Birds, bats and arthropods in tropical agroforestry landscapes: Functional diversity, multitrophic interactions and crop yield

TLDR: The importance of the quantification of final ecosystem services such as fruit productivity and crop yield to improve the valuation of ecosystem services provided by tropical birds and bats is demonstrated.

Abstract: Ecosystem services such as the suppression of pest insects may increase productivity of agroforestry systems and thereby increase well-being of smallholders. Tropical birds and bats are effective predators of arthropods and move within landscapes, representing mobile links that connect habitats in space and time. But information on the effects of birds and bats on multitrophic interactions and agricultural productivity in different types of agroforestry systems is limited. Similarly, the relative importance of local agroforestry management and the tropical landscape matrix for ecosystem services mediated by birds has not been investigated so far. Last but not least, a better understanding of dynamic tropical agroforestry landscapes and the effects of habitat conversion and land use intensification on important functional groups as well as for endangered species is urgently needed. We conducted a predator exclusion experiment in which we manipulated the access of birds and bats on 15 different cacao agroforestry sites to quantify their effects on diurnal and nocturnal insects and spiders, cacao fruit development, leaf herbivory and the final crop yield over a period of 15 months. The selected cacao agroforestry sites were located on the island of Sulawesi (Indonesia) and differed in local management and distance to forest. The absence of birds and bats led to an increased density of insect herbivores and caused a concurrent release of mesopredators such as ants and spiders despite negative effects on the development of cacao fruits and a remarkable decrease of final cacao crop yield of 31 % across local and landscape gradients. In addition to bird and bat field exclusion experiments, we investigated the group of insectivorous birds with two different sampling methods. Using an arthropod predation experiment (standardized exposure of dummy caterpillars), we quantified predation rates in relation to the identity and diversity of insectivorous birds. We discovered that responses of the insectivorous bird community and the predation activity differed with the landscape context and both increased with forest proximity. Our findings show that ecosystem services can be driven by single species rather than by overall communities of certain functional groups. Therefore, the conservation of species diversity and ecosystem services does not necessarily rely on the same management strategies, although nearby forests appeared to be of great importance for both bird diversity and avian ecosystem services. The importance of forest proximity and large trees in agroforestry landscapes was also shown in a species specific study we conducted on a declining local population of the Indonesian endemic Grosbeak Starling in our study area. Although this species is well adapted to anthropogenic landscapes, it is also closely associated with large remnant forest trees that remain along forest margin areas and land use systems as nesting sites. The rapid conversion of the forest margin landscape in Central Sulawesi led to a sharp decline of such nesting sites by 92% within only two years. Hence, the endemic Grosbeak Starling is likely to be currently endangered although it was locally very abundant a few years ago. These results show how fast conversion of natural habitats and resource extraction in increasingly intensified tropical agroforestry landscapes can result in changes of the local species diversity. In conclusion, we demonstrate the importance of the quantification of final ecosystem services such as fruit productivity and crop yield to improve the valuation of ecosystem services provided by tropical birds and bats. Species diversity and species identity are both important measures for functional diversity and ecosystem functioning, although with different importance for conservation and the smallholders’ economics. A single common species (Zosterops chloris) was more important for the service of arthropod suppression than overall bird species diversity. Nevertheless, nearby forest habitats and extensively used agroforests (shaded and without use of pesticides or other chemical compounds) turned out to be important for both biodiversity and ecosystem services. Multitrophic interactions between birds, bats and other natural enemies (ants and spiders) of phytophagous insects are likely to jointly impact the productivity of agroforestry systems in complex ways and therefore need to be considered simultaneously at different temporal and spatial scales.