Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Novel interaction between an octopus and an introduced macroalgae

Lorena Pía Storero https://orcid.org/0000-0001-5304-6203 A B * and Patricio Javier Pereyra A B
+ Author Affiliations
- Author Affiliations

A Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos Almirante Storni (CIMAS), CONICET/UNCo/Río Negro, San Antonio Oeste, Argentina.

B Escuela Superior de Ciencias Marinas, Universidad Nacional del Comahue, San Antonio Oeste, Argentina.

* Correspondence to: lorestorero@gmail.com

Handling Editor: Antony Knights

Marine and Freshwater Research 73(6) 866-871 https://doi.org/10.1071/MF21160
Submitted: 31 May 2021  Accepted: 18 February 2022   Published: 29 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Numerous macroalgae facilitate other species, modifying the diversity patterns, reducing the environmental stress, or providing non-trophic resources. In the sandy–pebbly bottoms of San Antonio Bay (north Patagonia, Argentina), where shelters are an important but limiting resource for the small Patagonian octopus (Octopus tehuelchus), the recently introduced macroalgae Undaria pinnatifida has shown a rapid increase in abundance. Herein, we documented the use of U. pinnatifida as shelter for octopuses and describe the size and maturity condition of individuals using the macroalgae. Our results suggest that U. pinnatifida facilitates octopuses by providing shelter in an environment where these are scarce and there is competition for high-quality shelters. The presence of small octopuses and brooding females under U. pinnatifida suggest that the structure of the macroalgae constitute an adequate shelter for brooding and may facilitate a portion of the population that usually lose the competition for traditional shelters. Indeed, the holdfast of U. pinnatifida, full of potential food sources, may provide a larger positive effect on octopuses. The effects of U. pinnatifida in north Patagonia should be tested on the different components of the community since there seem to be no similar native macroalgae providing structural complexity in these sandy–pebbly bottom ecosystems.

Keywords: Argentina, cephalopods, introduced species, Octopus tehuelchus, Patagonia, positive interaction, shelter, Undaria pinnatifida


References

Arcángel AE (2019) Interacción entre dos especies introducidas en un ambiente rocoso de la Bahía de San Antonio (Rio Negro, Argentina): la macroalga Undaria pinnatifida y la ascidia Styela clava. BSc Thesis, Escuela Superior de Ciencias Marinas, Universidad Nacional del Comahue, San Antonio Oeste, Argentina.

Barret, LT, Dempster, T, and Swearer, SE (2019). A nonnative habitat-former mitigates native habitat loss for endemic reef fishes. Ecological Applications 29, e01956.
A nonnative habitat-former mitigates native habitat loss for endemic reef fishes.Crossref | GoogleScholarGoogle Scholar |

Bulleri, F, Bruno, JF, Silliman, BR, and Stachowicz, JJ (2016). Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Functional Ecology 30, 70–78.
Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning.Crossref | GoogleScholarGoogle Scholar |

Carbone, ME, Perillo, GME, and Piccolo, MC (2007). Dinámica morfológica de los ambientes costeros de Bahía San Antonio Oeste, Provincia de Río Negro. Geoacta 32, 83–91.

Casas, GN, Piriz, ML, and Parodi, ER (2008). Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). Journal of the Marine Biological Association of the United Kingdom 88, 21–28.
Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina).Crossref | GoogleScholarGoogle Scholar |

Catford, JA, Wilson, JRU, Pyšek, P, Hulme, PE, and Duncan, RP (2022). Addressing context dependence in ecology. Trends in Ecology & Evolution 37, 158–170.
Addressing context dependence in ecology.Crossref | GoogleScholarGoogle Scholar |

Crain, CM, and Bertness, MD (2006). Ecosystem Engineering across Environmental Gradients: Implications for Conservation and Management. BioScience 56, 211–218.
Ecosystem Engineering across Environmental Gradients: Implications for Conservation and Management.Crossref | GoogleScholarGoogle Scholar |

Epstein, G, and Smale, DA (2017). Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecology and Evolution 7, 8624–8642.
Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management.Crossref | GoogleScholarGoogle Scholar | 29075477PubMed |

Gribben PE, Angelini C, Altieri AH, Bishop MJ, Thompsen MS, Bulleri F (2019) Facilitation cascades in marine ecosystems: a synthesis and future directions. In ‘Oceanography and Marine Biology. An Annual Review. Vol. 57 ’. (Eds SJ Hawkins, AL Allcock, AE Bates, LB Firth, IP Smith, SE Swearer, PA Todd) pp. 127–168. (CRC Press: Boca Raton, FL, USA)

Güller, M, and Zelaya, DG (2017). A hot‐spot of biodiversity in Northern Patagonia Argentina. Biodiversity and Conservation 26, 3329.

Iribarne, O (1990). Use of shelter by the small Patagonian octopus Octopus tehuelchus: availability, selection and effects on fecundity. Marine Ecology and Progress Series 66, 251–258.
Use of shelter by the small Patagonian octopus Octopus tehuelchus: availability, selection and effects on fecundity.Crossref | GoogleScholarGoogle Scholar |

Iribarne, O (1991). Intertidal harvest of the Patagonian octopus, Octopus tehuelchus (d’Orbigny). Fisheries Research 12, 375–390.
Intertidal harvest of the Patagonian octopus, Octopus tehuelchus (d’Orbigny).Crossref | GoogleScholarGoogle Scholar |

Iribarne, O, Fernández, M, and Zucchini, H (1991). Prey selection by the small Patagonian octopus Octopus tehuelchus d’Orbigny. Journal of Experimental Marine Biology and Ecology 148, 271–281.
Prey selection by the small Patagonian octopus Octopus tehuelchus d’Orbigny.Crossref | GoogleScholarGoogle Scholar |

Irigoyen, AJ, Trobbiani, G, Sgarlatta, MP, and Raffo, MP (2011a). Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biological Invasions 13, 1521–1532.
Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs.Crossref | GoogleScholarGoogle Scholar |

Irigoyen, AJ, Eyras, C, and Parma, AM (2011b). Alien algae Undaria pinnatifida causes habitat loss for rocky reef fishes in north Patagonia. Biological Invasion 13, 17–24.
Alien algae Undaria pinnatifida causes habitat loss for rocky reef fishes in north Patagonia.Crossref | GoogleScholarGoogle Scholar |

Isacch, JP, Costa, CSB, Rodríguez‐Gallego, L, Conde, D, Escapa, M, Gagliardini, DA, and Iribarne, OO (2006). Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient on the south‐west Atlantic coast. Journal of Biogeography 33, 888–900.

Jones, CG, Lawton, JH, and Shechak, M (1997). Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946–1957.
Positive and negative effects of organisms as physical ecosystem engineers.Crossref | GoogleScholarGoogle Scholar |

Narvarte, MA, González, R, Storero, L, and Fernández, M (2013). Effects of competition and egg predation on shelter use by Octopus tehuelchus females. Marine Ecology Progress Series 482, 141–151.
Effects of competition and egg predation on shelter use by Octopus tehuelchus females.Crossref | GoogleScholarGoogle Scholar |

Osovnikar PF, González RA, Narvarte MA (2006) Potencial de los refugios artificiales para el mejoramiento de los stocks de pulpito Octopus tehuelchus en Patagonia. In ‘Memorias de la Primera Conferencia de Pesquerías Costeras en América Latina y el Caribe. Evaluando, Manejando y Balanceando Acciones’, 4–8 October, 2004, Mérida, Yucatán, México. (Eds S Salas, MA Cabrera, J Ramos, D Flores, J Sánchez) pp. 107–121. (COASTFISH)

Pereyra, PJ, de la Barra, P, Gastaldi, M, Saad, JF, Firstater, FN, and Narvarte, MA (2017). When the tiny help the mighty: facilitation between two introduced species, a solitary ascidian and a macroalga in northern Patagonia, Argentina. Marine Biology 164, 185.
When the tiny help the mighty: facilitation between two introduced species, a solitary ascidian and a macroalga in northern Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Pujals, MA (1986). Contribución al conocimiento de la biología de Octopus tehuelchus d’Orbigny (Mollusca: Cephalopoda). Anales de la Sociedad Científica Argentina, Serie I 214, 29–71.

Ramus, AP, Silliman, BR, Thomsen, MS, and Long, ZT (2017). An invasive foundation species enhances multifunctionality in a coastal ecosystem. Proceedings of the National Academy of Sciences 114, 8580–8585.
An invasive foundation species enhances multifunctionality in a coastal ecosystem.Crossref | GoogleScholarGoogle Scholar |

Saul, WC, and Jescke, JM (2015). Eco-evolutionary experience in novel interactions. Ecology Letters 18, 236–245.
Eco-evolutionary experience in novel interactions.Crossref | GoogleScholarGoogle Scholar | 25626585PubMed |

South, PM, Floerl, O, Forrest, BM, and Thomsen, MS (2017). A review of three decades of research on the invasive kelp Undaria pinnatifida in Australia: an assessment of its success, impacts and status as one of the world’s worst invaders. Marine Environmental Research 131, 243–257.
| 28958575PubMed |

Stachowicz, JJ (2001). Mutualism, facilitation, and the structure of ecological communities: positive interactions play a critical, but underappreciated, role in ecological communities by reducing physical or biotic stresses in existing habitats and by creating new habitats on which many species depend. BioScience 515, 235–246.
Mutualism, facilitation, and the structure of ecological communities: positive interactions play a critical, but underappreciated, role in ecological communities by reducing physical or biotic stresses in existing habitats and by creating new habitats on which many species depend.Crossref | GoogleScholarGoogle Scholar |

Stachowicz, JJ, and Hay, ME (1999). Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores. Ecology 80, 495–509.
Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores.Crossref | GoogleScholarGoogle Scholar |

Storero, LP, Ocampo Reinaldo, M, González, RA, and Narvarte, MA (2010). Growth and life span of the small octopus Octopus tehuelchus in San Matias Gulf (Patagonia): three decades of study. Marine Biology 157, 555–564.
Growth and life span of the small octopus Octopus tehuelchus in San Matias Gulf (Patagonia): three decades of study.Crossref | GoogleScholarGoogle Scholar |

Storero, LP, Narvarte, MA, and González, RA (2013). Marine protected areas: reserve effect or natural variability? The Patagonian octopus case. Journal of the Marine Biological Association of the United Kingdom 93, 259–266.
Marine protected areas: reserve effect or natural variability? The Patagonian octopus case.Crossref | GoogleScholarGoogle Scholar |

Storero, LP, Botto, F, Narvarte, M, and Iribarne, O (2016). maturity condition and habitat type on food resources utilization by Octopus tehuelchus in Atlantic Patagonian coastal ecosystems. Marine Biology 163, 179.
maturity condition and habitat type on food resources utilization by Octopus tehuelchus in Atlantic Patagonian coastal ecosystems.Crossref | GoogleScholarGoogle Scholar |

Suarez-Jiménez, R, Hepburn, CD, Hyndes, GA, McLeod, RJ, Taylor, RB, and Hurd, CL (2017). The invasive kelp Undaria pinnatifida hosts an epifaunal assemblage similar to native seaweeds with comparable morphologies. Marine Ecology Progress Series 582, 45–55.
The invasive kelp Undaria pinnatifida hosts an epifaunal assemblage similar to native seaweeds with comparable morphologies.Crossref | GoogleScholarGoogle Scholar |

Thomsen, MS, Wernberg, T, Altieri, A, Tuya, F, Gulbransen, D, McGlathery, KJ, Holmer, M, and Silliman, BR (2010). Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrative and Comparative Biology 50, 158–175.
Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification.Crossref | GoogleScholarGoogle Scholar | 21558196PubMed |

Thomsen, MS, Wernberg, T, Olden, JD, Griffin, JN, and Silliman, BR (2011). A framework to study the context-dependent impacts of marine invasions. Journal of Experimental Marine Biology and Ecology 400, 322–327.
A framework to study the context-dependent impacts of marine invasions.Crossref | GoogleScholarGoogle Scholar |

Thomsen, M, Stæhr, P, Nejrup, L, and Schiel, D (2013). Effects of the invasive macroalgae Gracilaria vermiculophylla on two co-occurring foundation species and associated invertebrates. Aquatic Invasions 8, 133–145.

Valentine, JP, and Johnson, CR (2004). Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phylospora comosa in Tasmania, Australia. Marine and Freshwater Research 55, 223–230.
Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phylospora comosa in Tasmania, Australia.Crossref | GoogleScholarGoogle Scholar |

Vimercarti, G, Kumschick, S, Probert, AF, Volery, L, and Bacher, S (2020). The importance of assessing positive and beneficial impacts of alien species. Neobiota 62, 525–545.
The importance of assessing positive and beneficial impacts of alien species.Crossref | GoogleScholarGoogle Scholar |