Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages

Abstract

Overhunting in tropical forests reduces populations of vertebrate seed dispersers. If reduced seed dispersal has a negative impact on tree population viability, overhunting could lead to altered forest structure and dynamics, including decreased biodiversity. However, empirical data showing decreased animal-dispersed tree abundance in overhunted forests contradict demographic models which predict minimal sensitivity of tree population growth rate to early life stages. One resolution to this discrepancy is that seed dispersal determines spatial aggregation, which could have demographic consequences for all life stages. We tested the impact of dispersal loss on population viability of a tropical tree species, Miliusa horsfieldii, currently dispersed by an intact community of large mammals in a Thai forest. We evaluated the effect of spatial aggregation for all tree life stages, from seeds to adult trees, and constructed simulation models to compare population viability with and without animal-mediated seed dispersal. In simulated populations, disperser loss increased spatial aggregation by fourfold, leading to increased negative density dependence across the life cycle and a 10-fold increase in the probability of extinction. Given that the majority of tree species in tropical forests are animal-dispersed, overhunting will potentially result in forests that are fundamentally different from those existing now.

Keywords: extinction; overhunting; seed dispersal; spatial model; tree population; tropical forest dynamics.

Figure 1.

(a–d) Consistent negative effects of neighbourhood conspecific tree density on vital rates of Miliusa seeds, seedlings and trees greater than 1 cm DBH. Each panel shows effect of distance from a 90 cm DBH conspecific adult tree on individual growth and survival. For seedlings, we estimated effects for a 5 cm high seedling, the minimum size observed in the data, and for trees we estimated effects for a 1 cm DBH individual. Black lines represent median values for spatial functions. Each grey line is one of 1000 draws from the posterior distribution of parameters, collectively representing uncertainty.

Figure 2.

(a–c) Consistent negative effects of Miliusa conspecific seedling density on seed germination, seedling survival and growth. For seedlings, we estimated effects for a 5 cm high seedling, the minimum size observed in the data. Black and grey lines as in figure 1.

Figure 3.

High probability of seed dispersal distances far beyond parent tree for Miliusa in a faunally-intact forest. Black and grey lines as in figure 1.

Figure 4.

Loss of animal-mediated seed dispersal changes spatial distributions of Miliusa populations. This figure shows the location and size of seedlings and reproductive individuals (DBH > 20 cm) for representative runs of an IBM with current seed dispersal by animals (a) and without animal-mediated seed dispersal (b). Red circles represent reproductive trees, with circle size proportional to tree size. Green dots represent seedlings. The model begins with initial conditions determined by data from a 50 ha plot (initial conditions panel), then shows the pattern of seed arrival during the first year of the simulation (seed arrival panel), followed by the location of first-year seedlings immediately after germination (germination), and finally, adult trees and seedlings 17 and 97 years into the model runs.

Figure 5.

Loss of animal-mediated seed dispersal decreases population viability of Miliusa by an order of magnitude. Results for each scenario are based on 1000 runs of an IBM, each simulated for 100 years. (a) Displays population trajectories from IBM runs with natural seed dispersal, while the (b) IBM runs with no animal-mediated seed dispersal. Red lines show populations that have gone extinct.

Figure 6.

(a–c) Loss of animal-mediated seed dispersal decreases total population size, basal area and spatial aggregation of simulated Miliusa populations. Results are based on 1000 runs of an IBM, each simulated for 100 years. Boxes delineate first to third quartiles, the thick black line with boxes shows the median, and ‘whiskers' represent minimum and maximum observations within 1.5 times of the upper and lower quartiles.