Review
Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover

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Here, we outline a conceptual framework for biodiversity dynamics following environmental change. The model incorporates lags in extinction and immigration, which lead to extinction debt and immigration credit, respectively. Collectively, these concepts enable a balanced consideration of changes in biodiversity following climate change, habitat fragmentation and other forcing events. They also reveal transient phenomena, such as biodiversity surpluses and deficits, which have important ramifications for biological conservation and the preservation of ecosystem services. Predicting such transient dynamics poses a serious conservation challenge in a time of rapid environmental change.

Section snippets

Missing Concepts in Biodiversity Dynamics

Species immigration and extinction are the dominant forces underlying changes in species diversity on timescales of decades to millennia and spatial scales from local to regional 1, 2. Climate change, habitat fragmentation, resource exploitation and transcontinental species introductions are driving immigrations and extinctions 3, 4, 5, 6, 7, 8, 9. Although most ecologists and biogeographers recognize that both transience and determinism in these processes fundamentally influence changes in

The biodiversity budget and forcing events

The ecological processes of extinction and immigration can be set in motion by a forcing event that drives changes in the quality, size, density and connectivity of suitable habitat patches. Forcing events can be rapid (e.g. industrial deforestation or abrupt climate change) or gradual (e.g. suburban encroachment, sea-level rise or secular temperature change), and singular (e.g. permanent deforestation, creation of islands in a reservoir or transition to a new climate regime) or sequential

Delays in budget balancing

Equilibrium is rarely achieved quickly in biodiversity dynamics, owing to both delayed immigration and delayed extinction 7, 15, 22. Immigration of new species and extinction of doomed species could be delayed for several reasons, creating several potential transient conditions before biodiversity attains equilibrium.

Delayed immigration is well documented in the literature of both non-native species invasions [23] and natural, climate-driven immigrations 24, 25, 26. Colonization of a suitable

Consequences of differential rates: biodiversity deficit and surplus

Even if extinction debt and immigration credit balance each other, communities can experience transient periods of excess or deficient biodiversity if extinction and immigration rates or peaks are offset. If, for example, extinction debt is paid off faster than is immigration credit, then biodiversity values will fall below the equilibrium level until immigration catches up (Figure 2d). This constitutes a biodiversity deficit, in which the community is temporarily impoverished in terms of

Biodiversity forcing by environmental change and habitat fragmentation

Climate change is a powerful force in driving both immigration and extinction, as indicated by the numerous local– regional extinctions and immigrations documented from post-glacial paleoecological studies throughout the world 2, 31, 38, 47, 48. Recent climate change has also triggered immigration and extinction processes across the globe 6, 49, and current climate forecasts indicate that more ecological change will occur over the coming decades 50, 51, 52.

Human-driven habitat reduction and

Surprises and uncertainties in a world of global change

The biodiversity ledger spotlights three risks to biodiversity stemming from differential response times of immigration and extinction to forcing events. First, biodiversity deficits could become commonplace, particularly on broad geographic scales. Although many species are adjusting their elevational and/or latitudinal ranges in response to warming climate (e.g. Ref. [6]), many might lack the capacity to colonize new territory fast enough to match extirpation at their retreating margins. For

Conclusions

Understanding, predicting and mitigating global-change impacts on biodiversity pose crucial challenges for ecologists, conservation biologists and resource managers. The biodiversity-balance framework provides a starting point for identifying what is known and what needs to be learned to address these challenges. To date, there has been little integration of extinction processes and extinction debt with invasion processes and delayed immigration, despite considerable volumes of literature on

Acknowledgments

This paper was supported by the National Science Foundation. Mark Vellend, Simon Brewer, Tom Minckley and three anonymous reviewers provided valuable comments and discussion.

Glossary

Biodiversity accrual
a net increase in the number of species following a forcing event.
Biodiversity balance
the net difference between immigration credit and extinction debt once equilibrium is achieved.
Biodiversity loss
a net decrease in the number of species following a forcing event.
Biodiversity deficit
a transient decrease in the number of species following a forcing event.
Biodiversity surplus
a transient increase in the number of species following a forcing event.
Compositional turnover
community

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