Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease

Journal article


Sweet, Michael, Burian, Alfred, Fifer, James, Bulling, Mark, Elliott, D. and Raymundo, Laurie 2019. Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease. Microbiome. 7 (1), pp. 1-14. https://doi.org/10.1186/s40168-019-0759-6
AuthorsSweet, Michael, Burian, Alfred, Fifer, James, Bulling, Mark, Elliott, D. and Raymundo, Laurie
Abstract

Coral reefs face unprecedented declines in diversity and cover, a development largely attributed to climate change-induced bleaching and subsequent disease outbreaks. Coral-associated microbiomes may strongly influence the fitness of their hosts and alter heat tolerance and disease susceptibility of coral colonies. Here, we describe a new coral disease found in Micronesia and present a detailed assessment of infection-driven changes in the coral microbiome. Combining field monitoring and histological, microscopic and next-generation barcoding assessments, we demonstrate that the outbreak of the disease, named ‘grey-patch disease’, is associated with the establishment of cyanobacterial biofilm overgrowing coral tissue. The disease is characterised by slow progression rates, with coral tissue sometimes growing back over the GPD biofilm. Network analysis of the corals’ microbiome highlighted the clustering of specific microbes which appeared to benefit from the onset of disease, resulting in the formation of ‘infection clusters’ in the microbiomes of apparently healthy corals. Our results appear to be in contrast to the recently proposed Anna-Karenina principle, which states that disturbances (such as disease) trigger chaotic dynamics in microbial communities and increase β-diversity. Here, we show significantly higher community similarity (compositional homogeneity) in the pathobiome of diseased corals, compared to the microbiome associated with apparently healthy tissue. A possible explanation for this pattern is strong competition between the pathogenic community and those associated with the ‘healthy’ coral holobiont, homogenising the composition of the pathobiome. Further, one of our key findings is that multiple agents appear to be involved in degrading the corals’ defences causing the onset of this disease. This supports recent findings indicating a need for a shift from the one-pathogen-one-disease paradigm to exploring the importance of multiple pathogenic players in any given disease.

Keywordsmicrobiome; cyanobacteria; anna-karenina; microbial networks
Year2019
JournalMicrobiome
Journal citation7 (1), pp. 1-14
PublisherSpringer
ISSN2049-2618
Digital Object Identifier (DOI)https://doi.org/10.1186/s40168-019-0759-6
Web address (URL)https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-019-0759-6
hdl:10545/624397
Output statusPublished
Publication dates22 Nov 2019
Publication process dates
Deposited15 Jan 2020, 13:59
Accepted2019
ContributorsUniversity of Derby and University of Guam
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Robinson, Louise, Bryson, David, Bulling, Mark T., Sparks, N. and Wellard, K. S. 2018. Post-feeding activity of Lucilia sericata (Diptera: Calliphoridae) on common domestic indoor surfaces and its effect on development. Forensic Science International. https://doi.org/10.1016/j.forsciint.2018.03.010
The influence of trees, shrubs, and grasses on microclimate, soil carbon, nitrogen, and CO2 efflux: Potential implications of shrub encroachment for Kalahari rangelands.
Thomas, Andrew David, Elliott, D., Dougill, Andrew John, Stringer, Lindsay Carman, Hoon, Stephen Robert and Sen, Robin 2018. The influence of trees, shrubs, and grasses on microclimate, soil carbon, nitrogen, and CO2 efflux: Potential implications of shrub encroachment for Kalahari rangelands. Land Degradation & Development. 29 (5), pp. 1-11. https://doi.org/10.1002/ldr.2918
Involving recreational snorkelers in inventory improvement or creation: a case study in the Indian Ocean
Bourjon, Philippe, Ducarme, Frédéric, Quod, Jean-Pascal and Sweet, M. 2018. Involving recreational snorkelers in inventory improvement or creation: a case study in the Indian Ocean. CBM - Cahiers de Biologie Marine.. https://doi.org/10.21411/cbm.a.b05fc714
Mass mortality hits gorgonian forests at Montecristo Island.
Turicchia, Eva, Abbiati, Marco, Sweet, Michael J. and Ponti, Massimo 2018. Mass mortality hits gorgonian forests at Montecristo Island. Diseases of Aquatic Organisms. https://doi.org/10.3354/dao03284
Maintaining natural spawning timing in Acropora corals following long distance inter-continental transportation.
Craggs, Jamie, Guest, James R., Brett, Aaron, Davis, Michelle and Sweet, Michael J. 2018. Maintaining natural spawning timing in Acropora corals following long distance inter-continental transportation. Journal of zoo and aquarium research. https://doi.org/10.19227/jzar.v6i2.317
Topographic shading influences cryoconite morphodynamics and carbon exchange.
Cook, J. M., Sweet, Michael J., Cavalli, Ottavia, Taggart, Angus and Edwards, Arwyn 2018. Topographic shading influences cryoconite morphodynamics and carbon exchange. Arctic, Antarctic, and Alpine Research.. https://doi.org/10.1080/15230430.2017.1414463
Rediscovery of the critically endangered ‘scarce yellow sally stonefly’ Isogenus nubecula in United Kingdom after a 22 year period of absence.
Davy-Bowker, John, Hammett, Michael J., Mauvisseau, Quentin and Sweet, Michael J. 2018. Rediscovery of the critically endangered ‘scarce yellow sally stonefly’ Isogenus nubecula in United Kingdom after a 22 year period of absence. Zootaxa. https://doi.org/10.11646/zootaxa.4394.2.12
The use of gamification in the teaching of disease epidemics and pandemics.
Robinson, Louise, Turner, Ian J. and Sweet, Michael J. 2018. The use of gamification in the teaching of disease epidemics and pandemics. FEMS Microbiology Letters. 365 (11), pp. 1-4. https://doi.org/10.1093/femsle/fny111
Topographic shading influences cryoconite morphodynamics and carbon exchange.
Cook, J. M., Sweet, Michael J., Cavalli, O., Taggart, A. and Edwards, A. 2018. Topographic shading influences cryoconite morphodynamics and carbon exchange. Arctic, Antarctic, and Alpine Research.. https://doi.org/10.1080/15230430.2017.1414463
Maintaining natural spawning timing in Acropora corals following long distance inter-continental transportation.
Craggs, Jamie, Guest, James R., Brett, Aaron, Davis, Michelle and Sweet, Michael J. 2018. Maintaining natural spawning timing in Acropora corals following long distance inter-continental transportation. Journal of zoo and aquarium research. https://doi.org/10.19227/jzar.v6i2.317
First detection of a highly invasive freshwater amphipod (Crangonyx floridanus) in the United Kingdom
Mauvisseau, Q., John Davy-Bowker, David Bryson, Graham R. Souch, Burian, A. and Michael Sweet 2018. First detection of a highly invasive freshwater amphipod (Crangonyx floridanus) in the United Kingdom. Regional Euro-Asian biological Invasions Centre. https://doi.org/10.1101/437301
Effects of environmental temperature on oviposition behavior in three blow fly species of forensic importance
Ody, Helen, Bulling, Mark T. and Barnes, Kate M. 2017. Effects of environmental temperature on oviposition behavior in three blow fly species of forensic importance. Forensic Science International. https://doi.org/10.1016/j.forsciint.2017.03.001
An Introduction to Molecular Ecology
Rowe, G., Sweet, M. and Trevor Beebee 2017. An Introduction to Molecular Ecology. Oxford University Press.
Nocturnal oviposition behavior of forensically important Diptera in Central England
Barnes, Kate M., Grace, Karon A. and Bulling, Mark T. 2015. Nocturnal oviposition behavior of forensically important Diptera in Central England. Journal of Forensic Sciences. https://doi.org/10.1111/1556-4029.12841
Microbial effects on the development of forensically important blow fly species
Crooks, Esther R., Bulling, Mark T. and Barnes, Kate M. 2016. Microbial effects on the development of forensically important blow fly species. Forensic Science International. https://doi.org/10.1016/j.forsciint.2016.05.026
Symbiotic microbes from marine invertebrates: Driving a new era of natural product drug discovery.
Blockley, Alix, Elliott, D., Roberts, Adam and Sweet, Michael J. 2017. Symbiotic microbes from marine invertebrates: Driving a new era of natural product drug discovery. Diversity. 9 (4), pp. 1-13. https://doi.org/10.3390/d9040049
Designer reefs and coral probiotics; great concepts but are they good practice?
Sweet, M., Ramsey, A. and Bulling, M. 2017. Designer reefs and coral probiotics; great concepts but are they good practice? Biodiversity. https://doi.org/10.1080/14888386.2017.1307786
Detecting macroecological patterns in bacterial communities across independent studies of global soils.
Ramirez, Kelly S., Knight, Christopher G., de Hollander, Mattias, Brearley, Francis Q., Constantinides, Bede, Cotton, Anne, Creer, Si, Crowther, Thomas W., Davison, John, Delgado-Baquerizo, Manuel, Dorrepaal, Ellen, Elliott, D., Fox, Graeme, Griffiths, Robert I., Hale, Chris, Hartman, Kyle, Houlden, Ashley, Jones, David L., Krab, Eveline J., Maestre, Fernando T., McGuire, Krista L., Monteux, Sylvain, Orr, Caroline H., van der Putten, Wim H., Roberts, Ian S., Robinson, David A., Rocca, Jennifer D., Rowntree, Jennifer, Schlaeppi, Klaus, Shepherd, Matthew, Singh, Brajesh K., Straathof, Angela L., Bhatnagar, Jennifer M., Thion, Cécile, van der Heijden, Marcel G. A. and de Vries, Franciska T. 2017. Detecting macroecological patterns in bacterial communities across independent studies of global soils. Nature Microbiology. 3, p. 189–196. https://doi.org/10.1038/s41564-017-0062-x
Inducing broadcast coral spawning ex situ: Closed system mesocosm design and husbandry protocol.
Craggs, Jamie, Guest, James R., Davis, Michelle, Simmons, Jeremy, Dashti, Ehsan and Sweet, Michael J. 2017. Inducing broadcast coral spawning ex situ: Closed system mesocosm design and husbandry protocol. Ecology and Evolution. https://doi.org/10.1002/ece3.3538
Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera
Sweet, Michael J., Brown, Barbara E., Dunne, Richard P., Singleton, Ian and Bulling, Mark T. 2017. Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera. Coral Reefs. https://doi.org/10.1007/s00338-017-1572-y
The “resort effect”: Can tourist islands act as refuges for coral reef species?
Charlotte Moritz, Frédéric Ducarme, Sweet, M., Michael D. Fox, Brian Zgliczynski, Nizam Ibrahim, Ahmed Basheer, Kathryn A. Furby, Zachary R. Caldwell, Chiara Pisapia, Gabriel Grimsditch and Ameer Abdulla 2017. The “resort effect”: Can tourist islands act as refuges for coral reef species? Diversity and Distributions. https://doi.org/10.1111/ddi.12627
On the importance of the microbiome and pathobiome in coral health and disease
Sweet, M. and Bulling, M. 2017. On the importance of the microbiome and pathobiome in coral health and disease. Frontiers in Marine Sciences. https://doi.org/10.3389/fmars.2017.00009
'Yellow Syndrome' in scleractinian corals throughout Bintain District, Kepulauan Riau Province, Indonesia
Johan, O., Budianto, O. and Sweet, M. 2017. 'Yellow Syndrome' in scleractinian corals throughout Bintain District, Kepulauan Riau Province, Indonesia. Indonesia Aquaculture Journal. 12 (1), pp. 37-42. https://doi.org/10.15578/iaj.12.1.2017.37-42
Variation in size frequency distribution of coral populations under different fishing pressures in two contrasting locations in the Indian Ocean.
Grimsditch, Gabriel, Pisapia, Chiara, Huck, M., Karisa, Juliet, Obura, David and Sweet, M. 2017. Variation in size frequency distribution of coral populations under different fishing pressures in two contrasting locations in the Indian Ocean. Marine Environmental Research. https://doi.org/10.1016/j.marenvres.2017.09.017
Juvenile “black teatfish” in Maldives
Sweet, M., Ducarme, F. and Conand, C. 2016. Juvenile “black teatfish” in Maldives. SPC Beche-de-mer Information Bulletin #36. pp. 1-2.
Coral responses to anthropogenic stress in the twenty-first century: an ecophysiological perspective
Sweet, M. and Brown B.E. 2016. Coral responses to anthropogenic stress in the twenty-first century: an ecophysiological perspective. in: Oceanography and Marine Biology CRC Press. pp. 271 - 314
Is Acropora palmata recovering? A case study in Los Roques National Park, Venezula
Aldo Croquer, Francoise Cavada-Blanco, Ainhoa L Zubillaga, Esteban A Agudo-Adriani and Sweet, M. 2016. Is Acropora palmata recovering? A case study in Los Roques National Park, Venezula. PeerJ. (eCollection 2016). https://doi.org/10.7717/peerj.1539
Baseline reef health surveys at Bangka Island (North Sulawesi, Indonesia) reveal new threats
Massimo Ponti, Francesca Fratangeli, Nicolò Dondi, Marco Segre Reinach, Clara Serra and Sweet, M. 2016. Baseline reef health surveys at Bangka Island (North Sulawesi, Indonesia) reveal new threats. PeerJ. https://doi.org/10.7717/peerj.2614
The role of viruses in coral health and disease
Sweet, M. and John Bythell 2016. The role of viruses in coral health and disease. Journal of Invertebrate Biology. https://doi.org/10.1016/j.jip.2016.12.005
Molecular changes in skin pigmented lesions of the coral trout Plectropomus leopardus
Adélaïde Lerebours, Emma C Chapman, Sweet, M., Jeanette M Rotchell and Michelle R Heupel 2016. Molecular changes in skin pigmented lesions of the coral trout Plectropomus leopardus. Marine Environmental Research. https://doi.org/10.1016/j.marenvres.2016.07.009
Influence of Resource Availability on the Foraging Strategies of the Triangle Butterflyfish Chaetodon triangulum in the Maldives
Sweet, M. 2016. Influence of Resource Availability on the Foraging Strategies of the Triangle Butterflyfish Chaetodon triangulum in the Maldives. PLos ONE. https://doi.org/10.1371/journal.pone.0151923
New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs
Sweet, M. and Bulling, M. 2016. New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs. Marine Ecological Progress Series. https://doi.org/10.3354/meps11750
A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs
Martin Stelfox, Jillian Hudgins and Sweet, M. 2016. A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs. Marine Pollution Bulletin. https://doi.org/10.1016/j.marpolbul.2016.06.034
Is Acropora Palmata recovering? A case study in Los Roques National Park, Venezuela
Croquer, Aldo, Cavada-Blanco, Francoise, Zubillaga, Ainhoa L., Agudo-Adriani, Esteban A. and Sweet, Michael J. 2016. Is Acropora Palmata recovering? A case study in Los Roques National Park, Venezuela. PeerJ. https://doi.org/10.7717/peerj.1539
Sampling and Describing Glacier Ice
Toubes-Rodrigo, Mario, Cook, Simon J., Elliott, D. and Sen, Robin 2016. Sampling and Describing Glacier Ice. in: British Society for Geomorphology.
Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes
Joseph M Cook, Arwyn Edwards, Bulling, M., Luis A J Mur, Sophie Cook, Jarishma K Gokul, Karen A Cameron, Sweet, M. and Tristram D L Irvine-Fynn 2016. Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes. Environmental Microbiology. https://doi.org/10.1111/1462-2920.13349
Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana
Brearley, Francis Q., Elliott, D., Iribar, Amaia and Sen, Robin 2016. Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana. Plant and Soil. 403, p. 253–265. https://doi.org/10.1007/s11104-016-2818-0
Coral responses to anthropogenic stress in the 21st Century – An ecophysiological perspective.
Sweet, Michael J. and Brown, Barbara E. 2016. Coral responses to anthropogenic stress in the 21st Century – An ecophysiological perspective. in: Taylor & Francis.
Prevalence and Incidence of Black Band Disease of Scleractinian Corals in the Kepulauan Seribu Region of Indonesia
Johan, Ofri, Zamany, Neviaty P., Smith, David and Sweet, M. 2016. Prevalence and Incidence of Black Band Disease of Scleractinian Corals in the Kepulauan Seribu Region of Indonesia. Diversity. https://doi.org/10.3390/d8020011
Pastoralism and Kalahari Rangeland Soils
Thomas, A.D., Elliott, D., Griffith, T.N.L. and Mairs, H. 2015. Pastoralism and Kalahari Rangeland Soils. in: Brearley, F. Q. and Thomas, A. D. (ed.) Land-Use Change Impacts On Soil Processes: Tropical And Savannah Ecosystems Wallingford CABI. pp. 122-132
Microbial communities associated with healthy and white syndrome-affected Echinopora lamellose in aquaria and experimental treatment with the antibiotic ampicillin
Smith, D., Leary, P., Craggs, J., Bythell, J. and Sweet, M. 2015. Microbial communities associated with healthy and white syndrome-affected Echinopora lamellose in aquaria and experimental treatment with the antibiotic ampicillin. PLos ONE. 10 (3), pp. 1-17. https://doi.org/10.1371/journal.pone.0121780
Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean
Mathieu G Séré, Pablo Tortosa, Pascale Chabanet, Jean-Pascal Quod, Sweet, M. and Michael H Schleyer 2015. Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean. Molecular Ecology. https://doi.org/10.1111/mec.13326
Ciliate communities consistently associated with coral diseases
Sweet, Michael J. and Séré, Mathieu G. 2015. Ciliate communities consistently associated with coral diseases. Journal of Sea Research. https://doi.org/10.1016/j.seares.2015.06.008
Fostering effective international collaboration for marine science in small island states
Hind, Edward J., Alexander, Steven M., Green, Stephanie J., Kritzer, Jacob P., Sweet, M., Johnson, Ayana Elizabeth, Amargós, Fabian P., Smith, Nicola S. and Angelie M. 2015. Fostering effective international collaboration for marine science in small island states. Frontiers in Marine Science. https://doi.org/10.3389/fmars.2015.00086
Geographically conserved rates of background mortality among common reef-building corals in Lhaviyani Atoll, Maldives versus northern Great Barrier Reef, Australia
Sweet, M. 2015. Geographically conserved rates of background mortality among common reef-building corals in Lhaviyani Atoll, Maldives versus northern Great Barrier Reef, Australia. Marine Biology. 162 (8). https://doi.org/10.1007/s00227-015-2694-9
Diseases in marine invertebrates associated with mariculture and commercial fisheries
Sweet, M. and Kelly S Bateman 2015. Diseases in marine invertebrates associated with mariculture and commercial fisheries. Journal of Sea Research. https://doi.org/10.1016/j.seares.2015.06.016
Age-Related Shifts in Bacterial Diversity in a Reef Coral
Alex D Williams, Barbara E Brown, Lalita Putchim and Sweet, M. 2015. Age-Related Shifts in Bacterial Diversity in a Reef Coral. PLos ONE. 10 (2). https://doi.org/10.1371/journal.pone.0144902
A novel sponge disease caused by a consortium of micro-organisms
Sweet, M. 2015. A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs. https://doi.org/10.1007/s00338-015-1284-0
Baseline coral disease surveys within three marine parks in Sabah, Borneo
Jennifer Miller, Sweet, M., Elizabeth Wood and John Bythell 2015. Baseline coral disease surveys within three marine parks in Sabah, Borneo. PeerJ. https://doi.org/10.7717/peerj.1391
White Syndrome in Acropora muricata: Non-specific bacterial infection and ciliate histophagy
Sweet, M. and Bythell, J. 2015. White Syndrome in Acropora muricata: Non-specific bacterial infection and ciliate histophagy. Molecular Ecology. 24, p. 1150–1159. https://doi.org/10.1111/mec.13097
Bacterial and fungal communities in a degraded ombrotrophic peatland undergoing natural and managed re-vegetation
Elliott, D., Caporn, S., Nwaishi, F., Nilsson, R. H. and Sen, R. 2015. Bacterial and fungal communities in a degraded ombrotrophic peatland undergoing natural and managed re-vegetation. PLos ONE. 10 (5), pp. 1-20. https://doi.org/10.1371/journal.pone.0124726
The distribution and abundance of black band disease and white syndrome in Kepulauan Seribu, Indonesia
Johan, Ofri, Bengen, Dietriech Geoffrey, Zamani, Neviaty Putri, Suharsono and Sweet, M. 2015. The distribution and abundance of black band disease and white syndrome in Kepulauan Seribu, Indonesia. Journal of Biosciences. https://doi.org/10.1016/j.hjb.2015.09.001
Soil contamination with silver nanoparticles reduces Bishop pine growth and ectomycorrhizal diversity on pine roots
Sweet, M. and I Singleton 2015. Soil contamination with silver nanoparticles reduces Bishop pine growth and ectomycorrhizal diversity on pine roots. Journal of Nanoparticle Research. https://doi.org/10.1007/s11051-015-3246-4
Seasonal differences in soil CO2 efflux and carbon storage in Ntwetwe Pan, Makgadikgadi Basin, Botswana
Thomas, Andrew D., Dougill, Andrew J., Elliott, D. and Mairs, Helen 2014. Seasonal differences in soil CO2 efflux and carbon storage in Ntwetwe Pan, Makgadikgadi Basin, Botswana. Geoderma. 219-220. https://doi.org/10.1016/j.geoderma.2013.12.028
Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari
Elliott, D., Thomas, Andrew David, Hoon, Steve R. and Sen, Robin 2014. Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari. Biodiversity and conservation. 23, p. 1709–1733. https://doi.org/10.1007/s10531-014-0684-8
A novel investigation of a blister-like syndrome in aquarium Echinopora lamellosa
David Smith, Peter Leary, Mark Bendall, Edmund Flach, Rachel Jones and Sweet, M. 2014. A novel investigation of a blister-like syndrome in aquarium Echinopora lamellosa. PLos ONE. https://doi.org/10.1371/journal.pone.0097018
Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis
Sweet, M., A Croquer and J C Bythell 2014. Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis. Proc Roy Soc. https://doi.org/10.1098/rspb.2014.0094
Decadal environmental ‘memory’ in a reef coral?
Brown B.E., Dunne R.P., Edwards A.J., Sweet, M. and Phongsuwan N. 2014. Decadal environmental ‘memory’ in a reef coral? Marine Biology. https://doi.org/10.1007/s00227-014-2596-2
Coral diseases in aquaria and in nature
Sweet, Michael J., Jones, Rachel and Bythell, John C. 2013. Coral diseases in aquaria and in nature. https://doi.org/10.1017/S0025315411001688
Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals
Sweet, Michael J., Croquer, Aldo, Bythell, John C. and Lopez-Garcia, Purification 2013. Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals. https://doi.org/10.1371/journal.pone.0021195
Characterisation of the bacterial and fungal communities associated with different lesion sizes of Dark Spot Syndrome occurring in the Coral Stephanocoenia intersepta
Sweet, Michael J., Burn, Deborah, Croquer, Aldo, Leary, Peter and Bereswill, Stefan 2013. Characterisation of the bacterial and fungal communities associated with different lesion sizes of Dark Spot Syndrome occurring in the Coral Stephanocoenia intersepta. https://doi.org/10.1371/journal.pone.0062580
Evidence of melanoma in wild marine fish populations
Sweet, Michael J., Kirkham, Nigel, Bendall, Mark, Currey, Leanne, Bythell, John C., Heupel, Michelle and Vartanian, Jean-Pierre 2013. Evidence of melanoma in wild marine fish populations. https://doi.org/10.1371/journal.pone.0041989
Metal-based nanoparticles; size, function and areas for advancement
Sweet, Michael J. 2013. Metal-based nanoparticles; size, function and areas for advancement. in:
Using model systems to address the biodiversity-ecosystem functioning process
Bulling, Mark T., White, Piran C. L., Raffaelli, D. and Pierce, Graham J. 2013. Using model systems to address the biodiversity-ecosystem functioning process.
How biodiversity affects ecosystem processes: implications for ecological revolutions and benthic ecosystem function
Solan, Martin, Batty, P., Bulling, Mark T. and Godbold, J. A. 2013. How biodiversity affects ecosystem processes: implications for ecological revolutions and benthic ecosystem function. Aquatic Biology. https://doi.org/10.3354/ab00058
Global patterns of bioturbation intensity and mixed depth of marine soft sediments
Teal, L. R., Bulling, Mark T., Parker, E. R. and Solan, Martin 2013. Global patterns of bioturbation intensity and mixed depth of marine soft sediments. Aquatic Biology. https://doi.org/10.3354/ab00052
Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity
Langenheder, Silke, Bulling, Mark T., Solan, Martin, Prosser, James I. and Bell, Thomas 2013. Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLos ONE. https://doi.org/10.1371/journal.pone.0010834
Impact of biodiversity-climate futures on primary production and metabolism in a model benthic estuarine system
Hicks, Natalie, Bulling, Mark T., Solan, Martin, Raffaelli, D., White, Piran C. L. and Paterson, David M. 2013. Impact of biodiversity-climate futures on primary production and metabolism in a model benthic estuarine system. BMC Ecology. https://doi.org/10.1186/1472-6785-11-7
Role of functionally dominant species in varying environmental regimes: evidence for the performance-enhancing effect of biodiversity
Langenheder, Silke, Bulling, Mark T., Prosser, James I. and Solan, Martin 2013. Role of functionally dominant species in varying environmental regimes: evidence for the performance-enhancing effect of biodiversity. BMC Ecology. https://doi.org/10.1186/1472-6785-12-14
Funding begets biodiversity
Ahrends, Antje, Burgess, Neil D., Gereau, Roy E., Marchant, Rob, Bulling, Mark T., Lovett, Jon C., Platts, Philip J., Kindemba, Victoria Wilkins, Owen, Nisha, Fanning, Eibleis and Rahbek, Carsten 2013. Funding begets biodiversity. Diversity and Distributions. https://doi.org/10.1111/j.1472-4642.2010.00737.x
Conservation and the botanist effect
Ahrends, Antje, Rahbek, Carsten, Bulling, Mark T., Burgess, Neil D., Platts, Philip J., Lovett, Jon C., Kindemba, Victoria Wilkins, Owen, Nisha, Sallu, Albert Ntemi and Marshall, Andrew R. 2013. Conservation and the botanist effect. Biological Conservation. https://doi.org/10.1016/j.biocon.2010.08.008
Habitat structure mediates biodiversity effects on ecosystem properties
Godbold, J. A., Bulling, Mark T. and Solan, Martin 2013. Habitat structure mediates biodiversity effects on ecosystem properties. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2010.2414
Permeability of intertidal sandflats: impact of temporal variability on sediment metabolism
Zetzche, E., Bulling, Mark T. and Witte, U. 2013. Permeability of intertidal sandflats: impact of temporal variability on sediment metabolism.
Modelling the impact of vaccination on tuberculosis in badgers.
Hardstaff, Joanne L., Bulling, Mark T., Marion, Glenn, Hutchings, Michael R. and White, Piran C. L. 2013. Modelling the impact of vaccination on tuberculosis in badgers. Epidemiology and infection. https://doi.org/10.1017/S0950268813000642
Indirect effects of non-lethal predation on bivalve activity and sediment reworking
Maire, O., Merchant, J. N., Bulling, Mark T., Teal, L. R., Grémare, A., Duchêne, J. C. and Solan, Martin 2013. Indirect effects of non-lethal predation on bivalve activity and sediment reworking. Journal of Experimental Marine Biology and Ecology. https://doi.org/10.1016/j.jembe.2010.08.004
Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city
Ahrends, Antje, Burgess, Neil D., Milledge, Simon A. H., Bulling, Mark T., Fisher, Brendan, Smart, James C. R., Clarke, G. P., Mhoro, Boniface E. and Lewis, Simon L. 2013. Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.0914471107
Geographical variation in the response to nitrogen deposition in Arabidopsis lyrata petraea.
Vergeer, Philippine, van den Berg, Leon L. J., Bulling, Mark T., Ashmore, Mike R. and Kunin, William E. 2008. Geographical variation in the response to nitrogen deposition in Arabidopsis lyrata petraea. The new phytologist. https://doi.org/10.1111/j.1469-8137.2008.02445.x
Marine biodiversity-ecosystem functions under uncertain environmental futures
Bulling, Mark T., Hicks, Natalie, Murray, L., Paterson, David M., Raffaelli, D., White, Piran C. L. and Solan, Martin 2013. Marine biodiversity-ecosystem functions under uncertain environmental futures. Philosophical Transactions of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rstb.2010.0022
Species effects on ecosystem processes are modified by faunal responses to habitat composition.
Bulling, Mark T., Solan, Martin, Dyson, Kirstie E., Hernandez-Milian, Gema, Luque, Patricia, Pierce, Graham J., Raffaelli, D., Paterson, David M. and White, Piran C. L. 2008. Species effects on ecosystem processes are modified by faunal responses to habitat composition. Oecologia. https://doi.org/10.1007/s00442-008-1160-5
Influence of macrofaunal assemblages and environmental heterogeneity on microphytobenthic production in experimental systems
Dyson, Kirstie E., Bulling, Mark T., Solan, Martin, Hernandez-Milian, Gema, Raffaelli, D., White, Piran C. L. and Paterson, David M. 2013. Influence of macrofaunal assemblages and environmental heterogeneity on microphytobenthic production in experimental systems. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2007.0922
Quantifying individual feeding variability: implications for mollusc feeding experiments
Hanley, M. E., Bulling, Mark T. and Fenner, M. 2013. Quantifying individual feeding variability: implications for mollusc feeding experiments.
Dirichlet neighbours: revisiting Dirichlet tessellation for neighbourhood analysis
Halls, P. J., Bulling, Mark T., White, Piran C. L., Garland, Lynette and Harris, S. 2013. Dirichlet neighbours: revisiting Dirichlet tessellation for neighbourhood analysis.
Impact of external sources of infection on the dynamics of bovine tuberculosis in modelled badger populations
Hardstaff, Joanne L., Bulling, Mark T., Marion, Glenn, Hutchings, Michael R. and White, Piran C. L. 2013. Impact of external sources of infection on the dynamics of bovine tuberculosis in modelled badger populations. BMC Veterinary Research. https://doi.org/10.1186/1746-6148-8-92
Diversity of Planktonic and Attached Bacterial Communities in a Phenol-Contaminated Sandstone Aquifer
Rizoulis, Athanasios, Elliott, D., Rolfe, Stephen. A, Thornton, Steven. F, Banwart, Steven. A, Pickup, Roger. W and Scholes, Julie. D 2013. Diversity of Planktonic and Attached Bacterial Communities in a Phenol-Contaminated Sandstone Aquifer. Microbial Ecology. 66, p. 84–95. https://doi.org/10.1007/s00248-013-0233-0
Diseases in coral aquaculture: causes, implications and preventions
Kramarsky-Winter, Esti, Sweet, Michael J., Leal, Miguel Costa, Sheridan, Christopher and Kushmaro, Ariel 2013. Diseases in coral aquaculture: causes, implications and preventions. Aquaculture. https://doi.org/10.1016/j.aquaculture.2013.02.037
Assessment of the microbial communities associated with white syndrome and brown jelly syndrome in aquarium corals
Sweet, Michael J., Craggs, J., Robson, J. and Bythell, John C. 2013. Assessment of the microbial communities associated with white syndrome and brown jelly syndrome in aquarium corals.
Microsatellites for microbiologists
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