Abstract

•Utilized vertebrate populations declined by 50% on average from 1970 to 2016•Body size is an important predictor of trends in utilized populations•Importantly, populations that are managed are more likely to be increasing•Reversal of decline in utilized populations is crucial for biodiversity and people The use of wildlife supports many people for their food, medicine, and livelihoods. Ensuring that this use is sustainable is central to conservation to ensure the persistence of species alongside continued utilization by people. Using more than 11,000 wildlife population trends, we conducted a global analysis of local-scale data to better understand how populations respond to utilization. We found that utilized populations declined on average by 50% between 1970 and 2016 and showed steeper negative trends than populations that were not utilized (−3%). If these trends continue, then this may threaten species survival and be detrimental to people who rely on their use. We also highlight how these trends might be reversed. Encouragingly, populations under targeted management, whether utilized or not, fared better than those that are not managed. This evidence can be used to track progress toward international and national targets on the sustainable use of species. Sustainable use of wildlife is a core aspiration of biodiversity conservation but is the subject of intense debate in the scientific literature, including the extent to which use is impacting species and whether management can mitigate any impact. Although positive and negative outcomes of sustainable use are known for specific taxa or local communities, a global and regional picture of trends in wildlife populations in use is lacking. We use a global dataset of more than 11,000 time series to derive indices of “utilized” and “not utilized” wildlife populations. Our results show that population trends globally are negative on average but that utilized populations tend to decline more rapidly, especially in Africa and the Americas. Crucially, where populations are managed, they are more likely to be increasing. This evidence can inform global biodiversity assessments and provide an operational indicator to track progress toward the Post-2020 Global Biodiversity Framework. Sustainable use of wildlife is a core aspiration of biodiversity conservation but is the subject of intense debate in the scientific literature, including the extent to which use is impacting species and whether management can mitigate any impact. Although positive and negative outcomes of sustainable use are known for specific taxa or local communities, a global and regional picture of trends in wildlife populations in use is lacking. We use a global dataset of more than 11,000 time series to derive indices of “utilized” and “not utilized” wildlife populations. Our results show that population trends globally are negative on average but that utilized populations tend to decline more rapidly, especially in Africa and the Americas. Crucially, where populations are managed, they are more likely to be increasing. This evidence can inform global biodiversity assessments and provide an operational indicator to track progress toward the Post-2020 Global Biodiversity Framework. Direct use of wild species is one of the ways in which biodiversity is fundamental to the subsistence and livelihoods of people.1Hutton J.M. Leader-Williams N. Sustainable use and incentive-driven conservation: realigning human and conservation interests.Oryx. 2003; 37: 215-226https://doi.org/10.1017/s0030605303000395Crossref Scopus (0) Google Scholar, 2Díaz S. Demissew S. Carabias J. Joly C. Lonsdale M. Ash N. Larigauderie A. Adhikari J.R. Arico S. Báldi A. et al.The IPBES Conceptual Framework — connecting nature and people.Curr. Opin. Environ. 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Biol. 2021; 31: 1788-1797.e1783https://doi.org/10.1016/j.cub.2021.01.079Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar so striving for sustainable use is key. The importance of sustainable use of resources has been recognized as central to biodiversity conservation and is embedded in international bodies and conventions for nature.11United NationsConvention on Biological Diversity. United Nations, 1992Google Scholar, 12Hickey M.J. Acceptance of sustainable use within the CITES community.Vt. Law Rev. 1998; 23: 861Google Scholar, 13IUCNThe IUCN Policy Statement on Sustainable Use of Wild Living Resources. IUCN, 2000Google Scholar, 14United Nations General AssemblyTransforming Our World: The 2030 Agenda for Sustainable Development. United Nations General Assembly, 2015Google Scholar, 15IPBESReport of the Plenary of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on the Work of its Sixth Session. IPBES, 2018Google Scholar However, progress toward achieving the sustainable use of resources globally remains a challenge. As part of the Convention on Biological Diversity’s Strategic Plan for Biodiversity 2011–20, Aichi target 4.2 was set to keep the impacts of use of natural resources well within safe ecological limits by 2020. Progress toward this target was assessed as “poor” in the final decadal review of the Aichi targets,16Secretariat of the convention on biological diversity.Glob. Biodivers. Outlook. 2020; 5Google Scholar and an assessment of the research and management behind the use of wild meat found limited progress toward sustainability.9Ingram D.J. Coad L. Milner-Gulland E.J. Parry L. Wilkie D. Bakarr M.I. Benítez-López A. Bennett E.L. Bodmer R. Cowlishaw G. et al.Wild meat is still on the menu: progress in wild meat research, policy, and practice from 2002 to 2020.Annu. Rev. Environ. 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Biol. 2021; https://doi.org/10.1111/cobi.13844Crossref PubMed Scopus (4) Google Scholar with evidence showing that harvesting, logging, fishing, and hunting often occur at unsustainable levels.3Bongaarts J. IPBES, 2019. Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services.Popul. Dev. Rev. 2019; 45: 680-681https://doi.org/10.1111/padr.12283Crossref Google Scholar Together with activities such as logging and agriculture, hunting and trapping have a higher average probability of impacting species compared with other threats, with hotspots of this threat largely concentrated in the tropics.18Harfoot M.B.J. Johnston A. Balmford A. Burgess N.D. Butchart S.H.M. Dias M.P. Hazin C. Hilton-Taylor C. Hoffmann M. Isaac N.J.B. et al.Using the IUCN Red List to map threats to terrestrial vertebrates at global scale.Nat. Ecol. Evol. 2021; 5: 1510-1519https://doi.org/10.1038/s41559-021-01542-9Crossref PubMed Scopus (14) Google Scholar Combined pressures of land use change and hunting have reduced the distribution of terrestrial tropical mammals, with large-bodied species the most impacted.19Gallego-Zamorano J. Benítez-López A. Santini L. Hilbers J.P. Huijbregts M.A.J. Schipper A.M. Combined effects of land use and hunting on distributions of tropical mammals.Conserv. Biol. 2020; 34: 1271-1280https://doi.org/10.1111/cobi.13459Crossref PubMed Scopus (19) Google Scholar The effect of hunting, especially for commercial use, has been implicated in the population decline of 97 tropical bird and 254 tropical mammal species,20Benítez-López A. Alkemade R. Schipper A.M. Ingram D.J. Verweij P.A. Eikelboom J.A.J. Huijbregts M.A.J. The impact of hunting on tropical mammal and bird populations.Science. 2017; 356: 180-183https://doi.org/10.1126/science.aaj1891Crossref PubMed Scopus (233) Google Scholar and a global assessments of 301 terrestrial mammals threatened with extinction lists hunting as a primary threat.21Ripple W.J. Abernethy K. Betts M.G. Chapron G. Dirzo R. Galetti M. Levi T. Lindsey P.A. Macdonald D.W. Machovina B. et al.Bushmeat hunting and extinction risk to the world's mammals.R. Soc. Open Sci. 2016; 3: 160498https://doi.org/10.1098/rsos.160498Crossref PubMed Scopus (256) Google Scholar In the marine realm, the percentage of commercial fish stocks that are within biologically sustainable levels decreased from 90% to 65.8% between 1974 and 2017,22FAOThe State of World Fisheries and Aquaculture 2020. Sustainability in Action. FAO, 2020Google Scholar although recent trends suggest that stocks that are scientifically assessed are now increasing on average, and intensively managed stocks are faring better.23Hilborn R. Amoroso R.O. Anderson C.M. Baum J.K. Branch T.A. Costello C. de Moor C.L. Faraj A. Hively D. Jensen O.P. et al.Effective fisheries management instrumental in improving fish stock status.Proc. Natl. Acad. Sci. U S A. 2020; 117: 2218-2224https://doi.org/10.1073/pnas.1909726116Crossref PubMed Scopus (193) Google Scholar The role of wildlife management is also evident in some notable examples on land. The rise of community-based natural resource management over 30 years ago, which may include managing the use of species in place of more centralized wildlife management policies, has yielded examples of economic and ecological benefits in many countries.6Cooney R. Roe D. Dublin H. Booker F. Wild Life, Wild Livelihoods: Involving Communities in Sustainable Wildlife Management and Combatting the Illegal Wildlife Trade. United Nations Environment Programme, 2018http://wedocs.unep.org/bitstream/handle/20.500.11822/22864/WLWL_Report_web.pdfGoogle Scholar,24Anderson J. Mehta S. Global assessment of community based natural resource management: addressing the critical challenges of the rural sector.https://rmportal.net/library/content/global-assessment-cbnrm-challenges-rural-sector/at_download/fileGoogle Scholar,25Roe D. Nelson F. Sandbrook C. Community Management of Natural Resources in Africa: Impacts, Experiences and Future Directions. International Institute for Environment and Development, 2009Google Scholar Similarly, even in regions where utilized species have been heavily impacted over centuries,26Ceballos G. Ehrlich P.R. 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Biol. 2008; 22: 252-266https://doi.org/10.1111/j.1523-1739.2008.00899.xCrossref PubMed Scopus (108) Google Scholar To understand how species in use (hereafter called “utilized species” or “utilized populations”; see “definitions” in experimental procedures) are faring at the global scale, existing indicators have largely focused on the species level; e.g., the Red List Index for internationally traded species or those used for food and medicine and the Living Planet Index for utilized species.30Butchart S.H.M. Red list indices to measure the sustainability of species use and impacts of invasive alien species.Bird Conserv. Int. 2008; 18: S245-S262https://doi.org/10.1017/s095927090800035xCrossref Google Scholar,31Tierney M. Almond R. Stanwell-Smith D. McRae L. Zöckler C. Collen B. Walpole M. Hutton J. de Bie S. Use it or lose it: measuring trends in wild species subject to substantial use.Oryx. 2014; 48: 420-429https://doi.org/10.1017/s0030605313000653Crossref Google Scholar These indices cannot integrate any potential heterogeneity of impacts of use because of factors influencing individual populations within the same species differently, as identified for commercial harvesting.32Di Minin E. Brooks T.M. Toivonen T. Butchart S.H.M. Heikinheimo V. Watson J.E.M. Burgess N.D. Challender D.W.S. Goettsch B. Jenkins R. Moilanen A. Identifying global centers of unsustainable commercial harvesting of species.Sci. Adv. 2019; 5: eaau2879https://doi.org/10.1126/sciadv.aau2879Crossref PubMed Scopus (38) Google Scholar In the marine environment, indicators have measured fishing pressure and the proportion of fish stocks that are unsustainable.22FAOThe State of World Fisheries and Aquaculture 2020. Sustainability in Action. FAO, 2020Google Scholar At a smaller scale, harvest models are used to assess sustainability and the status of a utilized population, which can provide detailed information on how a population and ecosystem are impacted by use and inform local management.33Salo M. Sirén A. Kalliola R. Diagnosing Wild Species Harvest: Resource Use and Conservation. Academic Press, 2013Crossref Google Scholar We propose that global and large regional views are needed and present a population-based approach with information on utilization at the site-level aggregated to the global scale. This approach can provide important insights that are not available at the level of species assessments through incorporating population-level information on use, threats, and management into the analysis. To follow this approach, we develop an indicator of utilized vertebrate populations following the method used to calculate the Living Planet Index (LPI),34Loh J. Green R.E. Ricketts T. Lamoreux J. Jenkins M. Kapos V. 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The Living Planet Database, which underpins the index, collates data collected locally from around the world, which can be divided in different ways to deliver a suite of indices of species population change; the data are also suitable for within-species comparisons and identification of correlates predicting trends using mixed-effect models.40Collen B. McRae L. Deinet S. Palma A.D. Carranza T. Cooper N. Loh J. Baillie J.E.M. Predicting how populations decline to extinction.Philos. Trans. R. Soc. B Biol. Sci. 2011; 366: 2577-2586https://doi.org/10.1098/rstb.2011.0015Crossref PubMed Scopus (73) Google Scholar,41Hardesty-Moore M. Deinet S. Freeman R. Titcomb G.C. Dillon E.M. Stears K. Klope M. Bui A. Orr D. Young H.S. et al.Migration in the Anthropocene: how collective navigation, environmental system and taxonomy shape the vulnerability of migratory species.Philos. Trans. R. Soc. B Biol. Sci. 2018; 373: 20170017https://doi.org/10.1098/rstb.2017.0017Crossref PubMed Scopus (25) Google Scholar We then use this to contrast trends in utilized populations with those that are not used for the complete set of species in the dataset and only for species with data for utilized and non-utilized populations (“matched”). Finally, using mixed-effect models, we explore the role of targeted management (see “definitions” in experimental procedures) in predicting populations trends in utilized populations. Our results can help to measure progress toward policy targets and identify trends in resources that are important for people. Our results, thus, feed directly into global processes such as the IPBES thematic assessment of sustainable use of wild species15IPBESReport of the Plenary of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on the Work of its Sixth Session. IPBES, 2018Google Scholar and development of indicators for the Post-2020 Global Biodiversity Framework. Our final dataset comprised 11,123 population time series from 2,944 species, of which 5,811 populations from 1,348 species were coded as utilized, and 5,312 populations from 1,996 species were coded as not utilized (Table S1). For utilized populations, most data were available for fish (n = 3,233), followed by mammals (n = 2,098), birds (n = 331), reptiles (n = 142), and amphibians (n = 7). Fish and mammals had more utilized populations than not, whereas the reverse was true for birds, reptiles, and amphibians (Table S1). Compared with the expected distribution of body mass values for all species, the utilized dataset showed a skewed distribution toward larger-bodied species for birds and mammals but a distribution of body masses to all fish species (Figure S1). Geographically, our sample contained data from all IPBES regions and from 146 countries (Figure 1; Table S2). Utilized and not-utilized populations were found in all regions, but there were noticeable clusters of more utilized populations in parts of Africa, Central Asia, and Canada. The largest regional dataset was for the Americas. Results for Africa are based on the smallest dataset of the regions; data availability throughout the time series dropped after 2012, so the indices were shorter than for the other regions, finishing in 2015 and 2013 for terrestrial/freshwater and marine, respectively. Threat information was available for 3,195 populations—1,694 utilized and 1,501 not utilized (Table S3). There was a difference in the distribution of threats coded between utilized and not utilized populations, with a greater proportion of threats listed as overexploitation for utilized populations (Figure S2). Nearly three-quarters of the overexploitation threats coded for utilized populations were a result of hunting, fishing, and collecting (Figure S3). Of the utilized populations, 46% had information available on targeted management, and 23% were unmanaged (the remainder had no information; Table S4). The index for utilized populations shows a decrease of 69% for terrestrial and freshwater populations (Figure 2; index value in 2016, 0.31; range, 0.21–0.44) and a decrease of 34% for marine populations (Figure 2; index value in 2016, 0.66; range, 0.52–0.85) between 1970 and 2016. Although the overall trend for utilized populations showed a steep decline, there was considerable heterogeneity at the level of individual populations, with 46.3% showing an overall increase, 48.9% showing an overall decrease, and 4.8% were stable in the terrestrial and freshwater index. In the marine index, 53.2% of utilized populations showed an overall decline, 42.6% an overall increase, and 4.2% were stable. We tested the robustness of the indices to time series length. This is important to check when using population trends that vary in sample duration,43Wauchope H.S. Amano T. Sutherland W.J. Johnston A. When can we trust population trends? A method for quantifying the effects of sampling interval and duration.Methods Ecol. Evol. 2019; 10: 2067-2078https://doi.org/10.1111/2041-210x.13302Crossref Google Scholar particularly the effect of short time series that may exhibit more extreme or fluctuating trends and bias in the index.44Leung B. Hargreaves A.L. Greenberg D.A. McGill B. Dornelas M. Freeman R. Clustered versus catastrophic global vertebrate declines.Nature. 2020; 588: 267-271Crossref PubMed Scopus (27) Google Scholar,45Buschke F.T. Hagan J.G. Santini L. Coetzee B.W. Random population fluctuations bias the living Planet index.Nat. Ecol. Evol. 2021; 5: 1145-1152Crossref PubMed Scopus (2) Google Scholar We observed whether similar trends were seen when restricting the dataset to different thresholds for the minimum time series length in numbers of years. When a more stringent minimum threshold for time series length was applied, similar trajectories of decline were observed for indices with a minimum of 5 years, and shallower decline was reported for indices with a minimum of 10 years (Figure S4). The indices for utilized populations trends since 1970 grouped by IPBES regions show disparate trends, with largely tropical regions faring worse than the global indices of utilized populations (Figure 2) and compared with more temperate regions (Figure 3). Africa showed the greatest decline since 1970 in the terrestrial/freshwater and marine subsets; both indices show steeper decline than the global average for utilized species (Figure 3; terrestrial/freshwater index value in 2015, 0.07; range, 0.03–0.16; marine index value in 2013, 0.08; range, 0.04–0.17). The Asia-Pacific index shows a near-continuous decline in the marine index from 1970 to 2016 and an 83% overall decline, which is worse than the global marine index (Figure 3; index value in 2016, 0.17; range, 0.09–0.31); the terrestrial and freshwater index fluctuates from a positive to a negative trend, with high variation in the underlying species trends, and ends at a baseline value similar to 1970, above the global average (Figure 3; index value in 2016, 1.07; range, 0.31–3.76). The terrestrial/freshwater index for the Americas showed a trajectory of decline very similar to the global terrestrial and freshwater index of 67% between 1970 and 2016 (Figure 3; index value in 2016, 0.33; range, 0.19–0.58), whereas the marine index fluctuated throughout the time series and ended at a baseline value similar to 1970, with no significant overall change and a more positive trend than the global marine index (Figure 3; index value in 2016, 1.07; range, 0.78–1.45). The marine indices for Europe and Central Asia showed a slow increase for most of the time series after an initial decline, ending in an overall increase of 41% between 1970 and 2016 (Figure 3; index value in 2016, 1.41; range, 0.95–2.13). The terrestrial/freshwater index had a fluctuating trend for most of the time period but ended with a recent decline (Figure 3; index value in 2016, 0.76; range, 0.43–1.30). Both of these regional indices had trends that were better than the respective global indices. To explore the effect of utilization, we compared trends between utilized and non-utilized populations. For this analysis, we removed all reptile and amphibian data because these two taxa contained low numbers of species and populations in general but particularly those that are in the utilized category, resulting in a large proportional difference when comparing utilized with non-utilized populations. This is likely to make unbalanced comparisons, especially when dividing the dataset into systems (Table S1). This is not to suggest that these two taxa are not important to consider in the context of utilization; indeed, chelonians are one group particularly at risk from use.46Stanford C.B. Iverson J.B. Rhodin A.G.J. Paul van Dijk P. Mittermeier R.A. Kuchling G. Berry K.H. Bertolero A. Bjorndal K.A. Blanck T.E.G. et al.Turtles and tortoises are in trouble.Curr. Biol. 2020; 30: R721-R735https://doi.org/10.1016/j.cub.2020.04.088Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar Comparing the trend for mammals, birds, and fish, populations that are not utilized show a more stable trend, with index values above the 1970 baseline throughout the period, except for a recent decline, resulting in an overall decrease of 3% over the time period (Figure 4A; index value in 2016, 0.97; range, 0.80–1.18). In comparison, the index for utilized populations for the same taxa showed an overall decline of 50% (Figure 4A; index value in 2016, 0.50; range, 0.41–0.62). After 1985, there is no overlap in the confidence intervals of each index, which means they are significantly different. We used mixed-effects models to explore the relationship between utilization, taxonomic class, body size, and time series length with overall population trends as the response variable. Utilization was consistently a useful predictor of overall population trends, with utilized populations more likely to be declining than non-utilized ones (Tables S6–S9). Removing utilization from our models produced significantly worse predictions of population trends (ΔAIC = −10, χ2 = 11.835, p < 0.01). In general, our models did not suggest an interaction between utilization and taxonomic group, highlighting that all taxonomic groups are impacted by utilization. Using our most comprehensive dataset (mammals, birds, and fish in terrestrial, freshwater, and marine systems), body size interacting with class was in our top model, and the coefficients suggest that bird population trends are slightly positive, more so for larger birds; however, the confidence intervals span zero, so these are non-significant (Figures 4B and 4C). Fish trends were significantly positive

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