Responses of Dispersal Agents to Tree and Fruit Traits in Virola Calophylla (Myristicaceae): Implications for Selection

Oecologia (2003) 136:80–87 DOI 10.1007/s00442-003-1239-y PLANT ANIMAL INTERACTIONS Sabrina E. Russo Responses of dispersal agents to tree and fruit traits in Virola calophylla (Myristicaceae): implications for selection Received: 1 July 2002 / Accepted: 19 February 2003 / Published online: 9 April 2003 Springer-Verlag 2003 Abstract Variation in traits affecting seed dispersal in disperser assemblages at regional scales can be another plants has been attributed to selection exerted by dispersal factor contributing to inconsistency in disperser-mediated agents. The potential for such selection was investigated selection on plant traits. in Virola calophylla (Myristicaceae) in Manffl National Park, Peru, through identification of seed dispersal agents Keywords Ateles paniscus · Coevolution · Peru · Seed and of tree and fruit traits significantly affecting the dispersal · Tropical forest quantity of seeds dispersed. Seventeen bird and one primate species (the spider monkey, Ateles paniscus) dispersed its seeds. Spider monkeys dispersed the major- Introduction ity of seeds (a minimum of 83% of all dispersed seeds). Visitation by dispersal agents depended only on the Early investigations of the relationships between plants quantity of ripe fruit available during a tree observation. and the animals that disperse their seeds were guided by In contrast, seed removal increased with both greater the hypothesis that plant reproductive traits affecting seed quantity of ripe fruit and aril: seed ratio. When analyzed dispersal and the ecology and behavior of dispersal agents separately, seed removal by birds increased only with have been shaped through coevolution (Snow 1971; greater aril: seed ratio, whereas seed removal by spider McKey 1975). With the accumulation of observations monkeys was affected by the quantity of ripe fruit and indicating that specialized, coevolved relationships be- phenological stage. The finding that dispersal agents tween plants and dispersal agents were rare came the responded differently to some tree and fruit traits realization that many ecological and evolutionary factors indicates not only that dispersal agents can exert selection intervene to make fine-tuned, reciprocal evolutionary on traits affecting seed dispersal, but also that the change unlikely (Wheelwright and Orians 1982; Howe resulting selection pressures are likely to be inconsistent. 1984; Herrera 1985). However, because seed dispersal is This conclusion is supported by the result that the selected even if it is costly in terms of resource proportion of the seed crop that was dispersed from investment (Hamilton and May 1977; Comins et al. individual trees, which accounted for cumulative disper- 1980), plants are expected to evolve mechanisms pro- sal by all agents, was not influenced by any tree or fruit moting dispersal. In doing so, plant traits affecting trait evaluated. Comparing these results with those from dispersal may change in response to selection by dispersal studies of V. sebifera and V. nobilis in Panama revealed agents (e.g., Lord et al. 2002), provided that individual that the disperser assemblages of these three Virola plants experience fitness consequences resulting from species were congruent in their similar taxonomic repre- such selection. These fitness consequences are mediated sentation. In Panama the proportion of V. nobilis seed by effects on the quantity and quality of seed dispersal, crop dispersed was related positively to aril: seed ratio where seed dispersal quantity refers to the number of and negatively to seed mass, a result not found for V. seeds dispersed and quality refers to the probability that a calophylla in Peru. The greater importance of dispersal by dispersed seed will produce a reproductive adult (sensu primates versus birds in V. calophylla, relative to V. Schupp 1993). This study investigated the potential for nobilis, may explain this difference. Thus, variation in disperser-mediated selection on plant traits affecting the quantity of seeds dispersed. S. E. Russo ()) Visitation and seed removal can be influenced by University of Illinois, 515 Morrill Hall, many traits of fruiting plants, including local abundance 505 South Goodwin Avenue, Urbana, IL 61801, USA of fruit resources or neighborhood effects (Manasse and e-mail: [email protected] Howe 1983; Sargent 1990), phenology (Thompson and Fax: +1-217-265-0056 81 Willson 1979; Stiles 1980; Eriksson and Ehrlen 1998), the relationships between tree and fruit traits and the crop size (Howe and Vande Kerckhove 1979; Howe and quantity of seeds dispersed. Vande Kerckhove 1980; Howe and Vande Kerckhove 1981; Davidar and Morton 1986; Murray 1987; Foster 1990a; Gryj and Dominguez 1996; Korine et al. 2000), Materials and methods energetic and nutrient contents of fruits and their corre- lates (Howe and Vande Kerckhove 1980; Foster 1990a; Study site Sallabanks 1993), and seed size (Howe and Vande This study was conducted from August 1999 through December Kerckhove 1980). Considerable variation, however, exists 2000 at Cocha Cashu Biological Station (CCBS) in Manffl National among dispersal agents in their responses to these factors, Park, Peru (11540S, 71180W, elevation ca. 400 m). The average which can result in inconsistency in selection on repro- annual rainfall is 2,000 mm, with most precipitation falling ductive traits influencing the quantity of seeds dispersed between October and April (Terborgh 1983). CCBS is situated in the floodplain of the Manffl River and consists of a mosaic of mature (Herrera 1985), thereby increasing the relative influence and successional floodplain forest stands. Community-wide, fruit of non-adaptive processes, such as genetic drift, affecting production has two phenological peaks annually, one near the trait variation. Inconsistent selection can also result if beginning (November-December) and one near the middle (Febru- variation in these traits is constrained by processes ary) of the rainy season (Terborgh 1983). Manffl National Park has unrelated to seed dispersal, such as germination (Howe experienced little impact from human development and exploita- tion, so that population densities of dispersal agents and plants are and Richter 1982; Parciak 2002) and seed predation minimally influenced by human activities. This site has been (Benkman 1995). described in detail in previous publications (Terborgh 1983; Foster The hypothesis that dispersal agents exert selective 1990b; Gentry 1990; Terborgh et al. 1990). pressure on reproductive traits affecting seed dispersal leads to two predictions. First, patterns of visitation and Study species seed removal by dispersers should vary significantly with differences in reproductive traits among individual plants. Virola calophylla (Myristicaceae) is a common canopy tree in This can be considered a behavioral response by dispersal lowland moist forests of South America (Rodrigues 1980). At CCBS, V.calophylla begins to ripen fruit during the transition from agents. Second, a strong relationship should exist between the dry to wet seasons (mid-September) and continues through mid- reproductive traits and the proportion of all seeds December. Fruit of V. calophylla is similar to other Virola species, dispersed from individual tree crowns during an entire which are characterized by a bivalved, dark green capsule which fruiting season. This can be considered a measure of the opens upon ripening to expose a single arillate seed, the dispersible cumulative behavioral responses of dispersal agents. unit (diaspore; Rodrigues 1980; van Roosmalen 1985a; Ribeiro et al. 1999). The aril is bright red, lanceolate, and oily. Other species These predictions represent only the prerequisites for of Virola have been found to have high concentrations of lipids and selection, because a response to disperser-mediated secondary compounds (Howe and Vande Kerckhove 1981; Lemus selection on reproductive traits depends on both the and Castro 1989; Harrowven et al. 1998; Galetti et al. 2000). The fitness consequences of dispersal by particular agents and seed comprises most of the volume of the diaspore. the heritability and genetic architecture of traits. I evaluated whether these predictions held in the dispersal Focal trees and frugivore observations system of Virola calophylla (Myristicaeae), a subcanopy nutmeg tree species of lowland forests in South America Fruiting V. calophylla individuals were located within the study area in mature floodplain and late successional forest habitats. that produces vertebrate-dispersed, fleshy fruits. Focal trees were selected to represent the range of crop sizes Understanding the origins of plant-disperser interac- observed at the study site. Following the methodology of Howe tions requires using a comparative approach that accounts (1981) and Howe and Vande Kerckhove (1981), observations of for not only the ecological patterns across multiple frugivores were conducted at focal trees during the hours from closely related species, but, ideally, the evolutionary dawn to 11:00 a.m. and from 2:00 p.m. to dusk, and individual observation periods lasted 2–4 h. Observations sessions at each tree trends in those patterns, as well (Thompson 1999). were distributed in a stratified random fashion to ensure that Through such comparisons, the lability of plant-disperser observations sampled the entire fruiting period of each individual relationships and the consistency of trends in these tree. On some occasions, in order to follow spider monkeys (Ateles relationships replicated in different

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