Skip to main content
SpringerLink
Log in

Sexual reproduction in the invasive bryozoan Amathia verticillata (Ctenostomatida: Vesiculariidae)

  • Published:
Journal of Coastal Conservation Aims and scope Submit manuscript

Abstract

The invasive bryozoan Amathia verticillata has been associated with native biodiversity and economic losses around the world and in 2009, it was detected on one island of the Azores Archipelago and has since spread to other islands. The present study provides insights into the reproductive strategies of this species through the analysis of brooded embryos, the number of internodes and the degree of colony branching over a one year period in more than 200 colonies. These remote oceanic islands provide good environmental conditions for A. verticillata to diversify its gene pool, since the species is able to carry out sexual reproduction year-round. In contrast, population dynamics of A. verticillata seem to be strongly correlated with changes in temperature and the local photoperiod. Field intervention aimed at reducing the population in affected areas should be conducted in the winter when the number of potential colonizing fragments that might be generated by intervention is smaller.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 58:761–776

    Article  Google Scholar 

  • Beck SD (1968) Insect photoperiodism. Academic Press, New York

    Google Scholar 

  • Bock PE (1982) Bryozoans (Phylum Bryozoa or Ectoprocta). In: Shepherd SA, Thomas IM (eds) Marine invertebrates of Southern Australia, part I. South Australian Government Printer, Adelaide, pp 319–394

    Google Scholar 

  • Bullivant JS (1968) The rate of feeding of the bryozoan, Zoobotryon verticillatum. NZJ Mar Freshw Res 2:111–134

    Article  Google Scholar 

  • Carlton JT (1999) The scale and ecological consequences of biological invasions in the World’s oceans. In: Sandlund OT, Schei PJ, Viken A (eds) Invasive species and Biodiversity Management. Kluwer Academic Publishers, Dordrecht, pp 195–212

    Chapter  Google Scholar 

  • Carlton JT, Eldredge LG (2009) The introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian Archipelago. Bishop Mus Bull Cult Environ St 4:1–203

    Google Scholar 

  • Chainho P, Fernandes A, Amorim A, Ávila SP, Canning-Clode J, Castro J, Costa A, Costa JL, Cruz T, Gollasch S, Grazziotin-Soares C, Melo R, Micael J, Parente M, Semedo J, Silva T, Sobral D, Sousa M, Torres P, Veloso V, Costa MJ (2015) Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries, and islands. Estuar Coast Shelf Sci. https://doi.org/10.1016/j.ecss.2015.06.019

  • Cheetham AH, Jackson JBC, Sanner J (2001) Evolutionary significance of sexual and asexual modes of propagation in Neogene species of the bryozoan Metrarabdotos in tropical America. J Paleontol 75:564–577

    Article  Google Scholar 

  • Coleman FS (1999) Note on Zoobotryon verticillatum (Bryozoa) in a solar saltfield. Int J Salt Lake Res 8:71–74

    Google Scholar 

  • Cook PL (1985) Bryozoa from Ghana, a preliminary survey. Ann Mus R Afr Cent Sci Zool Tervuren 238:1–315

    Google Scholar 

  • Edyvean R (2010) Consequences of fouling on shipping. In: Dürr S, Thomason JC (eds) Biofouling. Wiley-Blackwell, Oxford, pp 217–223

    Google Scholar 

  • Eggleston D (1972) Patterns of reproduction in the marine Ectoprocta of the Isle of Man. J Nat Hist 6:31–38

    Article  Google Scholar 

  • Farrapeira CMR (2011) The introduction of the bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) in northeast of Brazil: A cause for concern. Biol Invasions 13:13–16

    Article  Google Scholar 

  • Galil BS, Gevili R (2014) Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar Biodivers Rec 7:e17. https://doi.org/10.1017/S1755267214000086

    Article  Google Scholar 

  • Ganapati PN, Rao KS (1968) Fouling bryozoans in Visakhapatnam Harbour. Curr Sci 37:81–83

    Google Scholar 

  • Geiger DL, Zimmer RL (2002) Anchoring rootlets in Bowerbankia imbricata (Bryozoa: Ctenostomata). Bull Mar Sci 70:791–797

    Google Scholar 

  • Gillon A, Costa AC, Micael J (2017) Caprella scaura Templeton, 1836, an invasive caprellid new to the Azores Archipelago. Mar Biodivers 47:499–510

    Article  Google Scholar 

  • Gitay A, Glazer A (1979) Biological fouling in Israel power stations and in a proposed inter-sea conduit. Israel J Zool 28(1):61

    Google Scholar 

  • Godwin LS (2003) Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling 19:123–131

    Article  Google Scholar 

  • Gossett L, Lester J, Gonzalez L (2004) Galveston Bay Invasive Species Risk Assessment, Final Report. Prepared for Galveston Bay Estuary Program. Texas Commission on Environmental Quality, Webster

    Google Scholar 

  • Hayward P (1985) Ctenostome Bryozoans. Keys and notes for the identification of the species. Synopses of the British fauna (new series), 33. Brill EJ, Backhuys W, London

  • IH – Instituto Hidrográfico (2010) Roteiro da costa de Portugal Arquipélago dos Açores Vol I - Grupos Oriental e Ocidental (3th Ed). Ministério da Defesa Nacional, Marinha

  • Je JG, Hong JS, Yi SK (1988) A study on the fouling organisms in the pearl oyster culture grounds in the southern coast of Korea. Ocean Res (Seoul) 10:85–105

    Google Scholar 

  • Keough M (1989) Variation in Growth Rate and Reproduction of the Bryozoan Bugula neritina. Biol Bull 177(2):277–286

    Article  Google Scholar 

  • Marchini A, Ferrario J, Minchin D (2015) Marinas may act as hubs for the spread of the pseudo-indigenous bryozoan Amathia verticillata (Delle Chiaje, 1822) and its associates. Sci Mar 73:355–365

    Article  Google Scholar 

  • Marchini A, Costa AC, Ferrario J, Micael J (2017) The global invader Paracerceis sculpta (Isopoda: Sphaeromatidae) has extended its range to the Azores Archipelago. Mar Biodivers. https://doi.org/10.1007/s12526-017-0674-7

  • McCann L, Keith I, Carlton JT, Ruiz GM, Dawson TP, Collins K (2015) First record of the non-native bryozoan Amathia (= Zoobotryon) verticillata (delle Chiaje, 1822) (Ctenostomata) in the Galapagos Islands. Bioinvas Rec 4:255–260

    Article  Google Scholar 

  • McKinney FK (1983) Asexual colony multiplication by fragmentation: an important mode of genet longevity in the Carboniferous bryozoan Archimedes. Paleobiology 9:35–43

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Micael J, Jardim N, Núñez C, Occhipinti-Ambrogi A, Costa AC (2017) Some Bryozoa species recently introduced into the Azores: reproductive strategies as a proxy for further spread. Helgol Mar Res 70:1–10

    Google Scholar 

  • Minchin D (2012) Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar Pollut Bull 64:2146–2150

    Article  Google Scholar 

  • Minchin D, Liu T-K, Cheng M (2016) First record of the bryozoan Amathia (=Zoobotryon) verticillata (Bryozoa: Vesiculariidae) from Taiwan. Pac Sci 70:509–518

    Article  Google Scholar 

  • Nair PSR, Krishnamurthy K (1992) Salinity tolerance in four estuarine species of bryozoan. Mar Foul 9:15–20

    Article  Google Scholar 

  • Nandakumar K (1996) Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms. Mar Ecol Prog Ser 131:191–203

    Article  Google Scholar 

  • O’Leary C, Anderson CD (2003) A new hull roughness penalty calculator, International Marine Coatings. Available from http://www.international-marine.com/foulingcontrol/hull-roughness.aspx. Accessed 13 June 2017

  • Relini G (1966) Le comunità dominanti nel ‘fouling’ portuale di Genova. Natura 57:136–156

    Google Scholar 

  • Robinson NM (2004) Interactions between the nudibranch Okenia zoobotryon and its bryozoan prey Zoobotryon verticillatum. Thesis (Master of Science in Biology), University of Central Florida, Orlando

  • Ryland JS (1965) Catalogue of main fouling organisms (found on ships coming into European waters), vol 2. Polyzoa. Organization for Economic Co-operation and Development, Paris

    Google Scholar 

  • Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98

    Article  Google Scholar 

  • Strahler AN (1957) Quantitative analysis of watershed geomorphology. EOS Trans Am Geophys Union 38:913–920

    Article  Google Scholar 

  • Thomsen E, Hakansson E (1995) Sexual Versus Asexual Dispersal in Clonal Animals: Examples from Cheilostome Bryozoans. Paleobiology 21:496–508

    Article  Google Scholar 

  • Williams SL (2007) Introduced species in seagrass ecosystems: Status and concerns. J Exp Mar Biol Ecol 350:89–110

    Article  Google Scholar 

  • Winston JE (1983) Patterns of growth, reproduction and mortality in bryozoans from the Ross Sea, Antarctica. Bull Mar Sci 33:688–702

    Google Scholar 

  • Winston JE (1995) Ectoproct diversity of the Indian River coastal lagoon. Bull Mar Sci 57:84–93

    Google Scholar 

  • Wirtz P, Canning-Clode J (2009) The invasive bryozoan Zoobotryon verticillatum has arrived at Madeira Island. Aquat Invasions 4:669–670

    Article  Google Scholar 

  • Zimmer RL, Woollacott RM (1977) Metamorphosis, ancestrula, and coloniality in bryozoan life cycles. In: Woollacott RM, Zimmer RL (eds) Biology of Bryozoans. Academic, New York, pp 91–142

    Chapter  Google Scholar 

  • Zirpolo G (1933) Zoobotryon verticillatum (Delle Chiaje), Memorie dell’Academia Pontifica dei Nuovi Lincei 2(17):109–442

Download references

Acknowledgements

The authors would like to thank Professor Richard Billington for improving the English on the manuscript. This project was funded by the Direcção Regional de Ciência e Tecnologia (DRCT) - ‘Açores: Stopover for Marine Alien Species?’ – ASMAS - M2.1.2/I/032/2011 and also by FEDER funds through the Operational Programme for Competitiveness Factors – COMPETE and by Portuguese National Funds through FCT–Foundation for Science and Technology under the UID/BIA/50027/2013 and POCI-01-0145-FEDER-006821. P. R. was supported by FONDECYT 3150617.

Author information

Authors and Affiliations

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

    J. Micael

  2. Departamento de Biologia, Universidade dos Açores, 9501-801, Ponta Delgada, Portugal

    A. Gillon & N. Jardim

  3. Instituto de Patología Animal, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Edificio Federico Saelzer, 3rd floor, Campus Isla Teja, 59000, Valdivia, Chile

    Pedro Rodrigues

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

    A. C. Costa

Authors
  1. J. Micael
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Gillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Jardim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pedro Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. C. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro Rodrigues.

Electronic supplementary material

ESM 1

(DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Micael, J., Gillon, A., Jardim, N. et al. Sexual reproduction in the invasive bryozoan Amathia verticillata (Ctenostomatida: Vesiculariidae). J Coast Conserv 22, 305–314 (2018). https://doi.org/10.1007/s11852-017-0577-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11852-017-0577-6

Keywords

Search

Navigation