Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

A tale of two key species in a subtropical mudflat: four-fold density increases produce minimal ecological response in macrofauna

Navodha G. Dissanayake https://orcid.org/0000-0003-3977-1753 A * , Bryony A. Caswell https://orcid.org/0000-0001-8488-0890 B and Christopher L. J. Frid A
+ Author Affiliations
- Author Affiliations

A School of Environment and Sciences, Griffith University, Parklands Drive, Gold Coast, Qld 4222, Australia.

B Department of Geography, Geology and Environment, University of Hull, Hull, HU6 7RX, UK.


Handling Editor: Martin Skov

Marine and Freshwater Research 73(7) 954-972 https://doi.org/10.1071/MF21308
Submitted: 19 October 2021  Accepted: 14 March 2022   Published: 26 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Understanding how ecosystems function to deliver services is essential if we are to limit the impacts off human activities.

Aim: We hypothesised that increased densities of whelk, Pyrazus ebeninus, and crab, Macrophthalmus setosus, up to four times (given their large body-size and ecological roles, e.g. consuming deposits and disturbing sediments) would affect the macrofaunal community and how it functions in a south-eastern Queensland mudflat.

Method: The biota and physical environment of the field-deployed cages (three density treatments, caged and control plots) were sampled up to 90 days.

Results: After 90 days, the redox discontinuity layer was deeper and sediment organic matter was higher in all density treatments. This is consistent with enhanced burrowing, surface disturbance, mucus and pellet production. However, no significant changes in the taxonomic composition of the unmanipulated portion of the macrofaunal resident assemblage were observed.

Conclusion: Whereas some communities change structurally when perturbated and then revert, this community remained in the new manipulated configuration for at least 90 days.

Implications: Limited understanding of the ecological relationships in these systems, such as the processes operating to support this large increase in deposit-feeding biomass constrains evidence-based management. These systems may be able to, at least temporally, support enhanced biomasses and levels of ecosystem services.

Keywords: benthic ecology, biological traits​, bioturbation​, ecological functioning​, ecosystem services​, environmental management​, experiment, invertebrate​.


References

Aguilera, MA, Dobringer, J, and Petit, IJ (2018). Heterogeneity of ecological patterns, processes, and funding of marine manipulative field experiments conducted in Southeastern Pacific coastal ecosystems. Ecology and Evolution 8, 8627–8638.
Heterogeneity of ecological patterns, processes, and funding of marine manipulative field experiments conducted in Southeastern Pacific coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 30250729PubMed |

Barbier, EB, Hacker, SD, Kennedy, C, Koch, EW, Stier, AC, and Silliman, BR (2011). The value of estuarine and coastal ecosystem services. Ecological Monographs 81, 169–193.
The value of estuarine and coastal ecosystem services.Crossref | GoogleScholarGoogle Scholar |

Barnes, RSK (2010). Review of the sentinel amdnand allied crabs (Crustacea: Brachyura: Macrophthalmidae), with particular reference to the genus Macrophthalmus. The Raffles Bulletin of Zoology 58, 31–49.

Beesley PL, Ross GJB, Wells A (Eds) (1998) ‘Mollusca: The Southern Synthesis. Fauna of Australia. Vol. 5, Part A.’ (Australian Biological Resources Study: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia)

Beesley PL, Ross GJB, Glasby CJ (Eds) (2000) ‘Polychaetes and allies: the southern synthesis. Fauna of Australia. Vol. 4A. Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula.’ (Australian Biological Resources Study: Canberra, ACT, Australia; and CSIRO Publishing: Melbourne, Vic., Australia)

Benedetti-Cecchi, L, and Cinelli, F (1997). Confounding in field experiments: direct and indirect effects of artifacts due to the manipulation of limpets and macroalgae. Journal of Experimental Marine Biology and Ecology 209, 171–184.
Confounding in field experiments: direct and indirect effects of artifacts due to the manipulation of limpets and macroalgae.Crossref | GoogleScholarGoogle Scholar |

Beninger, PG, Boldina, I, and Katsanevakis, S (2012). Strengthening statistical usage in marine ecology. Journal of Experimental Marine Biology and Ecology 426–427, 97–108.
Strengthening statistical usage in marine ecology.Crossref | GoogleScholarGoogle Scholar |

Bertness, MD, Brisson, CP, Coverdale, TC, Bevil, MC, Crotty, SM, and Suglia, ER (2014). Experimental predator removal causes rapid salt marsh die‐off. Ecology Letters 17, 830–835.
Experimental predator removal causes rapid salt marsh die‐off.Crossref | GoogleScholarGoogle Scholar | 24766277PubMed |

Biles, CL, Solan, M, Isaksson, I, Paterson, DM, Emes, C, and Raffaelli, DG (2003). Flow modifies the effect of biodiversity on ecosystem functioning: an in situ study of estuarine sediments. Journal of Experimental Marine Biology and Ecology 285–286, 165–177.
Flow modifies the effect of biodiversity on ecosystem functioning: an in situ study of estuarine sediments.Crossref | GoogleScholarGoogle Scholar |

Bishop, MJ, Kelaher, BP, Alquezar, R, York, PH, Ralph, PJ, and Greg Skilbeck, C (2007). Trophic cul-de-sac, Pyrazus ebeninus, limits trophic transfer through an estuarine detritus-based food web. Oikos 116, 427–438.
Trophic cul-de-sac, Pyrazus ebeninus, limits trophic transfer through an estuarine detritus-based food web.Crossref | GoogleScholarGoogle Scholar |

Bolam, SG, Fernandes, TF, and Huxham, M (2002). Diversity, biomass, and ecosystem processes in the marine benthos. Ecological Monographs 72, 599–615.
Diversity, biomass, and ecosystem processes in the marine benthos.Crossref | GoogleScholarGoogle Scholar |

Booty, JM, Underwood, GJC, Parris, A, Davies, RG, and Tolhurst, TJ (2020). Shorebirds affect ecosystem functioning on an intertidal mudflat. Frontiers in Marine Science 7, 685.
Shorebirds affect ecosystem functioning on an intertidal mudflat.Crossref | GoogleScholarGoogle Scholar |

Botto, F, and Iribarne, O (1999). Effect of the burrowing crab Chasmagnathus granulata (Dana) on the benthic community of a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 241, 263–284.
Effect of the burrowing crab Chasmagnathus granulata (Dana) on the benthic community of a SW Atlantic coastal lagoon.Crossref | GoogleScholarGoogle Scholar |

Braeckman, U, Provoost, P, Gribsholt, B, Van Gansbeke, D, Middelburg, JJ, Soetaert, K, Vincx, M, and Vanaverbeke, J (2010). Role of macrofauna functional traits and density in biogeochemical fluxes and bioturbation. Marine Ecology Progress Series 399, 173–186.
Role of macrofauna functional traits and density in biogeochemical fluxes and bioturbation.Crossref | GoogleScholarGoogle Scholar |

Bremner, J (2008). Species’ traits and ecological functioning in marine conservation and management. Journal of Experimental Marine Biology and Ecology 366, 37–47.
Species’ traits and ecological functioning in marine conservation and management.Crossref | GoogleScholarGoogle Scholar |

Bremner, J, Frid, CLJ, and Rogers, SI (2003). Assessing marine ecosystem health: the long-term effects of fishing on functional biodiversity in North Sea benthos. Aquatic Ecosystem Health & Management 6, 131–137.
Assessing marine ecosystem health: the long-term effects of fishing on functional biodiversity in North Sea benthos.Crossref | GoogleScholarGoogle Scholar |

Bremner, J, Rogers, SI, and Frid, CLJ (2006). Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecological Indicators 6, 609–622.
Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA).Crossref | GoogleScholarGoogle Scholar |

Bulling, MT, Hicks, N, Murray, L, Paterson, DM, Raffaelli, D, White, PCL, and Solan, M (2010). Marine biodiversity–ecosystem functions under uncertain environmental futures. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 365, 2107–2116.
Marine biodiversity–ecosystem functions under uncertain environmental futures.Crossref | GoogleScholarGoogle Scholar | 20513718PubMed |

Cardinale, BJ, Matulich, KL, Hooper, DU, Byrnes, JE, Duffy, E, Gamfeldt, L, Balvanera, P, O’connor, MI, and Gonzalez, A (2011). The functional role of producer diversity in ecosystems. American Journal of Botany 98, 572–592.
The functional role of producer diversity in ecosystems.Crossref | GoogleScholarGoogle Scholar | 21613148PubMed |

Caswell, BA, and Frid, CLJ (2017). Marine ecosystem resilience during extreme deoxygenation: the Early Jurassic oceanic anoxic event. Oecologia 183, 275–290.
Marine ecosystem resilience during extreme deoxygenation: the Early Jurassic oceanic anoxic event.Crossref | GoogleScholarGoogle Scholar | 27757544PubMed |

Cesar, CP, and Frid, CLJ (2009). Effects of experimental small‐scale cockle (Cerastoderma edule L.) fishing on ecosystem function. Marine Ecology 30, 123–137.
Effects of experimental small‐scale cockle (Cerastoderma edule L.) fishing on ecosystem function.Crossref | GoogleScholarGoogle Scholar |

Cesar, CP, and Frid, CLJ (2012). Benthic disturbance affects intertidal food web dynamics: implications for investigations of ecosystem functioning. Marine Ecology Progress Series 466, 35–41.
Benthic disturbance affects intertidal food web dynamics: implications for investigations of ecosystem functioning.Crossref | GoogleScholarGoogle Scholar |

Chevene, F, Doléadec, S, and Chessel, D (1994). A fuzzy coding approach for the analysis of long‐term ecological data. Freshwater Biology 31, 295–309.
A fuzzy coding approach for the analysis of long‐term ecological data.Crossref | GoogleScholarGoogle Scholar |

Clare, DS, Spencer, M, Robinson, LA, and Frid, CLJ (2016). Species densities, biological interactions and benthic ecosystem functioning: an in situ experiment. Marine Ecology Progress Series 547, 149–161.
Species densities, biological interactions and benthic ecosystem functioning: an in situ experiment.Crossref | GoogleScholarGoogle Scholar |

Colegrave, N, and Ruxton, GD (2017). Statistical model specification and power: recommendations on the use of test-qualified pooling in analysis of experimental data. Proceedings of the Royal Society of London – B. Biological Sciences 284, 20161850.
Statistical model specification and power: recommendations on the use of test-qualified pooling in analysis of experimental data.Crossref | GoogleScholarGoogle Scholar |

Como, S, Rossi, F, and Lardicci, C (2006). Caging experiment: relationship between mesh size and artifacts. Journal of Experimental Marine Biology and Ecology 335, 157–166.
Caging experiment: relationship between mesh size and artifacts.Crossref | GoogleScholarGoogle Scholar |

Crowe TP, Frid CLJ (2015) ‘Marine Ecosystems: Human Impacts on Biodiversity, Functioning and Services.’ (Cambridge University Press: Cambridge, UK)

Dayton, PK, Robilliard, GA, Paine, RT, and Dayton, LB (1974). Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecological Monographs 44, 105–128.
Biological accommodation in the benthic community at McMurdo Sound, Antarctica.Crossref | GoogleScholarGoogle Scholar |

DeWitt, TH, and Levinton, JS (1985). Disturbance, emigration, and refugia: how the mud snail, Ilyanassa obsoleta (Say), affects the habitat distribution of an epifaunal amphipod, Microdeutopus gryllotalpa (Costa). Journal of Experimental Marine Biology and Ecology 92, 97–113.
Disturbance, emigration, and refugia: how the mud snail, Ilyanassa obsoleta (Say), affects the habitat distribution of an epifaunal amphipod, Microdeutopus gryllotalpa (Costa).Crossref | GoogleScholarGoogle Scholar |

Díaz, S, Symstad, AJ, Chapin , FS, Wardle, DA, and Huenneke, LF (2003). Functional diversity revealed by removal experiments. Trends in Ecology & Evolution 18, 140–146.
Functional diversity revealed by removal experiments.Crossref | GoogleScholarGoogle Scholar |

Dissanayake, NG, Frid, CLJ, Drylie, TP, and Caswell, BA (2018). Ecological functioning of mudflats: global analysis reveals both regional differences and widespread conservation of functioning. Marine Ecology Progress Series 604, 1–20.
Ecological functioning of mudflats: global analysis reveals both regional differences and widespread conservation of functioning.Crossref | GoogleScholarGoogle Scholar |

Dissanayake, NG, Frid, CLJ, and Caswell, BA (2020a). Biodiversity, trait composition and ecological functioning: impacts of coastal urbanisation on subtropical mudflats. Marine and Freshwater Research 71, 1043–1061.
Biodiversity, trait composition and ecological functioning: impacts of coastal urbanisation on subtropical mudflats.Crossref | GoogleScholarGoogle Scholar |

Dissanayake, NG, Frid, CLJ, and Caswell, BA (2020b). Biodiversity, trait composition and ecological functioning: impacts of coastal urbanisation on subtropical mudflats. PANGAEA. , .
Biodiversity, trait composition and ecological functioning: impacts of coastal urbanisation on subtropical mudflats.Crossref | GoogleScholarGoogle Scholar |

Duffy, JE, Paul Richardson, J, and Canuel, EA (2003). Grazer diversity effects on ecosystem functioning in seagrass beds. Ecology Letters 6, 637–645.
Grazer diversity effects on ecosystem functioning in seagrass beds.Crossref | GoogleScholarGoogle Scholar |

Edwards, SF, and Welsh, BL (1982). Trophic dynamics of a mud snail [Ilyanassa obsoleta (Say)] population on an intertidal mudflat. Estuarine, Coastal and Shelf Science 14, 663–686.
Trophic dynamics of a mud snail [Ilyanassa obsoleta (Say)] population on an intertidal mudflat.Crossref | GoogleScholarGoogle Scholar |

Ehrnsten, E, Norkko, A, Timmermann, K, and Gustafsson, BG (2019). Benthic–pelagic coupling in coastal seas: modelling macrofaunal biomass and carbon processing in response to organic matter supply. Journal of Marine Systems 196, 36–47.
Benthic–pelagic coupling in coastal seas: modelling macrofaunal biomass and carbon processing in response to organic matter supply.Crossref | GoogleScholarGoogle Scholar |

Ehrnsten, E, Sun, X, Humborg, C, Norkko, A, Savchuk, OP, Slomp, CP, Timmermann, K, and Gustafsson, BG (2020). Understanding environmental changes in temperate coastal seas: linking models of benthic fauna to carbon and nutrient fluxes. Frontiers in Marine Science 7, 450.
Understanding environmental changes in temperate coastal seas: linking models of benthic fauna to carbon and nutrient fluxes.Crossref | GoogleScholarGoogle Scholar |

Faulwetter, S, Markantonatou, V, Pavloudi, C, Papageorgiou, N, Keklikoglou, K, Chatzinikolaou, E, Pafilis, E, Chatzigeorgiou, G, Vasileiadou, K, Dailianis, T, Fanini, L, Koulouri, P, and Arvanitidis, C (2014). Polytraits: a database on biological traits of marine polychaetes. Biodiversity Data Journal 2014, e1024.
Polytraits: a database on biological traits of marine polychaetes.Crossref | GoogleScholarGoogle Scholar |

Frid, CLJ, and Caswell, BA (2016). Does ecological redundancy maintain functioning of marine benthos on centennial to millennial time scales? Marine Ecology 37, 392–410.
Does ecological redundancy maintain functioning of marine benthos on centennial to millennial time scales?Crossref | GoogleScholarGoogle Scholar |

Gallucci, F, Sauter, E, Sachs, O, Klages, M, and Soltwedel, T (2008). Caging experiment in the deep sea: efficiency and artefacts from a case study at the Arctic long-term observatory Hausgarten. Journal of Experimental Marine Biology and Ecology 354, 39–55.
Caging experiment in the deep sea: efficiency and artefacts from a case study at the Arctic long-term observatory Hausgarten.Crossref | GoogleScholarGoogle Scholar |

Gammal, J, Norkko, J, Pilditch, CA, and Norkko, A (2017). Coastal hypoxia and the importance of benthic macrofauna communities for ecosystem functioning. Estuaries and Coasts 40, 457–468.
Coastal hypoxia and the importance of benthic macrofauna communities for ecosystem functioning.Crossref | GoogleScholarGoogle Scholar |

Gammal, J, Hewitt, J, Norkko, J, Norkko, A, and Thrush, S (2020). Does the use of biological traits predict a smooth landscape of ecosystem functioning? Ecology and Evolution 10, 10395–10407.
Does the use of biological traits predict a smooth landscape of ecosystem functioning?Crossref | GoogleScholarGoogle Scholar | 33072268PubMed |

Ghedini, G, Russell, BD, and Connell, SD (2015). Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecology Letters 18, 182–187.
Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances.Crossref | GoogleScholarGoogle Scholar | 25581377PubMed |

Glasby G, Fauchald K (2003) ‘POLiKEY: polychaete identification and information retrieval system, ver. 2.’ (Department of the Environment and Energy: Canberra, ACT, Australia) Available at https://www.environment.gov.au/science/abrs/online-resources/polikey [Verified 31 October 2018]

Griffin, JN, Méndez, V, Johnson, AF, Jenkins, SR, and Foggo, A (2009). Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118, 37–44.
Functional diversity predicts overyielding effect of species combination on primary productivity.Crossref | GoogleScholarGoogle Scholar |

Grinham, AR, Carruthers, TJB, Fisher, PL, Udy, JW, and Dennison, WC (2007). Accurately measuring the abundance of benthic microalgae in spatially variable habitats. Limnology and Oceanography: Methods 5, 119–125.
Accurately measuring the abundance of benthic microalgae in spatially variable habitats.Crossref | GoogleScholarGoogle Scholar |

Hall, SJ, Raffaelli, D, and Turrell, WR (1990). Predator-caging experiments in marine systems: a reexamination of their value. The American Naturalist 136, 657–672.
Predator-caging experiments in marine systems: a reexamination of their value.Crossref | GoogleScholarGoogle Scholar |

Harrison GW (2004). Field experiments and control. In ‘Field Experiments in Economics’. (Eds J Carpenter, GW Harrison, JA List) p. 47. (JAI Press: Greenwich, UK)

Hawkins, SJ, Pack, KE, Hyder, K, Benedetti-Cecchi, L, and Jenkins, SR (2020). Rocky shores as tractable test systems for experimental ecology. Journal of the Marine Biological Association of the United Kingdom 100, 1017–1041.
Rocky shores as tractable test systems for experimental ecology.Crossref | GoogleScholarGoogle Scholar |

Heiri, O, Lotter, AF, and Lemcke, G (2001). Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. Journal of Paleolimnology 25, 101–110.
Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results.Crossref | GoogleScholarGoogle Scholar |

Herbert, RA (1999). Nitrogen cycling in coastal marine ecosystems. FEMS Microbiology Reviews 23, 563–590.
Nitrogen cycling in coastal marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 10525167PubMed |

Himes-Cornell, A, Grose, SO, and Pendleton, L (2018). Mangrove ecosystem service values and methodological approaches to valuation: where do we stand? Frontiers in Marine Science 5, 376.
Mangrove ecosystem service values and methodological approaches to valuation: where do we stand?Crossref | GoogleScholarGoogle Scholar |

Holling, CS (1973). Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4, 1–23.
Resilience and stability of ecological systems.Crossref | GoogleScholarGoogle Scholar |

Hooper, DU, Chapin, FS, Ewel, JJ, et al. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.
Effects of biodiversity on ecosystem functioning: a consensus of current knowledge.Crossref | GoogleScholarGoogle Scholar |

Hulberg, LW, and Oliver, JS (1980). Caging manipulations in marine soft-bottom communities: importance of animal interactions or sedimentary habitat modifications. Canadian Journal of Fisheries and Aquatic Sciences 37, 1130–1139.
Caging manipulations in marine soft-bottom communities: importance of animal interactions or sedimentary habitat modifications.Crossref | GoogleScholarGoogle Scholar |

Huot, Y, Babin, M, Bruyant, F, Grob, C, Twardowski, MS, and Claustre, H (2007). Does chlorophyll a provide the best index of phytoplankton biomass for primary productivity studies? 4, 707–745.
Does chlorophyll a provide the best index of phytoplankton biomass for primary productivity studies?Crossref | GoogleScholarGoogle Scholar |

Hurlbert, SH (1984). Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.
Pseudoreplication and the design of ecological field experiments.Crossref | GoogleScholarGoogle Scholar |

IPCC (2014) ‘Climate change 2014: Impacts, Adaptation and Aulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press)

Jenkins, SR, and Uyà, M (2016). Temporal scale of field experiments in benthic ecology. Marine Ecology Progress Series 547, 273–286.
Temporal scale of field experiments in benthic ecology.Crossref | GoogleScholarGoogle Scholar |

Kanaya, G, Takagi, S, and Kikuchi, E (2008). Dietary contribution of the microphytobenthos to infaunal deposit feeders in an estuarine mudflat in Japan. Marine Biology 155, 543–553.
Dietary contribution of the microphytobenthos to infaunal deposit feeders in an estuarine mudflat in Japan.Crossref | GoogleScholarGoogle Scholar |

Karlson, K, Bonsdorff, E, and Rosenberg, R (2007). The impact of benthic macrofauna for nutrient fluxes from Baltic Sea sediments. AMBIO: A Journal of the Human Environment 36, 161–167.
The impact of benthic macrofauna for nutrient fluxes from Baltic Sea sediments.Crossref | GoogleScholarGoogle Scholar |

Karlson, AML, Niemand, C, Savage, C, and Pilditch, CA (2016). Density of key-species determines efficiency of macroalgae detritus uptake by intertidal benthic communities. PLoS One 11, e0158785.
Density of key-species determines efficiency of macroalgae detritus uptake by intertidal benthic communities.Crossref | GoogleScholarGoogle Scholar |

Kristensen, E, Penha-Lopes, G, Delefosse, M, Valdemarsen, T, Quintana, CO, and Banta, GT (2012). What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series 446, 285–302.
What is bioturbation? The need for a precise definition for fauna in aquatic sciences.Crossref | GoogleScholarGoogle Scholar |

Landi, P, Minoarivelo, HO, Brännström, Å, Hui, C, and Dieckmann, U (2018). Complexity and stability of ecological networks: a review of the theory. Population Ecology 60, 319–345.
Complexity and stability of ecological networks: a review of the theory.Crossref | GoogleScholarGoogle Scholar |

Ling, SD, Scheibling, RE, Rassweiler, A, et al. (2015). Global regime shift dynamics of catastrophic sea urchin overgrazing. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 370, 20130269.
Global regime shift dynamics of catastrophic sea urchin overgrazing.Crossref | GoogleScholarGoogle Scholar |

Lomovasky, BJ, Casariego, AM, Brey, T, and Iribarne, O (2006). The effect of the SW Atlantic burrowing crab Chasmagnathus granulatus on the intertidal razor clam Tagelus plebeius. Journal of Experimental Marine Biology and Ecology 337, 19–29.
The effect of the SW Atlantic burrowing crab Chasmagnathus granulatus on the intertidal razor clam Tagelus plebeius.Crossref | GoogleScholarGoogle Scholar |

Macdonald TA, Burd BJ, Macdonald VI, Van Roodselaar A (2010) ‘Taxonomic and feeding guild classification for the marine benthic macroinvertebrates of the Strait of Georgia, British Columbia.’ (Ocean Sciences Division, Fisheries and Ocean Canada: Sidney, BC, Canada)

MacIntyre, HL, Geider, RJ, and Miller, DC (1996). Microphytobenthos: the ecological role of the 'secret garden' of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19, 186–201.
Microphytobenthos: the ecological role of the 'secret garden' of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production.Crossref | GoogleScholarGoogle Scholar |

MarLIN (2006) ‘BIOTIC - Biological Trait Information Catalogue.’ (Marine Biological Association of the United Kingdom: Plymouth, UK) Available at http://www.marlin.ac.uk/biotic/ [Verified 1 December 2018]

McPhee D (2017) ‘Environmental History and Ecology of Moreton Bay.’ (CSIRO Publishing: Melbourne, Vic., Australia)

MEA (2005) ‘Ecosystems and human well-being: Synthesis, Millennium Ecosystem Assessment.’ (United Nations: New York, NY, USA)

Melville, AJ, and Connolly, RM (2005). Food webs supporting fish over subtropical mudflats are based on transported organic matter not in situ microalgae. Marine Biology 148, 363–371.
Food webs supporting fish over subtropical mudflats are based on transported organic matter not in situ microalgae.Crossref | GoogleScholarGoogle Scholar |

Menge, BA (1976). Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecological Monographs 46, 355–393.
Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity.Crossref | GoogleScholarGoogle Scholar |

Meyer, J, and Kröncke, I (2019). Shifts in trait-based and taxonomic macrofauna community structure along a 27-year time-series in the south-eastern North Sea. PLoS One 14, e0226410.
Shifts in trait-based and taxonomic macrofauna community structure along a 27-year time-series in the south-eastern North Sea.Crossref | GoogleScholarGoogle Scholar | 31851700PubMed |

Middelburg, JJ, Klaver, G, Nieuwenhuize, J, and Vlug, T (1995). Carbon and nitrogen cycling in intertidal sediments near Doel, Scheldt Estuary. Hydrobiologia 311, 57–69.
Carbon and nitrogen cycling in intertidal sediments near Doel, Scheldt Estuary.Crossref | GoogleScholarGoogle Scholar |

Morais, GC, Gusmao, JB, Oliveira, VM, and Lana, P (2019). Macrobenthic functional trait diversity at multiple scales along a subtropical estuarine gradient. Marine Ecology Progress Series 624, 23–37.
Macrobenthic functional trait diversity at multiple scales along a subtropical estuarine gradient.Crossref | GoogleScholarGoogle Scholar |

Morelli, G, and Gasparon, M (2014). Metal contamination of estuarine intertidal sediments of Moreton Bay, Australia. Marine Pollution Bulletin 89, 435–443.
Metal contamination of estuarine intertidal sediments of Moreton Bay, Australia.Crossref | GoogleScholarGoogle Scholar | 25457811PubMed |

Naeem, S, Chapin, FS, Costanza, R, Ehrlich, PR, Golley, FB, Hooper, DU, Lawton, JH, O’Neill, RV, Mooney, HA, Sala, OE, Symstad, AJ, and Tilman, D (1999). Biodiversity and ecosystem functioning: maintaining natural life support processes. Issues in Ecology 4, 2–12.

Newton, A, Icely, J, Cristina, S, et al. (2020). Anthropogenic, direct pressures on coastal wetlands. Frontiers in Ecology and Evolution 8, 144.
Anthropogenic, direct pressures on coastal wetlands.Crossref | GoogleScholarGoogle Scholar |

Norkko, A, Villnäs, A, Norkko, J, Valanko, S, and Pilditch, C (2013). Size matters: implications of the loss of large individuals for ecosystem function. Scientific Reports 3, 2646.
Size matters: implications of the loss of large individuals for ecosystem function.Crossref | GoogleScholarGoogle Scholar | 24025973PubMed |

Norling, K, Rosenberg, R, Hulth, S, Grémare, A, and Bonsdorff, E (2007). Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment. Marine Ecology Progress Series 332, 11–23.
Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment.Crossref | GoogleScholarGoogle Scholar |

O’Connor, NE, and Crowe, TP (2005). Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species. Ecology 86, 1783–1796.
Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species.Crossref | GoogleScholarGoogle Scholar |

Oliver, TH, Heard, MS, Isaac, NJB, Roy, DB, Procter, D, Eigenbrod, F, Freckleton, R, Hector, A, Orme, CDL, Petchey, OL, Proença, V, Raffaelli, D, Suttle, KB, Mace, GM, Martín-López, B, Woodcock, BA, and Bullock, JM (2015). Biodiversity and resilience of ecosystem functions. Trends in Ecology & Evolution 30, 673–684.
Biodiversity and resilience of ecosystem functions.Crossref | GoogleScholarGoogle Scholar |

O’Malley, BL, and Hunt, HL (2020). Role of predators in the recruitment of invertebrates in a rocky subtidal community in the southwest Bay of Fundy, NB. Marine Biology Research 16, 148–165.
Role of predators in the recruitment of invertebrates in a rocky subtidal community in the southwest Bay of Fundy, NB.Crossref | GoogleScholarGoogle Scholar |

Otani, S, Kozuki, Y, Yamanaka, R, Sasaoka, H, Ishiyama, T, Okitsu, Y, Sakai, H, and Fujiki, Y (2010). The role of crabs (Macrophthalmus japonicus) burrows on organic carbon cycle in estuarine tidal flat, Japan. Estuarine, Coastal and Shelf Science 86, 434–440.
The role of crabs (Macrophthalmus japonicus) burrows on organic carbon cycle in estuarine tidal flat, Japan.Crossref | GoogleScholarGoogle Scholar |

Paine, RT (1966). Food web complexity and species diversity. The American Naturalist 100, 65–75.
Food web complexity and species diversity.Crossref | GoogleScholarGoogle Scholar |

Passarelli C, Hubas C, Paterson DM (2018) Mudflat Ecosystem Engineers and Services. In ‘Mudflat Ecology’. (Eds PG Beninger) pp. 243–269. (Springer Nature Switzerland AG)

Percival JB, Lindsay PJ (1997) Measurements of physical properties of sediments. In ‘Physico-Chemical Analysis of Aquatic Sediments’. (Eds A Mudroch, JM Azcue, P Mudroch) pp. 7–38. (Lewis: Boca Raton, FL, USA)

Peterson, CH, and Black, R (1994). An experimentalist’s challenge: when artifacts of intervention interact with treatments. Marine Ecology Progress Series 111, 289–297.
An experimentalist’s challenge: when artifacts of intervention interact with treatments.Crossref | GoogleScholarGoogle Scholar |

Poore GCB (2004) ‘Marine decapod Crustacea of southern Australia: a guide to identification.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Queen JP, Quinn GP, Keough MJ (2002) ‘Experimental design and data analysis for biologists.’ (Cambridge University Press: Cambridge, UK)

Queirós, AM, Birchenough, SNR, Bremner, J, Godbold, JA, Parker, RE, Romero‐Ramirez, A, Reiss, H, Solan, M, Somerfield, PJ, and Colen, C (2013). A bioturbation classification of European marine infaunal invertebrates. Ecology and Evolution 3, 3958–3985.
A bioturbation classification of European marine infaunal invertebrates.Crossref | GoogleScholarGoogle Scholar | 24198953PubMed |

Raffaelli D, Moller H (1999) Manipulative field experiments in animal ecology: do they promise more than they can deliver? In ‘Advances in Ecological Research’. (Eds AH Fitter, DG Raffaelli) pp. 299–338. (Elsevier).
| Crossref |

Ratnasingham, S, and Hebert, PDN (2007). BOLD: the Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.
BOLD: the Barcode of Life Data System (http://www.barcodinglife.org).Crossref | GoogleScholarGoogle Scholar | 18784790PubMed |

Ritchie, RJ (2008). Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46, 115–126.
Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents.Crossref | GoogleScholarGoogle Scholar |

Snelgrove, PVR (1997). The importance of marine sediment biodiversity in ecosystem processes. Ambio 26, 578–583.

Snelgrove, PVR, Thrush, SF, Wall, DH, and Norkko, A (2014). Real world biodiversity–ecosystem functioning: a seafloor perspective. Trends in Ecology & Evolution 29, 398–405.
Real world biodiversity–ecosystem functioning: a seafloor perspective.Crossref | GoogleScholarGoogle Scholar |

Srivastava, DS, and Vellend, M (2005). Biodiversity–ecosystem function research: is it relevant to conservation? Annual Review of Ecology, Evolution, and Systematics 36, 267–294.
Biodiversity–ecosystem function research: is it relevant to conservation?Crossref | GoogleScholarGoogle Scholar |

Tanaka, Y, Horikoshi, A, Aoki, S, and Okamoto, K (2013). Experimental exclusion of the burrowing crab Macrophthalmus japonicus from an intertidal mud flat: effects on macro-infauna abundance. Plankton & Benthos. Research 8, 88–95.
Experimental exclusion of the burrowing crab Macrophthalmus japonicus from an intertidal mud flat: effects on macro-infauna abundance. Plankton & Benthos.Crossref | GoogleScholarGoogle Scholar |

Thomsen, MS, Godbold, JA, Garcia, C, Bolam, SG, Parker, R, and Solan, M (2019). Compensatory responses can alter the form of the biodiversity–function relation curve. Proceedings of the Royal Society of London – B. Biological Sciences 286, 20190287.
Compensatory responses can alter the form of the biodiversity–function relation curve.Crossref | GoogleScholarGoogle Scholar |

Thrush, SF, Cummings, VJ, Dayton, PK, Ford, R, Grant, J, Hewitt, JE, Hines, AH, Lawrie, SM, Pridmore, RD, and Legendre, P (1997). Matching the outcome of small-scale density manipulation experiments with larger scale patterns: an example of bivalve adult/juvenile interactions. Journal of Experimental Marine Biology and Ecology 216, 153–169.
Matching the outcome of small-scale density manipulation experiments with larger scale patterns: an example of bivalve adult/juvenile interactions.Crossref | GoogleScholarGoogle Scholar |

Thrush, SF, Hewitt, JE, Gibbs, M, Lundquist, C, and Norkko, A (2006). Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9, 1029–1040.
Functional role of large organisms in intertidal communities: community effects and ecosystem function.Crossref | GoogleScholarGoogle Scholar |

Thrush, SF, Hewitt, JE, Kraan, C, Lohrer, AM, Pilditch, CA, and Douglas, E (2017). Changes in the location of biodiversity–ecosystem function hot spots across the seafloor landscape with increasing sediment nutrient loading. Proceedings of the Royal Society of London – B. Biological Sciences 284, 20162861.
Changes in the location of biodiversity–ecosystem function hot spots across the seafloor landscape with increasing sediment nutrient loading.Crossref | GoogleScholarGoogle Scholar |

Tyler, EHM, Somerfield, PJ, Berghe, EV, Bremner, J, Jackson, E, Langmead, O, Palomares, MLD, and Webb, TJ (2012). Extensive gaps and biases in our knowledge of a well‐known fauna: implications for integrating biological traits into macroecology. Global Ecology and Biogeography 21, 922–934.
Extensive gaps and biases in our knowledge of a well‐known fauna: implications for integrating biological traits into macroecology.Crossref | GoogleScholarGoogle Scholar |

Underwood, AJ (1981). Techniques of analysis of variance in experimental marine biology and ecology. Annual Reviews of Oceanography and Marine Biology 19, 513–605.

Underwood, AJ (1990). Experiments in ecology and management: their logics, functions and interpretations. Australian Journal of Ecology 15, 365–389.
Experiments in ecology and management: their logics, functions and interpretations.Crossref | GoogleScholarGoogle Scholar |

Underwood, AJ (2000). Experimental ecology of rocky intertidal habitats: what are we learning? Journal of Experimental Marine Biology and Ecology 250, 51–76.
Experimental ecology of rocky intertidal habitats: what are we learning?Crossref | GoogleScholarGoogle Scholar | 10969163PubMed |

Underwood GJ C (2001) Microphytobenthos. In ‘Encyclopedia of Ocean Sciences’. (Ed. JH Steele) pp. 1770–1777. (Elsevier)

Volkenborn, N, and Reise, K (2007). Effects of Arenicola marina on polychaete functional diversity revealed by large-scale experimental lugworm exclusion. Journal of Sea Research 57, 78–88.
Effects of Arenicola marina on polychaete functional diversity revealed by large-scale experimental lugworm exclusion.Crossref | GoogleScholarGoogle Scholar |

Volkenborn, N, Hedtkamp, SIC, van Beusekom, JEE, and Reise, K (2007). Effects of bioturbation and bioirrigation by lugworms (Arenicola marina) on physical and chemical sediment properties and implications for intertidal habitat succession. Estuarine, Coastal and Shelf Science 74, 331–343.
Effects of bioturbation and bioirrigation by lugworms (Arenicola marina) on physical and chemical sediment properties and implications for intertidal habitat succession.Crossref | GoogleScholarGoogle Scholar |

Van Colen C (2018). The Upper Living Levels: Invertebrate Macrofauna. In ‘Mudflat Ecology’. (Eds PG Beninger) pp. 149–168. (Springer Nature)

Waldbusser, GG, Marinelli, RL, Whitlatch, RB, and Visscher, PT (2004). The effects of infaunal biodiversity on biogeochemistry of coastal marine sediments. Limnology and Oceanography 49, 1482–1492.
The effects of infaunal biodiversity on biogeochemistry of coastal marine sediments.Crossref | GoogleScholarGoogle Scholar |

Wantzen KM, Yule CM, Mathooko JM, Pringle CM (2008) Organic matter processing in tropical streams. In ‘Tropical Stream Ecology’. (Ed. D Dudgeon) pp. 43–64. (Elsevier: Oxford, UK).
| Crossref |

Webb, AP, and Eyre, BD (2004). The effect of natural populations of the burrowing and grazing soldier crab (Mictyris longicarpus) on sediment irrigation, benthic metabolism and nitrogen fluxes. Journal of Experimental Marine Biology and Ecology 309, 1–19.
The effect of natural populations of the burrowing and grazing soldier crab (Mictyris longicarpus) on sediment irrigation, benthic metabolism and nitrogen fluxes.Crossref | GoogleScholarGoogle Scholar |

Williams SJ, Dodd K, Gohn KK (1990) ‘Coasts in crisis.’ (US Department of the Interior, US Geological Survey: Denver, CO, USA)

Wilson, WH (1991). Competition and predation in marine soft-sediment communities. Annual Review of Ecology and Systematics 21, 221–241.
Competition and predation in marine soft-sediment communities.Crossref | GoogleScholarGoogle Scholar |

Woodin, SA (1981). Disturbance and community structure in a shallow water sand flat. Ecology 62, 1052–1066.
Disturbance and community structure in a shallow water sand flat.Crossref | GoogleScholarGoogle Scholar |