Ecology

1.Born, W., Rauschmayer, F. & Bräuer, I. Economic evaluation of biological invasions—a survey. Ecol. Econ. 55, 321–336 (2005).Article 

Google Scholar 
2.Jackson, T. Addressing the economic costs of invasive alien species: some methodological and empirical issues. Int. J. Sustain. Soc. 7, 221–240 (2015).Article 

Google Scholar 
3.Diagne, C. et al. InvaCost, a public database of the economic costs of biological invasions worldwide. Sci. Data 7, 277 (2020).CAS 
Article 

Google Scholar 
4.Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623 (2016).Article 

Google Scholar 
5.Kumschick, S. et al. Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience 65, 55–63 (2015).Article 

Google Scholar 
6.Ogden, N. H. et al. Emerging infectious diseases and biological invasions: a call for a One Health collaboration in science and management. R. Soc. Open Sci. 6, 181577 (2019).Article 

Google Scholar 
7.Jones, B. A. Invasive species impacts on human well-being using the life satisfaction index. Ecol. Econ. 134, 250–257 (2017).Article 

Google Scholar 
8.Bradshaw, C. J. A. et al. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 7, 12986 (2016).CAS 
Article 

Google Scholar 
9.Seebens, H. et al. Projecting the continental accumulation of alien species through to 2050. Glob. Change Biol. 27, 970–982 (2020).Article 

Google Scholar 
10.Essl, F. et al. Drivers of future alien species impacts: an expert-based assessment. Glob. Change Biol. 26, 4880–4893 (2020).Article 

Google Scholar 
11.Courchamp, F. et al. Invasion biology: specific problems and possible solutions. Trends Ecol. Evol. 32, 13–22 (2017).Article 

Google Scholar 
12.Lenzner, B. et al. A framework for global twenty-first century scenarios and models of biological invasions. Bioscience 69, 697–710 (2019).Article 

Google Scholar 
13.Heger, T. et al. Conceptual frameworks and methods for advancing invasion ecology. Ambio 42, 527–540 (2013).Article 

Google Scholar 
14.Larson, D. L. et al. A framework for sustainable invasive species management: environmental, social, and economic objectives. J. Environ. Manage. 92, 14–22 (2011).Article 

Google Scholar 
15.Hoffmann, B. D. & Broadhurst, L. M. The economic cost of managing invasive species in Australia. NeoBiota 31, 1–18 (2016).Article 

Google Scholar 
16.Pimentel, D. et al. Economic and environmental threats of alien plant, animal, and microbe invasions. Agric. Ecosyst. Environ. 84, 1–20 (2001).Article 

Google Scholar 
17.Paini, D. R. et al. Global threat to agriculture from invasive species. Proc. Natl Acad. Sci. USA 113, 7575–7579 (2016).CAS 
Article 

Google Scholar 
18.Latombe, G. et al. A vision for global monitoring of biological invasions. Biol. Conserv. 213, 295–308 (2017).Article 

Google Scholar 
19.Diagne, C., Catford, J. A., Essl, F., Nuñez, M. A. & Courchamp, F. What are the economic costs of biological invasions? A complex topic requiring international and interdisciplinary expertise. NeoBiota 63, 25–37 (2020).Article 

Google Scholar 
20.Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).CAS 
Article 

Google Scholar 
21.Bishop, M. J. et al. Effects of ocean sprawl on ecological connectivity: impacts and solutions. J. Exp. Mar. Biol. Ecol. 492, 7–30 (2017).Article 

Google Scholar 
22.Bacher, S. et al. Socio‐Economic Impact Classification of Alien Taxa (SEICAT). Methods Ecol. Evol. 9, 159–168 (2018).23.Angulo, E. et al. Non-English languages enrich scientific knowledge: the example of economic costs of biological invasions. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2020.144441 (2021).24.Colautti, R. I. & MacIsaac, H. J. A neutral terminology to define ‘invasive’ species. Divers. Distrib. 10, 135–141 (2004).Article 

Google Scholar 
25.Dana, E. D., Jeschke, J. M. & García-de-Lomas, J. Decision tools for managing biological invasions: existing biases and future needs. Oryx 48, 56–63 (2014).Article 

Google Scholar 
26.Jeschke, J. M., Keesing, F. & Ostfeld, R. S. Novel organisms: comparing invasive species, GMOs, and emerging pathogens. Ambio 42, 541–548 (2013).Article 

Google Scholar 
27.Jones, B. A. Tree shade, temperature, and human health: evidence from invasive species-induced deforestation. Ecol. Econ. 156, 12–23 (2019).Article 

Google Scholar 
28.Jones, B. A. & McDermott, S. M. Health impacts of invasive species through an altered natural environment: assessing air pollution sinks as a causal pathway. Environ. Resour. Econ. 71, 23–43 (2018).Article 

Google Scholar 
29.Pyšek, P. et al. Geographical and taxonomic biases in invasion ecology. Trends Ecol. Evol. 23, 237–244 (2008).Article 

Google Scholar 
30.Clout, M. N. & Russell, J. C. The invasion ecology of mammals: a global perspective. Wildl. Res. 35, 180–184 (2008).Article 

Google Scholar 
31.Early, R. et al. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 7, 12485 (2016).CAS 
Article 

Google Scholar 
32.Jarić, I. et al. Crypticity in biological invasions. Trends Ecol. Evol. 34, 291–302 (2019).Article 

Google Scholar 
33.Pascual, U. et al. in The Economics of Ecosystems and Biodiversity: Ecological and Economic Foundations (ed. Kumar, P.) 183–256 (Earthscan, 2010).34.Spangenberg, J. H. & Settele, J. Precisely incorrect? Monetising the value of ecosystem services. Ecol. Complex. 7, 327–337 (2010).Article 

Google Scholar 
35.Kallis, G., Gómez-Baggethun, E. & Zografos, C. To value or not to value? That is not the question. Ecol. Econ. 94, 97–105 (2013).Article 

Google Scholar 
36.Meinard, Y., Dereniowska, M. & Gharbi, J.-S. The ethical stakes in monetary valuation methods for conservation purposes. Biol. Conserv. 199, 67–74 (2016).Article 

Google Scholar 
37.Faulkner, K. T., Robertson, M. P. & Wilson, J. R. U. Stronger regional biosecurity is essential to prevent hundreds of harmful biological invasions. Glob. Change Biol. 26, 2449–2462 (2020).Article 

Google Scholar 
38.Pagad, S., Genovesi, P., Carnevali, L., Schigel, D. & McGeoch, M. A. Introducing the Global Register of Introduced and Invasive Species. Sci. Data 5, 170202 (2018).Article 

Google Scholar 
39.Holden, M. H., Nyrop, J. P. & Ellner, S. P. The economic benefit of time‐varying surveillance effort for invasive species management. J. Appl. Ecol. 53, 712–721 (2016).Article 

Google Scholar 
40.Hulme, P. E. et al. Integrating invasive species policies across ornamental horticulture supply chains to prevent plant invasions. J. Appl. Ecol. 55, 92–98 (2018).Article 

Google Scholar 
41.Chaffin, B. C. et al. Biological invasions, ecological resilience and adaptive governance. J. Environ. Manage. 183, 399–407 (2016).Article 

Google Scholar 
42.Sardain, A., Sardain, E. & Leung, B. Global forecasts of shipping traffic and biological invasions to 2050. Nat. Sustain. 2, 274–282 (2019).Article 

Google Scholar 
43.Seebens, H. Invasion ecology: expanding trade and the dispersal of alien species. Curr. Biol. 29, R120–R122 (2019).CAS 
Article 

Google Scholar 
44.Leroy, B. et al. Analysing global economic costs of invasive alien species with the invacost R package. Preprint at https://doi.org/10.1101/2020.12.10.419432 (2020). More

M.J.A.C. was funded by NWO-Veni grant 181002. R.A. was funded by Rohini Nilekani Philanthropies. T.A. was supported by the project UMBRAL CTM2017-86695-C3-3- R. J.F.P. was funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 795315. More

1.Bullock, J. M., Kenward, R. E. & Hails, R. S. Dispersal Ecology (Blackwell, 2002).
Google Scholar 
2.Dieckmann, U., O’Hara, B. & Weisser, W. The evolutionary Ecology Of Dispersal. Trends Ecol. Evol. 14, 88–90 (1999).Article 

Google Scholar 
3.Allendorf, F. W. & Luikart, G. Conservation and the Genetics of Populations (Blackwell Publishing, 2009).
Google Scholar 
4.Vøllestad, L. A. et al. Small-scale dispersal and population structure in stream-living brown trout (Salmo trutta) inferred by mark–recapture, pedigree reconstruction, and population genetics. Can. J. Fish. Aquat. Sci. 69, 1513–1524 (2012).Article 

Google Scholar 
5.Edelsparre, A. H., Shahid, A. & Fitzpatrick, M. J. Habitat connectivity is determined by the scale of habitat loss and dispersal strategy. Ecol. Evol. 8, 5508–5514 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
6.Filipe, A. F. et al. Forecasting fish distribution along stream networks: Brown trout (Salmo trutta) in Europe. Divers. Distrib. 19, 1059–1071 (2013).Article 

Google Scholar 
7.Cote, J., Clobert, J., Brodin, T., Fogarty, S. & Sih, A. Personality-dependent dispersal: Characterization, ontogeny and consequences for spatially structured populations. Philos. Trans. R. Soc. B. 365, 4065–4076 (2010).CAS 
Article 

Google Scholar 
8.Cote, J. et al. Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes. Ecography 40, 56–73 (2017).Article 

Google Scholar 
9.Comte, L. & Olden, J. D. Fish dispersal in flowing waters: A synthesis of movement- and genetic-based studies. Fish Fish. 19, 1063–1077 (2018).Article 

Google Scholar 
10.Ducatez, S. et al. Inter-individual variation in movement: is there a mobility syndrome in the large white butterfly Pieris brassicae?. Ecol. Entomol. 37, 377–385 (2012).Article 

Google Scholar 
11.Clobert, E., 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).PubMed 
Article 

Google Scholar 
12.Stevens, V. M. et al. Dispersal syndromes and the use of life-histories to predict dispersal. Evol. Appl. 6, 630–642 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
13.Daufresne, M., Capra, H. & Gaudin, P. Downstream displacement of post emergent brown trout: Effects of development stage and water velocity. J. Fish Biol. 67, 599–614 (2005).Article 

Google Scholar 
14.Chapman, D. W. Aggressive behaviour in juvenile coho salmon as a cause of emigration. J. Fish. Res. Bd. Can. 19, 1047–1079 (1962).Article 

Google Scholar 
15.McCarthy, I. D. Competitive ability is related to metabolic asymmetry in juvenile rainbow trout. J. Fish Biol. 59, 1002–1014 (2001).Article 

Google Scholar 
16.Metcalfe, N. B., Taylor, A. C. & Thorpe, J. E. Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim. Behav. 49, 431–436 (1995).Article 

Google Scholar 
17.Lahti, K., Huuskonen, H., Laurila, A. & Piironen, J. Metabolic rate and aggressiveness between Brown Trout populations. Funct. Ecol. 16, 167–174 (2002).Article 

Google Scholar 
18.Fraser, D. J., Weir, L. K., Darwish, T. L., Eddington, J. D. & Hutchings, J. A. Divergent compensatory growth responses within species: Linked to contrasting migrations in salmon?. Oecologia 153, 543–553 (2007).PubMed 
Article 
ADS 

Google Scholar 
19.Swain, D. P. & Holtby, L. B. Differences in morphology and agonistic behaviour in coho salmon (Oncorhynchus kisutch) rearing in a lake or its tributary stream. Can. J. Fish. Aquat. Sci. 46, 1406–1414 (1989).Article 

Google Scholar 
20.Kaiser, A., Merckx, T. & Van Dyck, H. Personality traits influence contest outcome, and vice versa, in a territorial butterfly. Sci. Rep. 9, 2778 (2019).PubMed 
PubMed Central 
Article 
ADS 
CAS 

Google Scholar 
21.Studds, C. E., Kyser, T. K. & Marra, P. P. Natal dispersal driven by environmental conditions interacting across the annual cycle of a migratory songbird. Proc. Natl. Acad. Sci. 105, 2929–2933 (2008).CAS 
PubMed 
Article 
ADS 

Google Scholar 
22.Behr, D. M., McNutt, J. W., Ozgul, A. & Cozzi, G. When to stay and when to leave? Proximate causes of dispersal in an endangered social carnivore. J. Anim. Ecol. 89, 2356–2366. https://doi.org/10.1111/1365-2656.13300 (2020).Article 
PubMed 

Google Scholar 
23.Keenleyside, M. H. & Yamamoto, F. T. Territorial behaviour of juvenile Atlantic salmon (Salmo salar L.). Behaviour 19, 139–169 (1962).Article 

Google Scholar 
24.Duckworth, R. A. & Badyaev, A. V. Coupling of dispersal and aggression facilitates the the rapid range expansion of a passerine bird. Proc. Natl. Acad. Sci. USA. 104, 15017–15022 (2007).CAS 
PubMed 
Article 
ADS 

Google Scholar 
25.Peery, C. A. & Bjornn, T. C. Dispersal of hatchery-reared chinook salmon parr following release into four Idaho streams. N. Am. J. Fish. Manag. 20, 19–27 (2000).Article 

Google Scholar 
26.Nagata, M. & Irvine, J. R. Differential dispersal patterns of male and female masu salmon fry. J. Fish Biol. 51, 601–606 (1997).Article 

Google Scholar 
27.Li, X.-Y. & Kokko, H. Sex-biased dispersal: A review of the theory. Biol. Rev. 94, 721–736. https://doi.org/10.1111/brv.12475 (2019).Article 
PubMed 

Google Scholar 
28.Hutchings, J. A. & Gerber, L. Sex-biased dispersal in a salmonid fish. Proc. R. Soc. B. 269, 2487–2493. https://doi.org/10.1098/rspb.2002.2176 (2002).Article 
PubMed 

Google Scholar 
29.Bekkevold, D., Hansen, M. M. & Mensberg, K.-L.D. Genetic detection of sex-specific dispersal in historical and contemporary populations of anadromous brown trout Salmo trutta. Mol. Ecol. 13, 1707–1712. https://doi.org/10.1111/j.1365-294X.2004.02156.x (2004).CAS 
Article 
PubMed 

Google Scholar 
30.Biro, P. A. & Stamps, J. A. Do consistent individual differences in metabolic rate promote consistent individual differences in behavior?. Trends Ecol. Evol. 25, 653–659 (2010).PubMed 
Article 

Google Scholar 
31.Le Galliard, J. F., Paquet, M., Cisel, M. & Montes-Poloni, L. Personality and the pace-of-life syndrome: Variation and selection on exploration, metabolism and locomotor performances. Funct. Ecol. 27, 136–144 (2013).Article 

Google Scholar 
32.Cano, J. M. & Nicieza, A. G. Temperature, metabolic rate, and constraints on locomotor performance in ectotherm vertebrates. Funct. Ecol. 20, 464–470 (2006).Article 

Google Scholar 
33.Van Leeuwen, T. E., Rosenfeld, J. S. & Richards, J. G. Adaptive tradeoffs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams. J. Anim. Ecol. 80, 1012–1023 (2011).PubMed 
Article 

Google Scholar 
34.Sundström, L. F., Petersson, E., Höjesjö, J., Johnsson, J. I. & Järvi, T. Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): Implications for dominance. Behav. Ecol. 15, 192–198 (2004).Article 

Google Scholar 
35.Clobert, J., Ims, R. A. & Rousset, F. Causes, mechanisms and consequences of dispersal. In Ecology, Genetics and Evolution of Metapopulations (eds Hanski, I. & Gaggiotti, O. E.) 307–336 (Elsevier Academic Press, 2004).
Google Scholar 
36.Bohlin, T., Sundström, L. F., Johnsson, J. I., Höjesjö, J. & Pettersson, J. Density-dependent growth in brown trout: Effects of introducing wild and hatchery fish. J. Anim. Ecol. 71, 683–692 (2002).Article 

Google Scholar 
37.Gerking, S. D. The restricted movement of fish populations. Biol. Rev. 34, 221–242 (1959).Article 

Google Scholar 
38.Rodríguez, M. A. Restricted movement in stream fish: The paradigm is incomplete, not lost. Ecology 83, 1–13 (2002).Article 

Google Scholar 
39.Sánchez-González, J.-R. & Nicieza, A. G. Phenotypic convergence of artificially reared and wild trout is mediated by shape plasticity. Ecol. Evol. 7, 5922–5929 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
40.Webb, P. W. Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24, 107–120 (1984).Article 

Google Scholar 
41.Blake, R. W. Fish functional design and swimming performance. J. Fish Biol. 65, 1193–1222 (2010).Article 

Google Scholar 
42.Lowe, W. H. What drives long-distance dispersal? A test of theoretical predictions. Ecology 90, 1456–1462 (2009).PubMed 
Article 

Google Scholar 
43.Nicieza, A. G. Morphological variation between geographically disjunct populations of Atlantic salmon: The effects of ontogeny and habitat shift. Funct. Ecol. 9, 448–456 (1995).Article 

Google Scholar 
44.Billman, E. J. et al. Body morphology differs in wild juvenile Chinook salmon Oncorhynchus tshawytscha that express different migratory phenotypes in the Willamette River, Oregon, USA. J. Fish Biol. 85, 1097–1110. https://doi.org/10.1111/jfb.12482 (2014).CAS 
Article 
PubMed 

Google Scholar 
45.Langerhans, R. B. & Reznick, D. N. Ecology and Evolution of Swimming Performance in Fishes: Predicting Evolution with Biomechanics. Fish Locomotion: An Ethoecological Perspective (Science Publishers, 2010).
Google Scholar 
46.Cano-Barbacil, C. et al. Key factors explaining critical swimming speed in freshwater fish: A review and statistical analysis for Iberian species. Sci. Rep. 10, 18947. https://doi.org/10.1038/s41598-020-75974-x (2020).CAS 
Article 
PubMed 
PubMed Central 
ADS 

Google Scholar 
47.Johnsson, J. I., Nöbbelin, F. & Bohlin, T. Territorial competition among wild brown trout fry: effects of ownership and body size. J. Fish Biol. 54, 469–472 (1999).Article 

Google Scholar 
48.Deverill, J. I., Adams, C. E. & Bean, C. W. Prior residence, aggression and territory acquisition in hatchery-reared and wild brown trout. J. Fish Biol. 55, 868–875 (1999).Article 

Google Scholar 
49.Weiss, S. & Schmutz, S. Performance of hatchery-reared brown trout and their effects on wild fish in two small Austrian streams. Trans. Am. Fish. Soc. 128, 302–316 (1999).Article 

Google Scholar 
50.Fagan, W. F. Connectivity, fragmentation, and extinction risk in dendritic metapopulations. Ecology 83, 3243–3249 (2002).Article 

Google Scholar 
51.Álvarez, D. & Nicieza, A. G. Is metabolic rate a reliable predictor of growth and survival of brown trout (Salmo trutta) in the wild?. Can. J. Fish. Aquat. Sci. 62, 643–649 (2005).Article 

Google Scholar 
52.Álvarez, D., Cano, J. M. & Nicieza, A. G. Microgeographic variation in metabolic rate and energy storage of brown trout: Countergradient selection or thermal sensitivity?. Evol. Ecol. 20, 345–363 (2006).Article 

Google Scholar 
53.Valentin, A. E. et al. Arching effect on fish body shape in geometric morphometric studies. J. Fish Biol. 73, 623–638 (2008).Article 

Google Scholar 
54.Leblanc, C. A. & Noakes, D. L. Visible Iiplant elastomer (VIE) tags for marking small rainbow trout. N. Am. J. Fish. Manag. 32, 716–719 (2012).Article 

Google Scholar 
55.Rohlf, F. J. tpsDig2: A Program Digitize Landmarks and Outlines (Springer, 2013).
Google Scholar 
56.Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. Geometric Morphometrics for Biologists: A Primer (Elsevier Academic Press, 2004).
Google Scholar 
57.Rohlf, F. J. tpsRelw: Relative Warps Analysis (Spinger, 2013).
Google Scholar 
58.Horton, R. E. Erosional development of streams and their drainage basins; hydrophysical approach to quantitative morphology. Bull. Geol. Soc. Am. 56, 275–370 (1945).Article 

Google Scholar 
59.Fraser, N. H. C., Metcalfe, N. B. & Thorpe, J. E. Temperature-dependent switch between diurnal and nocturnal foraging in salmon. Proc. R. Soc. B Biol. Sci. 252, 135–139 (1993).Article 
ADS 

Google Scholar 
60.Contor, C. R. & Griffith, J. S. Nocturnal emergence of juvenile rainbow trout from winter concealment relative to light intensity. Hydrobiologia 299, 179–183 (1995).Article 

Google Scholar 
61.Závorka, L., Aldvén, D., Näslund, J., Höjesjö, J. & Johnsson, J. I. Inactive trout come out at night: Behavioral variation, circadian activity, and fitness in the wild. Ecology 97, 2223–2231 (2016).PubMed 
Article 

Google Scholar 
62.Lyon, J. P. et al. Efficiency of electrofishing in turbid lowland rivers: Implications for measuring temporal change in fish populations. Can. J. Fish. Aquat. Sci. 71, 878–886 (2014).Article 

Google Scholar 
63.Clark, P. J. & Evans, F. C. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35, 445–453 (1954).Article 

Google Scholar 
64.Baddeley, A. & Turner, R. spatstat: An R package for analyzing spatial point patterns. J. Stat. Softw. 12, 1–42 (2005).Article 

Google Scholar 
65.Baddeley, A., Rubak, E. & Turner, R. Spatial Point Patterns: Methodology and Applications with R (Chapman & Hall/CRC Press Book, 2015).
Google Scholar 
66.R Development Core Team. R: A Language and Environment for Statistical Computing. R version 4.0.2: “Taking Off Again”. (2020).67.Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S. (Springer, 2002). https://doi.org/10.1007/978-0-387-21706-268.Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57, 289–300 (1995).MathSciNet 
MATH 

Google Scholar 
69.Benjamini, Y. Discovering the false discovery rate. J. R. Stat. Soc. B 57, 405–416 (2010).MathSciNet 
MATH 
Article 

Google Scholar 
70.Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: A practical information-theoretic approach. (Springer, 2002).
Google Scholar 
71.Symonds, M. R. E. & Moussalli, A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav. Ecol. Sociobiol. 65, 13–21 (2011).Article 

Google Scholar 
72.Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23–35 (2011).Article 

Google Scholar 
73.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  More

1.Murray, N. J. et al. The global distribution and trajectory of tidal flats. Nature 565(7738), 222 (2019).ADS 
CAS 
PubMed 
Article 

Google Scholar 
2.Bu, N. S. et al. Reclamation of coastal salt marshes promoted carbon loss from previously-sequestered soil carbon pool. Ecol. Eng. 81, 335–339 (2015).Article 

Google Scholar 
3.Cui, B. S., He, Q., Gu, B. H., Bai, J. H. & Liu, X. H. China’s coastal wetlands: understanding environmental changes and human impacts for management and conservation. Wetlands 36(Suppl 1), S1–S9 (2016).Article 

Google Scholar 
4.Cao, Z. Q. et al. Heavy metal pollution and the risk from tidal flat reclamation in coastal areas of Jiangsu, China. Mar. Pollut. Bull. 158, 111427 (2020).CAS 
PubMed 
Article 

Google Scholar 
5.Yin, A. J. et al. Salinity evolution of coastal soils following reclamation and intensive usage, Eastern China. Environ. Earth Sci. 75, 1281 (2016).Article 
CAS 

Google Scholar 
6.Wang, W., Liu, H., Li, Y. Q. & Su, J. L. Development and management of land reclamation in China. Ocean Coast. Manage. 102, 415–425 (2014).Article 

Google Scholar 
7.Laffoley, D. & Grimsditch, G. The Management of Natural Coastal Carbon Sinks (IUCN, 2009).
Google Scholar 
8.Cheong, S. et al. Coastal adaptation with ecological engineering. Nat. Clim. Change 3, 787–791 (2013).ADS 
Article 

Google Scholar 
9.Yang, W. et al. Seawall construction alters soil carbon and nitrogen dynamics and soil microbial biomass in an invasive Spartina alterniflora salt marsh in eastern China. Appl. Soil Ecol. 110, 1–11 (2017).ADS 
CAS 
Article 

Google Scholar 
10.Ding, L. J., Su, J. Q., Li, H., Zhu, Y. G. & Cao, Z. H. Bacterial succession along a long-term chronosequence of paddy soil in the Yangtze River Delta, China. Soil Biol. Biochem. 104, 59–67 (2017).CAS 
Article 

Google Scholar 
11.Zhang, H. et al. Changes in surface soil organic/inorganic carbon concentrations and their driving forces in reclaimed coastal tidal flats. Geoderma 352, 150–159 (2019).ADS 
CAS 
Article 

Google Scholar 
12.Han, G. X. et al. Agricultural reclamation effects on ecosystem CO2 exchange of a coastal wetland in the Yellow River Delta. Agr. Ecosyst. Environ. 196, 187–198 (2014).Article 

Google Scholar 
13.Hargreaves, S. K. & Hofmockel, K. S. Physiological shifts in the microbial community drive changes in enzyme activity in a perennial agroecosystem. Biogeochemistry 117, 67–79 (2014).CAS 
Article 

Google Scholar 
14.Ramirez, K. S., Lauber, C. L., Knight, R., Bradford, M. A. & Fierer, N. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91, 3463–3470 (2010).PubMed 
Article 
PubMed Central 

Google Scholar 
15.Rousk, J., Brookes, P. C. & Bååth, E. The microbial PLFA composition as affected by pH in an arable soil. Soil Biol. Biochem. 42, 516–520 (2010).CAS 
Article 

Google Scholar 
16.Kamble, P. N., Gaikwad, V. B., Kuchekar, S. R. & Bååth, E. Microbial growth, biomass, community structure and nutrient limitation in high pH and salinity soils from Pravaranagar (India). Eur. J. Soil Biol. 65, 87–95 (2014).CAS 
Article 

Google Scholar 
17.Gao, Y. C. et al. Effects of salinization and crude oil contamination on soil bacterial community structure in the Yellow River Delta region, China. Appl. Soil Ecol. 86, 165–173 (2015).Article 

Google Scholar 
18.Placella, S. A., Brodie, E. L. & Firestone, M. K. Rainfall – induced carbon oxide pulses results from sequential resuscitation of phylogenetically cluster microbial groups. Proc. Natl. Acad. Sci. 109, 10931–10936 (2012).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
19.Yuan, Y. et al. Responses of microbial community structure to land-use conversion and fertilization in southern China. Eur. J. Soil Biol. 70, 1–6 (2015).ADS 
Article 

Google Scholar 
20.Iost, S., Landgraf, D. & Makeschin, F. Chemical soil properties of reclaimed marsh soil from Zhejiang Province P.R. China. Geoderma 142, 245–250 (2007).ADS 
CAS 
Article 

Google Scholar 
21.Yang, W. et al. Shift in soil organic carbon and nitrogen pools in different reclaimed lands following intensive coastal reclamation on the coasts of eastern China. Sci. Rep. 9, 5921 (2019).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
22.Assefa, D. et al. Deforestation and land use strongly effect soil organic carbon and nitrogen stock in Northwest Ethiopia. Catena 153, 89–99 (2017).CAS 
Article 

Google Scholar 
23.Chen, G. X., Gao, D. Z., Wang, Z. P. & Zeng, C. S. Contents of carbon, nitrogen and phosphorus in sediments in aquaculture ponds for different reclamation years in Shanyutan wetlands and its pollution risk assessment. Wetland Sci. 15, 309–314 (2017).
Google Scholar 
24.Whitting, G. J. & Chanton, J. P. Greenhouse carbon balance of wetlands: methane emission versus carbon sequestration. Tellus B. 53, 521–528 (2001).ADS 

Google Scholar 
25.Wissing, L. et al. Management-induced organic carbon accumulation in paddy soils: the role of organo-mineral associations. Soil Tillage. Res. 126, 60–71 (2013).Article 

Google Scholar 
26.Xing, W. L., Cheng, X. R., Xiong, J., Yuan, H. J. & Yu, M. K. Variations in soil biological properties in poplar plantations along coastal reclamation stages. Appl. Soil Ecol. 154, 103649 (2020).Article 

Google Scholar 
27.Grybos, M., Davranche, M., Gruau, G., Petitjean, P. & Pedrot, M. Increasing pH drives organic matter solubilization from wetland soils under reducing conditions. Geoderma 154, 13–19 (2009).ADS 
CAS 
Article 

Google Scholar 
28.Krishnamoorthy, R., Kim, K., Kim, C. & Sa, T. Changes of arbuscular mycorrhizal traits and community structure with respect to soil salinity in a coastal reclamation land. Soil Biol. Biochem. 72, 1–10 (2014).CAS 
Article 

Google Scholar 
29.Chodak, M., Gołębiewski, M., Morawska-Płoskonka, J., Kuduk, K. & Niklińska, M. Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl. Soil Ecol. 64, 7–14 (2013).Article 

Google Scholar 
30.Peay, K. G., Baraloto, C. & Fine, P. V. Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J. 7, 1852–1861 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
31.Santonja, M. et al. Plant litter mixture partly mitigates the negative effects of extended drought on soil biota and litter decomposition in a Mediterranean oak forest. J. Ecol. 105, 801–815 (2017).Article 

Google Scholar 
32.Yang, W. et al. Response of the soil microbial community composition and biomass to a short-term Spartina alterniflora invasion in a coastal wetland of eastern China. Plant Soil 408, 443–456 (2016).CAS 
Article 

Google Scholar 
33.Anderson, C. R. et al. Biochar induced soil microbial community change: Implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 54, 309–320 (2011).CAS 
Article 

Google Scholar 
34.Mavi, M. S. & Marschner, P. Salinity affects the response of soil microbial activity and biomass to addition of carbon and nitrogen. Soil Res. 51, 68–75 (2013).CAS 
Article 

Google Scholar 
35.Xie, X. F. et al. Comparison of random forest and multiple linear regression models for estimation of soil extracellular enzyme activities in agricultural reclaimed coastal saline land. Ecol. Indic. 120, 106925 (2021).CAS 
Article 

Google Scholar 
36.Mohammad, M. J., Malkawi, H. I. & Shibli, R. Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J. Plant Nutr. 26, 125–137 (2003).CAS 
Article 

Google Scholar 
37.Cui, X. C., Hu, J. L., Wang, J. J., Yang, J. S. & Lin, X. G. Reclamation negatively influences arbuscular mycorrhizal fungal community structure and diversity in coastal saline-alkaline land in Eastern China as revealed by Illumina sequencing. Appl. Soil Ecol. 98, 140–149 (2016).Article 

Google Scholar 
38.Guo, X. & Gong, J. Differential effects of abiotic factors and host plant traits on diversity and community composition of root-colonizing arbuscular mycorrhizal fungi in a salt-stressed ecosystem. Mycorrhiza 24, 79–94 (2014).PubMed 
Article 

Google Scholar 
39.Yamato, M., Yagame, T., Yoshimura, Y. & Iwase, K. Effect of environmental gradient in coastal vegetation on communities of arbuscular mycorrhizal fungi associated with Ixeris repens (Asteraceae). Mycorrhiza 22, 622–630 (2012).Article 

Google Scholar 
40.Strickland, M. S. & Rousk, J. Considering fungal :bacterial dominance in soils: Methods, controls, and ecosystem implications. Soil Biol. Biochem. 42, 1385–1395 (2010).CAS 
Article 

Google Scholar 
41.Collins, C. G., Stajich, J. E., Weber, S. E., Pombubpa, N. & Diez, J. M. Shrub range expansion alters diversity and distribution of soil fungal communities across an alpine elevation gradient. Mol. Ecol. 27, 2461–2476 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
42.Yang, W. et al. Soil fungal communities vary with invasion by the exotic Spartina alternifolia Loisel. in coastal salt marshes of eastern China. Plant Soil 442, 215–232 (2019).CAS 
Article 

Google Scholar 
43.Yang, W. et al. Exotic Spartina alterniflora Loisel. invasion significantly shifts soil bacterial communities with the successional gradient of saltmarsh in eastern China. Plant Soil 449, 97–115 (2020).CAS 
Article 

Google Scholar 
44.Wang, C. et al. Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol. Biochem. 121, 103–112 (2018).CAS 
Article 

Google Scholar 
45.Högberg, M. N., Baath, E., Nordgren, A., Arnebrant, K. & Högberg, P. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs: A hypothesis based on field observations in boreal forests. New Phytol. 160, 225–238 (2003).Article 
CAS 

Google Scholar 
46.Joergensen, R. G. & Wichern, F. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol. Biochem. 40, 2977–2991 (2008).CAS 
Article 

Google Scholar 
47.Xu, S. Q. et al. Comparison of microbial community composition and diversity in native coastal wetlands and wetlands that have undergone long-term agricultural reclamation. Wetlands 37, 99–108 (2017).CAS 
Article 

Google Scholar 
48.Vangestel, M., Merckx, R. & Vlassak, K. Microbial biomass responses to soil drying and rewetting-the fate of fast-growing and slow-growing microorganisms in soils from different climates. Soil Biol. Biochem. 25, 109–123 (1993).Article 

Google Scholar 
49.Farrell, M. Microbial utilisation of biochar-derived carbon. Sci. Total Environ. 465, 288–297 (2013).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
50.Luo, S. S. Aggregate-related changes in soil microbial communities under different ameliorant applications in saline-sodic soils. Geoderma 329, 108–117 (2018).ADS 
CAS 
Article 

Google Scholar 
51.Tripathi, B. M. et al. Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb. Ecol. 64, 474–484 (2012).PubMed 
Article 
PubMed Central 

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

Google Scholar 
53.Huang, Y. M., Liu, D. & An, S. S. Effects of slope aspect on soil nitrogen and microbial properties in the Chinese Loess region. Catena 125, 135–145 (2015).CAS 
Article 

Google Scholar 
54.Bossio, D. A., Fleck, J. A., Scow, K. M. & Fujii, R. Alteration of soil microbial communities and water quality in restored wetlands. Soil Biol. Biochem. 38, 1223–1233 (2006).CAS 
Article 

Google Scholar 
55.Chang, E. H., Chen, C. P., Tian, G. L. & Chiu, C. Y. Replacement of natural hardwood forest with planted bamboo and cedar in a humid subtropical mountain affects soil microbial community. Appl. Soil Ecol. 124, 146–154 (2018).ADS 
Article 

Google Scholar 
56.Cao, Y. S. et al. Soil microbial community composition under Eucalyptus plantations of different age in subtropical China. Eur. J. Soil Biol. 46, 128–135 (2010).CAS 
Article 

Google Scholar 
57.Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).CAS 
Article 

Google Scholar 
58.Bossio, D. A. & Scow, K. M. Impacts of carbon and flooding on soil microbial communities: Phospholipid fatty acid profiles and substrate utilization patterns. Microbial. Ecol. 35, 265–278 (1998).CAS 
Article 

Google Scholar 
59.Bååth, E. & Anderson, T. H. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol. Biochem. 35, 955–963 (2003).Article 
CAS 

Google Scholar 
60.Kourtev, P. S., Ehrenfeld, J. G. & Häggblom, M. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152–3166 (2002).Article 

Google Scholar  More

1.Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN. Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett. 2008;278:1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x.Article 
PubMed 

Google Scholar 
2.Rodriguez R, White J Jr, Arnold A, Redman R. Fungal endophytes: diversity and functional roles. New Phytol. 2009;182:314–30.Article 

Google Scholar 
3.Wilson D. Endophyte: the evolution of a term, and clarification of its use and definition Oikos. 1995;73:274–6.4.Harrison JG, Griffin EA. The diversity and distribution of endophytes across biomes, plant phylogeny and host tissues: How far have we come and where do we go from here?. Environ Microbiol. 2020;22:2107–23. https://doi.org/10.1111/1462-2920.14968.Article 
PubMed 

Google Scholar 
5.Clay K, Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat. 2002;160:S99–S127. https://doi.org/10.1086/342161.Article 
PubMed 

Google Scholar 
6.Rudgers JA, Afkhami ME, Rúa MA, Davitt AJ, Hammer S, Huguet VM. A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology. 2009;90:1531–9. https://doi.org/10.1890/08-0116.1.Article 
PubMed 

Google Scholar 
7.Clay K, Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science. 1999;285:1742–4. https://doi.org/10.1126/science.285.5434.1742.Article 
PubMed 

Google Scholar 
8.Afkhami ME, Strauss SY. Native fungal endophytes suppress an exotic dominant and increase plant diversity over small and large spatial scales. Ecology. 2016;97:1159–69. https://doi.org/10.1890/15-1166.1.Article 
PubMed 

Google Scholar 
9.Rudgers JA, Clay K. An invasive plant–fungal mutualism reduces arthropod diversity. Ecol Lett. 2008;11:831–40. https://doi.org/10.1111/j.1461-0248.2008.01201.x.Article 
PubMed 

Google Scholar 
10.Gorischek AM, Afkhami ME, Seifert EK, Rudgers JA. Fungal symbionts as manipulators of plant reproductive biology. Am Nat. 2013;181:562–70. https://doi.org/10.1086/669606.Article 
PubMed 

Google Scholar 
11.Malloch D, Blackwell M. Dispersal of fungal diaspores. The fungal community: Its organization and role in the ecosystem. 2nd ed. New York, NY: Marcel Dekker, Inc; 1992. p. 147–71.
Google Scholar 
12.Devarajan P, Suryanarayanan T. Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. Fungal Divers. 2006;23:111–9.
Google Scholar 
13.Lodge DJ, Fisher P, Sutton B. Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia. 1996;88:733–8.14.Paine RT. A note on trophic complexity and community stability. Am Nat. 1969;103:91–93. https://doi.org/10.1086/282586.Article 

Google Scholar 
15.Jenkins SH, Busher PE. Castor canadensis, Mammalian Species. 1979. https://doi.org/10.2307/3503787.16.Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012;10:717–25. https://doi.org/10.1038/nrmicro2873.Article 
PubMed 
PubMed Central 

Google Scholar 
17.Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. Where less may be more: How the rare biosphere pulls ecosystems strings. ISME J. 2017;11:853–62. https://doi.org/10.1038/ismej.2016.174.Article 
PubMed 
PubMed Central 

Google Scholar 
18.Hassani MA, Durán P, Hacquard S. Microbial interactions within the plant holobiont. Microbiome. 2018;6:58. https://doi.org/10.1186/s40168-018-0445-0.Article 
PubMed 
PubMed Central 

Google Scholar 
19.Rockman MV. The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. Evolution. 2012;66:1–17. https://doi.org/10.1111/j.1558-5646.2011.01486.x.Article 
PubMed 

Google Scholar 
20.Beckers GJ, Conrath U. Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol. 2007;10:425–31. https://doi.org/10.1016/j.pbi.2007.06.002.Article 
PubMed 

Google Scholar 
21.Hartmann A, Rothballer M, Hense BA, Schröder P. Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci. 2014;5. https://doi.org/10.3389/fpls.2014.00131.22.Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E. Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst. 2011;42:23–46. https://doi.org/10.1146/annurev-ecolsys-102710-145039.Article 

Google Scholar 
23.Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev. 2015;79:293–320. https://doi.org/10.1128/MMBR.00050-14.Article 
PubMed 
PubMed Central 

Google Scholar 
24.Doty SL. Growth-promoting endophytic fungi of forest trees. In: Pirttilä AM, Frank AC, editors. Endophytes of forest trees: biology and applications. Dordrecht: Springer Netherlands; 2011;151–6.
Google Scholar 
25.Arnold AE, Herre EA. Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia. 2003;95:388–98. http://www.mycologia.org.unr.idm.oclc.org/content/95/3/388. Accessed 12 Dec 2016.Article 

Google Scholar 
26.Busby PE, Peay KG, Newcombe G. Common foliar fungi of Populus trichocarpa modify melampsora rust disease severity. New Phytol. 2016;209:1681–92. https://doi.org/10.1111/nph.13742.Article 
PubMed 

Google Scholar 
27.Christian N, Herre EA, Mejia LC, Clay K. Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage. Proc R Soc B. 2017;284:20170641. https://doi.org/10.1098/rspb.2017.0641.Article 
PubMed 

Google Scholar 
28.Cheplick GP, Cho R. Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytol. 2003;158:183–91. https://doi.org/10.1046/j.1469-8137.2003.00723.x.Article 

Google Scholar 
29.Zahn G, Amend AS. Foliar fungi alter reproductive timing and allocation in arabidopsis under normal and water-stressed conditions. 2019. https://www.biorxiv.org/content/10.1101/519678v1.30.Christian N, Herre EA, Clay K. Foliar endophytic fungi alter patterns of nitrogen uptake and distribution in Theobroma cacao. New Phytol. 2019;222:1573–83. https://doi.org/10.1111/nph.15693.Article 
PubMed 

Google Scholar 
31.Rosado BHP, Almeida LC, Alves LF, Lambais MR, Oliveira RS. The importance of phyllosphere on plant functional ecology: a phyllo trait manifesto. New Phytol. 2018;219:1145–9. https://doi.org/10.1111/nph.15235.Article 
PubMed 

Google Scholar 
32.Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, et al. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol. 2014;5:479.33.Dupont PY, Eaton CJ, Wargent JJ, Fechtner S, Solomon P, Schmid J, et al. Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol. 2015;208:1227–40. https://doi.org/10.1111/nph.13614.Article 
PubMed 
PubMed Central 

Google Scholar 
34.Dinkins RD, Nagabhyru P, Graham MA, Boykin D, Schardl CL. Transcriptome response of Lolium arundinaceum to its fungal endophyte Epichloë coenophiala. New Phytol. 2017;213:324–37. https://doi.org/10.1111/nph.14103.Article 
PubMed 

Google Scholar 
35.Welsh S, North American species of astragalus Linnaeus (Leguminosae): a taxonomic revision. Provo, Utah: Brigham Young University; 2007.36.Knaus BJ. Morphometric architecture of the most taxon-rich species in the U.S. Flora: Astragalus lentiginosus (Fabaceae). Am J Bot. 2010;97;1816–26. https://doi.org/10.3732/ajb.0900145.37.Baucom DL, Romero M, Belfon R, Creamer R. Two new species of undifilum, fungal endophytes of astragalus (locoweeds) in the United States. Botany. 2012;90:866–75. https://doi.org/10.1139/b2012-056.Article 

Google Scholar 
38.Woudenberg JHC, Groenewald JZ, Binder M, Crous PW. Alternaria redefined. Stud Mycol. 2013;75:171–212. https://doi.org/10.3114/sim0015.Article 
PubMed 
PubMed Central 

Google Scholar 
39.Cook D, Gardner DR, Martinez A, Robles CA, Pfister JA. Screening for swainsonine among South American astragalus species. Toxicon. 2017;139:54–7. https://doi.org/10.1016/j.toxicon.2017.09.014.Article 
PubMed 

Google Scholar 
40.Molyneux RJ, James LF. Loco intoxication: indolizidine alkaloids of spotted locoweed (Astragalus lentiginosus). Science. 1982;216:190–1. https://doi.org/10.1126/science.6801763.Article 
PubMed 

Google Scholar 
41.Cook D, Gardner DR, Ralphs MH, Pfister JA, Welch KD, Green BT. Swainsoninine concentrations and endophyte amounts of Undifilum oxytropis in different plant parts of Oxytropis sericea. J Chem Ecol. 2009;35:1272–8. https://doi.org/10.1007/s10886-009-9710-9.Article 
PubMed 

Google Scholar 
42.Harrison JG, Parchman TL, Cook D, Gardner DR, Forister ML. A heritable symbiont and host-associated factors shape fungal endophyte communities across spatial scales. J Ecol. 2018;106:2274–86. https://doi.org/10.1111/1365-2745.12967.Article 

Google Scholar 
43.Grum DS, Cook D, Baucom D, Mott IW, Gardner DR, Creamer R, et al. Production of the alkaloid swainsonine by a fungal endophyte in the host Swainsona canescens. J Nat Prod. 2013;76:1984–8. https://doi.org/10.1021/np400274n.44.Cook D, Gardner DR, Pfister JA. Swainsonine-containing plants and their relationship to endophytic fungi. J Agric Food Chem. 2014;62:7326–34. https://doi.org/10.1021/jf501674r.Article 
PubMed 

Google Scholar 
45.Panaccione DG, Beaulieu WT, Cook D. Bioactive alkaloids in vertically transmitted fungal endophytes. Funct Ecol. 2014;28:299–314. https://doi.org/10.1111/1365-2435.12076.Article 

Google Scholar 
46.Thompson DC, Knight JL, Sterling TM, Murray LW. Preference for specific varieties of woolly locoweed by a specialist weevil, Cleonidius trivittatus (Say). Southwest Entomol. 1995;20:325–325.
Google Scholar 
47.Parker JE. Effects of insect herbivory by the four-lined locoweed weevil, Cleonidius trivittatus (say) (Coleoptera: Curculionidae), on the alkaloid swainsonine in locoweeds Astragalus mollissimus and Oxytropis sericea. Ph.D. thesis. Las Cruces, New Mexico: New Mexico State University; 2008.48.Creamer R, Baucom D. Fungal endophytes of locoweeds: a commensal relationship? J Plant Physiol Pathol. 2013;1. https://doi.org/10.4172/2329-955X.1000104.49.Lu H, Quan H, Zhou Q, Ren Z, Xue R, Zhao B, et al. Endogenous fungi isolated from three locoweed species from rangeland in western China. Afr J Microbiol Res. 2017;11:155–70. https://doi.org/10.5897/AJMR2016.8392.Article 

Google Scholar 
50.Schulthess FM, Faeth SH. Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia. 1998;90:569–78. https://doi.org/10.1080/00275514.1998.12026945.Article 

Google Scholar 
51.Cook D, Gardner DR, Pfister JA, Stonecipher CA, Robins JG, Morgan JA. Effects of elevated CO2 on the swainsonine chemotypes of Astragalus lentiginosus and Astragalus mollissimus. J Chem Ecol. 2017;43:307–16. https://doi.org/10.1007/s10886-017-0820-5.Article 
PubMed 

Google Scholar 
52.Oldrup E, McLain-Romero J, Padilla A, Moya A, Gardner D, Creamer R. Localization of endophytic undifilum fungi in locoweed seed and influence of environmental parameters on a locoweed in vitro culture system. Botany. 2010;88:512–21. https://doi.org/10.1139/B10-026.Article 

Google Scholar 
53.Gardner DR, Molyneux RJ, Ralphs MH. Analysis of swainsonine: extraction methods, detection, and measurement in populations of locoweeds (oxytropis spp.). J Agric Food Chem. 2001;49:4573–80.Article 

Google Scholar 
54.Högberg P. 15N natural abundance in soil–plant systems. New Phytol. 1997;137:179–203. https://www.cambridge.org/core/journals/new-phytologist/article/tansley-review-no-95-15n-natural-abundance-in-soilplant-systems/304069FD5C8283EDB78D0AA594465E71. Accessed 2 Jul 2017.Article 

Google Scholar 
55.Wang Y, Qian P-Y. Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE. 2009;4:e7401. https://doi.org/10.1371/journal.pone.0007401.Article 
PubMed 
PubMed Central 

Google Scholar 
56.White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Glefand DH, Sninsky JJ, White TJ, editors, PCR protocols: a guide to methods and applications. London: Academic Press; 1990.57.Harrison JG, Calder WJ, Shuman B, Buerkle CA, The quest for absolute abundance: the use of internal standards for DNA-based community ecology. Mol Ecol Resour. 2020, https://doi.org/10.1111/1755-0998.13247.58.Tourlousse DM, Yoshiike S, Ohashi A, Matsukura S, Noda N, Sekiguchi Y. Synthetic spike-in standards for high-throughput 16S rRNA gene amplicon sequencing. Nucleic Acids Res. 2017;45:e23–e23. https://doi.org/10.1093/nar/gkw984.Article 
PubMed 

Google Scholar 
59.Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.Article 

Google Scholar 
60.Rognes T, Flouri T, Nichols B, Quince C, Mahé F, “VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016. https://doi.org/10.7717/peerj.2584.61.Edgar RC, UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. 2016. https://www.biorxiv.org/content/10.1101/081257v1.full.62.Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017:2639. https://doi.org/10.1038/ismej.2017.119.63.Edgar R, “SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. 2016. https://www.biorxiv.org/content/10.1101/074161v1.64.Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, et al. The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 2018, https://doi.org/10.1093/nar/gky1022.65.Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal database project: data and tools for high throughput rRNA analysis Nucleic Acids Res. 2014. 42, https://doi.org/10.1093/nar/gkt1244.66.Machida RJ, Leray M, Ho S-L, Knowlton N. Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples. Sci Data. 2017;4:17007 https://doi.org/10.1038/sdata.2017.27.Article 

Google Scholar 
67.Fordyce JA, Gompert Z, Forister ML, Nice CC. A hierarchical Bayesian approach to ecological count data: A flexible tool for ecologists. PLoS ONE. 2011;6;e26785. https://doi.org/10.1371/journal.pone.0026785.68.Harrison JG, Calder WJ, Shastry V, Buerkle CA. Dirichlet-multinomial modelling outperforms alternatives for analysis of microbiome and other ecological count data. Mol Ecol Resour. 2020;20:481–97. https://doi.org/10.1111/1755-0998.13128.Article 
PubMed 

Google Scholar 
69.R Core Team, R: a language and environment for statistical computing. Vienna: R Core Team; 2019.70.Harrison J, Shastry V, Calder WJ, Buerkle CA, “CNVRG: Dirichlet-multinomial modelling of relative abundance data.” Sep. 2020. https://CRAN.R-project.org/package=CNVRG. Accessed 28 Oct 2020.71.S. D. Team, Stan modeling language users guide and reference manual. 2020. https://mc-stan.org/users/documentation/72.S. D. Team, “RStan: The R interface to Stan. R package.” 2020. http://mc-stan.org/.73.Gelman A, Rubin DB. Inference from iterative simulation using multiple sequences. Stat Sci. 1992;7:457–72. http://www.jstor.org/stable/2246093. Accessed 16 Jun 2018.
Google Scholar 
74.Gloor GB, Macklaim JM, Vu M, Fernandes AD. Compositional uncertainty should not be ignored in high-throughput sequencing data analysis. Austrian J Stat. 2016;45:73–87. http://ajs.data-analysis.at/index.php/ajs/article/view/vol45-4-5. Accessed 4 Dec 2017.Article 

Google Scholar 
75.Jost L. Entropy and diversity. Oikos. 2006;113:363–75.Article 

Google Scholar 
76.Marion ZH, Fordyce JA, Fitzpatrick BM. A hierarchical Bayesian model to incorporate uncertainty into methods for diversity partitioning. Ecology. 2018;99:947–56. https://doi.org/10.1002/ecy.2174.Article 
PubMed 

Google Scholar 
77.Harrison JG, Gompert Z, Fordyce JA, Buerkle CA, Grinstead R, Jahner JP. et al. The many dimensions of diet breadth: phytochemical, genetic, behavioral, and physiological perspectives on the interaction between a native herbivore and an exotic host. PLoS ONE. 2016;11:e0147971. https://doi.org/10.1371/journal.pone.0147971.Article 
PubMed 
PubMed Central 

Google Scholar 
78.Plummer M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling,”. Proc 3rd Int workshop Distrib Stat Comput. 2003;124:1–8. 10.2003.
Google Scholar 
79.Plummer M. Rjags: Bayesian graphical models using MCMC. R package version 3-15. 2015. Https://CRAN.R-project.org/package=rjags.80.Breiman L. Random forests. Mach Learn. 2001;45:5–32. https://doi.org/10.1023/A:1010933404324.Article 

Google Scholar 
81.Liaw A, Wiener M. Classification and regression by randomForest. R News. 2002;2:18–22.
Google Scholar 
82.Grum DS, Cook D, Gardner DR, Roper JM, Pfister JA, Ralphs MH. Influence of seed endophyte amounts on swainsonine concentrations in astragalus and oxytropis locoweeds. J Agric Food Chem. 2012;60:8083–9. https://doi.org/10.1021/jf3024062.Article 
PubMed 

Google Scholar 
83.Marion ZH, Fordyce JA, Fitzpatrick BM. Extending the concept of diversity partitioning to characterize phenotypic complexity. Am Nat. 2015;186:348–61.Article 

Google Scholar 
84.Arnold AE, Lutzoni F. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots?”. Ecology. 2007;88:541–49. https://doi.org/10.1890/05-1459.Article 
PubMed 

Google Scholar 
85.Strong DR, Lawton JH, Southwood SR. Insects on plants. Community patterns and mechanisms. Oxford, UK: Blackwell Scientific Publicatons; 1984.
Google Scholar 
86.Carmona D, Lajeunesse MJ, Johnson MTJ. Plant traits that predict resistance to herbivores. Funct Ecol. 2011;25:358–67. https://doi.org/10.1111/j.1365-2435.2010.01794.x.Article 

Google Scholar 
87.Berry D, Widder S. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol. 2014;5. https://doi.org/10.3389/fmicb.2014.00219.88.Trosvik P, de Muinck EJ. Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa. Microbiome. 2015;3:44 https://doi.org/10.1186/s40168-015-0107-4.Article 
PubMed 
PubMed Central 

Google Scholar 
89.Banerjee S, Schlaeppi K, van der Heijden MGA, Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567. https://doi.org/10.1038/s41579-018-0024-1.90.Braun K, Romero J, Liddell C, Creamer R. Production of swainsonine by fungal endophytes of locoweed. Mycological Res. 2003;107:980–8. https://doi.org/10.1017/S095375620300813X.Article 

Google Scholar 
91.Noor AI, Nava A, Cooke P, Cook D, Creamer R. Evidence for nonpathogenic relationships of alternaria section undifilum endophytes within three host locoweed plant species. Botany. 2018;96:187–200. https://doi.org/10.1139/cjb-2017-0117.Article 

Google Scholar 
92.Kulpa SM, Leger EA. Strong natural selection during plant restoration favors an unexpected suite of plant traits. Evolut Appl. 2013;6:510–23. https://doi.org/10.1111/eva.12038.Article 

Google Scholar 
93.Leger EA, Baughman OW. What seeds to plant in the Great Basin? Comparing traits prioritized in native plant cultivars and releases with those that promote survival in the field. Nat Areas J. 2015;35:54–68. https://doi.org/10.3375/043.035.0108.Article 

Google Scholar 
94.Klypina N, Pinch M, Schutte BJ, Maruthavanan J, Sterling TM, Water-deficit stress tolerance differs between two locoweed genera (astragalus and oxytropis) with fungal endophytes. Weed Sci. 2017:1–13. https://doi.org/10.1017/wsc.2017.21.95.Stamp N. Out of the quagmire of plant defense hypotheses. Q Rev Biol. 2003;78:23–55. https://doi.org/10.1086/367580.Article 
PubMed 

Google Scholar 
96.Eades CJ, Hintz WE. Characterization of the α-mannosidase gene family in filamentous fungi: N-glycan remodelling for the development of eukaryotic expression systems. Biotechnol Bioprocess Eng. 2000;5:227. https://doi.org/10.1007/BF02942178.Article 

Google Scholar 
97.Schmid J, Day R, Zhang N, Dupont PY, Cox MP, Schardl CL, et al. Host tissue environment directs activities of an epichloë endophyte, while it induces systemic hormone and defense responses in its native perennial ryegrass host. Mol Plant Microbe Interact. 2016;30:138–49. https://doi.org/10.1094/MPMI-10-16-0215-R.98.Zamioudis C, Pieterse CMJ. Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact. 2011;25:139–50. https://doi.org/10.1094/MPMI-06-11-0179.Article 

Google Scholar 
99.Kannadan S, Rudgers JA. Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol. 2008;22:706–13. https://doi.org/10.1111/j.1365-2435.2008.01395.x.Article 

Google Scholar 
100.Barillas JRV, Paschke MW, Ralphs MH, Child RD. White locoweed toxicity is facilitated by a fungal endophyte and nitrogen-fixing bacteria. Ecology. 2007;88:1850–6. https://doi.org/10.1890/06-0728.1.Article 

Google Scholar 
101.Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, et al. High plant diversity is needed to maintain ecosystem services. Nature. 2011;477:199–202. https://doi.org/10.1038/nature10282. More

1.Ford, A. K. et al. Reefs under siege: the rise, putative drivers, and consequences of benthic cyanobacterial mats. Front. Mar. Sci. 5, 18 (2018).Article 

Google Scholar 
2.Brocke, H. J. et al. Organic matter degradation drives benthic cyanobacterial mat abundance on Caribbean coral reefs. PLoS ONE 10, e0125445 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
3.Charpy, L., Casareto, B. E., Langlade, M. J. & Suzuki, Y. Cyanobacteria in coral reef ecosystems: a review. J. Mar. Biol. 2012, e259571 (2012).Article 

Google Scholar 
4.Mangubhai, S. & Obura, D. O. Silent killer: black reefs in the Phoenix Islands Protected Area. Pac. Conserv. Biol. 25, 213 (2019).Article 

Google Scholar 
5.de Bakker, D. M. et al. 40 years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs 36, 355–367 (2017).ADS 
Article 

Google Scholar 
6.Albert, S., Dunbabin, M., Skinner, M., Moore, B. & Grinham, A. Benthic shift in a Solomon Islands’ lagoon: corals to cyanobacteria. In Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia, 9–13 July 2012 1–5 (2012).7.Puyana, M., Acosta, A., Bernal-Sotelo, K., Velásquez-Rodríguez, T. & Ramos, F. Spatial scale of cyanobacterial blooms in Old Providence Island Colombian Caribbean. Universitas Scientiarum 20, 83–105 (2015).Article 

Google Scholar 
8.Ford, A. K. et al. High sedimentary oxygen consumption indicates that sewage input from small islands drives benthic community shifts on overfished reefs. Environ. Conserv. 44, 405–411 (2017).Article 

Google Scholar 
9.Chapra, S. C. et al. Climate change impacts on harmful algal blooms in US freshwaters: a screening-level assessment. Environ. Sci. Technol. 51, 8933–8943 (2017).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
10.Huisman, J. et al. Cyanobacterial blooms. Nat. Rev. Microbiol. 16, 471–483 (2018).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
11.Gobler, C. J. Climate change and harmful algal blooms: insights and perspective. Harmful Algae 91, 101731 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
12.Wood, S. A. et al. Toxic benthic freshwater cyanobacterial proliferations: challenges and solutions for enhancing knowledge and improving monitoring and mitigation. Freshw. Biol. 65, 1824–1842 (2020).Article 

Google Scholar 
13.Brown, K. T., Bender-Champ, D., Bryant, D. E. P., Dove, S. & Hoegh-Guldberg, O. Human activities influence benthic community structure and the composition of the coral-algal interactions in the central Maldives. J. Exp. Mar. Biol. Ecol. 497, 33–40 (2017).Article 

Google Scholar 
14.Titlyanov, E. A., Yakovleva, I. M. & Titlyanova, T. V. Interaction between benthic algae (Lyngbya bouillonii, Dictyota dichotoma) and scleractinian coral Porites lutea in direct contact. J. Exp. Mar. Biol. Ecol. 342, 282–291 (2007).Article 

Google Scholar 
15.Carmichael, W. W. Cyanobacteria secondary metabolites—the cyanotoxins. J. Appl. Bacteriol. 72, 445–459 (1992).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
16.Ritson-Williams, R., Paul, V. J. & Bonito, V. Marine benthic cyanobacteria overgrow coral reef organisms. Coral Reefs 24, 629–629 (2005).ADS 
Article 

Google Scholar 
17.Kuffner, I. et al. Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar. Ecol. Prog. Ser. 323, 107–117 (2006).ADS 
Article 

Google Scholar 
18.Kuffner, I. B. & Paul, V. J. Effects of the benthic cyanobacterium Lyngbya majuscula on larval recruitment of the reef corals Acropora surculosa and Pocillopora damicornis. Coral Reefs 23, 455–458 (2004).Article 

Google Scholar 
19.Ritson-Williams, R., Arnold, S. N. & Paul, V. J. The impact of macroalgae and cyanobacteria on larval survival and settlement of the scleractinian corals Acropora palmata, A cervicornis and Pseudodiploria strigosa. Mar. Biol. 167, 31 (2020).Article 

Google Scholar 
20.McClanahan, T. R. et al. Prioritizing key resilience indicators to support coral reef management in a changing climate. PLoS ONE 7, e42884 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
21.Cardini, U., Bednarz, V. N., Foster, R. A. & Wild, C. Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol. Evol. 4, 1706–1727 (2014).PubMed 
PubMed Central 
Article 

Google Scholar 
22.Brocke, H. J. et al. Nitrogen fixation and diversity of benthic cyanobacterial mats on coral reefs in Curaçao. Coral Reefs 37, 861–874 (2018).ADS 
Article 

Google Scholar 
23.Brocke, H. J. et al. High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem. Sci. Rep. 5, 8852 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
24.Haas, A. F. et al. Global microbialization of coral reefs. Nat. Microbiol. 1, 1–7 (2016).Article 
CAS 

Google Scholar 
25.Box, S. J. & Mumby, P. J. Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar. Ecol. Prog. Ser. 342, 139–149 (2007).ADS 
Article 

Google Scholar 
26.Webster, F. J., Babcock, R. C., Keulen, M. V. & Loneragan, N. R. Macroalgae inhibits larval settlement and increases recruit mortality at Ningaloo Reef, Western Australia. PLoS ONE 10, e0124162 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
27.Barott, K. et al. Natural history of coral−algae competition across a gradient of human activity in the Line Islands. Mar. Ecol. Prog. Ser. 460, 1–12 (2012).ADS 
Article 

Google Scholar 
28.Bonaldo, R. M. & Hay, M. E. Seaweed-coral interactions: variance in seaweed allelopathy, coral susceptibility, and potential effects on coral resilience. PLoS ONE 9, e85786 (2014).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
29.Rasher, D. B., Hoey, A. S. & Hay, M. E. Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94, 1347–1358 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
30.Capper, A., Cruz-Rivera, E., Paul, V. J. & Tibbetts, I. R. Chemical deterrence of a marine cyanobacterium against sympatric and non-sympatric consumers. Hydrobiologia 553, 319 (2006).CAS 
Article 

Google Scholar 
31.Clements, K. D., German, D. P., Piché, J., Tribollet, A. & Choat, J. H. Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol. J. Linn. Soc. https://doi.org/10.1111/bij.12914 (2016).Article 

Google Scholar 
32.Cissell, E. C., Manning, J. C. & McCoy, S. J. Consumption of benthic cyanobacterial mats on a Caribbean coral reef. Sci. Rep. 9, 12693 (2019).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
33.Edwards, C. B. et al. Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc. Biol. Sci. 281, 20131835 (2014).CAS 
PubMed 
PubMed Central 

Google Scholar 
34.Goatley, C., Bonaldo, R., Fox, R. & Bellwood, D. Sediments and herbivory as sensitive indicators of coral reef degradation. Ecol. Soc. 21, 29 (2016).35.Robinson, J. P. W. et al. Habitat and fishing control grazing potential on coral reefs. Funct. Ecol. 34, 240–251 (2020).Article 

Google Scholar 
36.Mouillot, D. et al. Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. PNAS 111, 13757–13762 (2014).ADS 
CAS 
PubMed 
Article 

Google Scholar 
37.Elmqvist, T. et al. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494 (2003).Article 

Google Scholar 
38.Duperron, S. et al. New benthic cyanobacteria from Guadeloupe mangroves as producers of antimicrobials. Mar. Drugs https://doi.org/10.3390/md18010016 (2020).Article 

Google Scholar 
39.Bonaldo, R. M., Pires, M. M., Junior, P. R. G., Hoey, A. S. & Hay, M. E. Small marine protected areas in Fiji provide refuge for reef fish assemblages, feeding groups, and corals. PLoS ONE 12, e0170638 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
40.Ford, A. K. et al. Evaluation of coral reef management effectiveness using conventional versus resilience-based metrics. Ecol. Ind. 85, 308–317 (2018).Article 

Google Scholar 
41.Robinson, J. P. W. et al. Environmental conditions and herbivore biomass determine coral reef benthic community composition: implications for quantitative baselines. Coral Reefs 37, 1157–1168 (2018).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
42.Capper, A. et al. Palatability and chemical defences of benthic cyanobacteria to a suite of herbivores. J. Exp. Mar. Biol. Ecol. 474, 100–108 (2016).CAS 
Article 

Google Scholar 
43.Cruz-Rivera, E. & Paul, V. J. Chemical deterrence of a cyanobacterial metabolite against generalized and specialized grazers. J. Chem. Ecol. 33, 213–217 (2007).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
44.Bejarano, S. et al. The shape of success in a turbulent world: wave exposure filtering of coral reef herbivory. Funct. Ecol. 31, 1312–1324 (2017).Article 

Google Scholar 
45.Lefcheck, J. S. et al. Tropical fish diversity enhances coral reef functioning across multiple scales. Sci. Adv. 5, eaav6420 (2019).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
46.Nagle, D. G. & Paul, V. J. Chemical defense of a marine cyanobacterial bloom. J. Exp. Mar. Biol. Ecol. 225, 29–38 (1998).CAS 
Article 

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

Google Scholar 
48.Pratchett, M. S. et al. Effects of climate-induced coral bleaching on coral-reef fishes: ecological and economic consequences. Oceanogr. Mar. Biol. Ann. Rev. 46, 251–296 (2006).
Google Scholar 
49.Pratchett, M. S., Hoey, A. S., Wilson, S. K., Messmer, V. & Graham, N. A. J. Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3, 424–452 (2011).Article 

Google Scholar 
50.Potts, D. C. Suppression of coral populations by filamentous algae within damselfish territories. J. Exp. Mar. Biol. Ecol. 28, 207–216 (1977).Article 

Google Scholar 
51.Mumby, P. J. et al. Empirical relationships among resilience indicators on Micronesian reefs. Coral Reefs https://doi.org/10.1007/s00338-012-0966-0 (2012).Article 

Google Scholar 
52.Birrell, C. L., McCook, L. J. & Willis, B. L. Effects of algal turfs and sediment on coral settlement. Mar. Pollut. Bull. 51, 408–414 (2005).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
53.Wismer, S., Tebbett, S. B., Streit, R. P. & Bellwood, D. R. Spatial mismatch in fish and coral loss following 2016 mass coral bleaching. Sci. Total Environ. 650, 1487–1498 (2019).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
54.de la Morinière, E. C. et al. Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar. Ecol. Prog. Ser. 246, 279–289 (2003).ADS 
Article 

Google Scholar 
55.Komárek, J. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur. J. Phycol. 51, 346–353 (2016).Article 
CAS 

Google Scholar 
56.Xiao, X. et al. Use of high throughput sequencing and light microscopy show contrasting results in a study of phytoplankton occurrence in a freshwater environment. PLoS ONE 9, e106510 (2014).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
57.Palinska, K. A. & Surosz, W. Taxonomy of cyanobacteria: a contribution to consensus approach. Hydrobiologia 740, 1–11 (2014).Article 

Google Scholar 
58.Li, X. et al. Factors related to aggravated Cylindrospermopsis (cyanobacteria) bloom following sediment dredging in an eutrophic shallow lake. Environ. Sci. Ecotechnol. 2, 100014 (2020).Article 

Google Scholar 
59.Taton, A., Grubisic, S., Brambilla, E., De Wit, R. & Wilmotte, A. Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl. Environ. Microbiol. 69, 5157–5169 (2003).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Knight, R. et al. Best practices for analysing microbiomes. Nat. Rev. Microbiol. 16, 410–422 (2018).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
61.Kim, M., Oh, H.-S., Park, S.-C. & Chun, J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64, 346–351 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
62.Hoffmann, L. & Demoulin, V. Marine Cyanophyceae of Papua New Guinea. III. The genera Borzia and Oscillatoria. Bot. Mar. 36, 451–459 (1993).Article 

Google Scholar 
63.Engene, N. et al. Moorea producens gen. nov., sp. Nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int. J. Syst. Evol. Microbiol. 62, 1171–1178 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
64.Engene, N. et al. Five chemically rich species of tropical marine cyanobacteria of the genus Okeania gen. nov. (Oscillatoriales, Cyanoprokaryota). J. Phycol. 49, 1095–1106 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
65.Komarek, J., Kaštovský, J., Mares, J. & Johansen, J. R. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86, 295–335 (2014).
Google Scholar 
66.Wilmotte, A., Laughinghouse, H. D. I., Capelli, C., Rippka, R. & Salmaso, N. Taxonomic Identification of Cyanobacteria by a Polyphasic Approach. Molecular Tools for the Detection and Quantification of Toxigenic Cyanobacteria (Wiley, 2017).
Google Scholar 
67.Salmaso, N. et al. Diversity and cyclical seasonal transitions in the bacterial community in a large and deep perialpine lake. Microb. Ecol. 76, 125–143 (2018).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
68.Zubia, M. et al. Benthic cyanobacteria on coral reefs of Moorea Island (French Polynesia): diversity response to habitat quality. Hydrobiologia 843, 61–78 (2019).Article 

Google Scholar 
69.Bernard, C. et al. Appendix 2: Cyanobacteria Associated with the Production of Cyanotoxins. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis 501–525 (Wiley, 2017). https://doi.org/10.1002/9781119068761.app2.
Google Scholar 
70.Moritz, C. et al. Status and Trends of Coral Reefs in the Pacific (Global Coral Reef Monitoring Network, 2018).
Google Scholar 
71.Smith, J. E. et al. Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proc. R. Soc. B Biol. Sci. 283, 20151985 (2016).Article 
CAS 

Google Scholar 
72.Kelly, L. W. et al. Black reefs: iron-induced phase shifts on coral reefs. ISME J. 6, 638–649 (2012).CAS 
PubMed 
Article 

Google Scholar 
73.Bohnsack, J. A. & Bannerot, S. P. A stationary visual census technique for quantitatively assessing community structure of coral reef fishes. NOAA Technical Report NMFS 41, 21 (1986).74.Froese, R. & Pauly, D. FishBase. World Wide Web electronic publication. www.fishbase.orghttps://www.fishbase.org/.75.Heenan, A., Hoey, A. S., Williams, G. J. & Williams, I. D. Natural bounds on herbivorous coral reef fishes. Proc. R. Soc. B Biol. Sci. 283, 20161716 (2016).Article 

Google Scholar 
76.R Development Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2019).77.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 
78.Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.3.3.0. (2020). http://florianhartig.github.io/DHARMa/79.Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).
Google Scholar 
80.Komárek, J. & Anagnostidis, K. Cyanoprokaryota 2.Teil: Oscillatoriales (Elsevier, 2005).
Google Scholar 
81.Quince, C., Lanzen, A., Davenport, R. J. & Turnbaugh, P. J. Removing noise from pyrosequenced amplicons. BMC Bioinform. 12, 38 (2011).Article 

Google Scholar 
82.Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
83.Ramos, V., Morais, J. & Vasconcelos, V. M. A curated database of cyanobacterial strains relevant for modern taxonomy and phylogenetic studies. Sci. Data 4, 170054 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
84.Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20, 1160–1166 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
85.Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2: approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
86.Letunic, I. & Bork, P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucl. Acids Res. 47, W256–W259 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar  More

Confirmation of species, using DNA analysisBecause the DNA of our sphere samples matches that of adult squid identified as I. coindetii from Norwegian waters we infer that the spheres are from I. coindetii. Much has been written about taxonomic difficulties in Illex. The COI tree comprises four clades of Illex, one of which clearly pertains to Illex argentinus (Castellanos, 1960). There are three other described species: Illex coindetii, Illex illecebrosus (Lesueur, 1821), and I. oxygonius Roper, Lu & Mangold, 1969. We labelled our clades A, B, and C, to indicate their correspondence with the findings of Carlini et al.32, and assume that each pertains to one of the described species of Illex. Carlini was unable to match species to clades, but Clade A not only contains the adults identified in this project as I. coindetii, but also contains specimens from the Mediterranean (DQ373941). Since I. coindetii is the only species of Illex known from the Mediterranean, this is further confirmation of the identity of Clade A, and thus our spheres, as Illex coindetii.Using citizen science from roughly 200 divers secured observations of 90 spheres, including rare tissue samples of four of them, thus enabling a molecular approach towards the first confirmation of egg masses in situ as those of the broadtail shortfin squid, Illex coindetii. Illex coindetii was named in honour of Dr. Coindet from Geneva in 185137. It took 180 years from the description of the adult to identification of its egg mass in the wild. To our knowledge no whole egg mass of Illex spp. has previously been reported from the wild, except by Adolf Naef, who reported on live ommastrephid embryos and paralarvae from Naples, Italy2. The embryos were pulled out of a floating spawn or floating egg mass, or as he describes «Fig. 1 und 2 sind aus einem flottierenden Laich gezogene Larven von Ommatostrephiden». These illustrations were later identified as Illex coindetii by Boletzky et al.26, studying egg development of I. coindetii in the laboratory, claiming «The general characteristics of the embryonic developement observed by us match the figures given by Naef (1923 : plts 9–12) of an unidentified egg mass of a member of the Ommastrephidae (Naef 1921)». However, no drawing of the «laich» was provided.Challenges collecting in situ materialHuge gelatinous spheres from squid are difficult to study in situ. They are rarely reported, and hard to sample. We have collected 90 sphere observations from ~ 35 years back (~ 1985 to 2019), from an area stretching from the Mediterranean Sea north to the Norwegian Sea, which gives a good illustration on sphere findings of ~ 2.6 sphere observations per year. In addition, the spheres most likely have a short-life span. Life span of spheres spawned and reared in aquaria (between 40 and 120 cm in diameter) of Todarodes pacificus (Steenstrup, 1880) is 5–7 days, with the smallest disintegrating first38.Sphere shape and sizeGelatinous egg masses of cephalopods vary in size and form among species. Some egg masses are spherical, but there are also examples of oblong structures39,40,41. Sphere size may be up to 4 m in diameter1,5,42. Ringvold and Taite (op. cit.) collected information on a total of 27 spheres recorded in European waters varying from 0.3 to 2 m in diameter, as also for the additional spheres from this study. The four spheres in our study, confirmed to belong to I. coindetii, measured between 0.5 and 1 m in diameter.Egg mass of another ommastrephid squid, Todarodes sagittatus, has yet to be found in situ. The species is known to be larger than Illex species, and egg mass is also most probably larger. The largest spheres recorded in our study measured up to 2 m in diameter, but none of these were sampled for molecular analysis, nor were pictures taken. It is uncertain whether they could belong to other species e.g., Todaropsis eblanae (Ball, 1841), Todarodes sagittatus or Ommastrephes sp..Dark streak through coreAlmost 60% of the spheres had a dark streak through the center. This feature might be ink, one important characteristic of cephalopods, produced by most cephalopod orders. The ink sac with its ink glands produces black ink containing melanin43. During fertilization, sperm are released—as well as possibly some ink. Spheres with or without ink may be a result of spheres beeing at different maturity stages1, where spheres with ink are freshly spawned. After a while, when embryos starts developing, the whole sphere, including the streak, will start to disintegrate.Some of us speculate that one function of the streak through the center might serve as visual mimics e.g. of a large fish in order to scare off predators. Other possible functions discussed are also if the streak/structure can be caused by a sphere strengthening structure which is denser or having a higher optical density than the sourrounding structure. A disadvantage with the streak is that it might reveal the whole transparent sphere in the water, visible to e.g. scuba divers.Function of the gelatinous matrixObservations in captivity3,44 showed that species within the genus Illex produce gelatinous egg masses while swimming in open water. Gel functions as a buoyancy mechanism that prevents eggs from sinking, and complete density equilibration requires many days under most conditions44. Such a buoyancy mechanism keeps pelagically spawned eggs of Illex in areas where temperatures are most optimal for embryonic development. Optimal environmental conditions will likely have a positive effect on survival of both hatchlings and paralarvae. Despite consistency in where spawning areas are found, interannual variability has been recorded in the main recruitment areas, which could be related to e.g. mesoscale eddies and/or affecting post-hatching dispersal45.Huge spheres are formed of mucus produced by the nidamental glands, situated inside the mantle cavity of the female46,47. When fully developed, hatchlings emit an enzyme which starts to dissolve the mucus. Eggs and embryos from our four spheres were covered in sticky gelatinous mass, except for a few specimens (from Arendal, collected 7 August, and Søgne) laying in the petri dish outside the sticky gel, in the surrounding sea water following the tissue sample, and might have been old enough to start producing such enzymes.When at hatching, Illex coindetii eggs are about 2 mm long26,48, in line with other ommastrephids12. The longest of our embryos (from Arendal, collected 7 August) measured ~ 2 mm, a developed embryo with long proboscis, mantle about ½ of total body length, as well as chromatophores, large eyes and funnel visible (Fig. 3). It could possibly be a hatchling.Abiotic factors and locationsThe success and duration of embryonic development is related to water temperature. All observations available to date indicate that successful embryonic development for I. coindetii takes ca. 10–14 days at 15 °C; this temperature corresponds to the median temperature value reported for Mediterranean Sea midwater48. Boletzky et al.26 reports on a temperature minimum above 10 °C. Spheres in the Mediterranean were observed in temperatures ranging between 14 and 24 °C. Watermass temperature for one sphere with recently fertilized eggs (Ålesund sample, embryos stage ~ 3) from Norway was 8 °C. It was also observed north of the existing known distribution range for I. coindetii, in the Norwegian Sea, at 43 m depth. Most spheres from Norway were observed from July and August, in water mass 10–14 °C, with maximum temperature at 18 °C.It is unknown whether some of the observed spheres had drifted to water layers unsuitable for the development of the eggs, and, eventually, would have died due to unfavourable abiotic conditions (e.g. transport outside the optimal temperature- or depth range for that particular species), but most likely they were in an area where they would survive. Higher occurrence of sphere sightings from 2017 to 2019, could be a combination of higher abundance of these squid in the area as well as increased knowledge regarding our Citizen Science Sphere Project, and thereby increased reports of observations.Illex coindetii may be considered as an intermittent spawner with a spawning season extending throughout the year, reaching a peak in July–August18.Our sphere observations from all areas were made from March to October: The earliest sphere which can be documented (to month) in the North Sea to date was observed 27 May (2001), and the last sphere was reported on 20 October (2019), coinciding with a study on adult Illex condetii from the North Sea where the spawning season has been suggested to be between spring and autumn49. However, our data show a peak of sphere observations from July to September (all areas combined), from July to August in Norway and from August to September in the Mediterranean Sea. The two recordings from Galicia in Spain, and Seiano in Italy, were the earliest recordings of the year, observed 24 March (in 2017 and 2019, respectively). For all areas combined, no observations during wintertime (November to February) have been recorded.Embryonic development and consistencies of spheresWe collected tissue mass of four different spheres of I. coindetii, and embryos in each sphere were at different developmental stages, ~ 3 to 30, according to Sakai et al.36 based on I. argentinus. The sphere walls of the four spheres were also of different consistencies (Table 2); from Ålesund sphere with recently fertilized eggs and firm, transparent sphere wall to Søgne and Arendal spheres (the latter collected 7 August) with developed embryos and disintegrating sphere walls. The remains of the Arendal sphere was hanging as a long «scarf» in the water. Experienced divers, who previously had seen a few spherical spheres, recognized this disintegrating sphere.Function of spheresOmmastrephidae fecundity is extremely high, and a single sphere may contain thousands to several hundred thousands of eggs41,50,51,52. The function of the spheres is protection and transport of the offspring by sea currents for paralarval dispersal. Inside these gelatinous structures, the eggs and newly hatched paralarvae are protected from predation by e.g. fish, parasite infection and infestation by crustaceans and protozoans during a first relative short period of their lives5,51. Bottom trawlers operate in spawning areas of squids, exposing them to a risk of egg loss, as also for our fisherman at Askøy, Norway, who caught a sphere in his trawl1,5.Scientific cruises and fisheryThe Institute for Marine Research in Norway started identification of cephalopods on their regular scientific cruises in 2013, but no Illex coindetii was recorded that year. However, data show increasing catches from 2014 to 2019 (unpublished). No spheres are reported from Norway in 2013, but between 1995 to 2010, and from 2015 to 2019, observations were made. Most observations are between 2017 and 2019, indicating more frequent squid visits/spawnings. This coincides with more frequent sphere observations from 2017 to 2019.The broadtail shortfin squid, Illex coindetii, is probably the most widespread species found on both sides of the Atlantic and throughout the Mediterranean Sea12. In the NE Atlantic, it has been reported from Oslofjorden, Norway (59°N);53 and the Firth of Forth, east Scotland54, southwards along the European and African coasts to Namibia, including Hollam’s Bird Island (24°S) and Cape Frio (18°S)55. For example, I. coindetii is periodically very abundant in coastal waters of the eastern North Atlantic off Scotland, Ireland and Spain, where it supports opportunistic fisheries. However, the oceanographic and biological factors that drive this phenomenon, are still unknown12.Illex coindetii is widely distributed throughout the Mediterranean Sea11, where it is caught commercially mostly by Italian trawlers, usually as a by-catch, but also by recreational fishing, by means of squid jigging. Annual Italian landings during the last five years have varied between two and three thousand tonnes, but with historical landings reaching numbers of more than eight thousand tonnes during the 1980s and 1990s (FAO 2019)15.In the North Sea, studies show that inshore squids (Alloteuthis subulata (Lamarck, 1798) and Loligo forbesii Steenstrup, 1856) are more abundant than short-finned squid (Illex coindetii, Todaropsis eblanae and Todarodes sagittatus), and I. coindetii is among the rarest ommastrephid species caught49,56. However, two recent studies (1) on summer spawning stock of Illex coindetii in the North Sea57 and (2) I. coindetii recorded from the brackish Baltic Sea58 suggest more frequent visits to this area. Reports on Illex coindetii from Norwegian waters are scarce, but it has been reported from Oslofjorden53, and recently as by-catch from Stavanger area, and by divers from Oslofjorden and Bergen. More