Philippa Kaur

1.Jaramillo-Villa, U., Maldonado-Ocampo, J. A. & Escobar, F. Altitudinal variation in fish assemblage diversity in streams of the central Andes of Colombia. J. Fish Biol. 76, 2401–2417 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Mercado-silva, N., Lyons, J., Díaz-Pardo, E., Navarrete, S. & Gutiérrez-Hernández, A. Environmental factors associated with fish assemblage patterns in a high gradient river of the Gulf of Mexico slope. Revista Mexicana de Biodiversidad 83, 117–128 (2012).Article 

Google Scholar 
3.Cheng, D. et al. Quantifying the distribution and diversity of fish species along elevational gradients in the Weihe River Basin, Northwest China. Sustainability 11, 6177 (2019).Article 

Google Scholar 
4.Lorion, C. M., Kennedy, B. P. & Braatne, J. H. Altitudinal gradients in stream fish diversity and the prevalence of diadromy in the Sixaola River basin, Costa Rica. Environ. Biol. Fishes 91, 487–499 (2011).Article 

Google Scholar 
5.Li, J. et al. Spatial and temporal variation of fish assemblages and their associations to habitat variables in a mountain stream of north Tiaoxi River, China. Environ. Biol. Fishes 93, 403–417 (2012).Article 

Google Scholar 
6.Súarez, Y. R. et al. Patterns of species richness and composition of fish assemblages in streams of the Ivinhema River basin, Upper Paraná River. Acta Limnol. Bras. 23, 177–188 (2011).Article 

Google Scholar 
7.Vieira, T. B. & Tejerina-Garro, F. L. Relationships between environmental conditions and fish assemblages in tropical Savanna headwater streams. Sci. Rep. 10, 1–12 (2020).Article 
CAS 

Google Scholar 
8.Pokharel, K. K., Basnet, K. B., Majupuria, T. C. & Baniya, C. B. Correlations between fish assemblage structure and environmental variables of the Seti Gandaki River Basin, Nepal. J. Freshw. Ecol. 33, 31–43 (2018).CAS 
Article 

Google Scholar 
9.Carvajal-Quintero, J. D. et al. Variation in freshwater fish assemblages along a regional elevation gradient in the northern Andes, Colombia. Ecol. Evol. 5, 2608–2620 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
10.Li, J. et al. Climate and history explain the species richness peak at mid-elevation for Schizothorax fishes (Cypriniformes: Cyprinidae) distributed in the Tibetan Plateau and its adjacent regions. Glob. Ecol. Biogeogr. 18, 264–272 (2009).Article 

Google Scholar 
11.Fu, C., Wu, J., Chen, J., Wu, Q. & Lei, G. Freshwater fish biodiversity in the Yangtze River basin of China: Patterns, threats and conservation. Biodivers. Conserv. 12, 1649–1685 (2003).Article 

Google Scholar 
12.Orrego, R., Adams, S. M., Barra, R., Chiang, G. & Gavilan, J. F. Patterns of fish community composition along a river affected by agricultural and urban disturbance in south-central Chile. Hydrobiologia 620, 35–46 (2009).Article 

Google Scholar 
13.Nyanti, L. et al. Acidification tolerance of Barbonymus schwanenfeldii (Bleeker, 1854) and Oreochromis niloticus (Linnaeus, 1758)—Implication of fish size. AACL Bioflux 10, 746–753 (2017).
Google Scholar 
14.Nyanti, L. et al. Effects of water temperature, dissolved oxygen and total suspended solids on juvenile Barbonymus schwanenfeldii (Bleeker, 1854) and Oreochromis niloticus (Linnaeus, 1758). AACL Bioflux 11, 394–406 (2018).
Google Scholar 
15.Ling, T. Y. et al. Assessment of the water and sediment quality of tropical forest streams in upper reaches of the Baleh River, Sarawak, Malaysia, subjected to logging activities. J. Chem. 2016, 1–13 (2016).CAS 

Google Scholar 
16.Davies, P. & Nelson, M. Relationships between riparian buffer widths and the effects of logging on stream habitat, invertebrate community composition and fish abundance. Mar. Freshw. Res. 45, 1289–1305 (1994).Article 

Google Scholar 
17.Ikhwanuddin, M., Amal, M., Shohaimi, S., Hasan, H. & Jamil, N. Environmental influences on fish assemblages of the Upper Sungai Pelus, Kuala Kangsar, Perak, Malaysia. Sains Malaysiana 45, 1487–1495 (2016).CAS 

Google Scholar 
18.Zainuddin, Z., Jamal, P. & Akbar, I. Modeling the effect of dam construction and operation towards downstream water quality of Sg. Tawau and Batang Baleh. World J. Appl. Environ. Chem. 1, 57–66 (2012).
Google Scholar 
19.Nyanti, L., Ling, T. & Muan, T. Water quality of Bakun Hydroelectric Dam Reservoir, Sarawak, Malaysia, during the construction of Murum Dam. ESTEEM Acad. J. 11, 81–88 (2015).
Google Scholar 
20.Ling, T. Y. et al. Changes in water and sediment quality of a river being impounded and differences among functional zones of the new large tropical hydroelectric reservoir. Pol. J. Environ. Stud. 28, 4271–4285 (2019).CAS 
Article 

Google Scholar 
21.Osman, N. B., Othman, H. T., Karim, R. A. & Mazlan, M. A. F. Biomass in Malaysia: Forestry-based residues. Int. J. Biomass Renew. 3, 7–14 (2014).
Google Scholar 
22.Inger, R. F. & Chin, P. K. Freshwater Fish of North Borneo (Natural History Publications, 2002).
Google Scholar 
23.Mohsin, A. K. M. & Ambak, M. A. Freshwater fishes of Peninsular Malaysia (Universiti Pertanian Malaysia, 1983).
Google Scholar 
24.Kottelat, M. The fishes of the inland waters of Southeast Asia: A catalogue and core bibliography of the fishes known to occur in freshwaters, mangroves and estuaries. Raffles Bull. Zool. 27, 1–663 (2013).
Google Scholar 
25.Kottelat, M. Conspectus Cobitidum: An inventory of the loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull. Zool. 26, 1–199 (2012).
Google Scholar 
26.Kottelat, M. & Tan, H. H. A synopsis of the genus Lobocheilos in Java, Sumatra and Borneo, with descriptions of six new species (Teleostei: Cyprinidae). Ichthyol. Explor. Freshw. 19, 27–58 (2008).
Google Scholar 
27.Froese, R. & Pauly, D. FishBase. World Wide Web electronic publication. https://www.fishbase.se/search.php (2019).28.van der Laan, R., Fricke, R. & Eschmeyer, W. N. Eschmeyer’s Catalog of Fishes: Classification. http://www.calacademy.org/scientists/catalog-of-fishes-classification/ (2020).29.Shannon, C. E. & Weaver, W. The Mathematical Theory of Communication (The University of Illinois Press, 1964).MATH 

Google Scholar 
30.Margalef, R. Perspectives in Ecological Theory (University of Chicago Press, 1968).
Google Scholar 
31.Pielou, E. C. Species diversity and pattern diversity in the study of ecological succession. J. Theor. Biol. 10, 370–383 (1966).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
32.Ter Braak, C. J. F. Canonical correspondence analysis: A new eigenvector technique for multivariate direct gradient analysis. Ecology 67, 1167–1179 (1986).Article 

Google Scholar 
33.Ter Braak, C. J. F. & Verdonschot, P. F. M. Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat. Sci. 57, 255–289 (1995).Article 

Google Scholar 
34.Ward-Campbell, B. M. S., Beamish, F. W. H. & Kongchaiya, C. Morphological characteristics in relation to diet in five coexisting Thai fish species. J. Fish Biol. 67, 1266–1279 (2005).Article 

Google Scholar 
35.Beamish, F. W. H., Sa-ardrit, P. & Tongnunui, S. Habitat characteristics of the cyprinidae in small rivers in Central Thailand. Environ. Biol. Fishes 76, 237–253 (2006).Article 

Google Scholar 
36.Muchlisin, Z. A. & Siti Azizah, M. N. Diversity and distribution of freshwater fishes in Aceh water, northern Sumatra, Indonesia. Int. J. Zool. Res. 5, 62–79 (2009).Article 

Google Scholar 
37.Rashid, Z. A., Asmuni, M. & Amal, M. N. A. Fish diversity of Tembeling and Pahang rivers, Pahang, Malaysia. Check List 11, 1–6 (2015).Article 

Google Scholar 
38.Suvarnaraksha, A., Lek, S., Lek-Ang, S. & Jutagate, T. Fish diversity and assemblage patterns along the longitudinal gradient of a tropical river in the Indo-Burma hotspot region (Ping-Wang River Basin, Thailand). Hydrobiologia 694, 153–169 (2012).CAS 
Article 

Google Scholar 
39.Kottelat, M. Conspectus cobitidum: An inventory of the loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull. Zool. 26, 1–199 (2012).
Google Scholar 
40.Tan, H. H. The Borneo suckers. Revision of the Torrent Loaches of Borneo (Balitoridae: Gastromyzon, Neogastromyzon) (Natural History Publications, 2006).
Google Scholar 
41.Beamish, F. W. H., Sa-Ardrit, P. & Cheevaporn, V. Habitat and abundance of Balitoridae in small rivers of central Thailand. J. Fish Biol. 72, 2467–2484 (2008).Article 

Google Scholar 
42.Ahmad, A., Nek, S. A. R. T. & Ambak, M. A. Preliminary study on fish diversity of Ulu Tungud, Meliau range, Sandakan, Sabah. J. Sustain. Sci. Manag. 1, 21–26 (2006).
Google Scholar 
43.Odum, E. P. & Barret, G. W. Fundamental of Ecology (Cengage Learning, Inc, 2004).
Google Scholar 
44.Magurran, A. E. Ecological Diversity and Its Measurement (Princeton University Press, 1988).Book 

Google Scholar 
45.Au, D. W. T. et al. Chronic effects of suspended solids on gill structure, osmoregulation, growth, and triiodothyronine in juvenile green grouper Epinephelus coioides. Mar. Ecol. Prog. Ser. 266, 255–264 (2004).ADS 
CAS 
Article 

Google Scholar 
46.Kimbell, H. S. & Morrell, L. J. Turbidity influences individual and group level responses to predation in guppies, Poecilia reticulata. Anim. Behav. 103, 179–185 (2015).Article 

Google Scholar 
47.Li, W. et al. Effects of turbidity and light intensity on foraging success of juvenile mandarin fish Siniperca chuatsi (Basilewsky). Environ. Biol. Fishes 96, 995–1002 (2013).Article 

Google Scholar 
48.Kukula, K. & Bylak, A. Synergistic impacts of sediment generation and hydrotechnical structures related to forestry on stream fish communities. Sci. Total Environ. 737, 139751 (2020).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
49.Krause, K. P., Wu, C. L., Chu, M. L. & Knouft, J. H. Fish assemblage–environment relationships suggest differential trophic responses to heavy metal contamination. Freshw. Biol. 64, 632–642 (2019).CAS 
Article 

Google Scholar 
50.Askeyev, A. et al. River fish assemblages along an elevation gradient in the eastern extremity of Europe. Environ. Biol. Fishes 100, 585–596 (2017).Article 

Google Scholar 
51.Zamani Faradonbe, M. & Eagderi, S. Fish assemblages as influenced by environmental factors in Taleghan River (the Caspian Sea basin, Alborz Province, Iran). Caspian J. Environ. Sci. 13, 363–371 (2015).
Google Scholar 
52.Bolner, K. C. S., Copatti, C. E., Rosso, F. L., Loro, V. L. & Baldisserotto, B. Water pH and metabolic parameters in silver catfish (Rhamdia quelen). Biochem. Syst. Ecol. 56, 202–208 (2014).CAS 
Article 

Google Scholar 
53.Abbink, W. et al. The effect of temperature and pH on the growth and physiological response of juvenile yellowtail kingfish Seriola lalandi in recirculating aquaculture systems. Aquaculture 330–333, 130–135 (2012).Article 
CAS 

Google Scholar 
54.Paller, V. G. V., Corpuz, M. N. C. & Ocampo, P. P. Diversity and distribution of freshwater fish assemblages in Tayabas River, Quezon (Philippines). Philip. J. Sci. 142, 55–67 (2013).
Google Scholar 
55.Jeppesen, R. et al. Effects of hypoxia on fish survival and oyster growth in a highly eutrophic estuary. Estuaries Coasts 41, 89–98 (2018).CAS 
Article 

Google Scholar 
56.Rosso, J. J. & Quirós, R. Patterns in fish species composition and assemblage structure in the upper Salado river lakes, Pampa Plain, Argentina. Neotrop. Ichthyol. 8, 135–144 (2010).Article 

Google Scholar 
57.Batzer, D. P., Jackson, C. R. & Mosner, M. Influences of riparian logging on plants and invertebrates in small, depressional wetlands of georgia, U.S.A.. Hydrobiologia 441, 123–132 (2000).Article 

Google Scholar 
58.Cheimonopoulou, M. T., Bobori, D. C., Theocharopoulos, I. & Lazaridou, M. Assessing ecological water quality with macroinvertebrates and fish: A case study from a small mediterranean river. Environ. Manag. 47, 279–290 (2011).ADS 
Article 

Google Scholar 
59.Roberts, T. R. The Freshwater Fishes of Western Borneo (Kalimantan Barat, Indonesia) (California Academy of Science, 1989).
Google Scholar 
60.Tan, H. H. & Leh, C. U. M. Three new species of Gastromyzon (Teleostei: Balitoridae) from southern Sarawak. Zootaxa 19, 1–19 (2006).
Google Scholar 
61.Tan, H. H. & Martin-Smith, K. M. Two new species of Gastromyzon (Teleostei: Balitoridae) from the Kuamut headwaters, Kinabatangan basin, Sabah, Malaysia. Raffles Bull. Zool. 46, 361–371 (1998).
Google Scholar  More

Male snakes generally approached the diver, whereas few females did so (approaches recorded in 39 of 58 encounters with males vs. 35 of 100 encounters with females; Fisher Exact Test P  More

Active ingredients detected in bee collected pollenAll 188 pollen samples had at least 12 active ingredients detected in each sample, with a maximum of 31 AIs and an average of 22.0 ± 0.3 per sample. Over both years, 80 of the 259 screened pesticide active ingredients were detected in the pollen. These included 28 fungicides, 26 insecticides, 21 herbicides, two miticides, and one rodenticide. We also detected one synthetic antioxidant and one pesticide synergist (Table S1). We detected approximately twice as many AIs in pollen collected by honey bees (68 AIs) in 2019 than in pollen collected by bumble bees (32). All AIs detected in pollen from bumble bees were also collected by honey bees in either 2018 or 2019. Honey bee collected pollen also had significantly more AIs on average detected at each site (35.0 ± 0.9 S.E. AIs per site) compared to bumble bees (18.6 ± 0.6) in 2019 (R2m = 0.73; X2 = 68.2, df = 1, p  More

1.Zielińska, K. M., Kiedrzynski, M., Grzyl, A. & Rewicz, A. Forest roadsides harbour less competitive habitats for a relict mountain plant (Pulsatilla vernalis) in lowlands. Sci. Rep. https://doi.org/10.1038/srep31913 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
2.Zielińska, K. M., Kiedrzynski, M., Grzyl, A. & Tomczyk, P. P. Anthropogenic sites maintain the last individuals during the rapid decline of the lowland refugium of the alpine-arctic plant Pulsatilla vernalis (L.) Mill. Pak. J. Bot. 50, 211–215 (2018).3.Grzyl, A. & Ronikier, M. Pulsatilla vernalis (Ranunculaceae) in the Polish lowlands: Current population resources of a declining species. Pol. Bot. J. 56, 185–194 (2011).
Google Scholar 
4.Åström, S. & Stridh, B. The present status of Pulsatilla vernalis in Sweden. Sven. Bot. Tidskr. 97, 117–126 (2003).
Google Scholar 
5.Chappuis, E. Pulsatilla vernalis. The IUCN Red List of Threatened Species 2014: e.T55730086A55730098. (2014). https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T55730086A55730098.en. Downloaded on 02 December 2020 >.6.Ronikier, M. et al. Phylogeography of Pulsatilla vernalis (L.) Mill. (Ranunculaceae): Chloroplast DNA reveals two evolutionary lineages across central Europe and Scandinavia. J. Biogeogr. 35, 1650–1664. https://doi.org/10.1111/j.1365-2699.2008.01907.x (2008).7.Kiedrzyński, M., Zielińska, K. M., Kiedrzyńska, E. & Rewicz, A. Refugial debate: On small sites according to their function and capacity. Evol. Ecol. 31, 815–827. https://doi.org/10.1007/s10682-017-9913-4 (2017).Article 

Google Scholar 
8.Betz, C., Scheuerer, M. & Reisch, C. Population reinforcement—A glimmer of hope for the conservation of the highly endangered Spring Pasque flower (Pulsatilla vernalis). Biol. Conserv. 168, 161–167. https://doi.org/10.1016/j.biocon.2013.10.004 (2013).Article 

Google Scholar 
9.Nawrocka-Grześkowiak, U. & Frydel, K. Spring pasque-flower (Pulsatilla vernalis (L.) Miller) localities in the Kaliska Forest District. Zarządzanie Ochroną Przyrody w Lasach 6, 77–84 (2012).10.Gutterman, Y. In Seeds: The Ecology of Regeneration in Plant Communities (ed M. Fenner) 59–84 (CAB International, 2000).11.Luzuriaga, A. L., Escudero, A. & Perez-Garcia, F. Environmental maternal effects on seed morphology and germination in Sinapis arvensis (Cruciferae). Weed Res. 46, 163–174. https://doi.org/10.1111/j.1365-3180.2006.00496.x (2006).Article 

Google Scholar 
12.Rao, N. K., Dulloo, M. E. & Engels, J. M. M. A review of factors that influence the production of quality seed for long-term conservation in genebanks. Genet. Resour. Crop Evol. 64, 1061–1074. https://doi.org/10.1007/s10722-016-0425-9 (2017).CAS 
Article 

Google Scholar 
13.Doniak, M., Barciszewska, M. Z., Kaźmierczak, J. & Kaźmierczak, A. The crucial elements of the ‘last step’ of programmed cell death induced by kinetin in root cortex of V. faba ssp. minor seedlings. Plant Cell Rep. 33, 2063–2076. https://doi.org/10.1007/s00299-014-1681-9 (2014).14.Doniak, M., Byczkowska, A. & Kaźmierczak, A. Kinetin-induced programmed death of cortex cells is mediated by ethylene and calcium ions in roots of Vicia faba ssp minor. Plant Growth Regul. 78, 335–343. https://doi.org/10.1007/s10725-015-0096-0 (2016).CAS 
Article 

Google Scholar 
15.Doniak, M., Kaźmierczak, A., Byczkowska, A. & Glińska, S. Reactive oxygen species and sugars may be the messengers in kinetin-induced death of field bean root cortex cells. Biol. Plant. 61, 178–186. https://doi.org/10.1007/s10535-016-0654-y (2017).CAS 
Article 

Google Scholar 
16.Tudela-Isanta, M. et al. Habitat-related seed germination traits in alpine habitats. Ecol. Evol. 8, 150–161. https://doi.org/10.1002/ece3.3539 (2018).Article 
PubMed 

Google Scholar 
17.Baskin, J. M. & Baskin, C. C. A classification system for seed dormancy. Seed Sci. Res. 14, 1–16. https://doi.org/10.1079/ssr2003150 (2004).ADS 
Article 

Google Scholar 
18.Finch-Savage, W. E. & Leubner-Metzger, G. Seed dormancy and the control of germination. New Phytol. 171, 501–523. https://doi.org/10.1111/j.1469-8137.2006.01787.x (2006).CAS 
Article 
PubMed 

Google Scholar 
19.Latrasse, D., Benhamed, M., Bergounioux, C., Raynaud, C. & Delarue, M. Plant programmed cell death from a chromatin point of view. J. Exp. Bot. 20, 5887–5900 (2016).Article 

Google Scholar 
20.Baskin, J. M., Baskin, C. C. & Li, X. Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biol. 15, 139–152. https://doi.org/10.1046/j.1442-1984.2000.00034.x (2000).Article 

Google Scholar 
21.Grzyl, A. Biology and Ecology of Isolated Populations of Pulsatilla vernalis (L.) Mill. on the Eastern Limits of its RANGE in Poland. (PhD thesis. University of Lodz, Department of Geobotany and Plant Ecology, 2012).22.Grzyl, A., Kiedrzynski, M., Zielinska, K. M. & Rewicz, A. The relationship between climatic conditions and generative reproduction of a lowland population of Pulsatilla vernalis: The last breath of a relict plant or a fluctuating cycle of regeneration?. Plant Ecol. 215, 457–466. https://doi.org/10.1007/s11258-014-0316-0 (2014).Article 

Google Scholar 
23.Oostermeijer, J. G. B., Vaneijck, M. W. & Dennijs, J. C. M. Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae). Oecologia 97, 289–296. https://doi.org/10.1007/bf00317317 (1994).ADS 
CAS 
Article 
PubMed 

Google Scholar 
24.Ouborg, N. J. & Vantreuren, R. Variation in fitness-related characters among small and large populations of Salvia pratensis. J. Ecol. 83, 369–380. https://doi.org/10.2307/2261591 (1995).Article 

Google Scholar 
25.Fischer, M. & Matthies, D. RAPD variation in relation to population size and plant fitness in the rare Gentianella germanica (Gentianaceae). Am. J. Bot. 85, 811–819. https://doi.org/10.2307/2446416 (1998).CAS 
Article 
PubMed 

Google Scholar 
26.Frankham, R., Ballou, J. D. & Briscoe, D. A. Introduction to Conservation Genetics. (Cambridge University Press, 2002).27.Hensen, I., Oberprieler, C. & Wesche, K. Genetic structure, population size, and seed production of Pulsatilla vulgaris Mill. (Ranunculaceae) in Central Germany. Flora 200, 3–14. https://doi.org/10.1016/j.flora.2004.05.001 (2005).28.Jakobsson, A. & Eriksson, O. A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88, 494–502. https://doi.org/10.1034/j.1600-0706.2000.880304.x (2000).Article 

Google Scholar 
29.Melser, C. & Klinkhamer, P. G. L. Selective seed abortion increases offspring survival in Cynoglossum officinale (Boraginaceae). Am. J. Bot. 88, 1033–1040. https://doi.org/10.2307/2657085 (2001).CAS 
Article 
PubMed 

Google Scholar 
30.Meyer, K. M., Soldaat, L. L., Auge, H. & Thulke, H. H. Adaptive and selective seed abortion reveals complex conditional decision making in plants. Am. Nat. 183, 376–383. https://doi.org/10.1086/675063 (2014).Article 
PubMed 

Google Scholar 
31.Bochenková, M., Hejcman, M. & Karlík, P. Effect of plant community on recruitment of Pulsatilla pratensis in dry grassland. Sci. Agric. Bohem. 2012, 127–133. https://doi.org/10.7160/sab.2012.430402 (2012).Article 

Google Scholar 
32.Ghazoul, J. & Satake, A. Nonviable seed set enhances plant fitness: The sacrificial sibling hypothesis. Ecology 90, 369–377. https://doi.org/10.1890/07-1436.1 (2009).Article 
PubMed 

Google Scholar 
33.Laitinen, P. The Effects of Forest Fires on the Persistence of Pulsatilla vernalis (L.) Mill. edn, (Ms. thesis, University of Jyväskylä, Faculty of Mathematics and Science, Department of Biological and Environmental Science, 2008) [in Finnish with an English abstract].34.Skalická, R., Karlík, P., Hejcman, M. & Bochenková, M. In 17th Symposium of the European Grassland Federation. 388–390.35.Arathi, H. S., Ganeshaiah, K. N., Shaanker, R. U. & Hedge, S. G. Seed abortion in Pongamia pinnata (Fabaceae). Am. J. Bot. 86, 659–662. https://doi.org/10.2307/2656574 (1999).CAS 
Article 
PubMed 

Google Scholar 
36.Brookes, R. H., Jesson, L. K. & Burd, M. A test of simultaneous resource and pollen limitation in Stylidium armeria. New Phytol. 179, 557–565. https://doi.org/10.1111/j.1469-8137.2008.02453.x (2008).Article 
PubMed 

Google Scholar 
37.Yang, C. F., Sun, S. G. & Guo, Y. H. Resource limitation and pollen source (self and outcross) affecting seed production in two louseworts, Pedicularis siphonantha and P. longiflora (Orobanchaceae). Bot. J. Linn. Soc. 147, 83–89. https://doi.org/10.1111/j.1095-8339.2005.00363.x (2005).38.Cendán, C., Sampedro, L. & Zas, R. The maternal environment determines the timing of germination in Pinus pinaster. Environ. Exp. Bot. 94, 66–72. https://doi.org/10.1016/j.envexpbot.2011.11.022 (2013).Article 

Google Scholar 
39.Li, R. et al. Effects of cultivar and maternal environment on seed quality in Vicia sativa. Front. Plant Sci. 8. https://doi.org/10.3389/fpls.2017.01411 (2017).40.Valencia-Diaz, S. & Montaña, C. Temporal variability in the maternal environment and its effect on seed size and seed quality in Flourensia cernua DC. (Asteraceae). J. Arid Environ. 63, 686–695. https://doi.org/10.1016/j.jaridenv.2005.03.024 (2005).41.Chinnusamy, V., Gong, Z. Z. & Zhu, J. K. Abscisic acid-mediated epigenetic processes in plant development and stress responses. J. Integr. Plant Biol. 50, 1187–1195. https://doi.org/10.1111/j.1744-7909.2008.00727.x (2008).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
42.Butuzova, O. G. Peculiarities of seed formation in Pulsatilla vulgaris and Helleborus niger (Ranunculaceae) with embryo postdevelopment. Botanicheskii Zhurnal (St. Petersburg) 103, 313—330 (2018) [in Russian].43.Duncan, C., Schultz, N., Lewandrowski, W., Good, M. K. & Cook, S. Lower dormancy with rapid germination is an important strategy for seeds in an arid zone with unpredictable rainfall. PLoS ONE 14. https://doi.org/10.1371/journal.pone.0218421 (2019).44.Gremer, J. R., Kimball, S. & Venable, D. L. Within and among year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment. Ecol. Lett. 19, 1209–1218. https://doi.org/10.1111/ele.12655 (2016).Article 
PubMed 

Google Scholar 
45.Venable, D. L. Bet hedging in a guild of desert annuals. Ecology 88, 1086–1090. https://doi.org/10.1890/06-1495 (2007).Article 
PubMed 

Google Scholar 
46.Evans, M. E. K. & Dennehy, J. J. Germ banking: Bet-hedging and variable release from egg and seed dormancy. Q. R. Biol. 80, 431–451. https://doi.org/10.1086/498282 (2005).Article 

Google Scholar 
47.Goldberg, R. B., de Paiva, G. & Yadegari, R. Plant embryogenesis – zygote to seed. Science 266, 605–614. https://doi.org/10.1126/science.266.5185.605 (1994).ADS 
CAS 
Article 
PubMed 

Google Scholar 
48.Lester, R. N. & Kang, J. H. Embryo and endosperm function and failure in Solanum species and hybrids. Ann. Bot. 82, 445–453. https://doi.org/10.1006/anbo.1998.0695 (1998).Article 

Google Scholar 
49.Lopes, M. A. & Larkins, B. A. Endosperm origin, development, and function. Plant Cell 5, 1383–1399. https://doi.org/10.1105/tpc.5.10.1383 (1993).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
50.Yan, D. W., Duermeyer, L., Leoveanu, C. & Nambara, E. The functions of the endosperm during seed germination. Plant Cell Physiol. 55, 1521–1533. https://doi.org/10.1093/pcp/pcu089 (2014).CAS 
Article 
PubMed 

Google Scholar 
51.Willis, C. G. et al. The evolution of seed dormancy: Environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytol. 203, 300–309. https://doi.org/10.1111/nph.12782 (2014).Article 
PubMed 

Google Scholar 
52.Poisot, T., Bever, J. D., Nemri, A., Thrall, P. H. & Hochberg, M. E. A conceptual framework for the evolution of ecological specialisation. Ecol. Lett. 14, 841–851. https://doi.org/10.1111/j.1461-0248.2011.01645.x (2011).Article 
PubMed 
PubMed Central 

Google Scholar 
53.Pfeifer, E., Holderegger, R., Matthies, D. & Rutishauser, R. Investigation on the population biology of a flagship species of dry meadows: Pulsatilla vulgaris Mill. in north-eastern Switzerland. Bot. Helvet. 112, 153–171 (2002).54.Gargiulo, R. et al. Conservation of the threatened species, Pulsatilla vulgaris Mill. (Pasqueflower), is aided by reproductive system and polyploidy. J. Hered. 110, 618–628. https://doi.org/10.1093/jhered/esz035 (2019).55.Seglias, A. E., Williams, E., Bilge, A. & Kramer, A. T. Phylogeny and source climate impact seed dormancy and germination of restoration-relevant forb species. PLoS ONE 13. https://doi.org/10.1371/journal.pone.0191931 (2018).56.Byczkowska, A., Kunikowska, A. & Kaźmierczak, A. Determination of ACC-induced cell-programmed death in roots of Vicia faba ssp. minor seedlings by acridine orange and ethidium bromide staining. Protoplasma 250, 121–128. https://doi.org/10.1007/s00709-012-0383-9 (2013).57.Dray, S. & Dufour, A. B. The ade4 package: Implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20. https://doi.org/10.18637/jss.v022.i04 (2007).58.Kassambara, A. & Mundt, F. factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 1.0.7. https://CRAN.R-project.org/package=factoextra (2020).59.Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).Book 

Google Scholar 
60.Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan (2019).61.Fox, F. & Weisberg, S. An {R} Companion to Applied Regression, Third Edition. (Sage, 2019). https://socialsciences.mcmaster.ca/jfox/Books/Companion/. More

1.Schipper, J. et al. The status of the world’s land and marine mammals: Diversity, threat, and knowledge. Science 322, 225–230 (2008).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Cushman, S. A. Effects of habitat loss and fragmentation on amphibians: A review and prospectus. Biol. Conserv. 128, 231–240 (2006).Article 

Google Scholar 
3.Díaz, S. et al. Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366, 6471 (2019).Article 
CAS 

Google Scholar 
4.Geary, W. L., Nimmo, D. G., Doherty, T. S., Ritchie, E. G. & Tulloch, A. I. T. Threat webs: Reframing the co-occurrence and interactions of threats to biodiversity. J. Appl. Ecol. 56, 1992–1997 (2019).
Google Scholar 
5.Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Johnson, C. N. et al. Biodiversity losses and conservation responses in the Anthropocene. Science 356, 270–275 (2017).ADS 
CAS 
PubMed 
Article 

Google Scholar 
7.Di Prisco, G. et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and Health. Proc. Natl. Acad. Sci. USA. 113, 3203–3208 (2016).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
8.Grant, E. H. C. et al. Identifying management-relevant research priorities for responding to disease-associated amphibian declines. Glob. Ecol. Conserv. 16, 00441 (2018).
Google Scholar 
9.Schindler, D. W. The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can. J. Fish. Aquat. Sci. 58, 18–29 (2001).Article 

Google Scholar 
10.Cumulative Effects in Wildlife Management: Impact Mitigation. https://doi.org/10.1017/CBO9781107415324.004 (CRC Press, 2011). 11.Frid, A. & Dill, L. Human-caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 6, 11 (2002).
Google Scholar 
12.Rolland, R. M., Hunt, K. E., Kraus, S. D. & Wasser, S. K. Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. Gen. Comp. Endocrinol. 142, 308–317 (2005).CAS 
PubMed 
Article 

Google Scholar 
13.Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. Measuring stress in wildlife: Techniques for quantifying glucocorticoids. Oecologia 166, 869–887 (2011).ADS 
PubMed 
Article 

Google Scholar 
14.Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).PubMed 
Article 

Google Scholar 
15.Beal, A., Rodriguez-Casariego, J., Rivera-Casas, C., Suarez-Ulloa, V. & Eirin-Lopez, J. M. Environmental epigenomics and its applications in marine organisms. in Population Genomics: Marine Organisms (eds. Oleksiak, M. F. & Rajora, O. P.) 325–359. https://doi.org/10.1007/13836_2018_28 (Springer, 2018). 16.Eirin-Lopez, J. M. & Putnam, H. M. Marine environmental epigenetics. Ann. Rev. Mar. Sci. 11, 335–368 (2019).PubMed 
Article 

Google Scholar 
17.Laird, P. W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 3, 253–266 (2003).CAS 
PubMed 
Article 

Google Scholar 
18.Bird, A. P. CpG-rich islands and the function of DNA methylation. Nature 321, 209–213 (1986).ADS 
CAS 
PubMed 
Article 

Google Scholar 
19.Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295–304 (2009).CAS 
PubMed 
Article 

Google Scholar 
20.Matosin, N., Cruceanu, C. & Binder, E. B. Preclinical and clinical evidence of DNA methylation changes in response to trauma and chronic stress. Chronic Stress 1, 247054701771076 (2017).Article 

Google Scholar 
21.Radtke, K. M. et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry 1, e21–e26 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
22.Mueller, B. R. & Bale, T. L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 28, 9055–9065 (2008).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
23.Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A. & Chen, A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat. Neurosci. 13, 1351–1353 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
24.Boersma, G. J. et al. Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats. Epigenetics 9, 437–447 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
25.Turecki, G. & Meaney, M. J. Effects of the social environment and stress on glucocorticoid receptor gene methylation: A systematic review. Biol. Psychiatry 79, 87–96 (2016).CAS 
PubMed 
Article 

Google Scholar 
26.Sterrenburg, L. et al. Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PLoS ONE 6, 1–14 (2011).Article 
CAS 

Google Scholar 
27.Reeder, D. A. M. & Kramer, K. M. Stress in free-ranging mammals: Integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235 (2005).Article 

Google Scholar 
28.Jeanneteau, F. D. et al. BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus. Proc. Natl. Acad. Sci. USA. 109, 1305–1310 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
29.Smith, S. M. & Vale, W. W. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin. Neurosci. 8, 383–395 (2006).PubMed 
PubMed Central 
Article 

Google Scholar 
30.Turner, J. D. & Muller, C. P. Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: Identification, and tissue distribution of multiple new human exon 1. J. Mol. Endocrinol. 35, 283–292 (2005).CAS 
PubMed 
Article 

Google Scholar 
31.Bakusic, J., Schaufeli, W., Claes, S. & Godderis, L. Stress, burnout and depression: A systematic review on DNA methylation mechanisms. J. Psychosom. Res. 92, 34–44 (2017).PubMed 
Article 

Google Scholar 
32.Center for Whale Research. Population. https://www.whaleresearch.com. Accessed 11 Jan 2021 (2020).33.Fisheries and Oceans Canada. Recovery Strategy for the Northern and Southern Resident Killer Whales (Orcinus orca) in Canada [Proposed]. Species at Risk Act Recovery Strategy Series, Fisheries & Oceans Canada, Ottawa, x + 84 pp.(2018).34.DFO. Population Status Update for the Northern Resident Killer Whale (Orcinus orca) in 2018. DFO Can. Sci. Advis. Sec. Sci. Resp. 2019/025. (2019).35.Bigg, M. A., Olesiuk, P. F., Ellis, G. M., Ford, J. K. B. & Balcomb, K. C. Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Reports Int. Whal. Comm. 12, 383–405 (1990).
Google Scholar 
36.Ford, J. K. B. & Ellis, G. M. Selective foraging by fish-eating killer whales Orcinus orca in British Columbia. Mar. Ecol. Prog. Ser. 316, 185–199 (2006).ADS 
Article 

Google Scholar 
37.Chen, I.-H. et al. Selection of reference genes for RT-qPCR studies in blood of beluga whales (Delphinapterus leucas). PeerJ 4, e1810 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
38.Horvath, S. & Raj, K. DNA methylation-based biomarkers and the epigenetic clock theory of ageing. Nat. Rev. Genet. 19, 371–384 (2018).CAS 
PubMed 
Article 

Google Scholar 
39.Hoelzel, A. R., Dahlheim, M. E. & Stern, S. J. Low genetic variation among killer whales (Orcinus orca) in the eastern north Pacific and genetic differentiation between foraging specialists. J. Hered. 89, 121–128 (1998).CAS 
PubMed 
Article 

Google Scholar 
40.Yao, M., Stenzel-Poore, M. & Denver, R. J. Structural and functional conservation of vertebrate corticotropin- releasing factor genes: Evidence for a critical role for a conserved cyclic AMP response element. Endocrinology 148, 2518–2531 (2007).CAS 
PubMed 
Article 

Google Scholar 
41.Aguiniga, L. M., Yang, W., Yaggie, R. E., Schaeffer, A. J. & Klumpp, D. J. Acyloxyacyl hydrolase modulates depressive-like behaviors through aryl hydrocarbon receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 317, R289–R300 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
42.Hankinson, O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35, 307–340 (1995).CAS 
PubMed 
Article 

Google Scholar 
43.Lundin, J. I. et al. Pre-oil spill baseline profiling for contaminants in Southern Resident killer whale fecal samples indicates possible exposure to vessel exhaust. Mar. Pollut. Bull. 136, 448–453 (2018).CAS 
PubMed 
Article 

Google Scholar 
44.MacDonald, L. H. Evaluating and managing cumulative effects: Process and constraints. Environ. Manag. 26, 299–315 (2000).CAS 
Article 

Google Scholar 
45.National Academies of Sciences Engineering and Medicine. Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals. https://doi.org/10.17226/23479 (National Academies Press, 2017). 46.Barrett-Lennard, L. G., Smith, T. G. & Ellis, G. M. A cetacean biopsy system using lightweight pneumatic darts, and its effect on the behavior of killer whales. Mar. Mammal Sci. 12, 14–27 (1996).Article 

Google Scholar 
47.Sambrook, J., Fritsch, E. F. & Maniatis, H. Molecular Cloning: A Laboratory Manual (Cold Springs Harbor Laboratory Press, 1989).
Google Scholar 
48.Illumina. 16S Metagenomic Sequencing Library Preparation. Illumina.com 1–28 (2013).49.Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.j 17, 10–12 (2011).Article 

Google Scholar 
50.Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
51.Magoč, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
52.Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
53.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar  More

The location, diameter, height and circumference of the coral were measured (Table 1, Fig. 2). The Porites was brown to cream in colour and hemispherical in shape (Fig. 2). It was identified as either Porites lutea (Hump or Pore coral) or P. lobata (Lobe coral)14.The primary habitat on the Porites was live coral (70%), followed by sponge, live coral rock and a small amount of macroalgae (Table 2). No recently dead coral, coral rubble or sand was recorded (Table 2). We observed competition between the Porites and other species of coral and invertebrate including encrusting sponge, plating and branching Acropora spp., Montipora, Chlorodesmis, soft coral and zoanthids (Table 2, Figs. 3, 4).Table 2 Reef Health Impact Survey (RHIS) of habitat and species categories on Porites sp.Full size tableFigure 3Detail of the sub-habitats and competitive interactions Porites sp. and boring sponge Cliona viridis (left) and live coral Porites sp. and Montipora sp. (right) along interspecific contact zones.Full size imageFigure 4Detail of Reef Health Impact Survey (RHIS) of Porites.Full size imageThe boring sponge, Cliona viridis, is abundant on the Great Barrier Reef15. It is a common bioeroding species advancing laterally at around 1 cm and to a depth of 1.2 cm per annum15. Abundance of Cliona viridis is often correlated to substrate availability and water energy with the greatest abundance often on the windward side of bommies15. This correlates to our observations as the large proportion of the substrate estimated to cover the bommie (15%) was on the windward side. The sponge’s advances will likely continue to compromise the colony size and health.We recorded marine debris at the base of the Porites. The debris was 2–3 m of rope that appeared to have been wrapped around the base of an adjacent coral. Adjacent to the bommie were three concrete blocks.How big is the Porites coral at Goolboodi compared to other big corals in the GBR, and the world? Potts et al.6 reported a very large, rounded Porites colony, 6.9 m in diameter which is 3.1 m smaller than this study. Lough et al.16 reported coral cores from colonies between 1.6–8.0 m in height with the largest corals of 6.0 m at Havannah, North Molle and Masthead Islands, 7.5 m at Abraham Reef and 8.0 m at Sanctuary Reef. Recognising the limitations of published data, the Porites coral at Goolboodi is the largest diameter coral that has been measured, and the 6th tallest in the GBR. It is unknown if the other corals are still alive or dead.Other comparatively large massive Porites have previously been located throughout the Pacific. These have included multiple bommies measuring more than 10 m4 and one exceptionally large colony observed measuring 17 m × 12 m in American Samoa17. Additionally, large Porites sp. bommies have been observed at Green Island, 30 km east of Taiwan18 as well as an 11 m diameter Porites australiensis at Sesoko Island, Okinawa, Japan19.How old is this massive Porites? In discussions with the Australian Institute of Marine Science (AIMS), there is a robust, linear relationship ( > 80% variance explained) between Porites average linear extension rate and average annual sea surface temperature (SST)20,21 that provides an estimate of colony age from its height. Using average annual SST at 18.5S, 146.5E of 26.12C (from HadiSST data set), the estimated linear extension rate is determined by (2.97 × 26.12) − 65.46 = 1.21 cm/year. Given the colony height of 5.1–5.3 m, this gives an estimated age of 421–438 years. This is well before European exploration and settlement of Australia. AIMS has investigated over 328 colonies of massive Porites corals from 69 reefs along the GBR and has aged them as being from 10–436 years21. AIMS has not investigated this coral (pers. comm Neal Cantin). Based on limitations of published data, the Porites coral at Goolboodi is one of the oldest corals on the GBR.Why is the Porites partially dead on top and living on the side? The proportion of live coral tissue on a colony reflects the cumulative, integrated effect of both beneficial and adverse environmental factors. Substantial portions of coral tissue can die from exposure to sun at low tides or warm water without lethal consequences to the colony as a whole10. Partial mortality of large bommies provides available real estate for opportunistic, fast growing sessile organisms. In this instance, multiple species of tabulate and branching Acropora sp., encrusting Montipora sp. and encrusting sponges are among the benthic organisms to have colonised 30% of the coral bommies’ surface area. Intraspecific competition is also evident from the skeletal barriers created along contact zones22 (Fig. 3). There was no observation of disease or coral bleaching.The Porites is located in a relatively remote, rarely visited and highly protected Marine National Park (green) zone. Its location had not been previously reported and there is no existing database for significant corals in Australia or globally. Cataloguing the location of massive and long-lived corals can have multiple benefits. Scientific benefits include geochemical and isotopic analyses in coral skeletal cores which can help understand century-scale changes in oceanographic events and can be used to verify climate models. Social and economic benefits can include diving tourism, citizen science23 culture and stewardship. Perhaps the Significant Trees Register, which was designed by the National Trust24 to protect and celebrate Australia’s heritage could be considered as a model. There are risks of cataloguing the location of massive corals. It could be damaged by direct and indirect human uses including anchoring, research and pollution.Indigenous languages are an integral part of Indigenous culture, spirituality, and connection to country. We consulted Manbarra Traditional Owners about protocol and an appropriate cultural name for the Porites and they considered: Big (Muga), Home (Wanga), Coral reef (Muugar), Coral (Dhambi), Old (Anki, Gurgu), Old man (Gulula) and Old person (Gurgurbu)25. The recommendation by Manbarra Traditional Owners is that the Porites is named as Muga dhambi (Big coral). The feedback from the process of consultation was very positive with acknowledgement of the respect that the scientists have demonstrated to acknowledge Traditional Owners in this way.The large Porites coral at Goolboodi (Orpheus) Island is unusually rare and resilient. It has survived coral bleaching, invasive species, cyclones, severely low tides and human activities for almost 500 years. In an attempt to contextualise the resilience of these individual Porites we have reviewed major historic disturbances such as coral bleaching which has occurred since at least 1575 and potentially 99 bleaching events in the GBR over the past 400 plus years26. Other indicators such as high-density ‘stress bands’ were recorded from 1877 and are significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming27. In addition there have been an average of 1–2 tropical cyclones per decade (40–80 in total) that have potentially impacted the coral adjacent to Goolboodi Island28,29; 46 tropical cyclones impacted the area between Ingham and Townsville from 1858 to 200830. The cumulative impact of almost 100 bleaching events and up to 80 major cyclones over a period of four centuries, plus declining nearshore water quality contextualise the high resilience of this Porites coral. Looking to the future there is real concern for corals in the GBR due to many impacts including climate change, declining water quality, overfishing and coastal development31,32. This field note provides important geospatial, environmental, and cultural information of a rare coral that can be monitored, appreciated, potentially restored and hopefully inspire future generations to care more for our reefs and culture. More

1.Irwin AJ, Oliver MJ. Are ocean deserts getting larger? Geophys Res Lett. 2009;36:L18609.Article 

Google Scholar 
2.McClain CR, Signorini SR, Christian JR. Subtropical gyre variability observed by ocean-color satellites. Deep Sea Res Part II Topical Stud Oceanogr. 2004;51:281–301.CAS 
Article 

Google Scholar 
3.Signorini SR, Franz BA, McClain CR. Chlorophyll variability in the oligotrophic gyres: Mechanisms, seasonality and trends. Front Mar Sci. 2015;2:1–11.Article 

Google Scholar 
4.Polovina JJ, Howell EA, Abecassis M. Ocean’s least productive waters are expanding. Geophys Res Lett. 2008;35:L03618.Article 

Google Scholar 
5.Sharma P, Marinov I, Cabre A, Kostadinov T, Singh A. Increasing biomass in the warm oceans: unexpected new insights from SeaWIFS. Geophys Res Lett. 2019;46:3900–10.Article 

Google Scholar 
6.Flombaum P, Wang W-L, Primeau FW, Martiny AC. Global picophytoplankton niche partitioning predicts overall positive response to ocean warming. Nat Geosci. 2020;13:116–20.CAS 
Article 

Google Scholar 
7.Carr M-E, Friedrichs MAM, Schmeltz M, Noguchi Aita M, Antoine D, Arrigo KR, et al. A comparison of global estimates of marine primary production from ocean color. Deep Sea Res Part II Topical Stud Oceanogr. 2006;53:741–70.Article 

Google Scholar 
8.Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science. 1998;281:237–40.CAS 
PubMed 
Article 

Google Scholar 
9.DeVries T, Primeau F, Deutsch C. The sequestration efficiency of the biological pump. Geophys Res Lett. 2012;39:L13601.Article 
CAS 

Google Scholar 
10.Cabré A, Marinov I, Leung S. Consistent global responses of marine ecosystems to future climate change across the IPCC AR5 earth system models. Clim Dyn. 2015;45:1253–80.Article 

Google Scholar 
11.Behrenfeld MJ, O’Malley RT, Boss ES, Westberry TK, Graff JR, Halsey KH, et al. Revaluating ocean warming impacts on global phytoplankton. Nat Clim Change. 2015;6:323–30.Article 

Google Scholar 
12.Richardson K, Bendtsen J. Vertical distribution of phytoplankton and primary production in relation to nutricline depth in the open ocean. Mar Ecol Prog Ser. 2019;620:33–46.CAS 
Article 

Google Scholar 
13.Roshan S, DeVries T. Efficient dissolved organic carbon production and export in the oligotrophic ocean. Nat Commun. 2017;8:1–8.CAS 
Article 

Google Scholar 
14.Marañón E, Holligan PM, Barciela R, González N, Mouriño B, Pazó MJ, et al. Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments. Mar Ecol Prog Ser. 2001;216:43–56.Article 

Google Scholar 
15.Pérez V, Fernández E, Marañón E, Morán XAG, Zubkov MV. Vertical distribution of phytoplankton biomass, production and growth in the Atlantic subtropical gyres. Deep Sea Res Part I Oceanographic Res Pap. 2006;53:1616–34.Article 

Google Scholar 
16.Teira E, Mouriño B, Marañón E, Pérez V, Pazó MJ, Serret P, et al. Variability of chlorophyll and primary production in the Eastern North Atlantic subtropical gyre: potential factors affecting phytoplankton activity. Deep Sea Res Part I Oceanographic Res Pap. 2005;52:569–88.CAS 
Article 

Google Scholar 
17.Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, et al. Prochlorococcus marinus nov. Gen. Nov. Sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol. 1992;157:297–300.CAS 
Article 

Google Scholar 
18.Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, et al. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. PNAS. 2013;110:9824–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Partensky F, Hess WR, Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev. 1999;63:106–27.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
20.Li WK. Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting. Limnol Oceanogr. 1994;39:169–75.CAS 
Article 

Google Scholar 
21.Jardillier L, Zubkov MV, Pearman J, Scanlan DJ. Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical Northeast Atlantic Ocean. ISME J. 2010;4:1180–92.CAS 
PubMed 
Article 

Google Scholar 
22.Irion S, Christaki U, Berthelot H, L’Helguen S, Jardillier L. Small phytoplankton contribute greatly to CO2-fixation after the diatom bloom in the Southern Ocean. ISME J. 2021;15:1–14.Article 
CAS 

Google Scholar 
23.Liu K, Suzuki K, Chen B, Liu H. Are temperature sensitivities of Prochlorococcus and Synechococcus impacted by nutrient availability in the subtropical Northwest Pacific? Limnol Oceanogr. 2020;66:639–51.Article 
CAS 

Google Scholar 
24.D’Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP, Kallmeyer J, et al. Subseafloor sedimentary life in the South Pacific gyre. PNAS. 2009;106:11651–6.PubMed 
PubMed Central 
Article 

Google Scholar 
25.Longhurst A, Sathyendranath S, Platt T, Caverhill C. An estimate of global primary production in the ocean from satellite radiometer data. J Plankton Res. 1995;17:1245–71.Article 

Google Scholar 
26.Morel A, Gentili B, Claustre H, Babin M, Bricaud A, Ras J, et al. Optical properties of the “clearest” natural waters. Limnol Oceanogr. 2007;52:217–29.CAS 
Article 

Google Scholar 
27.Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, LaRoche J, et al. Heterotrophic organisms dominate nitrogen fixation in the south pacific gyre. ISME J. 2012;6:1238–49.CAS 
PubMed 
Article 

Google Scholar 
28.Raimbault P, Garcia N. Evidence for efficient regenerated production and dinitrogen fixation in nitrogen-deficient waters of the South Pacific Ocean: impact on new and export production estimates. Biogeosciences. 2008;5:323–38.CAS 
Article 

Google Scholar 
29.Shiozaki T, Bombar D, Riemann L, Sato M, Hashihama F, Kodama T, et al. Linkage between dinitrogen fixation and primary production in the oligotrophic South Pacific Ocean. Glob Biogeochem Cyc. 2018;32:1028–44.CAS 
Article 

Google Scholar 
30.Reintjes G, Tegetmeyer HE, Bürgisser M, Orlić S, Tews I, Zubkov M, et al. On-site analysis of bacterial communities of the ultraoligotrophic South Pacific gyre. Appl Environ Microbiol. 2019;85:e00184–19.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
31.Zielinski O, Henkel R, Voß D, Ferdelman TG. Physical oceanography during Sonne cruise SO245 (Ultrapac). PANGAEA. 2018. https://doi.org/10.1594/PANGAEA.890394.32.Ferdelman TG, Klockgether G, Downes P, Lavik G. Nutrient data from CTD Nisken bottles from Sonne expedition SO-245 “Ultrapac”. PANGAEA. 2019. https://doi.org/10.1594/PANGAEA.899228.33.Arar EJ, Collins GB. Method 445.0: In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence: U.S. Environmental Protection Agency, Washington, DC; 1997. https://cfpub.epa.gov/si/si_public_record_report.cfm?Lab=NERL&dirEntryId=309417.34.Welschmeyer N, Naughton S. Improved chlorophyll a analysis: single fluorometric measurement with no acidification. Lake Reserv Manag. 1994;9:123.
Google Scholar 
35.Osterholz H, Kilgour D, Storey DS, Lavik G, Ferdelman T, Niggemann J, et al. Accumulation of DOC in the South Pacific subtropical gyre from a molecular perspective. Mar Chem. 2021;231:103955.CAS 
Article 

Google Scholar 
36.Voß D, Henkel R, Wollschläger J, Zielinski O. Hyperspectral underwater light field measured during the cruise SO245 with R/V Sonne. PANGAEA. 2020. https://doi.org/10.1594/PANGAEA.911558.37.Martínez-Pérez C, Mohr W, Löscher CR, Dekaezemacker J, Littmann S, Yilmaz P, et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat Microbiol. 2016;1:1–7.Article 
CAS 

Google Scholar 
38.Marra J. Net and gross productivity: weighing in with 14C. Aquat Microb Ecol. 2009;56:123–31.Article 

Google Scholar 
39.Ribeiro CG, Marie D, Santos ALD, Brandini FP, Vaulot D. Estimating microbial populations by flow cytometry: comparison between instruments. Limnol Oceanogr Methods. 2016;14:750–8.Article 

Google Scholar 
40.Pernthaler A, Pernthaler J, Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol. 2002;68:3094–101.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
41.West NJ, Schönhuber WA, Fuller NJ, Amann RI, Rippka R, Post AF, et al. Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16 S rRNA-targeted oligonucleotides. Microbiology. 2001;147:1731–44.CAS 
PubMed 
Article 

Google Scholar 
42.Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS—a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.CAS 
PubMed 
Article 

Google Scholar 
43.Verity PG, Robertson CY, Tronzo CR, Andrews MG, Nelson JR, Sieracki ME. Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr. 1992;37:1434–46.CAS 
Article 

Google Scholar 
44.Khachikyan A, Milucka J, Littmann S, Ahmerkamp S, Meador T, Könneke M, et al. Direct cell mass measurements expand the role of small microorganisms in nature. Appl Environ Microbiol. 2019;85:AEM00493–19.Article 

Google Scholar 
45.Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, et al. Improved bacterial 16 S rRNA gene (v4 and v4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. MSystems. 2016;1:e00009–15.PubMed 
Article 

Google Scholar 
46.Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rrna primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
47.Comeau AM, Douglas GM, Langille MG. Microbiome helper: a custom and streamlined workflow for microbiome research. MSystems. 2017;2:e00127–16.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
48.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. Qiime allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
49.Haas S, Desai DK, LaRoche J, Pawlowicz R, Wallace DW. Geomicrobiology of the carbon, nitrogen and sulphur cycles in Powell Lake: a permanently stratified water column containing ancient seawater. Environ Microbiol. 2019;21:3927–52.CAS 
PubMed 
Article 

Google Scholar 
50.Zhang J, Kobert K, Flouri T, Stamatakis A. Pear: a fast and accurate Illumina paired-end read merger. Bioinformatics. 2013;30:614–20.51.Rognes T, Flouri T, Nichols B, Quince C, Mahé F. Vsearch: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.PubMed 
PubMed Central 
Article 

Google Scholar 
52.Kopylova E, Noé L, Touzet H. Sortmerna: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.CAS 
PubMed 
Article 

Google Scholar 
53.Mercier C, Boyer F, Bonin A, Coissac E (eds). Sumatra and Sumaclust: fast and exact comparison and clustering of sequences. SeqBio 2013 Workshop 2013: (abstract).54.DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16 S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
55.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–6.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
56.Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S, et al. PhytoREF: A reference database of the plastidial 16 S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Molec Ecol Res. 2015;15:1435–45.CAS 
Article 

Google Scholar 
57.Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2012;4:D597–604.Article 
CAS 

Google Scholar 
58.Del Campo J, Kolisko M, Boscaro V, Santoferrara LF, Nenarokov S, Massana R, et al. EukRef: phylogenetic curation of ribosomal RNA to enhance understanding of eukaryotic diversity and distribution. PLoS Biol. 2018;16:e2005849.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
59.Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: A software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Gruber-Vodicka HR, Seah BK, Pruesse E. Phyloflash: rapid small-subunit rRNA profiling and targeted assembly from metagenomes. Msystems. 2020;5:e00920.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
61.Farrant GK, Doré H, Cornejo-Castillo FM, Partensky F, Ratin M, Ostrowski M, et al. Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria. PNAS. 2016;113:E3365–74.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
62.Oggerin de Orube M, Fuchs BM. Personal communication: Unpublished shotgun metagenomes collected from in situ pump samples during R/V Sonne expedition SO245. Bremen, Germany. 2021.63.Schlitzer R. Ocean Data View. Bremerhaven, Germany. 2021. https://odv.awi.de.64.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna, Austria. 2017. https://www.R-project.org/.65.Wickham H. Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York. 2016.66.McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE. 2013;8:e61217.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
67.Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, et al. The vegan package: community ecology package. R package version 2.5–7. 2019. https://CRAN.R-project.org/package=vegan.68.Chaigneau A, Pizarro O. Surface circulation and fronts of the South Pacific Ocean, east of 120°W. Geophys Res Lett. 2005;32:L08605.69.Logares R, Sunagawa S, Salazar G, Cornejo‐Castillo FM, Ferrera I, Sarmento H, et al. Metagenomic 16 S rRNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol. 2014;16:2659–71.CAS 
PubMed 
Article 

Google Scholar 
70.Shi XL, Lepère C, Scanlan DJ, Vaulot D. Plastid 16 s rRNA gene diversity among eukaryotic picophytoplankton sorted by flow cytometry from the South Pacific Ocean. PLOS ONE. 2011;6:e18979.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
71.Fuller NJ, Campbell C, Allen DJ, Pitt FD, Zwirglmaier K, Le Gall F, et al. Analysis of photosynthetic picoeukaryote diversity at open ocean sites in the Arabian Sea using a pcr biased towards marine algal plastids. Aquat Micro Ecol. 2006;43:79–93.Article 

Google Scholar 
72.Raes EJ, Bodrossy L, Kamp JVD, Bissett A, Ostrowski M, Brown MV, et al. Oceanographic boundaries constrain microbial diversity gradients in the South Pacific Ocean. PNAS. 2018;115:E8266–75.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
73.Campbell L, Liu H, Nolla HA, Vaulot D. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at station ALOHA during the 1991-4 ENSO event. Deep Sea Res Part I Oceanogr Res Pap. 1997;44:167–92.CAS 
Article 

Google Scholar 
74.Viviani DA, Church MJ. Decoupling between bacterial production and primary production over multiple time scales in the North Pacific subtropical gyre. Deep Sea Res Part I Oceanogr Res Pap. 2017;121:132–42.CAS 
Article 

Google Scholar 
75.Rii YM, Duhamel S, Bidigare RR, Karl DM, Repeta DJ, Church MJ. Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the south east pacific ocean. Limnol Oceanogr. 2016;61:806–24.Article 

Google Scholar 
76.Shi XL, Marie D, Jardillier L, Scanlan DJ, Vaulot D. Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean. PLOS ONE. 2009;4:e7657.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
77.Kirkham AR, Lepere C, Jardillier LE, Not F, Bouman H, Mead A, et al. A global perspective on marine photosynthetic picoeukaryote community structure. ISME J. 2013;7:922–36.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
78.Lepère C, Vaulot D, Scanlan DJ. Photosynthetic picoeukaryote community structure in the South East Pacific Ocean encompassing the most oligotrophic waters on earth. Environ Microbiol. 2009;11:3105–17.PubMed 
Article 
CAS 

Google Scholar 
79.Bender ML, Jönsson B. Is seasonal net community production in the South Pacific subtropical gyre anomalously low? Geophys Res Lett. 2016;43:9757–63.Article 

Google Scholar 
80.Montégut CDB, Madec G, Fischer AS, Lazar A, Iudicone D. Mixed layer depth over the global ocean: an examination of profile data and a profile-based climatology. J Geophys Res Oceans. 2004;109:C12003.Article 

Google Scholar 
81.Liu Q, Lu Y. Role of horizontal density advection in seasonal deepening of the mixed layer in the subtropical Southeast Pacific. Adv Atmospher Sci. 2016;33:442–51.Article 

Google Scholar 
82.Sato K, Suga T. Structure and modification of the South Pacific eastern subtropical mode water. J Phys Oceanogr. 2009;39:1700–14.Article 

Google Scholar 
83.Jung J, Furutani H, Uematsu M. Atmospheric inorganic nitrogen in marine aerosol and precipitation and its deposition to the north and south pacific oceans. J Atmospher Chem. 2011;68:157–81.CAS 
Article 

Google Scholar 
84.Pavia FJ, Anderson RF, Winckler G, Fleisher MQ. Atmospheric dust inputs, iron cycling, and biogeochemical connections in the South Pacific Ocean from thorium isotopes. Glob Biogeochem Cycles. 2020;34:e2020GB006562.CAS 

Google Scholar 
85.Bonnet S, Guieu C, Bruyant F, Prášil O, Van Wambeke F, Raimbault P, et al. Nutrient limitation of primary productivity in the Southeast Pacific (Biosope Cruise). Biogeosciences. 2008;5:215–25.CAS 
Article 

Google Scholar 
86.Mahaffey C, Björkman KM, Karl DM. Phytoplankton response to deep seawater nutrient addition in the North Pacific subtropical gyre. Mar Ecol Prog Ser. 2012;460:13–34.CAS 
Article 

Google Scholar 
87.Grob C, Jardillier L, Hartmann M, Ostrowski M, Zubkov MV, Scanlan DJ. Cell-specific CO2 fixation rates of two distinct groups of plastidic protists in the Atlantic Ocean remain unchanged after nutrient addition. Environ Microbiol Rep. 2015;7:211–8.CAS 
PubMed 
Article 

Google Scholar 
88.Vaulot D, Marie D, Olson RJ, Chisholm SW. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial pacific ocean. Science. 1995;268:1480–2.CAS 
PubMed 
Article 

Google Scholar 
89.Grob C, Hartmann M, Zubkov MV, Scanlan DJ. Invariable biomass-specific primary production of taxonomically discrete picoeukaryote groups across the Atlantic Ocean. Environ Microbiol. 2011;13:3266–74.PubMed 
Article 

Google Scholar 
90.Berthelot H, Duhamel S, L’Helguen S, Maguer J-F, Wang S, Cetinić I, et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 2019;13:651.CAS 
PubMed 
Article 

Google Scholar 
91.Zubkov MV, Fuchs BM, Tarran GA, Burkill PH, Amann R. High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol. 2003;69:1299–304.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
92.Muñoz-Marín MC, Gómez-Baena G, López-Lozano A, Moreno-Cabezuelo JA, Díez J, García-Fernández JM. Mixotrophy in marine picocyanobacteria: use of organic compounds by Prochlorococcus and Synechococcus. ISME J. 2020;14:1065–73.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
93.Timmermans K, Van der Wagt B, Veldhuis M, Maatman A, De Baar H. Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res. 2005;53:109–20.CAS 
Article 

Google Scholar 
94.Vaulot D, Eikrem W, Viprey M, Moreau H. The diversity of small eukaryotic phytoplankton (≤ 3 μm) in marine ecosystems. FEMS Microbiol Rev. 2008;32:795–820.CAS 
PubMed 
Article 

Google Scholar 
95.Worden AZ, Janouskovec J, McRose D, Engman A, Welsh RM, Malfatti S, et al. Global distribution of a wild alga revealed by targeted metagenomics. Curr Biol. 2012;22:R675–7.CAS 
PubMed 
Article 

Google Scholar 
96.Le Gall F, Rigaut-Jalabert F, Marie D, Garczarek L, Viprey M, Gobet A, et al. Picoplankton diversity in the South-east Pacific Ocean from cultures. Biogeosciences. 2008;5:203–14.Article 

Google Scholar 
97.NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Chlorophyll Data; Reprocessing. NASA OB.DAAC, Greenbelt, MD, USA. 2018. https://oceancolor.gsfc.nasa.gov/data/10.5067/AQUA/MODIS/L3M/CHL/2018/ Accessed 2019/08/01. More

1.Borer ET, Seabloom EW, Mitchell CE, Cronin JP. Multiple nutrients and herbivores interact to govern diversity, productivity, composition, and infection in a successional grassland. Oikos. 2014;123:214–24.Article 

Google Scholar 
2.Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S. Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Natl Acad Sci. 2013;110:11911–6.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
3.Robinson RJ, Fraaije BA, Clark IM, Jackson RW, Hirsch PR, Mauchline TH. Endophytic bacterial community composition in wheat (Triticum aestivum) is determined by plant tissue type developmental stage and soil nutrient availability. Plant Soil. 2016;405:381–96.CAS 
Article 

Google Scholar 
4.Ratzke C, Barrere J, Gore J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol. 2020;4:376–83.PubMed 
Article 

Google Scholar 
5.Lambers JHR, Harpole WS, Tilman D, Knops J, Reich PB. Mechanisms responsible for the positive diversity–productivity relationship in minnesota grasslands. Ecol Lett. 2004;7:661–8.Article 

Google Scholar 
6.Essarioui A, LeBlanc N, Kistler HC, Kinkel LL. Plant community richness mediates inhibitory interactions and resource competition between Streptomyces and fusarium populations in the rhizosphere. Micro Ecol. 2017;74:157–67.Article 

Google Scholar 
7.Pan Y, Cassman N, de Hollander M, Mendes LW, Korevaar H, Geerts RH, et al. Impact of long-term n, p, k, and npk fertilization on the composition and potential functions of the bacterial community in grassland soil. FEMS Microbiol Ecol. 2014;90:195–205.CAS 
PubMed 
Article 

Google Scholar 
8.Schlatter DC, DavelosBaines AL, Xiao K, Kinkel LL. Resource use of soilborne Streptomyces varies with location phylogeny, and nitrogen amendment. Micro Ecol. 2013;66:961–71.Article 

Google Scholar 
9.Firn J, McGree JM, Harvey E, Flores-Moreno H, Schütz M, Buckley YM, et al. Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs. Nat Ecol Evol. 2019;3:400–6.PubMed 
Article 

Google Scholar 
10.Anderson TM, Griffith DM, Grace JB, Lind EM, Adler PB, Biederman LA, et al. Herbivory and eutrophication mediate grassland plant nutrient responses across a global climatic gradient. Ecol. 2018;99:822–31.Article 

Google Scholar 
11.Bernstein N, Gorelick J, Zerahia R, Koch S. Impact of n, p, k, and humic acid supplementation on the chemical profile of medical cannabis (Cannabis sativa L.). Front Plant Sci. 2019;10:736.PubMed 
PubMed Central 
Article 

Google Scholar 
12.Tangolar S, Tangolar S, Torun AA, Ada M, Göçmez S. Influence of supplementation of vineyard soil with organic substances on nutritional status, yield and quality of ‘black magic’ grape (Vitis vinifera L.) and soil microbiological and biochemical characteristics. OENO One. 2020;54:1143–57.Article 
CAS 

Google Scholar 
13.De Long JR, Sundqvist MK, Gundale MJ, Giesler R, Wardle DA. Effects of elevation and nitrogen and phosphorus fertilization on plant defence compounds in subarctic tundra heath vegetation. Funct Ecol. 2016;30:314–25.Article 

Google Scholar 
14.Dietrich R, Ploss K, Heil M. Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant Cell Environ. 2004;27:896–906.CAS 
Article 

Google Scholar 
15.Bryant JP, Chapin III FS, Klein DR. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos. 1983;40:357–68.16.Kinkel LL, Otto-Hanson LK, Otto-Hansen Z, Johnson M, Spawn S, Song Z, et al. Foliar endophytic microbiome composition and functional capacities vary with soil nutrient inputs. Phytopathol. 2018;108:77.
Google Scholar 
17.Seabloom EW, Condon B, Kinkel L, Komatsu KJ, Lumibao CY, May G, et al. Effects of nutrient supply, herbivory, and host community on fungal endophyte diversity. Ecol. 2019;100:e02758.Article 

Google Scholar 
18.Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. The importance of the microbiome of the plant holobiont. N. Phytol. 2015;206:1196–206.Article 

Google Scholar 
19.Stulberg E, Fravel D, Proctor LM, Murray DM, LoTempio J, Chrisey L, et al. An assessment of US microbiome research. Nat Microbiol. 2016;1:15015.CAS 
PubMed 
Article 

Google Scholar 
20.Hanson BM, Weinstock GM. The importance of the microbiome in epidemiologic research. Ann Epidemiol. 2016;26:301–5.PubMed 
Article 
PubMed Central 

Google Scholar 
21.Bell TH, Hockett KL, Alcalá-Briseño RI, Barbercheck M, Beattie GA, Bruns MA, et al. Manipulating wild and tamed phytobiomes: Challenges and opportunities. Phytobiomes J 2019;3:3–21.Article 

Google Scholar 
22.Henning JA, Kinkel L, May G, Lumibao CY, Seabloom EW, Borer ET. Plant diversity and litter accumulation mediate the loss of foliar endophyte fungal richness following nutrient addition. Ecol. 2021;102:e03210.Article 

Google Scholar 
23.Vacher C, Hampe A, Porté AJ, Sauer U, Compant S, Morris CE. The phyllosphere: microbial jungle at the plant–climate interface. Annu Rev Ecol Evol Syst. 2016;47:1–24.Article 

Google Scholar 
24.Berendsen RL, Pieterse CM, Bakker PA. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
25.Turner TR, James EK, Poole PS. The plant microbiome. Genome Biol. 2013;14:1–10.Article 
CAS 

Google Scholar 
26.Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
27.Sanchez-Gorostiaga A, Bajić D, Osborne ML, Poyatos JF, Sanchez A. High-order interactions distort the functional landscape of microbial consortia. PLOS Biol. 2019;17:e3000550.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
28.Gould AL, Zhang V, Lamberti L, Jones EW, Obadia B, Korasidis N, et al. Microbiome interactions shape host fitness. Proc Natl Acad Sci. 2018;115:E11951–E11960.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
29.O’Keeffe KR. Within-host Microbial Interactions and Plant Parasites: From Pairwise Interactions to the Microbiome. PhD thesis, The University of North Carolina at Chapel Hill, 2019.30.Wemheuer F, Kaiser K, Karlovsky P, Daniel R, Vidal S, Wemheuer B. Bacterial endophyte communities of three agricultural important grass species differ in their response towards management regimes. Sci Rep. 2017;7:1–13.Article 
CAS 

Google Scholar 
31.Wemheuer B, Thomas T, Wemheuer F. Fungal endophyte communities of three agricultural important grass species differ in their response towards management regimes. Microorg. 2019;7:37.CAS 
Article 

Google Scholar 
32.Layeghifard M, Hwang DM, Guttman DS. Disentangling interactions in the microbiome: a network perspective. Trends Microbiol. 2017;25:217–28.CAS 
PubMed 
Article 

Google Scholar 
33.Barabási AL Network science. (Cambridge University Press, Cambridge, 2016).
Google Scholar 
34.Scott J. Social network analysis. Sociol. 1988;22:109–27.Article 

Google Scholar 
35.Borgatti SP, Mehra A, Brass DJ, Labianca G. Network analysis in the social sciences. Science. 2009;323:892–5.CAS 
PubMed 
Article 

Google Scholar 
36.Nelson GD, Rae A. An economic geography of the United States: from commutes to megaregions. PLOS ONE. 2016;11:e0166083.Article 
CAS 

Google Scholar 
37.Danon L, Ford AP, House T, Jewell CP, Keeling MJ, Roberts GO, et al. Networks and the epidemiology of infectious disease. Interdiscip Perspectives on Infect Dis. 2011.38.Expert P, Evans TS, Blondel VD, Lambiotte R. Uncovering space-independent communities in spatial networks. Proc Natl Acad Sci. 2011;108:7663–8.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
39.Röttjers L, Faust K. From hairballs to hypotheses—biological insights from microbial networks. FEMS Microbiol Rev. 2018;42:761–80.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
40.Naqvi A, Rangwala H, Keshavarzian A, Gillevet P. Network-based modeling of the human gut microbiome. Chem Biodivers. 2010;7:1040–50.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
41.Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Sci. 2015;350:663–6.CAS 
Article 

Google Scholar 
42.Poudel R, Jumpponen A, Schlatter DC, Paulitz TC, McSpadden Gardener BB, Kinkel LL, et al. Microbiome networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathol. 2016;106:1083–96.CAS 
Article 

Google Scholar 
43.Bakker MG, Schlatter DC, Otto-Hanson L, Kinkel LL. Diffuse symbioses: roles of plant–plant, plant–microbe and microbe–microbe interactions in structuring the soil microbiome. Mol Ecol. 2014;23:1571–83.PubMed 
Article 

Google Scholar 
44.van der Heijden MG, Hartmann M. Networking in the plant microbiome. PLOS Biol. 2016;14:e1002378.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
45.Lau MK, Borrett SR, Baiser B, Gotelli NJ, Ellison AM. Ecological network metrics: opportunities for synthesis. Ecosphere. 2017;8:e01900.Article 

Google Scholar 
46.Billick I, Case TJ. Higher order interactions in ecological communities: what are they and how can they be detected? Ecol. 1994;75:1529–43.Article 

Google Scholar 
47.Carr A, Diener C, Baliga NS, Gibbons SM. Use and abuse of correlation analyses in microbial ecology. ISME J. 2019;13:2647–55.PubMed 
PubMed Central 
Article 

Google Scholar 
48.Vaz Jauri P, Bakker MG, Salomon CE, Kinkel LL. Subinhibitory antibiotic concentrations mediate nutrient use and competition among soil Streptomyces. PLOS ONE. 2013;8:e81064.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
49.Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL, Seabloom EW, et al. Finding generality in ecology: a model for globally distributed experiments. Methods Ecol Evol. 2014;5:65–73.Article 

Google Scholar 
50.Borer ET, Grace JB, Harpole WS, MacDougall AS, Seabloom EW. A decade of insights into grassland ecosystem responses to global environmental change. Nat Ecol Evol. 2017;1:1–7.Article 

Google Scholar 
51.Essarioui A, LeBlanc N, Kistler HC, Kinkel LL. Plant host and community diversity impact the dynamics of resource use by soil Streptomyces. Phytopathol. 2014;104:38.
Google Scholar 
52.LeBlanc N, Essarioui A, Kinkel LL, Kistler HC. Fusarium community structure and carbon metabolism phenotypes respond to grassland plant community richness and plant host. Phytopathol. 2014;104:67.Article 

Google Scholar 
53.Essarioui A, Kistler HC, Kinkel LL. Nutrient use preferences among soil Streptomyces suggest greater resource competition in monoculture than polyculture plant communities. Plant Soil. 2016;409:329–43.CAS 
Article 

Google Scholar 
54.Essarioui A, LeBlanc N, Otto-Hanson L, Schlatter DC, Kistler HC, Kinkel LL. Inhibitory and nutrient use phenotypes among coexisting fusarium and Streptomyces populations suggest local coevolutionary interactions in soil. Environ Microbiol. 2020;22:976–85.PubMed 
Article 
PubMed Central 

Google Scholar 
55.Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L. Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Micro Ecol. 2009;57:413–20.Article 

Google Scholar 
56.Kinkel LL, Schlatter DC, Xiao K, Baines AD. Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes. ISME J 2013;8:249–56.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
57.Reichardt J, Bornholdt S. Statistical mechanics of community detection. Phys Rev E 2006;74:016110.Article 
CAS 

Google Scholar 
58.Watts DJ, Strogatz SH. Collective dynamics of ‘small-world’ networks. Nat. 1998;393:440–2.CAS 
Article 

Google Scholar 
59.Allesina S, Levine JM. A competitive network theory of species diversity. Proc Natl Acad Sci. 2011;108:5638–42.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Maynard DS, Bradford MA, Lindner DL, van Diepen LT, Frey SD, Glaeser JA, et al. Diversity begets diversity in competition for space. Nat Ecol Evol. 2017;1:1–8.Article 

Google Scholar 
61.Maynard DS, Crowther TW, Bradford MA. Competitive network determines the direction of the diversity–function relationship. Proc Natl Acad Sci. 2017;114:11464–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
62.Gallien L, Zimmermann NE, Levine JM, Adler PB. The effects of intransitive competition on coexistence. Ecol Lett. 2017;20:791–800.PubMed 
Article 
PubMed Central 

Google Scholar 
63.Schlatter DC, Song Z, Vaz-Jauri P, Kinkel LL. Inhibitory interaction networks among coevolved Streptomyces populations from prairie soils. PLOS ONE. 2019;14:e0223779.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
64.Milo R. Network motifs: simple building blocks of complex networks. Sci. 2002;298:824–7.CAS 
Article 

Google Scholar 
65.Case TJ, Bender EA. Testing for higher order interactions. Am Nat. 1981;118:920–9.Article 

Google Scholar 
66.Levine JM, Bascompte J, Adler PB, Allesina S. Beyond pairwise mechanisms of species coexistence in complex communities. Nat. 2017;546:56–64.CAS 
Article 

Google Scholar 
67.Mayfield MM, Stouffer DB. Higher-order interactions capture unexplained complexity in diverse communities. Nat Ecol Evol. 2017;1:0062.Article 

Google Scholar 
68.Friedman J, Higgins LM, Gore J. Community structure follows simple assembly rules in microbial microcosms. Nat Ecol Evol. 2017;1:0109.Article 

Google Scholar 
69.Bender EA, Canfield E. The asymptotic number of labeled graphs with given degree sequences. J Comb Theory Ser A 1978;24:296–307.Article 

Google Scholar 
70.Newman ME. Modularity and community structure in networks. Proc Natl Acad Sci. 2006;103:8577–82.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
71.Guo X, Boedicker JQ. The contribution of high-order metabolic interactions to the global activity of a four-species microbial community. PLOS Comput Biol. 2016;12:e1005079.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
72.Borrelli JJ, Allesina S, Amarasekare P, Arditi R, Chase I, Damuth J, et al. Selection on stability across ecological scales. Trends Ecol Evol. 2015;30:417–25.PubMed 
Article 
PubMed Central 

Google Scholar 
73.Davis GH, Crofoot MC, Farine DR. Estimating the robustness and uncertainty of animal social networks using different observational methods. Anim Behav. 2018;141:29–44.Article 

Google Scholar 
74.Gilbertson ML, White LA, Craft ME. Trade-offs with telemetry-derived contact networks for infectious disease studies in wildlife. Methods Ecol Evol. 2020;12:76–87.PubMed 
Article 
PubMed Central 

Google Scholar 
75.Grilli J, Barabás G, Michalska-Smith MJ, Allesina S. Higher-order interactions stabilize dynamics in competitive network models. Nat. 2017;548:210–3.CAS 
Article 

Google Scholar 
76.Letten AD, Stouffer DB. The mechanistic basis for higher-order interactions and non-additivity in competitive communities. Ecol Lett. 2019;22:423–36.PubMed 
Article 

Google Scholar 
77.Dormann CF, Roxburgh SH. Experimental evidence rejects pairwise modelling approach to coexistence in plant communities. Proc R Soc B Biol Sci. 2005;272:1279–85.Article 

Google Scholar 
78.Staniczenko PP, Kopp JC, Allesina S. The ghost of nestedness in ecological networks. Nat Commun. 2013;4:1–6.Article 
CAS 

Google Scholar 
79.Großkopf T, Soyer OS. Synthetic microbial communities. Curr Opin Microbiol. 2014;18:72–77.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
80.Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat. 1979;6:65–70.
Google Scholar  More