Skip to main content

Advertisement

Log in

Novel mesophotic kelp forests in the Galápagos archipelago

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Kelps are among the most studied groups of macroalgae globally, as they are large foundation species that form some of the world’s most productive and diverse marine habitats. Yet little is known about diversity and ecology of tropical kelps, which tend to inhabit the more difficult to survey mesophotic zone. Eisenia galapagensis is the first tropical kelp species to be recorded globally, and is an endemic and endangered species to the Galapagos. Here, we reveal the presence of previously unknown off-shore mesophotic kelp populations in the Galapagos, made up by a potentially new Eisenia species for the region, and present phylogenetics and morphological analysis to support our claim. We find that these novel populations form extensive kelp forest habitats with a kelp density of 2.6 ± 1.5 m−2 at depths of 48–67 m, where mean water temperatures are 3–5 ℃ cooler than at the surface (18.1–19.9 ℃). Despite low levels of light and macronutrients (measured in August 2019), observations of juveniles and sori on blades suggests these kelp populations are successfully reproducing and recruiting. Our findings provide information about foundation species and complex marine communities previously unknown to managers of the Galápagos Marine Reserve. They also support the notion that this region is uniquely important for harboring brown macroalgal diversity. Our study highlights critical knowledge gaps on the distribution of primary foundation species in colder mesophotic zones, and how their invisibility from the surface prevents their inclusion in current conservation strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data that support the findings cannot be shared publicly because of Galapagos National Park research permit conditions. A previous authorization from the Galapagos National Park Directorate is required for further use of this data. Access to data can be requested via this email address at the Galapagos National Park Directorate Applied Research Department: investigacion@galapagos.gob.ec.

References

  • Altamirano M, Murakami A, Kawai H (2003) Photosynthetic performance and pigment content of different developmental stages of Ecklonia cava (Laminariales, Phaeophyceae). Bot Mar 46:9–16

    Article  CAS  Google Scholar 

  • Anderson AB, Assis J, Batista MB, Serrão EA, Guabiroba HC, Delfino SDT, Pinheiro HT, Pimentel CR, Gomes LEO, Vilar CC, Bernardino AF, Horta P, Ghisolfi RD, Joyeux J-C (2021) Global warming assessment suggests the endemic Brazilian kelp beds to be an endangered ecosystem. Mar Environ Res 168:105307

    Article  CAS  Google Scholar 

  • Atoche-Suclupe D, Alemán Mejía S, Perea de la Matta Á, Uribe RA (2021) Variabilidad espacio temporal de la estructura poblacional, morfología y morfometría de Eisenia cokeri MA Howe, 1914 (Phaeophycea: Laminariales) en el nor-centro de Perú. Boletin Instituto Del Mar Del Perú 48(3):414–429

    Google Scholar 

  • Bolton JJ (2010) The biogeography of kelps (Laminariales, Phaeophyceae): A global analysis with new insights from recent advances in molecular phylogenetics. Helgol Mar Res 64:263–279

    Article  Google 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, Wernberg T (2022) Loss of a globally unique kelp forest from Oman. Sci Rep 12:5020

    Article  CAS  Google Scholar 

  • Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294

    Article  CAS  Google Scholar 

  • Davis TR, Champion C, Coleman MA (2021) Climate refugia for kelp within an ocean warming hotspot revealed by stacked species distribution modelling. Mar Environ Res. https://doi.org/10.1016/j.marenvres.2021.105267

    Article  Google Scholar 

  • Dawson EY (2007) The Seaweeds Of Peru (nona Hedwigia Heft 13). Beihefte zur Nova Hedwigia. Heft 13:1–111

  • Dayton PK (1985) Ecology of Kelp Communities. Annu Rev Ecol Evol Syst 16:215–254

    Article  Google Scholar 

  • Drew EA (1974) An ecological study of Laminaria ochroleuca Pyl. growing below 50 metres in the straits of Messina. J Experim Marine 15:11–24

    Article  Google Scholar 

  • Edgar GJ, Banks S, Bensted-Smith R, Calvopiña M, Chiriboga A, Garske LE, Henderson S, Miller KA, Salazar S (2008) Conservation of threatened species in the Galapagos marine reserve through identification and protection of marine key biodiversity areas. Aquat Conserv 18:955–968

    Article  Google Scholar 

  • Edgar GJ, Banks SA, Brandt M, Bustamante RH, Chiriboga A, Earle SA, Garske LE, Glynn PW, Grove JS, Henderson S, Hickman CP, Miller KA, Rivera F, Wellington GM (2010) El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species. Glob Chang Biol 16:2876–2890

    Article  Google Scholar 

  • Eisaguirre JH, Eisaguirre JM, Davis K, Carlson PM, Gaines SD, Caselle JE (2020) Trophic redundancy and predator size class structure drive differences in kelp forest ecosystem dynamics. Ecology 101:1–11

    Article  Google Scholar 

  • Filbee-Dexter K, Wernberg T (2018) Rise of turfs: a new battlefront for globally declining kelp forests. Bioscience 68:64–76

    Article  Google Scholar 

  • Flores-Moya A (2012) Warm temperate seaweed communities: a case study of Deep Water kelp forests from the Alboran sea (SW Mediterranean sea) and the strait of Gibraltar. Ecological Studies. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 315–327

    Google Scholar 

  • Fragkopoulou E, Serrão EA, De Clerck O, Costello MJ, Araújo MB, Duarte CM, Krause-Jensen D, Assis J (2022) Global biodiversity patterns of marine forests of brown macroalgae. Glob Ecol Biogeogr 31:636–648

    Article  Google Scholar 

  • Garske LE (2002) Macroalgas Marinas. In: Danulat E, Edgar GJ (eds) Reserva Marina de Galápagos. Línea Base de la Biodiversidad, Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador, pp 419–439

    Google Scholar 

  • Gaylord BP, Denny MW (1997) Flow and flexibility: I. effects of size, shape and stiffness in determining wave forces on the stipitate kelps Eisenia arborea and Pterygophora californica. J Exp Biol 200:3141–3164

    Article  Google Scholar 

  • Giraldo-Ospina A, Kendrick GA, Hovey RK (2020) Depth moderates loss of marine foundation species after an extreme marine heatwave: could deep temperate reefs act as a refuge?: Deep thermal refuge. Proc Royal Soc b. https://doi.org/10.1098/rspb.2020.0709rspb20200709

    Article  Google Scholar 

  • Graham MH, Kinlan BP, Druehl LD, Garske LE, Banks S (2007) Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc Natl Acad Sci U S A 104:16576–16580

    Article  CAS  Google Scholar 

  • Joly AB, de Oliveira Filho EC (1967) Two Brazilian Laminarias. Instituto de Pesquisas da Marinha 4:1–13

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    Article  CAS  Google Scholar 

  • Kawai H, Akita S, Hashimoto K, Hanyuda T (2020) A multigene molecular phylogeny of Eisenia reveals evidence for a new species, Eisenia nipponica (Laminariales), from Japan. Eur J Phycol 55:234–241

    Article  Google Scholar 

  • Kirkman H (1984) Standing stock and production of Ecklonia radiata (C. Ag.). J Agardh J Exp Mar Bio Ecol 76:119–130

    Article  Google Scholar 

  • Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455

    Article  CAS  Google Scholar 

  • Krause-jensen D, Duarte CM (2016) Substantial role of macroalgae in marine carbon sequestration. Nat Publ Group. https://doi.org/10.1038/ngeo2790

    Article  Google Scholar 

  • Krumhansl KA, Okamoto DK, Rassweiler A, Novak M, Bolton JJ, Cavanaugh KC, Wernberg T, Anderson RJ, Barrett NS, Buschmann AH, Carr MH, Watson J, Witman JD, Byrnes JEK (2016) Global patterns of kelp forest change over the past half-century. Proc Nat Acad Sci 113:13785–13790

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Lis JT (1980) Fractionation of DNA fragments by polyethylene glycol induced precipitation. Methods Enzymol 65:347–353

    Article  CAS  Google Scholar 

  • Lüning K, Dring MJ (1979) Continuous underwater light measurement near Helgoland (North Sea) and its significance for characteristic light limits in the sublittoral region. Helgolander Wiss Meeresunters 32:403–424

    Article  Google Scholar 

  • Marins BV, Amado-Filho GM, Barreto MBB, Longo LL (2012) Taxonomy of the southwestern Atlantic endemic kelp: Laminaria abyssalis and Laminaria brasiliensis (Phaeophyceae, Laminariales) are not different species. Phycological Res 60:51–60

    Article  CAS  Google Scholar 

  • Marins BV, Amado-Filho GM, Barbarino E, Pereira-Filho GH, Longo LL (2014) Seasonal changes in population structure of the tropical deep-water kelp Laminaria abyssalis. Phycological Res 62:55–62

    Article  CAS  Google Scholar 

  • Markager S, Sand-jensen K (1992) Light requirements and depth zonation. Mar Ecol Prog Ser 88:83–92

    Article  Google Scholar 

  • Marzinelli EM, Williams SB, Babcock RC, Barrett NS, Johnson CR, Jordan A, Kendrick GA, Pizarro OR, Smale DA, Steinberg PD (2015) Large-scale geographic variation in distribution and abundance of Australian deep-water kelp forests. PLoS ONE 10:1–21

    Article  Google Scholar 

  • Matson PG, Edwards MS (2007) Effects of ocean temperature on the southern range limits of two understory kelps, Pterygophora californica and Eisenia arborea, at multiple life-stages. Mar Biol 151:1941–1949

    Article  Google Scholar 

  • Miller KA, Garske-Garcia L, Edgar GJ (2015) Eisenia galapagensis, Galápagos Kelp. The IUCN Red List of Threatened Species 2007:e.T63598A12686906

  • Morel A, Huot Y, Gentili B, Werdell PJ, Hooker SB, Franz BA (2007) Examining the consistency of products derived from various ocean color sensors in open ocean (Case 1) waters in the perspective of a multi-sensor approach. Remote Sens Environ 111:69–88

    Article  Google Scholar 

  • Nelson W, Duffy C, Trnski T, Stewart R (2018) Mesophotic Ecklonia radiata (Laminariales) at Rangitāhua, Kermadec Islands, New Zealand. Phycologia 57:534–538

    Article  Google Scholar 

  • Oliveira AP, Coutinho TP, Cabeçadas G, Brogueira MJ, Coca J, Ramos M, Calado G, Duarte P (2016) Primary production enhancement in a shallow seamount (Gorringe–Northeast Atlantic). J Mar Syst 164:13–29

    Article  Google Scholar 

  • Palacios DM (2004) Seasonal patterns of sea-surface temperature and ocean color around the Galápagos: regional and local influences. Deep Sea Res Part II Top Stud Oceanogr 51:43–57

    Article  Google Scholar 

  • Parada GM, Riosmena-rodríguez R, Martínez EA, Hernández-carmona G (2012) Morphological variability of intertidal Eisenia arborea (Laminariales, Ochrophyta ) at Punta Eugenia. Baja California Sur 27:109–114

    Google Scholar 

  • Parada GM, Riosmena-Rodríguez R, Martínez EA, Hernández-Carmona G (2009) Dinámica poblacional de Eisenia arborea Areschoug (Laminariales: Ochrophyta) en el intermareal de Punta Eugenia, Baja California Sur, México. Cienc Mar 13:3–13

    Google Scholar 

  • Pennington JT, Mahoney KL, Kuwahara VS, Kolber DD, Calienes R, Chavez FP (2006) Primary production in the eastern tropical pacific: a review. Prog Oceanogr 69:285–317

    Article  Google Scholar 

  • Petrov JE, Suchovejeva MV, Avdejev GV (1973) Species generis Laminaria Lam. e mari philippinensi nova. Novosti Sistematiki Nizshikh Rastenii 10:59–61

    Google Scholar 

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst Biol 67:901–904

    Article  CAS  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  Google Scholar 

  • Rothman MD, Wernberg T, Anderson RJ, Mohring MB, Bolton JJ (2015) A molecular investigation of the genus Ecklonia (Phaeophyceae, Laminariales ) with special focus on the Southern Hemisphere 1. J Phycolo 246:236–246

    Article  Google Scholar 

  • Salomon AK, Shears NT, Langlois TJ, Babcock RC (2008) Cascading effects of fishing can alter carbon flow through a temperate coastal ecosystem. Ecol Appl 18:1874–1887

    Article  Google Scholar 

  • Santelices B (2007) The discovery of kelp forests in deep-water habitats of tropical regions. Proc Natl Acad Sci 104:19163–19164

    Article  CAS  Google Scholar 

  • Schaeffer BA, Morrison JM, Kamykowski D, Feldman GC, Xie L, Liu Y, Sweet W, McCulloch A, Banks S (2008) Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sens Environ 112:3044–3054

    Article  Google Scholar 

  • Schramm KD, Marnane MJ, Elsdon TS, Jones C, Saunders BJ, Goetze JS, Driessen D, Fullwood LAF, Harvey ES (2020) A comparison of stereo-BRUVs and stereo-ROV techniques for sampling shallow water fish communities on and off pipelines. Mar Environ Res 162:105198

    Article  CAS  Google Scholar 

  • Shaffer JM, Beaulieu JJ (2012) Calibration of the Odyssey™ photosynthetic Irradiance recorder™ for absolute irradiance measures. J Freshw Ecol 27:599–605

    Article  Google Scholar 

  • Silva PC (2008) Conespecificidad de Eisenia desmarestioides y E. masonii (Laminariales, Phaeophyceae) de Isla Guadalupe, Baja California, México. Hidrobiologica 18(2):155–165

    Google Scholar 

  • Smale DA (2019) Impacts of ocean warming on kelp forest ecosystems. New Phytol. https://doi.org/10.1111/nph.16107Key

    Article  Google Scholar 

  • Smale DA, Burrows MT, Evans AJ, King N, Sayer MDJ, Yunnie ALE, Moore PJ (2016) Linking environmental variables with regional scale variability in ecological structure and standing stock of carbon within UK kelp forests. Mar Ecol Prog Ser 542:79–95

    Article  CAS  Google Scholar 

  • Starko S, Soto M, Darby H, Demes KW, Kawai H, Yotsukura N, Lindstrom SC, Keeling PJ, Graham SW, Martone PT (2019) Molecular phylogenetics and evolution a comprehensive kelp phylogeny sheds light on the evolution of an ecosystem. Mol Phylogenet Evol 136:138–150

    Article  Google Scholar 

  • Steneck RS, Johnson CR (2014) Kelp forests dynamic patterns, processes, and feedbacks. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer Associates Inc, Massachusetts, USA, pp 315–336

    Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Article  Google Scholar 

  • Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921

    Article  Google Scholar 

  • Taylor WR (1945) Pacific Marine Algae of the Allan Hancock Expeditions to the Galapagos Islands. In: University of Southern California Press

  • 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 Bio Ecol 492:81–98

    Article  Google Scholar 

  • Watson JC, Hawkes MW, Lee LC, Lamb A (2021) The dynamics and geographic disjunction of the kelp Eisenia arborea along the west coast of Canada. Bot Mar 64:395–406

    Article  Google Scholar 

  • 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, Wright JT (2019) Biology and ecology of the globally significant Kelp Ecklonia radiata. Oceanogr Mar Biol 57:236–246

    Google Scholar 

  • Žuljević A, Peters AF, Nikolić V, Antolić B, Despalatović M, Cvitković I, Isajlović I, Mihanović H, Matijević S, Shewring DM, Canese S, Katsaros C, Küpper FC (2016) The Mediterranean deep-water kelp Laminaria rodriguezii is an endangered species in the Adriatic Sea. Mar Biol 163:1–12

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Galápagos National Park Directorate for providing institutional support for this study and the Government of Ecuador and its navy for permission to operate in their territorial waters. We are indebted to Tom Glebas, Maria Jose Barragan, Izzy Morgante, Alize Bouriat, Paulina Sepa and Galápagos National Park warden Alberto Proaño and Jenifer Suarez for their assistance in undertaking the field expeditions for this study. We greatly thank Video Ray LLC who supported the pilot study with in-kind donations of ROV equipment and technical field assistance of their staff. We owe thanks to Dr. Sylvia Earle and the crew of the M/V Argos for helping to collect samples and record video footage during the Mission Blue’s Galápagos Expedition. We are grateful for local fisherman Nelson Ibarra, who shared with us the location of the Santa Fe kelp forest and kelp sample he found and provided. We thank David Buglass and anonymous reviewers whose edits greatly improved the manuscript, and Jose Marin Jarrin, Harmony Martell, Pedro Gonzales, Patrik Martone and the staff of the Charles Darwin Foundation for their technical assistance. We acknowledge the Sea Dog Productions for funding the tech diving expedition and National Geographic’s Science Exploration Education Initiative for donating a Trident ROV. This publication has the contribution number 2476 of the Charles Darwin Foundation for the Galapagos Islands.

Funding

This research was funded by the National Geographic Society (grant EC-50662R-18), Mrs. Karen Lo, and Natural Sciences and Engineering Research Council Discovery Grant (SD Donner).

Author information

Authors and Affiliations

Authors

Contributions

SB conceived of the study, conducted field work, and led the writing of the manuscript. HK and TH undertook the genetic analysis of and wrote the phylogenetic section of the manuscript. MA and JDR provided equipment, supported the data collection planning, carried out and wrote the morphological analysis of kelp specimens. EH provided stereo-video equipment and conceptualized video data analysis. JRB provided water sampling equipment and water analysis. SD provided funding and supported the data analysis. IK provided laboratory materials and logistical support. SB wrote the original manuscript and all authors commented on subsequent versions. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Salome Buglass.

Ethics declarations

Conflict of interest

Authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval

To collect data and samples (of macroalgae and associated invertebrates) in the Galápagos Marine Reserve, the authors acquired the necessary research permits (permits PC-81-18 and PC-56-19) and sample export approvals from the Galápagos National Park Directorate and Ecuador’s Ministry of Environment.

Additional information

Responsible Editor: Ulrich Sommer.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1880 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buglass, S., Kawai, H., Hanyuda, T. et al. Novel mesophotic kelp forests in the Galápagos archipelago. Mar Biol 169, 156 (2022). https://doi.org/10.1007/s00227-022-04142-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-022-04142-8

Keywords

Navigation