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Science | 2014

Global diversity and geography of soil fungi

Leho Tedersoo; Mohammad Bahram; Sergei Põlme; Urmas Kõljalg; Nourou S. Yorou; R.L.C. Wijesundera; Luis Villarreal Ruiz; Aída M. Vasco-Palacios; Pham Q uang Thu; Ave Suija; Matthew E. Smith; Cathy Sharp; Erki Saluveer; Alessandro Saitta; Miguel Rosas; Taavi Riit; Da Ratkowsky; Karin Pritsch; Kadri Põldmaa; Meike Piepenbring; Cherdchai Phosri; Marko Peterson; Kaarin Parts; Kadri Pärtel; Eveli Otsing; Eduardo Nouhra; André Ledoux Njouonkou; R. Henrik Nilsson; Luis N. Morgado; Jordan Mayor

Introduction The kingdom Fungi is one of the most diverse groups of organisms on Earth, and they are integral ecosystem agents that govern soil carbon cycling, plant nutrition, and pathology. Fungi are widely distributed in all terrestrial ecosystems, but the distribution of species, phyla, and functional groups has been poorly documented. On the basis of 365 global soil samples from natural ecosystems, we determined the main drivers and biogeographic patterns of fungal diversity and community composition. Direct and indirect effects of climatic and edaphic variables on plant and fungal richness. Line thickness corresponds to the relative strength of the relationships between the variables that affect species richness. Dashed lines indicate negative relationships. MAP, mean annual precipitation; Fire, time since last fire; Dist. equator, distance from the equator; Ca, soil calcium concentration; P, soil phosphorus concentration; pH, soil pH. Rationale We identified soil-inhabiting fungi using 454 Life Sciences (Branford, CN) pyrosequencing and through comparison against taxonomically and functionally annotated sequence databases. Multiple regression models were used to disentangle the roles of climatic, spatial, edaphic, and floristic parameters on fungal diversity and community composition. Structural equation models were used to determine the direct and indirect effects of climate on fungal diversity, soil chemistry, and vegetation. We also examined whether fungal biogeographic patterns matched paradigms derived from plants and animals—namely, that species’ latitudinal ranges increase toward the poles (Rapoport’s rule) and diversity increases toward the equator. Last, we sought group-specific global biogeographic links among major biogeographic regions and biomes using a network approach and area-based clustering. Results Metabarcoding analysis of global soils revealed fungal richness estimates approaching the number of species recorded to date. Distance from equator and mean annual precipitation had the strongest effects on richness of fungi, including most fungal taxonomic and functional groups. Diversity of most fungal groups peaked in tropical ecosystems, but ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal ecosystems, and many fungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus). Consistent with Rapoport’s rule, the geographic range of fungal taxa increased toward the poles. Fungal endemicity was particularly strong in tropical regions, but multiple fungal taxa had cosmopolitan distribution. Conclusions Climatic factors, followed by edaphic and spatial patterning, are the best predictors of soil fungal richness and community composition at the global scale. Richness of all fungi and functional groups is causally unrelated to plant diversity, with the exception of ectomycorrhizal root symbionts, suggesting that plant-soil feedbacks do not influence the diversity of soil fungi at the global scale. The plant-to-fungi richness ratio declined exponentially toward the poles, indicating that current predictions—assuming globally constant ratios—overestimate fungal richness by 1.5- to 2.5-fold. Fungi follow similar biogeographic patterns as plants and animals, with the exception of several major taxonomic and functional groups that run counter to overall patterns. Strong biogeographic links among distant continents reflect relatively efficient long-distance dispersal compared with macro-organisms. Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework. Global metagenomics detects hotspots of fungal diversity and macroecological patterns and indicates that plant and fungal diversity are uncoupled. [Also see Perspective by Wardle and Lindahl] Assessing fungal diversity worldwide Fungi are hyperdiverse but poorly known, despite their ecological and economic impacts. Tedersoo et al. collected nearly 15,000 topsoil samples from 365 sites worldwide and sequenced their genomes (see the Perspective by Wardle and Lindahl). Overall, they found a striking decline in fungal species richness with distance from the equator. For some specialist groups though, diversity depended more on the abundance of host plants than host diversity or geography. The findings reveal a huge gap between known and described species and the actual numbers of distinct fungi in the worlds soils. Science, this issue 10.1126/science.1256688; see also p. 1052


Proceedings of the National Academy of Sciences of the United States of America | 2015

An estimate of the number of tropical tree species

J. W. Ferry Slik; Víctor Arroyo-Rodríguez; Shin-ichiro Aiba; Patricia Alvarez-Loayza; Luciana F. Alves; Peter S. Ashton; Patricia Balvanera; Meredith L. Bastian; Peter J. Bellingham; Eduardo van den Berg; Luís Carlos Bernacci; Polyanna da Conceição Bispo; Lilian Blanc; Katrin Böhning-Gaese; Pascal Boeckx; Frans Bongers; Brad Boyle; M. Bradford; Francis Q. Brearley; Mireille Breuer-Ndoundou; Sarayudh Bunyavejchewin; Darley Calderado; Leal Matos; Miguel Castillo-Santiago; Eduardo Luís Martins Catharino; Shauna-Lee Chai; Yukai Chen; Eizi Suzuki; Natália Targhetta; Duncan W. Thomas

Significance People are fascinated by the amazing diversity of tropical forests and will be surprised to learn that robust estimates of the number of tropical tree species are lacking. We show that there are at least 40,000, but possibly more than 53,000, tree species in the tropics, in contrast to only 124 across temperate Europe. Almost all tropical tree species are restricted to their respective continents, and the Indo-Pacific region appears to be as species-rich as tropical America, with each of these two regions being almost five times as rich in tree species as African tropical forests. Our study shows that most tree species are extremely rare, meaning that they may be under serious risk of extinction at current deforestation rates. The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher’s alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼40,000 and ∼53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼19,000–25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼4,500–6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.


Proceedings of the National Academy of Sciences of the United States of America | 2011

Soils on exposed Sunda Shelf shaped biogeographic patterns in the equatorial forests of Southeast Asia

J. W. Ferry Slik; Shin-ichiro Aiba; Meredith L. Bastian; Francis Q. Brearley; Charles H. Cannon; Karl A. O. Eichhorn; Gabriella Fredriksson; Kuswata Kartawinata; Yves Laumonier; Asyraf Mansor; Antti Marjokorpi; Erik Meijaard; Robert J. Morley; Hidetoshi Nagamasu; Reuben Nilus; Eddy Nurtjahya; John A. Payne; Andrea Permana; Axel Dalberg Poulsen; Niels Raes; Soedarsono Riswan; Carel P. van Schaik; Douglas Sheil; Kade Sidiyasa; Eizi Suzuki; Johan L. C. H. van Valkenburg; Campbell O. Webb; Serge A. Wich; Tsuyoshi Yoneda; Rahmad Zakaria

The marked biogeographic difference between western (Malay Peninsula and Sumatra) and eastern (Borneo) Sundaland is surprising given the long time that these areas have formed a single landmass. A dispersal barrier in the form of a dry savanna corridor during glacial maxima has been proposed to explain this disparity. However, the short duration of these dry savanna conditions make it an unlikely sole cause for the biogeographic pattern. An additional explanation might be related to the coarse sandy soils of central Sundaland. To test these two nonexclusive hypotheses, we performed a floristic cluster analysis based on 111 tree inventories from Peninsular Malaysia, Sumatra, and Borneo. We then identified the indicator genera for clusters that crossed the central Sundaland biogeographic boundary and those that did not cross and tested whether drought and coarse-soil tolerance of the indicator genera differed between them. We found 11 terminal floristic clusters, 10 occurring in Borneo, 5 in Sumatra, and 3 in Peninsular Malaysia. Indicator taxa of clusters that occurred across Sundaland had significantly higher coarse-soil tolerance than did those from clusters that occurred east or west of central Sundaland. For drought tolerance, no such pattern was detected. These results strongly suggest that exposed sandy sea-bed soils acted as a dispersal barrier in central Sundaland. However, we could not confirm the presence of a savanna corridor. This finding makes it clear that proposed biogeographic explanations for plant and animal distributions within Sundaland, including possible migration routes for early humans, need to be reevaluated.


PLOS ONE | 2011

Forest Fruit Production Is Higher on Sumatra Than on Borneo

Serge A. Wich; Erin R. Vogel; Michael D. Larsen; Gabriella Fredriksson; Mark Leighton; Carey P. Yeager; Francis Q. Brearley; Carel P. van Schaik; Andrew J. Marshall

Background Various studies have shown that the population densities of a number of forest vertebrates, such as orangutans, are higher on Sumatra than Borneo, and that several species exhibit smaller body sizes on Borneo than Sumatra and mainland Southeast Asia. It has been suggested that differences in forest fruit productivity between the islands can explain these patterns. Here we present a large-scale comparison of forest fruit production between the islands to test this hypothesis. Methodology/Principal Findings Data on fruit production were collated from Sumatran and Bornean sites. At six sites we assessed fruit production in three forest types: riverine, peat swamp and dryland forests. We compared fruit production using time-series models during different periods of overall fruit production and in different tree size classes. We examined overall island differences and differences specifically for fruiting period and tree size class. The results of these analyses indicate that overall the Sumatran forests are more productive than those on Borneo. This difference remains when each of the three forest types (dryland, riverine, and peat) are examined separately. The difference also holds over most tree sizes and fruiting periods. Conclusions/Significance Our results provide strong support for the hypothesis that forest fruit productivity is higher on Sumatra than Borneo. This difference is most likely the result of the overall younger and more volcanic soils on Sumatra than Borneo. These results contribute to our understanding of the determinants of faunal density and the evolution of body size on both islands.


Bioscience Education | 2012

Providing Students with Formative Audio Feedback

Francis Q. Brearley; W. Rod Cullen

Abstract The provision of timely and constructive feedback is increasingly challenging for busy academics. Ensuring effective student engagement with feedback is equally difficult. Increasingly, studies have explored provision of audio recorded feedback to enhance effectiveness and engagement with feedback. Few, if any, of these focus on purely formative audio feedback on draft submissions of written assignments. This study encouraged a cohort of 40 students to submit drafts of written assignments, two weeks before formal submission, in order to receive audio recorded feedback. Nearly half the cohort either did not submit drafts or submitted only brief outlines. The level of draft completeness impacted on the characteristics of the lecturer’s feedback. While students receiving audio feedback gained significantly higher marks for finished work, this cannot be directly attributed to receipt/use of feedback as analysis suggests generally more able students are more likely to submit more complete drafts, which leads us to ask the question, are we simply helping better students to perform even better? Audio feedback was reported as clear, engaging and helpful; however, timing of feedback (before formal submission) may be of greater importance in terms of impact on attainment than the audio format. We suggest a model that focuses efforts on formative feedback (in advance of formal submission) and selective provision of summative feedback (targeted feed forward).


Journal of Tropical Ecology | 2011

Below-ground secondary succession in tropical forests of Borneo

Francis Q. Brearley

As the destruction and severe disturbance of primary tropical forest continues, it is important to understand how these forests may recover from perturbations. Considerable work has been done on above-ground recovery but below-ground processes are less well understood. To determine changes in root mass during tropical secondary succession in lowland forests of Central Borneo, samples were taken from stands of increasing ages since abandonment of agriculture (1, 3, 14 and 31 y) with a primary forest control (six plots from 1-y-old stands and three from all other ages). Root mass and elemental concentrations were determined and soils were chemically analysed. There was no increase in root mass with stand age for fine-root (< 2 mm diameter) or small-root (< 5 mm diameter) mass but there was a trend for coarse-root mass (5-10 mm diameter) to increase with stand age. Negative correlations were shown between root mass and soil nutrient status. Fine-root C concentrations increased with stand age but there was no clear effect of stand age on fine-root N or P. Fine-root mass did not increase significantly with stand age suggesting a rapid recovery; instead, soil nutrient status appeared to be the most important factor controlling root mass. Of the soil nutrients measured in this study, N had a stronger control over root mass than P suggesting that this element may be limiting during secondary succession in tropical lowland forests of Borneo.


Plant and Soil | 2013

Nitrogen stable isotopes indicate differences in nitrogen cycling between two contrasting Jamaican montane forests

Francis Q. Brearley

Background and aimsThe aim of this study is to enhance our knowledge of nitrogen (N) cycling and N acquisition in tropical montane forests through analysis of stable N isotopes (δ15N).MethodsLeaves from eight common tree species, leaf litter, soils from three depths and roots were sampled from two contrasting montane forest types in Jamaica (mull ridge and mor ridge) and were analysed for δ15N.ResultsAll foliar δ15N values were negative and varied among the tree species but were significantly more negative in the mor ridge forest (by about 2 ‰). δ15N of soils and roots were also more negative in mor ridge forests by about 3 ‰. Foliar δ15N values were closer to that of soil ammonium than soil nitrate suggesting that trees in these forests may have a preference for ammonium; this may explain the high losses of nitrate from similar tropical montane forests. There was no correlation between the rankings of foliar δ15N in the two forest types suggesting a changing uptake ratio of different N forms between forest types.ConclusionsThese results indicate that N is found at low concentrations in this ecosystem and that there is a tighter N cycle in the mor ridge forest, confirmed by reduced nitrogen availability and lower rates of nitrification. Overall, soil or root δ15N values are more useful in assessing ecosystem N cycling patterns as different tree species showed differences in foliar δ15N between the two forest types.


Biodiversity and Conservation | 2012

Tropical fungal diversity: closing the gap between species estimates and species discovery

M. Catherine Aime; Francis Q. Brearley

The collection of papers in this special issue examines the nature of some of the ecosystemand environmental interactions involving fungi in the tropics and the biodiversity of certainof these tropical fungal guilds in an effort to provide improved estimates to answer thequestion of just how much undescribed tropical fungal diversity remains to be discovered.Fungi are ubiquitously found in all tropical environments where they are essential forecosystem processes. For example, in interactions with plants, fungi facilitate nutrientuptake (as mycorrhizas), provide protection against phytopathogens (as endophytes,phylloplane constituents or mycoparasites), breakdown and recycle the nutrients otherwiselocked in cell wall compounds (as wood and litter decomposers), and act as agents ofdisease. They cover a broad range of life-forms and life-histories from microscopic yeaststo those having large and conspicuous sporocarps or genets covering many hectares.Tropical regions are incredibly species rich, harbouring the majority of terrestrial biodi-versity as well as a broad variety of often unusual interactions between species. Yet despiteincreasing interest, our understanding of the mycobiota and its roles in tropical ecosystemsis woefully incomplete.The question of how many fungal species there are is indisputably important. Currentestimates of these numbers range from 611,000 (Mora et al. 2011) to nearly ten million(Cannon 1997). However, Hawksworth’s (1991) estimate of 1.5 million species remains,for most, the benchmark. One of the several caveats of the Hawksworth (1991) study wasthe dearth of information with regard to fungal biodiversity within tropical ecosystems and


Microbial Ecology | 2015

Habitat Fragmentation can Modulate Drought Effects on the Plant-soil-microbial System in Mediterranean Holm Oak (Quercus ilex) Forests

Dulce Flores-Rentería; Jorge Curiel Yuste; Ana Rincón; Francis Q. Brearley; Juan Carlos García-Gil; Fernando Valladares

Ecological transformations derived from habitat fragmentation have led to increased threats to above-ground biodiversity. However, the impacts of forest fragmentation on soils and their microbial communities are not well understood. We examined the effects of contrasting fragment sizes on the structure and functioning of soil microbial communities from holm oak forest patches in two bioclimatically different regions of Spain. We used a microcosm approach to simulate the annual summer drought cycle and first autumn rainfall (rewetting), evaluating the functional response of a plant-soil-microbial system. Forest fragment size had a significant effect on physicochemical characteristics and microbial functioning of soils, although the diversity and structure of microbial communities were not affected. The response of our plant-soil-microbial systems to drought was strongly modulated by the bioclimatic conditions and the fragment size from where the soils were obtained. Decreasing fragment size modulated the effects of drought by improving local environmental conditions with higher water and nutrient availability. However, this modulation was stronger for plant-soil-microbial systems built with soils from the northern region (colder and wetter) than for those built with soils from the southern region (warmer and drier) suggesting that the responsiveness of the soil-plant-microbial system to habitat fragmentation was strongly dependent on both the physicochemical characteristics of soils and the historical adaptation of soil microbial communities to specific bioclimatic conditions. This interaction challenges our understanding of future global change scenarios in Mediterranean ecosystems involving drier conditions and increased frequency of forest fragmentation.


Plant and Soil | 2016

Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana

Francis Q. Brearley; David R. Elliott; Amaia Iribar; Robin Sen

AimsWe aimed to characterise the arbuscular mycorrhizal fungal (AMF) community structure and potential edaphic determinants in the dominating, but poorly described, root-colonizing Paris-type AMF community on co-occurring Amazonian leguminous trees.MethodsThree highly productive leguminous trees (Dicorynia guianensis, Eperua falcata and Tachigali melinonii were targeted) in species-rich forests on contrasting soil types at the Nouragues Research Station in central French Guiana. Abundant AMF SSU rRNA amplicons (NS31-AM1 & AML1-AML2 primers) from roots identified via trnL profiling were subjected to denaturing gradient gel electrophoresis (DGGE), clone library sequencing and phylogenetic analysis.ResultsClassical approaches targeting abundant SSU amplicons highlighted a diverse root-colonizing symbiotic AMF community dominated by members of the Glomeraceae. DGGE profiling indicated that, of the edaphic factors investigated, soil nitrogen was most important in influencing the AMF community and this was more important than any host tree species effect.ConclusionsDominating Paris-type mycorrhizal leguminous trees in Amazonian soils host diverse and novel taxa within the Glomeraceae that appear under edaphic selection in the investigated tropical forests. Linking symbiotic diversity of identified AMF taxa to ecological processes is the next challenge ahead.

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Serge A. Wich

Liverpool John Moores University

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