Low oxygen environments in marine, estuarine and fresh waters
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1 Low oxygen environments in marine, estuarine and fresh waters Oxygen Omnibus*: 25 years of [Open-Ocean] Oxygen Obs(ession) (an animal perspective) Liege, May 2014 Lisa A. Levin Center for Marine Biodiversity & Conservation Scripps Institution of Oceanography La Jolla, California *Omnibus - An anthology of previously released material linked together by theme or author
2 Low oxygen environments in marine, estuarine and fresh waters Paleoproxies Of Hypoxia Deoxygenation And Biochemical Cycles Modeling Hypoxia Deoxygenation in a global context Deoxygenation, marine resources, ecosystem functioning and structure of the foodweb Life and process in redox gradients Eastern Boundary Upwelling systems as natural SOLAS laboratories Oxygen time series and instrument developments
3 Oxygen minimum zone benthos DEOXYGENATION Oxygen as Hydrography OMZ as habitat animals/microbes Paleo/Future analogs O 2 as a multistressor Oxygen in IPCC AR5 Anthropocene OMZ Community Structure Bioturbation Community Function expanding OMZs Volcano 7 Oman Peru Chile CA, OR Pakistan India Costa Rica Namibia soca Bay of Bengal
4 Oxygen Term coined in 1777 by Antoine Lavoisier from the Greek roots: oxys, "acid", literally "sharp and genes, literally "begetter it was mistakenly thought that all acids required oxygen 211 years later
5 Discovering the Oxygen minimum zone on Volcano 7 Alvin Dive 2141 Nov Shrimp, Rattails: 900 m Brittle Stars: 850 m 750 m 3.5 mm Upper Summit Crabs, sponges: 800 m
6 Microbes Meiofauna Macrofauna Megafauna protozoan Volcano 7 metazoan Levin et al Wishner et al micron > 63micron >0.3 mm > 1 cm BIG Volcano 7 Levin et al Volcano 7 E. Tropical Pacific Body size influences oxygen thresholds. Small taxa are more tolerant. Density maxima occur just above thresholds.
7 Similar OMZ edge effects are evident worldwide with depressed densities in the OMZ and elevated densities at ml/l (4-9 mm) O 2 Peru margin Rowe 1971 Off Walvis Bay Sanders 1969 Oman margin Levin et al Macrofauna (> 0.3 mm) W. India margin 1100 Volcano 7, Mexico Levin et al Levin et al Central CA margin Mullins et al. 1985
8 1990s Oman Margin soft bodies dominate POLYCHAETE DOMINANCE ZONATION DIVERSITY SHIFTS Levin et al. 2000
9 Hypoxia homogenizes at small scales, Induces heterogeneity at larger scales OMZ 700 m 400 m Oman margin macrofauna 850 m 1000 m 1250 m OMZ 3400 m MDS PLOT Levin et al DSR II
10 1998 Peru: Bioturbation without deposit feeding and without much O 2! Gutless phallodrilinid oligochaetes bioturbate Peru Basin sediments 305 m 1 mm O 2 Santa Barbara Basin 505 m 15 mm O 2 Lucinoma aequizonata bioturbtation Levin et al Paleo 3
11 Chile: OMZs as chemosynthetic ecosystems! Non OMZ invertebrates 100, 500, 800 m Use of alternative metabolic pathways through symbiosis Olavius crassitunicatus (Oligochaeta) in Peru Basin (300 m) d 15 N Thioploca Lucinids OMZ annelids, nematodes m Thysirids Acharax frenulates
12 Pakistan Margin: Translating structure to function Transition Zone
13 Increasingly deeper abundance maxima reflect size-specific oxygen thresholds on the Pakistan Margin Foraminifera Macrofauna Megafauna Nekton Gooday et al. 2009, DSR II
14 DIVERSITY shifts rapidly across oxygen gradients Pakistan Margin 2003 Pakistan margin macrofauna - Lower OMZ Depth (m) Pre Monsoon Post Monsoon Dissolved Oxygen (ml/l) Levin et al DSR II
15 Sharp thresholds for bioturbation 700 m 737 m 800m 850m ml/l ml/l ml/l ml/l 900 m 940 m ml/l ml/l 1050 m 1100 m ml/l ml/l Levin et al DSR II
16 Laminae in the presence of burrowers! Linopherus sp. 97% of fauna at 850 m, Pakistan margin, 850 m 4, ind m g m ml/l Oxygen Jeffries et al MEPS
17 Hypoxia increases role of protozoans over metazoans in the remineralization processes ug 13C Post monsoon Premonsoon 13 C-Diatom uptake experiments on the Pakistan Margin Protozoa Oxystat controlling T and O Series1 Series2 Cossura Protozoans dominate C uptake at 300 m, and postmonsoon at 140 m when oxygen is < 5mM (0.11ml/l) Post-Monsoon Comparison of Label Uptake by macrofauna and Forams Macrofauna Foraminifera day day 140 in situ day day 300 in situ day 940 in situ day Animals dominate C uptake before (normoxic) the monsoon, and at 940 m where O 2 is > 7mM (0.16 ml/l) Uvigerina Metazoa Cossuridae Ampharetidae Woulds et al. 2007, 2009
18 Over 1.1 million km 2 of continental margin seafloor is naturally hypoxic One can use the upper & lower OMZ boundaries combined with seafloor topography to calculate area of hypoxic seabed. Image courtesy of J. Helly,, SDSC
19 India Margin - Shinkai 6500 Oct Bregmaceros sp. 535 m 700 m (< 0.02 ml/l O 2 ) (< 0.02 ml/l O 2 ) 2008 W. India Margin Off Goa 16 o N Collaboration with H. Kitazato 815 m (0.05 ml/l O 2 ) 900 m mm O 2 ) 850 m (0.07 mm O 2 ) 1100 m 2000 m (0.4 ml/l O 2 ) 2.3 ml/l O 2 )
20 Density (ind m^-2) Hypoxia reduces faunal resilience and recovery potential 4 to 8 day colonization on the W. India Margin Depth O 2 % OrgC Time (mm) to 6 4 d to 4.8 4,8 d to d No macrofaunal colonizers 4.3% 0 Depth (m) O 2 (mm) 0.1 Depth 1-2 (m) 20 Colonization: no colonization limited high Levin et al. in prep. 151% Background Colonizers
21 OMZ benthos as a (retrospective) living laboratory Animal evolution Trophic structure Oxygen as one of multiple stressors
22 Oxygenation and advent of carnivory may help explain the timing and nature of the Cambrian Explosion (540 MY) Sperling et al., 2013, PNAS 110: 13446
23 Does oxygen control carnivory in modern OMZs? energetically expensive:high mobility, demanding digestion S. California Baja Volcano 7 seamount Oman Pakistan India Bay of Bengal Chile Sperling et al., 2013, PNAS 110: Dataset: polychaete species - 10 published studies - 68 stations
24 Low Oxygen is associated with loss of carnivores in OMZs Sperling et al., 2013, PNAS 110: ANOVA: F 3, 64 = 20.4 p < ANOVA: F 3, 64 = p < of 28 stations (50%) have zero predators
25 Does oxygen affect trophic diversity across the OMZ? (as reflected by Stable Isotopic Metrics) Carbon Range Standard Elliptical Area d 15 N Species averages d 15 N Nitrogen Range d 13 C d 13 C Layman et al Jackson et al Deposit-feeders Carnivores Filter-feeders Chemosynthetic
26 Low oxygen may enhance trophic diversity! STABLE ISOTOPE METRICS (from 29 stations at 7 margin locations) Range d 15 N O 2 (ml/l) < > 0.4 Range d 13 C O 2 (ml/l) < > 0.4 Centroid Distance Standard Elliptical Area [ corrected] O 2 (ml/l) < > 0.4 O 2 (ml/l) < > 0.4
27 y y Northern California Group Group Group Group Trophic diversity (SEAc) is highest within the OMZ in the NE Pacific 800 m 0.25 ml/l Southern California x Group Group Group Group Group NA 800 m 0.29 ml/l x
28 Using strong gradients on OMZ/CMZ margins to unravel effects of climate stressors (O 2, pco 2, and T) on benthos Macrobenthos: Diversity Evenness Density NW Arabian Sea 92 macrobenthos stations Variance Partitioning: Random Forest/ Regression Tree
29 Random Forest Diversity H Regression Tree 49% var 8% var Evenness J 92 Stations Upwelling margins Density Density 24% var 9% var
30 2008- Present Deoxygenation Expanding Oxygen Minimum Zones High Frequency Variation Multiple Stressors
31 2010 (ARMS) 2008 Nature 2008 (GRL) Warsaw 2013 Natalya Gallo 2013 Plos Biol.
32 IPCC AR5 WG2 Chapter 6. Summary The expansion of hypoxic regions termed Oxygen Minimum Zones (OMZs) and anoxic dead zones, observed over the last 50 years and projected into the future under climate change, especially if combined with nutrient enrichment (eutrophication), will constrain the habitat of O 2 -dependent organisms and benefit anaerobic microbes (medium confidence).
33 O 2 in vs from m in tropics, subtropics At 200 m the area with < 70 mm O 2 has increased by 4.5 million km 2 area Stramma et al. 2010
34 25-50 year OXYGEN DECLINES in the NORTHEAST PACIFIC OCEAN Station P Stn P CALCOFI 26.9 isopycnal Oxygen loss of 0.67mM O 2 /y Whitney et al % decline in oxygen at m off southern CA over 22 y Shoaling of the hypoxic upper boundary (63mM) DZ max = -92 m San Diego Bograd et al. 2008
35 What are the relevant time & space scales of O 2 variation?! Diel Diurnal! Episodic/ Periodic Seasonal Upwelling OMZ Rabalais et al. 2010, Biogeosciences anthropogenic natural
36 REGIME SCALE McClatchie et al TIME SCALES OF VARIATION SOUTHERN CALIFORNIA ENSO Nam et al SEASONAL Send & Nam 2012 Oxygen and ph co-vary ph DO SEMIDIURNAL DIEL Frieder et al. unpubl. EVENT SCALE Send and Nam 2012
37 Small-Scale Spatial Variation in O 2 on the So. Cal Shelf Sharp Vertical Gradients Nov - Dec 2010 La Jolla Kelp Forest Jan Feb m 17 m 7 m 17 m Inshore-Offshore Gradients Oxygen (umol/kg) SD Coastal Expedition Bograd et al vs 1.9km Frieder et al. 2012, Biogeosciences
38 Laboratory Experiments to test effects of multiple stressors Geochemical Proxy development for faunal carbonates Baltic Cod Otoliths Limburg et al Mytilus larval shells Frieder 2014 R 2 =0.23
39 - Oxygen interacts with other climate stressors and anthropogenic stressors on continental margins CO 2 CO 2 Oil spill Acidification Eutrophication Deoxygenation Methane Release Seafloor mining Modified from Levin et al. 2009, Biogeosciences
40 Resource Extraction in OMZs Marine Phosphates -an emerging margin resource are associated with coastal upwelling Marine Geochemistry, Schulz
41 The Namibian phosphate mining interests in the OMZ coincide with highly productive fishery habitat Beggiatoa and Thiomargarita mats, Walvis Bay, Namibia Bearded goby hake OMZ expansion & warming could slow recovery from mining Horse mackerel Utne-Palm et al. (Science 2010)
42 Oxygen minimum zone benthos DEOXYGENATION Oxygen as Hydrography OMZ as habitat animals/microbes Paleo/Future analogs O 2 as a multistressor Oxygen in IPCC AR5 Anthropocene OMZ Community Structure Bioturbation Community Function expanding OMZs Volcano 7 Oman Peru Chile CA, OR Pakistan India Costa Rica Namibia soca Bay of Bengal
43 Acknowledgements Thanks to all my OMZ collaborators especially: G. Cowie, C. Woulds, J. Gage, A. Gooday, K. Wishner, V. Gallardo, D. Gutierrez, P. Lamont, J. Helly, H. Kitazato, R. Lee, A. Rathburn, K. Oguri, U.Witte, W. Hunter, H. Nomaki, B. Currie, A. Raman Present and Past Levin Lab/SIO Contributors: C. Frieder, G. Mendoza, J. Gonzalez, C. Neira, M. Navarro, A. McGreggor, A. Cau, C. Whitcraft, J. Crooks, T. Martz, U. Send, S. Nam Unpublished data from F. Whitney, Support Provided By: National Science Foundation, CA Sea Grant, UC Mexus, INDEEP, NATO, NERC, JAMSTEC, OCB Thanks to all of you for listening!
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