Abstract
The organisms that inhabit Oxygen Minimum Zones (OMZ) have specialized adaptations that allow them to survive within a very narrow range of environmental conditions. Consequently, even small environmental perturbations can result in local species distribution shifts that alter ecosystem trophodynamics. Here, we examined the effect of changing sea water temperatures and oxygen levels on the physiological performance and metabolic traits of the species forming marine demersal communities along the OMZ margins in the Costa Rican Pacific. The strong temperature and oxygen gradients along this OMZ margin provide a “natural experiment” to explore the effects of warming and hypoxia on marine demersal communities. We identified two distinct marine fauna communities separated by an environmental oxygen partial pressure threshold of 0.003–0.009 atm. The community inhabiting cooler waters with less oxygen was comprised of species with very low oxygen demands, while the second community inhabiting warmer waters with more oxygen was comprised by a higher diversity of species with higher oxygen demands. We also compared the community composition across different El Niño Southern Oscillation phases. During “neutral” and El Niño conditions, with relatively warmer temperatures and higher oxygen levels, species’ average oxygen demand was higher, and species stayed at greater depths than during the cooler, low oxygen, La Niña phases. Our findings suggest that the effects of environmental temperature and oxygen levels on the structure of demersal communities within OMZs can be predicted by understanding species’ oxygen demand. This study highlights the vulnerability of demersal ecosystem structures surrounding the Costa Rican OMZ to deoxygenation and warming under climate change.
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Data available upon request.
Code availability
Code for the Aerobic Growth Index published and available upon request. Clarke TM, Wabnitz CC, Striegel S, Frölicher TL, Reygondeau G, Cheung W W (2021) Aerobic growth index (AGI): An index to understand the impacts of ocean warming and deoxygenation on global marine fisheries resources. Progress in Oceanography 195: 102588. 10.1016/j.pocean.2021.102588.
References
A Paulmier Ruiz-Pino, 2009 Oxygen minimum zones (OMZs) in the modern ocean Prog Oceanogr 80 113 28 https://doi.org/10.1016/j.pocean.2008.08.001
Arana PM, Wehrtmann IS, Orellana JC, Nielsen-Muñoz V, Villalobos-Rojas F (2013) By-catch associated with fisheries of Heterocarpus vicarius (Costa Rica) and Heterocarpus reedi (Chile) (Decapoda: Pandalidae): A six-year study (2004–2009). J Crustac Biol 33:198–209. https://doi.org/10.1163/1937240X-00002123
Bertrand A, Chaigneau A, Peraltilla S, Ledesma J, Graco M, Monetti F, Chavez FP (2011) Oxygen: a fundamental property regulating pelagic ecosystem structure in the coastal southeastern tropical Pacific. PLOS ONE 6:e29558. https://doi.org/10.1371/journal.pone.0029558
Bianchi G (1991) Demersal assemblages of the continental shelf and slope edge between the Gulf of Tehuantepec ( Mexico ) and the Gulf of Papagayo ( Costa Rica ) Mar Ecol Prog Ser 73: 121–140.
Bopp L, Resplandy L, Orr JC, Doney SC, Dunne JP, Gehlen M, Halloran P, Heinze C, Ilyina T, Séférian R, Tjiputra J, Vichi M (2013) Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10:6225–6245. https://doi.org/10.5194/bg-10-6225-2013
Cabré A, Marinov I, Bernardello R, Bianchi D (2015) OMZs in the tropical Pacific across CMIP5 models: mean state differences and climate change trends. Biogeosciences 12:5429–5454. https://doi.org/10.5194/bg-12-5429-2015
Cheung WWL, Lam VWY, Sarmiento JL, Kearney K, Watson R, Pauly D (2009) Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish 10:235–251. https://doi.org/10.1111/j.1467-2979.2008.00315.x
Cheung WWL, Dunne J, Sarmiento JL, Pauly D (2011) Integrating ecophysiology and plankton dynamics into projected maximum fisheries catch potential under climate change in the northeast Atlantic. ICES J Mar Sci 68:1008–1018. https://doi.org/10.1093/icesjms/fsr012
Cheung WWL, Sarmiento JL, Dunne J, Frölicher TL, Lam VWY, Deng Palomares ML, Watson R, Pauly D (2013a) Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat Clim Change 3:254–258. https://doi.org/10.1038/nclimate1691
Cheung WWL, Watson R, Pauly D (2013b) Signature of ocean warming in global fisheries catch. Nature 497:365–368. https://doi.org/10.1038/nature12156
Chu JWF, Gale KSP (2017) Ecophysiological limits to aerobic metabolism in hypoxia determine epibenthic distributions and energy sequestration in the northeast Pacific ocean. Limnol Oceanogr 62:59–74. https://doi.org/10.1002/lno.10370
Claireaux G, Chabot D (2016) Responses by fishes to environmental hypoxia: integration through Fry’s concept of aerobic metabolic scope. J Fish Biol 88:232–251. https://doi.org/10.1111/jfb.12833
Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905. https://doi.org/10.1046/j.1365-2656.1999.00337.x
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18(1):117–143
Clarke TM, Naranjo-Elizondo B, Angulo A, Romero-Chaves R, Wehrtmann IS, Espinoza M (2022) Demersal fish assemblages in the Oxygen Minimum Zone along the Pacific coast of Costa Rica, Eastern Tropical Pacific Ocean. In prep
Clarke TM, Wabnitz CC, Striegel S, Frölicher TL, Reygondeau G, Cheung WW (2021) Aerobic growth index (AGI): an index to understand the impacts of ocean warming and deoxygenation on global marine fisheries resources. Prog Oceanogr 195:102588. https://doi.org/10.1016/j.pocean.2021.102588
Cocco V, Joos F, Steinacher M, Frölicher TL, Bopp L, Dunne J, Gehlen M, Heinze C, Orr J, Oschlies A, Schneider B (2013) Oxygen and indicators of stress for marine life in multi-model global warming projections. Biogeosciences 10:1849–68. https://doi.org/10.5194/bg-10-1849-2013
Craig JK (2012) Aggregation on the edge: effects of hypoxia avoidance on the spatial distribution of brown shrimp and demersal fishes in the northern Gulf of Mexico. Mar Ecol Prog Ser 445:75–95. https://doi.org/10.3354/meps09437
Danabasoglu G, Lamarque JF, Bacmeister J, Bailey DA, DuVivier AK, Edwards J, Emmons LK, Fasullo J, Garcia R, Gettelman A, Hannay C, Holland MM, Large WG, Lauritzen PH, Lawrence DM, Lenaerts JTM, Lindsay K, Lipscomb WH, Mills MJ, Strand WG (2020) The Community Earth System Model Version 2 (CESM2) J Adv Model Earth Syst 12: e2019MS001916. https://doi.org/10.1029/2019MS001916
Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB (2015) Climate change tightens a metabolic constraint on marine habitats. Science 348:1132–1135. https://doi.org/10.1126/science.aaa1605
Froese R, Pauly D (2019) FishBase. https://www.fishbase.org/
Frölicher TL, Joos F, Plattner GK, Steinacher M, Doney SC (2009) Natural variability and anthropogenic trends in oceanic oxygen in a coupled carbon cycle–climate model ensemble. Glob Biogeochem Cycles 23. https://doi.org/10.1029/2008GB003316
Gagné TO, Reygondeau G, Jenkins CN, Sexton JO, Bograd SJ, Hazen EL, Houtan KSV (2020) Towards a global understanding of the drivers of marine and terrestrial biodiversity. PLOS ONE 15:e0228065. https://doi.org/10.1371/journal.pone.0228065
Gallardo M, Rojas I, Brokordt K, Lovrich G, Nuñez V, Paschke K, Thiel M, Yannicelli B (2019) Life on the edge: incubation behaviour and physiological performance of squat lobsters in oxygen-minimum conditions. Mar Ecol Prog Ser 623:51–70. https://doi.org/10.3354/meps12984
Gallo ND, Levin LA (2016) Chapter Three - Fish ecology and evolution in the World’s OMZs and implications of ocean deoxygenation. In B. E. Curry (Ed.) Adv Mar Biol (Vol. 74, pp. 117–198) Academic Press. https://doi.org/10.1016/bs.amb.2016.04.001
Gallo ND, Beckwith M, Wei CL, Levin LA, Kuhnz L, Barry JP (2020) Dissolved oxygen and temperature best predict deep-sea fish community structure in the Gulf of California with climate change implications. Mar Ecol Prog Ser 637:159–180. https://doi.org/10.3354/meps13240
Garcia HE, Gordon LI (1992) Oxygen solubility in seawater: Better fitting equations. Limnol Oceanogr 37:1307–1312
Garçon V, Karstensen J, Palacz A, Telszewski M, Aparco Lara T, Breitburg D, Weng K (2019) Multidisciplinary observing in the world ocean’s oxygen minimum zone regions: from climate to fish—the VOICE Initiative. Frontiers Mar Sci 6:722. https://doi.org/10.3389/fmars.2019.00722
Gilbert CH (1890) Scientific results of explorations by the US Fish Commission steamer Albatross. No. XII. A preliminary report on the fishes collected by the steamer Albatross on the Pacific coast of North America during the year 1889, with descriptions of twelve new genera and ninety-two new species. Proceedings of the United States National Museum.
Gilly WF, Beman JM, Litvin SY, Robison BH (2013) Oceanographic and biological effects of shoaling of the OMZ. Ann Rev of Mar Sci 5:393–420. https://doi.org/10.1146/annurev-marine-120710-100849
Gnanadesikan A, Russell JL, Zeng F (2007) How does ocean ventilation change under global warming? Ocean Sci 3:43–53. https://doi.org/10.5194/os-3-43-2007
Grantham BA, Chan F, Nielsen KJ, Fox DS, Barth JA, Huyer A, Lubchenco J, Menge BA (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429:749–754. https://doi.org/10.1038/nature02605
Griffies SM, Danabasoglu G, Durack PJ, Adcroft AJ, Balaji V, Böning CW, Chassignet EP, Curchitser E, Deshayes J, Drange H, Fox-Kemper B, Gleckler PJ, Gregory JM, Haak H, Hallberg RW, Heimbach P, Hewitt HT, Holland DM, Ilyina T, Yeager SG (2016) OMIP contribution to CMIP6: experimental and diagnostic protocol for the physical component of the Ocean Model Intercomparison Project. Geosci Model Develop 9:3231–3296. https://doi.org/10.5194/gmd-9-3231-2016
Hofmann AF, Peltzer ET, Walz PM, Brewer PG (2011) Hypoxia by degrees: establishing definitions for a changing ocean. Deep Sea Res Part I Oceanogr Res Pap 58:1212–1226. https://doi.org/10.1016/j.dsr.2011.09.004
Keeling RF, Körtzinge A, Gruber N (2010) Ocean deoxygenation in a warming world. Ann Rev Mar Sci 2:199–229. https://doi.org/10.1146/annurev.marine.010908.163855
Keller AA, Ciannelli L, Wakefield WW, Simon V, Barth JA, Pierce SD (2017) Species-specific responses of demersal fishes to near-bottom oxygen levels within the California Current large marine ecosystem. Mar Ecol Prog Ser 568:151–173. https://doi.org/10.3354/meps12066
Kwiatkowski L, Torres O, Bopp L, Aumont O, Chamberlain M, Christian JR, Dunne JP, Gehlen M, Ilyina T, John JG, Lenton A (2020) Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17:3439–70. https://doi.org/10.5194/bg-17-3439-2020
Kwiecinski JV, Babbin A R (2021) A high‐resolution Atlas of the eastern tropical pacific oxygen deficient zones. Glob Biogeochem Cycle 35(12), e2021GB007001. https://doi.org/10.1029/2021GB007001
L Tiano E Garcia-Robledo T Dalsgaard AH Devol BB Ward O Ulloa DE Canfield Revsbech 2014 Oxygen distribution and aerobic respiration in the north and south eastern tropical Pacific OMZs Deep Sea Res Part I Oceanogr Res Pap 94 173 183 https://doi.org/10.1016/j.dsr.2014.10.001
Leung S, Thompson L, McPhaden MJ, Mislan KAS (2019) ENSO drives near-surface oxygen and vertical habitat variability in the tropical Pacific. Environ Res Lett 14:064020. https://doi.org/10.1088/1748-9326/ab1c13
Limburg KE, Breitburg D, Swaney DP, Jacinto G (2020) Ocean deoxygenation: a primer. One Earth 2:24–29. https://doi.org/10.1016/j.oneear.2020.01.001
Mangiafico SS (2016) Summary and analysis of extension program evaluation in R, version 1.18.1. New Brunswick: Rutgers Cooperative Extension. rcompanion.org/handbook/
Muggeo VMR (2008) Segmented: an R package to fit regression models with broken-line relationships. R NEWS 8(1):20–25
Muggeo VMR (2016) Testing with a nuisance parameter present only under the alternative: a score-based approach with application to segmented modelling. J Stat Comput Simul 86:3059–3067. https://doi.org/10.1080/00949655.2016.1149855
Muggeo VMR (2017) Interval estimation for the breakpoint in segmented regression: a smoothed score-based approach. Aust N. Z. J Stat 59:311–322. https://doi.org/10.1111/anzs.12200
Orr JC, Najjar RG, Aumon, O, Bopp L, Bullister JL, Danabasoglu G, Doney SC, Dunne JP, Dutay J.-C, Graven H, Griffies SM, John JG, Joos F, Levin I, Lindsay K, Matear RJ, McKinley GA, Mouchet A, Oschlies A, Yool A (2017) Biogeochemical protocols and diagnostics for the CMIP6 Ocean Model Intercomparison Project (OMIP) Geosci Model Develop 10: 2169–2199. https://doi.org/10.5194/gmd-10-2169-2017
Oschlies A, Duteil O, Getzlaff J, Koeve W, Landolfi A, Schmidtko S (2017) Patterns of deoxygenation: sensitivity to natural and anthropogenic drivers. Philos Trans Royal Soc A Math Phys Eng Sci 375:20160325. https://doi.org/10.1098/rsta.2016.0325
Oschlies A, Brandt P, Stramma L, Schmidtko S (2018) Drivers and mechanisms of ocean deoxygenation. Nature Geosci 11:467–473. https://doi.org/10.1038/s41561-018-0152-2
Papiol V, Hendrickx ME, Serrano D (2017) Effects of latitudinal changes in the OMZ of the northeast Pacific on the distribution of bathyal benthic decapod crustaceans. Deep Sea Res Part II Top Stud Oceanogr 137:113–130. https://doi.org/10.1016/j.dsr2.2016.04.023
Pauly D, Cheung WWL (2018) Sound physiological knowledge and principles in modeling shrinking of fishes under climate change. Glob Change Biol 24:e15–e26. https://doi.org/10.1111/gcb.13831
Peterson AT, Soberón J, Pearson RG, Anderson RP, Martínez-Meyer E, Nakamura M, Araújo M B (2011) Ecological Niches and Geographic Distributions (MPB-49) Princeton University Press; JSTOR. https://www.jstor.org/stable/j.ctt7stnh
Pörtner H-O, Bock C, Mark FC (2017) Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J Exp Biol 220:2685–2696. https://doi.org/10.1242/jeb.134585
Pörtner HO, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Weyer NM (2019) The ocean and cryosphere in a changing climate. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate
Quiroga E, Sellanes J, Arntz WE, Gerdes D, Gallardo VA, Hebbeln D (2009) Benthic megafaunal and demersal fish assemblages on the Chilean continental margin: the influence of the oxygen minimum zone on bathymetric distribution. Deep Sea Res Part II Top Stud Oceanogr 56:1112–1123. https://doi.org/10.1016/j.dsr2.2008.09.010
Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199. https://doi.org/10.1242/jeb.047951
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, Müller M (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinf 12:77. https://doi.org/10.1186/1471-2105-12-77
Rose KA, Gutiérrez D, Breitburg D, Conley D, Craig KJ, Froehlich HE, Jeyabaskaran R, Kripa V, Mbaye BC, Mohamed KS, Padua S, Prema D (2019) Impacts of ocean deoxygenation on fisheries. In Ocean deoxygenation: Everyone’s problem. Causes, impacts, consequences and solutions (pp. 519–544) Int Union Conserv Nat Nat Res https://portals.iucn.org/library/sites/library/files/documents/2019-048-En.pdf
Sarmiento JL, Gruber N (2006) Ocean biogeochemical dynamics. Princeton University Press
Sato KN, Levin LA, Schiff K (2017) Habitat compression and expansion of sea urchins in response to changing climate conditions on the California continental shelf and slope (1994–2013) Deep Sea Res Part II Top Stud Oceanogr 137: 377–389. https://doi.org/10.1016/j.dsr2.2016.08.012
Schmidtko S, Stramma L, Visbeck M (2017) Decline in global oceanic oxygen content during the past five decades. Nature 542:335–339. https://doi.org/10.1038/nature21399
Seland Ø, Bentsen M, Olivié D, Toniazzo T, Gjermundsen A, Graff LS, Schulz M (2020) Overview of the Norwegian Earth System Model (NorESM2) and key climate response of CMIP6 DECK, historical, scenario simulations. Geosci Model Develop 13:6165–6200. https://doi.org/10.5194/gmd-13-6165-2020
Stewart JS, Hazen EL, Bograd SJ, Byrnes JEK, Foley DG, Gilly WF, Robison BH, Field JC (2014) Combined climate- and prey-mediated range expansion of Humboldt squid (Dosidicus gigas) a large marine predator in the California Current System. Glob Change Biol 20:1832–1843. https://doi.org/10.1111/gcb.12502
Stramma L, Schmidtko S, Levin LA, Johnson GC (2010) Ocean oxygen minima expansions and their biological impacts. Deep Sea Res Part I Oceanogr Res Pap 57:587–595. https://doi.org/10.1016/j.dsr.2010.01.005
Stramma L, Oschlies A, Schmidtko S (2012) Anticorrelated observed and modeled trends in dissolved oceanic oxygen over the last 50 years. Biogeosci Discuss 9:4595–4626. https://doi.org/10.5194/bgd-9-4595-2012
Wehrtmann IS, Nielsen-Munoz V (2009) The deepwater fishery along the Pacific coast of Costa Rica, Central America. Lat Am J Aquat Res 37(3):543–554. https://doi.org/10.3856/vol37-issue3-fulltext-19
Wehrtmann IS, Arana PM, Barriga E, Gracia A, Pezzuto PR (2012) Deep-water fisheries in Latin America: a review. Lat Am J Aquat Res 40: 497–535. 103856/vol40-issue3-fulltext-2
Wishner KF, Ashjian CJ, Gelfman C, Gowing MM, Kann L, Levin LA, Mullineaux LS, Saltzman J (1995) Pelagic and benthic ecology of the lower interface of the Eastern Tropical Pacific OMZ. Deep Sea Res Part I Oceanogr Res Pap 42:93–115. https://doi.org/10.1016/0967-0637(94)00021-J
Wishner KF, Seibel BA, Roman C, Deutsch C, Outram D, Shaw CT, Birk MA, Mislan KAS, Adams TJ, Moore D, Rile S (2018) Ocean deoxygenation and zooplankton: very small oxygen differences matter. Sci Adv 4: eaau5180. https://doi.org/10.1126/sciadv.aau5180
Yukimoto S, Kawai H, Koshiro T, Oshima N, Yoshida K, Urakawa S, Ishii M (2019) The Meteorological Research Institute Earth System Model version 2.0, MRI-ESM2. 0: description and basic evaluation of the physical component. J Meteorol Soc Jpn Ser. II https://doi.org/10.2151/jmsj.2019-051
Acknowledgements
ISW appreciates the collaboration with The Rainbow Jewels Company (Puntarenas, Costa Rica). We are grateful for the hard work of the captains and crews of “Onuva” and “Sultana” shrimp trawlers during sampling surveys. We also thank the students and research assistants who collaborated during the fieldwork, lab work, and experimental design of the project (Andrés Beita-Jiménez, Catalina Benavides-Varela, Olga Durán-García, Silvia Echeverría-Saenz, Carlos Garita-Alvarado, Yurlandy Gutiérrez-Jara, Juliana Herrera-Correal, Marisol Luna, Solciré Martínez-Jiménez, Jaime Nivia-Ruiz, Vanessa Nielsen-Muñoz, Jeffry Ortíz-Gamboa, Edgar Villegas-Jiménez, Patricio Hernáez).
Funding
The Fondo de Incentivos of the Consejo Nacional para Investigaciones Científicas y Tecnológicas (CONICIT) and the Ministerio de Ciencia, Tecnología y Telecomunicaciones (MICITT) of Costa Rica funded Tayler Clarke’s doctoral scholarship. William W. L. Cheung received support from the Nippon Foundation-the University of British Columbia Nereus Program. Tayler Clarke and William W. L. Cheung received funding support from the Natural Sciences and Engineering Research Council of Canada (Discovery Grant). Fieldwork along the Pacific coast of Costa Rica was partially financed by the German Government (Ministerium für wirtschaftliche Zusammenarbeit und Entwicklung, BMZ), the Ristic AG (Oberferrieden, Germany), and the Universidad de Costa Rica (projects V.I. 111-A4-508; V.I. 808-A9-536, and V.I. 808-A9-537). Additional funds were provided by the Consejo Superior Universitario Centroamericano (CSUCA), University of Kassel, and the Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) for the project “The carcinofauna of deep waters and its sustainable use in the Pacific of Central America: A regional initiative” as part of the programm “Programa Universidad Desarrollo Sostenible” (PUEDES). TLF received funding from the Swiss National Science foundation under grant PP00P2_170687.
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Clarke, T.M., Frölicher, T., Reygondeau, G. et al. Temperature and oxygen supply shape the demersal community in a tropical Oxygen Minimum Zone. Environ Biol Fish 105, 1317–1333 (2022). https://doi.org/10.1007/s10641-022-01256-2
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DOI: https://doi.org/10.1007/s10641-022-01256-2