Effects of plant quality and ant defence on herbivory rates in a neotropical ant‐plant

1. Understanding the degree to which populations and communities are limited by both bottom‐up and top‐down effects is still a major challenge for ecologists, and manipulation of plant quality, for example, can alter herbivory rates in plants. In addition, biotic defence by ants can directly influence the populations of herbivores, as demonstrated by increased rates of herbivory or increased herbivore density after ant exclusion. The aim of this study was to evaluate bottom‐up and top‐down effects on herbivory rates in a mutualistic ant‐plant. 2. In this study, the role of Azteca alfari ants as biotic defence in individuals of Cecropia pachystachya was investigated experimentally with a simultaneous manipulation of both bottom‐up (fertilisation) and top‐down (ant exclusion) factors. Four treatments were used in a fully factorial design, with 15 replicates for each treatment: (i) control plants, without manipulation; (ii) fertilised plants, ants not manipulated; (iii) unfertilised plants and excluded ants and (iv) fertilised plants and ants excluded. 3. Fertilisation increased the availability of foliar nitrogen in C. pachystachya, and herbivory rates by chewing insects were significantly higher in fertilised plants with ants excluded. 4. Herbivory, however, was more influenced by bottom‐up effects – such as the quality of the host plant – than by top‐down effects caused by ants as biotic defences, reinforcing the crucial role of leaf nutritional quality for herbivory levels experienced by plants. Conditionality in ant defence under increased nutritional quality of leaves through fertilisation might explain increased levels of herbivory in plants with higher leaf nitrogen.     

A novel property of spider silk: chemical defence against ants

Spider webs are made of silk, the properties of which ensure remarkable efficiency at capturing prey. However, remaining on, or near, the web exposes the resident spiders to many potential predators, such as ants. Surprisingly, ants are rarely reported foraging on the webs of orb-weaving spiders, despite the formidable capacity of ants to subdue prey and repel enemies, the diversity and abundance of orb-web spiders, and the nutritional value of the web and resident spider. We explain this paradox by reporting a novel property of the silk produced by the orb-web spider Nephila antipodiana (Walckenaer). These spiders deposit on the silk a pyrrolidine alkaloid (2-pyrrolidinone) that provides protection from ant invasion. Furthermore, the ontogenetic change in the production of 2-pyrrolidinone suggests that this compound represents an adaptive response to the threat of natural enemies, rather than a simple by-product of silk synthesis: while 2-pyrrolidinone occurs on the silk threads produced by adult and large juvenile spiders, it is absent on threads produced by small juvenile spiders, whose threads are sufficiently thin to be inaccessible to ants.     

Effects of light on direct and indirect defences against herbivores of young plants of Mallotus japonicus demonstrate a trade-off between two indirect defence traits

Background and Aims

Although most studies on plant defence strategies have focused on a particular defence trait, some plant species develop multiple defence traits. To clarify the effects of light on the development of multiple defence traits, the production of direct and indirect defence traits of young plants of Mallotus japonicus were examined experimentally under different light conditions.

Methods

The young plants were cultivated under three light conditions in the experimental field for 3 months from May to July. Numbers of ants and pearl bodies on leaves in July were examined. After cultivation, the plants were collected and the developments of trichomes and pellucid dots, and extrafloral nectaries (EFNs) on the leaves were examined. On plants without nectar-collecting insects, the size of EFNs and the volume of extrafloral nectar secreted from the EFNs were examined.

Key results

Densities of trichomes and pellucid dots did not differ significantly among the plants under the different light conditions, suggesting that the chemical and physical defences function under both high and low light availability. The number of EFNs on the leaves did not differ significantly among the plants under the different light conditions, but there appeared to be a trade-off between the size of EFNs and the number of pearl bodies; the largest EFNs and the smallest number of pearl bodies were found under high light availability. EFN size was significantly correlated with the volume of extrafloral nectar secreted for 24 h. The number of ants on the plants was smaller under low light availability than under high and moderate light availability.

Conclusions

These results suggest that direct defence traits function regardless of light conditions, but light conditions affected the development of indirect defence traits.     

Plant polyphenols—secondary metabolism and chemical defence: Some observations

Secondary metabolism and theories of plant-animal co-evolution are briefly discussed. Current ideas concerning the role of polyphenols as mediators of a general form of chemical defence in plants are outlined. Studies are described of the association of a group of biosynthetically inter-related polyphenols based on gallic acid and D-glucose with the protein bovine serum albumin. The results are interpreted in terms of structure-activity relationships in protein-polyphenol complexation and are used to comment on the co-evolution theory and the position of plant polyphenols in higher plant secondary metabolism and defence.     

The price of safety: food deprivation in early life influences the efficacy of chemical defence in an aposematic moth

Aposematism is the combination of a primary signal with a secondary defence that predators must learn to associate with one another. However, variation in the level of defence, both within and between species, is very common. As secondary defences influence individual fitness, this variation in quality and quantity requires an evolutionary explanation, particularly as it may or may not correlate with variation in primary signals. The costs of defence production are expected to play a considerable role in generating this variation, yet studies of the cost of chemical defence have focused on species that sequester their defences, while studies in species that produce them de novo are scarce. Here we examine effects of resource availability on the production of chemical defences in female wood tiger moths Arctia plantaginis. This species produces defensive fluids when attacked, and advertises this protection with bright colours on its hindwings. Furthermore, the chemicals in these fluids are produced de novo. In order to establish if the production of this chemical protection is costly, and thus resource‐limited, we manipulated resource availability (i.e. food) during larval development and measured its subsequent effects on adult chemical defence. We presented defensive fluids from female moths to wild blue tits, in the absence of any visual cues, to determine their effectiveness against avian predators. Our results demonstrate that the defensive fluids produced by female moths repel birds, and that these defences require resource investment to produce. We found that moths that were resource‐limited during development had less effective chemical defences, despite producing the same volume of defensive fluids as the control moths. As a reduction in available resources negatively influences the effectiveness of the chemical defence, resource availability may explain the variation seen among individuals.     

Variable chemical defence in the checkerspot butterfly Euphydryas gillettii (Lepidoptera: NymphaIidae)

Abstract.

• 1 Like other checkerspots, Euphydryas gillettii butterflies may contain the defensive chemicals, iridoid glycosides, which are sequestered from their hostplants during larval feeding.
• 2 We analysed the iridoid glycoside content of E.gillettii adults from two different populations, Warm Lake, Idaho, and Granite Creek, Wyoming, that have different patterns of hostplant use.
• 3 Gas chromatographic analysis of thirty butterflies from the Wyoming population showed that they contained a mean of 1.27 (±0.19 SE) % dry weight iridoid glycosides. Notably, 20% of these butterflies contained no detectable iridoid glycosides.
• 4 In contrast, nineteen butterflies from the Idaho population contained a mean of 3.89 (±0.38 SE) % dry weight iridoid glycosides, and all butterflies contained iridoid glycosides.
• 5 These results illustrate how the chemical defence of herbivorous insects varies according to differential use of potential hostplants.

     

Pollen feeding,resource allocation and the evolution of chemical defence in passion vine butterflies

Evolution of pollen feeding in Heliconius has allowed exploitation of rich amino acid sources and dramatically reorganized life‐history traits. In Heliconius, eggs are produced mainly from adult‐acquired resources, leaving somatic development and maintenance to larva effort. This innovation may also have spurred evolution of chemical defence via amino acid‐derived cyanogenic glycosides. In contrast, nonpollen‐feeding heliconiines must rely almost exclusively on larval‐acquired resources for both reproduction and defence. We tested whether adult amino acid intake has an immediate influence on cyanogenesis in Heliconius. Because Heliconius are more distasteful to bird predators than close relatives that do not utilize pollen, we also compared cyanogenesis due to larval input across Heliconius species and nonpollen‐feeding relatives. Except for one species, we found that varying the amino acid diet of an adult Heliconius has negligible effect on its cyanide concentration. Adults denied amino acids showed no decrease in cyanide and no adults showed cyanide increase when fed amino acids. Yet, pollen‐feeding butterflies were capable of producing more defence than nonpollen‐feeding relatives and differences were detectable in freshly emerged adults, before input of adult resources. Our data points to a larger role of larval input in adult chemical defence. This coupled with the compartmentalization of adult nutrition to reproduction and longevity suggests that one evolutionary consequence of pollen feeding, shifting the burden of reproduction to adults, is to allow the evolution of greater allocation of host plant amino acids to defensive compounds by larvae.     

Cyanogenic and other glucosides in a neo-guinean bug Leptocoris isolata: Possible precursors in its host-plant

Two new glucosides, 3-β-d-glucopyranosyloxy-4-methyl-2(5H)-furanone and 4-β-d-glucopyranosyloxy-3-hydroxymethyl-butyronitril-2-en, were isolated from the hemolymph of adult Leptocoris isolata (Heteroptera). Besides these two compounds, the cyanogenic glucoside cardiospermin was found in whole adult bug extracts. The larvae contain the last two named compounds and a mixture of cyanolipids. Only the latter was found in the fruit of Allophylus cobbe, the host-plant of the insect. The possible relationship between the insect glucosides and the host-plant cyanolipids as well as their biological role is discussed.     

The dual role of sclerites in a gorgonian coral: Conflicting functions of support and defence

Sclerites in the gorgonian coral Briareum asbestinum perform the dual role of skeletal support against wave action and structural defence against predators. Local populations of B. asbestinum vary along gradients of decreasing water movement and decreasing predator abundance with increasing depth, such that sclerite length increases and sclerite density decreases with depth. Based on this pattern, I explored a possible trade-off between the sclerite composition that is most resistant to tearing versus most deterrent to predatory gastropods. Feeding assays revealed that artificial foods containing longer sclerites and those containing higher volume fractions of sclerites are less palatable to the gastropod Cyphoma gibbosum. However, real colonies appear constrained, in that they do not contain both long sclerites and high volume fractions at the same time. Given a choice among real colonies, snails prefer shallow-water colonies with shorter sclerites e ven though the sclerite volume fractions are high. Although least deterrent to snails, shallow-water colonies are 56% more resistant to tearing than their deep-water counterparts. Hence, variation in sclerite composition among local populations of B. asbestinum may be maintained by opposing selection for support versus defense.     

Isolation of a complementary DNA encoding the bean PR4 chitinase: an acidic enzyme with an amino-terminus cysteine-rich domain

The amino acid sequences of peptides generated by trypsin and chymotrypsin digestions of the acidic PR4 chitinase from bean were determined. Oligonucleotide primers derived from this sequence were used to synthesize a PR4 chitinase-specific probe by PCR-amplification. This probe allowed the isolation of cDNA clones encoding PR4 chitinase that have been sequenced. This acidic and extracellular chitinase shows some homology to the basic isoform from the same plant, and differs from other known acidic chitinases by the presence of an amino-terminal cysteine-rich domain. Southern blot analysis of bean genomic DNA revealed that PR4 chitinase is encoded by a single gene.     

Accumulation of phyllodulcin in sweet-leaf plants ofHydrangea serrata and its neutrality in the defence against a specialist leafmining herbivore

Among wild plants ofHydrangea serrata (Hydrangeaceae) in Japan, there are sweet plants whose leave contain a kind of isocoumarin, phyllodulcin, which happens to be 350 times as sweet as sucrose to the human tongue. In a primary beech forest in Ashu, Kyoto, the spatial distribution of sweet plants and temporal and the spatial distribution of phyllodulcin within and among plants were investigated using a high performance liquid chromatograph. The distribution of sweet plants was confined within a valley and was parapatric with non-sweet plants. A plant's characteristic phyllodulcin accumulation did not change, even when transplanted into the different habitats. The phyllodulcin content of the sweet plants varied greatly among plants, and the population mean peaked in July when the plants flowered. Within a plant, phyllodulcin content was elevated by partial defoliation. We examined the possible effect of phyllodulcin on herbivory by a specialist leafmining herbivore,Antispila hydrangifoliella (Lepidoptera: Heliozelidae). We transplanted sweet and nonsweet plants reciprocally between their original habitats, excluded attacks by parasitoids, and compared performance of the leafminer. Leafminer colonization and larval survivorship on transplanted andin situ plants was not significantly different between sites. The fact that accumulation of phyllodulcin did not augment a defensive function, at least against herbivory by the leafminer, and the sporadic distribution of phyllodulcin-accumulating plants, suggest that the genotypes synthesizing phyllodulcin emerged independently at separate localities by mutation, and that the genotypes are almost adaptively neutral in defence against the specialist herbivore.     

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.     

Pine sawfly defence and variation in host plant resin acids: a trade-off with growth

Abstract.

• 1 The defence capability of pine sawfly larvae reared on Scots pines with low or high concentrations of resin acids was determined in a field experiment, where larvae were exposed to predatory ants, and in a laboratory experiment in which the rate of defence droplet replenishment was measured.
• 2 Larvae on low resin-acid shoots disappeared faster than larvae on high resin-acid shoots when exposed to predatory ants.
• 3 Larvae fed high resin-acid needles produced 50% larger defence droplets than larvae fed low resin-acid needles.
• 4 In an additional experiment high predation pressure was simulated by repeatedly removing defence droplets. Larvae responded by feeding more on tissue rich in resin acids, but at the cost of a reduction in growth rate.
• 5 Based on these data and earlier findings that survival and development of sawfly larvae are negatively affected by high resin-acid concentrations, we conclude that pine sawflies face a dilemma of conflicting demands, i.e. although high needle resin-acid concentrations enhance defence capability, they also reduce growth and survival. Our data also suggest that it is not necessarily the ovipositing female that has to balance this trade-off: plasticity in larval feeding behaviour provides larvae with a means to at least partly solve the dilemma.

     

Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae)

Plants use chemical defences to reduce damage from herbivores and the effectiveness of these defences can be altered by biotic and abiotic factors, such as herbivory and soil resource availability. Streptanthus polygaloides , a nickel (Ni) hyperaccumulator, possesses both Ni-based defences and organic defences (glucosinolates), but the extent to which these defences interact and respond to environmental conditions is unknown. S. polygaloides plants were grown on high-Ni and low-Ni soil and concentrations of Ni and glucosinolates were compared with those of the congeneric non-hyperaccumulator, S. insignus spp. insignus , grown under the same conditions. Ni contents were highest (4000 μg g⁻¹ dry tissue) in S. polygaloides plants grown on high-Ni soil. Glucosinolate content was significantly higher in S. insignus than in S. polygaloides suggesting that plants defended by Ni produce a lower concentration of organic defences. In a separate experiment, high-Ni S. polygaloides plants were exposed to simulated herbivory or live folivores to determine the inducibility of Ni-based and organic defences. Contents of Ni were not affected by either herbivory treatment, whereas glucosinolate concentrations were >30% higher in damaged plants. We concluded that the Ni-based defence of S. polygaloides is not induced by herbivory.     

Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hu¨bner (Nymphalidae): A gravimetric and quantitative genetic analysis

Several recent studies document that specialist insect phytophages may be less subject to predation than generalists and suggest that hostplant-derived chemical defences may be an important explanation for the predominance of specialized feeding among insect herbivores. The evolution of such chemical defences depends upon both their advantages versus natural enemies and their physiological costs, but data on these costs, particularly genetic data, are few. Here I report the results of an ecological genetic investigation of food use efficiency and allelochemical sequestration in Junonia coenia Hu¨bner (Nymphalidae). I used standard gravimetric techniques to estimate the efficiency of dry matter incorporation and iridoid glycoside sequestration in the larvae of 37 full-sib families fed artificial diets containing trace, low (2%) and high (10%) concentrations of iridoid glycosides. I found a significant reduction in the efficiency of dry matter incorporation on a high iridoid diet that is entirely attributable to reduced digestibility rather than post-digestive toxic effects. Larvae fed high-iridoid diets sequestered them less efficiently, but this difference was due largely to post-digestive effects. Analyses of genetic variation and architecture of dry matter and iridoid budgets reveal substantial genetic variation in both suites of traits, but only chemical defence showed a significant genotype×environment interaction which would be conducive to the evolution of specialization. Neither group of traits showed across-diet trade-offs in the form of negative correlations of family means among diets. Family means correlations of sequestration indices with dry matter indices within diets reveals that chemical defence comes at a cost to growth, but only in the high diet. I also found evidence of specialized physiological machinery for iridoid glycoside processing. These data indicate that even adapted specialists are negatively affected by plant toxins, but in this species, dietary specialization is more likely to result from selection from natural enemies than from hostplant toxins.     

Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds

Many plants respond to herbivory with an increased production of extrafloral nectar (EFN) and/or volatile organic compounds (VOCs) to attract predatory arthropods as an indirect defensive strategy. In this study, we tested whether these two indirect defences fit the optimal defence hypothesis (ODH), which predicts the within-plant allocation of anti-herbivore defences according to trade-offs between growth and defence. Using jasmonic acid-induced plants of Phaseolus lunatus and Ricinus communis, we tested whether the within-plant distribution pattern of these two indirect defences reflects the fitness value of the respective plant parts. Furthermore, we quantified photosynthetic rates and followed the within-plant transport of assimilates with (13)C labelling experiments. EFN secretion and VOC emission were highest in younger leaves. Moreover, the photosynthetic rate increased with leaf age, and pulse-labelling experiments suggested transport of carbon to younger leaves. Our results demonstrate that the ODH can explain the within-plant allocation pattern of both indirect defences studied.