Skip to main content
Log in

Long-term trend in substratum occupation by a clonal, carbonate bryozoan in a temperate rocky reef in times of thermal anomalies

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

Abstract

Studies over time provide opportunities to detect variations in the spatial and temporal patterns of clonal organisms and measure changes on their population dynamics related to extreme events. We assessed population dynamics for a bryozoan species dominating a subtidal rocky reef at Tino Island, in the eastern Ligurian Sea (NW Mediterranean). Using 9 years of annual photosurveys (1997–2005), rapid decline in Pentapora fascialis colony cover was shown at 11 and 22 m depths following the anomalous warming events in 1999 and 2003. An 86 % reduction in live colony portion was found after the 1999 warming event (2.3 °C higher than normal), with larger colonies being most affected. Effects from the 2003 event were delayed, and gradual cover decline occurred during the following 2 years. At the “Shallow” photostations, none of the larger colonies (>1,000 cm2) survived after the first cover decline. Availability of new substrate after the 1999 disturbance resulted in enhanced recovery through new colony production. At the “Deep” photostations, the population structure did not change over the duration of the monitoring period showing the same monomodal structure and same dominant size class (50–500 cm²). In the 4 years following the first cover decline, the deeper population regained colony cover to levels similar to pre-disturbance level, showing a good resilience. This 9-year monitoring analysis provided the temporal resolution needed to detect changes occurring in the P. fascialis population and will contribute to the assessment of long-term changes on benthic populations suffering during recent decades from dramatic increases in extreme events.

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.

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

Similar content being viewed by others

References

  • Bader B, Schäfer P (2004) Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. J Nat Hist 38:2901–2922

    Article  Google Scholar 

  • Barnes DKA (1995) Seasonal and annual growth in erect species of Antarctic bryozoans. J Exp Mar Biol Ecol 188:181–198

    Article  Google Scholar 

  • Barnes DKA, Webb K, Linse K (2006) Slow growth of Antarctic bryozoans increases over 20 years and is anomalous high in 2003. Mar Ecol Prog Ser 314:187–195

    Article  Google Scholar 

  • Bellwood D, Hughes T, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  CAS  Google Scholar 

  • Bone EK, Keough MJ (2005) Responses to damage in an arborescent bryozoan: effects of injury location. J Exp Mar Biol Ecol 324:127–140

    Article  Google Scholar 

  • Bowden DA, Clarke A, Peck LS, Barnes DKA (2006) Antarctic sessile marine benthos: colonization and growth on artificial substrata over 3 yrs. Mar Ecol Prog Ser 316:1–16

    Article  Google Scholar 

  • Bythell JC, Hillis-Starr ZM, Rogers CS (2000) Local variability but landscape stability in coral reef communities following repeated hurricane impacts. Mar Ecol Prog Ser 204:93–100

    Article  Google Scholar 

  • Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol Lett 3:284–293

    Article  Google Scholar 

  • Cerrano C, Arillo A, Calcinai B, Castellano L, Muti C, Valisano L, Zega G, Bavestrello G (2005) Gorgonian population recovery after a mass mortality event. Aquatic Conserv Mar Freshw Ecosyst 15:147–157

    Article  Google Scholar 

  • Cocito S (2004) Bioconstruction and biodiversity: their mutual influence. Sci Mar 68(1):137–144

    Google Scholar 

  • Cocito S, Ferdeghini F (2001) Carbonate standing stock and carbonate production of the bryozoan Pentapora fascialis in the north-western Mediterranean. Facies 45:25–30

    Article  Google Scholar 

  • Cocito S, Sgorbini S, Bianchi CN (1998) Aspects of the biology of the bryozoan Pentapora fascialis in the north-western Mediterranean. Mar Biol 131:73–82

    Article  Google Scholar 

  • Cocito S, Bedulli D, Sgorbini S (2002) Distribution patterns of the sublittoral epibenthic assemblages on a rocky shoal in the Ligurian Sea (NW Mediterranean). Sci Mar 66(2):175–181

    Article  Google Scholar 

  • Cocito S, Novosel M, Novosel A (2004) Carbonate bioformations around underwater springs in the north-eastern Adriatic Sea. Facies 50:13–17

    Article  Google Scholar 

  • Coma R, Linares C, Ribes M, Diaz D, Garrabou J, Ballesteros E (2006) Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria:Octocorallia) in Menorca (NW Mediterranean). Mar Ecol Prog Ser 51:51–60

    Article  Google Scholar 

  • Connell JH, Keough MJ (1985) Disturbance and patch dynamics of subtidal marine animals on hard substrata. In: Pickett STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Academic Press Inc, London, pp 205–245

    Google Scholar 

  • Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488

    Article  Google Scholar 

  • Cupido R, Cocito S, Sgorbini S, Bordone A, Santangelo G (2008) Response of a gorgonian population to mortality events: recovery or loss? Aquatic Conserv Mar Freshw Ecosyst 18:984–992

    Article  Google Scholar 

  • Cupido R, Cocito S, Barsanti M, Peirano A, Santangelo G (2009) Unexpected long-term population dynamics in a canopy-forming gorgonian following mass mortality. Mar Ecol Prog Ser 394:195–200

    Article  Google Scholar 

  • Edmunds PJ (2004) Juvenile coral population dynamics track rising seawater temperature on a Caribbean reef. Mar Ecol Prog Ser 269:111–119

    Article  Google Scholar 

  • Edmunds PJ, Elahi R (2007) The demographics of a 15-year decline in cover of the Caribbean reef coral Montastrea annularis. Ecol Monogr 77(1):3–18

    Article  Google Scholar 

  • Garrabou J et al (2009) Mass mortality in NW Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103

    Article  Google Scholar 

  • Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63:90–104

    Article  Google Scholar 

  • Hageman SJ (2003) Complexity generated by iteration of hierarchical modules in Bryozoa. Integr Comp Biol 43(1):87–98

    Article  Google Scholar 

  • Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963

    Article  Google Scholar 

  • Hart SP, Keough MJ (2009) Does size predict demographic fate? Modular demography and constraints on growth determine response to decrease in size. Ecology 90(6):1670–1678

    Article  Google Scholar 

  • Hayward PJ, Ryland JS (1975) Growth, reproduction and larval dispersal in Alcyonidium hirsutum (Fleming) and some other Bryozoa. Pubbl Staz Zool Napoli 39(1):226–241

    Google Scholar 

  • Hayward PJ, Ryland JS (1999) Cheilostomatous bryozoa, part 2: Hippothooidea–Celleporoidea. In: Barnes RSK, Crothers JH (eds) Synopses of the British Fauna (New Series). Field Studies Council, Shrewsbury

    Google Scholar 

  • Hughes RN (2005) Lessons in modularity: the evolutionary ecology of colonial invertebrates. Sci Mar 69(1):169–179

    Google Scholar 

  • Hughes TP, Jackson JBC (1980) Do corals lie about their age? Some demographic consequences of partial mortality, fission and fusion. Science 209:713–715

    Article  CAS  Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Article  Google Scholar 

  • Hughes TP et al (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  Google Scholar 

  • Jackson JBC (1979) Morphological strategies of sessile organisms. In: Rosen B, Larwood G (eds) Biology and systematic of colonial animals. Academic Press, London, pp 499–555

    Google Scholar 

  • Linacre NA, Keough MJ (2003) Demographic effects of fragmentation history in modular organisms: illustrated using the bryozoan Mucropetraliella ellerii (MacGillivray). Ecol Model 170(1):61–71

    Article  Google Scholar 

  • Lombardi C, Cocito S, Occhipinti-Ambrogi A, Porter JS (2008) Distribution and morphological variation of colonies of the bryozoan Pentapora fascialis (Bryozoa: Cheilostomata) along the western coast of Italy. J Mar Biol Ass UK 88(4):711–717

    Google Scholar 

  • Lombardi C, Gambi MC, Vasapollo C, Taylor PT, Cocito S (2011a) Skeletal alterations and polymorphism in a Mediterranean bryozoan at natural CO2 vents. Zoomorphology 130:135–145

    Article  Google Scholar 

  • Lombardi C, Cocito S, Gambi MC, Cisterna B, Flach F, Taylor PD, Keltie K, Freer A, Cusack M (2011b) Effects of ocean acidification on growth, organic tissue and protein profile of the Mediterranean bryozoan Myriapora truncata. Aquatic Biol 13:251–262

    Article  Google Scholar 

  • Lombardi C, Taylor PD, Cocito S (2013) Bryozoan constructions in a changing Mediterranean Sea. In: Goffredo S, Dubinsky I (eds) The Mediterranean Sea: its history and present challenges. Springer ISBN 978-94-007-6703-4 (in press)

  • Maughan BC, Barnes DKA (2000) Seasonality of competition in early development of subtidal encrusting communities. Mar Ecol 21:205–220

    Article  Google Scholar 

  • McKinney FK, Jackson JBC (1989) Bryozoan life histories. In: McKinney FK, Jackson JBC (eds) Bryozoan evolution. University of Chicago Press, Chicago, pp 97–119

    Google Scholar 

  • Mustapha BK, Komatsu T, Hattour A, Sammari CH, Zarrouk S (2002) Bionomie des étages infra et circalittoral du golfe de Gabès. Bull Inst Nat Sci Techn Mer Salambò 29:1–16

    Google Scholar 

  • Novosel M (2005) Bryozoans of the Adriatic Sea. Denisia 16. Landesmuseen Neue Serie 28:231–246

    Google Scholar 

  • Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P, Vacelet J (2000) Mass mortality of marine invertebrates: an unprecedented event in the Northwestern Mediterranean. Compt Rend Acad Sci Sci Vie 323:853–865

    CAS  Google Scholar 

  • Pisano E, Boyer M (1985) Development of an infralittoral bryozoan community in the western Mediterranean Sea. Mar Ecol Prog Ser 27:195–202

    Article  Google Scholar 

  • Relini G, Zamboni N, Tixi F, Torchia G (1994) Patterns of sessile macrobenthos community development on an artificial reef in the Gulf of Genoa (northwestern Mediterranean). Bull Mar Sci 55:745–771

    Google Scholar 

  • Rodolfo-Metalpa R, Lombardi C, Cocito S, Hall-Spencer JM, Gambi MC (2010) Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar Ecol Evol Persp 31:447–456

    CAS  Google Scholar 

  • Sebens KP (1987) The ecology of indeterminate growth in animals. A Rev Ecol Syst 18:371–407

    Article  Google Scholar 

  • Smith AM (2007) Age, growth and carbonate production by erect rigid bryozoans in Antarctica. Palaeogeogr Palaeoclimatol Palaeoecol 256(1–2):86–98

    Article  Google Scholar 

  • Smith LD, Hughes TP (1999) An experimental assessment of survival, re-attachment and fecundity of coral fragments. J Exp Mar Biol Ecol 235:147–164

    Article  Google Scholar 

  • Smith AM, Stewart B, Key Jr MM, Jamet CM (2001) Growth and carbonate production by Adeonellopsis (Bryozoa: Cheilostomata) in Doubtful Sound, New Zealand. Palaeogeogr Palaeoclimatol Palaeoecol 175:201–210

    Article  Google Scholar 

  • Stebbing ARD (1971) Growth of Flustra foliacea (Bryozoa). Mar Biol 9:267–273

    Article  Google Scholar 

  • Tanner JE (2001) The influence of clonality on demography: patterns in expected longevity and survivorship. Ecology 82(7):1971–1981

    Article  Google Scholar 

  • Taylor PD, Wilson MA (2003) Palaeoecology and evolution of marine hard substrate communities. Earth-Science Rev 62:1–103

    Article  Google Scholar 

  • Teixidó N, Pineda MC, Garrabou J (2009) Decadal demographic trends of a long-lived temperate encrusting sponge. Mar Ecol Prog Ser 375:113–124

    Article  Google Scholar 

  • Teixidó N, Casas E, Cebrian E, Linares C, Garrabou J (2013) Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 8(1):e53742

    Article  Google Scholar 

  • Todd CD, Turner SJ (1986) Ecology of intertidal and sublittoral cryptic epifaunal assemblages. I. Experimental rationale and the analysis of larval settlement. J Exp Mar Biol Ecol 99:199–231

    Article  Google Scholar 

  • Watson DI, Barnes DKA (2004) Temporal and spatial components of variability in benthic recruitment, a 5-year temperate example. Mar Biol 145:201–214

    Article  Google Scholar 

  • Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Change Biol 12:2220–2234

    Article  Google Scholar 

  • Wood ACL, Probert PK, Rowden AA, Smith AM (2012) Complex habitat generated by marine bryozoans: a review of its distribution, structure, diversity, threats and conservation. Aquatic Conserv Mar Fresh Ecosys 22:547–563

    Article  Google Scholar 

  • Woodley JD et al (1981) Hurricane Allen’s impact on Jamaican coral reefs. Science 214:749–755

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors dedicated this paper to late M. Lorenzetti (Submariner, La Spezia) and late M. Morgigni (Lucca) that provided valuable field assistance. Authors are grateful to two anonymous reviewers for their constructive comments on this paper. We thank N.M. Lucey (Cambridge, Massachusetts) for her revision of the English text.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Cocito.

Additional information

Communicated by S. Connell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cocito, S., Sgorbini, S. Long-term trend in substratum occupation by a clonal, carbonate bryozoan in a temperate rocky reef in times of thermal anomalies. Mar Biol 161, 17–27 (2014). https://doi.org/10.1007/s00227-013-2310-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2310-9

Keywords

Navigation