Abstract
More than half of the fish biomass of coastal rocky reefs depends on zooplankton; however, the trophic basis of estuarine fish assemblages remains unknown. We quantified the trophic basis (i.e. basal energy sources) of fish community biomass inhabiting three habitat types (seagrass, natural reef and artificial reef) in two estuaries, compared with two coastal rocky reef sites. Fish assemblages were surveyed with Baited Remote Underwater Video (BRUVs) and the species abundance, richness and biomass of fish were classified into nine functional feeding groups (6 teleost and 3 elasmobranch). Comparable metrics for coastal fish assemblages were obtained from published surveys using BRUVs. Using the functional feeding group biomass and the group-specific diet composition, the breakdown of energy sources was calculated using a food web analysis. Estuarine reef habitats had different species and different functional feeding group composition than seagrass habitat. The majority of fish biomass in the seagrass habitat was supported by detritus (51% in Botany Bay) or macrophytes (58% in Lake Macquarie). In contrast, zooplankton supported most fish biomass (45–59%) at the coastal reef locations, and in reef habitat in one estuary (35–43%), but not the other estuary (33–34%). Trophic pathways which support fish assemblages, are key in identifying mitigation measures which can help conserve these populations with growing urbanisation of estuaries and coasts.
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Data and materials available at https://github.com/belindagoddard/Trophic-Basis-Fish-Assemblage.
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Code available at https://github.com/belindagoddard/Trophic-Basis-Fish-Assemblage.
References
Abrantes K, Sheaves M (2009) Food web structure in a near-pristine mangrove area of the Australian Wet Tropics. Estuar Coast Shelf Sci 82:597–607. https://doi.org/10.1016/j.ecss.2009.02.021
Abrantes KG, Barnett A, Baker R, Sheaves M (2015) Habitat-specific food webs and trophic interactions supporting coastal-dependent fishery species: an Australian case study. Rev Fish Biol Fish 25:337–363. https://doi.org/10.1007/s11160-015-9385-y
Ainsworth CH, Kaplan IC, Levin PS, Mangel M (2010) A statistical approach for estimating fish diet compositions from multiple data sources: Gulf of California case study. Ecol Appl 20:2188–2202. https://doi.org/10.1890/09-0611.1
Akin S, Winemiller KO (2006) Seasonal variation in food web composition and structure in a temperate tidal estuary. Estuaries Coasts 29:552–567. https://doi.org/10.1007/BF02784282
Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45:301–318. https://doi.org/10.1111/1467-842x.00285
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
Becker A, Laurenson LJB (2007) Seasonal and diel comparisons of the diets of four dominant fish species within the main channel and flood-zone of a small intermittently open estuary in south-eastern Australia. Mar Freshw Res 58:1086–1095. https://doi.org/10.1071/MF06135
Becker A, Cowley PD, Whitfield AK (2010) Use of remote underwater video to record littoral habitat use by fish within a temporarily closed South African estuary. J Exp Mar Biol Ecol 391:161–168
Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fishes 28:189–214. https://doi.org/10.1007/BF00751035
Bennett S, Wernberg T, Connell SD, Hobday AJ, Johnson CR, Poloczanska ES (2015a) The ‘Great Southern Reef’: social, ecological and economic value of Australia’s neglected kelp forests. Mar Freshw Res 67:47–56
Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ (2015b) Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol Lett 18:714–723. https://doi.org/10.1111/ele.12450
Cappo M, Speare P, De’Ath G (2004) Comparison of baited remote underwater video stations (BRUVS) and prawn (shrimp) trawls for assessments of fish biodiversity in inter-reefal areas of the Great Barrier Reef Marine Park. J Exp Marine Biol Ecol 302:123–152. https://doi.org/10.1016/j.jembe.2003.10.006
Champion C, Suthers IM, Smith JA (2015) Zooplanktivory is a key process for fish production on a coastal artificial reef. Mar Ecol-Prog Ser 541:1–14
Champion C, Hobday A, Zhang X, Pecl G, Tracey S (2018) Changing windows of opportunity: past and future climate-driven shifts in temporal persistence of kingfish (Seriola lalandi) oceanographic habitat within south-eastern Australian bioregions. Mar Freshw Res. https://doi.org/10.1071/MF17387
Champion C, Hobday AJ, Zhang X, Pecl GT, Tracey SR (2019) Changing windows of opportunity: past and future climate-driven shifts in temporal persistence of kingfish (Seriola lalandi) oceanographic habitat within south-eastern Australian bioregions. Mar Freshw Res 70:33–42
Chartrand K, Ralph P, Petrou K, Rasheed M (2012) Development of a light-based seagrass management approach for the Gladstone Western Basin Dredging Program. Fisheries Queensland, Cairns, p 126
Clarke K, Gorley RN (2006) Primer v6: User Manual/Tutorial
Connolly R (2009) Fish on Australian saltmarshes. In: Saintilan N (ed) Australian saltmarsh ecology. Csiro Publishing, Collingwood
Creese RG, Glasby TM, West G, Gallen C (2009) Mapping the habitats of NSW estuaries. Port Stephens, Australia
David V, Sautour B, Chardy P, Leconte M (2005) Long-term changes of the zooplankton variability in a turbid environment: the Gironde estuary (France). Estuar Coast Shelf Sci 64:171–184. https://doi.org/10.1016/j.ecss.2005.01.014
Davis TR, Harasti D, Kelaher B, Smith SD (2016) Diversity surrogates for estuarine fish assemblages in a temperate estuary in New South Wales, Australia. Reg Stud Mar Sci 7:55–62
Dennison WC, Orth RJ, Moore KA, Stevenson JC, Carter V, Kollar S, Bergstrom PW, Batiuk RA (1993) Assessing water-quality with submersed aquatic vegetation. Bioscience 43:86–94. https://doi.org/10.2307/1311969
Dorman SR, Harvey ES, Newman SJ (2012) Bait Effects In Sampling Coral Reef Fish Assemblages With Stereo-BRUVs. PLoS ONE 7:e41538. https://doi.org/10.1371/journal.pone.0041538
Edgar GJ, Cooper A, Baker SC, Barker W, Barrett NS, Becerro MA, Bates AE, Brock D, Ceccarelli DM, Clausius E, Davey M, Davis TR, Day PB, Green A, Griffiths SR, Hicks J, Hinojosa IA, Jones BK, Kininmonth S, Larkin MF, Lazzari N, Lefcheck JS, Ling SD, Mooney P, Oh E, Pérez-Matus A, Pocklington JB, Riera R, Sanabria-Fernandez JA, Seroussi Y, Shaw I, Shields D, Shields J, Smith M, Soler GA, Stuart-Smith J, Turnbull J, Stuart-Smith RD (2020) Reef life survey: establishing the ecological basis for conservation of shallow marine life. Biol Cons 252:108855. https://doi.org/10.1016/j.biocon.2020.108855
Folpp H, Lowry M, Gregson M, Suthers IM (2013) Fish assemblages on Estuarine Artificial Reefs: natural rocky-reef mimics or discrete assemblages? PLoS ONE 8:e63505. https://doi.org/10.1371/journal.pone.0063505
Folpp HR, Schilling HT, Clark GF, Lowry MB, Maslen B, Gregson M, Suthers IM (2020) Artificial reefs increase fish abundance in habitat-limited estuaries. J Appl Ecol 57:1752–1761. https://doi.org/10.1111/1365-2664.13666
Froese RP, D. Editors (2019) FishBase. World Wide Web electronic publication, version (12/2019)
Gillanders BM, Ferrell DJ, Andrew NL (2001a) Estimates of movement and life-history parameters of yellowtail kingfish (Seriola lalandi): how useful are data from a cooperative tagging programme? Mar Freshw Res 52:179–192. https://doi.org/10.1071/MF99153
Gillanders BM, Ferrell DJ, Andrew NL (2001b) Estimates of movement and life-history parameters of yellowtail kingfish (Seriola lalandi): how useful are data from a cooperative tagging programme? Mar Freshw Res 52:179–192
Glasby TM (1999) Differences between subtidal epibiota on pier pilings and rocky reefs at marinas in Sydney, Australia. Estuar Coast Shelf Sci 48:281–290. https://doi.org/10.1006/ecss.1998.0417
Glaspie CN, Seitz RD (2017) Role of habitat and predators in maintaining functional diversity of estuarine bivalves. Mar Ecol-Prog Ser 570:113–125. https://doi.org/10.3354/meps12103
Goetze JS, Bond T, McLean DL, Saunders BJ, Langlois TJ, Lindfield S, Fullwood LAF, Driessen D, Shedrawi G, Harvey ES, McPherson J (2019) A field and video analysis guide for diver operated stereo‐video. Methods Ecol Evol 10(7):1083–1090. https://doi.org/10.1111/2041-210X.13189
Gray CA, Ives MC, Macbeth WG, Kendall BW (2010) Variation in growth, mortality, length and age compositions of harvested populations of the herbivorous fish Girella tricuspidata. J Fish Biol 76:880–899. https://doi.org/10.1111/j.1095-8649.2010.02544.x
Gray CA, Haddy JA, Fearman J, Barnes LM, Macbeth WG, Kendall BW (2012) Reproduction growth and connectivity among populations of Girella tricuspidata (Pisces: Girellidae). Aquat Biol 16(1):53–68. https://doi.org/10.3354/ab00428
Hamner WM, Jones MS, Carleton JH, Hauri IR, Williams DM (1988) Zooplankton, Planktivorous fish, and water currents on a Windward Reef Face: Great Barrier Reef, Australia. Bull Mar Sci 42:459–479
Harasti D, Malcolm H, Gallen C, Coleman MA, Jordan A, Knott NA (2015) Appropriate set times to represent patterns of rocky reef fishes using baited video. J Exp Mar Biol Ecol 463:173–180. https://doi.org/10.1016/j.jembe.2014.12.003
Harasti D, Davis TR, Mitchell E, Lindfield S, Smith SDA (2018) A tale of two islands: decadal changes in rocky reef fish assemblages following implementation of no-take marine protected areas in New South Wales, Australia. Reg Stud Mar Sci 18:229–236. https://doi.org/10.1016/j.rsma.2017.10.011
Harvey ES, Cappo M, Butler JJ, Hall N, Kendrick GA (2007) Bait attraction affects the performance of remote underwater video stations in assessment of demersal fish community structure. Mar Ecol-Prog Ser 350:245–254. https://doi.org/10.3354/meps07192
Hindell JS (2006) Assessing the trophic link between seagrass habitats and piscivorous fishes. Mar Freshw Res 57:121–131. https://doi.org/10.1071/MF05082
Holland MM, Smith JA, Everett JD, Verges A, Suthers IM (2020) Latitudinal patterns in trophic structure of temperate reef-associated fishes and predicted consequences of climate change. Fish Fish. https://doi.org/10.1111/faf.12488
Irigoyen AJ, Galván DE, Venerus LA, Parma AM, Ferse SCA (2013) Variability in abundance of temperate reef fishes estimated by visual census. PLoS ONE 8(4):e61072. https://doi.org/10.1371/journal.pone.0061072
Kennish MJ (2019) Ecology of Estuaries: Volume 2 biological aspects. CRC Press, Boca Raton
Kuiter RH (1993) Coastal fishes of south-eastern Australia / Rudie H. Kuiter. University of Hawaii Press ; Crawford House Press, Honolulu : Bathurst, N.S.W
Langlois T, Goetze J, Bond T, Monk J, Abesamis RA, Asher J, Barrett N, Bernard ATF, Bouchet PJ, Birt MJ, Cappo M, Currey-Randall LM, Driessen D, Fairclough DV, Fullwood LAF, Gibbons BA, Harasti D, Heupel MR, Hicks J, Holmes TH, Huveneers C, Ierodiaconou D, Jordan A, Knott NA, Lindfield S, Malcolm HA, McLean D, Meekan M, Miller D, Mitchell PJ, Newman SJ, Radford B, Rolim FA, Saunders BJ, Stowar M, Smith ANH, Travers MJ, Wakefield CB, Whitmarsh SK, Williams J, Harvey ES (2020) A field and video annotation guide for baited remote underwater stereo-video surveys of demersal fish assemblages. Methods Ecol Evol 11:1401–1409. https://doi.org/10.1111/2041-210X.13470
Libralato S, Christensen V, Pauly D (2006) A method for identifying keystone species in food web models. Ecol Model 195:153–171. https://doi.org/10.1016/j.ecolmodel.2005.11.029
Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639. https://doi.org/10.1146/annurev.ecolsys.39.110707.173549
Malcolm HA, Gladstone W, Lindfield S, Wraith J, Lynch TP (2007) Spatial and temporal variation in reef fish assemblages of marine parks in New South Wales, Australia—baited video observations. Mar Ecol Prog Ser 350:277–290. https://doi.org/10.3354/meps07195
Mayer-Pinto M, Cole VJ, Johnston EL, Bugnot A, Hurst H, Airoldi L, Glasby TM, Dafforn KA (2018) Functional and structural responses to marine urbanisation. Environ Res Lett 13:014009. https://doi.org/10.1088/1748-9326/aa98a5
Melville AJ, Connolly RM (2003) Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136(4):499–507. https://doi.org/10.1007/s00442-003-1302-8
Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Johnson NC, McCann KS, Melville K, Morin PJ (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600
Morais RA, Bellwood DR (2019) Pelagic subsidies underpin fish productivity on a degraded coral reef. Curr Biol 29:1521-1527.e1526. https://doi.org/10.1016/j.cub.2019.03.044
Moreau S, Peron C, Pitt KA, Connolly RM, Lee SY, Meziane T (2008) Opportunistic predation by small fishes on epibiota of jetty pilings in urban waterways. J Fish Biol 72:205–217. https://doi.org/10.1111/j.1095-8649.2007.01705.x
Morton JK, Gladstone W (2011) Spatial temporal and ontogenetic variation in the association of fishes (family Labridae) with rocky-reef habitats. Mar Freshw Res 62(7):870. https://doi.org/10.1071/MF10315
Morton JK, Gladstone W (2014) Changes in rocky reef fish assemblages throughout an estuary with a restricted inlet. Hydrobiologia 724:235–253. https://doi.org/10.1007/s10750-013-1740-1
Motta PJ (1988) Functional morphology of the feeding apparatus of ten species of Pacific butterflyfishes (Perciformes, Chaetodontidae): an ecomorphological approach. Environ Biol Fishes 22:39–67. https://doi.org/10.1007/BF00000543
Nagelkerken I, Faunce CH (2008) What makes mangroves attractive to fish? Use of artificial units to test the influence of water depth, cross-shelf location, and presence of root structure. Estuar Coast Shelf Sci 79:559–565. https://doi.org/10.1016/j.ecss.2008.04.011
Oczkowski A, Hunt CW, Miller K, Oviatt C, Nixon S, Smith L (2016) Comparing measures of estuarine ecosystem production in a temperate New England Estuary. Estuaries Coasts 39:1827–1844. https://doi.org/10.1007/s12237-016-0113-1
Parrish CC, Deibel D, Thompson RJ (2009) Effect of sinking spring phytoplankton blooms on lipid content and composition in suprabenthic and benthic invertebrates in a cold ocean coastal environment. Mar Ecol-Prog Ser 391:33–51. https://doi.org/10.3354/meps08148
Paterson AW, Whitfield AK (1997) A stable carbon isotope study of the food-web in a freshwater-deprived South African Estuary with particular emphasis on the Ichthyofauna. Estuar Coast Shelf Sci 45(6):705–715. https://doi.org/10.1006/ecss.1997.0243
Pease BC (1999) A spatially oriented analysis of estuaries and their associated commercial fisheries in New South Wales, Australia. Fish Res 42:67–86. https://doi.org/10.1016/S0165-7836(99)00035-1
Qin H, Sheng Q, Chu T, Wang S, Wu J (2015) Import and export fluxes of macrozooplankton are taxa- and season-dependent at Jiuduansha marsh, Yangtze River estuary. Estuar Coast Shelf Sci 163:254–264. https://doi.org/10.1016/j.ecss.2014.11.024
R Core Team (2020) R: A language and environment for statistical computing
Roy PS, Williams RJ, Jones AR, Yassini I, Gibbs PJ, Coates B, West RJ, Scanes PR, Hudson JP, Nichol S (2001) Structure and function of south-east Australian estuaries. Estuar Coast Shelf Sci 53:351–384. https://doi.org/10.1006/ecss.2001.0796
Smith JA, Lowry MB, Champion C, Suthers IM (2016) A designed artificial reef is among the most productive marine fish habitats: new metrics to address “production versus attraction.” Mar Biol 163:8. https://doi.org/10.1007/s00227-016-2967-y
Truong L, Suthers IM, Cruz DO, Smith JA (2017) Plankton supports the majority of fish biomass on temperate rocky reefs. Mar Biol 164:73. https://doi.org/10.1007/s00227-017-3101-5
Wassmann P (1998) Retention versus export food chains: processes controlling sinking loss from marine pelagic systems. Hydrobiologia 363:29–57
Watson DL, Harvey ES, Anderson MJ, Kendrick GA (2005) A comparison of temperate reef fish assemblages recorded by three underwater stereo-video techniques. Mar Biol 148:415–425. https://doi.org/10.1007/s00227-005-0090-6
York PH, Booth DJ, Glasby TM, Pease BC (2006) Fish assemblages in habitats dominated by Caulerpa taxifolia and native seagrasses in south-eastern Australia. Mar Ecol-Prog Ser 312:223–234. https://doi.org/10.3354/meps312223
Young JW, Lansdell MJ, Campbell RA, Cooper SP, Juanes F, Guest MA (2010) Feeding ecology and niche segregation in oceanic top predators off eastern Australia. Mar Biol 157:2347–2368. https://doi.org/10.1007/s00227-010-1500-y
Zuercher R, Galloway AWE (2019) Coastal marine ecosystem connectivity: pelagic ocean to kelp forest subsidies. Ecosphere. https://doi.org/10.1002/ecs2.2602
Acknowledgements
We acknowledge the support of Centre for Marine Science and Innovation and the School of BEES at the University of New South Wales, and the NSW Department of Primary Industries. The authors recognise the data shared by the Reef Life Survey (reeflifesurvey.com).
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Alistair Becker was funded by the NSW Recreational Saltwater Fishing Trust for the Lake Macquarie and Botany Bay field work.
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The analysis and initial draft was completed by BKG. IMS and AB conceived the study. JAS updated and improved the numerical scripts. RCS provided the food web script. All authors contributed to the analysis and writing of the paper.
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Goddard, B.K., Becker, A., Harasti, D. et al. The trophic basis of fish assemblages in temperate estuarine and coastal ecosystems. Mar Biol 169, 19 (2022). https://doi.org/10.1007/s00227-021-04001-y
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DOI: https://doi.org/10.1007/s00227-021-04001-y