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Effects of herbivores and litter on Lithocarpus hancei seed germination and seedling survival in the understorey of a high diversity forest in SW China


Tanoak Lithocarpus hancei (Fagaceae) is one of the dominant species in the high diversity subtropical evergreen broad-leaved forests in SW China. However, seedlings of L. hancei and other oaks are quite rare in the understorey. To investigate the effects of seed (acorn) predation and seedling herbivory by mammals, and litter, on acorn germination and seedling survival of L. hancei in these forests, we set up a 2 × 2 factorial experiment (litter present or removed; ±herbivore exclosures (fences); plus natural control; 5 replications) in the Ailaoshan National Nature Reserve, central Yunnan from 2010 to 2015. Acorns and transplanted seedlings of L. hancei were placed in the four treatments plots and the influence of these treatments on acorn germination and seedling survival was monitored. Fences protected L. hancei acorns and seedlings against herbivory by rodents and other mammals; litter had a positive effect on acorn survival but no effect on seedling establishment. Moreover, those seedlings that escaped herbivory were mostly killed by fungal attack. Our results indicate that while litter and pathogens have some influence, herbivores are probably the major cause of the low frequency of L. hancei seedlings in the understorey.

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  1. Abbott HG (1961) White pine seed consumption by small mammals. J For 59:197–201

  2. Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712. doi:10.2307/1937766

  3. Augspurger CK, Kitajima K (1992) Experimental studies of seedling recruitment from contrasting seed distributions. Ecology 73:1270–1284. doi:10.2307/1940675

  4. Baskin CC, Baskin JM (2001) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego

  5. Burdon JJ, Leather SR (1990) Pests, pathogens and plant communities. Blackwell Scientific Publications, London

  6. Burrows CJ (1997) Reproductive ecology of New Zealand forests: 1. Natural seed storage phenomena. N Z Nat Sci 23:31–52

  7. Chang G, Jin TZ, Pei JF, Chen XN, Zhang B, Shi ZJ (2012) Seed dispersal of three sympatric oak species by forest rodents in the Qinling Mountains, Central China. Plant Ecol 213:1633–1642. doi:10.1007/s11258-012-0118-1

  8. Cintra R (1997) Leaf litter effects on seed and seedling predation of the palm Astrocaryum murumuru and the legume tree Dipteryx micrantha in Amazonian forest. J Trop Ecol 13:709–725

  9. Crow TR (1988) Reproductive mode and mechanisms for self-replacement of northern red oak (Quercus rubra)—a review. For Sci 34:19–40

  10. Dalgleish HJ, Shukle JT, Swihart RK (2012) Weevil seed damage reduces germination and seedling growth of hybrid American chestnut. Can J For Res 42:1107–1114. doi:10.1139/x2012-067

  11. Dalling JW, Davis AS, Schutte BJ, Arnold AE (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95. doi:10.1111/j.1365-2745.2010.01739.x

  12. Das CR, Mondal NK, Aditya P, Datta JK, Banerjee A, Das K (2012) Allelopathic potentialities of leachates of leaf litter of some selected tree species on gram seeds under laboratory conditions. Asian J Exp Biol Sci 3:59–65

  13. Datta SC, Chatterjee AK (1980) Allelopathic potential of Polygonum orientale L. in relation to germination and seedling growth of weeds. Flora 169:456–465

  14. Dechoum MS, Zenni RD, Castellani TT, Zalba SM, Rejmánek M (2015) Invasions across secondary forest successional stages: effects of local plant community, soil, litter, and herbivory on Hovenia dulcis seed germination and seedling establishment. Plant Ecol 216:823–833. doi:10.1007/s11258-015-0470-z

  15. Eckstein RL, Donath TW (2005) Interactions between litter and water availability affect seedling emergence in four familial pairs of floodplain species. J Ecol 93:807–816. doi:10.1111/j.1365-2745.2005.01015.x

  16. Editorial Committee for Vegetation of China (1980) Vegetation of China. Science Press, Beijing

  17. Eriksson O (1995) Seedling recruitment in deciduous forest herbs: the effects of litter, soil chemistry and seed bank. Flora 190:65–70

  18. García-Guzmán G, Benítez-Malvido J (2003) Effect of litter on the incidence of leaf-fungal pathogens and herbivory in seedlings of the tropical tree Nectandra ambigens. J Trop Ecol 19:171–177. doi:10.1017/S0266467403003195

  19. Gardiner ES, Hodges JD (1998) Growth and biomass distribution of cherrybark oak (Quercus pagoda Raf.) seedlings as influenced by light availability. For Ecol Manag 108:127–134. doi:10.1016/s0378-1127(98)00220-5

  20. Gashwiler JS (1967) Conifer seed survival in a western Oregon clearcut. Ecology 48:431–438

  21. Gong HD, Yang GP, Lu ZY, Liu YH (2011a) Diversity and spatial distribution patterns of trees in an evergreen broad-leaved forest in the Ailao Mountains, Yunnan. Biodivers Sci 19:143–150 (in Chinese with English abstract)

  22. Gong HD, Yang GP, Lu ZY, Liu YH, Cao M (2011b) Composition and spatio-temporal distribution of tree seedlings in an evergreen broad-leaved forest in the Ailao Mountains, Yunnan. Biodivers Sci 19:151–157. doi:10.3724/SP.J.1003.2011.07010 (in Chinese with English abstract)

  23. Hamrick JL, Lee JM (1987) Effect of soil surface topography and litter cover on the germination, survival, and growth of musk thistle (Carduus nutans). Am J Bot 74:451–457. doi:10.2307/2443821

  24. Harper JL (1977) Population biology of plants. Academic Press, London

  25. Jansen PA, Forget PM (2001) Scatterhoarding rodents and tree regeneration. In: Bongers F, Charles-Dominique P, Forget PM, Théry M (eds) Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer Academic Publisher, Dordrecht, pp 275–288

  26. Kitajima K, Augspurger CK (1989) Seed and seedling ecology of a monocarpic tropical tree, Tachigalia versicolor. Ecology 70:1102–1114. doi:10.2307/1941379

  27. Klinger R, Rejmánek M (2013) Experimental seed predator removal reveals shifting importance of predation and dispersal limitation in early life history stages of tropical forest trees. Folia Geobot 48:415–435. doi:10.1007/s12224-013-9178-9

  28. Kohler SL, Wiley MJ (1992) Parasite-induced collapse of populations of a dominant grazer in Michigan streams. Oikos 65:443–449

  29. Kon H, Noda T, Terazawa K, Koyama H, Yasaka M (2005) Evolutionary advantages of mast seeding in Fagus crenata. J Ecol 93:1148–1155. doi:10.1111/j.1365-2745.2005.01040.x

  30. Lawrence WH, Rediske JH (1962) Fate of sown Douglas-fir seed. For Sci 8:210–218

  31. Li QK, Ma KP (2003) Factors affecting establishment of Quercus liaotungensis Koidz. under mature mixed oak forest overstory and in shrubland. For Ecol Manag 176:133–146. doi:10.1016/s0378-1127(02)00274-8

  32. Li HJ, Zhang HM, Zhang ZB (2006) Acorn removal of Liaodong oak (Quercus liaotungensis) by rodents. Acta Theriol Sin 26:8–12

  33. Li S, Liu WY, Li DW, Song L, Shi XM, Lu HZ (2015) Species richness and vertical stratification of epiphytic lichens in subtropical primary and secondary forests in southwest China. Fungal Ecol 17:30–40. doi:10.1016/j.funeco.2015.02.005

  34. Liu WY, Fox JED, Xu ZF (2002) Biomass and nutrient accumulation in montane evergreen broad-leaved forest (Lithocarpus xylocarpus type) in Ailao Mountains, SW China. For Ecol Manag 158:223–235

  35. Lorimer CG, Chapman JW, Lambert WD (1994) Tall understorey vegetation as a factor in the poor development of oak seedlings beneath mature stands. J Ecol 82:227–237. doi:10.2307/2261291

  36. Loydi A, Eckstein RL, Otte A, Donath TW (2013) Effects of litter on seedling establishment in natural and semi-natural grasslands: a meta-analysis. J Ecol 101:454–464. doi:10.1111/1365-2745.12033

  37. McGee CE (1975) Change in forest canopy affects phenology and development of northern red and scarlet oak seedlings. For Sci 21:175–179

  38. Moles AT, Westoby M (2004) What do seedlings die from and what are the implications for evolution of seed size? Oikos 106:193–199

  39. Molofsky J, Augspurger CK (1992) The effect of leaf litter on early seedling establishment in a tropical forest. Ecology 73:68–77. doi:10.2307/1938721

  40. Muñoz A, Bonal R, Espelta JM (2014) Acorn—weevil interactions in a mixed-oak forest: outcomes for larval growth and plant recruitment. For Ecol Manag 322:98–105. doi:10.1016/j.foreco.2014.02.039

  41. Ni J (2001) Plant functional types and biomes of China at a regional scale. Acta Bot Sin 43:419–425 (in Chinese with English abstract)

  42. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Naturalist 147:813–846

  43. Price MV, Jenkins SH (1986) Rodents as seed consumers and dispersers. In: Murray DR (ed) Seed dispersal. Academic Press, Sydney, pp 191–235

  44. Qi SS, Dai ZC, Miao SL et al (2014) Light limitation and litter of an invasive clonal plant, Wedelia trilobata, inhibit its seedling recruitment. Ann Bot 114:425–433. doi:10.1093/aob/mcu075

  45. Qi JH, Zhang YJ, Zhang YP, Liu YH, Lu ZY, Wu CS, Wen HD (2015) The influence of changes in water availability on seedling mortality of a subtropical evergreen broadleaf forest on Ailao Mountain. Acta Ecol Sin 35:2521–2528 (in Chinese with English abstract)

  46. Qiu XZ, Xie SC, Liu WY et al (1998) Studies on the forest ecosystem in Ailao Mountains, Yunnan. Yunnan Science and Technology Press, Kunming (in Chinese with English abstract)

  47. Rai JPN, Tripathi RS (1984) Allelopathic effects of Eupatorium riparium on population regulation of two species of Galinsoga and soil microbes. Plant Soil 80:105–117. doi:10.1007/BF02232944

  48. Reader RJ (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. J Ecol 81:169–175. doi:10.2307/2261232

  49. Rotundo JL, Aguiar MR (2005) Litter effects on plant regeneration in arid lands: a complex balance between seed retention, seed longevity and soil-seed contact. J Ecol 93:829–838. doi:10.1111/j.1365-2745.2005.01022

  50. Schafer M, Kotanen PM (2003) The influence of soil moisture on losses of buried seeds to fungi. Acta Oecol 24:255–263. doi:10.1016/j.actao.2003.09.001

  51. Shaw EW (1954) Direct seeding in the Pacific Northwest. J For 52:827–828

  52. Sork VL (1983) Distribution of pignut hickory (Carya glabra) along a forest to edge transect, and factors affecting seedling recruitment. B Torrey Bot Club 110:494–506. doi:10.2307/2996284

  53. Stiling P, Rossi AM (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78:1602–1606

  54. Sunyer P, Boixadera E, Muñoz A, Bonal R, Espelta JM (2015) The interplay among acorn abundance and rodent behavior drives the spatial pattern of seedling recruitment in mature Mediterranean oak forests. PLoS One 10:e0129844. doi:10.1371/journal.pone.0129844

  55. Sydes C, Grime JP (1981) Effects of tree leaf litter on herbaceous vegetation in deciduous woodland: II. An experimental investigation. J Ecol 69:249–262. doi:10.2307/2259829

  56. Thadani R, Ashton PMS (1995) Regeneration of banj oak (Quercus leucotrichophora A. Camus) in the central Himalaya. For Ecol Manag 78:217–224. doi:10.1016/0378-1127(95)03561-4

  57. Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago and London

  58. Vander Wall SB (2002) Masting in animal-dispersed pines facilitates seed dispersal. Ecology 83:3508–3516

  59. Wang ZJ, Carpenter C, Young SS (2000) Bird distribution and conservation in the Ailao Mountains, Yunnan, China. Biol Conserv 92:45–57. doi:10.1016/S0006-3207(99)00058-0

  60. Wei TH, Wang ZJ, Cui QY (1988) The birds in northern and middle parts of the Ailaoshan Mountains. In: Xu YC, Jiang HQ (eds) Comprehensive survey reports of the Ailaoshan mountains natural reserve. Yunnan Ethnic Press, Kunming, pp 206–230 (in Chinese with English abstract)

  61. Willis CP (1914) The control of rodents in field seeding. Proc Soc Am For 9:365–379

  62. White TJ (2014) The effects of Phragmites Australis litter on seed emergence in the Erie-Huron Corridor, Michigan. Master Thesis, Wayne State University

  63. Xiao ZS, Zhang ZB (2012) Behavioural responses to acorn germination by tree squirrels in an old forest where white oaks have long been extirpated. Anim Behav 83:945–951. doi:10.1016/j.anbehav.2012.01.013

  64. Xiao ZS, Zhang ZB, Wang YS (2005) The effects of seed abundance on seed predation and dispersal by rodents in Castanopsis fargesii (Fagaceae). Plant Ecol 177:249–257. doi:10.1007/s11258-005-2321-9

  65. Xiao ZS, Gao X, Steele MA, Zhang ZB (2009) Frequency-dependent selection by tree squirrels: adaptive escape of nondormant white oaks. Behav Ecol. doi:10.1093/beheco/arp169

  66. Young SS, Herwitz SR (1995) Floristic diversity and co-occurrences in a subtropical broad-leaved forest and two contrasting regrowth stands in central-west Yunnan Province, China. Vegetatio 119:1–13

  67. Young SS, Carpenter C, Wang ZJ (1992) A study of the structure and composition of an old growth and secondary broad-leaved forest in the Ailao Mountains of Yunnan, China. Mt Res Dev 12:269–284. doi:10.2307/3673670

  68. Zhao TG, Wu DL, Deng XF (1988) Mammals in the Ailaoshan mountain natural reserve. In: Xu YC, Jiang HQ (eds) Comprehensive survey reports of the Ailaoshan mountains natural reserve. Yunnan Ethnic Press, Kunming, pp 194–205 (in Chinese with English abstract)

  69. Zhu H, Yan LC (2009) List of seed plants in the Ailao Mts of Yunnan Province. Yunnan Science and Technology Press, Kunming, China

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Financial support was provided by a Joint Fund from the National Natural Science Foundation of China and Yunnan Provincial Government (Grant no. U1502231). We are grateful to the Ailaoshan Station for Subtropical Forest Ecosystem Research, Chinese Academy of Sciences, for permission and support to conduct this research in the Ailaoshan National Nature Reserve. We also thank Prof. Zhi-Shu Xiao, the Institute of Zoology, Chinese Academy of Sciences, Beijing, for providing the photograph of the Asian red-cheeked squirrel.

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Correspondence to Roy Turkington or Zhe-Kun Zhou.

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Hu, J., Luo, C., Turkington, R. et al. Effects of herbivores and litter on Lithocarpus hancei seed germination and seedling survival in the understorey of a high diversity forest in SW China. Plant Ecol 217, 1429–1440 (2016).

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  • Herbivory
  • Litter
  • Seed germination
  • Seedling establishment
  • Lithocarpus hancei
  • Tanoak