Microbial activity of a secondary forest succession after shifting agriculture in the Afrotropics

Tropical secondary forests, i.e. regrowing forests after clearcutting through human activities, cover a larger area than primary tropical forests. This increasingly dynamic tropical landscape warrants a comprehensive understanding of carbon (C) sequestration and nutrient cycling in secondary tropical forest succession, particularly on the soil microbiome governing these processes. Yet, our current knowledge of soil microbial dynamics in secondary successions of tropical forests and their role in C turnover and sequestration is limited, particularly in deeper soil layers which are seldomly explored.

Here, we investigated microbial activity and growth along a soil depth gradient in an established space-for-time-substitution experiment in the Yoko forest reserve, Democratic Republic of the Congo. We sampled soils from four differently aged secondary forests (3 years, 8 years, 15 years and 63 years), and a primary forest acting as a control at six depths (10 cm, 30 cm, 50 cm, 100 cm, 175 cm, 250 cm). We assessed microbial growth through the incorporation of deuterium-labelled water into phospholipid fatty acids (²H-SIP), allowing us to distinguish growth and biomass of distinct microbial groups.

Microbial growth was highest in early successions, 3 to 15 years after the last biomass removal, whereas microbial respiration steadily increased with succession resulting in a decrease in soil microbial carbon use efficiency with forest successional age. Primary forests showed significantly lower microbial growth rates than early and middle-aged successions. This trend, while also present in shallow soil depths, was most evident at the depth of 100 cm.

Our results suggest an increase of labile C availability for soil microorganisms in early and middle-aged successions, most likely through higher quality and/or quantity of C inputs of regrowing plant biomass compared to the climax plant community. We further show that the response of microbial activity during secondary succession was seen beyond soil depths that are commonly considered, highlighting the importance of sampling deeper soil layers when assessing responses to land use changes. Contrary to our expectations, microbial growth decreased with successional age, and primary forests fostered lower microbial activity compared to secondary forests. Our results therefore demonstrate a complex response of soil microorganisms to secondary succession in Afrotropical forests that is decoupled from aboveground plant biomass.