Investment into Defensive Traits by Anuran Prey (Lithobates pipiens) Is Mediated by the Starvation-Predation Risk Trade-Off

Prey can invest in a variety of defensive traits when balancing risk of predation against that of starvation. What remains unknown is the relative costs of different defensive traits and how prey reconcile investment into these traits when energetically limited. We tested the simple allocation model of prey defense, which predicts an additive effect of increasing predation risk and resource availability, resulting in the full deployment of defensive traits under conditions of high risk and resource saturation. We collected morphometric, developmental, and behavioural data in an experiment using dragonfly larvae (predator) and Northern leopard frog tadpoles (prey) subject to variable levels of food availability and predation risk. Larvae exposed to food restriction showed limited response to predation risk; larvae at food saturation altered behaviour, development, and growth in response to predation risk. Responses to risk varied through time, suggesting ontogeny may affect the deployment of particular defensive traits. The observed negative correlation between body size and activity level for food-restricted prey – and the absence of a similar response among adequately-fed prey – suggests that a trade-off exists between behavioural and growth responses when energy budgets are limited. Our research is the first to demonstrate how investment into these defensive traits is mediated along gradients of both predation risk and resource availability over time. The interactions we demonstrate between resource availability and risk level on deployment of inducible defenses provide evidence that both internal condition and extrinsic risk factors play a critical role in the production of inducible defenses over time.     

Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all?

On the basis of physiological and ecological costs of defense allocation, most plant defense theories predict the occurrence of trade-offs between resource investment in different types of antiherbivore defenses. To test this prediction, we conducted a meta-analysis of 31 studies published in 1976-2002 that provided data on covariation of different defensive traits in plant genotypes. We found no overall negative association between different defensive traits in plants; instead, the relationship between defensive traits varied from positive to negative depending on the types of co-occurring defenses. Evidence of trade-off was found only between constitutive and induced defenses. Therefore, to a large extent, plants appear to be jacks-of-all-trades, masters of all and may successfully produce several types of defense without paying considerable trade-offs. Our survey thus provides little evidence that genetic trade-offs between defensive traits significantly constrain the evolution of multiple defenses in plants.     

COSTS OF INDUCED RESPONSES AND TOLERANCE TO HERBIVORY IN MALE AND FEMALE FITNESS COMPONENTS OF WILD RADISH

Theory predicts that plant defensive traits are costly due to trade-offs between allocation to defense and growth and reproduction. Most previous studies of costs of plant defense focused on female fitness costs of constitutively expressed defenses. Consideration of alternative plant strategies, such as induced defenses and tolerance to herbivory, and multiple types of costs, including allocation to male reproductive function, may increase our ability to detect costs of plant defense against herbivores. In this study we measured male and female reproductive costs associated with induced responses and tolerance to herbivory in annual wild radish plants (Raphanus raphanistrum). We induced resistance in the plants by subjecting them to herbivory by Pieris rapae caterpillars. We also induced resistance in plants without leaf tissue removal using a natural chemical elicitor, jasmonic acid; in addition, we removed leaf tissue without inducing plant responses using manual clipping. Induced responses included increased concentrations of indole glucosinolates, which are putative defense compounds. Induced responses, in the absence of leaf tissue removal, reduced plant fitness when five fitness components were considered together; costs of induction were individually detected for time to first flower and number of pollen grains produced per flower. In this system, induced responses appear to impose a cost, although this cost may not have been detected had we only quantified the traditionally measured fitness components, growth and seed production. In the absence of induced responses, 50% leaf tissue removal, reduced plant fitness in three out of the five fitness components measured. Induced responses to herbivory and leaf tissue removal had additive effects on plant fitness. Although plant sibships varied greatly (49–136%) in their level of tolerance to herbivory, costs of tolerance were not detected, as we did not find a negative association between the ability to compensate for damage and plant fitness in the absence of damage. We suggest that consideration of alternative plant defense strategies and multiple costs will result in a broader understanding of the evolutionary ecology of plant defense.     

Optimizing time and resource allocation trade-offs for investment into morphological and behavioral defense

Prey organisms are confronted with time and resource allocation trade-offs. Time allocation trade-offs partition time, for example, between foraging effort to acquire resources and behavioral defense. Resource allocation trade-offs partition the acquired resources between multiple traits, such as growth or morphological defense. We develop a mathematical model for prey organisms that comprise time and resource allocation trade-offs for multiple defense traits. Fitness is determined by growth and survival during ontogeny. We determine optimal defense strategies for environments that differ in their resource abundance, predation risk, and defense effectiveness. We compare the results with results of simplified models where single defense traits are optimized. Our results indicate that selection acts in favor of integrated traits. The selective advantage of expressing multiple defense traits is most pronounced at intermediate environmental conditions. Optimizing single traits generally leads to a more pronounced response of the defense traits, which implies that studying single traits leads to an overestimation of their response to predation. Behavioral defense and morphological defense compensate for and augment each other depending on predator densities and the effectiveness of the defense mechanisms. In the presence of time constraints, the model shows peak investment into morphological and behavioral defense at intermediate resource levels.     

Are there interactive effects of mate availability and predation risk on life history and defence in a simultaneous hermaphrodite?

Encountering mates and avoiding predators are ubiquitous challenges faced by many organisms and they can affect the expression of many traits including growth, timing of maturity and resource allocation to reproduction. However, these two factors are commonly considered in isolation rather than simultaneously. We examined whether predation risk and mate availability interact to affect morphology and life-history traits (including lifetime fecundity) of a hermaphroditic snail (Physa acuta). We found that mate availability reduced juvenile growth rate and final size. Predator cues from crayfish induced delayed reproduction, but there were no reduced fecundity costs associated with predator induction. Although there were interactive effects on longevity, lifetime fecundity was determined by the number of reproductive days. Therefore, our results indicate a resource-allocation trade-off among growth, longevity and reproduction. Future consideration of this interaction will be important for understanding how resource-allocation plasticity affects the integration of defensive, life-history and mating-system traits.     

Predator-induced defense makes Daphnia more vulnerable to parasites

Inducible defensive traits against herbivores or predators are widespread in plants and animals. Theory predicts that defended morphs have greater fitness in the presence of predators, but lower fitness than undefended morphs in the absence of predators. If such costs did not exist, then a constitutively defended morph would be favored by natural selection; yet, evidence for such costs has been elusive. Our current work reveals a significant cost to inducible defenses. Using the waterflea (Daphnia) model system, we show that induced defended morphs are significantly more vulnerable to infection by a virulent yeast parasite than undefended morphs. In two independent experiments, the proportion of successful infections and the number of parasite spores were higher among defended versus undefended Daphnia. Thus, by demonstrating a previously unknown and environmentally relevant cost to inducible defenses, this study enhances our understanding of adaptive phenotypic plasticity and its evolution.     

Tradeoff between physical and chemical defense in plant seeds is mediated by seed mass

Plants have evolved both physical and chemical defenses to make the nutrients of attacked organs difficult to access or more toxic to resist animal consumption or/and pathogen attack. Although it is intuitive that a tradeoff could exist between physical and chemical defenses because of finite defense resources, many studies have failed to detect this tradeoff. We hypothesized that tradeoff between physical and chemical defenses in individual organs was mediated by the total resource allocation to those organs. In this study, we tested whether a tradeoff between physical (i.e. fiber content, which has proved to be a good indicator of investment into seed coat) and chemical defenses (i.e. total phenolics, which are abundant chemical defenses in plant seeds) existed in plant seeds by using 163 common species collected from Xishuangbanna tropical forest, southwest China. Then we tested whether this tradeoff was mediated by seed mass which could be a potential proxy of total resource investment per seed. Among the 163 species, there was large interspecific variation in both total phenolics (from 0.01 to 20.52%) and fiber content (from 4.47 to 81.49%). Our results supported our hypothesis: negative relationships between physical and chemical defenses were much stronger among small seeds than among large seeds. Our study suggests that total resource acquisition must be considered when evaluating defense tradeoffs. However, it is usually extremely difficult to measure this resource acquisition variation, thus we suggest utilizing easily measured proxies of acquisition variation to quantify tradeoffs.     

Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on <Emphasis Type="Italic">Datura wrightii</Emphasis>

The costs and benefits of defensive traits in plants can have an ecological component that arises from the effect of defenses on the natural enemies of herbivores. We tested if glandular trichomes in Datura wrightii, a trait that confers resistance to several species of herbivorous insects, impose an ecological cost by decreasing rates of predation by the natural enemies of herbivores. For two common herbivores of D. wrightii, Lema daturaphila and Tupiocoris notatus, several generalized species of natural enemies exhibited lower rates of predation on glandular compared to non-glandular plants. Lower rates of predation were associated with reductions in the residence time and foraging efficiency of natural enemies on plants with glandular trichomes, but not with direct toxic effects of glandular exudate. Our results suggest that the benefit of resistance to herbivores conferred by glandular trichomes might be offset by the detrimental effect of this trait on the natural enemies of herbivores, and that the fitness consequences of this trichome defense might depend on the composition and abundance of the natural-enemy community.     

Optimal defense in plants: assessment of resource allocation costs

Genetic and environmental variation of functional traits within populations might be maintained by natural selection when resource allocation costs (RACs) balance trait benefits. Despite the intuitive appeal of optimization models, empirical tests have failed to support the importance of RACs for plant traits that confer resistance against pests. To address this discrepancy, we modified an early model by allowing the cost function to vary across a resource gradient as predicted for RACs and by assuming that the benefits depend on variation in the pest population for susceptibility. Instead of the intermediate defense optimum of the original model, defenses were predicted to be either high or absent, depending on resource availability and history. This result is not supported by empirical tests for ecological or evolutionary outcomes, including our own examination of glucosinolate toxins from sib-families of Boechera stricta (Brassicaceae) grown across an NPK fertilizer gradient. Although we detected an apparent cost of defense in the absence of herbivores, the cost did not increase as resources became more limiting. Also defense production did not vary across the resource gradient as predicted by the modified model. Thus, a model based on explicit expectations of RACs produced predictions that are not supported. Instead, other kinds of costs, such as ecological (indirect) costs may be more important. Alternatively, general conflicts in gene expression and antagonistic crosstalk among signaling pathways may underlie apparent costs.     

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.     

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.     

Difference in defense strategy in flower heads and leaves of Asteraceae: multiple-species approach

Although a vast number of studies have investigated defenses against herbivores in leaves, relatively little is known about defenses in flowers. Using wild individuals of 34 species of Asteraceae, we investigated differences in five traits that are thought to affect the intensity of herbivory (C, N, P, water, and total phenolic contents). Combinations of these traits between flower heads and leaves were studied as well. We also evaluated phylogenetic patterns of flower head and leaf traits. Flower heads had higher P and lower total phenolics than leaves. Water and C contents were negatively correlated both in the flower heads and leaves. N, P, and water contents were positively correlated in the flower heads, whereas this pattern was not found in the leaves. Thus, the traits we measured were more tightly inter-correlated in flower heads than in leaves. Because the flower heads had a lower total phenolic content, the relative allocation of defensive compounds could not be explained solely by fitness values of the organs. Perhaps plants employ an escape strategy rather than a defense strategy to cope with floral herbivores and higher allocation in P may enhance their escape from herbivores by improving the growth rate of flower heads, though our result might be affected in part by the plasticity of plants growing at different sites. Moreover, we found weak phylogenetic signals in the defensive traits. Because we found significant differences in the flower head traits, these weak signals may imply that the traits we measured evolved frequently.     

Interactive effects of habitat productivity and herbivore pressure on the evolution of anti-herbivore defense in invasive plant populations

The evolution of increased competitive ability (EICA) hypothesis predicts that plants released from natural enemies should evolve to become more invasive through a shift in resource allocation from defense to growth. Resource availability in the environment is widely regarded as a major determinant of defense investment and invasiveness, and thus should be incorporated into the conceptual framework of EICA. Analysis of a simple model from the optimal defense literature demonstrates that, in contrast to the EICA hypothesis, enemy release is neither sufficient nor necessary for evolution of reduced resistance among introduced plants when habitat productivity co-varies. In particular, if the invasive range is more nutrient-poor than the native range, there could be selection for more plant defenses even with enemy release.     

Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity

Abstract.— Adaptive phenotypic plasticity in chemical defense is thought to play a major role in plant-herbivore interactions. We investigated genetic variation for inducibility of defensive traits in wild radish plants and asked if the evolution of induction is constrained by costs of phenotypic plasticity. In a greenhouse experiment using paternal half-sibling families, we show additive genetic variation for plasticity in glucosinolate concentration. Genetic variation for glucosinolates was not detected in undamaged plants, but was significant following herbivory by a specialist herbivore, Pieris rapae . On average, damaged plants had 55% higher concentrations of glucosinolates compared to controls. In addition, we found significant narrow-sense heritabilities for leaf size, trichome number, flowering phenology, and lifetime fruit production. In a second experiment, we found evidence of genetic variation in induced plant resistance to P. rapae . Although overall there was little evidence for genetic correlations between the defensive and life-history traits we measured, we show that more plastic families had lower fitness than less plastic families in the absence of herbivory (i.e., evidence for genetic costs of plasticity). Thus, there is genetic variation for induction of defense in wild radish, and the evolution of inducibility may be constrained by costs of plasticity.     

Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis

Recent studies of allocation to defensive chemicals in plants have provided insights into the ecological controls over plant defensive chemicals. Both developmental and ecological studies now suggest that we can understand the factors influencing allocation to defense by examining the relative availability of resources, external needs for chemical defense, and the internal demands for growth that plants face. These studies have also shed light on one of the more popular theories in plant evolutionary ecology, the growth-differentiation balance hypothesis of plant resource allocation.     

Chemical defense of toad tadpoles under risk by four predator species

Many organisms use inducible defenses as protection against predators. In animals, inducible defenses may manifest as changes in behavior, morphology, physiology, or life history, and prey species can adjust their defensive responses based on the dangerousness of predators. Analogously, prey may also change the composition and quantity of defensive chemicals when they coexist with different predators, but such predator‐induced plasticity in chemical defenses remains elusive in vertebrates. In this study, we investigated whether tadpoles of the common toad (Bufo bufo) adjust their chemical defenses to predation risk in general and specifically to the presence of different predator species; furthermore, we assessed the adaptive value of the induced defense. We reared tadpoles in the presence or absence of one of four caged predator species in a mesocosm experiment, analyzed the composition and quantity of their bufadienolide toxins, and exposed them to free‐ranging predators. We found that toad tadpoles did not respond to predation risk by upregulating their bufadienolide synthesis. Fishes and newts consumed only a small percentage of toad tadpoles, suggesting that bufadienolides provided protection against vertebrate predators, irrespective of the rearing environment. Backswimmers consumed toad tadpoles regardless of treatment. Dragonfly larvae were the most voracious predators and consumed more predator‐naïve toad tadpoles than tadpoles raised in the presence of dragonfly cues. These results suggest that tadpoles in our experiment had high enough toxin levels for an effective defense against vertebrate predators even in the absence of predator cues. The lack of predator‐induced phenotypic plasticity in bufadienolide synthesis may be due to local adaptation for constantly high chemical defense against fishes in the study population and/or due to the high density of conspecifics.     

Combined threats of climate change and contaminant exposure through the lens of bioenergetics

Organisms face energetic challenges of climate change in combination with suites of natural and anthropogenic stressors. In particular, chemical contaminant exposure has neurotoxic, endocrine-disrupting, and behavioral effects which may additively or interactively combine with challenges associated with climate change. We used a literature review across animal taxa and contaminant classes, but focused on Arctic endotherms and contaminants important in Arctic ecosystems, to demonstrate potential for interactive effects across five bioenergetic domains: (1) energy supply, (2) energy demand, (3) energy storage, (4) energy allocation tradeoffs, and (5) energy management strategies; and involving four climate change-sensitive environmental stressors: changes in resource availability, temperature, predation risk, and parasitism. Identified examples included relatively equal numbers of synergistic and antagonistic interactions. Synergies are often suggested to be particularly problematic, since they magnify biological effects. However, we emphasize that antagonistic effects on bioenergetic traits can be equally problematic, since they can reflect dampening of beneficial responses and result in negative synergistic effects on fitness. Our review also highlights that empirical demonstrations remain limited, especially in endotherms. Elucidating the nature of climate change-by-contaminant interactive effects on bioenergetic traits will build toward determining overall outcomes for energy balance and fitness. Progressing to determine critical species, life stages, and target areas in which transformative effects arise will aid in forecasting broad-scale bioenergetic outcomes under global change scenarios.     

Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum

The resource allocation hypothesis is based on the assumption that defenses are costly, but relatively few studies have quantified the reproductive price of induced defenses, which represent the best means of measuring such costs in isolation from the genotypic costs that confound research involving constitutive defenses. Jasmonic acid (JA) is a plant signal molecule involved in the defensive responses of plants. It induces many of the same chemicals that are associated with herbivore damage, and thus offers a means of inducing plants without the removal of leaf area, which incurs its own costs. In tomato plants, JA induced resistance to Manduca sexta and increased levels of two defensive enzymes, polyphenol oxidase and peroxidase. We measured the impact of JA-induced defenses in tomato, Lycopersicon esculentum (Solanaceae), on several variables associated with reproductive success: fruit number, fruit weight, ripening time, time of fruit-set, number of seeds per fruit, total seeds per plant, the relationship between fruit weight and seed number, and germination success. Plants were grown in a pest-free greenhouse and treated biweekly with solvent or with JA at either of two concentrations: 10 mM or 1 mM. The high concentration of JA led to fewer but larger fruits, longer ripening time, delayed fruit-set, fewer seeds per plant, and fewer seeds per unit of fruit weight. The reproductive impact of induction was reduced at the lower dose, but still significant; 1 mM JA resulted in delayed fruit-set and fewer seeds per unit of fruit weight, compared to control plants. Our research indicates that JA-induced defenses impose significant costs on tomato plants.     

Toxin depletion has no effect on antipredator responses in common toad (Bufo bufo) tadpoles

Antipredator responses often involve changes in several phenotypic traits and these changes interactively influence fitness. However, gaining insight into how the overall fitness effect of the overall response comes about is notoriously difficult. One promising avenue is to manipulate a single defensive trait and observe how that modifies fitness as well as the expression of other inducible responses. In chemically‐defended animals, toxins are likely to be costly to produce but it is still unknown how their depletion influences other characteristics. In the present study, we artificially depleted bufadienolide toxin stores in common toad (Bufo bufo) tadpoles, and assessed the effect of this with respect to the interaction with predator presence and limited food availability. We found that toxin depletion in tadpoles did not significantly affect any of the measured life‐history traits. Tadpoles in the predator treatment exhibited an elevated development rate, although this was only apparent when food availability was limited. Also, body mass at metamorphosis was lower in tadpoles exposed to chemical cues indicating a predation threat and when food availability was limited. These results provide evidence that, in larval common toads, the expression of inducible defences may incur fitness costs, whereas chemical defences are either expressed constitutively or, if inducible, elevated toxin production has negligible costs.     

Tree species diversity alters plant defense investment in an experimental forest plantation in southern Mexico

How plant species diversity affects traits conferring herbivore resistance (e.g., chemical defenses), as well as the mechanisms underlying such effects, has received little attention. One potential mechanism for the effect of diversity on plant defenses is that increased plant growth at high diversity could lead to reduced investment in defenses via growth–defense trade‐offs. We measured tree growth (diameter at breast height) and collected leaves to quantify total phenolics in 2.5‐year‐old plants of six tropical tree species (N = 597 plants) in a young experimental plantation in southern Mexico. Selected plants were classified as monocultures or as polycultures represented by mixtures of four of the six species examined. Tree species diversity had a significant negative effect on total phenolics, where polycultures exhibited a 13 percent lower mean concentration than monocultures. However, there was marked variation in the effects of diversity on defenses among tree species, with some species exhibiting strong reductions in phenolic levels in mixtures, whereas others were unresponsive. In addition, tree species diversity had no effect on growth, nor was the negative effect of diversity on chemical defenses mediated by a growth–defense trade‐off. These results demonstrate that tree diversity can alter investment in chemical defenses in long‐lived tree species but that such effect may not always be under strong control by plant endogenous resource allocation trade‐offs. Regardless of the underlying mechanism, these findings have important implications for predicting effects on consumers and ecosystem function.