Changes in deep reef benthic community composition across a latitudinal and environmental gradient in temperate Eastern Australia

Deep reef assemblages in south-eastern Australia are poorly described, and have been surveyed by only a few studies conducted over small spatial scales. Here, we characterise the composition of deep (~30-90 m depth) sessile invertebrate communities from sub-tropical (27°S) to temperate eastern Australia (43°S). We estimated the cover of 51 preselected invertebrate types from over 1700 seafloor images collected by an autonomous underwater vehicle from >105 km of transects across the study region. Seafloor images were assessed using 3 alternative schemes reflecting different resolution of benthic invertebrate groupings, including the broad- level Collaborative and Automated Tools for Analysis of Marine Imagery project (‘CATAMI’) classification recently developed as a generic scoring approach for seafloor imagery. Ordination using canonical analysis of principal coordinates indicated a clear latitudinal gradient in benthic community composition and, particularly when based on individual morphotypes, 3 distinct community types (sub-tropical, warm temperate and cool temperate). Changes in community structure mostly correlated with primary productivity and the temperature climatology, while local-scale variability in community composition was most related to depth. Along with the gradual shift in deep reef community composition across latitudes, region-specific sessile invertebrates might serve as useful indicators of change in these deep benthic communities under future changes in ocean climate in the region, which has been identified as a global hotspot for ocean warming. Our methodological approach has general applicability for large-scale surveying and monitoring of benthic communities using underwater imagery.

[1]  Andrew R. Davis,et al.  Patterns in sponge (Porifera) assemblages on temperate coastal reefs off Sydney, Australia , 1996 .

[2]  Jane Fromont,et al.  Sponge gardens of Ningaloo Reef (Carnarvon Shelf, Western Australia) are biodiversity hotspots , 2011, Hydrobiologia.

[3]  K. M. Norderhaug,et al.  Macrophytes as habitat for fauna , 2009 .

[4]  R. Aronson,et al.  Climate flickers and range shifts of reef corals , 2004 .

[5]  M. Maldonado.  The ecology of the sponge larva , 2006 .

[6]  T. Wernberg,et al.  Extreme climatic event drives range contraction of a habitat-forming species , 2013, Proceedings of the Royal Society B: Biological Sciences.

[7]  M. Tegner,et al.  Ecosystem effects of fishing in kelp forest communities , 2000 .

[8]  Carlo Cerrano,et al.  Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave , 2008 .

[9]  Alan Williams,et al.  Living on the edge: the sponge fauna of Australia’s southwestern and northwestern deep continental margin , 2011, Hydrobiologia.

[10]  Robert K. Colwell,et al.  Defining and observing stages of climate-mediated range shifts in marine systems , 2014 .

[11]  G. Hosie,et al.  Climate change cascades: Shifts in oceanography, species' ranges and subtidal marine community dynamics in eastern Tasmania , 2011 .

[12]  Tony Rees,et al.  A Standardised Vocabulary for Identifying Benthic Biota and Substrata from Underwater Imagery: The CATAMI Classification Scheme , 2015, PloS one.

[13]  N. Holbrook,et al.  A Statistical Method for Improving Continental Shelf and Nearshore Marine Climate Predictions , 2014 .

[14]  P. Mooney,et al.  Conservation of natural wilderness values in the Port Davey marine and estuarine protected area, South-Western Tasmania , 2010 .

[15]  T. Wernberg,et al.  Satellite-derived SST data as a proxy for water temperature in nearshore benthic ecology , 2009 .

[16]  Mark A. Hemer,et al.  The magnitude and frequency of combined flow bed shear stress as a measure of exposure on the Australian continental shelf , 2006 .

[17]  M. Johnson-Roberson,et al.  Benthic monitoring with robotic platforms — The experience of Australia , 2013, 2013 IEEE International Underwater Technology Symposium (UT).

[18]  C. McClain,et al.  Calibration of SeaWiFS. II. Vicarious techniques. , 2001, Applied optics.

[19]  G. Pecl,et al.  Identification of global marine hotspots: sentinels for change and vanguards for adaptation action , 2014, Reviews in Fish Biology and Fisheries.

[20]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[21]  Stefan B. Williams,et al.  Stereo‐imaging AUV detects trends in sea urchin abundance on deep overgrazed reefs , 2016 .

[22]  G. Kendrick,et al.  Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. , 2010, Ecology letters.

[23]  J. Webster,et al.  Predicting the Location and Spatial Extent of Submerged Coral Reef Habitat in the Great Barrier Reef World Heritage Area, Australia , 2012, PloS one.

[24]  Stefan B. Williams,et al.  Variability in mesophotic coral reef communities along the Great Barrier Reef, Australia , 2011 .

[25]  Paul J. Rogers,et al.  Epifaunal assemblages of the eastern Great Australian Bight: Effectiveness of a benthic protection zone in representing regional biodiversity , 2006 .

[26]  J. Hewitt,et al.  Biophysical patterns in benthic assemblage composition across contrasting continental margins off New Zealand , 2013 .

[27]  M. Kavanaugh,et al.  Fifteen degrees of separation: Latitudinal gradients of rocky intertidal biota along the California Current , 2006 .

[28]  B. Agius.  Spatial and temporal effects of pre-seeding plates with invasive ascidians: Growth, recruitment and community composition , 2007 .

[29]  Marti J. Anderson,et al.  CANONICAL ANALYSIS OF PRINCIPAL COORDINATES: A USEFUL METHOD OF CONSTRAINED ORDINATION FOR ECOLOGY , 2003 .

[30]  J. Wilkin,et al.  Ocean Interpolation by Four-Dimensional Weighted Least Squares—Application to the Waters around Australasia , 2002 .

[31]  K. Ridgway,et al.  Mapping ocean properties in regions of complex topography , 2002 .

[32]  A. Hobday,et al.  Climate-driven range changes in Tasmanian intertidal fauna , 2010 .

[33]  C. McClain,et al.  Calibration of SeaWiFS. I. Direct techniques. , 2001, Applied optics.

[34]  Rudy J. Kloser,et al.  Scales of habitat heterogeneity and megabenthos biodiversity on an extensive Australian continental margin (100–1100 m depths) , 2010 .

[35]  Will F. Figueira,et al.  The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts , 2014, Proceedings of the Royal Society B: Biological Sciences.

[36]  S. Thrush,et al.  Macrobenthic communities of the north-western Ross Sea shelf: links to depth, sediment characteristics and latitude , 2010, Antarctic Science.

[37]  M. Byrne,et al.  Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs , 2008 .

[38]  K. ROTzLER,et al.  Impact of Crustose Clionid Sponges on Caribbean Reef Corals , 2006 .

[39]  N. Moltschaniwskyj,et al.  Rapid assessment of an ocean warming hotspot reveals ''high'' confidence in potential species' range extensions , 2015 .

[40]  A. Metaxas,et al.  Temperature explains settlement patterns of the introduced bryozoan Membranipora membranacea in Nova Scotia, Canada , 2007 .

[41]  A. Solé-Cava,et al.  Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks1 , 2005, Integrative and comparative biology.

[42]  Stefan B. Williams,et al.  Monitoring of Benthic Reference Sites: Using an Autonomous Underwater Vehicle , 2012, IEEE Robotics & Automation Magazine.

[43]  Gary A. Kendrick,et al.  Benthic assemblage composition on subtidal reefs along a latitudinal gradient in Western Australia , 2010 .

[44]  Jack J. Middelburg,et al.  Surviving in a Marine Desert: The Sponge Loop Retains Resources Within Coral Reefs , 2013, Science.

[45]  Stefan B. Williams,et al.  Large-Scale Geographic Variation in Distribution and Abundance of Australian Deep-Water Kelp Forests , 2015, PloS one.

[46]  P. Francour,et al.  [Massive mortality of marine invertebrates: an unprecedented event in northwestern Mediterranean]. , 2000, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[47]  Craig R. Johnson,et al.  Building Resilience Against Climate-Driven Shifts in a Temperate Reef System: Staying Away from Context-Dependent Ecological Thresholds , 2015, Ecosystems.

[48]  Eriko Hoshino,et al.  Modelling marine community responses to climate‐driven species redistribution to guide monitoring and adaptive ecosystem‐based management , 2016, Global change biology.

[49]  P. Picco,et al.  A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999 , 2000 .

[50]  J. Bell.  Contrasting patterns of species and functional composition of coral reef sponge assemblages , 2007 .

[51]  M. Attrill,et al.  Tolerance of Sponge Assemblages to Temperature Anomalies: Resilience and Proliferation of Sponges following the 1997–8 El-Niño Southern Oscillation , 2013, PloS one.

[52]  M. Úriz,et al.  Sponge Mass Mortalities in a Warming Mediterranean Sea: Are Cyanobacteria-Harboring Species Worse Off? , 2011, PloS one.

[53]  Euan S. Harvey,et al.  Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. , 2015, Ecology letters.

[54]  J. Stachowicz,et al.  Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[55]  O. Alves,et al.  Predicting thermal stress for coral bleaching in the Great Barrier Reef using a coupled ocean–atmosphere seasonal forecast model , 2013 .

[56]  Michael J. Fogarty,et al.  Marine Taxa Track Local Climate Velocities , 2013, Science.

[57]  Paul J. Somerfield,et al.  Exploring interactions by second-stage community analyses , 2006 .

[58]  Pierre Legendre,et al.  DISTANCE‐BASED REDUNDANCY ANALYSIS: TESTING MULTISPECIES RESPONSES IN MULTIFACTORIAL ECOLOGICAL EXPERIMENTS , 1999 .

[59]  J. Vacelet,et al.  Mortalité massive d'invertébrés marins : un événement sans précédent en Méditerranée nord-occidentale , 2000 .

[60]  John N. A. Hooper,et al.  Small-scale patterns of sponge biodiversity (Porifera) on Sunshine Coast reefs, eastern Australia , 2002 .

[61]  M. Chapman,et al.  Structure and dynamics of sponge-dominated assemblages on exposed and sheltered temperate reefs , 2006 .

[62]  T. Schlacher,et al.  High-resolution seabed imagery as a tool for biodiversity conservation planning on continental margins , 2010 .

[63]  Craig R. Johnson,et al.  Sensitivity analysis and pattern-oriented validation of TRITON, a model with alternative community states: Insights on temperate rocky reefs dynamics , 2013 .

[64]  C. Wilkinson,et al.  Patterns in the distribution of sponge populations across the central Great Barrier Reef , 2004, Coral Reefs.

[65]  Neil L. Andrew,et al.  Accounting for local scale variability in benthos: implications for future assessments of latitudinal trends in the coastal Ross Sea , 2006, Antarctic Science.

[66]  K. Rützler.  Impact of crustose clionid sponges on Caribbean reef corals , 2002 .

[67]  C. Johnson,et al.  Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift , 2009, Proceedings of the National Academy of Sciences.

[68]  D. Leduc,et al.  Spatial patterns and environmental drivers of benthic infaunal community structure and ecosystem function on the New Zealand continental margin , 2015 .

[69]  C. Folke,et al.  Alternative states on coral reefs: beyond coral–macroalgal phase shifts , 2009 .

[70]  K. Linse,et al.  Diversity, abundance and composition in macrofaunal molluscs from the Ross Sea (Antarctica): results of fine-mesh sampling along a latitudinal gradient , 2014, Polar Biology.

[71]  G. Kendrick,et al.  Marine sponges of the Dampier Archipelago, Western Australia: patterns of species distributions, abundance and diversity , 2006, Biodiversity & Conservation.

[72]  Manuel González-Rivero,et al.  The role of sponge competition on coral reef alternative steady states , 2011 .

[73]  Graham J. Edgar,et al.  Australian Marine Life: The plants and animals of temperate waters , 2009 .