Catherine Julliot’s research while affiliated with University of Cambridge and other places

The Guianas contain one of the largest single remaining tracts of undisturbed tropical rainforest in the world, but this forest and its fauna are facing increased threats. In the north of French Guiana both anthropogenic pressures and conflicts between settlements related to the use of natural resources are growing. Based on surveys in 17 forest sites we show that hunting pressure was the main factor determining current primate species richness, masking the effects of logging or forest type. Three of the larger species, the red howler monkey Alouatta seniculus, black spider monkey Ateles paniscus and tufted capuchin Cebus apella, were less abundant in hunted areas. In the areas around four settlements the harvested biomass of primates was low compared to other game species, but the harvests were close to or beyond the maximal sustainable thresholds for the red howler monkey and tufted capuchin. In French Guiana primates are either fully protected by law (the spider monkey and white-faced saki Pithecia pithecia), or their hunting is restricted to subsistence use (howler monkey, tufted capuchin and wedge-capped capuchin Cebus olivaceus). Most hunted meat is, however, destined for sale. Current conservation policy in French Guiana is limited to legal protection for some species and areas, and laws are poorly enforced. Although large areas of forest and its wildlife are protected simply by their remoteness, there is an increasingly urgent need for the legal protection of all primate species, and the establishment of large protected areas and efficient forest management schemes to minimize the impacts of logging and hunting.

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed–dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.

In Neotropical forests, a majority of plant species relies upon arboreal and flying frugivores for the dispersal of their seeds (Howe 1986, Howe & Smallwood 1982, Charles-Dominique Chapter 17). Once the fruits are consumed and the pulp or arillote digested, seeds are either regurgitated or dropped into faeces below the parent tree or a conspecific tree, a nearby perch tree or along canopy routes frequently used by animals (Howe 1989, Howe 1993, Julliot 1996, Julliot 1997, Schupp et al. 1989). As animals move along pathways in the canopy or fly over trees within their home range seeking other fruit sources, they may forage into forest areas where the previously consumed tree species is at low density or absent (van Roosmalen 1985). Given the retention time in the stomach and gut, and habit of frugivores, seeds may thus be dropped below the parent tree crown, in the parent neighbourhood, or farther away from any conspecific tree (Julliot 1997). Consequently, seeds may be deposited in areas varying in the density of the dispersed tree species (Schupp 1992).

The tropical rainforest is a mosaic both in the spatial distribution of plant species, which are often clumped, and in the forest dynamics with the juxtaposition of areas of different age (e.g. Hubbell 1979, Alexandre 1989, Whitmore 1991). The role of frugivorous animals is central to the mechanisms of natural regeneration of tropical forests, since 60 to 95% of tropical plant species mainly depend on them for their seed dispersal (Charles-Dominique Chapter 17). Though monkeys represent the largest biomass of frugivores in tropical forests (25 to 40%; according to Eisenberg & Thorington 1973), as yet, except for some particular studies (Sourd & Gautier-Hion 1986, Janson et al. 1986), most of the studies of fruit choice by frugivorous vertebrates mainly concern birds (Erard & Théry Chapter 22). Other studies analysed the interactions between fruits and a community of vertebrate frugivores including several primates species (Janson 1983, Knight & Siegfried 1983, Gautier-Hion et al. 1985, Dowsett-Lemaire 1988).

Field studies in recent decades have shown that idea of an overabundance of food for consumers in tropical evergreen rainforests is too simplistic (e.g. Milton 1980, Terborgh 1986). There is considerable evidence of difficulties encountered by animals when seeking foods. Among these, food availability is known to vary between locations, seasons and years, often in an unpredictable manner (e.g. Sabatier 1985). Plant defences against consumers can reduce access to nutrients in subtle ways. For example, leaf allelochemicals may vary qualitatively and quantitatively according to light exposure within a single tree (Waterman & Kool 1994) and in relation to herbivore pressure (Feeny 1970). Following such variability in food availability, fluctuations in food choices and nutrient intake throughout the year are the rule among primates (Hladik 1988). In this context, species exhibit a wide variety of feeding strategies, depending on specific metabolic needs, digestive efficiency, sensory perception of the environment and cognitive abilities, sometimes leading to the development of feeding traditions (Hladik & Simmen 1996). Although primate species are variously constrained in their niche breadth (Milton 1981), it has become clear, in view of these findings, that primate diets are best described as flexible (Gautier-Hion et al. 1993).

The net result of the multi-stage recruitment from seed production to seedling establishment was assessed along 3 consecutive years in Chrysophyllum lucentifolium (Sapotaceae) in a mature rain forest of French Guiana. According to year, between 37 and 42 % of seed production was primarily dispersed away from fruiting trees without damage, especially by primates. Seeds dispersed in howler monkeys' (Alouatta seniculus) defecation were serendipitously buried by dung beetles (14%), eaten by terrestrial vertebrates such as rodents, or destroyed by insects or pathogens. The proportion of seeds secondarily dispersed by scatterhoarding rodents Varied from 3 to 17 % according to year. The survival rate of unremoved and uneaten seeds after 20 days, varied from 2 to 56 % according to year and pattern of spatial distribution generated by primary dispersal (clump or scattered). The empirical model based on the seed and seedling fate diagram showed that, according to years, from 6 to 15 % of produced seeds lead to seedling establishment away from parent tree. Variations in patterns of seed removal and predation by rodents were the most crucial factors governing the effectiveness of primary and secondary dispersers and the spatial distribution of seedlings. Between-year variations of recruitment were important and stochastic because the fluctuations of seed production and seed dispersal/predation varied independently. The proposed empirical model has thus no predictive value. However it can be useful for instance to test the effects of seed size and of some faunal perturbations.

The net result of the multi-stage recruitment from seed production to seedling establishment was assessed along 3 consecutive years in Chrysophyllum lucentifolium (Sapotaceae) in a mature rain forest of French Guiana. According to year, between 37 and 42 % of seed production was primarily dispersed away from fruiting trees without damage, especially by primates. Seeds dispersed in howler monkeys’ (Mouatta seniculus) defecation were serendipitously buried by dung beetles (14%), eaten by terrestrial vertebrates such as rodents, or destroyed by insects or pathogens. The proportion of seeds secondarily dispersed by scatterhoarding rodents varied from 3 to 17 % according to year. The survival rate of unremoved and uneaten seeds after 20 days, varied from 2 to 56 % according to year and pattern of spatial distribution generated by primary dispersal (clump or scattered). The empirical model based on the seed and seedling fate diagram showed that, according to years, from 6 to 15 % of produced seeds lead to seedling establishment away from parent tree. Variations in patterns of seed removal and predation by rodents were the most crucial factors governing the effectiveness of primary and secondary dispersers and the spatial distribution of seedlings. Between-year variations of recruitment were important and stochastic because the fluctuations of seed production and seed dispersal/predation varied independently. The proposed empirical model has thus no predictive value. However it can be useful for instance to test the effects of seed size and of some faunal perturbations.

Although trichromacy in Old and New World primates is based on three visual pigments with spectral peaks in the violet (SW, shortwave), green (MW, middlewave) and yellow-green (LW, longwave) regions of the spectrum, the underlying genetic mechanisms differ. The SW pigment is encoded in both cases by an autosomal gene and, in Old World primates, the MW and LW pigments by separate genes on the X chromosome. In contrast, there is a single polymorphic X-linked gene in most New World primates with three alleles coding for spectrally distinct pigments. The one reported exception to this rule is the New World howler monkey that follows the Old World system of separate LW and MW genes. A comparison of gene sequences in these different genetic systems indicates that the duplication that gave rise to the separate MW and LW genes of Old World primates is more ancient than that in the howler monkey. In addition, the amino acid sequences of the two howler monkey pigments show similarities to the pigments encoded by the polymorphic gene of other New World primates. It would appear therefore that the howler monkey gene duplication arose after the split between New and Old World primates and was generated by an unequal crossover that placed two different forms of the New World polymorphic gene on to a single chromosome. In contrast, the lack of identity at variable sites within the New and Old World systems argues for the origin of the separate genes in Old World primates by the duplication of a single form of the gene followed by divergence to give spectrally distinct LW and MW pigments. In contrast, the similarity in amino acid variation across the tri-allelic system of New World primates indicates that this polymorphism had a single origin in New World primates. A striking feature of all these pigments is the use of a common set of substitutions at three amino acid sites to achieve the spectral shift from MW at around 530 nm to LW at around 560 nm. The separate origin of the trichromacy in New and Old World primates would indicate that the selection of these three sites is the result of convergent evolution, perhaps as a consequence of visual adaptation in both cases to foraging for yellow and orange fruits against a green foliage.