Impacts of protected colonial birds on soil microbial communities: When protection leads to degradation

Colonial nesting and roosting birds can degrade their habitat by soil salinization, eutrophication, and acidification associated with excessive deposition of avian excreta. We studied the impact of a protected wading bird colony on soil microbial communities from cork oak woodlands in Doñana National Park (SW Spain). Over one year we analyzed soil properties (pH, salinity, soluble N and P forms, extractable organic carbon - EOC -), microbial activity (basal respiration, community-level physiological profile, extracellular enzyme activities) and community structure (fungal, bacterial and archaeal terminal restriction fragments -TRFs-) along a gradient of bird nesting intensity. Bird nesting largely impacted soil chemical environment, with increases from 25 to 500 μS cm−1 in soil salinity, from 6 to 725 mg kg−1 in soil P, from 5 to 22 mg kg−1 in N-NH4, and from 5.4 to 245 mg kg−1 in N-NO3 between the extremes of the nesting intensity gradient in the wet season. Most of these chemical changes were enhanced in the dry season. We observed positive linear or log-linear relationships between the bird nesting footprint on soils (indicated by an integrated soil chemistry index) and microbial biomass, basal respiration and most of the studied enzyme activities. This was likely due to the concurrent increases in EOC along the avian intensity gradient, which counteracted the negative impacts of salinity. Soil P and EOC were the main drivers for fungal, bacterial and archaeal TRFs diversity. Bacterial TRFs richness and diversity index decreased along the avian intensity gradient in the dry season, while archaeal TRFs diversity increased in those soils highly salinized by excess of avian excreta deposition. Our study clearly shows that this oversized bird colony has profound effects on soil chemistry and biological activity, and highlights the need for a re-evaluation of management strategies in this protected area, towards a greater consideration of soil processes in conservation priorities.We are grateful to the Consejería de Medio Ambiente (Andalusian Government) and to the Organismo Autónomo Parques Nacionales for financial support, through the DECALDO (091/2009) and the BIOGEOBIRD (P09-RMN-4987) projects, and to the Doñana National Park and Doñana Biological Reserve managers for the use of their facilities and the support to carry out the field work. Rubén Rodríguez and Héctor Garrido from the Doñana Monitoring Team provide us with data of cork oak occupation by the colony. We also thank Adela Moreno fir her work with T-RFLP analysis. MTD was supported by a Juan de la Cierva Postdoctoral fellowship and JMA by a FPU-MEC grant from the Spanish Ministry of Economy and Competitiveness.Peer reviewe