Climate change impacts on plant canopy architecture

Climate change impacts on plant canopy architecture: implications for pest and pathogen managementIreneo B.Pangga&Jim Hanan&Sukumar ChakrabortyAccepted:15October2012/Published online:25October2012#KNPV2012Abstract Climate change influences on pests and pathogens are mainly plant-mediated.Rising carbon dioxide and temperature and altered precipitation modifies plant growth and development with concom-itant changes in canopy architecture,size,density, microclimate and the quantity of susceptible tissue. The modified host physiology and canopy microcli-mate at elevated carbon dioxide influences production, dispersal and survival of pathogen inoculum and feed-ing behaviour of insect pests.Elevated temperature accelerates plant growth and developmental rates to modify canopy architecture and pest and pathogen development.Altered precipitation affects canopy ar-chitecture through either drought or flooding stress with corresponding effects on pests and pathogens. But canopy-level interactions are largely ignored in epidemiology models used to project climate change impacts.Nevertheless,models based on rules of plant morphogenesis have been used to explore pest and pathogen dynamics and their trophic interactions un-der elevated carbon dioxide.The prospect of modify-ing canopy architecture for pest and disease management has also been raised.We offer a concep-tual framework incorporating canopy characteristics in the traditional disease triangle concept to advance understanding of host-pathogen-environment interac-tions and explore how climate change may influence these interactions.From a review of recent literature we summarize interrelationships between canopy ar-chitecture of cultivated crops,pest and pathogen biol-ogy and climate change under four areas of research: (a)relationships between canopy architecture,micro-climate and host-pathogen interaction;(b)effect of climate change related variables on canopy architec-ture;(c)development of pests and pathogens in mod-ified canopy under climate change;and(d)pests and pathogen management under climate change. Keywords Microclimate.Pathogen evolution. Polycyclic epidemics.Elevated CO2.Rules of plant morphogenesisIntroductionClimate change projections suggest that by the end of this century atmospheric CO2concentration may ex-ceed700μmol mol−1and global surface temperatureEur J Plant Pathol(2013)135:595–610DOI10.1007/s10658-012-0118-yI.B.PanggaCrop Protection Cluster,College of Agriculture, University of the Philippines Los Baños,College, Laguna,Philippines4031J.HananQueensland Alliance for Agriculture and Food Innovation, Biological Information Technology,The University of Queensland,Brisbane,Australia4072S.Chakraborty(*)CSIRO Plant Industry,Queensland Bioscience Precinct, 306Carmody Road,St.Lucia,Queensland4067,Australiae-mail:sukumar.chakraborty@csiro.aumay increase1.8–4°C depending on the emission sce-nario and there may be more heat waves and other extreme events(Pachauri and Reisinger2007).The “fertilization effect”of rising CO2will increase crop yield but this may be offset by other climatic,nutritional and biotic factors including pest and pathogens(PP).Plants interact with climate and atmosphere through a network of organs optimally deployed to exploit aerial and soil environments.Plant canopy architecture is the species-specific three-dimensional organization of the plant body(Reinhardt and Kuhlemeier2002).It is genetically regulated through hormone signalling pathways(Yang and Hwa2008),but the environment plays a significant role in determining the spatial ar-rangement of photosynthetic and reproductive units on a scaffold of branches.Canopy architecture optimizes radiation interception to enhance competitive ability and fitness of plants to improve crop yield(Haile 2001b)and exposure to pollinators for reproductive fitness of cross-pollinated species.Tall traditional varieties of rice are susceptible to lodging and have low yield.In contrast,the modified canopy of semi-dwarf varieties with improved light interception have nearly doubled the yield potential (Coyne1980)as they offer resistance to lodging under high nitrogen fertilization.Further architectural modifi-cations such as erect dark green leaves,reduced tillering and reduced number of unproductive tillers,improved grain filling and delayed leaf senescence of the top three leaves during ripening can further increase yield over that of the high yielding semi-dwarf cultivars(Khush 1995;Laza et al.2003;Peng et al.2008).All interactions between PP and host plants occur within canopy where microclimate influences the out-come of the interaction.In rice,tall plants had lower sheath blight severity due to Rhizoctonia solani (Willocquet et al.2011),but wide leaf angle allowed deposition of more Pyricularia grisea spores that led to higher leaf blast incidence(Ou1985).Among other crops,chickpea with fern-type leaves have less Ascochyta blight than ones with unifoliate leaves (Gan et al.2003).For pathogens,canopy architecture and microclimate influence their dispersal and devel-opment(Rotem1982;Royle and Butler1986). Examples include,sheath blight of rice[Rhizoctonia solani](Wu et al.2012),tan spot of wheat [Pyrenophora tritici-repentis](Fernandez et al.2002) and Phytophthora capsici fruit infection of cucumber (Ando and Grumet2006).Microclimate is significant for insects due to their small size(Chown2012).The abundance and diversity of arthropods depend on the size of canopy;large canopies provide more resources and may have more diverse insect fauna than smaller cano-pies.The mango leaf webber,Orthaga euadrusalis pre-fers large exposed leaf areas for egg laying and is most damaging on trees with high leaf density in the outer canopy layers(V erma and Tomar2010).Insect galls are strongly influenced by the number of fourth level shoots in Baccharis species(Espirito-Santo et al.2007).PP populations can modify canopy architecture and microclimate(Haile2001b).Herbivory can change plant morphology to modify access to resources,com-petitive ability and pollination(Delaney and Macedo 2001).But plants can adapt through compensatory re-sponse such as modified structure,delayed senescence and maturity without affecting yield(Haile2001b).Elevated CO2and temperature,changing precipita-tion and other climate change factors influence PP di-rectly by affecting their growth and development and indirectly via changes in chemical defenses,architecture, phenology(Caffarra et al.2012)and canopy microcli-mate of host plants.The spatio-temporal dynamics of PP (Ziska and Runion2007)are changed as a consequence and this impacts on their prevalence,severity and man-agement.Elevated CO2for instance,increases canopy size,density,structure and biomass that directly increase the number of susceptible organs and indirectly make the microclimate more favourable for pathogen develop-ment(Manning and von Tiedemann1995).There has been a recent resurgence in interest on climate change and PP(Pautasso et al.2012),including reviews on climate change interactions involving PP(Chakraborty et al.2012)and their impacts on quality such as the production of mycotoxins(EFSA2012).However,there is an overall paucity of knowledge on relationships be-tween canopy architecture,microclimate and pest and pathogen biology and how climate change may influence these relationships.This paper originates from the inter-national conference on plant canopy architecture impact on disease epidemiology and pest development.It aims to elucidate interrelationships between canopy architec-ture,microclimate and pest and pathogen biology and epidemiology to allow a discussion on the influence of climate change on these interrelationships.The main focus is on plant pathogens and any coverage of insect pests is mostly to illustrate how common principles and approaches may apply to both pest and pathogen populations.Relationships between canopy architecture, microclimate and host-pathogen interactionThe relationships between canopy architecture and mi-croclimate of host plant and pest and pathogen popula-tions are multi-dimensional,where changes in one relationship influence one or more relationships in an interactive manner.The impacts of these interactions are felt far beyond the canopy as they influence the struc-ture,survival and evolution of plant communities and the feedback of terrestrial ecosystems to global climate. Understanding these interactions is essential before any discussion on how climate change may further modify these and we have outlined key interactions in Fig.1to facilitate discussion.While the importance of host-pathogen-environment interactions to plant disease de-velopment is well recognized in the so-called‘disease triangle’that forms a basic tenet of plant pathology,the fact that most of these interactions take place within a plant canopy is not explicit in the literature.Although weather outside the canopy directly influences some aspects of host and pathogen biology,it is the influence of weather on the plant canopy,which modifies microclimate to determine the dynamics of PP(Fig.1). Weather outside of the canopy can influence host resis-tance and is responsible for long-distance dispersal of PP that helps to maintain and establish populations following local extinctions(Chown2012).More often than not,microclimate controls growth and reproduction of PP except in seasons when extreme weather such as heavy rainfall removes any effect of canopy architecture (Giesler et al.1996).The nature and extent of damage caused by PP further modify canopy architecture and microclimate to influence PP-host plant interactions. Changing climate and atmospheric composition and modified canopy architecture through human interven-tion act on the disease triangle adding further layers of complexity to these interactions.Weather factors including rainfall,temperature and moisture influence plants by modifying phenology, physiology and resistance to PP and the size and structure of canopy,all of which influence the biology and epidemiology of pests and pathogens(Caffarra et al.2012;Legreve and Duveiller2010).The microcli-mate within a canopy is very different to the weather outside and it changes during the growing seasondue Fig.1A conceptual diagram to link key interactions betweenweather and populations of host,pest and pathogen(PP)underchanging atmospheric composition and climate.Weather direct-ly influences(brown arrows)PP populations and host character-istics to modify canopy architecture and its microclimate,whichinfluences(blue arrows)the dynamics of PP development.Theinfluence of changing climate and atmospheric composition ispredominantly mediated through changes in canopy and othercharacteristics of host plant communities,which in turn altersthe feedback of terrestrial ecosystems to global climateto changing canopy morphology(Hatfield1982; Royle and Butler1986).As agents of change,PP influence structure,com-position,function and evolution of ecosystems to im-pact on the delivery of ecosystem services including carbon exchange(Olofsson et al.2011).For instance, the devastation of susceptible Eucalyptus by Phytophthora cinnamomi in Australia(Alexander 2010)has decimated Eucalyptus woodlands that have since been replaced by sedge and grass communities with very different feedback to climate systems.PP often interact at multitrophic levels to magnify impacts on plant canopy architecture and productivity(Wilson and Chakraborty1996).Canopy temperature relationshipsTemperature determines the rates of metabolic and developmental processes;controls evaporation and transpiration that influence water balance and ulti-mately plant growth.Temperature of plant organs such as leaves is determined by radiation load to control energy balance and the rate of physiological processes (Landsberg and Sands2011)and changing leaf orien-tation can reduce leaf temperature by up to6°C. Canopy architecture is influenced by diurnal fluctua-tions and internode lengths in determinate crops in-crease with increasing difference between maximum and minimum temperatures(Myster and Moe1995). The temperature inside a crop canopy may be2–3°C lower than outside,depending on outside temperature, transpiration and the type of crop(Monteith and Unsworth1990).Air temperature inside canopy varies with height,canopy architecture,time of day and cloud cover.Temperature extremes induce leaf dam-age,water stress and loss of turgor and a lowering of temperature through changes in canopy architecture can reduce thermal stress(Mahan et al.1995).Also, smaller leaves are often cooler than large leaves with thinner boundary layers that are more efficient in latent heat transfers(Nobel1991).Development of PP further modifies canopy micro-climate.The stripe rust pathogen can interfere with stomatal closure and induce leaf senescence to raise the temperature of wheat foliage by1.6°C(Smith et al.1986).Infestation by scale insects modifies canopy architecture by reducing leaf area index and the inter-ception of precipitation,but increasing soil moisture and temperature(Classen et al.2005).Canopy moisture relationshipsDense canopies are more efficient in the interception and retention of precipitation leading to extended peri-ods of surface wetness and high relative humidity. Canopy architecture,radiation,air and soil tempera-ture and wind are the main factors determining the moisture profile inside the canopy and these have typical diurnal cycles.Other factors including plant spacing and gaps in the canopy increase ventilation to influence canopy wetness.There is spatial hetero-geneity of dry and wet areas at both leaf and canopy scales.In a soybean canopy,the wetness duration was longer in upper layers from dew than in the lower layers where rain is the dominant moisture source (Schmitz and Grant2009).The duration of surface wetness,percolation of rain through the canopy and the level of relative humidity are important factors for the development of PP. Surface wetness is considered one of the most impor-tant for pathogen development.Pathogens have been classified as those with high(e.g.oomycetes)and low dependency(e.g.powdery mildews)on surface water (Huber and Gillespie1992).Dense canopies offer extended periods of surface wetness and favour the development of Sclerotinia sclerotiorum white mold disease in bean(Deshpande et al.1995),early onset of Erwinia carotovora pv.carotovora stem rot of potato (Cappaert and Powelson1990),and early infection and high severity of Phomopsis stem canker in sun-flower(Debaeke and Moinard2010),among others.There is spatial heterogeneity for moisture levels in the canopy and this influences the development of PP. Defoliation and other symptoms of late leaf spot dis-ease of peanuts caused by Cercosporidium persona-tum is most severe in the bottom canopy layer(Plaut and Berger1980).In alfalfa the incidence and severity of a disease complex is greater on the lower half of shoots that correlates with leaf wetness duration,va-pour pressure deficit and relative humidity higher than 90%,while less severe disease on the upper half of shoots correlates with cumulative rainfall(Emery and English1994).Insects commonly respond to humidity but surface water is less critical(Butler1996).Increased vegeta-tion cover due to high rainfall leads to increased Auchenorrhyncha in grasslands(Masters et al.1998). Dense canopies of dwarf apple trees are more condu-cive to Cydia pomonella development than tall treeswith higher canopy temperature(Kuhrt et al.2006). The variation in relative humidity at different heights relates to variation in insect distribution in the canopy (Haile2001a).For example,the distribution and sur-vival of Nilaparvata lugens in rice canopy are en-hanced by the humid microenvironment near the ground level(Isichaikul et al.1994).Effect of climate change related variableson canopy architectureElevated CO2Growth and biomass of plants with all three photosyn-thetic pathways are stimulated at elevated CO2 (Poorter and Perez-Soba2002),along with changes in plant physiology and morphology(Idso1989).Less well-known are changes in plant morphogenesis that modify size,structure and quality of plant canopies. Elevated CO2alters plant structure by modifying pri-mary and secondary meristems of shoots and roots. Cell division,expansion and patterning are influenced by increased substrate availability and differential ex-pression of genes in cell cycling or expansion. Developmental processes at the shoot apex and within the vascular cambium are altered under elevated CO2 leading to increased plant height,altered branching characteristics and increased stem diameters,but leaf initiation rate can be reduced(Pritchard et al.1999). Secondary shoot development rate and the probability of branching along secondary shoots increase at ele-vated CO2.These and other changes at elevated CO2 including a shortened dormancy of axillary buds, changed branching pattern,and increased shoot length and number of nodes change canopy architecture (Pangga2002).Changes to leaf characteristics at elevated CO2are particularly relevant to PP,although the magnitude of these changes depend on plant genetic plasticity,nutri-ent availability,temperature and phenology.Increased number of leaves per plant combines with increased leaf size and area to create a dense canopy.Thickness of leaf, specific leaf weight,the number of mesophyll cells,the cross-sectional areas of vascular tissue and the size and number of chloroplasts increase at elevated CO2 (Pritchard et al.1999;Thomas and Harvey1983). However,there is variation in the expression of leaf-related and other traits(Garbutt et al.1990).Elevated temperatureElevated temperature has significant influence on plant architecture.Arabidopsis can grow at28°C with elon-gated stem,reduced biomass and accelerated flowering (Koini et al.2009),but become heat-stressed at29/23°C day/night temperature,with reduced plant size,number of leaves,flower buds and fruits(Kipp2008).Increasing mean temperature by2–3°C increases height while raising maximum by4–7°C causes an early onset of maximum tillering in rice(Oh-e et al.2007).The influ-ence of rising temperature on plant growth and devel-opment at critical phenological stages,particularly at anthesis and grain filling(Luo2011)is well-known. Temperatures higher than32–36°C for1–3days at flowering greatly reduces seed set in many annual crops (Craufurd and Wheeler2009).Loss in grain yield due to heat stress stems from a shortening of developmental phases,reduced light interception over the shortened life cycle and perturbation of the processes associated with plant carbon balance(Barnabas et al.2008).Altered precipitationProjected changes in frequency and severity of floods and droughts will be the major concern,although increased water use efficiency at elevated CO2will assist with drought survival.Increased soil evapora-tion and plant transpiration due to rising temperature may add to drought stress(Orlandini et al.2009). Water deficit has well-known effects on canopy archi-tecture including reduced leaf area,stem elongation and root growth(Anjum et al.2011;Shao et al.2008), leading to a reduction in fresh and dry biomass pro-duction(Zhao et al.2006).On the other hand,flooding from excessive rainfall affects canopy architecture by suppressing leaf formation and expansion of leaves and internodes and by causing premature senescence, abscission and dieback.Flooding also affects repro-ductive growth by inhibiting flower bud initiation, anthesis,fruit set and by causing early flower and fruit abscission(Kozlowski1997).Development of PP in modified canopyunder climate changeResearch on host-pathogen interaction,almost exclu-sively,deals with interactions and mechanisms atmolecular,cellular,plant organ,whole plant or at best the plant community levels spanning a temporal scale from seconds to seasons.There is little or no empirical research in plant pathology that deals with processes and mechanisms operating at landscape or higher spa-tial scales transcending decadal or higher temporal scales.Similarly,much of the climate change projec-tions from the analytical and modelling research have been simple extrapolations of processes and relation-ships from findings at the plant or crop level.None of these studies incorporate processes and mechanisms that are only apparent at higher spatial or temporal scales.Exceptions are a handful of correlative studies linking pathogen prevalence to changes in atmospher-ic composition(Bearchell et al.2005),association& periodicity with El Nino/Southern Oscillation(Yang and Scherm1997),or anomalies in the climate system (Scherm and Yang1998).This obvious mismatch of scales makes any discussion of climate change influ-ence on pathogens,especially any attempt to incorpo-rate canopy characteristics,blatantly speculative.It also does not allow validation of model projections of future geographical distribution or other trends.The following discussion simply offers a summary of current knowledge on the influence of climate change-related weather variables on host-pathogen in-teraction at the canopy level.Elevated CO2A seminal review(Manning and von Tiedemann 1995)projected that increased biomass at elevated CO2will increase density and height of canopy to promote growth,sporulation and spread of leaf-infecting fungi.More recent literature has also empha-sized the importance of altered plant growth and de-velopment,including modified canopy architecture, under climate change to pathogen development (Burdon et al.2006;Chakraborty et al.2000;Pangga et al.2004).One recent review has focused solely on canopy level changes at elevated CO2and their influ-ence on canopy microclimate and disease develop-ment(Pangga et al.2011).However,the influence on ‘leaf-infecting fungi’and other pathogens is much more complex and varied than initially predicted (Manning and von Tiedemann1995).A summary of recent literature covering pathogen development,disease severity and concomitant changes in canopy architecture is given in Table1mainly to complement other recent literature(Eastburn et al. 2011;Pangga et al.2004).It does not include studies where the influence of elevated CO2has been explained solely by disease resistance due to changed physiology, biochemistry or gene expression and recent reviews pro-vide excellent summaries(Eastburn et al.2011;Yáñez-López et al.2012).Of the11necrotrophic fungal patho-gens studied,disease severity increased in six,decreased in three and remained unchanged in two(Table1).Of the four biotrophic fungal pathogens,disease severity in-creased in two,and either reduced or remained un-changed in the other two.Disease severity of both viruses(biotrophic)was reduced at elevated CO2.The influence of elevated CO2on insect pests is mediated mainly through altered plant metabolism to modify plant defence or insect feeding(Grodzinski et al.1999;Ziska et al.2011).Increased feeding activity to compensate for low nutrient content of leaves may also increase foliar damage(Kocsis and Hufnagel 2011)however,this response is often inconsistent and varies with chewers and sap-sucking insects (Cornelissen2011).Changes in insect population den-sity,growth rate,prolonged development time,re-duced pupal mass(Ayres1993),and changed abundance,richness and diversity are among other influences.These responses are largely due to changes in leaf quality(Cornelissen2011),and only a handful of studies has considered canopy architecture and insect damage and/or development.An increased can-opy size or biomass may increase population size, increase or decrease insect body size,reduce or in-crease herbivory or have no effect(Table2).The influence of elevated CO2depends on feeding modal-ity but interacting factors add complexity to the sys-tem that is difficult to interpret(Sutherst et al.2011). Elevated temperatureThe influence of elevated temperature on pathogen biology,host resistance and host-pathogen interaction that impacts on disease severity is well known. However,there is no detailed information on how rising temperature would impact on PP through changes in canopy architecture.Even a small increase in surface temperature has a large effect on the colo-nization and sporulation of Cercospora zeae-maydis (Paul and Munkvold2005).By allowing the comple-tion of certain life cycle stages,warming will favour Sclerotinia sclerotiorum,Verticillium longisporum andTable1A summary of recent findings on the influence of elevated CO2on plant pathogens and concomitant changes in canopy characteristicsHost plant Pathogen Pathogenlife style Disease severityat elevated CO2Canopy characteristics ReferencePotato Phytophthorainfestans Necrotrophic Reduced severity No effect on biomass;increased activity ofpathogenicity relatedproteins(Plessl et al.2007)Stylosanthes scabra ColletotrichumgloeosporioidesNecrotrophic Increased anthracnoselesions per plantEnhanced transientresistance;enlargedcanopy,leaf area,biomassaltered canopy relativehumidity,solar radiation(Pangga et al.2004,2011)Rice Rhizoctonia solani Necrotrophic Increased sheath blightincidenceIncreased number of tillers(Kobayashi et al.2006)Wheat Fusariumpseudograminearum Necrotrophic Increased fungal biomassand stem browning inresistant variety;higherseverity without irrigationEnlarged size and biomass(Melloy et al.2010)Soybean Fusariumvirguliforme Necrotrophic No effect Increased canopy heightand canopy density;nochange in stomatal densityor leaf chemistry(Eastburn et al.2010)Soybean Septoria glycines Necrotrophic Increased area underdisease progress curve Increased canopy heightand canopy density;nochange in stomatal densityor leaf chemistry(Eastburn et al.2010)Beech Phytophthoracitricola Necrotrophic Increased severity;addingnitrogen fertilizerreduced severityIncreased biomass in highnitrogen;enhanced wateruse efficiency and root tipdensity;altered root/shoot ratio(Fleischmann et al.2010)Acer rubrum Phyllosticta minima Necrotrophic Reduced incidence andseverity Reduced stomatalconductance;reducedleaf N;increasedphenolics and tannins;nochange in stomatal density(McElrone et al.2005)Silver birch Pyrenopezizabetulicola Necrotrophic No effect No change in stomataldensity;reduced stomatalconductance(Riikonen et al.2008)Tomato Phytophthoraparasitica Necrotrophic Increased diseasetolerance;Increasedbiomass made up forreductions due toinfectionIncreased photosynthesis,water use efficiency;turnover of pathogenicityrelated proteins(Jwa and Walling2001)Solidago rigida Cercospora sp.Septoria sp.Necrotrophic Reduced incidence No change in biomass,photosynthesis rate;reduced tissue N(Strengbom and Reich2006)Soybean Peronosporamanshurica Biotrophic Reduced area underdisease progresscurveIncreased canopy heightand canopy density;nochange in stomatal densityor leaf chemistry(Eastburn et al.2010)Potato Potato virus Y Biotrophic Reduced severity Increased biomass and protein;no effect on total non-structural carbohydrates or N(Ye et al.2010)Soybean Erysiphe diffusa Biotrophic Severity increased inall4varieties,Noeffect on pathogensporulation Increased plant height,dryweight of roots andBradyrhizobiumnodulation(Lessin and Ghini2009)。