicated that the number of photo-detection units in a retinal image greatly exceeded the minimal number needed to detect prey. We conclude that nocturnal vision in A. annularis is sufficiently sensitive to allow accommodation during prey capture.

Plant coloration undermines herbivorous insect camouflage.

The main point of our hypothesis "coloration undermines camouflage" is that many color patterns in plants undermine the camouflage of invertebrate herbivores, especially insects, thus exposing them to predation and causing them to avoid plant organs with unsuitable coloration, to the benefit of the plants. This is a common case of "the enemy of my enemy is my friend" and a visual parallel of the chemical signals that plants emit to call wasps when attacked by caterpillars. Moreover, this is also a common natural version of the well-known case of industrial melanism, which illustrates the great importance of plant-based camouflage for herbivorous insects and can serve as an independent test for our hypothesis. We claim that the enormous variations in coloration of leaves, petioles and stems as well as of flowers and fruits undermine the camouflage of invertebrate herbivores, especially insects. We assume that the same principle might operate in certain animal-parasite interactions. Our hypothesis, however, does not contrast or exclude other previous or future explanations of specific types of plant coloration. Traits such as coloration that have more than one type of benefit may be selected for by several agents and evolve more rapidly than ones with a single type of advantage.

Corneal power and underwater accommodation in great cormorants (Phalacrocorax carbo sinensis).

In great cormorants (Phalacrocorax carbo sinensis), corneal refractive powers, determined by photokeratometry, ranged between 52.1 diopters (52.1 D) and 63.2 D. Photorefractive reflexes, determined by infrared video photorefraction, indicated that in voluntary dives the cormorants accommodate within 40-80 ms of submergence and with myopic focusing relative to the photorefractor attained when prey was approximately one bill length from the plane of the eye. Underwater, the pupils were not constricted and retained diameters similar to those in air. These results support previously reported capacities of lenticular changes in amphibious birds yet do not fully correspond with earlier reports in terms of the coupling of iris constriction with accommodation, and time course.