A demographic approach to study effects of climate change in desert plants

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1606, 2012, Pages 3100-3114

  Salguero Gómez, Roberto ^a   Siewert, Wolfgang ^b   Casper, Brenda B ^c   Tielbörger, Katja ^b  

^a MAX PLANCK INSTITUTE FOR DEMOGRAPHIC RESEARCH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Climate change; Demographic buffering; Integral projection model; Periodic population matrix model; Precipitation; Stochastic population growth rate ( s)

Indexed keywords

ANNUAL PLANT; CLIMATE CHANGE; CLIMATE EFFECT; CLIMATE PREDICTION; DATA SET; DEMOGRAPHY; DESERT; GROWTH RATE; LIFE HISTORY TRAIT; PERENNIAL PLANT; PERIODICITY; PHENOLOGY; POPULATION GROWTH; POPULATION MODELING; PRECIPITATION (CLIMATOLOGY); RESOURCE AVAILABILITY; SEED BANK; STOCHASTICITY;

COLORADO DESERT; COLORADO PLATEAU; ISRAEL; NEGEV; SONORAN DESERT; SOUTHERN DISTRICT; UNITED STATES;

CARRICHTERA; CARRICHTERA ANNUA; CRYPTANTHA; CRYPTANTHA FLAVA;

EID: 84867174007     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0074     Document Type: Article

References (111)

1. United Nations Environmental Programme. 1992 Global biodiversity strategy. Guidelines for action to save, study and use earth's biotic wealth sustainably and equitably. Washington, DC: World Resources Institute.
2. Maestre, F. T., Salguero-Gómez, R. & Quero, J. L. 2012 It's getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Phil. Trans. R. Soc. B 367, 3062-3075. (doi:10.1098/rstb.2011.0323)
3. Reynolds, J. F. et al. 2007 Global desertification: building a science for dryland development. Science 316, 847-851. (doi:10.1126/science.1131634)
4. Intergovernmental Panel for Climate Change. 2007 Climate change 2007: synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland: IPCC.
5. Sala, O. E. & Lauenroth, W. K. 1982 Small rainfall events: an ecological role in semiarid regions. Oecologia 53, 301-304. (doi:10.1007/BF00389004)
6. Smith, W. K., Monson, R. K. & Anderson, J. E. 1997 Physiological ecology of North American desert plants. New York, NY: Springer.
7. Canadell, J., Jackson, R. B., Ehleringer, J. R., Mooney, H. A., Sala, O. E. & Schulze, E. D. 1996 Maximum rooting depth of vegetation types at the global scale. Oecologia 108, 583-595. (doi:10.1007/BF00329030)
8. Dodd, A. N., Borland, A. M., Haslam, R. P., Griffiths, H. & Maxwell, K. 2002 Crassulacean acid metabolism: plastic, fantastic. J. Exp. Bot. 53, 569-580. (doi:10. 1093/jexbot/53.369.569)
9. Schenk, H. J., Espino, S., Goedhart, C. M., Nordenstahl, M., Cabrera, H. I. M. & Jones, C. S. 2008 Hydraulic integration and shrub growth form linked across continental aridity gradients. Proc. Natl Acad. Sci. USA 105, 11 248-11 253. (doi:10.1073/ pnas.0804294105)
10. Angert, A. L., Horst, J. L., Huxman, T. E. & Venable, D. L. 2010 Phenotypic plasticity and precipitation response in Sonoran desert winter annuals. Am. J. Bot. 97, 405-411. (doi:10.3732/ajb.0900242)
11. Bowers, J. E., Webb, R. H. & Rondeau, R. J. 1995 Longevity, recruitment and mortality of desert plants in Grand Canyon, Arizona, USA. J. Veg. Sci. 6, 551-564. (doi:10.2307/3236354)
12. Schwinning, S., Sala, O. E., Loik, M. E. & Ehleringer, J. R. 2004 Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141, 191-193. (doi:10.1007/ s00442-004-1683-3)
13. Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon, S. A., Karl, T. R. & Mearns, L. O. 2000 Climate extremes: observations, modeling, and impacts. Science 289, 2068-2074. (doi:10.1126/science.289. 5487.2068)
14. Parmesan, C. et al. 1999 Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399, 579-583. (doi:10. 1038/21181)
15. Parmesan, C. & Yohe, G. 2003 A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42. (doi:10.1038/nature01286)
16. Zou, S. B., Cheng, G. D., Xiao, H. L., Xu, B. R. & Feng, Z. D. 2009 Holocene natural rhythms of vegetation and present potential ecology in the Western Chinese Loess Plateau. Quat. Int. 194, 55-67. (doi:10.1016/j.quaint.2008.09.009)
17. Huxman, T. E. et al. 2004 Convergence across biomes to a common rain-use efficiency. Nature 429, 651-654. (doi:10.1038/nature02561)
18. Noy-Meir, I. 1973 Desert ecosystems: environment and producers. Annu. Rev. Ecol. Evol. Syst. 4, 25-51. (doi:10.1038/nature02561)
19. Reynolds, J. F., Kemp, P. R., Ogle, K. & Fernández, R. J. 2004 Modifying the 'pulse-reserve' paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141, 194-210. (doi:10.1007/s00442-004-1524-4)
20. Midgley, G. F. & Thuiller, W. 2007 Potential vulnerability of Namaqualand plant diversity to anthropogenic climate change. J. Arid Environ. 70, 615-628. (doi:10.1016/j. jaridenv.2006.11.020)
21. Munson, S. M., Webb, R. H. & Hubbard, J. A. 2011 A comparison of methods to assess long-term changes in Sonoran Desert vegetation. J. Arid Environ. 75, 1228-1231. (doi:10.1016/j.jaridenv.2011.04.032)
22. Miranda, J. D., Armas, C., Padilla, F. M. & Pugnaire, F. I. 2011 Climatic change and rainfall patterns: effects on semi-arid plant communities of the Iberian Southeast. J. Arid Environ. 75, 1302-1309. (doi:10.1016/j. jaridenv.2011.04.022)
23. Caswell, H. 2001 Matrix population models: construction, analysis, and interpretation, 2nd edn. Sunderland, MA: Sinauer Associates.
24. Easterling, M. R., Ellner, S. & Dixon, P. 2000 Size-specific sensitivity: applying a new structured population model. Ecology 81, 694-708. (doi:10.1890/ 0012-9658(2000)081[0694:SSSAAN]2.0.CO;2)
25. van Tienderen, P. H. 2000 Elasticities and the link between demographic and evolutionary dynamics. Ecology 81, 666-679. (doi:10.1890/0012-9658(2000)081[0666:EATLBD]2.0.CO;2)
26. Morris, W. F. et al. 2008 Longevity can buffer plant and animal populations against changing climatic variability. Ecology 89, 19-25. (doi:10.1890/07-0774.1)
27. Murakami, H. & Wang, B. 2010 Future change of North Atlantic tropical cyclone tracks: projection by a 20-km-mesh global atmospheric model. J. Climate 23, 2699-2721. (doi:10.1175/2010JCLI3338.1)
28. Huxman, T. E., Barron-Gafford, G., Gerst, K. L., Angert, A. L., Tyler, A. P. & Venable, D. L. 2008 Photosynthetic resource-use efficiency and demographic variability in desert winter annual plants. Ecology 89, 1554-1563. (doi:10.1890/06-2080.1)
29. Lewontin, R. C. & Cohen, D. 1969 On population growth in a randomly varying environment. Proc. Natl Acad. Sci. USA 62, 1056-1060. (doi:10.1073/pnas. 62.4.1056)
30. Aronson, J., KIigel, J. & Shmida, A. 1993 Reproductive allocation strategies in desert and Mediterranean populations of annual plants grown with and without water-stress. Oecologia 93, 336-342. (doi:10.1007/ BF00317875)
31. Toft, C. A. 1995 A 10-year demographic study of rabbitbrush (Chrysothamnus nauseosus): growth, survival and water limitation. Oecologia 101, 1-12. (doi:10. 1007/BF00328893)
32. Koons, D. N., Pavard, S., Baudisch, A. & Metcalf, C. J. E. 2009 Is life-history buffering or liability adaptive in stochastic environments? Oikos 118, 972-980. (doi:10.1111/j.1600-0706.2009.16399.x)
33. Morris, W. F. & Doak, D. F. 2004 Buffering of life histories against environmental stochasticity: accounting for a spurious correlation between the variabilities of vital rates and their contributions to fitness. Am. Nat. 163, 579-90. (doi:10.1086/382550)
34. Doak, D. F. & Morris, W. F. 2010 Demographic compensation and tipping points in climate-induced range shifts. Nature 467, 959-962. (doi:10.1038/ nature09439)
35. Bowers, J. E. 2005 Effects of drought on shrub survival and longevity in the northern Sonoran Desert. J. Torrey Bot. Soc. 132, 421-431. (doi:10.3159/1095- 5674(2005)132[421:EODOSS]2.0.CO;2)
36. Bowers, J. E. & Turner, R. M. 2001 Dieback and episodic mortality of Cercidium microphyllum (foothill paloverde), a dominant Sonoran Desert tree. J. Torrey Bot. Soc. 128, 128-140. (doi:10.2307/3088735)
37. Miriti, M. N., Rodríguez-Buritica, S., Wright, S. J. & Howe, H. F. 2007 Episodic death across species of desert shrubs. Ecology 88, 32-36. (doi:10.1890/0012- 9658(2007)88[32:EDASOD]2.0.CO;2)
38. Bowers, J. E. & Turner, R. M. 2002 The influence of climatic variability on local populations dynamics of Cercidium microphyllum (foothill paloverde). Oecologia 130, 105-113. (doi:10.1007/s004420100779)
39. Goldberg, D. E. & Turner, R. M. 1986 Vegetation change and plant demography in permanent plots in the Sonoran Desert. Ecology 67, 695-712. (doi:10. 2307/1937693)
40. Pierson, E. A. & Turner, R. M. 1998 An 85-year study of saguaro (Carnegiea gigantea) demography. Ecology 79, 2676-2693. (doi:10.1890/0012-9658(1998)079[2676: AYSOSC]2.0.CO;2)
41. Bullock, S. H., Martijena, N. E., Webb, R. H. & Turner, R. M. 2005 Twentieth century demographic changes in cirio and cardon in Baja California, Mexico. J. Biogeogr. 32, 127-143. (doi:10.1111/j. 1365-2699.2004.01152.x)
42. Cody, M. L. 2000 Slow-motion population dynamics in Mojave Desert perennial plants. J. Veg. Sci. 11, 351-358. (doi:10.2307/3236627)
43. Nobel, P. S. & Zutta, B. R. 2005 Morphology, ecophysiology, and seedling establishment for Fouquieria splendens in the northwestern Sonoran Desert. J. Arid Environ. 62, 251-265. (doi:10.1016/j.jaridenv.2004.11.002)
44. Danzer, S. & Drezner, T. D. 2010 Demographics of more than 12,000 individuals of a keystone species in the northern Sonoran Desert since the mid-1800s. Int. J. Plant Sci. 171, 538-546. (doi:10.1086/652013)
45. Flanary, B. E. & Kletetschka, G. 2006 Analysis of telomere length and telomerase activity in tree species of various lifespans, and with age in the bristlecone pine Pinus longaeva. Rejuv. Res. 9, 61-3. (doi:10.1089/ rej.2006.9.61)
46. Vasek, F. C. 1980 Creosote bush: long-lived clones in the Mojave Desert. Am. J. Bot. 67, 246-255. (doi:10. 2307/2442649)
47. Hereford R.,Webb, R. H. & Longpre, C. I. 2006 Precipitation history and ecosystem response to multidecadal precipitation variability in the Mojave Desert region, 1893-2001. J. Arid Environ. 67, 13-34. (doi:10.1016/j. jaridenv.2006.09.01)
48. McAuliffe, J. R. & Hamerlynck, E. P. 2010 Perennial plant mortality in the Sonoran and Mojave deserts in response to severe, multi-year drought. J. Arid Environ. 74: 885-896. (doi:10.1016/j.jaridenv.2010.01.001)
49. Godínez-Á lvarez, H., Valverde, T. & Ortega-Baes, P. 2003 Demographic trends in the Cactaceae. Bot. Rev. 69, 173-203. (doi:10.1663/0006-8101(2003)069 [0173:DTITC]2.0.CO;2)
50. Meyer, S. E. & Pendleton, B. K. 2005 Factors affecting seed germination and seedling establishment of a long-lived desert shrub (Coleogyne ramosissima: Rosaceae). Plant Ecol. 178, 171-187. (doi:10.1007/ s11258-004-3038-x)
51. Herrera, C. M. 1998 Population-level estimates of interannual variability in seed production: what do they actually tell us? Oikos 82, 612-616. (doi:10.2307/ 3546384)
52. Salguero-Gómez, R. & Casper, B. B. 2010 Keeping plant shrinkage in the demographic loop. J. Ecol. 98, 312-323. (doi:10.1111/j.1365-2745.2009.01616.x)
53. Davis, S.D., Ewers, F. W., Sperry, J. S., Portwood, K. A., Crocker, M. C. & Adams, G. C. 2002 Shoot dieback during prolonged drought inCeanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure. Am. J. Bot. 89, 820-828. (doi:10.3732/ajb.89.5.820)
54. Kozlowski, T. T. 1973 Shedding of plant parts. New York, NY: Academic Press.
55. Casper, B. B., Forseth, I. N. & Wait, D. A. 2006 A stage-based study of drought response in Cryptantha flava (Boraginaceae): gas exchange, water use efficiency, and whole plant performance. Am. J. Bot. 93, 977-987. (doi:10.3732/ajb.93.7.978)
56. Salguero-Gómez, R. & Casper, B. B. 2010 A hydraulic explanation for size-specific plant shrinkage: developmental hydraulic sectoriality. New Phytol. 189, 229-240. (doi:10.1111/j.1469-8137.2010.03447.x)
57. Zanne, A. E., Sweeney, K., Sharma, M. & Orians, C. M. 2006 Patterns and consequences of differential vascular sectoriality in 18 temperate tree and shrub species. Funct. Ecol. 20, 200-206. (doi:10.1111/j. 1365-2435.2006.01101.x)
58. Schenk, H. J. 1999 Clonal splitting in desert shrubs. Plant Ecol. 141, 41-52. (doi:10.1023/A:1009895603783)
59. Miller, R. E. & Huenneke, L. F. 1996 Size decline in Larrea tridentata (creosotebush). Southwest. Nat. 41, 248-250. (doi:10.2151/jmsj.2012-A12)
60. Colling, G. & Matthies, D. 2006 Effects of habitat deterioration on population dynamics and extinction risk of an endangered, long-lived perennial herb (Scorzonera humilis). J. Ecol. 94, 959-972. (doi:10. 1111/j.1365-2745.2006.01147.x)
61. Verhulst, J., Montana, C., Mandujano, M. C. & Franco, M. 2008 Demographic mechanisms in the coexistence of two closely related perennials in a fluctuating environment. Oecologia 156, 95-105. (doi:10. 1007/s00442-008-0980-7)
62. Watson, I. W., Westoby, M. & Holm, A. M. 1997 Continuous and episodic components of demographic change in arid zone shrubs: models of two Eremophila species from Western Australia compared with published data on other species. J. Ecol. 85, 833-846. (doi:10.2307/2960605)
63. Clauss, M. & Venable, D. 2000 Seed germination in desert annuals: an empirical test of adaptive bet hedging. Am. Nat. 155, 168-186. (doi:10.1086/303314)
64. Kadmon, R. 1993 Population dynamic consequences of habitat heterogeneity: an experimental study. Ecology 74, 816-825. (doi:10.2307/1940808)
65. Aronson, J., Kigel, J., Shmida, A. & Klein, J. 1992 Adaptive phenology of desert and Mediterranean populations of annual plants grown with and without waterstress. Oecologia 89, 17-26. (doi:10.1007/BF00319010)
66. Evans, M. E. K., Ferriere, R., Kane, M. J. & Venable, D. L. 2007 Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations. Am. Nat. 169, 184-194. (doi:10.1086/510599)
67. Fox, L. R., Steele, H. N., Holl, K. D. & Fusari, M. H. 2006 Contrasting demographies and persistence of rare annual plants in highly variable environments. Plant Ecol. 183, 157-170. (doi:10.1007/s11258-005-9014-2)
68. Levine, J. M., McEachern, A. K. & Cowan, C. 2008 Rainfall effects on rare annual plants. J. Ecol. 96, 795-806. (doi:10.1111/j.1365-2745.2008.01375.x)
69. Adondakis, S. & Venable, D. 2004 Dormancy and germination in a guild of Sonoran Desert annuals. Ecology 85, 2582-2590. (doi:10.1890/03-0587)
70. Brown, G. 2002 Community composition and population dynamics in response to artificial rainfall in an undisturbed desert annual community in Kuwait. Basic Appl. Ecol. 3, 145-156. (doi:10.1078/1439- 1791-00097)
71. Sher, A., Goldberg, D. & Novoplansky, A. 2004 The effect of mean and variance in resource supply on survival of annuals from Mediterranean and desert environments. Oecologia 141, 353-362. (doi:10.1007/ s00442-003-1435-9)
72. Boeken, B. & Shachak, M. 1998 The dynamics of abundance and incidence of annual plant species during colonization in a desert. Ecography 21, 63-73. (doi:10.1111/j.1600-0587.1998.tb00394.x)
73. Levine, J. & Rees, M. 2004 Effects of temporal variability on rare plant persistence in annual systems. Am. Nat. 164, 350-363. (doi:10.1086/422859)
74. Meyer, S., Quinney, D. & Weaver, J. 2006 A stochastic population model for Lepidium papilaferum (Brassicaceae), a rare desert ephemeral with a persistent seed bank. Am. J. Bot. 93, 891-902. (doi:10.3732/ajb.93.6.891)
75. Cohen, D. 1966 Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. J. Theor. Biol. 16, 1-14. (doi:10.1016/0022-5193(67)90050-1)
76. Mizuta, R. et al. 2012 Climate simulations using MRIAGCM3.2 with 20-km grid. J. Meteorol. Soc. Jpn. 90A, 235-360.
77. Casper, B. B. 1996 Demographic consequences of drought in the herbaceous perennial Cryptantha flava: effects of density, associations with shrubs, and plant size. Oecologia 106, 144-152. (doi:10.1007/BF00328593)
78. Peek, M. S. & Forseth, I. N. 2005 Non-destructive estimation of lateral root distribution in an aridland perennial. Plant Soil 273, 211-217. (doi:10.1007/ s11104-004-7600-z)
79. Casper, B. B. 1981 Fixed rates of random ovule abortion in Cryptantha flava (Boraginaceae) and its possible relation to seed dispersal. Ecology 62, 866-869. (doi:10.2307/1937752)
80. Casper, B. B., Forseth, I. N., Kempenich, H., Seltzer, S. & Xavier, K. 2001 Drought prolongs leaf life span in the herbaceous desert perennial Cryptantha flava. Funct. Ecol. 15, 740-747. (doi:10.1046/j.0269-8463. 2001.00583.x)
81. Salguero-Gómez, R. & Casper, B. B. 2010 Introducing short roots in a desert perennial: anatomy and spatiotemporal foraging responses to increased precipitation. New Phytol. 191, 173-183. (doi:10.1111/j. 1469-8137.2011.03679.x)
82. Marhold, K. 2011 Brassicaceae. In Euro{thorn}Med Plantbase: the information resource for Euro-Mediterranean plant diversity. See http://www.emplantbase.org/home. html.
83. Cooke, J., Groves, R. H. & Ash, J. 2011 The distribution of Carrichtera annua in Australia: introduction, spread and probable limits. Rangeland J. 33, 23-35. (doi:10.1071/RJ10001)
84. Danin, A. 2006 Flora of Israel online. See http://flora. huji.ac.il/browse.asp?lang=en.
85. Gutterman, Y., Gendler, T. & Huang, Z.-Y. 2007 Plant dispersal strategies, seed bank distribution and germination of Neger Desert species. In Seeds: biology, development and ecology (eds S. Adkins, S. Ashmore & S. C. Navie), pp. 407-415. Brisbane, Australia: CAB International.
86. Lucas, R. W., Forseth, I. N. & Casper, B. B. 2008 Using rainout shelters to evaluate climate change effects on the demography of Cryptantha flava. J. Ecol. 96, 514-522. (doi:10.1111/j.1365-2745.2007. 01350.x)
87. Sternberg, M. et al. 2011 The use and misuse of climatic gradients for evaluating climate impact on dryland ecosystems-an example for the solution of conceptual problems. In Gradients in drylands: linking patterns and processes and their consequences for biodiversity (eds M. Veste, A. Linstädter & S. W. Breckle), pp. 361-374. New York, NY: Springer.
88. Metz, J., Liancourt, P., Kigel, J., Harel, D., Sternberg, M. & Tielbörger, K. 2010 Plant survival in relation to seed size along environmental gradients: a long-term study from semi-arid and Mediterranean annual plant communities. J. Ecol. 98, 697-704. (doi:10.1111/j. 1365-2745.2010.01652.x)
89. Harel, D., Holzapfel, C. & Sternberg, M. 2011 Seed mass and dormancy of annual plant populations and communities decreases with aridity and rainfall predictability. Basic Appl. Ecol. 12, 674-684. (doi:10.1016/j. baae.2011.09.003)
90. Caswell, H. & Trevisan, M. C. 1994 Sensitivity analysis of periodic matrix models. Ecology 75, 1299-1303. (doi:10.2307/1937455)
91. Li, S. L., Yu, F. H., Werger, M. J. A., Dong, M. & Zuidema, P. A. 2011 Habitat-specific demography across dune fixation stages in a semi-arid sandland: understanding the expansion, stabilization and decline of a dominant shrub. J. Ecol. 99, 610-620. (doi:10.1111/j. 1365-2745.2010.01777.x)
92. Ramula, S., Rees, M. & Buckley, Y. M. 2009 Integral projection models perform better for small demographic data sets than matrix projection models: a case study of two perennial herbs. J. Appl. Ecol. 46, 1048-1053. (doi:10.1111/j.1365- 2664.2009.01706.x)
93. Salguero-Gómez, R. & Plotkin, J. B. 2010 Matrix dimensions bias demographic inferences: implications for comparative plant demography. Am. Nat. 176, 710-722. (doi:10.1086/657044)
94. Ellner, S. P. & Rees, M. 2006 Integral projection models for species with complex demography. Am. Nat. 167, 410-428. (doi:10.1086/499438)
95. Smith, M., Caswell, H. & Mettler-Cherry, P. 2005 Stochastic flood and precipitation regimes and the population dynamics of a threatened floodplain plant. Ecol. Appl. 15, 1036-1052. (doi:10.1890/04-0434)
96. Ellner, S. P. & Rees, M. 2007 Stochastic stable population growth in integral projection models: theory and application. J. Math. Biol. 54, 227-256. (doi:10.1007/ s00285-006-0044-8)
97. Sokal, R. R. & Rohlf, F. J. 1995 Biometry: the principles and practices in statistics in biological sciences. New York, NY: WH Freeman.
98. Hunter, C.M., Caswell, H., Runge, M. C., Regehr, E. V., Amstrup, S.C.& Stirling, I. 2010 Climate change threatens polar bear populations: a stochastic demographic analysis. Ecology 91, 2883-2897. (doi:10.1890/09-1641.1)
99. de Kroon, H., Plaisier, A., van Groenendael, J. & Caswell, H. 1986 Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67, 1427-1431. (doi:10.2307/1938700)
100. Horvitz, C. C., Ehrlén, J. & Matlaga, D. 2010 Contextdependent pollinator limitation in stochastic environments: can increased seed set overpower the cost of reproduction in an understorey herb. J. Ecol. 98, 268-278. (doi:10. 1111/j.1365-2745.2009.01628.x)
101. R Development Core Team. 2010 R: a language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing.
102. Tuljapurkar, S. 1989 An uncertain life: demography in random environments. Theor. Popul. Biol. 35, 227-294. (doi:10.1016/0040-5809(89)90001-4)
103. Smart, K., Archibald, S., Scholes, R. J., Reyers, B., Nickless, A. & Knowles, T. In press. Ecosystem service trade-offs in drylands: examples from the Eastern Cape of South Africa. Phil. Trans. R. Soc. B.
104. Dougill, A. J., Stringer, L. C., Leventon, J., Riddell, M., Rueff, H., Spracklen, D. V. & Butt, E. 2012 Lessons from community-based payment for ecosystem service schemes: from forests to rangelands. Phil. Trans. R. Soc. B 367, 3178-3190. (doi:10.1098/rstb.2011.0418)
105. Grace, O. M. 2011 Current perspectives on the economic botany of the genus Aloe L. (Xanthorrhoeaceae). S Afr. J. Bot. 77, 980-987. (doi:10.1016/j.sajb.2011.07.002)
106. Hultine, K. R., Cable, W. L., Burgess, S. S. O. & Williams, D. G. 2003 Hydraulic redistribution by deep roots of a Chihuahuan Desert phreatophyte. Tree Physiol. 23, 353-360. (doi:10.1093/treephys/23.5.353)
107. Schwinning, S., Starr, B. I. & Ehleringer, J. R. 2003 Dominant cold desert plants do not partition warm season precipitation by event size. Oecologia 136, 252-260. (doi:10.1007/s00442-003-1255-y)
108. Sperry, J. S., Perry, A. H. & Sullivan, J. E. M. 1991 Pit membrane degradation and air-embolism formation in ageing xylem vessels of Populus tremuloides Michx. J. Exp. Bot. 42, 1399-406. (doi:10.1093/jxb/42.11.1399)
109. Jongejans, E. & de Kroon, H. 2005 Space versus time variation in the population dynamics of three cooccurring perennial herbs. J. Ecol. 93, 681-692. (doi:10.1111/j.1365-2745.2005.01003.x)
110. Escolar, C., Martínez, I., Bowker, M. A. & Maestre, F. T. 2012 Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Phil. Trans. R. Soc. B 367, 3087-3099. (doi:10.1098/ rstb.2011.0344)
111. Gomaa, N. H. & Pico, X. F. 2011 Seed germination, seedling traits, and seed bank of the tree Moringa peregrina (Moringaceae) in a hyper-arid environment. Am. J. Bot. 98, 1024-1030. (doi:10.3732/ajb.1000051)