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      Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator)

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          Abstract

          <p id="d15073931e262">Color vision variation is prevalent among neotropical monkeys. Captive studies indicate that trichromacy should confer a fruit feeding advantage. This hypothesis, however, has yet to be supported by field studies. We collected behavioral and genetic data from 72 capuchins and analyzed ca. 20,000 fruit intake events across 27 plant species. Controlling for plant species and phenological condition, we find that trichromats eat reddish, conspicuous fruits more quickly than do dichromatic (red-green colorblind) groupmates. We demonstrate an advantage of trichromacy for consuming fruit among wild monkeys. Previous research has revealed dichromatic advantage for cryptic tasks; our results suggest fruit foraging plays an important role in the maintenance of primate opsin polymorphism via balancing selection. </p><p class="first" id="d15073931e265">Intraspecific color vision variation is prevalent among nearly all diurnal monkeys in the neotropics and is seemingly a textbook case of balancing selection acting to maintain genetic polymorphism. Clear foraging advantages to monkeys with trichromatic vision over those with dichromatic “red-green colorblind” vision have been observed in captive studies; however, evidence of trichromatic advantage during close-range foraging has been surprisingly scarce in field studies, perhaps as a result of small sample sizes and strong impacts of environmental or individual variation on foraging performance. To robustly test the effects of color vision type on foraging efficiency in the wild, we conducted an extensive study of dichromatic and trichromatic white-faced capuchin monkeys ( <i>Cebus capucinus imitator</i>), controlling for plant-level and monkey-level variables that may affect fruit intake rates. Over the course of 14 months, we collected behavioral data from 72 monkeys in Sector Santa Rosa, Costa Rica. We analyzed 19,043 fruit feeding events within 1,602 foraging bouts across 27 plant species. We find that plant species, color conspicuity category, and monkey age class significantly impact intake rates, while sex does not. When plant species and age are controlled for, we observe that trichromats have higher intake rates than dichromats for plant species with conspicuously colored fruits. This study provides clear evidence of trichromatic advantage in close-range fruit feeding in wild monkeys. Taken together with previous reports of dichromatic advantage for finding cryptic foods, our results illuminate an important aspect of balancing selection maintaining primate opsin polymorphism. </p>

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          Finding a dominance order most consistent with a linear hierarchy: a new procedure and review.

          A procedure for ordering a set of individuals into a linear or near-linear dominance hierarchy is presented. Two criteria are used in a prioritized way in reorganizing the dominance matrix to find an order that is most consistent with a linear hierarchy: first, minimization of the numbers of inconsistencies and, second, minimization of the total strength of the inconsistencies. The linear ordering procedure, which involves an iterative algorithm based on a generalized swapping rule, is feasible for matrices of up to 80 individuals. The procedure can be applied to any dominance matrix, since it does not make any assumptions about the form of the probabilities of winning and losing. The only assumption is the existence of a linear or near-linear hierarchy which can be verified by means of a linearity test. A review of existing ranking methods is presented and these are compared with the proposed method. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.
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            Ecological importance of trichromatic vision to primates.

            Trichromatic colour vision, characterized by three retinal photopigments tuned to peak wavelengths of approximately 430 nm, approximately 535 nm and approximately 562 nm (refs 1, 2), has evolved convergently in catarrhine primates and one genus of New World monkey, the howlers (genus Alouatta). This uniform capacity to discriminate red-green colours, which is not found in other mammals, has been proposed as advantageous for the long-range detection of either ripe fruits or young leaves (which frequently flush red in the tropics) against a background of mature foliage. Here we show that four trichromatic primate species in Kibale Forest, Uganda, eat leaves that are colour discriminated only by red-greenness, a colour axis correlated with high protein levels and low toughness. Despite their divergent digestive systems, these primates have no significant interspecific differences in leaf colour selection. In contrast, eaten fruits were generally discriminated from mature leaves on both red-green and yellow-blue channels and also by their luminance, with a significant difference between chimpanzees and monkeys in fruit colour choice. Our results implicate leaf consumption, a critical food resource when fruit is scarce, as having unique value in maintaining trichromacy in catarrhines.
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              Evolution of colour vision in mammals.

              Colour vision allows animals to reliably distinguish differences in the distributions of spectral energies reaching the eye. Although not universal, a capacity for colour vision is sufficiently widespread across the animal kingdom to provide prima facie evidence of its importance as a tool for analysing and interpreting the visual environment. The basic biological mechanisms on which vertebrate colour vision ultimately rests, the cone opsin genes and the photopigments they specify, are highly conserved. Within that constraint, however, the utilization of these basic elements varies in striking ways in that they appear, disappear and emerge in altered form during the course of evolution. These changes, along with other alterations in the visual system, have led to profound variations in the nature and salience of colour vision among the vertebrates. This article concerns the evolution of colour vision among the mammals, viewing that process in the context of relevant biological mechanisms, of variations in mammalian colour vision, and of the utility of colour vision.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                September 26 2017
                September 26 2017
                September 26 2017
                September 11 2017
                : 114
                : 39
                : 10402-10407
                Article
                10.1073/pnas.1705957114
                5625910
                28894009
                5c90b27f-f2db-4d8e-826e-38ea01e982d2
                © 2017

                Free to read

                http://www.pnas.org/site/misc/userlicense.xhtml

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