1932

Abstract

All species within ecosystems contribute to regulating carbon cycling because of their functional integration into food webs. Yet carbon modeling and accounting still assumes that only plants, microbes, and invertebrate decomposer species are relevant to the carbon cycle. Our multifaceted review develops a case for considering a wider range of species, especially herbivorous and carnivorous wild animals. Animal control over carbon cycling is shaped by the animals’ stoichiometric needs and functional traits in relation to the stoichiometry and functional traits of their resources. Quantitative synthesis reveals that failing to consider these mechanisms can lead to serious inaccuracies in the carbon budget. Newer carbon-cycle models that consider food-web structure based on organismal functional traits and stoichiometry can offer mechanistically informed predictions about the magnitudes of animal effects that will help guide new empirical research aimed at developing a coherent understanding of the interactions and importance of all species within food webs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-011720-104730
2020-11-02
2024-06-20
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/51/1/annurev-ecolsys-011720-104730.html?itemId=/content/journals/10.1146/annurev-ecolsys-011720-104730&mimeType=html&fmt=ahah

Literature Cited

  1. Allen AP, Gillooly JF, Brown JH 2005. Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19:202–13
    [Google Scholar]
  2. Atwood TB, Hammill E, Greig HS, Kratina P, Shurin JB et al. 2013. Predator-induced reductions of freshwater carbon dioxide emissions. Nat. Geosci. 6:191–94
    [Google Scholar]
  3. Atwood TB, Madin EMP, Harborne AR, Hammill E, Luiz OJ et al. 2018. Predators shape sedimentary organic carbon storage in a coral reef ecosystem. Front. Ecol. Environ. 6:110
    [Google Scholar]
  4. Babst BA, Ferrieri RA, Thorpe MR, Orians CM 2008. Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol. Exp. Appl 128:117–25
    [Google Scholar]
  5. Bagchi S, Roy S, Maitra A, Sran RS 2017. Herbivores suppress soil microbes to influence carbon sequestration in the grazing ecosystem of Trans-Himalaya. Agr. Ecosyst. Environ. 239:199–206
    [Google Scholar]
  6. Bar-On YM, Phillips R, Milo R 2018. The biomass distribution on Earth. PNAS 115:6506–11
    [Google Scholar]
  7. Bassar RD, Ferriere R, López-Sepulcre A, Marshall MC, Travis J et al. 2012. Direct and indirect ecosystem effects of evolutionary adaptation in the Trinidadian Guppy (Poecilia reticulata). Am. Nat. 180:167–85
    [Google Scholar]
  8. Bell ATC, Murray DL, Prater C, Frost PC 2019. Fear and food: effect of predator-derived chemical cues and stoichiometric food quality on Daphnia. Limnol. . Oceanogr 64:1706–15
    [Google Scholar]
  9. Bernays EA. 1997. Evolution of feeding behavior in insect herbivores. BioScience 48:35–44
    [Google Scholar]
  10. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR et al. 2010. Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–613
    [Google Scholar]
  11. Bodelier PL, Stomp M, Santamaria L, Klaassen M, Laanbroek HJ 2006. Animal-plant-microbe interactions: Direct and indirect effects of swan foraging behavior modulate methane cycling in temperate shallow wetlands. Oecologia 149:233–44
    [Google Scholar]
  12. Bonaglia S, Brüchert V, Callac N, Vicenzi A, Chi Fru E et al. 2017. Methane fluxes from coastal sediments are enhanced by macrofauna. Sci. Rep. 7:13145
    [Google Scholar]
  13. Bonan GB, Doney SC. 2018. Climate, ecosystems, and planetary futures: the challenge to predict life in Earth system models. Science 359:eaam8328
    [Google Scholar]
  14. Brodie JF, Gibbs HK. 2005. Bushmeat hunting as climate threat. Science 326:364–65
    [Google Scholar]
  15. Brose U. 2010. Body-mass constraints on foraging behavior determine population and food-web dynamics. Funct. Ecol. 24:28–34
    [Google Scholar]
  16. Brose U, Blanchard JL, Eklöf A, Galiana N, Hartvig M et al. 2017. Predicting the consequences of species loss using size‐structured biodiversity approaches. Biol. Rev. 92:684–97
    [Google Scholar]
  17. Brousseau P‐M, Gravel D, Handa IT 2019. Traits of litter‐dwelling forest arthropod predators and detritivores covary spatially with traits of their resources. Ecology 100:e02815
    [Google Scholar]
  18. Buchkowski RW, Leroux SJ, Schmitz OJ 2019. Microbial and animal nutrient limitation change the distribution of nitrogen within coupled green and brown food chains. Ecology 100:e02674
    [Google Scholar]
  19. Butterfield NJ. 2011. Animals and the invention of the Phanerozoic Earth system. Trends Ecol. Evol. 26:81–7
    [Google Scholar]
  20. Cahoon SMP, Sullivan PF, Post E, Welker JM 2012. Large herbivores limit CO2 uptake and suppress carbon cycle responses to warming in West Greenland. Glob. Change Biol. 18:469–79
    [Google Scholar]
  21. Carpenter SR, Chisolm SW, Krebs CJ, Schindler DW, Wright RF 1995. Ecosystem experiments. Science 269:324–27
    [Google Scholar]
  22. Chalcraft DR, Resetarits WJ. 2003. Mapping functional similarity of predators on the basis of trait similarities. Am. Nat. 162:390–402
    [Google Scholar]
  23. Cherif M, Loreau M. 2013. Plant-herbivore-decomposer stoichiometric mismatches and nutrient cycling in ecosystems. Proc. R. Soc. B 280:20122453
    [Google Scholar]
  24. Chomel M, Lavallee JM, Alvarez‐Segura N, de Castro F, Rhymes JM et al. 2019. Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity. Glob. Change Biol. 25:3549–61
    [Google Scholar]
  25. Clark KL, Skowronski N, Hom J 2010. Invasive insects impact forest carbon dynamics. Glob. Change Biol. 16:88–101
    [Google Scholar]
  26. Codron D, Hofmann RR, Clauss M 2019. Morphological and physiological adaptations for browsing and grazing. The Ecology of Browsing and Grazing II IJ Gordon, HHT Prins pp. 81125 Cham, Switz.: Springer Int. Publ.
    [Google Scholar]
  27. Cohen Y, Pastor J, Vincent TL 2000. Evolutionary strategies and nutrient cycling in ecosystems. Evol. Ecol. Res. 2:719–43
    [Google Scholar]
  28. Cole L, Bardgett RD, Ineson P 2000. Enchytraeid worms (Oligochaeta) enhance mineralization of carbon in organic upland soils. Eur. J. Soil Sci. 51:185–92
    [Google Scholar]
  29. Dangal SRS, Tian H, Lu C, Ren W, Pan S et al. 2017. Integrating herbivore population dynamics into a global land biosphere model: plugging animals into the Earth system. J. Adv. Model. Earth Sys. 9:2920–45
    [Google Scholar]
  30. Daufresne T, Loreau M. 2001. Plant-herbivore interactions and ecological stoichiometry: When do herbivores determine plant nutrient limitation?. Ecol. Lett. 4:196–206
    [Google Scholar]
  31. Davies AB, Asner GP. 2019. Elephants limit aboveground carbon gains in African savannas. Glob. Change Biol. 25:1368–82
    [Google Scholar]
  32. De Deyn GB, Cornelissen JHC, Bardgett RD 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol. Lett. 11:516–31
    [Google Scholar]
  33. de Mazancourt C, Loreau M, Abbadie L 1998. Grazing optimization and nutrient cycling: When do herbivores enhance plant production?. Ecology 79:2242–52
    [Google Scholar]
  34. Deraison H, Badenhausser I, Börger L, Gross N 2015. Herbivore effect traits and their impact on plant community biomass: an experimental test using grasshoppers. Funct. Ecol. 29:650–61
    [Google Scholar]
  35. Devlin SP, Saarenheimo J, Syväranta J, Jones RI 2015. Top consumer abundance influences lake methane flux. Nat. Commun. 6:8787
    [Google Scholar]
  36. Dobson A, Lodge D, Alder J, Cumming GS, Keymer J et al. 2006. Habitat loss, trophic collapse and the decline of ecosystem services. Ecology 87:1915–24
    [Google Scholar]
  37. Ellis NM, Leroux SJ. 2017. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests. Funct. Ecol. 31:790–801
    [Google Scholar]
  38. Elschot K, Bakker JP, Temmerman S, van de Koppel J, Bouma TJ 2015. Ecosystem engineering by large grazers enhances carbon stocks in a tidal salt marsh. Mar. Ecol. Prog. Ser. 537:9–21
    [Google Scholar]
  39. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J et al. 2011. Trophic downgrading of planet Earth. Science 333:301–6
    [Google Scholar]
  40. Falk JM, Schmidt NM, Christensen TR, Ström L 2015. Large herbivore grazing affects the vegetation structure and greenhouse gas balance in a high Arctic mire. Environ. Res. Lett. 10:045001
    [Google Scholar]
  41. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D et al. 2000. The global carbon cycle: a test of our knowledge of Earth as a system. Science 290:291–96
    [Google Scholar]
  42. Flanagan KM, McCauley E, Wrona F 2006. Freshwater food webs control carbon dioxide saturation through sedimentation. Glob. Change Biol. 12:644–51
    [Google Scholar]
  43. Forbes ES, Cushman JH, Burkepile DE, Young TP, Klope M et al. 2019. Synthesizing the effects of large, wild herbivore exclusion on ecosystem function. Funct. Ecol. 33:1597–610
    [Google Scholar]
  44. Forister ML, Novotny V, Panorska AK, Baje L, Basset Y et al. 2015. The global distribution of diet breadth in insect herbivores. PNAS 112:442–47
    [Google Scholar]
  45. Funk JL, Larson JE, Ames GM, Butterfield BJ, Cavender-Bares J et al. 2017. Revisiting the Holy Grail: using plant functional traits to understand ecological processes. Biol. Rev. 92:1156–73
    [Google Scholar]
  46. García‐Callejas D, Molowny‐Horas R, Araújo MB, Gravel D 2019. Spatial trophic cascades in communities connected by dispersal and foraging. Ecology 100:e02820
    [Google Scholar]
  47. Goheen JR, Augustine DJ, Veblen KE, Kimuyu DM, Palmer TM et al. 2018. Conservation lessons from large‐mammal manipulations in East African savannas: the KLEE, UHURU, and GLADE experiments. Ann. N.Y. Acad. Sci. 1429:31–49
    [Google Scholar]
  48. Gravel D, Albouy C, Thuiller W 2016. The meaning of functional trait composition of food webs for ecosystem functioning. Philos. Trans. R. Soc. B 371:20150268
    [Google Scholar]
  49. Grime JP, Pierce S. 2012. The Evolutionary Strategies That Shape Ecosystems Oxford, UK: Wiley-Blackwell
    [Google Scholar]
  50. Grover JP. 2003. The impact of variable stoichiometry on predator‐prey interactions: a multinutrient approach. Am. Nat. 162:29–43
    [Google Scholar]
  51. Guariento RD, Luttbeg B, Carneiro LS, Caliman A 2018. Prey adaptive behaviour under predation risk modify stoichiometry predictions of predator-induced stress paradigms. Funct. Ecol. 32:1631–43
    [Google Scholar]
  52. Hall SR. 2009. Stoichiometrically explicit food webs: feedbacks between resource supply, elemental constraints, and species diversity. Annu. Rev. Ecol. Evol. Syst. 40:503–28
    [Google Scholar]
  53. Harfoot MBJ, Newbold T, Tittensor DP, Emmott S, Hutton J et al. 2014. Emergent global patterns of ecosystem structure and function from a mechanistic general ecosystem model. PLOS Biol 12:e1001841
    [Google Scholar]
  54. Hawlena D, Schmitz OJ. 2010a. Herbivore physiological response to fear of predation and implications for ecosystem nutrient dynamics. PNAS 107:15503–7
    [Google Scholar]
  55. Hawlena D, Schmitz OJ. 2010b. Physiological stress as a fundamental mechanism linking predation to ecosystem processes. Am. Nat. 176:537–56
    [Google Scholar]
  56. Hawlena D, Strickland MS, Bradford MA, Schmitz OJ 2012. Fear of predation slows plant-litter decomposition. Science 336:1434–38
    [Google Scholar]
  57. Hébert M-P, Beisner BE, Maranger R 2017. Linking zooplankton communities to ecosystem functioning: toward an effect-trait framework. J. Plankton Res. 39:3–12
    [Google Scholar]
  58. Hendry AP, Gotanda KM, Svensson EI 2017. Human influences on evolution, and the ecological and societal consequences. Philos. Trans. R. Soc. B 372:20160028
    [Google Scholar]
  59. Hessen DO, Ågren GI, Anderson TR, Elser JJ, de Ruiter PC 2004. Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–92
    [Google Scholar]
  60. Hillebrand H, Borer ET, Bracken MES, Cardinale BJ, Cebrian J et al. 2009. Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems. Ecol. Lett. 12:516–27
    [Google Scholar]
  61. Holdo RM, Holt RD, Fryxell JM 2009a. Grazers, browsers, and fire influence the extent and spatial pattern of tree cover in the Serengeti. Ecol. App. 19:95–109
    [Google Scholar]
  62. Holdo RM, Sinclair ARE, Dobson AP, Metger KL, Bolker BM et al. 2009b. A disease-mediated trophic cascade in the Serengeti and its implications for ecosystem C. PLOS Biol 7:e1000210
    [Google Scholar]
  63. Holt RD. 1995. Linking species and ecosystems: Where's Darwin?. Linking Species and Ecosystems GG Jones, JH Lawton 127–80 London: Chapman and Hall
    [Google Scholar]
  64. Houghton RA. 2007. Balancing the global carbon budget. Annu. Rev. Earth Planet. Sci. 35:313–47
    [Google Scholar]
  65. Howison RA, Olff H, van de Koppel J, Smit C 2017. Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction. Ecol. Monogr. 87:363–78
    [Google Scholar]
  66. Hunter WR, Ogle N, O'Connor N 2019. Warming affects predatory faunal impacts upon microbial carbon cycling. Funct. Ecol. 33:924–35
    [Google Scholar]
  67. Huntley ME, Lopez MDG, Karl DM 1991. Top predators in the Southern Ocean: a major leak in the biological carbon pump. Science 253:64–6
    [Google Scholar]
  68. Ings TC, Montoya JM, Bascompte J, Blüthgen N, Brown L et al. 2009. Ecological networks—beyond food webs. J. Anim. Ecol. 78:253–69
    [Google Scholar]
  69. Ives AR, Carpenter SR. 2007. Stability and diversity of ecosystems. Science 317:58–62
    [Google Scholar]
  70. Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG et al. 2017. The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu. Rev. Ecol. Evol. Syst. 48:419–45
    [Google Scholar]
  71. Janssens L, Van Dievel M, Stoks R 2015. Warming reinforces nonconsumptive predator effects on prey growth, physiology, and body stoichiometry. Ecology 96:3270–80
    [Google Scholar]
  72. Keenan TF, Williams CA. 2018. The terrestrial carbon sink. Annu. Rev. Environ. Resour. 43:219–43
    [Google Scholar]
  73. Kielland K, Bryant JP. 1998. Moose herbivory in taiga: effects on biogeochemistry and vegetation dynamics in primary succession. Oikos 82:377–83
    [Google Scholar]
  74. Klecka J, Boukal DS. 2013. Foraging and vulnerability traits modify predator-prey body mass allometry: freshwater macroinvertebrates as a case study. J. Anim. Ecol. 82:1031–41
    [Google Scholar]
  75. Kolar V, Boukal D, Sentis A 2019. Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies on a tri-trophic system. Freshwater Biol 64:1480–91
    [Google Scholar]
  76. Laigle I, Aubin I, Digel C, Brose U, Boulangeat I et al. 2018. Species traits as drivers of food web structure. Oikos 127:316–26
    [Google Scholar]
  77. Lara MJ, Johnson DR, Andresen C, Hollister RD, Tweedie CE 2017. Peak season carbon exchange shifts from a sink to a source following 50+ years of herbivore exclusion in an Arctic tundra ecosystem. J. Ecol. 105:122–31
    [Google Scholar]
  78. Le Quéré C, Andrew RM, Friedlingstein P, Sitch S, Pongratz J et al. 2018. Global carbon budget 2017. Earth Syst. Sci. Data 10:405–48
    [Google Scholar]
  79. le Roux E, Kerley G, Cromsigt JPGM 2018. Megaherbivores modify trophic cascades triggered by fear of predation in an African savanna ecosystem. Curr. Biol. 28:2493–99
    [Google Scholar]
  80. le Roux E, Marneweck DG, Clinning G, Druce DJ, Kerley GIH et al. 2019. Top-down limits on prey populations may be more severe in larger prey species, despite having fewer predators. Ecography 42:1115–23
    [Google Scholar]
  81. Leal MC, Seehausen O, Matthews B 2017. The ecology and evolution of stoichiometric phenotypes. Trends Ecol. Evol. 32:108–17
    [Google Scholar]
  82. Leffler AJ, Beard KH, Kelsey KC, Choi RT, Schmutz JA et al. 2019. Delayed herbivory by migratory geese increases summer‐long CO2 uptake in coastal western Alaska. Glob. Change Biol. 25:277–89
    [Google Scholar]
  83. Leroux SJ, Hawlena D, Schmitz OJ 2012. Predation risk, stoichiometric plasticity and ecosystem elemental cycling. Proc. R. Soc. B 279:4183–91
    [Google Scholar]
  84. Leroux SJ, Loreau M. 2015. Theoretical perspectives on bottom-up and top-down interactions across ecosystems. Trophic Ecology: Bottom-Up and Top-Down Interactions Across Aquatic and Terrestrial Systems3–27 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  85. Leroux SJ, Schmitz OJ. 2015. Predator-driven elemental cycling: the predation and risk effects on ecosystem elemental cycling. Ecol. Evol. 5:4976–88
    [Google Scholar]
  86. Leroux SJ, Vander Wal E, Wiersma YF, Charron L, Ebel JD et al. 2017. Stoichiometric distribution models: ecological stoichiometry at the landscape extent. Ecol. Lett. 20:1495–506
    [Google Scholar]
  87. Ligrone R. 2019. Biological Innovations That Built the World Cham, Switz.: Springer
    [Google Scholar]
  88. Limberger R, Birtel J, Peter H, Catalán N, Da Silva Farias D et al. 2019. Predator-induced changes in dissolved organic carbon dynamics. Oikos 128:430–40
    [Google Scholar]
  89. Loehle C, Pechmann JHK. 1988. Evolution: the missing ingredient in systems ecology. Am. Nat. 132:884–99
    [Google Scholar]
  90. Loreau M. 1995. Consumers as maximizers of matter and energy flow in ecosystems. Am. Nat. 145:22–42
    [Google Scholar]
  91. Loreau M. 2010. From Populations to Ecosystems: Theoretical Foundations for a New Ecological Synthesis Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  92. Ma S, He F, Tian D, Zou D, Yan Z et al. 2018. Variations and determinants of carbon contents in plants: a global synthesis. Biogeosciences 15:693–702
    [Google Scholar]
  93. Madji N, Boiche A, Traunspurger W, Lecerf A 2013. Predator effects on a detritus-based food web are primarily mediated by non-trophic interactions. J. Anim. Ecol. 83:953–62
    [Google Scholar]
  94. Marquet PA, Allen AP, Brown JH, Dunne JA, Enquist BJ et al. 2015. On the importance of first principles in ecological theory development. BioScience 65:342–3
    [Google Scholar]
  95. Matthews B, Narwani A, Hausch S, Nonaka E, Peter H et al. 2011. Toward an integration of evolutionary biology and ecosystem science. Ecol. Lett. 14:690–701
    [Google Scholar]
  96. McCauley DJ, Gellner G, Martinez ND, Williams RJ, Sandin SA et al. 2018. On the prevalence and dynamics of inverted trophic pyramids and otherwise top-heavy communities. Ecol. Lett. 21:439–54
    [Google Scholar]
  97. McGill BJ, Dornelas M, Gotelli NJ, Magurran AE 2015. Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol. Evol. 30:104–13
    [Google Scholar]
  98. McInnes PF, Naiman RJ, Pastor J, Cohen Y 1992. Effects of moose browsing on vegetation and litter of the boreal forest, Isle Royale, Michigan, USA. Ecology 73:2059–75
    [Google Scholar]
  99. McPeek MA, Grace M, Richardson JML 2001. Physiological and behavioral responses to predators shape the growth/predation risk trade-off in damselflies. Ecology 82:1535–45
    [Google Scholar]
  100. Metcalfe DB, Olofsson J. 2015. Distinct impacts of different mammalian herbivore assemblages on arctic tundra CO2 exchange during the peak of the growing season. Oikos 124:1632–38
    [Google Scholar]
  101. Metcalfe DB, Asner GP, Martin RE, Silva Espejo JE, Huaraca Huasco W et al. 2013. Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 17:324–32
    [Google Scholar]
  102. Meunier CL, Boersma M, El-Sabaawi R, Halvorson HM, Herstoff EM et al. 2017. From elements to function: toward unifying ecological stoichiometry and trait-based ecology. Front. Environ. Sci. 5:18
    [Google Scholar]
  103. Middelburg JJ. 2019. The return from organic to inorganic carbon. Marine Carbon Biogeochemistry: A Primer for Earth System Scientists JJ Middelburg 37–56 SpringerBriefs in Earth System Sciences Cham, Switz.: Springer
    [Google Scholar]
  104. Monroe JG, Markman DW, Beck WS, Felton AJ, Vahsen ML et al. 2018. Ecoevolutionary dynamics of carbon cycling in the Anthropocene. Trends Ecol. Evol. 33:213–55
    [Google Scholar]
  105. Mulder K. 2007. Modeling the dynamics of nutrient limited consumer populations using constant elasticity production functions. Ecol. Mod. 207:319–26
    [Google Scholar]
  106. Naeem S, Duffy JE, Zavaletta E 2012. The functions of biological diversity in an age of extinction. Science 336:1401–6
    [Google Scholar]
  107. Novak M, Yeakel JD, Noble AE, Doak DF, Emmerson M et al. 2016. Characterizing species interactions to understand press perturbations: What is the community matrix?. Annu. Rev. Ecol. Evol. Syst. 47:409–32
    [Google Scholar]
  108. Pastor J, Cohen Y. 1997. Herbivores, the functional diversity of plants species, and the cycling of nutrients in ecosystems. Theor. Pop. Biol. 51:165–79
    [Google Scholar]
  109. Pastor J, Dewey B, Moen R, Mladenoff DJ, White M et al. 1998. Spatial patterns in the moose-forest-soil ecosystem on Isle Royale, Michigan, USA. Ecol. Appl. 8:411–24
    [Google Scholar]
  110. Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y 1993. Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–80
    [Google Scholar]
  111. Persico EP, Sharp SJ, Angelini C 2017. Feral hog disturbance alters carbon dynamics in southeastern US salt marshes. Mar. Ecol. Prog. Ser. 580:57–68
    [Google Scholar]
  112. Pettorelli N, Schulte to Bühne H, Tulloch A, Dubois G, Macinnis-Ng C et al. 2018. Satellite remote sensing of ecosystem functions: opportunities, challenges and way forward. Remote Sensing Ecol. Conserv. 4:71–93
    [Google Scholar]
  113. Pringle RM. 2018. Ecology: Megaherbivores homogenize the landscape of fear. Curr. Biol. 28:R835–37
    [Google Scholar]
  114. Puccia CJ, Levins R. 1986. Qualitative Modeling of Complex Systems: An Introduction to Loop Analysis and Time Averaging Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  115. Rezende EL, Albert EM, Fortuna MA, Bascompte J 2009. Compartments within marine food webs associated with phylogeny, body mass and habitat structure. Ecol. Lett. 12:779–88
    [Google Scholar]
  116. Ricciardi A. 2007. Are modern biological invasions an unprecedented form of global change?. Conserv. Biol. 21:329–36
    [Google Scholar]
  117. Richter A, Kern T, Wolf S, Struck U, Ruess L 2019. Trophic and non-trophic interactions in binary links affect carbon flow in the soil micro-food web. Soil Biol. Biochem. 135:239–47
    [Google Scholar]
  118. Risch AC, Frank DA. 2006. Carbon dioxide fluxes in a spatially and temporally heterogeneous temperate grassland. Oecologia 147:291–302
    [Google Scholar]
  119. Risch AC, Haynes AG, Busse MD, Filli F, Schütz M 2013. The response of soil CO2 fluxes to progressively excluding vertebrate and invertebrate herbivores depends on ecosystem type. Ecosystems 16:1192–202
    [Google Scholar]
  120. Saleem M, Fetzer I, Harms H, Chatzinotas A 2016. Trophic complexity in aqueous systems: Bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen. Proc. R. Soc. B. 283:20152724
    [Google Scholar]
  121. Schimel D, Pavlick R, Fisher JB, Asner GP, Saatchi S et al. 2015. Observing terrestrial ecosystems and the carbon cycle from space. Glob. Change Biol. 21:1762–76
    [Google Scholar]
  122. Schindler DE, Carpenter SR, Cole JJ, Kitchell JF, Pace ML 1992. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 127:248–51
    [Google Scholar]
  123. Schmitz OJ. 1997. Press perturbations and the predictability of ecological interactions in a food web. Ecology 78:55–69
    [Google Scholar]
  124. Schmitz OJ. 2017. Predator and prey functional traits: understanding the adaptive machinery driving predator-prey interactions. F1000Research 6:1767
    [Google Scholar]
  125. Schmitz OJ, Grabowski JH, Peckarsky BL, Preisser EL, Trussell GC et al. 2008. From individuals to ecosystems: toward an integration of evolutionary and ecosystem ecology. Ecology 89:2436–45
    [Google Scholar]
  126. Schmitz OJ, Hawlena D, Trussell GC 2010. Predator control of ecosystem nutrient dynamics. Ecol. Lett. 13:1199–209
    [Google Scholar]
  127. Schmitz OJ, Raymond PA, Estes JA, Kurz WA, Holtgrieve GW et al. 2014. Animating the carbon cycle. Ecosystems 7:344–59
    [Google Scholar]
  128. Schmitz OJ, Buchkowski RW, Burghardt KT, Donihue CM 2015. Functional traits and trait-mediated interactions: connecting community-level interactions with ecosystem functioning. Adv. Ecol. Res. 52:319–44
    [Google Scholar]
  129. Schmitz OJ, Buchkowski RW, Smith JR, Telthorst M, Rosenblatt AE 2017. Predator community composition is linked to soil carbon retention across a human land use gradient. Ecology 98:1256–65
    [Google Scholar]
  130. Schmitz OJ, Wilmers CC, Leroux SJ, Doughty CE, Atwood TB et al. 2018. Animals and the zoogeochemistry of the carbon cycle. Science 362:eaar3213
    [Google Scholar]
  131. Schramski JR, Dell AI, Grady JM, Sibly RM, Brown JH 2015. Metabolic theory predicts whole ecosystem properties. PNAS 112:2617–22
    [Google Scholar]
  132. Sinclair ARE, Mduma S, Brashares JS 2003. Patterns of predation in a diverse predator-prey system. Nature 425:288–90
    [Google Scholar]
  133. Sitters J, Wubs ERJ, Bakker ES, Crowther TW, Adler PB et al. 2020. Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands. Glob. Change Biol. 26:2060–71
    [Google Scholar]
  134. Sitvarin MI, Rypstra AL. 2014. Fear or predation alters soil carbon dioxide flux and nitrogen content. Biol. Lett. 10:20140366
    [Google Scholar]
  135. Sitvarin MI, Rypstra AL, Harwood JD 2016. Linking the green and brown worlds through nonconsumptive predator effects. Oikos 125:1057–68
    [Google Scholar]
  136. Sjögersten S, van der Wal R, Woodin SJ 2008. Habitat type determines herbivory controls over CO2 fluxes in a warmer Arctic. Ecology 89:2103–16
    [Google Scholar]
  137. Smith FA, Lyons SK, Wagner PJ, Elliott SM 2015. The importance of considering animal body mass in IPCC greenhouse inventories and the underappreciated role of wild herbivores. Glob. Change Biol. 21:3880–88
    [Google Scholar]
  138. Smith FA, Hammond JL, Balk MA, Elliott SM, Lyons SK et al. 2016. Exploring the influence of ancient and historic megaherbivore extirpations on the global methane budget. PNAS 113:874–79
    [Google Scholar]
  139. Sobral M, Silvius KM, Overman H, Oliveira LFB, Rabb TK et al. 2017. Mammal diversity influences the carbon cycle through trophic interactions in the Amazon. Nat. Ecol. Evol. 1:1670–76
    [Google Scholar]
  140. Sørensen MV, Graae BJ, Hagen D, Enquist BJ, Nystuen KO et al. 2018. Experimental herbivore exclusion, shrub introduction, and carbon sequestration in alpine plant communities. BMC Ecol 18:29
    [Google Scholar]
  141. Staniczenko PP, Lewis OT, Jones NS, Reed‐Tsochas F 2010. Structural dynamics and robustness of food webs. Ecol. Lett. 13:891–99
    [Google Scholar]
  142. Stark S, Tuomi J, Strömmer R, Helle T 2003. Non-parallel changes in soil microbial carbon and nitrogen dynamics due to reindeer grazing in northern boreal forests. Ecography 26:51–59
    [Google Scholar]
  143. Steinberg DK, Landry MR. 2017. Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9:413–44
    [Google Scholar]
  144. Stephens JJ, Black AT, Jassal RS, Nesic Z, Grant NJ et al. 2018. Effects of forest tent caterpillar defoliation on carbon and water fluxes in a boreal aspen stand. Agric. For. Meteorol. 253–54:176–89
    [Google Scholar]
  145. Sterner RW, Elser JJ. 2002. Ecological Stoichiometry Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  146. Stone JP, Steinberg DK. 2018. Influence of top-down control in the plankton food web on vertical carbon flux: a case study in the Chesapeake Bay. J. Exp. Mar. Biol. Ecol. 498:16–24
    [Google Scholar]
  147. Strickland MS, Hawlena D, Reese A, Bradford MA, Schmitz OJ 2013. Trophic cascade alters ecosystem carbon exchange. PNAS 110:11035–38
    [Google Scholar]
  148. Tanentzap AJ, Coomes DA. 2012. Carbon storage in terrestrial ecosystems: Do browsing and grazing herbivores matter?. Biol. Rev. 87:72–94
    [Google Scholar]
  149. Taylor BW, Flecker AS, Hall RO 2006. Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–36
    [Google Scholar]
  150. Thébault E, Loreau M. 2003. Food-web constraints on biodiversity-ecosystem functioning relationships. PNAS 100:14949–54
    [Google Scholar]
  151. Thompson JN. 2009. Which ecologically important traits are most likely to evolve rapidly?. Oikos 118:1281–83
    [Google Scholar]
  152. Thomson ACG, Trevathan-Tackett SM, Maher DT, Ralph PJ, Macreadie PI 2019. Bioturbator-stimulated loss of seagrass sediment carbon stocks. Limnol. Oceanogr. 64:342–56
    [Google Scholar]
  153. Trebilco R, Baum JK, Salomon AK, Dulvy NK 2013. Ecosystem ecology: size-based constraints on the pyramids of life. Trends Ecol. Evol. 28:423–31
    [Google Scholar]
  154. Trumble JT, Kolodnyhirsch DM, Ting IP 1993. Plant compensation for arthropod herbivory. Annu. Rev. Entomol. 38:93–119
    [Google Scholar]
  155. Trussell GC, Ewanchuk PJ, Matassa CM 2006. The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–84
    [Google Scholar]
  156. Trussell GC, Ewanchuk PJ, Matassa CM 2008. Resource identity modifies the influence of predation risk on ecosystem function. Ecology 89:2798–807
    [Google Scholar]
  157. Trussell GC, Schmitz OJ. 2012. Species functional traits, trophic control and the ecosystem consequences of adaptive foraging in the middle of food chains. Trait-Mediated Indirect Interactions: Ecological and Evolutionary Perspectives T Ohgushi, O Schmitz, RD Holt 324–38 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  158. van der Wal R, Sjögersten S, Woodin SJ, Cooper EJ, Jónsdóttir IS et al. 2007. Spring feeding by pink-footed geese reduces carbon stocks and sink strength in tundra ecosystems. Glob. Change Biol. 13:539–45
    [Google Scholar]
  159. Veldhuis MP, Gommers MI, Olff H, Berg MP 2018. Spatial redistribution of nutrients by large herbivores and dung beetles in a savanna ecosystem. J. Ecol. 106:422–33
    [Google Scholar]
  160. Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C et al. 2007. Let the concept of trait be functional. ! Oikos 116:882–92
    [Google Scholar]
  161. Wilmers CC, Estes JA, Edwards M, Laidre KL, Konar B 2012. Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests. Front. Ecol. Environ. 10:409–15
    [Google Scholar]
  162. Wilmers CC, Schmitz OJ. 2016. Effects of gray wolf‐induced trophic cascades on ecosystem carbon cycling. Ecosphere 7:e01501
    [Google Scholar]
  163. Winton RS, Richardson CJ. 2017. Top-down control of methane emission and nitrogen cycling by waterfowl. Ecology 98:265–77
    [Google Scholar]
  164. Wootton JT. 1994. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25:443–66
    [Google Scholar]
  165. Ylänne H, Olofsson J, Oksanen L, Stark S 2018. Consequences of grazer-induced vegetation transitions on ecosystem carbon storage in the tundra. Funct. Ecol. 32:1091–102
    [Google Scholar]
  166. Ylänne H, Stark S. 2019. Distinguishing rapid and slow C cycling feedbacks to grazing in subarctic tundra. Ecosystems 22:1145–59
    [Google Scholar]
  167. Zaehle S, Medlyn BE, De Kauwe MG, Walker AP, Dietze MC et al. 2014. Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate Free-Air CO2 enrichment studies. New Phytol 202:803–22
    [Google Scholar]
  168. Zhou Y, Jing L, Jiao S, Chen A, Li N et al. 2019. Dynamics of greenhouse gas emission induced by different burrowing activities of fossorial vertebrates in the Qinghai-Tibetan Plateau alpine meadow ecosystem. Int. J. Meteorol. 64:115–22
    [Google Scholar]
  169. Zou K, Thébault E, Lacroix G, Barot S 2016. Interactions between the green and brown food web determine ecosystem functioning. Funct. Ecol. 30:1454–65
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-011720-104730
Loading
/content/journals/10.1146/annurev-ecolsys-011720-104730
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error