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    Habitat partitioning, co-occurrence patterns, and mixed-species group formation in sympatric delphinids

    Pianka, E. R. Niche overlap and diffuse competition. Proc. Natl. Acad. Sci. 71, 2141–2145 (1974).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).Article 

    Google Scholar 
    Tokeshi, M. Species Coexistence: Ecological and Evolutionary Perspectives. (Wiley-Blackwell, 2009).Grinnell, J. Geography and evolution. Ecology 5, 225–229 (1924).Article 

    Google Scholar 
    Roughgarden, J. Resource partitioning among competing species—A coevolutionary approach. Theor. Popul. Biol. 9, 388–424 (1976).Article 
    MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    Syme, J., Kiszka, J. J. & Parra, G. J. Dynamics of cetacean mixed-species groups: A review and conceptual framework for assessing their functional significance. Front. Mar. Sci. 8, 1–19 (2021).Article 

    Google Scholar 
    Stensland, E., Angerbjörn, A. & Berggren, P. Mixed species groups in mammals. Mamm. Rev. 33, 205–223 (2003).Article 

    Google Scholar 
    Cords, M. & Würsig, B. A Mix of Species: Associations of Heterospecifics Among Primates and Dolphins. in Primates and Cetaceans: Field Research and Conservation of Complex Mammalian Societies (eds. Yamagiwa, J. & Karczmarski, L.) 409–431 (Springer, 2014). doi:https://doi.org/10.1007/978-4-431-54523-1_21.Goodale, E., Beauchamp, G. & Ruxton, G. D. Mixed-Species Groups of Animals: Behavior, Community Structure, and Conservation. (Academic Press, 2017).Krause, J. & Ruxton, G. D. Living in Groups. Oxford Series in Ecology and Evolution (Oxford University Press, 2002).Heymann, E. W. & Buchanan-Smith, H. M. The behavioural ecology of mixed-species troops of callitrichine primates. Biol. Rev. 75, 169–190 (2000).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sridhar, H. & Guttal, V. Friendship across species borders: factors that facilitate and constrain heterospecific sociality. Philos. Trans. R. Soc. B Biol. Sci. 373, 1–9 (2018).Greenberg, R. Birds of many feathers: The formation and structure of mixed-species flocks of forest birds. in On the Move: How and Why Animals Travel in groups (eds. Boinski, S. & Gerber, P. A.) 521–558 (University of Chicago Press, 2000).Waser, P. M. ‘Chance’ and mixed-species associations. Behav. Ecol. Sociobiol. 15, 197–202 (1984).Article 

    Google Scholar 
    Whitesides, G. H. Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa: biological significance or chance?. Anim. Behav. 37, 760–776 (1989).Article 

    Google Scholar 
    Waser, P. M. Primate polyspecific associations: Do they occur by chance?. Anim. Behav. 30, 1–8 (1982).Article 

    Google Scholar 
    Alexander, R. D. The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325–383 (1974).Article 

    Google Scholar 
    Kasozi, H. & Montgomery, R. A. Variability in the estimation of ungulate group sizes complicates ecological inference. Ecol. Evol. 10, 6881–6889 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Syme, J., Kiszka, J. J. & Parra, G. J. How to define a dolphin ‘group’? Need for consistency and justification based on objective criteria. Ecol. Evol. 12, 1–18 (2022).Article 

    Google Scholar 
    Hutchinson, J. M. C. & Waser, P. M. Use, misuse and extensions of ‘ideal gas’ models of animal encounter. Biol. Rev. 82, 335–359 (2007).Article 
    PubMed 

    Google Scholar 
    Gotelli, N. J. Null model analysis of species co-occurrence patterns. Ecology 81, 2606–2621 (2000).Article 

    Google Scholar 
    Astaras, C., Krause, S., Mattner, L., Rehse, C. & Waltert, M. Associations between the drill (Mandrillus leucophaeus) and sympatric monkeys in Korup National Park. Cameroon. Am. J. Primatol. 73, 127–134 (2011).Article 
    PubMed 

    Google Scholar 
    Mammides, C., Chen, J., Goodale, U. M., Kotagama, S. W. & Goodale, E. Measurement of species associations in mixed-species bird flocks across environmental and human disturbance gradients. Ecosphere 9, 1–14 (2018).Article 

    Google Scholar 
    Ovaskainen, O., Abrego, N., Halme, P. & Dunson, D. Using latent variable models to identify large networks of species-to-species associations at different spatial scales. Methods Ecol. Evol. 7, 549–555 (2016).Article 

    Google Scholar 
    Pollock, L. J. et al. Understanding co-occurrence by modelling species simultaneously with a Joint Species Distribution Model (JSDM). Methods Ecol. Evol. 5, 397–406 (2014).Article 

    Google Scholar 
    Warton, D. I. et al. So Many variables: Joint modeling in community ecology. Trends Ecol. Evol. 30, 766–779 (2015).Article 
    PubMed 

    Google Scholar 
    Ovaskainen, O. et al. How to make more out of community data? A conceptual framework and its implementation as models and software. Ecol. Lett. 20, 561–576 (2017).Article 
    PubMed 

    Google Scholar 
    Ovaskainen, O. & Abrego, N. Joint Species Distribution Modelling. (Cambridge University Press, 2020). https://doi.org/10.1017/9781108591720.Blanchet, F. G., Cazelles, K. & Gravel, D. Co-occurrence is not evidence of ecological interactions. Ecol. Lett. 23, 1050–1063 (2020).Article 
    PubMed 

    Google Scholar 
    Haak, C. R., Hui, F. K., Cowles, G. W. & Danylchuk, A. J. Positive interspecific associations consistent with social information use shape juvenile fish assemblages. Ecology 101, 1–16 (2020).Article 

    Google Scholar 
    Bastianelli, G., Wintle, B. A., Martin, E. H., Seoane, J. & Laiolo, P. Species partitioning in a temperate mountain chain: Segregation by habitat vs. interspecific competition. Ecol. Evol. 7, 2685–2696 (2017).Aspin, T. & House, A. Alpha and beta diversity and species co-occurrence patterns in headwaters supporting rare intermittent-stream specialists. Freshw. Biol. n/a, (2022).Astarloa, A. et al. Identifying main interactions in marine predator-prey networks of the Bay of Biscay. ICES J. Mar. Sci. 76, 2247–2259 (2019).Article 

    Google Scholar 
    Parra, G. J. Resource partitioning in sympatric delphinids: space use and habitat preferences of Australian snubfin and Indo-Pacific humpback dolphins. J. Anim. Ecol. 75, 862–874 (2006).Article 
    PubMed 

    Google Scholar 
    Parra, G. J., Wojtkowiak, Z., Peters, K. J. & Cagnazzi, D. Isotopic niche overlap between sympatric Australian snubfin and humpback dolphins. Ecol. Evol. 12, 1–11 (2022).Article 

    Google Scholar 
    Kiszka, J. J. et al. Ecological niche segregation within a community of sympatric dolphins around a tropical island. Mar. Ecol. Prog. Ser. 433, 273–288 (2011).Article 
    ADS 

    Google Scholar 
    Bearzi, M. Dolphin sympatric ecology. Mar. Biol. Res. 1, 165–175 (2005).Article 

    Google Scholar 
    Zaeschmar, J. R. et al. Occurrence of false killer whales (Pseudorca crassidens) and their association with common bottlenose dolphins (Tursiops truncatus) off northeastern New Zealand. Mar. Mammal Sci. 30, 594–608 (2014).Article 

    Google Scholar 
    Elliser, C. R. & Herzing, D. L. Long-term interspecies association patterns of Atlantic bottlenose dolphins, Tursiops truncatus, and Atlantic spotted dolphins, Stenella frontalis, in the Bahamas. Mar. Mammal Sci. 32, 38–56 (2016).Article 

    Google Scholar 
    Kiszka, J. J., Perrin, W. F., Pusineri, C. & Ridoux, V. What drives island-associated tropical dolphins to form mixed-species associations in the southwest Indian Ocean?. J. Mammal. 92, 1105–1111 (2011).Article 

    Google Scholar 
    Brown, A. M., Bejder, L., Cagnazzi, D., Parra, G. J. & Allen, S. J. The north west cape, Western Australia: A potential hotspot for Indo-Pacific humpback dolphins Sousa chinensis?. Pacific Conserv. Biol. 18, 240–246 (2012).Article 

    Google Scholar 
    Allen, S. J., Cagnazzi, D., Hodgson, A. J., Loneragan, N. R. & Bejder, L. Tropical inshore dolphins of north-western Australia: Unknown populations in a rapidly changing region. Pacific Conserv. Biol. 18, 56–63 (2012).Article 

    Google Scholar 
    Palmer, C., Parra, G. J., Rogers, T. & Woinarski, J. Collation and review of sightings and distribution of three coastal dolphin species in waters of the Northern Territory. Australia. Pacific Conserv. Biol. 20, 116–125 (2014).Article 

    Google Scholar 
    Corkeron, P. J. Aspects of the Behavioral Ecology of Inshore Dolphins Tursiops truncatus and Sousa chinensis in Moreton Bay, Australia. in The Bottlenose Dolphin (eds. Leatherwood, S. & Reeves, R.) 285–293 (Elsevier, 1990). https://doi.org/10.1016/B978-0-12-440280-5.50018-4.Haughey, R. et al. Distribution and habitat preferences of Indo-Pacific Bottlenose Dolphins (Tursiops aduncus) inhabiting coastal waters with mixed levels of protection. Front. Mar. Sci. 8, 1–20 (2021).Article 

    Google Scholar 
    Hanf, D., Hodgson, A. J., Kobryn, H., Bejder, L. & Smith, J. N. Dolphin distribution and habitat suitability in North Western Australia: Applications and Implications of a Broad-Scale, Non-targeted Dataset. Front. Mar. Sci. 8, 1–18 (2022).Article 

    Google Scholar 
    Hunt, T. N., Allen, S. J., Bejder, L. & Parra, G. J. Identifying priority habitat for conservation and management of Australian humpback dolphins within a marine protected area. Sci. Rep. 10, 1–14 (2020).Article 

    Google Scholar 
    Hunt, T. N. Demography, habitat use and social structure of Australian humpback dolphins (Sousa sahulensis) around the North West Cape, Western Australia: Implications for conservation and management. PhD Thesis, Flinders University, Adelaide, Australia. (Flinders University, 2018).Cassata, L. & Collins, L. B. Coral reef communities, habitats, and substrates in and near sanctuary zones of Ningaloo marine park. J. Coast. Res. 241, 139–151 (2008).Article 

    Google Scholar 
    CALM MPRA. Management plan for the Ningaloo Marine Park and Muiron Islands Marine Management Area 2005–2015. (2005).Hunt, T. N. et al. Demographic characteristics of Australian humpback dolphins reveal important habitat toward the southwestern limit of their range. Endanger. Species Res. 32, 71–88 (2017).Article 

    Google Scholar 
    Mann, J. Behavioral sampling methods for cetaceans: A review and critique. Mar. Mammal Sci. 15, 102–122 (1999).Article 

    Google Scholar 
    Python Software Foundation. Python Language Reference, version 3.8.0. at https://www.python.org/ (2016).QGIS Development Team. QGIS Geographic Information System, version 3.8.3 Zanzibar. at http://qgis.osgeo.org (2019).Zanardo, N., Parra, G., Passadore, C. & Möller, L. Ensemble modelling of southern Australian bottlenose dolphin Tursiops sp. distribution reveals important habitats and their potential ecological function. Mar. Ecol. Prog. Ser. 569, 253–266 (2017).Hanberry, B. B. Finer grain size increases effects of error and changes influence of environmental predictors on species distribution models. Ecol. Inform. 15, 8–13 (2013).Article 

    Google Scholar 
    Gottschalk, T. K., Aue, B., Hotes, S. & Ekschmitt, K. Influence of grain size on species–habitat models. Ecol. Modell. 222, 3403–3412 (2011).Article 

    Google Scholar 
    Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).Article 

    Google Scholar 
    Passadore, C., Möller, L. M., Diaz-Aguirre, F. & Parra, G. J. Modelling dolphin distribution to inform future spatial conservation decisions in a marine protected area. Sci. Rep. 8, 1–14 (2018).Article 
    CAS 

    Google Scholar 
    Parra, G. J., Schick, R. & Corkeron, P. J. Spatial distribution and environmental correlates of Australian snubfin and Indo-Pacific humpback dolphins. Ecography (Cop.) 29, 396–406 (2006).Article 

    Google Scholar 
    Conrad, O. et al. System for Automated Geoscientific Analyses (SAGA) v. 2.1.4. Geosci. Model Dev. 8, 1991–2007 (2015).R Core Team. R version 3.6.1. at https://www.r-project.org/ (2019).RStudio Team. RStudio: Integrated Develpment for R. at http://rstudio.com/ (2019).Dormann, C. F. et al. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography (Cop.) 36, 27–46 (2013).Article 

    Google Scholar 
    Tikhonov, G. et al. Joint species distribution modelling with the r-package Hmsc. Methods Ecol. Evol. 11, 442–447 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).Article 
    MATH 

    Google Scholar 
    Pearce, J. & Ferrier, S. Evaluating the predictive performance of habitat models developed using logistic regression. Ecol. Modell. 133, 225–245 (2000).Article 

    Google Scholar 
    Tjur, T. Coefficients of determination in logistic regression models—A new proposal: The coefficient of discrimination. Am. Stat. 63, 366–372 (2009).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Syme, J. The behavioural ecology of mixed-species groups of delphinids. PhD Thesis, Flinders University, Adelaide, Australia. (Flinders University, 2023).Wang, J. Y. Bottlenose Dolphin, Tursiops aduncus, Indo-Pacific Bottlenose Dolphin. in Encyclopedia of Marine Mammals (eds. Würsig, B., Thewissen, J. G. M. & Kovacs, K. M.) 125–130 (Elsevier, 2018). https://doi.org/10.1016/B978-0-12-804327-1.00073-X.Parra, G. J. & Jefferson, T. A. Humpback Dolphins. in Encyclopedia of Marine Mammals (eds. Würsig, B., Thewissen, J. G. M. & Kovacs, K. M.) 483–489 (Elsevier, 2018). https://doi.org/10.1016/B978-0-12-804327-1.00153-9.Dröge, E., Creel, S., Becker, M. S. & M’soka, J. Spatial and temporal avoidance of risk within a large carnivore guild. Ecol. Evol. 7, 189–199 (2017).Article 
    PubMed 

    Google Scholar 
    Browning, N. E., Cockcroft, V. G. & Worthy, G. A. J. Resource partitioning among South African delphinids. J. Exp. Mar. Bio. Ecol. 457, 15–21 (2014).Article 

    Google Scholar 
    Kiszka, J. J., Méndez-Fernandez, P., Heithaus, M. R. & Ridoux, V. The foraging ecology of coastal bottlenose dolphins based on stable isotope mixing models and behavioural sampling. Mar. Biol. 161, 953–961 (2014).Article 
    CAS 

    Google Scholar 
    Saayman, G. S. & Tayler, C. K. The socioecology of humpback dolphins (Sousa sp.). in Behavior of Marine Animals Current Perspectives in Research Volume 3: Cetaceans (eds. Winn, H. E. & Olla, B. L.) 165–226 (Springer, 1979).Gowans, S. & Whitehead, H. Distribution and habitat partitioning by small odontocetes in the Gully, a submarine canyon on the Scotian Shelf. Can. J. Zool. 73, 1599–1608 (1995).Article 

    Google Scholar 
    Clua, E. Mixed-species feeding aggregation of dolphins, large tunas and seabirds in the Azores. Aquat. Living Resour. 14, 11–18 (2001).Article 

    Google Scholar 
    Quérouil, S. et al. Why do dolphins form mixed-species associations in the azores?. Ethology 114, 1183–1194 (2008).Article 

    Google Scholar 
    Heithaus, M. R. & Dill, L. M. Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83, 480–491 (2002).Article 

    Google Scholar  More

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    Impacts of recent climate change on crop yield can depend on local conditions in climatically diverse regions of Norway

    Rahaman, A. et al. The increasing hunger concern and current need in the development of sustainable food security in the developing countries. Trends Food Sci. Technol. 113, 423–429. https://doi.org/10.1016/j.tifs.2021.04.048 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Porter, J. R. et al. In Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 485–533 (Cambridge University Press, 2014).
    Google Scholar 
    Yan, H. et al. Crop traits enabling yield gains under more frequent extreme climatic events. Sci. Total Environ. 808, 152170. https://doi.org/10.1016/j.scitotenv.2021.152170 (2022).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Lobell, D. et al. The critical role of extreme heat for maize production in the United States. Nat. Clim. Change. 3, 497–501. https://doi.org/10.1038/nclimate1832 (2013).Article 
    ADS 

    Google Scholar 
    Vermeulen, S. J. et al. Addressing uncertainty in adaptation planning for agriculture. Proc. Natl. Acad. Sci. 110, 8357–8362. https://doi.org/10.1073/pnas.1219441110 (2013).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    FAO. Climate Change and Food Security: Risks and Responses (FAO, 2015).
    Google Scholar 
    Ray, D. K., Gerber, J. S., MacDonald, G. K. & West, P. C. Climate variation explains a third of global crop yield variability. Nat. Commun. 6, 5989. https://doi.org/10.1038/ncomms6989 (2015).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ding, Z. et al. Modeling the combined impacts of deficit irrigation, rising temperature and compost application on wheat yield and water productivity. Agric. Water Manag. 244, 106626. https://doi.org/10.1016/j.agwat.2020.106626 (2021).Article 

    Google Scholar 
    Malhi, G. S., Kaur, M. & Kaushik, P. Impact of climate change on agriculture and its mitigation strategies: A review. Sustainability 13, 1318 (2021).Article 
    CAS 

    Google Scholar 
    Persson, T. & Kværnø, S. Impact of projected mid-21st century climate and soil extrapolation on simulated spring wheat grain yield in Southeastern Norway. J. Agric. Sci. 155, 361–377. https://doi.org/10.1017/S0021859616000241 (2017).Article 

    Google Scholar 
    Zhu, X. & Troy, T. J. Agriculturally relevant climate extremes and their trends in the world’s major growing regions. Earth’s Future 6, 656–672. https://doi.org/10.1002/2017EF000687 (2018).Article 
    ADS 

    Google Scholar 
    Fischer, T. et al. Increase in irrigated wheat yield in north-west Mexico from 1960 to 2019: Unravelling the negative relationship to minimum temperature. Field Crops Res. 275, 108331. https://doi.org/10.1016/j.fcr.2021.108331 (2022).Article 
    ADS 

    Google Scholar 
    Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616–620. https://doi.org/10.1126/science.1204531 (2011).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Harkness, C. et al. Adverse weather conditions for UK wheat production under climate change. Agric. For. Meteorol. 282, 107862. https://doi.org/10.1016/j.agrformet.2019.107862 (2020).Article 
    ADS 
    PubMed 

    Google Scholar 
    Seehusen, T. & Uhlen, A. K. Analyses of yield gaps for the production of wheat and barley in Norway, potential to increase yields on existing farmland. Norwegian Institute for Bioeconomics, Report 5/166/2019 (2020).Hakala, K. et al. Sensitivity of barley varieties to weather in Finland. J. Agric. Sci. 150, 145–160. https://doi.org/10.1017/S0021859611000694 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Peltonen-Sainio, P., Jauhiainen, L., Hakala, K. & Ojanen, H. Climate change and prolongation of growing season, changes in regional potential for field crop production in Finland. Agric. Food Sci. 18, 171–190. https://doi.org/10.2137/145960609790059479 (2009).Article 

    Google Scholar 
    Fleisher, D. H. et al. A potato model intercomparison across varying climates and productivity levels. Glob. Change Biol. 23, 1258–1281. https://doi.org/10.1111/gcb.13411 (2017).Article 
    ADS 

    Google Scholar 
    Moen, A. National Atlas of Norway: Vegetation (Hønefoss, 1999).
    Google Scholar 
    Bakkestuen, V., Erikstad, L. & Halvorsen, R. Step-less models for regional environmental variation in Norway. J. Biogeogr. 35, 1906–1922 (2008).Article 

    Google Scholar 
    Statistics-Norway. 2020. https://www.ssb.no/jord-skog-jakt-og-fiskeri/statistikker/stjord (Accessed 10 November 2020).Hanssen-Bauer, I. et al. Climate in Norway 2100 – a knowledge base for climate adaptation. Norwegian Centre for Climate Sciences, Report 1/2017 49 (2017).Blandford, D., Gaasland, I., Vårdal, E. & McIntosh, C. Greenhouse gas emissions, land use, and food supply under the paris climate agreement—Policy choice in Norway. Appl. Econ. Perspect. Policy 41, 249–264. https://doi.org/10.1093/aepp/ppy011 (2019).Article 

    Google Scholar 
    Rötter, R. P. et al. What would happen to barley production in Finland if global warming exceeded 4 °C? A model-based assessment. Eur. J. Agron. 35, 205–214. https://doi.org/10.1016/j.eja.2011.06.003 (2011).Article 

    Google Scholar 
    Ozturk, I., Sharif, B., Baby, S., Jabloun, M. & Olesen, J. E. The long-term effect of climate change on productivity of winter wheat in Denmark, scenario analysis using three crop models. J. Agric. Sci. 155, 733–750. https://doi.org/10.1017/S0021859616001040 (2017).Article 
    CAS 

    Google Scholar 
    An, H. & Carew, R. Effect of climate change and use of improved varieties on barley and canola yield in Manitoba. Can. J. Plant Sci. 95, 127–139. https://doi.org/10.1139/CJPS-2014-221 (2014).Article 

    Google Scholar 
    Zhou, Z., Plauborg, F., Kristensen, K. & Andersen, M. Dry matter production, radiation interception and radiation use efficiency of potato in response to temperature and nitrogen application regimes. Agric. For. Meteorol. 232, 595–605. https://doi.org/10.1016/j.agrformet.2016.10.017 (2017).Article 
    ADS 

    Google Scholar 
    Jensen, K. J. S. et al. Yield and development of winter wheat (Triticum aestivum L.) and spring barley (Hordeum vulgare L.) in field experiments with variable weather and drainage conditions. Eur. J. Agron. 122, 126075. https://doi.org/10.1016/j.eja.2020.126075 (2021).Article 
    CAS 

    Google Scholar 
    Lobell, D. B., Cahill, K. N. & Field, C. B. Historical effects of temperature and precipitation on California crop yields. Clim. Change 81, 187–203. https://doi.org/10.1007/s10584-006-9141-3 (2007).Article 
    ADS 

    Google Scholar 
    Skjelvag, A. O. Climatic conditions for crop production in Nordic countries. Agric. Food Sci. Finland 7(2), 149–160 (1998).Article 

    Google Scholar 
    Norsk-Klimaservicesenter. https://seklima.met.no/ (2020).Erikstad, L. & Bakkestuen, V. Calculating cumulative effects in GIS using a stepless multivariate model. MethodsX 8, 101407. https://doi.org/10.1016/j.mex.2021.101407 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aune-Lundberg, L. & Strand, G.-H. The content and accuracy of the CORINE land cover dataset for Norway. Int. J. Appl. Earth Observ. Geoinform. 96, 102266. https://doi.org/10.1016/j.jag.2020.102266 (2021).Article 

    Google Scholar 
    QGIS Geographic Information System (QGIS Association, 2020).R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
    Google Scholar 
    Lobell, D. B. & Field, C. B. Global scale climate–crop yield relationships and the impacts of recent warming. Environ. Res. Lett. 2, 014002. https://doi.org/10.1088/1748-9326/2/1/014002 (2007).Article 
    ADS 

    Google Scholar 
    Shumway, R. H. & Stoffer, D. S. Time Series Analysis and its Applications Vol. 560 (Springer, 2016).MATH 

    Google Scholar 
    Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9, 378–400 (2017).Article 

    Google Scholar 
    Lüdecke, D., Ben Shachar, M., Patil, I., Waggoner, P. & Makowski, D. Performance: An R Package for Assessment, Comparison and Testing of Statistical Models (2021).Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.3.3.0 (2020).Friedman, J. H., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33(22), 2010. https://doi.org/10.18637/jss.v033.i01 (2010).Article 

    Google Scholar 
    Tibshirani, R. Regression shrinkage and selection via the Lasso. J. R. Stat. Soc. Ser. B-Methodol. 58, 267–288. https://doi.org/10.1111/j.2517-6161.1996.tb02080.x (1996).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Hastie, T., Tibshirani, R. & Friendman, J. The Elements of Statistical Learning: Data Mining, Inference, and Prediction (Springer, 2009).Book 
    MATH 

    Google Scholar 
    Meinshausen, N. & Bühlmann, P. Stability selection. J. Roy. Stat. Soc. B 72, 417–473. https://doi.org/10.2307/40802220 (2010).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Efron, B. & Stein, C. The jackknife estimate of variance. Ann. Stat. 9, 586–596. https://doi.org/10.1214/aos/1176345462 (1981).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Milborrow, S. plotmo: Plot a Model’s Residuals, Response, and Partial Dependence Plots. R package version 3.5.7 (2020).Liu, H. Xu, X. & Li, J.J. HDCI: High Dimensional Confidence Interval Based on Lasso and Bootstrap. R package version 1.0–2 (2017).. Seehusen, T. & Uhlen, A. K. Analyses of yield gaps for the production of wheat and barley in Norway, potential to increase yields on existing farmland. Norwegian Institute for Bioeconomics, Report 5/166/2019. http://hdl.handle.net/11250/2637490 (2019).Stabbetorp, H. Dyrkingsomfang og avling i kornproduksjonen. Norsk institutt for bioøkonomi, Report 4 (1) (2017).Ebrahimi, E. et al. Assessing the impact of climate change on crop management in winter wheat—A case study for Eastern Austria. J. Agric. Sci. 154, 1153–1170. https://doi.org/10.1017/S0021859616000083 (2016).Article 

    Google Scholar 
    Kristensen, K., Schelde, K. & Olesen, J. Winter wheat yield response to climate variability in Denmark. J. Agric. Sci. 148, 1–15. https://doi.org/10.1017/S0021859610000675 (2010).Article 

    Google Scholar 
    Thaler, S., Eitzinger, J., Trnka, M. & Dubrovsky, M. Impacts of climate change and alternative adaptation options on winter wheat yield and water productivity in a dry climate in Central Europe. J. Agric. Sci. 150, 537–555. https://doi.org/10.1017/S0021859612000093 (2012).Article 
    CAS 

    Google Scholar 
    Ortiz, R. et al. Climate change, can wheat beat the heat?. Agr. Ecosyst. Environ. 126, 46–58. https://doi.org/10.1016/j.agee.2008.01.019 (2008).Article 

    Google Scholar 
    Semenov, M., Stratonovitch, P., Alghabari, F. & Gooding, M. Adapting wheat in Europe for climate change. J. Cereal Sci. 59, 245–256. https://doi.org/10.1016/j.jcs.2014.01.006 (2014).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Roberts, M. J., Braun, N. O., Sinclair, T. R., Lobell, D. B. & Schlenker, W. Comparing and combining process-based crop models and statistical models with some implications for climate change. Environ. Res. Lett. 12, 095010. https://doi.org/10.1088/1748-9326/aa7f33 (2017).Article 
    ADS 

    Google Scholar 
    Zhu, X., Troy, T. & Devineni, N. Stochastically modeling the projected impacts of climate change on rainfed and irrigated US crop yields. Environ. Res. Lett. 14, 074021. https://doi.org/10.1088/1748-9326/ab25a1 (2019).Article 
    ADS 

    Google Scholar 
    Lobell, D. & Asseng, S. Comparing estimates of climate change impacts from process-based and statistical crop models. Environ. Res. Lett. 12, 015001. https://doi.org/10.1088/1748-9326/aa518a (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Flø, S. et al. Rom for bruk av Norsk korn. Felleskjøpet, Report 49 (2017).Lillemo, M., Reitan, L. & Bjornstad, A. Increasing impact of plant breeding on barley yields in central Norway from 1946 to 2008. Plant Breeding 129, 484–490. https://doi.org/10.1111/j.1439-0523.2009.01710.x (2010).Article 

    Google Scholar 
    Wonneberger, R., Ficke, A. & Lillemo, M. Mapping of quantitative trait loci associated with resistance to net form net blotch (Pyrenophora teres f. teres) in a doubled haploid Norwegian barley population. PLoS One 12, e0175773. https://doi.org/10.1371/journal.pone.0175773 (2017).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moore, F. C. & Lobell, D. B. The fingerprint of climate trends on European crop yields. Proc. Natl. Acad. Sci. 112, 2670–2675. https://doi.org/10.1073/pnas.1409606112 (2015).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Martin, P. et al. Recent warming across the North Atlantic region may be contributing to an expansion in barley cultivation. Clim. Change 145, 351–365. https://doi.org/10.1007/s10584-017-2093-y (2017).Article 
    ADS 

    Google Scholar 
    Martin, P., Wishart, J., Dalmannsdottir, S., Halland, H. & Thomsen, a. M. Recent warming and the thermal requirement of barley in coastal Norway. Norwegian Institute for Bioeconomics, Report T2.4.3 ii (2018).Cattivelli, L., Ceccarelli, S., Romagosa, I. & Stanca, M. Abiotic stresses in Barley: Problems and solutions. In Barley: Production, Improvement, and Uses Vol. 4 (ed. Ullrich, S.) 282–306 (Blackwell UP, 2011).
    Google Scholar 
    Hura, T. Wheat and barley acclimatization to abiotic and biotic stress. Int. J. Mol. Sci. 21, 7423. https://doi.org/10.3390/ijms21197423 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kolberg, D., Persson, T., Mangerud, K. & Riley, H. Impact of projected climate change on workability, attainable yield, profitability and farm mechanization in Norwegian spring cereals. Soil Till. Res. 185, 122–138. https://doi.org/10.1016/j.still.2018.09.002 (2019).Article 

    Google Scholar 
    Olesen, J. E. et al. Impacts and adaptation of European crop production systems to climate change. Eur. J. Agron. 34, 96–112. https://doi.org/10.1016/j.eja.2010.11.003 (2011).Article 

    Google Scholar 
    Gammans, M., Mérel, P. & Ortiz-Bobea, A. Negative impacts of climate change on cereal yields: Statistical evidence from France. Environ. Res. Lett. 12, 054007. https://doi.org/10.1088/1748-9326/aa6b0c (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Ahmed, I., Harrison, M., Meinke, H. & Zhou, M. Barley phenology: physiological and molecular mechanisms for heading date and modelling of genotype-environment- management interactions. Plant Growth InTech 8, 175–202. https://doi.org/10.5772/64827 (2016).Article 
    CAS 

    Google Scholar 
    Hossain, A., da Silva, J. A. T., Lozovskaya, M. V. & Zvolinsky, V. P. High temperature combined with drought affect rainfed spring wheat and barley in South-Eastern Russia. Saudi J. Biol. Sci. 19, 473–487. https://doi.org/10.1016/j.sjbs.2012.07.005 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Møllerhagen, P. Norsk potetproduksjon 2011. Bioforsk, Report 7(1) (2012).Hermansen, A., Lu, D. & Forbes, G. Potato production in China and Norway, similarities, differences and future challenges. Potato Res. 55, 197–203. https://doi.org/10.1007/s11540-012-9224-7 (2012).Article 

    Google Scholar 
    Hermansen, A., Nærstad, R., Le, V. & Nordskog, B. In Proceedings of the Eleventh EuroBlight Workshop (The Norwegian Institute for Agricultural and Environmental Research, Hamar, 2018).Raymundo, R. et al. Climate change impact on global potato production. Eur. J. Agron. 100, 87–98. https://doi.org/10.1016/j.eja.2017.11.008 (2018).Article 

    Google Scholar 
    Rabia, A., Yacout, D., Shahin, S., Mohamed, A. & Abdelaty, E. Towards sustainable production of potato under climate change conditions. Curr. J. Appl. Sci. Technol. 18, 200–207. https://doi.org/10.14456/cast.2018.15 (2018).Article 

    Google Scholar 
    Haverkort, A. J., Franke, A. C., Engelbrecht, F. A. & Steyn, J. M. Climate change and potato production in contrasting South African agro-ecosystems. Potato Res. 56, 67–84. https://doi.org/10.1007/s11540-013-9230-4 (2013).Article 

    Google Scholar 
    Martinelli, F. et al. Advanced methods of plant disease detection A review. Agron. Sustain. Dev. 35, 1–25. https://doi.org/10.1007/s13593-014-0246-1 (2015).Article 

    Google Scholar 
    Borus, D. Impacts of Climate Change on the Potato (Solanum Tuberosum L.) Productivity in Tasmania, Australia and Kenya (University of Tasmania, 2017).
    Google Scholar 
    Fageria, N., Baligar, V. & Jones, C. Growth and Mineral Nutrition of Field Crops Vol. 5, 586 (CRC Press, 2010).Book 

    Google Scholar 
    Fleisher, D. H. et al. Effects of elevated CO2 and cyclic drought on potato under varying radiation regimes. Agric. For. Meteorol. 171, 270–280. https://doi.org/10.1016/j.agrformet.2012.12.011 (2013).Article 
    ADS 

    Google Scholar 
    Haverkort, A. J. & Struik, P. C. Yield levels of potato crops: Recent achievements and future prospects. Field Crop Res. 182, 76–85. https://doi.org/10.1016/j.fcr.2015.06.002 (2015).Article 

    Google Scholar 
    Van Oort, P. A. J., Timmermans, B. G. H., Meinke, H. & Van Ittersum, M. K. Key weather extremes affecting potato production in the Netherlands. Eur. J. Agron. 37, 11–22. https://doi.org/10.1016/j.eja.2011.09.002 (2012).Article 

    Google Scholar 
    Najafi, E., Devineni, N., Khanbilvardi, R. & Kogan, F. Understanding the changes in global crop yields through changes in climate and technology. Earth’s Future 6, 410–427. https://doi.org/10.1002/2017EF000690 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Pulatov, B., Anna Maria, J. N., Karin, H. & Maj-Lena, L. Modeling climate change impact on potato crop phenology, and risk of frost damage and heat stress in northern Europe. Agric. For. Meteorol. 214, 281–292. https://doi.org/10.1016/j.agrformet.2015.08.266 (2015).Article 
    ADS 

    Google Scholar  More

  • in

    Rickettsia felis DNA recovered from a child who lived in southern Africa 2000 years ago

    Mounier, A. et al. Deciphering African late middle Pleistocene hominin diversity and the origin of our species. Nat. Commun. https://doi.org/10.1038/s41467-019-11213-w (2019).Schlebusch, C. M. et al. Southern African ancient genomes estimate modern human divergence to 350,000 to 260,000 years ago. Science 358, 652–655 (2017).CAS 
    PubMed 

    Google Scholar 
    Lombard, M. et al. Ancient human DNA: how sequencing the genome of a boy from Ballito Bay changed human history. S Afr. J. Sci. 114, 1–3 (2018).
    Google Scholar 
    Grün, R. et al. Direct dating of Florisbad hominid. Nature 382, 500–501 (1996).PubMed 

    Google Scholar 
    Grine, F. et al. The Middle Stone Age human fossil record from Klasies River Main Site. J. Hum. Evol. 103, 53–78 (2017).PubMed 

    Google Scholar 
    Henshilwood, C. S. et al. A 100,000-year-old ochre-processing workshop at Blombos Cave, South Africa. Science 33, 219–222 (2011).
    Google Scholar 
    Lombard, M. et al. Four-field co-evolutionary model for human cognition: variation in the Middle Stone Age/Middle Palaeolithic. J. Archeol. Method Theory 28, 142–177 (2021).
    Google Scholar 
    Wadley, L. What stimulated rapid, cumulative innovation after 100,000 years ago? J. Archeol. Method Theory 28, 120–141 (2021).
    Google Scholar 
    Tylen, K. et al. The evolution of early symbolic behavior in Homo sapiens. Proc. Natl Acad. Sci. USA 117, 4578–4584 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rifkin, R. F. et al. Ancient oncogenesis, infection, and human evolution. Evol. Appl. https://doi.org/10.1111/eva.12497 (2017).Pittman, K. J. et al. The legacy of past pandemics: common human mutations that protect against infectious disease. PLoS Pathog. 12, e1005680 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Andam, C. P. et al. Microbial genomics of ancient plagues and outbreaks. Trends Microbiol. 24, 978–990 (2016).CAS 
    PubMed 

    Google Scholar 
    Houldcroft, C. J. et al. Migrating microbes: what pathogens can tell us about population movements and human evolution. Ann. Hum. Biol. 44, 397–407 (2017).PubMed 

    Google Scholar 
    Reyes-Centeno, H. et al. Testing modern human out-of-Africa dispersal models using dental nonmetric data. Curr. Anthropol. 58, 406–417 (2017).
    Google Scholar 
    Pimenoff, V. N. et al. The role of aDNA in understanding the co-evolutionary patterns of human sexually transmitted infections. Genes https://doi.org/10.3390/genes9070317 (2018).Ferwerda, B. et al. Functional consequences of Toll-like Receptor 4 polymorphisms. Mol. Med. 14, 346–352 (2008).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tanabe, K. et al. Plasmodium falciparum accompanied the human expansion out of Africa. Curr. Biol. 20, 1283–1289 (2010).CAS 
    PubMed 

    Google Scholar 
    Linz, B. et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445, 915–918 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    Nédélec, Y. et al. Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell 167, 657–669 (2016).PubMed 

    Google Scholar 
    Owers, K. A. et al. Adaptation to infectious disease exposure in indigenous Southern African populations. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2017.0226 (2017).Schlebusch, C. M. et al. Khoe-San genomes reveal unique variation and confirm the deepest population divergence in Homo sapiens. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msaa140 (2020).Kessler, S. E. et al. Selection to outsmart the germs: the evolution of disease recognition and social cognition. J. Hum. Evol. 108, 92–109 (2017).PubMed 

    Google Scholar 
    Thornhill, R. et al. The parasite-stress theory of sociality, the behavioral immune system, and human social and cognitive uniqueness. Evol. Behav. Sci. 8, 257–264 (2014).
    Google Scholar 
    Gurven, M. et al. Longevity among hunter‐gatherers: a cross‐cultural examination. Popul Dev. Rev. 33, 321–365 (2007).
    Google Scholar 
    Pfeiffer, S. et al. The people behind the samples: biographical features of past hunter-gatherers from KwaZulu-Natal who yielded aDNA. Int. J. Paleopathol. 24, 158–164 (2019).PubMed 

    Google Scholar 
    Schriefer, M. E. et al. Identification of a novel rickettsial infection in a patient diagnosed with murine typhus. J. Clin. Microbiol. 32, 949–954 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pages, F. et al. The past and present threat of vector-borne diseases in deployed troops. Clin. Microbiol. Infect. 16, 209–224 (2010).CAS 
    PubMed 

    Google Scholar 
    Wood, D. E. et al. Improved metagenomic analysis with Kraken 2. Genome Biol. https://doi.org/10.1186/s13059-019-1891-0 (2019).Jónsson, H. et al. mapDamage 2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Gillespie, J. J. et al. Genomic diversification in strains of Rickettsia felis isolated from different arthropods. Genome Biol. Evol. 7, 35–56 (2015).CAS 

    Google Scholar 
    Cardwell, M. M. et al. The Sca2 autotransporter protein from Rickettsia conorii is sufficient to mediate adherence to and invasion of cultured mammalian cells. Infect. Immun. 77, 5272–5280 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kay, G. L. et al. Recovery of a Medieval Brucella melitensis genome using shotgun metagenomics. mBio. https://doi.org/10.1128/mBio.01337-14 (2014).Schuenemann, V. J. et al. Genome-wide comparison of medieval and modern Mycobacterium leprae. Science 341, 179–183 (2013).CAS 
    PubMed 

    Google Scholar 
    Müller, R. et al. Genotyping of ancient Mycobacterium tuberculosis strains reveals historic genetic diversity. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2013.3236 (2014).Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vågene, A. J. et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nat. Ecol. Evol. 2, 520–528 (2018).PubMed 

    Google Scholar 
    Guellil, M. et al. Genomic blueprint of a relapsing fever pathogen in 15th century Scandinavia. Proc. Natl Acad. Sci. USA 115, 10422–10427 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Patterson Ross, Z. et al. The paradox of HBV evolution as revealed from a 16th century mummy. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1006750 (2015).Marciniak, S. et al. Plasmodium falciparum malaria in 1st-2nd century CE southern Italy. Curr. Biol. 26, 1220–1222 (2016).
    Google Scholar 
    Margaryan, A. et al. Ancient pathogen DNA in human teeth and petrous bones. Ecol. Evol. https://doi.org/10.1002/ece3.3924 (2018).Zhou, Z. et al. Pan-genome analysis of ancient and modern Salmonella enterica demonstrates genomic stability of the invasive Para C lineage for millennia. Curr. Biol. 28, 2420–2428 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, K. M. Update on bone health in paediatric chronic disease. Endocrinol. Metab. Clin. North Am. https://doi.org/10.1016/j.ecl.2016.01.009 (2016).Latham, K.E. et al. DNA recovery and analysis from skeletal material in modern forensic contexts. Forensic Sci. Res. https://doi.org/10.1080/20961790.2018.1515594 (2019).Briggs, H. M. et al. Diagnosis and management of tickborne Rickettsial diseases: rocky mountain spotted fever and other spotted fever group Rickettsioses, Ehrlichioses, and Anaplasmosis – United States. MMWR Recomm. Rep. 65, 1–44 (2016).
    Google Scholar 
    Jonker, F. A. M. et al. Anaemia, iron deficiency and susceptibility to infection in children in sub‐Saharan Africa, guideline dilemmas. Br. J. Haematol. https://doi.org/10.1111/bjh.14593. (2017).Key, F. M. et al. Emergence of human-adapted Salmonella enterica is linked to the Neolithization process. Nat. Ecol. Evol. 4, 324–333 (2020).
    Google Scholar 
    Angelakis, E. et al. Rickettsia felis: the complex journey of an emergent human pathogen. Trends Parasitol. https://doi.org/10.1016/j.pt.2016.04.009 (2016).Legendre, K. P. et al. Rickettsia felis: A review of transmission mechanisms of an emerging pathogen. Trop. Med. Infect. Dis. https://doi.org/10.3390/tropicalmed2040064 (2017).Mediannikov, O. et al. Common epidemiology of Rickettsia felis infection and malaria, Africa. Emerg. Infect. Dis. https://doi.org/10.3201/eid1911.130361 (2014).Gonçalves, B. P. et al. Examining the human infectious reservoir for Plasmodium falciparum malaria in areas of differing transmission intensity. Nat. Commun. https://doi.org/10.1038/s41467-017-01270-4 (2017).Snowden, J. et al. Rickettsia rickettsiae (Rocky Mountain Spotted Fever). StatPearls Publishing, available from https://www.ncbi.nlm.nih.gov/books/NBK430881/ (2017).Azad, A. A. Pathogenic Rickettsiae as bioterrorism agents. Ann. N. Y Acad. Sci. 990, 734–738 (2007).
    Google Scholar 
    Oliveira, R. P. et al. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg. Infect. Dis. https://doi.org/10.3201/eid0803.010301 (2002).Parola, P. et al. Rickettsia felis: The next mosquito-borne outbreak? Lancet Infect. Dis. https://doi.org/10.1016/S1473-3099(16)30331-0 (2016).Wadley, L. Legacies from the Later Stone Age. S Afr Archaeol Bull. Goodwin Ser. 6, 42–53 (1989).
    Google Scholar 
    Henn, B. M. et al. The great human expansion. Proc. Natl Acad. Sci. USA 109, 17758–17764 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yang, D. Y. et al. Technical note: improved DNA extraction from ancient bones using silica-based spin columns. Am. J. Phys. Anthropol. 105, 539–543 (1998).CAS 
    PubMed 

    Google Scholar 
    Malmström, E. M. et al. More on contamination: the use of asymmetric molecular behavior to identify authentic ancient human DNA. Mol. Biol. Evol. 24, 998–1004 (2007).PubMed 

    Google Scholar 
    Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl Acad. Sci. USA 110, 15758–15763 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Meyer, M. et al. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protoc. https://doi.org/10.1101/pdb.prot5448 (2010).Li, H. et al. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Briggs, A. W. et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc. Natl Acad. Sci. USA 104, 14616–14621 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Borry, M. et al. PyDamage: automated ancient damage identification and estimation for contigs in ancient DNA de novo assembly. PeerJ. https://doi.org/10.7717/peerj.11845 (2021).Schubert, M. et al. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res. https://doi.org/10.1186/s13104-016-1900-2 (2016).Langmead, B. et al. Fast gapped-read alignment with Bowtie 2. Nat. Methods. https://doi.org/10.1038/nmeth.1923 (2012).Bankevich, A. et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. https://doi.org/10.1089/cmb.2012.0021 (2012).Jain, C. et al. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. https://doi.org/10.1038/s41467-018-07641-9 (2018).Gardner, S. H. et al. kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics. https://doi.org/10.1093/bioinformatics/btv271 (2015).Contreras-Moreira, B. et al. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.02411-13 (2013).Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. https://doi.org/10.1101/gr.092759.109 (2009).Parks, D. H. et al. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Genome Res. https://doi.org/10.1101/gr.186072.114 (2015).Suyama, M. et al. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dereeper, A. et al. Phylogeny. fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. https://doi.org/10.1093/nar/gkn180 (2008).Nguyen, L. T. et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msu300 (2015).Hoang, D. T. et al. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msx281 (2018).Kalyaanamoorthy, S. et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. https://doi.org/10.1038/nmeth.4285 (2017).Price, M. N. et al. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One. https://doi.org/10.1371/journal.pone.0009490 (2010).Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. https://doi.org/10.1093/bioinformatics/btl446 (2006).Kumar, S. et al. MEGA-CC: Computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics. https://doi.org/10.1093/bioinformatics/bts507 (2012).Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. https://doi.org/10.1080/10635150290069913 (2002).Olm, M. R. et al. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. https://doi.org/10.1038/ismej.2017.126 (2017).Posada, D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 7, 1253–1256 (2008).
    Google Scholar 
    Letunic, I. et al. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007).CAS 
    PubMed 

    Google Scholar  More

  • in

    Interspecific interactions alter the metabolic costs of climate warming

    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).Article 
    CAS 

    Google Scholar 
    Seebacher, F., White, C. R. & Franklin, C. E. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Change 5, 61–66 (2015).Article 

    Google Scholar 
    Havird, J. C. et al. Distinguishing between active plasticity due to thermal acclimation and passive plasticity due to Q10 effects: why methodology matters. Funct. Ecol. 34, 1015–1028 (2020).Article 

    Google Scholar 
    Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706 (2010).Article 
    CAS 

    Google Scholar 
    White, C. R., Alton, L. A., Bywater, C. L., Lombardi, E. J. & Marshall, D. J. Metabolic scaling is the product of life history optimization. Science 377, 834–839 (2022).Article 
    CAS 

    Google Scholar 
    Savage, V. M., Gilloly, J. F., Brown, J. H. & Charnov, E. L. Effects of body size and temperature on population growth. Am. Nat. 163, 429–441 (2004).Article 

    Google Scholar 
    Bernhardt, J. R., Sunday, J. M. & O’Connor, M. I. Metabolic theory and the temperature–size rule explain the temperature dependence of population carrying capacity. Am. Nat. 192, 687–697 (2018).Article 

    Google Scholar 
    Damuth, J. Population density and body size in mammals. Nature 290, 699–700 (1981).Article 

    Google Scholar 
    Schuster, L., Cameron, H., White, C. R. & Marshall, D. J. Metabolism drives demography in an experimental field test. Proc. Natl Acad. Sci. USA 118, e2104942118 (2021).Article 
    CAS 

    Google Scholar 
    Amarasekare, P. & Coutinho, R. M. The intrinsic growth rate as a predictor of population viability under climate warming. J. Anim. Ecol. 82, 1240–1253 (2013).Article 

    Google Scholar 
    Amarasekare, P. & Savage, V. A framework for elucidating the temperature dependence of fitness. Am. Nat. 179, 178–191 (2012).Article 

    Google Scholar 
    Lande, R. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142, 911–927 (1993).Article 

    Google Scholar 
    Comeault, A. A. & Matute, D. R. Temperature-dependent competitive outcomes between the fruit flies Drosophila santomea and Drosophila yakuba. Am. Nat. 197, 312–323 (2021).Article 

    Google Scholar 
    Davis, A. J., Jenkinson, L. S., Lawton, J. H., Shorrocks, B. & Wood, S. Making mistakes when predicting shifts in species range in response to global warming. Nature 391, 783–786 (1998).Article 
    CAS 

    Google Scholar 
    Davis, A. J., Lawton, J. H., Shorrocks, B. & Jenkinson, L. S. Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J. Anim. Ecol. 67, 600–612 (1998).Article 

    Google Scholar 
    Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).Article 

    Google Scholar 
    Janča, M. & Gvoždík, L. Costly neighbours: heterospecific competitive interactions increase metabolic rates in dominant species. Sci. Rep. 7, 5177 (2017).Article 

    Google Scholar 
    Pettersen, A. K., Hall, M. D., White, C. R. & Marshall, D. J. Metabolic rate, context-dependent selection, and the competition–colonization trade-off. Evol. Lett. 4, 333–344 (2020).Article 

    Google Scholar 
    DeLong, J. P., Hanley, T. C. & Vasseur, D. A. Competition and the density dependence of metabolic rates. J. Anim. Ecol. 83, 51–58 (2014).Article 

    Google Scholar 
    Reid, D., Armstrong, J. D. & Metcalfe, N. B. Estimated standard metabolic rate interacts with territory quality and density to determine the growth rates of juvenile Atlantic salmon. Funct. Ecol. 25, 1360–1367 (2011).Article 

    Google Scholar 
    Ayala, F. J. in Essays in Evolution and Genetics in Honor of Theodosius Dobzhansky (eds Hecht, M. K. & Steere, W. C.) 121–158 (Springer, 1970).Atkinson, W. D. & Shorrocks, B. Aggregation of larval Diptera over discrete and ephemeral breeding sites: the implications for coexistence. Am. Nat. 124, 336–351 (1984).Article 

    Google Scholar 
    McKenzie, J. A. & McKechnie, S. W. A comparative study of resource utilization in natural populations of Drosophila melanogaster and D. simulans. Oecologia 40, 299–309 (1979).Article 
    CAS 

    Google Scholar 
    Alton, L. A. et al. Developmental nutrition modulates metabolic responses to projected climate change. Funct. Ecol. 34, 2488–2502 (2020).Article 

    Google Scholar 
    Mitchell, K. A. & Hoffmann, A. A. Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila. Funct. Ecol. 24, 694–700 (2010).Article 

    Google Scholar 
    Overgaard, J., Kristensen, T. N., Mitchell, K. A. & Hoffmann, A. A. Thermal tolerance in widespread and tropical Drosophila species: does phenotypic plasticity increase with latitude? Am. Nat. 178, S80–S96 (2011).Article 

    Google Scholar 
    Kellermann, V. et al. Comparing thermal performance curves across traits: how consistent are they? J. Exp. Biol. 222, jeb193433 (2019).Article 

    Google Scholar 
    Terblanche, J. S., Clusella-Trullas, S. & Chown, S. L. Phenotypic plasticity of gas exchange pattern and water loss in Scarabaeus spretus (Coleoptera: Scarabaeidae): deconstructing the basis for metabolic rate variation. J. Exp. Biol. 213, 2940–2949 (2010).Article 

    Google Scholar 
    Tewksbury, J. J., Huey, R. B. & Deutsch, C. A. Putting the heat on tropical animals. Science 320, 1296–1297 (2008).Article 
    CAS 

    Google Scholar 
    Bos, M., Burnet, B., Farrow, R. & Woods, R. A. Mutual facilitation between larvae of the sibling species Drosophila melanogaster and D. simulans. Evolution 31, 824–828 (1977).Article 
    CAS 

    Google Scholar 
    Arthur, W. On the complexity of a simple environment: competition, resource partitioning and facilitation in a two-species Drosophila system. Phil. Trans. R. Soc. B 313, 471–508 (1986).
    Google Scholar 
    Hodge, S., Mitchell, P. & Arthur, W. Factors affecting the occurrence of facilitative effects in interspecific interactions: an experiment using two species of Drosophila and Aspergillus niger. Oikos 87, 166–174 (1999).Article 

    Google Scholar 
    Bath, E., Morimoto, J. & Wigby, S. The developmental environment modulates mating-induced aggression and fighting success in adult female Drosophila. Funct. Ecol. 32, 2542–2552 (2018).Article 

    Google Scholar 
    Thibert, J., Farine, J. P., Cortot, J. & Ferveur, J. F. Drosophila food-associated pheromones: effect of experience, genotype and antibiotics on larval behavior. PLoS ONE 11, e0151451 (2016).Article 

    Google Scholar 
    Chown, S. L. et al. Scaling of insect metabolic rate is inconsistent with the nutrient supply network model. Funct. Ecol. 21, 282–290 (2007).Article 

    Google Scholar 
    Becker, R. A., Wilks, A. R. & Brownrigg, R. mapdata: extra map databases. R version 2.3.0 https://CRAN.R-project.org/package=mapdata (2018).R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).Article 

    Google Scholar 
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    Bolker, B. & R Development Core Team bbmle: tools for general maximum likelihood estimation. R version 1.0.25 https://CRAN.R-project.org/package=bbmle (2022).Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression 3rd edn (Sage, 2019).Hartig, F. DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R version 0.4.6 https://CRAN.R-project.org/package=DHARMa (2022).Messamah, B., Kellermann, V., Malte, H., Loeschcke, V. & Overgaard, J. Metabolic cold adaptation contributes little to the interspecific variation in metabolic rates of 65 species of Drosophilidae. J. Insect Physiol. 98, 309–316 (2017).Article 
    CAS 

    Google Scholar 
    Chamberlain, S. et al. rgbif: interface to the global biodiversity information facility API. R version 3.7.3 https://CRAN.R-project.org/package=rgbif (2022).Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    Hijmans, R. J. raster: geographic data analysis and modeling. R version 3.6-3 https://CRAN.R-project.org/package=raster (2022).Alton, L. A. & Kellermann, V. Data for “Interspecific interactions alter the metabolic costs of climate warming”. Zenodo https://doi.org/10.5281/zenodo.7475922 (2023).White, C. R. et al. Geographical bias in physiological data limits predictions of global change impacts. Funct. Ecol. 35, 1572–1578 (2021).Article 

    Google Scholar  More

  • in

    Disentangling the mixed effects of soil management on microbial diversity and soil functions: A case study in vineyards

    Ritz, K. & Young, I. M. Interactions between soil structure and fungi. Mycologist 18, 52–59 (2004).Article 

    Google Scholar 
    Schimel, J. P. & Schaeffer, S. M. Microbial control over carbon cycling in soil. Front. Microbiol. 3, 348 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Six, J., Bossuyt, H., Degryze, S. & Denef, K. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res. 79, 7–31 (2004).Article 

    Google Scholar 
    van der Heijden, M. G. A. & Wagg, C. Soil microbial diversity and agro-ecosystem functioning. Plant Soil 363, 1–5 (2013).Article 
    CAS 

    Google Scholar 
    Winter, S. et al. Effects of vegetation management intensity on biodiversity and ecosystem services in vineyards: a meta-analysis. J. Appl. Ecol. 55, 2484–2495 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Belmonte, S. A. et al. Effect of long-term soil management on the mutual interaction among soil organic matter, microbial activity and aggregate stability in a vineyard. Pedosphere 28, 288–298 (2018).Article 
    CAS 

    Google Scholar 
    Bronick, C. J. & Lal, R. Soil structure and management: a review. Geoderma 124, 3–22 (2005).Article 
    ADS 
    CAS 

    Google Scholar 
    Kratschmer, S. et al. Enhancing flowering plant functional richness improves wild bee diversity in vineyard inter-rows in different floral kingdoms. Ecol. Evol. 11, 7927–7945 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Constancias, F. et al. Microscale evidence for a high decrease of soil bacterial density and diversity by cropping. Agron. Sustain. Dev. 34, 831–840 (2014).Article 
    CAS 

    Google Scholar 
    Schmidt, R., Gravuer, K., Bossange, A. V., Mitchell, J. & Scow, K. Long-term use of cover crops and no-till shift soil microbial community life strategies in agricultural soil. PLoS One 13, e0192953 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vink, S. N., Chrysargyris, A., Tzortzakis, N. & Salles, J. F. Bacterial community dynamics varies with soil management and irrigation practices in grapevines (Vitis vinifera L.). Appl. Soil Ecol. 158, 103807 (2021).Article 

    Google Scholar 
    Pingel, M., Reineke, A. & Leyer, I. A 30-years vineyard trial: plant communities, soil microbial communities and litter decomposition respond more to soil treatment than to N fertilization. Agr. Ecosyst. Environ. 272, 114–125 (2019).Article 
    CAS 

    Google Scholar 
    Sharma-Poudyal, D., Schlatter, D., Yin, C., Hulbert, S. & Paulitz, T. Long-term no-till: a major driver of fungal communities in dryland wheat cropping systems. PLoS One 12, e0184611 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hungria, M., Franchini, J. C., Brandão-Junior, O., Kaschuk, G. & Souza, R. A. Soil microbial activity and crop sustainability in a long-term experiment with three soil-tillage and two crop-rotation systems. Appl. Soil. Ecol. 42, 288–296 (2009).Article 

    Google Scholar 
    Pascault, N. et al. In situ dynamics of microbial communities during decomposition of wheat, rape, and alfalfa residues. Microb. Ecol. 60, 816–828 (2010).Article 
    PubMed 

    Google Scholar 
    Tresch, S. et al. Litter decomposition driven by soil fauna, plant diversity and soil management in urban gardens. Sci. Total Environ. 658, 1614–1629 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Faust, S., Koch, H.-J., Dyckmans, J. & Joergensen, R. G. Response of maize leaf decomposition in litterbags and soil bags to different tillage intensities in a long-term field trial. Appl. Soil. Ecol. 141, 38–44 (2019).Article 

    Google Scholar 
    Liu, Y.-R. et al. New insights into the role of microbial community composition in driving soil respiration rates. Soil Biol. Biochem. 118, 35–41 (2018).Article 
    CAS 

    Google Scholar 
    Yang, C., Liu, N. & Zhang, Y. Soil aggregates regulate the impact of soil bacterial and fungal communities on soil respiration. Geoderma 337, 444–452 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bruggisser, O. T., Schmidt-Entling, M. H. & Bacher, S. Effects of vineyard management on biodiversity at three trophic levels. Biol. Cons. 143, 1521–1528 (2010).Article 

    Google Scholar 
    Lienhard, P. et al. Pyrosequencing evidences the impact of cropping on soil bacterial and fungal diversity in Laos tropical grassland. Agron. Sustain. Dev. 34, 525–533 (2014).Article 

    Google Scholar 
    Schnoor, T. K., Lekberg, Y., Rosendahl, S. & Olsson, P. A. Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21, 211–220 (2011).Article 
    PubMed 

    Google Scholar 
    Kazakou, E. et al. A plant trait-based response-and-effect framework to assess vineyard inter-row soil management. Bot. Lett. 163, 373–388 (2016).Article 

    Google Scholar 
    Svensson, J. R., Lindegarth, M., Jonsson, P. R. & Pavia, H. Disturbance-diversity models: What do they really predict and how are they tested?. Proc. Biol. Sci. 279, 2163–2170 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Bao, T. et al. Moderate disturbance increases the PLFA diversity and biomass of the microbial community in biocrusts in the Loess Plateau region of China. Plant Soil 451, 499–513 (2020).Article 
    CAS 

    Google Scholar 
    Liu, J. et al. Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biol. Biochem. 83, 29–39 (2015).Article 
    CAS 

    Google Scholar 
    Cotton, J. & Acosta-Martínez, V. Intensive tillage converting grassland to cropland immediately reduces soil microbial community size and organic carbon. Agric. Environ. Lett. 3, 180047 (2018).Article 

    Google Scholar 
    Poeplau, C. et al. Temporal dynamics of soil organic carbon after land-use change in the temperate zone – carbon response functions as a model approach. Glob. Change Biol. 17, 2415–2427 (2011).Article 
    ADS 

    Google Scholar 
    Burns, K. N. et al. Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: differentiation by vineyard management. Soil Biol. Biochem. 103, 337–348 (2016).Article 
    CAS 

    Google Scholar 
    Steiner, M. et al. Local conditions matter: minimal and variable effects of soil disturbance on microbial communities and functions in European vineyards. PLoS One 18, e0280516 (2023).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zeng, J. et al. Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol. Biochem. 92, 41–49 (2016).Article 
    CAS 

    Google Scholar 
    Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 103, 626–631 (2006).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Eisenhauer, N. Plant diversity effects on soil microorganisms: spatial and temporal heterogeneity of plant inputs increase soil biodiversity. Pedobiologia 59, 175–177 (2016).Article 

    Google Scholar 
    Porazinska, D. L. et al. Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99, 1942–1952 (2018).Article 
    PubMed 

    Google Scholar 
    Prober, S. M. et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol. Lett. 18, 85–95 (2015).Article 
    PubMed 

    Google Scholar 
    Sun, Y.-Q., Wang, J., Shen, C., He, J.-Z. & Ge, Y. Plant evenness modulates the effect of plant richness on soil bacterial diversity. Sci. Total Environ. 662, 8–14 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kuzyakov, Y. Priming effects: interactions between living and dead organic matter. Soil Biol. Biochem. 42, 1363–1371 (2010).Article 
    CAS 

    Google Scholar 
    Huo, C., Luo, Y. & Cheng, W. Rhizosphere priming effect: a meta-analysis. Soil Biol. Biochem. 111, 78–84 (2017).Article 
    CAS 

    Google Scholar 
    Dimassi, B. et al. Effect of nutrients availability and long-term tillage on priming effect and soil C mineralization. Soil Biol. Biochem. 78, 332–339 (2014).Article 
    CAS 

    Google Scholar 
    Prescott, C. E. Litter decomposition: What controls it and how can we alter it to sequester more carbon in forest soils?. Biogeochemistry 101, 133–149 (2010).Article 
    CAS 

    Google Scholar 
    Petraglia, A. et al. Litter decomposition: effects of temperature driven by soil moisture and vegetation type. Plant Soil 435, 187–200 (2019).Article 
    CAS 

    Google Scholar 
    Vukicevich, E., Lowery, T., Bowen, P., Úrbez-Torres, J. R. & Hart, M. Cover crops to increase soil microbial diversity and mitigate decline in perennial agriculture. A review. Agron. Sustain. Dev. (2016).Bani, A. et al. The role of microbial community in the decomposition of leaf litter and deadwood. Appl. Soil. Ecol. 126, 75–84 (2018).Article 

    Google Scholar 
    Bonanomi, G., Capodilupo, M., Incerti, G., Mazzoleni, S. & Scala, F. Litter quality and temperature modulate microbial diversity effects on decomposition in model experiments. Community Ecol. 16, 167–177 (2015).Article 

    Google Scholar 
    Daebeler, A. et al. Pairing litter decomposition with microbial community structures using the Tea Bag Index (TBI). SOIL Discuss. [preprint]; 10.5194/soil-2021-110 (2021).Keuskamp, J. A., Dingemans, B. J. J., Lehtinen, T., Sarneel, J. M. & Hefting, M. M. Tea Bag Index: a novel approach to collect uniform decomposition data across ecosystems. Methods Ecol. Evol. 4, 1070–1075 (2013).Article 

    Google Scholar 
    Schaller, K. Praktikum zur Bodenkunde und Pflanzenernährung. Hochschule Geisenheim, (2000).Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Ihrmark, K. et al. New primers to amplify the fungal ITS2 region–evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol. Ecol. 82, 666–677 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Schoch, C. L. et al. SI: Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. U.S.A. 109, 6241–6246 (2012).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. Available at https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).Joshi, N. A. & Fass, J. N. sickle – A Windowed Adaptive Trimming Tool for FASTQ Files Using Quality. Available at https://github.com/najoshi/sickle (2011).Schloss, P. D. et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    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).Article 
    CAS 
    PubMed 

    Google Scholar 
    Westcott, S. L. & Schloss, P. D. OptiClust, an improved method for assigning amplicon-based sequence data to operational taxonomic units. mSphere 2, e00073 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cole, J. R. et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Gweon, H. S. et al. PIPITS: an automated pipeline for analyses of fungal internal transcribed spacer sequences from the Illumina sequencing platform. Methods Ecol. Evol. 6, 973–980 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).Article 
    PubMed 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. Available at https://www.R-project.org/ (2019).McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haegeman, B. et al. Robust estimation of microbial diversity in theory and in practice. ISME J. 7, 1092–1101 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Scheu, S. Automated measurement of the respiratory response of soil microcompartments: Active microbial biomass in earthworm faeces. Soil Biol. Biochem. 24, 1113–1118 (1992).Article 

    Google Scholar 
    Mori, T. Validation of the Tea Bag Index as a standard approach for assessing organic matter decomposition: a laboratory incubation experiment. Ecol. Ind. 141, 109077 (2022).Article 
    CAS 

    Google Scholar 
    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–142. Available at https://CRAN.R-project.org/package=nlme (2019).Lenth, R. Emmeans: Estimated Marginal Means, Aka Least-Squares Means. R package version 1.4.4. Available at https://CRAN.R-project.org/package=emmeans (2020).Lefcheck, J. S. piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).Article 

    Google Scholar 
    Grace, J. B., Anderson, T. M., Olff, H. & Scheiner, S. M. On the specification of structural equation models for ecological systems. Ecol. Monogr. 80, 67–87 (2010).Article 

    Google Scholar 
    Shipley, B. A new inferential test for path models based on directed acyclic graphs. Struct. Equ. Model. 7, 206–218 (2000).Article 
    MathSciNet 

    Google Scholar  More

  • in

    New machine learning-based automatic high-throughput video tracking system for assessing water toxicity using Daphnia Magna locomotory responses

    Test organisms and exposuresIn this study, we used test organisms and reagents according to the Acute Toxicity Test Method of Daphnia magna Straus(Cladocera, Crustacea); ES 04704.1b29. Daphnia magna were fostered at the National Institute of Environmental Research and were adopted. During the test, adult female Daphnia magna over two weeks of age, cultured over several generations, were transferred to a freshly prepared container the day before the test. Daphnia magna are neonates for less than 24 h after birth29. To maintain the sensitivity of the organism, young individuals less than 24 h old that reproduced the following day were used. Individuals of a similar size were selected for the test. Daphnia magna was fed YCT, which is a mixture of green algae in Chlorella sp., yeast, Cerophy II(R), and trout chow. Sufficient amounts of prey were supplied 2 h before the test to minimize the effects of prey during the test. The test medium was prepared by dissolving KCl (8 mg/L), (text {MgSO}_4) (120 mg/L), (text {CaSO}_4 cdot 2 text {H}_2 text {O} ) (120 mg/L), and (text {NaHCO}_3) (192 mg/L) in deionized water.Automatic high-throughput Daphnia magna tracking systemTo build an automatic high-throughput Daphnia magna tracking system, we equipped the system with a video analysis algorithm as well as flow cells (Fig. 1). In the tracking system, six flow cells filled with culture medium were installed in the device. Each flow cell contained 10 Daphnia magna. Subsequently, to automatically measure the state of Daphnia magna, the six flow cells were photographed at 15 frames per second using a camera (Industrial Development Systems imaging) equipped with a CMOSIS sensor capable of infrared imaging. A red light close to the infrared spectrum was placed at the back of the flow cells for uniform illumination and to minimize stress on Daphnia magna. To capture the size and movement of the Daphnia magna as accurately as possible, the camera was set to a frame rate of 15 fps and a resolution of 2048 (times ) 1088 (2.23 MB), using a 12 mm lens. The distance between the flow cell and the camera was set to 16 cm. To measure the number of mobile Daphnia magna, their lethality, and swimming inhibition automatically and simultaneously, one camera for every two cells was used to collect the status data of Daphnia magna. For assessing ecotoxicity, the video analysis system used images obtained from the six flow cells to track each Daphnia magna and estimate key statistics such as the number of mobile individuals, average distance, and radius of activity.Figure 1New automatic high-throughput video tracking system for behavioral analysis using Daphnia magna as a model organismFull size imageThe automatic high-throughput video tracking system in the ecotoxicity measuring device was designed to continuously measure the ecotoxicity of Daphnia magna (Fig. 2). Daphnia magna moves faster at high temperatures and is less active at low temperatures. Thus, a constant temperature module that can be set to an appropriate Daphnia magna habitat temperature (20 ± 2 (^{circ })C) was added to create a suitable culture environment for Daphnia magna29. Natural pseudo-light ((lambda >590) nm, 3000 k) was installed on the upper part of the detector for proper habitat light intensity (500 Lux–1000 Lux). The size of the flow cell was set as small as possible while observing the movement of the Daphnia magna. An automatic feeding system was installed so that food could be injected during the replacement cycle. The six independent multi-flow cells were designed with an automatic dilution injection module; therefore, these flow cells were diluted to six different concentrations (100%, 50%, 25%, 12.5%, 6.25%, and 0%).Figure 2Schematic representation of the automatic high-throughput video tracking systemFull size imageAutomatic tracking algorithmThe CPU used for Daphnia magna tracking was Intel i5-9300H @ 2.40 GHz, with 8 GB of memory and Windows 10 Pro 64-bit operating system. In this experiment, the algorithms were trained using 12 Daphnia magna videos and tested using an additional four Daphnia magna videos. Subsequently, the detection and tracking methods were compared. The videos, each of which had a duration of 30 s, were captured at a rate of 15 frames per second. Generally, for long-time or real-time videos, the following factors must be considered in tracking Daphnia magna: automatic binarization between the object and background, effective classification of Daphnia magna or noise, and the speed of the algorithm. Therefore, to develop an efficient tracking algorithm, we propose the following tracking process (Fig. 3A). In this process, each frame is initially converted into an image and the background is identified from the obtained video (Fig. 3B). The background is the average of the frames over the previous 20 s, and the tracking system takes 20 s to capture the first background image. The background is subtracted from the image for object detection (Fig. 3C). The objects include Daphnia magna and noise such as droplets and sediment. The difference between the background and frame images is binarized, and each area of the binarized values is regarded as an object. Conventionally, the binarized values are manually generated using specific thresholds. In this study, the images are automatically binarized using k-means clustering to select the threshold value. After binarization, several machine learning methods are used to classify the objects as Daphnia magna or noise (Fig. 3D). For a faster tracking algorithm, we use simple machine learning methods such as random forest (RF) and support vector machine (SVM). The predicted Daphnia magna are tracked using SORT24, which is a fast and highly accurate tracking algorithm (Fig. 3E). Finally, based on the tracked results, statistics for assessing ecotoxicity, such as the number of mobile individuals, average distance, and radius of activity, are estimated to evaluate the toxicity of the aquatic environment.Figure 3Automatic Daphnia magna tracking algorithm process. (A) Overview of automatic tracking algorithm process. (B) Image extraction step. (C) Background subtraction step. (D) Daphnia magna detection step. (E) Daphnia magna tracking step.Full size imagek-means clustering for automatic background subtractionMany tracking algorithms assume that the background is fixed. With fixed backgrounds, the difference between the frame and background can be used to identify objects. However, automatically selecting the precise threshold value for image pixel binarization becomes one of the key problems in identifying objects. The proposed method applies k-means clustering to the pixel values of the subtracted image30, and the center value of each calculated cluster mean is selected as the threshold value (Fig. 4). In the k-means clustering method, grouping is repeatedly performed using the distance between data points31. For binarization, two groups are formed. Let (mu _1 (t)) be the mean of pixels less than the threshold and (mu _2(t)) be the mean of pixels greater than the threshold. At first, (mu _1(t), mu _2(t)) are randomly initialized. Subsequently, each pixel is grouped into a closer mean of each group. The above steps are repeated several times until the group experiences a few changes. Finally, the threshold is calculated as an average of the two means.Figure 4Example of automatic threshold value setting for binarization between objects and background using k-means clusteringFull size imageClassification methodsObject detection based solely on the subtraction between the background and frame images may have low accuracy. As the background in the proposed process is the average value of the frame images, noise may occur. Although this noise is removed by threshold selection in binarization, using only the threshold selection is not efficient for long or real-time videos. Therefore, additional noise must be classified and removed using machine learning models, requiring the construction of a database. In the database, the obtained objects are manually labeled as noise or Daphnia magna and are called ground truth. For classification, the resized 8 (times ) 8 image of each object is stored in the database. The resized image is transformed into a feature using the Sobel edge detection algorithm32 and entered as inputs to the classification models. In this study, classification models such as RF33 SVM34 were used.RF is a model that integrates several decision tree models35. All training data are sampled with a replacement for training each decision tree model. The decision tree model is trained to split intervals of each independent variable by minimizing the gini index (Eq. 1) or entropy index (Eq. 2). The gini index and entropy index denote the impurity within the intervals.$$begin{aligned} G= & {} 1- sum _{i=1}^{c} p_i ^2 end{aligned}$$
    (1)
    $$begin{aligned} E= & {} – sum _{i=1}^{c} p_i log_2 p_i end{aligned}$$
    (2)
    where (p_i) is a probability within i-th interval, and c is the number of intervals. For better performance, the RF selects independent variables of training data randomly. This step serves to reduce the correlation of each model. If predictions of each decision tree are uncorrelated, then the variance of an integrated prediction of models is smaller than the variance of each model. RF integrates several model predictions using the voting method. An advantage of the RF method is that it avoids overfitting because the model uses the average of many predictions.SVM is a model designed to search for a hyperplane to maximize the distance, or margin, between support vectors. The hyperplane refers to the plane that divides two different groups, and the support vector represents the closest vector to the hyperplane. Let (D=({textbf{x}}_i, y_i), i=1, ldots , n, {textbf{x}}_i in {mathbb {R}}^p, y_n in { -1,1 }) be training data. Suppose that the training data are completely separated linearly by a hyperplane; then, the hyperplane is expressed as Eq. 3.$$begin{aligned} {textbf{w}}^T {textbf{x}} + b = 0, end{aligned}$$
    (3)
    where ({textbf{w}}) is a weight vector of the hyperplane, and b is a bias. The weight vector is updated by minimizing Eq. 4.$$begin{aligned} L = {1 over 2} {textbf{w}}^T {textbf{w}} text { subject to } y_i ({textbf{w}}^T {textbf{x}} + b) ge 1 end{aligned}$$
    (4)
    We can transform Eqs. 4 to  5 by using the Lagrange multiplier method.$$begin{aligned} L^* = {1 over 2} {textbf{w}}^T {textbf{w}} – sum _{i=1}^n a_i { y_i ({textbf{w}}^T x_i + {-}) – 1 }, end{aligned}$$
    (5)
    where (a_i) is the Lagrange multiplier. We can efficiently solve Eq. 5 using a dual form. Furthermore, Eq. 5 can be solved in a case where it is not completely separated using a slack variable and a kernel trick can be used to estimate the nonlinear hyperplane.SORT trackerSORT, one of the frameworks for solving the multiple object tracking (MOT) problem, aims to achieve efficient real-time tracking24. The SORT method framework is created by combining the estimation step and the association step. The estimation step forecasts the next position of each predicted Daphnia magna. The association step matches the forecasting position and next true position of each predicted Daphnia magna. In the estimation step, the SORT framework uses the Kalman filter to forecast the position of the predicted Daphnia magna in the next frame. The position of each predicted Daphnia magna is expressed as Eq. 6.$$begin{aligned} {textbf{x}} = [u,v,s,r,{dot{u}}, {dot{v}}, {dot{s}}]^T end{aligned}$$
    (6)
    where u and v are the center positions of each predicted Daphnia magna, s is the scale size of the bounding box, and r is the aspect ratio of the bounding box. ({dot{u}}), ({dot{v}}), and ({dot{s}}) are the amounts of change in each variable. In the association step, to associate the forecasting position and true position, the framework adopts the intersection-over-union (IOU)36 as the association metric. The Hungarian algorithm is loaded into the SORT framework to perform fast and efficient Daphnia magna association prediction. In this study, a mixed metric of IOU36 and Euclidean distance37 was used instead of only the IOU that is used in SORT (Eq. 7) for more efficient association.$$begin{aligned} C_{ij} = (1-lambda ) {max_d – d_{ij} over max_d} + lambda cdot IOU_{ij} end{aligned}$$
    (7)
    where (d_{ij}) is the Euclidean distance between the i-th predicted Daphnia magna in the before frame and the j-th predicted Daphnia magna in the next frame, and (lambda ) is the weight of (IOU_{ij}). (IOU_{ij}) is the IOU between the i-th predicted Daphnia magna in the before-frame and the j-th predicted Daphnia magna in the next frame.MetricsThe binary confusion matrix consists of true positive (TP), true negative (TN), false positive (FP), and false negative (FN)38. TP is the number of cases where the predicted Daphnia magna matches the actual Daphnia magna, TN is the number of cases where the objects predicted as noise are actual noise, FP is the number of cases where the predicted Daphnia magna differs from the actual Daphnia magna, and FN is the number of cases where the objects predicted as noise are not actual noise. In this study, accuracy, recall, precision, and F1 scores (Eq. 8) were used as the metrics for comparing the machine learning methods.$$begin{aligned} begin{aligned} Accuracy&= {TP + FP over TP + TN + FP + FN} \ Recall&= {TP over TP + TN} \ Precision&= {TP over TP + FP} \ F1 score&= 2 times {Precision times Recall over Precision + Recall} end{aligned} end{aligned}$$
    (8)
    Standard MOT metrics to evaluate tracking performance include multi-object tracking accuracy (MOTA) and multi-object tracking precision (MOTP). An important task of MOT is to identify and track the same object across two frames. Identification (ID) precision (IDP), ID recall (IDR), ID F1 measure (IDF1), and ID switches (IDs) may be used as measures for evaluating the identification and tracking of the same objects39,40.Data analysisThe toxicity test using Daphnia magna was performed following the Korean official Acute Toxicity Test Method29. The test medium was prepared by dissolving KCl (8 mg/L), (text {MgSO}_4) (120 mg/L), (text {CaSO}_4 cdot 2 text {H}_2 text {O} ) (120 mg/L), and (text {NaHCO}_3) (192 mg/L) in deionized water. Considering that Daphnia magna are neonates for less than 24 h after birth29, five neonates were exposed to 50 mL of different concentrations of heavy metals such as Potassium dichromate, Copper(II) sulfate pentahydrate, and Lead(II) sulfate (6.25, 12.5, 25, 50, and 100%) and 50 mL of culture media. Potassium dichromate is a common inorganic reagent used as an oxidizing agent in chemical industries. Copper(II) sulfate pentahydrate is a trace material widely used in industrial processes and agriculture. A significant amount of copper is emitted in semiconductor manufacturing processes, which adversely impacts the aquatic ecosystem. When present as an ion in water, copper can be acutely toxic to aquatic organisms such as Daphnia magna. Lead(II) sulfate is another nonessential and nonbiodegradable heavy metal. It is highly toxic to numerous organisms even at low concentrations and can accumulate in aquatic ecosystems41. Twenty Daphnia magna (four replicates of five each) were exposed to each test solution for 24 h. The term “immobility” means that the Daphnia magna remains stationary after exposure to chemicals such as Potassium dichromate, Copper(II) sulfate pentahydrate, and Lead(II) sulfate. In this study, immobility was used as an endpoint identifier, and the number of mobile Daphnia magna were counted to evaluate the EC50 values for the samples using the ToxCalc 5.0 program (Tidepoll Software, USA).The locomotory responses of Daphnia magna were tested after 0, 12, 18, and 24 h of exposure at different concentrations. Potassium dichromate ((text {K}_2text {Cr}_2text {O}_7)) at 2 mg/L was connected to the Daphnia magna tracking system, and standard toxic substances were automatically diluted to 100%, 50%, 25%, 12.5%, and 6.25%. The automatic high-throughput Daphnia magna tracking system automatically measured the tracking results of a 1-minute-long video at hourly intervals. The average moving distance for 20 s of each Daphnia magna in each chamber was analyzed using a repeated measures ANOVA (RMANOVA). RMANOVA was used for the analysis of data obtained by repeatedly measuring the same Daphnia magna42. It analyzes the concentration effect excluding the time effect at each hour. The time effect means the change in average distance per 20 s. RMANOVA was implemented using the agricolae package of the R 4.0.4 program43. To remove the noise affecting RMANOVA, the Daphnia magna that remained stationary for 20 s or more were removed from the observations. In this study, we used the significance level at 5%. More

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    Drosophilids with darker cuticle have higher body temperature under light

    Massey, J. H. & Wittkopp, P. J. The genetic basis of pigmentation differences within and between Drosophila species. Curr. Top. Dev. Biol. 119, 27–61 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yassin, A. et al. The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila. Curr. Biol. 26, 2412–2422 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, T. M. et al. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134, 610–623 (2008).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bastide, H. et al. A genome-wide, fine-scale map of natural pigmentation variation in Drosophila melanogaster. PLoS Genet. 9, e1003534 (2013).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pool, J. E. & Aquadro, C. F. The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol. Ecol. 16, 2844–2851 (2007).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wittkopp, P. J. et al. Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326, 540–544 (2009).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Jeong, S. et al. The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132, 783–793 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Rajpurohit, S. et al. Pigmentation and fitness trade-offs through the lens of artificial selection. Biol. Lett. 12, (2016).Massey, J. H. et al. Pleiotropic effects of ebony and tan on pigmentation and cuticular hydrocarbon composition in Drosophila melanogaster. Front. Physiol. 10, 518 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parkash, R., Rajpurohit, S. & Ramniwas, S. Impact of darker, intermediate and lighter phenotypes of body melanization on desiccation resistance in Drosophila melanogaster. J. Insect Sci. 9, 1–10 (2009).Article 
    PubMed 

    Google Scholar 
    Dombeck, I. & Jaenike, J. Ecological genetics of abdominal pigmentation in Drosophila falleni: A pleiotropic link to nematode parasitism. Evolution 58, 587–596 (2004).PubMed 

    Google Scholar 
    Kutch, I. C., Sevgili, H., Wittman, T. & Fedorka, K. M. Thermoregulatory strategy may shape immune investment in Drosophila melanogaster. J. Exp. Biol. 217, 3664–3669 (2014).PubMed 

    Google Scholar 
    Wittkopp, P. J. & Beldade, P. Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy. Semin. Cell Dev. Biol. 20, 65–71 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bastide, H., Yassin, A., Johanning, E. J. & Pool, J. E. Pigmentation in Drosophila melanogaster reaches its maximum in Ethiopia and correlates most strongly with ultra-violet radiation in sub-Saharan Africa. BMC Evol. Biol. 14, 179 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Arnold, S. J. Morphology, performance and fitness. Am. Zool. 23, 347–361 (1983).Article 

    Google Scholar 
    Gibert, P., Moreteau, B. & David, J. R. Developmental constraints on an adaptive plasticity: Reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol. Dev. 2, 249–260 (2000).Article 
    CAS 
    PubMed 

    Google Scholar 
    Parkash, R., Rajpurohit, S. & Ramniwas, S. Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster. J. Insect Physiol. 54, 1050–1056 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Telonis-Scott, M., Hoffmann, A. A. & Sgro, C. M. The molecular genetics of clinal variation: A case study of ebony and thoracic trident pigmentation in Drosophila melanogaster from eastern Australia. Mol. Ecol. 20, 2100–2110 (2011).Article 
    PubMed 

    Google Scholar 
    Munjal, A. K. et al. Thoracic trident pigmentation in Drosophila melanogaster: latitudinal and altitudinal clines in Indian populations. Genet. Sel. Evol. 29, 601–610 (1997).Article 
    PubMed Central 

    Google Scholar 
    David, J. R., Capy, P., Payant, V. & Tsakas, S. Thoracic trident pigmentation in Drosophila melanogaster: Differentiation of geographical populations. Genet. Sel. Evol. 17, 211–224 (1985).Article 
    CAS 

    Google Scholar 
    Clusella Trullas, S., van Wyk, J. H. & Spotila, J. R. Thermal melanism in ectotherms. J. Therm. Biol. 32, 235–245 (2007).Cordero, R. J. B. et al. Impact of yeast pigmentation on heat capture and latitudinal distribution. Curr. Biol. 28, 2657-2664.e3 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sibilia, C. D. et al. Thermal Physiology and Developmental Plasticity of Pigmentation in the Harlequin Bug (Hemiptera: Pentatomidae). J. Insect Sci. 18, (2018).Jong, P., Gussekloo, S. & Brakefield, P. Differences in thermal balance, body temperature and activity between non-melanic and melanic two-spot ladybird beetles (Adalia bipunctata) under controlled conditions. J. Exp. Biol. 199, 2655–2666 (1996).Article 
    CAS 
    PubMed 

    Google Scholar 
    Zverev, V., Kozlov, M. V., Forsman, A. & Zvereva, E. L. Ambient temperatures differently influence colour morphs of the leaf beetle Chrysomela lapponica: Roles of thermal melanism and developmental plasticity. J. Therm. Biol 74, 100–109 (2018).Article 
    PubMed 

    Google Scholar 
    Watt, W. B. Adaptive significance of pigment polymorphisms in Colias butterflies, II. Thermoregulation and photoperiodically controlled melanin variation in Colias eurytheme. Proc. Natl. Acad. Sci. USA 63, 767–74 (1969).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kuyucu, A. C., Sahin, M. K. & Caglar, S. S. The relation between melanism and thermal biology in a colour polymorphic bush cricket, Isophya rizeensis. J. Therm. Biol. 71, 212–220 (2018).Article 
    PubMed 

    Google Scholar 
    Köhler, G. & Schielzeth, H. Green-brown polymorphism in alpine grasshoppers affects body temperature. Ecol. Evol. 10, 441–450 (2020).Article 
    PubMed 

    Google Scholar 
    Willmer, P. G. & Unwin, D. M. Field analyses of insect heat budgets: Reflectance, size and heating rates. Oecologia 50, 250–255 (1981).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pecsenye, K., Bokor, K., Lefkovitch, L. P., Giles, B. E. & Saura, A. Enzymatic responses of Drosophila melanogaster to long- and short-term exposures to ethanol. Mol. Gen. Genet. 255, 258–268 (1997).Article 
    CAS 
    PubMed 

    Google Scholar 
    De Castro, S., Peronnet, F., Gilles, J.-F., Mouchel-Vielh, E. & Gibert, J.-M. bric à brac (bab), a central player in the gene regulatory network that mediates thermal plasticity of pigmentation in Drosophila melanogaster. PLoS Genet. 14, e1007573 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cooley, A. M., Shefner, L., McLaughlin, W. N., Stewart, E. E. & Wittkopp, P. J. The ontogeny of color: Developmental origins of divergent pigmentation in Drosophila americana and D. novamexicana. Evol. Dev. 14, 317–25 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    John, A. V., Sramkoski, L. L., Walker, E. A., Cooley, A. M. & Wittkopp, P. J. Sensitivity of allelic divergence to genomic position: Lessons from the Drosophila tan Gene. G3 (Bethesda) (2016) doi:https://doi.org/10.1534/g3.116.032029.Liu, Y. et al. Changes throughout a genetic network mask the contribution of hox gene evolution. Curr. Biol. 29, 2157-2166.e6 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    David, J. R. et al. Evolution of assortative mating following selective introgression of pigmentation genes between two Drosophila species. Ecol. Evol. 12, e8821 (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wittkopp, P. J., True, J. R. & Carroll, S. B. Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129, 1849–1858 (2002).Article 
    CAS 
    PubMed 

    Google Scholar 
    Davis, J. S. & Moyle, L. C. Desiccation resistance and pigmentation variation reflects bioclimatic differences in the Drosophila americana species complex. BMC Evol. Biol. 19, 204 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nagy, O. et al. Correlated evolution of two copulatory organs via a single cis-regulatory nucleotide change. Curr. Biol. 28, 3450-3457.e13 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lachaise, D. et al. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé. Proc. Biol. Sci. 267, 1487–1495 (2000).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haldane, J. B. S. Sex ratio and unisexual sterility in hybrid animals. J. Gen. 12, 101–109 (1922).Article 

    Google Scholar 
    Turissini, D. A. & Matute, D. R. Fine scale mapping of genomic introgressions within the Drosophila yakuba clade. PLoS Genet. 13, e1006971 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hoffmann, A. A. Physiological climatic limits in Drosophila: Patterns and implications. J. Exp. Biol. 213, 870–880 (2010).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sunaga, S., Akiyama, N., Miyagi, R. & Takahashi, A. Factors underlying natural variation in body pigmentation of Drosophila melanogaster. Genes Genet. Syst. 91, 127–137 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Rajpurohit, S. & Schmidt, P. S. Latitudinal pigmentation variation contradicts ultraviolet radiation exposure: A case study in Tropical Indian Drosophila melanogaster. Front. Physiol. 10, 84 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bergland, A. O., Behrman, E. L., O’Brien, K. R., Schmidt, P. S. & Petrov, D. A. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 10, e1004775 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rudman, S. M. et al. Direct observation of adaptive tracking on ecological time scales in Drosophila. Science 375, eabj7484 (2022).Fabian, D. K. et al. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol. Ecol. 21, 4748–4769 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zeuss, D., Brandl, R., Brändle, M., Rahbek, C. & Brunzel, S. Global warming favours light-coloured insects in Europe. Nat. Commun. 5, 3874 (2014).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Brakefield, P. M. & de Jong, P. W. A steep cline in ladybird melanism has decayed over 25 years: A genetic response to climate change?. Heredity (Edinb) 107, 574–578 (2011).Article 
    CAS 
    PubMed 

    Google Scholar 
    Zvereva, E. L., Hunter, M. D., Zverev, V., Kruglova, O. Y. & Kozlov, M. V. Climate warming leads to decline in frequencies of melanic individuals in subarctic leaf beetle populations. Sci. Total Environ. 673, 237–244 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Balanyá, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. Global genetic change tracks global climate warming in Drosophila subobscura. Science 313, 1773–1775 (2006).Article 
    ADS 
    PubMed 

    Google Scholar  More

  • in

    Spatial ecology of the invasive Asian common toad in Madagascar and its implications for invasion dynamics

    Hui, C. & Richardson, D. M. Invasion Dynamics (Oxford University Press, 2017).Book 
    MATH 

    Google Scholar 
    Clobert, J., Baguette, M., Benton, T. G. & Bullock, J. M. Dispersal Ecology and Evolution (Oxford University Press, 2012).Book 

    Google Scholar 
    Shigesada, N., Kawasaki, K. & Takeda, Y. Modeling stratified diffusion in biological invasions. Am. Nat. 146, 229–251 (1995).Article 

    Google Scholar 
    Chuang, A. & Peterson, C. R. Expanding population edges: Theories, traits, and trade-offs. Glob. Change Biol. 22, 494–512 (2016).Article 
    ADS 

    Google Scholar 
    Cayuela, H. et al. Determinants and consequences of dispersal in vertebrates with complex life cycles: A review of pond-breeding amphibians. Q. Rev. Biol. 95, 36 (2020).Article 

    Google Scholar 
    Measey, G. J. et al. A global assessment of alien amphibian impacts in a formal framework. Divers. Distrib. 22, 970–981 (2016).Article 

    Google Scholar 
    Antonelli, A., Smith, R. J., Perrigo, A. L. & Crottini, A. Madagascar’s extraordinary biodiversity: Evolution, distribution, and use. Science 378, eabf0869 (2022).
    Article 
    CAS 
    PubMed 

    Google Scholar 
    Marshall, B. M. et al. Widespread vulnerability of Malagasy predators to the toxins of an introduced toad. Curr. Biol. 28, R654–R655 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    Licata, F. et al. Toad invasion of Malagasy forests triggers severe mortality of a predatory snake. Biol. Inv. 24, 1189–1198 (2022).Article 

    Google Scholar 
    Licata, F. et al. Abundance, distribution and spread of the invasive Asian toad Duttaphrynus melanostictus in eastern Madagascar. Biol. Inv. 21, 1615–1626 (2019).Article 

    Google Scholar 
    McClelland, P., Reardon, J. T., Kraus, F., Raxworthy, C. J. & Randrianantoandro, C. Asian toad eradication feasibility report for Madagascar (Te Anau, 2015).Smith, M. A. & Green, D. M. Dispersal and the metapopulation paradigm in amphibian ecology and conservation: Are all amphibian populations metapopulations?. Ecography 28, 110–128 (2005).Article 

    Google Scholar 
    Shine, R. et al. Increased rates of dispersal of free-ranging cane toads (Rhinella marina) during their global invasion. Sci. Rep. 11, 23574 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Myles-Gonzalez, E., Burness, G., Yavno, S., Rooke, A. & Fox, M. G. To boldly go where no goby has gone before: Boldness, dispersal tendency, and metabolism at the invasion front. Behav. Ecol. 26, 1083–1090 (2015).Article 

    Google Scholar 
    Van Petegem, K. H. P. et al. Empirically simulated spatial sorting points at fast epigenetic changes in dispersal behaviour. Evol. Ecol. 29, 299–310 (2015).Article 

    Google Scholar 
    Stuart, Y. E. et al. Rapid evolution of a native species following invasion by a congener. Science 346, 463–466 (2014).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Licata, F., Andreone, F., Crottini, A., Harison, R. F. & Ficetola, G. F. Does spatial sorting occur in the invasive Asian toad in Madagascar? Insights into the invasion unveiled by morphological analyses. JZSER 2021, 1–9 (2021).
    Google Scholar 
    Schwarzkopf, L. & Alford, R. A. Nomadic movement in tropical toads. Oikos 96, 492–506 (2002).Article 

    Google Scholar 
    Brown, G. P., Kelehear, C. & Shine, R. Effects of seasonal aridity on the ecology and behaviour of invasive cane toads in the Australian wet–dry tropics. Funct. Ecol. 25, 1339–1347 (2011).Article 

    Google Scholar 
    Duellman, W. E. & Trueb, L. Biology of Amphibians (JHU Press, 1994).Book 

    Google Scholar 
    Wells, K. D. The Ecology and Behavior of Amphibians (University of Chicago Press, 2010). https://doi.org/10.7208/9780226893334.Book 

    Google Scholar 
    Shaw, A. K., Kokko, H. & Neubert, M. G. Sex difference and Allee effects shape the dynamics of sex-structured invasions. J. Anim. Ecol. 87, 36–46 (2018).Article 
    PubMed 

    Google Scholar 
    Schwarzkopf, L. & Alford, R. A. Desiccation and shelter-site use in a tropical amphibian: Comparing toads with physical models. Funct. Ecol. 10, 193–200 (1996).Article 

    Google Scholar 
    Wogan, G. O. U., Stuart, B. L., Iskandar, D. T. & McGuire, J. A. Deep genetic structure and ecological divergence in a widespread human commensal toad. Biol. Lett. 12, 20150807 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Licata, F. Exploring the invasion dynamics and impacts of the invasive Asian common toad in Madagascar (University of Porto, 2022).
    Google Scholar 
    Reilly, S. B. et al. Toxic toad invasion of Wallacea: A biodiversity hotspot characterized by extraordinary endemism. Glob. Change Biol. 23, 5029–5031 (2017).Article 
    ADS 

    Google Scholar 
    Jørgensen, C. B., Shakuntala, K. & Vijayakumar, S. Body size, reproduction and growth in a tropical toad, Bufo melanostictus, with a comparison of ovarian cycles in tropical and temperate zone anurans. Oikos 46, 379 (1986).Article 

    Google Scholar 
    Vences, M. et al. Tracing a toad invasion: Lack of mitochondrial DNA variation, haplotype origins, and potential distribution of introduced Duttaphrynus melanostictus in Madagascar. Amphib. Reptilia 38, 197–207 (2017).Article 

    Google Scholar 
    Ngo, B. V. & Ngo, C. D. Reproductive activity and advertisement calls of the Asian common toad Duttaphrynus melanostictus (Amphibia, Anura, Bufonidae) from Bach Ma National Park, Vietnam. Zool. Stud. 52, 12 (2013).Article 

    Google Scholar 
    Licata, F. et al. The Asian toad (Duttaphrynus melanostictus) in Madagascar: A report of an ongoing invasion. In Problematic Wildlife II: New Conservation and Management Challenges in the Human-Wildlife Interactions (eds Angelici, F. M. & Rossi, L.) 617–638 (Springer, 2020). https://doi.org/10.1007/978-3-030-42335-3_21.Chapter 

    Google Scholar 
    Moore, M., Solofo Niaina Fidy, J. F. & Edmonds, D. The new toad in town: Distribution of the Asian toad, Duttaphrynus melanostictus, in the Toamasina area of eastern Madagascar. Trop. Conserv. Sci. 8, 440–455 (2015).Article 

    Google Scholar 
    Licata, F. et al. Using public surveys to rapidly profile biological invasions in hard-to-monitor areas. Anim. Conserv. https://doi.org/10.1111/acv.12835 (2023).Article 

    Google Scholar 
    Zhang, M. et al. Automatic high-resolution land cover production in madagascar using sentinel-2 time series, tile-based image classification and google earth engine. Remote Sensing 12, 3663 (2020).Article 
    ADS 

    Google Scholar 
    Peel, M. C., Finlayson, B. L. & Mcmahon, T. A. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 4, 439–473 (2007).
    Google Scholar 
    Merkel, A. Toamasina Climate (Madagascar). Accessed 20 July 2022. https://en.climate-data.org/africa/madagascar/toamasina/toamasina-4029/
    (2021).Gordon, A. Secondary sexual characters of Bufo melanostictus schneider. Copeia 1933, 204–207 (1933).Article 

    Google Scholar 
    Alford, R. & Rowley, J. Techniques for tracking amphibians: The effects of tag attachment, and harmonic direction finding versus radio telemetry. Amphib. Reptilia 28, 367–376 (2007).Article 

    Google Scholar 
    Lassueur, T., Joost, S. & Randin, C. F. Very high resolution digital elevation models: Do they improve models of plant species distribution?. Ecol. Modell. 198, 139–153 (2006).Article 

    Google Scholar 
    Abrams, M., Crippen, R. & Fujisada, H. ASTER global digital elevation model (GDEM) and ASTER global water body dataset (ASTWBD). Remote Sensing 12, 1156 (2020).Article 
    ADS 

    Google Scholar 
    Brown, G. P., Phillips, B. L., Webb, J. K. & Shine, R. Toad on the road: Use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biol. Conserv. 133, 88–94 (2006).Article 

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

    Google Scholar 
    Hijmans, R. J. et al. raster: Geographic data analysis and modeling. https://CRAN.R-project.org/package=raster (2021).Yagi, K. T. & Green, D. M. Performance and movement in relation to postmetamorphic body size in a pond-breeding amphibian. J. Herpetol. 51, 482–489 (2017).Article 

    Google Scholar 
    Labocha, M. K., Schutz, H. & Hayes, J. P. Which body condition index is best?. Oikos 123, 111–119 (2014).Article 

    Google Scholar 
    Tingley, R. & Shine, R. Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the australian semi-desert. PLoS ONE 6, e25979 (2011).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Richards, S. J., Sinsch, U. & Alford, R. A. Radio Tracking. In Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians (eds Heyer, R. et al.) 155–158 (Smithsonian Institution, 1994).
    Google Scholar 
    Altobelli, J. T., Dickinson, K. J. M., Godfrey, S. S. & Bishop, P. J. Methods in amphibian biotelemetry: Two decades in review. Austral. Ecol. 47, 1382–1395 (2022).Article 

    Google Scholar 
    Dormann, C. F. et al. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).Article 

    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002). https://doi.org/10.1007/978-1-4757-2917-7_3.Book 
    MATH 

    Google Scholar 
    Richards, S. A., Whittingham, M. J. & Stephens, P. A. Model selection and model averaging in behavioural ecology: The utility of the IT-AIC framework. Behav. Ecol. Sociobiol. 65, 77–89 (2011).Article 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. (2021).Bates, D. et al. lme4: Linear Mixed-Effects Models using ‘Eigen’ and S4. (2020).Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar 
    Barton, K. MuMIn: Multi-Model Inference. (2022).Hodges, C. W., Marshall, B. M., Hill, J. G. & Strine, C. T. Malayan kraits (Bungarus candidus) show affinity to anthropogenic structures in a human dominated landscape. bioRxiv https://doi.org/10.1101/2021.09.08.459477 (2021).Article 

    Google Scholar 
    Muller, B. J., Cade, B. S. & Schwarzkopf, L. Effects of environmental variables on invasive amphibian activity: Using model selection on quantiles for counts. Ecosphere 9, e02067 (2018).Article 

    Google Scholar 
    Linsenmair, K. E. & Spieler, M. Migration patterns and diurnal use of shelter in a ranid frog of a West African savannah: A telemetric study. Amphib. Reptilia 19, 43–64 (1998).Article 

    Google Scholar 
    Clobert, J., Le Galliard, J.-F., Cote, J., Meylan, S. & Massot, M. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol. Lett. 12, 197–209 (2009).Article 
    PubMed 

    Google Scholar 
    Ward-Fear, G., Greenlees, M. J. & Shine, R. Toads on lava: spatial ecology and habitat use of invasive cane yoads (Rhinella marina) in Hawai’i. PLoS ONE 11, e0151700 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huang, W.-S., Lin, J.-Y. & Yu, J.Y.-L. Male reproductive cycle of the toad Bufo melanostictus in Taiwan. Zool. Sci. 14, 497–503 (1997).Article 

    Google Scholar 
    Brown, G. P., Phillips, B. L. & Shine, R. The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front. Proc. R. Soc. B 281, 20141385 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Perkins, T. A., Phillips, B. L., Baskett, M. L. & Hastings, A. Evolution of dispersal and life history interact to drive accelerating spread of an invasive species. Ecol. Lett. 16, 1079–1087 (2013).Article 
    PubMed 

    Google Scholar 
    Ochocki, B. M. & Miller, T. E. X. Rapid evolution of dispersal ability makes biological invasions faster and more variable. Nat. Commun. 8, 14315 (2017).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Phillips, B. L., Brown, G. P., Travis, J. M. J. & Shine, R. Reid’s paradox revisited: The evolution of dispersal kernels during range expansion. Am. Nat. 172, S34–S48 (2008).Article 
    PubMed 

    Google Scholar 
    Kot, M., Lewis, M. A. & van den Driessche, P. Dispersal data and the spread of invading organisms. Ecology 77, 2027–2042 (1996).Article 

    Google Scholar 
    Deguise, I. & Richardson, J. S. Movement behaviour of adult western toads in a fragmented, forest landscape. Can. J. Zool. 87, 1184–1194 (2009).Article 

    Google Scholar 
    Mitrovich, M. J., Gallegos, E. A., Lyren, L. M., Lovich, R. E. & Fisher, R. N. Habitat use and movement of the endangered Arroyo toad (Anaxyrus californicus) in coastal southern California. J. Herpetol. 45, 319–328 (2011).Article 

    Google Scholar 
    Urban, M. C., Phillips, B. L., Skelly, D. K. & Shine, R. A toad more traveled: The heterogeneous invasion dynamics of cane toads in Australia. Am. Nat. 171, E134–E148 (2008).Article 
    PubMed 

    Google Scholar 
    Enriquez-Urzelai, U., Montori, A., Llorente, G. A. & Kaliontzopoulou, A. Locomotor mode and the evolution of the hindlimb in western mediterranean anurans. Evol. Biol. 42, 199–209 (2015).Article 

    Google Scholar 
    Junior, B. T. & Gomes, F. R. Relation between water balance and climatic variables associated with the geographical distribution of anurans. PLoS ONE 10, e0140761 (2015).Article 

    Google Scholar 
    Klockmann, M., Günter, F. & Fischer, K. Heat resistance throughout ontogeny: Body size constrains thermal tolerance. Glob. Change Biol. 23, 686–696 (2017).Article 
    ADS 

    Google Scholar 
    Petrovskii, S., Mashanova, A. & Jansen, V. A. A. Variation in individual walking behavior creates the impression of a Lévy flight. PNAS 108, 8704–8707 (2011).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lindström, T., Brown, G. P., Sisson, S. A., Phillips, B. L. & Shine, R. Rapid shifts in dispersal behavior on an expanding range edge. PNAS 110, 13452–13456 (2013).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tingley, R. et al. New weapons in the toad toolkit: A review of methods to control and mitigate the biodiversity impacts of invasive Cane toads (Rhinella marina). Q. Rev. Biol. 92, 123–149 (2017).Article 
    PubMed 

    Google Scholar 
    Novoa, A. et al. Invasion syndromes: A systematic approach for predicting biological invasions and facilitating effective management. Biol. Invasions 22, 1801–1820 (2020).Article 

    Google Scholar 
    DeVore, J. L., Crossland, M. R., Shine, R. & Ducatez, S. The evolution of targeted cannibalism and cannibal-induced defenses in invasive populations of cane toads. Proc. Natl. Acad. Sci. 118, e2100765118 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Muller, B. J. & Schwarzkopf, L. Relative effectiveness of trapping and hand-capture for controlling invasive cane toads (Rhinella marina). Int. J. Pest Manag. 64, 185–192 (2018).Article 
    CAS 

    Google Scholar  More