Marine Ecology Progress Series
MEPS is a leading hybrid research journal on all aspects of marine, coastal and estuarine ecology. Priority is given to outstanding research that advances our ecological understanding.
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DOI: https://doi.org/10.3354/meps14940
copiedTurf proliferation depends on kelp loss and maintenance by sea urchin grazing
ABSTRACT:
Temperate reef ecosystems are increasingly challenged by acute marine heatwaves and chronic overfishing which can lead to trophic cascades. While these disturbances differ in their impact and temporal expression, both can manifest as a collapse of kelp followed by proliferation of filamentous algal turfs. However, the importance of these disturbance types in turf proliferation remains unclear. Here, we investigate whether turf proliferation on Tasmanian reefs is driven primarily by acute kelp loss or chronic urchin grazing. Using standardised settlement tiles, we quantified short-term (2.5 mo) turf proliferation across 4 treatments: (1) intact kelp beds, (2) intact urchin barrens, (3) kelp beds with kelp removed, and (4) urchin barrens with urchins removed. Additionally, we tracked the longer-term (~12 mo) fate of these experimental patches to assess either kelp recovery or turf persistence. Turf proliferated in all treatments where kelp was absent or removed, with approximately 50-fold higher turf cover in disturbed kelp beds. This suggests that acute kelp loss is the predominant mechanism that allows turf proliferation in this system. However, the capacity of turf to persist was dependent on chronic urchin grazing. After 12 mo, our results revealed that at a site with lower urchin densities, kelp recovered within the patches with an associated decline in turf cover. At a site with higher urchin densities, kelp failed to recover, and turf continued to proliferate. Overall, when kelps are lost, competitive release allow turfs to establish, but their persistence appears dependent on chronically elevated levels of herbivory preventing kelp re-establishment.
KEYWORDS
Agostini S, Harvey BP, Milazzo M, Wada S and others (2021) Simplification, not ‘tropicalization’, of temperate marine ecosystems under ocean warming and acidification. Glob Change Biol 27:4771-4784 PubMed Crossref
Airoldi L (2000) Responses of algae with different life histories to temporal and spatial variability of disturbance in subtidal reefs. Mar Ecol Prog Ser 195:81-92 Crossref
Bartoń K (2020) MuMIn: multi-model inference. R package version 1.43.17. Link
Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827-833 PubMed Crossref
Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ (2015) Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol Lett 18:714-723 PubMed Crossref
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A and others (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378-400 Crossref
Bulleri F (2013) Grazing by sea urchins at the margins of barren patches on Mediterranean rocky reefs. Mar Biol 160:2493-2501 Crossref
Carpenter RC (1984) Predator and population density control of homing behavior in the Caribbean echinoid Diadema antillarum. Mar Biol 82:101-108 Crossref
Carranza DM, Stotz GC, Vásquez JA, Stotz WB (2024) Trends in the effects of kelp removal on kelp populations, herbivores, and understory algae. Glob Ecol Conserv 49:e02805 Crossref
Connell SD (2003) Negative effects overpower the positive of kelp to exclude invertebrates from the understorey community. Oecologia 137:97-103 PubMed Crossref
Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B 277:1409-1415 PubMed Crossref
Connell SD, Russell BD, Turner DJ, Shepherd SA and others (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol Prog Ser 360:63-72 Crossref
Connell SD, Russell BD, Irving AD (2011) Can strong consumer and producer effects be reconciled to better forecast ‘catastrophic’ phase-shifts in marine ecosystems? J Exp Mar Biol Ecol 400:296-301 Crossref
Connell SD, Foster MS, Airoldi L (2014) What are algal turfs? Towards a better description of turfs. Mar Ecol Prog Ser 495:299-307 Crossref
Crain CM, Halpern BS, Beck MW, Kappel CV (2009) Understanding and managing human threats to the coastal marine environment. Ann N Y Acad Sci 1162:39-62 PubMed Crossref
Cresswell K, Little L, Hartmann K, Gardner C, Keane J, Ling SD, Bradshaw S (2025) When overfishing is the sustainable option. Nat Sustain 8:498-507 Crossref
Filbee-Dexter K, Scheibling RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1-25 Crossref
Filbee-Dexter K, Wernberg T (2018) Rise of turfs: a new battlefront for globally declining kelp forests. Bioscience 68:64-76 Crossref
Fraser KM, Stuart-Smith RD, Ling SD, Heather FJ, Edgar GJ (2020) Taxonomic composition of mobile epifaunal invertebrate assemblages on diverse benthic microhabitats from temperate to tropical reefs. Mar Ecol Prog Ser 640:31-43 Crossref
Gorgula SK, Connell SD (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613-619 Crossref
Gorman D, Connell SD (2009) Recovering subtidal forests in human-dominated landscapes. J Appl Ecol 46:1258-1265 Crossref
Halpern BS, Selkoe KA, Micheli F, Kappel CV (2007) Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conserv Biol 21:1301-1315 PubMed Crossref
Hartig F (2021) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6. Link
Hobday AJ, Alexander LV, Perkins SE, Smale DA and others (2016) A hierarchical approach to defining marine heatwaves. Prog Oceanogr 141:227-238 Crossref
Irving AD, Connell SD (2006) Physical disturbance by kelp abrades erect algae from the understorey. Mar Ecol Prog Ser 324:127-137 Crossref
Irving AD, Connell SD (2006) Predicting understory structure from the presence and composition of canopies: an assembly rule for marine algae. Oecologia 148:491-502 PubMed Crossref
Irving AD, Witman JD (2009) Positive effects of damselfish override negative effects of urchins to prevent an algal habitat switch. J Ecol 97:337-347 Crossref
Johnson CR, Banks SC, Barrett NS, Cazassus F and others (2011) Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Biol Ecol 400:17-32 Crossref
Keane JP, Cresswell K, McAllister J, Rainer S, Smith J, Johnson OJ, Ling S (2024) Subsidizing the overharvest of an overgrazing, range-extending sea urchin for kelp restoration and abalone habitat protection. In: Azzurro E, Bahri T, Valbo-Jørgensen J, Ma X, Strafella P, Vasconcellos M (eds) Fisheries responses to invasive species in a changing climate - lessons learned from case studies. FAO Fisheries Technical Paper No. 704. FAO, Rome, p 147-158 Link
Korzen L, Israel A, Abelson A (2011) Grazing effects of fish versus sea urchins on turf algae and coral recruits: possible implications for coral reef resilience and Restoration. J Mar Sci 2011:960207 Crossref
Krumhansl KA, Okamoto DK, Rassweiler A, Novak M and others (2016) Global patterns of kelp forest change over the past half-century. Proc Natl Acad Sci USA 113:13785-13790 PubMed Crossref
Layton C, Coleman MA, Marzinelli EM, Steinberg PD and others (2020) Kelp forest restoration in Australia. Front Mar Sci 7:74 Crossref
Lenth RV (2021) emmeans: estimated marginal means, aka least-squares means. R package version 1.6.2-1. Link
Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883-894 PubMed Crossref
Ling SD, Johnson CR (2009) Population dynamics of an ecologically important range-extender: kelp beds versus sea urchin barrens. Mar Ecol Prog Ser 374:113-125 Crossref
Ling SD, Johnson CR (2012) Marine reserves reduce risk of climate-driven phase shift by reinstating size- and habitat-specific trophic interactions. Ecol Appl 22:1232-1245 PubMed Crossref
Ling SD, Keane JP (2024) Climate-driven invasion and incipient warnings of kelp ecosystem collapse. Nat Commun 15:400 PubMed Crossref
Ling SD, Johnson CR, Frusher SD, Ridgway KR (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Natl Acad Sci USA 106:22341-22345 PubMed Crossref
Ling SD, Scheibling RE, Rassweiler A, Johnson CR and others (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc B 370:20130269 Crossref
Ling SD, Barrett NS, Edgar GJ (2018) Facilitation of Australia’s southernmost reef-building coral by sea urchin herbivory. Coral Reefs 37:1053-1073 Crossref
Miller KI, Balemi CA, Bell DR, Blain CO and others (2024) Large-scale one-off sea urchin removal promotes rapid kelp recovery in urchin barrens. Restor Ecol 32:e14060 Crossref
Mourin M, Barroso I, Pessarrodona A, Navarro-Mayoral S, Tuya F, Bosch NE (2025) Local human pressures modulate turf sediment loads in a warm-temperate oceanic island. Mar Environ Res 205:107030 PubMed Crossref
Oliver ECJ, Lago V, Hobday AJ, Holbrook NJ, Ling SD, Mundy CN (2018) Marine heatwaves off eastern Tasmania: trends, interannual variability, and predictability. Prog Oceanogr 161:116-130 Crossref
Pedersen T (2024) patchwork: the composer of plots. R package version 1.3.0.9000. Link
Pessarrodona A, Foggo A, Smale DA (2019) Can ecosystem functioning be maintained despite climate-driven shifts in species composition? Insights from novel marine forests. J Ecol 107:91-104 Crossref
Pessarrodona A, Filbee-Dexter K, Alcoverro T, Boada J and others (2021) Homogenization and miniaturization of habitat structure in temperate marine forests. Glob Change Biol 27:5262-5275 PubMed Crossref
Pessarrodona A, Filbee-Dexter K, Wernberg T (2023) Recovery of algal turfs following removal. Mar Environ Res 192:106185 PubMed Crossref
R Core Team (2024) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reed DC, Foster MS (1984) The effects of canopy shadings on algal recruitment and growth in a giant kelp forest. Ecology 65:937-948 Crossref
Reeves SE, Kriegisch N, Johnson CR, Ling SD (2018) Reduced resistance to sediment-trapping turfs with decline of native kelp and establishment of an exotic kelp. Oecologia 188:1239-1251 PubMed Crossref
Reeves SE, Kriegisch N, Johnson CR, Ling SD (2022) Kelp habitat fragmentation reduces resistance to overgrazing, invasion and collapse to turf dominance. J Appl Ecol 59:1619-1631 Crossref
Sanderson JC, Ling SD, Dominguez JG, Johnson CR (2015) Limited effectiveness of divers to mitigate ‘barrens’ formation by culling sea urchins while fishing for abalone. Mar Freshw Res 67:84-95 Crossref
Shears NT, Babcock RC (2002) Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia 132:131-142 PubMed Crossref
Smale DA, Wernberg T, Oliver ECJ, Thomsen M and others (2019) Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat Clim Change 9:306-312 Crossref
Strain EMA, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob Change Biol 20:3300-3312 PubMed Crossref
Teagle H, Hawkins SJ, Moore PJ, Smale DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J Exp Mar Biol Ecol 492:81-98 Crossref
Toohey BD, Kendrick GA, Harvey ES (2007) Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos 116:1618-1630 Crossref
Vergés A, Steinberg PD, Hay ME, Poore AGB and others (2014) The tropicalization of temperate marine ecosystems: Climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846 PubMed Crossref
Vergés A, Doropoulos C, Malcolm HA, Skye M and others (2016) Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc Natl Acad Sci USA 113:13791-13796 PubMed Crossref
Vergés A, McCosker E, Mayer-Pinto M, Coleman MA, Wernberg T, Ainsworth T, Steinberg PD (2019) Tropicalisation of temperate reefs: implications for ecosystem functions and management actions. Funct Ecol 33:1000-1013 Crossref
Wernberg T, Smale DA, Tuya F, Thomsen MS and others (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78-82 Crossref
Wernberg T, Bennett S, Babcock RC, de Bettignies T and others (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169-172 PubMed Crossref
Wickham H, Averick M, Bryan J, Chang W and others (2019) Welcome to the tidyverse. J Open Source Softw 4:1686 Crossref
Zarco-Perello S, Wernberg T, Langlois TJ, Vanderklift MA (2017) Tropicalization strengthens consumer pressure on habitat-forming seaweeds. Sci Rep 7:820 PubMed Crossref
Zarco-Perello S, Bosch NE, Bennett S, Vanderklift MA, Wernberg T (2021) Persistence of tropical herbivores in temperate reefs constrains kelp resilience to cryptic habitats. J Ecol 109:2081-2094 Crossref
Paula Ruiz-Ruiz (Corresponding Author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
Matthew Rose (Co-author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
Sterling Tebbett (Co-author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
Elisabeth Strain (Co-author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
- Centre for Marine Socioecology, University of Tasmania, Hobart, Tasmania 7001, Australia
Scott Bennett (Co-author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
- Centre for Marine Socioecology, University of Tasmania, Hobart, Tasmania 7001, Australia
Scott Ling (Co-author)
- Institute for Marine & Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tasmania 7001, Australia
Handling Editor:
Jean-Sebastien Lauzon-Guay,
Reviewers:
B.P. Harvey, C. Feehan
Acknowledgements:
This research was supported by an Australian Research Council Future Fellowship (FT2001000949 to S.D.L.) and conducted under scientific research permit nos. 22111 and 21169.