Biogenic habitats as drivers of invertebrate benthic community variability in Tongoy Bay (SE Pacific coast): implications of macroalga harvesting

Jorge E.  González; Beatriz  Yannicelli; Fabián  Rodríguez-Zaragoza; Marco  Ortiz

doi:10.3989/scimar.05350.057

Autores/as

Jorge E. González Grupo de Ecología Marina y Manejo, Departamento de Biología Marina, Universidad Católica del Norte (UCN) https://orcid.org/0000-0003-2823-5998
Beatriz Yannicelli Centro Universitario de la Región Este, Universidad de la República https://orcid.org/0000-0002-5512-1921
Fabián Rodríguez-Zaragoza Laboratorio de Ecología Molecular, Microbiología y Txonomía (LEMITAX), Departamento de Ecología, CUCBA, Universidad de Guadalajara https://orcid.org/0000-0002-0066-4275
Marco Ortiz Laboratorio de Modelamiento de Sistemas Ecológicos Complejos (LAMSEC), Instituto Antofagasta de Recursos Naturales, Universidad de Antofagasta, - Instituto de Ciencias Naturales Alexander Humboldt, Universidad de Antofagasta https://orcid.org/0000-0002-1126-7216

DOI:

https://doi.org/10.3989/scimar.05350.057

Palabras clave:

comunidades bentónicas, hábitat biogénico, diversidad, macroalgas, pesquerías

Resumen

La complejidad biogénica del hábitat ejercería una importante influencia positiva sobre las comunidades bentónicas. Examinamos la relación entre la variabilidad estacional de la estructura de las comunidades de macroinvertebrados (riqueza, diversidad y biomasa de especies y grupos tróficos) en hábitats con diferentes ensambles de macroalgas. Identificamos macroinvertebrados y algas en 336 muestras distribuidas en cuatro tipos de hábitats: arena, lodo, arena-grava y praderas de pastos marinos. En este estudio, considerando todo el conjunto de macroalgas y macroinvertebrados, confirmamos que la variabilidad de la comunidad de macroinvertebrados dentro y entre los hábitats puede ser explicada principalmente (pero no sólo) por unas pocas especies estructurantes de macroalgas. La variabilidad de la comunidad de macroinvertebrados entre hábitats y estaciones dependió de los cambios de la contribución relativa de las especies biostructurales explicativas en la comunidad algal. La biomasa, el comportamiento trófico y la riqueza de especies permanecieron estables en los hábitats con comunidades de macroalgas conspicuas, en contraste con los hábitats desprovistos de macroalgas. Sin embargo, la riqueza de especies de invertebrados y la biomasa sólo se mantuvieron estables en los hábitats cuyas especies dominantes no cambiaron entre estaciones, pero no en aquellos en los que las especies estructurantes dominantes cambiaron. El cambio estacional de una especie de macroalga estructurante clave (Condracanthus chamissoi), probablemente debido a su cosecha, tuvo importantes consecuencias en la reducción de la biomasa y la riqueza de la comunidad de invertebrados, tanto en su hábitat como en los hábitats adyacentes. Estas consecuencias son especialmente relevantes para los invertebrados vinculados por relaciones tróficas y que además son recursos pesqueros.

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Airoldi L., Balata D., Beck M.W. 2008. The gray zone: relationships between habitat loss and marine diversity and their applications in conservation. J. Exp. Mar. Biol. Ecol. 366(1): 8-15. https://doi.org/10.1016/j.jembe.2008.07.034

Almany G.R. 2004. Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106: 275-284. https://doi.org/10.1111/j.0030-1299.2004.13193.x

Anderson M.J., Gorely R.N., Clarke K.R. 2008. PERMANOVA + Primer: Guide to software and statistical methods. PRIMER-E Limited.

Attrill M.J., Strong J.A., Rowden A.A. 2000. Are macroinvertebrate communities inﬂuenced by structural complexity? Ecography 23: 114-121. https://doi.org/10.1111/j.1600-0587.2000.tb00266.x

Bates C.R., DeWreede R.E. 2007. Do changes in seaweed biodiversity influence associated invertebrate epifauna? J. Exp. Mar. Biol. Ecol. 344: 206-214. https://doi.org/10.1016/j.jembe.2007.01.002

Beck M.W. 2000. Separating the elements of habitat structure: independent effects of habitat complexity and structural components on rocky intertidal gastropods. J. Exp. Mar. Biol. Ecol. 249: 29-49. https://doi.org/10.1016/S0022-0981(00)00171-4 PMid:10817826

Blanchard F., Le Loc'h F., Hily C., Boucher J. 2004. Fishing effects on diversity, size and community structure of the benthic invertebrate and fish megafauna on the Bay of Biscay coast of France. Mar. Ecol. Prog. Ser. 280: 249-260. https://doi.org/10.3354/meps280249

Borja A., Heinrich H. 2005. Implementing the European Water Framework Directive: the debate continues. Mar. Pollut. Bull. 5: 486-488. https://doi.org/10.1016/j.marpolbul.2005.01.002 PMid:15823313

Bremner J., Rogers S.I., Frid C.L.J. 2006. Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecol. Indic. 6: 609-622. https://doi.org/10.1016/j.ecolind.2005.08.026

Bruno J.F., Bertness M.D. 2001. Habitat modification and facilitation in benthic marine communities. In: Bertness, M.D. (ed) Marine Community Ecology. Sinauer Associates Inc., Sunderland, MA, pp. 201-218.

Buschmann A.H., Hernandez-González M.D.C., Varela D. 2008. Seaweed future cultivation in Chile: perspectives and challenges. Int. J. Environ. Pollut, 33: 432-456. https://doi.org/10.1504/IJEP.2008.020571

Clarke, K.R, Gorley R.N. 2006. Primer v6: user manual/tutorial. Primer-E Ltd, Plymouth, UK. 260 pp.

Duffy J. E. 2002. Biodiversity and ecosystem function: the consumer connection. Oikos 99: 201-219. https://doi.org/10.1034/j.1600-0706.2002.990201.x

Duplisea D.E., Blanchard F. 2005. Relating species and community dynamics in an heavily exploited marine fish community. Ecosystems 8: 899-910. https://doi.org/10.1007/s10021-005-0011-z

Edgar G. J., Barrett N. S. 2002. Benthic macrofauna in Tasmanian estuaries: scales of distribution and relationships with environmental variables. J. Exp. Mar. Biol. Ecol. 270: 1-24. https://doi.org/10.1016/S0022-0981(02)00014-X

Gaymer C. F., Himmelman, J. H. 2008. A keystone predatory sea star in the intertidal zone is controlled by a higher-order predatory sea star in the subtidal zone. Mar. Ecol. Prog.Ser, 370: 143-153. https://doi.org/10.3354/meps07663

González J., Meneses I., Vásquez J. 1997. Field studies in Chondracanthus chamissoi (C. Agardh) Kützing. Seasonal and spatial variations in life cycle phases. Biología Pesquera (Chile) 26: 3-12.

González J., Ortiz M., Rodríguez-Zaragoza F., Ulanowicz R.E. 2016. Assessment of long-term changes of ecosystem indexes in Tongoy Bay (SE Pacific coast): Based on trophic network analysis. Ecol. Indic. 69: 390-399. https://doi.org/10.1016/j.ecolind.2016.04.019

Handley S.J., Willis T.J., Cole R.G., et al. 2014. The importance of benchmarking habitat structure and composition for understanding the extent of fishing impacts in soft sediment ecosystems. J. Sea Res. 86: 58-68. https://doi.org/10.1016/j.seares.2013.11.005

Hacker S.D., Steneck R.S. 1990. Habitat architecture and the abundance and body size dependent habitat selection of a phytal amphipod. Ecol. 71: 2269-2285. https://doi.org/10.2307/1938638

Hauser A. M., Attrill J., Cotton P. A. 2006. Effects of habitat complexity on the diversity and abundance of macrofauna colonising artificial kelp holdfasts. Mar. Ecol. Prog. Ser. 325: 93-100. https://doi.org/10.3354/meps325093

Hereu B., Zabala M., Linares C., Sala E. 2005. The effects of predator abundance and habitat structural complexity on survival of juvenile sea urchins. Mar.Biol. 146: 293-299. https://doi.org/10.1007/s00227-004-1439-y

Hermosillo-Nuñez B., Rodríguez-Zaragoza F., Ortiz M., Galván-Villa M. C., et al. 2015. Effect of habitat structure on the most frequent echinoderm species inhabiting coral reef communities at Isla Isabel National Park (Mexico). Community Ecol. 16: 125-134. https://doi.org/10.1556/168.2015.16.1.14

Hewitt J. E., Thrush S. F., Dayton P.D. 2008. Habitat variation, species diversity and ecological functioning in a marine system. J. Exp. Mar. Bio. Ecol. 366: 116-122. https://doi.org/10.1016/j.jembe.2008.07.016

Jesse S., Stotz W. 2002. Spatio-temporal distribution patterns of the crab assemblage in the shallow subtidal of the north Chilean Pacific coast. Crustaceana, 75: 1161-1200. https://doi.org/10.1163/156854002321518135

Jones C.G., Lawton J.H., Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69: 373-386. https://doi.org/10.2307/3545850

Kelaher B.P., Castilla J.C. 2005. Habitat characteristics influence macrofaunal communities in coralline turf more than mesoscale coastal upwelling on the coast of northern Chile. Estuar. Coast. Shelf Sci. 63, 155-165. https://doi.org/10.1016/j.ecss.2004.10.017

Kovalenko K. E., Thomaz S. M., Warfe D. M. 2012. Habitat complexity: approaches and future directions. Hydrobiologia, 685: 1-17. https://doi.org/10.1007/s10750-011-0974-z

Legendre P., Borcard D., Peres-Neto P. 2005. Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol. Monogr. 75: 435-450. https://doi.org/10.1890/05-0549

Lindsey E.L., Altier A.H., Witman J.D. 2006. Influence of biogenic habitat on the recruitment and distribution of a subtidal xanthid crab. Mar. Ecol. Prog. Ser. 306: 223-231. https://doi.org/10.3354/meps306223

León R.I., Stotz W. 2004. Diet and prey selection dynamics of Cancer polyodon in three different habitat typesin Tongoy Bay, Chile. J. Mar. Biolog. Assoc. 84: 751-756. https://doi.org/10.1017/S0025315404009865h

Lotze H.K., Milewski I., Fast J., et al. 2019. Ecosystem-based management of seaweed harvesting. Bot. Mar. 62: 395-409. https://doi.org/10.1515/bot-2019-0027

McGuinness K.A., Underwood A.J. 1986. Habitat structure and the nature of communities on intertidal boulders. J. Exp. Mar. Biol. 104: 97-123. https://doi.org/10.1016/0022-0981(86)90099-7

McQuaid C.D., Branch G.M. 1985. Trophic structure of rocky intertidal communities: Response to wave action and implications for energy flow. Mar. Ecol. Prog. Ser. 22: 153-161. https://doi.org/10.3354/meps022153

Mac Monagail M., Cornish L., Morrison L., et al. 2017. Sustainable harvesting of wild seaweed resources. Eur. J. Phycol. 52: 371-390. https://doi.org/10.1080/09670262.2017.1365273

Montecino V., Quiroz D. 2000. Specific primary production and phytoplankton cell size structure in an upwelling area off the coast of Chile (30º S). Aquat. Sci. 62: 364-380. https://doi.org/10.1007/PL00001341

Morrison M., Jones E.G., Consalvey M., Berkenbusch K. 2014. Linking marine fisheries species to biogenic habitats in New Zealand: a review and synthesis of knowledge. Ministry for Primary Industries.

Ortiz M., Wolff M. 2002a. Trophic models of four benthic communities in Tongoy Bay (Chile): comparative analysis and assessment of management strategies. J. Exp. Mar. Biol. Ecol. 268: 205-235. https://doi.org/10.1016/S0022-0981(01)00385-9

Ortiz M., Wolff M. 2002b. Spatially explicit trophic modelling of a harvested benthic ecosystem in Tongoy Bay (central northern Chile). Aquat. Conserv.: Mar. Freshw. Ecosyst. 12, 601-618. https://doi.org/10.1002/aqc.512

Ortiz M., Jesse S., Stotz W., Wolff M. 2003. Feeding behaviour of the asteroid Meyenaster gelatinosus in response to changes in abundance of the scallop Argopecten purpuratus in northern Chile. Arch. Hydrobiol. 157: 213-225. https://doi.org/10.1127/0003-9136/2003/0157-0213

Pearson T.H., Rosenberg R. 1987. Feast and famine: structuring factors in marine benthic communities. In Symposium of the British Ecological Society.

Pérez‐Matus A., Carrasco S. A., Gelcich S., et al. 2017. Exploring the effects of fishing pressure and upwelling intensity over subtidal kelp forest communities in Central Chile. Ecosphere, 8(5), e01808. https://doi.org/10.1002/ecs2.1808

Pimm S.L. 1984. The complexity and stability of ecosystems. Nature, 307: 321-326. https://doi.org/10.1038/307321a0

Reise K. 2002. Sediment mediated species interactions in coastal waters. J. Sea Res. 48: 127-141. https://doi.org/10.1016/S1385-1101(02)00150-8

Santelices B. 1989. Algas marinas de Chile: distribución, ecología, utilización, diversidad. Santiago. Ediciones Universidad Católica de Chile. 399 pp.

Sepúlveda R., Cancino J.M., Thiel M. 2003. The peracarid epifauna associated with the ascidian Pyura chilensis (Molina, 1782) (Ascidiacea: Pyuridae). J. Nat. Hist. 37: 1555-1569. https://doi.org/10.1080/00222930110099615

Short F.T., Polidoro B., Livingstone S.R., et al. 2011. Extinction risk assessment of the world's seagrass species. Biol. Conserv. 144: 1961-1971. https://doi.org/10.1016/j.biocon.2011.04.010

Smith R.S., Johnston E.L., Clark G.F. 2014. The role of habitat complexity in community development is mediated by resource availability. PloS ONE 9: e102920. https://doi.org/10.1371/journal.pone.0102920 PMid:25054325 PMCid:PMC4108414

Stagnol D., Renaud M., Davoult D. 2013. Effects of commercial harvesting of intertidal macroalgae on ecosystem biodiversity and functioning. Estuar. Coast. Shelf Sci. 130: 99-110. https://doi.org/10.1016/j.ecss.2013.02.015

Stelling‐Wood T.P., Gribben P.E., Poore A.G. 2020. Habitat variability in an underwater forest: Using a trait‐based approach to predict associated communities. Funct. Ecol. 34: 888-898. https://doi.org/10.1111/1365-2435.13523

Stotz W., González S.A. 1997. Abundance, growth, and production of the sea scallop Argopecten purpuratus (Lamarck 1819): bases for sustainable exploitation of natural scallop beds in north-central Chile. Fish. Res. 32: 173-183. https://doi.org/10.1016/S0165-7836(97)00010-6

Taniguchi H., Tokeshi M. 2004. Effects of habitat complexity on benthic assemblages in a variable environment. Freshwater Biol. 49: 1164-1178. https://doi.org/10.1111/j.1365-2427.2004.01257.x

terBraak C.J.F., Smilauer P. 2002. CANOCO Reference Manual and Cano Draw for Windows User's Guide: Software for Canonical Community Ordination, version 4.5. Microcomputer Power, Ithaca, NY.

Thiel M., Castilla J. C., Fernández Bergia M. E., Navarrete S. 2007. The Humboldt current system of northern and central Chile.

Thrush S.F., Hewitt J.E., Funnell G.A., et al. 2001. Fishing disturbance and marine biodiversity: the role of habitat structure in simple soft-sediment systems. Mar. Ecol. Prog. Ser. 223: 277-286. https://doi.org/10.3354/meps223277

Umanzor S., Ladah L., Calderon-Aguilera L.E., Zertuche-González J.A. 2019. Testing the relative importance of intertidal seaweeds as ecosystem engineers across tidal heights. J. Exp. Mar. Biol. 511: 100-107. https://doi.org/10.1016/j.jembe.2018.11.008

Vásquez J.A., Vega J.A. 2001. Chondracanthus chamissoi (Rhodophyta, Gigartinales) in northern Chile: ecological aspects for management of wild populations. J. Appl. Phycol. 13: 267-277.

Vásquez J.A., Vega J.M.A. 2005. Macro invertebrados asociados a discos de adhesión de algas pardas: biodiversidad de comunidades discretas como indicadora de perturbaciones locales y de gran escala. In: E. Figueroa (ed) Biodiversidad Marina: Valoración, Uso y Perspectivas. ¿Hacia dónde va Chile? Santiago, Chile: Ediciones Universitaria, 429-450

Vásquez N., Guerra García J.M., Thiel M., Lancellotti D.A. 2003. The distribution of littoral caprellids (Crustacea: Amphipoda: Caprellidea) along the Pacific coast of continental Chile. Rev. Chil. Hist. Nat. 76: 297-311. https://doi.org/10.4067/S0716-078X2003000200014

Witman J.D., Dayton P.K. 2001. Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates Inc, Sunderland. 339 - 366.

Wolff M., Alarcón E. 1993. Structure of a scallop Argopecten purpuratus (Lamarck, 1819) dominated subtidal macro-invertebrate assemblage in northern Chile. J. SheIlfish Res. 12: 295-304.

Wright J.T., Byers J.E., DeVore J. L., Sotka E.E. 2014. Engineering or food? Mechanisms of facilitation by a habitat‐forming invasive seaweed. Ecology, 95: 2699-2706. https://doi.org/10.1890/14-0127.1