At the global scale, human activities are threatening the extinction of many species. It remains debated, however, whether there has been corresponding loss of biodiversity at the smaller spatial scales at which species loss often erodes ecosystem functioning, stability and services. Here we consider changes in local biodiversity and productivity over 37 years in 21 grasslands and savannahs with known agricultural land-use histories. We show that, during the century following agricultural abandonment, local plant diversity recovers only incompletely and plant productivity does not significantly recover. By 91 years after agricultural abandonment, despite many local species gains, formerly ploughed fields still had only three quarters of the plant diversity and half of the plant productivity observed in a nearby remnant ecosystem that has never been ploughed. The large and growing extent of recovering ecosystems provides an unprecedented opportunity to reverse the impacts of habitat loss. Active restoration efforts are needed to enable and accelerate recovery.
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The plant biomass and cover data that support the findings of this study are available from the Cedar Creek Long-Term Ecological Research project website (www.cedarcreek.umn.edu/research/data).
Ceballos, G. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).
Pimm, S. L. et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).
Tilman, D. et al. Future threats to biodiversity and pathways to their prevention. Nature 546, 73–81 (2017).
Barger, N. N. et al. in The IPBES Assessment Report on Land Degradation and Restoration (eds Montanarella, L. et al.) Ch. 3 (Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 2018).
Isbell, F. et al. Linking the influence and dependence of people on biodiversity across scales. Nature 546, 65–72 (2017).
Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).
O’Connor, M. I. et al. A general biodiversity–function relationship is mediated by trophic level. Oikos 126, 18–31 (2017).
Sax, D. F., Gaines, S. D. & Brown, J. H. Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am. Nat. 160, 766–783 (2002).
Sax, D. F. & Gaines, S. D. Species diversity: from global decreases to local increases. Trends Ecol. Evol. 18, 561–566 (2003).
Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010).
Murphy, G. E. P. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).
Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).
Vellend, M. et al. Global meta-analysis reveals no net change in local-scale plant biodiversity over time. Proc. Natl Acad. Sci. USA 110, 19456–19459 (2013).
Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).
Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).
Vellend, M. et al. Estimates of local biodiversity change over time stand up to scrutiny. Ecology 98, 583–590 (2017).
Primack, R. B. et al. Biodiversity gains? The debate on changes in local- vs global-scale species richness. Biol. Conserv. 219, A1–A3 (2018).
Cardinale, B. J., Gonzalez, A., Allington, G. R. H. & Loreau, M. Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biol. Conserv. 219, 175–183 (2018).
Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).
Benayas, J. M. R., Newton, A. C., Diaz, A. & Bullock, J. M. Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325, 1121–1124 (2009).
Moreno-Mateos, D. et al. Anthropogenic ecosystem disturbance and the recovery debt. Nat. Commun. 8, 14163 (2017).
Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015).
Tilman, D. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol. Monogr. 57, 189–214 (1987).
Clark, C. M. & Tilman, D. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451, 712–715 (2008).
Isbell, F. et al. Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc. Natl Acad. Sci. USA 110, 11911–11916 (2013).
Inouye, R. S. et al. Old-field succession on a Minnesota sand plain. Ecology 68, 12–26 (1987).
Clark, A. T., Knops, J. M. H. & Tilman, D. Contingent factors explain average divergence in functional composition over 88 years of old field succession. J. Ecol. 107, 545–558 (2019).
Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).
Hurtt, G. C. et al. Harmonization of land-use scenarios for the period 1500–2100: 600 years of global gridded annual land-use transitions, wood harvest, and resulting secondary lands. Climatic Change 109, 117 (2011).
Bullock, J. M., Pywell, R. F. & Walker, K. J. Long-term enhancement of agricultural production by restoration of biodiversity. J. Appl. Ecol. 44, 6–12 (2007).
Peterson, D. W. & Reich, P. B. Prescribed fire in oak savanna: fire frequency effects on stand structure and dynamics. Ecol. Appl. 11, 914–927 (2001).
Peterson, D. W. & Reich, P. B. Fire frequency and tree canopy structure influence plant species diversity in a forest-grassland ecotone. Plant Ecol. 194, 5–16 (2008).
Cavender-Bares, J. & Reich, P. B. Shocks to the system: community assembly of the oak savanna in a 40-year fire frequency experiment. Ecology 93, S52–S69 (2012).
Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).
Smith, B. & Wilson, J. B. A consumer’s guide to evenness indices. Oikos 76, 70–82 (1996).
Tilman, D. & Downing, J. A. Biodiversity and stability in grasslands. Nature 367, 363–365 (1994).
Haddad, N. M., Tilman, D. & Knops, J. M. H. Long-term oscillations in grassland productivity induced by drought. Ecol. Lett. 5, 110–120 (2002).
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team nlme: linear and nonlinear mixed effects models. R package version 3.1-140 (2019).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).
Bond, W. J. & Keeley, J. E. Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol. Evol. 20, 387–394 (2005).
USDA & NRCS The PLANTS Database (National Plant Data Team, 2019); http://plants.usda.gov, 11 October 2019
We thank T. Mielke, K. Worm and the many undergraduate student interns for assistance with field work. We acknowledge funding support from the US National Science Foundation’s Long-Term Ecological Research (LTER) programme (DEB-1831944), the LTER Network Communications Office (DEB-1545288) and an NSF CAREER award (DEB-1845334).
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Range of years sampled, range of years since agricultural abandonment (YSA), number of years in which sampling occurred, and number of observations for fields sampled in the old field chronosequence study (Cedar Creek study E054) and in the control plots of the long-term fertilization study (Cedar Creek study E001). Field D is the never-plowed primary vegetation reference.
The most parsimonious model, based on the Akaike Information Criterion (AIC), is bolded for each response variable. In each case, models with linear or decelerating (logarithmic) fixed effects for YSA (years since agricultural abandonment) were first compared. The most parsimonious of these fixed effect structures was retained for subsequent comparisons of alternative random effects and autocorrelation structures. df = degrees of freedom; YSA = years since agricultural abandonment.
That is, these ten species are found in Minnesota, including at our study site, but not in Manitoba or Ontario, the Canadian Provinces that are more than 350 km north of study site. Gains of these species during our study could possibly be attributable to range shifts in response to climate change. However, 9 of these 10 species were already present at the beginning of these studies, observed in 1982, the first year of observations, or in 1983, the first year of observations in another survey of plants in these fields (E014), or in 1984 in another experiment (E002) that is also located in these same fields. Furthermore, an additional 166 plant species observed in our study are found in Minnesota and in Manitoba or Ontario and thus are not near their northern range limit. Thus, only 1 of the 176 plant species identified in our studies, Aristida tuberculosa, possibly arrived at the study site during recent decades due to a range shift in response to climate change. Even this species may have been present, but failed to be detected, during early years, due to dormancy or observation error.
The 42 plant species listed here were introduced to Minnesota. About half of these species were already observed in 1982, during the first year of observations. About three quarters of the species were observed by 1988, the first year of the annual sampling of the old field chronosequence (E054). This leaves only 8 of the 176 plant species identified in our studies that possibly arrived at the study site during recent decades due to biotic homogenization resulting from species introductions. Even these eight species may have been present from the start, but failed to be detected, during early years, due to dormancy or observation error.
Range of years sampled, number of years in which sampling occurred, and number of observations for fields sampled in the old field chronosequence study that collected plant cover data (Cedar Creek study E014) and in the long-term prescribed fire study that collected plant cover data (Cedar Creek study E133). The Field numbers given for E014 correspond to the Field numbers given for E054 in Extended Data Fig. 1. The Field numbers given for E133 are its plot numbers and do not correspond to the field numbers of E014 or E054.
Extended Data Fig. 6 Spatial comparison of local (0.5 m2) plant species richness between 18 fields that were never-plowed and 26 fields that were formerly-plowed.
Data shown are based on plant cover measurements and were averaged over all observations (quadrats and years) within fields, such that the variation shown is only across fields. Here, rather than having a single never-plowed field as a reference remnant (as in Fig. 2), values are shown as a percentage of the average plant species richness observed in 18 fields that were never-plowed. Note that these percentages are not directly comparable to those shown in Fig. 2 because they were collected by a different method (cover estimates, rather than clipped biomass) and at a different spatial scale (0.5 m2, rather than 0.3 m2). Nevertheless, the results are similar in that, in both cases, formerly-plowed fields tend to have lower local plant species richness than never-plowed fields. Details for each field are provided in Extended Data Fig. 5. Box plots summarize observed data: black band, median; bottom and top of boxes respectively correspond to lower and upper quartiles; error bars show 1.5 times the interquartile range.
Extended Data Fig. 7 Many lands worldwide are now recovering after agricultural abandonment, especially in the regions where most biodiversity monitoring has occurred in recent decades (that is, Northern America and Western Europe).
Decreases in agricultural land area over time indicate that more land is being abandoned from agriculture than is being converted to it. Given that abandoned agricultural lands are now widespread, and that it can take more than a century for recovery of biodiversity following agricultural abandonment (Fig. 2), many species gains observed during recent decades may be the reduction of a biodiversity deficit, rather than a local biodiversity surplus (Fig. 1). Data shown are from the Food and Agriculture Organization (FAO) of the United Nations (www.fao.org/faostat). Agricultural area includes arable land (temporary crops, temporary pastures and hay meadows, gardens), permanent crops (crops that do not need to be replanted after each harvest), and permanent pastures (herbaceous forage crops, either sown or natural vegetation).
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Isbell, F., Tilman, D., Reich, P.B. et al. Deficits of biodiversity and productivity linger a century after agricultural abandonment. Nat Ecol Evol 3, 1533–1538 (2019). https://doi.org/10.1038/s41559-019-1012-1
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