Can the growth–differentiation balance hypothesis be tested rigorously?

The growth–differentiation balance (GDB) hypothesis (as elaborated by Herms and Mattson) provides a framework for examining the impact of a resource gradient on the constant tradeoff between growth and differentiation in cells and tissues of plants, in particular with the consequences for plant defense. The GDB hypothesis, which is the most mature of the hypotheses of plant defensive levels, has not been tested directly. Examination of the requirements for a rigorous test indicates that, like the other hypotheses of plant defense, it cannot be tested directly. Furthermore, rigorously testing the primary derivative hypotheses, while possible, would require considerable methodological effort, on a scale not previously attempted for tests of plant defense, which is likely to discourage researchers, and understandably so, even though the GDB hypothesis warrants methodical investigation due to its potential explanatory power. Although farther removed from the abstract model (i.e. the GDB framework), other derivative hypotheses can be tested, but doing so will require thoughtful consideration and acknowledgement of that. Study of a few carefully chosen systems (i.e. plant species) may provide considerable insight and potentially useful refinement of the GDB framework.     

Out of the quagmire of plant defense hypotheses

Several hypotheses, mainly Optimal Defense (OD), Carbon: Nutrient Balance (CNB), Growth Rate (GR), and Growth-Differentiation Balance (GDB), have individually served as frameworks for investigating the patterns of plant defense against herbivores, in particular the pattern of constitutive defense. The predictions and tests of these hypotheses have been problematic for a variety of reasons and have led to considerable confusion about the state of the "theory of plant defense." The primary contribution of the OD hypothesis is that it has served as the main framework for investigation of genotypic expression of plant defense, with the emphasis on allocation cost of defense. The primary contribution of the CNB hypothesis is that it has served as the main framework for investigation of how resources affect phenotypic expression of plant defense, often with studies concerned about allocation cost of defense. The primary contribution of the GR hypothesis is that it explains how intrinsic growth rate of plants shaped evolutionarily by resource availability affects defensive patterns. The primary contribution of the expanded GDB hypothesis is that it recognizes the constant physiological tradeoff between growth and differentiation at the cellular and tissue levels relative to the selective pressures of resource availability, including explicitly taking into account plant tolerance of damage by enemies. A clearer understanding of these hypotheses and what we have learned from investigations that use them can facilitate development of well-designed experiments that address the gaps in our knowledge of plant defense.     

Costs of Defense and a Test of the Carbon-Nutrient Balance and Growth-Differentiation Balance Hypotheses for Two Co-Occurring Classes of Plant Defense

One of the goals of chemical ecology is to assess costs of plant defenses. Intraspecific trade-offs between growth and defense are traditionally viewed in the context of the carbon-nutrient balance hypothesis (CNBH) and the growth-differentiation balance hypothesis (GDBH). Broadly, these hypotheses suggest that growth is limited by deficiencies in carbon or nitrogen while rates of photosynthesis remain unchanged, and the subsequent reduced growth results in the more abundant resource being invested in increased defense (mass-balance based allocation). The GDBH further predicts trade-offs in growth and defense should only be observed when resources are abundant. Most support for these hypotheses comes from work with phenolics. We examined trade-offs related to production of two classes of defenses, saponins (triterpenoids) and flavans (phenolics), in Pentaclethra macroloba (Fabaceae), an abundant tree in Costa Rican wet forests. We quantified physiological costs of plant defenses by measuring photosynthetic parameters (which are often assumed to be stable) in addition to biomass. Pentaclethra macroloba were grown in full sunlight or shade under three levels of nitrogen alone or with conspecific neighbors that could potentially alter nutrient availability via competition or facilitation. Biomass and photosynthesis were not affected by nitrogen or competition for seedlings in full sunlight, but they responded positively to nitrogen in shade-grown plants. The trade-off predicted by the GDBH between growth and metabolite production was only present between flavans and biomass in sun-grown plants (abundant resource conditions). Support was also only partial for the CNBH as flavans declined with nitrogen but saponins increased. This suggests saponin production should be considered in terms of detailed biosynthetic pathway models while phenolic production fits mass-balance based allocation models (such as the CNBH). Contrary to expectations based on the two defense hypotheses, trade-offs were found between defenses and photosynthesis, indicating that studies of plant defenses should include direct measures of physiological responses.     

Macroevolution of plant defense strategies

Theories of plant defense expression are typically based on the concepts of tradeoffs among traits and of phylogenetic conservatism within clades. Here, I review recent developments in phylogenetic approaches to understanding the evolution of plant defense strategies and plant-herbivore coevolutionary interactions. I focus particularly on multivariate defense against insect herbivores, which is the simultaneous deployment of multiple traits, often arranged as convergently evolved defense syndromes. Answering many of the outstanding questions in the biology of plant defense will require generating broad hypotheses that can be explicitly tested by using comparative approaches and interpreting phylogenetic patterns. The comparative approach has wide-spread potential to reinvigorate tests of classic hypotheses about the evolution of interspecific interactions.     

A quantitative evaluation of major plant defense hypotheses, nature versus nurture, and chemistry versus ants

Variation in plant secondary metabolite content can arise due to environmental and genetic variables. Because these metabolites are important in modifying a plant’s interaction with the environment, many studies have examined patterns of variation in plant secondary metabolites. Investigations of chemical defenses are often linked to questions about the efficacies of plant defenses and hypotheses on their evolution in different plant guilds. We performed a series of meta-analyses to examine the importance of environmental and genetic sources of variation in secondary metabolites as well as the antiherbivore properties of different classes of defense. We found both environmental and genetic variation affect secondary metabolite production, supporting continued study of the carbon-nutrient balance and growth-differentiation balance hypotheses. Defenses in woody plants are more affected by genetic variation, and herbaceous plant defenses are more influenced by environmental variation. Plant defenses in agricultural and natural systems show similar responses to manipulations, as do plants in laboratory, greenhouse, or field studies. What does such variation mean to herbivores? A comparison of biotic, physical, and chemical defenses revealed the most effective defensive strategy for a plant is biotic mutualisms with ants. Fast-growing plants are most often defended with qualitative defenses and slow-growing plants with quantitative defenses, as the plant apparency and resource availability hypotheses predict. However, we found the resource availability hypothesis provides the best explanation for the evolution of plant defenses, but the fact that there is considerable genetic and environmental variation in defenses indicates herbivores can affect plant chemistry in ecological and evolutionary time.     

植物防卫的碳-养分平衡假说

碳-养分平衡假说(carbon-nutrient balance hypothesis,CNBH)认为,植物组织中次生代谢物浓度受环境碳-资源有效性控制;植物体内次生代谢物按照化学计量的要求进行分配;资源分配给防卫物的必要条件是资源供应量满足植物生长需求后仍过剩。CNBH自提出以来,其适用范围不断受到限制,解释与预测研究结果的能力逐渐显现不足。期间,对CNBH进行过优化和修改,设置了多种限制条件,以期能使CNBH得到补救,继续成为指导植物-草食动物间相互作用和植物体内资源分配的相关理论。然而,随着研究的逐渐深入,CNBH被证实缺乏逻辑性和内在一致性;CNBH不能满足假说本身的发展要求,缺乏明确可行的量化指标体系,也没有明确地标识出理论预测范围与可测试范围之间的界限。研究表明,CNBH的基本假设本身是错误的;随着人们对植物-草食动物间相互作用的认知能力加强,更深刻地认识到资源在植物体内的分配模式,意识到CNBH假说的严重缺陷。在现有的植物防卫理论中,生长-分化平衡假说(growth-differentiation balance hypothesis)较为成熟,不但具有CNBH的优点,而且更具有植物生理学和进化...     

IMPACT OF ENVIRONMENTAL CHANGES ON PRODUCTION OF BROWN ALGAL PHLOROTANNINS

Targett, N. M. Graduate College of Marine Studies, University of Delaware, Lewes, DE 19958 USA Ecological theories such as resource availability theory (e.g. carbon-nutrient balance hypothesis) and growth differentiation balance theory have attempted to provide a theoretical framework in which to balance putative improvements in plant fitness resulting from secondary metabolite production with the metabolic costs of these compounds. However, experimental tests of these theories have yielded mixed results, in part because they have relied upon static measures of phlorotannin concentrations and have incorrectly assumed phlorotannins to be immobile defenses with negligible rates of turnover. To test these theories more effectively, in situ rates of phlorotannin biosynthesis were examined in several species of brown algae as they responded to manipulations of their surrounding environmental conditions (light, nutrients, and simulated herbivory). The rates of phlorotannin synthesis measured for damaged Fucus vesiculosus from Maine (USA) were dramatically in-creased relative to controls. Carbon resources required for this response were supplied via wound-induced increases in photosynthetic rates, rather than changes in patterns of internal resource allocation. The lack of internal resource trade-offs indicates that phlorotannin production may not always generate allocation costs in these plants. Shading decreased the magnitude of the induced response but growth vs. defenses trade-offs were not identified. For Sargassum hystrix var. buxifolium from the Bahamas, rates of phlorotannin synthesis and total phenolic contents were decreased by both shading and nutrient enrichment. Overall, rates of phlorotannin synthesis were often, but not always, correlated with the eventual changes in total phlorotannin concentrations. Where synthesis and accumulations were uncoupled, differential rates of phlorotannin turnover are expected.     

Benefits and costs to pollinating,seed-eating insects: the effect of flower size and fruit abortion on larval performance

Plant–pollinator interactions are well-known examples of mutualism, but are not free of antagonism. Antagonistic interactions and defenses or counter-defenses are expected particularly in nursery pollination. In these systems, adult insects, while pollinating, lay their eggs in flowers, and juveniles consume the seeds from one or several fruits, thereby substantially reducing plant fitness. The outcome of such interactions will depend, for the plant, on the balance between pollination versus seed predation and for the larvae on the balance between the food and shelter provided versus the costs imposed by plant defenses, e.g., through abortion of infested fruits. Here, we examine the costs and benefits to the larvae in the nursery-pollination system Silene latifolia/Hadena bicruris. Using selection lines that varied in flower size (large- vs. small-flowered plants), we investigated the effects of variation in flower and fruit size and of a potential defense, fruit abortion, on larval performance. In this system, infested fruits are significantly more likely to be aborted than non-infested fruits; however, it is unclear whether fruit abortion is effective as a defense. Larger flowers gave rise to larger fruits with more seeds, and larvae that were heavier at emergence. Fruit abortion was frequently observed (ca. 40% of the infested fruits). From aborted fruits, larvae emerged earlier and were substantially lighter than larvae emerging from non-aborted fruits. The lower mass at emergence of larvae from aborted fruits indicates that abortion is a resistance mechanism. Assuming that lower larval mass implies fewer resources invested in the frugivore, these results also suggest that abortion is likely to benefit the plant as a defense mechanism, by limiting both resources invested in attacked fruits, as well as the risk of secondary attack. This suggests that selective fruit abortion may contribute to the stability of mutualism also in this non-obligate system.     

Can we use plant traits and soil characteristics to predict leaf damage in savanna woody species?

Although several hypotheses aim to explain insect herbivory on plants, the relative importance of plant traits, environment, and organizational scale (i.e., individual or community) to herbivory damage level is not well understood. We used an approach based on a local scale, divided into individual and community levels, to test if plant traits, soil characteristics, and plant density explain leaf damage. We sampled 983 individuals in 49 plots distributed over dense and open savanna formations in Emas National Park. In order to explain plant damage, we performed a multi-model inference analysis of four plant traits associated with plant damage, five soil characteristics, and plant density. We did not find any support to plant vigor or plant stress hypotheses at individual plant level. However, the resource concentration hypothesis and plant stress hypothesis explained leaf damage at the community level. We found that increased availability of calcium (Ca) in soils reduced plant damage at the community level. Because soil Ca concentration is a major constraint to plant development in the Brazilian savanna, we postulated that its increasing availability permits plants to invest more in defense strategies. We demonstrate that plant density, Ca soil concentration, and leaf size can be used to predict the plant damage suffered by woody species in savannas at community level.     

To grow and defend: lack of tradeoffs for brown algal phlorotannins

The concept of cost is an integral element of ecological theories, including optimal defense theory, resource availability theory, and growth-differentiation balance theory. Indeed most frameworks that attempt to explain within-plant patterns of secondary metabolites, as well as account for the evolution of induced defenses, presume that defenses are 'costly'. One way in which investigators have sought to quantify the cost of secondary metabolites is to examine growth/defense tradeoffs, which are predicted to occur wherever resources cannot be simultaneously allocated to both growth and defense. However, emerging evidence suggests that these critical assumptions may not be valid for brown algal phlorotannins, compounds that occur throughout the division Phaeophyta and have served as analogs to vascular plant tannins in numerous tests of terrestrial-derived ecological theories in the marine environment. Here we present a model of phlorotannins as metabolites with both primary and secondary roles and argue that apparent trade-offs between algal growth and phlorotannin content are not a reliable indicator for establishing a cost of defense. We suggest the ecological theories which presume that defenses are costly because resources allocated to defense cannot also be allocated to other 'primary' functions are unlikely to accurately predict the striking variations in algal phlorotannin concentrations that are observed in nature.     

Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs

Predictions based on the plant age and growth-differentiation balance hypotheses of defense were tested in two congeneric species, Plantago lanceolata and P. major, by quantifying iridoid glycosides, defensive chemicals, in seeds and leaves during the first 6 wk of growth. Concentrations decreased from the seed to 2-wk-old seedling stage in P. lanceolata, but increased during this period in P. major. In both species, levels were similar for 2- and 4-wk-old plants, then significantly increased from 4 to 6 wk. Genetic variation in the ontogeny of iridoid glycoside production was significant in both species at the maternal family level and at the population level. To examine whether allocation costs could explain the low production of iridoid glycosides in seedlings, relationships between growth and defense (iridoid glycosides) were characterized. Growth and defense had a positive or null relationship in all age groups, indicating that there was no trade-off in these plants at any age. This study provides some support for the growth-differentiation balance hypothesis, but offers no support for the plant age hypothesis. Measuring how herbivory affects plant fitness at different ontogenetic stages may shed light on these patterns in Plantago and on the evolution of the ontogeny of defense.     

The use of modelling and simulation approach in reconstructing past landscapes from fossil pollen data: a review and results from the POLLANDCAL network

Information on past land cover in terms of absolute areas of different landscape units (forest, open land, pasture land, cultivated land, etc.) at local to regional scales is needed to test hypotheses and answer questions related to climate change (e.g. feedbacks effects of land-cover change), archaeological research, and nature conservancy (e.g. management strategy). The palaeoecological technique best suited to achieve quantitative reconstruction of past vegetation is pollen analysis. A simulation approach developed by Sugita (the computer model POLLSCAPE) which uses models based on the theory of pollen analysis is presented together with examples of application. POLLSCAPE has been adopted as the central tool for POLLANDCAL (POLlen/LANdscape CALibration), an international research network focusing on this topic. The theory behind models of the pollen–vegetation relationship and POLLSCAPE is reviewed. The two model outputs which receive greatest attention in this paper are the relevant source area of pollen (RSAP) and pollen loading in mires and lakes. Six examples of application of POLLSCAPE are presented, each of which explores a possible use of the POLLANDCAL tools and a means of validating or evaluating the models with empirical data. The landscape and vegetation factors influencing the size of the RSAP, the importance of pollen productivity estimates (PPEs) for the model outputs, the detection of small and rare patches of plant taxa in pollen records, and quantitative reconstructions of past vegetation and landscapes are discussed on the basis of these examples. The simulation approach is seen to be useful both for exploring different vegetation/landscape scenarios and for refuting hypotheses.     

The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum

The evolution of endothermy in birds and mammals was one of the most important events in the evolution of the vertebrates. Past tests of hypotheses on the evolution of endothermy in mammals have relied largely on analyses of the relationship between basal and maximum metabolic rate, and artificial selection experiments. I argue that components of existing hypotheses, as well as new hypotheses, can be tested using an alternative macrophysiological modeling approach by examining the development of endothermy during the Cenozoic. Recent mammals display a 10°C range in body temperature which is sufficiently large to identify the selective forces that have driven the development of endothermy from a plesiomorphic (ancestral) Cretaceous or Jurassic condition. A model is presented (the Plesiomorphic‐Apomorphic Endothermy Model, PAE Model) which proposes that heterothermy, i.e. bouts of normothermy (constant body temperature) interspersed with adaptive heterothermy (e.g. daily torpor and/or hibernation), was the ancestral condition from which apomorphic (derived), rigid homeothermy evolved. All terrestrial mammal lineages are examined for existing data to test the model, as well as for missing data that could be used to test the model. With the exception of Scandentia and Dermoptera, about which little is known, all mammalian orders that include small‐sized mammals (<500 g), have species which are heterothermic and display characteristics of endothermy which fall somewhere along a plesiomorphic‐apomorphic continuum. Orders which do not have heterothermic representatives (Cetartiodactyla, Perissodactyla, Pholidota, and Lagomorpha) are comprised of medium‐ to large‐sized mammals that have either lost the capacity for heterothermy, or in which heterothermy has yet to be measured. Mammalian heterothermy seems to be plesiomorphic and probably evolved once in the mammalian lineage. Several categories of endothermy are identified (protoendothermy, plesioendothermy, apoendothermy, basoendothermy, mesoendothermy, supraendothermy, and reversed mesoendothermy) to describe the evolution of endothermy during the Cenozoic. The PAE Model should facilitate the testing of hypotheses using a range of macrophysiological methods (e.g. the comparative method and the reconstruction of ancestral states).     

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?

Severe droughts have been associated with regional-scale forest mortality worldwide. Climate change is expected to exacerbate regional mortality events; however, prediction remains difficult because the physiological mechanisms underlying drought survival and mortality are poorly understood. We developed a hydraulically based theory considering carbon balance and insect resistance that allowed development and examination of hypotheses regarding survival and mortality. Multiple mechanisms may cause mortality during drought. A common mechanism for plants with isohydric regulation of water status results from avoidance of drought-induced hydraulic failure via stomatal closure, resulting in carbon starvation and a cascade of downstream effects such as reduced resistance to biotic agents. Mortality by hydraulic failure per se may occur for isohydric seedlings or trees near their maximum height. Although anisohydric plants are relatively drought-tolerant, they are predisposed to hydraulic failure because they operate with narrower hydraulic safety margins during drought. Elevated temperatures should exacerbate carbon starvation and hydraulic failure. Biotic agents may amplify and be amplified by drought-induced plant stress. Wet multidecadal climate oscillations may increase plant susceptibility to drought-induced mortality by stimulating shifts in hydraulic architecture, effectively predisposing plants to water stress. Climate warming and increased frequency of extreme events will probably cause increased regional mortality episodes. Isohydric and anisohydric water potential regulation may partition species between survival and mortality, and, as such, incorporating this hydraulic framework may be effective for modeling plant survival and mortality under future climate conditions.     

Diversity of plant–animal interactions: Possibilities for a new plant defense indicator value?

The interactions between herbivores and plants are of general interest in ecology. Even though the extensive research carried out during the last decades has culminated in many theories, additional studies are necessary to validate these findings. In particular, the hypotheses dealing with the complex interrelations of plant defense mechanisms and herbivores continue to be debated.In this paper, we develop a new indicator value that quantifies the defense mechanisms of Central European woody plants against large mammalian herbivores. The indicator value is based on three plant-specific traits: chemical defense (toxic compounds, digestion inhibitors), mechanical defense and leaf size. Our validation of the newly established indicator shows that evergreen woody plants have a significantly higher indicator value than deciduous woody plants. Moreover, plant defense is correlated with growth height: woody plants growing in the browsing zone preferred by large mammalian herbivores have significantly higher levels of defense compared with woody plants capable of growth high above the reach of large herbivores.We conclude that the new plant defense indicator value is a valuable tool for the validation of existing hypotheses and habitat calibration on a statistical basis. The quantification of plant mechanisms of defense against large herbivores produces a significantly better understanding of the multifaceted nature of plant–animal interactions and should contribute positively to future studies.     

The territorial defense hypothesis and the ecology of insular vertebrates

Insular lizards, birds, and mammals in high-density populations often exhibit reduced situation-specific aggression toward conspecifics. This aggressive behavior can be expressed in the form of (1) reduced territory sizes, (2) increased territory overlap with neighbors, (3) acceptance of subordinates on the territory, (4) reduced aggressiveness to certain classes of conspecifics, or (5) abandonment of territorial defense. These behavioral traits can be explained by two nonexclusive hypotheses. The resource hypothesis suggests that territorial behavior is primarily adjusted to resource densities, and that resources are more abundant on islands than on the mainland (e.g., because of a lack of competing species). The defense hypothesis suggests that, in addition to any effects of resources, the costs of defense against both territorial intruders and contenders for vacant territories are higher on islands. Recent theoretical and empirical studies indicate that these behavioral changes can occur as a result of elevated defense costs, independent of resource densities. Reduced predation, more benign climates, and an absence of habitat sinks on islands would all tend to increase the density of potential intruders and contenders, and hence the costs of defense for owners of insular territories. The two hypotheses differ in their predictions about the rates of biomass production (growth or reproduction) for holders of insular territories. Reproductive and growth data from insular-mainland pairs indicate the importance of elevated defense costs, and also suggest that many insular vertebrates reallocate their breeding resources so as to produce young that are more competitive. The suite of ecological and behavioral traits exhibited by insular territorial vertebrates can best be explained by three factors operating in concert: higher available resource densities, higher defense costs, and (sometimes) a reallocation of resources to produce young that are more competitive.     

Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation

A tremendous diversity of plants exude sticky and toxic latex upon tissue damage, and its production has been widely studied as a defensive adaptation against insect herbivores. Here, we address variation in latex production and its constituent chemical properties (cardenolides and cysteine proteases) in 53 milkweeds [Asclepias spp. (Apocynaceae)], employing a phylogenetic approach to test macroevolutionary hypotheses of defense evolution. Species were highly variable for all three traits, and they showed little evidence for strong phylogenetic conservatism. Latex production and the constituent chemical defenses are thus evolutionarily labile and may evolve rapidly. Nonetheless, in phylogenetically independent analyses, we show that the three traits show some correlations (and thus share a correlated evolutionary history), including a positive correlation between latex exudation and cysteine protease activity. Conversely, latex exudation and cysteine protease activity both showed a trade‐off with cardenolide concentrations in latex. We also tested whether these traits have increased in their phenotypic values as the milkweeds diversified, as predicted by plant defense escalation theory. Alternative methods of testing this prediction gave conflicting results – there was an overall negative correlation between amount of evolutionary change and amount of latex exudation; however, ancestral state reconstructions indicated that most speciation events were associated with increases in latex. We conclude by (i) summarizing the evidence of milkweed latex itself as a multivariate defense including the amount exuded and toxin concentrations within, (ii) assessing the coordinated evolution of latex traits and how this fits with our previous notion of ‘plant defense syndromes’, and finally, (iii) proposing a novel hypothesis that includes an ‘evolving community of herbivores’ that may promote the escalation or decline of particular defensive strategies as plant lineages diversify.     

Convective-diffusive model of two-dimensional root growth and proliferation

Simulations of crop productivity and environmental quality depend strongly on the root activity model used. Flexible, generic root system models are needed that can easily be coupled to various process-based soil models and can easily be modified to test various hypotheses about how roots respond to their environment. In this paper, we develop a convective-diffusive model of root growth and proliferation, and use it to test some of these hypotheses with data on the growth of roots on potted chrysanthemum cuttings. The proliferation of roots is viewed as a result of a diffusion-like gradient-driven propagation in all directions and convection-like propagation downwards caused by geotropism. The finite element method was used to solve the boundary problem for the convective-diffusive equation. To test hypotheses, we wrote modules in a way that caused a test parameter to be zero, should the hypothesis be rejected. These modules were added or removed to test each hypothesis in turn and in various combinations. The model explained 92% of the variation in the experimental data of Chen and Lieth (1993) on root growth of potted chrysanthemum cuttings. For this dataset the following hypotheses were accepted: (1) root diffusivity (colonization of new soil) did not depend on root density, (2) there was no geotropic trend in root development, (3) potential root growth increased linearly with root density, (4) there were (at least) two classes of roots with different rates of growth and proliferation, and (5) potential root growth rate decreased with distance from the plant stem base.