Contribution of echinoderms to keystone species complexes and macroscopic properties in kelp forest ecosystems (northern Chile)

  • Brenda B. Hermosillo-NúñezEmail author
Primary Research Paper


Quantitative and semi-qualitative multispecies trophic network models were used to evaluate the importance of echinoderms to keystone species complexes (KSCs) and their contribution to macroscopic properties in kelp forest ecosystems in the northern Chilean coast. The KSC is a core of species and functional groups playing a key role in the ecosystems. The macroscopic properties quantify the ecosystem’s development, organisation and ‘health’. Dynamical simulations were used to determine the most sensitive species of echinoderms compared to the main carnivores and herbivores in the networks. The echinoderms were present in all the studied KSCs, and their contribution to macroscopic properties was low, except their influence to the ecosystem complexity in comparison to the remaining components of KSCs. The sea star Meyenaster gelatinosus and the sea urchins Tetrapygus niger and Loxechinus albus were the most sensitive species in response to an increase of their total mortality, and the ecosystems would take more time to return to initial steady-state after disturbances. The results indicated that echinoderms play a key role in the benthic ecosystems of kelp forests along northern Chile and principally contribute to the complexity and resistance against perturbations in such ecosystems.


Macroscopic ecosystem properties Dynamic simulations Subtidal Invertebrates Disturbances Conservation 



I am deeply grateful to Dr. Marco Ortiz for suggestions, critical review and valuable comments. The information used for this study was obtained via the Grants INNOVA-CORFO 05CR11IXM-03 (Región de Atacama) and 09CN14-5873 (Región de Antofagasta).

Supplementary material

10750_2019_4134_MOESM1_ESM.docx (26.7 mb)
Supplementary material 1 (DOCX 27,348 kb)


  1. Allen, K. R., 1971. Relation between production and biomass. Journal of Fisheries Research Board of Canada 28: 1573–1581.CrossRefGoogle Scholar
  2. Almunia, J., G. Basterretxea, J. Arístegui & R. E. Ulanowicz, 1999. Benthic-pelagic switching in a coastal subtropical lagoon. Estuarine, Coastal and Shelf Science 49: 363–384.CrossRefGoogle Scholar
  3. Baird, D. & R. E. Ulanowicz, 1989. The seasonal dynamics of the Cheaspeake Bay ecosystem. Ecological Monographs 59: 329–364.CrossRefGoogle Scholar
  4. Baird, D. & R. E. Ulanowicz, 1993. Comparative study on the trophic structure, cycling and ecosystem properties of four tidal estuaries. Marine Ecology Progress Series 99: 221–237.CrossRefGoogle Scholar
  5. Baird, D., J. M. McGlade & R. E. Ulanowicz, 1991. The comparative ecology of six marine ecosystems. Philosophical Transactions—Royal Society of London, B 333: 15–29.CrossRefGoogle Scholar
  6. Banerjee, A., U. M. Scharler, B. D. Fath & S. Ray, 2017. Temporal variation of keystone species and their impact on system performance in a South African estuarine ecosystem. Ecological Modelling 363: 207–220.CrossRefGoogle Scholar
  7. Brey, T., J. Pearse, L. Basch, J. McClintock & M. Slattery, 1995. Growth and production of Sterechinus neumayeri (Echinoidea: Echinodermata) in McMurdo Sound, Antarctica. Marine Biology 124: 279–292.CrossRefGoogle Scholar
  8. Bronstein, O. & Y. Loya, 2014. Echinoid community structure and rates of herbivory and bioerosion on exposed and sheltered reefs. Journal of Experimental Marine Biology and Ecology 456: 8–17.CrossRefGoogle Scholar
  9. Carreiro-Silva, M. & T. R. McClanahan, 2001. Echinoid bioerosion and herbivory on Kenyan coral reefs: the role of protection from fishing. Journal of Experimental Marine Biology and Ecology 262: 133–153.PubMedCrossRefGoogle Scholar
  10. Cerda, G. & M. Wolff, 1993. Feeding ecology of the crab Cancer polyodon in La Herradura Bay, northern Chile. II. Food spectrum and prey consumption. Marine Ecology Progress Series 100: 119–125.CrossRefGoogle Scholar
  11. Christensen, V., 1995. Ecosystem maturity – towards quantification. Ecological Modelling 77: 3–32.CrossRefGoogle Scholar
  12. Christensen, V. & D. Pauly, 1992. ECOPATH II – a software for balancing steady-state ecosystem models and calculating network characteristics. Ecological Modelling 61: 169–185.CrossRefGoogle Scholar
  13. Christensen, V. & D. Pauly, 1993. Trophic Models of Aquatic Ecosystems. Trophic Models of Aquatic Ecosystem. International Center for Living Aquatic Resources Management, Manila.Google Scholar
  14. Christensen, V. & C. J. Walters, 2004. Ecopath with Ecosim: methods, capabilities and limitations. Ecological Modelling 172: 109–139.CrossRefGoogle Scholar
  15. Claoué, C., T. Hodges, T. Hill, W. Blyth & D. Easty, 1988. Neural spread of herpes simplex virus to the eye of the mouse: microbiological aspects and effect on the blink reflex. Eye (Basingstoke) 2: 318–323.Google Scholar
  16. Coleman, F. C. & S. L. Williams, 2002. Overexploiting marine ecosystems engineers: potential consequences for biodiversity. Trends in Ecology and Evolution 17: 40–44.CrossRefGoogle Scholar
  17. Costanza, R., 1992. Toward an operational definition of ecosytem health Ecosystem Health: New Goals for Environmental Management: 239–256.Google Scholar
  18. Costanza, R. & M. Mageau, 1999. What is a healthy ecosystem? Aquatic Ecology 33: 105–115.CrossRefGoogle Scholar
  19. Dambacher, J. M., D. J. Gaughan, M. Rochet, P. A. Rossignol & V. M. Trenkel, 2009. Qualitative modelling and indicators of exploited ecosystems. Fish and Fisheries 10: 305–322.CrossRefGoogle Scholar
  20. Dayton, P. K., G. A. Robilliard, R. T. Paine & L. B. Dayton, 1974. Biological accommodation in the Benthic Community at McMurdo Sound, Antarctica. Ecological Monographs 44: 105–128.CrossRefGoogle Scholar
  21. Dayton, P. K., M. J. Tegner, P. B. Edwards & K. L. Riser, 1999. Temporal and spatial scales of kelp demography: the role of oceanographic climate. Ecological Monographs 69: 219–250.CrossRefGoogle Scholar
  22. Docmac, F., M. Araya, I. A. Hinojosa, C. Dorador & C. Harrod, 2017. Habitat coupling writ large: pelagic-derived materials fuel benthivorous macroalgal reef fishes in an upwelling zone. Ecology 98: 2267–2272.PubMedCrossRefGoogle Scholar
  23. Dunne, J. A., R. J. Williams & N. D. Martinez, 2002. Food-web structure and network theory: the role of connectance and size. Proceedings of the National Academy of Sciences of the United States of America 99: 12917–12922.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fetahi, T. & S. Mengistou, 2007. Trophic analysis of Lake Awassa (Ethiopia) using mass-balance Ecopath model. Ecological Modelling 201: 398–408.CrossRefGoogle Scholar
  25. Gaedke, U. & D. Straile, 1998. Daphnids: keystone species for the pelagic food web structure and energy flow.- A body size-related analysis linking seasonal changes at the population and ecosystem levels. Advances in Limnology 53: 587–610.Google Scholar
  26. Gaymer, C. F. & J. H. Himmelman, 2008. A keystone predatory sea star in the intertidal zone is controlled by a higher-order predatory sea star in the subtidal zone. Marine Ecology Progress Series 370: 143–153.CrossRefGoogle Scholar
  27. Giacaman-Smith, J., S. Neira & H. Arancibia, 2016. Community structure and trophic interactions in a coastal management and exploitation area for benthic resources in central Chile. Ocean and Coastal Management 119: 155–163.CrossRefGoogle Scholar
  28. Gilbert, A. J., 2009. Connectance indicates the robustness of food webs when subjected to species loss. Ecological Indicators 9: 72–80.CrossRefGoogle Scholar
  29. Glynn, P. W., G. M. Wellington & C. Birkeland, 1979. Coral reef growth in the galapagos: limitation by sea urchins. Science 203: 8–10.CrossRefGoogle Scholar
  30. González, J., M. Ortiz, F. Rodríguez-Zaragoza & R. E. Ulanowicz, 2016. Assessment of long-term changes of ecosystem indexes in Tongoy Bay (SE Pacific coast): based on trophic network analysis. Ecological Indicators 69: 390–399.CrossRefGoogle Scholar
  31. Halfon, E., N. Schito & R. E. Ulanowicz, 1996. Energy flow through the Lake Ontario food web: conceptual model and an attempt at mass balance. Ecological Modelling 86: 1–36.CrossRefGoogle Scholar
  32. Harrold, C. & J. S. Pearse, 1987. The ecological role of echinoderms in kelp forest. In Press, C. (ed.), Echinoderms studies, Vol. 2. Academic Press, New York: 137–233.Google Scholar
  33. Hermosillo-Núñez, B. B., 2018. Determinación del complejo de especies clave y macrodescriptores en ecosistemas de coral y bosques de macroalgas: una contribución para el diseño de estrategias de manejo y protección de áreas marinas. PhD thesis, Universidad de Antofagasta, Chile.Google Scholar
  34. Hermosillo-Núñez, B. B., M. Ortiz & F. A. Rodríguez-Zaragoza, 2018. Keystone species complexes in kelp forest ecosystems along the northern Chilean coast (SE Pacific): improving multispecies management strategies. Ecological Indicators 93: 1101–1111.CrossRefGoogle Scholar
  35. Heymans, J. J., M. Coll, J. S. Link, S. Mackinson, J. Steenbeek, C. Walters & V. Christensen, 2016. Best practice in Ecopath with Ecosim food-web models for ecosystem-based management. Ecological Modelling 331: 173–184.CrossRefGoogle Scholar
  36. Hixon, M. A. & W. N. Brostoff, 1996. Succession and herbivory: effects of differential fish grazing on hawaiian coral-reef algae. Ecological Monographs 66: 67–90.CrossRefGoogle Scholar
  37. Hunter, M. D. & P. W. Price, 1992. Playing chutes and ladders: bottom-up and top-down forces in natural communities. Ecology 73: 724–732.Google Scholar
  38. Jones, C. G., J. H. Lawton & M. Shachak, 1994. Organisms as ecosystem emgineers. Oikos 69: 373–386.CrossRefGoogle Scholar
  39. Jordán, F., 2001. Trophic fields. Community Ecology 2: 181–185.CrossRefGoogle Scholar
  40. Jordan, F. & I. Molnár, 1999. Reliable ows and preferred patterns in food webs. Evolutionary Ecology 1(5): 591–609.Google Scholar
  41. Jordán, F., T. A. Okey, B. Bauer & S. Libralato, 2008. Identifying important species: linking structure and function in ecological networks. Ecological Modelling 216: 75–80.CrossRefGoogle Scholar
  42. Kaufman, A. G. & S. R. Borrett, 2010. Ecosystem network analysis indicators are generally robust to parameter uncertainty in a phosphorus model of Lake Sidney Lanier, USA. Ecological Modelling 221: 1230–1238.CrossRefGoogle Scholar
  43. Konar, B., M. S. Edwards & J. A. Estes, 2014. Biological interactions maintain the boundaries between kelp forests and urchin barrens in the Aleutian Archipelago. Hydrobiologia 724: 91–107.CrossRefGoogle Scholar
  44. Krebs, C. J., S. Boutin, R. Boonstra, A. R. E. Sinclair, J. N. M. Smith, M. R. T. Dale, K. Martin & R. Turkington, 1995. Impact of food and predation on the snowshoe hare cycle. Science 269: 1112–1115.PubMedCrossRefGoogle Scholar
  45. Leinaas, H. & H. Christie, 1996. Effects of removing sea urchins (Strongylocentrotus droebachiensis): stability of the barren state and succession of kelp forest recovery in the east Atlantic. Oecologia 105: 524–536.PubMedCrossRefGoogle Scholar
  46. Levins, R., 1968. Evolution in changing environments. Princeton Monograph Series.Google Scholar
  47. Levins, R., 1974. Discussion paper: the qualitative analysis of partially specified systems. Annals of the New York Academy of Sciences 231: 123–138.PubMedCrossRefGoogle Scholar
  48. Levins, R., 1998. The internal and external in explanatory theories. Science as Culture 7: 557–582.CrossRefGoogle Scholar
  49. Levins, R. & R. C. Lewontin, 1985. The Dialectical Biologist. Harvard University Press, Cambridge, MA.Google Scholar
  50. Libralato, S., V. Christensen & D. Pauly, 2006. A method for identifying keystone species in food web models. Ecological Modelling 195: 153–171.CrossRefGoogle Scholar
  51. Mann, K. H., 1982. Kelp, sea urchins and predators: a review of strong interactions in rocky subtidal systems of eastern Canada, 1970-1980. Netherlands Journal of Sea Research 16: 414–423.CrossRefGoogle Scholar
  52. Masterson, P., F. A. Arenas, R. C. Thompson & S. R. Jenkins, 2008. Interaction of top down and bottom up factors in intertidal rockpools: effects on early successional macroalgal community composition, abundance and productivity. Journal of Experimental Marine Biology and Ecology 363: 12–20.CrossRefGoogle Scholar
  53. May, R. M., 1972. Will a large complex system be stable? Nature 238: 413–414.PubMedCrossRefGoogle Scholar
  54. McClintock, J. B., J. S. Pearse & I. Bosch, 1988. Population structure and energetics of the shallow-water antarctic sea star Odontaster validus in contrasting habitats. Marine Biology 99: 235–246.CrossRefGoogle Scholar
  55. Monaco, M. E. & R. E. Ulanowicz, 1997. Comparative ecosystem trophic structure of three U.S. mid-Atlantic estuaries. Marine Ecology Progress Series 161: 239–254.CrossRefGoogle Scholar
  56. Muhly, T. B., M. Hebblewhite, D. Paton, J. A. Pitt, M. S. Boyce & M. Musiani, 2013. Humans strengthen bottom-up effects and weaken trophic cascades in a terrestrial food web. PLoS ONE. Scholar
  57. Navarrete, S. A. & J. C. Castilla, 2003. Experimental determination of predation intensity in an intertidal predator guild: dominant versus subordinate prey. Oikos 100: 251–262.CrossRefGoogle Scholar
  58. Okey, T. A., 2004. Shifted community states in four marine ecosystems: some potential mechanisms. PhD thesis, University of British Columbia, Vancouver.Google Scholar
  59. Ortiz, M., 2003. Qualitative modelling of the kelp forest of Lessonia nigrescens Bory (Laminariales: Phaeophyta) in eulittoral marine ecosystems of the south-east pacific: an approach to management plan assessment. Aquaculture 220: 423–436.CrossRefGoogle Scholar
  60. Ortiz, M., 2008a. Mass balance and dynamic simulations of trophic models of kelp ecosystems near the Mejillones Peninsula of northern Chile (SE Pacific): comparative network structure and assessment of harvest strategies. Ecological Modelling 216: 31–46.CrossRefGoogle Scholar
  61. Ortiz, M., 2008b. The effect of a crab predator (Cancer porteri) on secondary producers versus ecological model predictions in Tongoy Bay (south-east Pacific coast): implications for management and fisheries. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 923–929.CrossRefGoogle Scholar
  62. Ortiz, M., 2010. Dynamic and spatial models of kelp forest of Macrocystis integrifolia and Lessonia trabeculata (SE Pacific) for assessment harvest scenarios: short-term responses. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 494–506.CrossRefGoogle Scholar
  63. Ortiz, M., 2018. Robustness of macroscopic-systemic network indices after disturbances on diet-community matrices. Ecological Indicators 95: 509–517.CrossRefGoogle Scholar
  64. Ortiz, M. & R. Levins, 2011. Re-stocking practices and illegal fishing in northern Chile (SE Pacific coast): a study case. Oikos 120: 1402–1412.CrossRefGoogle Scholar
  65. Ortiz, M. & R. Levins, 2017. Self-feedbacks determine the sustainability of human interventions in eco-social complex systems: impacts on biodiversity and ecosystem health. PLoS ONE 12: 1–18.Google Scholar
  66. Ortiz, M. & M. Wolff, 2002a. Trophic models of four benthic communities in Tongoy Bay (Chile): comparative analysis and preliminary assessment of management strategies. Journal of Experimental Marine Biology and Ecology 268: 205–235.CrossRefGoogle Scholar
  67. Ortiz, M. & M. Wolff, 2002b. Dynamical simulation of mass-balance trophic models for benthic communities of north-central Chile: assessment of resilience time under alternative management scenarios. Ecological Modelling 148: 277–291.CrossRefGoogle Scholar
  68. Ortiz, M. & M. Wolff, 2008. Mass-balanced trophic and loop models of complex benthic systems in northern Chile (SE Pacific) to improve sustainable interventions: a comparative analysis. Hydrobiologia 605: 1–10.CrossRefGoogle Scholar
  69. Ortiz, M., M. Avendaño, L. Campos & F. Berrios, 2009. Spatial and mass balanced trophic models of La Rinconada Marine Reserve (SE Pacific coast), a protected benthic ecosystem: management strategy assessment. Ecological Modelling 220: 3413–3423.CrossRefGoogle Scholar
  70. Ortiz, M., M. Avendaño, M. Cantillañez, F. Berrios & L. Campos, 2010. Trophic mass balanced models and dynamic simulations of benthic communities from La Rinconada Marine Reserve off Northern Chile: network properties and multispecies harvest scenario assessments. Aquatic Conservation: Marine Freshwater Ecosystem 20: 58–73.CrossRefGoogle Scholar
  71. Ortiz, M., L. Campos, F. Berrios, F. A. Rodríguez-Zaragoza, B. B. Hermosillo-Núñez & J. González, 2013a. Network properties and keystoneness assessment in different intertidal communities dominated by two ecosystem engineer species (SE Pacific coast): a comparative analysis. Ecological Modelling 250: 307–318.CrossRefGoogle Scholar
  72. Ortiz, M., R. Levins, L. Campos, F. Berrios, F. Campos, F. Jordán, B. B. Hermosillo-Núñez, J. González & F. A. Rodríguez-Zaragoza, 2013b. Identifying keystone trophic groups in benthic ecosystems: implications for fisheries management. Ecological Indicators 25: 133–140.CrossRefGoogle Scholar
  73. Ortiz, M., F. Berrios, L. Campos, R. Uribe, A. Ramirez, B. B. Hermosillo-Núñez, J. González & F. A. Rodríguez-Zaragoza, 2015. Mass balanced trophic models and short-term dynamical simulations for benthic ecological systems of Mejillones and Antofagasta bays (SE Pacific): comparative network structure and assessment of human impacts. Ecological Modelling 309–310: 153–162.CrossRefGoogle Scholar
  74. Ortiz, M., B. B. Hermosillo-Núñez, J. González, F. A. Rodríguez-Zaragoza, I. Gómez & F. Jordán, 2017. Quantifying keystone species complexes: ecosystem-based conservation management in the King George Island (Antarctic Peninsula). Ecological Indicators 81: 453–460.CrossRefGoogle Scholar
  75. Paine, R. T., J. C. Castillo & J. Cancino, 1985. Perturbation and recovery patterns of starfish-dominated intertidal assemblages in Chile, New Zeland, and Washington State. The American Naturalist 125: 679–691.CrossRefGoogle Scholar
  76. Patrício, J., R. E. Ulanowicz, M. A. Pardal & J. C. Marques, 2004. Ascendency as an ecological indicator: a case study of estuarine pulse eutrophication. Estuarine, Coastal and Shelf Science 60: 23–35.CrossRefGoogle Scholar
  77. Pauly, D., V. Christensen & C. Walters, 2000. Ecopath, Ecosim, and Ecospace as tools for evaluating ecosystem impact of fisheries. ICES Journal of Marine Sciences 57: 697–706.CrossRefGoogle Scholar
  78. Pérez-Matus, A., S. A. Carrasco, S. Gelcich, M. Fernandez & E. A. Wieters, 2017. Exploring the effects of fishing pressure and upwelling intensity over subtidal kelp forest communities in Central Chile. Ecosphere 8: 1–18.CrossRefGoogle Scholar
  79. Polovina, J. J., 1984. Model of a coral reef ecosystem – I. The ECOPATH model and its application to French Frigate Shoals. Coral Reefs 3: 1–11.CrossRefGoogle Scholar
  80. Puccia, C. & R. Levins, 1991. Qualitative Modeling in Ecology: Loop Analysis, Signed Digraphs, and Time Averaging Qualitative Simulation Modeling and Analysis. Springer, New York: 119–143.Google Scholar
  81. Ray, S., R. E. Ulanowicz, N. C. Majee & A. B. Roy, 2000. Network analysis of a benthic food web model of a partly reclaimed island in the Sundarban mangrove ecosystem, India. Journal of Biological Systems 08: 263–278.CrossRefGoogle Scholar
  82. Ricker, W. E., 1968. Food from the Sea Committee on Resources and Man. US National Academy of Sciences, San Francisco, CA: 87–108.Google Scholar
  83. Rodríguez-Zaragoza, F. A., M. Ortiz, F. Berrios, L. Campos, A. de Jesús-Navarrete, J. M. Castro-Pérez, A. Hernández-Flores, M. García-Rivas, F. Fonseca-Peralta & E. Gallegos-Aguilar, 2016. Trophic models and short-term dynamic simulations for benthic-pelagic communities at Banco Chinchorro Biosphere Reserve (Mexican Caribbean): a conservation case. Community Ecology 17: 48–60.CrossRefGoogle Scholar
  84. Scheibling, R., 1986. Increased macroalgal abundance following mass mortalities of sea urchins (Strongylocentrotus droebachiensis) along the Atlantic coast of Nova Scotia. Oecologia 186–198.PubMedCrossRefGoogle Scholar
  85. Sparre, P., & S. C. Venema, 1997. Introduction to tropical fish stock assessment. Part 1. Manual. In: FAO Fisheries Technical Paper, No. 306. FAO, UN.Google Scholar
  86. Steneck, R., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. Estes & M. J. Tegner, 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29: 436–459.CrossRefGoogle Scholar
  87. Steneck, R. S., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. Estes & M. J. Tegner, 2018. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29: 436–459.CrossRefGoogle Scholar
  88. Strub, P. T., J. M. Mesías, V. Montecino, J. Rutllant & S. Salinas, 1998. Coastal ocean circulation off western south America coastal segment. In Robinson, A. R. & K. H. Brink (eds.), The Sea, Vol. 11. Wiley, New York.Google Scholar
  89. Tegner, M. J. & P. K. Dayton, 2000. Ecosystem effects of fishing in kelp forest communities. ICES Journal of Marine Science 57: 579–589.CrossRefGoogle Scholar
  90. Ulanowicz, R. E., 1986. Growth and Development: Ecosystems Phenomenology. Springer, New York.CrossRefGoogle Scholar
  91. Ulanowicz, R. E., 1997. Ecology, the Ascendent Perspective: Robert E. Columbia University Press, Ulanowicz.Google Scholar
  92. Ulanowicz, R. E. & C. J. Puccia, 1990. Mixed trophic impacts in ecosystems. Coenoses 5: 7–16.Google Scholar
  93. Uribe, R. A., M. Ortiz, A. S. Pacheco & R. Araya, 2015a. Early succession of micro-periphyton communities in kelp bed and barren ground ecological systems. Marine Ecology 36: 1415–1427.CrossRefGoogle Scholar
  94. Uribe, R. A., M. Ortiz, E. C. Macaya & A. S. Pacheco, 2015b. Successional patterns of hard-bottom macrobenthic communities at kelp bed (Lessonia trabeculata) and barren ground sublittoral systems. Journal of Experimental Marine Biology and Ecology 472: 180–188.CrossRefGoogle Scholar
  95. Urriago, J. D., J. H. Himmelman & C. F. Gaymer, 2011. Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster gelatinosus under field conditions. Journal of Experimental Marine Biology and Ecology 399: 17–24.CrossRefGoogle Scholar
  96. Urriago, J. D., J. H. Himmelman & C. F. Gaymer, 2012. Sea urchin Tetrapygus niger distribution on elevated surfaces represents a strategy for avoiding predatory sea stars. Marine Ecology Progress Series 444: 85–95.CrossRefGoogle Scholar
  97. Uthicke, S., B. Schaffelke & M. Byrne, 2009. A boom-bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecological Monographs 79: 3–24.CrossRefGoogle Scholar
  98. Valls, A., M. Coll, V. Christensen & A. M. Ellison, 2015. Keystone species: toward an operational concept for marine biodiversity conservation. Ecological Monographs 85: 29–47.CrossRefGoogle Scholar
  99. Vasas, V., C. Lancelot, V. Rousseau & F. Jordán, 2007. Eutrophication and overfishing in temperate nearshore pelagic food webs: a network perspective. Marine Ecology Progress Series 336: 1–14.CrossRefGoogle Scholar
  100. Vásquez, J. A., 2008. Production, use and fate of Chilean brown seaweeds: re-sources for a sustainable fishery. Journal of Applied Phycology 20: 457–467.CrossRefGoogle Scholar
  101. Vásquez, J. A. & A. H. Buschmann, 1997. Herbivore-kelp_interactions in Chilean subtidal communities: a review. Revista Chilena de Historia Natural 70: 41–52.Google Scholar
  102. Vásquez, J. A. & G. A. Donoso, 2013. Loxechinus albus Sea Urchins: Biology and Ecology. Elsevier, Amsterdam: 285–296.CrossRefGoogle Scholar
  103. Vásquez, J. A., N. Piaget & J. M. A. Vega, 2012. The Lessonia nigrescens fishery in northern Chile: “how you harvest is more important than how much you harvest”. Journal of Applied Phycology 24: 417–426.CrossRefGoogle Scholar
  104. Vásquez, J. A., S. Zuñiga, F. Tala, N. Piaget, D. C. Rodríguez & J. M. A. Vega, 2014. Economic valuation of kelp forests in northern Chile: values of goods and services of the ecosystem. Journal of Applied Phycology 26: 1081–1088.CrossRefGoogle Scholar
  105. Vega, J. M. A., B. R. Broitman & J. A. Vásquez, 2013. Monitoring the sustainability of Lessonia nigrescens (Laminariales, Phaeophyceae) in northern Chile under strong harvest pressure. Journal of Applied Phycology 26: 791–801.CrossRefGoogle Scholar
  106. Vermaat, J. A., J. A. Dunne & A. J. Gilbert, 2009. Major dimensions in food-web structure properties. Ecology 90: 278–282.PubMedCrossRefGoogle Scholar
  107. Villegas, M. J., J. Laudien, W. Sielfeld & W. E. Arntz, 2008. Macrocystis integrifolia and Lessonia trabeculata (Laminariales; Phaeophyceae) kelp habitat structures and associated macrobenthic community off northern Chile. Helgoland Marine Research 62: 33–43.CrossRefGoogle Scholar
  108. Walters, C. & V. Christensen, 2007. Adding realism to foraging arena predictions of trophic flow rates in Ecosim ecosystem models: shared foraging arenas and bout feeding. Ecological Modelling 209: 342–350.CrossRefGoogle Scholar
  109. Walters, C., V. Christensen & D. Pauly, 1997. Structuring dynamic models of exploited ecosystems from trophic mass-balance assessments. Reviews in Fish Biology and Fisheries 7: 139–172.CrossRefGoogle Scholar
  110. Warwick, R. M. & K. R. Clarke, 1993. Comparing the severity of disturbance: a meta-analysis of marine macrobenthic community data. Marine Ecology Progress Series 92: 221–231.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratorio de Modelamiento de Sistemas Ecológicos Complejos (LAMSEC), Instituto AntofagastaUniversidad de AntofagastaAntofagastaChile

Personalised recommendations