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Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Reproductive phenology of the kelp Ecklonia radiata at its Australian warm-range edge and the influence of environmental factors

R. J. Veenhof https://orcid.org/0000-0002-5856-6475 A B * , C. Champion A B , S. A. Dworjanyn A , T. C. Shalders https://orcid.org/0000-0002-3656-2318 A B and M. A. Coleman A B
+ Author Affiliations
- Author Affiliations

A National Marine Science Centre, Faculty of Science and Engineering, Southern Cross University, Coffs Harbour, NSW, Australia.

B NSW Department of Primary Industries, National Marine Science Centre, Coffs Harbour, NSW, Australia.

* Correspondence to: reina.veenhof@scu.edu.au

Handling Editor: Thomas Wernberg

Marine and Freshwater Research 74(11) 928-940 https://doi.org/10.1071/MF22259
Submitted: 1 December 2022  Accepted: 14 May 2023   Published: 7 June 2023

© 2023 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: Range-edge populations persist closer to their physiological thresholds, often limiting reproductive output. Kelps are foundation species on temperate reefs, but their reproductive phenology at range edges remains poorly understood.

Aims: We assess the reproductive phenology of Ecklonia radiata at its eastern Australian warm range edge in relation to local environmental conditions and make comparisons with populations throughout Australia.

Methods: E. radiata fertility was monitored over multiple years and environmental predictors of fertility were assessed using generalised additive models. Fertility responses were compared with data from centre and cold range-edge populations.

Key results: The proportion of fertile E. radiata plants increased as daylength declined and the length of fertile tissue was positively correlated with temperature. The magnitude of spore release was variable and responded to episodic swell and rainfall events. This is contrary to spore-release data from centre and cold range-edge populations, which demonstrated seasonal patterns correlated with temperature.

Conclusion: Spore release was lower at the warm range edge, yet year-round spore release demonstrated flexibility in response to local environmental conditions.

Implications: Flexible reproductive phenology of E. radiata at its warm range edge may be advantageous for sustaining populations at low latitudes under climate change.

Keywords: Ecklonia radiata, environmental analysis, fertility, kelp, reproduction, reproductive phenology, spores, warm-range edge.


References

Abeli, T, Gentili, R, Mondoni, A, Orsenigo, S, and Rossi, G (2014). Effects of marginality on plant population performance. Journal of Biogeography 41, 239–249.
Effects of marginality on plant population performance.Crossref | GoogleScholarGoogle Scholar |

Almeida, SC, Nicastro, KR, Zardi, GI, Pearson, GA, Valero, M, and Serrão, EA (2017). Reproductive strategies and population genetic structure of Fucus spp. across a Northeast Atlantic biogeographic transition. Aquatic Living Resources 30, 16.
Reproductive strategies and population genetic structure of Fucus spp. across a Northeast Atlantic biogeographic transition.Crossref | GoogleScholarGoogle Scholar |

Alsuwaiyan, NA, Mohring, MB, Cambridge, M, Coleman, MA, Kendrick, GA, and Wernberg, T (2019). A review of protocols for the experimental release of kelp (Laminariales) zoospores. Ecology and Evolution 9, 8387–8398.
A review of protocols for the experimental release of kelp (Laminariales) zoospores.Crossref | GoogleScholarGoogle Scholar |

Alsuwaiyan, NA, Vranken, S, Filbee-Dexter, K, Cambridge, M, Coleman, MA, and Wernberg, T (2021). Genotypic variation in response to extreme events may facilitate kelp adaptation under future climates. Marine Ecology Progress Series 672, 111–121.
Genotypic variation in response to extreme events may facilitate kelp adaptation under future climates.Crossref | GoogleScholarGoogle Scholar |

Amsler, CD, and Neushul, M (1989). Diel periodicity of spore release from the kelp Nereocystis luetkeana (Mertens) Postels et Ruprecht. Journal of Experimental Marine Biology and Ecology 134, 117–127.
Diel periodicity of spore release from the kelp Nereocystis luetkeana (Mertens) Postels et Ruprecht.Crossref | GoogleScholarGoogle Scholar |

Assis, J, Berecibar, E, Claro, B, Alberto, F, Reed, D, Raimondi, P, and Serrão, EA (2017). Major shifts at the range edge of marine forests: the combined effects of climate changes and limited dispersal. Scientific Reports 7, 44348.
Major shifts at the range edge of marine forests: the combined effects of climate changes and limited dispersal.Crossref | GoogleScholarGoogle Scholar |

Bartsch, I, Vogt, J, Pehlke, C, and Hanelt, D (2013). Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea). Journal of Phycology 49, 1061–1073.
Prevailing sea surface temperatures inhibit summer reproduction of the kelp Laminaria digitata at Helgoland (North Sea).Crossref | GoogleScholarGoogle Scholar |

Brown, CJ, O’Connor, MI, Poloczanska, ES, Schoeman, DS, Buckley, LB, Burrows, MT, Duarte, CM, Halpern, BS, Pandolfi, JM, Parmesan, C, and Richardson, AJ (2016). Ecological and methodological drivers of species’ distribution and phenology responses to climate change. Global Change Biology 22, 1548–1560.
Ecological and methodological drivers of species’ distribution and phenology responses to climate change.Crossref | GoogleScholarGoogle Scholar |

Buschmann, AH, Vásquez, JA, Osorio, P, Reyes, E, Filún, L, Hernández-González, MC, and Vega, A (2004). The effect of water movement, temperature and salinity on abundance and reproductive patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile. Marine Biology 145, 849–862.
The effect of water movement, temperature and salinity on abundance and reproductive patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile.Crossref | GoogleScholarGoogle Scholar |

Buschmann, AH, Moreno, C, Vásquez, JA, and Hernández-González, MC (2006). Reproduction strategies of Macrocystis pyrifera (Phaeophyta) in southern Chile: the importance of population dynamics. Journal of Applied Phycology 18, 575–582.
Reproduction strategies of Macrocystis pyrifera (Phaeophyta) in southern Chile: the importance of population dynamics.Crossref | GoogleScholarGoogle Scholar |

Camus, C, Solas, M, Martínez, C, Vargas, J, Garcés, C, Gil-Kodaka, P, Ladah, LB, Serrão, EA, and Faugeron, S (2021). Mates matter: gametophyte kinship recognition and inbreeding in the giant kelp, Macrocystis pyrifera (Laminariales, Phaeophyceae). Journal of Phycology 57, 711–725.
Mates matter: gametophyte kinship recognition and inbreeding in the giant kelp, Macrocystis pyrifera (Laminariales, Phaeophyceae).Crossref | GoogleScholarGoogle Scholar |

Carnell, PE, and Keough, MJ (2019). Reconstructing historical marine populations reveals major decline of a kelp forest ecosystem in Australia. Estuaries and Coasts 42, 765–778.
Reconstructing historical marine populations reveals major decline of a kelp forest ecosystem in Australia.Crossref | GoogleScholarGoogle Scholar |

Coleman, MA, Reddy, M, Nimbs, MJ, Marshell, A, Al-Ghassani, SA, Bolton, JJ, Jupp, BP, De Clerck, O, Leliaert, F, Champion, C, Pearson, GA, Serrão, EA, Madeira, P, and Wernberg, T (2022). Loss of a globally unique kelp forest from Oman. Scientific Reports 12, 5020.
Loss of a globally unique kelp forest from Oman.Crossref | GoogleScholarGoogle Scholar |

Coumou, D, and Rahmstorf, S (2012). A decade of weather extremes. Nature Climate Change 2, 491–496.
A decade of weather extremes.Crossref | GoogleScholarGoogle Scholar |

Dangremond, EM, Hill, CH, Louaibi, S, and Muñoz, I (2022). Phenological responsiveness and fecundity decline near the southern range limit of Trientalis borealis (Primulaceae). Plant Ecology 223, 41–52.
Phenological responsiveness and fecundity decline near the southern range limit of Trientalis borealis (Primulaceae).Crossref | GoogleScholarGoogle Scholar |

Davis, TR, Champion, C, and Coleman, MA (2021). Climate refugia for kelp within an ocean warming hotspot revealed by stacked species distribution modelling. Marine Environmental Research 166, 105267.
Climate refugia for kelp within an ocean warming hotspot revealed by stacked species distribution modelling.Crossref | GoogleScholarGoogle Scholar |

Davis, TR, Champion, C, and Coleman, MA (2022). Ecological interactions mediate projected loss of kelp biomass under climate change. Diversity and Distributions 28, 306–317.
Ecological interactions mediate projected loss of kelp biomass under climate change.Crossref | GoogleScholarGoogle Scholar |

Dayton, PK (1985). Ecology of kelp communities. Annual Review of Ecology and Systematics 16, 215–245.
Ecology of kelp communities.Crossref | GoogleScholarGoogle Scholar |

de Bettignies, T, Wernberg, T, Lavery, PS, Vanderklift, MA, and Mohring, MB (2013). Contrasting mechanisms of dislodgement and erosion contribute to production of kelp detritus. Limnology and Oceanography 58, 1680–1688.
Contrasting mechanisms of dislodgement and erosion contribute to production of kelp detritus.Crossref | GoogleScholarGoogle Scholar |

De Wreede RE, Klinger T (1988) Reproductive strategies in algae. In ‘Plant reproductive ecology: patterns and strategies’. (Eds J Lovett Doust, L Lovett Doust) pp. 267–284. (Oxford University Press: New York, NY, USA)

Duarte, L, and Viejo, RM (2018). Environmental and phenotypic heterogeneity of populations at the trailing range-edge of the habitat-forming macroalga Fucus serratus. Marine Environmental Research 136, 16–26.
Environmental and phenotypic heterogeneity of populations at the trailing range-edge of the habitat-forming macroalga Fucus serratus.Crossref | GoogleScholarGoogle Scholar |

Edding, ME, Fonck, E, Orrego, P, Venegas, M, and Macchiavello, J (1993). A comparison between two populations of Lessonia trabeculata (Phaeophyta: Laminariales) microscopic stages. Hydrobiologia 260, 231–237.
A comparison between two populations of Lessonia trabeculata (Phaeophyta: Laminariales) microscopic stages.Crossref | GoogleScholarGoogle Scholar |

Edwards, MS (2022). It’s the little things: the role of microscopic life stages in maintaining kelp populations. Frontiers in Marine Science 9, 871204.
It’s the little things: the role of microscopic life stages in maintaining kelp populations.Crossref | GoogleScholarGoogle Scholar |

Filbee-Dexter, K, Wernberg, T, Grace, SP, Thormar, J, Fredriksen, S, Narvaez, CN, Feehan, CJ, and Norderhaug, KM (2020). Marine heatwaves and the collapse of marginal North Atlantic kelp forests. Scientific Reports 10, 13388.
Marine heatwaves and the collapse of marginal North Atlantic kelp forests.Crossref | GoogleScholarGoogle Scholar |

Forbes, H, Shelamoff, V, Visch, W, and Layton, C (2022). Farms and forests: evaluating the biodiversity benefits of kelp aquaculture. Journal of Applied Phycology 34, 3059–3067.
Farms and forests: evaluating the biodiversity benefits of kelp aquaculture.Crossref | GoogleScholarGoogle Scholar |

Gaston KJ (2003) ‘The structure and dynamics of geographic ranges.’ (Oxford University Press: UK)

Gaylord, B, Reed, DC, Raimondi, PT, and Washburn, L (2006). Macroalgal spore dispersal in coastal environments: mechanistic insights revealed by theory and experiment. Ecological Monographs 76, 481–502.
Macroalgal spore dispersal in coastal environments: mechanistic insights revealed by theory and experiment.Crossref | GoogleScholarGoogle Scholar |

Giraldo-Ospina, A, Kendrick, GA, and Hovey, RK (2021). Reproductive output, synchrony across depth and influence of source depth in the development of early life stages of kelp. Journal of Phycology 57, 311–323.
Reproductive output, synchrony across depth and influence of source depth in the development of early life stages of kelp.Crossref | GoogleScholarGoogle Scholar |

Gordon, R, and Brawley, SH (2004). Effects of water motion on propagule release from algae with complex life histories. Marine Biology 145, 21–29.
Effects of water motion on propagule release from algae with complex life histories.Crossref | GoogleScholarGoogle Scholar |

Graham, MH (2003). Coupling propagule output to supply at the edge and interior of a giant kelp forest. Ecology 84, 1250–1264.
Coupling propagule output to supply at the edge and interior of a giant kelp forest.Crossref | GoogleScholarGoogle Scholar |

Granado-Yela, C, Balaguer, L, García-Verdugo, C, Carrillo, K, and Méndez, M (2013). Thriving at the limit: differential reproductive performance in range-edge populations of a Mediterranean sclerophyll (Olea europaea). Acta Oecologica 52, 29–37.
Thriving at the limit: differential reproductive performance in range-edge populations of a Mediterranean sclerophyll (Olea europaea).Crossref | GoogleScholarGoogle Scholar |

Grebe, GS, Byron, CJ, Gelais, AS, Kotowicz, DM, and Olson, TK (2019). An ecosystem approach to kelp aquaculture in the Americas and Europe. Aquaculture Reports 15, 100215.
An ecosystem approach to kelp aquaculture in the Americas and Europe.Crossref | GoogleScholarGoogle Scholar |

Habibzadeh, N, Ghoddousi, A, Bleyhl, B, and Kuemmerle, T (2021). Rear-edge populations are important for understanding climate change risk and adaptation potential of threatened species. Conservation Science and Practice 3, e375.
Rear-edge populations are important for understanding climate change risk and adaptation potential of threatened species.Crossref | GoogleScholarGoogle Scholar |

Hampe, A, and Petit, RJ (2005). Conserving biodiversity under climate change: the rear edge matters. Ecology Letters 8, 461–467.
Conserving biodiversity under climate change: the rear edge matters.Crossref | GoogleScholarGoogle Scholar |

Hargreaves, AL, and Eckert, CG (2014). Evolution of dispersal and mating systems along geographic gradients: implications for shifting ranges. Functional Ecology 28, 5–21.
Evolution of dispersal and mating systems along geographic gradients: implications for shifting ranges.Crossref | GoogleScholarGoogle Scholar |

Hargreaves, AL, and Eckert, CG (2019). Local adaptation primes cold-edge populations for range expansion but not warming-induced range shifts. Ecology Letters 22, 78–88.
Local adaptation primes cold-edge populations for range expansion but not warming-induced range shifts.Crossref | GoogleScholarGoogle Scholar |

Hobday, AJ, and Lough, JM (2011). Projected climate change in Australian marine and freshwater environments. Marine and Freshwater Research 62, 1000–1014.
Projected climate change in Australian marine and freshwater environments.Crossref | GoogleScholarGoogle Scholar |

Hoffmann, AJ (1987). The arrival of seaweed propagules at the shore: a review. Botanica Marina 30, 151–166.
The arrival of seaweed propagules at the shore: a review.Crossref | GoogleScholarGoogle Scholar |

Hollarsmith, JA, Buschmann, AH, Camus, C, and Grosholz, ED (2020). Varying reproductive success under ocean warming and acidification across giant kelp (Macrocystis pyrifera) populations. Journal of Experimental Marine Biology and Ecology 522, 151247.
Varying reproductive success under ocean warming and acidification across giant kelp (Macrocystis pyrifera) populations.Crossref | GoogleScholarGoogle Scholar |

Hu, Z-M, Shan, T-F, Zhang, J, Zhang, Q-S, Critchley, AT, Choi, H-G, Yotsukura, N, Liu, F-L, and Duan, D-L (2021). Kelp aquaculture in China: a retrospective and future prospects. Reviews in Aquaculture 13, 1324–1351.
Kelp aquaculture in China: a retrospective and future prospects.Crossref | GoogleScholarGoogle Scholar |

Johnson, CR, Banks, SC, Barrett, NS, Cazassus, F, Dunstan, PK, Edgar, GJ, Frusher, SD, Gardner, C, Haddon, M, Helidoniotis, F, Hill, KL, Holbrook, NJ, Hosie, GW, Last, PR, Ling, SD, Melbourne-Thomas, J, Miller, K, Pecl, GT, Richardson, AJ, Ridgway, KR, Rintoul, SR, Ritz, DA, Ross, DJ, Sanderson, JC, Shepherd, SA, Slotwinski, A, Swadling, KM, and Taw, N (2011). Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 400, 17–32.
Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania.Crossref | GoogleScholarGoogle Scholar |

Joska, MAP, and Bolton, JJ (1987). In situ measurement of zoospore release and seasonality of reproduction in Ecklonia maxima (Alariaceae, Laminariales). British Phycological Journal 22, 209–214.
In situ measurement of zoospore release and seasonality of reproduction in Ecklonia maxima (Alariaceae, Laminariales).Crossref | GoogleScholarGoogle Scholar |

Kain, JM (1979). A view of the genus Laminaria. Oceanography and Marine Biology: an Annual Review 17, 101–161.

Kain, JM (1989). The seasons in the subtidal. British Phycological Journal 24, 203–215.
The seasons in the subtidal.Crossref | GoogleScholarGoogle Scholar |

Kawecki, TJ (2008). Adaptation to marginal habitats. Annual Review of Ecology, Evolution, and Systematics 39, 321–342.
Adaptation to marginal habitats.Crossref | GoogleScholarGoogle Scholar |

King, NG, McKeown, NJ, Smale, DA, Wilcockson, DC, Hoelters, L, Groves, EA, Stamp, T, and Moore, PJ (2019). Evidence for different thermal ecotypes in range centre and trailing edge kelp populations. Journal of Experimental Marine Biology and Ecology 514–515, 10–17.
Evidence for different thermal ecotypes in range centre and trailing edge kelp populations.Crossref | GoogleScholarGoogle Scholar |

Lara-Romero, C, García-Camacho, R, Escudero, A, and Iriondo, JM (2014). Genetic variation in flowering phenology and reproductive performance in a Mediterranean high-mountain specialist, Armeria caespitosa (Plumbaginaceae). Botanical Journal of the Linnean Society 176, 384–395.
Genetic variation in flowering phenology and reproductive performance in a Mediterranean high-mountain specialist, Armeria caespitosa (Plumbaginaceae).Crossref | GoogleScholarGoogle Scholar |

Layton, C, Cameron, MJ, Tatsumi, M, Shelamoff, V, Wright, JT, and Johnson, CR (2020). Habitat fragmentation causes collapse of kelp recruitment. Marine Ecology Progress Series 648, 111–123.
Habitat fragmentation causes collapse of kelp recruitment.Crossref | GoogleScholarGoogle Scholar |

Lester, SE, Gaines, SD, and Kinlan, BP (2007). Reproduction on the edge: large-scale patterns of individual performance in a marine invertebrate. Ecology 88, 2229–2239.
Reproduction on the edge: large-scale patterns of individual performance in a marine invertebrate.Crossref | GoogleScholarGoogle Scholar |

Levin, DA (2012). Mating system shifts on the trailing edge. Annals of Botany 109, 613–620.
Mating system shifts on the trailing edge.Crossref | GoogleScholarGoogle Scholar |

Liesner, D, Fouqueau, L, Valero, M, Roleda, MY, Pearson, GA, Bischof, K, Valentin, K, and Bartsch, I (2020). Heat stress responses and population genetics of the kelp Laminaria digitata (Phaeophyceae) across latitudes reveal differentiation among North Atlantic populations. Ecology and Evolution 10, 9144–9177.
Heat stress responses and population genetics of the kelp Laminaria digitata (Phaeophyceae) across latitudes reveal differentiation among North Atlantic populations.Crossref | GoogleScholarGoogle Scholar |

Liu, X, Bogaert, K, Engelen, AH, Leliaert, F, Roleda, MY, and De Clerck, O (2017). Seaweed reproductive biology: environmental and genetic controls. Botanica Marina 60, 89–108.
Seaweed reproductive biology: environmental and genetic controls.Crossref | GoogleScholarGoogle Scholar |

Lüning, K (1979). Growth strategies of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Helgoland (North Sea). Marine Ecology Progress Series 1, 195–207.

Lüning, K, and tom Dieck, I (1989). Environmental triggers in algal seasonality. Botanica Marina 32, 389–398.
Environmental triggers in algal seasonality.Crossref | GoogleScholarGoogle Scholar |

Mabin, CJT, Gribben, PE, Fischer, A, and Wright, JT (2013). Variation in the morphology, reproduction and development of the habitat-forming kelp Ecklonia radiata with changing temperature and nutrients. Marine Ecology Progress Series 483, 117–131.
Variation in the morphology, reproduction and development of the habitat-forming kelp Ecklonia radiata with changing temperature and nutrients.Crossref | GoogleScholarGoogle Scholar |

MacArthur RH (1972) ‘Geographical ecology: patterns in the distribution of species.’ (Harper and Row: New York, NY, USA)

McConnico, LA, and Foster, MS (2005). Population biology of the intertidal kelp, Alaria marginata Postels and Ruprecht: a non-fugitive annual. Journal of Experimental Marine Biology and Ecology 324, 61–75.
Population biology of the intertidal kelp, Alaria marginata Postels and Ruprecht: a non-fugitive annual.Crossref | GoogleScholarGoogle Scholar |

Mohring, MB, Wernberg, T, Kendrick, GA, and Rule, MJ (2013a). Reproductive synchrony in a habitat-forming kelp and its relationship with environmental conditions. Marine Biology 160, 119–126.
Reproductive synchrony in a habitat-forming kelp and its relationship with environmental conditions.Crossref | GoogleScholarGoogle Scholar |

Mohring, MB, Kendrick, GA, Wernberg, T, Rule, MJ, and Vanderklift, MA (2013b). Environmental influences on kelp performance across the reproductive period: an ecological trade-off between gametophyte survival and growth? PLoS ONE 8, e65310.
Environmental influences on kelp performance across the reproductive period: an ecological trade-off between gametophyte survival and growth?Crossref | GoogleScholarGoogle Scholar |

Mohring, MB, Wernberg, T, Wright, JT, Connell, SD, and Russell, BD (2014). Biogeographic variation in temperature drives performance of kelp gametophytes during warming. Marine Ecology Progress Series 513, 85–96.
Biogeographic variation in temperature drives performance of kelp gametophytes during warming.Crossref | GoogleScholarGoogle Scholar |

Muth, AF, Graham, MH, Lane, CE, and Harley, CDG (2019). Recruitment tolerance to increased temperature present across multiple kelp clades. Ecology 100, e02594.
Recruitment tolerance to increased temperature present across multiple kelp clades.Crossref | GoogleScholarGoogle Scholar |

Nimbs, MJ, Wernberg, T, Davis, TR, Champion, C, and Coleman, MA (2023). Climate change threatens unique evolutionary diversity in Australian kelp refugia. Scientific Reports 13, 1248.
Climate change threatens unique evolutionary diversity in Australian kelp refugia.Crossref | GoogleScholarGoogle Scholar |

Novaczek, I (1984a). Development and phenology of Ecklonia radiata at two depths in Goat Island Bay, New Zealand. Marine Biology 81, 189–197.
Development and phenology of Ecklonia radiata at two depths in Goat Island Bay, New Zealand.Crossref | GoogleScholarGoogle Scholar |

Novaczek, I (1984b). Response of gametophytes of Ecklonia radiata (Laminariales) to temperature in saturating light. Marine Biology 82, 241–245.
Response of gametophytes of Ecklonia radiata (Laminariales) to temperature in saturating light.Crossref | GoogleScholarGoogle Scholar |

Oppliger, LV, von Dassow, P, Bouchemousse, S, Robuchon, M, Valero, M, Correa, JA, Mauger, S, and Destombe, C (2014). Alteration of sexual reproduction and genetic diversity in the kelp species Laminaria digitata at the southern limit of its range. PLoS ONE 9, e102518.
Alteration of sexual reproduction and genetic diversity in the kelp species Laminaria digitata at the southern limit of its range.Crossref | GoogleScholarGoogle Scholar |

Parmesan, C, and Hanley, ME (2015). Plants and climate change: complexities and surprises. Annals of Botany 116, 849–864.
Plants and climate change: complexities and surprises.Crossref | GoogleScholarGoogle Scholar |

Pedersen P (1981) Phaeophyta: life histories. In ‘The biology of seaweeds, Vol. 17’. (Eds CS Lobban, MJ Wynne) pp. 194–217. (University of California Press: Berkeley, CA, USA)

Pironon, S, Papuga, G, Villellas, J, Angert, AL, García, MB, and Thompson, JD (2017). Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biological Reviews 92, 1877–1909.
Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm.Crossref | GoogleScholarGoogle Scholar |

Praeger, C, Magnusson, M, and Lawton, R (2022). Optimising the zoospore release, germination, development of gametophytes and formation of sporophytes of Ecklonia radiata. Journal of Applied Phycology 34, 2535–2549.
Optimising the zoospore release, germination, development of gametophytes and formation of sporophytes of Ecklonia radiata.Crossref | GoogleScholarGoogle Scholar |

Reed, DC, Ebeling, AW, Anderson, TW, and Anghera, M (1996). Differential reproductive responses to fluctuating resources in two seaweeds with different reproductive strategies. Ecology 77, 300–316.
Differential reproductive responses to fluctuating resources in two seaweeds with different reproductive strategies.Crossref | GoogleScholarGoogle Scholar |

Reed, DC, Anderson, TW, Ebeling, AW, and Anghera, M (1997). The role of reproductive synchrony in the colonization potential of kelp. Ecology 78, 2443–2457.
The role of reproductive synchrony in the colonization potential of kelp.Crossref | GoogleScholarGoogle Scholar |

Rehm, EM, Olivas, P, Stroud, J, and Feeley, KJ (2015). Losing your edge: climate change and the conservation value of range-edge populations. Ecology and Evolution 5, 4315–4326.
Losing your edge: climate change and the conservation value of range-edge populations.Crossref | GoogleScholarGoogle Scholar |

Robuchon, M, Le Gall, L, Mauger, S, and Valero, M (2014). Contrasting genetic diversity patterns in two sister kelp species co-distributed along the coast of Brittany, France. Molecular Ecology 23, 2669–2685.
Contrasting genetic diversity patterns in two sister kelp species co-distributed along the coast of Brittany, France.Crossref | GoogleScholarGoogle Scholar |

Sagarin, RD, Gaines, SD, and Gaylord, B (2006). Moving beyond assumptions to understand abundance distributions across the ranges of species. Trends in Ecology & Evolution 21, 524–530.
Moving beyond assumptions to understand abundance distributions across the ranges of species.Crossref | GoogleScholarGoogle Scholar |

Santelices, B (1990). Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanography and Marine Biology: An Annual Review 28, 177–276.

Sexton, JP, McIntyre, PJ, Angert, AL, and Rice, KJ (2009). Evolution and ecology of species range limits. Annual Review of Ecology, Evolution, and Systematics 40, 415–436.
Evolution and ecology of species range limits.Crossref | GoogleScholarGoogle Scholar |

Shay, JE, Pennington, LK, Mandussi Montiel-Molina, JA, Toews, DJ, Hendrickson, BT, and Sexton, JP (2021). Rules of plant species ranges: applications for conservation strategies. Frontiers in Ecology and Evolution 9, 700962.
Rules of plant species ranges: applications for conservation strategies.Crossref | GoogleScholarGoogle Scholar |

Sinclair, EA, Edgeloe, JM, Anthony, JM, Statton, J, Breed, MF, and Kendrick, GA (2020). Variation in reproductive effort, genetic diversity and mating systems across Posidonia australis seagrass meadows in Western Australia. AoB PLANTS 12, plaa038.
Variation in reproductive effort, genetic diversity and mating systems across Posidonia australis seagrass meadows in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Tala, F, Edding, M, and Vasquez, J (2004). Aspects of the reproductive phenology of Lessonia trabeculata (Laminariales: Phaeophyceae) from three populations in northern Chile. New Zealand Journal of Marine and Freshwater Research 38, 255–266.
Aspects of the reproductive phenology of Lessonia trabeculata (Laminariales: Phaeophyceae) from three populations in northern Chile.Crossref | GoogleScholarGoogle Scholar |

Tatsumi, M, and Wright, JT (2016). Understory algae and low light reduce recruitment of the habitat-forming kelp Ecklonia radiata. Marine Ecology Progress Series 552, 131–143.
Understory algae and low light reduce recruitment of the habitat-forming kelp Ecklonia radiata.Crossref | GoogleScholarGoogle Scholar |

Tatsumi, M, Mabin, CJT, Layton, C, Shelamoff, V, Cameron, MJ, Johnson, CR, and Wright, JT (2022). Density-dependence and seasonal variation in reproductive output and sporophyte production in the kelp, Ecklonia radiata. Journal of Phycology 58, 92–104.
Density-dependence and seasonal variation in reproductive output and sporophyte production in the kelp, Ecklonia radiata.Crossref | GoogleScholarGoogle Scholar |

tom Dieck, I (1991). Circannual growth rhythm and photoperiodic sorus induction in the kelp Laminaria setchellii (Phaeophyta). Journal of Phycology 27, 341–350.
Circannual growth rhythm and photoperiodic sorus induction in the kelp Laminaria setchellii (Phaeophyta).Crossref | GoogleScholarGoogle Scholar |

Vergés, A, Doropoulos, C, Malcolm, HA, Skye, M, Garcia-Pizá, M, Marzinelli, EM, Campbell, AH, Ballesteros, E, Hoey, AS, Vila-Concejo, A, Bozec, Y-M, and Steinberg, PD (2016). Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proceedings of the National Academy of Sciences 113, 13791–13796.
Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp.Crossref | GoogleScholarGoogle Scholar |

Vranken, S, Wernberg, T, Scheben, A, Severn-Ellis, AA, Batley, J, Bayer, PE, Edwards, D, Wheeler, D, and Coleman, MA (2021). Genotype–environment mismatch of kelp forests under climate change. Molecular Ecology 30, 3730–3746.
Genotype–environment mismatch of kelp forests under climate change.Crossref | GoogleScholarGoogle Scholar |

Wernberg, T, Smale, DA, Tuya, F, Thomsen, MS, Langlois, TJ, de Bettignies, T, Bennett, S, and Rousseaux, CS (2013). An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3, 78–82.
An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |

Wernberg, T, Bennett, S, Babcock, RC, de Bettignies, T, Cure, K, Depczynski, M, Dufois, F, Fromont, J, Fulton, CJ, Hovey, RK, Harvey, ES, Holmes, TH, Kendrick, GA, Radford, B, Santana-Garcon, J, Saunders, BJ, Smale, DA, Thomsen, MS, Tuckett, CA, Tuya, F, Vanderklift, MA, and Wilson, S (2016). Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172.
Climate-driven regime shift of a temperate marine ecosystem.Crossref | GoogleScholarGoogle Scholar |

Wernberg T, Krumhansl K, Filbee-Dexter K, Pedersen MF (2019a) Status and trends for the world’s kelp forests. In ‘World seas: an environmental evaluation’. (Ed. C Sheppard) pp. 57–78. (Elsevier: London, UK)

Wernberg, T, Coleman, MA, Babcock, RC, Bell, SY, Bolton, JJ, Connell, SD, Hurd, CL, Johnson, CR, Marzinelli, EM, Shears, NT, Steinberg, PD, Thomsen, MS, Vanderklift, MA, Vergés, A, and Wright, JT (2019b). Biology and ecology of the globally significant kelp Ecklonia radiata. Oceanography and Marine Biology: An Annual Review 57, 265–324.

Whetton, PH (1990). Relationships between monthly anomalies of sea-surface temperature and mean sea level pressure in the Australian region. Australian Meteorological Magazine 38, 17–30.

Wijffels, SE, Beggs, H, Griffin, C, Middleton, JF, Cahill, M, King, E, Jones, E, Feng, M, Benthuysen, JA, Steinberg, CR, and Sutton, P (2018). A fine spatial-scale sea surface temperature atlas of the Australian regional seas (SSTAARS): seasonal variability and trends around Australasia and New Zealand revisited. Journal of Marine Systems 187, 156–196.
A fine spatial-scale sea surface temperature atlas of the Australian regional seas (SSTAARS): seasonal variability and trends around Australasia and New Zealand revisited.Crossref | GoogleScholarGoogle Scholar |

Wiltshire KH, Tanner JE, Gurgel CFD, Deveney MR (2015) Feasibility study for integrated multitrophic aquaculture in southern Australia. Report to the Fisheries Research & Development Corporation; SARDI 883, F2015/000786-1, Adelaide, SA, Australia.

Wood, SN, Pya, N, and Säfken, B (2016). Smoothing parameter and model selection for general smooth models. Journal of the American Statistical Association 111, 1548–1563.
Smoothing parameter and model selection for general smooth models.Crossref | GoogleScholarGoogle Scholar |

Zardi, GI, Nicastro, KR, Serrão, EA, Jacinto, R, Monteiro, CA, and Pearson, GA (2015). Closer to the rear edge: ecology and genetic diversity down the core-edge gradient of a marine macroalga. Ecosphere 6, 1–25.
Closer to the rear edge: ecology and genetic diversity down the core-edge gradient of a marine macroalga.Crossref | GoogleScholarGoogle Scholar |

Zeileis, A, Kleiber, C, and Jackman, S (2008). Regression models for count data in R. Journal of Statistical Software 27, 1–25.
Regression models for count data in R.Crossref | GoogleScholarGoogle Scholar |

Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) ‘Mixed effects models and extensions in ecology with R.’ (Springer: New York, NY, USA)