What factors influence (1) inter- and intraspecific tolerances to environmental stressors and what are the implications for (2) community responses to global change?
My research combines laboratory and field experiments with long-term monitoring to understand the effects of global change stressors (ocean acidification, warming, hypoxia, nutrient pollution) on key marine organisms and communities. I typically focus on crustose coralline algae (CCA) and other calcifying algae as model organisms based on their global distribution and critical ecological functions.
My research uses field and laboratory approaches to test the effects of global change stressors on key marine organisms and ecosystems.
BIOTIC DRIVERS OF ORGANISMAL TOLERANCES TO GLOBAL CHANGE
Ocean acidification (OA), warming, hypoxia and nutrient pollution have detrimental consequences for marine ecosystems, particularly those that are dominated by calcium-carbonate secreting organisms (calcifiers). My research focuses on the effects of global stressors on coral and oyster reefs because of their ecological and economic importance. One core theme of my research is to identify biotic factors underlying inter- and intraspecific tolerances (or susceptibility) to environmental stress associated with global change.
Eleven species of algae used in experiments on Palmyra Atoll (from Johnson et al. 2014).
Taxa-specific calcification increases susceptibility to OA
Using controlled OA experiments on Palmyra Atoll, we demonstrated that not all algae are created equal in their response to simulated OA. Using a meta-analysis of our own OA experiments with 11 species of tropical algae, we found that elevated CO2 increased growth rates of fleshy macroalgae, but decreased growth rates of crustose coralline algae (CCA) and upright calcareous algae. These results have important implications for community structure of coral reefs in the near-future if decreasing pH (increasing CO2) facilitates the growth of some taxa over others.
Johnson MD, NN Price, JE Smith (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411. DOI 10.7717/peerj.411
Acclimatization of crustose coralline algae to OA
From field surveys of in situ carbonate chemistry on shallow reefs of Moorea, French Polynesia, I found that the magnitude of pH variability over one day can exceed projected decreases in pH due to OA by the end of the century. Prior exposure to natural pH variability increased calcification rates of the reef-building crustose coralline alga Porolithon onkodes during subsequent exposure to high pH variability, relative to the same species from a nearby reef with diurnally stable pH. These findings indicate that inherent environmental variability has long-lasting effects on CCA calcification rates and on their responses to subsequent exposure to pH variability. However, prior exposure to high pH variability did not increase CCA tolerances to OA, which has been a prevailing theory in recent studies.
Johnson MD, VW Moriarty, RC Carpenter (2014) Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2. PloS One 9(2): e87678
We exposed Porolithon onkodes (top), a common reef-building CCA on Pacific coral reefs, to stable and variable pH in mesocosm facilities in Moorea, French Polynesia (bottom).
ABIOTIC DRIVERS OF ORGANISMAL TOLERANCES
Coastal natural ecosystems are often highly variable with respect to environmental conditions including pH and temperature. This inherent variability provides and important context to global change experiments, and may either promote acclimatization to environmental change or increase susceptibility. My research characterizes the magnitude of environmental variability on nearshore, shallow reefs and then uses this context to frame lab experiments. Furthermore, the combination of multiple co-occurring stressors in natural systems could lead to differences in organismal responses to global change. Thus, we need to understand potential synergisms between co-occurring stressors such as OA, warming, and nutrient pollution.
DIEL PH VARIABILITY
The applicability of OA predictions to nearshore systems remains unclear, because they are modeled on the open ocean where conditions are stable over time. On reefs in Hawaii, I found that diel pH variability on shallow reefs often surpass year 2100 OA predictions. In Panamá, I found that, rather than increasing tolerances to OA as predicted by ecological theory, simultaneous exposure to pH variability exacerbated the effects of OA on CCA calcification. Moreover, history of exposure to extreme variability can have lasting negative legacy effects on subsequent responses of corallines to OA in the lab. These findings imply that some ecosystems with dynamic pH regimes may be more sensitive, and not more resilient, to global change.
Johnson MD, LM Rodriguez, SE O'Connor, NF Varley, AH Altieri (2019) pH variability exacerbates effects of ocean acidification on a Caribbean crustose coralline alga. Frontiers in Marine Science 6(150). DOI 10.3389/fmars.2019.00150
Johnson MD, LM Rodriguez Bravo¥, N Lucey, AH Altieri (2021) Environmental legacy effects and acclimatization of a crustose coralline alga to ocean acidification. Climate Change Ecology. 100016. DOI 10.1016/j.ecochg.2021.100016
We exposed a common Caribbean crustose coralline alga to stable and variable pH in wet lab facilities in Bocas del Toro, Panama.
The combination of multiple co-occurring stressors in natural systems could lead to differences in organismal responses to global change. Thus, we need to understand potential synergisms between co-occurring stressors such as OA, warming, and nutrient pollution. Further, these synergisms likely vary depending on background environmental conditions so comparable research must be conducted over broad spatial scales. In Hawaii, I found that OA and warming synergistically decreased CCA calcification rates and increased susceptibility to damage by sea urchin grazing (Johnson & Carpenter 2012). In French Polynesia, I found that temperature exacerbated the effects of OA on turf algal assemblages (Johnson et al. 2017). This implies that warmer, more acidic waters may fuel growth of algal turfs, which are frequent and dominant competitors with reef-building corals. In a subsequent experiment, increased availability of nitrogen (simulating pollution) offset negative effects of OA on CCA calcification (Johnson & Carpenter 2018). Collectively, these results indicate that, not only do common global stressors interact to drive organismal responses, but also that their combined effects can vary as a function of background environmental conditions.
Johnson MD, RC Carpenter (2012) Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. Journal of Experimental Marine Biology and Ecology 434: 94-101
Johnson MD, S Comeau, C Lantz, JE Smith (2017) Complex and interactive effects of ocean acidification and temperature on epilithic and endolithic coral reef turf algal assemblages. Coral Reefs. DOI 10.1007/s00338-017-1597-2
Johnson MD, RC Carpenter (2018) Nitrogen enrichment offsets the direct negative effects of ocean acidification on a reef-building crustose coralline alga. Biology Letters. DOI 10.1098/rsbl.2018.0371
In a series of experiments, I tested the combined effects of sea urchin grazing and warming on a reef-building CCA (top), warming and OA on ubiquitous turf algae (middle), and nitrogen enrichment and OA on CCA (bottom).
DEOXYGENATION AS AN EMERGING STRESSOR ON CORAL REEFS
Hypoxia caused by ocean deoxygenation is one of the lesser-known evils associated with local and global environmental change, particularly on coral reefs. Depletion of oxygen resulting from warmer water temperatures and local nutrient pollution, among other factors, can have catastrophic consequences for benthic communities.
Acute Deoxygenation on a Caribbean coral reef
In Sept. 2017 we documented the first repeat of a massive acute deoxygenation and mass mortality event on coral reefs in Bahia Almirante, Bocas del Toro Panama. As part of a collaborative effort with researchers from the Smithsonian Tropical Research Institute, we uncovered the immediate and long-term response of benthic corals and associated microbial communities to the acute event while it was in progress. We found that the deoxygenation event was associated with coral bleaching and mortality, resulting in a 50% decrease in live coral cover. The loss in live coral cover was apparent a year after the event. The microbial community associated with the impacted coral reef shifted in response to the event, with taxa representative of hypoxic conditions, but the microbial community rapidly reverted to a normoxic assemblage within a month of the event.
Johnson MD, JS Scott, M Leray, N Lucey, LM Rodriguez Bravo, W Wied, AH Altieri (2021) Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef. Nature Communications. 12(4522). DOI 10.1038/s41467-021-24777-3.
Johnson MD, LM Rodriguez, AH Altieri (2018) Shallow-water hypoxia and mass mortality on a Caribbean coral reef. Bulletin of Marine Science. 94. DOI 10.5343/bms.2017.1163
Brittle stars and sea urchins were among the mass mortalities of the hypoxia event (from Johnson et al. 2018)
Coral tolerances to ocean deoxygenation
The acute deoxygenation event in 2017 spurred a series of laboratory-based experiments to identify how reef-building corals are affected by exposure to chronic ocean deoxygenation. Through a grant from NOAA's Coastal Hypoxia Research Program, I developed and built facilities at the Smithsonian Marine Station in Fort Pierce, FL to test effects of deoxygenation on different coral species. From our first set of experiments, conducted in 2019, we found that different key species of coral have dramatically different hypoxia-thresholds. The staghorn coral Acropora cervicornis was highly sensitive to extreme deoxygenation, on par with levels experience during an acute event. Conversely, the boulder coral Orbicella faveolata was highly tolerant and persisted under extreme conditions for nearly two weeks with virtually no detectable effects. Notably, both species were tolerant to levels of deoxygenation that are lethal for other marine taxa, indicating that some reef corals have higher hypoxia thresholds than expected.
This work is possible through funding from NOAA's CHRP, with co-PI's Andrew Altieri of the University of Florida and Valerie Paul of the Smithsonian Marine Station, and through the hard work of students and interns, including Sara Swaminathan, Emily Nixon, and Tessa Vekich.
Johnson MD, SD Swaminathan, EN Nixon, V Paul, AH Altieri (2021) Differential
susceptibility of reef-building corals to deoxygenation reveals remarkable hypoxia tolerance. Scientific Reports. 11(23168). DOI 10.1038/s41598-021-01078-9
Acropora cervicornisl suffered tissue loss in response to extreme deoxygenation after just days of exposure to treatment conditions, while Orbicella faveolata remained unaffected under the same conditions for nearly two weeks (Johnson et al. 2021).