Effects of Ocean Climate on Spatiotemporal Variation in Sea Urchin Settlement and Recruitment

Sea urchins are voracious herbivores that influence the ecological structure and function of nearshore ecosystems throughout the world. Like many species that produce planktonic larvae, their recruitment is thought to be particularly sensitive to climatic fluctuations in temperature that directly or indirectly affect adult reproduction and larval transport and survival. Yet how climate alters sea urchin populations in space and time by modifying larval recruitment and year-class strength on the time-scales that regulate populations remains understudied. Using an unprecedented, spatially replicated weekly-biweekly dataset spanning 27 years and 1100 km of coastline, we characterized seasonal, interannual, and spatial patterns of larval settlement of the purple sea urchin (Strongylocentrotus purpuratus). We show that large spatial differences in temporal patterns of larval settlement were associated with different responses to fluctuations in ocean temperature and climate. Importantly, we found a strong correlation between larval settlement and regional year class strength suggesting that such temporal and spatial variation in settlement plays an important role in controlling population dynamics. These results provide strong evidence over extensive temporal and spatial domains that climatic fluctuations shape broad-scale patterns of larval settlement and subsequent population structure of an important marine herbivore known to control the productivity and function of marine ecosystems.

[1]  T. Ebert.  Recruitment in Echinoderms , 2020 .

[2]  S. Rumrill,et al.  Differential mortality during the embryonic and larval lives of northeast Pacific echinoids , 2020 .

[3]  M. Bennett,et al.  3-D radar imaging unlocks the untapped behavioral and biomechanical archive of Pleistocene ghost tracks , 2019, Scientific Reports.

[4]  L. Rogers‐Bennett,et al.  Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens , 2019, Scientific Reports.

[5]  A. Cucco,et al.  Hydrodynamic patterns favouring sea urchin recruitment in coastal areas: A Mediterranean study case. , 2018, Marine environmental research.

[6]  J. Romero,et al.  Herbivore control in connected seascapes: habitat determines when population regulation occurs in the life history of a key herbivore , 2018 .

[7]  A. Salomon,et al.  Sudden collapse of a mesopredator reveals its complementary role in mediating rocky reef regime shifts , 2018, Proceedings of the Royal Society B: Biological Sciences.

[8]  J. Pineda,et al.  Reduced barnacle larval abundance and settlement in response to large‐scale oceanic disturbances: Temporal patterns, nearshore thermal stratification, and potential mechanisms , 2018, Limnology and Oceanography.

[9]  J. Largier,et al.  Nearshore Larval Retention and Cross-Shelf Migration of Benthic Crustaceans at an Upwelling Center , 2018, Front. Mar. Sci..

[10]  Kevin M. Johnson,et al.  Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels , 2018, Molecular ecology.

[11]  A. Bakun,et al.  Coastal Upwelling Indices, West Coast of North America, 1946-71 , 2018 .

[12]  T. Frölicher,et al.  Emerging risks from marine heat waves , 2018, Nature Communications.

[13]  A. Shanks,et al.  Testing the intermittent upwelling hypothesis: upwelling, downwelling, and subsidies to the intertidal zone , 2018 .

[14]  A. Reniers,et al.  Alongshore variation in barnacle populations is determined by surf zone hydrodynamics , 2017 .

[15]  Aki Vehtari,et al.  Sparsity information and regularization in the horseshoe and other shrinkage priors , 2017, 1707.01694.

[16]  Jiqiang Guo,et al.  Stan: A Probabilistic Programming Language. , 2017, Journal of statistical software.

[17]  L. Washburn,et al.  Extreme warming challenges sentinel status of kelp forests as indicators of climate change , 2016, Nature Communications.

[18]  C. Griesemer,et al.  Surfzone hydrodynamics as a key determinant of spatial variation in rocky intertidal communities , 2016, Proceedings of the Royal Society B: Biological Sciences.

[19]  Cody S. Szuwalski,et al.  Examining common assumptions about recruitment: a meta‐analysis of recruitment dynamics for worldwide marine fisheries , 2015 .

[20]  W. Sydeman,et al.  Climate change and marine vertebrates , 2015, Science.

[21]  D. Okamoto.  Competition among Eggs Shifts to Cooperation along a Sperm Supply Gradient in an External Fertilizer , 2015, The American Naturalist.

[22]  David A. Siegel,et al.  Geographical variability in the controls of giant kelp biomass dynamics , 2015 .

[23]  J. Thorson,et al.  The importance of spatial models for estimating the strength of density dependence. , 2015, Ecology.

[24]  Jarrett E.K. Byrnes,et al.  Effects of five southern California macroalgal diets on consumption, growth, and gonad weight, in the purple sea urchin Strongylocentrotus purpuratus , 2015, PeerJ.

[25]  S. Morgan.  Behaviorally Mediated Larval Transport in Upwelling Systems , 2014 .

[26]  R. Scheibling,et al.  Effects of sea urchin disease on coastal marine ecosystems , 2014 .

[27]  W. Peterson,et al.  Does larval advection explain latitudinal differences in recruitment across upwelling regimes , 2014 .

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

[29]  K. Filbee‐Dexter,et al.  Sea urchin barrens as alternative stable states of collapsed kelp ecosystems , 2014 .

[30]  B. Taguchi,et al.  Synthesis of Pacific Ocean Climate and Ecosystem Dynamics , 2013 .

[31]  K. Lafferty,et al.  A multi-decade time series of kelp forest community structure at the California Channel Islands , 2013 .

[32]  B. Menge,et al.  Dynamics of coastal meta-ecosystems: the intermittent upwelling hypothesis and a test in rocky intertidal regions , 2013 .

[33]  J. Padilla‐Gamiño,et al.  Temperature and CO2 additively regulate physiology, morphology and genomic responses of larval sea urchins, Strongylocentrotus purpuratus , 2013, Proceedings of the Royal Society B: Biological Sciences.

[34]  R. Kudela,et al.  Trends in the surface chlorophyll of the California Current: Merging data from multiple ocean color satellites , 2012 .

[35]  A. Azad,et al.  Influence of stocking density and temperature on early development and survival of the purple sea urchin, Strongylocentrotus purpuratus (Stimpson, 1857) , 2012 .

[36]  Sayan Mukherjee,et al.  Genetics of gene expression responses to temperature stress in a sea urchin gene network , 2012, Molecular ecology.

[37]  S. Pinna,et al.  Habitat and Scale Shape the Demographic Fate of the Keystone Sea Urchin Paracentrotus lividus in Mediterranean Macrophyte Communities , 2012, PloS one.

[38]  M. McManus,et al.  Plankton distribution and ocean dispersal , 2012, Journal of Experimental Biology.

[39]  Libe Washburn,et al.  Coastal fronts set recruitment and connectivity patterns across multiple taxa , 2012 .

[40]  J. Lubchenco,et al.  Linking long-term, large-scale climatic and environmental variability to patterns of marine invertebrate recruitment: Toward explaining “unexplained” variation , 2011 .

[41]  James G. Scott,et al.  On the half-cauchy prior for a global scale parameter , 2011, 1104.4937.

[42]  M. Mangel,et al.  Fluctuations of fish populations and the magnifying effects of fishing , 2011, Proceedings of the National Academy of Sciences.

[43]  D. Vaughn,et al.  The peril of the plankton. , 2010, Integrative and comparative biology.

[44]  A. Brito,et al.  Effect of temperature on settlement and postsettlement survival in a barrens-forming sea urchin , 2010 .

[45]  James G. Scott,et al.  The horseshoe estimator for sparse signals , 2010 .

[46]  G. De’ath,et al.  Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation , 2010, Coral Reefs.

[47]  T. Ebert.  Demographic patterns of the purple sea urchin Strongylocentrotus purpuratus along a latitudinal gradient, 1985–1987 , 2010 .

[48]  J. Largier,et al.  Nearshore larval retention in a region of strong upwelling and recruitment limitation. , 2009, Ecology.

[49]  David A. Siegel,et al.  Quantifying connectivity in the coastal ocean with application to the Southern California Bight , 2009 .

[50]  Dorota Kurowicka,et al.  Generating random correlation matrices based on vines and extended onion method , 2009, J. Multivar. Anal..

[51]  Marco Scutari,et al.  Learning Bayesian Networks with the bnlearn R Package , 2009, 0908.3817.

[52]  R. Shearman,et al.  Paradigm lost? Cross-shelf distributions of intertidal invertebrate larvae are unaffected by upwelling or downwelling , 2009 .

[53]  A. Shanks.  Pelagic Larval Duration and Dispersal Distance Revisited , 2009, The Biological Bulletin.

[54]  Maria Byrne,et al.  Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios , 2009, Proceedings of the Royal Society B: Biological Sciences.

[55]  M. Haddon,et al.  Climate‐driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics , 2009 .

[56]  Russ E. Davis,et al.  Glider surveillance of physics and biology in the southern California Current System , 2008 .

[57]  L. Ladah,et al.  Population structure of purple sea urchin Strongylocentrotus purpuratus along the Baja California peninsula , 2008, Fisheries Science.

[58]  B. Kendall,et al.  The stochastic nature of larval connectivity among nearshore marine populations , 2008, Proceedings of the National Academy of Sciences.

[59]  James C. McWilliams,et al.  North Pacific Gyre Oscillation links ocean climate and ecosystem change , 2008 .

[60]  Thomas M. Smith,et al.  Daily High-Resolution-Blended Analyses for Sea Surface Temperature , 2007 .

[61]  Jonathan D. Allen,et al.  Testing rates of planktonic versus benthic predation in the field , 2007 .

[62]  J. Pearse.  Ecological Role of Purple Sea Urchins , 2006, Science.

[63]  Steven D. Gaines,et al.  Intertidal community structure and oceanographic patterns around Santa Cruz Island, CA, USA , 2006 .

[64]  S. Gaines,et al.  Recruitment of intertidal invertebrates and oceanographic variability at Santa Cruz Island, California , 2005 .

[65]  Libe Washburn,et al.  Sub‐mesoscale coastal eddies observed by high frequency radar: A new mechanism for delivering nutrients to kelp forests in the Southern California Bight , 2005 .

[66]  G. Eckert,et al.  POPULATION PERSISTENCE OF CALIFORNIA CURRENT FISHES AND BENTHIC CRUSTACEANS: A MARINE DRIFT PARADOX , 2005 .

[67]  K. Lafferty.  FISHING FOR LOBSTERS INDIRECTLY INCREASES EPIDEMICS IN SEA URCHINS , 2004 .

[68]  E. Sala,et al.  Temporal and spatial variability in settlement of the sea urchin Paracentrotus lividus in the NW Mediterranean , 2004 .

[69]  David A. Siegel,et al.  Lagrangian descriptions of marine larval dispersion , 2003 .

[70]  L. Botsford,et al.  Inter-annual variability in larval supply to populations of three invertebrate taxa in the northern California Current , 2003 .

[71]  Kevin B. Johnson,et al.  Low rates of predation on planktonic marine invertebrate larvae , 2003 .

[72]  Carl E. Rasmussen,et al.  Gaussian processes for machine learning , 2005, Adaptive computation and machine learning.

[73]  A. G. Bazhin,et al.  Status and management of world sea urchin fisheries , 2002 .

[74]  John P. Ryan,et al.  Biological and chemical consequences of the 1997–1998 El Niño in central California waters , 2002 .

[75]  S. Bograd,et al.  Dynamic evolution of the 1997–1999 El Niño–La Niña cycle in the southern California Current System , 2002 .

[76]  N. Mantua,et al.  The Pacific Decadal Oscillation , 2002 .

[77]  Benjamin Holt,et al.  Satellite observations of small coastal ocean eddies in the Southern California Bight , 2001 .

[78]  R. Carpenter,et al.  Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Steven D. Gaines,et al.  Temperature or Transport? Range Limits in Marine Species Mediated Solely by Flow , 2000, The American Naturalist.

[80]  M. Lamare,et al.  In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) , 1999 .

[81]  J. Valentine,et al.  Seagrass herbivory: evidence for the continued grazing of marine grasses , 1999 .

[82]  Ransom A. Myers,et al.  When Do Environment–recruitment Correlations Work? , 1998, Reviews in Fish Biology and Fisheries.

[83]  K. Wolter,et al.  Measuring the strength of ENSO events: How does 1997/98 rank? , 1998 .

[84]  P. Chesson.  Spatial scales in the study of reef fishes: A theoretical perspective , 1998 .

[85]  J. Roughgarden,et al.  Barnacle recruitment and population dynamics predicted from coastal upwelling , 1997 .

[86]  Kevin B. Johnson,et al.  The importance of prey densities and background plankton in studies of predation on invertebrate larvae , 1997 .

[87]  J. Wallace,et al.  A Pacific Interdecadal Climate Oscillation with Impacts on Salmon Production , 1997 .

[88]  Andy W. Sheppard,et al.  Frontiers of population ecology , 1997 .

[89]  D. J. Gilbert.  Towards a new recruitment paradigm for fish stocks , 1997 .

[90]  T. Ebert,et al.  Effects of kelp forests Macrocystis pyrifera on the larval distribution and settlement of red and purple sea urchins Strongylocentrotus franciscanus and S. purpuratus , 1996 .

[91]  O. Hoegh‐Guldberg,et al.  Temperature, Food Availability, and the Development of Marine Invertebrate Larvae , 1995 .

[92]  J. Estes,et al.  Sea Otters and Kelp Forests in Alaska: Generality and Variation in a Community Ecological Paradigm , 1995 .

[93]  M. Ratner,et al.  Electron conduction in molecular wires. I. A scattering formalism , 1994 .

[94]  J. Pineda.  Internal tidal bores in the nearshore: warm-water fronts, seaward gravity currents and the onshore transport of neustonic larvae , 1994 .

[95]  R. Grosberg,et al.  For adults only? Supply-side ecology and the history of larval biology. , 1992, Trends in ecology & evolution.

[96]  S. Rumrill,et al.  Natural mortality of marine invertebrate larvae , 1990 .

[97]  R. Rowley,et al.  Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes? , 1989 .

[98]  J. Roughgarden,et al.  Recruitment dynamics in complex life cycles. , 1988, Science.

[99]  D. Reed,et al.  Food Availability, Sea Urchin Grazing, and Kelp Forest Community Structure , 1985 .

[100]  T. E. Schroeder,et al.  "Spiral asters" and cytoplasmic rotation in sea urchin eggs: induction in Strongylocentrotus purpuratus eggs by elevated temperature , 1985, The Journal of cell biology.

[101]  R. Cochran,et al.  Environmental regulation of the annual reproductive season of Strongylocentrotus purpuratus (Stimpson). , 1975, The Biological bulletin.

[102]  J. Gonor.  Reproductive cycles in oregon populations of the echlnoid, Strongylocentrotvs purpuratus (Stimpson). I. Annual gonad growth and ovarian gametogenic cycles , 1973 .

[103]  L. Rogers‐Bennett,et al.  Mesocentrotus franciscanus and Strongylocentrotus purpuratus , 2020 .

[104]  J. Pineda,et al.  Larval Transport in the Coastal Zone : Biological and Physical Processes , 2017 .

[105]  D. Okamoto.  The role of fluctuating food supply on recruitment, survival and population dynamics in the sea , 2014 .

[106]  H. M. Page,et al.  SCALES OF VARIABILITY IN LARVAL SETTLEMENT WITHIN THE CHANNEL ISLANDS NATIONAL MARINE SANCTUARY AND ALONG THE MAINLAND COAST , 2009 .

[107]  Iain Murray,et al.  Introduction to Gaussian Processes , 2008 .

[108]  M. Tegner,et al.  Reproductive responses of purple sea urchin (Strongylocentrotus purpuratus) populations to environmental conditions across a coastal depth gradient , 2007 .

[109]  J. Hay,et al.  Coastal systems and low-lying areas , 2007 .

[110]  Mathew A. Leibold,et al.  Metacommunities: Spatial Dynamics and Ecological Communities , 2005 .

[111]  S. Schroeter.  Biology of the Red Sea Urchin , Strongylocentrotus franciscanus , and Its Fishery in California , 2004 .

[112]  R. R. Strathmann,et al.  EFFECTS OF MATERNAL AND LARVAL NUTRITION ON GROWTH AND FORM OF PLANKTOTROPHIC LARVAE , 1998 .

[113]  D. Mackay,et al.  Introduction to Gaussian processes , 1998 .

[114]  G. Abraham-Frois,et al.  The dynamic evolution , 1997 .

[115]  Terry P. Hughes,et al.  RECRUITMENT AND THE LOCAL DYNAMICS OF OPEN MARINE POPULATIONS , 1996 .

[116]  T. Ebert,et al.  Settlement patterns of red and purple sea urchins [Strongylocentrotus franciscanus and S. purpuratus) in California, USA , 1994 .

[117]  M. Tegner,et al.  Sea urchins, El Ninos, and the long term stability of Southern California kelp forest communities , 1991 .

[118]  Michael C. Kenner,et al.  Size at first reproduction of the sea urchin Strongylocentrotus purpuratus in a central California kelp forest , 1991 .

[119]  P. Fairweather,et al.  Supply-side ecology and benthic marine assemblages. , 1989, Trends in ecology & evolution.

[120]  M. F. Strathmann,et al.  Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae , 1987 .

[121]  J. Pearse,et al.  Photoperiodic regulation of gametogenesis and growth in the sea urchin Strongylocentrotus purpuratus , 1986 .

[122]  Jh Himmelman,et al.  Population biology of green sea urchins on rocky barrens , 1986 .

[123]  J. Connell.  The consequences of variation in initial settlement vs. post-settlement mortality in rocky intertidal communities , 1985 .

[124]  C. Young,et al.  Differential predation on marine invertebrate larvae by two benthic predators , 1984 .

[125]  A. Shanks.  Surface slicks associated with tidally forced internal waves may transport pelagic larvae of benthic invertebrates and fishes shoreward , 1983 .

[126]  R. R. Strathmann.  Length of pelagic period in echinoderms with feeding larvae from the Northeast Pacific , 1978 .

[127]  Juliet M. Wong,et al.  Transcriptomics reveal transgenerational effects in purple sea urchins exposed to low pH conditions - , 2022 .