Duncan D. Cameron

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2

The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO2 concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon-for-nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid-Palaeozoic (1500 ppm) and near-contemporary (440 ppm) CO2 concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza-like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon-for-nutrient exchange between partners across CO2 concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild-collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO2, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.

Chapter 3 You are What You Eat: Interactions Between Root Parasitic Plants and Their Hosts

Abstract In this review we will discuss three main areas of research in plant–parasitic plant interactions. In the first section, we will deal with the physiology and biochemistry of the plant parasitic interaction, primarily focusing on the effects of resource abstraction. A functional split shall be introduced between parasites that are either predominantly xylem- or predominantly phloem feeding, and the implications of these two parasitic strategies discussed. In the second section we shall discuss the events leading up to the mature system, and the defenses employed by host plants against parasites. This section will focus on parasites’ life cycles, and on the hosts’ defense mechanisms against parasitism. Host plants and parasites are locked in a perpetual evolutionary arms race, with host plants evolving defenses, and parasites evolving counter-defense mechanisms. Significant events, such as parasite germination, and its subsequent attachment (or not) are discussed in reference to the functional groups introduced earlier. Finally, we discuss the evolution of parasitic plants and their ecological effects, from the negative effects of parasitic plants on agro-ecosystems, to their positive effects on plant biodiversity, via the suppression of dominant species, in natural and seminatural ecosystems.

Suppression of host photosynthesis by the parasitic plant Rhinanthus minor.

BACKGROUND AND AIMS Parasitism is well understood to have wide-ranging deleterious effects on host performance in species thus far characterized. Photosynthetic performance reductions have been noted in the Striga-Zea mays association; however, no such information exists for facultative hemiparasitic plants and their hosts, nor are the effects of host species understood. METHODS Chlorophyll fluorimetry was used to study the effects of parasitism by the hemiparasite Rhinanthus minor on the grass Phleum bertolinii and the forb Plantago lanceolata, and the effects of host species on the photosynthetic apparatus of R. minor. KEY RESULTS Parasitism by Rhinanthus led to a significant decrease in the host, and total (host + parasite) biomass in Phleum; however, in Plantago, no significant repression of growth was noted. Maximum quantum yield (F(v)/F(m)) was reduced in parasitized Plantago, relative to control plants, but not in Phleum. F(v)/F(m) was significantly lower in R. minor parasitizing Phleum than Plantago, suggesting Phleum to be a superior host to Plantago for R. minor. Steady-state quantum yield (Phi(PSII)) was significantly depressed in parasitized Phleum, but only at low irradiances in Plantago. Phi(PSII) was very low for R. minor grown on Plantago, but not Phleum. CONCLUSIONS Shown here is the first evidence of the suppression of host photosynthesis by a facultative hemiparasitic plant, which has significant effects on total biomass production. Host identity is a significant factor in parasite success, with the forb Plantago lanceolata exhibiting apparent chemical as well as previously identified physical defences to parasitism. It is proposed that the electron transport rate (as denoted by Phi(PSII)) represents the limiting factor for biomass accumulation in this system, and that Plantago is able to suppress the growth of Rhinanthus by suppressing the electron transport rate.

Interactions between the hemiparasitic angiospermRhinanthus minor and its hosts: From the cell to the ecosystem

Parasitic plants can significantly influence the species to which they attach. The host response is variable however, and ranges from death of the host to no detectable effects in terms of both growth and physiology. The parasite can directly influence its hosts through resource abstraction, and indirectly by influencing inter- and intra-specific interactions. Abiotic factors interact with these direct and indirect effects to moderate the potential outcome of the host parasite interaction. This paper sets out to review a series of experiments that have been undertaken in our laboratory over a number of years that examine these effects and help us to understand mechanisms underpinning the variability in host response.

Arbuscular mycorrhizal fungi as (agro)ecosystem engineers

Symbiotic interactions have been shown to facilitate shifts in the structure and function of host plant communities. For example, parasitic plants can induce changes in plant diversity through the suppression of competitive community dominants. Arbuscular mycorrhizal (AM) fungi have also be shown to induce shifts in host communities by increasing host plant nutrient uptake and growth while suppressing non-mycorrhizal species. AM fungi can therefore function as ecosystem engineers facilitating shifts in host plant communities though the presumed physiological suppression of non-contributing or non-mycorrhizal plant species. This dichotomy in plant response to AM fungi has been suggested as a tool to suppress weed species (many of which are non-mycorrhizal) in agro-ecosystems where mycorrhizal crop species are cultivated. Rinaudo et al. (2010), this issue, have demonstrated that AM fungi can suppress pernicious non-mycorrhizal weed species including Chenopodium album (fat hen) while benefiting the crop plant Helianthus annuus (sunflower). These findings now suggest a future for harnessing AM fungi as agro-ecosystem engineers representing potential alternatives to costly and environmentally damaging herbicides.

Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated Palaeozoic CO2 decline

The arbuscular mycorrhizal (AM) fungal symbiosis is widely hypothesized to have promoted the evolution of land plants from rootless gametophytes to rooted sporophytes during the mid-Palaeozoic (480-360 Myr, ago), at a time coincident with a 90% fall in the atmospheric CO(2) concentration ([CO(2)](a)). Here we show using standardized dual isotopic tracers ((14)C and (33)P) that AM symbiosis efficiency (defined as plant P gain per unit of C invested into fungi) of liverwort gametophytes declines, but increases in the sporophytes of vascular plants (ferns and angiosperms), at 440 p.p.m. compared with 1,500 p.p.m. [CO(2)](a). These contrasting responses are associated with larger AM hyphal networks, and structural advances in vascular plant water-conducting systems, promoting P transport that enhances AM efficiency at 440 p.p.m. [CO(2)](a). Our results suggest that non-vascular land plants not only faced intense competition for light, as vascular land floras grew taller in the Palaeozoic, but also markedly reduced efficiency and total capture of P as [CO(2)](a) fell.

The chlorophyll‐containing orchid Corallorhiza trifida derives little carbon through photosynthesis

While measurements of tissue stable isotope signatures and isotope mixing models have suggested that the green orchid Corallorhiza trifida is photosynthetically active and hence only partially mycoheterotrophic, these assumptions have not been validated by direct analysis of carbon assimilation. The photosynthetic capabilities of three orchid species assumed on the basis of the indirect methods or chlorophyll content to have differing trophic strategies: Neottia nidus-avis (fully mycoheterotrophic), Cephalanthera damasonium (partially autotrophic), C. trifida (partially autotrophic), as well as saplings of an autotrophic tree, Fagus sylvatica, were investigated by combining the determination of chlorophyll content and fluorescence, with direct measurement of the potential for CO(2) assimilation using (13)C isotope tracers in the field. Chlorophyll content and fluorescence values were indicative of ineffective photochemical processes in Neottia and reduced efficiency of photochemical processes in Corallorhiza. These differences are reflected in the mean assimilation rates of (13)CO(2) of 594 +/- 129, 331 +/- 72, 12.4 +/- 2.4 and 7.3 +/- 0.9 microg g(-1) h(-1) for Fagus, Cephalanthera, Corallorhiza and Neottia, respectively. Our study, while confirming the fully mycoheterotrophic status of Neottia and the partially autotrophic condition in Cephalanthera, also demonstrates under field conditions that Corallorhiza is physiologically closer to the fully mycoheterotrophic condition than has previously been recognized.

Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake

Summary Manipulation of stomatal density was investigated as a potential tool for enhancing drought tolerance or nutrient uptake. Drought tolerance and soil water retention were assessed using Arabidopsis epidermal patterning factor mutants manipulated to have increased or decreased stomatal density. Root nutrient uptake via mass flow was monitored under differing plant watering regimes using nitrogen‐15 (15N) isotope and mass spectrometry. Plants with less than half of their normal complement of stomata, and correspondingly reduced levels of transpiration, conserve soil moisture and are highly drought tolerant but show little or no reduction in shoot nitrogen concentrations especially when water availability is restricted. By contrast, plants with over twice the normal density of stomata have a greater capacity for nitrogen uptake, except when water availability is restricted. We demonstrate the possibility of producing plants with reduced transpiration which have increased drought tolerance, with little or no loss of nutrient uptake. We demonstrate that increasing transpiration can enhance nutrient uptake when water is plentiful.

Parasitic plant litter input: a novel indirect mechanism influencing plant community structure

Parasitic plants have major impacts on plant community structure through their direct negative influence on host productivity and competitive ability. However, the possibility that these parasites may also have indirect impacts on community structure (via the mechanism of nutrient-rich litter input) while long hypothesized, has remained unsupported until now. Using the hemiparasite Rhinanthus minor, we established experimental grassland mesocosms to quantify the impacts of Rhinanthus litter and parasitism across two soil fertility levels. We measured the biomass and tissue nutrient concentration of three functional groups within these communities to determine their physiological response to resource abstraction and litter input by the parasite. We show that Rhinanthus alters the biomass and nutrient status of co-occurring plants with contrasting effects on different functional groups via the mechanism of nutrient-rich litter input. Critically, in the case of grass and total community biomass, this partially negates biomass reductions caused directly by parasitism. This demonstrates that the influence of parasitic plant litter on plant community structure can be of equal importance to the much-reported direct impacts of parasitism. We must consider both positive indirect (litter) and negative direct (parasitism) impacts of parasitic plants to understand their role in structuring plant communities.