Introduction
Several species of primates consume nectar and/or pollen (Sussman, 1979; Torres de Assumpção, 1981; Puertas et al., 1992; Peres, 1994; Carthew & Goldingay, 1997; Birkinshaw & Colquhoun, 1998; Passos & Kim, 1999; Riba-Hernández & Stoner, 2005; Marín-Gómez, 2008). Nectar is a high-energy resource and an important food source for mammals living in habitats with marked seasonality (Janson et al., 1981; Garber, 1988; Ferrari & Strier, 1992). Also, mammals including primates can be possible pollinators of different plant species (Kress et al., 1994; Carthew & Goldingay, 1997).
Black and gold howler monkeys, Alouatta caraya, are characterized by a folivore-frugivore opportunistic diet (Milton, 1998). This arboreal species inhabits different types of tropical and subtropical forests in NE Argentina, SE Brazil, Paraguay, and Bolivia (Crockett & Eisenberg, 1987; Zunino & Kowalewski, 2008). Grevillea robusta (Family Proteaceae) is a tree native to eastern Australia and it has been widely planted in subtropical and tropical environments of Africa, America, and Asia (Harwood, 1992). In Argentina, this species was introduced in the late nineteenth century for construction of furniture (Moscovich et al., 2004). Grevillea robusta has hermaphroditic and bright yellow-orange flowers (approximately 23 mm long) grouped into terminal racemes. Fruits are black leathery dehiscent follicles with two seeds. The pollen is deposited onto a cone around the stigma and the nectary secretes yellow nectar that accumulates in a large drop between the style and the perianth segment (McGillivray, 1993; Kalinganire et al., 2000). The species shows both protandry (anthers dehisce prior to stigma receptivity) and a self-incompatibility mechanism (Kalinganire et al., 2000). Therefore, the flowers need pollinators to produce fruits. The species of Proteaceae are not specialized to certain groups of pollinators; they are generalists (Collins & Rebelo, 1987). The clustering of flowers on the ends of branches, brush-type presentation, bright color, and copious nectar production suggest that G. robusta is pollinated by diurnal animals, similar to other proteaceous species (Collins & Rebelo, 1987; Kalinganire et al., 2000).
For exotic plants like G. robusta in forests in northeast Argentina, pollination success depend on density of plant populations which may affect the attractiveness of enough pollinators, the competition with native vegetation for pollinator attention, and the low number of suitable generalist pollinator species (Stout et al., 2006). However, if generalist native species pollinate introduced plants and these pollinators are abundant, exotic species may be reproductively successful and spread rapidly (Parker, 1997). The aim of this study is to describe the nectar feeding behavior of Alouatta caraya on an exotic tree (Grevillea robusta, Proteaceae) and suggest the possible role of this primate in flower pollination.
Materials and methods
The study was carried out at San Cayetano (27° 30′ S, 58° 41 W), Corrientes Province, Argentina (Rumiz, 1990). The climate is subtropical with an average annual temperature of 21.7° C and an average annual of rainfall of 1,230 mm; the rainfall decreases slightly in the winter (July to August) (Zunino et al., 2007). The site presents a fragmented forest and the vegetation is characterized by dense, semideciduous upland and riparian forests, open lowland forests with palm trees, and grasslands (Zunino et al., 2007). The forest has been heavily modified by logging, the presence of cattle, and burning (Zunino et al., 2007). In addition, there are some individuals of exotic vegetation such as Citrus spp, Grevillea robusta, Hovenia dulcis, and Melia azedarach.
Observations were collected on two groups of howlers (Ariscos and Huerta) between 2005 and 2008 during a long-term ecological and behavioral study on A. caraya in San Cayetano. We used scan and focal sampling techniques (Altmann, 1974) from sunrise to sunset. During the scan sampling we recorded behaviors and spatial distributions of the whole group every 10 min. During focal sampling we recorded the behavior, height and tree species used, and distance to the nearest individual. We present data from the two sampling techniques but quantitative data on nectar-feeding behavior are based only on scan sampling. We calculated the percentage of feeding records and the rate of nectar-feeding per group per hour. In Table 1 we present the two study groups including study period, date of nectar-feeding, sampling technique, sex-age composition, and flower damage.
Results
The home range size of Ariscos and Huerta groups are 3.78 ha y 6.26 ha respectively. There are two G. robusta trees (separated by 80m) within Ariscos's home range, and one within Huerta. Howlers were observed exploiting the flowers of G. robusta in spring (October and November). The nectar-feeding records are the following:
Ariscos group. November 2005 (Table 1). We observed nectar-feeding on one of the two trees within the home range. Nectar-feeding accounted for 6.2% of the 97 scan sampling feeding records (rate: 0.004 records per hour). The whole group consumed nectar and two of them (an adult female and a juvenile male) fed simultaneously on the same tree 1 m one from the other. Howlers brought their mouth near to the flowers attached to the inflorescence and licked nectar. They obtained nectar from different inflorescences of the same tree. They did not eat any other part of the flower except the nectar. After each feeding bout, howlers carried abundant yellow pollen on their snouts.
Ariscos group. October 2007 (Tabla 1). Nectarfeeding accounted for 5.5% of the 165 scan sampling feeding records (rate: 0.24 nectar-feeding records per hour). Two individuals (a subadult male and a juvenile male) consumed nectar and the same tree was visited 2 consecutive days. Howlers fed on nectar in the same way as observed in November 2005. They fed simultaneously on the same tree 3–4 m one from the other.
Huerta group. October 2007 (Table 1). In October 26, we observed one juvenile male eating one flower of G. robusta and drinking rainwater accumulated in the flowers (1h total of focal sampling). On October 27th, the same individual drank rainwater from the flowers. Two juvenile females and the infant were observed drinking rainwater from the flowers at 1m of the juvenile male (1h total of focal sampling). In the two days of focal after drinking the juvenile male carried pollen on its snout.
Huerta group. October, 2008. During the scan sampling, we observed nectar-feeding by four individuals (Table 1). This accounted for 4% of the 99 scan sampling feeding records (rate: 0.17 nectar-feeding records per hour). One individual obtained nectar from different inflorescences of the same tree and two individuals fed simultaneously on the same tree between 0.5 and 2m of distance. Howlers fed on nectar as was observed in Ariscos group. They did not eat any other part of the flower except the nectar. After feeding bouts, howlers carried abundant yellow pollen on their snouts. During the focal sampling, we only observed the infant feeding on nectar. This infant consumed nectar in three occasions for a total of 21.24h of focal sampling. On one occasion, the infant consumed both nectar and flower parts.
Table 1.
Summary of nectar-feeding records in two groups of Alouatta caraya in San Cayetano.
Discussion
This study shows that nectar-feeding was a rare behavior in the feeding repertory of A. caraya (the average rate of nectar-feeding was 0.14 records per hour). The nectar is an opportunistic food resource. Only young individuals ate part or all of the flowers together with the nectar. In this regard, Pereira & Fairbanks (1993) show that juveniles spent more time exploring novel objects, including food, in comparison to adult individuals. The rest of the age-classes licked the nectar and did not eat any other part of the flower. Garber (1988) and Riba-Hernández & Stoner (2005) found that adult individuals of Ateles geoffroyi, Saguinus mystax, and S. fuscicollis destroy the flowers of Symphonia globulifera (Guttiferae) when they were feeding on nectar. In contrast, studies on Aotus trivirgatus, Ateles paniscus, Brachyteles arachnoides, Callithrix flaviceps, Cebuella pygmaea, Cebus albifrons, C. apella, Eulemur macaco, Saguinus fuscicollis, S. imperator, and Saimiri sciureus (Janson et al., 1981; Torres de Assumpção, 1981; Ferrari & Strier, 1992; Birkinshaw & Colquhoun, 1998) found that animals did not eat or caused little damage to the flowers when they were feeding on nectar.
Every time howlers visited flowers to feed on nectar they removed pollen with their snouts. They moved between different inflorescences on the same tree, potentially facilitating pollen movement between flowers of the same tree. However, monkeys did not engage in cross-pollination because in Huerta's home range there was just one tree of G. robusta and in Ariscos's home range there were two trees but separated by 80m. Nevertheless, we observed effective seed production in the three G. robusta trees used by the howlers. Other non-human primates appear to be involved in pollination, i.e Aotus lemurinus (Marín-Gómez, 2008), B. arachnoides (Torres de Assumpção, 1981), C. apella (Torres de Assumpção, 1981), and E. macaco (Birkinshaw & Colquhoun, 1998).
Grevillea robusta has features that can allow its pollination by diurnal vertebrates such as A. caraya including a partially fused perianth, brightly colored flowers in terminal racemes, simultaneous flower opening, and abundant nectar and pollen production (Janson et al., 1981; Carthew & Goldingay, 1997). In Australia, 28 species of Proteaceae are visited by non-flying mammals for nectar-feeding (Carthew & Goldingay, 1997). Also, in some proteaceous species, large vertebrates as the marsupials are important pollinators (Goldingay et al., 1991). In the study area, two species of nectar-feeding bats and at least 320 species of birds have been identified (Zunino & Kowalewski, 2008) and some of them may act as effective pollinators of G. robusta. Grevillea robusta is not a threat to native biodiversity because it did not become invasive (Mooney & Cleland, 2001). The role of primates and other vertebrates in the maintenance of this plant species remains unclear. Experimental research is needed to evaluate the real importance of A. caraya in pollination. Also, further research is critical as exotic species invasions and pollinator ecology are high priority issues in conservation biology.
Acknowledgments
We thank Amparo Perez Rueda, Carlos A. González, Dana Banegas, Freddy Ramírez Pinto, Miguel Blanco, Ramón Martinez, Ramón Romero, for helping us with the field studies. This study was funded by the American Society of Mammalogists, the American Society of Primatologists, Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina, Idea Wild, and the Rufford Small Grants Foundation.
