Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 4, 2016, Pages 847-855

  Bakker, Elisabeth S ^a   Gill, Jacquelyn L ^b   Johnson, Christopher N ^c   Vera, Frans W M ^d   Sandom, Christopher J ^e   Asner, Gregory P ^f   Svenning, Jens Christian ^g  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UNIVERSITY OF MAINE   (United States)

^c UNIVERSITY OF TASMANIA   (Australia)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f GEOPHYSICAL LABORATORY   (United States)

^g AARHUS UNIVERSITY   (Denmark)

Author keywords

Browsers; Ecosystem functions; Herbivore diversity; Landscape structure; Megaherbivore

Indexed keywords

CONCEPTUAL FRAMEWORK; DENSITY; ECOSYSTEM; FORAGING; HERBIVORE; HERBIVORY; LANDSCAPE ECOLOGY; LATE QUATERNARY; NONHUMAN; PALEOECOLOGY; PLEISTOCENE; POPULATION ABUNDANCE; PRIORITY JOURNAL; REVIEW; SPECIES COMPOSITION; SPECIES DIVERSITY; SPECIES EXTINCTION; UPPER PLEISTOCENE; WOODY PLANT; ANIMAL; ANIMAL BEHAVIOR; ANIMAL DISPERSAL; BIODIVERSITY; BIOLOGICAL MODEL; BODY SIZE; CARBON CYCLE; ELEPHANT; FORECASTING; FOREST; HISTORY; MAMMAL; MASTODON; PALEONTOLOGY; PHYSIOLOGY; PLANT DISPERSAL; PREDATION; TREE;

ANIMAL DISTRIBUTION; ANIMALS; BEHAVIOR, ANIMAL; BIODIVERSITY; BODY SIZE; CARBON CYCLE; ECOSYSTEM; ELEPHANTS; EXTINCTION, BIOLOGICAL; FORECASTING; FORESTS; HERBIVORY; HISTORY, ANCIENT; MAMMALS; MASTODONS; MODELS, BIOLOGICAL; PALEONTOLOGY; PLANT DISPERSAL; PREDATORY BEHAVIOR; TREES;

EID: 84955471237     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1502545112     Document Type: Review

References (123)

1. Sandom C, Faurby S, Sandel B, Svenning JC (2014) Global late Quaternary megafauna extinctions linked to humans, not climate change. Proc R Soc Lond B Biol Sci 281(1787):20133254.
2. Koch PL, Barnosky AD (2006) Late quaternary extinctions: State of the debate. Annu Rev Ecol Evol Syst 37:215-250.
3. Estes JA, et al. (2011) Trophic downgrading of planet Earth. Science 333(6040):301-306.
4. Zalasiewicz J, et al. (2015) When did the Anthropocene begin? A mid-twentieth century boundary level is stratigraphically optimal. Quat Int, in press, 10.1016/j. quaint.2014.11.045.
5. McCauley DJ, et al. (2015) Marine defaunation: Animal loss in the global ocean. Science 347(6219):1255641.
6. Young HS, et al. (2013) Effects of mammalian herbivore declines on plant communities: Observations and experiments in an African savanna. J Ecol 101(4):1030-1041.
7. Dirzo R, et al. (2014) Defaunation in the Anthropocene. Science 345(6195):401-406.
8. Ripple WJ, et al. (2015) Collapse of the world's largest herbivores. Sci Adv 1(4):e1400103:1-12.
9. Danell K, Bergström R, Duncan P, Pastor J, eds (2006) Large Herbivore Ecology, Ecosystem Dynamics and Conservation (Cambridge Univ Press, Cambridge, UK).
10. Johnson CN (2009) Ecological consequences of Late Quaternary extinctions of megafauna. Proc R Soc Lond B Biol Sci 276(1667):2509-2519.
11. Gill JL (2014) Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytol 201(4):1163-1169.
12. Asner GP, et al. (2009) Large-scale impacts of herbivores on the structural diversity of African savannas. Proc Natl Acad Sci USA 106(12):4947-4952.
13. Sankaran M, Augustine DJ, Ratnam J (2013) Native ungulates of diverse body sizes collectively regulate long-term woody plant demography and structure of a semi-arid savanna. J Ecol 101(6):1389-1399.
14. Augustine DJ, McNaughton SJ (2004) Regulation of shrub dynamics by native browsing ungulates on East African rangeland. J Appl Ecol 41(1):45-58.
15. Keesing F, Young TP (2014) Cascading consequences of the loss of large mammals in an African savanna. Bioscience 64(6):487-495.
16. Pringle RM, et al. (2014) Low functional redundancy among mammalian browsers in regulating an encroaching shrub (Solanum campylacanthum) in African savannah. Proc R Soc Lond B Biol Sci 281(1785):20140390.
17. Staver AC, Bond WJ (2014) Is there a 'browse trap'? Dynamics of herbivore impacts on trees and grasses in an African savanna. J Ecol 102(3):595-602.
18. Owen-Smith N (1989) Megafaunal extinctions: The conservation message from 11, 000 years B.p. Conserv Biol 3(4):405-412.
19. Guldemond R, Van Aarde R (2008) A meta-analysis of the impact of African elephants on savanna vegetation. J Wildl Manage 72(4):892-899.
20. Maron JL, Crone E (2006) Herbivory: Effects on plant abundance, distribution and population growth. Proc Biol Sci 273(1601):2575-2584.
21. Owen-Smith RN (1988) Megaherbivores: The Influence of Very Large Body Size on Ecology (Cambridge Univ Press, Cambridge, UK).
22. Asner GP, Levick SR (2012) Landscape-scale effects of herbivores on treefall in African savannas. Ecol Lett 15(11):1211-1217.
23. Kimuyu DM, Sensenig RL, Riginos C, Veblen KE, Young TP (2014) Native and domestic browsers and grazers reduce fuels, fire temperatures, and acacia ant mortality in an African savanna. Ecol Appl 24(4):741-749.
24. Kuiters AT, van der Sluijs LAM, Wytema GA (2006) Selective bark-stripping of beech, Fagus sylvatica, by free-ranging horses. For Ecol Manage 222(1-3):1-8.
25. Prins HHT, Van der Jeugd HP (1993) Herbivore population crashes and woodland structure in East Africa. J Ecol 81(2):305-314.
26. O'Kane CAJ, Duffy KJ, Page BR, Macdonald DW (2011) Are the long-term effects of mesobrowsers on woodland dynamics substitutive or additive to those of elephants? Acta Oecol 37(5):393-398.
27. Moe SR, Rutina LP, Hytteborn H, du Toit JT (2009) What controls woodland regeneration after elephants have killed the big trees? J Appl Ecol 46(1):223-230.
28. Keesing F (2000) Cryptic consumers and the ecology of an African Savanna. Bioscience 50(6):205-215.
29. du Toit JT (1990) Feeding height stratification among African browsing ruminants. Afr Ecol 28(1):55-61.
30. Goheen JR, Palmer TM, Keesing F, Riginos C, Young TP (2010) Large herbivores facilitate savanna tree establishment via diverse and indirect pathways. J Anim Ecol 79(2):372-382.
31. Maclean JE, Goheen JR, Doak DF, Palmer TM, Young TP (2011) Cryptic herbivores mediate the strength and form of ungulate impacts on a long-lived savanna tree. Ecology 92(8):1626-1636.
32. Codron D, et al. (2007) Diets of savanna ungulates from stable carbon isotope composition of faeces. J Zool (Lond) 273(1):21-29.
33. Gill R (2006) The influence of large herbivores on tree recruitment and forest dynamics. Large Herbivore Ecology, Ecosystem Dynamics and Conservation, eds Danell K, Bergström R, Duncan P, Pastor J (Cambridge Univ Press, Cambridge, UK), pp 170-202.
34. Ford AT, et al. (2014) Large carnivores make savanna tree communities less thorny. Science 346(6207):346-349.
35. Vera FWM, Bakker ES, Olff H (2006) Large herbivores: Missing partners of western European light-demanding tree and shrub species? Large Herbivore Ecology, Ecosystem Dynamics and Conservation, eds Danell K, Bergström R, Duncan P, Pastor J (Cambridge Univ Press, Cambridge, UK), pp 203-231.
36. Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forest of Isle Royale National Park. Ecology 74(2):467-480.
37. 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(6):2059-2075.
38. Hidding B, Tremblay JP, Côté SD (2013) A large herbivore triggers alternative successional trajectories in the boreal forest. Ecology 94(12):2852-2860.
39. Tanentzap AJ, et al. (2011) Seeing the forest for the deer: Do reductions in deer-disturbance lead to forest recovery? Biol Conserv 144(1):376-382.
40. Wigley BJ, Fritz H, Coetsee C, Bond WJ (2014) Herbivores shape woody plant communities in the Kruger National Park: Lessons from three long-term exclosures. Koedoe 56(1):1-12.
41. Bernadzki E, Bolibok L, Brzeziecki B, Zajaczkowski J, Zybura H (1998) Compositional dynamics of natural forests in the Bialowieza National Park, northeastern Poland. J Veg Sci 9(2):229-238.
42. Vera FWM (2000) Grazing Ecology and Forest History (CAB International, Wallingford, UK).
43. Jedrzejewska B, Jedrzejewski W, Bunevich AN, Milkowski L, Krasinski ZA (1997) Factors shaping population densities and increase rates of ungulates in Bialowieza Primeval Forest (Poland and Belarus) in the 19th and 20th centuries. Acta Theriol (Warsz) 42(4):399-451.
44. Pigott D (2012) Lime-Trees and Basswoods: A Biological Monograph of the Genus Tilia (Cambridge Univ Press, Cambridge, UK).
45. Kuijper DPJ, et al. (2013) Landscape of fear in Europe: Wolves affect spatial patterns of ungulate browsing in Bialowieza Primeval Forest, Poland. Ecography 36(12):1263-1275.
46. Olff H, et al. (1999) Shifting mosaics in grazed woodlands driven by the alternation of plant facilitation and competition. Plant Biol 1(2):127-137.
47. Bakker ES, et al. (2004) Ecological anachronisms in the recruitment of temperate light-demanding tree species in wooded pastures. J Appl Ecol 41(3):571-582.
48. Smit C, Vandenberghe C, den Ouden J, Müller-Schärer H (2007) Nurse plants, tree saplings and grazing pressure: Changes in facilitation along a biotic environmental gradient. Oecologia 152(2):265-273.
49. Milchunas DG, Noy-Meir I (2002) Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99(1):113-130.
50. Smit C, Kuijper DPJ, Prentice D, Wassen MJ, Cromsigt J (2012) Coarse woody debris facilitates oak recruitment in Bialowieza Primeval Forest, Poland. For Ecol Manage 284:133-141.
51. Lima SL, Dill L (1990) Behavioral decisions made under the risk of predation: A review and prospectus. Can Zool 68(4):619-640.
52. Kauffman MJ, et al. (2007) Landscape heterogeneity shapes predation in a newly restored predator-prey system. Ecol Lett 10(8):690-700.
53. Riginos C, Grace JB (2008) Savanna tree density, herbivores, and the herbaceous community: Bottom-up vs. top-down effects. Ecology 89(8):2228-2238.
54. Laundre JW, Hernandez L, Altendorf KB (2001) Wolves, elk, and bison: Re-establishing the "landscape of fear" in Yellowstone National Park, USA. Can Zool 79(8):1401-1409.
55. Painter LE, Beschta RL, Larsen EJ, RippleWJ (2015) Recovering aspen follow changing elk dynamics in Yellowstone: Evidence of a trophic cascade? Ecology 96(1):252-263.
56. Callan R, Nibbelink NP, Rooney TP, Wiedenhoeft JE, Wydeven AP (2013) Recolonizing wolves trigger a trophic cascade in Wisconsin (USA). J Ecol 101(4):837-845.
57. Metcalfe JZ, Longstaffe FJ, Hodgins G (2013) Proboscideans and paleoenvironments of the Pleistocene Great Lakes: Landscape, vegetation, and stable isotopes. Quat Sci Rev 76:102-113.
58. Teale CL, Miller NG (2012) Mastodon herbivory in mid-latitude late-Pleistocene boreal forests of eastern North America. Quat Res 78(1):72-81.
59. Owen-Smith N (1987) Pleistocene extinctions: The pivotal role of megaherbivores. Paleobiology 13(3):351-362.
60. Green JL, Semprebon GM, Solounias N (2005) Reconstructing the palaeodiet of Florida Mammut americanum via low-magnification stereomicroscopy. Palaeogeogr Palaeocl 223(1-2):34-48.
61. Mann DH, Groves P, Kunz ML, Reanier RE, Gaglioti BV (2013) Ice-age megafauna in Arctic Alaska: Extinction, invasion, survival. Quat Sci Rev 70:91-108.
62. Franca LD, et al. (2015) Review of feeding ecology data of Late Pleistocene mammalian herbivores from South America and discussions on niche differentiation. Earth Sci Rev 140:158-165.
63. Willerslev E, et al. (2014) Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506(7486):47-51.
64. van Asperen EN, Kahlke RD (2015) Dietary variation and overlap in Central and Northwest European Stephanorhinus kirchbergensis and S. hemitoechus (Rhinocerotidae, Mammalia) influenced by habitat diversity. Quat Sci Rev 107:47-61.
65. Kissling WD, et al. (2014) Establishing macroecological trait datasets: Digitalization, extrapolation, and validation of diet preferences in terrestrial mammals worldwide. Ecol Evol 4(14):2913-2930.
66. Lister A, Bahn P (2009) Mammoths: Giants of the Ice Age (Univ of California Press, Oakland, CA).
67. Janzen DH, Martin PS (1982) Neotropical anachronisms: The fruits the gomphotheres ate. Science 215(4528):19-27.
68. Campos-Arceiz A, Blake S (2011) Megagardeners of the forest: The role of elephants in seed dispersal. Acta Oecol 37(6):542-553.
69. Haynes G (2012) Elephants (and extinct relatives) as earth-movers and ecosystem engineers. Geomorphology 157:99-107.
70. Zimov SA, et al. (1995) Steppe-tundra transition: A herbivore-driven biome shift at the end of the pleistocene. Am Nat 146(5):765-794.
71. Kgope BS, Bond WJ, Midgley GF (2010) Growth responses of African savanna trees implicate atmospheric CO2 as a driver of past and current changes in savanna tree cover. Austral Ecol 35(4):451-463.
72. Ward JK, et al. (2005) Carbon starvation in glacial trees recovered from the La Brea tar pits, southern California. Proc Natl Acad Sci USA 102(3):690-694.
73. Burney DA, Robinson GS, Burney LP (2003) Sporormiella and the late Holocene extinctions in Madagascar. Proc Natl Acad Sci USA 100(19):10800-10805.
74. Robinson GS, Burney LP, Burney DA (2005) Landscape paleoecology and megafaunal extinction in southeastern New York state. Ecol Monogr 75(3):295-315.
75. Gill JL, Williams JW, Jackson ST, Lininger KB, Robinson GS (2009) Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326(5956):1100-1103.
76. Rule S, et al. (2012) The aftermath of megafaunal extinction: Ecosystem transformation in Pleistocene Australia. Science 335(6075):1483-1486.
77. Johnson CN, et al. (2015) Using dung fungi to interpret decline and extinction of megaherbivores: problems and solutions. Quat Sci Rev 110:107-113.
78. Gill JL, Williams JW, Jackson ST, Donnelly JP, Schellinger GC (2012) Climatic and megaherbivory controls on late-glacial vegetation dynamics: A new, highresolution, multi-proxy record from Silver Lake, Ohio. Quat Sci Rev 34:66-80.
79. Faison EK, Foster DR, Oswald WW, Hansen BCS, Doughty E (2006) Early holocene openlands in southern New England. Ecology 87(10):2537-2547.
80. Weigl PD, Knowles TW (2014) Temperate mountain grasslands: A climate-herbivore hypothesis for origins and persistence. Biol Rev Camb Philos Soc 89(2):466-476.
81. Sandom CJ, Ejrnæs R, Hansen MDD, Svenning JC (2014) High herbivore density associated with vegetation diversity in interglacial ecosystems. Proc Natl Acad Sci USA 111(11):4162-4167.
82. Svenning J-C (2002) A review of natural vegetation openness in north-western Europe. Biol Conserv 104(2):133-148.
83. Alexander K (2005) Wood decay, insects, palaeoecology, and woodland conservation policy and practice: Breaking the halter. Antenna 29:171-178.
84. Whitehouse NJ, Smith D (2010) How fragmented was the British Holocene wildwood? Perspectives on the "Vera" grazing debate from the fossil beetle record. Quat Sci Rev 29(3-4):539-553.
85. Zimov SA, Zimov NS, Tikhonov AN, Chapin FS (2012) Mammoth steppe: A high-productivity phenomenon. Quat Sci Rev 57:26-45.
86. Kienast F, et al. (2011) Paleontological records indicate the occurrence of open woodlands in a dry inland climate at the present-day Arctic coast in western Beringia during the Last Interglacial. Quat Sci Rev 30(17-18):2134-2159.
87. Olofsson J, et al. (2009) Herbivores inhibit climate-driven shrub expansion on the tundra. Glob Change Biol 15(11):2681-2693.
88. Post E, Pedersen C (2008) Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci USA 105(34):12353-12358.
89. Barlow C (2002) The Ghosts of Evolution: Nonsensical Fruit, Missing Partners, and Other Ecological Anachronisms (Basic Books, New York).
90. Zaya DN, Howe HF (2009) The anomalous Kentucky coffeetree: Megafaunal fruit sinking to extinction? Oecologia 161(2):221-226.
91. Perry GLW, Wheeler AB, Wood JR, Wilmshurst JM (2014) A high-precision chronology for the rapid extinction of New Zealand moa (Aves, Dinornithiformes). Quat Sci Rev 105:126-135.
92. Bond WJ, Lee WG, Craine JM (2004) Plant structural defences against browsing birds: A legacy of New Zealand's extinct moas. Oikos 104(3):500-508.
93. Wilson JB, Lee WG (2012) Is New Zealand vegetation really 'problematic'? Dansereau's puzzles revisited. Biol Rev Camb Philos Soc 87(2):367-389.
94. Bond WJ, Silander JA (2007) Springs and wire plants: Anachronistic defences against Madagascar's extinct elephant birds. Proc Biol Sci 274(1621):1985-1992.
95. Lee WG, Wood JR, Rogers GM (2010) Legacy of avian-dominated plant-herbivore systems in New Zealand. New Zeal Ecol 34(1):28-47.
96. Colgan MS, Asner GP, Levick SR, Martin RE, Chadwick OA (2012) Topo-edaphic controls over woody plant biomass in South African savannas. Biogeosciences 9(5):1809-1821.
97. Diedrich CG (2012) Cave bear killers and scavengers from the last ice age of central Europe: Feeding specializations in response to the absence of mammoth steppe fauna from mountainous regions. Quat Int 255:59-78.
98. Pop E, Bakels C (2015) Semi-open environmental conditions during phases of hominin occupation at the Eemian Interglacial basin site Neumark-Nord 2 and its wider environment. Quat Sci Rev 117:72-81.
99. Fritz H, Duncan P (1994) On the carrying capacity for large ungulates of African savanna ecosystems. Proc Biol Sci 256(1345):77-82.
100. Olff H, Ritchie ME, Prins HHT (2002) Global environmental controls of diversity in large herbivores. Nature 415(6874):901-904.
101. Cromsigt J, Kuijper DPJ (2011) Revisiting the browsing lawn concept: Evolutionary interactions or pruning herbivores? Perspect Plant Ecol Evol Syst 13(3):207-215.
102. Kuijper DPJ, et al. (2010) Bottom-up versus top-down control of tree regeneration in the Bialowieza Primeval Forest, Poland. J Ecol 98(4):888-899.
103. Van Valkenburgh B, Hayward MW, Ripple WJ, Meloro C, Roth VL (2016) The impact of large terrestrial carnivores on Pleistocene ecosystems. Proc Natl Acad Sci USA 113:862-867.
104. Pachzelt A, Rammig A, Higgins S, Hickler T (2013) Coupling a physiological grazer population model with a generalized model for vegetation dynamics. Ecol Modell 263:92-102.
105. Rackham O (1980) Ancient Woodland: Its History, Vegetation and Uses in England (Edward Arnold, London).
106. Putman RJ (1986) Grazing in Temperate Ecosystems: Large Herbivores and the Ecology of the New Forest (Croom Helm, London, UK).
107. Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of savanna and forest as alternative biome states. Science 334(6053):230-232.
108. Greve M, et al. (2012) Continental-scale variability in browser diversity is a major driver of diversity patterns in acacias across Africa. J Ecol 100(5):1093-1104.
109. Vare H, Ohtonen R, Mikkola K (1996) The effect and extent of heavy grazing by reindeer in oligotrophic pine heaths in northeastern Fennoscandia. Ecography 19(3):245-253.
110. Svenning J-C, et al. (2015) Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research. Proc Natl Acad Sci USA 113:898-906.
111. Mitchell FJG, Cole E (1998) Reconstruction of long-term successional dynamics of temperate woodland in Bialowieza Forest, Poland. J Ecol 86(6):1042-1059.
112. Kerley GIH, Kowalczyk R, Cromsigt J (2012) Conservation implications of the refugee species concept and the European bison: King of the forest or refugee in a marginal habitat? Ecography 35(6):519-529.
113. Cromsigt J, te BeestM(2014) Restoration of a megaherbivore: Landscape-level impacts of white rhinoceros in Kruger National Park, South Africa. J Ecol 102(3):566-575.
114. Pennisi E (2014) The river masters. Science 346(6211):802-805.
115. Bond WJ (2008) What limits trees in C4 grasslands and savannas? Annu Rev Ecol Evol Syst 39:641-659.
116. Sankaran M, Ratnam J, Hanan N (2008) Woody cover in African savannas: The role of resources, fire and herbivory. Glob Ecol Biogeogr 17(2):236-245.
117. Bond WJ, Keeley JE (2005) Fire as a global 'herbivore': The ecology and evolution of flammable ecosystems. Trends Ecol Evol 20(7):387-394.
118. Gill JL, et al. (2013) Linking abundances of the dung fungus Sporormiella to the density of bison: Implications for assessing grazing by megaherbivores in palaeorecords. J Ecol 101(5):1125-1136.
119. Smith D, Nayyar K, Schreve D, Thomas R, Whitehouse N (2014) Can dung beetles from the palaeoecological and archaeological record indicate herd concentration and the identity of herbivores? Quat Int 341:119-130.
120. Widga C, Colburn M (2015) Paleontology and paleoecology of guano deposits in Mammoth Cave, Kentucky, USA. Quat Res 83(3):427-436.
121. Cerling TE, et al. (2011) Woody cover and hominin environments in the past 6 million years. Nature 476(7358):51-56.
122. Asner GP, et al. (2007) Carnegie Airborne Observatory: In-flight fusion of hyperspectral imaging and waveform light detection and ranging (wLiDAR) for threedimensional studies of ecosystems. J Appl Remote Sens 1:013536.
123. Cornelissen P, Gresnigt MC, Vermeulen RA, Bokdam J, Smit R (2014) Transition of a Sambucus nigra L. dominated woody vegetation into grassland by a multispecies herbivore assemblage. J Nat Conserv 22(1):84-92.