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Step-wise drops in modularity and the fragmentation of exploited marine metapopulations

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Abstract

Context

Many nearshore species are distributed in habitat patches connected only through larval dispersal. Genetic research has shown some spatial structure of such metapopulations and modeling studies have shed light onto possible patterns of connectivity and barriers. However, little is known about human impact on their spatial structure and patterns of connectivity.

Objectives

We examine the effects of fishing on the spatial and temporal dynamics of metapopulations of sedentary marine species (red sea urchin and red abalone) interconnected by larval dispersal.

Methods

We constructed a metapopulation model to simulate abalone and sea urchin metapopulations experiencing increasing levels of fishing mortality. We performed the modularity analysis on the yearly larval connectivity matrices produced by these simulations, and analyzed the changes of modularity and the formation of modules over time as indicators of spatial structure.

Results

The analysis revealed a strong modular spatial structure for abalone and a weak spatial signature for sea urchin. In abalone, under exploitation, modularity takes step-wise drops on the path to extinction, and modules breakdown into smaller fragments followed by module and later metapopulation collapse. In contrast, sea urchin showed high modularity variation, indicating high- and low-mixing years, but an abrupt collapse of the metapopulation under strong exploitation.

Conclusions

The results identify a disruption in larval connectivity and a pattern of collapse in highly modular nearshore metapopulations. These results highlight the ability of modularity to detect spatial structure in marine metapopulations, which varies among species, and to show early changes in the spatial structure of exploited metapopulations.

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References

  • Bell SS, Brooks RA, Robbins BD, Fonseca MS, Hall MO (2001) Faunal response to fragmentation in seagrass habitats: implications for seagrass conservation. Biol Conserv 100:115–123. doi:10.1016/S0006-3207(00)00212-3

    Article  Google Scholar 

  • Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends Ecol Evol 22:185–191

    Article  PubMed  Google Scholar 

  • Bonin MC, Almany GR, Jones GP (2011) Contrasting effects of habitat loss and fragmentation on coral-associated reef fishes. Ecology 92:1503–1512

    Article  PubMed  Google Scholar 

  • Borthagaray AI, Barreneche JM, Abades S, Arim M (2014) Modularity along organism dispersal gradients challenges a prevailing view of abrupt transitions in animal landscape perception. Ecography 37:564–571

    Article  Google Scholar 

  • Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500. doi:10.1146/annurev.ecolsys.27.1.477

    Article  Google Scholar 

  • California Department of Fish and Game (2005) Abalone recovery and management plan. The Resources Agency, Sacramento

    Google Scholar 

  • Carlisle J (1962) Spawning and early life history of Haliotis rufescens. Nautilus 76:44–48

    Google Scholar 

  • Cavanaugh KC, Siegel DA, Raimondi PT, Alberto F (2014) Patch definition in metapopulation analysis: a graph theory approach to solve the mega-patch problem. Ecology 95:316–328

    Article  PubMed  Google Scholar 

  • Ciannelli L, Fisher JAD, Skern-Mauritzen M, Hunsicker ME, Hidalgo M, Frank KT, Bailey KM (2013) Theory, consequences and evidence of eroding population spatial structure in harvested marine fishes: a review. Mar Ecol Prog Ser 480:227–243. doi:10.3354/meps10067

    Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  PubMed  Google Scholar 

  • Crandall ED, Treml EA, Liggins L, Gleeson L, Yasuda N, Barber PH, Wörheide G, Riginos C (2014) Return of the ghosts of dispersal past: historical spread and contemporary gene flow in the blue sea star Linckia laevigata. Bull Mar Sci 90:399–425. doi:10.5343/bms.2013.1052

    Article  Google Scholar 

  • Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJ Complex Syst, 1695. http://igraph.org

  • De Wit P, Palumbi SR (2013) Transcriptome-wide polymorphisms of red abalone (Haliotis rufescens) reveal patterns of gene flow and local adaptation. Mol Ecol 22:2884–2897

    Article  PubMed  Google Scholar 

  • Debenham P, Brzezinski M, Foltz K, Gaines S (2000) Genetic structure of populations of the red sea urchin, Strongylocentrotus franciscanus. J Exp Mar Biol Ecol 253:49–62

    Article  CAS  PubMed  Google Scholar 

  • Denny MW, Shibata MF (1989) Consequences of surf-zone turbulence for settlement and external fertilization. Am Nat 134:859–889

    Article  Google Scholar 

  • Deza AA, Anderson TW (2010) Habitat fragmentation, patch size, and the recruitment and abundance of kelp forest fishes. Mar Ecol Prog Ser 416:229–240

    Article  Google Scholar 

  • Dong C, McWilliams JC (2007) A numerical study of island wakes in the Southern California Bight. Cont Shelf Res 27:1233–1248

    Article  Google Scholar 

  • Dong C, McWilliams JC, Shchepetkin AF (2007) Island wakes in deep water. J Phys Oceanogr 37:962–981

    Article  Google Scholar 

  • Dong C, Idica EY, McWilliams JC (2009) Circulation and multiple-scale variability in the Southern California Bight. Prog Oceanogr 82:168–190

    Article  Google Scholar 

  • Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–567

    Article  Google Scholar 

  • FAO (2012) The state of the world fisheries and aquaculture 2012. Rome

  • Fletcher Jr RJ, Revell A, Reichert BE, Kitchens WM, Dixon JD, Austin JD (2013) Network modularity reveals critical scales for connectivity in ecology and evolution. Nat Commun. doi:10.1038/ncomms3572

    PubMed Central  Google Scholar 

  • Fortunato S (2010) Community detection in graphs. Phys Rep 486:75–174

    Article  Google Scholar 

  • Fortunato S, Barthélemy M (2007) Resolution limit in community detection. Proc Natl Acad Sci 104:36–41

    Article  CAS  PubMed  Google Scholar 

  • Gascoigne J, Lipcius RN (2004) Allee effects in marine systems. Mar Ecol Prog Ser 269:49–59

    Article  Google Scholar 

  • Girvan M, Newman MEJ (2002) Community structure in social and biological networks. Proc Natl Acad Sci 99:7821–7826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodsell PJ, Connell SD (2002) Can habitat loss be treated independently of habitat configuration? Implications for rare and common taxa in fragmented landscapes. Mar Ecol Prog Ser 239:37–44

    Article  Google Scholar 

  • Gruenthal KM, Acheson LK, Burton RS (2007) Genetic structure of natural populations of California red abalone (Haliotis rufescens) using multiple genetic markers. Mar Biol 152:1237–1248

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi:10.1126/science.1149345

    Article  CAS  PubMed  Google Scholar 

  • Harrold C, Reed DC (1985) Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–1169

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. doi:10.1126/science.1059199

    Article  CAS  PubMed  Google Scholar 

  • Jacobi MN, André C, Döös K, Jonsson PR (2012) Identification of subpopulations from connectivity matrices. Ecography 35:1004–1016

    Article  Google Scholar 

  • Johnson SY, Dartnell P, Cochrane GR, Golden NE, Phillips EL, Ritchie AC, Greene HG, Krigsman LM, Kvitek RG, Dieter BE, Endris CA, Seitz GG, Sliter RW, Erdey MD, Gutierrez CI, Wong FL, Yoklavich MM, Draut AE, Hart PE, Conrad JE (2013) California state waters map series: offshore of Santa Barbara, California. United States Geological Survey, Reston, VA

    Google Scholar 

  • Kaplan DM, Botsford LW, O’Farrell MR, Gaines SD, Jorgensen S (2009) Model-based assessment of persistence in proposed marine protected area designs. Ecol Appl 19:433–448. doi:10.1890/07-1705.1

    Article  PubMed  Google Scholar 

  • Karpov KA, Haaker PL, Taniguchi IK, Rogers-Bennett L (2000) Serial depletion and the collapse of the California abalone (Haliotis spp.) fishery. In: Campbell A (ed) Workshop on rebuilding abalone stocks in British Columbia. NRC Research Press, Ottawa, pp 11–24

    Google Scholar 

  • Kashtan N, Parter M, Dekel E, Mayo AE, Alon U (2009) Extinctions in heterogeneous environments and the evolution of modularity. Evolution 63:1964–1975. doi:10.1111/j.1558-5646.2009.00684.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Kato S, Schroeter SC (1985) Biology of the red sea urchin, Strongylocentrotus franciscanus, and its fishery in California. Mar Fish Rev 47:1–20

    Google Scholar 

  • Keitt TH, Urban DL, Milne BT (1997) Detecting critical scales in fragmented landscapes. Conserv Ecol 1:4

    Article  Google Scholar 

  • Kikuchi S, Uki N (1974) Technical study on artificial spawning of abalone, genus Haliotis III. Reasonable sperm density for fertilization. Bull Tohoku Reg Fish Res Lab 34:67–71

    Google Scholar 

  • Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Article  Google Scholar 

  • Kirby VL, Villa R, Powers DA (1998) Identification of microsatellites in the California red abalone, Haliotis rufescens. J Shellfish Res 17:801–804

    Google Scholar 

  • Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish Fish 5:131–140

    Article  Google Scholar 

  • Leaf RT, Andrews AH, Cailliet GM, Brown TA (2008) The feasibility of bomb radiocarbon analysis to support an age-at-length relationship for red abalone, Haliotis rufescens Swainson in Northern California. J Shellfish Res 27:1177–1182

    Article  Google Scholar 

  • Leet WS, Dewees CM, Klingbeil R, Larson EJ (2001) California’s living marine resources: a status report. UCANR Publications, Sacramento

    Google Scholar 

  • Leighton DL (1966) Studies of food preference in algivorous invertebrates of Southern California kelp beds. Pac Sci 20:104–113

    Google Scholar 

  • Leighton DL (1974) The influence of temperature on larval and juvenile growth in three species of Southern California abalones. Fish Bull 72:1137–1145

    Google Scholar 

  • Levitan DR (2002) Density-dependent selection on gamete traits in three congeneric sea urchins. Ecology 83:464–479

    Article  Google Scholar 

  • Miller KJ, Maynard BT, Mundy CN (2008) Genetic diversity and gene flow in collapsed and healthy abalone fisheries. Mol Ecol 18:200–211

    Article  PubMed  Google Scholar 

  • Minor ES, Urban DL (2007) Graph theory as a proxy for spatially explicit population models in conservation planning. Ecol Appl 17:1771–1782

    Article  PubMed  Google Scholar 

  • Mitarai S, Siegel DA, Watson JR, Dong C, McWilliams JC (2009) Quantifying connectivity in the coastal ocean with application to the Southern California Bight. J Geophys Res Oceans 114:C10026. doi:10.1029/2008JC005166

    Article  Google Scholar 

  • Moberg PE, Burton RS (2000) Genetic heterogeneity among adult and recruit red sea urchins, Strongylocentrotus franciscanus. Mar Biol 136:773–784

    Article  CAS  Google Scholar 

  • Myers RA, Barrowman NJ, Hutchings JA, Rosenberg AA (1995) Population dynamics of exploited fish stocks at low population levels. Science 269:1106–1108

    Article  CAS  PubMed  Google Scholar 

  • Newman MEJ (2006a) Modularity and community structure in networks. Proc Natl Acad Sci 103:8577–8582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman MEJ (2006b) Finding community structure in networks using the eigenvectors of matrices. Phys Rev E 74:36104

    Article  CAS  Google Scholar 

  • Opdam P (1991) Metapopulation theory and habitat fragmentation: a review of holarctic breeding bird studies. Landscape Ecol 5:93–106

    Article  Google Scholar 

  • Paris CB, Helgers J, van Sebille E, Srinivasan A (2013) Connectivity modeling system: a probabilistic modeling tool for the multi-scale tracking of biotic and abiotic variability in the ocean. Environ Model Softw 42:47–54

    Article  Google Scholar 

  • Pauly D (2009) Beyond duplicity and ignorance in global fisheries. Sci Mar. 73:215–224

    Article  Google Scholar 

  • Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci 106:5693–5697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pons P, Latapy M (2006) Computing communities in large networks using random walks. J Graph Algorithms Appl 10:191–218

    Article  Google Scholar 

  • Rogers-Bennett L (2013) Strongylocentrotus franciscanus and Strongylocentrotus purpuratus. In: Lawrence John M (ed) Sea urchins: biology and ecology. Elsevier, Amsterdam, pp 413–435

    Chapter  Google Scholar 

  • Rogers-Bennett L, Dondanville RF, Kashiwada J (2004) Size specific fecundity of red abalone (Haliotis rufescens): evidence for reproductive senescence? J Shellfish Res 23:553–560

    Google Scholar 

  • Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V, Held H, van Nes EH, Rietkerk M, Sugihara G (2009) Early-warning signals for critical transitions. Nat 461:53–59. doi:10.1038/nature08227

    Article  CAS  Google Scholar 

  • Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V, van de Koppel J, van de Leemput I, Levin SA, van Nes EH, Pascual M, Vandermeer J (2012) Anticipating critical transitions. Science 338:344–348. doi:10.1126/science.1225244

    Article  CAS  PubMed  Google Scholar 

  • Shchepetkin AF, McWilliams JC (2005) The regional oceanic modeling system (ROMS): a split-explicit, free-surface, topography-following-coordinate oceanic model. Ocean Model 9:347–404

    Article  Google Scholar 

  • Steinhaeuser K, Chawla NV (2010) Identifying and evaluating community structure in complex networks. Pattern Recognit Lett 31:413–421

    Article  Google Scholar 

  • Sterner T (2007) Unobserved diversity, depletion and irreversibility. The importance of subpopulations for management of cod stocks. Ecol Econ 61:566–574

    Article  Google Scholar 

  • Svedäng H, Stål J, Sterner T, Cardinale M (2010) Consequences of subpopulation structure on fisheries management: cod (Gadus morhua) in the Kattegat and Öresund (North Sea). Rev Fish Sci 18:139–150

    Article  Google Scholar 

  • Treml EA, Halpin PN, Urban DL, Pratson LF (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecol 23:19–36

    Article  Google Scholar 

  • van Nes EH, Scheffer M (2005) Implications of spatial heterogeneity for catastrophic regime shifts in ecosystems. Ecology 86:1797–1807

    Article  Google Scholar 

  • Watson JR, Mitarai S, Siegel DA, Caselle JE, Dong C, McWilliams JC (2010) Realized and potential larval connectivity in the Southern California Bight. Mar Ecol Prog Ser 401:31–48. doi:10.3354/meps08376

    Article  Google Scholar 

  • Watson JR, Siegel DA, Kendall BE, Mitarai S, Rassweiller A, Gaines SD (2011) Identifying critical regions in small-world marine metapopulations. Proc Natl Acad Sci 108:E907–E913. doi:10.1073/pnas.1111461108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White JW, Botsford LW, Moffitt EA, Fischer DT (2010) Decision analysis for designing marine protected areas for multiple species with uncertain fishery status. Ecol Appl 20:1523–1541

    Article  PubMed  Google Scholar 

  • Yang Z, Algesheimer R, Tessone CJ (2016) A comparative analysis of community detection algorithms on artificial networks. Sci Rep 6:30750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by NSF Grants OCE-0410439 as part of the Project “Linking Human and Biophysical Processes in the Coastal Marine Ecosystem of Baja California”, and GEO-1211972 as part of the CNH Project “Complexity and Adaptation in Marine Social-ecological Systems”. We also thank Satoshi Mitarai and David Siegel for creating the connectivity data, Laura Rogers-Bennett and Cynthia Catton for the useful information of red abalone and red sea urchin, and the Pisco Project for the abalone and sea urchin data made available in their website (http://www.piscoweb.org).

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Authors and Affiliations

  1. Department of Integrative Biology, University of Texas at Austin, 2415 Speedway, Stop C0390, Austin, Texas, 78712-0253, USA

    Tania S. Peña, Laura I. González-Guzmán & Timothy H. Keitt

  2. Stockholm Resilience Centre, Stockholm University, Kräftriket 2B, 106 91, Stockholm, Sweden

    James R. Watson

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  1. Tania S. Peña
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Correspondence to Tania S. Peña.

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Peña, T.S., Watson, J.R., González-Guzmán, L.I. et al. Step-wise drops in modularity and the fragmentation of exploited marine metapopulations. Landscape Ecol 32, 1643–1656 (2017). https://doi.org/10.1007/s10980-017-0532-9

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