Mycorrhizal mycelium as a global carbon pool.

For more than 400 million years, mycorrhizal fungi and plants have formed partnerships that are crucial to the emergence and functioning of global ecosystems. The importance of these symbiotic fungi for plant nutrition is well established. However, the role of mycorrhizal fungi in transporting carbon into soil systems on a global scale remains under-explored. This is surprising given that ∼75% of terrestrial carbon is stored belowground and mycorrhizal fungi are stationed at a key entry point of carbon into soil food webs. Here, we analyze nearly 200 datasets to provide the first global quantitative estimates of carbon allocation from plants to the mycelium of mycorrhizal fungi. We estimate that global plant communities allocate 3.93 Gt CO2e per year to arbuscular mycorrhizal fungi, 9.07 Gt CO2e per year to ectomycorrhizal fungi, and 0.12 Gt CO2e per year to ericoid mycorrhizal fungi. Based on this estimate, 13.12 Gt of CO2e fixed by terrestrial plants is, at least temporarily, allocated to the underground mycelium of mycorrhizal fungi per year, equating to ∼36% of current annual CO2 emissions from fossil fuels. We explore the mechanisms by which mycorrhizal fungi affect soil carbon pools and identify approaches to increase our understanding of global carbon fluxes via plant-fungal pathways. Our estimates, although based on the best available evidence, are imperfect and should be interpreted with caution. Nonetheless, our estimations are conservative, and we argue that this work confirms the significant contribution made by mycorrhizal associations to global carbon dynamics. Our findings should motivate their inclusion both within global climate and carbon cycling models, and within conservation policy and practice.

The 'enigma' of Richard Schultes, Amazonian hallucinogenic plants, and the limits of ethnobotany.

This story is about the twentieth-century ethnobotanist, Richard Evans Schultes (1915-2001), and his research on hallucinogenic plants. Ethnobotany can contribute directly to science and technology studies in that the discipline makes cultural ways of knowing its scientific subject. Ethnobotanists must learn about plants through people, and are not able to conceal their interactions with indigenous informants and other ethnobotanists. I focus on an 'enigma' that Schultes presented, concerning the peculiar ability of indigenous Amazonians to distinguish between local varieties of vine that he was unable to tell apart, notably those used to prepare the hallucinogenic beverage ayahuasca. The enigma describes a complicated and irresolvable question thrown up at the uneasy intersection between different ways of knowing about the world, and shows how modern scientific travellers might navigate - or fail to navigate - the uncertain passage between them. Together with Schultes's accounts of his own non-ordinary states of consciousness elicited by ayahuasca, and his writings on the Victorian botanist Richard Spruce, I chart an epistemological gulf between Schultes's modern scientific cosmology and that of his Amazonian informants. In describing his inability to learn about the ayahuasca varieties from Amazonians, Schultes's enigma traces the very limits of the ethnobotanical discipline and reveals the fragility of the processes by which scientific naturalists might impose categories such as 'nature' and 'culture'.

Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest.

Improved understanding of the nutritional ecology of arbuscular mycorrhizal (AM) fungi is important in understanding how tropical forests maintain high productivity on low-fertility soils. Relatively little is known about how AM fungi will respond to changes in nutrient inputs in tropical forests, which hampers our ability to assess how forest productivity will be influenced by anthropogenic change. Here we assessed the influence of long-term inorganic and organic nutrient additions and nutrient depletion on AM fungi, using two adjacent experiments in a lowland tropical forest in Panama. We characterised AM fungal communities in soil and roots using 454-pyrosequencing, and quantified AM fungal abundance using microscopy and a lipid biomarker. Phosphorus and nitrogen addition reduced the abundance of AM fungi to a similar extent, but affected community composition in different ways. Nutrient depletion (removal of leaf litter) had a pronounced effect on AM fungal community composition, affecting nearly as many OTUs as phosphorus addition. The addition of nutrients in organic form (leaf litter) had little effect on any AM fungal parameter. Soil AM fungal communities responded more strongly to changes in nutrient availability than communities in roots. This suggests that the 'dual niches' of AM fungi in soil versus roots are structured to different degrees by abiotic environmental filters, and biotic filters imposed by the plant host. Our findings indicate that AM fungal communities are fine-tuned to nutrient regimes, and support future studies aiming to link AM fungal community dynamics with ecosystem function.

Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.

Mycorrhizal fungi show regular community compositions in natural ecosystems.

Dissimilarity overlap curve analysis has shown that 'universality' is a common feature in many complex microbial communities, suggesting that the same taxa interact in a similar manner when shared between communities. We present evidence that arbuscular mycorrhizal fungi, common plant root symbionts, show universal community compositions in natural ecosystems and that this pattern is conserved even at larger spatial scales. However, universality was not detected in agricultural ecosystems potentially implying that agricultural symbiont communities are formed in a different manner.

A phosphorus threshold for mycoheterotrophic plants in tropical forests.

The majority of terrestrial plants associate with arbuscular mycorrhizal (AM) fungi, which typically facilitate the uptake of limiting mineral nutrients by plants in exchange for plant carbon. However, hundreds of non-photosynthetic plant species-mycoheterotrophs-depend entirely on AM fungi for carbon as well as mineral nutrition. Mycoheterotrophs can provide insight into the operation and regulation of AM fungal relationships, but little is known about the factors, fungal or otherwise, that affect mycoheterotroph abundance and distribution. In a lowland tropical forest in Panama, we conducted the first systematic investigation into the influence of abiotic factors on the abundance and distribution of mycoheterotrophs, to ask whether the availability of nitrogen and phosphorus altered the occurrence of mycoheterotrophs and their AM fungal partners. Across a natural fertility gradient spanning the isthmus of Panama, and also in a long-term nutrient-addition experiment, mycoheterotrophs were entirely absent when soil exchangeable phosphate concentrations exceeded 2 mg P kg-1 Experimental phosphorus addition reduced the abundance of AM fungi, and also reduced the abundance of the specific AM fungal taxa required by the mycoheterotrophs, suggesting that the phosphorus sensitivity of mycoheterotrophs is underpinned by the phosphorus sensitivity of their AM fungal hosts. The soil phosphorus concentration of 2 mg P kg-1 also corresponds to a marked shift in tree community composition and soil phosphatase activity across the fertility gradient, suggesting that our findings have broad ecological significance.

Arbuscular mycorrhizal fungal community composition is altered by long-term litter removal but not litter addition in a lowland tropical forest.

Tropical forest productivity is sustained by the cycling of nutrients through decomposing organic matter. Arbuscular mycorrhizal (AM) fungi play a key role in the nutrition of tropical trees, yet there has been little experimental investigation into the role of AM fungi in nutrient cycling via decomposing organic material in tropical forests. We evaluated the responses of AM fungi in a long-term leaf litter addition and removal experiment in a tropical forest in Panama. We described AM fungal communities using 454-pyrosequencing, quantified the proportion of root length colonised by AM fungi using microscopy, and estimated AM fungal biomass using a lipid biomarker. AM fungal community composition was altered by litter removal but not litter addition. Root colonisation was substantially greater in the superficial organic layer compared with the mineral soil. Overall colonisation was lower in the litter removal treatment, which lacked an organic layer. There was no effect of litter manipulation on the concentration of the AM fungal lipid biomarker in the mineral soil. We hypothesise that reductions in organic matter brought about by litter removal may lead to AM fungi obtaining nutrients from recalcitrant organic or mineral sources in the soil, besides increasing fungal competition for progressively limited resources.

Albert Howard and the mycorrhizal association.

Albert Howard worked as an imperial agronomist for the British Government in India. Following his retirement in 1931, he returned to England and embarked on a passionate global campaign to reform agricultural practices. Central to Howard's project was the mycorrhizal association, a symbiotic relationship between plant roots and subterranean fungi, believed to play an important part in plant nutrition. I show that there are a number of close parallels between Howard's work in India and his portrayal of the mycorrhizal association, and argue that Howard used these fungi to naturalise his imperial project. Understood in this way, these mycorrhizal and imperial associations reveal ways that Howard was able to negotiate the boundaries between the local and global, England and India, science and agriculture, institute and village, and soil and plant. In contrast to Thomas Gieryn's work on hybridisation at the cultural boundaries between science and non-science, I concentrate on Howard's use of intermediaries to negotiate and articulate specific boundaries within his imperial project. Arguing that this approach reveals limitations in Gieryn's hybrid framework, I suggest that a focus on Howard's dependence on intermediaries draws attention to the discontinuities between entities, besides the dynamic ways that they might be coupled.