Plant Secondary Chemicals Research Articles

Use of high spectral resolution remote sensing to determine leaf palatability of eucalypt trees for folivorous marsupials

In this study we assess the feasibility of remotely measuring canopy biochemistry, and thus the potential for conducting large-scale mapping of habitat quality. A number of studies have found nutrient composition of eucalypt foliage to be a major determinant of the distribution of folivorous marsupials. More recently it has been demonstrated that a specific group of secondary plant chemicals, the diformylphloroglucinols (DFPs), are the most important feeding deterrents, and are thus vital determinants of habitat quality. We report on the use of laboratory spectroscopy to attempt to identify one such DFP, sideroxylonal-A, in the foliage of Eucalyptus melliodora, one of the few eucalypt species browsed by folivorous marsupials. Reflectance spectra were obtained for freeze-dried, ground leaves using near infrared spectroscopy (NIRS) and for both oven-dried and fresh whole leaves using a laboratory-based (FieldSpec) spectroradiometer. Modified partial least squares (MPLS) regression was used to develop calibration equations for sideroxylonal-A concentration based on the reflectance spectra transformed as both the first and second difference of absorbance (Log 1/R). The predictive ability of the calibration equations was assessed using the standard error of calibration statistic (SECV). Coefficients of determination (r2) were highest for the ground leaf spectra (0.98), followed by the fresh leaf and dry leaf spectra (0.94 and 0.87, respectively). When applied to independent validation sub-sets, sideroxylonal-A was most accurately predicted from the ground leaf spectra (r2 = 0.94), followed by the dry leaf and fresh leaf spectra (0.72 and 0.53, respectively). Two spectral regions, centred on 674 nm and 1394 nm, were found to be highly correlated with sideroxylonal-A concentration for each of the three spectral data sets studied. Results from this study suggest that calibration equations derived from modified partial least squares regression may be used to predict sideroxylonal-A concentration, and hence leaf palatability, of Eucalyptus melliodora trees, thereby indicating that the remote estimation of habitat quality of eucalypt forests for marsupial folivores is feasible.

Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective.

Most herbivorous arthropods are specialists that feed on one or a few related plant species. To understand why this is so, both mechanistic and functional studies have been carried out, predominantly restricted to bitrophic aspects. Host-selection behaviour of herbivorous arthropods has been intensively studied and this has provided ample evidence for the role of secondary plant chemicals as source of information in behavioural decisions of herbivores. Many evolutionary studies have regarded co-evolution between plants and herbivores to explain the diversity of secondary plant chemicals and host specialisation of herbivores. However, many cases remain unexplained where herbivores select host plants that are suboptimal in terms of fitness returns. A stimulating paper by Bernays and Graham [(1988) Ecology 69, 886-892)] has initiated a discussion on the need of a multitrophic perspective to understand the evolution of host-plant specialisation by herbivorous arthropods. However, this has hardly resulted in ecological studies on host-selection behaviour that take a multitrophic perspective. Yet, evidence is accumulating that constitutive and induced infochemicals from natural enemies and competitors can affect herbivore behaviour. These cues may constitute important information on fitness prospects, just as plant cues can do. In this paper I selectively review how information from organisms at different trophic levels varies in space and time and how herbivores can integratively exploit this information during host selection. In doing so, research areas are identified that are likely to provide important new insights to explain several of the questions in herbivore host selection that remain unanswered so far. These research areas are at the interface of evolutionary ecology, behavioural ecology and chemical ecology.

Functional foods: an ecologic perspective

A functional food is defined as any food or food ingredient that may provide a health benefit beyond that conferred by the nutrients the food contains. As nutrition scientists move into this arena, they must build on the wealth of information that already exists in plant biology. In particular, the evolutionary and physiologic bases for the production of secondary plant chemicals in plants must be considered in order to plan meaningful experiments for testing the functionality of these chemical compounds for humans. One problem that may arise is that in using the term functional food, the meaning may be lost in the continued proliferation of related terms used in product marketing. The new National Institutes of Health Office of Dietary Supplements addressed some of these issues as it developed the operating definitions described in this report.

GENÉTICA DA ASSOCIAÇÃO DE INSETOS COM PLANTAS HOSPEDEIRAS

We present here the theoretical principles and main genetic methodologies for the study of speciation in insect herbivores. The presence of genetic polymorphism in herbivore populations may be associated to ecological factors, like the chemical variability in host plants. In this sense, we study the genetic-ecological relations like oviposition preference and larval performance, use of life tables of herbivore placed over different host plants, and mainly the geographic variation of characters associated to host plant exploitation. The use of the concept of host-race, or, herbivore populations that present specializations to a certain host plants, adds, to the study of crypyic species. We search the existence of these species when we find, in the same locus , different alleles fixed in different sympatric species host-races. We believe that host shifts were the prevalent events in the sympatric differentiation of herbivores, and that these would be associated to shifts in the polymorph characters associated to host exploitation. It is suggested that host shifts are associated to ecological and genetic restrictions. It is accepted that the great diversity of plant secondary chemicals evolved as a response to the attack of insect herbivores and that some insects evolved in response to the changes in their host plants, so, resulting from a diffuse coevolution between plants and herbivores. A similar process seeks to explain the patterns of herbivore and plant diversification, namely, “escape and radiation coevolution”. Finally, the analysis of phylogenies may provide evidence, based on the patterns of diversification of herbivores and their host plants, for the functions played by genetics, physiology, ecology, and geography in the evolution of these groups.

The raison d'être of secondary plant chemicals?

It is 40 years since Gottfried Fraenkel published ‘The raison d'être of secondary plant substances’1. Fraenkel acknowledged that many of the original ideas relating to the action of secondary chemicals on herbivores had been highlighted at the end of the 19th century by Ernst Stahl, a botany professor from Jena, Germany2. Plants can defend themselves, either directly, as eluded to by Fraenkel, or indirectly by utilizing natural enemies of the herbivores attacking the plant. The study of these indirect defences (tritrophic interactions) has been extremely active in the past decade, and the recent opening of the Max Plank Institute for Chemical Ecology in Jena3 is testament to the field's perceived importance. The first series of presentations at the recent Novartis Symposia**Novartis Symposia No. 223 Insect–Plant Interactions and Induced Plant Defence, Novartis Foundation, London, UK, 13–15 October 1998. on insect–plant interactions further highlighted this trend.

Diet choice and nutrition of captive snowshoe hares (Lepus americanus): Interactions of energy, protein, and plant secondary compounds

:We examined consumption and digestibility of winter browse in captive snowshoe hares (Lepus americanus Erxl.) to determine how energy content, protein quality and plant secondary chemicals interact to affect their diet choice and nutrition. We found that preferred foods of snowshoe hares have higher apparent digestibilities of dry matter and energy than nonpreferred foods. Digested crude protein was unaffected by increased consumption of preferred foods, but declined when hares consumed nonpreferred foods. Rate of weight loss in hares increased with increasing consumption of nonpreferred twigs. Hares did not compensate for low protein or low energy content by eating more twigs. Weight changes were correlated with the energy content of the food and its digestibility, whereas consumption was correlated with phenol and protein content. If hares can increase consumption of preferred foods, they may simultaneously meet both their energy and protein requirements. If they are obliged to increase consumption of nonpreferred foods, then protein requirements may never be met due to the effects of secondary compounds. During periods of limited food availability, snowshoe hares should select a mixed diet that may include small quantities of poor-quality food items, regardless of preference, allowing them time to find good-quality foods.

Roots, nutrients and their relationship to spatial patterns

Ecosystem sustainability and resilience after a disturbance may be regulated by processes occurring at smaller spatial scales. The matrix of different spatial environments are created by (1) individual plants that accumulate higher concentrations of specific nutrients, trace elements or defensive plant secondary chemicals and thereby modify the chemistry of their ecological space and/or rates of processes, (2) the presence of structures (e.g., coarse woody debris) that may buffer some micro-environments from disturbances by functioning as a hospitable environment or as a reservoir for mycorrhizal fungi to sustain them into the next phase of stand development, and (3) chemical changes in soils during soil development which may result in distinct soil chemical environments. The response of the plants or change in the sustainability of carbon and nutrient cycles may be expressed more strongly at this smaller ecological space of an individual plant and furthermore must be frequently examined separately by the above- and belowground space of that individual.

Conclusions on the role of salt-affected soils in primary succession on the Tanana River floodplain, interior Alaska

Results of the study of salt-affected soils on the Tanana River floodplain in interior Alaska raised a number of key issues that are important to resolve with future research in this fluvial environment. The results emphasized the prominent role of plant succession in ecosystem structure and function in northern boreal forests. For example, alder plays a crucial role in organic matter and nitrogen dynamics in floodplain ecosystems. This plant species has an impact on ecosystem processes in successional stages beyond its period of dominance on the floodplain. The potential facilitative nature of nitrogen accumulation, mediated by alder, to plant community development during and subsequent to the alder phase of succession should be examined in future studies. Organic matter chemistry and soil temperature appeared to be more important controls of soil processes than high soil salt content. Moreover, secondary plant chemicals may play a role in determining rates of soil nitrification in these floodplain ecosystems. The importance of ion balance to plant nutrition and primary production in salt-affected soils is an important topic for future research. Groundwater may be a unique source of water and nutrients to floodplain plant communities. The magnitude of water flux to the rooting zone in relation to terrace elevation and river level and its importance to plant growth is a significant consideration in the semiarid environment of interior Alaska. The established plant community indicates which species are successful in this environment. Optimum species-terrace combinations may exist that maximize productivity through use of unique moisture and nutrient supplies associated with a shallow water table. Results of this work suggested that new research initiatives are crucial to advance the fundamental understanding of controls of ecosystem processes and as a base of information to support forest resource management.

Nutrition and the protein economy in grasshoppers and locusts

1. 1. The protein and amino acid requirements of grasshoppers are similar to those of other mandibulate, phytophagous insects and are met by soluble leaf protein. 2. 2. The acquisition, digestion, assimilation and utilization of leaf protein are all subject to the negative effects of plant secondary chemicals. 3. 3. Adaptations to secondary plant chemicals have been reported in some grasshoppers but the presence of certain chemicals can have serious consequences in protein nutrition. 4. 4. Interference with protein intake, or the enforced secretion of digestive proteinases caused by some plants, results in symptoms resembling starvation. 5. 5. Negative effects on the protein economy of grasshoppers can severely reduce growth, survival and reproduction and stimulate compensatory feeding and dietary self-selection. 6. 6. Starvation or diets resulting in low protein acquisition can stimulate the reallocation of protein reserves, and ultimately tissue resorption.

Plant Chemical Defense and Twig Selection by Snowshoe Hare: An Optimal Foraging Perspective

We examined preferences of snowshoe hares for twigs of 2 winter forage plants: chemically defended balsam poplar Populus balsamifera and comparatively less defended gray willow Salix glauca. We used an optimal foraging model that explicitly incorporates the effects of secondary plant chemicals to predict foraging preferences of hares. The model predicted that the foraging preferences should be conditional: preference should depend on the ratio of digestible nutrient content in the defended and comparativeIy less defended plants relative to the ratio of the wet mass/dry mass of defended and comparatively less defended plants

Generalized plant defense: effects on multiple species.

Two species of lepidopteran herbivores, Manduca sexta (Sphingidae) and Trichoplusia ni (Noctuidae), were reared on synthetic diet containing either the alkaloid nicotine or the flavonoid rutin. Survival and pupal weight of the specialist M. sexta did not differ when larvae were reared on diet containing nicotine or rutin. In contrast, the generalist T. ni did not survive on diet containing 0.125% nicotine or greater, whereas larvae survived on all concentrations of rutin. These data demonstrate that the alkaloid nicotine is inhibitory toward generalist, but not specialist herbivores, whereas the flavonoid rutin has no effect on specialist herbivores and limited effects on generalist herbivores. Five species of Pseudomonas bacterial pathogens: P. syringae, P. syringae pv. angulata, P. syringae pv. tabaci, P. fluorescens, and P. solanacearum were grown on nutrient agar containing nicotine or rutin at concentrations ranging from 0.0 to 1.0% wet weight in 0.1% intervals. No species of Pseudomonas grew at concentrations greater than 0.5% nicotine when 106 colony forming units (cfu) were used, but growth occurred at all concentrations of rutin when 102 cfu were used. These data indicate that nicotine was inhibitory to growth of both herbivores and pathogens, suggesting that certain plant secondary chemicals with high toxicity are of a generalized nature and affect multiple species. Differences in the sensitivity of organisms to allelochemicals such as generalist or specialist can make it appear that specific allelochemicals affect specific organisms, when in fact it is the tolerance of the organism to the plant chemical that is responsible. In four separate studies, the growth of M. sexta, T. ni and Helicoverpa zea was significantly lower on plants inoculated with P. solanacearum. Alteration in leaf quality by P. solanacearum was due to either reductions in leaf nutrients or increases in allelochemicals. We speculate that localized or systemic induction by both herbivores and pathogens can cause changes in leaf quality, effecting each other's subsequent colonization. The generalized nature of plant secondary compounds and potential reciprocal effects on induction by both species suggests that herbivores and pathogens may affect plant quality through induction and diffuse interactions of disparate species can alter the community of organisms colonizing a plant.

Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats.

Ecosystems are structurally organized as food webs within which energy is transmitted between trophic levels and dissipated into the environment. Energy flow between two trophic levels is given by the amount of production at the lower level and by the proportion of production that is consumed, assimilated and respired at the higher level. Considerable evidence indicates that food-web structure varies predictably in different habitats, but much less is known about quantitative relationships among food web fluxes. Many of the energetic properties of herbivores in African game parks are associated with rainfall and, by inference, with net primary productivity. Respiratory costs per unit production at the consumer trophic level are higher for homeotherms than for heterotherms. Plant secondary chemicals affect herbivore dietary choices and the allocation of plant resources to those chemicals varies with resource availability. How these phenomena are translated into ecosystem fluxes is unknown. We present evidence that herbivore biomass, consumption and productivity are closely correlated with plant productivity, suggesting that the latter is a principal integrator and indicator of functional processes in food webs.

Interspecific differences among swallowtail larvae (Lepidoptera: Papilionidae) in susceptibility to aristolochic acids and berberine

Abstract. 1. The larvae of four swallowtail butterfly species, Papilio polyxenes Fabr. in the Papilionini, Parides bunichus (Hübner) and Battus polydamas (L.) in the Troidini, and Eurytides marcellus (Cramer) in the Graphiini, were grown on host leaves to which test compounds had been added.2. The test chemicals are biosynthetically related. Berberine, a 1‐benzyl‐tetrahydroisoquinoline‐related (1‐BTIQ) alkaloid, is found in many rutaceous hosts of the Papilionini; laudanosine, a simpler 1‐BTIQ alkaloid, is found in the Papaveraceae, plants on which no papilionids feed; aristolochic acids are found only in the Aristolochiaceae, hosts of the Troidini.3. Swallowtail larvae can tolerate the compounds characteristic of their host plants, but not chemicals found in the hosts of other papilionid groups. Diets with laudanosine did not affect the test species.4. Our results support the contention that plant secondary chemicals, such as berberine and aristolochic acids, are important feeding barriers, and are partially responsible for host specificity in swallowtails.

Primate species separation in relation to secondary plant chemicals

Food selection of different primate species is reviewed in relation to secondary plant chemicals such as alkaloids and tannins. Different species discriminate differently against these chemicals. The tolerance of potentially toxic substances (e.g. alkaloids) is not restricted to species with enlarged foreguts but is also found among lemurs with rather unspecialized digestive systems. On the community level different reactions towards food chemicals seem to be an important mechanism contributing to species separation and thus allowing coexistence.

An antifeedant in balsam poplar inhibits browsing by snowshoe hares.

The 'plant defense guild' hypothesis for the evolution of plant secondary chemicals predicts that plant species defend themselves against generalist herbivores such as the snowshoe hare (Lepus americanus) in the Canadian boreal forest by evolving unique antifeedant chemicals. Plant species may coevolve in an ecosystem by presenting an array of chemicals to herbivores. We report further evidence for this idea from the presence of 2,4,6-trihydroxydihydrochalcone in the CH2Cl2 extracts of Populus balsamifera juvenile twigs. These extracts, added to rabbit chow, were offered to hares in choice tests. The bioassay established that the chemical acted as an antifeedant for hares.

Food partitioning among Malagasy primates

Food partitioning among lemurs was studied in relation to food patch size and plant chemistry in the eastern rainforest and a western deciduous forest of Madagascar. Patch size (i.e. crown diameter of food trees) is significantly correlated with group body weight of different lemur species. But intraspecific variability is high and prevents effective species separation. Chemical analyses of more than 400 plant parts eaten by seven different lemur species revealed major differences in their food choice with respect to protein concentrations, condensed tannins and alkaloids. Among the leaf eating lemurs discriminant analysis segregates three groups à two species based on chemical characteristics of their food. Whereas differences in food chemistry are pronounced between groups they are lacking between the two species within each group. The two species of each group avoid interference competition by different activity rhythms. Actual competition for slowly renewable resources such as leaves and fruit, however, can not be reduced by different activities. Here interspecific differences in gross categories of food, food species composition and different habitat utilization due to other constraints may contribute to the possible coexistence of species. Thus interspecific differences in food selection in relation to primary and secondary plant chemicals is an integrated part of the mechanisms allowing several primate species to coexist in sympatry.

HOST-PLANT RELATIONSHIPS IN THE PAPILIONIDAE (LEPIDOPTERA): PARALLEL CLADOGENESIS OR COLONIZATION?

Abstract- Stepwise coevolution, as defined by Ehrlich and Raven (1964) and others, can be equated with parallel cladogenesis or association by descent (Mitter and Brooks, 1983). I review the insect/plant literature and discuss recent cladistic findings for the Papilionidae, and compare two contrasting theories: 1) that insect/host associations have evolved through parallel cladogenesis; or 2) that insects have 'colonized' their hosts subsequent to plant cladogenesis. I conclude that no documented examples of parallel cladogenesis between insects and plants are known. The swallowtail cladograms instead offer evidence in support of the second theory. They suggest that host association patterns in the Papilionidae have resulted from repeated colonization of plants belonging to a relatively small number of families. I discuss data which indicate that plant secondary chemicals have been important 'barriers' to colonization (sensu Ehrlich and Raven, 1964), and have in large part mediated host switching in the Papilionidae.

Are chemical barriers necessary for evolution of butterfly-plant associations?

The association between heliconiine butterflies and Passion flower vines is composed of three or more subassociations, in which each Heliconius species group feeds on a different Passiflora subgenus. The relationships are consistent with the adaptive zone hypothesis of Ehrlich and Raven, which would suggest that (1) species of the subgenus Plectostemma proliferated as a result of chemical barriers to herbivory, which created a herbivore-free adaptive zone in which speciation and diversification took place, and (2) species of the H. erato-charitonia group overcame these barriers and entered a competitor-free adaptive zone, in which they proliferated and speciated with those plants as hosts. The hypothesis that plant secondary chemicals were responsible for creating such barriers to herbivory was tested using heliconiine species as bioassays, in which reduced growth rates indicated presence of chemical barriers to feeding. Contrary to expectation, plants of the subgenus Plectostemma showed little or no chemical defense against any species of heliconiine caterpillar. In contrast many plants of the "primitive" subgenus Granadilla possessed significant chemical barriers against herbivory by heliconiine larvae, excepting those species in the H. numata-melpomene species group. I concluded that chemical barriers to feeding were not responsible for proliferation and diversification in the subgenus Plectostemma, nor did chemicals create a competitor-free "adaptive zone" in which the H. erato-charitonia species-group could proliferate and speciate. Chemical barriers may have been important in the evolution of the subgenus Granadilla-heliconiine association. I suggest that plant allelochemics are only one of many possible barriers to herbivory which can help create "adaptive zones" for plants and their herbivores, and that the patterns of butterfly foodplant specialization discussed by Ehrlich and Raven (1964) are not necessarily the result of biochemical adaptation and counteradaptation.

Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies,Danaus plexippus L. Reared on milkweed plants in California: 2.Asclepias speciosa

The pattern of variation in gross cardenolide concentration of 111Asclepias speciosa plants collected in six different areas of California is a positively skewed distribution which ranges from 19 to 344 μg of cardenolide per 0.1 g dry weight with a mean of 90 μg per 0.1 g. Butterflies reared individually on these plants in their native habitats ranged from 41 to 547 μg of cardenolide per 0.1 g dry weight with a mean of 179 μg. Total cardenolide per butterfly ranged from 54 to 1279 μg with a mean of 319 μg. Differences in concentrations and total cardenolide contents in the butterflies from the six geographic areas appeared minor, and there were no differences between the males and the females, although the males did weigh significantly more than females. The uptake of cardenolide by the butterflies was found to be a logarithmic function of the plant concentration. This results in regulation: larvae which feed on low-concentration plants produce butterflies with increased cardenolide concentrations relative to those of the plants, and those which feed on high-concentration plants produce butterflies with decreased concentrations. No evidence was adduced that high concentrations of cardenolides in the plants affected the fitness of the butterflies. The mean emetic potencies of the powdered plant and butterfly material were 5.62 and 5.25 blue jay emetic dose fifty units per milligram of cardenolide and the number of ED50 units per butterfly ranged from 0.28 to 6.7 with a mean of 1.67. Monarchs reared onA. speciosa, on average, are only about one tenth as emetic as those reared onA. eriocarpa. UnlikeA. eriocarpa which is limited to California,A. speciosa ranges from California to the Great Plains and is replaced eastwards byA. syriaca L. These two latter milkweed species appear to have a similar array of chemically identical cardenolides, and therefore both must produce butterflies of relatively low emetic potency to birds, with important ecological implications. About 80% of the lower emetic potency of monarchs reared on A. speciosa compared to those reared onA. eriocarpa appears attributable to the higher polarity of the cardenolides inA. speciosa. Thin-layer Chromatographie separation of the cardenolides in two different solvent systems showed that there are 23 cardenolides in theA. speciosa plants of which 20 are stored by the butterflies. There were no differences in the cardenolide spot patterns due either to geographic origin or the sex of the butterflies. As when reared onA. eriocarpa, the butterflies did not store the plant cardenolides withR f values greater than digitoxigenin. However, metabolic transformation of the cardenolides by the larvae appeared minor in comparison to when they were reared onA. eriocarpa. AlthoughA. eriocarpa andA. speciosa contain similar numbers of cardenolides and both contain desglucosyrioside, the cardenolides ofA. speciosa overall are more polar. ThusA. speciosa has no or only small amounts of the nonpolar labriformin and labriformidin, whereas both occur in high concentrations inA. eriocarpa. A. speciosa plants and butterflies also contain uzarigen, syriogenin, and possibly other polar cardenolides withR f values lower than digitoxin. The cardenolide concentration in the leaves is not only considerably less than inA. eriocarpa, but the latex has little to immeasurable cardenolide, whereas that ofA. eriocarpa has very high concentrations of several cardenolides. Quantitative analysis ofR f values of the cardenolide spots, their intensities, and their probabilities of occurrence in the chloroform-methanol-formamide TLC system produced a cardenolide fingerprint pattern very different from that previously established for monarchs reared onA. eriocarpa. This dispels recently published skepticism about the predictibility of chemical fingerprints based upon ingested secondary plant chemicals.

Insect--plant adaptations.

The adaptation of insects to plants probably commenced in the early Permian period, though most current associations will be more recent. A major burst of adaptation must have followed the rise of the Angiosperms in the Cretaceous period, though some particular associations are as recent as this century. Living plants form a large proportion of the potential food in most habitats, though insects have had to overcome certain general hurdles to live and feed on them. Insects affect the reproduction and survival of plants, and thus the diversity of plant secondary chemicals may have evolved as a response. Where an insect species has a significant effect on a plant species that is its only host, coevolution may be envisaged. A spectacular example is provided by Heliconius butterflies and passion flower vines, studied by L.E. Gilbert and others. But such cases may be likened to 'vortices in the evolutionary stream': most plant species are influenced by a range of phytophagous insects so that selection will be for general defences--a situation termed diffuse coevolution. Evidence is presented on recent host-plant shifts to illustrate both the restrictions and the flexibility in current insect-plant associations.