Annals of Forest Science

, 74:70 | Cite as

Shrubs facilitate recruitment of Caragana stenophylla Pojark: microhabitat amelioration and protection against herbivory

  • Li-Na Xie
  • Hong-Yu Guo
  • Zhe Liu
  • Christopher A. Gabler
  • Wei-Zhong Chen
  • Song Gu
  • Cheng-Cang Ma
Original Paper


Key message

Mature Caragana stenophylla shrubs facilitated intraspecific sapling establishment by two mechanisms: microhabitat amelioration and protection against herbivory. Facilitation was mediated by climate, grazing, and sapling age.


Pre-existing shrubs could facilitate sapling establishment of woody plants; however, how these facilitation vary across abiotic and biotic stress gradients and the underlying mechanisms remain unclear.


The aim of this study is understanding the facilitation of shrub on sapling establishment and how the two underlying mechanisms, microhabitat amelioration and protection against herbivory, vary across climatic aridity gradients, grazing gradients, and sapling age.


We conducted field sowing experiments to examine the facilitation of mature Caragana stenophylla Pojark on intraspecific sapling establishment.


Facilitation of C. stenophylla on sapling survival increased as drought stress, grazing intensity, and sapling age increased. Microhabitat amelioration increased as drought stress and sapling age increased. Similarly, protection against herbivory increased as drought stress, grazing intensity, and sapling age increased. Relative importance of microhabitat amelioration increased as drought stress increased, and relative importance of protection against herbivory increased as grazing intensity and sapling age increased.


Facilitation of shrub on sapling establishment involves both microhabitat amelioration and protection against herbivory. Facilitation, the two mechanisms, and relative importance between the two mechanisms would all be affected by climatic aridity, grazing intensity, and sapling age. Shrub establishment has a positive feedback effect.


Climatic aridity gradient Grazing Sapling establishment Nurse plants Plant facilitation efficiency Stress gradient hypothesis 

Supplementary material

13595_2017_668_MOESM1_ESM.docx (358 kb)
ESM 1(DOCX 357 kb)
13595_2017_668_MOESM2_ESM.docx (17 kb)
ESM 2(DOCX 17 kb)


  1. Aerts R, November E, Borght I, Behailu M, Hermy M, Muys B (2006) Effects of pioneer shrubs on the recruitment of the fleshy-fruited tree Olea europaea ssp. cuspidata in Afromontane savanna. Appl Veg Sci 9:117–126CrossRefGoogle Scholar
  2. Aerts R, Negussie A, Maes W, November E, Hermy M, Muys B (2007) Restoration of dry Afromontane Forest using pioneer shrubs as nurse-plants for Olea europaea ssp. cuspidata. Restor Ecol 15:129–138CrossRefGoogle Scholar
  3. Ameztegui A, Coll L (2015) Herbivory and seedling establishment in Pyrenean forests: influence of micro- and meso-habitat factors on browsing pressure. Forest Ecol Manag 342:103–111CrossRefGoogle Scholar
  4. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686CrossRefGoogle Scholar
  5. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefPubMedGoogle Scholar
  6. Boulant N, Navas ML, Corcket E, Lepart J (2008) Habitat amelioration and associational defence as main facilitative mechanisms in Mediterranean grasslands grazed by domestic livestock. Ecoscience 15:407–415CrossRefGoogle Scholar
  7. Boulant N, Garnier A, Curt T, Lepart J (2009) Disentangling the effects of land use, shrub cover and climate on the invasion speed of native and introduced pines in grasslands. Divers Distrib 15:1047–1059CrossRefGoogle Scholar
  8. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Georges K, Liancourt P, Katja T, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34CrossRefGoogle Scholar
  9. Caldeira MC, Ibanez I, Nogueira C, Bugalho MN, Lecomte X, Moreira A, Pereira JS (2014) Direct and indirect effects of tree canopy facilitation in the recruitment of Mediterranean oaks. J Appl Ecol 51:349–358CrossRefGoogle Scholar
  10. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefPubMedGoogle Scholar
  11. Callaway RM, Kikodze D, Chiboshvili M, Khetsuriani L (2005) Unpalatable plants protect neighbors from grazing and increase plant community diversity. Ecology 86:1856–1862CrossRefGoogle Scholar
  12. Castro J, Zamora R, Hódar JA, Gómez JM, Gómez-Aparicio L (2004) Benefits of using shrubs as nurse plants for reforestation in Mediterranean mountains: a 4-year study. Restor Ecol 12:352–358CrossRefGoogle Scholar
  13. Cavieres LA, Badano EI, Sierra-Almeida A, Gómez-González S, Molina-Montenegro MA (2006) Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol 169:59–69CrossRefPubMedGoogle Scholar
  14. Chambers JC (2001) Pinus monophylla establishment in an expanding Pinus-Juniperus woodland: environmental conditions, facilitation and interacting factors. J Veg Sci 12:27–40CrossRefGoogle Scholar
  15. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308CrossRefGoogle Scholar
  16. Dong X, Zhang X, Bao X, Wang J (2009) Spatial distribution of soil nutrients after the establishment of sand-fixing shrubs on sand dune. Plant Soil Environ 55:288–294Google Scholar
  17. Gómez-Aparicio L (2009) The role of plant interactions in the restoration of degraded ecosystems: a meta-analysis across life-forms and ecosystems. J Ecol 97:1202–1214CrossRefGoogle Scholar
  18. Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138CrossRefGoogle Scholar
  19. Gómez-Aparicio L, Gómez JM, Zamora R, Boettinger JL (2005a) Canopy vs. soil effects of shrubs facilitating tree seedlings in Mediterranean montane ecosystems. J Veg Sci 16:191–198CrossRefGoogle Scholar
  20. Gómez-Aparicio L, Valladares F, Zamora R, Luis Quero J (2005b) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28:757–768CrossRefGoogle Scholar
  21. Gómez-Aparicio L, Zamora R, Castro J, Hódar JA (2008) Facilitation of tree saplings by nurse plants: microhabitat amelioration or protection against herbivores? J Veg Sci 19:161–172CrossRefGoogle Scholar
  22. Graff P, Aguiar MR, Chaneton EJ (2007) Shifts in positive and negative plant interactions along a grazing intensity gradient. Ecology 88:188–199CrossRefPubMedGoogle Scholar
  23. Grau O, Rautio P, Heikkinen J, Saravesi K, Kozlov MV, Markkola A (2010) An ericoid shrub plays a dual role in recruiting both pines and their fungal symbionts along primary succession gradients. Oikos 119:1727–1734CrossRefGoogle Scholar
  24. Guan LJ, Mei XF, Zhang YY, Han L, Li QF, Ma CC (2016) The temporal and spatial distribution of soil water and nutrient of Caragana stenophylla Nabkha in the different habitats of the Inner Mongolia Plateau. Arid Zone Res 33:253–259Google Scholar
  25. Gutiérrez JR, Holmgren M, Manrique R, Squeo FA (2007) Reduced herbivore pressure under rainy ENSO conditions could facilitate dryland reforestation. J Arid Environ 68:322–330CrossRefGoogle Scholar
  26. Harmer R, Kiewitt A, Morgan G, Gill R (2010) Does the development of bramble (Rubus fruticosus L. agg.) facilitate the growth and establishment of tree seedlings in woodlands by reducing deer browsing damage? Forestry 83: 93–102Google Scholar
  27. Hastwell GT, Facelli JM (2003) Differing effects of shade-induced facilitation on growth and survival during the establishment of a chenopod shrub. J Ecol 91:941–950CrossRefGoogle Scholar
  28. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706CrossRefPubMedGoogle Scholar
  29. Holl KD (2002) Effect of shrubs on tree seedling establishment in an abandoned tropical pasture. J Ecol 90:179–187CrossRefGoogle Scholar
  30. Holmgren M, Gómez-Aparicio L, Quero JL, Valladares F (2012) Non-linear effects of drought under shade: reconciling physiological and ecological models in plant communities. Oecologia 169:293–305CrossRefPubMedGoogle Scholar
  31. Holmgren M, Lin CY, Murillo JE, Nieuwenhuis A, Penninkhof J, Sanders N, Bart T, Veen H, Vasander H, Vollebregt ME (2015) Positive shrub–tree interactions facilitate woody encroachment in boreal peatlands. J Ecol 103:58–66CrossRefGoogle Scholar
  32. Jankju M (2013) Role of nurse shrubs in restoration of an arid rangeland: effects of microclimate on grass establishment. J Arid Environ 89:103–109CrossRefGoogle Scholar
  33. Legras EC, Vander Wall SB, Board DI (2010) The role of germination microsite in the establishment of sugar pine and Jeffrey pine seedlings. Forest Ecol Manag 260:806–813CrossRefGoogle Scholar
  34. Liu Z, Mei XF, Zhang W, Ma CC, Li QF (2016) The microclimate characteristics of Caragana stenophylla shrub canopy in desert region. Arid Zone Res 33:308–312Google Scholar
  35. López RP, Valdivia S, Sanjinés N, De la Quintana D (2007) The role of nurse plants in the establishment of shrub seedlings in the semi-arid subtropical Andes. Oecologia 152:779–790CrossRefPubMedGoogle Scholar
  36. Ma CC, Zhang JH, Guo HY, Li QF, Xie LN, Gao YB (2013) Alterations in canopy size and reproduction of Caragana stenophylla along a climate gradient on the Inner Mongolian Plateau. Flora 208:97–103CrossRefGoogle Scholar
  37. Maestre FT, Valladares F, Reynolds JF (2005) Is the change of plant-plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments. J Ecol 93:748–757CrossRefGoogle Scholar
  38. Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205CrossRefGoogle Scholar
  39. Maher KA, Hobbs RJ, Yates CJ (2010) Woody shrubs and herbivory influence tree encroachment in the sandplain heathlands of southwestern Australia. J Appl Ecol 47:441–450CrossRefGoogle Scholar
  40. Martínez ML (2003) Facilitation of seedling establishment by an endemic shrub in tropical coastal sand dunes. Plant Ecol 168:333–345CrossRefGoogle Scholar
  41. Meng M, Zhi Z (2004) Aridity index and its applications in geo-ecological study. Acta Phytoecologica Sin 28:853–861Google Scholar
  42. Otto R, Krüsi BO, Delgado JD, Fernández-Palacios JM, García-Del-Rey E, Arévalo JR (2010) Regeneration niche of the Canarian juniper: the role of adults, shrubs and environmental conditions. Ann Forest Sci 67:709CrossRefGoogle Scholar
  43. Petrou P, Milios E (2012) Establishment and survival of Pinus brutia Ten. seedlings over the first growing season in abandoned fields in central Cyprus. Plant Biosyst 146:522–533Google Scholar
  44. Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49CrossRefGoogle Scholar
  45. 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 152:265–273CrossRefPubMedGoogle Scholar
  46. Smit C, Ouden J, Díaz M (2008) Facilitation of Quercus ilex recruitment by shrubs in Mediterranean open woodlands. J Veg Sci 19:193–200CrossRefGoogle Scholar
  47. Tálamo A, Barchuk A, Cardozo S, Trucco C, MarÁs G, Trigo C (2015a) Direct versus indirect facilitation (herbivore mediated) among woody plants in a semiarid Chaco forest: a spatial association approach. Austral Ecol 40:573–580CrossRefGoogle Scholar
  48. Tálamo A, Barchuk AH, Garibaldi LA, Trucco CE, Cardozo S, Mohr F (2015b) Disentangling the effects of shrubs and herbivores on tree regeneration in a dry Chaco forest (Argentina). Oecologia 178:847–854CrossRefPubMedGoogle Scholar
  49. Tielbörger K, Kadmon R (2000) Temporal environmental variation tips the balance between facilitation and interference in desert plants. Ecology 81:1544–1553CrossRefGoogle Scholar
  50. Tíscar PA, Linares JC (2014) Large-scale regeneration patterns of Pinus nigra subsp. salzmannii: poor evidence of increasing facilitation across a drought gradient. Forests 5:1–20CrossRefGoogle Scholar
  51. Torres RC, Renison D (2015) Effects of vegetation and herbivores on regeneration of two tree species in a seasonally dry forest. J Arid Environ 121:59–66CrossRefGoogle Scholar
  52. Williams K, Westrick LJ, Williams B (2006) Effects of blackberry (Rubus discolor) invasion on oak population dynamics in a California savanna. Forest Ecol Manag 228:187–196CrossRefGoogle Scholar
  53. Xie LN, Guo HY, Gabler CA, Li QF, Ma CC (2015) Changes in spatial patterns of Caragana stenophylla along a climatic drought gradient on the Inner Mongolian Plateau. PLoS One 10:e0121234CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhao HL, Zhou RL, YZ S, Zhang H, Zhao LY, Drake S (2007) Shrub facilitation of desert land restoration in the Horqin Sand Land of Inner Mongolia. Ecol Eng 31:1–8CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS 2017

Authors and Affiliations

  • Li-Na Xie
    • 1
    • 2
  • Hong-Yu Guo
    • 1
  • Zhe Liu
    • 1
  • Christopher A. Gabler
    • 3
  • Wei-Zhong Chen
    • 1
  • Song Gu
    • 2
  • Cheng-Cang Ma
    • 1
  1. 1.Tianjin Key Laboratory of Animal and Plant Resistance, College of Life SciencesTianjin Normal UniversityTianjinChina
  2. 2.College of Life SciencesNankai UniversityTianjinChina
  3. 3.School of Earth, Environmental, and Marine Sciences and Department of BiologyUniversity of Texas Rio Grande ValleyBrownsvilleUSA

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