I am a plant biologist with a strong interest in the field of plant ecophysiology. I have a passion for understanding the unique and novel strategies with which plants are able to survive in harsh environments and how this knowledge can be applied to improving current/future agricultural practices and in maintaining the natural environment around us.
In my current research project at the University of Western Australia (UWA) I am investigating the links between nitrogen uptake restraint and improved phosphorus-use efficiency in a range of species native to south-western Australia. My previous research project was based in Japan (Japan International Research Center for Agricultural Sciences) and was focused on understanding phosphorus-use efficiency in rice and how it could be optimised through a greater understanding of the physiological mechanisms involved and their genetic links. My earlier, PhD research at UWA involved using cryoSEM and X-ray microanalysis, as well as glasshouse experiments and field studies to investigate the role of calcium enhanced phosphorus toxicity in explaining the absence of most Proteaceae from calcareous habitats. My Honours research at UWA was similar to my current project and was centred on understanding plant nutrient-use efficiency and nutrient acquisition strategies in species from severely P-impoverished environments.
I currently hold a Research Associate position at the University of Western Australia, where my research is funded through an Australia Research Council (ARC) Discovery Project titled "Plant nitrate restraint: Does constraining nitrate influx systems accompany high leaf phosphorus-use efficiency in a phosphorus-impoverished ecosystem?" (CI: E/Prof Hans Lambers and Assoc/Prof Patrick Finnegan). In 2018 I was awarded a 2-year postdoctoral fellowship through the Japanese Society for the Promotion of Science (JSPS), where I joined the internationally renowned group of Dr Matthias Wissuwa at the Japan International Research Center for Agricultural Sciences in Tsukuba City, Japan. I completed my undergraduate, Honours (sups: Assoc/Prof Etienne Laliberté & E/Prof Hans Lambers) and PhD (sups: E/Prof Hans Lambers & Assoc/Prof Peta Clode) at the University of Western Australia.
Key Skills and Expertise
Plant Nutrient-Use Efficiency
Long-Term Ecosystem Development
Cell-Level Nutrient Allocation
Plant Nutrient Analysis
Plant Phosphorus Fractionation
Leaf Gas Exchange
Data Analysis (R and others)
Scanning Electron Microscopy
Energy Dispersive Spectroscopy
The plant family Proteaceae is exceptionally diverse and our recent paper in Plant and Soil explores why this is
Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus-impoverished landscapes
Hayes P.E.*, Nge F.J.*, Cramer M.D., Finnegan P.M., Fu P., Hopper S.D., Oliveira R.S., Turner B.L., Zemunik G., Zhong H., Lambers H. (2021) Plant and Soil https://doi.org/10.1007/s11104-021-04886-0
An insightful Commentary on this article was also written by Mark Westoby and Daniel Falster
The conservative low-phosphorus niche in Proteaceae
Three exciting new papers out in August!!
Leaf manganese concentrations as a tool to assess belowground plant functioning in phosphorus-impoverished environments (Plant and Soil)Lambers H., Wright I.J., Guilherme Pereira C., Bellingham P.J., Bentley L.P., Boonman A., Cernusak L.A., Foulds W., Gleason S.M., Gray E.F., Hayes P.E., Kooyman R.M., Malhi Y., Richardson S.J., Shane M.W., Staudinger C., Stock W.D., Swarts N.D., Turner B.L., Turner J., Veneklaas E.J., Wasaki J., Westoby M., Xu Y.
First cryo-scanning electron microscopy images and X-ray microanalysis of mucoromycotinian fine root endophytes in vascular plants (Frontiers in Microbiology)Albornoz F.E., Hayes P.E., Orchard S., Clode P.L., Nazeri N., Standish R.J., Dickie I.A., Bending G.D., Hilton S., Ryan M.H. https://doi.org/10.3389/fmicb.2020.02018
The influence of soil age on ecosystem structure and function across biomes (Nature Communications)Delgado-Baquerizo M., Reich P.B., Bardgett R.D., Eldridge D.J., Lambers H., Wardle D.A., Reed S.C., Plaza C., Png G.K., Sigrid N., Berhe A.A., Hart S.C., Hu H.-W., He J.-Z., Bastida F., Abades S., Alfaro F.D., Cutler N.A., Gallardo A., García-Velázquez L., Hayes P.E., Hseu Z.-Y., Pérez C.A., Santos F., Siebe C., Trivedi P., Sullivan B.W., Weber-Grullon L., Williams M.A., Fierer N. https://doi.org/10.1038/s41467-020-18451-3
New Postdoctoral Research Associate position at the University of Western Australia
I have now begun my second postdoctoral position. A three year Research Associate position on an Australian Research Council (ARC) funded Discovery Project at the University of Western Australia. The project is titled "Plant nitrate restraint: Does constraining nitrate influx systems accompany high leaf phosphorus-use efficiency in a phosphorus-impoverished ecosystem?", and will be led by E/Prof Hans Lambers and Assoc/Prof Patrick Finnegan. I am very excited to be involved in this project and am looking forward to the new discoveries we will be sure to make.
Hakea neurophylla - Jurien Bay, WA
Nature Ecology & Evolution article: Multiple elements of soil biodiversity drive ecosystem functions across biomes
Delgado-Baquerizo, M., Reich, P.B., Trivedi, C., Eldridge, D.J., Abades, S., Alfaro, F.D., Bastida, F., Berhe, A.A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., He, J.-Z., Hseu, Z.-Y., Hu, H.-W., Kirchmair, M., Neuhauser, S., Pérez, C.A., Reed, S.C., Santos, F., Sullivan, B.W., Trivedi, P., Wang, J.-T., Weber-Grullon, L., Williams, M.A., Singh, B.K., 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution 4: 210–220 (https://doi.org/10.1038/s41559-019-1084-y) Link to free view
The role of soil biodiversity in regulating multiple ecosystem functions is poorly understood, limiting our ability to predict how soil biodiversity loss might affect human wellbeing and ecosystem sustainability. Here, combining a global observational study with an experimental microcosm study, we provide evidence that soil biodiversity (bacteria, fungi, protists and invertebrates) is significantly and positively associated with multiple ecosystem functions. These functions include nutrient cycling, decomposition, plant production, and reduced potential for pathogenicity and belowground biological warfare. Our findings also reveal the context dependency of such relationships and the importance of the connectedness, biodiversity and nature of the globally distributed dominant phylotypes within the soil network in maintaining multiple functions. Moreover, our results suggest that the positive association between plant diversity and multifunctionality across biomes is indirectly driven by soil biodiversity. Together, our results provide insights into the importance of soil biodiversity for maintaining soil functionality locally and across biomes, as well as providing strong support for the inclusion of soil biodiversity in conservation and management programmes.
New Phytologist article is now 'ISI Highly Cited'
I am extremely pleased to report that our article published earlier this year in New Phytologist has received enough citations to place it in the top 1% of the academic field of Plant & Animal Sciences.
This study reports on the role of Ca-enhanced P toxicity in explaining the distribution of Proteaceae species, providing a novel mechanism for the calcifuge habit of most Proteaceae, and possibly for other calcifuge species. This knowledge is critical in management of this iconic and ecologically important plant family, the Proteaceae, which contribute significantly to Australia's biodiversity, particularly south-western Australia, a global biodiversity hotspot.
Presented at Microscopy and Microanalysis 2019: Analysing cell-level allocation of calcium and phosphorus in leaves of Proteaceae from south-western Australia
Hayes, P.E., Clode, P.L., Pereira, C.G., Lambers, H., 2019. Analysing Cell-Level Allocation of Calcium and Phosphorus in Leaves of Proteaceae from South-Western Australia. Microscopy and Microanalysis 25: 1080–1081 (https://doi.org/10.1017/S1431927619006135)
Nature Communications article: Global ecological predictors of the soil priming effect
Bastida, F., García, C., Fierer, N., Eldridge, D.J., Bowker, M.A., Abades, S., Alfaro, F.D., Asefaw Berhe, A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., Hernández, T., Hseu, Z.-Y., Jehmlich, N., Kirchmair, M., Lambers, H., Neuhauser, S., Peña-Ramírez, V.M., Pérez, C.A., Reed, S.C., Santos, F., Siebe, C., Sullivan, B.W., Trivedi, P., Vera, A., Williams, M.A., Luis Moreno, J., Delgado-Baquerizo, M., 2019. Global ecological predictors of the soil priming effect. Nature Communications 10: 3481 (https://doi.org/10.1038/s41467-019-11472-7)
Identifying the global drivers of soil priming is essential to understanding C cycling in terrestrial ecosystems. We conducted a survey of soils across 86 globally-distributed locations, spanning a wide range of climates, biotic communities, and soil conditions, and evaluated the apparent soil priming effect using 13C-glucose labeling. Here we show that the magnitude of the positive apparent priming effect (increase in CO2 release through accelerated microbial biomass turnover) was negatively associated with SOC content and microbial respiration rates. Our statistical modeling suggests that apparent priming effects tend to be negative in more mesic sites associated with higher SOC contents. In contrast, a single-input of labile C causes positive apparent priming effects in more arid locations with low SOC contents. Our results provide solid evidence that SOC content plays a critical role in regulating apparent priming effects, with important implications for the improvement of C cycling models under global change scenarios.
PNAS article: Changes in belowground biodiversity during ecosystem development
Delgado-Baquerizo, M., Bardgett, R.D., Vitousek, P.M., Maestre, F.T., Williams, M.A., Eldridge, D.J., Lambers, H., Neuhauser, S., Gallardo, A., García-Velázquez, L., Sala, O.E., Abades, S.R., Alfaro, F.D., Berhe, A.A., Bowker, M.A., Currier, C.M., Cutler, N.A., Hart, S.C., Hayes, P.E., Hseu, Z.-Y., Kirchmair, M., Peña-Ramírez, V.M., Pérez, C.A., Reed, S.C., Santos, F., Siebe, C., Sullivan, B.W., Weber-Grullon, L., Fierer, N. 2019. Changes in belowground biodiversity during ecosystem development. Proceedings of the National Academy of Sciences 116: 6891–6896 (https://doi.org/10.1073/pnas.1818400116)
Belowground organisms play critical roles in maintaining multiple ecosystem processes, including plant productivity, decomposition, and nutrient cycling. Despite their importance, however, we have a limited understanding of how and why belowground biodiversity (bacteria, fungi, protists, and invertebrates) may change as soils develop over centuries to millennia (pedogenesis). Moreover, it is unclear whether belowground biodiversity changes during pedogenesis are similar to the patterns observed for aboveground plant diversity. Here we evaluated the roles of resource availability, nutrient stoichiometry, and soil abiotic factors in driving belowground biodiversity across 16 soil chronosequences (from centuries to millennia) spanning a wide range of globally distributed ecosystem types. Changes in belowground biodiversity during pedogenesis followed two main patterns. In lower-productivity ecosystems (i.e., drier and colder), increases in belowground biodiversity tracked increases in plant cover. In more productive ecosystems (i.e., wetter and warmer), increased acidification during pedogenesis was associated with declines in belowground biodiversity. Changes in the diversity of bacteria, fungi, protists, and invertebrates with pedogenesis were strongly and positively correlated worldwide, highlighting that belowground biodiversity shares similar ecological drivers as soils and ecosystems develop. In general, temporal changes in aboveground plant diversity and belowground biodiversity were not correlated, challenging the common perception that belowground biodiversity should follow similar patterns to those of plant diversity during ecosystem development. Taken together, our findings provide evidence that ecological patterns in belowground biodiversity are predictable across major globally distributed ecosystem types and suggest that shifts in plant cover and soil acidification during ecosystem development are associated with changes in belowground biodiversity over centuries to millennia.
Research article published in the European Journal of Soil Science
Turner, B.L., Hayes, P.E., Laliberté, E., 2018. A climosequence of chronosequences in southwestern Australia. European Journal of Soil Science 69, 69–85.
To examine how climate affects soil development and nutrient availability over long timescales, we studied a series of four long-term chronosequences along a climate gradient in southwestern Australia. Annual rainfall ranged from 533 to 1185mm (water balance from −900 to +52 mm) and each chronosequence included Holocene (≤6.5 ka), Middle Pleistocene (120–500 ka) and Early Pleistocene (∼2000 ka) dunes. Vegetation changed markedly along the climosequence, from shrubland at the driest site to Eucalyptus forest at the wettest. Soil pH was similar in the youngest soil of each chronosequence, although the carbonate and P contents of the parent sand declined from dry to wet along the climosequence, presumably linked to variation in offshore productivity. Despite this, soil development and associated nutrient status followed remarkably consistent patterns along the four chronosequences. Pedogenesis involved decalcification and secondary carbonate precipitation in Holocene soils and leaching of iron oxides fromMiddle Pleistocene soils, leading ultimately to bleached quartz sands in the oldest soils. Along all chronosequences soil pH and total P declined, whereas C:P and N:P ratios increased, which is consistent with the predicted change from N to P limitation of vegetation during ecosystem development. The expected unimodal pattern of leaf area index was most pronounced along wetter chronosequences, suggesting an effect of climate on the expression of retrogression. The four chronosequences do not appear to span a pedogenic climate threshold, defined as an abrupt change in soil properties across a relatively small change in climate, because exchangeable phosphate and base cations declined consistently during long-term pedogenesis. However, the proportion of total P in organic form was greater along wetter chronosequences. We conclude that soil and nutrient availability on the coastal sand plains of southwestern Australia change consistently during long-term pedogenesis, despite marked variation in modern vegetation and climate. The four chronosequences provide a rare soil-age X climate framework within which to study long-term ecosystem development.
New PCE article is now 'ISI Highly Cited' and an 'ISI Hot Paper'
I am extremely pleased to report that our recent article in PCE has received enough citations to place it in the top 0.1% of the academic field of Plant & Animal Sciences.
This paper presents novel insight into the cell-specific allocation of phosphorus (P) within leaves, discussing how a preferential allocation of P to mesophyll cells can improve P-use efficiency. This is highly relevant to improving P-use efficiency in crop species, to understanding and improving management of native species in ancient P-impoverished landscapes and to more generally understanding the regulation of nutrients in higher plants.
New article published in New Phytologist
Hayes, P.E., Guilherme Pereira, C., Clode, P.L., Lambers, H. 2018. Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytologist. doi:10.1111/nph.15447
· Many Proteaceae are highly phosphorus (P)-sensitive and occur exclusively on old nutrient-impoverished acidic soils (calcifuge), whilst a few also occur on young calcareous soils (soil-indifferent), higher in available calcium (Ca) and P. Calcium increases the severity of P-toxicity symptoms, but its underlying mechanisms are unknown. We propose that Ca-enhanced P-toxicity explains the calcifuge habit of most Proteaceae.
· Four calcifuge and four soil-indifferent Proteaceae from south-western Australia were grown in hydroponics, at a range of P and Ca concentrations.
· Calcium increased the severity of P-toxicity symptoms in all species. Calcifuge Proteaceae were more sensitive to Ca-enhanced P toxicity than soil-indifferent ones. Calcifuges shared these traits: low leaf zinc concentration ([Zn]), low Zn allocation to leaves, low leaf [Zn]:[P], low root:shoot ratio, and high seed P content, compared with soil-indifferent species.
· This is the first demonstration of Ca-enhanced P toxicity across multiple species. Calcium-enhanced P toxicity provides an explanation for the calcifuge habit of most Proteaceae and is critical to the management of this iconic Australian family. This study represents a major advance towards an understanding of the physiological mechanisms of P toxicity and its role in the distribution of Proteaceae.
Research featured on the cover of Plant, Cell & Environment
Published the first chapter of my PhD thesis in Plant, Cell & Environment
Hayes, P.E., Clode, P.L., Oliveira, R.S., Lambers, H., 2018. Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. Plant, Cell and Environment 41: 605–619.
Plants allocate nutrients to specific leaf cell types; eudicots are thought to predominantly allocate phosphorus (P) to epidermal/bundle sheath cells. However, three Proteaceae species have been shown to preferentially allocate P to mesophyll cells instead. These Proteaceae species are highly adapted to P‐impoverished habitats, with exceptionally high photosynthetic P‐use efficiencies (PPUE). We hypothesized that preferential allocation of P to photosynthetic mesophyll cells is an important trait in species adapted to extremely P‐impoverished habitats, contributing to their high PPUE. We used elemental X‐ray mapping to determine leaf cell‐specific nutrient concentrations for 12 Proteaceae species, from habitats of strongly contrasting soil P concentrations, in Australia, Brazil, and Chile. We found that only species from extremely P‐impoverished habitats preferentially allocated P to photosynthetic mesophyll cells, suggesting it has evolved as an adaptation to their extremely P‐impoverished habitat and that it is not a family‐wide trait. Our results highlight the possible role of soil P in driving the evolution of ecologically relevant nutrient allocation patterns and that these patterns cannot be generalized across families. Furthermore, preferential allocation of P to photosynthetic cells may provide new and exciting strategies to improve PPUE in crop species.
Co-authored a really nice project with Gang Huang; looking at P-acquisition in the Australian native Peppermint tree, which shifts its P-acquisition strategy with decreasing soil P availability, from mycorrhizal to mass flow
Huang, G., Hayes, P. E., Ryan, M. H., Pang, J., Lambers, H. 2017. Peppermint trees shift their phosphorus-acquisition strategy along a strong gradient of plant-available phosphorus by increasing their transpiration at very low phosphorus availability. Oecologia (in press)
Some plant species use different strategies to acquire phosphorus (P) dependent on environmental conditions, but studies investigating the relative significance of P-acquisition strategies with changing P availability are rare. We combined a natural P availability gradient and a glasshouse study with 10 levels of P supplies to investigate the roles of rhizosphere carboxylates and transpiration-driven mass flow in P acquisition by Agonis flexuosa. Leaf P concentrations of A. flexuosa decreased and leaf manganese (Mn) concentrations increased with decreasing soil P concentration along a dune chronosequence. In the glasshouse, in response to decreasing P supply, shoot growth and root length decreased, leaf P and Mn concentrations decreased, rhizosphere carboxylates decreased, transpiration rate and transpiration ratio increased and the percentage of root length colonized by arbuscular mycorrhizal fungi was unchanged. Although it was proved leaf Mn concentration was a good proxy for rhizosphere carboxylate amounts in the glasshouse study, the enhanced plant P acquisition at low P supply was related to transpiration-induced mass flow rather than carboxylates. We deduced that the higher leaf Mn concentrations in low soil P availability of the field were likely a result of increased mass flow. In summary, as soil P availability declined, A. flexuosa can shift its P-acquisition strategy away from a mycorrhizal mode towards one involving increased mass flow.
Attended the International Plant Nutrition Colloquium 2017, Copenhagen, Denmark
An amazing week of science and ideas with friends and colleagues in one of the most innovative and amazing cities, Copenhagen. The conference was all about plant nutrition, with a focus on 'plant nutrition for a global green growth'. There were lots of innovative ideas and strategies to improve worldwide food production, as well some recent advances in plant nutrition. I was lucky enough to be awarded the Marschner Young Scientist Award and was invited to give a plenary presentation, in which I presented one of the most exciting parts of my PhD research, see attached. Thank you to everyone who attended the conference, it was an amazing experience for me, both professionally and personally.
One of four finalists in the 2017 Premier's Science Awards - Student Scientist of the Year
Mr Patrick Hayes
PhD candidate (The University of Western Australia)
Mr Hayes is a PhD student within the School of Biological Sciences and the Centre for Microscopy, Characterisation and Analysis at UWA. His PhD research is focused on the plant family Proteaceae and their distribution in WA and abroad. Mr Hayes uses cutting-edge techniques such as electron microscopy and energy dispersive spectroscopy to investigate and analyse how these native Australian plants are able to survive on nutrient poor soils. This research will further understanding of Australia’s unique endemic plants, improving ecosystem conservation and restoration strategies and thus preserving Australia’s naturally high biodiversity.
Recipient of the 2017 Marschner Young Scientist Award
Awarded by the International Plant Nutrition Colloquium
A highly prestigious and competitive award for outstanding early-career researchers and PhD students with a potential to become future research leaders.
Invited to give a plenary oral presentation at IPNC2017 Copenhagen, free registration and 500 € financial support to attend IPNC2017.
Co-authored an exciting new publication with UWA PhD graduate Dr Kenny Png
Png, G. K., Turner, B. L., Albornoz, F. E., Hayes, P. E., Lambers, H. and Laliberté, E. 2017. Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. Journal of Ecology (in press)
The abundance of nitrogen (N)-fixing plants in ecosystems where phosphorus (P) limits plant productivity poses a paradox because N fixation entails a high P cost. One explanation for this paradox is that the N-fixing strategy allows greater root phosphatase activity to enhance P acquisition from organic sources, but evidence to support this contention is limited.
We measured root phosphomonoesterase (PME) activity of 10 N-fixing species, including rhizobial legumes and actinorhizal Allocasuarina species, and eight non-N-fixing species across a retrogressive soil chronosequence showing a clear shift from N to P limitation of plant growth and representing a strong natural gradient in P availability.
Legumes showed greater root PME activity than non-legumes, with the difference between these two groups increasing markedly as soil P availability declined. By contrast, root PME activity of actinorhizal species was always lower than that of co-occurring legumes and not different from non-N-fixing plants.
The difference in root PME activity between legumes and actinorhizal plants was not reflected in a greater or similar reliance on N fixation for N acquisition by actinorhizal species compared to co-occurring legumes.
Synthesis. Our results support the idea that N-fixing legumes show high root phosphatase activity, especially at low soil P availability, but suggest that this is a phylogenetically conserved trait rather than one directly linked to their N-fixation capacity.