Investment In Chemical Defenses Research Articles

Diet influences resource allocation in chemical defence but not melanin synthesis in an aposematic moth.

For animals that synthesise their chemical compounds de novo, resources, particularly proteins, can influence investment in chemical defences and nitrogen-based wing colouration such as melanin. Competing for the same resources often leads to trade-offs in resource allocation. We manipulated protein availability in the larval diet of the wood tiger moth, Arctia plantaginis, to test how early life resource availability influences relevant life history traits, melanin production and chemical defences. We expected higher dietary protein to result in more effective chemical defences in adult moths and a higher amount of melanin in the wings. According to the resource allocation hypothesis, we also expected individuals with less melanin to have more resources to allocate to chemical defences. We found that protein-deprived moths had a slower larval development, and their chemical defences were less unpalatable for bird predators, but the expression of melanin in their wings did not differ from that of moths raised on a high-protein diet. The amount of melanin in the wings, however, unexpectedly correlated positively with chemical defences. Our findings demonstrate that the resources available in early life have an important role in the efficacy of chemical defences, but melanin-based warning colours are less sensitive to resource variability than other fitness-related traits.

Ecogeographical determinants of investment in chemical defences in pines

Ecogeographical determinants of investment in chemical defences in pines

Phenolics lie at the centre of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning.

Saplings in the shade of the tropical understorey face the challenge of acquiring sufficient carbon for growth as well as defence against intense pest pressure. A minor increase in light availability via canopy thinning may allow for increased investment in chemical defence against pests, but it may also necessitate additional biochemical investment to prevent light-induced oxidative stress. The shifts in secondary metabolite composition that increased sun exposure may precipitate in such tree species present an ideal milieu for evaluating the potential of a single suite of phenolic secondary metabolites to be used in mitigating both abiotic and biotic stressors. To conduct such an evaluation, we exposed saplings of two unrelated species to a range of light environments and compared changes in their foliar secondary metabolome alongside corresponding changes in the abiotic and biotic activity of their secondary metabolite suites. Among the numerous classes of secondary metabolites found in both species, phenolics accounted for the majority of increases in antioxidant and UV-absorbing properties as well as activity against an invertebrate herbivore and a fungal pathogen. Our results support the hypothesis that phenolics contribute to the capacity of plants to resist co-occurring abiotic and biotic stressors in resource-limited conditions.

Trade-offs between defenses against herbivores in goldenrod (Solidago altissima)

In the goldenrod Solidago altissima, most stems are erect, but “ducking” genotypes bend the tip of the apical stem downward for much of the growing season, and this morphology protects against at least two gall-forming herbivore species. Despite this advantage to defense, ducking remains a rare strategy in goldenrod, yet the costs that prevent ducking genotypes from outcompeting erect genotypes remain unclear. We tested whether ducking (an architectural defense) trades off with chemical defense against aphids (Uroleucon nigrotuberculatum). We hypothesized that signaling related to the ducking defense might interfere with investment in chemical defenses, making ducking plants more susceptible to some herbivores. To test this hypothesis, we compared aphid survival and preference on ducking and erect genotypes. We also measured terpenoid concentration in S. altissima leaf tissue to determine whether plant investment in these compounds correlated with either ducking or aphid performance. Aphids had higher survival on all three ducking genotypes than their erect counterparts and preferred ducking to erect plants in two of three genotype pairings. However, terpenoid concentrations did not track with either ducking or aphid performance and cannot therefore explain the differences between ducking and erect host-plants. Although the mechanism remains unknown, the data supported the predicted trade-off in defenses against different herbivores, which may contribute to the distribution and abundance of these two defensive strategies.

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

AbstractHow 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.

Egg Production Constrains Chemical Defenses in a Neotropical Arachnid.

Female investment in large eggs increases the demand for fatty acids, which are allocated for yolk production. Since the biosynthetic pathway leading to fatty acids uses the same precursors used in the formation of polyketides, allocation trade-offs are expected to emerge. Therefore, egg production should constrain the investment in chemical defenses based on polyketides, such as benzoquinones. We tested this hypothesis using the harvestman Acutiosoma longipes, which produces large eggs and releases benzoquinones as chemical defense. We predicted that the amount of secretion released by ovigerous females (OFs) would be smaller than that of non-ovigerous females (NOF). We also conducted a series of bioassays in the field and in the laboratory to test whether egg production renders OFs more vulnerable to predation. OFs produce less secretion than NOFs, which is congruent with the hypothesis that egg production constrains the investment in chemical defenses. Results of the bioassays show that the secretion released by OFs is less effective in deterring potential predators (ants and spiders) than the secretion released by NOFs. In conclusion, females allocate resources to chemical defenses in a way that preserves a primary biological function related to reproduction. However, the trade-off between egg and secretion production makes OFs vulnerable to predators. We suggest that egg production is a critical moment in the life of harvestman females, representing perhaps the highest cost of reproduction in the group.

Tri-trophic effects of seasonally variable induced plant defenses vary across the development of a shelter building moth larva and its parasitoid.

Plant chemical defenses can negatively affect insect herbivore fitness, but they can also decrease herbivore palatability to predators or decrease parasitoid fitness, potentially changing selective pressures on both plant investment in production of chemical defenses and host feeding behavior. Larvae of the fern moth Herpetogramma theseusalis live in and feed upon leaf shelters of their own construction, and their most abundant parasitoid Alabagrus texanus oviposits in early instar larvae, where parasitoid larvae lay dormant for most of host development before rapidly developing and emerging just prior to host pupation. As such, both might be expected to live in a relatively constant chemical environment. Instead, we find that a correlated set of phenolic compounds shows strong seasonal variation both within shelters and in undamaged fern tissue, and the relative level of these compounds in these two different fern tissue types switches across the summer. Using experimental feeding treatments, in which we exposed fern moth larvae to different chemical trajectories across their development, we show that exposure to this set of phenolic compounds reduces the survival of larvae in early development. However, exposure to this set of compounds just before the beginning of explosive parasitoid growth increased parasitoid survival. Exposure during the period of rapid parasitoid growth and feeding decreased parasitoid survival. These results highlight the spatial and temporal complexity of leaf shelter chemistry, and demonstrate the developmental contingency of associated effects on both host and parasitoid, implying the existence of complex selective pressures on plant investment in chemical defenses, host feeding behavior, and parasitoid life history.

Does Prescribed Burning Affect Leaf Secondary Metabolites in Pine Stands?

Prescribed burning (PB) is gaining popularity as a low-cost forest protection measure that efficiently reduces fuel build-up, but its effects on tree health and growth are poorly understood. Here, we evaluated the impact of PB on plant defenses in Mediterranean pine forests (Pinus halepensis and P. nigra ssp. laricio). These chemical defenses were estimated based on needle secondary metabolites (terpenes and phenolics including flavonoids) and discussed in terms of chlorophyll fluorescence and soil nutrients. Three treatments were applied: absence of burning (control plots); single burns (plots burned once); and repeated burns (plots burned twice). For single burns, we also explored changes over time. In P. laricio, PB tended to trigger only minor modifications consisting exclusively of short-lived increases (observed within 3 months after PB) in flavonoid index, possibly due to the leaf temperature increase during PB. In P. halepensis, PB had detrimental effects on physiological performance, consisting of (i) significant decreases in actual PSII efficiency (ΦPSII) in light-adapted conditions after repeated PB, and (ii) short-lived decreases in variable-to-maximum fluorescence ratio (Fv/Fm) after single PB, indicating that PB actually stressed P. halepensis trees. Repeated PB also promoted terpene-like metabolite production, which increased 2 to 3-fold compared to control trees. Correlations between terpene metabolites and soil chemistry were found. These results suggest that PB impacts needle secondary metabolism both directly (via a temperature impact) and indirectly (via soil nutrients), and that these impacts vary according to species/site location, frequency and time elapsed since last fire. Our findings are discussed with regard to the use of PB as a forest management technique and its consequences on plant investment in chemical defenses.

Defence Cheats Can Degrade Protection of Chemically Defended Prey

AbstractMany species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.

Changes in plant chemical defenses and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae)

Numerous empirical studies have examined ontogenetic trajectories in plant defenses but only a few have explored the potential mechanisms underlying those patterns. Furthermore, most documented ontogenetic trajectories in plant defenses have generally concentrated on aboveground tissues; thus, our knowledge regarding whole plant trends in plant defenses throughout development or potential allocation constraints between growth and defenses is limited. Here, we document changes in plant biomass, nutritional quality and chemical defenses for below- and aboveground tissues across seven age classes of Plantago lanceolata (Plantaginaceae) to evaluate: (1) partial and whole plant ontogenetic trajectories in constitutive chemical defenses and nutritional quality, and (2) the role of resource allocation constraints, namely root:shoot (R:S) ratios, in explaining whole plant investment in chemical defenses over time. Overall investment in iridoid glycosides (IGs) significantly increased, while water and nitrogen concentrations in shoot tissues decreased with plant age. Significant variation in IG content between shoot and root tissues across development was observed: allocation of IGs into root tissues linearly increased from younger to older plants, while non-linear shifts in allocation of IGs during ontogeny were observed for shoot tissues. Finally, R:S ratios only weakly explained overall allocation of resources into defenses, with young stages showing a positive relationship, while older stages showed a negative relationship between R:S ratios and IG concentrations. Ontogenetic trajectories in plant quality and defenses within and among plant tissues can strongly influence insect herbivores' performance and/or predation risk; thus, they are likely to play a significant role in mediating species interactions.

Costs of constitutive and herbivore‐induced chemical defences in pine trees emerge only under low nutrient availability

Summary 1. Production of antiherbivore chemical defences is generally assumed to be costly in terms of fitness, although some studies have failed to detect such costs. A convincing explanation is that the expression of fitness costs depends on environmental conditions such as nutrient availability. 2. We performed a greenhouse experiment with 33 half‐sib families in order to study the phenotypic plasticity of constitutive and methyl jasmonate‐induced chemical defences to soil phosphorus (P) availability, the existence of genetic trade‐offs (costs) between growth and the production of those defences and the extent to which P availability may modulate the expression of those costs. 3. We measured some proxies of vegetative fitness (primary growth, secondary growth and total biomass), plant reserves (soluble sugars and starch) and the concentration of quantitative chemical defences (diterpene content in the stem, total polyphenolics and condensed tannins in the needles). 4. Phosphorus availability had a considerable effect, both on the allocation of resources to constitutive and induced defences and on the expression of vegetative costs associated with those chemical defences. Constitutive investment in chemical defences was greater under P‐limited conditions for all studied traits. Inducibility of foliar phenolic compounds was greater under P‐limited conditions, and it was strongly constrained under high P availability. Availability of P did not affect the inducibility of stem diterpenes. 5. All defensive traits showed significant genetic variation, with different levels of genetic control in constitutive and induced modes, and genetic variation in their inducibility. We found significant negative genetic correlations (i.e. trade‐offs) between growth and defensive investment, but costs of chemical defences emerged only in P‐limited conditions. Vegetative costs of constitutive defences were detected for stem diterpenes but not for needle phenolics, while costs of induced defences were found for leaf phenolics but not for stem diterpenes. 6. Synthesis. Our results indicate that P availability controls the production of chemical defences in this pine species, influencing the resource allocation to constitutive defences, the inducibility of those defences and the emergence of related vegetative costs. Phosphorus availability thus appears as a major driver in the evolution of pine resistance to insects and a potential factor in maintaining genetic variation in defences.

Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2

How species interactions may modify the effects of environmental change on evolutionary adaptation is poorly understood. Elevated CO2 is known to alter plant–herbivore interactions, but the evolutionary consequences for plant populations have received little attention. We conducted an experiment to determine the effects of elevated CO2 and herbivory by a specialist insect herbivore (Danaus plexippus) on the expression of constitutive and induced plant defense traits in five genotypes of Asclepias syriaca, and assessed the heritability of these traits. We also examined changes in relative fitness among plant genotypes in response to altered CO2 and herbivory. The expression of plant defense traits varied significantly among genotypes. Elevated CO2 increased plant growth and physical defenses (toughness and latex), but decreased investment in chemical defenses (cardenolides). We found no effect of elevated CO2 on plant induction of cardenolides in response to caterpillar herbivory. Elevated CO2 decreased the expression of chemical defenses (cardenolides) to a different extent depending on plant genotype. Differential effects of CO2 on plant defense expression, rather than direct effects on relative fitness, may alter A. syriaca adaptation to changing climate.

Pheromone-induced life-history shifts

In a recent paper,1 we showed that recurrent exposure to alarm pheromones reduced development time and size at metamorphosis in larval cane toads (Bufo marinus). Subsequent measurements of post-metamorphic toads revealed larger parotoid glands relative to body size and increased amounts of bufalin (a toxic bufodienalide) in animals from the experimental treatment, suggesting increased investment in chemical defences. These findings are of interest for evolutionary theory. But the study was also part of a larger conservation-based research program of which this pheromone work was an important component in the development of a management strategy for reducing the ecological impact of invasive cane toads in Australia. For example, our study1 aimed to quantify biochemical and life-history effects as well as assess the likely long-term impact of pheromone exposure on toads. In this addendum, I discuss the conservation potential of our research, with emphasis on exploiting alarm pheromones to induce viability reducing life-history shifts.

Alarm cues experienced by cane toad tadpoles affect post‐metamorphic morphology and chemical defences

1 In many anuran species, larvae modify their developmental trajectories and behaviour in response to chemical cues that predict predator risk. Recent reviews highlight a dearth of studies on delayed (post-metamorphic) consequences of larval experience. 2 We raised cane toad (Bufo marinus) tadpoles either under control conditions or in the presence of non-lethal predator cues (crushed conspecifics). 3 Exposure to these chemical cues massively reduced size at metamorphosis, as predicted by theory. Parotoid glands were larger relative to body size in post-metamorphic animals from the experimental treatment, suggesting higher investment in chemical defences. 4 Exposure to chemical cues from crushed conspecifics during larval life reduced total bufadienolide content of metamorphs, but increased amounts of one specific bufadienolide (bufalin). 5 Hence, cane toads respond to perceived predation risk in the aquatic environment by metamorphosing at a smaller size and modifying their investment in defensive toxins during post-metamorphic life. 6 Phenotypically flexible responses to larval conditions vary among amphibian taxa, and can involve significant carry-over effects into post-metamorphic life.

Latitudinal variation in spongivorous fishes and the effectiveness of sponge chemical defenses

It has been proposed that predation pressure declines with increasing latitude and a positive correlation exists between predation intensity and the investment into chemical defenses. However, little direct evidence supports the idea that tropical species are better defended chemically than their temperate counterparts. Temperate reefs of the South Atlantic Bight (SAB) off Georgia, USA, provide a unique opportunity to study tropical sponges in a temperate environment. We documented sponge species richness and abundance, sponge predator density, and examined the ability of eight sponge species to chemically deter predation by fishes on two reefs in the SAB. We used rarefaction analysis and ANOVA to compare our results for sponge species richness and density, respectively, with similar published studies conducted on reefs of the sub-tropical Atlantic (i.e., Florida Keys). These analyses were combined with similar statistical comparisons for spongivorous fish species richness and density. Results showed that sponge species richness was lower, but sponge density was higher, on the temperate SAB reefs than on the subtropical reefs. Both spongivorous fish diversity and density were lower on the SAB reefs. The greater abundance of sponges and lower density of predators on SAB reefs suggest a lower frequency of predation on sponges on SAB reefs. Of the eight sponge species assayed from the SAB reefs, five possessed chemical extracts that were significantly less deterrent to fish predators than their tropical/subtropical conspecifics. When the results were combined across all sponge species, the chemical deterrence of fish predators was significantly lower for extracts obtained from the temperate sponge community as compared to the tropical/subtropical assemblage. These results support the more general hypothesis that a lower density and diversity of sponge predators occurs at high as compared to low latitudes in the western Atlantic and may contribute to decreased investment in chemical defenses.

Changes in resource concentration and defence during leaf development in a tough-leaved (Nothofagus moorei) and soft-leaved (Toona ciliata) species

Developing leaves that are soft, with high concentrations of resources, can be particularly vulnerable to herbivore damage. Since a developing leaf cannot be very tough, given the constraints of cell expansion, the major form of protection is likely to be chemical defence. We investigated changes in concentration of herbivore resources (protein, carbohydrates and water) and putative defences (total phenolics, tannin activity, cyanogenic glycosides, alkaloids, cell wall, and leaf mechanics) across five leaf development stages of the soft-leaved Toona ciliata M. Roem. and the tough-leaved Nothofagus moorei (F. Muell.) Krasser. Chemical defences were predicted to be more highly developed in young than expanded leaves of both species, and to decline more in expanded leaves of N. moorei, which become tough and strong at maturity, than in the softer expanded leaves of T. ciliata. Resources and defences were dynamic within the developing leaves. Highest concentrations of protein were recorded in young leaves in both species, and highest levels of non-structural carbohydrate were recorded in young leaves of T. ciliata. Allocation to defence varied in both amount and type across leaf stages. In T. ciliata, there was an increase in chemical defence in expanded leaves (tannin activity, alkaloids). However, in N. moorei, increasing strength and toughness of developing leaves coincided with decreasing chemical defence, consistent with our hypothesis. For phenolics, this decrease was partly due to dilution by cell wall, but cyanogenic glycosides were present in young leaves and absent in fully mature leaves. These results are consistent with leaf toughness acting as an effective anti-herbivore defence, thereby reducing the need for investment in chemical defence.

Effects of cessation of grazing on leaf‐level photosynthesis of Periploca laevigata

Abstract. The impact of grazing pressure on gas exchange of Periploca laevigata was studied in relation to its nutritional status. P. laevigata, a woody and highly palatable shrub, is an important forage species in the dry season in Cabo de Gata Natural Park (Almeria, SE Spain) where this study was carried out. Seasonal and diurnal courses of net photosynthesis, transpiration and stomatal conductance were measured in the field. In addition, soil and plant nutrient status were measured as potential factors influencing leaf photosynthetic levels. Early in the growing season, ungrazed P. laevigata had higher photosynthetic activity than grazed plants suggesting that the defoliated plants were still recovering from herbivore damage in the previous summer. Later in the growing season grazed P. laevigata had higher photosynthetic activity than ungrazed plants, suggesting higher metabolic activity and a possible investment in chemical defences. Concentrations of P and N in the soil were higher in the grazed area. The nutrient concentration of the leaves of P. laevigata was similar in grazed and ungrazed plants.

Do plant species with high relative growth rates have poorer chemical defences?

1. Most theories of plant strategies assume the presence of certain ‘trade‐offs’. One such evolutionary trade‐off assumes a decrease in growth rate with increasing investment in chemical defences in species adapted to different levels of habitat fertility. 2. To test this hypothesis, we grew 31 herbaceous species of Asteraceae under controlled conditions of temperature (25 °C), humidity (80%), light (500 μmol m–2 s–1) and photoperiod (16 h day–1) in a modified Hoagland hydroponic solution. The plants grew from seed for 35 days post‐germination and were harvested at 14, 21, 28 and 35 days. Relative growth rate (RGR) was calculated as well as a general measure of potential phytochemical toxicity (LC50) using an alcohol extraction of secondary compounds followed by Brine Shrimp bioassay and an assay of total phenolics. 3. The interspecific correlation between RGR and the potential phytochemical toxicity was weak and non‐significant (rS = 0·12, P = 0·53). The correlation between RGR and total phenolics was weak, positive but significant (rS = 0·40, P = 0·03). 4. These results suggest that such an evolutionary trade‐off does not exist in this group of Asteraceae.

Nutritional adaptations of caper shrub(Capparis OvataDesf.) to environmental stress

Abstract Capparis ovata, a prostrate shrub found in most arid zones of Mediterranean countries, has been cultivated extensively for the last ten years, although its physiology is unknown. To test the effect of fertilization on Capparis, two year old seedlings were grown in pots, and doses of nitrogen (N), phosphorus (P), and potassium (K) were added in a factorial design. Total bio‐mass production, nutrient concentration and uptake, and allocation patterns were studied. Fertilization induced an increase in productivity and nutrient tissue concentrations of both N and P. Capparis showed characteristics of a plant adapted to poor soils, where water and nutrients are strongly limiting. Increased K and Ca uptake to maintain the hydric balance, thorny stems and a heavy investment in chemical defences to prevent grazing, and a deep mycorrhizal root system allow Capparis to grow successfully in very infertile soils and to endure environmental stress.