Forest degradation limits the complementarity and quality of animal seed dispersal

Abstract

Forest degradation changes the structural heterogeneity of forests and species communities, with potential consequences for ecosystem functions including seed dispersal by frugivorous animals. While the quantity of seed dispersal may be robust towards forest degradation, changes in the effectiveness of seed dispersal through qualitative changes are poorly understood. Here, we carried out extensive field sampling on the structure of forest microhabitats, seed deposition sites and plant recruitment along three characteristics of forest microhabitats (canopy cover, ground vegetation and deadwood) in Europe's last lowland primeval forest (Białowieża, Poland). We then applied niche modelling to study forest degradation effects on multi-dimensional seed deposition by frugivores and recruitment of fleshy-fruited plants. Forest degradation was shown to (i) reduce the niche volume of forest microhabitat characteristics by half, (ii) homogenize the spatial seed deposition within and among frugivore species, and (iii) limit the regeneration of plants via changes in seed deposition and recruitment. Our study shows that the loss of frugivores in degraded forests is accompanied by a reduction in the complementarity and quality of seed dispersal by remaining frugivores. By contrast, structure-rich habitats, such as old-growth forests, safeguard the diversity of species interactions, forming the basis for high-quality ecosystem functions.

Keywords: environmental niche modelling; forest degradation; functional redundancy; old-growth forest; plant–frugivore interactions; seed dispersal effectiveness.

Figure 1.

The three-dimensional forest microhabitat space of old-growth and degraded forest in Białowieża Forest (a–c), and the deposition microhabitat space of frugivores (mixed dispersers, S. atricapilla, T. merula and T. philomelos) in old-growth (d–f) and degraded (g–i) forest, illustrated by two-dimensional representations of (a,d,g) canopy cover and ground vegetation, (b,e,h) canopy cover and the volume of deadwood and (c,f,i) ground vegetation and the volume of deadwood. Circles represent the transect segments of the forest (a–c) or the deposited seeds of the frugivores therein (d–i). The centroids (squares) indicate the centre of the forest (a–c) and the deposition microhabitat spaces (d–i) along each of the three microhabitat characteristics (canopy cover, ground vegetation and volume of deadwood). (Online version in colour.)

Figure 2.

(a) Volume of the deposition microhabitat space of frugivore species (S. atricapilla, T. merula and T. philomelos, mixed dispersers) in Białowieża Forest, Poland. (b–d) Centroids of the forest microhabitat spaces ('habitat') and the deposition microhabitat spaces of the combined frugivore community ('community') and of frugivore species (S. atricapilla, T. merula and T. philomelos, mixed dispersers) along the three environmental dimensions of forest microhabitats in old-growth and degraded forest: (b) canopy cover, (c), ground vegetation and (d) volume of deadwood. (Online version in colour.)

Figure 3.

(a) Volume of the deposition microhabitat space in old-growth (solid lines) and degraded (dotted lines) forest as a function of different combinations of frugivore species (S. atricapilla, T. merula and T. philomelos, mixed dispersers) in Białowieża Forest, Poland. The lines indicate the mean volume of the bootstrapped deposition microhabitat spaces for each combination of frugivore species, and the shaded areas the best and worst combinations of the different frugivore species. (b,c) The volume and uniqueness of the deposition microhabitat space of the different frugivores, and the uniqueness of the community in the (b) old-growth and (c) degraded forest. The upper part of the chord-diagram shows the niche space of seed deposition (i.e. the volume of the microhabitat space) of the different frugivores; the lower chord-diagram shows the proportion of each frugivore's deposition to community uniqueness (i.e. part of the microhabitat space only filled by one frugivore) and the summed proportions of the uniqueness of depositions of frugivore species (‘community uniqueness', light green).

Figure 4.

Seedling recruitment in the peak year and early survival of the fleshy-fruited plant community in Białowieża Forest, Poland. (a) The effect of forest type (old-growth versus degraded) on seedling recruitment. Mean ± 95%CI. (b) The relationship between ground vegetation and seedling recruitment. (c) The relationship between canopy cover and early survival of the seedlings. In (b,c), the black line represents the predicted mean of the plant species, and the coloured lines represent the mean of the plant species. (Online version in colour.)