Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales.
Losses of corals worldwide emphasize the need to understand what drives reef decline. Stressors such as overfishing and nutrient pollution may reduce resilience of coral reefs by increasing coral-algal competition and reducing coral recruitment, growth and survivorship. Such effects may themselves develop via several mechanisms, including disruption of coral microbiomes. Here we report the results of a 3-year field experiment simulating overfishing and nutrient pollution. These stressors increase turf and macroalgal cover, destabilizing microbiomes, elevating putative pathogen loads, increasing disease more than twofold and increasing mortality up to eightfold. Above-average temperatures exacerbate these effects, further disrupting microbiomes of unhealthy corals and concentrating 80% of mortality in the warmest seasons. Surprisingly, nutrients also increase bacterial opportunism and mortality in corals bitten by parrotfish, turning normal trophic interactions deadly for corals. Thus, overfishing and nutrient pollution impact reefs down to microbial scales, killing corals by sensitizing them to predation, above-average temperatures and bacterial opportunism.
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Jesse R
JR
Zaneveld
Department of Biological Sciences, Florida International University, 3000 NE 151st St, North Miami, Florida 33181, USA.|Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California 93106-9610, USA.
Deron E
DE
Burkepile
Department of Biological Sciences, Florida International University, 3000 NE 151st St, North Miami, Florida 33181, USA.
Andrew A
AA
Shantz
Department of Biological Sciences, Florida International University, 3000 NE 151st St, North Miami, Florida 33181, USA.|Department of Ecosystem Sciences, Penn State University, 235 Forest Resources Building, University Park, Pennsylvania 16802, USA.
Catharine E
CE
Pritchard
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Ryan
R
McMinds
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Jérôme P
JP
Payet
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Rory
0000-0003-2448-0128
R
Welsh
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.|Department of BioSciences, Rice University, 6100 Main Street, Houston, Texas 77005, USA.
Adrienne M S
AM
Correa
Department of Biological Sciences, Florida International University, 3000 NE 151st St, North Miami, Florida 33181, USA.
Nathan P
NP
Lemoine
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Stephanie
S
Rosales
Department of Biology, University of Florida, Gainesville, Florida 32611, USA.
Corinne
C
Fuchs
SymbioSeas and Marine Applied Research Center, Wilmington, North Carolina, 28411, USA.|Laboratoire d'Excellence «CORAIL» USR 3278 CNRS - EPHE, CRIOBE, Papetoai, Polynésie Française.
Jeffrey A
JA
Maynard
Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, Oregon 97331, USA.
Rebecca Vega
RV
Thurber
D000818:Animals; D037421:Anthozoa / Q000254:growth & development / Q000382:microbiology; D044822:Biodiversity; D057894:Coral Reefs; D004787:Environmental Pollution; D005068:Eutrophication; D005398:Fisheries; D060434:Herbivory / Q000502:physiology; D064307:Microbiota; D011235:Predatory Behavior; D012621:Seasons; D013696:Temperature