We are studying the multitrophic interactions which affect the diversity of plant communities. The research focuses on the interactions between organisms from more than two trophic levels, in natural, semi-natural and managed plant assemblages. In particular, we are interested in how non-pathogenic fungi in plants affect the insect herbivores which also feed on those plants. The two categories of fungi under investigation are root-inhabiting arbuscular mycorrhizas (AM fungi) and foliar endophytes. Natural plant communities include those regenerating from seedbanks on abandoned land such as that which has been taken out of agricultural production under the set-aside scheme. Semi-natural communities include areas where mixtures of wildflower seeds have been sown, in order to recreate species-rich meadowlands. Managed communities involve golf courses, and the production of high-quality turfgrass.

		This strange looking fungus is Helvella crispa. It is an example of a species that has shown dramatic changes in its fruiting season over the last 50 years. Ted Gange (father of Alan) has collected over 55,000 records of fungi fruiting in the New Forest over the last 55 years. These records have been analysed and published in Science . The abstract to this paper can be found here [link] and full text of the article can be found here [full text link].

The length of the autumnal fungal fruiting season has more than doubled in the last 50 y in the UK. Species that used to start fruiting in September now do so in July or August. The end of the season has got later. It used to be in October, now it is December. These events have been caused by elevated temperature in July (makes them start earlier) and in October (no frosts anymore, so autumn stays warmer for longer). Many species now fruit twice a year. Species that used to fruit only in October now do so also in April. The reason is that as spring has got warmer, the fungus body in the soil has become active in February (Feb. used to be too cold for this to happen, so the fungi remained dormant). Activity in February means the fungus acquires sufficient nutrients to enable it fruit a month or two later.

Russula ochroleuca is the commonest fungus in our database. It too shows an extension of its autumnal fruiting season. However, what's really interesting is that this species shows fruiting extensions when growing beneath deciduous trees, but not when with coniferous trees. It's mycorrhizal with both and its fruiting must be linked to tree physiology - deciduous trees are showing a response to climate change by retaining their leaves for longer, but conifers are not showing such a response

Biologists measure these changes in appearance of organisms in a season in days per decade. The rate we calculated is higher than that for all previous reports - the latter include birds, fish, mammals and plants. Thus it seems that fungi are the most sensitive organisms on the planet to changes in climate. Furthermore, it is unheard of for an organism to start reproducing twice a year instead of once, in two opposing seasons (e.g. birds nest in the spring and even though climate has got warmer, they have not started to nest in autumn as well).

We are looking for other long-term data sets on fungal fruiting that we can compare with our data. If you know of such data please contact Alan at the e-mail address above.

We have found that the presence of arbuscular mycorrhizal (AM) fungi in plant root systems can change the biochemical and architectural features of plants. We are interested in the consequences of these changes for insects which are associated with the foliar and subterranean parts of plants. With root-feeding insects, fungal colonisation can reduce the growth rate and survival of insects such as the Black Vine weevil, Otiorhynchus sulcatus, and Garden Chafer, Phyllopertha horticola. If we can identify the resistance features concerned, then we may be able to manipulate plants so that they are resistant to root-feeding pests. A collaborative project with the Institute of Grassland and Environmental Research (IGER) and the Macaulay Land Use Research Institute (MLURI) has studied how root-feeding insects interact with AM fungi in the NERC Soil Biodiversity Thematic Programme (see http://www.mluri.sari.ac.uk/~at5032/Pages/Index.html for the team's web site). With foliar-feeding insects, the position is a little more complicated. It appears that those insects which have a wide diet range (generalists) are either unaffected or negatively affected by the presence of the fungi, while those which are host specific are positively affected. We believe the mechanism is concerned with an alteration of the carbon/nitrogen ratio, which determines the allocation to defence compounds in a plant. Generalist insects are affected by elevated plant defence levels, while specialists often sequester these chemicals and need them in their diets.

We have been studying these interactions from an evolutionary viewpoint and have examined the entire British flora, to see if there are general patterns between the degree of occurrence of AM fungi in plant families and the insect herbivore loads associated with those families. We have found that plant families with high mycorrhizal incidence have higher numbers of phytophagous insects associated with them than do families which contain few mycorrhizal species (Figure 1).

In addition, high mycorrhizal incidence is associated with insect assemblages with lower proportions of chewers and higher proportions of sucking insects. As most sucking insects are specialists, we believe that AM fungal occurrence may have contributed to the evolution of insect specialism.

If the growth and population dynamics of foliar-feeding insect can be affected by AM fungi, then it is also possible that these changes may be detectable in higher trophic levels, such as the parasitoids of herbivores. A recent grant from the NERC has investigated this question and we have found that some mycorrhizal fungi can increase parasitism, while others can decrease it (Figure 2). We think that these effects are mediated through mycorrhizal effects on plant size, rather than chemistry.

There has been a great deal of work with endophytic fungi in grasses and their interactions with insect herbivores. However, much less is known about endophytes in herbs and trees and their interactions with insects and other fungi. We started out using two model systems, namely Rhododendron ponticum, an introduced shrub, and Cirsium arvense (Creeping thistle), a pernicious weed, and have developed our research now to include other important host plants. We have found that insect herbivores appear to stimulate endophyte growth in the leaves of R. ponticum, while in thistle, the presence of endophytes may be one reason for the failure of thistle gall flies to colonise the majority of plants in any field situation. This finding may have important consequences for the biological control of this plant in certain parts of the world.

The diversity of endophytes within these plants is staggering. So far, we have found 64 different species within Rhododendron and 58 within Cirsium and that is just in the above-ground tissues! The most common foliar endophyte species in Cirsium are Cladosporium cladosporioides, Chaetomium cochliodes, and Alternaria alternata. Several other species isolated have not previously been recorded from live tissues or from the UK! Further details on our endophyte research can be found on our Endophyte Research Page.

We are studying the role of AM fungi and insects in the establishment of wildflower meadow mixtures, suitable for sandy soils in the U.K. We are applying fungicide to the soil in an attempt to reduce AM fungal colonisation of roots.

We have found that AM fungi were significantly reduced by the chemical application, but none of the pathogens occurring in the site were affected. In the first establishment year of the meadow, few plant species were mycorrhizal. However, the competitive dominants Anthemis arvensis and Chrysanthemum segetum did form the association. Reducing AM levels resulted in reduced growth of these two species, meaning that more of the weaker competitors were able to coexist. Therefore, in this situation, the presence of mycorrhizal fungi served to reduce plant species richness. This is in direct contrast to our previous work on early plant succession at Imperial College, Silwood Park. In the Silwood sites, mycorrhizal fungi promoted species richness, because the competitive dominants were not mycorrhizal, but the rarer species were.

A major problem with the majority of golf greens in the U.K. is the presence of Annual Meadow Grass (Poa annua) as a weed species and the accompanying loss of bent grass (Agrostis species). Annual Meadow Grass (AMG) is a problem because it provides an uneven putting surface, is less resistant to drought than bentgrass and is attacked by a wide range of fungal pathogens. This means that large amounts of fungicide are applied to golf greens and we need to find ways of biologically reducing AMG abundance and hence fungicide application. We have performed microbial (bacteria and AM fungi) surveys of golf green soil and have found that levels of these organisms are often extremely low indeed. In addition, we have found that the abundance of AM fungi is positively related to the abundance of the desirable grasses and negatively related to that of AMG. Therefore, we are studying ways of increasing AM fungal levels in turfgrass, in order to provide a biological method for the production of high-quality, disease-resistant grass. It is prohibitively expensive to apply AM inoculum directly to greens, but we believe that an indirect way may be to apply biostimulant products, many of which are becoming available. It is known that the abundance of AM fungi may be increased by increasing levels of soil bacteria. Therefore, we are studying the application of these compounds to greens on a number of courses, in order to see if we can biologically reduce AMG abundance and make the greens more pest and disease resistant. This work could have applications to golf courses all over the world, and we have recently extended it to football pitches, where we are working with a number of Premier League clubs.

We believe that overall, golf courses are beneficial to the environment. They tie up large areas of land in a relatively stable, undisturbed condition for many years, and therefore act as potentially important reservoirs for rare species. We are studying the role that courses play in the conservation of two endangered habitats in the U.K., namely heathland and calcareous grassland. We have produced guidelines for the management of heather on golf courses and aim to extend these studies to document the role of courses in the conservation of rare plant and animal species. The successful management of the natural habitats on a course can help in a greater integration of the game with the environment, and more effective, integrated and disease control.

Our interests in subterranean insects and conservation are brought together in this project which is seeking to describe the biology and ecology of the stag beetle, Lucanus cervus. This is Britain's largest beetle and a recent survey shows it to be very much a south-eastern insect in the UK. Furthermore, it appears to be a denizen of urban areas, with the majority of records from gardens. This is curous, given that the larvae feed on subterranean, decaying wood. We know surprisingly little about its basic biology and this gap in our knowledge needs to be filled if we are to effectively conserve the species. Over the next seven years, we will attempt to determine things such as food preference, larval growth rates, sex ratios, adult food, clutch size and growth rates. We are developing a web site for this project which can be found at http://www.stagbeetlehelpline.co.uk

Green roofs may be planted with Sedum matting (Figs. 3 & 4) or fitted with a substrate that is allowed to colonise naturally (Fig. 5). These roofs could provide new habitats in areas which are currently lacking wildlife habitats, could act as wildlife corridors or stepping stones, linking existing habitats, could facilitate movement and dispersal of wildlife and be refuges for rare and declining species. In large cities such as London, green roofs can provide refuges for brownfield flora and fauna and help to meet UK and London Biodiversity targets.

Figure 3. Sedum matting planted on the roof of a building in Canary Wharf

 

Figure 4. Sedum in flower

 

Figure 5. Natural roof colonisation

We are studying the insect diversity of these roofs across London. For further details on living roofs in Britain, contact http://www.livingroofs.org

The project is particularly appropriate for Royal Holloway as our new hall of residence is the first in Britain to have a living roof

Figure 6. Laying and planting the green roof at Royal Holloway

We have experiments on the roof of London Zoo gift shop (Figure 7) and Canary Wharf (Figure 8)

Figure 7. Experimental roof at London Zoo

 

Figure 8. Experimental roof at Canary Wharf

Why are we so interested in these roofs? It is because the diversity of rare invertebrates is astonishing - the roofs provide unsual habitats, similar in conditions to Mediterranean areas. It seems that species that might be at their thermal limits at ground level can find a home in the arid, warm conditions on a roof. The numbers of notable species are remarkably high:

Figure 9. Total number of rare insects found on green roofs in 2003     

Gange, A.C., Gange, E.G., Sparks, T.H. & Boddy, L. (2007). Rapid and recent changes in fungal fruiting patterns. Science 316, 71-71 [Abstract] [Full text]

Omacini, M., Eggers, T., Bonkowski, M., Gange, A.C. & Jones, T.H. (2006). Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Functional Ecology 20, 226-232

Currie, A.F., Murray, P.J. & Gange, A.C. (2006). Root herbivory by Tipula paludosa larvae increases colonization of Agrostis capillaris by arbuscular mycorrhizal fungi. Soil Biology & Biochemistry 38, 1994-1997

Murray, P.J., Cook, R., Currie, A.F., Dawson, L.A., Gange, A.C., Grayston, S.J. & Treonis, A.M. (2006). Interactions between fertilizer addition, plants and the soil environment: implications for soil faunal structure and diversity. Applied Soil Ecology 33, 199-207

Manning, P, Newington, J.N., Robson, H.R., Saunders, M.A., Eggers, T., Bradford, M.A, Bardgett, R.D., Bonkowski, M., Ellis, R.J. Gange, A.C., Grayston, S.J., Kandeler, E, Marhan, S., Reid, E., Tscherko, D., Godfray, H.C.J. & Rees, M. (2006). Decoupling the direct and indirect effects of nitrogen deposition on ecosystem function. Ecology Letters 9, 1015-1024

Harvey, D.J. & Gange, A.C. (2006). Size variation and mating success in the stag beetle, Lucanus cervus L. Physiological Entomology 31, 218-226

Ayres, R.L., Gange, A.C. & Aplin, D.M. (2006). Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size and size inequality of Plantago lanceolata L. Journal of Ecology 94: 285-294 [article on-line]

Gange AC, Smith AK (2005) Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecological Entomology 30: 600-606 [article on-line]

Gange AC, Gane DRJ, Chen YL, Gong MQ (2005) Dual colonization of Eucalyptus urophylla ST Blake by arbuscular and ectomycorrhizal fungi affects levels of insect herbivore attack. Agricultural and Forest Entomology 7: 253-263 [article on-line]

Gange AC, Brown VK, Aplin DM (2005) Ecological specificity of arbuscular mycorrhizae: evidence from foliar- and seed-feeding insects. Ecology 86: 603-611 [Full text 104 KB]

Tanner RA, Gange AC (2005) Effects of golf courses on local biodiversity. Landscape and Urban Planning 71: 137-146

Bary F, Gange AC, Crane M, Hagley KJ (2005) Fungicide levels and arbuscular mycorrhizal fungi in golf putting greens. Journal of Applied Ecology 42: 171-180 [article on-line]

Gange AC, Brown VK & Aplin DM (2003). Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecology Letters 6: 1051-1055 [article on-line]

Dawson LA, Grayston SJ, Murray PJ, Cook R, Gange AC, Ross JM, Pratt SM, Duff EI & Treonis A (2003). Influence of pasture management (nitrogen and lime addition and insecticide treatment) on soil organisms and pasture root system dynamics in the field. Plant and Soil, 255: 121-130 [article on-line]

Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setala H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298: 615-618.

Gange AC, Bower E, Brown VK (2002) Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia 131: 103-112

Gange AC, Brown VK (2002) Soil food web components affect plant community structure during early succession. Ecol. Res. 17: 217-227. [Full text 108 KB]

Gange AC, Stagg PG, Ward LK (2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol. Lett. 5: 11-15. [Full text 96 KB]

Gange AC, Brown VK (2001) All mycorrhizas are not equal. Trends Ecol. Evol. 16: 671-672. [Full text 45 KB]

Gange AC (2001) Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol. 150: 611-618.

Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol. Evol. 15: 369-372. [ Full text 140 KB]

Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant 'benefit'. Oikos 87: 615-621

Gange AC, Lindsay DE, Ellis LS (1999) Can arbuscular mycorrhizal fungi be used to control the undesirable grass Poa annua on golf courses? J. Appl. Ecol. 36: 909-919

Gange AC, Bower E, Brown VK (1999) Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia 120: 123-131

Gange AC, Bower E, Stagg PG, Aplin DM, Gillam AE, Bracken M (1999) A comparison of visualization techniques for recording arbuscular mycorrhizal colonization. New Phytol. 142: 123-132

Wu WP, Sutton BC, Gange AC (1998) Pseudophragmotrichum cubense gen. et sp. nov. on culms of Oncidium lucidum from Cuba. Mycol. Res. 102: 179-183

Wu WP, Sutton BC, Gange AC (1997) Notes on three fungicolous fungi: Anastomyces microsporus gen. et sp. nov., Idriella rhododendri sp. nov. and Infundibura adhaerens. Mycol. Res. 101: 1318-1322.

Gange AC, Nice HE (1997) Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization. New Phytol. 137: 335-343.

Wu W, Sutton BC, Gange AC (1996) Revision of Septoria species on Hebe and Veronica and description of Kirramyces hebes sp nov. Mycol. Res. 100: 1207-1217.

Wu WP, Sutton BC, Gange AC (1996) Coleophoma fusiformis sp nov from leaves of Rhododendron, with notes on the genus Coleophoma. Mycol. Res. 100: 943-947.

Gange AC (1996) Positive effects of endophyte infection on sycamore aphids. Oikos 75: 500-510.

Wu WP, Sutton BC, Gange AC (1996) Dactylaria endophytica sp nov, an endophyte from leaves of Prunus lusitanica. Mycol. Res. 100: 524-526.