The species-energy hypothesis as a mechanism for species richness patterns

doi:10.3724/SP.J.1003.2009.09161

Abstract

Abstract:

Large-scale patterns of species diversity are one of the most important and attractive issues for ecology and biogeography. Many hypotheses have been proposed to understand the mechanisms that shape and maintain the diversity patterns. Among them, the energy hypothesis, which focuses on the influence of energy on species diversity, has generated the most attention. Based on the forms of energy and the mechanisms of energy effects on diversity patterns, five versions of the energy hypothesis have been recognized, i.e. productivity hypothesis, water-energy dynamic hypothesis, ambient energy hypothesis, freezing tolerance hypothesis, and metabolic theory of ecology. The current paper reviews the development of the energy hypothesis, and then presents the context, energy forms, variables, predictions, and underlying mechanisms for the five versions of the energy hypothesis. Furthermore, we discuss the advantages, shortcomings, and challenges of each version of the energy hypothesis.

Key words: species diversity, kinetic energy, thermal energy, productivity hypothesis, water-energy dynamic hypothesis, ambient energy hypothesis, freezing tolerance hypothesis, metabolic theory of ecology

Zhiheng Wang, Zhiyao Tang, Jingyun Fang. The species-energy hypothesis as a mechanism for species richness patterns[J]. Biodiv Sci, 2009, 17(6): 613-624.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.3724/SP.J.1003.2009.09161

https://www.biodiversity-science.net/EN/Y2009/V17/I6/613

Figures/Tables 3

Fig. 1 Relationships between species richness and actual evapotranspiration (AET) for North American trees (A, from Currie & Paquin, 1987) and global birds (B, from Hawkins et al., 2003a). AET is a surrogate of net primary productivity (NPP).

Fig. 2 Relationships between species richness of North American vertebrates and ambient energy measured by potential evapotranspiration (PET) (from Currie, 1991).

Fig. 3 Collective mechanisms for influences of thermal kinetic energy and potential energy on species diversity (from Allen et al., 2007).

References 117

[1]	Abramsky Z, Rosenzweig ML (1984) Tilman's predicted productivity-diversity relationship shown by desert rodents. Nature, 309, 150-151. DOI URL PMID
[2]	Adams JM, Woodward FI (1989) Patterns in tree species richness as a test of the glacial extinction hypothesis. Nature, 339, 699-701.
[3]	Allcock KG, Hik DS (2003) What determines disturbance-productivity-diversity relationships? The effect of scale, species and environment on richness patterns in an Australian woodland. Oikos, 102, 173-185.
[4]	Allen AP, Brown JH, Gillooly JF (2002) Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science, 297, 1545-1548. URL PMID
[5]	Allen AP, Brown JH, Gillooly JF (2003) Response to comment on “global biodiversity, biochemical kinetics, and the energetic-equivalence rule”. Science, 299, 346. DOI URL PMID
[6]	Allen AP, Gillooly JF, Brown JH (2007) Recasting the species-energy hypothesis: the different roles of kinetic and potential energy in regulating biodiversity, In: Scaling Biodiversity (eds Storch D, Marquet PA, Brown JH), pp. 283-299. Cambridge University Press, Cambridge.
[7]	Andre HM, Ducarme X, Lebrun P (2002) Soil biodiversity: myth, reality or conning? Oikos, 96, 3-24.
[8]	Barthlott W, Lauer W, Placke A (1996) Global distribution of species diversity in vascular plants: towards a world map of phytodiversity. Erdkunde, 50, 317-327.
[9]	Blackburn T, Gaston K (1996) A sideways look at patterns in species richness, or why there are so few species outside the tropics. Biodiversity Letters, 3, 44-53.
[10]	Brown J (1981) Two decades of homage to Santa Rosalia: toward a general theory of diversity. Integrative and Comparative Biology, 21, 877-888.
[11]	Brown JH, Lomolino MV (1998) Biogeography, 2nd edn. Sinauer Associates, Sunderland, MA.
[12]	Brown JH, Allen AP, Gillooly JF (2003) Response: heat and biodiversity. Science, 299, 512-513. DOI URL PMID
[13]	Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789.
[14]	Chave J (2004) Neutral theory and community ecology. Ecology Letters, 7, 241-253.
[15]	Clarke A, Gaston KJ (2006) Climate, energy and diversity. Proceedings of the Royal Society B: Biological Sciences, 273, 2257-2266. URL PMID
[16]	Colwell RK, Rahbek C, Gotelli NJ (2004) The mid-domain effect and species richness patterns: what have we learned so far? The American Naturalist, 163, E1-E23. DOI URL PMID
[17]	Connell JH, Orias E (1964) The ecological regulation of species diversity. The American Naturalist, 98, 399-414.
[18]	Cousins SH (1989) Species richness and the energy theory. Nature, 340, 350-351.
[19]	Currie DJ, Francis AP (2004) Regional versus climatic effect on taxon richness in angiosperms: reply to Qian and Ricklefs. The American Naturalist, 163, 780-785.
[20]	Currie DJ, Paquin V (1987) Large-scale biogeographical patterns of species richness of trees. Nature, 329, 326-327.
[21]	Currie DJ (1991) Energy and large-scale patterns of animal- and plant-species richness. The American Naturalist, 137, 27-49.
[22]	Currie DJ, Mittelbach GG, Cornell HV, Field R, Guegan JF, Hawkins BA, Kaufman DM, Kerr JT, Oberdorff T, O’Brien E, Turner JRG (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecology Letters, 7, 1121-1134.
[23]	Davies RG, Orme CDL, Storch D, Olson VA, Thomas GH, Ross SG, Ding TS, Rasmussen PC, Bennett PM, Owens IPF, Blackburn T, Gaston KJ (2007) Topography, energy and the global distribution of bird species richness. Proceedings of the Royal Society B: Biological Sciences, 274, 1189-1197. DOI URL PMID
[24]	Evans KL, James NA, Gaston KJ (2006) Abundance, species richness and energy availability in the North American avifauna. Global Ecology and Biogeography, 15, 372-385.
[25]	Evans KL, Newson SE, Storch D, Greenwood JJD, Gaston KJ (2008) Spatial scale, abundance and the species-energy relationship in British birds. Journal of Animal Ecology, 77, 395-405.
[26]	Evans KL, Warren PH, Gaston KJ (2005) Species-energy relationships at the macroecological scale: a review of the mechanisms. Biological Reviews, 80, 1-25. DOI URL PMID
[27]	Fang JY (方精云), Kanzaki M, Wang XP (王襄平), Yoda K, Sun SZ (孙世洲), Shimota K (2004) Community structure of alpine sparse vegetation and effects of microtopography in Pushila, Everest-Choyu region, Tibet, China. Biodiversity Science (生物多样性), 12, 190-199. (in Chinese with English abstract)
[28]	Fang JY, Yoda K (1991) Climate and vegetation of China V: effects of climate factors on the upper limit of distribution of evergreen broadleaf forest. Ecological Research, 6, 113-125.
[29]	Field R, O’Brien EM, Whittaker RJ (2005) Global models for predicting woody plant richness from climate: development and evaluation. Ecology, 86, 2263-2277.
[30]	Francis AP, Currie DJ (2003) A globally consistent richness-climate relationship for angiosperms. The American Naturalist, 161, 523-536. DOI URL PMID
[31]	Fraser RH, Currie DJ (1996) The species richness-energy hypothesis in a system where historical factors are thought to prevail: coral reefs. The American Naturalist, 148, 138-159.
[32]	Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proceedings of the National Academy of Sciences, USA, 105, 7774-7778.
[33]	Gaston KJ (2000) Global patterns in biodiversity. Nature, 405, 220-227. DOI URL PMID
[34]	Gillooly JF, Allen AP (2007) Linking global patterns in biodiversity to evolutionary dynamics using metabolic theory. Ecology, 88, 1890-1894. DOI URL PMID
[35]	Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science, 293, 2248-2251. DOI URL PMID
[36]	Grace JB, Anderson TM, Smith MD, Seabloom E, Andelman SJ, Meche G, Weiher E, Allain LK, Jutila H, Sankaran M, Knops J, Ritchie M, Willig MR (2007) Does species diversity limit productivity in natural grassland communities? Ecology Letters, 10, 680-689. DOI URL PMID
[37]	Guegan J-F, Lek S, Oberdorff T (1998) Energy availability and habitat heterogeneity predict global riverine fish diversity. Nature, 391, 382-384.
[38]	Guo Q, Berry WL (1998) Species richness and biomass: dessection of the hump-shaped relationships. Ecology, 79, 2555-2559.
[39]	Gurevitch J, Scheiner S, Fox G (2002) The Ecology of Plants. Sinauer Associates, Inc., Sunderland, MA.
[40]	Hawkins BA (2001) Ecology’s oldest pattern? Trends in Ecology and Evolution, 16, 470.
[41]	Hawkins BA, Albuquerque FS, Araújo MB, Beck J, Bini LM, Cabrero-Sanúdo FJ, Castro-Parga I, Diniz-Filho JAF, Ferrer-Castán D, Field R, Gómez J, Hortal J, Kerr JT, Kitching IJ, León-Cortés JL, Lobo JM, Montoya D, Moreno JC, Olalla-Tárraga M, Pausas JG, Qian H, Rahbek C, Rodríguez M, Sanders NJ, Williams P (2007a) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology, 88, 1877-1888. DOI URL PMID
[42]	Hawkins BA, DeVries PJ (2009) Tropical niche conservatism and the species richness gradient of North American butterflies. Journal of Biogeography, 36, 1698-1711.
[43]	Hawkins BA, Diniz-Filho JAF, Bini LM, Araújo MB, Field R, Hortal J, Kerr JT, Rahbek C, Rodríguez MA, Sanders NJ (2007b) Metabolic theory and diversity gradients: where do we go from here? Ecology, 88, 1898-1902. DOI URL PMID
[44]	Hawkins BA, Diniz-Filho JAF, Soeller SA (2005) Water links the historical and contemporary components of the Australian bird diversity gradient. Journal of Biogeography, 32, 1035-1042.
[45]	Hawkins BA, Field R, Cornell HV, Currie DJ, Guegan J-F, Kaufman DM, Kerr JT, Mittelbach GG, Oberdorff T, O’Brien EM, Porter EE, Turner JRG (2003b) Energy, water, and broad-scale geographic patterns of species richness. Ecology, 84, 3105-3117.
[46]	Hawkins BA, Montoya D, Rodríguez M, Olalla-Tárraga M, Zavala M (2007c) Global models for predicting woody plant richness from climate: comment. Ecology, 88, 255-259. DOI URL PMID
[47]	Hawkins BA, Porter EE (2003) Relative influences of current and historical factors on mammal and bird diversity patterns in deglaciated North America. Global Ecology and Biogeography, 12, 475-481.
[48]	Hawkins BA, Porter EE, Diniz-Filho JAF (2003a) Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology, 84, 1608-1623.
[49]	Hoffmann MD, Dodson SI (2005) Land use, primary productivity, and lake area as descriptors of zooplankton diversity. Ecology, 86, 255-261.
[50]	Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton.
[51]	Hunt G, Cronin TM, Roy K (2005) Species-energy relationship in the deep sea: a test using the quaternary fossil record. Ecology Letters, 8, 739-747.
[52]	Hurlbert AH, Haskell JP (2003) The effect of energy and seasonality on avian species richness and community composition. The American Naturalist, 161, 83-97. DOI URL PMID
[53]	Hurlbert AH (2004) Species-energy relationships and habitat complexity in bird communities. Ecology Letters, 7, 714-720.
[54]	Huston MA (2003) Heat and biodiversity. Science, 299, 512. DOI URL PMID
[55]	Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist, 93, 145-159.
[56]	Jetz W, Rahbek C (2002) Geographic range size and determinants of avian species richness. Science, 297, 1548-1551. DOI URL PMID
[57]	Kaspari M, O’Donnell S, Kercher JR (2000) Energy, density, and constraints to species richness: ant assemblages along a productivity gradient. The American Naturalist, 155, 280-293. DOI URL PMID
[58]	Kreft H, Jetz W (2007) Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences, USA, 104, 5925-5930.
[59]	Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist, 142, 911-927. DOI URL PMID
[60]	Latham RE, Ricklefs RE (1993) Global patterns of tree species richness in moist forests: energy-diversity theory does not account for variation in species richness. Oikos, 67, 325-333.
[61]	Lennon JJ, Greenwood JJD, Turner JRG (2000) Bird diversity and environmental gradients in Britain: a test of the species-energy hypothesis. Journal of Animal Ecology, 69, 581-598.
[62]	Lieth H, Box E (1972) Evapotranspiration and primary productivity: CW Thornthwaite memorial model. Publications in Climatology, 25, 37-46.
[63]	Lieth H (1975) Modeling the primary productivity of the world. Primary Productivity of the Biosphere, 14, 237-263.
[64]	Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proceedings of the National Academy of Sciences, USA, 95, 5632-5636.
[65]	Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos, 91, 3-17.
[66]	Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science, 294, 804-808. DOI URL PMID
[67]	MacPherson E, Duarte CM (1994) Patterns in species richness, size, and latitudinal range of East Atlantic fishes. Ecography, 17, 242-248.
[68]	McCain CM (2004) The mid-domain effect applied to elevational gradients: species richness of small mammals in Costa Rica. Journal of Biogeography, 31, 19-31.
[69]	McCain CM (2005) Elevational gradients in diversity of small mammals. Ecology, 86, 366-372.
[70]	McCain CM (2007) Area and mammalian elevational diversity. Ecology, 88, 76-86. DOI URL PMID
[71]	Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between species richness and productivity? Ecology, 82, 2381-2396.
[72]	Montoya D, Rodríguez MA, Zavala MA, Hawkins BA (2007) Contemporary richness of Holarctic trees and the historical pattern of glacial retreat. Ecography, 30, 173-182.
[73]	Mulder CPH, Bazeley-White E, Dimitrakopoulos PG, Hector A, Scherer-Lorenzen M, Schmid B (2004) Species evenness and productivity in experimental plant communities. Oikos, 107, 50-63.
[74]	O’Brien EM (1993) Climatic gradients in woody plant species richness: towards an explanation based on an analysis of southern Africa’s woody flora. Journal of Biogeography, 20, 181-198.
[75]	O’Brien EM (1998) Water-energy dynamics, climate, and prediction of woody plant species richness: an interim general model. Journal of Biogeography, 25, 379-398.
[76]	O’Brien EM (2006) Biological relativity to water-energy dynamics. Journal of Biogeography, 33, 1868-1888.
[77]	O’Brien EM, Whittaker RJ, Field R (1998) Climate and woody plant diversity in southern Africa: relationships at species, genus and family levels. Ecography, 21, 495-509.
[78]	Öpik H, Rolfe S (2005) The Physiology of Flowering Plants. Cambridge University Press, Cambridge, UK.
[79]	Palmer M (1994) Variation in species richness: towards a unification of hypotheses. Folia Geobotanica, 29, 511-530.
[80]	Prentice IC, Cramer W, Harrison SP, Leemans R, Monserud RA, Solomon AM (1992) A global biome model based on plant physiology and dominance, soil properties and climate. Journal of Biogeography, 19, 117-134.
[81]	Preston FW (1962) The canonical distribution of commonness and rarity, Part I. Ecology, 43, 185-215.
[82]	Preston FW (1968) On modeling islands. Ecology, 49, 592-594.
[83]	Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature, 407, 180-182. DOI URL PMID
[84]	Rajaniemi TK (2003) Explaining productivity-diversity relationships in plants. Oikos, 101, 449-457.
[85]	Reyjol Y, Hugueny B, Pont D, Bianco PG, Beier U, Caiola N, Casals F, Cowx I, Economou A, Ferreira T, Haidvogl G, Noble R, de Sostoa A, Vigneron T, Virbickas T (2007) Patterns in species richness and endemism of European freshwater fish. Global Ecology and Biogeography, 16, 65-75.
[86]	Ricklefs RE (2007) History and diversity: explorations at the intersection of ecology and evolution. The American Naturalist, 170, S56-S70. DOI URL PMID
[87]	Rosenzweig ML (1995) Species Diversity in Space and Time. Cambridge University Press, Cambridge, UK.
[88]	Sakai A, Malla SB (1981) Winter hardiness of tree species at high altitudes in the east Himalaya, Nepal. Ecology, 62, 1288-1298.
[89]	Sakai A, Weiser CJ (1973) Freezing resistance of trees in North America with reference to tree regions. Ecology, 54, 118-126.
[90]	Sakai A (1979) Freezing avoidance mechanism of primordial shoots of conifer buds. Plant and Cell Physiology, 20, 1381-1390.
[91]	Sanders NJ, Lessard J-P, Fitzpatrick MC, Dunn RR (2007) Temperature, but not productivity or geometry, predicts elevational diversity gradients in ants across spatial grains. Global Ecology and Biogeography, 16, 640-649.
[92]	Schall J, Pianka E (1977) Species densities of reptiles and amphibians on the Iberian Peninsuls. Doñana, Acta Vertebrata, 4, 27-34.
[93]	Schall JJ, Pianka ER (1978) Geographical trends in numbers of species. Science, 201, 679-686. DOI URL PMID
[94]	Schmid B (2002) The species richness-productivity controversy. Trends in Ecology and Evolution, 17, 113-114.
[95]	Srivastava D, Lawton J (1998) Why more productive sites have more species: an experimental test of theory using tree-hole communities. The American Naturalist, 152, 510-529.
[96]	Storch D (2003) Comment on “global biodiversity, biochemical kinetics, and the energetic-equivalence rule”. Science, 299, 346b.
[97]	Storch D, Davies RG, Zajicek S, Orme CDL, Olson V, Thomas GH, Ding T-S, Rasmussen PC, Ridgely RS, Bennett PM, Blackburn TM, Owens IPF, Gaston KJ (2006) Energy, range dynamics and global species richness patterns: reconciling mid-domain effects and environmental determinants of avian diversity. Ecology Letters, 9, 1308-1320. DOI URL PMID
[98]	Terborgh J, Winter B (1980) Some causes of extinction, In: Conservation Biology: An Evolutionary-Ecological Perspective (eds Soule ME, Wilcox BA), pp. 119-134. Sinauer Associates, Inc., Sunderland, MA
[99]	Thornthwaite CW, Hare FK (1955) Climatic classification in forest. Unasylva, 9, 51-59.
[100]	Tilman D, Pacala S (1993) The maintenance of species richness in plant communities. In: Species Diversity in Ecological Communities: Historical and Geographical Perspectives (eds Ricklefs RE, Schluter D). University of Chicago Press, Chicago.
[101]	Tilman D (1982) Resource Competition and Community Structure. Princeton University Press, Princeton.
[102]	Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science, 294, 843-845. DOI URL PMID
[103]	Turner JRG (2004) Explaining the global biodiversity gradient: energy, area, history and natural selection. Basic and Applied Ecology, 5, 435-448.
[104]	Turner JRG, Gatehouse CM, Corey CA (1987) Does solar energy control organic diversity? Butterflies, moths and the British climate. Oikos, 48, 195-205.
[105]	Turner JRG, Lennon JJ, Lawrenson JA (1988) British bird species distributions and the energy theory. Nature, 335, 539-541.
[106]	Walker SC, Cyr H (2007) Testing the standard neutral model of biodiversity in lake communities. Oikos, 116, 143-155.
[107]	Wang ZH (王志恒), Tang ZY (唐志尧), Fang JY (方精云) (2009) Metabolic theory of ecology: an explanation for species richness patterns based on the metabolic processes of organisms. Biodiversity Science (生物多样性), 17, 625-634. (in Chinese with English abstract)
[108]	Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP, Parmenter R (1999) The relationship between productivity and species richness. Annual Review of Ecology and Systematics, 30, 257-300.
[109]	Weiher E (1999) The combined effects of scale and productivity on species richness. Journal of Ecology, 87, 1005-1011.
[110]	Whittaker RJ, Nogues-Bravo D, Araujo MB (2007) Geographical gradients of species richness: a test of the water-energy conjecture of Hawkins et al. (2003) using European data for five taxa. Global Ecology and Biogeography, 16, 76-89.
[111]	Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology, and species richness. Trends in Ecology and Evolution, 19, 639-644. DOI URL PMID
[112]	Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annual Review of Ecology Evolution and Systematics, 34, 273-309.
[113]	Woodward FI (1987) Climate and Plant Distribution. Cambridge University Press, Cambridge.
[114]	Wright DH (1983) Species-energy theory: an extension of species-area theory. Oikos, 41, 496-506.
[115]	Yang YH (杨元合), Rao S (饶胜), Hu HF (胡会峰), Chen AP (陈安平), Ji CJ (吉成均), Zhu B (朱彪), Zuo WY (左闻韵), Li XR (李轩然), Shen HH (沈海花), Wang ZH (王志恒), Tang YH (唐艳鸿), Fang JY (方精云) (2004) Plant species richness of alpine grasslands in relation to environmental factors and biomass on the Tibetan Plateau. Biodiversity Science (生物多样性), 12, 200-205. (in Chinese with English abstract)
[116]	Zhao S, Fang J, Peng C, Tang Z, Piao S (2006) Patterns of fish species richness in China’s lakes. Global Ecology and Biogeography, 15, 386-394.
[117]	Zobel M, Pärtel M (2008) What determines the relationship between plant diversity and habitat productivity? Global Ecology and Biogeography, 17, 679-684.