Dispersal of Stemmadenia donnell-smithii (Apocynaceae) by Birds

The dispersal ecology of Stemmadenia donnell-smithii was studied in the tropical dry forest zone of northwestern Costa Rica. Fruit was most abundant late in the dry season and was eaten by 22 species of birds, many of which are primarily insectivorous. Stomach-content analyses substantiated our observations. Total crop size per tree and rate of fruit opening were greatest in pasture-edge trees and smallest in forest trees. Rates and percent of seed germination were highest for seeds from which the surrounding aril was removed, scarified seeds, and seeds which had passed through the digestive tract of a bird. The mean compositions of the fruit tissues were, aril: 7.9% ash, 63.9% lipid, 10.9% protein, 16.8% carbohydrate; seed: 3.4% ash, 31.4% lipid, 10.9% protein, 54.2% carbohydrate; husk: 17.0% ash, 24.0% lipid, 11.2% protein, 47.6% carbohydrate. The foraging behavior of birds taking S. donnell-smithii included hovering, and perching and reaching. Rates of pulp utilization in each habitat were relatively constant; all pulp plus seeds were removed in only a few hours. Calculations of daily energy expenditures suggest that Stemmadenia may provide up to 25 percent of the total energy requirement of individuals of several bird species. Interspecific displacements of birds at fruit were rare. Characteristics of S. donnell-smithii that enhance dispersal include peak fruit availability in dry season, slow rate of opening, seed protection until maturation by husk, bright color of arils, relative accessibility and ease of separation of seed from husk and aril from seed, and high nutritive value of aril. Energetically the plant expends the most calories for protection (husk), followed by expenditures for germination (seed) and dispersal (aril). However, on a calorieper-gram, ash-free, dry-weight basis, the plant puts the greatest amount of energy into aril for dispersal, followed by seed for germination, and then husk for protection. Percent nutrient composition and caloric content of seeds and husk were relatively uniform, whereas lipid, protein, and caloric content of aril tissue varied among samples from different fruits, habitats, and years. This variation may be important in allowing the plant to maintain protection and seed quality while maximizing seed production under varying environmental conditions. THE NATURE OF PLANT-ANIMAL INTERACTIONS has Stemmadenia donnell-smithii (Rose) Woodson and been the focus of extensive work for hundreds of the several species of birds which utilize its fruit. In years. Many studies on the mutualistic aspects of the dry region of northwestern Costa Rica, the large plant-animal interactions (Gilbert and Raven 1975) conspicuous fruits of Stemmadenia are fed upon by emphasize the intricate associations of plants and birds for several months during the dry season and animals in pollination systems (e.g., Faegri and Pijl early wet season. We were able to determine rates 1971). Ecological studies on the interactions beof utilization of fruits by birds and the caloric value tween plants and animals with regard to seed disof fruit produced by the plant. We also discuss the persal are scarce (McKey 1975). Among vertebrates, peculiar structure of the fruit in the context of adapbirds are perhaps most commonly associated with tations for seed dispersal. Finally, we comment on seed dispersal (Pijl 1972). Their fruit-eating habits the relative "quality" of seed dispersal in Stemmaare well known (e.g., Lein 1972, Brown 1974), and denia and speculate on its importance to the commusome tropical species have evolved obligate frugivory nity of dispersal agents. (Morton 1973). Although several studies have described the utilization of fruit by birds at various tropical localities (e.g., Land 1963, Willis 1966, METHODS AND MATERIALS Leek 1969, 1972, Haverschmidt 1971), little is Most observations were made between 18 and 26 known about the energetics of the relationships beApril 1971 during the Organization for Tropical Sturween birds and the plants whose seeds they disperse, dies Course: Habitat Exploitation and Diversity: An or about the mechanisms used by plants to promote Ecological Approach with Vertebrates. Additional seed dispersal. data were collected in 1972 and 1973 as time perThis study considers the interaction between mitted. BIOTROPICA 9(1): 9-25 1977 9 Germination experiments were conducted in May 1971 as follows: scarified seeds were nicked at one end with a scalpel; acid-treated seeds were placed in sulfuric acid (pH 2) for 3 minutes. Seeds were stored in a cool, dark place between layers of moist paper towel in plastic boxes, the sides of which were perforated to allow air circulation. In June 1972 fruits collected at random from many of the trees observed in 1971 were weighed and measured. Five were separated into husk, aril, and seed components in the field and dried. Four others were taped shut, frozen, and returned to Florida where components were separated in the laboratory. The components of four other fruits (two from a pasture tree, 23 May; one each from two forest edge trees, 20 and 21 June) were separated in the field in 1973. All samples were vacuum desiccated over concentrated sulfuric acid in the laboratory. Dried material was ground in a Wiley Mill before analyzing organic components. Ash content was determined by incinerating subsamples in a muffle furnace for four hours at 500°C. The total lipid content of the husk, aril, and seed was determined by chloroform-methanol extraction (Freeman et al. 1957). The percent total protein was determined using Vasu's (1965) modification of Lowry et al.'s (1951) colorimetric method with alanine as the standard. Soluble carbohydrate was determined by using the phenol-sulfuric acid method of Dubois et al. (1956) with glycogen as the standard. Structural carbohydrates were determined by subtraction (Merrill and Watt 1973). The ash-free dry weights of each component were converted into caloric units using: 9.45 kcal/ash-free g lipid, 5.65 kcal/ ash-free g protein, and 4.10 kcal/ash-free g carbohydrate (Paine 1971). Voucher specimens of S. donnell-smithii are deposited in the University of South Florida Herbarium, Tampa. In this report, the term pulp includes both seeds and arils. One pulp unit consists of one seed plus its aril. Fruit refers to the entire reproductive structure, including the husk, seeds, and arils. STUDY AREA.•Field observations were made near the Rio Higueron, 1.6 km SE of Estacion Experimental Enrique Jimenez Nunez (Finca Jimenez) agricultural station located 12 km SW Cafias, Guanacaste Province, Costa Rica. The general area, sometimes referred to as Taboga, was described by Orians and Paulson (1969) and Janzen (1973a). The study site lies in the Tropical Dry Forest (Tosi 1969) and has a seasonal climate. Much of the region surrounding Finca Jimenez is devoted to cattle production, sugar cane, and other agricultural development. Remnants of dry forest are still found on the hills behind the station. Rainfall averages 1725 mm per year (x of four years) and is highly seasonal in distribution (fig. 1). In most years, little or no rain falls during the dry season, which begins in November and continues through April. The wet season (May to October) is interrupted by a short dry period (Veranillo de San Juan) of a few weeks to a month in July or August. In 1971 the rains began early in April and had slowed by late June (fig. 1). Much of the community activity ceased as birds abandoned nests and trees dropped their newly formed leaves. Near-normal rains began again in August and continued through October (fig. 1). This unusual year was followed by a very long dry season beginning in November of 1971 and essentially continuing into 1973. In 1972 there was essentially no wet season. Both the total amount and distribution of rain falling from June through October were reduced greatly (fig. 2).