1. Despite recent interest in linkages between above- and below-ground communities and their consequences for ecosystem processes, much remains unknown about their responses to long-term ecosystem change. We synthesize multiple lines of evidence from a long-term ‘natural experiment’ to illustrate how ecosystem retrogression (the decline in ecosystem process rates due to long-term absence of major disturbance) drives vegetation change, and thus above-ground and below-ground carbon (C) sequestration, and communities of consumer biota.
2. Our study system involves 30 islands in Swedish boreal forest that form a 5000-year, fire-driven retrogressive chronosequence. Here, retrogression leads to lower plant productivity and slower decomposition and a community shift from plants with traits associated with resource acquisition to those linked with resource conservation.
3. We present consistent evidence that above-ground ecosystem C sequestration declines, while below-ground and total C storage increases linearly for at least 5000 years following fire absence. This increase is driven primarily by changes in vegetation characteristics, impairment of decomposer organisms and absence of humus combustion.
4. Data from contrasting trophic groups show that during retrogression, biomass or abundance of plants and decomposer biota decreases, while that of above-ground invertebrates and birds increases, due to different organisms accessing resources via distinct energy channels. Meanwhile, diversity measures of vascular plants and above-ground (but not below-ground) consumers respond positively to retrogression.
5. We show that taxonomic richness of plants and above-ground consumers are positively correlated with total ecosystem C storage, suggesting that conserving old-growth forests simultaneously maximizes biodiversity and C sequestration. However, we find little observational or experimental evidence that plant diversity is a major driver of ecosystem C storage on the islands relative to other biotic and abiotic factors.
6. Synthesis.Our study reveals that across contrasting islands differing in exposure to a key extrinsic driver (historical disturbance regime and resulting retrogression), there are coordinated responses of soil fertility, vegetation, consumer communities and ecosystem C sequestration, which all feed back to one another. It also highlights the value of well-replicated natural experiments for tackling questions about above-ground–below-ground linkages over temporal and spatial scales that are otherwise unachievable.