News Reader.info

ABSTRACT The dependence of hunter-gatherers on local net primary production (NPP) to provide food played a major role in shaping long-term human population dynamics. Observations of

contemporary hunter-gatherers have shown an overall correlation between population density and annual NPP but with a 1,000-fold variation in population density per unit NPP that remains

unexplained. Here, we build a process-based hunter-gatherer population model embedded within a global terrestrial biosphere model, which explicitly addresses the extraction of NPP through

dynamically allocated hunting and gathering activities. The emergent results reveal a strong, previously unrecognized effect of seasonality on population density via diet composition,

whereby hunter-gatherers consume high fractions of meat in regions where growing seasons are short, leading to greatly reduced population density due to trophic inefficiency. This seasonal

carnivory bottleneck largely explains the wide variation in population density per unit NPP and questions the prevailing usage of annual NPP as the proxy of carrying capacity for ancient

humans. Our process-based approach has the potential to greatly refine our understanding of dynamical responses of ancient human populations to past environmental changes. Access through

your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Access Nature and 54 other Nature

Portfolio journals Get Nature+, our best-value online-access subscription $32.99 / 30 days cancel any time Learn more Subscribe to this journal Receive 12 digital issues and online access to

articles $119.00 per year only $9.92 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which

are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY

OTHERS CLIMATE-DRIVEN HABITAT SHIFTS OF HIGH-RANKED PREY SPECIES STRUCTURE LATE UPPER PALEOLITHIC HUNTING Article Open access 14 March 2023 CHANGES IN LIMITING FACTORS FOR FORAGER POPULATION

DYNAMICS IN EUROPE ACROSS THE LAST GLACIAL-INTERGLACIAL TRANSITION Article Open access 06 September 2022 ECOSYSTEM PRODUCTIVITY AFFECTED THE SPATIOTEMPORAL DISAPPEARANCE OF NEANDERTHALS IN

IBERIA Article Open access 29 September 2022 DATA AVAILABILITY The contemporary hunter-gatherer data and environmental variables used in the analysis are available in the Supplementary Data.

CODE AVAILABILITY Source code (in Python) of the FORGE model and its output files (in NetCDF format) for this study, including the three sets of global simulations (S0, S1, S2), are

provided in Supplementary Software. The corresponding input files for the FORGE model are available at https://doi.org/10.6084/m9.figshare.14995320.v2. REFERENCES * Binford, L. R.

_Constructing Frames of Reference: An Analytical Method for Archaeological_ _Theory Building Using Hunter-Gatherer and Environmental Data Sets_ (Univ. of California Press, 2001). * Kelly, R.

L. _The Lifeways of Hunter-Gatherers: The Foraging Spectrum_ (Cambridge Univ. Press, 2013). * Tallavaara, M., Eronen, J. T. & Luoto, M. Productivity, biodiversity, and pathogens

influence the global hunter-gatherer population density. _Proc. Natl Acad. Sci. USA_ 115, 1232–1237 (2018). Article  CAS  PubMed  Google Scholar  * Eriksson, A. et al. Late Pleistocene

climate change and the global expansion of anatomically modern humans. _Proc. Natl Acad. Sci. USA_ 109, 16089–16094 (2012). Article  CAS  PubMed  PubMed Central  Google Scholar  * Gurven, M.

D. & Davison, R. J. Periodic catastrophes over human evolutionary history are necessary to explain the forager population paradox. _Proc. Natl Acad. Sci_. _USA_

https://doi.org/10.1073/pnas.1902406116 (2019). * Tallavaara, M., Luoto, M., Korhonen, N., Järvinen, H. & Seppä, H. Human population dynamics in Europe over the Last Glacial Maximum.

_Proc. Natl Acad. Sci. USA_ 112, 8232–8237 (2015). Article  CAS  PubMed  PubMed Central  Google Scholar  * Bradshaw, C. J. A. et al. Minimum founding populations for the first peopling of

Sahul. _Nat. Ecol. Evol._ 3, 1057–1063 (2019). Article  PubMed  Google Scholar  * Kavanagh, P. H. et al. Hindcasting global population densities reveals forces enabling the origin of

agriculture. _Nat. Hum. Behav._ 2, 478–484 (2018). Article  PubMed  Google Scholar  * Porter, C. C. & Marlowe, F. W. How marginal are forager habitats? _J. Archaeol. Sci._ 34, 59–68

(2007). Article  Google Scholar  * Reyes-García, V. & Pyhälä, A. _Hunter-Gatherers in a Changing World_ (Springer International Publishing, 2017). * Lee, R. B. & Daly, R. _The

Cambridge Encyclopedia of Hunters and Gatherers_ (Cambridge Univ. Press, 1999). * Kitanishi, K. Seasonal changes in the subsistence activities and food intake of the Aka hunter-gatherers in

northeastern Congo. _Afr. Study Monogr._ 16, 73–118 (1995). Google Scholar  * Timmermann, A. & Friedrich, T. Late Pleistocene climate drivers of early human migration. _Nature_ 538,

92–95 (2016). Article  CAS  PubMed  Google Scholar  * Keeley, L. H. Hunter-gatherer economic complexity and ‘population pressure’: a cross-cultural analysis. _J. Anthropol. Archaeol._ 7,

373–411 (1988). * Fisher, J. B., Huntzinger, D. N., Schwalm, C. R. & Sitch, S. Modeling the terrestrial biosphere. _Annu. Rev. Environ. Resour._ 39, 91–123 (2014). Article  Google

Scholar  * Pachzelt, A., Forrest, M., Rammig, A., Higgins, S. I. & Hickler, T. Potential impact of large ungulate grazers on African vegetation, carbon storage and fire regimes. _Glob.

Ecol. Biogeogr._ 24, 991–1002 (2015). Article  Google Scholar  * Zhu, D. et al. The large mean body size of mammalian herbivores explains the productivity paradox during the Last Glacial

Maximum. _Nat. Ecol. Evol._ 2, 640–649 (2018). Article  PubMed  PubMed Central  Google Scholar  * Dyble, M., Thorley, J., Page, A. E., Smith, D. & Migliano, A. B. Engagement in

agricultural work is associated with reduced leisure time among Agta hunter-gatherers. _Nat. Hum. Behav_. 3, 792–796 (2019). * Hill, K., Kaplan, H., Hawkes, K. & Hurtado, A. M. Men’s

time allocation to subsistence work among the Ache of eastern Paraguay. _Hum. Ecol._ 13, 29–47 (1985). Article  Google Scholar  * Hill, K., Hawkes, K., Hurtado, M. & Kaplan, H. Seasonal

variance in the diet of Ache hunter-gatherers in eastern Paraguay. _Hum. Ecol._ 12, 101–135 (1984). Article  CAS  Google Scholar  * Marlowe, F. W. et al. Honey, Hadza, hunter-gatherers, and

human evolution. _J. Hum. Evol._ 71, 119–128 (2014). Article  PubMed  Google Scholar  * Cordain, L. et al. Plant–animal subsistence ratios and macronutrient energy estimations in worldwide

hunter-gatherer diets. _Am. J. Clin. Nutr._ 71, 682–692 (2000). Article  CAS  PubMed  Google Scholar  * Gurven, M. & Kaplan, H. Longevity among hunter-gatherers: a cross-cultural

examination. _Popul. Dev. Rev._ 33, 321–365 (2007). Article  Google Scholar  * Klein Goldewijk, K., Beusen, A. & Janssen, P. Long-term dynamic modeling of global population and built-up

area in a spatially explicit way: HYDE 3.1. _Holocene_ 20, 565–573 (2010). Article  Google Scholar  * Marlowe, F. W. Hunter-gatherers and human evolution. _Evol. Anthropol._ 14, 54–67

(2005). Article  Google Scholar  * Burger, J. R. & Fristoe, T. S. Hunter-gatherer populations inform modern ecology. _Proc. Natl Acad. Sci. USA_ 115, 1137–1139 (2018). Article  PubMed 

PubMed Central  CAS  Google Scholar  * Hurtado, A. M. & Hill, K. R. Seasonality in a foraging society: variation in diet, work effort, fertility, and sexual division of labor among the

Hiwi of Venezuela. _J. Anthropol. Res._ 46, 293–346 (1990). Article  Google Scholar  * Wilmsen, E. N. Studies in diet, nutrition, and fertility among a group of Kalahari Bushmen in Botswana.

_Soc. Sci. Inf._ 21, 95–125 (1982). Article  Google Scholar  * Lee, R. B. in _Man the Hunter_ (eds. Lee, R. B. & DeVore, I.) 30–48 (Aldine de Gruyter, 1968). * Hamilton, M. J., Milne,

B. T., Walker, R. S. & Brown, J. H. Nonlinear scaling of space use in human hunter-gatherers. _Proc. Natl Acad. Sci. USA_ 104, 4765–4769 (2007). Article  CAS  PubMed  PubMed Central 

Google Scholar  * Messer, E. Anthropological perspectives on diet. _Annu. Rev. Anthropol._ 13, 205–249 (1984). Article  Google Scholar  * Testart, A. et al. The significance of food storage

among hunter-gatherers: residence patterns, population densities, and social Inequalities [and Comments and Reply]. _Curr. Anthropol._ 23, 523–537 (1982). Article  Google Scholar  *

Winterhalder, B. Diet choice, risk, and food sharing in a stochastic environment. _J. Anthropol. Archaeol._ 5, 369–392 (1986). Article  Google Scholar  * Kelly, R. L., Pelton, S. R. &

Robinson, E. in _Towards a Broader View of Hunter-Gatherer Sharing_ (eds Lavi, N. & Friesem, D. E.) Ch. 10 (McDonald Institute for Archaeological Research, 2019). * Joannes-Boyau, R. et

al. Elemental signatures of _Australopithecus africanus_ teeth reveal seasonal dietary stress. _Nature_ 572, 112–115 (2019). Article  CAS  PubMed  PubMed Central  Google Scholar  * Smits, S.

A. et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. _Science_ 357, 802–806 (2017). Article  CAS  PubMed  PubMed Central  Google Scholar  * Barnosky,

A. D. Assessing the causes of Late Pleistocene extinctions on the continents. _Science_ 306, 70–75 (2004). Article  CAS  PubMed  Google Scholar  * Henrich, J. Demography and cultural

evolution: how adaptive cultural processes can produce maladaptive losses—the Tasmanian case. _Am. Antiq._ 69, 197–214 (2004). Article  Google Scholar  * Powell, A., Shennan, S. &

Thomas, M. G. Late Pleistocene demography and the appearance of modern human behavior. _Science_ 324, 1298–1301 (2009). Article  CAS  PubMed  Google Scholar  * D’Alpoim Guedes, J. A.,

Crabtree, S. A., Bocinsky, R. K. & Kohler, T. A. Twenty-first century approaches to ancient problems: climate and society. _Proc. Natl Acad. Sci. USA_ 113, 14483–14491 (2016). Article 

PubMed  PubMed Central  CAS  Google Scholar  * Cegielski, W. H. & Rogers, J. D. Rethinking the role of Agent-based modeling in archaeology. _J. Anthropol. Archaeol._ 41, 283–298 (2016).

Article  Google Scholar  * Axtell, R. L. et al. Population growth and collapse in a multiagent model of the Kayenta Anasazi in long house valley. _Proc. Natl Acad. Sci. USA_ 99, 7275–7279

(2002). Article  CAS  PubMed  PubMed Central  Google Scholar  * Hayden, B. Research and development in the stone age: technological transitions among hunter-gatherers. _Curr. Anthropol._ 22,

519–548 (1981). Article  Google Scholar  * Itkonen, T. I. _Suomen Lappalaiset Vuoteen 1945. Ensimmäinen Osa_ (WSOY, 1848). * Kirby, K. R. et al. D-PLACE: a global database of cultural,

linguistic and environmental diversity. _PLoS ONE_ 11, e0158391 (2016). Article  PubMed  PubMed Central  CAS  Google Scholar  * _MODIS NPP_ (MOD17A3) (NTSG, accessed 12 March 2015);

http://files.ntsg.umt.edu/data/NTSG_Products/MOD17/ * Defries, R.S. et al. _ISLSCP II Continuous Fields of Vegetation Cover, 1992–1993_ (ORNL DAAC, 2009);

https://doi.org/10.3334/ORNLDAAC/931 * Bodesheim, P., Jung, M., Gans, F., Mahecha, M. D. & Reichstein, M. Upscaled diurnal cycles of land–atmosphere fluxes: a new global half-hourly data

product. _Earth Syst. Sci. Data_ 10, 1327–1365 (2018). Article  Google Scholar  * Šímová, I. & Storch, D. The enigma of terrestrial primary productivity: measurements, models, scales

and the diversity–productivity relationship. _Ecography_ 40, 239–252 (2017). Article  Google Scholar  * Bontemps, S. et al. Consistent global land cover maps for climate modelling

communities: current achievements of The ESA Land Cover CCI. In _Proc. ESA Living Planet Symposium 2013_ (ESA, 2013). * Bliege Bird, R. & Bird, D. W. Why women hunt—risk and contemporary

foraging in a western desert aboriginal community. _Curr. Anthropol._ 49, 655–693 (2008). Article  Google Scholar  * Bliege Bird, R., Codding, B. F. & Bird, D. W. What explains

differences in men’s and women’s production? _Hum. Nat._ 20, 105–129 (2009). Article  PubMed  Google Scholar  * Reyes-García, V., Díaz-Reviriego, I., Duda, R., Fernández-Llamazares, Á. &

Gallois, S. ‘Hunting otherwise’—women’s hunting in two contemporary forager-horticulturalist societies. _Hum. Nat._ 31, 203–221 (2020). Article  PubMed  Google Scholar  * Krinner, G. et al.

A dynamic global vegetation model for studies of the coupled atmosphere-biosphere system. _Global Biogeochem. Cycles_ 19, GB1015 (2005). * Hamilton, M. J., Lobo, J., Rupley, E., Youn, H.

& West, G. B. The ecological and evolutionary energetics of hunter‐gatherer residential mobility. _Evol. Anthropol._ 25, 124–132 (2016). Article  PubMed  PubMed Central  Google Scholar 

* Abrams, P. A. & Ginzburg, L. R. The nature of predation: prey dependent, ratio dependent or neither? _Trends Ecol. Evol._ 15, 337–341 (2000). Article  CAS  PubMed  Google Scholar  *

Winterhalder, B., Baillargeon, W., Cappelletto, F., Randolph Daniel, I. & Prescott, C. The population ecology of hunter-gatherers and their prey. _J. Anthropol. Archaeol._ 7, 289–328

(1988). Article  Google Scholar  * Illius, A. W. & O’Connor, T. G. Resource heterogeneity and ungulate population dynamics. _Oikos_ 89, 283–294 (2000). Article  Google Scholar  * Golley,

F. B. Energy values of ecological materials. _Ecology_ 42, 581–584 (1961). Article  Google Scholar  * Herbers, J. M. Time resources and laziness in animals. _Oecologia_ 49, 252–262 (1981).

Article  PubMed  Google Scholar  * Raichlen, D. A. et al. Sitting, squatting, and the evolutionary biology of human inactivity. _Proc. Natl Acad. Sci_. _USA_

https://doi.org/10.1073/pnas.1911868117 (2020). * Abrams, H., Jr. in _Food and Evolution_ (eds Harris, M. & Ross, E.) 207–223 (Temple Univ. Press, 1987). * Hanya, G. & Aiba, S. Fruit

fall in tropical and temperate forests: implications for frugivore diversity. _Ecol. Res._ 25, 1081–1090 (2010). Article  Google Scholar  * Gherardi, L. A. & Sala, O. E. Global patterns

and climatic controls of belowground net carbon fixation. _Proc. Natl Acad. Sci. USA_ https://doi.org/10.1073/pnas.2006715117 (2020). * van Zonneveld, M. et al. Human diets drive range

expansion of megafauna-dispersed fruit species. _Proc. Natl Acad. Sci. USA_ 115, 3326–3331 (2018). Article  PubMed  PubMed Central  CAS  Google Scholar  * Max R., Hannah R. & Esteban

Ortiz-Ospina _World Population Growth_ (GCDL, 2020); https://ourworldindata.org/world-population-growth * Pontzer, H. et al. Metabolic acceleration and the evolution of human brain size and

life history. _Nature_ 533, 390 (2016). Article  CAS  PubMed  PubMed Central  Google Scholar  * Viovy, N. _CRUNCEP Version 7—Atmospheric Forcing Data for the Community Land Model_ (Research

Data Archive at the National Center for Atmospheric Research, Computational and Information Systems Laboratory, 2018); https://doi.org/10.5065/PZ8F-F017 * Sobol, I. Global sensitivity

indices for nonlinear mathematical models and their Monte Carlo estimates. _Math. Comput. Simul._ 55, 271–280 (2001). Article  Google Scholar  Download references ACKNOWLEDGEMENTS D.Z. and

E.D.G. acknowledge the financial support from the European Research Council under the European Union’s Horizon 2020 Research and Innovation Programme (agreement no. 682602, to E.D.G.). D.Z.

also acknowledges support from the National Natural Science Foundation of China (grant no. 41988101). V.R.-G. acknowledges support from the European Research Council under agreement no.

771056. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Sino-French Institute for Earth System Science, College of Urban and Environmental Sciences, Peking University, Beijing, China Dan Zhu *

Institut de Ciència i Tecnologia Ambientals (ICTA-UAB), Universitat Autònoma de Barcelona, Barcelona, Spain Dan Zhu, Eric D. Galbraith & Victoria Reyes-García * Department of Earth and

Planetary Sciences, McGill University, Montreal, Quebec, Canada Eric D. Galbraith * ICREA (Catalan Institution for Research and Advanced Studies), Barcelona, Spain Eric D. Galbraith & 

Victoria Reyes-García * Laboratoire des Sciences du Climat et de l’Environnement, IPSL-LSCE, CEA-CNRS-UVSQ-UPSACLAY, Gif sur Yvette, France Philippe Ciais * Climate and Atmosphere Research

Center (CARE-C), The Cyprus Institute, Nicosia, Cyprus Philippe Ciais Authors * Dan Zhu View author publications You can also search for this author inPubMed Google Scholar * Eric D.

Galbraith View author publications You can also search for this author inPubMed Google Scholar * Victoria Reyes-García View author publications You can also search for this author inPubMed 

Google Scholar * Philippe Ciais View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS D.Z. and E.D.G. conceived the study and model design. D.Z.

built the model, performed the analyses and wrote the first draft. E.D.G. provided discussion and suggestions throughout the process. V.R.-G. and P.C. contributed to the interpretation of

the results and writing of the manuscript. CORRESPONDING AUTHOR Correspondence to Dan Zhu. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing interests. ADDITIONAL

INFORMATION PEER REVIEW INFORMATION _Nature Ecology & Evolution_ thanks Trevor Fristoe and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer

reviewer reports are available. PUBLISHER’S NOTE Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. SUPPLEMENTARY

INFORMATION SUPPLEMENTARY INFORMATION Supplementary Figs. 1–23, Discussion 1–3 and Tables 1–4. REPORTING SUMMARY PEER REVIEW FILE SUPPLEMENTARY DATA The contemporary hunter-gatherer data and

environmental variables used in the analysis. SUPPLEMENTARY SOFTWARE Source code (in Python) of the FORGE model and its output files (in NetCDF format) including the three sets of global

simulations (S0, S1, S2). RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Zhu, D., Galbraith, E.D., Reyes-García, V. _et al._ Global hunter-gatherer

population densities constrained by influence of seasonality on diet composition. _Nat Ecol Evol_ 5, 1536–1545 (2021). https://doi.org/10.1038/s41559-021-01548-3 Download citation *

Received: 23 September 2020 * Accepted: 04 August 2021 * Published: 09 September 2021 * Issue Date: November 2021 * DOI: https://doi.org/10.1038/s41559-021-01548-3 SHARE THIS ARTICLE Anyone

you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the

Springer Nature SharedIt content-sharing initiative