More stories

  • in

    Managed pollination is a much better way of increasing productivity and essential oil content of dill seeds crop

    Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B. 274, 303–313 (2007).PubMed 
    Article 

    Google Scholar 
    IPBES. The assessment report of the intergovernmental science-policy platform on biodiversity and ecosystem services on pollinators, pollination and food production. in Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, Germany (Potts, S.G., Imperatriz-Fonseca, V.L., Ngo, H.T. eds.). 1–552. https://ipbes.net/sites/default/files/downloads/pdf/individual_chapters_pollination_20170305.pdf (2016).Ollerton, J. et al. How many flowering plants are pollinated by animals?. Oikos 120, 321–326 (2011).Article 

    Google Scholar 
    Linder, H. P. Morphology and the Evolution of Wind Pollination. Reproductive Biology 123–135 (Royal Botanic Gardens, 1998).
    Google Scholar 
    Friedman, J. & Barrett, S. C. H. Wind of change: New insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann. Bot. 103, 1515–1527 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gallai, N. et al. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 (2009).Article 

    Google Scholar 
    Potts, S. G. et al. Safeguarding pollinators and their values to human well-being. Nature 540, 220–229 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Srinivasan, M. R. et al. Impact of Pesticides on Honey Bees and Pollinators. Pesticide Application in Agro Ecosystem-Its Dynamics and Implications 243–248 (TNAU Publications, 2015).
    Google Scholar 
    Sanchez-Bayo, F. & Goka, K. Impacts of Pesticides on Honey Bees. Beekeeping and Bee Conservation—Advances in Research. https://doi.org/10.5772/62487. (InTech, 2016).Berry, I. Dead bees don’t pollinate. Orchardist. New Zealand, 60, 287 (1987). Rev. Appl. Entomol. Ser. A 76, 1087 (1998).
    Google Scholar 
    Chandrasekaran, S. et al. Disposed paper cups and declining bees. Curr. Sci. 101(10), 1262 (2011).
    Google Scholar 
    Sandilyan, S. Decline in honey bee population in Southern India: Role of disposable paper cups. J. Zool. Biosci. Res. 1, 6–9 (2014).
    Google Scholar 
    Allen-Wardell, G. et al. The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv. Biol. 12, 8–17 (1998).Article 

    Google Scholar 
    FAO. Declining Bee Populations Pose Threat to Global Food Security and Nutrition. UN World Bee Day, 20 May, Rome. https://www.fao.org/news/story/en/item/1194910/icode/. (2019).Najaran, Z.T. et al. Dill (Anethum graveolens L.) Essential Oils in Food Preservation, Flavor and Safety. https://doi.org/10.1016/C2012-0-06581-7 (Academic Press, 2016). Khare, C.P. Indian Herbal Remedies: Rational Western Therapy, Ayurvedic, and Other Traditional Usage, Botany. 1st edn. 326–327. (Springer, 2004).Jana, S. & Shekhawat, G. S. Anethum graveolens: An indian traditional medicinal herb and spice. Pharmacogn. Rev. 4, 179–184 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Biesiada, A. et al. Nutritional value of garden dill (Anethum graveolens L.), depending on genotype. Notulae Bot. Horti Agrobot. Cluj-Napoca 47, 784–791 (2019).CAS 

    Google Scholar 
    Pulliah, T. Medicinal Plants in India. Vol. 1. 55–56. (Regency Publications New Delhi, 2002).Hornok, L. Cultivation and Processing of Medicinal Plants. 338. (Academic Publications, 1992).Nair, R. & Chanda, S. Antibacterial activities of some medicinal plants of the western region of India. Turk. J. Biol. 31, 231–236 (2007).
    Google Scholar 
    DASD. State Agriculture/Horticulture Departments/DASD Kozhikode, Kerala. https://www.dasd.gov.in/index.php/content/index/statistics (2020).Nemeth, E. & Szekely, G. Floral biology of medicinal plants I. Apiaceae species. Int. J. Horticult. Sci. 6, 133–136 (2000).
    Google Scholar 
    Weiss, E. A. Spice Crops. 268–283 (CAB International, 2002).Book 

    Google Scholar 
    Peter, K.V. Dill in Handbook of Herbs and Spices (Gupta, R., Answer, M.M., Sharma, Y.K. Eds.). 275–285. (Woodhead Publishing Limited, 2012).Meena, N. K. et al. Role of insect pollinators in pollination of seed spices—A review. Int. J. Seed Spices 5, 1–17 (2015).
    Google Scholar 
    Faegri, K. & van der Pijl, L. The Principles of Pollination Ecology 3rd edn. (Pergamon, 1980).
    Google Scholar 
    Ali, M., Saeed, S., Sajjad, A. & Whittington, A. In search of the best pollinators for canola (Brassica napus L.) production in Pakistan. Appl. Entomol. Zool. 46, 353–361 (2011).Article 

    Google Scholar 
    Singh, H., Swaminathan, R. & Hussain, T. Influence of certain plant products on the insect pollinators of coriander. J. Biopest. 3, 208–211 (2010).
    Google Scholar 
    Kant, K. et al. Relative abundance and foraging behavior of honey bee species on minor seed spice crops. Int. J. Seed Spices 3, 51–54 (2013).
    Google Scholar 
    Willmer, P. G. et al. The superiority of bumblebees to honeybees as pollinators: Insect visits to raspberry flowers. Ecol. Entomol. 19, 271–284 (1994).Article 

    Google Scholar 
    Stone, J. L. Components of pollination effectiveness in Psychotria suerrensis, a tropical distylous shrub. Oecologia 107, 504–512 (1996).ADS 
    PubMed 
    Article 

    Google Scholar 
    Olsen, K. M. Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109, 114–121 (1997).ADS 

    Google Scholar 
    Ivey, C. T. et al. Variation in pollinator effectiveness in swamp milkweed, Asclepias incarnate (Apocynaceae). Am. J. Bot. 90, 214–225 (2003).PubMed 
    Article 

    Google Scholar 
    Korpela, S. The influence of honeybee pollination on turnip rape (Brassica campestris) yield and yield components. Ann. Agric. Fenniae 27, 295–303 (1988).
    Google Scholar 
    Sabbahi, R. et al. Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Cruciferae: Brassicacae). J. Econ. Entomol. 98, 267–372 (2005).Article 

    Google Scholar 
    Warakomska, Z. et al. Biology of the bloom and pollination of the umbelliferous vegetables. Part 1: garden dill (Anethum graveolens L.). Acta Agrobot. 35, 69–78 (1982).Article 

    Google Scholar 
    Meena, N. K. et al. Pollinator’s diversity and abundance on cumin (Cuminum cyminum L.) and their impact on yield enhancement at semi-arid region. J. Entomol. Zool. Stud. 6, 1017–1021 (2018).
    Google Scholar 
    Malhotra, S.K. & Vashishtha, B.B. Package of practices for production of seed spices. in Book Published by the Director, ICAR-National Research Centre on Seed Spices, Ajmer. 71–79. (2008).Chaudhary, O. P. diversity, foraging behaviour of floral visitors and pollination ecology of fennel (Foeniculum vulgare Mill). J. Spices Aromatic Crops 15, 34–41 (2006).
    Google Scholar 
    Rianti, P. et al. Diversity and effectiveness of insect pollinators of Jatropha curcas L. (Euphorbiaceae). HAYATI J. Biosci. 17, 38–42 (2010).Article 

    Google Scholar 
    Choi, S. W. & Jung, C. Diversity of insect pollinators in different agricultural crops and wild flowering plants in korea: Literature review. J. Apicult. 30, 191–201 (2015).MathSciNet 
    Article 

    Google Scholar 
    Siregar, E. F. et al. Diversity and abundance of insect pollinators in different agricultural lands in Jambi, Sumatera. HAYATI J. Biosci. 23, 13–17 (2016).Article 

    Google Scholar 
    Devi, M. et al. Diversity of insect pollinators in reference to seed set of mustard (Brassica juncea L.). Int. J. Curr. Microbiol. Appl. Sci. 6, 2131–2144 (2017).Article 

    Google Scholar 
    Martin, P. & Bateson, P. Measuring Behaviour: An Introductory Guide. 2nd edn. (Cambridge University Press, 1993).Dafni, A. Pollination Ecology: A Practical Approach (Oxford University Press, 1992).
    Google Scholar 
    Chaudhary, O. P. & Singh, J. Diversity, temporal abundance, foraging behaviour of floral visitors and effect of different modes of pollination on coriander (Coriandrum sativum L.). J. Spices Aromatic Crops 16, 8–14 (2007).
    Google Scholar 
    Kulkarni, S. R., Gurve, S. S. & Chormule, A. J. Effect of different indigenous bee attractants in onion (Allium cepa L.) crop. Ann. Plant Protect. Sci. 25, 78–82 (2017).
    Google Scholar 
    Manhare, J. S. & Painkra, G. P. Impact of bee attractants on bee visitation on buckwheat (Fagopyrum esculentum L.) crop. J. Entomol. Zool. Stud. 6, 28–31 (2018).
    Google Scholar 
    Kapas, A. et al. The kinetic of essential oil separation from fennel by microwave assisted hydro-distillation (MWHD). UPB Sci. Bull. Ser. B 73, 113–120 (2011).CAS 

    Google Scholar 
    Warrier, P. K. et al. Indian Medicinal Plants. Vol. 1. 153–157. (Orient Longman Limited, 1994).Baswana, K. S. Role of insect pollination on seed production in coriander and fennel. South Indian Horticult. 32, 117–118 (1984).
    Google Scholar 
    Koul, A. K. Pollination mechanism in Coriandrum sativum L. (Apiaceae). Proc. Indian Acad. Sci. Plant Sci. 99, 509–515 (1989).Article 

    Google Scholar 
    Narayana, E. S., Sharma, P. L. & Phadke, K. G. Insect pollinators of saunf (Foenicuum vulgare) with particular reference to the honeybees at Pusa (Bihar). Indian Bee J. 22, 7–13 (1960).
    Google Scholar 
    Mukherjee, S. et al. Pollination events in Nigella sativa L. black cumin. Int. J. Res. Ayurveda Pharm. 4, 342–344 (2013).Article 

    Google Scholar 
    Abrar, M. et al. Insect pollinators and their relative abundance on black cumin Nigella sativa L. at Dera Ismail Khan. J. Entomol. Zool. Stud. 5, 1252–1258 (2017).
    Google Scholar 
    Ollerton, J. & Louise, C. Latitudinal trends in plant-pollinator interactions: Are tropical plants more specialized?. Oikos 98, 340–350 (2002).Article 

    Google Scholar 
    Meena, N. K. et al. Diversity of floral visitors and foraging behavior and abundance of major pollinators on fennel under semi-arid conditions of Rajasthan. Int. J. Trop. Agric. 34, 1891–1897 (2016).
    Google Scholar 
    Sikdar, S. et al. Diurnal foraging activity of flower visiting insects on some seed spices under terai agro-climatic zone of West Bengal. J. Entomol. Zool. Stud. 7, 299–303 (2019).
    Google Scholar 
    Kapil, R. P. et al. Integration of bee behaviour with aphid control for seed production of Brassica campestris var. toria. Indian J. Entomol. 33, 221–223 (1971).
    Google Scholar 
    Bhalla, O. P. et al. Insect visitors of mustard bloom Brassica campestris var sarson, their number and foraging behavior under mid-hill conditions. J. Entomol. Res. 1, 15–17 (1983).
    Google Scholar 
    Rao, G. M. & Suryanarayana, M. C. Studies on the foraging behaviour of honeybees and its effect in seed yield of niger. Indian Bee J. 52, 31–33 (1990).
    Google Scholar 
    Abrol, D. P. Foraging behavior of Apis mellifera L. and A. cerana F. as determined by the energetics of nectar production in different cultivars of Brassica campestris var toria. J. Apicult. Sci. 51, 19–24 (2007).
    Google Scholar 
    Inouye, D. W. The effect of proboscis and corolla tube lengths on patterns and rates of flower visitation by bumble bees. Oecologia 45, 197–201 (1980).ADS 
    PubMed 
    Article 

    Google Scholar 
    Vicens, N. & Bosch, J. Pollination efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on ‘Red Delicious’ apple. Environ. Entomol. 29, 235–240 (2000).Article 

    Google Scholar 
    Singh, J. et al. Foraging rates of different Apis species visiting parental lines of Brassica napus L. Zoos’ Print J. 21, 2226–2227 (2006).Article 

    Google Scholar 
    Engel, E. C. & Irwin, R. E. Linking pollinator visitation and rate of pollen receipt. Am. J. Bot. 90, 1612–1618 (2003).Article 

    Google Scholar 
    Sihag, R. C. Insect pollination increase seed production in cruciferous and umbelliferous crops. J. Apic. Res. 25, 121–126 (1986).Article 

    Google Scholar 
    Verma, S. & Dwivedi, S. N. Floral biology of Trachyspermum ammi (Linn.) Spr. Inventi rapid. Planta Activa 2, 1–6 (2018).
    Google Scholar 
    Singh, B. Effectiveness of different pollinators on yield and quality of greenhouse grown tomatoes and melons: A review. Haryana J. Horticult. Sci. 31, 245–250 (2002).ADS 

    Google Scholar 
    Biswanath, B. et al. Role of insect pollinators in seed yield of coriander (Coriandrum sativum L.) and their electroantennogram response to crop volatiles. Agric. Res. J. 54, 227–235 (2017).Article 

    Google Scholar 
    Giannini, T. C. et al. The dependence of crops for pollinators and the economic value of pollination in Brazil. J. Econ. Entomol. 108, 849–857 (2015).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Risk assessment for the native anurans from an alien invasive species, American bullfrogs (Lithobates catesbeianus), in South Korea

    Pimentel, D. Economic and environmental impacts of invasive species and their management. Pesticides 21, 10–11 (2001).
    Google Scholar 
    Beck, K. G. et al. Invasive species defined in a policy context: Recommendations from the Federal Invasive Species Advisory Committee. Invasive. Plant. Sci. Manag. 1, 414–421. https://doi.org/10.1614/IPSM-08-089.1 (2008).Article 

    Google Scholar 
    Arya, A. K., Joshi, K. K., Bachheti, A. & Rawat, R. Status and impact of invasive and alien species on environment, and human welfare: an overview. Uttar Pradesh J. Zool. 42, 49–58 (2021).
    Google Scholar 
    Boone, M. D., Little, E. E. & Semlitsch, R. D. Overwintered bullfrog tadpoles negatively affect salamanders and anurans in native amphibian communities. Copeia 2004, 683–690. https://doi.org/10.1643/CE-03-229R1 (2004).Article 

    Google Scholar 
    Borzée, A., Kosch, T. A., Kim, M. & Jang, Y. Introduced bullfrogs are associated with increased Batrachochytrium dendrobatidis prevalence and reduced occurrence of Korean treefrogs. PLoS ONE 12, e0177860. https://doi.org/10.1371/journal.pone.0177860 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yap, T. A., Koo, M. S., Ambrose, R. F. & Vredenburg, V. T. Introduced bullfrog facilitates pathogen invasion in the western United States. PLoS ONE 13, e0188384. https://doi.org/10.1371/journal.pone.0188384 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gobel, N., Laufer, G. & Cortizas, S. Changes in aquatic communities recently invaded by a top predator: Evidence of American bullfrogs in Aceguá, Uruguay. Aquat. Sci. 81, 1–11. https://doi.org/10.1007/s00027-018-0604-1 (2019).Article 

    Google Scholar 
    Li, Y., Ke, Z., Wang, Y. & Blackburn, T. M. Frog community responses to recent American bullfrog invasions. Curr. Zool. 57, 83–92. https://doi.org/10.1093/czoolo/57.1.83 (2011).Article 

    Google Scholar 
    Vitousek, P. M., D’antonio, C. M., Loope, L. L., Rejmanek, M. & Westbrooks, R. Introduced species: a significant component of human-caused global change. N. Z. J. Ecol. 21, 1–16 (1997).
    Google Scholar 
    Ficetola, G. F. et al. Pattern of distribution of the American bullfrog Rana catesbeiana in Europe. Biol. Invasions. 9, 767–772. https://doi.org/10.1007/s10530-006-9080-y (2007).Article 

    Google Scholar 
    Lorvelec, O., & Détaint, M. Lithobates catesbeianus (Shaw), American bullfrog (Ranidae, Amphibia). Handbook of alien species in Europe. DAISIE (ed.). (Springer, 2009).Koo, K. S., Park, H. R., Choi, J. H. & Sung, H. C. Present status of non-native amphibians and reptiles traded in Korean online pet shops. J. Ecol. Environ. 3, 106–114. https://doi.org/10.13047/KJEE.2020.34.2.106 (2020).Article 

    Google Scholar 
    Lowe, S., Browne, M., Boudjelas, S., & De Poorter, M. 100 of the world’s worst invasive alien species: A selection from the global invasive species database (Vol. 12) (Auckland: Invasive Species Specialist Group, 2000).Ficetola, G. F., Thuiller, W. & Miaud, C. Prediction and validation of the potential global distribution of a problematic alien invasive species—The American bullfrog. Divers. Distrib. 13, 476–485. https://doi.org/10.1111/j.1472-4642.2007.00377.x (2007).Article 

    Google Scholar 
    Orchard, S. A. Removal of the American bullfrog, Rana (Lithobates) catesbeiana, from a pond and a lake on Vancouver Island, British Columbia, Canada Island invasives: Eradication and management. IUCN (Gland, Switzerland). 2011, 1–542 (2011).
    Google Scholar 
    Oh, H. S. & Hong, C. E. Current conditions of habitat for Rana catesbeiana and Trachemys scripta elegans imported to Jeju-do, including proposed management plans. J. Ecol. Environ. 21, 311–317 (2007).
    Google Scholar 
    Park, D. et al. Conservation of amphibians in South Korea. Das, M. Wilkinson, and H. Heatwole (eds.). (2014).Groffen, J., Kong, S., Jang, Y. & Borzee, A. The invasive American bullfrog (Lithobates catesbeianus) in the Republic of Korea: history and recommendations for population control. Manag. Biol. Invasions. 10, 517. https://doi.org/10.3391/mbi.2019.10.3.08 (2019).Article 

    Google Scholar 
    Jang, H. J. & Suh, J. H. Distribution of amphibian species in South Korea. Korean J. Herpetol. 2, 45–51 (2010).
    Google Scholar 
    Kim, J. B. Taxonomic list and distribution of Korean amphibians. Korean J. Herpetol. 1, 1–13. https://doi.org/10.5145/KJCM.2010.13.3.144 (2010).CAS 
    Article 

    Google Scholar 
    Liu, X., McGarrity, M. E. & Li, Y. The influence of traditional Buddhist wildlife release on biological invasions. Conserv. Lett. 5, 107–114. https://doi.org/10.1111/j.1755-263X.2011.00215.x (2012).Article 

    Google Scholar 
    Snow, N. P. & Witmer, G. American bullfrogs as invasive species: a review of the introduction, subsequent problems, management options, and future directions. Proc. Vertebrate Pest Conf. 24, 86–89. https://doi.org/10.5070/V424110490 (2010).Article 

    Google Scholar 
    Lee, J. H., & Park, D. The encyclopedia of Korean amphibians. (Nature and Ecology, 2016).Park, C. D., Lee, C. W., Lim, J. C., Yang, B. G. & Lee, J. H. A study on the diet items of American Bullfrog (Lithobates catesbeianus) in Ga-hang Wetland Korea. J. Ecol. Environ. 32, 55–65. https://doi.org/10.13047/KJEE.2018.32.1.55 (2018).Article 

    Google Scholar 
    Kim, H. W., Adhikari, P., Chang, M. H. & Seo, C. Potential distribution of amphibians with different habitat characteristics in response to climate change in South Korea. Animals 11, 2185. https://doi.org/10.3390/ani11082185 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Adhikari, P., Kim, B. J., Hong, S. H. & Lee, D. H. Climate change induced habitat expansion of nutria (Myocastor coypus) in South Korea. Sci. Rep. 12, 1–12. https://doi.org/10.1038/s41598-022-07347-5 (2022).CAS 
    Article 

    Google Scholar 
    Shim, J. H. et al. A study to determine factors affecting bullfrog decline in Korea. Gwacheon, Republic of Korea. 38. (2005).Ra, N. Y. et al. Habitat requirements of the Gold-spotted pond frog (Rana chosenica): Implications for conservation and management plans. In 63th Annual Meeting of the Korean Association of Biological Sciences. (2008).Ministry of Environment. Act on the conservation and use of biological diversity. (2020).Bellard, C., Genovesi, P. & Jeschke, J. M. Global patterns in threats to vertebrates by biological invasions. Proc. R. Soc. B: Biol. Sci. 283, 20152454. https://doi.org/10.1098/rspb.2015.2454 (2016).Article 

    Google Scholar 
    Blackburn, T. M., Bellard, C. & Ricciardi, A. Alien versus native species as drivers of recent extinctions. Front. Ecol. Environ. 17, 203–207. https://doi.org/10.1002/fee.2020 (2019).Article 

    Google Scholar 
    Marino, C., Leclerc, C. & Bellard, C. Profiling insular vertebrates prone to biological invasions: What makes them vulnerable?. Glob. Change Biol. 28, 1077–1090. https://doi.org/10.1111/gcb.15941 (2022).CAS 
    Article 

    Google Scholar 
    Pearl, C. A., Adams, M. J., Bury, R. B. & McCreary, B. Asymmetrical effects of introduced bullfrogs (Rana catesbeiana) on native ranid frogs in Oregon. Copeia 2004, 11–20. https://doi.org/10.1643/CE-03-010R2 (2004).Article 

    Google Scholar 
    Wu, Z., Li, Y., Wang, Y. & Adams, M. J. Diet of introduced Bullfrogs (Rana catesbeiana): predation on and diet overlap with native frogs on Daishan Island, China. J. Herpetol. 39, 668–674. https://doi.org/10.1670/78-05N.1 (2005).Article 

    Google Scholar 
    Liu, X. et al. Diet and prey selection of the Invasive American bullfrog (Lithobates catesbeianus) in southwestern China. Asian Herpetol. Res. 6, 34–44. https://doi.org/10.16373/j.cnki.ahr.140044 (2015).Article 

    Google Scholar 
    Wang, Y., Wang, Y., Lu, P., Zhang, F. & Li, Y. Diet composition of post-metamorphic bullfrogs (Rana catesbeiana) in the Zhoushan archipelago, Zhejiang Province, China. Front. Biol. China. 3, 219–226. https://doi.org/10.1007/s11515-008-0036-8 (2008).CAS 
    Article 

    Google Scholar 
    Da Silva, E. T., Dos Reis, E. P., Feio, R. N. & Ribeiro Filho, O. P. Diet of the invasive frog Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae) in Viçosa, Minas Gerais State, Brazil. S. Am. J. Herpetol. 4, 286–294. https://doi.org/10.2994/057.004.031 (2009).Article 

    Google Scholar 
    Ortíz-Serrato, L., Ruiz-Campos, G. & Valdez-Villavicencio, J. H. Diet of the exotic American bullfrog, Lithobates catesbeianus, in a stream of northwestern Baja California, Mexico. West. N. Am. Nat. 74, 116–122. https://doi.org/10.3398/064.074.0112 (2014).Article 

    Google Scholar 
    Ryan, M. J. The reproductive behavior of the bullfrog (Rana catesbeiana). Copeia 1, 108–114 (1980).Article 

    Google Scholar 
    Gahl, M. K., Calhoun, A. J. & Graves, R. Facultative use of seasonal pools by American bullfrogs (Rana catesbeiana). Wetlands 29, 697–703. https://doi.org/10.1672/08-56.1 (2009).Article 

    Google Scholar 
    Louette, G., Devisscher, S. & Adriaens, T. Control of invasive American bullfrog Lithobates catesbeianus in small shallow water bodies. Eur. J. Wildl. Res. 59, 105–114 (2013).Article 

    Google Scholar 
    Descamps, S. & De Vocht, A. Movements and habitat use of the invasive species Lithobates catesbeianus in the valley of the Grote Nete (Belgium). Belg. J. Zool. 146, 90–100. https://doi.org/10.26496/bjz.2016.44 (2016).Article 

    Google Scholar 
    Willis, Y. L., Moyle, D. L. & Baskett, T. S. Emergence, breeding, hibernation, movements and transformation of the bullfrog, Rana catesbeiana in Missouri. Copeia 1956, 30–41 (1956).Article 

    Google Scholar 
    Cooper, M. C. Movement, Habitat, and Home Range of Introduced Bullfrogs (Lithobates Catesbeianus) on Mad River Gravel Ponds (Humboldt Co., CA, USA), With Implications for Hydro-Modification as a Method of Management. Dissertation, Humboldt State University. https://digitalcommons.humboldt.edu/etd/40 (2017).Updated guidelines for reporting animal research. Percie du Sert, N. et al. The ARRIVE guidelines 2.0. J. Cereb. Blood Flow Metab. 40, 1769–1777. https://doi.org/10.1177/0271678X20943823 (2020).Article 

    Google Scholar 
    Stebbins, R. C. A Field Guide to Western Reptiles and Amphibians (Houghton Mifflin, 2003).
    Google Scholar 
    Howard, R. D. Alternative mating behaviors of young male bullfrogs. Am. Zool. 24, 397–406. https://doi.org/10.1093/icb/24.2.397 (1984).Article 

    Google Scholar 
    Lee, J. H., Jang, H. J., & Suh, J. H. Ecological Guide Book of Herpetofauna in Korea. 56–142 (National Institute of Environmental Research, 2011).Schmidt, K. & Schwarzkopf, L. Visible implant elastomer tagging and toe-clipping: Effects of marking on locomotor performance of frogs and skinks. Herpetol. J. 20, 99–105 (2010).
    Google Scholar 
    Heyer, R., Donnelly, M. A., Foster, M., & Mcdiarmid, R. Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. (Smithsonian Institution, 2014).Muths, E. A radio transmitter belt for small ranid frogs. Herpetol. Rev. 34, 345–347 (2003).
    Google Scholar 
    McGarrity, M. E. & Johnson, S. A. A radio telemetry study of invasive Cuban treefrogs. Florida Sci. 73, 225–235 (2010).
    Google Scholar 
    Stinner, J., Zarlinga, N. & Orcutt, S. Overwintering behavior of adult bullfrogs, Rana catesbeiana, in northeastern Ohio. Ohio. J. Sci. 94, 8–13 (1994).
    Google Scholar 
    Wassens, S., Watts, R. J., Jansen, A. & Roshier, D. Movement patterns of southern bell frogs (Litoria raniformis) in response to flooding. Wildl. Res. 35, 50–58. https://doi.org/10.1071/WR07095 (2008).Article 

    Google Scholar 
    Bury, R. B., & Whelan, J. A. Ecology and management of the bullfrog (Vol. 155) (US Department of the Interior, Fish and Wildlife Service, 1985).Sepulveda, A. J. & Layhee, M. Description of fall and winter movements of the introduced American Bullfrog (Lithobates catesbeianus) in a Montana, USA, pond. Herpetol. Conserv. Biol. 10, 978–984 (2015).
    Google Scholar 
    Ingram, W. M. & Raney, E. C. Additional studies on the movement of tagged bullfrogs, Rana catesbeiana Shaw. Am. Midl. Nat. 29, 239–241 (1943).Article 

    Google Scholar 
    Wang, Y. & Li, Y. Habitat selection by the introduced American bullfrog (Lithobates catesbeianus) on Daishan Island, China. J. Herpetol. 43, 205–211. https://doi.org/10.1670/0022-1511-43.2.205 (2009).Article 

    Google Scholar 
    Werner, E. E., Wellborn, G. A. & McPeek, M. A. Diet composition in postmetamorphic bullfrogs and green frogs: implications for interspecific predation and competition. J. Herpetol. 29, 600–607 (1995).Article 

    Google Scholar 
    Yoo, M. S., Ra, C. H., Kwon, H. B., Kim, J. Y. & Kang, S. G. Reproductive cycle and maturation induction of oocytes in Rana rugosa. Korean J. Zool. 38, 96–105 (1995).
    Google Scholar 
    Chung, H. H. A Study on the Ecological Characteristics, Capture and Use of Bullfrog. Dissertation, Chosun University. (2002).Hirai, T. Diet composition of introduced bullfrog, Rana catesbeiana, in the Mizorogaike Pond of Kyoto, Japan. Ecol. Res. 19, 375–380. https://doi.org/10.1111/j.1440-1703.2004.00647.x (2004).Article 

    Google Scholar 
    Quagliata, S., Delfino, G., Giachi, F. & Malentacchi, C. Chemical skin defence in the Eastern fire-bellied toad Bombina orientalis: an ultrastructural approach to the mechanism of poison gland rehabilitation after discharge. Acta. Herpetol. https://doi.org/10.1400/181560 (2008).Article 

    Google Scholar 
    Lee, J. H. & Park, D. Effects of body size, operational sex ratio, and age on pairing by the Asian toad, Bufo stejnegeri. Zool. Stud. 48, 334–332 (2009).
    Google Scholar 
    Kim, I. H., Ham, C. H., Jang, S. W., Kim, E. Y. & Kim, J. B. Determination of breeding season, and daily pattern of calling behavior of the endangered Suweon-tree frog (Hyla suweonensis). Korean J. Herpetol. 4, 23–29 (2012).
    Google Scholar 
    Jancowski, K. & Orchard, S. Stomach contents from invasive American bullfrogs Rana catesbeiana (= Lithobates catesbeianus) on southern Vancouver Island, British Columbia, Canada. NeoBiota. 16, 17–37. https://doi.org/10.3897/neobiota.16.3806 (2013).Article 

    Google Scholar 
    An, D. & Waldman, B. Enhanced call effort in Japanese tree frogs infected by amphibian chytrid fungus. Biol. Lett. 12, 20160018. https://doi.org/10.1098/rsbl.2016.0018 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Borzée, A. et al. Temporal and spatial differentiation in microhabitat use: Implications for reproductive isolation and ecological niche specification. Integr. Zool. 11, 375–387. https://doi.org/10.1111/1749-4877.12200 (2016).Article 
    PubMed 

    Google Scholar 
    Borzee, A. et al. Yellow sea mediated segregation between North East Asian Dryophytes species. PLoS ONE 15, e0234299. https://doi.org/10.1371/journal.pone.0234299 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Park, J. K., Kim, J. B. & Do, Y. Examination of physiological and morphological differences between farm-bred and wild black-spotted pond frogs (Pelophylax nigromaculatus). Life. 11, 1089. https://doi.org/10.3390/life11101089 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Peterson, A. C., Richgels, K. L., Johnson, P. T. & McKenzie, V. J. Investigating the dispersal routes used by an invasive amphibian, Lithobates catesbeianus, in human-dominated landscapes. Biol. Invasions. 15, 2179–2191. https://doi.org/10.1007/s10530-013-0442-y (2013).Article 

    Google Scholar 
    Austin, J. D., Dávila, J. A., Lougheed, S. C. & Boag, P. T. Genetic evidence for female-biased dispersal in the bullfrog, Rana catesbeiana (Ranidae). Mol. Ecol. 12, 3165–3172. https://doi.org/10.1046/j.1365-294X.2003.01948.x (2003).Article 
    PubMed 

    Google Scholar 
    Doubledee, R. A., Muller, E. B. & Nisbet, R. M. Bullfrogs, disturbance regimes, and the persistence of California red-legged frogs. J. Wildl. Manage. 67, 424–438 (2003).Article 

    Google Scholar 
    Hanselmann, R. et al. Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biol. Conserv. 120, 115–119. https://doi.org/10.1016/j.biocon.2004.02.013 (2004).Article 

    Google Scholar 
    Adams, M. J., & Pearl, C. A. Problems and opportunities managing invasive bullfrogs: is there any hope? In Biological Invaders in Inland Waters: Profiles, Distribution, and Threats. 679–693 (Springer, 2007).Fisher, M. C. & Garner, T. W. The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal. Biol. Rev. 21, 2–9. https://doi.org/10.1016/j.fbr.2007.02.002 (2007).Article 

    Google Scholar 
    IUCN. The IUCN Red List of Threatened Species. Version 2021–3. https://www.iucnredlist.org. Accessed on [10.02.2022].Ministry of Environment. Enforcement decree of the wildlife protection and management act. (2018). More

  • in

    The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs

    Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F. & Bronstein, J. L. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13, 1459–1474 (2010).Article 

    Google Scholar 
    Idjadi, J. & Edmunds, P. Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar. Ecol. Prog. Ser. 319, 117–127 (2006).Article 

    Google Scholar 
    Norström, A., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 295–306 (2009).Article 

    Google Scholar 
    Richardson, L. E., Graham, N. A. J., Pratchett, M. S., Eurich, J. G. & Hoey, A. S. Mass coral bleaching causes biotic homogenization of reef fish assemblages. Glob. Chang. Biol. 24, 3117–3129 (2018).PubMed 
    Article 

    Google Scholar 
    Wilson, S. K., Graham, N. A. J., Pratchett, M. S., Jones, G. P. & Polunin, N. V. C. Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob. Chang. Biol. 12, 2220–2234 (2006).Article 

    Google Scholar 
    Apprill, A. The role of symbioses in the adaptation and stress responses of marine organisms. Ann. Rev. Mar. Sci. 12, 291–314 (2020).Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do Vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31, 689–699 (2016).PubMed 
    Article 

    Google Scholar 
    Voolstra, C. R. & Ziegler, M. Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. BioEssays 42, e2000004 (2020).Webster, N. S. & Reusch, T. B. H. Microbial contributions to the persistence of coral reefs. ISME J. 11, 2167–2174 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wilkins, L. G. E. et al. Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol. 17, e3000533 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776–788 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Egerton, S., Culloty, S., Whooley, J., Stanton, C. & Ross, R. P. The gut microbiota of marine fish. Front. Microbiol. 9, 873 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Llewellyn, M. S., Boutin, S., Hoseinifar, S. H. & Derome, N. Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front. Microbiol. 5, 1–1 (2014).Article 

    Google Scholar 
    Tarnecki, A. M., Burgos, F. A., Ray, C. L. & Arias, C. R. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J. Appl. Microbiol. 123, 2–17 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang, A. R., Ran, C., Ringø, E. & Zhou, Z. G. Progress in fish gastrointestinal microbiota research. Rev. Aquac. 10, 626–640 (2018).Article 

    Google Scholar 
    Legrand, T. P. R. A., Wynne, J. W., Weyrich, L. S. & Oxley, A. P. A. A microbial sea of possibilities: current knowledge and prospects for an improved understanding of the fish microbiome. Rev. Aquac. 12, 1101–1134 (2019).Rawls, J. F., Mahowald, M. A., Ley, R. E. & Gordon, J. I. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423–433 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shade, A. & Handelsman, J. Beyond the Venn diagram: the hunt for a core microbiome. Environ. Microbiol. 14, 4–12 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sullam, K. E. et al. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol. 21, 3363–3378 (2012).PubMed 
    Article 

    Google Scholar 
    Ainsworth, T. D. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261–2274 (2015).CAS 
    Article 

    Google Scholar 
    Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio. 7, e00560–16 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Roeselers, G. et al. Evidence for a core gut microbiota in the zebrafish. ISME J. 5, 1595–1608 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Clements, K. D., Angert, E. R., Montgomery, W. L. & Choat, J. H. Intestinal microbiota in fishes: what’s known and what’s not. Mol. Ecol. 23, 1891–1898 (2014).PubMed 
    Article 

    Google Scholar 
    Jones, J. et al. The microbiome of the gastrointestinal tract of a range-shifting marine herbivorous fish. Front. Microbiol. 9, 2000 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Miyake, S., Ngugi, D. K. & Stingl, U. Diet strongly influences the gut microbiota of surgeonfishes. Mol. Ecol. 24, 656–672 (2015).PubMed 
    Article 

    Google Scholar 
    Ngugi, D. K. et al. Genomic diversification of giant enteric symbionts reflects host dietary lifestyles. Proc. Natl Acad. Sci. USA 114, E7592–E7601 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Degregori, S., Casey, J. M. & Barber, P. H. Nutrient pollution alters the gut microbiome of a territorial reef fish. Mar. Pollut. Bull. 169, 112522 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gómez, G. D. & Balcázar, J. L. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol. Med. Microbiol. 52, 145–154 (2008).PubMed 
    Article 
    CAS 

    Google Scholar 
    Butt, R. L. & Volkoff, H. Gut microbiota and energy homeostasis in fish. Front. Endocrinol. 10, 9 (2019).Article 

    Google Scholar 
    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bellwood, D. R. et al. Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. J. Evol. Biol. 23, 335–349 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Berumen, M., S., M. & McCormick, M. Within-reef differences in diet and body condition of coral-feeding butterflyfishes (Chaetodontidae). Mar. Ecol. Prog. Ser. 287, 217–227 (2005).Article 

    Google Scholar 
    Pratchett, M. S. Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar. Biol. 148, 373–382 (2005).Article 

    Google Scholar 
    Nagelkerken, I., van der Velde, G., Wartenbergh, S. L. J., Nugues, M. M. & Pratchett, M. S. Cryptic dietary components reduce dietary overlap among sympatric butterflyfishes (Chaetodontidae). J. Fish. Biol. 75, 1123–1143 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bouchon & Harmelin-Vivien Impact of coral degradation on a chaetodontid fish assemblage, Moorea, French Polynesia. Fifth Int. Coral Tahiti 5, 427–432 (1985).
    Google Scholar 
    Graham, N. A. J. Ecological versatility and the decline of coral feeding fishes following climate driven coral mortality. Mar. Biol. 153, 119–127 (2007).Article 

    Google Scholar 
    Pratchett, M. S., Wilson, S. K. & Baird, A. H. Declines in the abundance of Chaetodon butterflyfishes following extensive coral depletion. J. Fish. Biol. 69, 1269–1280 (2006).Article 

    Google Scholar 
    Birkeland & Neudecker. Foraging behavior of two Caribbean Chaetodontids: Chaetodon capistratus and C. aculeatus. Copeia 1981, 169–178 (1981).Gore, M. A. Factors affecting the feeding behavior of a coral reef fish, Chaetodon capistratus. Bull. Mar. Sci. 35, 211–220 (1984).
    Google Scholar 
    Liedke, A. M. R. et al. Resource partitioning by two syntopic sister species of butterflyfish (Chaetodontidae). J. Mar. Biol. Assoc. UK 98, 1767–1773 (2018).CAS 
    Article 

    Google Scholar 
    Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl Acad. Sci. USA 114, 3660–3665 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 17121 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ricaboni, D., Mailhe, M., Khelaifia, S., Raoult, D. & Million, M. Romboutsia timonensis, a new species isolated from human gut. N. Microbes N. Infect. 12, 6–7 (2016).CAS 
    Article 

    Google Scholar 
    Zhang, L. et al. Characterization of the microbial community structure in intestinal segments of yak (Bos grunniens). Anaerobe 61, 102115 (2020).Gerritsen, J. et al. A comparative and functional genomics analysis of the genus Romboutsia provides insight into adaptation to an intestinal lifestyle. Preprint at bioRxiv https://doi.org/10.1101/845511 (2019).Fernández-Cadena, J. C. et al. Detection of sentinel bacteria in mangrove sediments contaminated with heavy metals. Mar. Pollut. Bull. 150, 110701 (2020).Williams, B., Landay, A. & Presti, R. M. Microbiome alterations in HIV infection a review. Cell. Microbiol. 18, 645–651 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ahmed, H. I., Herrera, M., Liew, Y. J. & Aranda, M. Long-term temperature stress in the Coral Model Aiptasia supports the ‘Anna Karenina principle’ for bacterial microbiomes. Front. Microbiol. 10, 975 (2019).Beatty, D. S. et al. Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen. Sci. Adv. 5, eaay1048 (2019).Zaneveld, J. R. et al. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7, 11833 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ma, Q. et al. Impact of microbiota on central nervous system and neurological diseases: the gut-brain axis. J. Neuroinflammation 16, 53 (2019).Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6, 46 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Johnson, K. V. A. & Foster, K. R. Why does the microbiome affect behaviour? Nat. Rev. Microbiol. 16, 647–655 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Werbner, M. et al. Social-stress-responsive microbiota induces stimulation of self-reactive effector T helper cells. mSystems 4, e00292-18 (2019).Keith, S. A. et al. Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nat. Clim. Chang. 8, 986–991 (2018).Article 

    Google Scholar 
    Thompson, C. A., Matthews, S., Hoey, A. S. & Pratchett, M. S. Changes in sociality of butterflyfishes linked to population declines and coral loss. Coral Reefs 38, 527–537 (2019).Article 

    Google Scholar 
    Almany, G. R. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141, 105–113 (2004).PubMed 
    Article 

    Google Scholar 
    Clinchy, M., Sheriff, M. J. & Zanette, L. Y. Predator-induced stress and the ecology of fear. Funct. Ecol. 27, 56–65 (2013).Article 

    Google Scholar 
    Bolnick, D. I., Svanbäck, R., Araújo, M. S. & Persson, L. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc. Natl Acad. Sci. USA 104, 10075–10079 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Svanbäck, R. & Bolnick, D. I. Intraspecific competition drives increased resource use diversity within a natural population. Proc. R. Soc. B Biol. Sci. 274, 839–844 (2007).Article 

    Google Scholar 
    Neudecker, S. Foraging patterns of Chaetodontid and Pomacanthis fishes at St. Croix (U.S. Virgin Islands). Proc. Fifth International Coral Reef Symposium. 415–414 (1985).Lasker, H. Prey preferences and browsing pressure of the butterflyfish Chaetodon capistratus on Caribbean gorgonians. Mar. Ecol. Prog. Ser. 21, 213–220 (1985).Article 

    Google Scholar 
    Cole, A. J., Pratchett, M. S. & Jones, G. P. Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish Fish. 9, 286–307 (2008).Article 

    Google Scholar 
    Pratchett, M. S., Wilson, S. K., Berumen, M. L. & McCormick, M. I. Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23, 352–356 (2004).Article 

    Google Scholar 
    Fishelson, L., Montgomery, W. L. & Myrberg, A. A. A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: teleostei) from the red sea. Science 229, 49–51 (1985).Article 

    Google Scholar 
    Miyake, S., Ngugi, D. K. & Stingl, U. Phylogenetic diversity, distribution, and cophylogeny of giant bacteria (Epulopiscium) with their surgeonfish hosts in the Red Sea. Front. Microbiol. 7, 285 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Choat, J. H., Robbins, W. & Clements, K. The trophic status of herbivorous fishes on coral reefs II. Mar. Biol. 145, 445–454 (2004).Article 

    Google Scholar 
    Elifantz, H., Horn, G., Ayon, M., Cohen, Y. & Minz, D. Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiol. Ecol. 85, 348–357 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pujalte, M. J., Lucena, T., Ruvira, M. A., Arahal, D. R. & Macián, M. C. In The Prokaryotes: Alphaproteobacteria and Betaproteobacteria (Springer, 2014).Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280–2292 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sunagawa, S. et al. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512–521 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J. 8, 31–39 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Morrow, K. M., Moss, A. G., Chadwick, N. E. & Liles, M. R. Bacterial associates of two caribbean coral species reveal species-specific distribution and geographic variability. Appl. Environ. Microbiol. 78, 6438–6449 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chiarello, M. et al. Exceptional but vulnerable microbial diversity in coral reef animal surface microbiomes. Proc. R. Soc. B Biol. Sci. 287, 20200642 (2020).Article 

    Google Scholar 
    Sunagawa, S., Woodley, C. M. & Medina, M. Threatened corals provide underexplored microbial habitats. PLoS ONE 5, e9554 (2010).Zhang, C. et al. Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME J. 10, 2235–2245 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Uren Webster, T. M. et al. Environmental plasticity and colonisation history in the Atlantic salmon microbiome: a translocation experiment. Mol. Ecol. 29, 886–898 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Fietz, K. et al. Mind the gut: genomic insights to population divergence and gut microbial composition of two marine keystone species. Microbiome 6, 82 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Smith, C. C., Snowberg, L. K., Caporaso, J. G., Knight, R. & Bolnick, D. I. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 9, 2515 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Uren Webster, T. M., Consuegra, S., Hitchings, M. & Garcia de Leaniz, C. Interpopulation variation in the Atlantic salmon microbiome reflects environmental and genetic diversity. Appl. Environ. Microbiol. 84, e00691-18 (2018).Fiore, C. L., Labrie, M., Jarett, J. K. & Lesser, M. P. Transcriptional activity of the giant barrel sponge, Xestospongia muta holobiont: molecular evidence for metabolic interchange. Front. Microbiol. 6, 364 (2015).Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, C. R. Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci. Rep. 7, 40579 (2017).Pogoreutz, C. et al. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8, 2240–2252 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Reverter, M., Sasal, P., Tapissier-Bontemps, N., Lecchini, D. & Suzuki, M. Characterisation of the gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems. FEMS Microbiol. Ecol. 93 (2017).Parris, D. J., Brooker, R. M., Morgan, M. A., Dixson, D. L. & Stewart, F. J. Whole gut microbiome composition of damselfish and cardinalfish before and after reef settlement. PeerJ 4, e2412 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Reese, E. S. Coevolution of corals and coral feeding fishes of the family Chaetodontidae. In Proc. 3rd International Coral Reef Symposium, 267–274 (Rosenstiel School of Marine and Atmospheric Science, Miami, Florida., 1977).Hammer, T. J. & Bowers, M. D. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1–14 (2015).Kohl, K. D., Weiss, R. B., Cox, J., Dale, C. & Denise Dearing, M. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17, 1238–1246 (2014).PubMed 
    Article 

    Google Scholar 
    Emslie, M. J., Pratchett, M. S., Cheal, A. J. & Osborne, K. Great Barrier Reef butterflyfish community structure: the role of shelf position and benthic community type. Coral Reefs 29, 705–715 (2010).Article 

    Google Scholar 
    Noble, M. M., Pratchett, M. S., Coker, D. J., Cvitanovic, C. & Fulton, C. J. Foraging in corallivorous butterflyfish varies with wave exposure. Coral Reefs 33, 351–361 (2014).Article 

    Google Scholar 
    Greb, L. et al. Ökologie und Sedimentologie eines rezenten Rampensystems an der Karibikküste von Panamá (Inst. für Geologie und Paläontologie, Stuttgart, 1996).Aronson, R., Hilbun, N., Bianchi, T., Filley, T. & McKee, B. Land use, water quality, and the history of coral assemblages at Bocas del Toro, Panamá. Mar. Ecol. Prog. Ser. 504, 159–170 (2014).Article 

    Google Scholar 
    Collin, R., D’Croz, L., Gondola, P. & Del Rosario, J. B. Climate and hydrological factors affecting variation in chlorophyll concentration and water clarity in the Bahia Almirante, Panama. Smithson. Contrib. Mar. Sci. 323–334 (2009).D’Croz, L., Rosario, J. B.del. & Gondola, P. The effect of fresh water runoff on the distribution of dissolved inorganic nutrients and plankton in the Bocas del Toro Archipelago, Caribbean Panamá. Caribb. J. Sci. 41, 414–429 (2005).
    Google Scholar 
    Seemann, J. et al. Assessing the ecological effects of human impacts on coral reefs in Bocas del Toro, Panama. Environ. Monit. Assess. 186, 1747–1763 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Guzmán, H. M., Barnes, P. A. G., Lovelock, C. E. & Feller, I. C. A site description of the CARICOMP mangrove, seagrass and coral reef sites in Bocas del Toro, Panamá. Caribb. J. Sci. 41, 430–440 (2005).
    Google Scholar 
    Beijbom, O. et al. Towards automated annotation of benthic survey images: variability of human experts and operational modes of automation. PLoS ONE 10, e0130312 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Rocha, L. A., Jogan, J., Király, G., Feráková, V. & Bernhardt, K.-G. Chaetodon capistratus. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2010-4.RLTS.T165695A6094300.en (2010).Froese, R. & D. P. E. FishBase. FishBase. 2019. www.fishbase.org (2020)Smith, L. C. National Audubon Society Field Guide to Tropical Marine Fishes Caribbean, Gulf of Mexico, Florida, Bahamas, Bermuda (Alfred A. Knopf, 1997).Nguyen, B. N. et al. Environmental DNA survey captures patterns of fish and invertebrate diversity across a tropical seascape. Sci. Rep. 10, 1–14 (2020).Article 
    CAS 

    Google Scholar 
    Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).Article 

    Google Scholar 
    Weber, L. et al. EMP 16S Illumina amplicon protocol. https://doi.org/10.17504/protocols.io.nuudeww (2018).R Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria, 2019).
    Google Scholar 
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10 (2011).Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wright, E. S. Using DECIPHER v2.0 to analyze big biological sequence data in R. R. J. 8, 352–359 (2016).Article 

    Google Scholar 
    Schliep, K., Potts, A. J., Morrison, D. A. & Grimm, G. W. Intertwining phylogenetic trees and networks. Methods Ecol. Evol. 8, 1212–1220 (2017).Article 

    Google Scholar 
    Weiss, S. et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5, 27 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Astudillo-García, C. et al. Evaluating the core microbiota in complex communities: a systematic investigation. Environ. Microbiol. 19, 1450–1462 (2017).PubMed 
    Article 

    Google Scholar 
    Dufrêne, M. & Legendre, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).
    Google Scholar 
    Roberts, D. W. labdsv: ordination and multivariate analysis for ecology. (2019).Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    Leray, M. & Knowlton, N. Random sampling causes the low reproducibility of rare eukaryotic OTUs in Illumina COI metabarcoding. PeerJ 5, e3006 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hill, M. O. Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432 (1973).Article 

    Google Scholar 
    Alberdi, A. & Gilbert, M. T. P. A guide to the application of Hill numbers to DNA‐based diversity analyses. Mol. Ecol. Resour. 19, 1755–0998.13014 (2019).
    Google Scholar 
    Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).Article 

    Google Scholar 
    Chiu, C. H. & Chao, A. Estimating and comparing microbial diversity in the presence of sequencing errors. PeerJ 2016, e1634 (2016).Article 
    CAS 

    Google Scholar 
    Oksanen, J. et al. Community Ecology Package. Vienna R Found. Stat. Comput. https://doi.org/10.4135/9781412971874.n145 (2012).Chen, J. et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28, 2106–2113 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576–1585 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jaccard, P. The distribution of the flora in the alpine zone.1. N. Phytol. 11, 37–50 (1912).Article 

    Google Scholar 
    Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693 (2006).PubMed 
    Article 

    Google Scholar 
    Bray, J. R. & Curtis, J. T. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27, 325–349 (1957).Article 

    Google Scholar 
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 
    Anderson, M. J. & Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol. Monogr. 83, 557–574 (2013).Article 

    Google Scholar 
    Martinez Arbizu, P. pairwiseAdonis: pairwise multilevel comparison using adonis. R package version 0.3. https://github.com/pmartinezarbizu/pairwiseAdonis (2019).Roesch, L. F. W. et al. Pime: a package for discovery of novel differences among microbial communities. Mol. Ecol. Resour. 20, 415–428 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).Article 

    Google Scholar 
    Klaus, J. S., Janse, I., Heikoop, J. M., Sanford, R. A. & Fouke, B. W. Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ. Microbiol. 9, 1291–1305 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ward, R. J. et al. Gastrointestinal Bacterial Symbionts: Reproductive Strategy and Community Structure. Thesis, Cornell Univ. (2009).Séré, M. G. et al. Bacterial communities associated with Porites White Patch Syndrome (PWPS) on three Western Indian Ocean (WIO) coral reefs. PLoS ONE 8, e83746 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Moran, D., Turner, S. J. & Clements, K. D. Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microb. Ecol. 49, 590–597 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mausz, M., Schmitz-Esser, S. & Steiner, G. Identification and comparative analysis of the endosymbionts of Loripes lacteus and Anodontia fragilis (Bivalvia: Lucinidae). (University of Vienna, 2008).Bano, N., DeRae Smith, A., Bennett, W., Vasquez, L. & Hollibaugh, J. T. Dominance of mycoplasma in the guts of the long-jawed mudsucker, Gillichthys mirabilis, from five California salt marshes. Environ. Microbiol. 9, 2636–2641 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Frade, P. R., Roll, K., Bergauer, K. & Herndl, G. J. Archaeal and Bacterial Communities associated with the surface mucus of Caribbean corals differ in their degree of host specificity and community turnover over reefs. PLoS ONE 11, e0144702 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kimes, N. E. et al. The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline. Environ. Microbiol. 15, 2082–2094 (2013).PubMed 
    Article 

    Google Scholar 
    Smriga, S., Sandin, S. A. & Azam, F. Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol. Ecol. 73, no–no (2010).Article 
    CAS 

    Google Scholar 
    Zhang, X. et al. Effects of dietary supplementation of Ulva pertusa and non-starch polysaccharide enzymes on gut microbiota of Siganus canaliculatus. J. Oceanol. Limnol. 36, 438–449 (2018).CAS 
    Article 

    Google Scholar 
    Klaus, J. S., Janse, I. & Fouke, B. W. Coral black band disease microbial communities and genotypic variability of the dominant cyanobacteria (CD1C11). Bull. Mar. Sci. 87, 795–821 (2011).Article 

    Google Scholar 
    Lu, J., Santo Domingo, J. W., Hill, S. & Edge, T. A. Microbial diversity and host-specific sequences of Canada goose feces. Appl. Environ. Microbiol. 75, 5919–5926 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ueki, A., Goto, K., Ohtaki, Y., Kaku, N. & Ueki, K. Description of Anaerotignum aminivorans gen. Nov., sp. nov., a strictly anaerobic, amino-acid-decomposing bacterium isolated from a methanogenic reactor, and reclassification of Clostridium propionicum, Clostridium neopropionicum and Clostridium lactatifermentans as species of the genus Anaerotignum. Int. J. Syst. Evol. Microbiol. 67, 4146–4153 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bowman, K. S., Rainey, F. A. & Moe, W. M. Production of hydrogen by Clostridium species in the presence of chlorinated solvents. FEMS Microbiol. Lett. 290, 188–194 (2008).PubMed 
    Article 
    CAS 

    Google Scholar 
    Bueno de Mesquita, C. P., Sartwell, S. A., Schmidt, S. K. & Suding, K. N. Growing‐season length and soil microbes influence the performance of a generalist bunchgrass beyond its current range. Ecology 101, e03095 (2020).Clever, F. et al. The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs. Dryad Datasets. https://doi.org/10.5061/dryad.m905qfv28 (2022).Clever, F. & Scott, J. J. R code for reproducing the statistical analyses and figures of ‘The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs’. Commun. Biol. https://github.com/bocasbiome/web/ (2022). More

  • in

    Stylasterid corals build aragonite skeletons in undersaturated water despite low pH at the site of calcification

    Stocker, T. F. et al. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds T.F. Stocker et al.) Ch. TS, 33–115 (Cambridge University Press, 2013).Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: The other CO2 problem. Ann. Rev. Mar. Sci. 1, 169–192 (2009).PubMed 
    Article 

    Google Scholar 
    Albright, R. et al. Carbon dioxide addition to coral reef waters suppresses net community calcification. Nature 555, 516–519 (2018).ADS 
    PubMed 
    Article 

    Google Scholar 
    Chen, C.-T.A. et al. Deep oceans may acidify faster than anticipated due to global warming. Nat. Clim. Chang. 7, 890–894 (2017).ADS 
    Article 

    Google Scholar 
    Guinotte, J. M. et al. Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals?. Front. Ecol. Environ. 4, 141–146 (2006).Article 

    Google Scholar 
    Figuerola, B. et al. A review and meta-analysis of potential impacts of ocean acidification on marine calcifiers from the southern ocean. Front. Mar. Sci. 8, 584445 (2021).Article 

    Google Scholar 
    Ries, J. B. Skeletal mineralogy in a high-CO2 world. J. Exp. Mar. Biol. Ecol. 403, 54–64 (2011).Article 

    Google Scholar 
    Blackmon, P. D. & Todd, R. Mineralogy of some foraminifera as related to their classification and ecology. J. Paleontol. 33, 1–15 (1959).
    Google Scholar 
    Oliver, W. A. Jr. The relationship of the scleractinian corals to the rugose corals. Paleobiology 6, 146–160 (1980).Article 

    Google Scholar 
    Sinclair, D. J. et al. Reproducibility of trace element profiles in a specimen of the deep-water bamboo coral Keratoisis sp. Geochim. Cosmochim. Acta 75, 5101–5121 (2011).ADS 
    Article 

    Google Scholar 
    Liu, Y.-W., Sutton, J. N., Ries, J. B. & Eagle, R. A. Regulation of calcification site pH is a polyphyletic but not always governing response to ocean acidification. Sci. Adv. 6, eaax1314 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cornwall, C. E. et al. Understanding coralline algal responses to ocean acidification: Meta-analysis and synthesis. Glob. Change Biol. 28, 362–374 (2022).Article 

    Google Scholar 
    Al-Horani, F. A., Al-Moghrabi, S. M. & de Beer, D. Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: Active internal carbon cycle. J. Exp. Mar. Biol. Ecol. 288, 1–15 (2003).Article 

    Google Scholar 
    Al-Horani, F. A., Al-Moghrabi, S. M. & de Beer, D. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar. Biol. 142, 419–426 (2003).Article 

    Google Scholar 
    Le Goff, C. et al. In vivo pH measurement at the site of calcification in an octocoral. Sci. Rep. 7, 11210 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McCulloch, M. et al. Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation. Geochim. Cosmochim. Acta 87, 21–34 (2012).ADS 
    Article 

    Google Scholar 
    Gilbert, P. U. P. A. et al. Biomineralization: Integrating mechanism and evolutionary history. Sci. Adv. 8, eabl9653 (2022).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Donald, H. K., Ries, J. B., Stewart, J. A., Fowell, S. E. & Foster, G. L. Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga. Geochim. Cosmochim. Acta 217, 240–253 (2017).ADS 
    Article 

    Google Scholar 
    Krief, S. et al. Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim. Cosmochim. Acta 74, 4988–5001 (2010).ADS 
    Article 

    Google Scholar 
    Hönisch, B. et al. Assessing scleractinian corals as recorders for paleo-pH: Empirical calibration and vital effects. Geochim. Cosmochim. Acta 68, 3675–3685 (2004).ADS 
    Article 

    Google Scholar 
    Anagnostou, E., Williams, B., Westfield, I., Foster, G. L. & Ries, J. B. Calibration of the pH-δ11B and temperature-Mg/Li proxies in the long-lived high-latitude crustose coralline red alga Clathromorphum compactum via controlled laboratory experiments. Geochim. Cosmochim. Acta 254, 142–155 (2019).ADS 
    Article 

    Google Scholar 
    Cornwall, C. E., Comeau, S. & McCulloch, M. T. Coralline algae elevate pH at the site of calcification under ocean acidification. Glob. Change Biol. 23, 4245–4256 (2017).ADS 
    Article 

    Google Scholar 
    Rosenthal, Y., Lear, C. H., Oppo, D. W. & Linsley, B. K. Temperature and carbonate ion effects on Mg/Ca and Sr/Ca ratios in benthic foraminifera: Aragonitic species Hoeglundina elegans. Paleoceanography 21, PA1007 (2006).ADS 
    Article 

    Google Scholar 
    Gori, A. et al. Physiological response of the cold-water coral Desmophyllum dianthus to thermal stress and ocean acidification. PeerJ 4, e1606 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gagnon, A. C., Gothmann, A. M., Branson, O., Rae, J. W. B. & Stewart, J. A. Controls on boron isotopes in a cold-water coral and the cost of resilience to ocean acidification. Earth Planet. Sci. Lett. 554, 116662 (2021).Article 

    Google Scholar 
    Cairns, S. D. Global diversity of the Stylasteridae (Cnidaria: Hydrozoa: Athecatae). PLoS ONE 6, e21670 (2011).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cairns, S. D. Deep-water corals: An overview with special reference to diversity and distribution of deep-water scleractinian corals. Bull. Mar. Sci. 81, 311–322 (2007).
    Google Scholar 
    Samperiz, A. et al. Stylasterid corals: A new paleotemperature archive. Earth Planet. Sci. Lett. 545, 116407 (2020).Article 

    Google Scholar 
    Cairns, S. D. & Macintyre, I. G. Phylogenetic implications of calcium carbonate mineralogy in the Stylasteridae (Cnidaria: Hydrozoa). Palaios, 96–107 (1992).Anagnostou, E., Huang, K. F., You, C. F., Sikes, E. L. & Sherrell, R. M. Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: Evidence of physiological pH adjustment. Earth Planet. Sci. Lett. 349–350, 251–260 (2012).ADS 
    Article 

    Google Scholar 
    Rae, J. W. B. et al. CO2 storage and release in the deep Southern Ocean on millennial to centennial timescales. Nature 562, 569–573 (2018).ADS 
    PubMed 
    Article 

    Google Scholar 
    Farmer, J. R., Hönisch, B., Robinson, L. F. & Hill, T. M. Effects of seawater-pH and biomineralization on the boron isotopic composition of deep-sea bamboo corals. Geochim. Cosmochim. Acta 155, 86–106 (2015).ADS 
    Article 

    Google Scholar 
    Sutton, J. N. et al. δ11B as monitor of calcification site pH in divergent marine calcifying organisms. Biogeosciences 15, 1447–1467 (2018).ADS 
    Article 

    Google Scholar 
    Heinemann, A. et al. Conditions of Mytilus edulis extracellular body fluids and shell composition in a pH-treatment experiment: Acid-base status, trace elements and δ11B. Geochem. Geophys. Geosyst. 13, 1–17 (2012).Article 

    Google Scholar 
    Rae, J. W. B., Foster, G. L., Schmidt, D. N. & Elliott, T. Boron isotopes and B/Ca in benthic foraminifera: Proxies for the deep ocean carbonate system. Earth Planet. Sci. Lett. 302, 403–413 (2011).ADS 
    Article 

    Google Scholar 
    Auscavitch, S. R. et al. Distribution of deep-water scleractinian and stylasterid corals across abiotic environmental gradients on three seamounts in the Anegada Passage. PeerJ 8, e9523 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    DeCarlo, T. M., Holcomb, M. & McCulloch, M. T. Reviews and syntheses: Revisiting the boron systematics of aragonite and their application to coral calcification. Biogeosciences 15, 2819–2834 (2018).ADS 
    Article 

    Google Scholar 
    McCulloch, M. T., D’Olivo, J. P., Falter, J., Holcomb, M. & Trotter, J. A. Coral calcification in a changing world and the interactive dynamics of pH and DIC upregulation. Nat. Commun. 8, 15686 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Henehan, M. J. et al. Calibration of the boron isotope proxy in the planktonic foraminifera Globigerinoides ruber for use in palaeo-CO2 reconstruction. Earth Planet. Sci. Lett. 364, 111–122 (2013).ADS 
    Article 

    Google Scholar 
    Rink, S., Kühl, M., Bijma, J. & Spero, H. Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa. Mar. Biol. 131, 583–595 (1998).Article 

    Google Scholar 
    Fietzke, J. & Wall, M. Distinct fine-scale variations in calcification control revealed by high-resolution 2D boron laser images in the cold-water coral Lophelia pertusa. Sci. Adv. 8, eabj4172 (2022).PubMed 
    PubMed Central 

    Google Scholar 
    Drake, J. L. et al. How corals made rocks through the ages. Glob. Change Biol. 26, 31–53 (2020).ADS 
    Article 

    Google Scholar 
    Blamart, D. et al. Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa: Implications for biomineralization and paleo-pH. Geochem. Geophys. Geosyst. 8, Q12001 (2007).ADS 
    Article 

    Google Scholar 
    Jurikova, H. et al. Boron isotope composition of the cold-water coral Lophelia pertusa along the Norwegian margin: Zooming into a potential pH-proxy by combining bulk and high-resolution approaches. Chem. Geol. 513, 143–152 (2019).ADS 
    Article 

    Google Scholar 
    NOAA Deep Sea Coral Research & Technology Program. NOAA National Database for Deep-Sea Corals and Sponges (version 20201021-0), https://deepseacoraldata.noaa.gov/ (2017).Dickson, A. G. Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep Sea Res. Part A Oceanogr. Res. Pap. 37, 755–766 (1990).ADS 
    Article 

    Google Scholar 
    Stewart, J. A., Anagnostou, E. & Foster, G. L. An improved boron isotope pH proxy calibration for the deep-sea coral Desmophyllum dianthus through sub-sampling of fibrous aragonite. Chem. Geol. 447, 148–160 (2016).ADS 
    Article 

    Google Scholar 
    Mavromatis, V., Montouillout, V., Noireaux, J., Gaillardet, J. & Schott, J. Characterization of boron incorporation and speciation in calcite and aragonite from co-precipitation experiments under controlled pH, temperature and precipitation rate. Geochim. Cosmochim. Acta 150, 299–313 (2015).ADS 
    Article 

    Google Scholar 
    Holcomb, M., DeCarlo, T. M., Gaetani, G. A. & McCulloch, M. Factors affecting B/Ca ratios in synthetic aragonite. Chem. Geol. 437, 67–76 (2016).ADS 
    Article 

    Google Scholar 
    DeCarlo, T. M., Gaetani, G. A., Holcomb, M. & Cohen, A. L. Experimental determination of factors controlling U/Ca of aragonite precipitated from seawater: Implications for interpreting coral skeleton. Geochim. Cosmochim. Acta 162, 151–165 (2015).ADS 
    Article 

    Google Scholar 
    Reeder, R. J., Nugent, M., Lamble, G. M., Tait, C. D. & Morris, D. E. Uranyl Incorporation into Calcite and Aragonite: XAFS and Luminescence Studies. Environ. Sci. Technol. 34, 638–644 (2000).ADS 
    Article 

    Google Scholar 
    Anagnostou, E. et al. Seawater nutrient and carbonate ion concentrations recorded as P/Ca, Ba/Ca, and U/Ca in the deep-sea coral Desmophyllum dianthus. Geochim. Cosmochim. Acta 75, 2529–2543 (2011).ADS 
    Article 

    Google Scholar 
    Chen, S., Littley, E. F. M., Rae, J. W. B., Charles, C. D. & Adkins, J. F. Uranium distribution and incorporation mechanism in deep-sea corals: Implications for seawater [CO32–] proxies. Front. Earth Sci. 9, 159 (2021).ADS 

    Google Scholar 
    Inoue, M., Suwa, R., Suzuki, A., Sakai, K. & Kawahata, H. Effects of seawater pH on growth and skeletal U/Ca ratios of Acropora digitifera coral polyps. Geophys. Res. Lett. 38, L12809 (2011).ADS 

    Google Scholar 
    Gothmann, A. M. & Gagnon, A. C. The primary controls on U/Ca and minor element proxies in a cold-water coral cultured under decoupled carbonate chemistry conditions. Geochim. Cosmochim. Acta 315, 38–60 (2021).ADS 
    Article 

    Google Scholar 
    Mass, T. et al. Cloning and characterization of four novel coral acid-rich proteins that precipitate carbonates in vitro. Curr. Biol. 23, 1126–1131 (2013).PubMed 
    Article 

    Google Scholar 
    Rogers, A. D. Advances in Marine Biology, Vol. 79 (ed Sheppard, C.) 137–224 (Academic Press, 2018).Rodolfo-Metalpa, R. et al. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat. Clim. Chang. 1, 308–312 (2011).ADS 
    Article 

    Google Scholar 
    Hoarau, L. et al. Unexplored refugia with high cover of scleractinian Leptoseris spp. and hydrocorals Stylaster flabelliformis at lower mesophotic depths (75–100 m) on lava flows at Reunion Island (Southwestern Indian Ocean). Diversity 13, 141 (2021).Article 

    Google Scholar 
    Lindner, A., Cairns, S. D. & Cunningham, C. W. From offshore to onshore: Multiple origins of shallow-water corals from deep-sea ancestors. PLoS ONE 3, e2429 (2008).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stewart, J. A. et al. Refining trace metal temperature proxies in cold-water scleractinian and stylasterid corals. Earth Planet. Sci. Lett. 545, 116412 (2020).Article 

    Google Scholar 
    Seacarb: Seawater Carbonate Chemistry. R package version 3.0.6 .http://CRAN.R-project.org/package=seacarb (2015).Lueker, T. J., Dickson, A. G. & Keeling, C. D. Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: Validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Mar. Chem. 70, 105–119 (2000).Article 

    Google Scholar 
    Lee, K. et al. The universal ratio of boron to chlorinity for the North Pacific and North Atlantic oceans. Geochim. Cosmochim. Acta 74, 1801–1811 (2010).ADS 
    Article 

    Google Scholar 
    Olsen, A. et al. The Global Ocean Data Analysis Project version 2 (GLODAPv2)—An internally consistent data product for the world ocean. Earth Syst. Sci. Data 8, 297–323 (2016).ADS 
    Article 

    Google Scholar 
    Hemming, N. G. & Hanson, G. N. Boron isotopic composition and concentration in modern marine carbonates. Geochim. Cosmochim. Acta 56, 537–543 (1992).ADS 
    Article 

    Google Scholar 
    Zeebe, R. E. & Wolf-Gladrow, D. A. CO2 in Seawater: Equilibrium, Kinetics, Isotopes Vol. 65 (Elsevier, 2001).
    Google Scholar 
    Foster, G. L., Pogge von Strandmann, P. A. E. & Rae, J. W. B. Boron and magnesium isotopic composition of seawater. Geochem. Geophys. Geosyst. 11, Q08015 (2010).ADS 
    Article 

    Google Scholar 
    Klochko, K., Kaufman, A. J., Yao, W., Byrne, R. H. & Tossell, J. A. Experimental measurement of boron isotope fractionation in seawater. Earth Planet. Sci. Lett. 248, 276–285 (2006).ADS 
    Article 

    Google Scholar 
    Stewart, J. A. et al. NIST RM 8301 boron isotopes in marine carbonate (simulated coral and foraminifera solutions): Inter-laboratory δ11B and trace element ratio value assignment. Geostand. Geoanal. Res. 45, 77–96 (2020).Article 

    Google Scholar 
    Foster, G. L. Seawater pH, pCO2 and [CO32−] variations in the Caribbean Sea over the last 130 kyr: A boron isotope and B/Ca study of planktic foraminifera. Earth Planet. Sci. Lett. 271, 254–266 (2008).ADS 
    Article 

    Google Scholar 
    Schlitzer, R. Ocean Data View, Version 4.6.5 http://odv.awi.de, (2021). More

  • in

    Spatial–temporal evolution of ESV and its response to land use change in the Yellow River Basin, China

    Analysis of changes in ecosystem services value in the YRBThe results showed that from 1990 to 2020, the total ecosystem services value in the YRB showed a dynamic trend of decrease-increase–decrease, with overall increasing trend, and a total increase of 31.85 × 1010 USD, with an average annual increase of 1.14 × 1010 USD (Table 2). This changing trend is consistent with land use cover change in the area. In 30a, YRB cultivated land decreased by 8663 km2, due to rapid urbanization. In addition, after year 2000, China began to implement the policy of returning farmland to forest and grassland on a large scale, which accelerated the reduction of cultivated land. Results again showed that the forest area increased by 30,933,093 km2, indicating that the implementation of “returning farmland to forest and grassland”policy achieved great results, thus increased the value of ecosystem services generated by forest land by 167.66 × 1010 USD. Grassland increased by 738 km2, as corresponding ESV increased by 28.73 × 1010 USD, while unused land decreased by 8131 km2, with 9.52 × 1010 USD ESV decrease. In general, the ecological protection and management measures in the YRB have achieved remarkable results, and ecosystem service values has been significantly improved due to forest and grassland increase.Table 2 The value of ecosystem services in the YRB from 1990 to 2020.Full size tableIn terms of ecosystem service structure in the YRB (Table 3), the relative proportions of various ESVs did not change significantly, resulting in relatively stable ESV structure. Soil conservation and waste disposal are the most important among them, accounting for about 37% of ESV’s total value. The YRB ecosystem, as can be seen, emphasises the importance of soil conservation and waste disposal in the basin, with Climate regulation, Biodiversity conservation, and Entertainment accounting for only 11.99 percent of the total. Various services have changed to varying degrees during the study period. Waste disposal and climate regulation, for example, have suffered losses of 22.23 × 1010 USD and 20.29 × 1010 USD, respectively.The rest of the services showed an upward trend, among which the value of the Food production service increased the most, which was 19.03 × 1010 USD, owing to the obvious increase of the forest land and grassland area in the YRB.Table 3 The value of individual ecosystem functions in the YRB from 1990 to 2020.Full size tableSpatial distribution and variation characteristics of ecosystem services in the YRBThe total ESV value of the study area and changes in the value of each service could not reflect their spatial differences. To describe the temporal and spatial distribution pattern of ESV in the study area, the natural breakpoint method was used. This method was further used to classify ESV with reference to existing studies, and divided the area into four levels: low-value, lower-value, higher-value, and high-value areas. Takin the three-level watershed of the YRB as the statistical unit for analysis, the result showed that the higher the level, the higher the ESV. As shown in Fig. 2, from 1990 to 2020, the spatial characteristics of ESV were relatively stable. The YRB’s upper reaches, from Shizuishan to the north bank of Hekou Town, the Fenhe River Basin, from Hekou Town to Longmen, and the Jinghe River Basin are all rich in high-values. The forest and grassland are relatively concentrated in the above-mentioned areas, the ESV coefficient is high, and the watershed area is large, resulting in a high total ESV. The higher value areas are mainly distributed in the areas from Longyang Gorge to Lanzhou main stream basin, the Daxia River and Tao River basin, and the Wei River basin. The area above Baoji Gorge and the inflow area fall in the transition zone between the high-value area and the lower-value area. For example, the transition area between the Loess and Qinghai-Tibet Plateaus is a higher-value area. The lower-value area mainly includes the Huangshui River Basin, the Datong River Basin, the basin below Lanzhou, and the Guanzhong Plain area. Thus, the unused land in this area is widely distributed. Due to the large area of construction land in the Guanzhong Plain, the ecosystem service value has shrunk. The low-value area is found in the YRB’s lower reaches, which contains the most extensive and large area of construction land in the basin, has a poor ecosystem service function, and is also the YRB’s most economically developed area. In terms of changes in the value of watershed ecosystem services, the number of watersheds at the ESV level did not change significantly between 1990 and 2020. The average ESV of the watershed is 40.52 × 1010 USD. There were 7 high-value, 5 higher-value, 12 lower-value, and 5 low-value watersheds respectively. Figure 2Spatial distribution of ESV changes in YRB from 1990 to 2020. (a) 1990, (b) 2000, (c) 2010, (d) 2020.Full size imageThe hotspot analysis revealed the spatial agglomeration characteristics and ESV evolution law in the YRB from 1990 to 2020 (Fig. 3). In most of the YRB, the ESV accumulation characteristics were not significant in space, and significant areas were dominated with high and low ESV accumulation. The Maqu-Longyangxia River Basin, Daxia River and Tao River Basin, the Datong River Basin, and Fen River Basin were the five core areas where ESV had the highest value. The Inner River, YRB’s northern and eastern margins, and the lower reaches are primarily low-value agglomeration areas. The high-value agglomeration area and low-value agglomeration area did not change significantly in space from 1990 to 2020, but the number of grids in each decreased from 647 to 627 and 699 to 681, respectively. In general, the YRB’s high-value agglomeration areas are strewn about, whereas the low-value agglomeration areas are scattered.Figure 3Spatial agglomeration characteristics of ESV in the YRB from 1990 to 2020. (a) 1990, (b) 2000, (c) 2010, (d) 2020.Full size imageFrom 1990 to 2020, the barycenter coordinates of the ESV in the YRB remained stable between 106.78°–106.94° E and 36.40°–36.65° N (Fig. 4). During the study period, the ESV barycenter coordinates showed a transfer trajectory of first to southwest, then to northeast, and then to southwest. From the perspective of overall transfer direction, ESV barycenter shifted from northeast of Huanxian County to southwest from 1990 to 2020. The ESV in the northeast decreased, while that in southeast increased. From 1995 to 2000 and from 2000 to 2005, the migration distance of ESV barycenter in the YRB was longer by 16.33 km and 15.75 km, respectively, while the barycenter migration distance of ESV from 2005 to 2020 was shorter.Figure 4Barycenter coordinates of ecosystem services in the YRB from 1990 to 2020.Full size imageResponse of ecosystem services to land-use changeThe area of land use type change in the YRB increased by 64,356 km2 between 1990 and 2020. Each land type’s area has changed to varying degrees. Cultivated land and construction land are the two land types that have seen the most changes. The area of cultivated land has shrunk by 8663 km2, while the area of construction land has grown by 13,109 km2. In comparison to water, forest, and grassland, unused land has undergone significant transformations. However, in comparison to 1990, it shrunk by 8131 km2 in 2020. The forest increased by 3093 km2 while grassland increased by 738 km2. Ecosystem services are significantly impacted by changes in land use types. Using the spatial analysis method, the researcher introduces a resilience index to reflect ESV’s response to land-use change in this paper. During 1990–2000 and 2000–2010, average elasticity of ESV change in the YRB relative to land use change was 0.27 and 0.44, respectively, but dropped to 0.04 during 2010–2020. This indicates that the disturbance capacity of land-use change on ecosystem services was low between 1990 and 2000, but increased between 2000 and 2010. Land-use change has had less of an impact on ecosystem services since 2010. The range of changes in land land-use types was wide during this time, but the average elasticity index was low because there were so many different types of land land-use changes, such as the conversion of forest land and cultivated land to construction land, and the conversion of forest land and water area to cultivated land. The decrease in ESV caused by the change in land use per unit area was minor. Furthermore, the forest land and grassland in the river basin have been effectively increased, as ESV has increased. Overall, the value of ecosystem services has remained relatively constant.Accurate spatial statistics on the elasticity index from 1990 to 2020 was carried out (Fig. 5). The elastic index of the upper YRB and Loess Plateau is higher, and the impact of land use change on ecosystem services is more apparent in this region, according to the findings. This is mainly due to the implementation of large-scale ecological engineering measures in response to vegetation degradation in the upper reaches of the YRB and soil erosion in the middle reaches (Loess Plateau), by the Chinese government. In addition, Lanzhou New District, Guanzhong Plain, and the lower Yellow River region also showed higher elasticity index. The above-mentioned regional development and construction, as well as human activities, have resulted in a rapid increase in construction land, resulting in a significant decline in ecosystem services and a higher resilience index as a result of rapid urbanisation.Figure 5Spatial distribution of elastic coefficients in the YRB from 1990 to 2020.Full size imageIn general, the land use types in the YRB have changed dramatically, and land type conversion is very common. The conversion of ecological land to urban construction land, as well as the conversion of unused and cultivated land to ecological land, has resulted in significant changes in ecosystem service value. This demonstrates that the basin’s ecological construction projects have yielded positive environmental results. More

  • in

    Country-level fire perimeter datasets (2001–2021)

    Global fire activity is changing in many areas as temperatures increase and land use intensifies1,2,3,4,5. This is sparking an increase in attention given to fire activity and fire ecology. However, the availability of data for spatially delineated fire events is limited or non-existent in many countries6, with most global fire data coming from satellite-based active fire detections7,8 and gridded burned area products9,10. The lack of products containing delineated events has led to many global studies about fire ecology that are computationally-intensive, coarse-scale trend analyses1,4.A key advantage of datasets like Monitoring Trends in Burn Severity (MTBS)11 or the Fire Occurrence Dataset12 lies in their ease of use. Since its inception in 2007 MTBS has been cited 947 times in peer-reviewed studies according to a Google Scholar search at the time of this writing, despite documented limitations for scientific use of some facets of the product13. The MTBS dataset is regularly updated, easy to find on the internet, and it is free, fast and easy to download and use. Many environmental scientists and resource managers do not have the computational budget or expertise in big data or remote sensing to deal with the challenges one must overcome to process large fire datasets. This is especially true for cases when all that is needed is a shapefile of fire perimeters that can be used to map fire history. Other global fire perimeter datasets have been produced from satellite-derived burned area products14,15, but these are only available in yearly or monthly global shapefiles. Often field-based studies of fire effects require an entire time series over study areas that are only a few hundred km in diameter16 or a single ecoregion17. The end user who wants to understand the fire history for their region would have to download yearly shapefiles with a global extent, clip all of those shapefiles to their area of interest, and then combine them into one shapefile, just to get started. We suspect that the lack of accessible fire perimeter datasets that are easy to download and use contributes to a disparity in research, where fire ecology studies are conducted mostly in developed countries that have either research infrastructure capable of handling big data or longer-term government records, or temperate forested regions that have substantial tree-ring records18.There are two existing global perimeter products, the Global Fire Atlas (GFA) (Andela et al.14) and the Global Wildfire Information System (GWIS) (Artes et al.15). Both were created by applying spatiotemporal flooding algorithms to the MODIS MCD64 Burned Area Product. These algorithms assign burned pixels from the MCD64 products using a moving window whose size is defined by spatial and temporal parameters. They are created as monthly or yearly slices of the entire globe, and they can be subsetted. These products are extremely valuable for global scale studies. But when we look at how those products delineate known fire events we see a consistent problem in that they both seem to over-segment events in ways that appear unrealistic. This inconsistent event delineation is not problematic for coarse-scale or regional estimates of burned area or fire seasonality, but can lead to unrealistic estimates for number of fire events and event-level characteristics like fire size and spread rate. In Fig. 1 we illustrate this with an example of the 2013 Rim Fire in California, United States, which was unmistakably a single event that burned about 90,000 ha over the course of three months. Figure 2 illustrates how the day-to-day progression of the Rim Fire was a steady progression from a single ignition in late August. Table 1 shows how the differences in event delineation propagate to calculations of burned area and number of events. In the GFA, the Rim Fire is delineated as one large event of 804.5 km2, and 13 additional events totaling 88.7 km2. in GWIS it is delineated as one event of 878 km2 and 47 additional events totalling 20 km2. With FIRED, there is one event of 892 km2 and 2 single pixel events totalling less than one km2. One cause for potential differences is how one defines a “fire event”. Large fires often have multiple ignition sources. The Global Fire Atlas algorithm and others19, for example, search for local minima to identify various ignition locations that may begin as small patches, only to later form a large complex and in the end described with a single fire perimeter. The choice of outside sources for optimizing the spatial-temporal parameters, the method of optimization, and the intent of the final product’s meaning (defining events as single ignition patches vs contiguous burned area) all lead to different outcomes in the final events that are delineated. Another likely source of this discrepancy is that GWIS and GFA are calibrated to create a single global product. Because different geographical areas have different types of fire regimes, they have fires that grow at different rates and to different sizes, and occur in greater or fewer frequencies, and so the spatial and temporal parameters that work well for defining a fire event in one area may result in over- or under-segmentation in other areas. Here, we decided upon an approach of creating many regional products across the globe, rather than one product for everywhere on earth.Fig. 1Comparison of global fire event products performance for the 2013 Rim Fire (a). In the FIRED product (b), the Rim fire was classified as one very large event with two single pixel events. The Global Fire Atlas (GFA, c) and Global Wildfire Information System (GWIS, d) each delineated a very large event, with 13 and 47 smaller events, respectively.Full size imageFig. 2The two primary outputs FIREDpy provides are a daily- and event-level product. Panel a shows the default single event polygon. In b, each day has a separate polygon, with associated statistics generated, within each event. Panel c shows the daily perimeters derived from the airborne infrared by the incident management team for comparison.Full size imageTable 1 Rim fire comparison.Full size tableBesides the ease of access and use, the advantage of the FIRED product lies in the user’s ability to use the open-source software, FIREDpy, to tailor the spatial and temporal parameters of the moving window algorithm in order to realistically delineate events for their region of interest. In Fig. 3, we illustrate this by comparing the three products for a pair of small fires in Florida. In this case, the FIRED product that was created with a larger moving window (5 pixels and 11 days) over-aggregated the events, but it only required one line of code at command line to recreate the product with a smaller moving window (1 pixel and 5 days) to get more realistic results.Fig. 3Product comparison for two small events in Florida, the Moonshine Bay and Sour Orange fires (outlined) that both ignited in February of 2007 and were delineated by MTBS. In b the firedpy product that was optimized for the entire United States with a moving window of 5 pixels, 11 days resulted in aggregation of the two fires delineated by MTBS, but also several smaller fires nearby. In b, it was re-ran with a window of one pixel and five days, for a more realistic result. Delineations by the Global Fire Atlas (c) and the Global Wildfire Information System (d) are shown for comparison.Full size imageHere, we present a collection of regionally-tailored fire perimeter datasets for every country in the world with significant fire activity20, which we created with the open source algorithm, FIREDpy21. Each dataset is either a single country or a broader region, depending on the data volume. These datasets differ from other similar efforts14,15 in that each dataset created by FIREDpy is a single file containing a collection of polygons that is generated for the entire time series, rather than monthly or yearly aggregations with a global extent. Furthermore, we have generated the data products at a spatial extent land managers and ecologists would typically use to do regional-scale research, and we adjusted the spatial and temporal parameters for each country to yield realistic event delineations. We also made every effort to ensure that download sizes are reasonable (  More

  • in

    The bacterial and fungal communities of the larval midgut of Spodoptera frugiperda (Lepidoptera: Noctuidae) varied by feeding on two cruciferous vegetables

    Douglas, A. E. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ma, Q. et al. Gut bacterial communities of Lymantria xylina and their associations with host development and diet. Microorganisms 9(9), 1860 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yuan, X. et al. Comparison of gut bacterial communities of Grapholita molesta (Lepidoptera: Tortricidae) reared on different host plants. Int. J. Mol. Sci. 22(13), 6843 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Liu, Y. et al. Comparison of gut bacterial communities and their associations with host diets in four fruit borers. Pest Manag. Sci. 76(4), 1353–1362 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lauzon, C. R., Sjogren, R. E. & Prokopy, R. J. Enzymatic capabilities of bacteria associated with apple maggot flies: A postulated role in attraction. J. Chem. Ecol. 26, 953–967 (2000).CAS 
    Article 

    Google Scholar 
    Douglas, A. E. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38–47 (2009).Article 

    Google Scholar 
    Kaltenpoth, M. & Engl, T. Defensive microbial symbionts in Hymenoptera. Funct. Ecol. 28(2), 315–327 (2014).Article 

    Google Scholar 
    Bruner-Montero, G., Wood, M., Horn, H. A., Gemperline, E., Li, L. & Currie, C. R. Symbiont-mediated protection of acromyrmex leaf-cutter ants from the entomopathogenic fungus Metarhizium anisopliae. mBio 12(6), e0188521 (2021).Zhang, Q. et al. Enterobacter hormaechei in the intestines of housefly larvae promotes host growth by inhibiting harmful intestinal bacteria. Parasit. Vector. 14(1), 598 (2021).CAS 
    Article 

    Google Scholar 
    Zhang, S., et al. The gut microbiota in Camellia weevils are influenced by plant secondary metabolites and contribute to saponin degradation. mSystems 5(2), e00692–19 (2020).Sato, Y. et al. Insecticide resistance by a host-symbiont reciprocal detoxification. Nat. Commun. 12(1), 6432 (2021).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jordan, H. R. & Tomberlin, J. K. Microbial influence on reproduction, conversion, and growth of mass produced insects. Curr. Opin. Insect Sci. 48, 57–63 (2021).PubMed 
    Article 

    Google Scholar 
    Strano, C. P., Malacrinò, A., Campolo, O. & Palmeri, V. Influence of host plant on Thaumetopoea pityocampa gut bacterial community. Microb. Ecol. 75(2), 487–494 (2018).PubMed 
    Article 

    Google Scholar 
    Mason, C. J. et al. Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae. PLoS ONE 15(3), e0229848 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hammer, T. J., Janzen, D. H., Hallwachs, W., Jaffe, S. P. & Fierer, N. Caterpillars lack a resident gut microbiome. Proc. Natl. Acad. Sci. USA 114, 9641–9646 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Scully, E. D. et al. Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis). Sci. Rep. 8(1), 9620 (2018).ADS 
    MathSciNet 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Goergen, G., Kumar, P. L., Sankung, S. B., Togola, A. & Tamò, M. F. irst report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS ONE 11(10), e0165632 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Nagoshi, R. N. et al. Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration. Sci. Rep. 10, 1–10 (2020).Article 
    CAS 

    Google Scholar 
    Beuzelin, J. M., Larsen, D. J., Roldán, E. L. & Schwan Resende, E. Susceptibility to chlorantraniliprole in fall armyworm (Lepidoptera: Noctuidae) populations infesting sweet corn in southern florida. J. Econ. Entomol. 115(1), 224–232 (2022).Montezano, D. G. et al. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr. Entomol. 26, 286–300 (2018).Article 

    Google Scholar 
    Jones, A. G., Mason, C. J., Felton, G. W. & Hoover, K. Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci. Rep. 9(1), 2792 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Mason, C. J., Hoover, K. & Felton, G. W. Effects of maize (Zea mays) genotypes and microbial sources in shaping fall armyworm (Spodoptera frugiperda) gut bacterial communities. Sci. Rep. 119(1), 4429 (2021).ADS 
    Article 
    CAS 

    Google Scholar 
    Lv, D. et al. Comparison of gut bacterial communities of fall armyworm (Spodoptera frugiperda) reared on different host plants. Int. J. Mol. Sci. 22(20), 11266 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, Y. P. et al. Effects of host plants on bacterial community structure in larvae midgut of Spodoptera frugiperda. Insects 13(4), 373 (2022).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, J. et al. Cabbage cultivars influence transfer and toxicity of cadmium in soil-Chinese flowering cabbage Brassica campestris-cutworm Spodoptera litura larvae. Ecotoxicol. Environ. Saf. 213, 112076 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Abdullah, A., Ullah, M. I., Raza, A. M., Arshad, M. & Afzal, M. Host plant selection affects biological parameters in armyworm, Spodoptera litura (Lepidoptera: Noctuidae). Pak. J. Zool. 51(6), 2117–2123 (2019).Article 

    Google Scholar 
    Gopalakrishnan, R. & Kalia, V. K. Biology and biometric characteristics of Spodoptera frugiperda (Lepidoptera: Noctuidae) reared on different host plants with regard to diet. Pest Manag. Sci. 78(5), 2043–2051 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    He, L. et al. Larval diet affects development and reproduction of East Asian strain of the fall armyworm Spodoptera frugiperda. J. Integr. Agr. 20(3), 736–744 (2021).Article 

    Google Scholar 
    He, L., Wu, Q., Gao, X. & Wu, K. Population life tables for the invasive fall armyworm, Spodoptera frugiperda fed on major oil crops planted in China. J. Integr. Agr. 20(3), 745–754 (2021).Article 

    Google Scholar 
    Xie, W. et al. Age-stage, two-sex life table analysis of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) reared on maize and kidney bean. Chem. Biol. Technol. Ag. 8, 44 (2021).CAS 
    Article 

    Google Scholar 
    Gopalakrishnan, R. & Kalia, V. K. Biology and biometric characteristics of Spodoptera frugiperda (Lepidoptera: Noctuidae) reared on different host plants with regard to diet. Pest Manag. Sci. 78(5), 2043–2051 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang, P. et al. Host selection and adaptation of the invasive pest Spodoptera frugiperda to indica and japonica rice cultivars. Entomol. Gen. https://doi.org/10.1127/entomologia/2022/1330 (2022).Article 

    Google Scholar 
    Wu, L. et al. Fitness of fall armyworm, Spodoptera frugiperda to three solanaceous vegetables. J. Integr. Agr. 20(3), 755–763 (2021).Article 

    Google Scholar 
    Wu, F. et al. Population development, fecundity, and flight of Spodoptera frugiperda (Lepidoptera: Noctuidae) reared on three green manure crops: implications for an ecologically based pest management approach in China. J. Econ. Entomol. 115(1), 124–132 (2022).PubMed 
    Article 

    Google Scholar 
    Hou, M. L. & Sheng, C. F. Effects of different foods on growth, development and reproduction of cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Acta Entomol. Sin. 43, 168–175 (2000).CAS 

    Google Scholar 
    Wang, X. L. et al. Variability of gut microbiota across the life cycle of Grapholita molesta (Lepidoptera: Tortricidae). Front. Microbiol. 11, 1366 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Näsvall, K. et al. Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly. Mol. Ecol. 30(2), 499–516 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Ort, B. S., Bantay, R. M., Pantoja, N. A. & O’Grady, P. M. Fungal diversity associated with Hawaiian Drosophila host plants. PLoS ONE 7(7), e40550 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Majumder, R., Sutcliffe, B., Taylor, P. W. & Chapman, T. A. Fruit host-dependent fungal communities in the microbiome of wild Queensland fruit fly larvae. Sci. Rep. 10(1), 16550 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zeng, J. Y. et al. Avermectin stress varied structure and function of gut microbial community in Lymantria dispar asiatica (Lepidoptera: Lymantriidae) larvae. Pestic. Biochem Physiol. 164, 196–202 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chen, C., Zhang, J., Tan, H., Fu, Z. & Wang, X. Characterization of the gut microbiome in the beet armyworm Spodoptera exigua in response to the short-term thermal stress. J. Asia-Pac. Entomol. 25, 101863 (2022).Article 

    Google Scholar 
    Rozadilla, G., Cabrera, N. A., Virla, E. G., Greco, N. M. & McCarthy, C. B. Gut microbiota of Spodoptera frugiperda (J.E. Smith) larvae as revealed by metatranscriptomic analysis. J. Appl. Entomol. 144, 351–363 (2020).CAS 
    Article 

    Google Scholar 
    Ugwu, J. A., Liu, M., Sun, H. & Asiegbu, F. O. Microbiome of the larvae of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) from maize plants. J. Appl. Entomol. 144, 764–776 (2020).CAS 
    Article 

    Google Scholar 
    Wang, X. et al. Variability of gut microbiota across the life cycle of Grapholita molesta (Lepidoptera: Tortricidae). Front. Microbiol. 11, 1366 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yang, F. Y. et al. Differential profiles of gut microbiota and metabolites associated with host shift of Plutella xylostella. Int. J. Mol. Sci. 21, 6283 (2020).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Shao, Y. et al. Crystallization of alpha- and beta-carotene in the foregut of Spodoptera larvae feeding on a toxic food plant. Insect Biochem. Mol. Biol. 41, 273–281 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Santos, T. A., Scorzoni, L., Correia, R., Junqueira, J. C. & Anbinder, A. L. Interaction between Lactobacillus reuteri and periodontopathogenic bacteria using in vitro and in vivo (G mellonella) approaches. Pathog. Dis. 78(8), ftaa044 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Biedermann, P. & Vega, F. E. Ecology and evolution of insect-fungus mutualisms. Annu. Rev. Entomol. 65, 431–455 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Guo, Q., Yao, Z., Cai, Z., Bai, S. & Zhang, H. Gut fungal community and its probiotic effect on Bactrocera dorsalis. Insect Sci. https://doi.org/10.1111/1744-7917.12986 (2021).Article 
    PubMed 

    Google Scholar 
    Bing, X. L., Gerlach, J., Loeb, G. & Buchon, N. Nutrient-dependent impact of microbes on Drosophila suzukii development. MBio 9, e02199-e2117 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Keebaugh, E. S., Ryuichi, Y., Benjamin, O., Ludington, W. B. & Ja, W. W. Microbial quantity impacts Drosophila nutrition, development, and lifespan. Iscience 4, 247–259 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Deutscher, A. T., Chapman, T. A., Shuttleworth, L. A., Riegler, M. & Reynolds, O. L. Tephritid-microbial interactions to enhance fruit fly performance in sterile insect technique programs. BMC Microbiol. 19, 287 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gurung, K., Wertheim, B. & Falcao Salles, J. The microbiome of pest insects: it is not just bacteria. Entomol. Exp. Appl. 167, 156–170 (2019).Article 

    Google Scholar 
    Sun, J., Xia, Y. & Ming, D. Whole-genome sequencing and bioinformatics analysis of Apiotrichum mycotoxinivorans: Predicting putative zearalenone-degradation enzymes. Front. Microbiol. 11, 1866 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Qian, X. J. et al. Bioconversion of volatile fatty acids into lipids by the oleaginous yeast Apiotrichum porosum DSM27194. Fuel 290, 119811 (2021).CAS 
    Article 

    Google Scholar 
    Passos, D. F., Pereira, N. & Castro, A. M. A comparative review of recent advances in cellulases production by Aspergillus, Penicillium and Trichoderma strains and their use for lignocellulose deconstruction. Curr. Opin. Green Sustain Chem. 14, 60–66 (2018).Article 

    Google Scholar 
    Višňovská, D. et al. Caterpillar gut and host plant phylloplane mycobiomes differ: a new perspective on fungal involvement in insect guts. FEMS Microbiol. Ecol. 96(9), fiaa116 (2020).PubMed 
    Article 
    CAS 

    Google Scholar 
    Shu, B. et al. Growth inhibition of Spodoptera frugiperda larvae by camptothecin correlates with alteration of the structures and gene expression profiles of the midgut. BMC Genomics 22, 391 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Estimation of nutrient loads with the use of mass-balance and modelling approaches on the Wełna River catchment example (central Poland)

    Case study areaThe studied catchment (2 621 km2) is located in the central-western part of Poland, and constitutes a part of the Oder River basin. The Wełna River (118 km) discharges to the Warta River near the town of Oborniki18, with an average flow rate of 8.1 m3s−1 (1980–2019) in this profile19. The natural conditions in this catchment favour the development of intensive agriculture, which covers almost 72% of this area (1888 km2) and contributes to the high consumption of mineral fertilizers20. Forest areas cover another 22% of this catchment (589 km2), while urbanised ones only 4% (93 km2) (Fig. 1). The Wełna River catchment is inhabited by approx. 230,000 people, of which only approx. 74% is served by wastewater treatment facilities21.Figure 1Localisation of the Wełna River catchment with its land use forms and nutrient sources. This figure was created using ArcGIS 10.2.1 for Desktop available at https://www.esri.com/en-us/home. Licence granted to Institute of Meteorology and Water Management.Full size imageInput dataBoth the mass-balance method and the modelling method require a similar amount and type of input data (Supplementary Table S1). Basic information on the Wełna River daily flow rates and nutrient concentrations in the closing profile of the catchment (Oborniki) has been obtained from the state monitoring services (Institute of Meteorology and Water Management—National Research Institute—IMGW-PIB13 and State Environmental Monitoring22—SEM) (Supplementary Table S1). They have formed the basis for the estimation of the share of individual sources in the mass-balance method, as well as for the calibration of the Macromodel DNS/SWAT in the modelling method. Other data, such as maps of elevation, river network and soil maps, as well as meteorological data, necessary for the development of an accurate representation of the studied catchment area on the Macromodel DNS/SWAT digital platform, were also obtained from state repositories. Data on the land use comes from the Corine Land Cover8, while detailed information on nutrient sources has been obtained mostly from the Local Data Bank of statistical information. The utilisation of the collected database has been presented in Fig. 2, and described in the following text. The comparison of the results for nutrient loads from both method was based on the year 2017, which was characterised by the maximum amount of monitoring data for both flows (365 measurements) (IMGW-PIB) and total nitrogen (TN) and total phosphorus (TP) (12 measurements–SEM). The average air temperature in 2017 in Poland was 1.5 °C higher than the long-term average (1971–2000) and was over 10 °C which resulted from the warm autumn and the end of the year. The time of the snow cover presence was shorter than the long-term data, and the rest of the year was classified as thermally normal.Figure 2Methodology diagram with relevant chapters marked in grey ovals (green—steps and data used for Mass Balance method, blue—steps data used for Modelling method, green/blue—steps and data used for both methods).Full size imageIn terms of precipitation, 2017 was assessed as wet, similarly due to rainy autumn and summer. In the Wełna River catchment area, the annual rainfall was about 770 mm, however high variability of precipitation conditions in particular months, from extremely wet to very dry, should be noted23. Therefore hydrologically, 2017 was considered normal with the flows only slightly lower than the long-term average.Mass-balance methodThe first method used for the quantification of sources and loads in the studied area was the static mass-balance method. It is widely used by the Polish administration authorities responsible for water management17. This method is based on the assumption that the sum of the nutrient loads in the river’s closing profile (selected based on access to the monitoring data) and its retention in the catchment equals the emission of nutrients in a given time. Such assumption allows the apportioning of the river loads among identified sources and the estimation of their contribution to the total loads, based on known or assumed values of their retention.River load calculationThe total load of nutrients discharged from the catchment was calculated using the daily flow rate and nutrient concentrations in the closing profile of the catchment area (Oborniki, Fig. 1) from the SEM (Supplementary Table S1). The daily river load was calculated using the following Eq. 5:$${L}_{river}=0.0864sum_{t=1}^{n=365}{({Q}_{t}cdot {C}_{t})}_{t}$$
    (1)
    where: Lriver is the annual load [kga-1], n is the number of days, t is the consecutive day, Ct is the concentration [mg L-1], Qt is the mean daily flow rate [Ls-1], and 0.0864 is the unit conversion.Due to the fact that the flow rate is measured daily and nutrient concentrations only 12 times a year, the linear interpolation method5 was used to obtain the daily concentration values:$${x}_{k}={x}_{a}+kcdot frac{{x}_{b}-{x}_{a}}{n+1}$$
    (2)
    where: xk is the interpolated concentration value, xa is the first of the two measured concentration values between which the concentrations are interpolated, xb is the second of the two measured concentration values between which the concentrations are interpolated, k is the consecutive number of missing value and n is number of missing values.Source apportionmentFor the mass-balance method, data on nutrient loads for source apportionment (emission inventory) was collected in order to proceed with further calculations. The calculations were performed for 2017, due to the availability of river monitoring data and the nutrient sources were divided into 7 categories, based on the HELCOM guidelines5: municipal (MWS) and industrial (INS) point sources, municipal diffuse sources (SCS), forestry (MFS), agriculture (AGS), natural background (NBS) and atmospheric deposition (ATS). The category of “unknown sources” (UKS) was taken into account, in order to include possible discrepancies in nutrients load apportionment, and to cover eventual differences between calculated river load and inventoried emission.The MWS loads were calculated on the basis of the number of inhabitants served by the wastewater treatment plants (WWTPs)21. In the Wełna River catchment, 151 771 inhabitants were served by the 12 WWTPs covered by the National Wastewater Treatment Program (NWTP)24, which provides information on the total discharge volume from each facility. For 5 of these plants, information on influent/effluent nutrient concentrations was also available, allowing the direct calculation of discharged loads. For the remaining seven facilities, the loads were calculated on the basis of the mean influent concentration information, available for the WWTPs covered by the NWTP (80 mgL−1 and 12 mgL−1 for TN and TP, respectively), and approximated nutrient reduction level in non-biological WWTPs. This reduction level, based on data from the NWTP, was set at 65% for TN and 35% for TP24. Another 19 350 inhabitants of this catchment were connected to the small WWTPs, not included in the NWTP. This part of the MWS load was calculated using the mean daily wastewater outflow (0.12 m3day−1 per person), the same mean nutrient concentrations and reduction levels as presented above. Additionally, the remaining 25% of the catchment’s population (58,000) is not connected to any WWTP and uses septic tanks and other types of individual wastewater treatment systems. The load from this source was expressed as SCS, and calculated using unit loads set on 11 gday−1 per person and 1.6 gday-1 per person for TN and TP, respectively17. The industrial nutrient input information (INS) was gathered directly from the Statistics Poland office database21.The AGS load was calculated using nitrate and phosphate concentrations in shallow groundwater (90 cm below the ground surface), from 22 sampling points located on agricultural areas in the Wełna River catchment17. Concentrations were recalculated to TN and TP respectively and averaged. Thus, the obtained mean concentrations were 8.25 mgL−1 of TN and 1.92 mgL−1 of TP. Subsequently, load values were calculated by multiplying these concentrations by the outflow from agricultural areas, calculated as a share of the total catchment outflow respective to the agricultural use of the area. The calculated loads were multiplied by coefficients reflecting the share of monitored outflow (groundwaters and tile drainage) from the agricultural runoff (1.11 for TN and 4.17 for TP)25. Subsequently, the natural background (NBS) was subtracted from the AGS load.The load corresponding to NBS was calculated using the total catchment outflow and nutrient concentration values reflecting conditions in undisturbed areas of pre-human activity, set as 0.15 mgL−1 and 0.02 mgL−1, for TN and TP respectively17. The MFS load was also calculated in a similar way, using nutrient concentrations set to represent forest catchment as 0.31 mgL−1 and 0.038 mgL−117 and the outflow calculated as the share of the total catchment area, respective for the catchment part covered by forest. Also in this case, the NBS load has been subtracted. As for the ATS load, data on pollutant deposition into the ground from precipitation was taken from the SEM network26. This data was based on precipitation and its chemistry measurements taken from 22 monitoring stations covering the entire territory of Poland. The total load from the point and diffuse sources was calculated by adding the loads mentioned above. The eventual difference between the river load (“River load calculation” Section) and inventoried emission (“Mass-balance method” Section) accounted for the other sources (UKS).Load apportionmentThe contribution of each source to the calculated river load was calculated based on a simplified equation modified from HELCOM5:$${L}_{river}=DP+LOD-RP-RD$$
    (3)
    where: Lriver is the river load [kga−1], DP is the load from point sources (MWS and INS) [kga−1], LOD is the load from diffuse sources (SCS, ATS, MFS, AGS and, NBS) [kga−1], RP is the point source retention [kga−1] and RD is the diffuse source retention [kga−1].In the adopted mass-balance method, it is assumed that nutrient load from the point sources (DP) is introduced directly into the river bed phase, while load from the diffuse sources (LOD) is discharged into both phases of the catchment, land and river bed ones. In both phases, self-purification processes are taking place, resulting in the reduction of nutrient loads on the way from the source to the catchment closing profile. However, due to the limited amount of data, the self-purification processes in the river have been omitted, therefore the point source retention (RP) equalled 0 kga−1. Subsequently, the diffuse source retention (RD) has been estimated on the basis of the difference between each nutrient load of the river (Lriver) and the point sources (LOD). The remaining river load has been then attributed proportionally to the contribution of the particular diffuse sources to the total source apportionment (emission inventory).Modelling methodThe digital platform, the Macromodel DNS with the SWAT module27,28,29,30,31,32, was used for comparison for the nutrient balancing method described in “Mass-balance method” Section. This advanced dynamic tool tracks nitrogen and phosphorus migration paths in the river basin taking into account their spatial and temporal variability. For this purpose, it takes into account a very extensive input database, similar to that used in the mass balance method (Supplementary Table S1). Natural and anthropogenic processes that affect the transport and transformation of nutrients, are also part of this platform. The SWAT module (version 2012) is a tool which operates in the spatial information system (GIS) and is fully integrated with it. Using the digital elevation model (DEM), the SWAT module divided the entire analysed Wełna River catchment into a total of 225 sub-catchments of an average area of 11.5 km2. The subsequent use of data on land use (forests, agriculture and urbanised areas) and the types of soils (31 classes) allowed the authors to identify a total of 2824 hydrological response units (HRUs), homogeneous in terms of vegetation, soil and topography33. Afterwards, a simulation of soil water content, evapotranspiration, surface runoff, primary and underground flows was carried out in accordance with the water balance Eq. (4), which represents the basis for the quantitative component and the HRU.$${SW}_{t}={SW}_{0}+sum_{i=1}^{t}({R}_{day}-{Q}_{surf}-{E}_{a}-{W}_{seep}-{Q}_{gw})$$
    (4)
    where: SWt is the final soil water content (mm H2O), SW0 is the initial soil water content (mm H2O), Rday is the amount of precipitation (mm H2O), Qsurf is amount of surface runoff (mm H2O), Ea is the amount of evapotranspiration (mm H2O), Wseep is the amount of water entering the vadose zone from the soil profile (mm H2O), Qgw is the amount of return flow (mm H2O).The model directs all runoff flows generated by each HRU through the channel network, thus simulating a catchment. The water balance equation also represents a basis for the simulation, transport and transformation of nutrients required for the quantitative component of the model. This tool models forms of nitrogen, organic and inorganic , different forms of phosphorus in soil34, as well as organic nitrogen and phosphorus forms associated with plant residues, microbial biomass and soil humus35,36,37,38. Final results of simulations are produced by the SWAT model as all the forms of nitrogen and phosphorus (in kilograms of N and P per a time unit, respectively) are then summed up to give TN and TP values. To verify that the model properly predicts TN and TP values its results are calibrated with the TN and TP values resulting from SEM, as described in Sect. 2.4.1. Moreover, the particular forms of nitrogen and phosphorus have also been compared with the modelling results (Supplementary Table S4). A detailed overview of the migration and transformation pathways of nitrogen and phosphorus forms in the catchment has been presented in the Supplementary Information (Sect. S1), while mathematical description of these processes is included in the theoretical documentation of the SWAT model39.Similarly, as in the case of the mass-balance method, diffuse sources of nutrients from agriculture (AGS), forestry (MFS) or urban areas (URB) in SWAT were simulated in the land phase of the catchment. In the land phase, the model simulates both the infiltration of nutrients into the soil (fertilization, plant biomass, precipitation) and their removal from it (volatilization, denitrification, erosion, surface runoff). Additionally, changes in the distribution of nutrients in the soil (uptake by plants) and the low mobility of phosphorus itself are also taken into account39,40,41.Pollutants from municipal and industrial point sources (MWS, INS) are introduced directly into the river bed phase. The exception here is the nutrient load from municipal diffuse sources (SCS) which, reduced as a result of the self-purification processes taking place in the land phase, is also treated in the model as point sources. The SCS nutrient load mainly derives from leaking or illegally emptied septic tanks. For this purpose, septic tanks have been divided into three types: leaky, partially illegally emptied, and sealed septic tanks, legally emptied. The loads from the legally emptied tanks are included in the effluents from WWTPs reported in the catchment. While for the remaining types, their loads are calculated using factors depending on their effectiveness in nutrient removal (15 – 50%). The final nutrient load derived from these types of facilities is then calculated, taking into consideration the number of inhabitants using the different types of septic tanks and the average chemical composition of wastewater21.The load of nutrients from the atmospheric deposition (ATS) affects both land and river phases due to the presence of two deposition mechanisms in the SWAT module, i.e., wet and dry deposition. The model also allows for the determination of nutrient loads generated as a result of natural processes of nitrogen and phosphorus transformation and transport in the soil, with the omission of all anthropogenic pressure—natural background (NBS).Calibration, verification and validationThe SWAT module for the Wełna River has been calibrated, verified and validated using the SWAT-CUP software42. For the quantitative component (water circulation in the catchment), the implemented daily flow data (source: IMGW-PIB) for the period of 18 years (2001–2018) came from the water gauge stations on the Wełna River (Pruśce and Kowanówko) and its tributary (the Flinta River-Ryczywół) (Fig. 1). The qualitative component (nitrogen and phosphorus concentration in the catchment) was gathered from the SEM stations localised at the Wełna River (Oborniki and Rogoźno) (Fig. 1) and covered a period of 13 years (2005–2018). Three statistical measures, coefficient of determination (R2)43, percent bias (PBIAS)44, and Kling-Gupta efficiency (KGE)45, have been used to indicate the Wełna River model performance (Supplementary Tables S2 and S3). In terms of the quantitative component, the calibration and verification coefficients R2, KGE and PBIAS classified the model performance generally as good and very good for the main river (Wełna), and satisfactory and good for its tributary (Flinta). During the validation procedure, all coefficient values rated the model performance for daily flow simulations as very good. In terms of qualitative components, the model performance for TN simulations can be considered as very good or good, according to the all-applied coefficients. Lower model performance, mostly satisfactory, was observed for TP mainly due to the variability of phosphorus temporal distribution patterns (Supplementary Table S2). The entire process was described in detail in Orlińska-Woźniak et al46.Variant scenariosIn order to determine the contribution of individual sources to the total load of nutrients in the profile closing the analysed catchment, a final simulation of the model was used and subjected to calibration, verification and validation procedures, and called the baseline scenario (A0). Subsequent so-called variant scenarios (A1–A5), i.e. model simulations, were developed. In variant scenarios the values of selected parameters were changed in relation to the A0 scenario. This was used both in the river bed phase for point sources (A1) and for individual diffuse sources (A2–5), thus imitating surface changes for particular types of land use in the land phase of the catchment (Fig. 3).Figure 3Variant analysis diagram for assessment of nutrient loads (L) for particular modelling scenarios and sources described in the text: MWS, INS, SCS—point sources, URB—urban, AGS—agricultural, MFS—forest.Full size imageIn the A1 scenario, all parameterized and aggregated point sources (MWS, INS, SCS) for each relevant sub-basin (LMWS,INS,SCS), were removed from the model to calculate their contribution to the total nutrient loads in the closing profile of the studied catchment (LA1).In the next two scenarios (A2 and A3), concerning urban and agricultural land use, their surface areas (5 663 ha and 192 917 ha, respectively) were successively replaced by the forest land use. This procedure was based on the assumption that the forest is the primary type of land use for this catchment area47. In order to completely eliminate the influence of these areas, the nutrient loads from the relevant surface area occupied by forest land use were subtracted, in order to estimate the contribution of urban and agricultural land (LURB and LAGS, respectively).The change in land use from urbanised and agricultural areas to forest areas increased their percentage of the catchment area to almost 100%, thus the original image of the catchment area and the nutrient load at its mouth. On this basis, in scenario A4, the nutrient load from forests LMFS, which currently occupy only 20% of the catchment area (A0), flowing to the closing profile, was calculated from the proportion.The A5 scenario is the difference between the nutrient load from the A0 scenario and the sum of the remaining loads from the subsequent variant scenarios (A1–A4). In this way, both the natural background (NBS) and atmospheric deposition (ATS) were taken into account. More