Tannin allocation in blackbrush (Coleogyne ramosissima)

Blackbrush (Coleogyne ramosissima) is a spinescent shrub occurring in nearly monospecific stands in the southwestern United States. Winter browsing by domestic goats stimulates spring twig production by blackbrush plants. Current season's twigs produced by older branches growing on the outer edges of the plant canopy (terminal branches) contained 2.37 times more tannins than did older twigs. Within blackbrush plants, current season's twigs on terminal branches contained 1.34 times more tannins than did current season's twigs on sprouts and younger branches (basal branches). When analysed separately, current season's terminal twigs contained 1.47 times more tannins than did leaves, while current season's basal twigs contained 1.10 times more tannins than did leaves. Phytochemicals, mainly phenolics, in blackbrush reduce its risk of being over-utilized by domestic herbivores, and the occurrence and distribution of tannins in blackbrush lend support to hypotheses dealing with secondary compounds as plant defences.     

Patterns in the production of antiherbivore chemical defenses in plant communities

The diversity of chemical identity and mode of action of toxic substances present in plants is suggested to be partially the result of generalist herbivore grazing pressure, while convergence in digestibility-reducing substances and their method of function is due primarily to specialist herbivore. Analysis of alkaloid patterns from herbaceous and woody perennials show that most species differ in their alkaloid composition and many sympatric species and subspecies show unique patterns. The high degree of functional convergence in digestibility-reducing substances is supported by convergent patterns in tannins among woody perennials.     

Impacts of urbanization on insect herbivory and plant defences in oak trees

Systematic comparisons of species interactions in urban versus rural environments can improve our understanding of shifts in ecological processes due to urbanization. However, such studies are relatively uncommon and the mechanisms driving urbanization effects on species interactions (e.g. between plants and insect herbivores) remain elusive. Here we investigated the effects of urbanization on leaf herbivory by insect chewers and miners associated with the English oak Quercus robur by sampling trees in rural and urban areas throughout most of the latitudinal distribution of this species. In performing these comparisons, we also controlled for the size of the urban areas (18 cities) and gathered data on CO₂ emissions. In addition, we assessed whether urbanization affected leaf chemical defences (phenolic compounds) and nutritional traits (phosphorus and nitrogen), and whether such changes correlated with herbivory levels. Urbanization significantly reduced leaf chewer damage but did not affect leaf miners. In addition, we found that leaves from urban locations had lower levels of chemical defences (condensed and hydrolysable tannins) and higher levels of nutrients (nitrogen and phosphorus) compared to leaves in rural locations. The magnitude of urbanization effects on herbivory and leaf defences was not contingent upon city size. Importantly, while the effects of urbanization on chemical defences were associated with CO₂ emissions, changes in leaf chewer damage were not associated with either leaf traits or CO₂ levels. These results suggest that effects of urbanization on herbivory occur through mechanisms other than changes in the plant traits measured here. Overall, our simultaneous assessment of insect herbivory, plant traits and abiotic correlates advances our understanding of the main drivers of urbanization effects on plant–herbivore interactions.     

Regrowth and tannin production in woody and succulent karoo shrubs in response to simulated browsing

Allocation of carbon to chemical defences has often been suggested to be a direct response to browsing or grazing by herbivores. This study quantitatively compares total polyphenol and tannin production in response to simulated browsing of three karoo shrubs in order to test this induced defence hypothesis. The three species studied responded to browsing either by rapid regrowth or by increasing polyphenol production in the remaining tissues. The patterns did not follow any phylogenetic relationships but were weakly associated with the palatability of each species. The highly palatable deciduous species Osteospermum sinuatum, which is capable of rapid regrowth, showed no or very low levels of constitutive and browsing-induced total polyphenols, condensed tannins and protein-precipitating tannins. The evergreen sclerophyllous species Pteronia pallens showed a limited regrowth capacity and had intermediate levels of polyphenols, while the evergreen succulent species Ruschia spinosa showed almost no regrowth over the study period. R. spinosa contained the highest constitutive and browsing-induced levels of polyphenols, condensed tannins and protein-precipitating tannins. In two of the species more than one anti-herbivore defence feature co-occur. P. pallens foliage contains both hepatotoxins and polyphenols while R. spinosa has both structural (spines) and chemical defences. Responses of karoo shrubs to simulated browsing are interpreted as the result of passive alterations in plant chemistry rather than as an active defence response to herbivores.     

You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants

Plant defences against herbivores include direct defences such as secondary metabolites or physical structures (e.g. trichomes) as well as indirect defences mediated via mutualistic interactions with other organisms including ants. Production of both direct defences and rewards for mutualistic ants may be costly for a plant, and it has been suggested that trade-offs may exist between direct and ant-mediated defences. We have conducted a meta-analysis of 25 studies testing the above hypothesis and found a significant negative correlation between plant allocation to direct and ant-mediated defences. The strength of correlation was similar for across- and within-species comparisons, and for chemical and physical direct defences. However, trade-offs with direct defences were significant only in plants which offered to ants more costly rewards such as food bodies and/or domatia, but not in plants which attracted ants with relatively cheap extrafloral nectaries. Our results therefore support the hypothesis that plant investment in ant-mediated defences may reduce the requirement for direct chemical and physical defences, but only in plants which offer more costly rewards to their bodyguards.     

Leaf herbivory and nutrients increase nectar alkaloids

Correlations between traits may constrain ecological and evolutionary responses to multispecies interactions. Many plants produce defensive compounds in nectar and leaves that could influence interactions with pollinators and herbivores, but the relationship between nectar and leaf defences is entirely unexplored. Correlations between leaf and nectar traits may be mediated by resources and prior damage. We determined the effect of nutrients and leaf herbivory by Manduca sexta on Nicotiana tabacum nectar and leaf alkaloids, floral traits and moth oviposition. We found a positive phenotypic correlation between nectar and leaf alkaloids. Herbivory induced alkaloids in nectar but not in leaves, while nutrients increased alkaloids in both tissues. Moths laid the most eggs on damaged, fertilized plants, suggesting a preference for high alkaloids. Induced nectar alkaloids via leaf herbivory indicate that species interactions involving leaf and floral tissues are linked and should not be treated as independent phenomena in plant ecology or evolution.     

Taxon size predicts rates of rarity in vascular plants

We surveyed rarity in the vascular plants of the continental U.S.A. and Canada and the vascular plants of Hawaii to test the hypothesis that rates of rarity are independent of taxonomic group size. We demonstrated that taxonomic groups of plants with few species consistently contained fewer than the expected numbers of rare species. This pattern was apparent at the levels of genus, family, order and class. We also found that the pattern remained when we examined rates of rarity by comparing sister taxa that share a common ancestor. This pattern may arise from either differential speciation and extinction patterns or taxonomic bias in species designations (lumping and splitting). The pattern of lineages with few species demonstrating reduced rates of rarity is opposite to that previously observed in mammals and birds. If the protection of representatives from a diversity of lineages is a conservation objective, plant conservation is facilitated by the fact that relatively few species-poor lineages contain rare species.     

Chemical and mechanical defense against herbivory in two sympatric species of desert Acacia

Abstract. Most African Acacia trees occur in semi-arid savannas, but some species grow in deserts at the periphery of their range in northern Africa and the Middle East. We studied Acacia raddiana and A. tortilis in the southern Negev desert of Israel. According to the resource availability hypothesis, plants in poor habitats invest heavily into anti-herbivore defense because losses to browsers are costly when growth rates are low. Few plants invest simultaneously in different categories of defense. This suggests that trade-offs exist, although little is known about how individuals allocate resources to defence in natural populations. In a field experiment, we studied chemical and mechanical defences as a response to differential browsing for more than 10 yr. Both Acacia species increased spinescence but there was no clear response in the production of total polyphenols, condensed tannins, and protein-precipitating tannins (only A. raddiana may increase secondary compounds under very high browsing levels). There was an age effect in spinescence but not in secondary compounds for both species, with younger trees investing more into anti-herbivore defense than older individuals. We were unable to find negative correlations between traits of chemical and mechanical defense. We conclude that inducibility and age effects suggest a cost for mechanical but not necessarily for chemical defense. Contrary to the predictions of the resource availability hypothesis, concentrations of secondary compounds were not higher in this desert environment than in savannas.     

A preliminary investigation of some Maruthamalai forest plants for phytochemical compounds

Twenty five plant species from the Maruthamalai hills, Coimbatore, were screened for the presence of phytoconstituents. Among 25 plants, 19 gave positive tests for flavonoids, 23 for alkaloids, 20 for saponins, 25 for tannins, 22 for steroids and terpenoids, 23 for phenolic compounds, and tests indicated the presence of rotenoids in all the plants.     

Age-related changes in defensive traits of Acacia tortilis Hayne

The theory of plant defences proposes that investments in physical and chemical defences are driven by the risk of herbivore damage, and limited by the cost of producing the particular defensive trait in terms of resources that could be directed to other sinks, such as growth and reproduction. We sampled twigs of 18 mature Acacia tortilis trees and their cohort of juveniles to test some predictions of this hypothesis. We expected a higher allocation of defensive traits to leaves and twigs in the young plants than in the mature ones as a result of a higher risk of damage by ungulates at the juvenile stage. Our results show that the juvenile plants produce more spines along their twigs, but have lower concentrations of phenolic compounds in their leaves than in the mature ones. We also expected a negative relation between the concentration of foliar nutrients and phenolic compounds, as predicted by the carbon/nutrient hypothesis. Only mature plants showed this pattern. Reproduction (in mature plants) and water stress (in juvenile plants) did not relate to allocation to secondary compounds as predicted by current hypotheses of plant defence.     

Phenotypic plasticity in chemical defence of butterflies allows usage of diverse host plants

Host plant specialization is a major force driving ecological niche partitioning and diversification in insect herbivores. The cyanogenic defences of Passiflora plants keep most herbivores at bay, but not the larvae of Heliconius butterflies, which can both sequester and biosynthesize cyanogenic compounds. Here, we demonstrate that both Heliconius cydno chioneus and H. melpomene rosina have remarkable plasticity in their chemical defences. When feeding on Passiflora species with cyanogenic compounds that they can readily sequester, both species downregulate the biosynthesis of these compounds. By contrast, when fed on Passiflora plants that do not contain cyanogenic glucosides that can be sequestered, both species increase biosynthesis. This biochemical plasticity comes at a fitness cost for the more specialist H. m. rosina, as adult size and weight for this species negatively correlate with biosynthesis levels, but not for the more generalist H. c. chioneus. By contrast, H. m rosina has increased performance when sequestration is possible on its specialized host plant. In summary, phenotypic plasticity in biochemical responses to different host plants offers these butterflies the ability to widen their range of potential hosts within the Passiflora genus, while maintaining their chemical defences.     

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

The present study is the first to consider human and nonhuman consumers together to reveal several general patterns of plant utilization. We provide evidence that at a global scale, plant apparency and phylogenetic isolation can be important predictors of plant utilization and consumer diversity. Using the number of species or genera or the distribution area of each plant family as the island “area” and the minimum phylogenetic distance to common plant families as the island “distance”, we fitted presence–area relationships and presence–distance relationships with a binomial GLM (generalized linear model) with a logit link. The presence–absence of consumers among each plant family strongly depended on plant apparency (family size and distribution area); the diversity of consumers increased with plant apparency but decreased with phylogenetic isolation. When consumers extended their host breadth, unapparent plants became more likely to be used. Common uses occurred more often on common plants and their relatives, showing higher host phylogenetic clustering than uncommon uses. On the contrary, highly specialized uses might be related to the rarity of plant chemicals and were therefore very species‐specific. In summary, our results provide a global illustration of plant–consumer combinations and reveal several general patterns of plant utilization across humans, insects and microbes. First, plant apparency and plant phylogenetic isolation generally govern plant utilization value, with uncommon and isolated plants suffering fewer parasites. Second, extension of the breadth of utilized hosts helps explain the presence of consumers on unapparent plants. Finally, the phylogenetic clustering structure of host plants is different between common uses and uncommon uses. The strength of such consistent plant utilization patterns across a diverse set of usage types suggests that the persistence and accumulation of consumer diversity and use value for plant species are determined by similar ecological and evolutionary processes.     

Nutrient and secondary metabolite concentrations in a savanna are independently affected by large herbivores and shoot growth rate

Carbon-based secondary metabolites (CBSMs) such as tannins are assumed to function as plant defences against herbivores. CBSMs are thought to be inversely related to growth rate and nutrient concentrations because a physiological trade-off exists between cellular growth and differentiation, but CBSM concentrations can be altered by herbivory-induced changes in the trade-off. We predicted that a significant interaction exists between herbivory and growth phase, such that the effects of large herbivores (or their exclusion) on nutrient or CBSM concentrations are greatest during phases of rapid shoot or leaf growth. Leaf samples were collected during phases of different growth rate from six woody species 4 years after establishment of a large-scale long-term herbivore exclusion experiment in Kruger National Park, South Africa. Samples were analysed for N, P, condensed tannins and total phenolics. Interactions between growth phase and herbivores were rare. However, the assumption that elevated nutrients and reduced CBSMs occurs during fast phases of growth was supported by four species (consistent with the growth-differentiation balance hypothesis), but not the other two. Large herbivores generally did not affect nutrients, but CBSMs in four species were reduced by large herbivores other than elephants, while CBSMs in two species were reduced by elephants. Carbon limitation ultimately prevailed among woody plants taller than 2 m under long-term browsing. Large herbivores and plant growth phase are independent and important determinants of nutrients or CBSMs in African savannas, but the effects depend on the interacting assemblages of species, which poses challenges to the application of current general hypotheses of plant defence.     

Leaf chemistry of woody plants in relation to season,canopy retention and goat browsing in a semiarid subtropical savanna

Abstract It is assumed that the phytochemistry of browse species protects their biomass and nutrients against herbivory. In this study we were primarily interested in (i) seasonal and phenology‐related variations in leaf chemistry, and (ii) chemistry‐related variations in the feeding behaviour of domestic goats. Such knowledge would guide management‐orientated modelling of browse–browser interactions in seasonal, subtropical zones where goats are abundant. The browse species studied were typical of semiarid savannas in southern Africa: Grewia occidentalis L. (Tiliaceae), Scutia myrtina (Burm. f) Kurz (Rhamnaceae), Diospyros lycioides Desf. ssp. lycioides (Ebenaceae), Rhus longispina Eckl. and Zeyh. (Anacardiaceae), Ehretia rigida (Thunb.) Druce (Boraginaceae) and Acacia karroo Hayne (Mimosoideae). Nitrogen (N), phosphorus (P), condensed tannins (CT), protein‐precipitating tannins (PPT), total phenols (TP), cellulose and lignin concentrations were estimated for each species during the late dormant and early growing seasons. N, P, CT and TP were elevated during the growth season, while cellulose, lignin and PPT decreased. Unlike cytoplasm contents, which varied seasonally, cell wall and vacuole contents varied both seasonally and among species. Except that seasonal variation in N of deciduous species was greater than that of evergreen species, leaf phenology was not related to variations in forage quality. Short‐term intake rates were not related to primary metabolite concentrations, but were positively related to secondary metabolites. Elevated intake rates of putative defences were concluded to be side‐effects of attempts by goats to increase nutrient intake rate, indicating tolerance of chemical defences. Without support for the hypothesis that chemical defences are correlated to canopy retention, we propose an alternative hypothesis, that defences are distributed among woody plants in semiarid, subtropical savannas according to shoot morphology because it affects the vulnerability of plant parts to browsers.     

Host plant defences and voltinism in European butterflies

Abstract.  1. With respect to seasonal availability for herbivores, plants defended by synthesising qualitative compounds differ from those protected by accumulation of quantitative macromolecules, leaf toughness, and low water and/or nutrient content. While the palatability of the former plants remains relatively constant during the season, the palatability of the latter group decreases with leaf age.
2. It was hypothesised that in seasonal temperate environments, quantitative plant defences should restrict the annual numbers of insect generations. To test this hypothesis, European butterflies were used as a model, both non-corrected regressions and tests controlling for phylogeny were carried out, and potentially confounding factors such as body size or occurrence in short-season environments were treated as covariables.
3. Non-phylogenetically controlled regressions corroborated that butterflies feeding on quantitatively protected hosts (woody plants + grasses) form fewer generations than species feeding on qualitatively protected forbs. Plant defences fitted voltinism better than butterfly size, and remained significant even after controlling for short seasons. Using independent contrasts, feeding on woody plants plus grasses, and feeding on woody plants only, predicted fewer generations. These patterns, however, applied exclusively for foliage-feeding species.
4. The association between plant defences and voltinism represents a hitherto overlooked pattern in the ecology of temperate herbivores. It may explain why large insects tend to form fewer generations and feed on structurally complex hosts, and why some species remain monovoltine although they are not restricted by short season.     

A seasonal census of phenolics, fibre and alkaloids in foliage of forest trees in Costa Rica: some factors influencing their distribution and relation to host selection by Sphingidae and Saturniidae

The foliage of 80 species common in the Santa Rosa National Park, Costa Rica, has been analysed for content of total phenolics, condensed tannins, acid detergent fibre and water. Wherever possible analyses were performed at three stages in the life cycle of the leaf: young but fully expanded (coinciding with the beginning of the rainy season); middle-aged (two months later); and old (six months later). A comparison of the three age classes showed no significant change in the levels of phenolics or fibre as leaves aged but water content decreased significantly. A comparison of deciduous and evergreen species in the sample showed that the latter group had leaves with a significantly higher fibre content at all three sampling times, most particularly at the beginning of the rainy season, but other measures were not significantly different. Alkaloids were much more common in the foliage of deciduous species and it was observed that their distribution differed significantly from that of total phenolics and condensed tannins. It is suggested that the interaction that occurs between many tannins and alkaloids would be liable to reduce the defence capability of both classes of compounds if they occurred together.
High levels of defoliation occur in the early rainy season (third to tenth weeks) due to larvae of moths of the Sphingidae and Saturniidae. A comparison of investigated tree species that host larvae of these two taxa shows a striking dichotomy. Species that are selected by Sphingidae tend to be relatively deficient in levels of phenolics but are more likely to contain alkaloids, and probably other small toxic molecules. Saturniidae, on the other hand, appear to prefer host-species rich in phenolics but poor in alkaloids.     

Plant ontogeny and chemical defence: older seedlings are better defended

Although patterns of seedling selection by herbivores are strongly influenced by plant age and the expression of anti-herbivore defence, it is unclear how these characteristics interact to influence seedling susceptibility to herbivory. We tracked ontogenetic changes in a range of secondary metabolites (total phenolics, alkaloids and cyanogenic glycosides) commonly associated with seedling defence for nine sympatric British grassland species. Although there was marked variation in concentrations of secondary metabolites between different species, we found a consistent increase in the deployment of phenolics, alkaloids and cyanogenics with seedling age for six of the seven dicotyledonous species examined. The two grass species by contrast exhibited low levels of secondary metabolites across all developmental stages, possibly due to an investment in structural (silica phytoliths) defence. Our results corroborate species-specific patterns of seedling herbivory observed in field studies, and offer some explanation for the relatively high sensitivity to herbivore attack frequently observed for relatively young seedlings compared with their older conspecifics. Our results also support predictions made by the growth–differentiation balance hypothesis regarding ontogenetic changes in resource allocation to anti-herbivore defence for a range of potential chemical defences and across a range of sympatric plant species presumably subject to broadly similar selective pressures at the regeneration stage.     

Latitudinal variation in plant chemical defences drives latitudinal patterns of leaf herbivory

A long‐standing paradigm in ecology holds that herbivore pressure and thus plant defences increase towards lower latitudes. However, recent work has challenged this prediction where studies have found no relationship or opposite trends where herbivory or plant defences increase at higher latitudes. Here we tested for latitudinal variation in herbivory, chemical defences (phenolic compounds), and nutritional traits (phosphorus and nitrogen) in leaves of a long‐lived tree species, the English oak Quercus robur. We further investigated the underlying climatic and soil factors associated with such variation. Across 38 populations of Q. robur distributed along an 18° latitudinal gradient, covering almost the entire latitudinal and climatic range of this species, we observed strong but divergent latitudinal gradients in leaf herbivory and leaf chemical defences and nutrients. As expected, there was a negative relationship between latitude and leaf herbivory where oak populations from lower latitudes exhibited higher levels of leaf herbivory. However, counter to predictions there was a positive relationship between leaf chemical defences and latitude where populations at higher latitudes were better defended. Similarly, leaf phosphorus and nitrogen increased with latitude. Path analysis indicated a significant (negative) effect of plant chemical defences (condensed tannins) on leaf herbivory, suggesting that the latitudinal gradient in leaf herbivory was driven by an inverse gradient in defensive investment. Leaf nutrients had no independent influence on herbivory. Further, we found significant indirect effects of precipitation and soil porosity on leaf herbivory, which were mediated by plant chemical defences. These findings suggest that abiotic factors shape latitudinal variation in plant defences and that these defences in turn underlie latitudinal variation in leaf herbivory. Overall, this study contributes to a better understanding of latitudinal variation in plant–herbivore interactions by determining the identity and modus operandi of abiotic factors concurrently shaping plant defences and herbivory.     

The plant hormone salicylic acid interacts with the mechanism of anti‐herbivory conferred by fungal endophytes in grasses

The plant hormone salicylic acid (SA) is recognized as an effective defence against biotrophic pathogens, but its role as regulator of beneficial plant symbionts has received little attention. We studied the relationship between the SA hormone and leaf fungal endophytes on herbivore defences in symbiotic grasses. We hypothesize that the SA exposure suppresses the endophyte reducing the fungal‐produced alkaloids. Because of the role that alkaloids play in anti‐herbivore defences, any reduction in their production should make host plants more susceptible to herbivores. Lolium multiflorum plants symbiotic and nonsymbiotic with the endophyte Epichloë occultans were exposed to SA followed by a challenge with the aphid Rhopalosiphum padi. We measured the level of plant resistance to aphids, and the defences conferred by endophytes and host plants. Symbiotic plants had lower concentrations of SA than did the nonsymbiotic counterparts. Consistent with our prediction, the hormonal treatment reduced the concentration of loline alkaloids (i.e., N‐formyllolines and N‐acetylnorlolines) and consequently decreased the endophyte‐conferred resistance against aphids. Our study highlights the importance of the interaction between the plant immune system and endophytes for the stability of the defensive mutualism. Our results indicate that the SA plays a critical role in regulating the endophyte‐conferred resistance against herbivores.     

Reduced chemical defence in ant‐plants? A critical re‐evaluation of a widely accepted hypothesis

Since its original formulation by Janzen in 1966, the hypothesis that obligate ant‐plants (myrmecophytes) defended effectively against herbivores by resident mutualistic ants have reduced their direct, chemical defence has been widely adopted. We tested this hypothesis by quantifying three classes of phenolic compounds (hydrolysable tannins, flavonoids, and condensed tannins) spectrophotometrically in the foliage of 20 ant‐plant and non‐ant‐plant species of the three unrelated genera Leonardoxa,Macaranga and Acacia (and three other closely related Mimosoideae from the genera Leucaena, Mimosa and Prosopis). We further determined biological activities of leaf extracts of the mimosoid species against fungal spore germination (as measure of pathogen resistance), seed germination (as measure of allelopathic activity), and caterpillar growth (as measure of anti‐herbivore defence).
Condensed tannin content in three of four populations of the non‐myrmecophytic Leonardoxa was significantly higher than in populations of the myrmecophyte. In contrast, we observed no consistent differences between ant‐plants and non‐ant‐plants in the Mimosoideae and in the genus Macaranga, though contents of phenolic compounds varied strongly among different species in each of these two plant groups. Similarly, among the investigated Mimosoideae, biological activity against spore or seed germination and caterpillar growth varied considerably but showed no clear relation with the existence of an obligate mutualism with ants. Our results did not support the hypothesis of ‘trade‐offs’ between indirect, biotic and direct, chemical defence in ant‐plants.
A critical re‐evaluation of the published data suggests that support for this hypothesis is more tenuous than is usually believed. The general and well‐established phenomenon that myrmecophytes are subject to severe attack by herbivores when deprived of their ants still lacks an explanation. It remains to be studied whether the trade‐off hypothesis holds true only for specific compounds (such as chitinases and amides whose cost may be the direct negative effects on plants’ ant mutualists), or whether the pattern of dramatically reduced direct defence of ant‐plants is caused by classes of defensive compounds not yet studied.