Skip to main content
Log in

Pathogen-Induced Tree Mortality Modifies Key Components of the C and N Cycles with No Changes on Microbial Functional Diversity

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

An increase in tree mortality rates as a consequence of biotic disturbances has been detected worldwide. Biotic disturbances in forests might cause significant impacts at ecosystem-level, with strong effects on soil biological activity and organic matter transformation. However, very few empirical studies have explored to date the consequences of biotic disturbances for soil microbial communities and C and N cycles. Here, we assessed the effects of Quercus suber dieback, caused by the exotic root pathogen Phytophthora cinnamomi, on the soil microbial community and key components of the C and N cycle. We used a spatially explicit neighborhood approach to analyze the effects of Q. suber trees with different health status and non-declining coexistent species on soil variables. The study was replicated in the two main Q. suber forest types of the region (closed forests and open woodlands) with contrasting soil texture characteristics. Pathogen-induced tree dieback did not affect microbial functional diversity or biomass, but translated into lower soil microbial respiration. Tree mortality induced changes in several variables of the C and N cycle, but the sign and magnitude of these effects varied depending on the local characteristics of soil texture. Coexistent species differed strongly from Q. suber in their effects on the C and N cycle. Overall, our results show that tree dieback due to invasive pathogens translates into complex short- and long-term effects on different components of the C and N cycles, despite no effects on microbial functional diversity and biomass.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

Data Availability

All data used for tables and figures in the main text and in Supporting information are accessible at https://doi.org/10.17632/y8k3fddnz2.1.

References

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

    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. For Ecol Manag 259:660–84.

    Google Scholar 

  • Allison FE. 1973. Nonbiological Immobilization of Nitrogen. Developments in Soil Science, Volume 3. Soil Organic Matter and Its Role in Crop Production. Amsterdam: Elsevier. pp 206–29.

  • Aponte C, García LV, Pérez-Ramos IM, Gutiérrez E, Marañón T. 2011. Oak trees and soil interactions in Mediterranean forests: A positive feedback model. J Veg Sci 22:856–67.

    Google Scholar 

  • Ávila JM, Gallardo A, Ibáñez B, Gómez-Aparicio L. 2016. Quercus suber dieback alters soil respiration and nutrient availability in Mediterranean forests. J Ecol 104:1441–52.

    Google Scholar 

  • Ávila JM, Linares JC, García-Nogales A, Sánchez ME, Gómez-Aparicio L. 2017. Across-scale patterning of plant–soil–pathogen interactions in Quercus suber decline. Eur J Forest Res 136:677–88.

    Google Scholar 

  • Banning NC, Lalor BM, Cookson WR, Grigg AH, Murphy DV. 2012. Analysis of soil microbial community level physiological profiles in native and post-mining rehabilitation forest: Which substrates discriminate? Appl Soil Ecol 56:27–34.

    Google Scholar 

  • Bardgett RD, Wardle DA. 2010. Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. New York: Oxford University Press.

    Google Scholar 

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

    Google Scholar 

  • Bell T, Gessner MO, Griffiths RI, McLaren JR, Morin PJ, van der Heijden M, van der Putten W. 2009. Microbial biodiversity and ecosystem functioning under controlled conditions and in the wild. In: Biodiversity, ecosystem functioning, and human wellbeing: an ecological and economic perspective. Oxford University Press: Oxford. pp 121–33.

  • Boyden S, Montgomery R, Reich PB, Palik B. 2012. Seeing the forest for the heterogeneous trees: stand-scale resource distributions emerge from tree-scale structure. Ecol Appl 22:1578–88.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS. 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–42.

    CAS  Google Scholar 

  • Burnham KP, Anderson DR. 2002. Model selection and multi-model inference: a practical information-theoretic approach. Secaucus: Springer.

    Google Scholar 

  • Cai YF, Barber P, Dell B, O’Brien P, Williams N, Bowen B, Hardy G. 2010. Soil bacterial functional diversity is associated with the decline of Eucalyptus gomphocephala. For Ecol Manag 260:1047–57.

    Google Scholar 

  • Camilo-Alves CSP, da Clara MIE, Ribeiro NA. 2013. Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. Eur J Forest Res 132:411–32.

    Google Scholar 

  • Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM. 2003. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–9.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Case MF, Staver AC. 2018. Soil texture mediates tree responses to rainfall intensity in African savannas. New Phytol 219:1363–72.

    PubMed  Google Scholar 

  • Cobb RC, Eviner VT, Rizzo DM. 2013. Mortality and community changes drive sudden oak death impacts on litterfall and soil nitrogen cycling. New Phytol 200:422–31.

    CAS  PubMed  Google Scholar 

  • Creamer RE, Stone D, Kuiper I, Berry P. 2016. Measuring respiration profiles of soil microbial communities across Europe using MicroRespTM method. Appl Soil Ecol Sect Agric Ecosyst Environ 97:36–43.

    Google Scholar 

  • Chantigny MH, Angers DA, Kaiser K, Kalbitz K. 2008. Extraction and characterization of dissolved organic matter. In: Carter MR, Gregorich EG, Eds. Soil sampling and methods of analysis. Ottwa: Canadian Society of Soil Science. p 617–35.

    Google Scholar 

  • Chesire MV. 1979. Nature and origin of carbohydrates in soils. London: Academic Press.

    Google Scholar 

  • Chodak M, Klimek B, Niklińska M. 2016. Composition and activity of soil microbial communities in different types of temperate forests. Biol Fertil Soils 52:1093–104.

    CAS  Google Scholar 

  • D’Elia CF, Steudler PA, Corwin N. 1977. Determination of total nitrogen in aqueous samples using persulfate digestion. Limnol Oceanogr 22:760–4.

    Google Scholar 

  • Delgado-Baquerizo M, Covelo F, Gallardo A. 2011. Dissolved organic nitrogen in Mediterranean ecosystems. Pedosphere 21:309–18.

    CAS  Google Scholar 

  • Delgado-Baquerizo M, García-Palacios P, Milla R, Gallardo A, Maestre FT. 2015. Soil characteristics determine soil carbon and nitrogen availability during leaf litter decomposition regardless of litter quality. Soil Biol Biochem 81:134–42.

    CAS  Google Scholar 

  • Delgado-Baquerizo M, Morillas L, Maestre FT, Gallardo A. 2013. Biocrusts control the nitrogen dynamics and microbial functional diversity of semi-arid soils in response to nutrient additions. Plant Soil 372:643–54.

    CAS  Google Scholar 

  • Durán J, Rodríguez A, Fernández-Palacios JM, Gallardo A. 2009. Changes in net N mineralization rates and soil N and P pools in a pine forest wildfire chronosequence. Biol Fertil Soils 45:781–8.

    Google Scholar 

  • Edburg SL, Hicke JA, Brooks PD, Pendall EG, Ewers BE, Norton U, Gochis D, Gutmann ED, Meddens AJH. 2012. Cascading impacts of bark beetle-caused tree mortality on coupled biogeophysical and biogeochemical processes. Front Ecol Environ 10:416–24.

    Google Scholar 

  • Franzluebbers AJ, Haney RL, Hons FM, Zuberer DA. 1996. Active fractions of organic matter in soils with different texture. Soil Biol Biochem 28:1367–72.

    CAS  Google Scholar 

  • García-Palacios P, Bowker MA, Chapman SJ, Maestre FT, Soliveres S, Gallardo A, Valladares F, Guerrero C, Escudero A. 2011. Early-successional vegetation changes after roadside prairie restoration modify processes related with soil functioning by changing microbial functional diversity. Soil Biol Biochem 43:1245–53.

    Google Scholar 

  • García-Palacios P, Milla R, Delgado-Baquerizo M, Martín-Robles N, Álvaro-Sánchez M, Wall DH. 2013. Side-effects of plant domestication: ecosystem impacts of changes in litter quality. New Phytol 198:504–13.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Gómez-Aparicio L, Canham CD. 2008. Neighborhood models of the effects of invasive tree species on ecosystem processes. Ecol Monogr 78:69–86.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hancock JE, Arthur MA, Weathers KC, Lovett GM. 2008. Carbon cycling along a gradient of beech bark disease impact in the Catskill Mountains, New York. Can J For Res 38:1267–74.

    CAS  Google Scholar 

  • Hassink J. 1997. The capacity of soils to preserve organic C and N by their association with clay and silt particles. Plant Soil 191:77–87.

    CAS  Google Scholar 

  • Hassink J, Whitmore AP. 1997. A model of the physical protection of organic matter in soils. Soil Sci Soc Am J 61:131–9.

    CAS  Google Scholar 

  • Hicke JA, Allen CD, Desai AR, Dietze MC, Hall RJ, Hogg EH, Kashian DM, Moore D, Raffa KF, Sturrock RN, Vogelmann J. 2012. Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Glob Change Biol 18:7–34.

    Google Scholar 

  • Hobara S, Tokuchi N, Ohte N, Koba K, Katsuyama M, Kim SJ, Nakanishi A. 2001. Mechanism of nitrate loss from a forested catchment following a small-scale, natural disturbance. Can J For Res 31:1326–35.

    CAS  Google Scholar 

  • Holden SR, Treseder KK. 2013. A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol 4:163.

    PubMed  PubMed Central  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.

    PubMed  PubMed Central  Google Scholar 

  • Ibáñez B, Ibáñez I, Gómez-Aparicio L, Ruiz-Benito P, García LV, Marañón T. 2014. Contrasting effects of climate change along life stages of a dominant tree species: the importance of soil-climate interactions. Divers Distrib 20:872–83.

    Google Scholar 

  • Insam H, Parkinson D, Domsch KH. 1989. Influence of macroclimate on soil microbial biomass. Soil Biol Biochem 21:211–21.

    Google Scholar 

  • Joergensen RG. 1996. The fumigation–extraction method to estimate soil microbial biomass: Calibration of the kEC value. Soil Biol Biochem 28:25–31.

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Jones DL, Willett VB. 2006. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–9.

    CAS  Google Scholar 

  • Lovett GM, Arthur MA, Weathers KC, Griffin JM. 2010. Long-term changes in forest carbon and nitrogen cycling caused by an introduced pest/pathogen complex. Ecosystems 13:1188–200.

    CAS  Google Scholar 

  • Lovett GM, Weiss M, Liebhold AM, Holmes TP, Leung B, Lambert KF, Orwig DA, Campbell FT, Rosenthal J, McCullough DG. 2016. Nonnative forest insects and pathogens in the United States: Impacts and policy options. Ecol Appl 26:1437–55.

    PubMed  PubMed Central  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M. 2000. 100 of the world’s worst invasive alien species: a selection from the global invasive species database: Invasive Species Specialist Group Species Survival Commission, World Conservation Union (IUCN), Auckland, New Zealand.

  • McIntosh ACS, Macdonald SE. 2013. Short-term resistance of ecosystem properties and processes to simulated mountain pine beetle attack in a novel region. Ecosphere 4:1–28.

    Google Scholar 

  • Mikkelson KM, Lozupone CA, Sharp JO. 2016. Altered edaphic parameters couple to shifts in terrestrial bacterial community structure associated with insect-induced tree mortality. Soil Biol Biochem 95:19–29.

    CAS  Google Scholar 

  • Morehouse K, Johns T, Kaye J, Kaye A. 2008. Carbon and nitrogen cycling immediately following bark beetle outbreaks in southwestern ponderosa pine forests. For Ecol Manag 255:2698–708.

    Google Scholar 

  • Müller T, Höper H. 2004. Soil organic matter turnover as a function of the soil clay content: consequences for model applications. Soil Biol Biochem 36:877–88.

    Google Scholar 

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

  • Nave LE, Gough CM, Maurer KD, Bohrer G, Hardiman BS, Le Moine J, Munoz AB, Nadelhoffer KJ, Sparks JP, Strahm BD, Vogel CS, Curtis PS. 2011. Disturbance and the resilience of coupled carbon and nitrogen cycling in a north temperate forest. J Geophys Res Biogeosci 116:G04016.

    Google Scholar 

  • Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M. 2018. More than “100 worst” alien species in Europe. Biol Invasions 20:1611–21.

    Google Scholar 

  • Ninyerola M, Pons X, Roure JM. 2005. Atlas climático digital de la Península Ibérica: metodología y aplicaciones en bioclimatología y geobotánica. Barcelona: Universidad Autónoma de Barcelona.

    Google Scholar 

  • Norton U, Ewers BE, Borkhuu B, Brown NR, Pendall E. 2015. Soil nitrogen five years after bark beetle infestation in lodgepole pine forests. Soil Sci Soc Am J 79:282–93.

    CAS  Google Scholar 

  • Ojeda F, Marañón T, Arroyo J. 2000. Plant diversity patterns in the Aljibe Mountains (S. Spain): a comprehensive account. Biodivers Conserv 9:1323–43.

    Google Scholar 

  • Oren A, Steinberger Y. 2008. Catabolic profiles of soil fungal communities along a geographic climatic gradient in Israel. Soil Biol Biochem 40:2578–87.

    CAS  Google Scholar 

  • Pignataro A, Moscatelli MC, Mocali S, Grego S, Benedetti A. 2012. Assessment of soil microbial functional diversity in a coppiced forest system. Appl Soil Ecol 62:115–23.

    Google Scholar 

  • R Core Team. 2016. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Robertson GP, Wedin D, Groffmann P, Blair J, Holland E, Nadelhoffer K, Harris D. 1999. Soil carbon and nitrogen availability: nitrogen mineralization, nitrification, and soil respiration potentials. Standard soil methods for long-term ecological research. Oxford: Oxford University Press. pp 258–71.

    Google Scholar 

  • Rodríguez A, Curiel Yuste J, Rey A, Durán J, García-Camacho R, Gallardo A, Valladares F. 2016. Holm oak decline triggers changes in plant succession and microbial communities, with implications for ecosystem C and N cycling. Plant Soil 414:247–63.

    Google Scholar 

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

    Google Scholar 

  • Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.

    Google Scholar 

  • Schwendenmann L, Michalzik B. 2019. Dissolved and particulate carbon and nitrogen fluxes along a Phytophthora agathidicida infection gradient in a kauri (Agathis australis) dominated forest. Fungal Ecol 42:100861.

    Google Scholar 

  • Sims GK, Ellsworth TR, Mulvaney RL. 1995. Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26:303–16.

    CAS  Google Scholar 

  • Stadler B, Müller T, Orwig D, Cobb R. 2005. Hemlock woolly adelgid in New England forests: canopy impacts transforming ecosystem processes and landscapes. Ecosystems 8:233–47.

    Google Scholar 

  • Trumbore S, Brando P, Hartmann H. 2015. Forest health and global change. Science 349:814–18.

    CAS  PubMed  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. J Biogeogr 35:1688–700.

    Google Scholar 

  • Van Der Heijden MGA, Bardgett RD, Van Straalen NM. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:651.

    Google Scholar 

  • Van Der Putten WH, Bardgett RD, De Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA. 2009. Empirical and theoretical challenges in aboveground–belowground ecology. Oecologia 161:1–14.

    PubMed  PubMed Central  Google Scholar 

  • Van Veen JA, Kuikman PJ. 1990. Soil structural aspects of decomposition of organic matter by micro-organisms. Biogeochemistry 11:213–33.

    Google Scholar 

  • Vitousek PM, Melillo JM. 1979. Nitrate losses from disturbed forests: patterns and mechanisms. Forest Science 25:605–19.

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Putten WH, Putten DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629–33.

    CAS  PubMed  Google Scholar 

  • Wardle DA, Peltzer DA. 2017. Impacts of invasive biota in forest ecosystems in an aboveground–belowground context. Biol Invasions 19:3301–16.

    Google Scholar 

  • Weil RR, Brady NC, Weil RR. 2016. The nature and properties of soils. London: Pearson.

    Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D. 2003. Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–50.

    Google Scholar 

  • Zak JC, Willig MR, Moorhead DL, Wildman HG. 1994. Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–8.

    Google Scholar 

  • Zhang B, Zhou X, Zhou L, Ju R. 2015. A global synthesis of below-ground carbon responses to biotic disturbance: a meta-analysis. Glob Ecol Biogeogr 24:126–38.

    Google Scholar 

  • Zornoza R, Mataix-Solera J, Guerrero C, Arcenegui V, Mataix-Beneyto J. 2009. Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid Land Res Manag 23:213–22.

    CAS  Google Scholar 

Download references

Acknowledgements

We thank the director and technicians of Los Alcornocales Natural Park for facilities and support to carry out the field work. We specially thank to Ana Pozuelos, Cristina Allely, Ana Prado and several students for invaluable laboratory and field assistance. We thank Dr. Charles Canham for his help with the statistical analyses. This research was supported by the Ministerio de Ciencia e Innovación (MICINN) projects CGL2010-21381 and CGL2011-26877 (RETROBOS). J.M.A. was supported by a FPU-MEC grant (AP2010-0229) and B.I. FPI-MICINN grant (BES-2009-017111).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. M. Ávila.

Additional information

Authors Contributions

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ávila, J.M., Gallardo, A., Ibáñez, B. et al. Pathogen-Induced Tree Mortality Modifies Key Components of the C and N Cycles with No Changes on Microbial Functional Diversity. Ecosystems 24, 451–466 (2021). https://doi.org/10.1007/s10021-020-00528-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-020-00528-1

Keywords

Navigation