Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant-frugivore networks

Abstract

There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.

Keywords: antagonism; ecological networks; fleshy fruits; frugivorous birds; mutualism; mutualistic networks; pulp pecking; seed predation.

Figure 1

(a) Types of interactions between avian frugivores and fleshy fruits, and sign of the interaction from the plant's perspective. (b) Location and codes (roman numbers and colours) of the bird‐fruit visitation networks included in this study (I: P. Jordano, unpublished; II: García, 2016; III: Sorensen, 1981; IV: Snow & Snow, 1988; V: Plein et al., 2013; VI: Stiebel & Bairlein, 2008; VII: Farwig et al., 2017). (c) Representation of one of the studied networks (III); note that some frugivore species can have different interaction types depending on the plant species they feed on. (d) Frequency (%) of the different interaction types in the studied networks in terms of identity and quantity [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

The composition of species’ links (a, b) and interaction frequency (c, d) for each plant (a, c) and bird (b, d) species across all networks. Each bar shows the proportion of a species’ links or interaction frequency which are seed dispersal (mutualistic), pulp pecking or seed predation (non‐mutualistic). Species are placed in order of decreasing proportion of links or interaction frequency, which are seed dispersal [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Changes (y‐axes) in the studied network‐level metrics after the removal of non‐mutualistic interactions (seed predation and pulp pecking). Colour codes denote network identity (see Figure 1b). The black diamonds are mean values across networks. The dashed line is y = x, indicating the position of points if there was no change in metric values. The significance of Wilcoxon matched pairs tests is shown in the top‐left corner of the panels (ns: non‐significant; *p < .05; **p < .01). Unless specified, all Spearman's ρ are significant (ρ ≥ .75, p < .05); we consider a non‐significant ρ to indicate a change in the ranks across networks [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Changes (y‐axes) in species‐level metrics for plants (a–d) and frugivores (e) after the removal of non‐mutualistic interactions (seed predation and pulp pecking). Colour codes denote network identity (see Figure 1b). The dashed line is y = x, indicating the position of points if there was no change in metric values. Points below the horizontal black lines in panels (a) and (b) highlight those species that lose all their partners (a: degree) and interactions (b: frequency) after pruning. The significance of Wilcoxon matched pairs tests is shown in the top‐left corner of the panels (***p < .001)