Observing frugivores or collecting scats: a method comparison to construct quantitative seed dispersal networks

Abstract

Mutualistic interactions form the basis for many ecological processes and are often analyzed within the framework of ecological networks. These interactions can be sampled with a range of methods and first analyses of pollination networks sampled with different methods showed differences in common network metrics. However, it is yet unknown if metrics of seed dispersal networks are similarly affected by the sampling method and if different methods detect a complementary set of frugivores. This is necessary to better understand the (dis‐)advantages of each method and to identify the role of each frugivore for the seed dispersal process. Here, we compare seed removal networks based on the observation of 2189 frugivore visits on ten focal plant species with seed deposition networks constructed by DNA barcoding of plant seeds in 3094 frugivore scats. We were interested in whether both methods identify the same disperser species and if species‐level network metrics of plant species were correlated between network types. Both methods identified the same avian super‐generalist frugivores, which accounted for the highest number of dispersed seeds. However, only with DNA barcoding, we detected elusive but frequent mammalian seed dispersers. The overall networks created by both methods were congruent but the plant species' degree, their interaction frequency and their specialization index (d′) differed. Our study suggests that DNA barcoding of defecated and regurgitated seeds can be used to construct quantitative seed deposition networks similar to those constructed by focal observations. To improve the overall completeness of seed dispersal networks it might be useful to combine both methods to detect interactions by both birds and mammals. Most importantly, the DNA barcoding method provides information on the post‐dispersal stage and thus on the qualitative contribution of each frugivore for the plant community thereby linking species interactions to regeneration dynamics of fleshy‐fruited plant species.

Within-Species Trait Variation Can Lead to Size Limitations in Seed Dispersal of Small-Fruited Plants

“…They produce red (n = 4) or black (n = 5) fruits and their fruiting season starts in June (P. padus and R. spicatum) and ends in October (E. europaeus). The seeds of these plants are dispersed by many different animal species (Supplementary Table 2), including at least 10 mammalian and 31 avian frugivores (Albrecht et al, 2013;Jaroszewicz et al, 2013;Schlautmann et al, 2021). However, the contribution of these species to the total seed dispersal of the plant community in the Białowieża Forest is highly heterogeneous, as only five bird species, i.e., Erithacus rubecula (European robin), Sylvia atricapilla (Eurasian blackcap), S. borin (garden warbler), Turdus merula (common blackbird), T. philomelos (song thrush) and one mammal, the European pine marten Martes martes, account for 97.0% of the fruit removal interactions and 98.6% of the seed rain (Schlautmann et al, 2021).…”

“…We summarized the community-wide trait variation in the fruit diameter of plants and the gape width of frugivores at the species level (Figure 1). Frugivores were defined as all animal species recorded eating fruits of any of the studied plant species at least once, either during fruit removal observations in 2011/2012 (Albrecht et al, 2013) or based on the seeds found in the scat of animals collected in 2016-2018 (Schlautmann et al, 2021). Because we did not have direct measures of the gape widths of mammals, a cut-off was set at 2 cm.…”

“…We tested if the gape width of seed disperser species was related to the maximum and mean diameters of the consumed fruits at the species level. The maximum diameter of the consumed fruits was defined as the mean fruit diameter of the largest-fruited plant species fed upon by a given seed disperser species, based either on observations of fruit removal (Albrecht et al, 2013) or on seed deposition (Schlautmann et al, 2021). The mean diameter of fruits removed by a given seed disperser species was calculated by weighting the fruit diameter of each plant species by the disperser-specific fruit consumption rate.…”

“…FIGURE 1 | Distribution of (A) the gape widths of animal dispersers and (B) the fruit diameter of associated plants at species level in temperate forests in Białowieża Forest, Poland. This is a summary of the local plant-frugivore community, whose contributing species were identified either based on fruit removal observations (Albrecht et al, 2013) or based on seeds in scats of animals (Schlautmann et al, 2021). Vertical lines illustrate the median value of a distribution.…”

“…In this study, we describe the extent to which gape-size limitations structure species interactions between small-fruited plants and their associated frugivores, and how gape-size limitations influence the mass or number of dispersed seeds by small-gaped frugivores. We combined data on fruit removal (Albrecht et al, 2013), seed deposition (Schlautmann et al, 2021), fruit and seed traits, and gape widths (Herrera, 1984;Jordano, 1984a) of a diverse plant-frugivore community of the lowland temperate forests in Białowieża Forest (Eastern Poland). First, we characterized the community-wide trait variation in both the fruit diameter of plants and the gape widths of seed dispersers at the species level.…”