Rewiring coral: Anthropogenic nutrients shift diverse coral-symbiont nutrient and carbon interactions toward symbiotic algal dominance

被引:19
作者
Allgeier, Jacob E. [1 ]
Andskog, Mona A. [1 ]
Hensel, Enie [2 ]
Appaldo, Richard [1 ]
Layman, Craig [2 ]
Kemp, Dustin W. [3 ]
机构
[1] Univ Michigan, Dept Ecol & Evolutionary Biol, Ann Arbor, MI 48109 USA
[2] North Carolina State Univ, Dept Appl Ecol, Raleigh, NC USA
[3] Univ Alabama Birmingham, Dept Biol, Birmingham, AL 35294 USA
基金
美国国家科学基金会;
关键词
coral reefs; eutrophication; fish nutrient supply; marine conservation; nitrogen; phase shift; phosphorus; Symbiodiniaceae; symbiosis; REEF PRIMARY PRODUCTIVITY; ENVIRONMENTAL-STRESS; ARTIFICIAL REEFS; FISH; ENRICHMENT; DYNAMICS; ZOOXANTHELLAE; HETEROTROPHY; INCREASES; COMMUNITY;
D O I
10.1111/gcb.15230
中图分类号
X176 [生物多样性保护];
学科分类号
090705 ;
摘要
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 palmataandPorites 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.
引用
收藏
页码:5588 / 5601
页数:14
相关论文
共 82 条
[1]   Anthropogenic versus fish-derived nutrient effects on seagrass community structure and function [J].
Allgeier, Jacob E. ;
Layman, Craig A. ;
Montana, Carmen G. ;
Hensel, Enie ;
Appaldo, Richard ;
Rosemond, Amy D. .
ECOLOGY, 2018, 99 (08) :1792-1801
[2]   Animal pee in the sea: consumer-mediated nutrient dynamics in the world's changing oceans [J].
Allgeier, Jacob E. ;
Burkepile, Deron E. ;
Layman, Craig A. .
GLOBAL CHANGE BIOLOGY, 2017, 23 (06) :2166-2178
[3]   Biogeochemical implications of biodiversity and community structure across multiple coastal ecosystems [J].
Allgeier, Jacob E. ;
Layman, Craig A. ;
Mumby, Peter J. ;
Rosemond, Amy D. .
ECOLOGICAL MONOGRAPHS, 2015, 85 (01) :117-132
[4]   Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems [J].
Allgeier, Jacob E. ;
Layman, Craig A. ;
Mumby, Peter J. ;
Rosemond, Amy D. .
GLOBAL CHANGE BIOLOGY, 2014, 20 (08) :2459-2472
[5]   Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems [J].
Allgeier, Jacob E. ;
Yeager, Lauren A. ;
Layman, Craig A. .
ECOLOGY, 2013, 94 (02) :521-529
[6]   Variation in nutrient limitation and seagrass nutrient content in Bahamian tidal creek ecosystems [J].
Allgeier, Jacob E. ;
Rosemond, Amy D. ;
Layman, Craig A. .
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY, 2011, 407 (02) :330-336
[7]   Synergistic nutrient colimitation across a gradient of ecosystem fragmentation in subtropical mangrove-dominated wetlands [J].
Allgeier, Jacob E. ;
Rosemond, Amy D. ;
Mehring, Andrew S. ;
Layman, Craig A. .
LIMNOLOGY AND OCEANOGRAPHY, 2010, 55 (06) :2660-2668
[8]  
[Anonymous], 2011, Principles of Terrestrial Ecosystem Ecology
[9]   Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching [J].
Anthony, Kenneth R. N. ;
Hoogenboom, Mia O. ;
Maynard, Jeffrey A. ;
Grottoli, Andrea G. ;
Middlebrook, Rachael .
FUNCTIONAL ECOLOGY, 2009, 23 (03) :539-550
[10]   Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity [J].
Anthony, KRN ;
Fabricius, KE .
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY, 2000, 252 (02) :221-253