Grassland biodiversity bounces back from long-term nitrogen addition.

The negative effect of increasing atmospheric nitrogen (N) pollution on grassland biodiversity is now incontrovertible. However, the recent introduction of cleaner technologies in the UK has led to reductions in the emissions of nitrogen oxides, with concomitant decreases in N deposition. The degree to which grassland biodiversity can be expected to 'bounce back' in response to these improvements in air quality is uncertain, with a suggestion that long-term chronic N addition may lead to an alternative low biodiversity state. Here we present evidence from the 160-year-old Park Grass Experiment at Rothamsted Research, UK, that shows a positive response of biodiversity to reducing N addition from either atmospheric pollution or fertilizers. The proportion of legumes, species richness and diversity increased across the experiment between 1991 and 2012 as both wet and dry N deposition declined. Plots that stopped receiving inorganic N fertilizer in 1989 recovered much of the diversity that had been lost, especially if limed. There was no evidence that chronic N addition has resulted in an alternative low biodiversity state on the Park Grass plots, except where there has been extreme acidification, although it is likely that the recovery of plant communities has been facilitated by the twice-yearly mowing and removal of biomass. This may also explain why a comparable response of plant communities to reduced N inputs has yet to be observed in the wider landscape.

Estimating the functional form for the density dependence from life history data.

Two contrasting approaches to the analysis of population dynamics are currently popular: demographic approaches where the associations between demographic rates and statistics summarizing the population dynamics are identified; and time series approaches where the associations between population dynamics, population density, and environmental covariates are investigated. In this paper, we develop an approach to combine these methods and apply it to detailed data from Soay sheep (Ovis aries). We examine how density dependence and climate contribute to fluctuations in population size via age- and sex-specific demographic rates, and how fluctuations in demographic structure influence population dynamics. Density dependence contributes most, followed by climatic variation, age structure fluctuations and interactions between density and climate. We then simplify the density-dependent, stochastic, age-structured demographic model and derive a new phenomenological time series which captures the dynamics better than previously selected functions. The simple method we develop has potential to provide substantial insight into the relative contributions of population and individual-level processes to the dynamics of populations in stochastic environments.

Spatial heterogeneity and plant species richness at different spatial scales under rabbit grazing.

Herbivores influence spatial heterogeneity in soil resources and vegetation in ecosystems. Despite increasing recognition that spatial heterogeneity can drive species richness at different spatial scales, few studies have quantified the effect of grazing on spatial heterogeneity and species richness simultaneously. Here we document both these variables in a rabbit-grazed grassland. We measured mean values and spatial patterns of grazing intensity, rabbit droppings, plant height, plant biomass, soil water content, ammonia and nitrate in sites grazed by rabbits and in matched, ungrazed exclosures in a grassland in southern England. Plant species richness was recorded at spatial scales ranging between 0.0001 and 150 m(2). Grazing reduced plant height and plant biomass but increased levels of ammonia and nitrate in the soil. Spatial statistics revealed that rabbit-grazed sites consisted of a mixture of heavily grazed patches with low vegetation and nutrient-rich soils (lawns) surrounded by patches of high vegetation with nutrient-poor soils (tussocks). The mean patch size (range) in the grazed controls was 2.1 +/- 0.3 m for vegetation height, 3.8 +/- 1.8 m for soil water content and 2.8 +/- 0.9 m for ammonia. This is in line with the patch sizes of grazing (2.4 +/- 0.5 m) and dropping deposition (3.7 +/- 0.6 m) by rabbits. In contrast, patchiness in the ungrazed exclosures had a larger patch size and was not present for all variables. Rabbit grazing increased plant species richness at all spatial scales. Species richness was negatively correlated with plant height, but positively correlated to the coefficient of variation of plant height at all plot sizes. Species richness in large plots (<25 m(2)) was also correlated to patch size. This study indicates that the abundance of strong competitors and the nutrient availability in the soil, as well as the heterogeneity and spatial pattern of these factors may influence species richness, but the importance of these factors can differ across spatial scales.

Contrasting effects of rabbit exclusion on nutrient availability and primary production in grasslands at different time scales.

Herbivores influence nutrient cycling and primary production in terrestrial plant communities. However, both empirical and theoretical studies have indicated that the mechanisms by which herbivores influence nutrient availability, and thus their net effects on primary production, might differ between time scales. For a grassland in southeast England, we show that the effects of rabbits on primary production change over time in a set of grazed plots paired with exclosures ranging from 0 to 14 years in age. Herbivore exclusion decreased net aboveground primary production (APP) in the short term, but increased APP in the long term. APP was closely correlated with N mineralization rates in both grazed and ungrazed treatments, and accumulation of litter within the grazing exclosures led to higher N mineralization rates in exclosures in the long run. Rabbit grazing did not influence litter quality. The low contrast in palatability between species and the presence of grazing-tolerant plants might prevent rabbits from favoring unpalatable plant species that decompose slowly, in contrast to results from other ecosystems. Our results indicate that it is essential to understand the effects on N cycling in order to predict the effect of rabbit grazing on APP. Rabbits might decrease N mineralization and APP in the long term by increasing losses of N from grasslands.

Determinants of species richness in the Park Grass Experiment.

The Park Grass Experiment at Rothamsted in southeast England was started in 1856, making it the longest-running experiment in plant ecology anywhere in the world. Experimental inputs include a range of fertilizers (nitrogen, phosphorus, potassium, and organic manures) applied annually, with lime applied occasionally, and these have led to an increase in biomass and, where nitrogen was applied in the form of ammonium sulfate, to substantial decreases in soil pH. The number of species per plot varies from three to 44 per 200 m(2), affording a unique opportunity to study the determinants of plant species richness and to estimate the effect sizes attributable to different factors. The response of species richness to biomass depends on the amount and type of nitrogen applied; richness declined monotonically with increasing biomass on plots receiving no nitrogen or receiving nitrogen in the form of sodium nitrate, but there was no relationship between species richness and biomass on plots acidified by ammonium sulfate application. The response to lime also depended on the type of nitrogen applied; there was no relationship between lime treatment and species richness, except in plots receiving nitrogen in the form of ammonium sulfate, where species richness increased sharply with increasing soil pH. The addition of phosphorus reduced species richness, and application of potassium along with phosphorus reduced species richness further, but the biggest negative effects were when nitrogen and phosphorus were applied together. The analysis demonstrates how multiple factors contribute to the observed diversity patterns and how environmental regulation of species pools can operate at the same spatial and temporal scale as biomass effects.

Contrasting dynamics in the same plant-herbivore interaction.

Long-term studies of two-species interactions under field conditions are unusual; most long-term field studies are of single species dynamics (1-6). Concurrent long-term studies on the dynamics of the same two interacting species in different locations are very rare. This result has led to the tacit assumption that different cases of the same two-species interaction would involve essentially quantitative differences (e.g., context-specific differences in the numeric values of demographic parameters like fecundity or death rates). Here, we show that for one of the best-known two-species systems (ragwort and cinnabar moth), this finding does not hold. The interaction between the plant and its herbivore is fundamentally different in coastal dunes in The Netherlands and in grasslands in Southeast England. In the first case, the dynamics are cyclic and the interaction involves both direct and delayed density dependence; in the second case, the insect has little impact on plant dynamics and there are no time lags in density dependence. The difference is caused by differences in the importance of seed-limitation in plant recruitment in the two locations.

Age, sex, density, winter weather, and population crashes in Soay sheep.

Quantifying the impact of density, extrinsic climatic fluctuations, and demography on population fluctuations is a persistent challenge in ecology. We analyzed the effect of these processes on the irregular pattern of population crashes of Soay sheep on the St. Kilda archipelago, United Kingdom. Because the age and sex structure of the population fluctuates independently of population size, and because animals of different age and sex respond in different ways to density and weather, identical weather conditions can result in different dynamics in populations of equal size. In addition, the strength of density-dependent processes is a function of the distribution of weather events. Incorporating demographic heterogeneities into population models can influence dynamics and their response to climate change.

Scale dependence in plant biodiversity.

The relationship between the number of species and the area sampled is one of the oldest and best-documented patterns in community ecology. Several theoretical models and field data from a wide range of plant and animal taxa suggest that the slope, z, of a graph of the logarithm of species richness against the logarithm of area is roughly constant, with z approximately 0.25. We collected replicated and randomized plant data at 11 spatial scales from 0.01 to 10(8) square meters in Great Britain which show that the slope of the log-log plot is not constant, but varies systematically with spatial scale, and from habitat to habitat at the same spatial scale. Values of z were low (0.1 to 0.2) at small scales (<100 square meters), high (0.4 to 0.5) at intermediate scales (1 hectare to 10 square kilometers), and low again (0.1 to 0.2) for the largest scale transitions (e.g., East Berks to all of Berkshire). Instead of one process determining changes in species richness across a wide range of scales, different processes might determine plant biodiversity at different spatial scales.

Quantitative webs as a means of assessing the impact of alien insects.

1. We use quantitative linkage webs to investigate the impact of alien gall wasps on community structure. Britain has been invaded by four alien species of cynipid gallwasp, Andricus corruptrix, A. lignicola, A. kollari and A. quercuscalicis, over the last 150 years. To date, Britain can be divided into four zones from the north to the south with one, two, three and four invading species established in each zone. 2. The four species are naturalized in their new ranges and are locally the most abundant cynipid species, especially in their spring (sexual) generations. Like the native cynipid species they showed dramatic changes (up to three orders of magnitude) in density between generations, and the dominance structure of alien and native host species changed radically from generation to generation. 3. All four invading cynipid species were attacked by native parasitoid species. Using quantified linkage webs, we assess the contribution made by individual host gall species to each parasitoids population size. Although the parasitoid species have been described as broadly polyphagous, suggesting that the aliens should be richly linked with the native cynipid communities, we found that the galls of the invading species have become the main, and in a few cases the sole, contributors to local parasitoid populations, indicating major host shifts by the parasitoid species. 4. Within generations we found very little overlap among the parasitoid and inquiline communities associated with native and alien galls within generations. Similarly, the quantification of indirect interactions among cynipids between generations suggests that parasitoids and inquilines are not main factors in the dynamics of local cynipid communities. The recruitment of parasitoids and inquilines by the invading cynipid species is therefore unlikely to have a strong affect on native cynipid species.

Rodent seed predation and seedling recruitment in mesic grassland.

Seedling recruitment of two grasses (Arrhenatherum elatius and Festuca rubra) and two herbs (Centaurea nigra and Rumex acetosa) was measured in areas with and without rodents to which seeds of each species were sown at three seed densities (1000, 10,000 and 50,000 seeds m-2) in two seasons (spring and autumn 1995). Seed removal was measured for 10-day periods and the fate of seedlings was followed for 15 months after sowing. The proportion of seed removed ranged from 6 to 85% and increased with increasing seed density for each species. Rodents had no effect on seedling emergence or survival in the spring sowing. In the autumn sowing, rodents reduced seedling emergence of all four species sown at 1000 and 10,000 seeds m-2 but had no impact at 50,000 seeds m-2, presumably because of microsite limitation. We suggest the difference between spring and autumn arose because emergence was seed limited in autumn but microsite limited in spring; microsite availability was higher in autumn because a summer drought killed plants, reduced plant biomass and opened up the sward. Fifteen months after the autumn sowing, fewer A. elatius and C. nigra seedlings survived on plots exposed to rodents. This result reflected not only the reduced seedling emergence but also increased seedling mortality (seedling herbivory) in sites exposed to rodents. In contrast, F. rubra and R.acteosa showed density-dependent seedling survival which compensated for initial differences in seedling emergence, so that no effect of rodents remained after 15 months. The results suggest that rodent seed predation and seedling herbivory exert strong effects on seedling recruitment of A.elatius and C. nigra when recruitment conditions are favourable (conditions that lead to high microsite availability) and may contribute to both species being maintained at low densities in the grassland. The results also demonstrate that highly significant impacts of rodent seed predation at the seedling emergence stage can disappear by the time of plant maturation.

Top-down versus bottom-up and the Ruritanian bean bug.

In a recent article, Hunter uses the late George Varley and George Gradwell's long-term data on the winter moth (Operophtera brumata) and green tortrix (Tortrix viridana) populations to propose a method of quantifying the relative importance of top-down effects (because of natural enemies) and bottom-up effects (because of resource competition) in influencing population dynamics. We believe this approach is deeply flawed. Using Varley and Gradwell's winter moth study, we show that the problems with Hunter's analysis lie in his misinterpretation of the population dynamics and his inappropriate use of statistical techniques. We also emphasize the importance of distinguishing clearly between two quite different things: firstly, top-down and bottom-up regulation of populations and secondly, the much simpler task of categorizing factors affecting changes in population density as either top-down or bottom-up processes.

Burial and seed survival in Brassica napus subsp. oleifera and Sinapis arvensis including a comparison of transgenic and non-transgenic lines of the crop.

The creation of transgenic plants through genetic engineering has focused interest on how the fitness of a plant species may be altered by small changes in its genome. This study concentrates on a key component of fitness: persistence of seeds overwinter. Seeds of three lines of oilseed rape (Brassica napus subsp. oleifera DC Metzger) and of charlock (Sinapis arvensis L.) were buried in nylon mesh bags at two depths in four habitats in each of three geographically separated sites: Cornwall, Berkshire and Sutherland. Seeds were recovered after 12 and 24 months. Charlock exhibited much greater seed survival (average 60% surviving the first year and 32.5% surviving the second year) than oilseed rape (1.5% surviving the first year and 0.2% surviving the second) at all sites. Charlock showed higher survival at 15 cm burial than 2 cm burial at certain sites, but oilseed rape showed no depth effect. Different genetic lines of oilseed rape displayed different rates of seed survival; non-transgenic rape showed greater survival (2%) than the two transgenic lines, one developed for tolerance to the antibiotic kanamycin (0.3%) and one for tolerance to both kanamycin and the herbicide glufosinate (0.25%). The absolute and relative performances of the different genetic lines of oilseed rape were context specific, illustrating the need to test hypotheses in a wide range of ecological settings.

Herbivores and plant diversity.

We study spatial lottery models of competition between two plant species in which competitive ability is affected by levels of herbivory. Herbivory may enhance plant diversity in two qualitatively different ways. The first is global frequency dependence; the level of herbivory suffered by a plant decreases as the species becomes rare. Second, spatial variability in levels of herbivory can create ephemeral, local refuges for herbivory for each plant species. Both of these mechanisms operate only if there is not a negative correlation between a plant's palatability and its competitive ability. Both mechanisms also require that herbivores have sufficiently strong diet preferences (or, equivalently, that the plants have sufficiently different grazing tolerances). If there is no relationship between palatability and competitive ability, then plant diversity is a monotonically increasing function of the herbivore's degree of monophagy. In contrast, if there is a positive correlation between palatability and competitive ability, then the diversity/degree-of-monophagy relationship may be either monotonically increasing or humped.

A comparative evaluation of models of cinnabar moth dynamics.

1. A complex model of cinnabar moth dynamics proposed by Dempster and Lakhani (1979) with 23 parameters is reduced to a single equation with five parameters, and the behaviour of the reduced model shown to explain most features of the full model. 2. The efficiency of the full model is compared with the reduced model and with two even simpler models (the two parameter discrete logistic and a four parameter model based on a step-function for mortality) in their abilities to describe time series data of cinnabar moth population densities from Weeting Heath. Models with more parameters were not significantly better than few-parameter models in describing population trajectories. 3. Models that included a driving variable (in this case observed rainfall data) were no better at describing the data than simpler models without driving variables. It appears, therefore, that the routine inclusion of driving variables may be counterproductive, unless there is compelling empirical or theoretical evidence of their importance and the mode of action of the driving variables can be modelled mechanistically. For example, the regression model used to describe the relationship between rainfall and plant biomass in Dempster and Lakhani (1979), breaks down if rainfall is assumed to be constant, because there is no explicit model for the regulation of plant biomass. 4. The parameter values of the cinnabar-ragwort interaction suggest that cinnabar moth dynamics may be chaotic. Whether or not field data exhibit chaos or environmental stochasticity (or a mixture of both) is impossible to determine from inspection of time series data on population density. There is an urgent need for experimental and theoretical protocols to disentangle these two sources of population fluctuation.

The effects of host plant defoliation and fertilizer application on larval growth and oviposition behaviour in cinnabar moth.

Defoliated ragwort plants produced regrowth foliage that was higher in alkaloid, but lower in amino acid concentrations than primary foliage. Total N was not affected. 2) Plants fertilized with nitrogen (as ammonium sulphate) had lower amino acid concentrations than unfertilized control plants, slightly increased alkaloid levels but similar total N concentrations. 3) Ovipositing females laid eggs upon plants with equal probability for controls, regrowth and fertilized foliage (one rosette in 5 received an egg batch). However, the probability of receiving eggs was significantly lower on the primary leaves of 'cut-back' plants that had had their lower leaves removed a few days before egg laying (only one rosette in 13 was selected). 4) Egg batch size was higher on fertilized control foliage than on other treatments. 5) Larvae attained greater final weights when fed a diet of regrowth foliage, despite the higher levels of alkaloid they contained. Larval development rate was not affected by experimental treatment of the foliage. 6) Larval growth was lowest on the leaves of fertilized plants. This was associated with significant reductions in the concentrations of three amino acids (methionine down 29%, tyrosine 33% and lysine 25%).

Benevolent herbivores?

Two questions dominate current thinking on plant-herbivore interactions: what is the impact of feeding by herbivores on the distribution and abundance of plants; and what is the role of herbivory as an agency of natural selection, leading to differential performance of host plant genotypes? These two questions come together in discussions of how the evolutionary consequences of herbivory are manifest at the population and ecosystem levels.