Through frugivory and seed dispersal, vertebrates influence plant demography and forest regeneration. Variation in local habitat surrounding fruiting plants can influence frugivore foraging decisions, thereby creating intraspecific variation in seed dispersal services. However, we have little knowledge of drivers of local variation in frugivory. Here, we investigate factors that may influence frugivore diversity and fruit removal at the level of individual plants. We focus on a common understory palm within a continuous Chocó forest with mixed land-use histories in Ecuador. The density of pioneer tree species in the genus Cecropia around focal palms was negatively related to fruit removal and the diversity of frugivores visiting palms. This may relate to the fact that the presence and abundance of Cecropia species often indicate the existence and severity of past disturbances. Local Cecropia density was also related to an overall shift in the frugivore community that corresponded with an increase in fruit removal by lower-quality seed dispersers (rodents). We also found that the local density of fruiting conspecifics was positively related to frugivore diversity, but not fruit removal. Our results provide information on drivers of intraspecific inequalities in plant populations across tropical forest landscapes. The reduction in fruit removal and frugivore diversity associated with local Cecropia abundance suggests that seed dispersal services can be sensitive to fine-scale variation in habitat structure. Furthermore, because Cecropia are often indicative of past disturbances, this indicates that even small-scale habitat degradation by humans can have lasting effects by creating localized pockets of forest unfavored by frugivores.

Study system

Our study was conducted at Bilsa Biological Station in northwest Ecuador (79”45’W, 0”22’N; 350-750 m elevation; 2-3 m precipitation annually), a 3500-ha private reserve of humid evergreen rainforest located within the Chocó biogeographic region (Durães et al. 2013). The Chocó forest has exceptionally high levels of endemism in both plant and animal species and is recognized as one of the most biologically diverse regions on the planet (Myers et al. 2000). The study area consists of continuous forest that is composed of a complex matrix of undisturbed forest with patches of varying size that have been regenerating naturally for the past 24-34 years after selective logging and small-scale farming (Durães et al. 2013).

Our focal plant species, Prestoea decurrens (Arecaceae) is a monoecious, insect-pollinated understory palm that is common in our study area (Browne & Karubian 2016) and throughout lowland tropical forests ranging from Bolivia to Nicaragua (Ervick & Bernal 1996, Steege et al. 2013). The palm is clonal, and individuals form distinct clusters of stems with a mean height of approximately 4 m (± 1.4 standard deviation (SD), N = 252).  Prestoea decurrens produces fleshy animal-dispersed fruit 2-3 cm in diameter, with a purple epicarp, that contain a single seed measuring 6-7 mm in diameter. Fruits are arrayed on infructescences, each holding approximately 100-600 fruits, and individual trees may hold up to six separate infructescences concurrently (unpublished data). We selected this focal palm species because it is a widespread and abundant fruiting resource in the understory environment and important for many frugivores across a large proportion of neotropical forests. The size and characteristics of P. decurrens fruits are common among many tropical plants, which makes it possible to extrapolate relevant information from our results into a broader context across tropical forests.

Frugivore observations

We deployed camera traps on 31 fruiting P. decurrens palms located across approximately 40 ha of continuous, but heterogeneous, forest in Bilsa from August-November 2018, a period that coincided with high fruit production in this species (J. Karubian, unpublished data). We selected focal palms with mature fruits in locations that represented the spectrum of past-habitat use found in the 130-ha study area. Focal palms were geolocated by GPS (Garmin model 64s, Atchison, KS, USA) with 3-7 meters accuracy. We deployed Browning Strike Force® HD motion-sensor trail cameras (2014 and 2018 models) with nighttime capability in front of the mature infructescences of each palm. In most cases (all but 2), all mature infructescences on an individual palm were included in the camera frame, generally 1-3 infructescences. Palms were located in most cases before fruits were ripe, and cameras were installed once fruits ripened. A small proportion of focal palms were already ripe when found, and camera traps were immediately set in front of them. Palm crop size was estimated for each infructescence by counting the number of fruits on 3 rachilla, averaging them, and multiplying the average by the number of rachilla on an infructescence, then summing the estimate for all infructescences on a given palm.

Cameras were deployed for approximately 25 days or until all fruits were removed. Cameras were programed to capture 30-second videos with a 5-second delay between videos and as such recorded most or all visitation events during the sampling period. Because the maximum continuous recording time allowed by our cameras was only a few minutes, we did not have the ability to record and compare the full length of foraging events by frugivores. However, we can draw conclusions about relative rates and visitation frequencies through our 30-second capture method.

Visitors were identified to the species level, using Ridgely and Greenfield (2001) The Birds of Ecuador and Tirira, (2017) A field guide to the mammals of Ecuador. The majority of the toucans we recorded were Chocó toucans (Ramphastos brevis); however, Chestnut-mandibled toucans (R. swainsonii) are also common in the area and due to the similarity in appearance we categorize these birds broadly as ‘toucans’ here. We recorded the number of fruits handled, removed, or dropped by each visitor in each video. We summed the total fruit removed from each focal palm and calculated the mean percentage of overall fruit removal that each frugivore species contributed. We also calculated for each frugivore species the mean percentage of fruit it swallowed/carried away versus dropped (which can provide information on disperser quality).

Local habitat characterization

To understand how local habitat might influence visitation and fruit removal, we selected habitat metrics known to influence frugivore habitat use at this site: (Durães et al. 2013, Mahoney et al. 2018): canopy density, canopy height, the number of large trees ( > 50 cm diameter at breast height (DBH)) within 20 m of each focal palm, the number of trees belonging to the genus Cecropia within 10 m of each focal palm, and the presence of conspecifics fruiting in the understory within 20 m of focal palms. Variation in neighborhood fruit availability was estimated by counting conspecifics because P. decurrens was the only observed fruiting plant in the understory near focal plants during the study period. We recorded Cecropia species abundance because these prevalent neotropical pioneer trees indicate past disturbance (Mesquita et al. 2001, Zalamea et al. 2008, 2012). We estimated canopy density as percentage canopy cover using a spherical densiometer (Forestry Supplies no. 43888), and canopy cover measurements were taken 0.5 m from the base of the focal palm in each cardinal direction and averaged. Canopy density, as well as canopy height and the presence of large trees, are typically attributed to lower disturbance levels. We quantified canopy height as the tallest tree within 10 m around the focal palm; this height was estimated individually by the same two observers for each palm and averaged.