The impact of Grey Heron (Ardea cinerea L.) colony on soil biogeochemistry and vegetation: a natural long-term in situ experiment in a planted pine forest

Increased anthropogenic pressure including intensification of agricultural activities leads to long-term decline of natural biotopes, with planted forests often considered as promising compensatory response, although reduced biodiversity and ecosystem stability represent their common drawbacks. Here we present a complex investigation of the impact of a large Grey Heron (Ardea cinerea L.) colony on soil biogeochemistry and vegetation in a planted Scots pine forest representing a natural in situ experiment on an engineered ecosystem. After settling around 2006, the colony expanded for 15 years, leading to the intensive deposition of nutrients with feces, food remains and feather thereby considerably altering the local soil biogeochemistry. Thus, lower pH levels around 4.5, 10- and 2-fold higher concentrations of phosphorous and nitrogen, as well as 1.2-fold discrepancies in K, Li, Mn, Zn and Co., respectively, compared to the surrounding control forest area could be observed. Unaltered total organic carbon (Corg) suggests repressed vegetation, as also reflected in the vegetation indices obtained by remote sensing. Moreover, reduced soil microbial diversity with considerable alternations in the relative abundance of Proteobacteria, Firmicutes, Acidobacteriota, Actinobacteriota, Verrucomicrobiota, Gemmatimonadota, Chujaibacter, Rhodanobacter, and Bacillus has been detected. The above alterations to the ecosystem also affected climate stress resilience of the trees indicated by their limited recovery from the major 2010 drought stress, in marked contrast to the surrounding forest (p = 3∙10−5). The complex interplay between geographical, geochemical, microbiological and dendrological characteristics, as well as their manifestation in the vegetation indices is explicitly reflected in the Bayesian network model. Using the Bayesian inference approach, we have confirmed the predictability of biodiversity patterns and trees growth dynamics given the concentrations of keynote soil biogeochemical alternations with correlations R > 0.8 between observations and predictions, indicating the capability of risk assessment that could be further employed for an informed forest management.

[1]  A. Kayumov,et al.  Milti-Scale Detrended Partial Cross-Correlation Analysis of Tree Ring Width and Climate Variations: Revealing Heat and Drought Stress Resilience Factors in a Forest Ecosystem , 2023, bioRxiv.

[2]  Miguel Angel Mendoza-Lugo,et al.  PyBanshee version (1.0): A Python implementation of the MATLAB toolbox BANSHEE for Non-Parametric Bayesian Networks with updated features , 2023, SoftwareX.

[3]  T. Minkina,et al.  Effect of chicken manure on soil microbial community diversity in poultry keeping areas , 2022, Environmental Geochemistry and Health.

[4]  Yinguang Chen,et al.  Enhanced removal of sulfur-containing organic pollutants from actual wastewater by biofilm reactor: Insights of sulfur transformation and bacterial metabolic traits. , 2022, Environmental pollution.

[5]  Z. Xie,et al.  Diverse transformations of sulfur in seabird-affected sediments revealed by microbial and stable isotope analyses , 2022, Journal of Oceanology and Limnology.

[6]  B. Rasti,et al.  Effect of Samarium Oxide Nanoparticles Fabricated by Curcumin on Efflux Pump and Virulence Genes Expression in MDR Pseudomonas aeruginosa and Staphylococcus aureus , 2022, Journal of Cluster Science.

[7]  A. Bond,et al.  The influence of seabirds on their breeding, roosting and nesting grounds: A systematic review and meta‐analysis , 2022, The Journal of animal ecology.

[8]  R. Thomson,et al.  Ecological engineering across a spatial gradient: Sociable weaver colonies facilitate animal associations with increasing environmental harshness , 2022, The Journal of animal ecology.

[9]  P. Ivinskis,et al.  In the Shadow of Cormorants: Succession of Avian Colony Affects Selected Groups of Ground Dwelling Predatory Arthropods , 2022, Forests.

[10]  Yonglin Ren,et al.  Differential responses of the rhizosphere microbiome structure and soil metabolites in tea (Camellia sinensis) upon application of cow manure , 2022, BMC microbiology.

[11]  B. Deák,et al.  The Eurasian crane (Grus grus) as an ecosystem engineer in grasslands: Conservation values, ecosystem services, and disservices related to a large iconic bird species , 2022, Land Degradation & Development.

[12]  D. Hawke The biogeochemistry and ecological impact of Westland petrels (Procellaria westlandica) on terrestrial ecosystems , 2022, New Zealand journal of ecology.

[13]  Q. Hou,et al.  Comparative Analysis of Fecal Bacterial Microbiota of Six Bird Species , 2021, Frontiers in Veterinary Science.

[14]  E. Abakumov,et al.  The role of the ornithogenic factor in soil formation on the Antarctic oasis territory Bunger Hills (East Antarctica) , 2021, Eurasian Journal of Soil Science.

[15]  S. Muzaffar,et al.  Impact of Nesting Socotra Cormorants on Terrestrial Invertebrate Communities , 2021, Insects.

[16]  Snigdhansu Chatterjee,et al.  The influence of decision-making in tree ring-based climate reconstructions , 2021, Nature Communications.

[17]  R. Thomson,et al.  Ecological engineering across a temporal gradient: sociable weaver colonies create year-round animal biodiversity hotspots. , 2021, The Journal of animal ecology.

[18]  I. Parnikoza,et al.  Ornithogenic Factor of Soil Formation in Antarctica: A Review , 2021, Eurasian Soil Science.

[19]  D. Jäger,et al.  [153Sm]Samarium-labeled FAPI-46 radioligand therapy in a patient with lung metastases of a sarcoma , 2021, European Journal of Nuclear Medicine and Molecular Imaging.

[20]  S. Espín,et al.  Bird Feces as Indicators of Metal Pollution: Pitfalls and Solutions , 2020, Toxics.

[21]  Ż. Polkowska,et al.  Seashore sediment and water chemistry at the Admiralty Bay (King George Island, Maritime Antarctica) - Geochemical analysis and correlations between the concentrations of chemical species. , 2020, Marine pollution bulletin.

[22]  P. Moore,et al.  Nutrient Characteristics of Poultry Manure and Litter , 2020 .

[23]  Christa Beckmann,et al.  Prevalence of feather-degrading Bacillus spp. on the plumage of birds in Australia , 2020 .

[24]  B. Dorr,et al.  Double-crested cormorant colony effects on soil chemistry, vegetation structure and avian diversity , 2019, Forest Ecology and Management.

[25]  Z. Xie,et al.  Transformation of sulfur species in lake sediments at Ardley Island and Fildes Peninsula, King George Island, Antarctic Peninsula. , 2019, The Science of the total environment.

[26]  R. A. Saifutdinov,et al.  Influence of Seabird Colonies on Soil Macrofauna Communities at the Black Sea Coast Forests , 2019, Russian Journal of Ecology.

[27]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[28]  Han Y. H. Chen,et al.  Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration , 2019, Nature Communications.

[29]  E. Abakumov Content of available forms of nitrogen, potassium and phosphorus in ornithogenic and other soils of the Fildes Peninsula (King George Island, Western Antarctica) , 2018 .

[30]  Wenbing Han,et al.  Direct and Indirect Effects of Penguin Feces on Microbiomes in Antarctic Ornithogenic Soils , 2018, Front. Microbiol..

[31]  S. Espín,et al.  Experimental manipulation of dietary arsenic levels in great tit nestlings: Accumulation pattern and effects on growth, survival and plasma biochemistry. , 2018, Environmental pollution.

[32]  J. Motiejūnaitė,et al.  Decline of a protected coastal pine forest under impact of a colony of great cormorants and the rate of vegetation change under ornithogenic influence , 2018 .

[33]  X. Otero,et al.  Seabird colonies as important global drivers in the nitrogen and phosphorus cycles , 2018, Nature Communications.

[34]  Armin Bunde,et al.  Fractals and Multifractals in Geophysical Time Series , 2017 .

[35]  Wenyan Zhang,et al.  Mutual Dependence Between Sedimentary Organic Carbon and Infaunal Macrobenthos Resolved by Mechanistic Modeling , 2017 .

[36]  Christopher A. Lepczyk,et al.  Impacts of Endangered Seabirds on Nutrient Cycling in Montane Forest Ecosystems of Hawai‘i 1 , 2017, Pacific Science.

[37]  A. Camacho,et al.  Soil features in rookeries of Antarctic penguins reveal sea to land biotransport of chemical pollutants , 2017, PloS one.

[38]  Katarzyna Zmudczyńska-Skarbek,et al.  Following the flow of ornithogenic nutrients through the Arctic marine coastal food webs , 2017 .

[39]  J. Gonzalez,et al.  Impacts of protected colonial birds on soil microbial communities: When protection leads to degradation , 2017 .

[40]  Gregory P. Brown,et al.  Biotic interactions mediate the influence of bird colonies on vegetation and soil chemistry at aggregation sites. , 2017, Ecology.

[41]  Diane E. Boellstorff,et al.  Estimating the contribution of nitrogen and phosphorus to waterbodies by colonial nesting waterbirds. , 2017, The Science of the total environment.

[42]  R. Martin,et al.  Contribution of Arctic seabird-colony ammonia to atmospheric particles and cloud-albedo radiative effect , 2016, Nature Communications.

[43]  Filippo Bussotti,et al.  Positive biodiversity-productivity relationship predominant in global forests , 2016, Science.

[44]  W. Vyverman,et al.  Bacterial community composition in relation to bedrock type and macrobiota in soils from the Sør Rondane Mountains, East Antarctica. , 2016, FEMS microbiology ecology.

[45]  D. Paprotny,et al.  Estimating extreme river discharges in Europe through a Bayesian network , 2016 .

[46]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[47]  S. Talbot,et al.  Organic matter quantity and source affects microbial community structure and function following volcanic eruption on Kasatochi Island, Alaska. , 2016, Environmental microbiology.

[48]  P. Klimaszyk,et al.  The complexity of ecological impacts induced by great cormorants , 2016, Hydrobiologia.

[49]  J. Blake,et al.  Associations of grassland birds with vegetation structure in the Northern Campos of Uruguay , 2016 .

[50]  Oswaldo Morales-Nápoles,et al.  Non-parametric Bayesian networks: Improving theory and reviewing applications , 2015, Reliab. Eng. Syst. Saf..

[51]  Hua Xu,et al.  Bacterial diversity is strongly associated with historical penguin activity in an Antarctic lake sediment profile , 2015, Scientific Reports.

[52]  Hui Ding,et al.  Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454 pyrosequencing , 2015, Front. Microbiol..

[53]  R. Piotrowicz,et al.  Black spots for aquatic and terrestrial ecosystems: impact of a perennial cormorant colony on the environment. , 2015, The Science of the total environment.

[54]  Ç. Şekercioğlu,et al.  Why birds matter: from economic ornithology to ecosystem services , 2015, Journal of Ornithology.

[55]  P. Kukliński,et al.  An assessment of seabird influence on Arctic coastal benthic communities , 2015 .

[56]  M. Bird,et al.  The biogeochemistry of insectivorous cave guano: a case study from insular Southeast Asia , 2015, Biogeochemistry.

[57]  C. Scrimgeour,et al.  Lichen response to ammonia deposition defines the footprint of a penguin rookery , 2015, Biogeochemistry.

[58]  L. Hou,et al.  Penguins significantly increased phosphine formation and phosphorus contribution in maritime Antarctic soils , 2014, Scientific Reports.

[59]  K. Schaefer,et al.  The impact of the permafrost carbon feedback on global climate , 2014 .

[60]  M. H. Fernandes,et al.  Samarium doped glass-reinforced hydroxyapatite with enhanced osteoblastic performance and antibacterial properties for bone tissue regeneration. , 2014, Journal of materials chemistry. B.

[61]  L. Hinzman,et al.  Bacterial community structure and soil properties of a subarctic tundra soil in Council, Alaska , 2014, FEMS microbiology ecology.

[62]  S. Wanless,et al.  Measurement of ammonia emissions from tropical seabird colonies , 2014 .

[63]  Yuhong Wang,et al.  Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic. , 2014, The Science of the total environment.

[64]  Pelin Yilmaz,et al.  The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks , 2013, Nucleic Acids Res..

[65]  M. Kukwa,et al.  Changes in the epiphytic lichen biota in Scots pine (Pinus sylvestris) stands affected by a colony of grey heron (Ardea cinerea): a case study from northern Poland , 2013, The Lichenologist.

[66]  R. Peixoto,et al.  Plant and Bird Presence Strongly Influences the Microbial Communities in Soils of Admiralty Bay, Maritime Antarctica , 2013, PloS one.

[67]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[68]  R. Iršėnaitė,et al.  Myxomycetes in a forest affected by great cormorant colony: a case study in Western Lithuania , 2013, Fungal Diversity.

[69]  M. G. Pereira,et al.  Soil bacterial community abundance and diversity in ice-free areas of Keller Peninsula, Antarctica , 2012 .

[70]  C. Palmborg,et al.  The impact of nesting cormorants on plant and arthropod diversity , 2012 .

[71]  G. Daily,et al.  Biodiversity loss and its impact on humanity , 2012, Nature.

[72]  T. Osono Excess Supply of Nutrients, Fungal Community, and Plant Litter Decomposition: A Case Study of Avian-Derived Excreta Deposition in Conifer Plantations , 2012 .

[73]  C. Schadt,et al.  Denitrifying Bacteria from the Genus Rhodanobacter Dominate Bacterial Communities in the Highly Contaminated Subsurface of a Nuclear Legacy Waste Site , 2011, Applied and Environmental Microbiology.

[74]  J. Corbeil,et al.  Metagenomic Analysis of Stress Genes in Microbial Mat Communities from Antarctica and the High Arctic , 2011, Applied and Environmental Microbiology.

[75]  R. Redondo,et al.  Protected wading bird species threaten relict centenarian cork oaks in a Mediterranean Biosphere Reserve: A conservation management conflict , 2011 .

[76]  R. Zhu,et al.  Potential ammonia emissions from penguin guano, ornithogenic soils and seal colony soils in coastal Antarctica: effects of freezing-thawing cycles and selected environmental variables , 2010, Antarctic Science.

[77]  J. Gregersen,et al.  Influence of perennial colonies of piscivorous birds on soil nutrient contents in a temperate humid climate , 2010 .

[78]  H. Doğan,et al.  Mineral composite assessment of Kelkit River Basin in Turkey by means of remote sensing , 2009 .

[79]  P. Convey,et al.  Environmental influences on bacterial diversity of soils on Signy Island, maritime Antarctic , 2009, Polar Biology.

[80]  J. Aislabie,et al.  Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica , 2008 .

[81]  M. V. D. van der Heijden,et al.  The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. , 2008, Ecology letters.

[82]  H. Qiu,et al.  Global warming and the emergence of ancient pathogens in Canada's arctic regions. , 2007, Medical Hypotheses.

[83]  T. Noda,et al.  Effects of material inputs by the Grey Heron Ardea cinerea on forest-floor necrophagous insects and understory plants in the breeding colony , 2006 .

[84]  S. Cary,et al.  Co-variation in soil biodiversity and biogeochemistry in northern and southern Victoria Land, Antarctica , 2006, Antarctic Science.

[85]  T. Osono,et al.  Pattern of natural 15N abundance in lakeside forest ecosystem affected by cormorant-derived nitrogen , 2006, Hydrobiologia.

[86]  Ç. Şekercioğlu Increasing awareness of avian ecological function. , 2006, Trends in ecology & evolution.

[87]  Susan Newman,et al.  Overestimation of organic phosphorus in wetland soils by alkaline extraction and molybdate colorimetry. , 2006, Environmental science & technology.

[88]  J. Witman,et al.  Nutrient transfer from sea to land: the case of gulls and cormorants in the Gulf of Maine. , 2006, The Journal of animal ecology.

[89]  J. Moore Animal Ecosystem Engineers in Streams , 2006 .

[90]  R. Holdaway,et al.  Surface soil chemistry at an alpine procellariid breeding colony in New Zealand, and comparison with a lowland site , 2006 .

[91]  B. Gu,et al.  Mechanisms for Organic Matter and Phosphorus Burial in Sedimentsof a Shallow, Subtropical, Macrophyte-Dominated Lake , 2006 .

[92]  J. Ellis Marine Birds on Land: A Review of Plant Biomass, Species Richness, and Community Composition in Seabird Colonies , 2005, Plant Ecology.

[93]  H. Tomassen,et al.  How bird droppings can affect the vegetation composition of ombrotrophic bogs , 2005 .

[94]  Heiko Balzter,et al.  Modelling relationships between birds and vegetation structure using airborne LiDAR data: a review with case studies from agricultural and woodland environments , 2005 .

[95]  John R. Miller,et al.  Hyperspectral vegetation indices and novel algorithms for predicting green LAI of crop canopies: Modeling and validation in the context of precision agriculture , 2004 .

[96]  H. Mun Effects of colony nesting of Adrea cinerea and Egretta alba modesta on soil properties and herb layer composition in a Pinus densiflora forest , 1997, Plant and Soil.

[97]  A. Ishida,et al.  Nitrogen and phosphorus enrichment and balance in forests colonized by cormorants: Implications of the influence of soil adsorption , 2004, Plant and Soil.

[98]  Slawomir Ligeza,et al.  Accumulation of nutrients in soils affected by perennial colonies of piscivorous birds with reference to biogeochemical cycles of elements. , 2003, Chemosphere.

[99]  A. Huete,et al.  Overview of the radiometric and biophysical performance of the MODIS vegetation indices , 2002 .

[100]  A. Dijk,et al.  Exponential Distribution Theory and the Interpretation of Splash Detachment and Transport Experiments , 2002 .

[101]  John R. Miller,et al.  Integrated narrow-band vegetation indices for prediction of crop chlorophyll content for application to precision agriculture , 2002 .

[102]  E. Chuvieco,et al.  Assessment of different spectral indices in the red-near-infrared spectral domain for burned land discrimination , 2002 .

[103]  Ronald D. Jones,et al.  Phosphorus Biogeochemistry and the Impact of Phosphorus Enrichment: Why Is the Everglades so Unique? , 2001, Ecosystems.

[104]  T. Osono,et al.  Forest Floor Quality and N Transformations in a Temperate Forest Affected by Avian-Derived N Deposition , 2001 .

[105]  Y. Steinberger,et al.  Soil microbial community and bacterial functional diversity at Machu Picchu, King George Island, Antarctica , 2001, Polar Biology.

[106]  David Tilman,et al.  Human-caused environmental change: Impacts on plant diversity and evolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Henri D. Grissino-Mayer,et al.  Evaluating Crossdating Accuracy: A Manual and Tutorial for the Computer Program COFECHA , 2001 .

[108]  G. Polis,et al.  Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands , 1999, Oecologia.

[109]  M. Legrand,et al.  Ammonium in coastal Antarctic aerosol and snow: Role of polar ocean and penguin emissions , 1998 .

[110]  A. Gitelson,et al.  Use of a green channel in remote sensing of global vegetation from EOS- MODIS , 1996 .

[111]  A. Ishida Effects of the common cormorant, phalacrocorax carbo, on evergreen forests in two nest sites at Lake Biwa, Japan , 1996, Ecological Research.

[112]  J. Lawton,et al.  Organisms as ecosystem engineers , 1994 .

[113]  Claus Buschmann,et al.  In vivo spectroscopy and internal optics of leaves as basis for remote sensing of vegetation , 1993 .

[114]  E. Cook,et al.  Methods of Dendrochronology - Applications in the Environmental Sciences , 1991 .

[115]  E. Wada,et al.  Nitrogen and Carbon Isotope Ratios in Seabird Rookeries and their Ecological Implications , 1988 .

[116]  J. A. Schell,et al.  Monitoring vegetation systems in the great plains with ERTS , 1973 .