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    Closing the energetics gap

    Stanier, R. Y. & Van Niel, C. B. Arch. Mikrobiol. 42, 17–35 (1962).CAS 
    Article 

    Google Scholar 
    Schavemaker, P. E. & Muñoz-Gómez, S. A. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-022-01833-9 (2022).Article 

    Google Scholar 
    Lane, N. & Martin, W. F. Nature 467, 929–934 (2010).CAS 
    Article 

    Google Scholar 
    Lynch, M. & Marinov, G. K. PNAS 112, 15690–15695 (2015).CAS 
    Article 

    Google Scholar 
    Cavalier-Smith, T. & Chao, E. E. Protoplasma 257, 621–753 (2020).CAS 
    Article 

    Google Scholar 
    Zachar, I. & Szathmáry, E. Biol. Direct 12, 19 (2017).Article 

    Google Scholar 
    Cavalier-Smith, T. Cold Spring Harb. Perspect. Biol. 6, 1–31 (2014).Article 

    Google Scholar 
    de Duve, C. Nat. Rev. Genet. 8, 395–403 (2007).Article 

    Google Scholar 
    Shiratori, T., Suzuki, S., Kakizawa, Y. & Ishida, K. Nat. Commun. 10, 5529 (2019).Article 

    Google Scholar 
    Martin, W. F., Tielens, A. G. M., Mentel, M., Garg, S. G. & Gould, S. B. Microbiol. Mol. Biol. Rev. 81, 8–17 (2017).Article 

    Google Scholar 
    Jékely, G. Biol. Direct 2, 3 (2007).Article 

    Google Scholar 
    Stanier, R. Y. Some aspects of the biology of cells and their possible evolutionary significance. Organization and Control in Prokaryotic and Eukaryotic Cells. In Proc. 20th Symposium of the Society for General Microbiology (eds Charles, H. P. & Knight, B. C. J. G) 20, 1–38 (Cambridge University Press, Cambridge, 1970).Zachar, I., Szilágyi, A., Számadó, S. & Szathmáry, E. PNAS USA 115, E1504–E1510 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Burns, J. A., Pittis, A. A. & Kim, E. Nat. Ecol. Evol. 2, 697–704 (2018).Article 

    Google Scholar 
    Bremer, N., Tria, F. D. K., Skejo, J., Garg, S. G. & Martin, W. F. Genome Biol. Evol. 14, evac079 (2022).Article 

    Google Scholar 
    Imachi, H. et al. Nature 577, 519–525 (2020).CAS 
    Article 

    Google Scholar 
    Zachar, I. & Boza, G. Cell. Mol. Life Sci. 77, 3503–3523 (2020).CAS 
    Article 

    Google Scholar 
    Devos, D. P. Mol. Biol. Evol. 38, 3531–3542 (2021).CAS 
    Article 

    Google Scholar  More

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    An experimental study: effects of boulder placement on hydraulic metrics of instream habitat complexity

    Effects of grid spacing on habitat hydraulic complexity metricsThe sensitivity of the habitat hydraulic complexity metrics to Δs was examined by calculating the metrics for Δs = 0.06, 0.12, 0.18, and 0.24 m (for M4, Δs = Δx = Δy). Figure 3 shows the variation of the metrics with grid spacing for scenarios with boulders. A preliminary assessment of no-boulder scenarios (S1-L and S1-H) showed that all the metrics decreased by increasing the grid spacing. However, because the metrics are mostly used in complex rather than non-obstructed and 1-D flows, the plots only include scenarios with boulder placement to highlight the effects of grid spacing on the metrics in complex flows. All the metrics generally decreased as Δs increased. At the low flow rate, by changing the Δs from the smallest to largest, i.e., 0.06 m to 0.024, the mean decreases in the M1, M2, and M4 metrics (averaged over all the scenarios with boulders) were 45.1, 9.9, and 74.7%, respectively. At the high flow rate, these reductions were 34.8, 14.7, and 82.5% for M1, M2, and M4, respectively. Table 2 shows the p-values associated with the changes in the metrics due to increasing Δs from 0.06 to 0.24 m for all scenarios. The table indicates that changes in M1 and M4 were statistically significant while for M2 they were not (p-values  > 0.05 for all scenarios except for S2-H). This result indicated the considerable influence of grid spacing on M1 and M4 metrics in the reaches with boulder placement. Additionally, the differences in the reported average reductions due to changing the flow rate were less than 10%, indicating an insubstantial effect of flow rate on the habitat hydraulic complexity metrics’ sensitivity to the grid spacing. The significant sensitivity of the metrics M1 and M4 to the grid spacing in this study is contrary to the findings of a previous study in which an insignificant correlation was found between the habitat hydraulic complexity metrics and Δs29. This difference can be attributed to different topographic features in the studied reaches. In the previous findings, measurements were mainly taken around the bends and reaches with no significant obstruction29, in which a more uniform flow with smaller velocity gradients is expected. However, in this study, the systematic boulder placement generated more complex flow patterns with noticeable velocity gradients. Therefore, due to the variations of flow velocities in the zone studied, substantially different values for the metrics are anticipated by computing the metrics over different spatial scales.Figure 3Variation of the habitat hydraulic complexity metrics with grid spacing (Δs) for scenarios with boulder placement. (a) kinetic energy gradient metric, M1, (b) normalized kinetic energy gradient metric, M2, (c) modified recirculation metric M4.Full size imageTable 2 p-values associated with changing the grid spacing from 0.06 to 0.24 m.Full size tableStatistical distribution of habitat hydraulic complexity metricsTable 3 lists the mean, minimum, maximum, and standard deviations of the habitat hydraulic complexity metrics (Δs = 0.06 m) for all the scenarios. To complement the results from Table 3 and assess whether the influences of solely changing the boulder concentration or flow rate on the metrics were statistically significant, Table 4 shows p-values associated with changing flow rate from low to high for a given boulder concentration, and Table 5 shows p-values associated with gradually increasing the boulder concentration for a given flow rate.Table 3 The statistical parameters of the habitat hydraulic complexity metrics in the detailed measurement zone.Full size tableTable 4 p-values from a t-test associated with changes in flow rate for a given boulder concentration.Full size tableTable 5 p-values from a t-test associated with changes in boulder concertation for a given flow rate.Full size tableFor metric M1, the mean M1 values for scenarios incorporating boulders showed the same order of magnitude as values from previous studies for reaches with single and multiple boulders27 but they were about one order of magnitude larger than calculated values in the confluence of two rivers11. Using a larger grid spacing in the study in the confluence of two rivers11 can be the reason for this difference. For a scenario at the higher flow rate, the mean M1 was on average (averaged for all the scenarios) 36% greater than its counterpart at the lower flow rate and this change in M1 values was statistically significant with p  More

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    Clay and climatic variability explain the global potential distribution of Juniperus phoenicea toward restoration planning

    Pecl, G. T. et al. Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science (80-) https://doi.org/10.1126/science.aai9214 (2017).Article 

    Google Scholar 
    Walther, G. R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Thuiller, W. et al. Consequences of climate change on the tree of life in Europe. Nature 470, 531–534 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Zimmermann, N. E., Edwards, T. C. Jr., Graham, C. H., Pearman, P. B. & Svenning, J. New trends in species distribution modelling. Ecography (Cop.) 33, 985–989 (2010).Article 

    Google Scholar 
    Norberg, A. et al. A comprehensive evaluation of predictive performance of 33 species distribution models at species and community levels. Ecol. Monogr. 89, e01370 (2019).Article 

    Google Scholar 
    Smeraldo, S. et al. Generalists yet different: Distributional responses to climate change may vary in opportunistic bat species sharing similar ecological traits. Mamm. Rev. 51, 571–584 (2021).Article 

    Google Scholar 
    Sohlström, E. H. et al. Future climate and land-use intensification modify arthropod community structure. Agric. Ecosyst. Environ. 327, 107830 (2022).Article 
    CAS 

    Google Scholar 
    Araújo, M. B. & New, M. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22, 42–47 (2007).PubMed 
    Article 

    Google Scholar 
    Stohlgren, T. J. et al. Ensemble habitat mapping of invasive plant species. Risk Anal. Int. J. 30, 224–235 (2010).Article 

    Google Scholar 
    Meller, L. et al. Ensemble distribution models in conservation prioritization: from consensus predictions to consensus reserve networks. Divers. Distrib. 20, 309–321 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dubuis, A. et al. Improving the prediction of plant species distribution and community composition by adding edaphic to topo-climatic variables. J. Veg. Sci. 24, 593–606 (2013).Article 

    Google Scholar 
    Walthert, L. & Meier, E. S. Tree species distribution in temperate forests is more influenced by soil than by climate. Ecol. Evol. 7, 9473–9484 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Figueiredo, F. O. G. et al. Beyond climate control on species range: The importance of soil data to predict distribution of Amazonian plant species. J. Biogeogr. 45, 190–200 (2018).Article 

    Google Scholar 
    Arar, A., Nouidjem, Y., Bounar, R., Tabet, S. & Kouba, Y. Potential future changes of the geographic range size of Juniperus phoenicea in Algeria based on present and future climate change projections. Contemp. Probl. Ecol. 13, 429–441 (2020).Article 

    Google Scholar 
    Coudun, C., Gégout, J., Piedallu, C. & Rameau, J. Soil nutritional factors improve models of plant species distribution: An illustration with Acer campestre (L.) in France. J. Biogeogr. 33, 1750–1763 (2006).Article 

    Google Scholar 
    Buri, A. et al. What are the most crucial soil variables for predicting the distribution of mountain plant species? A comprehensive study in the Swiss Alps. J. Biogeogr. 47, 1143–1153 (2020).Article 

    Google Scholar 
    Buri, A. et al. Soil factors improve predictions of plant species distribution in a mountain environment. Prog. Phys. Geogr. 41, 703–722 (2017).Article 

    Google Scholar 
    Mod, H. K., Scherrer, D., Luoto, M. & Guisan, A. What we use is not what we know: environmental predictors in plant distribution models. J. Veg. Sci. 27, 1308–1322 (2016).Article 

    Google Scholar 
    Scherrer, D. & Guisan, A. Ecological indicator values reveal missing predictors of species distributions. Sci. Rep. 9, 1–8 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Boulos, L. Flora of Egypt, Vol. 1. vol. 1 (Al Hadara Publishing, 1999).Farjon, A. & Filer, D. An atlas of the world’s conifers: An analysis of their distribution, biogeography, diversity and conservation status. (Brill, 2013).Allen, DJ. Juniperus phoenicea. The IUCN red list of threatened species 2017: e.T16348983A99965052. https://doi.org/10.2305/IUCN.UK.2017-2.RLTS. T16348983A99965052.en. Downloaded on 19 May 2020El-Bana, M., Shaltout, K., Khalafallah, A. & Mosallam, H. Ecological status of the Mediterranean Juniperus phoenicea L. relicts in the desert mountains of North Sinai Egypt. Flora-Morphol. Distrib. Funct. Ecol. Plants 205, 171–178 (2010).Article 

    Google Scholar 
    Moustafa, A. et al. Ecological Prominence of Juniperus phoenicea L. Growing in Gebel Halal, North Sinai Egypt. Catrina Int. J. Environ. Sci. 15, 11–23 (2016).
    Google Scholar 
    Farahat, E. A. Age structure and static life tables of the endangered Juniperus phoenicea L. in North Sinai Mountains, Egypt. J. Mt. Sci. 17, 2170–2178 (2020).Article 

    Google Scholar 
    El-Wahab, A. Condition assessment of plant diversity of Gebel Maghara, North Sinai, Egypt. Catrina Int. J. Environ. Sci. 3, 21–40 (2008).
    Google Scholar 
    Youssef, A. M., Morsy, A. A., Mosallam, H. A. & Hashim, A. M. Vegetation and soil relationships in some wadis from the North-Central part of Sinai Peninsula Egypt. Minia Sci. Bull. 25, 1–28 (2014).
    Google Scholar 
    Fisher, M. Decline in the juniper woodlands of Raydah Reserve in southwestern Saudi Arabia: A response to climate changes?. Glob. Ecol. Biogeogr. Lett. 6, 379–386 (1997).Article 

    Google Scholar 
    Salvà-Catarineu, M. et al. Past, present, and future geographic range of the relict Mediterranean and Macaronesian Juniperus phoenicea complex. Ecol. Evol. 11, 5075–5095 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Quevedo, L., Rodrigo, A. & Espelta, J. M. Post-fire resprouting ability of 15 non-dominant shrub and tree species in Mediterranean areas of NE Spain. Ann. For. Sci. 64(8), 883–890 (2007).Article 

    Google Scholar 
    Trabucco, A. & Zomer, R. J. Global aridity index (global-aridity) and global potential evapo-transpiration (global-PET) geospatial database. CGIAR Consort. Spat. Inf. 89, 1–2 (2009).
    Google Scholar 
    Hengl, T. et al. SoilGrids1km—Global soil information based on automated mapping. PLoS One 9, e105992 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kennedy, C. M., Oakleaf, J. R., Theobald, D. M., Baruch-Mordo, S. & Kiesecker, J. Documentation for the global human modification of terrestrial systems (2020).Naimi, B. & Araújo, M. B. sdm: a reproducible and extensible R platform for species distribution modelling. Ecography (Cop.) 39, 368–375 (2016).Article 

    Google Scholar 
    Naimi, B. usdm: Uncertainty analysis for species distribution models. R Packag. Version 1, 1–12 (2015).
    Google Scholar 
    Guisan, A., Thuiller, W. & Zimmermann, N. E. In Habitat Suitability and Distribution Models: With Applications in R. (Cambridge University Press, 2017).Dakhil, M. A. et al. Global invasion risk assessment of Prosopis juliflora at biome level : Does soil matter?. Biology 10, 203 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Iturbide, M., Bedia, J. & Gutiérrez, J. M. Background sampling and transferability of species distribution model ensembles under climate change. Glob. Planet. Change 166, 19–29 (2018).ADS 
    Article 

    Google Scholar 
    Barbet-Massin, M., Jiguet, F., Albert, C. H. & Thuiller, W. Selecting pseudo-absences for species distribution models: How, where and how many?. Methods Ecol. Evol. 3, 327–338 (2012).Article 

    Google Scholar 
    Zhang, Z., Mammola, S., Xian, W. & Zhang, H. Modelling the potential impacts of climate change on the distribution of ichthyoplankton in the Yangtze Estuary, China. Divers. Distrib. 26, 126–137 (2020).Article 

    Google Scholar 
    Thuiller, W., Guéguen, M., Renaud, J., Karger, D. N. & Zimmermann, N. E. Uncertainty in ensembles of global biodiversity scenarios. Nat. Commun. 10, 1–9 (2019).CAS 
    Article 

    Google Scholar 
    Breiner, F. T., Nobis, M. P., Bergamini, A. & Guisan, A. Optimizing ensembles of small models for predicting the distribution of species with few occurrences. Methods Ecol. Evol. 9, 802–808 (2018).Article 

    Google Scholar 
    Liu, C., Newell, G. & White, M. On the selection of thresholds for predicting species occurrence with presence-only data. Ecol. Evol. 6, 337–348 (2016).PubMed 
    Article 

    Google Scholar 
    Haider, S. M., Benscoter, A. M., Pearlstine, L., D’Acunto, L. E. & Romañach, S. S. Landscape-scale drivers of endangered Cape Sable Seaside Sparrow (Ammospiza maritima mirabilis) presence using an ensemble modeling approach. Ecol. Modell. 461, 109774 (2021).Article 

    Google Scholar 
    Allouche, O., Tsoar, A. & Kadmon, R. Assessing the accuracy of species distribution models: Prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43, 1223–1232 (2006).Article 

    Google Scholar 
    Franklin, J. Mapping Species Distributions: Spatial Inference and Prediction (Cambridge University Press, 2010).Book 

    Google Scholar 
    Kabiel, H. F., Hegazy, A. K., Lovett-Doust, L., Al-Rowaily, S. L. & Al Borki, A. E. N. S. Ecological assessment of populations of Juniperus phoenicea L. in the Al-Akhdar mountainous landscape of Libya. Arid L. Res. Manag. 30, 269–289 (2016).Article 

    Google Scholar 
    Camarero, J. J. et al. Dieback and mortality of junipers caused by drought: Dissimilar growth and wood isotope patterns preceding shrub death. Agric. For. Meteorol. 291, 108078 (2020).ADS 
    Article 

    Google Scholar 
    Sánchez-Salguero, R. & Camarero, J. J. Greater sensitivity to hotter droughts underlies juniper dieback and mortality in Mediterranean shrublands. Sci. Total Environ. 721, 137599 (2020).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Cramer, W. et al. Climate change and interconnected risks to sustainable development in the Mediterranean. Nat. Clim. Chang. 8, 972–980 (2018).ADS 
    Article 

    Google Scholar 
    Forzieri, G. et al. Ensemble projections of future streamflow droughts in Europe. Hydrol. Earth Syst. Sci. 18, 85–108 (2014).ADS 
    Article 

    Google Scholar 
    González-Hidalgo, J. C. et al. High-resolution spatio-temporal analyses of drought episodes in the western Mediterranean basin (Spanish mainland, Iberian Peninsula). Acta Geophys. 66, 381–392 (2018).ADS 
    Article 

    Google Scholar 
    Stockhecke, M. et al. Millennial to orbital-scale variations of drought intensity in the Eastern Mediterranean. Quat. Sci. Rev. 133, 77–95 (2016).ADS 
    Article 

    Google Scholar 
    Navarro Cerrillo, R. M. et al. Can habitat prediction models contribute to the restoration and conservation of the threatened tree Abies pinsapo Boiss. in Southern Spain?. New For. 52, 89–112 (2021).Article 

    Google Scholar  More

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    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

    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

    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

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    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

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    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