Diet and Food Choice in Peruvian Red Uakaris ( Cacajao calvus ucayalii ): Selective or Opportunistic Seed Predation

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Even primates considered dietary specialists tend to eat a combination of fruit pulp, seeds, other plant parts, or animals. Specialist seed predators could either feed on seeds preferentially, or to avoid competition when ripe pulps are scarce.
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  Diet and Food Choice in Peruvian Red Uakaris( Cacajao calvus ucayalii  ): Selectiveor Opportunistic Seed Predation? Mark Bowler  &  Richard E. Bodmer Received: 5 August 2010 /Accepted: 11 April 2011 # Springer Science+Business Media, LLC 2011 Abstract  Even primates considered dietary specialists tend to eat a combination of fruit pulp, seeds, other plant parts, or animals. Specialist seed predators could either feed on seeds preferentially, or to avoid competition when ripe pulps are scarce.Pitheciin monkeys have specialized dentition that allows them to feed on seeds protected by hard shells, and the upper limit on the hardness of these is likely to be a function of jaw size. We recorded the diet of Peruvian red uakaris ( Cacajao calvusucayalii ) on the Yavari River, Peru, to test the prediction that this seed predator would feed on the seeds of hard-shelled fruits preferentially over softer ones inrelation to their availability in the forest. We also tested predictions that adult male,adult female, and juvenile diets would differ, with larger individuals eating morehard fruits. Uakaris ate 55.4% seeds, 38.9% pulps and arils, and 5.6% other items, but proportions varied through the year. More pulps, especially from the palm  Mauritia flexuosa , were eaten when fruit availability was low, and more hard fruitswere positively selected for than softer ones. Juveniles did not open the hardest fruit species opened by adults, and adult males ate harder fruits than females. Theseresults provide evidence that seed eating in some primates has evolved beyond a means of avoiding competition for the ripe pulps typically preferred by many primates. Specialist seeding-eating primates therefore occupy divergent niches that require separate consideration from those of similar-sized primates. Keywords  Cacajao.Diet .Pitheciin.Pitheciini.Uacari.Uakari Int J PrimatolDOI 10.1007/s10764-011-9527-6 Electronic supplementary material  The online version of this article (doi:10.1007/s10764-011-9527-6)contains supplementary material, which is available to authorized users.M. Bowler ( * )Department of Psychology, University of St. Andrews, St. Mary ’ s College,St. Andrews KY16 9JU, UK e-mail: mtb21@st-andrews.ac.uk M. Bowler  :  R. E. Bodmer Durrell Institute of Conservation and Ecology, University of Kent, Canterbury CT2 7NR, UK   Introduction Although most primates are largely frugivorous, diets are diverse and can includeripe or unripe fruit pulps and seeds as well as leaves, exudates, and other plant  parts or animals in various proportions (Rosenberger  1992). Primates that feed  predominantly on any particular resource category are considered dietary special-ists, but even such specialists tend to use a combination of foods (Rosenberger 1992). The diets of sympatric primates typically overlap considerably when ripefruit pulp is abundant, and it is during periods of relative ripe fruit pulp scarcitythat the diets of sympatric species differentiate (Stevenson  et al  . 2000; Terborgh1983; Tutin  et al  . 1997). Several primate species are considered specialists in masticating and digestingseeds. Among the Old World primates, seeds make up a large proportion of thediets of colobine monkeys (subfamily Colobinae: Dasilva  1994; Kool 1993; Maisels  et al.  1994), mangabeys ( Cercocebus : Waser  1984), mandrills (  Mandrillus sphinx : Lahm 1986), orangutans (  Pongo pygmaeus : Ungar  1995), and sifakas (  Propithecus diadema : Hemingway 1998; Yamashita  1996). Of the New World  primates, brown capuchins ( Cebus paella : Peres 1991; Terborgh 1983), woolly monkeys (  Lagothrix lagothricha : Peres 1994), and titis ( Callicebus personatus :Heiduck  1997) show some dependence on seeds, but the sakis (  Pithecia ), beardedsakis ( Chiropotes ), and uakaris ( Cacajao ), collectively the tribe Pitheciini (Rosenberger  et al  . 1996), are unique among Neotropical primates in that they are specialized seed predators (Aquino 1995, Aquino and Encarnación 1999; Ayres 1986, 1989; Barnett   et al.  2005; Boubli 1999; Buchanan  et al.  1981; Cunningham and Janson 2006; Johns 1986; Kinzey and Norconk  1993; Norconk and Conklin-Brittain 2004; Peres 1993; Setz 1994; van Roosmalen  et al.  1988). Large, palatable seeds are often protected byhard shells (Fischer and Chapman 1993; Norconk   et al.  1998), and pitheciins areequipped to open such fruits. Their enlarged canines pierce hard shells, and they thenremove seeds from the shells with forward-pointing incisors; a process calledsclerocarpic harvesting (Kinzey 1992; Kinzey and Norconk  1990). The puncture resistance of fruits eaten by bearded sakis is up to 15 times greater than of thoseconsumed by spider monkeys (  Ateles ), and hardness of fruit pericarps may play a significant role in food choice in sympatric primates (Kinzey and Norconk  1990). That primate diets tend to converge when ripe fruit pulp is abundant begs thequestion: Do primates that are specialized to predate seeds feed on them preferentially or do they do so to avoid competition when ripe pulps are scarce?Some primates select food based on nutritional needs; e.g., sympatric howlers(  Alouatta palliata ) and spider monkeys (  Ateles geoffroyi ) appear to eat proportionsof leaves and ripe fruits depending on their abilities to digest these food types andextract the proteins and carbohydrates they require (Milton 1981). However, masked titis ( Callicebus personatus ) feed on higher proportions of seeds duringlean periods when fleshy fruits are less abundant and nutrient content does not appear to affect selection (Heiduck  1997). Similar examples, in which food abundance is the main factor in determining food selection, suggest that many primates feed opportunistically on foods available to them (Dasilva  1994; Barton and Whiten 1994; Mowry  et al  . 1996). The proportion of ripe pulps and arils vs.seeds in the diet of white uakaris ( Cacajao calvus calvus ) at Tefé, Brazil increases M. Bowler, R. Bodmer   when fruit production is high (Ayres 1986). Similarly, in white-faced sakis(  Pithecia pithecia ) and bearded sakis ( Chiropotes satanas ) the ripening of themost-eaten resources brings about a switch from unripe seeds to ripe pulps( Norconk  1996). Contrary to these studies, black uakaris ( Cacajao melanocepha-lus ) at Pico da Neblina, Brazil, eat proportionally more ripe pulps and arils andfewer seeds when fruits are scarce in the forest (Boubli 1999), and  Pithecia pithecia  at Guri Lake, Venezuela eat fewer seeds and more leaves, insects, andflowers when fruits are scarce (Cunningham and Janson 2006). In all of these studies on pitheciins, the proportions of seeds and pulps in the diet variedseasonally and the authors related this to the relative availability of the plant parts, but they did not measure the selectivity for the fruit species concerned compared totheir availability in the environment.One consequence of a diet of hard-shelled fruits is that the upper limit on thehardness of fruits eaten is likely to be a function of jaw size and muscle mass.Thus smaller individuals may not be able to access harder fruits (Boubli 1999). Chiropotes  eats harder fruits on average than the smaller   Pithecia  (Kinzey and Norconk  1993), and juvenile black uakaris appear unable to open several fruit species eaten by adults (Boubli 1999), but no researchers have ever directly compared the diets of wild uakaris of different sizes in the same group. Highsexual dimorphism in uakaris (Hershkovitz 1987) may mean that males andfemales, as well as individuals of different age classes, differ in their ability to openhard fruits.We here examine the diet of one of the most specialized seed predators, thePeruvian red uakari ( Cacajao calvus ucayalii ), to test the prediction that specializedseed predators will feed on the seeds of hard-shelled fruits preferentially over ripe pulps, selecting fruits with harder shells more frequently than softer ones in relationto their availability in the forest. We also test the prediction that adults feed on harder fruits on average than juveniles, and that adult males feed on harder fruits on averagethan adult females. Methods Study Area We conducted the study in the 9926.19-ha Lago Preto Conservation Concession,Loreto, Peru (S04°27.5 ′  W071°45.9 ′ ), bordered by the Yavarí and Yavarí-Mirínrivers in the south and west, and by the Iquitos-Yavarí logging concessions in thenorth and east (Fig. 1). The concession contains nonflooding  terra firme  forest,white-water   várzea  forest that floods with silt-laden water between November andMay each year, and permanently waterlogged forest known as  aguajal   dominated by the palm  Mauritia flexuosa  and sometimes with a more open canopy similar tothe  chavascal   habitat (Boubli 1999). There are 13 primate species including red uakaris.Total annual precipitation is 2,000  –  3,000 mm, and though the climate is not veryseasonal, average rainfall peaks between December and March with drier months between May and August (Pitman  et al.  2003). Mean temperatures are between 24 Food Choice in Peruvian Red Uakaris  and 26°C and are fairly constant throughout the year, aside from rare southerly windsthat can produce minimum temperatures of 10°C (Pitman  et al.  2003).Fruit AvailabilityTo determine changes in the availability of fruit at Lago Preto, we measured transectson 8 randomly selected trails in each of the main habitats. All transects were 5 mwide except 1  ,  which was created as part of another survey and was 20 m wide(Pitman  et al  . 2003). We tagged and identified every tree of diameter at breast height (DBH) >10 cm within the transects and every vine or liana of DBH >7 cm on all5-m wide transects (Ayres 1986). To obtain a reasonable sample of the diversity ineach habitat, we sampled habitats until the rate of discovery of new species slowed(Sutherland 2000), thus determining the length and area of each transect. We sampled 589 trees and vines in 8,970 m 2 of   terra firme , 387 trees and vines in6,135 m 2 of   várzea , and 386 trees and vines in 5,150 m 2 of   aguajal   habitat.Between March 2004 and February 2005, starting as close to the middle of eachmonth as possible, we examined the canopy of each tagged tree or vine with binoculars and a small telescope, recording the presence of immature fruit (unripefruits smaller than mature fruits of the species), unripe fruit (full-sized fruits that had not ripened), and ripe fruit.We used the number of trees bearing fruit per hectare as a measure of fruit availability in each habitat (Ayres 1986; Stevenson  et al  . 1998), and combined theseto produce monthly estimates of fruit availability in the uakaris ’  home range for each plant genus and for immature, unripe, and ripe fruit, adjusting for the proportions of each habitat in home range. Fig. 1  Map showing the location of the Lago Preto Conservation Concession and surrounding areas.(From Bowler and Bodmer  2009).M. Bowler, R. Bodmer   Behavioral SamplingMore than 150 uakaris were present in the study area in groups of variable size(1 to >150 individuals; mean±SD=43.57±24.1) that often fissioned and fusedthroughout the day (Bowler and Bodmer  2009). We located groups by walking trails or searching flooded  várzea  by canoe, following them until dusk, or we lost the group. Groups sometimes disappeared for up to 5 d, but were more commonlyfound within 2 d of searching. When we were able to follow the group to itssleeping trees, we often relocated it before dawn the following day. Between April2003 and July 2005, including all months except February 2004 and April and May2005, we made 239 contacts with uakari groups during which we collected 945 hand 10 min of behavioural observations (33  –  123 h of data per calendar month).We used point scan sampling (Altmann 1974) at 10-min intervals, allowing 1 min to complete the scans. In each scan, we recorded the location of the group using a GPS (Garmin GPS72) and the age  –  sex class and behavior of each visible monkey,using the following age  –  sex classes: infant 1 (1  –  3 mo), infant 2 (3  –  12 mo), juvenile(12  –  36 mo), subadult male, unsexed subadult, adult male, and adult female (Bowler and Bodmer  2009; Fontaine 1981). We recorded the following behavioral categories: feed, search, move, social, and rest (Bowler and Bodmer  2009). Feed included masticating, swallowing, processing, or carrying food items. Where possible, werecorded the plant species, parts (seeds, pulp, arils, flowers, leaves, or others), andthe maturity of the fruit eaten by the individual through observation and bycollecting discarded parts. Search included breaking apart or examining branches or foliage.Because differing canopy densities between tree species can lead to under- or overrepresentation in the recorded diet through visibility bias, an effect exaggerated by scan sampling, and because insects and fruits with short  processing times are disproportionately rare in scan samples, we also used 1  –  0sampling (Altmann 1974), recording a 1 for each species used by  ≥ 1 individualsduring a 10-min period. This method underestimates the importance of species that were fed on intensively by uakaris, but ensures that all species observed beingeaten are recorded. We also recorded the plant parts used for each species on a 1  –  0 basis.Professional botanists identified plant species that we recorded on transects or inthe diet from photographs and voucher specimens and they deposited the plants at the Herbarium at the Universidad Nacional de la Amazonía Peruana (UNAP),Iquitos.Fruit Hardness CategoriesWe gave each fruit species eaten a subjective score for the hardness and punctureresistance of the fruit using criteria similar to those of Boubli (1999), but further subdividing the harder fruits.Hardness categories:1) Soft; fruits as soft as grapes, crushable with the fingers2) Medium; fruits with husks comparable to those of avocados Food Choice in Peruvian Red Uakaris
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