DOI: 10.7291/d14t2w
title: Toucan dispersal of large-seeded trees

description: Large-seeded, animal-dispersed (LSAD) trees include some of the most
 valuable and threatened species in the tropics, but they are chronically
 underrepresented in regenerating forests. Toucans disperse many LSAD
 species, so attracting toucans to regenerating forests should help
 re-establish more diverse tree communities. We ask: (1) What constitutes
 suitable toucan habitat in premontane southern Costa Rica? (2) How much do
 small-scale restoration strategies influence toucan visitation compared to
 landscape-scale habitat suitability outside of restoration sites? (3) How
 well does toucan visitation predict the richness of LSAD tree species
 recruiting into regenerating forests? We combined habitat suitability
 models with long-term toucan observations and comprehensive tree
 recruitment surveys to assess these questions in a multi-site forest
 restoration experiment. Restoration treatments included tree plantations,
 natural regeneration, and applied nucleation. Habitat suitability obtained
 by modeling for three sympatric toucan species was predicted by elevation
 and the extent and age of landscape forest cover. Within suitable
 landscapes, toucans visited areas restored via tree planting ≥5 years
 sooner and ≥2× more often than plots restored via natural regeneration.
 Tree plantations in suitable toucan habitat at the landscape scale had
 LSAD tree recruitment communities that were 2-3× richer in species than
 plantations in poor toucan habitat, and 71% (15/21) of all recruiting LSAD
 species were found only in plantations where landscape habitat was
 suitable for the largest toucan, Ramphastos ambiguus. Results support a
 multi-spatial-scale model for predicting toucan-mediated dispersal of LSAD
 trees. Tree planting increases toucan visitation and LSAD tree
 recruitment, but only within landscapes that represent suitable toucan
 habitat. More broadly, habitat suitability modeling for key seed
 dispersers can help prioritize restoration actions within heterogenous
 landscapes.
description: 1 - Experimental restoration design: We selected 11 forest
 restoration sites established in 2004-2006 on former agricultural lands
 that had been farmed for ≥18 years. Study sites spanned a deforestation
 gradient ranging from 13-82% tree cover within 1 km and represented a
 randomized block design. Each site contained three 0.25-ha plots, which
 were separated from one another by ≥5 m. Plots were randomly assigned one
 of three experimental treatments: (1) natural regeneration, (2) applied
 nucleation, or (3) plantation. Natural regeneration plots were left to
 recover without tree planting. Applied nucleation plots were planted with
 six patches of tree seedlings (86  seedlings plot-1). Plantations were
 planted with rows of tree seedlings throughout (313 seedlings plot-1). All
 plots were fenced to prevent cattle incursion and were hand-cleared with
 machete for 2.5 years. Study sites were separated from one another by ≥0.7
 km. Tree seedlings planted in applied nucleation and plantation plots
 consisted of two widely-planted native species, Terminalia amazonia
 (Combretaceae) and Vochysia guatemalensis (Vochysiaceae), and two
 naturalized legumes, Inga edulis and Erythrina poeppigiana (both
 Fabaceae). Inga produces an indehiscent fruit with an edible pulp that is
 consumed by primates, Terminalia and Vochysia produce winged seeds adapted
 for wind dispersal, and Erythrina produces brown seeds with no obvious
 dispersal mechanism. None of the planted tree species produce fruits
 regularly eaten by toucans.  2 - Focal avian LSAD
 dispersers: Among several groups of large-bodied (&gt;100 g)
 fruit-eating birds in southern Costa Rica, we investigated the three
 toucan species (Piciformes, Ramphastidae) that occur in the region:
 Aulacorhynchus prasinus, Pteroglossus frantzii, and Ramphastos ambiguus
 ssp. swainsonii. Toucans are consistently important seed dispersers for a
 variety of neotropical trees; collectively, they can remove as much as 65%
 of a tree’s seed crop. Despite being dependent on forest for nesting and
 foraging, they have the potential to fly long distances across open
 country, making them effective long-distance dispersal agents. We excluded
 large-bodied Cracids (curassows, guans, and chachalacas), which are either
 not found (or very rarely found) in regenerating forests in the study
 area, or are not forest-dependent (e.g., the chachalaca Ortalis
 cinereiceps) and may be less likely to disperse forest tree seeds. We also
 excluded Psittacids (parrots and parakeets), which sometimes disperse
 viable propagules over long distances and were often observed flying
 overhead, but were rarely observed in restoration sites. Finally, we
 excluded some large-bodied omnivores (e.g., the crake Aramides cajaneus)
 that occasionally eat fruit as part of a diet consisting primarily of
 invertebrates.  3 - Toucan surveys: In 2011-2012, we
 quantified the occurrence of three toucan species in 55 forest fragments
 in our study region in order to develop habitat suitability models. The
 forest fragments represented two uncorrelated gradients in fragment size
 and forest cover within a 1000-m radius, stratified across elevation. The
 area covered by a 1000-m radius approximates the upper range of home range
 sizes reported in previous studies. The fragments included the 49
 fragments in Kormann et al. (2018), plus six additional fragments which we
 added to make the sample more balanced altitudinally. Fragments were
 selected according to a stratified-random design, based on aerial-based
 forest cover maps (2-m resolution). A priori, we assigned fragments to a
 size class (small: &lt;5 ha, large: &gt;30 ha), and from both
 categories we selected fragments that represented a forest cover gradient
 (5 – 80%), included two elevational bands (880 – 1100 m a.s.l. and
 &gt;1100 – 1500 m a.s.l.), and were spatially spread across the study
 area. Due to this selection procedure, all correlations between altitude,
 forest cover, and fragment size were low (all Pearson’s r &lt;0.5). We
 assessed toucan abundance using 50 m fixed-radius point counts and
 stopping rule-based walkabouts, all performed by the same experienced
 observer (Jeisson Figueroa Sandí, JFS). Forest fragments were visited once
 between May and June (2011, 2012) in the early morning in a randomized
 order. Walkabouts lasted an average of 80 minutes in small fragments, and
 155 minutes in large fragments. We performed 12-minute point counts; three
 in each small fragment and six in each large fragment. We also assessed
 toucan visitation three times per year (Apr-May, Jul-Aug, and Nov-Dec) in
 each of 11 restoration sites from 2010-2018. This monitoring was used to
 test habitat suitability model predictions and in turn predict
 large-seeded tree recruitment. Within each site, we actively searched each
 of three experimental plots for 20 min, walking along pre-established
 trails, and recorded when toucans were seen or heard within the plot. When
 possible, we also recorded the tree or plant species in which the bird was
 observed and its foraging and reproductive behavior. During each sampling
 effort, we visited sites and plots in random order. We made observations
 from 0600 to 0900 hours during mild weather, including light fog or mist
 but excluding hard wind or rain. A single skilled observer (JAR) conducted
 all surveys in restoration sites.  4 - Seedling
 surveys: In February to April 2017, RAZ and JAR comprehensively surveyed
 seven 50 × 50 m tree plantation restoration plots for LSAD tree species
 recruitment. Species were classified as LSAD based on dispersal syndrome
 (zoochorous) and seed width (&gt;10 mm; N = 21 species). We selected a
 10-mm threshold for “large” seeds because this is approximately the
 maximum diameter that smaller birds such as tanagers and thrushes are
 capable of swallowing. We selected all LSAD species rather than filtering
 for those with documented toucan dispersal because toucans
 characteristically have broad diets and the specific diets of toucans in
 our region have not been quantified. All naturally-recruiting individuals
 ≥10 cm in height were recorded in each plantation. We did not survey LSAD
 tree species recruitment in applied nucleation or natural regeneration
 treatment plots, largely due to the challenge of thoroughly detecting all
 recruits within the dense grass cover found in parts of these
 treatments.  5 - GIS variables: We used four local and
 four landscape-level environmental variables to build habitat suitability
 models for the three focal toucan species. At the local scale, we used:
 (1) elevation and (2) forest age (secondary vs. old-growth) at the point
 of occurrence; (3) the fragment area; and (4) the area of the fragment
 covered by old-growth forest. At the landscape scale, we used the area
 covered by forest irrespective of forest age within a buffer of (5) radius
 = 500 m and (6) radius = 1000 m around the point of occurrence. Further,
 we used the area covered by old-growth forest only within a buffer of (7)
 radius = 500 m and (8) radius = 1000 m around the point of occurrence.
 Elevation was derived from a digital elevation model (EROS 2017).
 Orthophoto-based forest cover maps were derived from Hadley et al. (2014)
 (2-m resolution), and forest age was assigned based on regional forest age
 classification maps based on aerial photography (Zahawi et al. 2015). We
 considered forest to be old-growth if it had been forested continuously
 from 1947-2015. We filled in forest age coverage gaps for about 10% of the
 study area using the Costa Rican National Forest Inventory
 (REDD/CCAD-GIZ-SINAC 2015).
description: See Read Me file.