Growth-differentiation Balance Hypothesis Research Articles

Divergent growth‐differentiation balance strategies and resource competition shape mortality patterns in ponderosa pine

AbstractDynamic resource availability leads to trade‐offs among functions in plants. The growth‐differentiation balance hypothesis (GDBH) predicts greater allocation of carbon to defense than growth when resources are scarce, with optimum defense production occurring at a point between the minimum and maximum growth rates. While the GDBH has been widely tested, consideration of phenotypic variation in rates for which defense is traded for growth and what this variation means for plant resistance remains rare. For defense, pines produce and store oleoresin in “resin ducts.” Retrospective comparisons of resin ducts in pines have revealed that trees with greater numbers, sizes, or areas of xylem resin ducts are more likely to avoid or survive insect attack. We used tree ring chronologies to quantify phenotypic variation in growth and resin duct defenses in pairs of living and bark beetle‐killed Pinus ponderosa trees in southern New Mexico, USA, and to test the utility of the GDBH for explaining tree mortality. We also assessed the sensitivity of annual growth to climate and competitor density in years preceding mortality in each pair. Survivors had greater growth rates and total cross‐sectional areas of resin ducts than trees killed by bark beetles. We did not observe a difference in climate–growth relationships among the groups; however, trees killed by bark beetles suffered negative effects of competition while survivors did not. Growth‐defense trade‐offs conformed to the GDBH's prediction of a quadratic relationship; however, the two groups significantly differed in the rate at which defense was traded for increasing levels of annual growth. Our results demonstrate that phenotypic variation in the trade‐off between growth and defense could be used to characterize trees that were killed by or survived recent natural enemy epidemics. We hypothesize that the GDBH could be integrated with the characterization of phenotypic variation in growth‐differentiation strategies—along with parsing of gene versus environment influences on phenotypes—at both local and landscape scales to increase our understanding of patterns of natural enemy impacts in plant populations.

Changes in spinescence across leaf ontogeny support the optimal defence hypothesis in blackberries (Rubus adenotrichos)

Abstract Hypotheses based on allocation theory and herbivore selection offer opposite predictions about how defence levels against herbivores change as the plant tissue grows. The growth differentiation balance hypothesis (GDBH) assumes that defences will be resource-limited in immature tissues and predict that defence levels increase as the plant tissue grows. Conversely, the optimal defence hypothesis (ODH) proposes that plants would have the highest level of defences in the parts that have the highest value in terms of fitness and/or are more frequently attacked by herbivores, such as young tissues. We examine whether spinescence in the shrub Rubus adenotrichos (blackberry) change as the leaf grows, and if this change is consistent with the GDBH or the ODH. We compare the petiole area occupied by prickles, the prickles density and the individual prickle area in mature versus young petioles from Rubus adenotrichos. Our results show that, in R. adenotrichos, young tissues are more protected than mature tissues. Prickles density and the petiole area occupied by prickles were up to 25% higher in young petioles than in mature ones. These results support the ODH, reinforcing the idea that extrinsic factors such as herbivores pressure might drive the change of structural defences level across leaf ontogeny.

Analysis and correlations of the protein content and selected 'antinutrients' of faba beans (Vicia faba) in a German sample set of the cultivation years 2016, 2017, and 2018.

Faba beans (Vicia faba) experienced a significant revival in cultivation in Western Europe in the last decade. In this study, potential correlations between protein content (PC), trypsin inhibitory activity (TIA), and tannin content were investigated in a large German sample set with bean samples obtained from 50 different farms present in 11 German federal states. Three consecutive cultivation years (2016, 2017, and 2018) were included. The faba bean samples were grown under real cultivation conditions without any specific experimental design and finally marketed by the farmers. This enabled researchers to identify the relationship and extent of the three quality parameters towards the varying cultivation conditions and practices. Moreover, the correlations observed between the parameters were brought into the context of well-known theoretical plant hypotheses such as the carbon-nutrient balance hypothesis (CNBH), the growth-differentiation balance hypothesis (GDBH), as well as the protein competition model (PCM) for evaluating the potential for use in predictions. The study showed a significant negative correlation between PC and tannin content in faba beans over each cultivation year, whereas a positive correlation between TIA and tannin content was found. No clear correlation was observed between PC and TIA. The three plant hypotheses (CNBH, GDBH, and PCM) seem to be not fully valid. Nonetheless, these findings might be a useful guideline for predicting the composition of selected compounds, and sustainable recommendations about cultivation and exploitation for the feed and food sector can be derived. © 2022 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Effects of climate change on plant resource allocation and herbivore interactions in a Neotropical rainforest shrub

AbstractClimate change is a mounting global issue, but its consequences will be variable across regions. Tropical species are hypothesized to have reduced climatic adaptability and plasticity. Yet, relative to temperate species, less is understood about how they will respond to climate change. Rising temperature and atmospheric CO2 could impact plant–herbivore systems directly by altering species traits or abundances, or the effects could be indirect by altering the strength and direction of the relationships that govern organismal strategies and interactions. Using open‐top chambers in a Neotropical wet forest, we applied a full‐factorial combination of active warming and CO2 fertilization to investigate the above‐ground, short‐term effects of climate change on plant–herbivore interactions in a common Neotropical shrub, Piper generalense. We aimed to answer two main questions: (1) Could climate change alter plant–herbivore systems through direct effects on plant growth rate, chemical defense, and/or insect herbivore damage rate? and (2) Could climate change affect plant–herbivore systems indirectly by altering (a) the strength of plant resource allocation trade‐offs between growth and defense or (b) the effectiveness of plant chemical defense against herbivory? None of the microclimate treatments had direct effects on plant growth, chemical defense, or herbivore damage. However, we did observe a positive relationship between growth and chemical defense in treatments mimicking climate‐change conditions, which partially supports the growth–differentiation balance hypothesis. We did not detect any effects of treatments on the effectiveness of plant chemical defense against herbivory. It appears that, in this system, increased CO2 concentration and temperature may cause indirect, cascading consequences, even where direct effects are not observable. We recommend more climate‐change experiments addressing multi‐trophic interactions that focus not only on the direct responses of organisms but also on the ways in which climate change can restructure the relationships that govern complex biotic systems.

Exploring evolutionary theories of plant defence investment using field populations of the deadly carrot.

There are a number of disparate models predicting variation in plant chemical defences between species, and within a single species over space and time. These can give conflicting predictions. Here we review a number of these theories, before assessing their power to predict the spatial-temporal variation of thapsigargins between and within populations of the deadly carrot (Thapsia garganica). By utilizing multiple models simultaneously (optimum defence theory, growth rate hypothesis, growth-differentiation balance hypothesis, intra-specific framework and resource exchange model of plant defence), we will highlight gaps in their predictions and evaluate the performance of each. Thapsigargins are potent anti-herbivore compounds that occur in limited richness across the different plant tissues of T. garganica, and therefore represent an ideal system for exploring these models. Thapsia garganica plants were collected from six locations on the island of Ibiza, Spain, and the thapsigargins quantified within reproductive, vegetative and below-ground tissues. The effects of sampling time, location, mammalian herbivory, soil nutrition and changing root-associated fungal communities on the concentrations of thapsigargins within these in situ observations were analysed, and the results were compared with our model predictions. The models performed well in predicting the general defence strategy of T. garganica and the above-ground distribution of thapsigargins, but failed to predict the considerable proportion of defences found below ground. Models predicting variation over environmental gradients gave conflicting and less specific predictions, with intraspecific variation remaining less understood. Here we found that multiple models predicting the general defence strategy of plant species could likely be integrated into a single model, while also finding a clear need to better incorporate below-ground defences into models of plant chemical defences. We found that constitutive and induced thapsigargins differed in their regulation, and suggest that models predicting intraspecific defences should consider them separately. Finally, we suggest that in situ studies be supplemented with experiments in controlled environments to identify specific environmental parameters that regulate variation in defences within species.

Attack rates of Sirex noctilio and patterns of pine tree defenses and mortality in northern Patagonia.

Accidental and intentional global movement of species has increased the frequency of novel plant-insect interactions. In Patagonia, the European woodwasp, Sirex noctilio, has invaded commercial plantations of North American pines. We compared the patterns of resin defenses and S. noctilio-caused mortality at two mixed-species forests near San Carlos de Bariloche, Argentina. We observed lower levels of resin flow and higher levels of mortality in Pinus contorta compared with Pinus ponderosa. In general, S. noctilio attacked trees with lower resin compared with neighboring trees. Resin production in P. ponderosa was not related to growth rates, but for P. contorta, slower growing trees produced less resin than faster growing conspecifics. For all infested trees, attack density and number of drills (ovipositor probes) per attack did not vary with resin production. Most attacks resulted in one or two drills. Attack rates and drills/attack were basically uniform across the bole of the tree except for a decrease in both drills/attack and attack density in the upper portion of the crown, and an increase in the attack density for the bottom 10% of the tree. Planted pines in Patagonia grow faster than their counterparts in North America, and produce less resin, consistent with the growth-differentiation balance hypothesis. Limited resin defenses may help to explain the high susceptibility of P. contorta to woodwasps in Patagonia.

Genetic control and evolutionary potential of a constitutive resistance mechanism against the spruce budworm (Choristoneura fumiferana) in white spruce (Picea glauca).

Insect herbivory may drive evolution by selecting for trees with heritable resistance against defoliation. The spruce budworm (Choristoneura fumiferana, SBW) is a highly damaging forest insect pest that can affect population structure of white spruce (Picea glauca) in North America. Resistance against SBW was recently described in white spruce and was linked to three constitutive resistance biomarkers: the phenolic compounds piceol and pungenol, and expression of a beta-glucosidase encoding gene (Pgβglu-1). We investigated the phenotypic variability and heritability of these resistance biomarkers and of picein, the precursor of piceol, in the foliage of 874 trees belonging to 33 full-sib families and 71 clonal lines under evaluation in seven field locations in Eastern Canada. We aimed to (i) determine their genetic control, (ii) estimate the genetic and phenotypic correlations among defense biomarkers, and (iii) determine whether their constitutive levels are associated with detrimental trade-offs on growth. Quantitative genetics analyses indicated that all four traits are moderately to highly heritable. The full-sib and clonal analyses showed that additive and non-additive genetic effects play major and minor roles, respectively. Positive genetic and phenotypic correlations between resistance biomarkers and primary growth indicated that there is no trade-off between total height and height increment and resistance traits, contradicting the GDBH (Growth Differentiation Balance Hypothesis). Our findings about the predominant additive genetic basis of the resistance biomarkers show that adaptive evolution of white spruce natural populations to resist to SBW is possible and that potentially important gains could also be expected from artificial selection.

Genetic down-regulation of gibberellin results in semi-dwarf poplar but few non-target effects on chemical resistance and tolerance to defoliation

Plant stature can be strongly modified via regulation of endogenous levels and signalling of the plant hormone gibberellin (GA). Down-regulation of GA can produce semi-dwarf tree varieties with improved qualities such as reduced susceptibility to wind damage, enhanced root growth and more compact cultivation. However, these modifications may have unintended, non-target consequences for defence against herbivores, via either of two mechanisms: (i) reduced biomass production may cause trade-offs with chemical resistance traits, as predicted by the growth-differentiation balance hypothesis, and (ii) altered biomass allocation to either roots or photosynthetic tissues may affect regrowth potential and thus tolerance to defoliation. We studied GA down-regulated (GE) and non-transgenic wild-type hybrid poplar (Populus alba × P. tremula) in an outdoor, aboveground common garden and defoliated half of all replicate trees to simulate defoliation. We then quantified the independent and interactive effects of genotype and defoliation on growth and chemical resistance-related traits, including phenolic glycosides (PGs), condensed tannin and nitrogen. We also calculated tolerance to defoliation as the differential in relative growth between undefoliated and defoliated trees. Our results indicate that two of the four GA down-regulated genotypes had significantly reduced stem height, basal diameter, volume (d²h), total biomass and increased allocation to leaves relative to the wild type. One of those two genotypes also had reduced allocation to roots. One and sometimes both of these same two genotypes also had at least 20% lower levels of condensed tannins and PGs and similar increases in lignin and nitrogen. Tolerance, as calculated by the differential in relative growth between undefoliated and defoliated trees, was similar among all experimental genotypes. However, two GE genotypes flushed fewer leaves in response to defoliation relative to the wild type. Our results indicate that GA down-regulation strongly alters biomass production and allocation in poplar but does not necessarily compromise the ability of these trees to tolerate damage. However, some of the modifications we observed do have the potential to alter non-target resistance traits over time, and warrant further research, especially under plantation conditions.

Foliar flavonol concentration in Sclerocarya birrea saplings responds to nutrient fertilisation according to growth-differentiation balance hypothesis

The growth-differentiation balance hypothesis (GDBH) postulates a nonlinear, ‘hump-shaped’ response of plant secondary metabolites (PSMs), such as flavonoids, in relation to nitrogen (N) availability. The response is most easily detected when there are at least five levels of N availability, but very few studies that directly or indirectly tested the GDBH have used three or more levels. Fifty Sclerocarya birrea (marula) saplings (mean basal diameter = 35.5 mm, SEM = 0.52; mean height = 80.9 cm, SEM = 1.02), were randomly assigned to five fertiliser application rates in an orchard. Fertilizer [N:P:K (3:1:5) (26)] containing slow release nitrate was applied to each sapling as a top dressing every two months during the growing season at rates equivalent to 0, 20, 40, 80 and 120 g N m−2. Average flavonoid content of 30–35 recently matured leaves per sapling was indirectly measured every two months during the growing season using the Dualex® Series 4 instrument. The nonlinear, ‘hump-shaped’ response predicted by GDBH was observed, indicating that allocation of carbon to PSMs was more limited at both high and low nutrient availability than at intermediate nutrient availability. Successful detection of the quadratic response was probably facilitated by only measuring flavonols, which are the main PSMs in S. birrea, and by conducting the experiment on soils of very low fertility.

Regulation of Fatty Acid Production and Release in Benthic Algae: Could Parallel Allelopathy Be Explained with Plant Defence Theories?

Many organisms produce chemical compounds, generally referred as secondary metabolites, to defend against predators and competitors (allelopathic compounds). Several hypotheses have been proposed to explain the interaction between environmental factors and secondary metabolites production. However, microalgae commonly use simple metabolites having a role in primary metabolism as allelopathic compounds. The aim of this study was to determine whether classical theories of plant chemical defences could be applied to microalgae producing allelochemicals derived from the primary metabolism. Our study was designed to investigate how growth phase, algal population density, nutrient limitation and carbon assimilation affect the production and release of allelopathic free fatty acids (FFAs) among other FFAs. The model species used was Uronema confervicolum, a benthic filamentous green alga that produces two allelopathic FFAs (linoleic and α-linolenic acids) inhibiting diatom growth. FFAs have been quantified in algal biomass and in culture medium. Our results were analysed according to two classical plant defence theories: the growth-differentiation balance hypothesis (GDBH) and the optimal defence theory (ODT), based on the metabolic capacities for defence production and on the need for defence, respectively. While a higher production of allelopathic compounds under increased light conditions supports the use of GDBH with this microalga, the observation of a negative feedback mechanism mostly supports ODT. Therefore, both theories were insufficient to explain all the observed effects of environmental factors on the production of these allelochemicals. This highlights the needs of new theories and models to better describe chemical interactions of microalgae.

Does the Growth Differentiation Balance Hypothesis Explain Allocation to Secondary Metabolites in Combretum apiculatum , an African Savanna Woody Species?

The growth differentiation balance hypothesis (GDBH) provides a framework that predicts a trade-off between costs of secondary metabolites (SMs) relative to the demand for photosynthate by growth. However, this hypothesis was developed using empirical evidence from plant species in northern boreal and temperate systems, leaving its applicability to species under different abiotic and biotic conditions questionable and generalizations problematic. The objective of this study was to investigate whether the GDBH explains allocation to SMs in the deciduous African savanna woody species C. apiculatum along a 6-point N gradient. The cornerstone prediction of the GDBH, i.e., the parabolic response in SMs along the N gradient, was not observed, with secondary metabolism showing compound-specific responses. Quercetin, myricetin, and kaempferol glycoside concentrations, all produced via the same pathway, responded differently across the N gradient. Flavonol glycoside, cinnamic acid, and quercetin glycoside concentrations decreased as N increased, which provides partial support for the carbon nutrient balance hypothesis. Simulated herbivory had no effect on photosynthesis, decreased foliar N and consequently increased C:N ratio, but did not induce an increase in SMs, with condensed tannins and flavonol glycosides being unaffected. Defoliated plants at low N concentration compensated for lost biomass, which suggests a tolerance response, but as predicted by the limiting resource model, plants at higher N concentration were evidently C limited and thus unable to compensate. Our results show that the GDBH does not explain allocation to SMs in C. apiculatum, and suggest that mechanistic explanations of plant allocation should consider the integrative defensive effect of changed SMs.

Growth, nitrogen and tannins of semi-arid savanna saplings in response to herbivory and water

Large herbivores and water availability are important factors determining the growth of woody plants from the sapling stage to the adult stage and hence the abundance of woody plants in African savannas. We tested specific predictions derived from the growth-differentiation balance hypothesis that either severe browsing intensity or low watering frequency (i) reduce plant height, stem circumference, plant mass or new shoot abundance, or (ii) reduce nitrogen or condensed tannin concentrations. We applied four levels of browsing by domestic goats and three levels of watering frequency to saplings growing in pots in two experiments under a clear plastic roof. One experiment was on Combretum apiculatum and the other was on Dichrostachys cinerea. Our predictions were not consistently supported by both experiments. However, the responses did indirectly suggest that C. apiculatum saplings were more prone than D. cinerea saplings to carbon limitation (e.g., reduced abundance of new shoots, reduced tannin concentration) under either severe browsing or low watering frequency. We attributed this difference to the contrasting morphology of the two species and concluded that the extent to which severe herbivory or water stress limit the recruitment of adult woody plants in semi-arid savannas is species-dependent.

Reuse of Organomineral Substrate Waste from Hydroponic Systems as Fertilizer in Open-Field Production Increases Yields, Flavonoid Glycosides, and Caffeic Acid Derivatives of Red Oak Leaf Lettuce (Lactuca sativa L.) Much More than Synthetic Fertilizer.

Effects of organic waste from a hydroponic system added with minerals (organomineral fertilizer) and synthetic fertilizer on major polyphenols of red oak leaf lettuce using HPLC-DAD-ESI-MS(3) were investigated. Interestingly, contents of the main flavonoid glycosides and caffeic acid derivatives of lettuce treated with organomineral fertilizer were equal to those synthesized without soil additives. This was found although soil nutrient concentrations, including that of nitrogen, were much lower without additives. However, lettuce treated with synthetic fertilizer showed a significant decrease in contents of caffeic acid derivatives and flavonoid glycosides up to 78.3 and 54.2%, respectively. It is assumed that a negative effect of a high yield on polyphenols as described in the growth-differentiation balance hypothesis can be counteracted by (i) a higher concentration of Mg or (ii) optimal physical properties of the soil structure. Finally, the organomineral substrate waste reused as fertilizer and soil improver resulted in the highest yield (+78.7%), a total fertilizer saving of 322 kg ha(-1) and waste reduction in greenhouses.

The role of nitrogen and phosphorus in regulating Phormidium sp. (cyanobacteria) growth and anatoxin production.

Benthic proliferations of the cyanobacteria Phormidium can cover many kilometres of riverbed. Phormidium can produce neurotoxic anatoxins and ingestion of benthic mats has resulted in numerous animal poisonings in the last decade. Despite this, there is a poor understanding of the environmental factors regulating growth and anatoxin production. In this study, the effects of nitrogen and phosphorus on the growth of two Phormidium strains (anatoxin-producing and non-anatoxin-producing) were examined in batch monocultures. Cell concentrations were significantly reduced under reduced nitrogen (ca. <0.100 mM) and phosphorus conditions (ca. <0.003 mM). Cell concentrations and maximum growth rates were higher for the non-anatoxin-producing strain in all treatments, suggesting there may be an energetic cost to toxin production. Cellular anatoxin concentrations were lowest (169 fg cell(-1)) under the high-nitrogen and high-phosphorus treatment. This supports the growth-differentiation balance hypothesis that suggests actively dividing and expanding cells are less likely to produce secondary-metabolites. Anatoxin quota was highest (>407 fg cell(-1)) in the reduced phosphorus treatments, possibly suggesting that it is produced as a stress response to growth limiting conditions. In all treatments there was a 4-5-fold increase in anatoxin quota in the lag growth phase, possibly indicating it may provide a physiological benefit during initial substrate colonization.

Plant defence as a complex and changing phenotype throughout ontogeny.

Ontogenetic changes in anti-herbivore defences are common and result from variation in resource availability and herbivore damage throughout plant development. However, little is known about the simultaneous changes of multiple defences across the entire development of plants, and how such changes affect plant damage in the field. The aim of this study was to assess if changes in the major types of plant resistance and tolerance can explain natural herbivore damage throughout plant ontogeny. An assessment was made of how six defensive traits, including physical, chemical and biotic resistance, simultaneously change across the major transitions of plant development, from seedlings to reproductive stages of Turnera velutina growing in the greenhouse. In addition, an experiment was performed to assess how plant tolerance to artificial damage to leaves changed throughout ontogeny. Finally, leaf damage by herbivores was evaluated in a natural population. The observed ontogenetic trajectories of all defences were significantly different, sometimes showing opposite directions of change. Whereas trichome density, leaf toughness, extrafloral nectary abundance and nectar production increased, hydrogen cyanide and compensatory responses decreased throughout plant development, from seedlings to reproductive plants. Only water content was higher at the intermediate juvenile ontogenetic stages. Surveys in a natural population over 3 years showed that herbivores consumed more tissue from juvenile plants than from younger seedlings or older reproductive plants. This is consistent with the fact that juvenile plants were the least defended stage. The results suggest that defensive trajectories are a mixed result of predictions by the Optimal Defence Theory and the Growth-Differentiation Balance Hypothesis. The study emphasizes the importance of incorporating multiple defences and plant ontogeny into further studies for a more comprehensive understanding of plant defence evolution.

Compartmentalization, Resource Allocation, and Wood Quality

The concept of a trade-off of tree resources between growth and defense is readily grasped. The most detailed development of the concept is for the growth-differentiation balance hypothesis that predicts that resources for normal growth and primary metabolism are diverted to support plant defense and secondary or stress metabolism. This hypothesis has been applied to the biosynthetic cost of stress metabolites that protect wood and foliage from herbivory. This review suggests that the trade-offs of primary to stress metabolism is an ongoing theme throughout the evolution of land plants. This review extends the concept of the growth/defense trade-off to processes of apoptosis in the constitutive development of tracheary elements and heartwood as well as to the induced boundary-setting processes of compartmentalization of decay in living trees. For wood utilization, the confusion of heartwood with wound-initiated discoloration continues to obscure the sources of value loss, particularly for high-value hardwood lumber. Examples are drawn from the anatomical effects of tree injury from fire, storms, and vascular wilt disease.

Down-regulation of gibberellic acid in poplar has negligible effects on host-plant suitability and insect pest response

Endogenous levels and signaling of gibberellin plant hormones such as gibberellic acid (GA) have been genetically down-regulated to create semi-dwarf varieties of poplar. The potential benefits of semi-dwarf stature include reduced risk of wind damage, improved stress tolerance, and improved wood quality. Despite these benefits, modification of growth traits may have consequences for nontarget traits that confer defense against insect herbivores. According to the growth-differentiation balance hypothesis, reductions in growth may shift allocation of carbon from growth to chemical resistance traits, thereby altering plant defense. To date, host-plant suitability and pest response have not been comprehensively evaluated in GA down-regulated plants. We quantified chemical resistance and nitrogen (an index of protein) in GA down-regulated and wild-type poplar (Populus alba × P. tremula) genotypes. We also evaluated the performance of both generalist (Lymantria dispar) and specialist (Chrysomela scripta) insect pests reared on these genotypes. Our evaluation of resistance traits in four GA down-regulated genotypes revealed increased phenolic glycosides in one modified genotype and reduced lignin in two modified genotypes relative to the non-transgenic wild type. Nitrogen levels did not vary significantly among the experimental genotypes. Generalists reared on the four GA down-regulated genotypes exhibited reduced performance on only one modified genotype relative to the wild type. Specialists, however, performed similarly across all genotypes. Results from this study indicate that although some nontarget traits varied among GA down-regulated genotypes, the differences in poplar pest susceptibility were modest and highly genotype-specific.

Dynamic extrafloral nectar production: the timing of leaf damage affects the defensive response in Senna mexicana var. chapmanii (Fabaceae).

• Extrafloral nectar (EFN) mediates food for protection mutualisms between plants and defensive insects. Understanding sources of variation in EFN production is important because such variations may affect the number and identity of visitors and the effectiveness of plant defense. We investigated the influence of plant developmental stage, time of day, leaf age, and leaf damage on EFN production in Senna mexicana var. chapmanii. The observed patterns of variation in EFN production were compared with those predicted by optimal defense theory.• Greenhouse experiments with potted plants were conducted to determine how plant age, time of day, and leaf damage affected EFN production. A subsequent field study was conducted to determine how leaf damage, and the resulting increase in EFN production, affected ant visitation in S. chapmanii.• More nectar was produced at night and by older plants. Leaf damage resulted in increased EFN production, and the magnitude of the response was greater in plants damaged in the morning than those damaged at night. Damage to young leaves elicited a stronger defensive response than damage to older leaves, in line with optimal defense theory. Damage to the leaves of S. chapmanii also resulted in significantly higher ant visitation in the field.• Extrafloral nectar is an inducible defense in S. chapmanii. Developmental variations in its production support the growth differentiation balance hypothesis, while within-plant variations and damage responses support optimal defense theory.

Chemical defense lowers plant competitiveness.

Both plant competition and plant defense affect biodiversity and food web dynamics and are central themes in ecology research. The evolutionary pressures determining plant allocation toward defense or competition are not well understood. According to the growth-differentiation balance hypothesis (GDB), the relative importance of herbivory and competition have led to the evolution of plant allocation patterns, with herbivore pressure leading to increased differentiated tissues (defensive traits), and competition pressure leading to resource investment towards cellular division and elongation (growth-related traits). Here, we tested the GDB hypothesis by assessing the competitive response of lima bean (Phaseolus lunatus) plants with quantitatively different levels of cyanogenesis-a constitutive direct, nitrogen-based defense against herbivores. We used high (HC) and low cyanogenic (LC) genotypes in different competition treatments (intra-genotypic, inter-genotypic, interspecific), and in the presence or absence of insect herbivores (Mexican bean beetle, Epilachna varivestis) to quantify vegetative and generative plant parameters (above and belowground biomass as well as seed production). Highly defended HC-plants had significantly lower aboveground biomass and seed production than LC-plants when grown in the absence of herbivores implying significant intrinsic costs of plant cyanogenesis. However, the reduced performance of HC- compared to LC-plants was mitigated in the presence of herbivores. The two plant genotypes exhibited fundamentally different responses to various stresses (competition, herbivory). Our study supports the GDB hypothesis by demonstrating that competition and herbivory affect different plant genotypes differentially and contributes to understanding the causes of variation in defense within a single plant species.

Sex-related differences in growth and carbon allocation to defence in Populus tremula as explained by current plant defence theories.

Plant defence theories have recently evolved in such a way that not only the quantity but also the quality of mineral nutrients is expected to influence plant constitutive defence. Recently, an extended prediction derived from the protein competition model (PCM) suggested that nitrogen (N) limitation is more important for the production of phenolic compounds than phosphorus (P). We aimed at studying sexual differences in the patterns of carbon allocation to growth and constitutive defence in relation to N and P availability in Populus tremula L. seedlings. We compared the gender responses in photosynthesis, growth and whole-plant allocation to phenolic compounds at different combination levels of N and P, and studied how they are explained by the main plant defence theories. We found no sexual differences in phenolic concentrations, but interestingly, slow-growing females had higher leaf N concentration than did males, and genders differed in their allocation priority. There was a trade-off between growth and the production of flavonoid-derived phenylpropanoids on one hand, and between the production of salicylates and flavonoid-derived phenylpropanoids on the other. Under limited nutrient conditions, females prioritized mineral nutrient acquisition, flavonoid and condensed tannin (CT) production, while males invested more in above-ground biomass. Salicylate accumulation followed the growth differentiation balance hypothesis as low N mainly decreased the production of leaf and stem salicylate content while the combination of both low N and low P increased the amount of flavonoids and CTs allocated to leaves and to a lesser extent stems, which agrees with the PCM. We suggest that such a discrepancy in the responses of salicylates and flavonoid-derived CTs is linked to their clearly distinct biosynthetic origins and/or their metabolic costs.