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Ficus Spp.) in a Tropical Cloud Forest: Evaluation of a Potential Keystone Resource

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Ficus Spp.) in a Tropical Cloud Forest: Evaluation of a Potential Keystone Resource Journal of Tropical Ecology (2013) 29:401–407. © Cambridge University Press 2013 doi:10.1017/S0266467413000461 Phenology, abundance and consumers of figs (Ficus spp.) in a tropical cloud forest: evaluation of a potential keystone resource Gustavo H. Kattan∗,†,1 and Leonor A. Valenzuela∗,‡ ∗ Fundacion´ EcoAndina, Carrera 2 A Oeste No. 12-111, Cali, Colombia † Departamento de Ciencias Naturales y Matematicas,´ Pontificia Universidad Javeriana Cali, Avenida Canasgordas˜ No. 118-250, Cali, Colombia ‡ Departamento de Ecolog´ıa, Pontificia Universidad Catolica´ de Chile and Instituto de Ecolog´ıa y Biodiversidad (IEB), Santiago, Chile (Received 21 January 2013; revised 21 June 2013; accepted 22 June 2013; first published online 26 July 2013) Abstract: Fig trees (Ficus spp) produce fruit year-round and figs are consumed by a large proportion of frugivores throughout the tropics. Figs are potential keystone resources that sustain frugivore communities during periods of scarcity, but studies have produced contradictory results. Over 1 y we monitored the phenology of 206 trees of five Ficus species in a Colombian cloud forest, to test whether figs produced fruit during periods of low overall fruit availability. We also measured fig tree densities in 18 0.5-ha plots and made 190 h of observations at 24 trees of three species to determine whether figs were abundant and consumed by a large proportion of the local frugivores. The five species produced fruit year-round but fig availability varied monthly by orders of magnitude. Fig trees reached comparatively high densities of 1–5 trees ha−1 and were consumed by 36 bird species (60% of the local frugivore assemblage) and three mammal species. However, there was no season of fruit scarcity and figs represented on average 1.5% of the monthly fruit biomass. Figs in this Andean forest are part of a broad array of fruiting species and at least during our study did not seem to constitute a keystone resource. Key Words: cloud forest, Colombia, Ficus, frugivory, keystone resource, phenology, tree density INTRODUCTION which, with few exceptions, is species-specific (Cook & Rasplus 2003). Female wasps emerging from a tree need The fruits of fig trees (Ficus spp., Moraceae) are to find another tree in a short time, with syconia in the an important food source for fruit-eating vertebrates appropriate stage for colonization. Thus, syconium pro- throughout the tropics and subtropics. Globally, over duction within a tree is synchronous but among trees it is 1200 species of bird and mammal (>10% of the world’s asychronous. Fruit production of figs is usually abundant, birds and >6% of mammals) are known to feed on figs and trees of different species at a particular locality initiate and Ficus is considered the most important plant genus syconium production at different times, resulting in fruit for tropical frugivores (Shanahan et al. 2001). Locally, being available every month of the year (Milton 1991, Ficus is usually the most diverse genus and always ranks Ragusa-Netto 2002, Tweheyo & Lye 2003). among the top 10 most diverse genera in lowland tropical The abundance and constancy of fig availability forests (Harrison 2005). Figs are consumed by up to 45% year-round support the proposition that these trees of the local bird and mammal faunas (Shanahan et al. are keystone resources for the frugivore community of 2001). Figs also represent a critical resource for particular tropical forests. The role of figs as a keystone resource groups of species such as Asian hornbills (Bucerotidae), by has been supported by work in Malaysia (Lambert & providing a large proportion of their diet and influencing Marshall 1991), India (Kannan & James 1999), South their grouping and ranging patterns (Kinnaird & O’Brien Africa (Bleher et al. 2003) and Panama (Korine et al. 2005, Kinnaird et al. 1996). 2000). However, for various reasons that include low The importance of fig trees hinges on their capacity fig densities and not providing sufficient resources during to produce fruit throughout the year. Fig pollination periods of scarcity, other studies have not found support depends on a specialized relationship with agaonid wasps for the keystone role of figs in localities in Gabon (Gautier- Hion & Michaloud 1989), Uganda (Chapman et al. 2005), 1 Corresponding author. Email: [email protected] India (Patel 1997) and Colombia (Stevenson 2005). Downloaded from https:/www.cambridge.org/core. Pontificia Universidad Catolica de Chile, on 11 Jan 2017 at 18:36:59, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. http://dx.doi.org/10.1017/S0266467413000461 402 GUSTAVO H. KATTAN AND LEONOR A. VALENZUELA Peres (2000) proposed that a keystone resource should meet the following criteria: (1) exhibit low redundancy, i.e. be available during periods of overall fruit scarcity, (2) be consumed by a large percentage of the frugivore community, (3) exhibit interannual reliability, and (4) be abundant.Inthispaperwedescribethefigtreeassemblage of a cloud forest in the tropical Andes of Colombia to evaluate its potential role as a keystone plant resource. Over 1 y, we followed the phenology of five species of fig tree and quantified fruit production in comparison with overall fruit production in the forest, to test the hypothesis that figs provided abundant food during periods when other fruits were scarce. We also estimated fig tree density and surveyed bird and diurnal mammal consumers to determine whether fig trees at this site met the criteria of being abundant and consumed by a large proportion of local frugivores. Our study lasted only 1 y so we cannot test the criterion of interannual reliability, but we can Figure 1. Precipitation regime at El Cedral meteorological station, 2000 determine whether during our study figs were a keystone masl,6kmeastoftheOtun´ Quimbaya Flora and Fauna Sanctuary, central range of the Colombian Andes. The graph shows mean and SD resource. for 30 y. the herbarium of Universidad del Valle (CUVC) in Cali, STUDY AREA Colombia. The study was conducted at Otun´ Quimbaya Flora and To test for temporal differences in number of individuals Fauna Sanctuary, a 411-ha protected area on the western in fruit, number of fruits and dry biomass, we used a χ 2 slope of the central range of the Andes of Colombia, near test, with the mean value for the 12 mo as the the city of Pereira. Otun´ Quimbaya spans altitudes of expected value. We tested for asynchrony in the inter- 1800–2000 m asl and is adjacent to Ucumar´ıRegional tree phenological patterns with the evenness index H (Bronstein & Patel 1992), Park, another protected area of 4000 ha encompassing altitudes between 1700 and 2600 m asl. The area is 5 = − − 0.2 covered with humid, montane cloud forest in a mosaic H 1 Pi 1.6 of mature forest and secondary regeneration of different i=1 ages between 10 and 60 y old. Annual precipitation is where Pi is the proportion of trees with syconia in the 2650 mm, with two peaks of rainfall in April and October five phases of development. The index varies between 0 and relatively drier seasons in December–January and and 1 and a value of 1 indicates an even distribution, i.e. July–August (Aguilar & Rangel 1994; Figure 1). asynchrony. To estimate fig tree density we marked and counted fig trees in 0.5-ha plots (N = 18). Between December 2003 METHODS and September 2004 we conducted 190 h of observation of bird and mammal consumers in 24 focal trees of three We collected data along 14 trails of variable length. species of Ficus (F. andicola, F. killipii and F. mutisii; Each fig tree within 8 to 22 m of either side of the Table 1). The number of trees monitored varied between trails (depending on visibility) was marked and located one and six per month. For each tree, we made between on a map of the study area. Phenology was monitored three and eight observation sessions between 06h00 and monthly between November 2003 and November 2004. 10h00. For each bird and mammal visitor, we noted the We recognized five phases of syconium development: pre- species and counted the number of consumption events. A female, female, interfloral, male and postfloral (mature consumption event was defined as an individual arriving syconia). We estimated crop size by counting the number at the tree and feeding on fruits, independently of the of fruits on a visible branch and extrapolating to the number of figs eaten. entire tree. We collected 50 fruits from different trees To determine whether Ficus spp. were fruiting during (dependingonhowmanytreesfruited)foreachfigspecies, periods of fruit scarcity, we used community-wide and obtained dry mass by drying fruits in an oven until phenological data obtained in a parallel study over constant mass. We also measured their height and width. the same time period (M. Kessler-Rios & G. Kattan, Voucher specimens of the five species were deposited at unpubl. data). Monthly estimates of fruit production were Downloaded from https:/www.cambridge.org/core. Pontificia Universidad Catolica de Chile, on 11 Jan 2017 at 18:36:59, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. http://dx.doi.org/10.1017/S0266467413000461 Fig trees of a cloud forest 403 Table 1. Ficus species recorded at the study site, Otun´ Quimbaya Flora and Fauna Sanctuary, Central Andes of Colombia. Taxonomic order according to www.figweb.org/Ficus/Classification_of_figs. For each species, the table shows median crop size (with range and sample size in parentheses), the total number of trees monitored (N), fig dimensions based on 50 syconia of each species, and mean tree density ± SD obtained from 0.5-ha plots (N = 18). Ficus species Crop size N Mean fig dimensions (mm) Mean fig mass (g) Density (trees ha−1) Subgenus Pharmacosycea F.
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