Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds

The diet selection of two groups of red colobus monkeys (Procolobus badius) in Kibale National Park, Uganda are considered with respect to protein, fiber, digestibility, alkaloids, total phenolics, tannins, saponins, and cyanogenic glycosides. Both groups selected young leaves over mature leaves and young leaves had more protein, were more digestible, and had a higher protein to fiber ratio than mature leaves. Young and mature leaves did not differ with respect to secondary compounds. There were no differences in the phytochemical factors examined between frequently eaten foods and leaves that red colobus were never known to eat, but were relatively common in the environment. Regression analyses predicting foraging effort from the phytochemical components of the large group's diet revealed selection for only one factor, foods that are high in protein and low in fiber, when differences in food tree availability were taken into consideration. A similar analysis with the small group did not suggest selection or avoidance of foods with respect to any of the factors considered. Previous studies have found the biomass of folivorous primates to be related to the ratio of protein to fiber concentration of mature leaves in the environment. These investigations have considered variation in folivore biomass and forest composition among sites separated by hundreds of kilometers; however, large variation in folivore abundance occurs over much smaller spatial scales. In Kibale National Park the average protein to fiber ratio of the mature leaves of the 20 most abundant tree species predicted the biomass of red colobus among four neighboring sites. We examined the generality of this relationship by adding our biomass and leaf chemistry values to previously published values; 62% of the variance in colobine biomass was explained by variation in the protein to fiber ratios of mature leaves at the sites. There was no evidence that red colobus avoided plants with high levels of secondary compounds. In fact, one of the most preferred trees (Prunus africana) was the species with the highest levels of cyanogenic glycosides, and the highest saponin levels were found in the young leaves of Albizia grandibracteata, the sixth and fourth most preferred plant species for the large and small groups, respectively.     

Herbivore-deterring secondary compounds in heterophyllous woody species of the Mascarene Islands

Heterophylly (juvenile-adult leaf dimorphism) is widespread among native woody species of the Mascarene Islands, but the causes to this phenomenon have so far not been fully explained. The absence of mammals and dominance of now extinct giant tortoises and flightless birds are characteristics of the original Mascarene fauna. The present study investigates the hypothesis that the distinct morphology and colouration of juvenile leaves signalled unpalatability to browsing giant tortoises or birds. Juvenile and adult leaves of 28 heterophyllous woody species endemic to the islands of Mauritius and Rodrigues were screened for possible chemical defences against herbivory. The screening comprised the following classes of secondary compounds: alkaloids, cyanogenic constituents, saponins, simple phenolics, tannins and anthocyanins. The screening showed that there are no consistent significant differences between juvenile and adult leaves regarding any of the studied secondary compound classes, with the exception of the level of anthocyanins, which was significantly higher in juvenile leaves. This difference was also clearly reflected in a generally high degree of red patterning of juvenile leaves. Based on comparisons with floras of other oceanic islands once inhabited by tortoises and birds, and an evaluation of feeding habits of these herbivores, we suggest that the reduced lamina and partly red colouration of juvenile leaves may be an evolutionary response to selective herbivory by birds.     

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.     

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.     

Patterns in the phytochemistry of arctic plants

Ninety-one species of arctic tundra plants were screened for possible chemical defences against herbivory. Tannins were found in one-third of the species, whereas two-thirds of the plants contained alkaloids. Anthraquinones, cyanogenic glycosides and saponins accounted for only 6% of the positive reactions. The results were used to test the apparency hypothesis for the distribution of chemical plant defences which states that rare or unpredictable species should contain qualitative defences (toxins, such as alkaloids) while common or predictable species should contain quantitative defences (digestibility-reducing compounds, such as tannins). Abundance of plant species showed no relationship to chemical content, except that the relatively abundant shrubs more often contained tannins than the relatively rare forbs. Common graminoids (grasses and related taxa) did not contain tannins and data for the other classes of compounds did not support the apparency hypothesis. Graminoids appeared to rely on tolerance to grazing rather than chemical defences and common ericaceous plants produced both digestibility-reducing and toxic compounds.     

Use of leaf resources by howling monkeys (Alouatta palliata) and leaf-cutting ants (Atta cephalotes) in the tropical rain forest of Los Tuxtlas,Mexico

Use of leaf resources by a troop of howling monkeys and two colonies of leaf cutting ants was studied for an annual cycle in the rain forest of Los Tuxtlas, Mexico. Howling monkeys spent half their annual foraging time feeding on leaves; leaf-cutting ants spent at least 80% of their recorded foraging time harvesting leaves. Both herbivores preferred young leaves over nature ones, and chemical analysis showed that the protein: fibre ratio of the leaves used was correlated with these preferences. Howling monkeys used 34 tree species as leaf sources. Leaf-cutting ants used 40 plant species of which 38 were trees. Eighteen species used by Alouatta were also used by Atta; species of Moraceae and Lauraceae were among the most important in their foraging preferences. The plant species used by monkeys and ants occurred at low densities (? 4.0 ind/ha). The seasonal production of leaves, the high density of leaf-cutting ant colonies at the study site, and the high amounts of young foliage harvested by the ants from tree species, and individual trees used by howling monkeys as sources of young leaves suggest that the foraging activities of Atta may represent a significant pressure upon leaf resources available to Alouatta.     

Warming the tundra: reciprocal responses of invertebrate herbivores and plants

Rapid warming in northern ecosystems is simultaneously influencing plants, herbivores and the interactions among them. Recent studies suggest that herbivory could buffer plant responses to environmental change, but this has only been shown for vertebrate herbivores so far. The role of invertebrate herbivory in tundra ecosystems is often overlooked, but can be relevant in determining the structure and dynamics of tundra plant communities and may also affect how plants respond to warming. Invertebrate herbivores are also likely to respond more rapidly to warming than vertebrates because their behaviour and life cycles strongly depend on temperature. We investigated the effects of current season warming on Arctic moth caterpillars, their herbivory rates, and the subsequent responses of two common tundra plants, Salix arctica and Dryas octopetala. We manipulated both herbivore presence and temperature in a full‐factorial field experiment at two elevations, using enclosures and passive warming chambers. Changes in temperature achieved through elevation and/or experimental warming directly affected caterpillars, herbivory and the responses of plants. Caterpillars performed worse (higher respiration rates and lower growth rates) in warmer, lower elevation plots and shifted their diets towards more nutritious foods, such that the relative intensity of herbivory changed for the two studied plants. Within‐season responses of both forage plant species were weak, but invertebrate herbivores affected the responses of plants to elevation or experimental warming. Our results suggest that increased temperatures can reduce the performance of cold‐adapted invertebrate herbivores, with potential consequences to the longer term responses of tundra plants to warming due to changes in herbivory rates and selective foraging.     

Contributions to the botany and nutritional value of some wild amaranthus species (Amaranthaceae) of Nuevo leon,Mexico

Seeds and plants of Amaranthus have been a source of food for many cultures in the world. Some species can be found as weeds or growing wild under severe climatic and soil conditions, but their potential as food sources has not been studied. The objective of this work was to study the nutritional quality of four wild species ofAmaranthus,A. retroflexus (AR),A. viridis (A V),A. palmeri (AP) andA. blitoides (AB) as potential sources of vegetable greens. Histochemical studies showed higher levels of starch in leaves of AR and AB, moderate amounts of tannins in all leaves, high protein concentration in stems and leaves, and moderate amounts of alkaloids in all tissues of AV and AB. Antinutritional factors (nitrates, oxalates, cyanogenic glycosides, tannins and phytates) were quantified in plants at the preflowering stage, but only nitrates were found at levels (0.34-2% dw) above those generally considered as safe, but at similar levels found in spinach. No cyanogenic glycosides were detected in any species. Bromatologic analysis of whole or different plant parts at preflowering and maturity (mature seeds) showed that mature whole plants or individual sections can be recommended as animal feed since they contain high levels of protein (20.6-24.7% whole plant, 25.3-32.9% leaves) and soluble carbohydrate (>40%).Amaranthus plants could be best consumed as vegetables at the preflowering stage. At this stage, the highest protein concentrations were found in leaves (22.8-27.8%), while the remaining chemical composition was very similar to that found in other food vegetables. The four species showed similar chemical compositions, and had no detrimental chemicals which would deter their use as vegetable foods. Organoleptic taste preference studies would best indicate the stage at which the plant should be harvested for human consumption.     

Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function

Herbivores induce plants to undergo diverse processes that minimize costs to the plant, such as producing defences to deter herbivory or reallocating limited resources to inaccessible portions of the plant. Yet most plant tissue is consumed by decomposers, not herbivores, and these defensive processes aimed to deter herbivores may alter plant tissue even after detachment from the plant. All consumers value nutrients, but plants also require these nutrients for primary functions and defensive processes. We experimentally simulated herbivory with and without nutrient additions on red alder (Alnus rubra), which supplies the majority of leaf litter for many rivers in western North America. Simulated herbivory induced a defence response with cascading effects: terrestrial herbivores and aquatic decomposers fed less on leaves from stressed trees. This effect was context dependent: leaves from fertilized-only trees decomposed most rapidly while leaves from fertilized trees receiving the herbivory treatment decomposed least, suggesting plants funnelled a nutritionally valuable resource into enhanced defence. One component of the defence response was a decrease in leaf nitrogen leading to elevated carbon : nitrogen. Aquatic decomposers prefer leaves naturally low in C : N and this altered nutrient profile largely explains the lower rate of aquatic decomposition. Furthermore, terrestrial soil decomposers were unaffected by either treatment but did show a preference for local and nitrogen-rich leaves. Our study illustrates the ecological implications of terrestrial herbivory and these findings demonstrate that the effects of selection caused by terrestrial herbivory in one ecosystem can indirectly shape the structure of other ecosystems through ecological fluxes across boundaries.     

Cyanogenesis in plants

Several thousand plant species, including many economically important food plants, synthesize cyanogenic glycosides and cyanolipids. Upon tissue disruption, these natural products are hydrolyzed liberating the respiratory poison hydrogen cyanide. This phenomenon of cyanogenesis accounts for numerous cases of acute and chronic cyanide poisoning of animals including man. This article reviews information gathered during the past decade about the enzymology and molecular biology of cyanogenesis in higher plants. How compartmentation normally prevents the large-scale, suicidal release of HCN within the intact plant is discussed. A renewed interest in the physiology of these cyanogenic compounds has revealed that, in addition to providing protection for some species against herbivory, they may also serve as storage forms for reduced nitrogen.     

Spatially complex neighboring relationships among grassland plant species as an effective mechanism of defense against herbivory

Close spatial relationships between plant species are often important for defense against herbivory. The associational plant defense may have important implications for plant community structure, species diversity, and species coexistence. An increasing number of studies have focused on associational plant defense against herbivory at the scale of the individual plant and its nearest neighbors. However, the average neighborhood effects between plant species at the scale of whole plant communities have received almost no attention. The aims of this study were to determine patterns of spatial relationship between different plant species that can provide effective defense against herbivory. We conducted a manipulative experiment using sheep and three native plant species with different palatability. Consumption of palatable plants by herbivores was largest when the three plant species were isolated in three patches and independent of each other. A homogenous and spatially equal neighbor relationship between the three species did not reduce the risk of herbivory of palatable species compared to isolation of these species, but it reduced the total intake of all plant species. The palatable species was subject to less herbivory in a complex spatial neighborhood of several plant species. High complexity of spatial neighborhood resulted in herbivores passively reducing selectivity, thereby reducing the probability of damage to palatable species in the community, or making inaccurate judgments in foraging selectivity between and within patches, thereby reducing the vulnerability of palatable plants and even the whole plant community. We conclude that compelling herbivores to passively reduce the magnitude of foraging selectivity by establishing spatially complex neighborhoods between plant species is a compromise and optimal spatial strategy by plants to defend themselves again herbivory. This may contribute not only to maintenance of plant species diversity but also to a stable coexistence between herbivores and plants in grassland ecosystems.     

How do differences in species and part consumption affect diet nutrient concentrations? A test with red colobus monkeys in Kibale National Park,Uganda

Within a primate species, diet can be highly variable in composition, even at small spatial scales within the same forest, or temporally, suggesting that primates use different plant species and parts to meet similar nutritional needs. To test whether such differences in the plant species and parts that primates eat affects the nutrient concentrations that they obtain, we observed feeding of seven groups of red colobus monkeys ( Procolobus rufomitratus) residing in Kibale National Park, Uganda. The different groups consumed mostly young leaves from many of the same plant species, but spent different amounts of time feeding on them. As protein and fibre are suggested to be important determinants of colobine food choice and abundance, we analysed multiple samples of 47 food species for protein and fibre. Despite the differences in the plant species and parts eaten, the protein and fibre concentrations for the seven red colobus groups were similar. Our results suggest that colobus monkeys eating diets with differing amounts of species and parts may ultimately receive similar concentrations of nutrients.     

Induced defences in the neotropical tree Bauhinia brevipes (Vog.) to herbivory: effects of damage-induced changes on leaf quality and insect attack

Induced defences to herbivory are physical, nutritional, and allelochemical traits that change in plants following damage or stress, and that reduce the performance and/or preference of herbivores. The aim of this study was to verify the occurrence and effect of induced responses in Bauhinia brevipes (Vog.) (Leguminosae) which defend it against herbivores, through the manipulation of its leaves, and their effects on herbivore foraging behaviour. We selected 15 plants in the field, and three shoots per plant were subjected to one of three treatments: (1) damaged shoots (simulation of the main types of foliar herbivory and insect exclusion); (2) damaged control shoots (insect exclusion); and (3) control shoots (not manipulated). Water and nitrogen content, tannin concentration, levels of herbivory, and shoot growth rates were compared among treatments. Leaf quality varied among treatments. Damaged leaves showed higher tannin concentration, and lower water and nitrogen content compared to undamaged leaves. On the other hand, they experienced higher rates of herbivory than leaves on control shoots. Moreover, shoots that were experimentally induced showed a higher increase in final shoot length. These results suggest that simulated herbivory on B. brevipes reduced the nutritional quality of its leaves and increased the amount of secondary compounds, therefore altering insect herbivore attack and increasing shoot performance.     

Attract and deter: a dual role for pyrrolizidine alkaloids in plant–insect interactions

Pyrrolizidine alkaloids (PAs) are the major defense compounds of plants in the Senecio genus. Here I will review the effects of PAs in Senecio on the preference and performance of specialist and generalist insect herbivores. Specialist herbivores have evolved adaptation to PAs in their host plant. They can use the alkaloids as cue to find their host plant and often they sequester PAs for their own defense against predators. Generalists, on the other hand, can be deterred by PAs. PAs can also affect survival of generalist herbivores. Usually generalist insects avoid feeding on young Senecio leaves, which contain a high concentration of alkaloids. Structurally related PAs can differ in their effects on insect herbivores, some are more toxic than others. The differences in effects of PAs on specialist and generalists could lead to opposing selection on PAs, which may maintain the genetic diversity in PA concentration and composition in Senecio species.     

Plant volatiles as method of communication

Plants emit volatile compounds that can act as a communication method to insects, neighboring plants and pathogens. Plants respond to leaf and root damage by herbivores and pathogens by emitting these compounds. The volatile compounds can deter the herbivores or pathogens directly or indirectly by attracting their natural enemies to kill them. The simultaneous damage of plants by herbivores and pathogens can influence plant defense. The induced plant volatiles can also make neighboring plants ready for defense or induce defense in parts distant from the damaged area of the same plant. Belowground root herbivory can alter the defense response to aboveground leaf herbivory. In addition, most plants normally emit volatile compounds from their flowers that directly attract foraging mutualistic insects for nectar, which in turn perform the very important function of pollination for subsequent reproduction. The volatile compounds emitted from the floral and vegetative parts of plants belong to three main classes of compounds: terpenoids, phenylpropanoids/benzenoids, and C6-aldehydes (green-leaf volatiles). The volatile phytohormones methyl salicylate and methyl jasmonate serve as important signaling molecules for communication purposes, and interact with each other to optimize the plant defense response. Here we discuss and integrate the current knowledge on all types of communication between plants and insects, neighboring plants and pathogens that are mediated through plant volatiles.     

Mechanisms of resistance to self-produced toxic secondary metabolites in plants

Plants produce a variety of secondary metabolites to protect themselves from pathogens and herbivores and/or to influence the growth of neighbouring plants. Some of these metabolites are toxic to the producing cells when their target sites are present in the producing organisms. Therefore, a specific self-resistance mechanism must exist in these plants. Self-resistance mechanisms, including extracellular excretion, vacuolar sequestration, vesicle transport, extracellular biosynthesis, and accumulation of the metabolite in a non-toxic form, have been proposed thus far. Recently, a new mechanism involving mutation of the target protein of the toxic metabolite has been elucidated. We review here the mechanisms that plants use to prevent self-toxicity from the following representative compounds: cannabinoids, flavonoids, diterpene sclareol, alkaloids, benzoxazinones, phenylpropanoids, cyanogenic glycosides, and glucosinolates.     

Cyanogenic glycosides: a case study for evolution and application of cytochromes P450

Cyanogenic glycosides are ancient biomolecules found in more than 2,650 higher plant species as well as in a few arthropod species. Cyanogenic glycosides are amino acid-derived β-glycosides of α-hydroxynitriles. In analogy to cyanogenic plants, cyanogenic arthropods may use cyanogenic glycosides as defence compounds. Many of these arthropod species have been shown to de novo synthesize cyanogenic glycosides by biochemical pathways that involve identical intermediates to those known from plants, while the ability to sequester cyanogenic glycosides appears to be restricted to Lepidopteran species. In plants, two atypical multifunctional cytochromes P450 and a soluble family 1 glycosyltransferase form a metabolon to facilitate channelling of the otherwise toxic and reactive intermediates to the end product in the pathway, the cyanogenic glycoside. The glucosinolate pathway present in Brassicales and the pathway for cyanoalk(en)yl glucoside synthesis such as rhodiocyanosides A and D in Lotus japonicus exemplify how cytochromes P450 in the course of evolution may be recruited for novel pathways. The use of metabolic engineering using cytochromes P450 involved in biosynthesis of cyanogenic glycosides allows for the generation of acyanogenic cassava plants or cyanogenic Arabidopsis thaliana plants as well as L. japonicus and A. thaliana plants with altered cyanogenic, cyanoalkenyl or glucosinolate profiles.     

Herbivory-induced signalling in plants: perception and action

Plants and herbivores have been interacting for millions of years. Over time, plants have evolved mechanisms to defend against herbivore attacks. Herbivore-challenged plants reconfigure their metabolism to produce compounds that are toxic, repellant or anti-digestive for the herbivores. Some compounds are volatile signals that attract the predators of herbivores. All these responses are tightly regulated by a signalling network triggered by the plant's perception machinery. Several compounds that specifically elicit herbivory-induced responses in plants have been isolated from herbivore oral secretions and oviposition fluids. Elicitor perception is rapidly followed by cell membrane depolarization, calcium influx and mitogen-activated protein kinase (MAPK) activation; plants also elevate the concentrations of reactive oxygen and nitrogen species, and modulate phytohormone levels accordingly. In addition to these reactions in the herbivore-attacked regions of a leaf, defence responses are also mounted in unattacked parts of the attacked leaf and as well in unattacked leaves. In this review, we summarize recent progress in understanding how plants recognize herbivory, the involvement of several important signalling pathways that mediate the responses to herbivore attack and the signals that transduce local into systemic responses.     

Age-dependent shift in response to food element composition in Collembola: contrasting effects of dietary nitrogen

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.     

Cyanogenesis in plants and arthropods

Cyanogenic glucosides are phytoanticipins known to be present in more than 2500 plant species. They are regarded as having an important role in plant defense against herbivores due to bitter taste and release of toxic hydrogen cyanide upon tissue disruption, but recent investigations demonstrate additional roles as storage compounds of reduced nitrogen and sugar that may be mobilized when demanded for use in primary metabolism. Some specialized herbivores, especially insects, preferentially feed on cyanogenic plants. Such herbivores have acquired the ability to metabolize cyanogenic glucosides or to sequester them for use in their own defense against predators. A few species of arthropods (within diplopods, chilopods and insects) are able to de novo biosynthesize cyanogenic glucosides and some are able to sequester cyanogenic glucosides from their food plant as well. This applies to larvae of Zygaena (Zygaenidae). The ratio and content of cyanogenic glucosides is tightly regulated in Zygaena filipendulae, and these compounds play several important roles in addition to defense in the life cycle of Zygaena. The transfer of a nuptial gift of cyanogenic glucosides during mating of Zygaena has been demonstrated as well as the involvement of hydrogen cyanide in male attraction and nitrogen metabolism. As more plant and arthropod species are examined, it is likely that cyanogenic glucosides are found to be more widespread than formerly thought and that cyanogenic glucosides are intricately involved in many key processes in the life cycle of plants and arthropods.