Life history responses of meerkats to seasonal changes in extreme environments
Timing matters
How a species responds to rapid climate change is complicated. Paniw et al. used long-term data on the Kalahari meerkat, an arid specialist, to explore how predicted changes might affect population persistence over time. Warming and rainfall changes in one part of the year had a negative impact on survival and persistence, whereas similar changes during another part of the year had the opposite effect. Understanding such variability will be essential as we attempt to understand the broader influence of climate change.
Science, this issue p. 631
Abstract
Species in extreme habitats increasingly face changes in seasonal climate, but the demographic mechanisms through which these changes affect population persistence remain unknown. We investigated how changes in seasonal rainfall and temperature influence vital rates and viability of an arid environment specialist, the Kalahari meerkat, through effects on body mass. We show that climate change–induced reduction in adult mass in the prebreeding season would decrease fecundity during the breeding season and increase extinction risk, particularly at low population densities. In contrast, a warmer nonbreeding season resulting in increased mass and survival would buffer negative effects of reduced rainfall during the breeding season, ensuring persistence. Because most ecosystems undergo seasonal climate variations, a full understanding of species vulnerability to global change relies on linking seasonal trait and population dynamics.
Get full access to this article
View all available purchase options and get full access to this article.
Already a Subscriber?Sign In
Supplementary Material
Summary
Materials and Methods
Supplementary Text
Figs. S1 to S18
Tables S1 to S4
R Scripts S1 to S3
Data S1 to S18
Resources
References and Notes
1
F. T. Maestre, R. Salguero-Gómez, J. L. Quero, It is getting hotter in here: Determining and projecting the impacts of global environmental change on drylands. Philos. Trans. R. Soc. London Ser. B 367, 3062–3075 (2012).
2
A. Greenville, G. M. Wardle, V. Nguyen, C. R. Dickman, Population dynamics of desert mammals: Similarities and contrasts within a multispecies assemblage. Ecosphere 7, e01343 (2016).
3
G. Midgley, W. Bond, Future of African terrestrial biodiversity and ecosystems under anthropogenic climate change. Nat. Clim. Chang. 5, 823–829 (2015).
4
J. Ogutu, N. Owen-Smith, ENSO, rainfall and temperature influences on extreme population declines among African savanna ungulates. Ecol. Lett. 6, 412–419 (2003).
5
R. Woodroffe, R. Groom, J. W. McNutt, Hot dogs: High ambient temperatures impact reproductive success in a tropical carnivore. J. Anim. Ecol. 86, 1329–1338 (2017).
6
M. Paniw, A. Ozgul, R. Salguero-Gómez, Interactive life-history traits predict sensitivity of plants and animals to temporal autocorrelation. Ecol. Lett. 21, 275–286 (2018).
7
M. Wichmann, F. Jeltsch, W. R. J. Dean, K. A. Moloney, C. Wissel, Implication of climate change for the persistence of raptors in arid savanna. Oikos 102, 186–202 (2003).
8
A. Ozgul, A. W. Bateman, S. English, T. Coulson, T. H. Clutton-Brock, Linking body mass and group dynamics in an obligate cooperative breeder. J. Anim. Ecol. 83, 1357–1366 (2014).
9
P. Buston, Size and growth modification in clownfish. Nature 424, 145–146 (2003).
10
A. Ozgul, D. Z. Childs, M. K. Oli, K. B. Armitage, D. T. Blumstein, L. E. Olson, S. Tuljapurkar, T. Coulson, Coupled dynamics of body mass and population growth in response to environmental change. Nature 466, 482–485 (2010).
11
T. Clutton-Brock, M. Manser, “Meerkats: cooperative breeding in the Kalahari” in Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior (Cambridge Univ. Press, 2016), pp. 294–317.
12
A. W. Bateman, A. Ozgul, J. F. Nielsen, T. Coulson, T. H. Clutton-Brock, Social structure mediates environmental effects on group size in an obligate cooperative breeder, Suricata suricatta. Ecology 94, 587–597 (2013).
13
F. Courchamp, B. Grenfell, T. Clutton-Brock, Population dynamics of obligate cooperators. Proc. Biol. Sci. 266, 557–563 (1999).
14
T. Clutton-Brock, Breeding together: Kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (2002).
15
M. Gamelon, V. Grøtan, A. L. K. Nilsson, S. Engen, J. W. Hurrell, K. Jerstad, A. S. Phillips, O. W. Røstad, T. Slagsvold, B. Walseng, N. C. Stenseth, B.-E. Sæther, Interactions between demography and environmental effects are important determinants of population dynamics. Sci. Adv. 3, e1602298 (2017).
16
S. J. Hodge, A. Manica, T. P. Flower, T. H. Clutton-Brock, Determinants of reproductive success in dominant female meerkats. J. Anim. Ecol. 77, 92–102 (2008).
17
S. Ellner et al., Data-driven Modelling of Structured Populations: A Practical Guide to the Integral Projection Model (Springer, 2016).
18
J. Zscheischler, S. Westra, B. J. J. M. van den Hurk, S. I. Seneviratne, P. J. Ward, A. Pitman, A. AghaKouchak, D. N. Bresch, M. Leonard, T. Wahl, X. Zhang, Future climate risk from compound events. Nat. Clim. Chang. 8, 469–477 (2018).
19
J. L. Hoogland, Prairie dogs disperse when all close kin have disappeared. Science 339, 1205–1207 (2013).
20
A. C. Markham, L. R. Gesquiere, S. C. Alberts, J. Altmann, Optimal group size in a highly social mammal. Proc. Natl. Acad. Sci. U.S.A. 112, 14882–14887 (2015).
21
E. Angulo, G. M. Luque, S. D. Gregory, J. W. Wenzel, C. Bessa-Gomes, L. Berec, F. Courchamp, Review: Allee effects in social species. J. Anim. Ecol. 87, 47–58 (2018).
22
C. F. Clements, A. Ozgul, Including trait-based early warning signals helps predict population collapse. Nat. Commun. 7, 10984 (2016).
23
F. Courchamp, T. Clutton-Brock, B. Grenfell, Inverse density dependence and the Allee effect. Trends Ecol. Evol. 14, 405–410 (1999).
24
R. D. Bassar, B. H. Letcher, K. H. Nislow, A. R. Whiteley, Changes in seasonal climate outpace compensatory density-dependence in eastern brook trout. Glob. Change Biol. 22, 577–593 (2016).
25
D. R. Easterling, G. A. Meehl, C. Parmesan, S. A. Changnon, T. R. Karl, L. O. Mearns, Climate extremes: Observations, modeling, and impacts. Science 289, 2068–2074 (2000).
26
A. Kruger, S. Shongwe, Temperature trends in South Africa: 1960–2003. Int. J. Climatol. 24, 1929–1945 (2004).
27
D. Lukas, T. Clutton-Brock, Climate and the distribution of cooperative breeding in mammals. R. Soc. Open Sci. 4, 160897 (2017).
28
A. Bateman, T. Coulson, T. H. Clutton-Brock, What do simple models reveal about the population dynamics of a cooperatively breeding species? Oikos 120, 787–794 (2011).
29
T. Clutton-Brock, A. Maccoll, P. Chadwick, D. Gaynor, R. Kansky, J. D. Skinner, Reproduction and survival of suricates (Suricata suricatta) in the southern Kalahari. Afr. J. Ecol. 37, 69–80 (1999).
30
S. English, A. W. Bateman, T. H. Clutton-Brock, Lifetime growth in wild meerkats: Incorporating life history and environmental factors into a standard growth model. Oecologia 169, 143–153 (2012).
31
T. H. Clutton-Brock, P. N. Brotherton, R. Smith, G. M. McIlrath, R. Kansky, D. Gaynor, M. J. O’Riain, J. D. Skinner, Infanticide and expulsion of females in a cooperative mammal. Proc. Biol. Sci. 265, 2291–2295 (1998).
32
A. J. Young, A. A. Carlson, S. L. Monfort, A. F. Russell, N. C. Bennett, T. Clutton-Brock, Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl. Acad. Sci. U.S.A. 103, 12005–12010 (2006).
33
S. P. Doolan, D. W. Macdonald, Breeding and juvenile survival among slender-tailed meerkats (Suricatu suricatta) in the south-western Kalahari: Ecological and social influences. J. Zool. 242, 309–327 (1997).
34
N. Maag, G. Cozzi, T. Clutton-Brock, A. Ozgul, Density-dependent dispersal strategies in a cooperative breeder. Ecology 99, 1932–1941 (2018).
35
P. A. Stephens, A. F. Russell, A. J. Young, W. J. Sutherland, T. H. Clutton-Brock, Dispersal, eviction, and conflict in meerkats (Suricata suricatta): An evolutionarily stable strategy model. Am. Nat. 165, 120–135 (2005).
36
T. Clutton-Brock, S. J. Hodge, T. P. Flower, Group size and the suppression of subordinate reproduction in Kalahari meerkats. Anim. Behav. 76, 689–700 (2008).
37
S. P. Sharp, T. H. Clutton-Brock, Reproductive senescence in a cooperatively breeding mammal. J. Anim. Ecol. 79, 176–183 (2010).
38
C. Calenge, The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecol. Modell. 197, 516–519 (2006).
39
G. Cozzi, N. Maag, L. Börger, T. H. Clutton-Brock, A. Ozgul, Socially informed dispersal in a territorial cooperative breeder. J. Anim. Ecol. 87, 838–849 (2018).
40
S. N. Wood, Generalized Additive Models: An Introduction with R (Chapman and Hall, 2006).
41
H. Akaike, “Information theory and an extension of the maximum likelihood principle” in Proceedings of the 2nd International Symposium on Information Theory (Akadémiai Kiadó, 1971), pp. 267–281.
42
A. F. Russell, T. H. Clutton-Brock, P. N. M. Brotherton, L. L. Sharpe, G. M. Mcilrath, F. D. Dalerum, E. Z. Cameron, J. A. Barnard, Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta. J. Anim. Ecol. 71, 700–709 (2002).
43
R. F. Adler, M. Sapiano, G. J. Huffman, J. Wang, G. Gu, D. Bolvin, L. Chiu, U. Schneider, A. Becker, E. Nelkin, P. Xie, R. Ferraro, D.-B. Shin, The Global Precipitation Climatology Project (GPCP) Monthly Analysis (New Version 2.3) and a Review of 2017 Global Precipitation. Atmosphere 9, 138 (2018).
44
National Center for Atmospheric Research (NCAR) GIS Program, Climate Change Scenarios, version 2.0 (NCAR/UCAR, 2012); https://gisclimatechange.ucar.edu/.
45
A. W. Bateman, A. Ozgul, T. Coulson, T. H. Clutton-Brock, Density dependence in group dynamics of a highly social mongoose, Suricata suricatta. J. Anim. Ecol. 81, 628–639 (2012).
46
K. Bartón, MuMIn: Multi-Model Inference. R package version 1.42.1 (2018); https://CRAN.R-project.org/package=MuMIn..
47
M. R. Easterling, S. P. Ellner, P. M. Dixon, Size-specific sensitivity: Applying a new structured population model. Ecology 81, 694–708 (2000).
48
S. Leclaire, J. F. Nielsen, S. P. Sharp, T. H. Clutton-Brock, Mating strategies in dominant meerkats: Evidence for extra-pair paternity in relation to genetic relatedness between pair mates. J. Evol. Biol. 26, 1499–1507 (2013).
49
A. W. Bateman, A. Ozgul, M. Krkošek, T. H. Clutton-Brock, Matrix Models of Hierarchical Demography: Linking Group- and Population-Level Dynamics in Cooperative Breeders. Am. Nat. 192, 188–203 (2018).
50
A. Kruger, S. Sekele, Trends in extreme temperature indices in South Africa: 1962–2009. Int. J. Climatol. 33, 661–676 (2013).
51
A. C. Davison, D. Hinkley, Bootstrap Methods and Their Application (Cambridge Univ. Press, 1997).
52
M. Paniw, P. F. Quintana-Ascencio, F. Ojeda, R. Salguero-Gómez, Accounting for uncertainty in dormant life stages in stochastic demographic models. Oikos 126, 900–909 (2017).
53
H. Caswell, Matrix Population Models (Sinauer Associates, 2006).
54
J. A. Stamps, Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol. Lett. 10, 355–363 (2007).
55
T. H. Clutton-Brock, D. Gaynor, R. Kansky, A. D. C. MacColl, G. McIlrath, P. Chadwick, P. N. M. Brotherton, J. M. O’Riain, M. Manser, J. D. Skinner, Costs of cooperative behaviour in suricates (Suricata suricatta). Proc. Biol. Sci. 265, 185–190 (1998).
56
L. Ciannelli, K.-S. Chan, K. M. Bailey, N. C. Stenseth, Non-additive effects of the environment on the survival of a large marine fish population. Ecology 85, 3418–3427 (2004).
57
M. Llope, G. M. Daskalov, T. A. Rouyer, V. Mihneva, K.-S. Chan, A. N. Grishin, N. C. Stenseth, Overfishing of top predators eroded the resilience of the Black Sea system regardless of the climate and anthropogenic conditions. Glob. Change Biol. 17, 1251–1265 (2011).
Information & Authors
Information
Published In
Science
Volume 363 | Issue 6427
8 February 2019
8 February 2019
Copyright
Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
This is an article distributed under the terms of the Science Journals Default License.
Submission history
Received: 26 June 2018
Accepted: 10 January 2019
Published in print: 8 February 2019
Acknowledgments
We are grateful to the many volunteers and field managers, in particular T. Vink, of the Kalahari Meerkat Project (KMP) for their contribution to data collection; and to M. Manser for her contribution to the organization of the KMP. Data collection was supported logistically by the Mammal Research Institute of the University of Pretoria. We also thank the Trustees of the Kalahari Research Centre and the Directors of the Kalahari Meerkat Project for access to the data used in this paper, D. Gaynor for access to prior analysis of climate effects on meerkat dynamics and for discussion, and S. Albon for comments on the analysis. Funding: Data used in this paper were collected under ERC Advanced Grants (294494 and 742808) to T.C.B. Analysis of data was funded by an ERC Starting Grant (33785) and a Swiss National Science Foundation Grant (31003A_182286) to A.O. and an ERC Advanced Grant (742808) to T.C.-B. Author contributions: T.C.-B. led the long-term study and data collection; M.P. and A.O. conceived the ideas for the paper and its structure; M.P., A.O., N.M., and G.C. designed the analyses; M.P. conducted the analyses and wrote the manuscript; and all authors discussed the results and commented on the manuscript. Competing interests: The authors declare no competing interests. Data and materials availability: The parameters and datasets generated and analyzed during our study, which are required to build and project meerkat population dynamics, are freely available in the GitHub repository: https://github.com/MariaPaniw/meerkats. All analyses in this study were performed using the freely available statistical software environment R. All R scripts necessary to run the analyses are available at the GitHub site noted above.
Authors
Funding Information
H2020 European Research Council: #337785
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Understanding the potential impact of climate change on the behavior and demography of social species: The pied babbler (Turdoides bicolor) as a case study, , (225-266), (2021).https://doi.org/10.1016/bs.asb.2021.03.005
- The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis, Journal of Animal Ecology, 90, 6, (1398-1407), (2021).https://doi.org/10.1111/1365-2656.13467
- Group size increases inequality in cooperative behaviour, Proceedings of the Royal Society B: Biological Sciences, 288, 1945, (20202104), (2021).https://doi.org/10.1098/rspb.2020.2104
- Forest management affects seasonal source-sink dynamics in a territorial, group-living bird, Oecologia, 196, 2, (399-412), (2021).https://doi.org/10.1007/s00442-021-04935-6
- Changing Lengths of the Four Seasons by Global Warming, Geophysical Research Letters, 48, 6, (2021).https://doi.org/10.1029/2020GL091753
- Seasonality impacts collective movements in a wild group-living bird, Movement Ecology, 9, 1, (2021).https://doi.org/10.1186/s40462-021-00271-9
- Increasing temperature threatens an already endangered coastal dune plant, Ecosphere, 12, 3, (2021).https://doi.org/10.1002/ecs2.3454
- Direct and indirect effects of high temperatures on fledging in a cooperatively breeding bird, Behavioral Ecology, (2021).https://doi.org/10.1093/beheco/arab087
- No sex‐specific differences in the influence of high air temperatures during early development on nestling mass and fledgling survival in the Southern Pied Babbler ( Turdoides bicolor ) , Ibis, (2021).https://doi.org/10.1111/ibi.12990
- Factors influencing distributional shifts and abundance at the range core of a climate‐sensitive mammal, Global Change Biology, (2021).https://doi.org/10.1111/gcb.15793
- See more
Loading...
View Options
Get Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Register for free to read this article
As a service to the community, this article is available for free. Login or register for free to read this article.
Buy a single issue of Science for just $15 USD.
View options
PDF format
Download this article as a PDF file
Download PDF