Large herbivore assemblages in a changing climate: incorporating water dependence and thermoregulation.

The coexistence of different species of large herbivores (ungulates) in grasslands and savannas has fascinated ecologists for decades. However, changes in climate, land-use and trophic structure of ecosystems increasingly jeopardise the persistence of such diverse assemblages. Body size has been used successfully to explain ungulate niche differentiation with regard to food requirements and predation sensitivity. But this single trait axis insufficiently captures interspecific differences in water requirements and thermoregulatory capacity and thus sensitivity to climate change. Here, we develop a two-dimensional trait space of body size and minimum dung moisture content that characterises the combined food and water requirements of large herbivores. From this, we predict that increased spatial homogeneity in water availability in drylands reduces the number of ungulate species that will coexist. But we also predict that extreme droughts will cause the larger, water-dependent grazers as wildebeest, zebra and buffalo-dominant species in savanna ecosystems - to be replaced by smaller, less water-dependent species. Subsequently, we explore how other constraints such as predation risk and thermoregulation are connected to this two-dimensional framework. Our novel framework integrates multiple simultaneous stressors for herbivores and yields an extensive set of testable hypotheses about the expected changes in large herbivore community composition following climate change.

Benthic primary producers are key to sustain the Wadden Sea food web: stable carbon isotope analysis at landscape scale.

Coastal food webs can be supported by local benthic or pelagic primary producers and by the import of organic matter. Distinguishing between these energy sources is essential for our understanding of ecosystem functioning. However, the relative contribution of these components to the food web at the landscape scale is often unclear, as many studies lack good taxonomic and spatial resolution across large areas. Here, using stable carbon isotopes, we report on the primary carbon sources for consumers and their spatial variability across one of the world's largest intertidal ecosystems (Dutch Wadden Sea; 1460 km2 intertidal surface area), at an exceptionally high taxonomic (178 species) and spatial resolution (9,165 samples from 839 locations). The absence of overlap in δ13 C values between consumers and terrestrial organic matter suggests that benthic and pelagic producers dominate carbon input into this food web. In combination with the consistent enrichment of benthic primary producers (δ13 C -16.3‰) relative to pelagic primary producers (δ13 C -18.8) across the landscape, this allowed the use of a two-food-source isotope-mixing model. This spatially resolved modelling revealed that benthic primary producers (microphytobenthos) are the most important energy source for the majority of consumers at higher trophic levels (worms, molluscs, crustaceans, fish, and birds), and thus to the whole food web. In addition, we found large spatial heterogeneity in the δ13 C values of benthic primary producers (δ13 C -19.2 to -11.5‰) and primary consumers (δ13 C -25.5 to -9.9‰), emphasizing the need for spatially explicit sampling of benthic and pelagic primary producers in coastal ecosystems. Our findings have important implications for our understanding of the functioning of ecological networks and for the management of coastal ecosystems.

Effects of large herbivores on grassland arthropod diversity.

Both arthropods and large grazing herbivores are important components and drivers of biodiversity in grassland ecosystems, but a synthesis of how arthropod diversity is affected by large herbivores has been largely missing. To fill this gap, we conducted a literature search, which yielded 141 studies on this topic of which 24 simultaneously investigated plant and arthropod diversity. Using the data from these 24 studies, we compared the responses of plant and arthropod diversity to an increase in grazing intensity. This quantitative assessment showed no overall significant effect of increasing grazing intensity on plant diversity, while arthropod diversity was generally negatively affected. To understand these negative effects, we explored the mechanisms by which large herbivores affect arthropod communities: direct effects, changes in vegetation structure, changes in plant community composition, changes in soil conditions, and cascading effects within the arthropod interaction web. We identify three main factors determining the effects of large herbivores on arthropod diversity: (i) unintentional predation and increased disturbance, (ii) decreases in total resource abundance for arthropods (biomass) and (iii) changes in plant diversity, vegetation structure and abiotic conditions. In general, heterogeneity in vegetation structure and abiotic conditions increases at intermediate grazing intensity, but declines at both low and high grazing intensity. We conclude that large herbivores can only increase arthropod diversity if they cause an increase in (a)biotic heterogeneity, and then only if this increase is large enough to compensate for the loss of total resource abundance and the increased mortality rate. This is expected to occur only at low herbivore densities or with spatio-temporal variation in herbivore densities. As we demonstrate that arthropod diversity is often more negatively affected by grazing than plant diversity, we strongly recommend considering the specific requirements of arthropods when applying grazing management and to include arthropods in monitoring schemes. Conservation strategies aiming at maximizing heterogeneity, including regulation of herbivore densities (through human interventions or top-down control), maintenance of different types of management in close proximity and rotational grazing regimes, are the most promising options to conserve arthropod diversity.

Trait similarity patterns within grass and grasshopper communities: multitrophic community assembly at work.

Trait-based community assembly theory suggests that trait variation among co-occurring species is shaped by two main processes: abiotic filtering, important in stressful environments and promoting similarity, and competition, more important in productive environments and promoting dissimilarity. Previous studies have indeed found trait similarity to decline along productivity gradients. However, these studies have always been done on single trophic levels. Here, we investigated how interactions between trophic levels affect trait similarity patterns along environmental gradients. We propose three hypotheses for the main drivers of trait similarity patterns of plants and herbivores along environmental gradients: (1) environmental control of both, (2) bottom-up control of herbivore trait variation, and (3) top-down control of grass trait variation. To test this, we collected data on the community composition and trait variation of grasses (41 species) and grasshoppers (53 species) in 50 plots in a South African savanna. Structural equation models were used to investigate how the range and spacing of within-community functional trait values of both grasses and their insect herbivores (grasshoppers; Acrididae) respond to (1) rainfall and fire frequency gradients and (2) the trait similarity patterns of the other trophic level. The analyses revealed that traits of co-occurring grasses became more similar toward lower rainfall and higher fire frequency (environmental control), while showing little evidence for top-down control. Grasshopper trait range patterns, on the other hand, were mostly directly driven by vegetation structure and grass trait range patterns (bottom-up control), while environmental factors had mostly indirect effects via plant traits. Our study shows the potential to expand trait-based community assembly theory to include trophic interactions.

Experimental manipulation of predation risk and food quality: effect on grazing behaviour in a central-place foraging herbivore.

The relative importance of predation risk and food quality on spatial grazing pressure and activity patterns was tested in a central-place foraging herbivore: the European rabbit. Rabbits grazed less with increasing distance from their burrows into adjacent grassland, thereby creating a gradient of increasing vegetation height and plant biomass and decreasing plant nutrient concentration. When nitrogen concentration was experimentally increased by 150% through fertilizing and mowing, rabbits visited these plots four times more frequently than the untreated control plots. Addition of predator scent (mink pellets) did not result in different patch use by rabbits. The combined addition of fertilizer and mink pellets had the same effect as addition of fertilizer alone. However, the mink pellets changed the temporal activity pattern of rabbits as measured with infrared detectors. Rabbits were predominantly nocturnal but shifted their activities to the day when mink pellets were added, resulting in equal activities during night and day. We conclude that rabbits are sensitive to perceived predation risk, but that this does not influence their spatial grazing pressure. A selection for the highest food quality on the other hand can explain the observed natural rabbit grazing gradient. Food quality was highest close to the burrows, therefore rabbits selecting for high quality food should forage most intensely close to the burrows and only move further away for higher quality items or when the vegetation close to their burrows is depleted. Through intensive grazing close to the burrows rabbits facilitated for themselves either through stimulating fresh protein rich re-growth or the return of nutrients through faeces or both. This is in contrast with central-place foraging theory where intense feeding close to the burrow is assumed to lead to reduced food resources.

Impact of herbivores on nitrogen cycling: contrasting effects of small and large species.

Herbivores are reported to slow down as well as enhance nutrient cycling in grasslands. These conflicting results may be explained by differences in herbivore type. In this study we focus on herbivore body size as a factor that causes differences in herbivore effects on N cycling. We used an exclosure set-up in a floodplain grassland grazed by cattle, rabbits and common voles, where we subsequently excluded cattle and rabbits. Exclusion of cattle lead to an increase in vole numbers and a 1.5-fold increase in net annual N mineralization at similar herbivore densities (corrected to metabolic weight). Timing and height of the mineralization peak in spring was the same in all treatments, but mineralization in the vole-grazed treatment showed a peak in autumn, when mineralization had already declined under cattle grazing. This mineralization peak in autumn coincides with a peak in vole density and high levels of N input through vole faeces at a fine-scale distribution, whereas under cattle grazing only a few patches receive all N and most experience net nutrient removal. The other parameters that we measured, which include potential N mineralization rates measured under standardized laboratory conditions and soil parameters, plant biomass and plant nutrient content measured in the field, were the same for all three grazing treatments and could therefore not cause the observed difference. When cows were excluded, more litter accumulated in the vegetation. The formation of this litter layer may have added to the higher mineralization rates under vole grazing, through enhanced nutrient return through litter or through modification of microclimate. We conclude that different-sized herbivores have different effects on N cycling within the same habitat. Exclusion of large herbivores resulted in increased N annual mineralization under small herbivore grazing.

Small-scale shifting mosaics of two dominant grassland species: the possible role of soil-borne pathogens.

We analyzed the dynamics of dominant plant species in a grazed grassland over 17 years, and investigated whether local shifts in these dominant species, leading to vegetation mosaics, could be attributed to interactions between plants and soil-borne pathogens. We found that Festuca rubra and Carex arenaria locally alternated in abundance, with different sites close together behaving out of phase, resulting in a shifting mosaic. The net effect of killing all soil biota on the growth of these two species was investigated in a greenhouse experiment using gamma radiation, controlling for possible effects of sterilization on soil chemistry. Both plant species showed a strong net positive response to soil sterilization, indicating that pathogens (e.g., nematodes, pathogenic fungi) outweighed the effect of mutualists (e.g., mycorrhizae). This positive growth response towards soil sterilization appeared not be due to effects of sterilization on soil chemistry. Growth of Carex was strongly reduced by soil-borne pathogens (86% reduction relative to its growth on sterilized soil) on soil from a site where this species decreased during the last decade (and Festuca increased), while it was reduced much less (50%) on soil from a nearby site where it increased in abundance during the last decade. Similarly, Festuca was reduced more (67%) on soil from the site where it decreased (and Carex increased) than on soil from the site where it increased (55%, the site where Carex decreased). Plant-feeding nematodes showed high small-scale variation in densities, and we related this variation to the observed growth reductions in both plant species. Carex growth on unsterilized soil was significantly more reduced at higher densities of plant-feeding nematodes, while the growth reduction in Festuca was independent of plant-feeding nematode densities. At high plant-feeding nematode densities, growth of Carex was reduced more than Festuca, while at low nematode densities the opposite was found. Each plant species thus seems to be affected by different (groups of) soil-borne pathogens. The resulting interaction web of plants and soil-borne pathogens is discussed. We hypothesize that soil disturbances by digging ants and rabbits may explain the small-scale variation in nematode densities, by locally providing "fresh" sand. We conclude that soil-borne pathogens may contribute to plant diversity and spatial mosaics of plants in grasslands.

Spatial scaling laws yield a synthetic theory of biodiversity.

Ecologists still search for common principles that predict well-known responses of biological diversity to different factors. Such factors include the number of available niches in space, productivity, area, species' body size and habitat fragmentation. Here we show that all these patterns can arise from simple constraints on how organisms acquire resources in space. We use spatial scaling laws to describe how species of different sizes find food in patches of varying size and resource concentration. We then derive a mathematical rule for the minimum similarity in size of species that share these resources. This packing rule yields a theory of species diversity that predicts relations between diversity and productivity more effectively than previous models. Size and diversity patterns for locally coexisting East African grazing mammals and North American savanna plants strongly support these predictions. The theory also predicts relations between diversity and area and between diversity and habitat fragmentation. Thus, spatial scaling laws provide potentially unifying first principles that may explain many important patterns of species diversity.

Effects of herbivores on grassland plant diversity.

The role of herbivores in controlling plant species richness is a critical issue in the conservation and management of grassland biodiversity. Numerous field experiments in grassland plant communities show that herbivores often, but not always, increase plant diversity. Recent work suggests that the mechanisms of these effects involve alteration of local colonization of species from regional species pools or local extinction of species, and recent syntheses and models suggest that herbivore effects on plant diversity should vary across environmental gradients of soil fertility and precipitation.

Within-population variability in morphology and life history of Plantago major L. ssp. pleiosperma Pilger in relation to environmental heterogeneity.

An attempt was made to relate variation in life-history characteristics within a population of Plantago major ssp. pleiosperma to small-scale environmental variability. At a beach plain, embanked in 1966, a mosaic environment was distinguished with spatial variability in vegetation structure as well as in nutrient availability and water content of the soil. Differences between three subsites in comtemporary selection were demonstrated, e.g. in shoot morphology and allocation to reproductive tissue. The effects of nutrient supply and waterlogging on morphology and life history were studied on lines from the three subsites in a greenhouse. For most of the traits high levels of phenotypic plasticity were observed, covering almost entirely the observed phenotypic variability at the beach plain. In all treatments lines from the shrubs had, however, a higher leaf-area ratio as well as delayed flowering when compared to lines from more open subsites. In addition, in a reciprocal transplant experiment it was demonstrated that lines from the shrubs had larger shoots with e.g. broader leaves in the shady environment of the shrubs than other lines.From the experiments no indications were obtained that lines from any subsite were especially adapted to specific levels of nutrient supply or water content of the soil. With respect to these environmental factors P. major ssp. pleisoperma might occur and reproduce at all subsites by means of phenotypic plasticity, e.g. in plant form. However, it is suggested that spatial variability in vegetation structure caused a population subdivision in allocation patterns, leaf form and life history at the beach plain, over distances of about 15-25 m. This differentation occurred during primary succession over a period of twenty years.