Glenn R. Iason

The response of heather (Calluna vulgaris) to shade and nutrients: predictions of the carbon-nutrient balance hypothesis

Two treatments, shade and a compound fertilizer (N, P, K, Ca, Mg) were applied in the field to heather (Calluna vulgaris) in a factorial design with two levels (presence or absence) of each treatment. Treatments were designed to mimic the changes in shade and soil nutrients occurring with incursion of birch woodland to heather moorland and were continued for two growing seasons. The resulting morphological and chemical changes to Calluna were measured, the latter to test some of the premises of the carbon-nutrient balance hypothesis. Shading resulted in etiolation of shoots, lower shoot densities and almost complete cessation of flowering. Overall lower shoot weights were due solely to reduced flowering. The concentration of total nitrogen increased whereas lignin, total phenolics and condensed tannins, all carbon-based constituents, decreased in the green shoot material with application of shade (...)

The role of plant secondary metabolites in mammalian herbivory: ecological perspectives

Plant secondary metabolites (PSM) have many ecological functions, but have long been considered as defences against pathogens or herbivores (vertebrate or invertebrate), reducing the likelihood and extent of attack. However, mammalian herbivores ingest many foods containing PSM and use both behavioural methods and physiological strategies to limit their negative effects. Most physiological counter-adaptations are inducible in response to ingested PSM, providing efficient protection against toxic effects. Possible positive effects of PSM include antioxidant and anthelminthic properties and complex formation between protein and condensed tannins that protects dietary protein from degradation by the symbiotic microflora of foregut fermenters, increasing its utilisation by the animal. This protein effect is probably only beneficial to animals under a narrow range of nutrient-rich conditions found mainly in agricultural systems. There are many examples of PSM causing food avoidance or reducing food intake, but there is as yet relatively little evidence for positive selection of them by herbivores. Although the feedback mechanisms relating the post-ingestive consequences of PSM to subsequent foraging behaviour are beginning to be understood, knowledge of the integration of behavioural and physiological strategies for regulating the effects of PSM is relatively poor. The opportunities for learned avoidance of PSM may be restricted in animals with complex diets that cannot associate a particular feedback signal with a given food type. A greater emphasis on the study of subclinical effects of PSM rather than acute effects, on pharmaco-kinetic studies in relation to behavioural studies and on the use of realistic experimental models is advocated.

The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L.

Abstract This study investigated changes in carbon-based plant secondary metabolite concentrations in the needles of Pinus sylvestris saplings, in response to long-term elevation of atmospheric CO2, at two rates of nutrient supply. Experimental trees were grown for 3 years in eight open-top chambers (OTCs), four of which were maintained at ambient (∼350 μmol mol−1) and four at elevated (700 μmol mol−1) CO2 concentrations, plus four open air control plots. Within each of these treatments, plants received either high (7.0 g N m−2 year−1 added) or low (no nutrients added) rates of nutrient supply for two years. Needles from lateral branches were analysed chemically for concentrations of condensed tannins and monoterpenes. Biochemical determinations of cellulase digestibility and protein precipitating capacity of their phenolic extracts were made because of their potential of importance in ecological interactions between pine and other organisms including herbivores and decomposers. Elevated CO2 concentration caused an increase (P<0.05) in dry mass per needle, tree height and the concentration of the monoterpene α-pinene, but there were no direct effects of CO2 concentration on any of the other chemical measurements made. High nutrient availability increased cellulase digestibility of pine needles. There was a significant negative effect of the OTCs on protein precipitating capacity of the needle extracts in comparison to the open-air controls. Results suggest that predicted changes in atmospheric CO2 concentration will be insufficient to produce large changes in the concentration of condensed tannins and monoterpenes in Scots pine. Processes which are influenced by these compounds, such as decomposition and herbivore food selection, along with their effects on ecosystem functioning, are therefore unlikely to be directly affected through changes in these secondary metabolites.

The flexibility of an intermediate feeder: dietary selection by mountain hares measured using faecal n-alkanes

Herbivores with an intermediate feeding strategy either vary their diet between a grazing (bulk roughage feeders) or browsing (concentrate selectors) strategy on a seasonal basis or select a mixed diet at any one time. The underlying ecological causes of the seasonal dietary shift in a small non-ruminant intermediate feeder – the mountain or arctic hare (Lepus timidus L.) were determined. Diet composition and selection relative to availability were investigated for 41 individual free-ranging mountain hares (of which 18 female hares were radio-collared) occupying an upland mosaic landscape in north-east Scotland. Diet composition was determined using faecal n-alkane analysis. Radio-collared hares were designated as pasture, woodland or moorland hares according to the habitat that predominated their home-range. In common with previous studies, mountain hares switched from a browse-dominated diet during winter to a Gramineae-dominated diet in summer, although it was only significant for reproductively active females during the peak breeding season. Diet composition remained consistent regardless of habitat occupied. However, the diet of radio-tracked hares differed significantly from the biomass available in the individual home-ranges; Gramineae were preferentially selected over browse species throughout the year. During winter and in particular during the early breeding season, intermediate feeders, such as mountain hares, ate browse material when the availability of higher quality was restricted. The ability to browse or graze represents a flexible foraging strategy permitting survival and production through periods of changing or unpredictable forage quality and availability.

Habitat utilization in a stratified upland landscape by two lagomorphs with different feeding strategies

Mountain hares (Lepus timidus L.) are summer grazers that switch to browse in winter, while rabbits (Oryctolagus cuniculus L.) eat mostly grasses throughout the year. These different feeding strategies may underlie seasonal patterns of habitat selection by the two species. In this study the habitat utilization by adult female mountain hares and adult female rabbits was studied by radio-tracking in a habitat composed of open moorland, upland pasture and young forestry plantation with an abundant ground flora. The selection of feeding habitats by populations of both species was assessed by faecal counts within the same landscape. Despite the common perception that mountain hares in Britain are associated with moorland, open moorland was avoided by the radio-tracked adult female mountain hares relative to its availability. Throughout the year, the radio-tracked hares preferred the forest and pasture habitats relative to availability. Only seven of the 20 hares radio-tracked were ever located on the moorland, which would suggest that the presence of moorland is not a prerequisite for the presence of mountain hares. Radio-tracked adult female rabbits utilized the habitats in proportion to their availability. Counts of faecal pellets indicated that utilization of forestry plantations by both species declined as a spruce forest matures although hare populations persist in mature pine plantations with an abundant ground flora. Mountain hares appear to be more adaptable than rabbits in their use of the habitats in this study, a behavioural tactic underpinned by their flexible feeding strategy. Rabbit populations would persist in areas following afforestation, especially where upland pastures are in close proximity to woodland and mountain hares would be capable of exploiting many of the new habitats that are created, at least in the early years of forest development.

High genetic diversity at the extreme range edge: nucleotide variation at nuclear loci in Scots pine (Pinus sylvestris L.) in Scotland

Nucleotide polymorphism at 12 nuclear loci was studied in Scots pine populations across an environmental gradient in Scotland, to evaluate the impacts of demographic history and selection on genetic diversity. At eight loci, diversity patterns were compared between Scottish and continental European populations. At these loci, a similar level of diversity (θsil=∼0.01) was found in Scottish vs mainland European populations, contrary to expectations for recent colonization, however, less rapid decay of linkage disequilibrium was observed in the former (ρ=0.0086±0.0009, ρ=0.0245±0.0022, respectively). Scottish populations also showed a deficit of rare nucleotide variants (multi-locus Tajimas D=0.316 vs D=−0.379) and differed significantly from mainland populations in allelic frequency and/or haplotype structure at several loci. Within Scotland, western populations showed slightly reduced nucleotide diversity (πtot=0.0068) compared with those from the south and east (0.0079 and 0.0083, respectively) and about three times higher recombination to diversity ratio (ρ/θ=0.71 vs 0.15 and 0.18, respectively). By comparison with results from coalescent simulations, the observed allelic frequency spectrum in the western populations was compatible with a relatively recent bottleneck (0.00175 × 4Ne generations) that reduced the population to about 2% of the present size. However, heterogeneity in the allelic frequency distribution among geographical regions in Scotland suggests that subsequent admixture of populations with different demographic histories may also have played a role.

The Energy Costs of Ingestion of Naturally Occurring Nontannin Plant Phenolics by Sheep

We examined the energetic consequences to a ruminant herbivore of ingestion and absorption of low-molecular-weight phenolics, which commonly occur in ericaceous plant species. The first experiment simulated the entrance of absorbable xenobiotics into the general circulation, as might occur if the detoxification capacity of the animal were exceeded. Orcinol was administered intravenously to six sheep for 10 d at a low rate equivalent to about 5% of the total nontannin phenolics likely to be ingested by free-ranging sheep. This led to a 5% increase in energy expenditure (P < 0.05), measured by indirect calorimetry. In a further experiment orcinol and quinol were continuously infused into the rumen of five ewes, at a rate equivalent to the likely dietary intake of nontannin phenolics. When administered via this normal oral route, within the normal physiological range, the phenolics had no detectable effect on energy expenditure but led to a reduction in the intake of digestible energy (P < 0.05) and an increase in urinary energy excretion (P < 0.01). These experiments suggest that the effectiveness of the detoxification system is crucial to permit use of toxin-containing plants by herbivores, and it should be strongly associated with their foraging strategies.

Assessment and Implications of Intraspecific and Phenological Variability in Monoterpenes of Scots Pine (Pinus sylvestris) Foliage

Scots pine populations contain individuals with widely differing amounts and composition of monoterpenes and exist as one of two chemotypes: with or without Δ3-carene. We investigated the significance for ecological studies of two types of variation in monoterpenes: (1) the inherent variability in the concentration of monoterpenes or their relative amounts in needles of seedlings, saplings, and mature trees; and (2) phenological variation in developing needles. The relative composition of needle monoterpenes in 5-year-old saplings changed during the needle development period until the final composition was reached upon needle maturity. Changes in composition depended on chemotype. Needles of the “no-Δ3-carene” chemotype had higher absolute concentrations of α-pinene, β-pinene, camphene, and total monoterpenes than “Δ3-carene” chemotype. For the “Δ3-carene” chemotype, the relative concentration of Δ3-carene during the needle growing season and immediately after emergence of seedlings was higher compared to that reached at needle maturity. Repeated removal of single needles (at weekly intervals during growth) from 5-year-old saplings did not influence the composition of monoterpenes. Within a natural Scots pine dominated woodland, 18% of mature Scots pines (N = 574) belonged to the “no-Δ3-carene” chemotype. Chemotypic variation within populations means that the statistical power with which differences in monoterpene concentrations can be detected is lower when sampling from the whole population compared to sampling within chemotypes. Reduction of this background variation and accounting for chiral variation if present, would significantly aid efficiency, interpretation, and understanding of processes in chemical and ecological research. One method for achieving this is the screening of plants for chemotypes before the establishment of experiments or field sampling regimes. We present a summary of suitable analytical methods for needle tissue that facilitates this prior screening.

Chemical composition of Calluna vulgaris (Ericaceae): do responses to fertilizer vary with phenological stage?

Abstract The effects of ammonium nitrate fertilizer on the content of total nitrogen, acid detergent fiber (ADF), lignin, total phenolics and condensed tannins of current seasons shoots of Calluna vulgaris were measured. Fertilizer applications were either (i) prior to flowering or (ii) after flowering. Samples of green shoots were collected from the pre-flowering fertilizer treatment at the onset of flowering (August) and from both treatments at the end of the growth season (November); all showed increased total nitrogen and decreased ADF, consistent with increased growth, as compared with unfertilized controls. Contrary to the predictions of the carbon-nutrient balance hypothesis, levels of total phenolics and condensed tannins did not decline significantly with fertilizer additions. However, fertilizer applied prior to flowering tended to reduce total phenolics and condensed tannins whereas fertilizer applications after flowering tended to increase them. There was a strong seasonal increase in condensed tannins and total phenolics between August and September, at the time of flowering. These results are discussed in relation to Callunas changing demand for and supply of resources at different phenological stages.

Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes

A central issue in our understanding of the evolution of the diversity of plant secondary metabolites (PSMs) is whether or not compounds are functional, conferring an advantage to the plant, or non-functional. We examine the hypothesis that the diversity of monoterpene PSMs within a plant species (Scots pine Pinus sylvestris) may be explained by different compounds acting as defences against high-impact herbivores operating at different life stages. We also hypothesize that pairwise coevolution, with uncorrelated interactions, is more likely to result in greater PSM diversity, than diffuse coevolution. We tested whether up to 13 different monoterpenes in Scots pine were inhibitory to herbivory by slugs (Arion ater), bank voles (Clethrionomys glareolus), red deer (Cervus elaphus) and capercaillie (Tetrao urogallus), each of which attack trees at a different life stage. Plants containing more α-pinene were avoided by both slugs and capercaillie, which may act as reinforcing selective agents for this dominant defensive compound. Herbivory by red deer and capercaillie were, respectively, weakly negatively associated with δ3-carene, and strongly negatively correlated with the minor compound β-ocimene. Three of the four herbivores are probably contributory selective agents on some of the terpenes, and thus maintain some, but by no means all, of the phytochemical diversity in the species. The correlated defensive function of α-pinene against slugs and capercaillie is consistent with diffuse coevolutionary processes.