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Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees

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Reduced growth but high NSC after severe defoliation of evergreen trees can be explained by three, non-exclusive processes: critical loss of non-C reserves, hormonal changes, and prioritisation of C storage over growth.

Abstract

In an attempt to simulate processionary moth impact on pines, we explored the extent to which late winter defoliation affects growth and carbon reserves in the following season. In separate treatments we removed 100, and 50 % of needles of whole trees and defoliated single branches in naturally grown, 2–3-m-tall Pinus pinaster trees in Italy. Shoot and stem growth (lateral shoot length and basal area increment, respectively) were substantially reduced after 100 % defoliation (−45 % for shoots, −84 % for stems). In 50 % defoliated trees only stem growth was reduced (−37 %), and in trees with a single branch defoliated, growth remained unaffected. Although substantial carbon and nitrogen reserves were removed from defoliated trees prior to bud break, non-structural carbohydrates (NSC) concentrations in branches and needles fell below control values only during the first half of the growing season, and considerable amounts of NSC persisted throughout the year. By the end of the dry and hot Mediterranean summer, NSC concentrations in branch xylem, branch phloem, previous year needles, stem sapwood and root xylem were similar among all treatments. Reduced growth and high late season NSC after defoliation can be explained by (1) a critical loss of reserves other than C (e.g. N and P), (2) hormonal changes which affected cambial activity, or (3) a prioritisation of carbon storage over growth, with all three mechanisms potentially contributing to the observed growth and NSC response.

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References

  • Bale JS, Masters GJ, Hodkinson ID et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16

    Article  Google Scholar 

  • Barry KM, Quentin A, Eyles A, Pinkard EA (2011) Consequences of resource limitation for recovery from repeated defoliation in Eucalyptus globulus Labilladière. Tree Physiol 32:24–35

    Article  PubMed  Google Scholar 

  • Battisti A, Stastny M, Netherer S, Robinet C, Schopf A, Roques A, Larsson S (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecol Appl 15(6):2084–2096

    Article  Google Scholar 

  • Benigni M, Battisti A (1999) Climate change and the pine processionary caterpillar: adaptation of a defoliator to changing environmental conditions. Italia Forestale e Montana 54(2):76–86

    Google Scholar 

  • Cappelli F, Cappelli V, Fabbrizzi F, Olivari S, Piussi P, Sbragia M, Stiavelli S (2004) La Riserva naturale di Montefalcone—storia, ambiente e territorio. Corpo Forestale dello Stato Ufficio Gestione ex. A.S.F.D. Lucca, Tipografia la Grafica Pisana, Bientina, Italy

  • Carus S (2004) Impact of defoliation by the pine processionary moth (Thaumetopoea pityocampa) on radial, height and volume growth of Calabrian pine (Pinus brutia) trees in Turkey. Phytoparasitica 32(5):459–469

    Article  Google Scholar 

  • Carus S (2009) Effects of defoliation caused by the processionary moth on growth of Crimean pines in western Turkey. Phytoparasitica 37:105–114

    Article  Google Scholar 

  • Chapin FS III, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Ericsson A, Larsson S, Tenow O (1980) Effects of early and late season defoliation on growth and carbohydrate dynamics in Scots pine. J Appl Ecol 17:747–769

    Article  Google Scholar 

  • Ericsson A, Hellqvist C, Långström D, Larsson S, Tenow O (1985) Effects on growth of simulated and induced shoot pruning by Tomicus piniperda as related to carbohydrate and nitrogen dynamics in Scots pine. J Appl Ecol 22:105–124

    Article  Google Scholar 

  • Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol 29:753–764

    Article  CAS  PubMed  Google Scholar 

  • Fischer C, Höll W (1991) Food reserves of Scots pine (Pinus sylvestris L.) I. Seasonal changes in the carbohydrate and fat reserves of pine needles. Trees Struct Funct 5:187–195

    Article  Google Scholar 

  • Fischer C, Höll W (1992) Food reserves of Scots pine (Pinus sylvestris L.) II. Seasonal changes and radial distribution of carbohydrate and fat reserves in pine wood. Trees Struct Funct 6:147–155

    Article  Google Scholar 

  • Goussard F, Saintonge FX, Geri C, Auger-Rozenberg G, Pasquier-Barre F, Rousselet J (1999) Accroissement des risques de dégâts de la processionnaire du pin, Thaumetopoea pityocampa Denis & Schiff. en région Centre, dû au réchauffement climatique (Lepidoptera, Thaumetopoeidae). Ann Soc Entomol Fr 35:341–343

    Google Scholar 

  • Handa IT, Körner C, Hättenschwiler S (2005) Carbon economy in treeline conifers: a test of the carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86:1288–1300

    Article  Google Scholar 

  • Hansen J, Beck E (1990) The fate and path of assimilation products in the stem of 8-year-old Scots pine (Pinus sylvestris L.) trees. Trees Struct Funct 4:16–21

    Article  Google Scholar 

  • Hansen J, Beck E (1994) Seasonal-changes in the utilization and turnover of assimilation products in 8-year-old Scots pine (Pinus sylvestris L.) trees. Trees Struct Funct 8:172–182

    Article  Google Scholar 

  • Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659

    Article  CAS  Google Scholar 

  • Hoch G (2015) Carbon reserves as indicators for carbon limitation in trees. In: Lüttge U, Beyschlag W, Cushman J (eds) Progress in Botany, vol 76. Springer Verlag, Heidelberg, pp 321–346

  • Hoch G, Popp M, Körner C (2002) Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98(3):361–374

    Article  CAS  Google Scholar 

  • Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081

    Article  CAS  Google Scholar 

  • Hódar JA, Castro J, Zamora R (2003) Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biol Conserv 110:123–129

    Article  Google Scholar 

  • Huttunen L, Niemelä P, Peltola H, Heiska S, Rousi M, Kellomäki S (2007) Is a defoliated silver birch seedling able to overcompensate the growth und changing climate? Environ Exp Bot 60:227–238

    Article  Google Scholar 

  • Jacquet JS, Orazio C, Jactel H (2012) Defoliation by processionary moth significantly reduces tree growth: a quantitative review. Ann For Sci 69:857–866

    Article  Google Scholar 

  • Jacquet JS, Bosc A, O’Grady AP, Jactel H (2013) Pine growth response to processionary moth defoliation across a 40-year chronosequence. For Ecol Manag 293:29–38

    Article  Google Scholar 

  • Jacquet JS, Bosc A, O’Grady A, Jactel H (2014) Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiol 34:367–376

    Article  CAS  PubMed  Google Scholar 

  • Kanat M, Alma MH, Sivrikaya F (2005) Effect of defoliation by Thaumetopoea pityocampa (Den. & Schiff.) (Lepidoptera: Thaumetopoeidae) on annual diameter increment of Pinus brutia Ten. in Turkey. Ann For Sci 62:91–94

    Article  Google Scholar 

  • Kolb TE, McCormick LH, Simons EE, Jeffery DJ (1992) Impacts of pear thrips damage on root carbohydrate, sap, and crown characteristics of sugar maples in a Pennsylvania sugarbush. Forest Sci 38:381–392

    Google Scholar 

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Article  Google Scholar 

  • Körner C (2013) Growth controls photosynthesis—mostly. Nova Acta Leopoldina NF 114(391):273–283

    Google Scholar 

  • Körner C, Sarris D, Christodoulakis D (2005) Long-term increase in climatic dryness in the East-Mediterranean as evidenced for the Island of Samos. Reg Environ Change 5:27–36

    Article  Google Scholar 

  • Kosola KR, Dickmann DI, Paul EA, Parry D (2001) Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars. Oecologia 129:65–74

    Article  Google Scholar 

  • Landhäusser S (2011) Aspen shoots are carbon autonomous during bud break. Trees Struct Funct 25:531–536

    Article  Google Scholar 

  • Li MH, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees Struct Funct 16:331–337

    Article  CAS  Google Scholar 

  • Markalas S (1998) Biomass production of Pinus pinaster after defoliation by the pine processionary moth (Thaumetopoea pityocampa Schiff.). In: McManus ML, Liebhold AM (eds) Proceedings of Population dynamics, and integrated management of forest defoliating insects, Forest Service General Technical Report, NE-247. USDA, CT, USA, pp 292–302

  • McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stit M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532

    Article  PubMed  Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Hester A, Wendler R, Baillie G (2001) Interspecific defoliation responses of trees depends on sites of winter nitrogen storage. Funct Ecol 15:535–543

    Article  Google Scholar 

  • Millard P, Sommerkorn M, Grelet GA (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28

    Article  CAS  PubMed  Google Scholar 

  • Obeso JR (1998) Effects of defoliation and girdling on fruit production in Ilex aquifolium. Funct Ecol 12:486–491

    Article  Google Scholar 

  • Oleksyn J, Zytkowiak R, Karolewski P, Reich PB, Tjoelker MG (2000) Genetic and environmental control of seasonal carbohydrate dynamics in trees of diverse Pinus sylvestris populations. Tree Physiol 20:837–847

    Article  PubMed  Google Scholar 

  • Palacio S, Hernández R, Maestro-Martínez M, Camarero JJ (2012) Fast replenishment of initial carbon stores after defoliation by the pine processionary moth and its relationship to the re-growth ability of trees. Trees Struct Funct 26:1627–1640

    Article  Google Scholar 

  • Palacio S, Hoch G, Sala A, Körner C, Millard P (2014) Does carbon storage limit tree growth? New Phytol 201:1096–1100

    Article  CAS  PubMed  Google Scholar 

  • Piper FI, Fajardo A (2014) Foliar habit, tolerance to defoliation and their link to carbon and nitrogen storage. J Ecol 102:1101–1111

    Article  CAS  Google Scholar 

  • Popp M, Lied W, Meyer A, Richter A, Schiller P, Schwitte H (1996) Sample preservation for determination of organic compounds: microwave versus freeze-drying. J Exp Bot 47:1469–1473

    Article  CAS  Google Scholar 

  • Raitio H, Paukkonen K, Kauppi A (1994) Effects of defoliation, nitrogen nutrition, and temperature on leafing and root carbohydrates of birch seedlings. Can J For Res 24:1914–1920

    Article  Google Scholar 

  • Reich PB, Walters MB, Krause SC, Vanderklein DW, Raffa KF, Tabone T (1993) Growth, nutrition and gas exchange of Pinus resinosa following artificial defoliation. Trees Struct Funct 7:67–77

    Article  Google Scholar 

  • Sarris D, Christodoulakis D, Körner C (2007) Recent decline in precipitation and tree growth in the eastern Mediterranean. Glob Change Biol 13:1187–1200

    Article  Google Scholar 

  • Schädel C, Richter A, Blöchl A, Hoch G (2010) Hemicellulose concentration and composition in plant cell walls under extreme carbon source–sink imbalances. Physiol Plant 139:241–255

    PubMed  Google Scholar 

  • Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37(1):153–161

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334

    Article  Google Scholar 

  • Tschaplinski TJ, Blake TJ (1994) Carbohydrate mobilization following shoot defoliation and decapitation in hybrid poplar. Tree Physiol 14:141–151

    Article  CAS  PubMed  Google Scholar 

  • Vanderklein DW, Reich PB (1999) The effect of defoliation intensity and history on photosynthesis, growth and carbon reserves of two conifers with contrasting leaf lifespans and growth habits. New Phytol 144:121–132

    Article  CAS  Google Scholar 

  • Wang Q, Little CHA, Odén PC (1997) Control of longitudinal and cambial growth by gibberellins and indole-3-acetic acid in current-year shoots of Pinus sylvestris. Tree Physiol 17:715–721

    Article  CAS  PubMed  Google Scholar 

  • Wargo PM, Parker J, Houston DR (1972) Starch content in roots of defoliated sugar maple. For Sci 1:203–204

    Google Scholar 

  • Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285–289

    Article  CAS  PubMed  Google Scholar 

  • Wiley E, Huepenbecker S, Casper BB, Helliker B (2014) The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol 33:1216–1228

    Article  Google Scholar 

  • Zhao J, Hartmann H, Trumbore S, Ziegler W, Zhang Y (2013) High temperature causes negative whole-plant carbon balance under mild drought. New Phytol 200:330–339

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Special thanks go to the Corpo Forestale dello Stato, Italy, (Ufficio Territoriale per la biodiversità di Lucca) for permitting this study in the Riserva Naturale di Montefalcone, Pisa, Italy. Further, we thank Pierangela de Benedetto, Cristina De Monte and Massimo Monti for their sustained help during the fieldwork. We further thank Armando Lenz and Martin Bader for statistical advice, Daniel Nelson for proofreading of the manuscript and the two anonymous referees for their very constructive and important comments on a previous version of this paper.

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The authors declare that they have no conflict of interest.

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Correspondence to Günter Hoch.

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Communicated by L. Gratani.

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Puri, E., Hoch, G. & Körner, C. Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees. Trees 29, 1187–1196 (2015). https://doi.org/10.1007/s00468-015-1199-y

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