Tree Physiology 35, 107–111 doi:10.1093/treephys/tpv015

Commentary

To grow or defend? Pine seedlings grow less but induce more defences when a key resource is limited

1Department

of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80303, USA; 2Department of Forestry and Wildland Resources, Humboldt State University, Arcata, CA 95521, USA; 3Department of Chemistry, Seattle University, Seattle, WA 98122, USA; 4Present address: U.S. Geological Survey, Canyonlands Research Station, Moab, UT 84532, USA; 5Corresponding author ([email protected]) Received January 12, 2015; accepted January 27, 2015; published online February 25, 2015; handling Editor Danielle Way

Plants are subject to attack from organisms ranging from microbes to insects and large mammals, and thus have evolved an array of defence and resistance mechanisms to combat natural enemies (Howe and Jander 2008, War et al. 2012). This arsenal of chemical and physical traits can generally be thought of as either constitutive defences, which are produced and present before natural enemies attack, or inducible defences, which are produced in response to attack. While the importance of defence and resistance mechanisms for plant fitness has long been accepted, the presence of substantial variation in defence quantities and types (i.e., constitutive versus induced, chemical versus physical/anatomical) within and across plant species remains somewhat enigmatic (Zangerl and Bazzaz 1992, Endara and Coley 2011). Several major hypotheses of plant defence expression and evolution have gained experimental support. Central to each is the notion that defences increase plant fitness, and the production of these defences comes at the cost of resource allocation trade-offs with other important functions (Stamp 2003). The hypotheses tend to differ in the mechanisms presumed to underlie these functional trade-offs. Resources available to a plant have long been hypothesized to influence not only trade-offs among quantities of plant defences and other functions, but also the dominant types of defences expressed (Herms and Mattson 1992, Stamp 2003, Endara and Coley 2011). Because constitutive defences are always present, they require a more continuous allocation of resources, while the diversion of resources to inducible defences can usually be minimized to times of need. While it may seem paradoxical, the resource availability hypothesis (RAH) posits that larger investment into constitutive defences should occur in slow-growing plants in resource-poor

environments where the production and loss of plant tissue is relatively costly. In contrast, inducible defences should be more common in resource-rich environments where generating and replacing plant tissue is faster and less costly (Endara and Coley 2011). Similar to the RAH, the growth–differentiation balance hypothesis (GDBH) also predicts greater defences where resources are scarce because plant growth is more constrained by resource limitation than photosynthesis. Slow growth in the midst of ongoing photosynthesis leaves plants with a surplus of carbon to divert toward differentiating cells for defence; however, differentiation of constitutive and induced defences are not explicitly separated under the GDBH since they can be adaptively responsive to ecological and evolutionary pressures (Herms and Mattson 1992). Support for both the RAH and the GDBH in woody plants is mixed. Nevertheless, a recent meta-analysis suggests wide applicability of the RAH in a range of deciduous trees and shrubs, which tend to have higher levels of constitutive defences and lower growth rates in resource poor environments (Endara and Coley 2011). Meanwhile, conclusions about the applicability of the GDBH are more tentative given wide variation in experimental protocols, but there is context-dependent support for the GDBH in both deciduous (e.g., Glynn et al. 2007) and coniferous trees (e.g., Lombardero et al. 2000). To date, however, explicit tests of the RAH and the GDBH in coniferous trees are limited primarily to a handful of species, with little data available for intermediate and mature age classes. Under the framework of both the RAH and the GDBH, coniferous trees are expected to be relatively well protected by constitutive defences when resources are limited, although not to the complete exclusion of inducible defences.

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Scott Ferrenberg1,4,5, Jeffrey M. Kane2 and Joseph M. Langenhan3 

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Drivers of variation in conifer defence phenotypes Moreira et al. found that P-limitation alone reduced pine seedling biomass by roughly 58% compared with seedlings grown under

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complete fertilization, and led to an increase in resin duct density and relative area [a measure combining resin duct density and size that positively correlates to resin production and flow (Blanche et al. 1992)]. Similar to P-limitation, simulated herbivory (methyl jasmonate application) also led to a significant, but less pronounced reduction in biomass, and an increase in resin duct density and area (Figure 1). While both treatments led to changes in resin duct characteristics, when simulated herbivory took place under P-limitation it spurred a dramatic increase in resin duct defences, with genetic provenance having a strong influence on the response (Figure 1). These results support the existence of a trade-off among growth and defence in the juvenile stages of this relatively longlived pine species. Specifically, the production of resin ducts was costly regardless of resource availability, as indicated by the additional decrease in growth rates caused by the increase in resin ducts under simulated herbivory. The study also offers mixed support for the RAH since resource limitation did lead to greater constitutive defences at the expense of growth as predicted by the hypothesis. However, there was a far greater increase in induced defences, which is not expected under the RAH. At the same time, the study would seem to offer more ­support for the GDBH as the reduction in growth seen under P-limitation was accompanied by greater differentiation of both constitutive and inducible resin duct cells indicating an overall defense response to resource availability. A similar pattern was

Figure 1.  Illustrated results from Moreira et al. (2015), who demonstrated that phosphorus limitation alone or coupled with simulated herbivory (via application of the plant hormone methyl jasmonate) drastically reduced biomass, but increased the number and size of resin ducts in seedlings of P. pinaster. Variation in tree size and in the number and size of resin ducts in the stem cross-sections shown here are proportional to changes in biomass and resin duct characteristics reported by the authors. Phosphorus-limiting treatments are shown on the right (yellow) half of the illustration.

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The GDBH would further predict an increase in overall conifer defences when resources become scarce enough to inhibit growth but not photosynthesis (see Stamp 2003). Conifers defend themselves against natural enemies primarily with oleoresin (hereafter resin) produced in a system of ducts (also referred to as canals) found throughout the tree (­Franceschi et al. 2005). Resin ducts are a constitutive anatomical defence naturally produced in conifer needles and in the developing secondary xylem and phloem of the roots, limbs and stem, but they can also be induced in developing tissue in response to wounding or infection (Franceschi et al. 2005, Kolosova and Bohlmann 2012). Conifer resin functions as a mechanical defence by repelling or miring natural enemies as it is exuded from resin ducts. Additionally, resin also functions as a chemical defence consisting of carbon-based secondary compounds such as monoterpenes, sesquiterpenes and diterpene acids, which have been documented to reduce natural enemy attacks and reproductive success (Trapp and Croteau 2001, Mumm and Hilker 2006). While extensive tree mortality during forest-insect epidemics would seem to suggest otherwise, conifer resin is a formidable defence and phenotypic variation in resin duct characteristics has a particularly strong influence on tree fitness in the presence of natural enemies (O'Neill et al. 2002, Kane and Kolb 2010, King et al. 2011, Moreira et al. 2012, Ferrenberg et al. 2014, Zas et al. 2014). Given that resin duct traits correlate with conifer susceptibility to attack and subsequent survival, pines can be useful models for studying plant defences. While it may seem obvious that studies of plant defences should be focused on chemical, physical and anatomical traits that clearly serve a defensive role, a large number of commonly measured traits appear to be poor indicators of defence and resistance on larger scales (Carmona et al. 2011). It is against this backdrop that Moreira et al. (2015) report, in this issue of Tree Physiology, their study of resin duct defence allocation in juvenile Pinus pinaster (Aiton) trees representing 15 different half-sib families subjected to phosphorus (P) limitation and simulated herbivory (via methyl jasmonate application) in a full factorial greenhouse experiment. Roughly 7 months after germination, and 2 weeks after methyl jasmonate treatments were applied to simulate herbivore attack, the authors measured tree growth (height and biomass) and harvested the trees to measure resin duct characteristics (total number and size in various regions of each seedling). The authors not only looked for phenotypic responses to both P-limitation and methyl jasmonate treatments, but also for genetic influences on treatment responses that might indicate a role of heritable, locally adaptive trade-offs between resource availability and tree growth and defence.

To grow or defend? 109

Figure 2.  Conceptual hierarchy of factors experimentally demonstrated to influence resin duct number and size within individuals and populations in various species of conifers. Increased number/size of resin ducts under P-limitation and herbivory were demonstrated in P. pinaster by Moreira et al., while decreased number/size of resin ducts in drought experiments using P. edulis were reported by Gaylord et al. (2013). ­Wimmer and Grabner (1997) reported positive effects of above average temperatures during the growing season on resin duct production, while finding negative effects of above average precipitation. A positive ­relationship between tree growth and resin duct production was found in  P. ponderosa (Kane and Kolb 2010), P. edulis (Kläy 2011), and P. ­contorta and P. flexilis (Ferrenberg et al. 2014). In addition to the P. pinaster studied by Moreira et al. (2015), Rosner and Hannrup (2004) also demonstrated a significant influence of seedling provenance (genetic lines) on resin duct characteristics of P. abies in responses to environmental factors. Strong selection pressure exerted by tree-killing bark beetles against trees with fewer or smaller resin ducts was reported by Kane and Kolb (2010) and Ferrenberg et al. (2014).

numbers in Picea abies (Karst) decreased with above average growing-season precipitation, but increased in years with above average growing-season temperatures, suggesting an important influence of the timing of stresses and resource availability on resin duct production and characteristics. A number of studies have also found a positive relationship between tree growth and resin duct production in annual xylem rings of mature trees in several species of pines including: Pinus ponderosa (var. scopulorum Engelm.) (Kane and Kolb 2010), P. edulis (Kläy 2011), and Pinus contorta (var. latifolia Engelm.) and Pinus f­ lexilis (James) (Ferrenberg et al. 2014). As discussed above, Moreira et al. (2015) found genetic provenance was an important influence on resin duct induction in P. pinaster, a finding presaged by ­Rosner and Hannrup's (2004) study of the responses of resin duct traits to environmental factors among different genetic lines of P. abies. Finally, strong evidence that natural enemies exert selection pressure on resin duct traits comes from Kane and Kolb (2010), who found that tree-killing bark beetles selectively attacked P. ponderosa trees with fewer/smaller resin ducts in the most recent 20 years of annual growth, and from Ferrenberg et al. (2014), who demonstrated that P. contorta and P. flexilis trees that were killed by bark beetles had fewer resin ducts than individuals of both species that were attacked and survived.

Future directions in the study of conifer defences The mounting evidence that resin ducts are an important defence in pines and other conifers justifies the continued use of these

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found for the chemical defences of the same seedlings used by Moreira et al., as previously reported in a companion study by Sampedro et al. (2011). Specifically, P-limitation increased the chemical concentration of both constitutive and induced resin in P. pinaster seedlings, with induced resin being more potent than constitutive resin. The greater induction of resin ducts under key nutrient limitation alone would be interesting enough to draw attention to their study, but Moreira et al. also found that seedling provenance (family genetic lines) interacted with P-availability to strongly influence resin duct induction. This genetic effect on tree responses to resource availability and herbivory has important implications as it demonstrates that differences in defence phenotypes within a species can be due to heritable variation and is not simply plasticity in the face of environmental gradients. This finding is of note because it indicates that plant defence expression in response to resource limitation and herbivory is contextually adaptive. In other words, the evidence of strong genetic influences on the number and size of resin ducts induced among openly pollinated P. pinaster in response to simulated herbivory under P-limitation suggests the possibility of strong local adaptation to these pressures. Conifers, including pines, are known to be locally adapted to climate and edaphic properties even in cases where gene flow among populations is present (e.g., Cobb et al. 1994, Mitton et al. 1998). Likewise, resin defence traits such as chemical profile, flow rates and resin duct characteristics have been demonstrated as heritable (Strom et al. 2002, Rosner and Hannrup 2004, ­Westbrook et al. 2015). Thus, given their influence on fitness— either from benefits of protecting plants from attack, or through trade-off costs with other key functions—variation in resin defence phenotypes within and across species is likely to be adaptive to selection pressures from local environments and biotic interactions (Agrawal 2007). This scenario might explain the mixed support that various plant defence theories have garnered, but also highlights a need to further integrate plant defence studies with the geographic mosaic theory, which posits that natural selection pressures vary among populations due to changes in biotic communities and environments (Thompson 2005). To the extent that number and size of resin ducts influence components of fitness such as growth, survival and reproduction, these responses define selection pressures driving the evolution of tree defences. Moreira et al. have contributed two additional variables—herbivory and nutrient limitation—to the growing list of local and regional factors shown to influence the characteristics of resin ducts in pines and other conifers (­Figure  2). While P-limitation had a positive effect on resin duct size and density as reported by Moreira et al., Gaylord et al. (2013) found that prolonged experimental drought led to decreased resin duct density and size in Pinus edulis (Engelm.). Conversely, Wimmer and Grabner (1997) found that resin duct

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“when multiple adaptive peaks are occupied, we usually have no basis for asserting that one solution is better than another. The solution followed in any spot is a result of history; the first steps went in one direction, though others would have led to adequate prosperity as well.” Nevertheless, our understanding of the evolution and ecology of conifer defences has been greatly advanced by recent studies of resin defence phenotypes in relation to resource availability, population genetics and tree resistance to natural enemies under field conditions. Continued focus on the mechanisms and

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­ atterns of pine defences across species and ecosystems is p sure to yield exciting results.

Acknowledgments The authors thank Jeffry Mitton, the Editor, and reviewers for their helpful comments and suggestions.

Conflict of interest None declared.

References Agrawal AA (2007) Macroevolution of plant defense strategies. Trends Ecol Evol 22:103–109. Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493. Blanche CA, Lorio PL, Sommers RA, Hodges JD, Nebeker TE (1992) Seasonal cambial growth and development of loblolly pine: xylem formation, inner bark chemistry, resin ducts, and resin flow. For Ecol ­Manag 49:151–165. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448. Carmona D, Lajeunesse MJ, Johnson MT (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367. Cobb NS, Mitton JB, Whitham TG (1994) Genetic variation associated with chronic water and nutrient stress in pinyon pine. Am J Bot 81:936–940. Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398. Ferrenberg S, Mitton JB (2014) Smooth bark surfaces can defend trees against insect attack: resurrecting a ‘slippery’ hypothesis. Funct Ecol 28:837–845. Ferrenberg S, Kane JM, Mitton JB (2014) Resin duct characteristics associated with tree resistance to bark beetles across lodgepole and limber pines. Oecologia 174:1283–1292. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, Pangle RE, McDowell NG (2013) Drought predisposes piñon-juniper woodlands to insect attacks and mortality. New Phytol 198:567–578. Glynn C, Herms DA, Orians CM, Hansen RC, Larsson S (2007) Testing the growth-differentiation balance hypothesis: dynamic responses of willows to nutrient availability. New Phytol 176:623–634. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205:581–598. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. Kane JM, Kolb TE (2010) Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia ­ 164:601–609. King JN, Alfaro RI, Lopez MG, Van Akker L (2011) Resistance of Sitka spruce (Picea sitchensis (Bong.) Carr.) to white pine weevil (Pissodes strobi Peck): characterizing the bark defence mechanisms of resistant populations. Forestry 84:83–91.

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traits in plant defence hypothesis testing; however, a number of key gaps exist in our understanding of these traits and their defence roles. Specifically, changes in resin duct allocation, size and effectiveness against natural enemies across stages of phenology and ontogeny are likely and require investigation among species and environments (Boege and Marquis 2005, Barton and Koricheva 2010, Muola et al. 2010). These defences might also vary in relation to other anatomical defence mechanisms that can dramatically reduce natural enemy attack density on conifers (e.g., Ferrenberg and Mitton 2014). As shown under greenhouse conditions by Moreira et al. (2015), constitutive and induced resin duct production varies in response to edaphic properties, suggesting a need to consider how variation in parent material, nutrient pools and soil processes might influence defence production in other conifer species and tree life stages. For example, how might the results of Moreira et al. change if the source pine populations have a surplus of phosphorus in their home soils but chronically lack other key nutrients? Variation in both evolutionary and ecological processes across the landscape have likely generated a mosaic of functional tradeoffs within and among conifer species. While it may seem daunting to consider all sources of variation in experimental studies, the examples of Rosner and Hannrup (2004), Sampedro et al. (2011) and Moreira et al. (2015), to name but a few, represent efficient and illustrative approaches for understanding how local adaptations might influence plant defences in relation to environmental and biotic pressures. Even as we collectively and incrementally move toward a more nuanced, dynamic framework of plant defences, it is necessary to verify that presumed defence traits have measurable influences on plant fitness in the face of various natural enemy communities. This key step is often neglected in favour of interspecific or cross-system comparisons of specific secondary chemicals (e.g., tannin concentration, monoterpene profiles) or physical traits (e.g., leaf toughness) that have been demonstrated to be defensive in some plants and against some natural enemies, but that have yet to be widely related to plant fitness on larger scales (see Carmona et al. 2011). As noted by Gould and Lewontin (1979), who cautioned against viewing existing phenotypes as resulting from improvements through selection:

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Kläy M (2011) Are defensive structures good predictors of tree mortality under drought and insect pressure? Master thesis, Swiss Federal Institute of Technology, Bern, Switzerland. Kolosova N, Bohlmann J (2012) Conifer defenses against insects and pathogens. In: Schnyder H, Oßwald W (eds) Growth and defence in plants: resource allocation at multiple scales, Vol. 220. Springer, Berlin. Lombardero MJ, Ayres MP, Lorio PL Jr, Ruel JJ (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3:329–339. Mitton JB, Grant MC, Yoshino AM (1998) Variation in allozymes and stomatal size in pinyon (Pinus edulis, pinaceae), associated with soil moisture. Am J Bot 85:1262–1265. Moreira X, Alfaro RI, King JN (2012) Constitutive defenses and damage in Sitka spruce progeny obtained from crosses between white pine weevil resistant and susceptible parents. Forestry 85:87–97. Moreira X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol 35:112–123. Mumm R, Hilker M (2006) Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci 11:351–358. Muola A, Mutikainen P, Laukkanen L, Lilley M, Leimu R (2010) Genetic variation in herbivore resistance and tolerance: the role of plant lifehistory stage and type of damage. J Evol Biol 23:2185–2196. O'Neill GA, Aitken SN, King JN, Alfaro RI (2002) Geographic variation in resin canal defenses in seedlings from the Sitka spruce × white spruce introgression zone. Can J For Res 32:390–400. Rosner S, Hannrup B (2004) Resin canal traits relevant for constitutive resistance of Norway spruce against bark beetles: environmental and genetic variability. For Ecol Manag 200:77–87.

To grow or defend? Pine seedlings grow less but induce more defences when a key resource is limited.

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