Kasey E. Barton

The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis.

Defense against herbivores often changes dramatically as plants develop. Hypotheses based on allocation theory and herbivore selection patterns predict that defense should increase or decrease, respectively, across ontogeny, and previous research partly supports both predictions. Thus, it remains unclear which pattern is more common and what factors contribute to variability among studies. We conducted a meta‐analysis of 116 published studies reporting ontogenetic patterns in plant defense traits and herbivory. Patterns varied depending on plant life form (woody, herbaceous, grass), type of herbivore (insect, mollusk, mammal), and type of defense trait (secondary chemistry, physical defense, tolerance). In woody plants, chemical defense increased during the seedling stage, followed by an increase in physical defenses during the vegetative juvenile stage. Mammalian herbivores showed a strong preference for mature compared to juvenile tissues in woody plants. Herbs experienced a significant increase in secondary chemistry across the entire ontogenetic trajectory, although the magnitude of increase was greatest during the seedling stage. Correspondingly, mollusks preferred young compared to older herbs. Future research investigating growth/defense trade‐offs, allometry, herbivore selection patterns, and ecological costs would shed light on the mechanisms driving the ontogenetic patterns observed.

Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses

We examined variation in leaf size and specific leaf area (SLA) in relation to the distribution of 22 chaparral shrub species on small-scale gradients of aspect and elevation. Potential incident solar radiation (insolation) was estimated from a geographic information system to quantify microclimate affinities of these species across north- and south-facing slopes. At the community level, leaf size and SLA both declined with increasing insolation, based on average trait values for the species found in plots along the gradient. However, leaf size and SLA were not significantly correlated across species, suggesting that these two traits are decoupled and associated with different aspects of performance along this environmental gradient. For individual species, SLA was negatively correlated with species distributions along the insolation gradient, and was significantly lower in evergreen versus deciduous species. Leaf size exhibited a negative but non-significant trend in relation to insolation distribution of individual species. At the community level, variance in leaf size increased with increasing insolation. For individual species, there was a greater range of leaf size on south-facing slopes, while there was an absence of small-leaved species on north-facing slopes. These results demonstrate that analyses of plant functional traits along environmental gradients based on community level averages may obscure important aspects of trait variation and distribution among the constituent species.

Seedling-herbivore interactions: insights into plant defence and regeneration patterns.

BACKGROUND Herbivores have the power to shape plant evolutionary trajectories, influence the structure and function of vegetation, devastate entire crops, or halt the spread of invasive weeds, and as a consequence, research into plant-herbivore interactions is pivotal to our understanding of plant ecology and evolution. However, the causes and consequences of seedling herbivory have received remarkably little attention, despite the fact that plants tend to be most susceptible to herbivory during establishment, and this damage can alter community composition and structure. SCOPE In this Viewpoint article we review why herbivory during early plant ontogeny is important and in so doing introduce an Annals of Botany Special Issue that draws together the latest work on the topic. In a synthesis of the existing literature and a collection of new studies, we examine several linked issues. These include the development and expression of seedling defences and patterns of selection by herbivores, and how seedling selection affects plant establishment and community structure. We then examine how disruption of the seedling-herbivore interaction might affect normal patterns of plant community establishment and discuss how an understanding of patterns of seedling herbivory can aid our attempts to restore semi-natural vegetation. We finish by outlining a number of areas where more research is required. These include a need for a deeper consideration of how endogenous and exogenous factors determine investment in seedling defence, particularly for the very youngest plants, and a better understanding of the phylogenetic and biogeographical patterns of seedling defence. There is also much still be to be done on the mechanisms of seedling selection by herbivores, particularly with respect to the possible involvement of volatile cues. These inter-related issues together inform our understanding of how seedling herbivory affects plant regeneration at a time when anthropogenic change is likely to disrupt this long-established, but all-too-often ignored interaction.

Ontogenetic patterns in the mechanisms of tolerance to herbivory in Plantago.

BACKGROUND AND AIMS Herbivory and plant defence differ markedly among seedlings and juvenile and mature plants in most species. While ontogenetic patterns of chemical resistance have been the focus of much research, comparatively little is known about how tolerance to damage changes across ontogeny. Due to dramatic shifts in plant size, resource acquisition, stored reserves and growth, it was predicted that tolerance and related underlying mechanisms would differ among ontogenetic stages. METHODS Ontogenetic patterns in the mechanisms of tolerance were investigated in Plantago lanceolata and P. major (Plantaginaceae) using the genetic sib-ship approach. Pot-grown plants were subjected to 50 % defoliation at the seedling, juvenile and mature stages and either harvested in the short-term to look at plasticity in growth and photosynthesis in response to damage or allowed to grow through seed maturation to measure phenology, shoot compensation and reproductive fitness. KEY RESULTS Tolerance to defoliation was high in P. lanceolata, but low in P. major, and did not vary among ontogenetic stages in either species. Mechanisms underlying tolerance did vary across ontogeny. In P. lanceolata, tolerance was significantly related to flowering (juveniles) and pre-damage shoot biomass (mature plants). In P. major, tolerance was significantly related to pre-damage root biomass (seedlings) and induction of non-photochemical quenching, a photosynthetic parameter (juveniles). CONCLUSIONS Biomass partitioning was very plastic in response to damage and showed associations with tolerance in both species, indicating a strong role in plant defence. In contrast, photosynthesis and phenology showed weaker responses to damage and were related to tolerance only in certain ontogenetic stages. This study highlights the pivotal role of ontogeny in plant defence and herbivory. Additional studies in more species are needed to determine how seedlings tolerate herbivory in general and whether mechanisms vary across ontogeny in consistent patterns.

Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences

Plant defence often varies by orders of magnitude as plants develop from the seedling to juvenile to mature and senescent stages. Ontogenetic trajectories can involve switches among defence traits, leading to complex shifting phenotypes across plant lifetimes. While considerable research has characterised ontogenetic trajectories for now hundreds of plant species, we still lack a clear understanding of the molecular, ecological and evolutionary factors driving these patterns. In this study, we identify several non-mutually exclusive factors that may have led to the evolution of ontogenetic trajectories in plant defence, including developmental constraints, resource allocation costs, multi-functionality of defence traits, and herbivore selection pressure. Evidence from recent physiological studies is highlighted to shed light on the underlying molecular mechanisms involved in the regulation and activation of these developmental changes. Overall, our goal is to promote new research avenues that would provide evidence for the factors that have promoted the evolution of this complex lifetime phenotype. Future research focusing on the questions and approaches identified here will advance the field and shed light on why defence traits shift so dramatically across plant ontogeny, a widespread but poorly understood ecological pattern.

The Ecology of Plant Secondary Metabolites: Temporal changes in plant secondary metabolite production

Introduction Both overall concentrations and composition of plant secondary metabolites (PSMs) may vary strongly not only among different plant species or different plant individuals within a species, but also within a single individual plant over time. We distinguish two types of temporal changes in plants: ontogenetic and seasonal . Ontogeny refers to genetically programmed developmental changes that take place during a plant’s life; the terms ‘maturation’ and ‘phase change’ are also sometimes used to describe the same process (Kozlowski, 1971; Poethig, 1990). Commonly recognised ontogenetic stages in plants include seedlings, juvenile plants (saplings) and mature plants. Each stage is characterised by distinctive anatomical, morphological and biochemical features (e.g. dependence on seed reserves in seedlings, and ability to flower and set seeds in mature plants). Since plants are modular organisms composed of numerous semi-autonomous units (e.g. branches and leaves), in addition to ontogenetic changes at the whole-plant level, each plant module/organ also experiences ontogenetic changes as it develops and matures. For instance, leaves formed during a specific phase of shoot growth retain morphological and physiological features characteristic of that phase, resulting in variation in the character of structures along the axis of the shoot; this phenomenon is known as heteroblasty (Poethig, 1990; O’Reilly-Wapstra et al ., Chapter 2). While these within-module ontogenetic changes are genetically programmed just as whole-plant ontogenetic changes are, they are not necessarily synchronised with the latter because new modules are produced continuously through the plant’s lifetime. As a result, long-lived plants like trees may represent a complex mosaic or a gradient of plant tissues at different ontogenetic phases of development (sometimes referred to as a ‘developmental stream’) (Kearsley & Whitham, 1998). In addition to ontogenetic changes, in seasonal environments, plant modules experience a series of physiological changes over the season caused by changes in temperature and the availability of light (photoperiod), water and nutrients. We refer to these changes as seasonal changes. In annual and short-lived herbaceous plants, seasonal and ontogenetic changes are confounded, but in long-lived woody plants like trees they can be distinguished because both juvenile and mature ontogenetic stages last many seasons, and within-plant ontogenetic changes such as leaf expansion usually occur within a relatively short time interval during the season (e.g. a few weeks in spring in temperate ecosystems). Both ontogenetic and seasonal changes may affect PSM production in plants.

Prickly poppies can get pricklier: ontogenetic patterns in the induction of physical defense traits.

Plant ontogeny is a common source of variation in defense and herbivory. Yet, few studies have investigated how the induction of physical defense traits changes across plant ontogeny. Physical defense traits are costly to produce, and thus, it was predicted that induction as a cost-saving strategy would be particularly favorable for seedlings, leading to ontogenetic declines in the inducibility of these traits. We tested for induction of three different physical defense traits (prickles, latex and leaf toughness) in response to mechanical defoliation and jasmonic acid application using prickly poppies (Argemone glauca and A. mexicana, Papaveraceae) as a model system. Genetic variation in the induction of physical defenses was tested using maternal sib-ships sampled from multiple populations. Both species induced higher densities of laminar prickles, although the magnitude of induction was much higher in the endemic Hawaiian prickly poppy, A. glauca, than in the cosmopolitan A. mexicana. The magnitude of prickle induction was also higher in young compared to older juvenile plant stages in A. glauca, demonstrating a strong role of ontogeny. Neither latex exudation nor leaf toughness was induced in either species. Although significant genetic variation was detected within and among populations for constitutive expression of physical defense traits in Argemone, there was no evidence for genetic variation in the induction of these traits. This study provides the first evidence for the induction of physical defenses in prickly poppies, emphasizing how an ontogenetically explicit framework can reveal new insights into plant defense. Moreover, this study illustrates how sister species comparisons between island vs. continental plants can provide new insights into plant functional and evolutionary ecology, highlighting a fruitful area for future research on more species pairs.

The Effects of Proximity and Colony Age on Interspecific Interference Competition between the Desert Ants Pogonomyrmex barbatus and Aphaenogaster cockerelli

Abstract The ants Aphaenogaster cockerelli and Pogonomyrmex barbatus compete for seed resources in the Chihuahuan desert. Previous work showed that intraspecific competition in P. barbatus is more intense between near neighbors with overlapping foraging ranges and depends on colony age. Just before reaching reproductive maturity (3–4 y), colonies are more aggressive and persistent in intraspecific competition for foraging area than younger or older colonies. In this study we examine how interspecific interference behavior by A. cockerelli towards P. barbatus depends on the age and proximity of P. barbatus colonies. Before sunrise when P. barbatus colonies become active, A. cockerelli colonies completely plug the nest entrances of some P. barbatus colonies, thereby delaying the onset of P. barbatus foraging behavior. Pogonomyrmex barbatus colonies closer to A. cockerelli were plugged more frequently than more distant colonies. As distance from A. cockerelli nests increased, older P. barbatus colonies were plugged more frequently than younger ones. Our results suggest that the intensity of interspecific interference competitive interactions may depend on the proximity and age of competing colonies.

Risk of herbivore attack and heritability of ontogenetic trajectories in plant defense

Ontogeny has been identified as a main source of variation in the expression of plant phenotypes. However, there is limited information on the mechanisms behind the evolution of ontogenetic trajectories in plant defense. We explored if risk of attack, herbivore damage, heritability, and phenotypic plasticity can promote or constrain the evolutionary potential of ontogenetic trajectories in three defensive traits. We exposed 20 genotypes of Turnera velutina to contrasting environments (shadehouse and field plots), and measured the cyanogenic potential, trichome density, and sugar content in extrafloral nectar in seedlings, juveniles and reproductive plants. We also assessed risk of attack through oviposition preferences, and quantified herbivore damage in the field. We estimated genetic variance, broad sense heritability, and evolvability of the defensive traits at each ontogenetic stage, and of the ontogenetic trajectories themselves. For plants growing in the shadehouse, we found genetic variation and broad sense heritability for cyanogenic potential in seedlings, and for trichome density at all ontogenetic stages. Genetic variation and heritability of ontogenetic trajectories was detected for trichome density only. These genetic pre-requisites for evolution, however, were not detected in the field, suggesting that environmental variation and phenotypic plastic responses mask any heritable variation. Finally, ontogenetic trajectories were found to be plastic, differing between shadehouse and field conditions for the same genetic families. Overall, we provide support for the idea that changes in herbivore pressure can be a mechanism behind the evolution of ontogenetic trajectories. This evolutionary potential, however, can be constrained by phenotypic plasticity expressed in heterogeneous environments.

Pre‐damage biomass allocation and not invasiveness predicts tolerance to damage in seedlings of woody species in Hawaii

Plant-herbivore interactions have been predicted to play a fundamental role in plant invasions, although support for this assertion from previous research is mixed. While plants may escape from specialist herbivores in their introduced ranges, herbivory from generalists is common. Tolerance traits may allow non-native plants to mitigate the negative consequences of generalist herbivory that they cannot avoid in their introduced range. Here we address whether tolerance to herbivory, quantified as survival and compensatory growth, is associated with plant invasion success in Hawaii and investigate traits that may enhance tolerance in seedlings, the life stage most susceptible to herbivory. In a greenhouse experiment, we measured seedling tolerance to simulated herbivory through mechanical damage (50% leaf removal) of 16 non-native woody plant species differing in invasion status (invasive vs. non-invasive). Seedlings were grown for 2 weeks following damage and analyzed for biomass to determine whether damaged plants could fully compensate for the lost leaf tissue. Over 99% of all seedlings survived defoliation. Although species varied significantly in their levels of compensation, there was no consistent difference between invasive and non-invasive species. Seedlings of 11 species undercompensated and remained substantially smaller than control seedlings 2 weeks after damage; four species were close to compensating, while one species overcompensated. Across species, compensation was positively associated with an increased investment in potential storage reserves, specifically cotyledons and roots, suggesting that these organs provide resources that help seedlings re-grow following damage. Our results add to a growing consensus that pre-damage growth patterns determine tolerance to damage, even in young seedlings which have relatively low biomass. The lack of higher tolerance in highly invasive species may suggest that invaders overcome herbivory barriers to invasion in other ways, such as resistance traits, or that herbivory does not play an important role in the seedling invasion dynamics of these woody species in Hawaii.