Skip to main content

Advertisement

SpringerLink
Log in

Effects of Quercus suber Decline on Woody Plant Regeneration: Potential Implications for Successional Dynamics in Mediterranean Forests

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

In the last two decades, widespread tree decline and mortality have been documented in forests worldwide. These mortality events usually show certain level of host-specificity, translating into rapid changes in the relative abundance of the adult community. Despite these short-term changes, it is poorly understood whether the decline and mortality of certain tree species are likely to result in long-term vegetation shifts. Trajectories of forest recovery and the probability of occurrence of permanent vegetation shifts are to a large extent determined by post-mortality regeneration dynamics. Using a spatially explicit neighborhood approach, we evaluated the spatial patterns of natural regeneration of the woody plant community in mixed Mediterranean forests affected by the decline of their dominant tree species, Quercus suber. We predicted the abundance, survival, and richness of the seedling and sapling bank as a function of the distribution and health status of the tree and shrub community. Results indicated that Q. suber decline had detectable effects on seedlings and saplings of coexistent woody species from very different functional groups (trees, shrubs, and lianas). The sign and magnitude of these effects varied substantially among coexistent species, which could imply shifts in the species ranking of seedling and sapling abundance, affecting successional trajectories and potentially leading to vegetation shifts. Because most of these changes pointed towards a loss of dominance of Q. suber, management strategies are urgently needed in order to attenuate adult mortality or promote its regeneration, counteracting the negative effects of global change drivers (exotic pathogens, climate change) on these valuable forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

REFERENCES

  • Acácio V, Holmgren M, Jansen PA, Schrotter O. 2007. Multiple recruitment limitation causes arrested succession in Mediterranean cork oak systems. Ecosystems 10:1220–30.

    Article  Google Scholar 

  • Allen CD, Breshears DD. 1998. Drought-induced shift of a forest–woodland ecotone: rapid landscape response to climate variation. Proceedings of the National Academy of Sciences 95:14839–42.

    Article  CAS  Google Scholar 

  • Allen CD, Breshears DD, McDowell NG. 2015. On understimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:129.

    Article  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259:660–84.

    Article  Google Scholar 

  • Amoroso MM, Suarez ML, Daniels LD. 2012. Nothofagus dombeyi regeneration in declining Austrocedrus chilensis forests: effects of overstory mortality and climatic events. Dendrochronologia 30:105–12.

    Article  Google Scholar 

  • Anonymous. 2005. PORN/PRUG/PDS Parque Natural de los Alcornocales. Sevilla: Junta de Andalucía, Consejeria de Medio Ambiente.

    Google Scholar 

  • Aronson J, Pereira JS, Pausas JG. 2009. Cork oak woodlands on the edge: ecology, adaptive management, and restoration. Washington DC: Island Press.

    Google Scholar 

  • Axelson JN, Alfaro RI, Hawkes BC. 2009. Influence of fire and mountain pine beetle on the dynamics of lodgepole pine stands in British Columbia, Canada. Forest Ecology and Management 257:1874–82.

    Article  Google Scholar 

  • Baribault TW, Kobe RK. 2011. Neighbour interactions strengthen with increased soil resources in a northern hardwood forest. Journal of Ecology 99:1358–72.

    Article  Google Scholar 

  • Battles JJ, Fahey TJ. 2000. Gap dynamics following forest decline: a case study of red spruce forests. Ecological Applications 10:760–74.

    Article  Google Scholar 

  • Bonanomi G, Rietkerk M, Dekker SC, Mazzoleni S. 2008. Islands of fertility induce co-occurring negative and positive plant-soil feedbacks promoting coexistence. Plant Ecology 197:207–18.

    Article  Google Scholar 

  • Brasier C. 1992. Oak tree mortality in Iberia. Nature 360:539.

    Article  Google Scholar 

  • Brasier CM. 1996. Phytophthora cinnamomi and oak decline in southern Europe. environmental constraints including climate change. Annales Des Sciences Forestieres 53:347–58.

    Article  Google Scholar 

  • Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT. 2009. Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Frontiers in Ecology and the Environment 7:185–9.

    Article  Google Scholar 

  • Brown LB, Allen-Diaz B. 2009. Forest stand dynamics and sudden oak death: mortality in mixed-evergreen forests dominated by coast live oak. Forest Ecology and Management 257:1271–80.

    Article  Google Scholar 

  • Burnham KP, Anderson DR, Eds. 2002. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer.

    Google Scholar 

  • Cahill DM, Rookes JE, Wilson BA, Gibson L, McDougall KL. 2003. Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control. Australian Journal of Botany 56:279–310.

    Article  Google Scholar 

  • Canham CD, Uriarte M. 2006. Analysis of neighborhood dynamics of forest ecosystems using likelihood methods and modeling. Ecological Applications 16:62–73.

    Article  PubMed  Google Scholar 

  • Carnicer J, Coll M, Ninyerola M, Pons X, Sanchez G, Peñuelas J. 2011. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences of the United States of America 108:1474–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catovsky S, Bazzaz FA. 2002. Feedbacks between canopy composition and seedling regeneration in mixed conifer broad-leaved forests. Oikos 98:403–20.

    Article  Google Scholar 

  • Coates KD, Canham CD, LePage PT. 2009. Above- versus below-ground competitive effects and responses of a guild of temperate tree species. Journal of Ecology 97:118–30.

    Article  Google Scholar 

  • Collins BJ, Rhoades CC, Hubbard RM, Battaglia MA. 2011. Tree regeneration and future stand development after bark beetle infestation and harvesting in Colorado lodgepole pine stands. Forest Ecology and Management 261:2168–75.

    Article  Google Scholar 

  • Connell JH. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell G, Eds. Dynamics of populations. PUDOC, 298:312.

  • DeRose RJ, Long JN. 2010. Regeneration response and seedling bank dynamics on a Dendroctonus rufipennis-killed Picea engelmannii landscape. Journal of Vegetation Science 21:377–87.

    Article  Google Scholar 

  • Diskin M, Rocca ME, Nelson KN, Aoki CF, Romme W. 2011. Forest developmental trajectories in mountain pine beetle disturbed forests of Rocky Mountain National Park, Colorado. Canadian Journal of Forest Research 41:782–92.

    Article  Google Scholar 

  • Edwards AWF, Ed. 1992. Likelihood-expanded edition. Baltimore: Johns Hopkins University Press.

    Google Scholar 

  • Fensham RJ, Holman JE. 1999. Temporal and spatial patterns in drought-related tree dieback in Australian savanna. Journal of Applied Ecology 36:1035–50.

    Article  Google Scholar 

  • Fetcher N, Oberbauer S, Strain B. 1985. Vegetation effects on microclimate in lowland tropical forest in Costa Rica. International Journal of Biometeorology 29:145–55.

    Article  Google Scholar 

  • Frelich LE, Reich PB. 1995. Neighborhood effects, disturbance, and succession in forests of the western Great Lakes region. Ecoscience 2:148–58.

    Article  Google Scholar 

  • Galiano L, Martínez-Vilalta J, Eugenio M, Granzow-de la Cerda Í, Lloret F. 2013. Seedling emergence and growth of Quercus spp. following severe drought effects on a Pinus sylvestris canopy. Journal of Vegetation Science 24:580–8.

    Article  Google Scholar 

  • García LV, Ramo C, Aponte C, Moreno A, Domínguez MT, Gómez-Aparicio L, Redondo R, Marañón T. 2011. Protected wading bird species threaten relict centenarian cork oaks in a Mediterranean Biosphere Reserve: a conservation management conflict. Biological Conservation 144:764–71.

    Article  Google Scholar 

  • Goffe WL, Ferrier GD, Rogers J. 1994. Global optimization of statistical functions with simulated annealing. Journal of Econometrics 60:65–99.

    Article  Google Scholar 

  • Gómez-Aparicio L. 2008. Spatial patterns of recruitment in Mediterranean plant species: linking the fate of seeds, seedlings and saplings in heterogeneous landscapes at different scales. Journal of Ecology 96:1128–40.

    Article  Google Scholar 

  • Gómez-Aparicio L, Canham CD, Martin PH. 2008a. Neighbourhood models of the effects of the invasive Acer platanoides on tree seedling dynamics: linking impacts on communities and ecosystems. Journal of Ecology 96:78–90.

    Google Scholar 

  • Gómez-Aparicio L, Ibáñez B, Serrano MS, De Vita P, Ávila JM, Pérez-Ramos IM, García LV, Esperanza Sánchez M, Marañón T. 2012. Spatial patterns of soil pathogens in declining Mediterranean forests: implications for tree species regeneration. New Phytologist 194:1014–24.

    Article  PubMed  Google Scholar 

  • Gómez-Aparicio L, Pérez-Ramos IM, Mendoza I, Matias L, Quero JL, Castro J, Zamora R, Marañón T. 2008b. Oak seedling survival and growth along resource gradients in Mediterranean forests: implications for regeneration in current and future environmental scenarios. Oikos 117:1683–99.

    Article  Google Scholar 

  • Ibáñez B, Gómez-Aparicio L, Stoll P, Ávila JM, Pérez-Ramos IM, Marañón T. 2015. A neighborhood analysis of the consequences of Quercus suber decline for regeneration dynamics in Mediterranean forests. PLoS ONE 10:e0117827.

    Article  PubMed  PubMed Central  Google Scholar 

  • Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501–28.

    Article  Google Scholar 

  • Johnson JB, Omland KS. 2004. Model selection in ecology and evolution. Trends Ecology & Evolution 19:101–8.

    Article  Google Scholar 

  • Kayes LJ, Tinker DB. 2012. Forest structure and regeneration following a mountain pine beetle epidemic in southeastern Wyoming. Forest Ecology and Management 263:57–66.

    Article  Google Scholar 

  • Koepke DF, Kolb TE, Adams HD. 2010. Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163:1079–90.

    Article  PubMed  Google Scholar 

  • Legendre P, Fortin MJ. 1989. Spatial pattern and ecological analysis. Vegetatio 80(2):107–38.

    Article  Google Scholar 

  • Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F. 2012. Extreme climatic events and vegetation: the role of stabilizing processes. Global Change Biology 18:797–805.

    Article  Google Scholar 

  • Loo J. 2009. Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biological Invasions 11:81–96.

    Article  Google Scholar 

  • Matías L, Zamora R, Castro J. 2012. Sporadic rainy events are more critical than increasing of drought intensity for woody species recruitment in a Mediterranean community. Oecologia 169:833–44.

    Article  PubMed  Google Scholar 

  • McDowell NG, Ryan MG, Zeppel MJB, Tissue DT. 2013. Feature: improving our knowledge of drought-induced forest mortality through experiments, observations, and modeling. New Phytologist 200:289–93.

    Article  PubMed  Google Scholar 

  • Mendoza I, Gómez-Aparicio L, Zamora R, Matías L. 2009. Recruitment limitation of forest communities in a degraded Mediterranean landscape. Journal of Vegetation Science 20:367–76.

    Article  Google Scholar 

  • Mueller RC, Scudder CM, Porter ME, Talbot Trotter R, Gehring CA, Whitham TG. 2005. Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts. Journal of Ecology 93:1085–93.

    Article  Google Scholar 

  • Murphy L 2012. Likelihood: methods for maximum likelihood estimation. R package version 1.6.

  • Nigh GD, Antos JA, Parish R. 2008. Density and distribution of advance regeneration in mountain pine beetle killed lodgepole pine stands of the Montane Spruce zone of southern British Columbia. Canadian Journal of Forest Research 38:2826–36.

    Article  Google Scholar 

  • Ojeda F, Marañón T, Arroyo J. 1996. Patterns of ecological, chorological and taxonomic diversity at both sides of the Strait of Gibraltar. Journal of Vegetation Science 7:63–72.

    Article  Google Scholar 

  • Pérez-Ramos IM, Marañón T. 2008. Factors affecting post-dispersal seed predation in two coexisting oak species: microhabitat, burial and exclusion of large herbivores. Forest Ecology and Management 255:3506–14.

    Article  Google Scholar 

  • Pérez-Ramos IM, Marañón T. 2012. Community-level seedling dynamics in Mediterranean forests: uncoupling between the canopy and the seedling layers. Journal of Vegetation Science 23:526–40.

    Article  Google Scholar 

  • Pérez-Ramos IM, Urbieta IR, Zavala MA, Marañón T. 2012. Ontogenetic conflicts and rank reversals in two Mediterranean oak species: implications for coexistence. Journal of Ecology 100:467–77.

    Article  Google Scholar 

  • Pulido FJ, Díaz M. 2005. Regeneration of a Mediterranean oak: a whole-cycle approach. Ecoscience 12:92–102.

    Article  Google Scholar 

  • R Development Core Team. 2009. R: A language and environment for statistical computing. Vienna: R Foundation for statistical Computing.

    Google Scholar 

  • Ramage BS, Forrestel AB, Moritz MA, O’Hara KL. 2012. Sudden oak death disease progression across two forest types and spatial scales. Journal of Vegetation Science 23:151–63.

    Article  Google Scholar 

  • Redmond MD, Barger NN. 2013. Tree regeneration following drought-and insect-induced mortality in piñon–juniper woodlands. New Phytologist. doi:10.1111/nph.12366.

    PubMed  Google Scholar 

  • Rey PJ, Alcántara JM. 2000. Recruitment dynamics of a fleshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. Journal of Ecology 88:622–33.

    Article  Google Scholar 

  • Romero MA, Sanchez JE, Jimenez JJ, Belbahri L, Trapero A, Lefort F, Sanchez ME. 2007. New Pythium taxa causing root rot on Mediterranean Quercus species in South-West Spain and Portugal. Journal of Phytopathology 155:289–95.

    Article  Google Scholar 

  • Royer PD, Cobb NS, Clifford MJ, Huang C-Y, Breshears DD, Adams HD, Villegas JC. 2011. Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. Journal of Ecology 99:714–23.

    Article  Google Scholar 

  • Sánchez M, Caetano P, Romero M, Navarro R, Trapero A. 2006. Phytophthora root rot as the main factor of oak decline in southern Spain. In, Progress in research on Phytophthora diseases of forest trees. Farnham, UK: Forest Research, p 149–154.

  • Sánchez ME, Caetano P, Ferraz J, Trapero A. 2002. Phytophthora disease of Quercus ilex in south-western Spain. Forest Pathology 32:5–18.

    Article  Google Scholar 

  • Suarez ML, Kitzberger T. 2008. Recruitment patterns following a severe drought: long-term compositional shifts in Patagonian forests. Canadian Journal of Forest Research 38:3002–10.

    Article  Google Scholar 

  • Tuset JJ, Sánchez G. 2004. La Seca: El decaimiento de encinas, alcornoques y otros Quercus en España. Organismo Autónomo de Parques Nacionales, Madrid: Ministerio de Medio Ambiente.

    Google Scholar 

  • Urbieta IR, Zavala MA, Marañón T. 2008. Human and non-human determinants of forest composition in southern Spain: evidence of shifts towards cork oak dominance as a result of management over the past century. Journal of Biogeography 35:1688–700.

    Article  Google Scholar 

  • Van Breemen N, Finzi A. 1998. Plant-soil interactions: ecological aspects and evolutionary implications. Biogeochemistry 42:1–19.

    Article  Google Scholar 

  • Van Mantgem PJ, Stephenson NL. 2007. Apparent climatically induced increase of tree mortality rates in a temperate forest. Ecology Letters 10:909–16.

    Article  PubMed  Google Scholar 

  • Van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH. 2009. Widespread increase of tree mortality rates in the western United States. Science 323:521–4.

    Article  PubMed  Google Scholar 

  • Veblen TT, Hadley KS, Reid MS, Rebertus AJ. 1991. The response of subalpine forests to spruce beetle outbreak in Colorado. Ecology 72:213–31.

    Article  Google Scholar 

  • Vyse A, Ferguson C, Huggard DJ, Roach J, Zimonick B. 2009. Regeneration beneath lodgepole pine dominated stands attacked or threatened by the mountain pine beetle in the south central Interior, British Columbia. Forest Ecology and Management 258:S36–43.

    Article  Google Scholar 

  • Wilson JB, Agnew AD. 1992. Positive-feedback switches in plant communities. London: Academic Press.

    Book  Google Scholar 

Download references

ACKNOWLEDGMENTS

We thank the director and technicians of Los Alcornocales Natural Park for the facilities and support to carry out the field work. We are also indebted to Eduardo Gutiérrez, Ana Pozuelos, Luis V. García, and several students for invaluable laboratory and field assistance. This research was supported by the Ministerio de Ciencia e Innovación (MICIIN) projects INTERBOS (CGL2008-04503-C03-03), DIVERBOS (CGL2011-30285-C02-01), RETROBOS (CGL2011-26877), and RESTECO (CGL2014-52858-R), and the Junta de Andalucía project ANASINQUE (PGC2010-RNM-5782). BI was supported by a Formación de Personal Investigador (FPI)-MICINN Grant, J.M.A. by a Formación de Personal Universitario (FPU)-MEC Grant, and I.M.P.R. by a JAEdoc-Consejo Superior de Investigaciones Científicas (CSIC) contract.

Author information

Authors and Affiliations

  1. Instituto de Recursos Naturales y Agrobiología (IRNAS, CSIC), PO Box 1052, 41080, Seville, Spain

    Beatriz Ibáñez, Lorena Gómez-Aparicio, José M. Ávila, Ignacio M. Pérez-Ramos & Teodoro Marañón

Authors
  1. Beatriz Ibáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lorena Gómez-Aparicio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José M. Ávila
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ignacio M. Pérez-Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Teodoro Marañón
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Beatriz Ibáñez.

Additional information

Author Contributions

BI and LGA designed the study. BI, LGA, JMA and IMP performed the research. BI analyzed the data. BI led the writing of the paper with inputs from LGA, JMA, IMP and TM.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 238 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ibáñez, B., Gómez-Aparicio, L., Ávila, J.M. et al. Effects of Quercus suber Decline on Woody Plant Regeneration: Potential Implications for Successional Dynamics in Mediterranean Forests. Ecosystems 20, 630–644 (2017). https://doi.org/10.1007/s10021-016-0044-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-016-0044-5

Keywords

Search

Navigation