Abstract
In forest communities, conspecific density/distance dependence (CDD) is an important factor regulating diversity. It remains unknown how and the extent to which gap creation alters the mode and strength of CDD via changes in the relative importance of pathogens and mycorrhizae. Seeds of two hardwoods (i.e., Acer mono associated with arbuscular mycorrhizae [AM] and Quercus serrata associated with ectomycorrhizae [EM]) were sown reciprocally at four distances from the boundary between Acer- and Quercus-dominated forests towards forest interior in each of forest understories (FUs) and gaps. The causes of seed and seedling mortality, seedling growth and colonization of mycorrhizal fungi were investigated. In Acer, seed and seedling mortality were highest in Acer forests and gradually decreased towards the interior of Quercus forests in FU, mainly due to severe attack of soil pathogens, invertebrates, and leaf diseases. The reverse was true in gaps, due to reduction of damping-off damage caused by distance-dependent colonization of AM. In Quercus, most seeds and seedlings were eaten by vertebrates in FUs. The seedling mortality caused by leaf diseases was not high, even beneath conspecific forests with higher colonization of EM in gaps, suggesting a positive EM influence. In both species, seedling mass was greatest in conspecific forests and gradually decreased towards the interior of heterospecific forests in gaps, due to higher colonization of mycorrhizae near conspecifics. In conclusion, light conditions strongly altered the mode of CDD via changes in relative influence of pathogens and mycorrhizae, suggesting that gap creation may regulate species diversity via changes in the mode of CDD.
Similar content being viewed by others
References
Abe S, Masaki T, Nakashizuka T (1995) Factors influencing sapling composition in canopy gaps of a temperate deciduous forest. Vegetatio 120:21–32. https://doi.org/10.1007/BF00033455
Agrios GN (1997) Plant pathology, 4th edn. Academic Press, London, UK
Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant–soil feedback and its implications for plant abundance. Ecol Lett 17:1613–1621. https://doi.org/10.1111/ele.12378
Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712. https://doi.org/10.2307/1937766
Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical seedlings: experimental studies of the effects of dispersal distances, seedling density, and light conditions. Oecologia 61:211–217. https://doi.org/10.1007/BF00396763
Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88. https://doi.org/10.1038/nature12911
Bardgett RD, Wardle DA (2010) Aboveground–belowground linkages biotic interactions, ecosystem processes, and global change. Oxford University Press, New York
Bayandala, Fukasawa Y, Seiwa K (2016) Roles of pathogens on replacement of tree seedlings in heterogeneous light environments in a temperate forest: a reciprocal seed sowing experiment. J Ecol 104:765–772. https://doi.org/10.1111/1365-2745.12552
Bayandala, Masaka K, Seiwa K (2017) Leaf diseases facilitate the Janzen–Connell mechanism regardless of light conditions: a 3-year field study. Oecologia 83:191–199. https://doi.org/10.1007/s00442-016-3757-4
Bennett JA, Klironomos J (2018) Climate, but not trait, effects on plant–soil feedback depend on mycorrhizal type in temperate forests. Ecosphere 9:e02132. https://doi.org/10.1002/ecs2.2132
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Bever JD (2002a) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290. https://doi.org/10.1023/A:102022160
Bever JD (2002b) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B Biol Sci 269:2595–2601. https://doi.org/10.1098/rspb.2002.2162
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004
Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325. https://doi.org/10.1146/annurev-ecolsys-112414-054306
Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR Monograph, Canberra, pp 120–290
Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335. https://doi.org/10.1146/annurev.ecolsys.27.1.305
Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332. https://doi.org/10.1126/science.1190772
Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19:383–392. https://doi.org/10.1111/ele.12570
Craig ME, Turner BL, Liang C, Clay K, Johnson DJ, Phillips RP (2018) Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Glob Chang Biol 24:3317–3330
Crawley MJ (2005) Statistics, an introduction using R. Wiley, New York
Denslow JS (1987) Tropical rain forest gaps and tree species diversity. Annu Rev Ecol Syst 18:431–451. https://doi.org/10.1146/annurev.es.18.110187.002243
Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255. https://doi.org/10.1111/j.1365-2745.2005.00977.x
Dickie IA, Koide RT, Steiner KC (2002) Influence of established trees on mycorrhizas, nutrition, and growth of Quercus rubra seedlings. Ecol Monogr 72:505–521. https://doi.org/10.1890/0012-9615(2002)072[0505:IOETOM]2.0.CO;2
Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–160. https://doi.org/10.1139/cjb-2013-0091
Ferguson JJ, Menge JA (1982) The influence of light intensity and artificially extended photoperiod upon infection and sporulation of Glomus fasciculatus on sudan grass and on root exudation of sudan grass. New Phytol 92:183–191. https://doi.org/10.1111/j.1469-8137.1982.tb03375.x
Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA), version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University, The Institute of Ecosystem Studies, Milbrook, Burnaby
Fricke EC, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17:593–598. https://doi.org/10.1111/ele.12261
Gehring CA, Connel JH (2006) Arbuscular mycorrhizal fungi in the tree seedlings of two Australian rain forests: occurrence, colonization, and relationships with plant performance. Mycorrhiza 16:89–98. https://doi.org/10.1007/s00572-005-0018-5
Hobbie EA, Hogberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382. https://doi.org/10.1111/j.1469-8137.2012.04300.x
Hood LA, Swaine MD, Mason PA (2004) The influence of spatial patterns of damping-off disease and arbuscular mycorrhizal colonization on tree seedling establishment in Ghanaian tropical forest soil. J Ecol 92:816–823. https://doi.org/10.1111/j.0022-0477.2004.00917.x
Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge D, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922
Horst RK (2001) Westcott’s plant disease handbook, 6th edn. Kluwer Academic Publishers, Norwell
Ibáñez I, McCarthy-Neumann S (2016) Effects of mycorrhizal fungi on tree seedling growth: quantifying the parasitism-mutualism transition along a light gradient. Can J For Res 46:48–57. https://doi.org/10.1139/cjfr-2015-0327
Imaji A, Seiwa K (2010) Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species. Oecologia 162:273–281. https://doi.org/10.1007/s00442-009-1453-3
Ishizuka M, Sugawara S (1989) Composition and structure of natural mixed forests in central Hokkaido (II). Effects of disturbances on the forest vegetation patterns along the topographic moisture gradients. J Jpn For Soc 71:89–98. https://doi.org/10.11519/jjfs1953.71.3_89
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528. https://doi.org/10.1086/282687
Jo I, Potter KM, Domke GM, Fei S (2017) Dominant forest tree mycorrhizal type mediates understory plant invasions. Ecol Lett 21:217–224. https://doi.org/10.1111/ele.12884
John MK (1970) Colorimetric determination of phosphorus in soil and plant materials with ascorbic acid. Soil Sci 109:214–220. https://doi.org/10.1097/00010694-197004000-00002
Johnson DJ, Clay K, Phillips RP (2018) Mycorrhizal associations and the spatial structure of an old-growth forest community. Oecologia 186:195–204. https://doi.org/10.1007/s00442-017-3987-0
Kikuzawa K (1988) Dispersal of Quercus mongolica acorns in a broad-leaved deciduous forest. 1: Disappearance. For Ecol Manage 25:1–8. https://doi.org/10.1016/0378-1127(88)90129-6
Kishi K (1998) Plant diseases in Japan. Zenkoku Noson Kyoiku Kyokai, Tokyo, Japan
Kobe RK (1999) Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80:187–201. https://doi.org/10.1890/0012-9658(1999)080[0187:LGPATT]2.0.CO;2
Komiyama T, Niizuma S, Fujisawa E, Morikuni H (2009) The rapid methods of total soil phosphorus analysis. Jpn Soc Soil Sci Plant Nutr 80:616–620. https://doi.org/10.20710/dojo.80.5_516
Konno M, Iwamoto S, Seiwa K (2011) Specialization of a fungal pathogen on host tree species in a cross-inoculation experiment. J Ecol 99:1394–1401. https://doi.org/10.1111/j.1365-2745.2011.01869.x
Kotanen PM (2007) Effects of fungal seed pathogens under conspecific and heterospecific trees in a temperate forest. Can J Bot 85:918–925. https://doi.org/10.1139/B07-088
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. https://doi.org/10.1111/j.1461-0248.2008.01209.x
LaManna JA, Mangan SA, Alonso A, Bourg NA, Brockelman WY, Bunyavejchewin S, Chang L-W, Chiang J-M, Chuyong GB, Clay K, Condit R, Cordell S, Davies SJ, Furniss TJ, Giardina CP, Gunatilleke IAUN, Gunatilleke CVS, Fangliang H, Howe RW, Hubbell SP, Hsieh C-F, Inman-Narahari FM, Janík D, Johnson DJ, Kenfack D, Korte L, Král K, Larson AJ, Lutz JA, McMahon SM, McShea WJ, Memiaghe HR, Nathalang A, Novotny V, Ong PS, Orwig DA, Ostertag R, Parker GC, Phillips RP, Sack L, Sun I-F, Tello JS, Thomas DW, Turner BL, Vela Díaz DM, Vrška T, Weiblen GD, Wolf A, Yap S, Myers JA (2017) Plant diversity increases with the strength of negative density dependence at the global scale. Science 356:1389–1392. https://doi.org/10.1126/science.aam5678
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748. https://doi.org/10.1126/science.1143082
Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010a) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. https://doi.org/10.1038/nature09273
Mangan SA, Herre EA, Bever JD (2010b) Specificity between neotropical tree seedlings and their fungal mutualists leads to plant–soil feedback. Ecology 91:2594–2603. https://doi.org/10.1890/09-0396.1
McCarthy MA (2007) Bayesian methods for ecology. Cambridge University Press, Cambridge
McCarthy-Neumann S, Ibáñez I (2013) Plant–soil feedback links negative distance dependence and light gradient partitioning during seedling establishment. Ecology 94:780–786. https://doi.org/10.1890/12-1338.1
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
McGuire KL (2007) Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–574. https://doi.org/10.1890/05-1173
Mizui N (1991) Classification of seed production based on the correlation between seed weight and seed number in deciduous broad-leaved tree species. J Jpn For Soci 73:258–263
Nara K (2006) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol 169:169–178. https://doi.org/10.1111/j.1469-8137.2005.01545.x
Nathan R, Casagrandi R (2004) A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen–Connell and beyond. J Ecol 92:733–746. https://doi.org/10.1111/j.0022-0477.2004.00914.x
O’Hanlon-Manners DL, Kotanen PM (2004) Evidence that fungal pathogens inhibit recruitment of a shade-intolerant tree, white birch (Betula papyrifera), in understory habitats. Oecologia 140:650–653. https://doi.org/10.1007/s00442-004-1625-0
Pacala SW, Canham CD, Saponara J, Silande JA Jr, Kobe RK, Ribbens E (1996) Forest models defined by field measurements: estimation, error analysis and dynamics. Ecol Monogr 66:1–43. https://doi.org/10.2307/2963479
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal associated nutrient economy: a new framework for predicting carbon nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221
R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. https://www.R-project.org
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457. https://doi.org/10.1111/j.1469-8137.2006.01715.x
Sasaki T, Konno M, Hasegawa Y, Imaji A, Terabaru M, Nkamura R, Ohra N, Matsukura K, Seiwa K (2019) Role of mycorrhizal associations in ontogenetic changes in spatial distribution patterns of hardwoods in an old-growth forest. Oecologia 189:971–980. https://doi.org/10.1007/s00442-019-04376-2
Seiwa K (1998) Advantages of early germination for growth and survival of seedlings of Acer mono under different overstorey phenologies in deciduous broad-leaved forests. J Ecol 86:219–228. https://doi.org/10.1046/j.1365-2745.1998.00245.x
Seiwa K, Kikuzawa K (1996) Importance of seed size for establishment of seedlings of five deciduous broad-leaved tree species. Vegetatio 123:51–64. https://doi.org/10.1007/BF00044887
Seiwa K, Miwa Y, Sahashi N, Kanno H, Tomita M, Ueno N, Yamazaki M (2008) Pathogen attack and spatial patterns of juvenile mortality and growth in a temperate tree, Prunus grayana. Can J For Res 38:2445–2454. https://doi.org/10.1139/X08-084
Seiwa K, Masaka K, Konno M, Iwamoto S (2019) Role of seed size and relative abundance in conspecific negative distance-dependent seedling mortality for eight tree species in a temperate forest. For Ecol Manag 453:117537
Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modeling. Fungal Biol Rev 26:39–60. https://doi.org/10.1016/j.fbr.2012.01.001
Smith LM, Reynolds HL (2015) Plant–soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96:2523–2532. https://doi.org/10.1890/14-2150.1
Terborgh J (2012) Enemies maintain hyperdiverse tropical forests. Am Nat 179:303–314. https://doi.org/10.1086/664183
Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant–soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176. https://doi.org/10.1126/science.aai8291
van der Putten WH (2017) Belowground drivers of plant diversity. Science 355:134–135. https://doi.org/10.1126/science.aal4549
Yamazaki M, Iwamoto S, Seiwa K (2009) Distance- and density-dependent seedling mortality caused by several diseases in eight tree species co-occurring in a temperate forest. For Ecol 201:181–196. https://doi.org/10.1007/s11258-008-9531-x
Acknowledgements
We are very grateful to two anonymous reviewers, who provided useful comments on the article. We thank Tomonori Sasaki and members of the Laboratory of Forest Ecology, Tohoku University, for help with the experiments.
Funding
This research was funded by the Ministry of Education, Culture, Sports, Science and Technology, Japan (No. 23380079 to KS).
Author information
Authors and Affiliations
Contributions
KS conceived of the idea. W, B, YF, KMat and KS collected the data in the field. KMas, W and KS performed the analyses. W and KS wrote the initial draft. All authors wrote and edited the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Casey P. terHorst.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wulantuya, Masaka, K., Bayandala et al. Gap creation alters the mode of conspecific distance-dependent seedling establishment via changes in the relative influence of pathogens and mycorrhizae. Oecologia 192, 449–462 (2020). https://doi.org/10.1007/s00442-020-04596-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04596-x