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

INTRODUCTION

Habitat complexity and heterogeneity have been linked to changes in organism abundance and diversity in a variety of aquatic habitats (Beck 2000Beck 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 , Thrush et al. 2001Thrush 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 , Hauser et al. 2006Hauser 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 , Smith et al. 2014Smith 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 ). Habitat complexity is one of the most important factors structuring biotic assemblages (Kovalenko et al. 2012Kovalenko 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 ). It is associated with habitat heterogeneity, which exerts an important influence on ecological patterns and processes, affecting species distributions (Hewitt et al. 2008Hewitt 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 ) and persistence and resilience (Pimm 1984Pimm S.L. 1984. The complexity and stability of ecosystems. Nature, 307: 321-326. https://doi.org/10.1038/307321a0 , Kovalenko et al. 2012Kovalenko 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 ). Most studies of benthic communities define habitat complexity on the basis of the categorical geomorphological classifications of the substrate (Taniguchi and Tokeshi 2004Taniguchi 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 , Thrush et al. 2001Thrush 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 ), but some have suggested that the characterization of heterogeneity should include physical and biological components such as substrate type, algal assemblages, currents, depth, type of recruitment and ecological relationships (Witman and Dayton 2001Witman 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., Hauser et al. 2006Hauser 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 , Hermosillo-Nuñez et al. 2015Hermosillo-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 ).

Biogenic substrates, three-dimensional structures formed by living species (Morrison et al. 2014Morrison 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.) such as bivalve reefs, worm tubes, sea grass, coral and algae have been appropriately termed foundation species (Bruno and Bertness 2001Bruno 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.) and ecosystem engineers (sensu Jones et al. 1994Jones C.G., Lawton J.H., Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69: 373-386. https://doi.org/10.2307/3545850 ) and are thought to play a major role in structuring subtidal benthic marine communities (Lindsey et al. 2006Lindsey 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 ). Community biomass, species richness, and density of marine fauna tend to be much greater in biogenic habitats than on adjacent bare substrate (Reise 2002Reise 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 ). The biogenic complexity of habitats affects organisms living in their structures. Biogenic components can stabilize underlying substrates against erosion and can provide a hard substrate in an otherwise soft-sediment environment, facilitating the presence of sessile, encrusting or epifaunal organisms (Reise 2002Reise 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 , Lindsey et al. 2006Lindsey 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 ). Furthermore, the structural complexity afforded by these habitats can allow them to become a nursery habitat and refuge for small and young organisms against predation (Almany 2004Almany 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 , Hereu et al. 2005Hereu 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 ), disturbance and environmental stresses (Bruno and Bertness 2001Bruno 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.). Furthermore, the role of complexity is likely also dependent on whether species exhibit mobile or sessile life histories (McGuinness and Underwood, 1986McGuinness 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 ). Finally, habitat complexity is one of the most important factors structuring biotic assemblages (Kovalenko et al. 2012Kovalenko 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 , Smith et al. 2014Smith 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 ). The characteristics of the bottom could affect the local food supply for predators and grazers, making them an important factor in bottom-up trophic control of ecosystems (Witman and Dayton 2001Witman 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.).

In the subtidal benthic habitats, spatial complexity is partly generated by irregularities on the bottom, such as boulders, cracks and other projections (including caves), as well as by the presence of algal communities that exert a significant influence on the abundance and diversity of benthic species (Hauser et al. 2006Hauser 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 , Hermosillo-Nuñez et al. 2015Hermosillo-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 , Attrill et al. 2000Attrill 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 ). In communities dominated by macroalgae, the habitat complexity is identified as the most powerful factor influencing the richness and abundance of organisms (Thrush et al. 2001Thrush 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 , Almany 2004Almany 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 , Hauser et al. 2006Hauser 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 , Stelling-Wood et al. 2020Stelling‐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 ). The cover and morphological traits of different macroalgae species create a biogenic structure that plays an important role in defining the complexity of the studied habitats. Studies have found a positive correlation between algal and coral complexity and species abundance for echinoderm assemblages (Hermosillo-Nuñez et al. 2015Hermosillo-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 ), and complex algae have been found to have a higher amphipod density than structurally simpler algae (Hacker and Steneck 1990Hacker 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 ).

Though the role of structuring biogenic macroalgae in macroinvertebrate communities has been widely reported in the literature (Airoldi et al. 2008Airoldi 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 , Morrison et al. 2014Morrison 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.), most studies have focused on the particular structuring species, ignoring the variability of the macroalgal ensembles and their potential contribution to variability of macroinvertebrates, as well as that of species with a minor presence but a large impact. As a consequence of the increasing human impacts on coastal habitats, such as that of commercial harvesting, efforts have been focused on understanding the structure and function of these systems for conservation purposes (Stagnol et al. 2013Stagnol 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 et al. 2020Stelling‐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 ). To achieve this, it is necessary to obtain biological and ecological community data to determine baseline conditions for habitats subject to exploitation (Borja and Heinrich 2005Borja 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 ).

Community studies often consider species composition as the basic level of analysis (Hewitt et al. 2008Hewitt 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 ). However, the use of functional groups such as trophic behaviour can be highly suitable for the analysis of benthic communities, because species associations can be examined through variable responses to particular habitats (Duffy 2002Duffy 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 , Bremner et al. 2006Bremner 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 ). This approach could be used, as a complement to species diversity for evaluating the community structure, thus providing a better understanding of processes operating within habitats (Hewitt et al. 2008Hewitt 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 ). The distribution and abundance of functional groups are partially linked to the physical factors in the environment, and their trophic relationships determine the function of the community (Pearson and Rosenberg 1987Pearson T.H., Rosenberg R. 1987. Feast and famine: structuring factors in marine benthic communities. In Symposium of the British Ecological Society., Duffy 2002Duffy 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 ). The relationship among trophic groups determine the flow of energy within the communities (McQuaid and Branch 1985McQuaid 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 ), one of the central processes structuring marine ecosystems, which is related to properties such as stability and resilience of ecosystem function (Bremner et al. 2006Bremner 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 , Hewitt et al. 2008Hewitt 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 , Kovalenko et al. 2012Kovalenko 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 ).

Multispecific fisheries develop thanks to subtidal communities, so both biogenic species and those dependent on them at some point of their life cycle or along the food web can be targeted by fisheries in the same area, with feedback interactions overlaying on the particular environment with poorly reported consequences so far (Wright et al. 2014Wright 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 , Pérez-Matus et al. 2017Pérez‐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 ). Rocky subtidal habitats in eastern boundary upwelling systems, such as the Humboldt current system, are well recognized for sustaining productive benthic communities that have historically been under human exploitation (Thiel et al. 2007Thiel M., Castilla J. C., Fernández Bergia M. E., Navarrete S. 2007. The Humboldt current system of northern and central Chile.). Along the Chilean coast, in the last few decades, the collection of stranded kelps and other algae from the coast has been complemented by the direct diving to remove living biogenic specimens (Buschmann et al. 2008Buschmann 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 , Mac Monagail et al. 2017Mac 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 ). In the last two decades the brown seaweed (Lessonia spp) has been heavily extracted (Berrios et al. 2022). Among the red algae, harvesting of Chondracanthus chamissoi has been variable since the beginning of its commercialization in the 1980s (www.Sernapesca.cl). This variability seems related to time and area harvested, with harvest volumes driven by demand cycles on the international markets (Vásquez and Vega 2001Vásquez 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., Lotze et al. 2019Lotze 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 ) and heavy harvests in the last few years, especially in Tongoy Bay (González et al. 2016González 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 ).

In central Chile, the productivity of benthic communities depends on periodic upwelling (Montecino and Quiroz 2000Montecino 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 ), which has enabled the development of large benthic fisheries (González et al. 2016González 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 ). Exposed rocky subtidal habitats and those of protected bays sustain a variety of multispecific fisheries. While communities from exposed areas have been widely covered in the literature (Thiel et al, 2007Thiel M., Castilla J. C., Fernández Bergia M. E., Navarrete S. 2007. The Humboldt current system of northern and central Chile.), those of coastal bays have not. In Tongoy Bay, the main targets for exploitation are the crab Romaleon setosus, the snail Xanthochorus cassidiformis, the bivalve Mulinia edulis, the scallop Argopecten purpuratus and the red alga C. chamissoi. The latter, a biogenic species that adheres to sand-gravel substrates forming heterogeneous algal beds (González et al. 1997González 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., Uribe et al. 2020), where the stability of its populations could be related to the variability of the structuring of coastal communities (Vásquez and Vega 2001Vásquez 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.), indicates that habitat-forming organisms can influence the interspecific relationships of the macroinvertebrate community in the intertidal system (Umanzor et al. 2019Umanzor 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 ). Moreover, studies usually focus on very narrow coastal bands, comprising only partially the range of occupancy through which community members actually spread. In addition, the structuring role of the ecologically important C. chamissoi has not yet been addressed despite the serious problems of over-exploitation that extensive commercial harvesting seems to have posed (González et al. 2016González 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 . Lotze et al. 2019Lotze 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 ). Thus, the aim of this study was to elucidate the relationship between habitats with different degrees of bio-physical complexity (associated with biogenic structure) and benthic communities, with C. chamissoi as a model for analysis.

MATERIALS AND METHODS

Study area

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Tongoy Bay is influenced by a nearby upwelling centre (“Lengua de vaca”), which provides periodic intrusions of nutrient-rich water (Montecino and Quiroz 2000Montecino 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 ), and strong daily winds in the afternoon maintain a high degree of water circulation. The water temperature ranges from approximately 11ºC on the bottom to 19ºC on the surface in the summer. Under the summer conditions of high radiation and weak winds, a thermocline develops at a depth of approximately 10 to 15 m, which separates the warm surface water (16ºC-19ºC) from the colder bottom water (12ºC-15ºC). The deepest part of the bay reaches 90 m, and the average depth is approximately 25 m. Approximately 70% of the bay’s substrate is composed of sand, but gravel bottoms, sand mixed with shell debris, and areas with stones can also be found (Wolff and Alarcón 1993Wolff 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.).

Four different types of habitat were detected in Tongo Bay according to depth and basal substrate (Fig. 1): seagrass beds, sand-gravel, sand and mud (Jesse and Stotz 2002Jesse 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 , Ortiz and Wolff 2002aOrtiz 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 et al. 2003Ortiz 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 ). The seagrass beds (constituted of Zostera chilensis) are the shallowest, between 0 and 4 m depth. The sand habitat dominates at depths between 10 m and 14 m and is characterized by coarse sand and shells with a low organic matter content. The sand-gravel habitat is located between 4 and 10 m depth, and it is a transition zone characterized by high heterogeneity with sectors dominated by gravel, stones or rocks. The mud habitat is located in deeper waters (>14 m) with higher organic content (Ortiz and Wolff 2002aOrtiz 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 ).

Fig. 1.  Study area and habitat types with different structural complexities present in the Tongoy Bay benthic system: A, seagrass; B, sand-gravel; C, mud; and D, sand.

RESULTS

A total of 175 taxa were recorded from four habitats. Taxa of the Arthropoda and Mollusca accounted for 75% of the total species richness. The sample-based rarefaction for season and habitat type curves indicated that the efficiency and representativeness of total species richness was over 85% given by the best fit of Chao 1.

Most macrophytes included in Table 1 showed a widespread distribution in the study area despite between-substrate and seasonal variability. Nevertheless, Zostera chilensis, the species that defined the shallower sea grass habitat, was the only species restricted to that particular habitat between 0 and 4 m depth, while Gracilaria chilensis was absent in the mud habitat. Invertebrate species that contributed the largest overall mean biomass were distinguished as i) those that showed a widespread distribution among habitats e.g. the grazer snail T. cingulata, the middle predator Romaleon setosus and the filter feeder Argopecten. Purpuratus; ii) those restricted to a particular habitat type regardless of season, such as the structuring filter feeder Pyura chilensis and the grazer snail Trochita trochiformis in the sand-gravel; and iii) those that were only absent from a particular habitat: e.g. Heliaster helianthus and Luidia magallanica never occurred in the mud habitat and M. edulis did not occur in the seagrass habitat.

The richness, diversity and community structure of the invertebrate species were significantly different between seasons and habitats (Table 2). The greatest species richness occurred in winter, the greatest diversity was observed in summer, and biomass was similar in the two seasons. (Fig. 2A, B, C; Table 2). The three community indices showed the greatest difference at the substrate level. Meanwhile, the richness, biomass and diversity of total macroalgae were higher in summer than in winter (Fig. 2G, H, I; Table 2). The sand-gravel and seagrass habitats showed the greatest richness and diversity of algal species, whereas the sand and seagrass habitats showed the highest biomasses. Within seagrass, the mean biomass contribution of macrophytes was about 10 times that of invertebrates (Table 1, Fig. 2) and accounted for 6 of the 10 species of greatest within-habitat biomass. Most invertebrate species listed in Table 1showed two- to tenfold differences in mean biomass between seasons, but large standard deviations, with grazing snails tending to diminish in winter and no clear pattern for predators. The largest individual species contributors of biomass by an order of magnitude were the macrophytes Z. chilensis (accounting for over 40% of the biomass), which were also the least variable between seasons in fractional terms. Sarcodiotheca gaudichaudii, by contrast, dropped tenfold in winter. The other macrophytes also dropped in winter but within narrower ranges and large standard variability. In sand-gravel, on the other hand, the contribution of macrophytes was lower than that of invertebrates, which peaked in this habitat (Fig. 2, Table 1), and also lower than that in seagrass and sand (Fig. 2). Despite the significantly larger biomass of invertebrates in sand-gravel than in sand and seagrass, sand-gravel invertebrate species and trophic richness and diversity remained statistically indistinguishable from those of seagrass. All meaningful species regarding biomass contribution to any other habitat type could also be found in sand-gravel (Table 1). On the other hand, in the seagrass habitat at least one of the dominant macrophytes was conspicuously present regardless of season, and three of the macrophytes that peaked in sand-gravel experienced several-fold increases (C. chamissoi) and decreases (S. gaudichaudii and Rhodymenia skottsbergii) in mean biomass in winter in comparison with summer. Dominant grazer snails and filter feeders remained within a fractional seasonal change, while middle and top predators again varied several-fold. (Table 1).

In the sand habitat, macrophyte biomass was equal to that of seagrass, but with significantly lower richness and diversity. Invertebrate biomass was the lowest among the studied habitats and an order of magnitude lower than that of macrophytes. In this habitat, species and trophic invertebrate richness were the lowest, as was species diversity, while trophic diversity was lower than in the previous cases. M. edulis (suspension feeders) and the macrophyte Gracilaria chilensis showed the highest biomass in the sand habitat. G. chilensis had a biomass one to two orders of magnitude larger than that of any other macrophyte in the sand habitat and remained within a fractional change between seasons. In fact, this species accounted for 85% of macroalgal biomass in the sand habitat. Though it was also found in sand-gravel and seagrass habitats, its contribution there was marginal. In fact, in contrast with all other macrophytes listed in Table 1 that made an important contribution to more than a single habitat, G. chilensis contributed significantly only within the sand habitat, as did M. edulis among the invertebrate community. Only the middle predator R. setosus and the suspension feeder Sinum cymba contributed comparably with M. edulis in winter. Top predators were barely present in terms of biomass contributors. Finally, invertebrate biomass was two orders of magnitude higher than macrophyte biomass in the mud habitat, where the lowest macrophyte biomass was recorded.

Seasonal trends in the mud habitat were the opposite of those of the sand-gravel habitat for the most important macrophytes. The large invertebrate community was similar to that in the sand-gravel and seagrass habitats at species level, although trophic diversity matched that of the sand habitat. All the most important middle predators and surface filter feeders in the mud habitat in terms of biomass were present in a single season. Three middle predators present only in winter only in the mud habitat, Cancer coronatus in particular, showed the opposite pattern in the other habitats, diminishing overall in winter and disappearing completely from seagrass in that season. The targeted species R. setosus followed the same trend, increasing several-fold in sand-gravel in winter and remaining relatively stable in the other habitats, where it maintained similar levels within seasons. C. coronatus, on the other hand, diminished in sand-gravel in winter. The filter feeder A. purpuratus, one of the important target species for fisheries, appeared in the largest numbers in winter in the mud habitat, an order of magnitude higher than in the other substrates, while its lower biomass in the sand, sand-gravel and seagrass habitats also showed an increase in winter. The top predator Megynaster gelatinosus appeared in the mud habitat only in summer, when it decreased in sand-gravel and seagrass.

The SIMPER results for the invertebrate community (Table 3) showed the highest dissimilarities between the seagrass and sand habitats (94%), as well as the sand-gravel and sand habitats (93%). The species that contributed to the greatest dissimilarity were the clam A. purpuratu and the crab R. setosus, both present in all the habitats with large seasonal and spatial variability, whereas Oliva peruviana and Mulinia. edulis were only present in the sand habitat. The mud habitat exhibited over 86% dissimilarity to the other habitats, the species with the greatest contribution to this difference being the grazing snail Turritela cingulata. (Table 3), which in spite of its presence in all the habitats had a biomass two orders of magnitude larger in mud than in sand and seagrass.

The comparison of richness and biodiversity indices according to trophic groups showed differences between habitats, but not between seasons for the three indices evaluated (Fig. 2D, E, F, Table 2). The lowest values for biomass, diversity and richness (based on trophic groups) were observed in the sand habitat, while the other three habitats showed no significant differences in richness and intermediate diversity in muds. The sand-gravel and mud habitats showed higher biomass and richness diversity at the trophic group level than the other habitats.

For the invertebrate community, the RDA ordination revealed significant spatial and temporal variation of the community with a good fit and high statistical significance (Trace=0.910, p=0.002). In the RDA biplot, sites were separated mainly along the first axis, with sand and seagrass, the lowest biomass communities within negative x axis quadrants and sand-gravel and mud and sand-gravel in positive x quadrants, while the second axis indicated temporal separation between summer and winter. The differences between habitats were driven by the presence of differences species in a particular habitat (Fig. 3A). Consistent with the SIMPER analysis, some species showed a high degree of habitat specificity (e.g. the crab Gaudichaudia gaudichaudii and the clam M. edulis), while other species, such as the suspension feeder scallop A. purpuratus and the top predator crab R. setosus were present in more than one habitat. Pyura chilensis showed a significant role for sand-gravel habitat separation at the substrate level (first axis) but not along the seasonal dimension (second axis). Seasonal differences were mostly associated with changes in the relative contribution of species to overall biomass within substrates rather than changes in species composition.

RDA forward selection detected that the invertebrate community biomass variability in the sand-gravel habitat was associated with the presence of C. chamissoi, especially in winter (Fig. 3A). In this habitat snails (Tegula spp.) and sea stars (Luidia magallanica and Meyenaster gelatinosus) were associated with C. chamissoi in the winter season. Meanwhile, snails (e.g. Priene rude and X. cassidiformis) showed a strong relationship with the alga Rhodymenia corallina, which was also present in the mud habitat. The sand habitat was clearly associated with the alga G. chilensis, on which the clam P. theca was a characteristic species (Fig. 3A).

The RDA analyses conducted on trophic groups also showed great spatial and temporal variability of the communities, although the variance explained was lower than the analysis based on species (Trace=0.960, p=0.001). Different trophic groups characterized the different habitats. Temporal variability of each habitat (separation along the second axis of RDA) was associated with changes in the relative contribution of the same trophic group except in the mud habitat, where there was a shift in the dominant trophic group. Scavenger snails and suspension feeders dominated in winter in the mud habitat but were almost absent in summer. Grazer snails contributed to both the mud and the sand-gravel habitat in winter, but lower and middle predators dominated exclusively the sand-gravel habitat (Fig. 3B). The biomass of the commercial alga C. chamissoi was positively correlated with the occurrence of these predators and deposited feeders. C. chamissoi showed the largest biomass in sand-gravel, especially in winter. Meanwhile, the algae G. chilensis and Z. chilensis, which were present in the sand and seagrass habitat, respectively, were not related to the presence of any trophic group category (Fig. 3B).

DISCUSSION

In this study considering the entire macroalgal and macroinvetebrate assemblage from four different habitats and two seasons, we confirmed that macroinvertebrate community variability within and between habitats can be mainly (but not only) explained by a few macroalgal structuring species and previously neglected species. This study is one of the few that deals with macrobenthic communities in a depth range from intertidal to subtidal in four different types of habitat that share species of invertebrates and macrophytes, showing that population and community level analysis are interdependent between habitats, and seasonal changes cannot be understood in isolation from neighbouring habitats and pelagic conditions (Ortiz and Wolff 2002bOrtiz 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 ). Structuring macrophyte distribution in the habitats of this protected oceanic bay also depends on substrate type, #since the substrate required to hold also depend on the stability and energy of the environment, and depth#.

Despite the seasonal biomass change of Zostera chilensis and Sarcodiotheca gaudichaudii in the intertidal sea grass habitat and of Gracilaria chilensis in subtidal sand, which typically dominate in summer (Santelices 1989Santelices B. 1989. Algas marinas de Chile: distribución, ecología, utilización, diversidad. Santiago. Ediciones Universidad Católica de Chile. 399 pp.), they remained as the dominant species in winter in their respective substrates. Macroalgae are considered “niche constructers” for themselves or other organisms or as “ecosystem engineers” (Jones et al. 1994Jones C.G., Lawton J.H., Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69: 373-386. https://doi.org/10.2307/3545850 ). G. chilensis and S. gaudichaudii are coarsely-branched species and, together with the seagrass bed of Z. chilensis, constitute a complex seagrass habitat that seems to offer optimum conditions for other species/groups, such as microepifauna, epiphytes and infauna (Vásquez et al. 2003Vásquez 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 , Short et al. 2011Short 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 ). It has been widely reported that seagrass beds rank among the most productive ecosystems supporting benthic communities (Edgar and Barrett 2002Edgar 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 ), and this habitat could offer an optimum refuge (structural function) for recruits of the commercial species Argopecten purpuratus (Jesse and Stotz 2002Jesse 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 ) and serve as a nursery (Stotz and González 1997Stotz 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 ). However, the high productivity and ecological importance of a complex habitat is not necessarily translated into stable high in situ biomass, but rather into high richness and diversity of macroinvertebrate communities, as occurs in the sea grass in the present case. The structuring role of a diverse macrophyte habitat in sea grass throughout the year could also explain the fact that, despite seasonal changes, the macroinvertebrate community was stable between seasons. Habitat complexity supports a community structure that increases stability if food webs are organized (Duffy 2002Duffy 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 and Blanchard 2005Duplisea 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 , Kovalenko et al. 2012Kovalenko 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 ). More complex environments contain more refuges and suitable substrates, increasing the ecological interactions (Jesse and Stotz 2002Jesse 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 , Ortiz and Wolff 2002bOrtiz 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 , Almany 2004Almany 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 , Vásquez and Vega 2005Vásquez 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). In contrast with sea grass, in the more unstable sand substrate, the habitat was formed by the filamentous Gracilaria chilensis, which dominated the low-diversity macroalgal community throughout the year, and the very simple macrobenthic community at species and trophic level showed little change in the trophic structure.

Both mud and sand-gravel showed structural changes in macroalgal communities between seasons. In the mud habitat, which had the lowest macroalgal biomass, the diversity and richness increased in summer, while in the sand-gravel habitat there was a change in dominance of structuring species despite a more stable large biomass. In the mud and sand-gravel habitats we found the largest macroinvertebrate variability in biomass and species richness (but not trophic richness). In the mud habitat, invertebrate community structure at trophic level was not associated with macrophyta structuring species. Small snail species (e.g. T. cingulata and Priene rude), dominated the mud habitat and can be considered “opportunistic” species because they inhabit sediment enriched with organic matter (Pearson and Rosenberg 1987Pearson T.H., Rosenberg R. 1987. Feast and famine: structuring factors in marine benthic communities. In Symposium of the British Ecological Society.). Likewise, there was a high abundance (especially in winter) of T. cingulata, #which could stabilize the soft-sediment habitat# (Gaymer and Himmelman 2008Gaymer 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 ) and could be directly related to the richness and abundance of the associated infaunal species. In addition, in winter mobile species such as A. purpuratus and R. setosus were the main species responsible for the overall biomass increase of macrofauna, which could be associated with migratory responses to environmental seasonality (Ortiz and Wolf 2002bOrtiz 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 , León and Stotz 2004León 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 ). R. setosus is a highly mobile predator of A. purpuratus, so environmental changes that drive A. purpuratus distribution would indirectly affect the predator distribution (Ortiz and Wolff 2002aOrtiz 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 et al. 2003Ortiz 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 ).

In sand-gravel, overall macroalgal biomass did not change between summer and winter, but the macrophyte community structure did. Chondracanthus chamissoi increased its biomass by two orders of magnitude from summer to winter, and appeared as one of the two main structuring species. The abundance and morphological traits of C. chamissoi (a shrubby structure that offers surface area and internal space) increases the complexity of habitats and could play an important role in the biodiversity productivity of the habitats of Tongoy Bay, as has been reported for other algae (Vásquez and Vega 2001Vásquez 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., Stelling-Wood et al. 2020Stelling‐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 ). In winter, macroinvertebrate biomass and richness increased together with C. chamissoi, while trophic richness and diversity remained constant. A contribution to the stable structure at the trophic level between seasons can be associated with the high presence of the structuring filter feeder Pyura chilensis (Sepúlveda et al. 2003Sepúlveda 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 ). Sand-gravel shows higher production in the Tongoy Bay benthic system (Ortiz and Wolff 2002aOrtiz 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 ), where the hard, shrub-like C. chamissoi can offer a refuge and settlement habitat for other organisms, thus also contributing to sediment stability (Jesse and Stotz 2002Jesse 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 ). The second important species in sand-gravel was Rhodymenia corallina, which had a larger biomass in summer. The red alga R. corallina in the sand-gravel habitat was associated with herbivorous epifauna. In sand-gravel, R. setosus was the dominant top predator and fed mainly on the scallop A. purpuratus. By switching prey in response to changes in food availability (e.g. by reducing habitat complexity), top predators can modify the community structure in response to changes in prey availability (Ortiz et al. 2003Ortiz 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 ). This allows for a view of dynamic communities with an integrity beyond habitat types that at different times of the year display different combinations of biomass and biodiversity, allowing the persistence of populations that redistribute themselves and re-form bio-physical associations.

The distribution and abundance of the alga C. chamissoi and the filter feeder Pyura chilensis associated with the sand-gravel habitat generates high spatial heterogeneity. The higher sand-gravel habitat complexity could also reflect the interactions of algae with grazers and of preys with predators (filter feeders and top and middle carnivores), as reported by Kovalenko et al. (2012)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 and observed in the benthic community of the Tongoy Bay in the present study and in Jesse and Stotz (2002)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 and Ortiz et al. (2003)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 . Our results therefore coincide with Stelling-Wood et al. (2020)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 , who conclude from a literature review that the availability of more microhabitats can lead to an increase in the number of organisms or species that can reside in a given habitat through more available substrate and the fact that biogenic structures also articulate trophic interactions .

The commercial resources such as the crab R. setosus, the snail X. cassidiformis, the bivalve A. purpuratus, the red alga C. chamissoi and the filter feeder P. chilensis are trophically linked in the four habitats. The presence of C. chamissoi and P. chilensis could be increasing the habitat complexity and may decouple trophic interaction with a subsequent increase in ecosystem stability, as suggested by Kovalenko et al. (2012)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 for predator-prey relationships. C. chamissoi has a natural annual cycle regarding standing stock with maximums in spring-summer (González et al. 1997González 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., Vásquez and Vega 2001Vásquez 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.). This contrasted with our results, but González et al. (2016)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 reported that 37 t of C. chamissoi was harvested from Tongoy Bay in the summer of 2012, and our summer sampling was carried out post-harvest. Macroalgal harvesting often disturbs both the seabed and the organisms living within or on it, directly affecting the community attributes of the benthic system and indirectly changing the properties of the habitat structure (Blanchard et al. 2004Blanchard 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 ). The same type of disturbance of spatial heterogeneity and diversity could be expected from the removal of P. chilensis, a filter feeder harvested along the Chilean coast in large amounts, but it was not harvested in the Tongoy Bay during our study period. Therefore, the increase in the richness and biomass of the macrobenthic community observed in winter in sand-gravel was related to the increase in the commercial alga C. chamissoi. An intensive harvest of C. chamissoi could be regulating the overall dynamics of the benthic community, as is suggested by this study. The loss of such biogenic structures would have concomitant impacts on marine communities, because the loss of habitat structure generally leads to lower abundances and often declines in species richness, as has been found in other studies (Airoldi et al. 2008Airoldi 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 , Stagnol et al. 2013Stagnol 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 ). Therefore, it is necessary to include habitat heterogeneity explicitly within studies trying to predict the effect of fisheries on ecosystems. This is important to fisheries management. Habitats that are less damaged are suggested to contribute more recruits to fisheries, and to contain greater diversity than disturbed habitats (Thrush et al. 2001Thrush 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 , Ortiz and Wolf 2002bOrtiz 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 ).

Invertebrate community attributes cannot be directly inferred from single habitat seaweed diversity or biomass. Changes in seaweed biodiversity are likely to have implications for invertebrate epifauna only under specific scenarios or algal change (Bates and De Wreede 2007Bates 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 , Kelaher and Castilla 2005Kelaher 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 ). According to our results, the consequences of macroalgal/sea grass community variability on invertebrate communities will depend on the dominance of structuring species within each algal assemblage and habitat. As pointed out, the association of benthic communities and their particular habitats (physical and biogenic) could be used as an indicator of ecological variability in coastal ecosystems and has important implications for marine conservation and resource management (Airoldi et al. 2008Airoldi 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 ). The impact of fisheries activities on seafloor habitats and associated assemblages has only recently become the focus of research (Morrison et al. 2014Morrison 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.). Identifying and monitoring biogenic habitats of high conservation value has the potential to improve the efficacy of resource management (Handley et al. 2014Handley 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 , Lotze et al. 2019Lotze 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 ).