Impacts of warming on phytoplankton abundance and phenology in a typical tropical marine ecosystem

In the tropics, thermal stratification (during warm conditions) may contribute to a shallowing of the mixed layer above the nutricline and a reduction in the transfer of nutrients to the surface lit-layer, ultimately limiting phytoplankton growth. Using remotely sensed observations and modelled datasets, we study such linkages in the northern Red Sea (NRS) - a typical tropical marine ecosystem. We assess the interannual variability (1998–2015) of both phytoplankton biomass and phenological indices (timing of bloom initiation, duration and termination) in relation to regional warming. We demonstrate that warmer conditions in the NRS are associated with substantially weaker winter phytoplankton blooms, which initiate later, terminate earlier and are shorter in their overall duration (~ 4 weeks). These alterations are directly linked with the strength of atmospheric forcing (air-sea heat fluxes) and vertical stratification (mixed layer depth [MLD]). The interannual variability of sea surface temperature (SST) is found to be a good indicator of phytoplankton abundance, but appears to be less important for predicting bloom timing. These findings suggest that future climate warming scenarios may have a two-fold impact on phytoplankton growth in tropical marine ecosystems: 1) a reduction in phytoplankton abundance and 2) alterations in the timing of seasonal phytoplankton blooms.

[1]  William E. Johns,et al.  Observations of the summer Red Sea circulation , 2007 .

[2]  B. Lazar,et al.  Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo , 1995, Nature.

[3]  Jordan G. Powers,et al.  A Description of the Advanced Research WRF Version 2 , 2005 .

[4]  E. Boss,et al.  Regional ocean-colour chlorophyll algorithms for the Red Sea , 2015 .

[5]  W. Johns,et al.  Water Mass Formation, Overturning Circulation, and the Exchange of the Red Sea with the Adjacent Basins , 2015 .

[6]  N. Stambler,et al.  Population dynamics and life strategies of Rhincalanus nasutus (Copepoda) at the onset of the spring bloom in the Gulf of Aqaba (Red Sea). , 2008 .

[7]  A. Robinson,et al.  Eddy-induced nutrient supply and new production in the Sargasso Sea , 1997 .

[8]  R. Murtugudde,et al.  A wind comparison study using an ocean general circulation model for the 1997–1998 El Niño , 2001 .

[9]  Y. Loya,et al.  Vertical water mass mixing and plankton blooms recorded in skeletal stable carbon isotopes of a Red Sea coral , 1998 .

[10]  Lakshmi Kantha,et al.  An oceanographic nowcast/forecast system for the Red Sea , 1997 .

[11]  Robert J. W. Brewin,et al.  Seasonal phytoplankton blooms in the Gulf of Aden revealed by remote Sensing , 2017 .

[12]  Xiaoping Zhou,et al.  Marine ecology: Spring algal bloom and larval fish survival , 2003, Nature.

[13]  C. Field Climate change 2014 : impacts, adaptation and vulnerability : Working Group II contribution to the fifth assessment report of the Intergovernmental Panel on Climate Change , 2014 .

[14]  J. Bouwmeester,et al.  The status of coral reef ecology research in the Red Sea , 2013, Coral Reefs.

[15]  Mohammed Rasheed,et al.  Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges , 2001, Nature.

[16]  Ibrahim Hoteit,et al.  Sensing coral reef connectivity pathways from space , 2017, Scientific Reports.

[17]  Trevor Platt,et al.  Phytoplankton phenology on the Scotian Shelf , 2011 .

[18]  C. Jantzen,et al.  Collapse of a New Living Species of Giant Clam in the Red Sea , 2008, Current Biology.

[19]  Corinne Le Quéré,et al.  Phytoplankton phenology in the global ocean , 2012 .

[20]  L. Fishelson,et al.  Ecology and behavior of Anthias squamipinnis (peters, 1855) (Anthiidae, Teleostei) in the coral habitat of eilat (Red Sea) , 1973 .

[21]  Ibrahim Hoteit,et al.  Exploring the Red Sea seasonal ecosystem functioning using a three‐dimensional biophysical model , 2014 .

[22]  Ibrahim Hoteit,et al.  Remote Sensing the Phytoplankton Seasonal Succession of the Red Sea , 2013, PloS one.

[23]  Ibrahim Hoteit,et al.  The Gulf of Aden Intermediate Water Intrusion Regulates the Southern Red Sea Summer Phytoplankton Blooms , 2016, PloS one.

[24]  D. H. Cushing,et al.  Plankton Production and Year-class Strength in Fish Populations: an Update of the Match/Mismatch Hypothesis , 1990 .

[25]  T. Platt,et al.  Basin-Scale Coherence in Phenology of Shrimps and Phytoplankton in the North Atlantic Ocean , 2009, Science.

[26]  Daniel E. Schindler,et al.  CLIMATE CHANGE UNCOUPLES TROPHIC INTERACTIONS IN AN AQUATIC ECOSYSTEM , 2004 .

[27]  J. Sarmiento,et al.  Decadal variability in North Atlantic phytoplankton blooms , 2009 .

[28]  Mette Dalgaard Agersted,et al.  Heterogeneous distribution of plankton within the mixed layer and its implications for bloom formation in tropical seas , 2015, Scientific Reports.

[29]  Ibrahim Hoteit,et al.  Abrupt warming of the Red Sea , 2011 .

[30]  K. Trenberth,et al.  Evolution of El Niño–Southern Oscillation and global atmospheric surface temperatures , 2002 .

[31]  Ibrahim Hoteit,et al.  Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea , 2015 .

[32]  John R. Lanzante,et al.  The Atmospheric Bridge: The Influence of ENSO Teleconnections on Air-Sea Interaction over the Global Oceans , 2002 .

[33]  S. M. Head CHAPTER 7 – Corals and Coral Reefs of the Red Sea , 1987 .

[34]  Harriet Cole The natural variability and climate change response in phytoplankton phenology , 2014 .

[35]  Mark G. Meekan,et al.  Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem , 2011 .

[36]  T. Platt,et al.  Ecological indicators for the pelagic zone of the ocean from remote sensing , 2008 .

[37]  D. A. Siegel,et al.  The North Atlantic Spring Phytoplankton Bloom and Sverdrup's Critical Depth Hypothesis , 2002, Science.

[38]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[39]  I. Hoteit,et al.  The climatology of the Red Sea – part 1: the wind , 2017 .

[40]  Ibrahim Hoteit,et al.  Seasonal overturning circulation in the Red Sea: 1. Model validation and summer circulation , 2014 .

[41]  Ibrahim Hoteit,et al.  Eddies in the Red Sea: A statistical and dynamical study , 2014 .

[42]  J. Dunne,et al.  A comparison of methods to determine phytoplankton bloom initiation , 2013 .

[43]  E. Martinez,et al.  Warmer, deeper, and greener mixed layers in the North Atlantic subpolar gyre over the last 50 years , 2016, Global change biology.

[44]  A. Khater,et al.  Environmental characterization and radio-ecological impacts of non-nuclear industries on the Red Sea coast. , 2004, Journal of environmental radioactivity.

[45]  William E. Johns,et al.  An Oceanic General Circulation Model (OGCM) investigation of the Red Sea circulation: 2. Three‐dimensional circulation in the Red Sea , 2003 .

[46]  I. Hoteit,et al.  Impacts of Climate Modes on Air–Sea Heat Exchange in the Red Sea , 2015 .

[47]  Robert J. W. Brewin,et al.  Plankton indicators and ocean observing systems: support to the marine ecosystem state assessment , 2014 .

[48]  P. Steerenberg,et al.  Targeting pathophysiological rhythms: prednisone chronotherapy shows sustained efficacy in rheumatoid arthritis. , 2010, Annals of the rheumatic diseases.

[49]  P. Beninger,et al.  In situ evidence for pre-capture qualitative selection in the tropical bivalve Lithophaga simplex , 2009 .

[50]  Joo‐Hong Kim,et al.  The unique 2009–2010 El Niño event: A fast phase transition of warm pool El Niño to La Niña , 2011 .

[51]  G. Powers,et al.  A Description of the Advanced Research WRF Version 3 , 2008 .

[52]  E. Peters,et al.  Ecotoxicology of tropical marine ecosystems , 1997 .

[53]  K. N. Dollman,et al.  - 1 , 1743 .

[54]  Richard W. Gould,et al.  An Ocean-Colour Time Series for Use in Climate Studies: The Experience of the Ocean-Colour Climate Change Initiative (OC-CCI) , 2019, Sensors.

[55]  Peter Regner,et al.  Ocean Colour Climate Change Initiative — Approach and initial results , 2012, 2012 IEEE International Geoscience and Remote Sensing Symposium.

[56]  I. Hoteit,et al.  Climatic features of the Red Sea from a regional assimilative model , 2017 .

[57]  Scott C. Doney,et al.  Oceanography: Plankton in a warmer world , 2006, Nature.

[58]  Janet Sprintall,et al.  Southern Ocean mixed-layer depth from Argo float profiles , 2008 .

[59]  I. Hoteit,et al.  Decadal trends in Red Sea maximum surface temperature , 2017, Scientific Reports.

[60]  Ibrahim Hoteit,et al.  Seasonal overturning circulation in the Red Sea: 2. Winter circulation , 2014 .

[61]  A. Timmermann,et al.  Increasing frequency of extreme El Niño events due to greenhouse warming , 2014 .

[62]  Ibrahim Hoteit,et al.  Monsoon oscillations regulate fertility of the Red Sea , 2015 .

[63]  Mohammad Reza Shokri,et al.  Environmental impacts of tourism in the Gulf and the Red Sea. , 2013, Marine pollution bulletin.

[64]  Tong Zhu,et al.  Remotely-sensed chlorophyll a observations of the northern Red Sea indicate seasonal variability and influence of coastal reefs , 2008 .

[65]  I. Hoteit,et al.  Atmospheric forcing of the winter air–sea heat fluxes over the Northern Red Sea , 2013 .

[66]  B. Funnell,et al.  The Gulf of Aqaba: Ecological Micropaleontology , 2011 .

[67]  R. Reynolds,et al.  The NCEP/NCAR 40-Year Reanalysis Project , 1996, Renewable Energy.

[68]  F. D’Ortenzio,et al.  Climate-Driven Basin-Scale Decadal Oscillations of Oceanic Phytoplankton , 2009, Science.

[69]  Igor M. Belkin,et al.  Rapid warming of Large Marine Ecosystems , 2009 .

[70]  Ibrahim Hoteit,et al.  Factors governing the deep ventilation of the Red Sea , 2015 .

[71]  T. Platt,et al.  Phenological Responses to ENSO in the Global Oceans , 2016, Surveys in Geophysics.