Integrating multiple species connectivity and habitat quality into conservation planning for coral reefs

Incorporating connectivity into the design of marine protected areas (MPAs) has met with conceptual, theoretical, and practical challenges, which include: 1) the need to consider connectivity for multiple species with different dispersal abilities, and 2) the role played by variable habitat quality in determining the spatial patterns of connectivity. We propose an innovative approach, combining biophysical modeling with a routinely-used tool for marine-reserve design (Marxan), to address both challenges by using ecologically-informed connectivity parameters. We showed how functional demographic connectivity for four candidate reef-associated species with varying dispersal abilities and a suite of connectivity metrics weighted by habitat quality can be used to set conservation objectives and inform MPA placement. Overall, the strength of dispersal barriers varied across modeled species and, also across species, we found a lack of spatial concordance of reefs that were high-quality sources, self-persistent, and stepping-stones. Including spatially-heterogeneous habitat quality made a considerable difference to connectivity patterns, significantly reducing the potential reproductive output from many reefs. We also found that caution is needed in combining connectivity data from modeled species into multi-species matrices, which do not perform reliably as surrogates for all connectivity metrics of individual species. We then showed that restricting the habitat available for conservation has an inequitable impact on different connectivity objectives and species, with greatest impact on betweenness centrality and long-distance dispersers. We used Brazilian coral reefs as a case study but our approach is applicable to both marine and terrestrial conservation planning, and offers a holistic way to design functionally-connected reserves to tackle the complex issues relevant to planning for persistence.

[1]  K. Selkoe,et al.  Ocean currents help explain population genetic structure , 2010, Proceedings of the Royal Society B: Biological Sciences.

[2]  R. Steneck,et al.  Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges , 2009, Coral Reefs.

[3]  Simon Jennings,et al.  Extinction vulnerability of coral reef fishes , 2011, Ecology letters.

[4]  Benjamin S. Halpern,et al.  THE IMPACT OF MARINE RESERVES: DO RESERVES WORK AND DOES RESERVE SIZE MATTER? , 2003 .

[5]  S. Palumbi,et al.  MARINE RESERVES AND OCEAN NEIGHBORHOODS: The Spatial Scale of Marine Populations and Their Management , 2004 .

[6]  Richard M Cowling,et al.  Conservation planning in a changing world. , 2007, Trends in ecology & evolution.

[7]  Florent E. Angly,et al.  Microbial Ecology of Four Coral Atolls in the Northern Line Islands , 2008, PloS one.

[8]  R. Pressey,et al.  Incorporating ontogenetic dispersal, ecological processes and conservation zoning into reserve design , 2010 .

[9]  Hugh P. Possingham,et al.  Dispersal connectivity and reserve selection for marine conservation , 2011 .

[10]  Atte Moilanen,et al.  Methods and workflow for spatial conservation prioritization using Zonation , 2013, Environ. Model. Softw..

[11]  Patrick N. Halpin,et al.  Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation , 2007, Landscape Ecology.

[12]  Dean L Urban,et al.  A Graph‐Theory Framework for Evaluating Landscape Connectivity and Conservation Planning , 2008, Conservation biology : the journal of the Society for Conservation Biology.

[13]  Hugh P Possingham,et al.  Setting Conservation Priorities , 2009, Annals of the New York Academy of Sciences.

[14]  Moa Berglund,et al.  Optimal selection of marine protected areas based on connectivity and habitat quality , 2012 .

[15]  Atte Moilanen,et al.  On the limitations of graph‐theoretic connectivity in spatial ecology and conservation , 2011 .

[16]  D. O. Pires,et al.  Reef coral reproduction in the Abrolhos Reef Complex, Brazil: the endemic genus Mussismilia , 1999 .

[17]  G. Jones,et al.  Population connectivity and conservation of marine biodiversity , 2007 .

[18]  Claire B. Paris,et al.  Direct evidence of a biophysical retention mechanism for coral reef fish larvae , 2004 .

[19]  E. Neves,et al.  Sexual reproduction of Brazilian coral Mussismilia hispida (Verrill, 1902) , 2002, Coral Reefs.

[20]  D. Bellwood,et al.  New paradigms for supporting the resilience of marine ecosystems. , 2005, Trends in ecology & evolution.

[21]  Robert L. Pressey,et al.  Integrating connectivity and climate change into marine conservation planning , 2014 .

[22]  J. Castilla,et al.  ECOLOGICAL CRITERIA FOR EVALUATING CANDIDATE SITES FOR MARINE RESERVES , 2003 .

[23]  R. Cowen,et al.  Larval dispersal and marine population connectivity. , 2009, Annual review of marine science.

[24]  L. A. Barnett,et al.  Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. , 2014, Ecological applications : a publication of the Ecological Society of America.

[25]  Z. M. Leão,et al.  Tropical coast of Brazil , 2000 .

[26]  Claire B Paris-Limouzy,et al.  Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs , 2009, Coral Reefs.

[27]  Justin M. Calabrese,et al.  A comparison-shopper's guide to connectivity metrics , 2004 .

[28]  C. Castro,et al.  Four-year monthly sediment deposition on turbid southwestern Atlantic coral reefs, with a comparison of benthic assemblages , 2012 .

[29]  E. Neves,et al.  Release of planula larvae, settlement and development of Siderastrea stellata Verrill, 1868 (Anthozoa, Scleractinia) , 2003, Hydrobiologia.

[30]  C. Castro,et al.  Coral community structure and sedimentation at different distances from the coast of the Abrolhos Bank, Brazil , 2011 .

[31]  S. Purkis,et al.  Satellite imaging coral reef resilience at regional scale. A case-study from Saudi Arabia. , 2012, Marine pollution bulletin.

[32]  Simon A. Levin,et al.  Designing marine reserves for interacting species: Insights from theory , 2007 .

[33]  Analysis of Progress Towards a Comprehensive System of Marine Protected Areas in Brazil , 2013 .

[34]  Timothy H. Keitt,et al.  LANDSCAPE CONNECTIVITY: A GRAPH‐THEORETIC PERSPECTIVE , 2001 .

[35]  M Cabeza,et al.  Design of reserve networks and the persistence of biodiversity. , 2001, Trends in ecology & evolution.

[36]  Serge Planes,et al.  Larval Export from Marine Reserves and the Recruitment Benefit for Fish and Fisheries , 2012, Current Biology.

[37]  D. O. Pires,et al.  Reproductive effort of an endemic major reef builder along an inshore–offshore gradient in south-western Atlantic , 2010, Journal of the Marine Biological Association of the United Kingdom.

[38]  L. Gerber,et al.  Habitat-specific larval dispersal and marine connectivity: implications for spatial conservation planning , 2013 .

[39]  G. Jones,et al.  Larval dispersal connects fish populations in a network of marine protected areas , 2009, Proceedings of the National Academy of Sciences.

[40]  Brendan A. Wintle,et al.  Habitat area, quality and connectivity: striking the balance for efficient conservation , 2011 .

[41]  Z. M. Leão,et al.  Coral bleaching in the Caramuanas reef (Todos os Santos Bay, Brazil) during the 2010 El Niño event , 2013 .

[42]  K. Gaston,et al.  Balancing alternative land uses in conservation prioritization. , 2011, Ecological applications : a publication of the Ecological Society of America.

[43]  D. Bellwood,et al.  Confronting the coral reef crisis , 2004, Nature.

[44]  B. Willis,et al.  Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals , 2009 .

[45]  David A Siegel,et al.  Identifying critical regions in small-world marine metapopulations , 2011, Proceedings of the National Academy of Sciences.

[46]  Hugh P. Possingham,et al.  Conservation planning for connectivity across marine, freshwater, and terrestrial realms , 2010 .

[47]  J. C. Day,et al.  Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs , 2009, Coral Reefs.

[48]  Carrie V. Kappel,et al.  A Global Map of Human Impact on Marine Ecosystems , 2008, Science.

[49]  Z. M. Leão,et al.  A relic coral fauna threatened by global changes and human activities, Eastern Brazil. , 2005, Marine pollution bulletin.

[50]  A. Olds,et al.  Habitat connectivity improves reserve performance , 2012 .

[51]  Johnathan T. Kool,et al.  Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems , 2010 .

[52]  J. Kool,et al.  Population connectivity: recent advances and new perspectives , 2012, Landscape Ecology.

[53]  David Mouillot,et al.  A functional approach reveals community responses to disturbances. , 2013, Trends in ecology & evolution.

[54]  Christopher A. Edwards,et al.  The Value of Larval Connectivity Information in the Static Optimization of Marine Reserve Design , 2014 .

[55]  Hugh P. Possingham,et al.  Incorporating asymmetric connectivity into spatial decision making for conservation , 2010 .

[56]  Patrick N. Halpin,et al.  Marine population connectivity identifies ecological neighbors for conservation planning in the Coral Triangle , 2012 .

[57]  R. L. Pressey,et al.  Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs , 2009, Coral Reefs.

[58]  Claire B Paris-Limouzy,et al.  The Role of Long Distance Dispersal Versus Local Retention in Replenishing Marine Populations , 2003 .

[59]  Dean L Urban,et al.  Graph theory as a proxy for spatially explicit population models in conservation planning. , 2007, Ecological applications : a publication of the Ecological Society of America.

[60]  Claire B Paris-Limouzy,et al.  Connectivity of marine populations: open or closed? , 2000, Science.

[61]  T. Hughes Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef , 1994, Science.

[62]  Avichal Mehra,et al.  A Real Time Ocean Forecast System for the North Atlantic Ocean , 2010 .

[63]  Robert L. Pressey,et al.  The plan of the day: managing the dynamic transition from regional conservation designs to local conservation actions , 2013 .

[64]  Wilfried Thuiller,et al.  Extending networks of protected areas to optimize connectivity and population growth rate , 2015 .

[65]  B. Halpern,et al.  Review Paper. Matching marine reserve design to reserve objectives , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[66]  J. McWilliams,et al.  Currents connecting communities: nearshore community similarity and ocean circulation. , 2011, Ecology.

[67]  Panagiotis Dendrinos,et al.  The Structure of Mediterranean Rocky Reef Ecosystems across Environmental and Human Gradients, and Conservation Implications , 2012, PloS one.

[68]  Camilo Mora,et al.  Coral Reefs and the Global Network of Marine Protected Areas , 2006, Science.

[69]  V. Venus,et al.  Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models , 2008 .

[70]  R. Francini-Filho,et al.  Spawning patterns of commercially important reef fish (Lutjanidae and Serranidae) in the tropical western South Atlantic , 2011 .

[71]  W. Figueira Connectivity or demography: Defining sources and sinks in coral reef fish metapopulations , 2009 .

[72]  Alan Hastings,et al.  Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal , 2010 .

[73]  R. Steneck,et al.  Critical science gaps impede use of no-take fishery reserves. , 2005, Trends in ecology & evolution.

[74]  Claire B Paris-Limouzy,et al.  Scaling of Connectivity in Marine Populations , 2006, Science.

[75]  S. Andelman,et al.  Mathematical Methods for Identifying Representative Reserve Networks , 2000 .

[76]  Jason J. Roberts,et al.  Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations. , 2012, Integrative and comparative biology.

[77]  D. R. Robertson,et al.  Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae) , 2002, Molecular ecology.

[78]  Z. M. Leão,et al.  Conservation status and spatial patterns of AGRRA vitality indices in Southwestern Atlantic reefs. , 2010, Revista de biologia tropical.

[79]  Martin Nilsson Jacobi,et al.  Optimal networks of nature reserves can be found through eigenvalue perturbation theory of the connectivity matrix. , 2011, Ecological applications : a publication of the Ecological Society of America.