Skip to main content
SpringerLink
Log in

Shallow-water bryozoans from the Azores (central North Atlantic): native vs. non-indigenous species, and a method to evaluate taxonomic uncertainty

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Bryozoan records from the shores and upper shelf (≤50 m depth) of the remote Azores Archipelago (central North Atlantic) have been analyzed, along with unpublished data and data from recent surveys. A checklist of 67 shallow-water species is hereby compiled for the region, of which more than one third represent records from campaigns conducted during the last 20 years. A classification on the origin of the species indicates that the majority (62%) are cryptogenic while 27% (n = 18) are considered native. Given the natural limitations for genetic exchange between the archipelago’s bryozoan populations and those from neighboring shores, the taxa presently considered as cryptogenic may yield a considerable amount of endemic species after taxonomic revision. The remaining 11% are confirmed as non-indigenous species, highlighting the importance of human-mediated transport in considerably enhancing the diversity of bryozoans in remote oceanic archipelagos, which would otherwise be off-limits to their natural dispersal capacity. In view of the need to quantitatively evaluate the certainty of species-level identification when assembling such biodiversity inventories, we have developed a method to attribute a degree of certainty to species records. The application of this method to the current checklist highlights the importance of further studies to ascertain the identification of many species recorded for the Azores, and to be able to categorize them confidently as either native, cryptogenic or non-indigenous.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Acosta H, Forrest BM (2009) The spread of marine non-indigenous species via recreational boating: A conceptual model for risk assessment based on fault tree analysis. Ecol Model 220:1586–1598

    Article  Google Scholar 

  • Aguilar LR, Ugaz LT, Garay JC (2014) Variación estacional de Bugula neritina (Bryozoa, Cheilostomata) en las estructuras de cultivo suspendido de Argopecten purpuratus en bahía Samanco (Ancash, Perú). Rev Cient Soc Española Acuicult 40:1–10

    Google Scholar 

  • Amat JN, Tempera F (2009) Zoobotryon verticillatum Delle Chiaje, 1822 (Bryozoa), a new occurrence in the archipelago of the Azores (North-eastern Atlantic). Mar Pollut Bull 58:761–764

    Article  CAS  PubMed  Google Scholar 

  • Ávila SP, da Silva CM, Schiebel R, Cecca F, Backeljau T, de Frias MA (2009) How did they get there? The biogeography of the marine molluscs of the Azores. Bull Soc Géol Fr 180:295–307

    Article  Google Scholar 

  • Ávila SP, Ramalho R, Habermann J, Quartau R, Kroh A, Berning B, Johnson M, Kirby M, Zanon V, Titschack J, Goss A, Rebelo AC, Melo C, Madeira P, Cordeiro R, Meireles R, Bagaço L, Hipólito A, Uchman A, da Silva CM, Cachão M, Madeira J (2015) Palaeoecology, taphonomy, and preservation of a lower Pliocene shell bed (coquina) from a volcanic oceanic island (Santa Maria Island, Azores). Palaeogeogr Palaeoclimatol Palaeoecol 430:57–73

    Article  Google Scholar 

  • Bayer M, Todd CD (1997) Evidence for zooid senescence in the marine bryozoan Electra pilosa. Invertebr Biol 116:331–340

    Article  Google Scholar 

  • Berning B (2006) The cheilostome bryozoan fauna from the late Miocene of Niebla (Guadalquivir Basin, SW Spain): Environmental and biogeographic implications. Mitt Geol-Paläontol Inst Univ Hamburg 90:7–156

    Google Scholar 

  • Berning B (2013) New and little-known Cheilostomata (Bryozoa, Gymnolaemata) from the NE Atlantic. Eur J Taxon 44:1–25

    Google Scholar 

  • Berning B, Kuklinski P (2008) North-east Atlantic and Mediterranean species of the genus Buffonellaria (Bryozoa, Cheilostomata): Implications for biodiversity and biogeography. Zool J Linnean Soc 152:537–566

    Article  Google Scholar 

  • Bradstock M, Gordon DP (1983) Coral-like bryozoan growths in Tasman Bay, and their protection to conserve commercial fish stocks. New Zeal J Mar Fresh 17:159–163

    Article  Google Scholar 

  • Bushnell JH, Rao KS (1974) Dormant or quiescent stages and structures among the Ectoprocta: Physical and chemical factors affecting viability and germination of statoblasts. Trans Am Microsc Soc 93:524–543

    Article  Google Scholar 

  • Calvet L (1931) Bryozoaires provenant des campagnes scientifiques du Prince Albert I de Monaco. Imprimerie de Monaco, Monaco

    Google Scholar 

  • Campbell ML, Nair R, Hewitt CL (2003) Xenodiversity of the marine bryozoan fauna in Australian waters. Rec South Aust Mus 7:31–37

    Google Scholar 

  • Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: The biology of ballast water. Oceanogr Mar Biol 23:313–371

    Google Scholar 

  • Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

  • Clarke A, Lidgard S (2000) Spatial patterns of diversity in the sea: Bryozoan species richness in the North Atlantic. J Anim Ecol 69:799–814

    Article  PubMed  Google Scholar 

  • Collyer ML, Heilveil JS, Stockwell CA (2011) Contemporary evolutionary divergence for a protected species following assisted colonization. PLoS One 6(8):e22310. https://doi.org/10.1371/journal.pone.0022310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in evolutionary biology. Trends Ecol Evol 15:290–295

    Article  CAS  PubMed  Google Scholar 

  • Davidson IC, McCann LD, Fofonoff P, Systma MD, Ruiz GM (2008) The potential for hull-mediated species transfers by obsolete ships on their final voyages. Divers Distrib 14:518–529

    Article  Google Scholar 

  • Day J, Dudley N, Hockings M, Holmes G, Laffoley D, Stolton S, Wells S (2012) Guidelines for applying the IUCN protected area management categories to marine protected areas. IUCN, Gland

    Google Scholar 

  • d'Hondt J-L (1975) Bryozoaires cténostomes et cheilostomes (Cribrimorphes et Escharellidae exceptés) provenant des dragages de la campagne océanographique Biaçores du “Jean-Charcot”. Bull Mus Natl Hist Nat 209:553–600

    Google Scholar 

  • Edwards M, Morse DR (1995) The potential for computer-aided identification in biodiversity research. Trends Ecol Evol 10:153–158

    Article  CAS  PubMed  Google Scholar 

  • El Hajjaji K (1992) Les Bryozoaires du Miocène supérieur du Maroc nord-oriental. Doc Lab Géol Lyon 123:1–355

    Google Scholar 

  • Fernández-Palacios JM, de Nascimiento L, Otto R, Delgado JD, García-del-Rey E, Arévalo JR, Whittaker RJ (2011) A reconstruction of Palaeo-Macaronesia, with particular reference to the long-term biogeography of the Atlantic island laurel forests. J Biogeogr 38:226–246

    Article  Google Scholar 

  • Floerl O, Pool TK, Inglis GJ (2004) Positive interactions between nonindigenous species facilitate transport by human vectors. Ecol Appl 14:1724–1736

    Article  Google Scholar 

  • Floerl O, Inglis GJ, Dey K, Smith A (2009) The importance of transport hubs in stepping-stone invasions. J Appl Ecol 46:37–45

    Article  Google Scholar 

  • Gaston KJ, O’Neill MA (2004) Automated species identification: Why not? Philos Trans R Soc Lond B 359:655–667

    Article  Google Scholar 

  • Gordon DP (1972) Biological relationships of an intertidal bryozoan population. J Nat Hist 6:503–514

    Article  Google Scholar 

  • Gordon DP, Ramalho LV, Taylor PD (2006) An unreported invasive bryozoan that can affect livelihoods - Membraniporopsis tubigera in New Zealand and Brazil. Bull Mar Sci 78:331–442

    Google Scholar 

  • Gossett L, Lester J, Gonzalez L (2004) Galveston Bay invasive species risk assessment, final report. Webster, Texas

    Google Scholar 

  • Guia APO, Saitoh T (2007) The gap between the concept and definitions in the evolutionarily significant unit: The need to integrate neutral genetic variation and adaptive variation. Ecol Res 22:604–612

    Article  Google Scholar 

  • Harmelin J-G (1978) Sur Quelques Cribrimorphes (Bryozoa, Cheilostomata) de l'Atlantique Oriental. Tethys 8:173–192

    Google Scholar 

  • Harmelin J-G (2006) The Puellina flabellifera species complex: A remarkable example of worldwide species radiation in cribrimorph bryozoans. Cour Forschungsinst Senckenb 257:73–91

    Google Scholar 

  • Harmelin J-G (2014) Alien bryozoans in the eastern Mediterranean Sea - new records from the coast of Lebanon. Zootaxa 3893:301–338

    Article  PubMed  Google Scholar 

  • Hayward PJ, McKinney FK (2002) Northern Adriatic Bryozoa from the vicinity of Rovinj, Croatia. Bull Am Mus Nat Hist 270:1–139

    Article  Google Scholar 

  • Inglis G, Gust N, Fitridge I, Floerl O, Woods C, Hayden B, Fenwick G (2006) Whangarei harbour (Whangarei port and Marsden point) baseline survey for non-indigenous marine species. Biosecurity. New Zealand Technical Paper 2005/16:1–101

    Google Scholar 

  • IUCN International Union for Conservation of Nature (2000) Guidelines for the prevention of biodiversity loss caused by alien invasive species. IUCN Council, Gland

    Google Scholar 

  • Jullien J, Calvet L (1903) Bryozoaires Provenant des Campagnes de l'Hirondelle (1886–1888). Résultats des Campagnes Scientifiques Accomplies sur son Yacht par Albert 1er Prince Souverain de Monaco 23:1–188

  • Kinnison MT, Unwin MJ, Hendry AP, Quinn TP (2001) Migratory costs and the evolution of egg size and number in introduced and indigenous salmon populations. Evolution 55:1656–1667

    Article  CAS  Google Scholar 

  • Lambert WJ, Levin PS, Berman J (1992) Changes in the structure of a New England (USA) kelp bed: The effects of an introduced species? Mar Ecol Prog Ser 88:303–307

    Article  Google Scholar 

  • Lewis PN, Riddle MJ, Smith SDA (2005) Assisted passage or passive drift: A comparison of alternative transport mechanisms for nonindigenous coastal species into the Southern Ocean. Antarct Sci 17:183–191

    Article  Google Scholar 

  • Lidgard S (2008) Predation in marine bryozoan colonies: Taxa, traits and trophic groups. Mar Ecol Prog Ser 359:117–131

    Article  Google Scholar 

  • Marchini A, Cunha MR, Occhipinti-Ambrogi A (2007) First observations on bryozoans and entoprocts in the ria de Aveiro (NW Portugal) including the first record of the Pacific invasive cheilostome Tricellaria inopinata. Mar Ecol 28:154–160

    Article  Google Scholar 

  • Marchini A, Galil BS, Occhipinti-Ambrogi A (2015) Recommendations on standardizing lists of marine alien species: Lessons from the Mediterranean Sea. Mar Pollut Bull 10:267–273

    Article  CAS  Google Scholar 

  • McCann LD, Hitchcock NG, Winston JE, Ruiz GM (2007) Non-native bryozoans in coastal embayments of the southern United States: New records for the western Atlantic. Bull Mar Sci 80:319–342

    Google Scholar 

  • Meyer CP, Paulay G (2005) DNA barcoding: Error rates based on comprehensive sampling. PLoS Biol 3:2229–2238

    CAS  Google Scholar 

  • Micael J, Parente M, Costa AC (2014a) Tracking macroalgae introductions in North Atlantic oceanic islands. Helgol Mar Res 68:209–219

    Article  Google Scholar 

  • Micael J, Marina J, Costa AC, Occhipinti-Ambrogi A (2014b) The non-indigenous Schizoporella errata (Bryozoa: Cheilostomatida) introduced into the Azores archipelago. Mar Biodivers Rec. https://doi.org/10.1017/S1755267214001298

  • Micael J, Jardim N, Núñez C, Occhipinti-Ambrogi A, Costa AC (2016) Some Bryozoa species recently introduced into the Azores: Reproductive strategies as a proxy for further spread. Helgol Mar Res. https://doi.org/10.1186/s10152-016-0458-7

  • Morton B, Britton JC, de Frias Martins AM (1998) Coastal ecology of the Açores. Sociedade Afonso Chaves, Ponta Delgada

    Google Scholar 

  • Nelson CS, Hyden FM, Keane SL, Leask WL, Gordon DP (1988) Application of bryozoan zoarial growth-form studies in facies analysis of non-tropical carbonate deposits in New Zealand. Sediment Geol 60:301–322

    Article  Google Scholar 

  • Occhipinti-Ambrogi A (1991) The spread of Tricellaria inopinata into the lagoon of Venice: An ecological hypothesis. Bull Soc Sci Nat Ouest Fr 1:299–308

    Google Scholar 

  • Occhipinti-Ambrogi A (2000) Biotic invasions in the lagoon of Venice: Ecological considerations. Biol Invasions 2:165–176

    Article  Google Scholar 

  • Pouyet S, Moissette P (1992) Bryozoaires du Pliocène d'Altavilla (Sicile-Italie): révision de la collection Cipolla, nouvelles données, paléoécologie. Palaeontogr Abt A 223:19–101

    Google Scholar 

  • Reverter-Gil O, Fernández-Pulpeiro E (2007) Species of genus Schizotheca Hincks (Bryozoa, Cheilostomata) described in the Atlantic-Mediterranean region, with notes on some species of Parasmittina Osburn. J Nat Hist 41:1929–1953

    Article  Google Scholar 

  • Reverter-Gil O, Berning B, Souto J (2015) Diversity and systematics of Schizomavella species (Bryozoa: Bitectiporidae) from the bathyal NE Atlantic. PLoS One 10(10):e0139084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryland JS (1967) Polyzoa. Oceanogr Mar Biol 5:343–369

    Google Scholar 

  • Ryland JS, Hayward PJ (1991) Marine flora and Fauna of the Northeast United States: Erect Bryozoa. N.O.A.A. Techn. Report NMFS 99:1–48

    Google Scholar 

  • Ryland JS, Bishop JDD, de Blauwe H, Nagar AE, Minchin D, Wood CA, Yunnie ALE (2011) Alien species of Bugula (Bryozoa) along the Atlantic coasts of Europe. Aquat Invasions 6:17–31

    Article  Google Scholar 

  • Sala I, Caldeira RMA, Estrada-Allis SN, Froufe E, Coulevard X (2013) Lagrangian transport pathways in the northeast Atlantic and their environmental impact. Limnol & Oceanogr Fluids & Environ 3:40–60

    Article  Google Scholar 

  • Sellheim K, Stachowicz JJ, Coates RC (2010) Effects of a non-native habitat-forming species on mobile and sessile epifaunal communities. Mar Ecol Prog Ser 398:69–80

    Article  Google Scholar 

  • Stachowicz J, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: Disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262

    Article  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: Reconciling pattern and process. Ecology 83:2575–2590

    Article  Google Scholar 

  • Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101

    Article  Google Scholar 

  • Stockwell CA, Heilveil JS, Purcell K (2013) Estimating divergence time for two evolutionarily significant units of a protected fish species. Conserv Genet 14:215–222

    Article  Google Scholar 

  • Taylor PD, James NP (2013) Secular changes in colony-forms and bryozoan carbonate sediments through geological history. Sedimentology 60:1184–1212

    Article  Google Scholar 

  • Taylor PD, Lombardi C, Cocito S (2015) Biomineralization in bryozoans: Present, past and future. Biol Rev 90:1118–1150

    Article  PubMed  Google Scholar 

  • Tempera F, Afonso P, Morato T, Prieto R, Silva M, Cruz A, Gonçalves J, Santos RS (2001) Comunidades Biológicas dos Sítios de Interesse Comunitário do Canal Faial-Pico. Arquivos do DOP, Horta

    Google Scholar 

  • Tempera F, Torres P, de la Cuadra C, Costa AC (2010) A list of coastal marine invertebrates. In: Borges PAV, Costa A, Cunha R, Gabriel R, Gonçalves V, Martins AF, Melo I, Parente M, Raposeiro P, Rodrigues P, Santos RS, Silva L, Vieira P, Vieira V (eds) A list of the terrestrial and marine biota from the Azores. Princípia, Cascais, pp 320–321

    Google Scholar 

  • Tompsett S (2010) Taxonomy, morphometrics and phylogeography of the cheilostome bryozoan genus Schizoporella in Europe. Dissertation, Aberystwyth University

  • Vieira LM, Spencer-Jones ME, Winston JE (2013) Cradoscrupocellaria, a new bryozoan genus for Scrupocellaria bertholletii (Audouin) and related species (Cheilostomata, Candidae): Taxonomy, biodiversity and distribution. Zootaxa 3707:1–63

    Article  PubMed  Google Scholar 

  • Vieira LM, Jones MS, Taylor PD (2014) The identity of the invasive fouling bryozoan Watersipora subtorquata (d’Orbigny) and some other congeneric species. Zootaxa 3857:151–182

    Article  PubMed  Google Scholar 

  • Watts PC, Thorpe JP, Taylor PD (1998) Natural and anthropogenic dispersal mechanisms in the marine environment: A study using cheilostome Bryozoa. Philos Trans R Soc Lond Ser B Biol Sci 353:453–464

    Article  Google Scholar 

  • Whittaker RJ (1998) Island biogeography: Ecology, evolution and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wisshak M, Berning B, Jakobsen J, Freiwald (2015) A temperate carbonate production: Biodiversity of calcareous epiliths from intertidal to bathyal depths (Azores). Mar Biodivers 45:87–112

    Article  Google Scholar 

Download references

Acknowledgements

Thanks are due to projects MARÉ (Life-Nature B4-3200/98/509), MAROV (PDCTM/P/MAR/15249/1999), POOC Costa N de São Miguel and Missões Bancos. IMAR-DOP/UAz is Research and Development Unit no. 531. LARSyS is Associated Laboratory no. 9. They are funded by the Portuguese Foundation for Science and Technology (FCT) through PEst-OE/EEI/LA0009/2011-2014 (OE, COMPETE & QREN) and by the Azores Fund for Science and Technology (FRCT) through funding schemes (RAA and Pro-Convergência).

This research is also part of project ‘Açores: Stopover for Marine Alien Species?’ – ASMAS - M2.1.2/I/032/2011 funded by the Direção Regional de Ciência e Tecnologia (DRCT). BB received the support from the SYNTHESYS Project (http://www.synthesys.info/), which is financed by the European Community Research Infrastructure Action under the FP7 “Capacities” Program, and which allowed studying some of the type material at the MNHN (FR-TAF-1902, -5579). BB also profited from workshops held in the Azores, which were organized by Sérgio Ávila (Universidade dos Açores), and funded by the DRCT, FCT and the Câmara Municipal de Vila do Porto (Santa Maria). Acknowledgements are also due to the funding by FEDER through COMPETE ‘Operational Programme for Competitiveness Factors and to Portuguese National Funds received from FCT –Foundation for Science and Technology under the UID/BIA/50027/2013 and POCI-01-0145-FEDER-006821.

Personal thanking notes are due to Jorge Fontes, Telmo Gomes, Pedro Afonso, Paulo Martins and Vítor Rosa for their hard work during the surveys. Ricardo Santos is acknowledged for the coordination of projects MARÉ and MAROV and for supporting the work on taxonomic groups poorly studied in the Azores. Peter Wirtz is thanked for the donation of samples. Aylin Ulman for the English revision of the text.

Author information

Authors and Affiliations

  1. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos Açores, Universidade dos Açores, Campus de Ponta Delgada Apartado 1422, PT 9501-801, Ponta Delgada, Açores, Portugal

    Joana Micael, Björn Berning & Ana Cristina Costa

  2. Bird Ecology Lab, Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile

    Joana Micael

  3. MARE – Marine and Environmental Sciences Centre, Centro do IMAR da Universidade dos Açores, Rua Prof. Dr. Frederico Machado, n° 4, 9901-862, Horta, Açores, Portugal

    Fernando Tempera

  4. IFREMER, Centre de Bretagne, DYNECO-LEBCO, 29280, Plouzané, France

    Fernando Tempera

  5. Upper Austrian State Museum, Geoscience Collections, Welser Str. 20, 4060, Leonding, Austria

    Björn Berning

  6. Laboratorio de Biología Marina, Universidad de Sevilla, Avenida Reina Mercedes 6, 41012, Sevilla, Spain

    Carlos M. López-Fé

  7. Department of Earth and Environmental Sciences, University of Pavia, Via S. Epifanio 14, 27100, Pavia, Italy

    Anna Occhipinti-Ambrogi

Authors
  1. Joana Micael
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Tempera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Björn Berning
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlos M. López-Fé
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna Occhipinti-Ambrogi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana Cristina Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joana Micael.

Additional information

Communicated by P. Martinez Arbizu

Electronic supplementary material

ESM 1

(DOCX 23 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Micael, J., Tempera, F., Berning, B. et al. Shallow-water bryozoans from the Azores (central North Atlantic): native vs. non-indigenous species, and a method to evaluate taxonomic uncertainty. Mar Biodiv 49, 469–480 (2019). https://doi.org/10.1007/s12526-017-0833-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-017-0833-x

Keywords

Search

Navigation