The impact of moving to a novel environment on social networks, activity and wellbeing in two new world primates.

Among the stressors that can affect animal welfare in zoos, the immediate effect of relocation to a novel environment is one that has received little attention in the literature. Here, we compare the social network, daily activity and the expression of stress-related behavior in capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) before and just after they were relocated to a new enriched enclosure. Results showed similar immediate responses to the move in the two species. Both showed a substantial increase in the time spent resting and spent more time in the highest and "safest" part of their enclosure after relocation. Both capuchins and squirrel monkeys spent significantly more time in close proximity to other group members after relocation, compared to before. In squirrel monkeys, the structure of the social network, which was initially correlated to affiliation, was no longer so after the move. In capuchins, the network analysis showed that individuals regrouped by age, with the youngsters who were potentially more affected by stress being in the center of the network. Social network analysis helped to achieve a more complete picture of how individuals were affected by relocation. We suggest that this type of analysis should be used alongside traditional methods of observation and analysis to encompass the most complex aspects of animal behavior in times of stress and to improve welfare.

Color vision pigment frequencies in wild tamarins (Saguinus spp.).

The adaptive importance of polymorphic color vision found in many New World and some prosimian primates has been discussed for many years. Polymorphism is probably maintained in part through a heterozygote advantage for trichromatic females, as such individuals are observed to have greater foraging success when selecting ripe fruits against a background of forest leaves. However, recent work also suggests there are some situations in which dichromatic individuals may have an advantage, and that variation in color vision among individuals possessing different alleles may also be significant. Alleles that confer a selective advantage to individuals are expected to occur at a higher frequency in populations than those that do not. Therefore, analyzing the frequencies of color vision alleles in wild populations can add to our understanding of the selective advantages of some color vision phenotypes over others. With this aim, we used molecular techniques to determine the frequencies of color vision alleles in 12 wild tamarin groups representing three species of the genus Saguinus. Our results show that allele frequencies are not equal, possibly reflecting different selective regimes operating on different color vision phenotypes.

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus).

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.

Detection of Fruit and the Selection of Primate Visual Pigments for Color Vision.

Primates have X chromosome genes for cone photopigments with sensitivity maxima from 535 to 562 nm. Old World monkeys and apes (catarrhines) and the New World (platyrrhine) genus Alouatta have separate genes for 535-nm (medium wavelength; M) and 562-nm (long wavelength; L) pigments. These pigments, together with a 425-nm (short wavelength) pigment, permit trichromatic color vision. Other platyrrhines and prosimians have a single X chromosome gene but often with alleles for two or three M/L photopigments. Consequently, heterozygote females are trichromats, but males and homozygote females are dichromats. The criteria that affect the evolution of M/L alleles and maintain genetic polymorphism remain a puzzle, but selection for finding food may be important. We compare different types of color vision for detecting more than 100 plant species consumed by tamarins (Saguinus spp.) in Peru. There is evidence that both frequency-dependent selection on homozygotes and heterozygote advantage favor M/L polymorphism and that trichromatic color vision is most advantageous in dim light. Also, whereas the 562-nm allele is present in all species, the occurrence of 535- to 556-nm alleles varies between species. This variation probably arises because trichromatic color vision favors widely separated pigments and equal frequencies of 535/543- and 562-nm alleles, whereas in dichromats, long-wavelength pigment alleles are fitter.

The behavioural ecology of mixed-species troops of callitrichine primates.

This review summarizes information on the behavioural ecology of mixed-species troops (interspecific associations) formed by different species of callitrichines, small New World monkeys, in western and central Amazonia. The formation of mixed-species troops is an integral part of the biology of several species of this subfamily. Niche separation between associated species is obtained through vertical segregation which results in differences in the prey spectrum. The degree of niche separation is a predictor for the stability of mixed-species troops. Individuals may benefit from the formation of mixed-species troops through increased safety from predators, increased foraging efficiency, and/or increased resource defence. Costs of mixed-species troop formation are probably very low and mainly relate to patterns of interspecific behavioural interactions. We point to gaps in our knowledge and suggest pathways for future research into mixed-species troops.

Tamarin polyspecific associations: Forest utilization and stability of mixed-species groups.

Niche separation is likely to play a key role in the formation of mixed-species groups. Saddle-backed tamarins (Saguinus fuscicollis) were studied at three sites with different primate communities in northern Bolivia: (1) with red-bellied tamarins,S. labiatus; (2) with emperor tamarins,S. imperator; and (3) without a congeneric species. The degree of association is higher betweenS. labiatus andS. fuscicollis than betweenS. imperator andS. fuscicollis and is related to differences in forest utilization between associating pairs. Niche separation is found to be greater betweenS. labiatus andS. fuscicollis than betweenS. fuscicollis andS. imperator. The mean height and habitat utilization ofS. fuscicollis does not differ greatly across the three sites, nor does the height of tamarins in and out of association. It is concluded that combined with differences in body size and dietary overlap, vertical segregation plays an important role in tamarin polyspecific associations (increasing the potential of both foraging and anti-predatory benefits) and that this is not a consequence of vertical displacement ofS. fuscicollis by its dominant congeners.

The influence of stimulus shape on orientation acuity.

Orientation acuity was estimated for vertical and oblique bar stimuli. Discrimination thresholds were affected by changes in the length and width of the targets, falling as bar length was increased and, conversely, rising as the bars were made wider. These changes are complimentary, in that overall discrimination performance can be predicted by a single measure of the orientation "entropy" of the target, namely the height-to-width ratio. The data provide support for a model of orientation coding where discrimination performance is not simply a reflection of the signal-to-noise ratio in single cells in the striate cortex.

The oblique effect in orientation acuity.

We have examined the dependence of rotational acuity on the orientation bandwidth of a stimulus using two-dimensional, band-pass filtered, spatial noise. Stimuli had a bandwidth of 0.5 octave of spatial frequency, centred at 5.0 cyc/deg, and an orientation bandwidth that covered the range from 0.0 to 25.0 deg. Thresholds were obtained on one principal (vertical), and one oblique axis (45 deg). It was found that acuity declined on both axes as bandwidth increased, in a manner that was compatible with simple statistical principles with virtually perfect sampling of the image. There was some evidence that the intrinsic noise is greater on the oblique axis than on the vertical, and that oblique axes are less densely sampled than the principal axes. These differences are small and are insufficient, either on their own or taken together to explain the oblique effect.

Mechanisms specialized for the perception of image geometry.

Angle discrimination thresholds were obtained for V-shaped targets with a base angle of 90 deg at four different pattern orientations (0, 45, 90 and 135 deg). A comparison of these thresholds with the orientation discrimination thresholds for the single lines from which the patterns had been constructed, revealed that angle acuity cannot be predicted from component acuity. Angle acuity is finer than the corresponding orientation acuity in all cases and does not exhibit the pronounced oblique effect that is found for orientation discrimination. Other experiments showed that acuity for pattern angle depends critically on base angle, with minima close to 0, 90 and 180 deg. The shape and amplitude of this function are independent of pattern orientation. It was found that the angle acuity was unaffected by excluding a large portion of the target in the region of the vertex, and that the pattern of dependence of acuity on angle changed radically when the target was reduced ultimately to three blobs that defined the cardinal points of the stimulus. The data suggest that when the target comprises line segments, angle discrimination is not limited by noise that arises at early levels of processing and that angle perception is mediated by mechanisms that are specialized for the perception of image geometry. An opponent process model, that is based on the combined outputs of just two types of filter, is proposed as the basis for the perception of image geometry. This type of system is appropriate for computing one of the differential invariants in an optic flow field.

Evidence for separate, task dependent noise processes in orientation and size perception.

Spatial acuity was estimated as the minimum difference in target spatial frequency which could act as a cue in a double concurrent, single interval orientation discrimination task. Experiments were conducted with vertical and oblique (45 deg) targets at three different spatial frequencies covering a range of two octaves. Frequency thresholds were found to be lower than those estimated by conventional methods by a factor of nearly 50%. They followed Weber's law for target frequency and were independent of target orientation. The orientation thresholds exhibited a normal oblique effect, and were not affected by the simultaneous judgements of target frequency. The data support the contention that the neural codes for image size and image orientation are segregated at an early stage of processing, and that the main source of noise that limits the precision of coding in these domains exists beyond the level of early mechanisms.

Changes in the perceived direction of drifting plaids, induced by asymmetrical changes in the spatio-temporal structure of the underlying components.

When a plaid pattern with symmetrical velocity components (Type I) is changed to a plaid pattern with asymmetrical velocity components (Type IA), the overall direction of drift appears to undergo a rotation without any other change to the spatial parameters of the components. This change in the perceived drift direction can be induced by altering either the temporal frequency of the components or by altering their spatial frequency. In separate experiments, we have estimated the magnitude of the temporal and spatial frequency thresholds that are necessary to create a liminal change in direction of this type. The results from both temporal and spatial frequency experiments are closely similar. We find that liminal rotations can be induced by changes in the spatio-temporal structure of the sine-wave grating components that are undetectable when these components are presented in isolation. Further, we find that the "velocity threshold for direction" is not a constant factor, but critically depends on the relative orientation of the two elements that form the plaid. Forced-choice experiments were also conducted to estimate the extent of the apparent rotation of the plaid pattern for differing levels of asymmetry in the spatial frequency and temporal frequency of the components. The magnitude of the pattern rotation is predicted by a model of motion direction that encodes the successive displacements of the intersections of the gratings. Finally, we demonstrate that the velocity thresholds for perceived rotation exhibit a meridional anisotropy that depends on the direction of drift of the overall pattern and not on the orientation of the components.(ABSTRACT TRUNCATED AT 250 WORDS)

Orientation acuity for sine-wave gratings with random variation of spatial frequency.

Orientation discrimination thresholds were estimated for sine-wave grating stimuli using a two-alternative forced-choice procedure on the two principal, and the two main oblique axes. The two discriminanda within any trial were subject to independent random variation of their spatial frequency. The variation of spatial frequency was defined by a Gaussian probability density function. Thresholds were obtained for five different depths of frequency variation within the range 0.0-1.0 octave. We find that orientation acuity on any of the axes tested is unaffected by variation in the spatial frequency of the targets. The data support the hypothesis that orientation and spatial frequency are independent and orthogonal neural codes.

Anisotropic axes in orientation perception are not retinotopically mapped.

The effect of the posture of an observer on the pattern of meridional anisotropy for orientation acuity was examined. Orientation acuity was estimated for the two principal and for one oblique axis with three bodily postures: normal vertical sitting, vertical sitting with the head rotated to 45 degrees from vertical, and prone. The test stimuli were sine-wave gratings covering a range of two octaves of spatial frequency, thin lines, and step edges. Acuity estimates were obtained by two different psychophysical procedures: a single-interval two-alternative forced choice, and a two-interval two-alternative forced choice. Both experimental procedures revealed a strong interaction between the shape of the function that describes the meridional variation of orientation acuity and the posture of the observer. The data are incompatible with models of the oblique effect in orientation perception that are based on a meridional anisotropy in neural properties early in the visual hierarchy.

Directional acuity for drifting plaids.

Orientation discrimination thresholds were estimated for symmetrical "plaids", constructed by the super-imposition of two, independent drifting sine-wave gratings of 2.5 c/deg. Experiments were conducted when the apparent direction of drift was on the two principal meridians (vertical and horizontal), and when the apparent direction of drift was at the two oblique orientations (45 and 135 deg). Acuity for the direction of drift for these stimuli is of the same order of precision as orientation acuity for static or drifting gratings, and exhibits a meridional anisotropy that favours the principal meridians. This anisotropy follows a pattern that is determined by the apparent direction of drift, and not the orientation of the underlying elements. Acuity for orientation is lowest for oblique drift directions, even though both of the elements are oriented on the principal meridians. This finding was confirmed when the orientation of the underlying elements was subject to a random variation. The results are not easily accommodated by models that propose that the individual elements of the plaid are analysed separately. Second, the data are incompatible with models of the oblique effect of orientation discrimination that are based on an axis dependent, differential sampling of the retinal image.

Orientation acuity estimated with simultaneous and successive procedures.

Orientation discrimination thresholds for medium contrast sinewave grating stimuli were estimated by a forced-choice procedure for the two principal, and the two main oblique axes. The results obtained for simultaneous presentation with a centre/surround stimulus arrangement are compared with the threshold estimates obtained when the two stimuli to be discriminated do not overlap in time. We find that orientation acuity depends on the temporal relationship of the discriminanda. Estimates of orientation threshold with simultaneous presentation are lower on all axes tested than those obtained with successive presentation; the greatest difference in orientation acuity was found at obliques. The data support the hypothesis that the meridional anisotropy in orientation discrimination that is found with conventional, two-interval forced-choice methods is not entirely attributable to anatomical and physiological changes at the level of the striate cortex.

Recognition of stimulus orientation.

The threshold for detecting a deviation in the orientation of a test stimulus from vertical and from horizontal was measured with a single test interval. The test stimuli were step edges, thin lines, and sine wave gratings of 2.5, 5.0 and 10.0 c/deg. Recognition thresholds were found to be independent of the frequency content and nature of the test stimulus. The average threshold value on the principal meridians was found to be approx. 0.6 deg. Additional testing was conducted with two interval forced choice designs, both with and without random perturbation of the orientation of the stimuli. Random perturbation of orientation reduces acuity estimates. The results are compared with those obtained by testing on the oblique meridia. We conclude that the meridional anisotropy of orientation discrimination, which favours the vertical and horizontal is a result, in part, of the influence of non-visual mechanisms.