Rewiring coral: Anthropogenic nutrients shift diverse coral–symbiont nutrient and carbon interactions toward symbiotic algal dominance
dc.contributor.author | Allgeier, Jacob E. | |
dc.contributor.author | Andskog, Mona A. | |
dc.contributor.author | Hensel, Enie | |
dc.contributor.author | Appaldo, Richard | |
dc.contributor.author | Layman, Craig | |
dc.contributor.author | Kemp, Dustin W. | |
dc.date.accessioned | 2020-10-01T23:30:09Z | |
dc.date.available | WITHHELD_13_MONTHS | |
dc.date.available | 2020-10-01T23:30:09Z | |
dc.date.issued | 2020-10 | |
dc.identifier.citation | Allgeier, Jacob E.; Andskog, Mona A.; Hensel, Enie; Appaldo, Richard; Layman, Craig; Kemp, Dustin W. (2020). "Rewiring coral: Anthropogenic nutrients shift diverse coral–symbiont nutrient and carbon interactions toward symbiotic algal dominance." Global Change Biology 26(10): 5588-5601. | |
dc.identifier.issn | 1354-1013 | |
dc.identifier.issn | 1365-2486 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/162733 | |
dc.description.abstract | Improving coral reef conservation requires heightened understanding of the mechanisms by which coral cope with changing environmental conditions to maintain optimal health. We used a long‐term (10 month) in situ experiment with two phylogenetically diverse scleractinians (Acropora palmata and Porites porites) to test how coral–symbiotic algal interactions changed under real‐world conditions that were a priori expected to be beneficial (fish‐mediated nutrients) and to be harmful, but non‐lethal, for coral (fish + anthropogenic nutrients). Analyzing nine response variables of nutrient stoichiometry and stable isotopes per coral fragment, we found that nutrients from fish positively affected coral growth, and moderate doses of anthropogenic nutrients had no additional effects. While growing, coral maintained homeostasis in their nutrient pools, showing tolerance to the different nutrient regimes. Nonetheless, structural equation models revealed more nuanced relationships, showing that anthropogenic nutrients reduced the diversity of coral–symbiotic algal interactions and caused nutrient and carbon flow to be dominated by the symbiont. Our findings show that nutrient and carbon pathways are fundamentally “rewired” under anthropogenic nutrient regimes in ways that could increase corals’ susceptibility to further stressors. We hypothesize that our experiment captured coral in a previously unrecognized transition state between mutualism and antagonism. These findings highlight a notable parallel between how anthropogenic nutrients promote symbiont dominance with the holobiont, and how they promote macroalgal dominance at the coral reef scale. Our findings suggest more realistic experimental conditions, including studies across gradients of anthropogenic nutrient enrichment as well as the incorporation of varied nutrient and energy pathways, may facilitate conservation efforts to mitigate coral loss.We provide a long‐term field experiment to test the implications of different nutrient sources, fish excretion and moderate levels of anthropogenic nutrients, for coral health and coral–symbiont interactions. Our study identifies a potentially novel "transition state" whereby despite maintaining high growth rates and creating no apparent negative external effects, anthropogenic nutrient enrichment drives coral–algal interactions to be dominated by the algal symbiont—that is, increased prominence of energy and nutrient flow from the algal symbiont under conditions of Fish + anthropogenic nutrients (NPK) in the figure. We hypothesize that this “rewiring” of the coral–symbiont interactions may render the coral more vulnerable to additional stressors. | |
dc.publisher | Springer‐Verlag | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | phase shift | |
dc.subject.other | phosphorus | |
dc.subject.other | Symbiodiniaceae | |
dc.subject.other | symbiosis | |
dc.subject.other | fish nutrient supply | |
dc.subject.other | eutrophication | |
dc.subject.other | coral reefs | |
dc.subject.other | marine conservation | |
dc.subject.other | nitrogen | |
dc.title | Rewiring coral: Anthropogenic nutrients shift diverse coral–symbiont nutrient and carbon interactions toward symbiotic algal dominance | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Geology and Earth Sciences | |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | |
dc.subject.hlbtoplevel | Science | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/162733/2/gcb15230_am.pdf | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/162733/1/gcb15230.pdf | en_US |
dc.identifier.doi | 10.1111/gcb.15230 | |
dc.identifier.source | Global Change Biology | |
dc.identifier.citedreference | Rougerie, F., Fagerstrom, J. A., & Andrie, C. ( 1992 ). Geothermal endoupwelling – A solution to the reef nutrient paradox. Continental Shelf Research, 12, 785 – 798. https://doi.org/10.1016/0278‐4343(92)90044‐K | |
dc.identifier.citedreference | Muscatine, L., Falkowski, P. G., Dubinsky, Z., Cook, P. A., & McCloskey, L. R. ( 1989 ). The effects of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proceedings of the Royal Society B‐Biological Sciences, 236, 311 – 324. | |
dc.identifier.citedreference | Muscatine, L., Goiran, C., Land, L., Jaubert, J., Cuif, J. P., & Allemand, D. ( 2005 ). Stable isotopes (delta C‐13 and delta N‐15) of organic matrix from coral skeleton. Proceedings of the National Academy of Sciences of the United States of America, 102, 1525 – 1530. | |
dc.identifier.citedreference | Muscatine, L., & Porter, J. W. ( 1977 ). Reef corals – Mutualistic symbiosis adapted to nutrient‐poor environments. BioScience, 27, 454 – 460. | |
dc.identifier.citedreference | Odum, H. T., & Odum, E. P. ( 1955 ). Trohic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecological Monographs, 25, 291 – 320. | |
dc.identifier.citedreference | Okubo, N., Taniguchi, H., & Motokawa, T. ( 2005 ). Successful methods for transplanting fragments of Acropora formosa and Acropora hyacinthus. Coral Reefs, 24, 333 – 342. https://doi.org/10.1007/s00338‐005‐0496‐0 | |
dc.identifier.citedreference | Palardy, J. E., Rodrigues, L. J., & Grottoli, A. G. ( 2008 ). The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. Journal of Experimental Marine Biology and Ecology, 367, 180 – 188. https://doi.org/10.1016/j.jembe.2008.09.015 | |
dc.identifier.citedreference | Porter, J. W. ( 1976 ). Autotrophy, heterotrophy, and resource partitioning in Caribbean reef‐building corals. The American Naturalist, 110, 731 – 742. https://doi.org/10.1086/283100 | |
dc.identifier.citedreference | Richter, C., Wunsch, M., Rasheed, M., Kotter, I., & Badran, M. I. ( 2001 ). Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity‐dwelling sponges. Nature, 413, 726 – 730. https://doi.org/10.1038/35099547 | |
dc.identifier.citedreference | Savage, C. ( 2019 ). Seabird nutrients are assimilated by corals and enhance coral growth rates. Scientific Reports, 9, 4284. https://doi.org/10.1038/s41598‐019‐41030‐6 | |
dc.identifier.citedreference | Shantz, A. A., Ladd, M. C., Schrack, E., & Burkepile, D. E. ( 2015 ). Fish‐derived nutrient hotspots shape coral reef benthic communities. Ecological Applications, 25, 2142 – 2152. https://doi.org/10.1890/14‐2209.1 | |
dc.identifier.citedreference | Shantz, A. A., Lemoine, N. P., & Burkepile, D. E. ( 2016 ). Nutrient loading alters the performance of key nutrient exchange mutualisms. Ecology Letters, 19, 20 – 28. https://doi.org/10.1111/ele.12538 | |
dc.identifier.citedreference | Shaver, E. C., & Silliman, B. R. ( 2017 ). Time to cash in on positive interactions for coral restoration. PeerJ, 5, e3499. https://doi.org/10.7717/peerj.3499 | |
dc.identifier.citedreference | Shipley, B. ( 2009 ). Confirmatory path analysis in a generalized multilevel context. Ecology, 90, 363 – 368. https://doi.org/10.1890/08‐1034.1 | |
dc.identifier.citedreference | Smith, S. V., Kimmerer, W. J., Laws, E. A., Brock, R. E., & Walsh, T. W. ( 1981 ). Kaneohe bay sewage diversion experiment – Perspectives on ecosystem responses to nutrient perturbation. Pacific Science, 35, 279 – 402. | |
dc.identifier.citedreference | Sterner, R. W., & Elser, J. J. ( 2002 ). Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton, NJ: Princeton University Press. | |
dc.identifier.citedreference | Stimson, J., & Kinzie, R. A. ( 1991 ). The temporal pattern and rate of release of zooxanthellae from the reef coral pocillopora‐damicornis under nitrogen‐enrichment and control conditions. Journal of Experimental Marine Biology and Ecology, 153, 63 – 74. | |
dc.identifier.citedreference | Stoner, E. W., Layman, C. A., Yeager, L. A., & Hassett, H. M. ( 2011 ). Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. Marine Pollution Bulletin, 62, 1109 – 1114. https://doi.org/10.1016/j.marpolbul.2011.03.023 | |
dc.identifier.citedreference | Szmant, A. M. ( 2002 ). Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries, 25, 743 – 766. https://doi.org/10.1007/BF02804903 | |
dc.identifier.citedreference | Szmant, A. M., & Gassman, N. J. ( 1990 ). The effects of prolonged bleaching on the tissue of biomass and reproduction of the reef coral Montastreat annularis. Coral Reefs, 8, 217 – 224. | |
dc.identifier.citedreference | Tanaka, Y., Miyajima, T., Koike, I., Hayashibara, T., & Ogawa, H. ( 2007 ). Imbalanced coral growth between organic tissue and carbonate skeleton caused by nutrient enrichment. Limnology and Oceanography, 52 ( 3 ), 1139 – 1146. | |
dc.identifier.citedreference | Tanaka, Y., Suzuki, A., & Sakai, K. ( 2018 ). The stoichiometry of coral‐dinoflagellate symbiosis: Carbon and nitrogen cycles are balanced in the recycling and double translocation system. The ISME Journal, 12, 860 – 868. https://doi.org/10.1038/s41396‐017‐0019‐3 | |
dc.identifier.citedreference | Thurber, R. L. V., Burkepile, D. E., Fuchs, C., Shantz, A. A., McMinds, R., & Zaneveld, J. R. ( 2014 ). Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Global Change Biology, 20, 544 – 554. https://doi.org/10.1111/gcb.12450 | |
dc.identifier.citedreference | Tilman, D. ( 1982 ). Resource competition and community structure, Princeton, NJ: Princeton University Press. | |
dc.identifier.citedreference | Tremblay, P., Grover, R., Maguer, J. F., Hoogenboom, M., & Ferrier‐Pages, C. ( 2014 ). Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata. Coral Reefs, 33, 1 – 13. https://doi.org/10.1007/s00338‐013‐1100‐7 | |
dc.identifier.citedreference | Tremblay, P., Maguer, J. F., Grover, R., & Ferrier‐Pages, C. ( 2015 ). Trophic dynamics of scleractinian corals: Stable isotope evidence. Journal of Experimental Biology, 218, 1223 – 1234. https://doi.org/10.1242/jeb.115303 | |
dc.identifier.citedreference | Veal, C. J., Carmi, M., Fine, M., & Hoegh‐Guldberg, O. ( 2010 ). Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs, 29, 893 – 897. https://doi.org/10.1007/s00338‐010‐0647‐9 | |
dc.identifier.citedreference | Venn, A. A., Loram, J. E., & Douglas, A. E. ( 2008 ). Photosynthetic symbioses in animals. Journal of Experimental Botany, 59, 1069 – 1080. https://doi.org/10.1093/jxb/erm328 | |
dc.identifier.citedreference | Wiedenmann, J., D’Angelo, C., Smith, E. G., Hunt, A. N., Legiret, F. E., Postle, A. D., & Achterberg, E. P. ( 2013 ). Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Climate Change, 3, 160 – 164. https://doi.org/10.1038/nclimate1661 | |
dc.identifier.citedreference | Yeager, L. A., Allgeier, J. E., & Layman, C. A. ( 2011 ). Effects of heterogeneity at multiple spatial scales on fish community assembly. Oecologia, 167, 157 – 168. https://doi.org/10.1007/s00442‐011‐1959‐3 | |
dc.identifier.citedreference | Yellowlees, D., Rees, T. A., & Leggat, W. ( 2008 ). Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell and Environment, 31, 679 – 694. https://doi.org/10.1111/j.1365‐3040.2008.01802.x | |
dc.identifier.citedreference | Allgeier, J. E., Burkepile, D. E., & Layman, C. A. ( 2017 ). Animal pee in the sea: Consumer‐mediated nutrient dynamics in the world’s changing oceans. Global Change Biology, 23, 2166 – 2178. https://doi.org/10.1111/gcb.13625 | |
dc.identifier.citedreference | Allgeier, J. E., Layman, C. A., Montaña, C. G., Hensel, E., Appaldo, R., & Rosemond, A. D. ( 2018 ). Anthropogenic versus fish‐derived nutrient effects on seagrass community structure and function. Ecology, 99, 1792 – 1801. https://doi.org/10.1002/ecy.2388 | |
dc.identifier.citedreference | Allgeier, J. E., Layman, C. A., Mumby, P. J., & Rosemond, A. D. ( 2014 ). Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems. Global Change Biology, 20, 2459 – 2472. https://doi.org/10.1111/gcb.12566 | |
dc.identifier.citedreference | Allgeier, J. E., Layman, C. A., Mumby, P. J., & Rosemond, A. D. ( 2015 ). Biogeochemical implications of biodiversity loss across regional gradients of coastal marine ecosystems. Ecological Monographs, 85 ( 117 ), 132. | |
dc.identifier.citedreference | Allgeier, J. E., Layman, C. A., & Rosemond, A. D. ( 2011 ). Variation in nutrient limitation and seagrass nutrient content in Bahamian tidal creek ecosystems. Journal of Experimental Marine Biology and Ecology, 407, 330 – 336. https://doi.org/10.1016/j.jembe.2011.07.005 | |
dc.identifier.citedreference | Allgeier, J. E., Rosemond, A. D., Mehring, A. S., & Layman, C. A. ( 2010 ). Synergistic nutrient co‐limitation across a gradient of ecosystem fragmentation in subtropical mangrove‐dominated wetlands. Limnology and Oceanography, 55, 2660 – 2668. https://doi.org/10.4319/lo.2010.55.6.2660 | |
dc.identifier.citedreference | Allgeier, J. E., Yeager, L. A., & Layman, C. A. ( 2013 ). Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems. Ecology, 94, 521 – 529. https://doi.org/10.1890/12‐1122.1 | |
dc.identifier.citedreference | Anthony, K. R. N., & Fabricius, K. E. ( 2000 ). Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology, 252, 221 – 253. https://doi.org/10.1016/S0022‐0981(00)00237‐9 | |
dc.identifier.citedreference | Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. A., Grottoli, A. G., & Middlebrook, R. ( 2009 ). Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Functional Ecology, 23, 539 – 550. https://doi.org/10.1111/j.1365‐2435.2008.01531.x | |
dc.identifier.citedreference | Baker, A., & Cunning, R. ( 2012 ). Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nature Climate Change, 3, 259. https://doi.org/10.1038/nclimate1711 | |
dc.identifier.citedreference | Bruno, J. F., Cote, I. M., & Toth, L. T. ( 2019 ). Climate change, coral loss, and the curious case of the parrotfish paradigm: Why don’t marine protected areas improve reef resilience? Annual Review of Marine Science, 11 ( 11 ), 307 – 334. | |
dc.identifier.citedreference | Burnham, K. P., & Anderson, D. R. ( 2002 ). Model selection and multimodel inference: A practical information theoretic approach ( 2nd ed.). New York, NY: Springer‐Verlag. | |
dc.identifier.citedreference | Carr, M. H., & Hixon, M. A. ( 1995 ). Predation effects on early post‐settlement survivorship of coral reef fishes. Marine Ecology‐Progress Series, 124, 31 – 42. https://doi.org/10.3354/meps124031 | |
dc.identifier.citedreference | Carr, M. H., & Hixon, M. A. ( 1997 ). Artificial reefs: The importance of comparisons with natural reefs. Fisheries, 22, 28 – 33. https://doi.org/10.1577/1548‐8446(1997)022<0028:ARTIOC>2.0.CO;2 | |
dc.identifier.citedreference | Chapin, F. S., Matson, P. A., & Vitousek, P. ( 2011 ). Principles of terrestrial ecosystem ecology ( 2nd ed. ). New York, NY: Springer. | |
dc.identifier.citedreference | D’Angelo, C., & Wiedenmann, J. ( 2014 ). Impacts of nutrient enrichment on coral reefs: New perspectives and implications for coastal management and reef survival. Current Opinion in Environmental Sustainability, 7, 82 – 93. https://doi.org/10.1016/j.cosust.2013.11.029 | |
dc.identifier.citedreference | Doropoulos, C., Roff, G., Bozec, Y. M., Zupan, M., Werminghausen, J., & Mumby, P. J. ( 2016 ). Characterizing the ecological trade‐offs throughout the early ontogeny of coral recruitment. Ecological Monographs, 86, 20 – 44. | |
dc.identifier.citedreference | Dubinsky, Z., & Stambler, N. ( 1996 ). Marine pollution and coral reefs. Global Change Biology, 2, 511 – 526. https://doi.org/10.1111/j.1365‐2486.1996.tb00064.x | |
dc.identifier.citedreference | Dunne, J. A., Williams, R. J., & Martinez, N. D. ( 2002 ). Network structure and biodiversity loss in food webs: Robustness increases with connectance. Ecology Letters, 5, 558 – 567. https://doi.org/10.1046/j.1461‐0248.2002.00354.x | |
dc.identifier.citedreference | Ezzat, L., Maguer, J.‐F., Grover, R., & Ferrier‐Pagès, C. ( 2015 ). New insights into carbon acquisition and exchanges within the coral–dinoflagellate symbiosis under NH 4+ and NO 3− supply. Proceedings of the Royal Society of London B: Biological Sciences, 282. https://doi.org/10.1098/rspb.2015.0610 | |
dc.identifier.citedreference | Fabricius, K. E. ( 2005 ). Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Marine Pollution Bulletin, 50, 125 – 146. https://doi.org/10.1016/j.marpolbul.2004.11.028 | |
dc.identifier.citedreference | Fabricius, K. E. ( 2011 ). Factors determining the resilience of coral reefs to eutrophication: A review and conceptual model. In Z. Dubinsky & N. Stambler (Eds.), Coral reefs: An ecosystem in transition (pp. 493 – 505 ). Dordrecht, the Netherlands: Springer. https://doi.org/10.1007/978‐94‐007‐0114‐4 | |
dc.identifier.citedreference | Falkowski, P. G., Dubinsky, Z., Muscatine, L., & McCloskey, L. ( 1993 ). Population control in symbiotic corals. BioScience, 43, 606 – 611. https://doi.org/10.2307/1312147 | |
dc.identifier.citedreference | Gleason, D. F., & Hofmann, D. K. ( 2011 ). Coral larvae: From gametes to recruits. Journal of Experimental Marine Biology and Ecology, 408, 42 – 57. https://doi.org/10.1016/j.jembe.2011.07.025 | |
dc.identifier.citedreference | Grace, J. B., Schoolmaster, D. R., Guntenspergen, G. R., Little, A. M., Mitchell, B. R., Miller, K. M., & Schweiger, E. W. ( 2012 ). Guidelines for a graph‐theoretic implementation of structural equation modeling. Ecosphere, 3, 44. https://doi.org/10.1890/ES12‐00048.1 | |
dc.identifier.citedreference | Graham, E. M., Baird, A. H., & Connolly, S. R. ( 2008 ). Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs, 27, 529 – 539. https://doi.org/10.1007/s00338‐008‐0361‐z | |
dc.identifier.citedreference | Graham, E. M., Baird, A. H., Connolly, S. R., Sewell, M. A., & Willis, B. L. ( 2013 ). Rapid declines in metabolism explain extended coral larval longevity. Coral Reefs, 32, 539 – 549. https://doi.org/10.1007/s00338‐012‐0999‐4 | |
dc.identifier.citedreference | Graham, N. A. J., Wilson, S. K., Carr, P., Hoey, A. S., Jennings, S., & MacNeil, M. A. ( 2018 ). Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature, 559, 250 – 253. https://doi.org/10.1038/s41586‐018‐0202‐3 | |
dc.identifier.citedreference | Grottoli, A. G., Rodrigues, L. J., & Palardy, J. E. ( 2006 ). Heterotrophic plasticity and resilience in bleached corals. Nature, 440, 1186 – 1189. https://doi.org/10.1038/nature04565 | |
dc.identifier.citedreference | Harii, S., Yasuda, N., Rodriguez‐Lanetty, M., Irie, T., & Hidaka, M. ( 2009 ). Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals. Marine Biology, 156, 1203 – 1212. https://doi.org/10.1007/s00227‐009‐1162‐9 | |
dc.identifier.citedreference | Hatcher, B. G. ( 1988 ). Coral reef primary productivity – A beggar’s banquet. Trends in Ecology & Evolution, 3, 106 – 111. https://doi.org/10.1016/0169‐5347(88)90117‐6 | |
dc.identifier.citedreference | Hatcher, B. G. ( 1990 ). Coral reef primary productivity – A hierarchy of patterns and process. Trends in Ecology & Evolution, 5, 149 – 155. | |
dc.identifier.citedreference | Hixon, M. A., & Beets, J. P. ( 1989 ). Shelter characteristics and Caribbean fish assemblages – Experiments with artificial reefs. Bulletin of Marine Science, 44, 666 – 680. | |
dc.identifier.citedreference | Hoadley, K. D., Pettay, D. T., Dodge, D., & Warner, M. E. ( 2016 ). Contrasting physiological plasticity in response to environmental stress within different cnidarians and their respective symbionts. Coral Reefs, 35, 529 – 542. https://doi.org/10.1007/s00338‐016‐1404‐5 | |
dc.identifier.citedreference | Holbrook, S. J., Brooks, A. J., Schmitt, R. J., & Stewart, H. L. ( 2008 ). Effects of sheltering fish on growth of their host corals. Marine Biology, 155, 521 – 530. https://doi.org/10.1007/s00227‐008‐1051‐7 | |
dc.identifier.citedreference | Houlbreque, F., & Ferrier‐Pages, C. ( 2009 ). Heterotrophy in tropical scleractinian corals. Biological Reviews of the Cambridge Philosophical Society, 84, 1 – 17. https://doi.org/10.1111/j.1469‐185X.2008.00058.x | |
dc.identifier.citedreference | Humanes, A., Fink, A., Willis, B. L., Fabricius, K. E., de Beer, D., & Negri, A. P. ( 2017 ). Effects of suspended sediments and nutrient enrichment on juvenile corals. Marine Pollution Bulletin, 125, 166 – 175. https://doi.org/10.1016/j.marpolbul.2017.08.003 | |
dc.identifier.citedreference | Huntington, B. E., Miller, M. W., Pausch, R., & Richter, L. ( 2017 ). Facilitation in Caribbean coral reefs: High densities of staghorn coral foster greater coral condition and reef fish composition. Oecologia, 184, 247 – 257. https://doi.org/10.1007/s00442‐017‐3859‐7 | |
dc.identifier.citedreference | Jokiel, P. L., Maragos, J. E., & Franziskey, L. ( 1978 ). Coral growth: Buoyant weight technique. In D. R. Stoddart & R. E. Johannes (Eds.), Coral reefs: Research methods. UNESCO monographs on oceanographic methodology (pp. 529 – 542 ). Paris, France: UNESCO. | |
dc.identifier.citedreference | Lapointe, B. E., Brewton, R. A., Herren, L. W., Porter, J. W., & Hu, C. M. ( 2019 ). Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: A 3‐decade study. Marine Biology, 166, 31. | |
dc.identifier.citedreference | Layman, C. A., Allgeier, J. E., & Montaña, C. G. ( 2016 ). Mechanistic evidence of enhanced production on artificial reefs: A case study in a Bahamian seagrass ecosystem. Ecological Engineering, 95, 574 – 579. | |
dc.identifier.citedreference | Layman, C. A., Allgeier, J. E., Yeager, L. A., & Stoner, E. W. ( 2013 ). Thresholds of ecosystem response to nutrient enrichment from fish aggregations. Ecology, 94, 530 – 536. https://doi.org/10.1890/12‐0705.1 | |
dc.identifier.citedreference | Lefcheck, J. S. ( 2016 ). piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods in Ecology and Evolution, 7 ( 5 ), 573 – 579. https://doi.org/10.1111/2041‐210X.12512 | |
dc.identifier.citedreference | Levas, S., Grottoli, A. G., Schoepf, V., Aschaffenburg, M., Baumann, J., Bauer, J. E., & Warner, M. E. ( 2016 ). Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs, 35, 495 – 506. https://doi.org/10.1007/s00338‐015‐1390‐z | |
dc.identifier.citedreference | Lirman, D., & Fong, P. ( 2007 ). Is proximity to land‐based sources of coral stressors an appropriate measure of risk to coral reefs? An example from the Florida Reef Tract. Marine Pollution Bulletin, 54, 779 – 791. https://doi.org/10.1016/j.marpolbul.2006.12.014 | |
dc.identifier.citedreference | Marsh, J. A. ( 1970 ). Primary productivity or reef‐building calcareous red algae. Ecology, 51, 255 – 263. https://doi.org/10.2307/1933661 | |
dc.identifier.citedreference | Marubini, F., & Davies, P. S. ( 1996 ). Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Marine Biology, 127, 319 – 328. https://doi.org/10.1007/BF00942117 | |
dc.identifier.citedreference | McCann, K. S., Hastings, A., & Huxel, G. R. ( 1998 ). Weak trophic interactions and the balance of nature. Nature, 395, 794 – 798. https://doi.org/10.1038/27427 | |
dc.identifier.citedreference | Meyer, J. L., Schultz, E. T., & Helfman, G. S. ( 1983 ). Fish schools – An asset to corals. Science, 220, 1047 – 1049. https://doi.org/10.1126/science.220.4601.1047 | |
dc.identifier.citedreference | Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G., & Bay, L. K. ( 2019 ). Nutrient availability and metabolism affect the stability of coral‐symbiodiniaceae symbioses. Trends in Microbiology, 27, 678 – 689. https://doi.org/10.1016/j.tim.2019.03.004 | |
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