**4.5 Fig foraging**

36 Zoology

The concise answer to the question of who eats figs was offered by Daniel Janzen (1979): "Everybody." Indeed, figs are notable for the number of bird and mammal species that consume their fruits and they comprise a part of the diet for more species of animal than any other genus of wild tropical perennial fruit (Janzen, 1979). In this section, we focus on the

A review of the literature on neotropical primates reveals that all diurnal frugivorous genera with a body mass exceeding Kay's 500g threshold (Fleagle, 1999) include figs in their diet to varying extents, with the exception of uakari monkeys of the genus *Cacajao* (Mivart, 1865) for which dietary information is scant (Boubli, 1999). Tamarins (*Saguinus* species) and marmosets (*Callithrix kuhlii*, Coimbra-Filho, 1985) have been found to include a variety of fig species in their diet across sites (Knogge et al., 2003; Raboy et al., 2008; Terborgh, 1983). Three of the four *Ficus* species present at a Brazilian site are included in the 55 "extremely valuable" species consumed by golden-lion tamarins (*Leontopithecus chrysomelas*, Kuhl, 1820) (Oliveira et al., 2009). The seventh most frequently consumed fruit of black titi monkeys (*Callicebus torquatus lugens*, Hoffmannsegg, 1807) in Columbia was the single species *Ficus mathewsii* (Palacios et al., 1997). At five different sites in South America (Yasuni, Caparu, Urucu, Tinigua and Pacaya) figs were one of the top seven genera consumed by woolly monkeys (*Lagothrix lagotricha*, Humboldt, 1812) at each site (di Fiore, 2004). In Cocha Cashu, Peru, brown capuchin monkeys (*Cebus apella*, Linnaeus, 1758) were found to eat figs whenever they were available, and South American squirrel monkeys (*Saimiri sciurius*, Linnaeus, 1758) and white-fronted capuchin monkeys (*Cebus albifrons*, Humboldt, 1812) concentrated feasting on figs whenever they were available (Terborgh, 1983). White-faced capuchins (*Cebus capucinus*) in Santa Rosa, Costa Rica prefer figs over all other ripe fruits, and concentrate their foraging efforts on *Ficus* whenever available, regardless of the presence and abundance of other ripe fruits in their habitat (Melin et al., 2009). Figs comprised nearly one-third of capuchin annual fruit foraging effort which represents overselection relative to fig abundance (Melin et al., 2009). For black-faced spider monkeys (*Ateles chamek*) in the Guarayos Forest Reserve in Bolivia, the preference for figs relative to all other ripe fruits is striking, and when combined with data on habitat-wide fruit availability indicates that "spider monkeys consumed a diverse array of ripe fruits to overcome periods of fig scarcity rather than vice versa" (Felton et al., 2009). Even species that are considered to be folivorous show a preference for *Ficus* fruits. One study of Mexican howler monkeys (*Alouatta palliata mexicana*, Merriam, 1902) found that six *Ficus* species were amongst the eight most important species consumed at one site in Veracruz, Mexico (Serio-Silva et al., 2002). Diurnal frugivorous and folivorous neotropical primates thus all eat figs to a greater or lesser extent, with some species showing an unequivocal preference for them even during periods of high habitat wide fruit availability. The feeding ecology of platyrrhines, coupled with preliminary evidence for the protein content of neotropical figs indicate that rather than viewing figs as a fallback foods in times of habitat-wide fruit scarcity (Dominy et al., 2003; Shanahan et al., 2001) it may be more appropriate to view them

role of figs in the diet and feeding ecology of platyrrhines.

as important, preferred and limiting resources.

**4.4 The relative abundance of Ficus species in Africa and the Neotropics** 

In order for figs to be a more important source of protein for New World monkeys vis-à-vis catarrhines, it is necessary to demonstrate that figs are abundantly present in the neotropics

**4.3 Who eats figs?** 

Colour vision polymorphism has persisted in primates for up to 14 million years (Surridge & Mundy, 2002). In order for polymorphic trichromacy in platyrrhines to be considered as an adaptive strategy it must be demonstrated that there is some advantage to the maintenance of different colour vision phenotypes within a population (Melin et al., 2008). There exists ample evidence for a trichromat advantage during ripe fruit foraging (Melin et al., 2009; Regan et al., 1998; Riba-Hernández et al., 2005; Smith et al., 2003; Sumner & Mollon, 2000b; Yamashita et al., 2005). To our knowledge, the only published study on fig foraging by wild platyrrhines (Melin et al., 2009) found that trichromatic white-faced

Protein Limitation Explains Variation in Primate

Colour Vision Phenotypes: A Unified Model for the Evolution of Primate Trichromatic Vision 39

adaptive strategies aimed at the detection of proteinaceous foods. In continental Africa where frugivorous primates rely on young, reddish leaves as protein sources (Dominy et al., 2003), routine trichromacy is the rule. In New World tropical forests efficient foraging for conspicuously coloured proteinaceous figs may favor trichromats and maintain colour vision polymorphism via heterozygote advantage. It is also worthwhile to mention that the selection pressures acting on trichromacy may be less in the New World because insects represent a protein source to many neotropical monkeys and dichromacy is useful in the detection of surface-dwelling insects (Melin et al., 2007; Melin et al., 2010) via the enhanced

Rather than viewing figs as fallback resources (Dominy et al., 2003; Shanahan et al., 2001) we propose that they are preferred and limiting resources. Additionally, given the timing of Old World phenophases, where young leaves are most widely available during periods of overall fruit scarcity (Dominy et al., 2003), it is not possible to clearly identify young leaves as fallback foods, since the definition of a fallback food requires spatial and temporal ubiquity (Marshall & Wrangham, 2007). The evolution and maintenance of polymorphic trichromacy is a response to variation in the detectability not of fallback foods, but of the

Our analysis has been restricted to continental Africa and the neotropics due to the availability of data from these continents. However, the recent discovery of polymorphic trichromacy amongst some Malagasy strepsirrhines (Tan & Li, 1999; Veilleux & Bolnick, 2009) will provide an interesting comparative dataset against which to test hypotheses. Under the protein limitation hypotheses, we predict that balancing selection will favor polymorphic trichromacy via a heterozygote advantage in frugivorous strepsirrhines whose protein source is conspicuous. Given current evidence for the low abundance of *Ficus* in Malagasy forests and the recent discovery of a paucity of available protein in Malagasy *Ficus* fruits (Ganzhorn et al., 2009), it seems likely that Malagasy protein resources and resulting

Many hypotheses regarding primate morphological adaptations hinge on the importance of fallback foods (Dominy & Lucas, 2001; Marshall & Wrangham, 2007), and foods that are dominant in primate diets (Osorio & Vorobyev, 1996; Regan et al., 2001; Smith et al., 2003). This represents an unusual departure from studies of primate behaviour which tend to focus on the centrality of limiting resources (e.g. Sterck et al., 1997; van Schaik, 1989; Wrangham, 1980). Studies of primate foraging adaptations might benefit from the additional consideration of morphological and sensory adaptations to foraging on limiting resources.

We would like to thank the staff of the Área de Conservación Guanacaste, especially Roger Blanco, Maria Marta Chavarria and the administration of the Sector Santa Rosa, for help and for permission to conduct research in the park. We also thank the STRI Center for Tropical Forest Science: all *Ficus* data denoted as being from STRI came from their website: www.ctfs.si.edu. The authors gratefully acknowledge Adrián Guadamuz, John Addicott, Mike Lemmon, Barbara Kowalsic and Nigel Parr for contributions to the *Ficus* project, as well as Linda Fedigan, Carl Toborowsky, Adrienne Blauel, Mackenzie Bergstrom, Brandon Klug, Laura Weckman, Fernando Campos and Valerie Schoof for their assistance. We thank

ability of dichromats to break camouflage (Caine et al., 2010; Morgan et al., 1992).

limiting resources of frugivorous primates: proteinaceous foods.

effects on strepsirrhine colour vision capabilities will be found elsewhere.

**6. Acknowledgements** 

capuchin monkeys (*Cebus capucinus*) demonstrate a foraging advantage when feeding on ripe figs. Conspicuous figs were more common than cryptic figs at the research site, and were fed on much more frequently. Trichromatic monkeys had a higher acceptance index of conspicuous figs than did dichromats, suggesting an ability to select riper figs based on visual cues. Dichromats, on the other hand, used longer and more diverse foraging sequences (e.g. frequent sniffing) when assessing figs. While the variation in foraging behaviour did not result in a net variation of fig intake rate, the authors suggest that it is possible that the improved discrimination ability of trichromats may lead to higher feeding rates under conditions where ripe fruit is less available and quickly depleted. Additionally, trichromatic monkeys seemed better able to select the ripest figs, while dichromats consumed mid-ripe (yellowish) figs more often (A.D Melin, pers. obs).


\* 8 species of *Ficus* are known in Sector Santa Rosa (Melin et al., 2009) however only 2 species have been encountered to date in transects (Parr et al., In Press).

\*\* If only those fig trees with a DBH of 10cm or greater are included, then the number of individuals drops to three, and density drops to 1.13 (N.Parr, pers. comm.).

Table 1. Number of species and individuals of the genus *Ficus* in African and neotropical forests.

## **5. Conclusion**

While most hypotheses for the variation in colour vision capabilities of catarrhines and platyrrhines posit the importance of either the ability to detect ripe fruit (Regan et al., 2001) or young leaves (Dominy et al., 2003) there is evidence that this variation stems from visual adaptive strategies aimed at the detection of proteinaceous foods. In continental Africa where frugivorous primates rely on young, reddish leaves as protein sources (Dominy et al., 2003), routine trichromacy is the rule. In New World tropical forests efficient foraging for conspicuously coloured proteinaceous figs may favor trichromats and maintain colour vision polymorphism via heterozygote advantage. It is also worthwhile to mention that the selection pressures acting on trichromacy may be less in the New World because insects represent a protein source to many neotropical monkeys and dichromacy is useful in the detection of surface-dwelling insects (Melin et al., 2007; Melin et al., 2010) via the enhanced ability of dichromats to break camouflage (Caine et al., 2010; Morgan et al., 1992).

Rather than viewing figs as fallback resources (Dominy et al., 2003; Shanahan et al., 2001) we propose that they are preferred and limiting resources. Additionally, given the timing of Old World phenophases, where young leaves are most widely available during periods of overall fruit scarcity (Dominy et al., 2003), it is not possible to clearly identify young leaves as fallback foods, since the definition of a fallback food requires spatial and temporal ubiquity (Marshall & Wrangham, 2007). The evolution and maintenance of polymorphic trichromacy is a response to variation in the detectability not of fallback foods, but of the limiting resources of frugivorous primates: proteinaceous foods.

Our analysis has been restricted to continental Africa and the neotropics due to the availability of data from these continents. However, the recent discovery of polymorphic trichromacy amongst some Malagasy strepsirrhines (Tan & Li, 1999; Veilleux & Bolnick, 2009) will provide an interesting comparative dataset against which to test hypotheses. Under the protein limitation hypotheses, we predict that balancing selection will favor polymorphic trichromacy via a heterozygote advantage in frugivorous strepsirrhines whose protein source is conspicuous. Given current evidence for the low abundance of *Ficus* in Malagasy forests and the recent discovery of a paucity of available protein in Malagasy *Ficus* fruits (Ganzhorn et al., 2009), it seems likely that Malagasy protein resources and resulting effects on strepsirrhine colour vision capabilities will be found elsewhere.

Many hypotheses regarding primate morphological adaptations hinge on the importance of fallback foods (Dominy & Lucas, 2001; Marshall & Wrangham, 2007), and foods that are dominant in primate diets (Osorio & Vorobyev, 1996; Regan et al., 2001; Smith et al., 2003). This represents an unusual departure from studies of primate behaviour which tend to focus on the centrality of limiting resources (e.g. Sterck et al., 1997; van Schaik, 1989; Wrangham, 1980). Studies of primate foraging adaptations might benefit from the additional consideration of morphological and sensory adaptations to foraging on limiting resources.
