Proof of concept for measuring growth of shelf marine calcifiers: ‘a Bryozoan odyssey’

Katerina Achilleos; Abigail M. Smith

doi:10.1071/MF23114

RESEARCH ARTICLE (Open Access)

Previous Contents Vol 74(14)

Proof of concept for measuring growth of shelf marine calcifiers: ‘a Bryozoan odyssey’

Katerina Achilleos

^A ^* and Abigail M. Smith ^A

+ Author Affiliations

- Author Affiliations

^A Department of Marine Science, University of Otago, PO Box 56, Dunedin 9054, New Zealand.

^* Correspondence to: katerina.achilleos@otago.ac.nz

Handling Editor: Man Ying Jill Chiu

Marine and Freshwater Research 74(14) 1262-1273 https://doi.org/10.1071/MF23114
Submitted: 6 April 2023 Accepted: 22 August 2023 Published: 8 September 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

The variation observed in growth rate estimates of bryozoans raise questions regarding the validity of the methods used to measure growth in these animals. Naturally, the best way for measuring growth rate is to understand the growth in situ, but access is not always straightforward.

Aims

This study assesses a field experiment for measuring in situ growth of heavily calcified bryozoans in the open ocean at 56 m, the deepest such deployment attempted for bryozoans.

Methods

Cellaria immersa colonies were collected by dredge from the continental shelf off Otago, marked using calcein, mounted on a purpose-built frame, called ‘Odyssey’, and returned to the shelf for 3 months in the Austral summer (November–February).

Key results

Data from 10 internodes indicated that growth was, on average, 0.97 ± 0.84 mm year⁻¹ and showed some interesting intracolonial growth patterns.

Conclusions and implications

The data obtained from this study are only indicative at this stage, but we have succeeded in developing a reproducible experimental set-up for in situ growth experiments of shelf bryozoans, enabling us to record growth, lifespan, and calcification rates of heavily calcified and ecologically important species. Understanding such key species is critical to identifying their role in the ecosystem and providing valuable information for future conservation initiatives.

Keywords: bryozoans, calcein, Cellaria, continental shelf, experimental set-up, growth rate, in situ, marine calcifiers, mark–recapture.

References

Achilleos K, Smith AM, Gordon DP (2019) The articulated bryozoan genus Cellaria in the southern Zealandian region: distribution and associated fauna. Marine Biodiversity 49, 2801-2812.
| Crossref | Google Scholar |

Achilleos K, Gordon DP, Smith AM (2020) Cellaria (Bryozoa, Cheilostomata) from the deep: new species from the southern Zealandian region. Zootaxa 4801(2), 201-236.
| Crossref | Google Scholar |

Achilleos K, Jimenez C, Petrou A (2022) Wreck site formation process: the use of Bryozoans. In ‘The Kyrenia ship final excavation report, Volume I: history of the excavation, amphoras, pottery and coins as evidence for dating’. (Eds SW Katsev, LW Swiney) pp. 242–248. (Oxbow Books: Oxford, UK)

Amui-Vedel A-M, Hayward PJ, Porter JS (2007) Zooid size and growth rate of the bryozoan Cryptosula pallasiana Moll in relation to temperature, in culture and in its natural environment. Journal of Experimental Marine Biology and Ecology 353(1), 1-12.
| Crossref | Google Scholar |

Bader B (2001) Modern bryomol-sediments in a cool-water, high-energy setting: the inner shelf off Northern Brittany. Facies 44(1), 81-103.
| Crossref | Google Scholar |

Bader B, Schäfer P (2004) Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. Journal of Natural History 38(22), 2901-2922.
| Crossref | Google Scholar |

Bader B, Schäfer P (2005) Impact of environmental seasonality on stable isotope composition of skeletons of the temperate bryozoan Cellaria sinuosa. Palaeogeography, Palaeoclimatology, Palaeoecology 226(1–2), 58-71.
| Crossref | Google Scholar |

Barnes DKA, Clarke A (1998) Seasonality of polypide recycling and sexual reproduction in some erect Antarctic bryozoans. Marine Biology 131(4), 647-658.
| Crossref | Google Scholar |

Barnes DKA, Webb K, Linse K (2006) Slow growth of Antarctic bryozoans increases over 20 years and is anomalously high in 2003. Marine Ecology Progress Series 314, 187-195.
| Crossref | Google Scholar |

Bastos AC, Moura RL, Moraes FC, Vieira LS, Braga JC, Ramalho LV, Amado-Filho GM, Magdalena UR, Webster JM (2018) Bryozoans are major modern builders of south Atlantic oddly shaped reefs. Scientific Reports 8(1), 9638.
| Crossref | Google Scholar | PubMed |

Batson PB, Tamberg Y, Taylor PD, Gordon DP, Smith AM (2020) Skeletal resorption in bryozoans: occurrence, function and recognition. Biological Reviews 95(5), 1341-1371.
| Crossref | Google Scholar | PubMed |

Bernal MA, Schunter C, Lehmann R, Lightfoot DJ, Allan BJM, Veilleux HD, Rummer JL, Munday PL, Ravasi T (2020) Species-specific molecular responses of wild coral reef fishes during a marine heatwave. Science Advances 6(12), eaay3423.
| Crossref | Google Scholar |

Brey T, Gerdes D, Gutt J, Mackensen A, Starmans A (1999) Growth and age of the Antarctic bryozoan Cellaria incula on the Weddell Sea shelf. Antarctic Science 11(4), 408-414.
| Crossref | Google Scholar |

Camp EF, Krause S-L, Santos LMF, Naumann MS, Kikuchi RKP, Smith DJ, Wild C, Suggett DJ (2015) The “Flexi-Chamber”: a novel cost-effective in situ respirometry chamber for coral physiological measurements. PLoS ONE 10(10), e0138800.
| Crossref | Google Scholar | PubMed |

Gissi E, Manea E, Mazaris AD, Fraschetti S, Almpanidou V, Bevilacqua S, Coll M, Guarnieri G, Lloret-Lloret E, Pascual M, Petza D, Rilov G, Schonwald M, Stelzenmüller V, Katsanevakis S (2021) A review of the combined effects of climate change and other local human stressors on the marine environment. Science of The Total Environment 755, 142564.
| Crossref | Google Scholar | PubMed |

Hart SP, Keough MJ (2009) Does size predict demographic fate? Modular demography and constraints on growth determine response to decreases in size. Ecology 90(6), 1670-1678.
| Crossref | Google Scholar | PubMed |

Hirose M, Ide A, Shirai K (2020) The growth of Celleporina attenuata estimated based on the oxygen isotopic compositions and microfocus X-ray CT imaging analysis. In ‘Bryozoan Studies 2019’. (Eds PW Jackson, K Zágoršek) pp. 69–82. (Czech Geological Society: Prague, Czech Republic)

Key MM Jr. (2020) Estimating colony age from colony size in encrusting cheilostomes. In ‘Bryozoan studies 2019’. (Eds PW Jackson, K Zágoršek) pp. 83–90. (Czech Geological Society: Prague, Czech Republic)

Key MM, Jr., Jackson PNW, Falvey LW, Roth BJ (2014) Use of fossil bryozoans in sourcing lithic artifacts. Geoarchaeology 29(5), 397-409.
| Crossref | Google Scholar |

Key MM, Jr, Rossi RK, Smith AM, Hageman SJ, Patterson WP (2018) Stable isotope profiles of skeletal carbonate validate annually-produced growth checks in the bryozoan Melicerita chathamensis from Snares Platform, New Zealand. Bulletin of Marine Science 94(4), 1447-1464.
| Crossref | Google Scholar |

Lartaud F, Pareige S, de Rafelis M, Feuillassier L, Bideau M, Peru E, Romans P, Alcala F, Le Bris N (2013) A new approach for assessing cold-water coral growth in situ using fluorescent calcein staining. Aquatic Living Resources 26(2), 187-196.
| Crossref | Google Scholar |

Lartaud F, Meistertzheim AL, Peru E, Le Bris N (2017) In situ growth experiments of reef-building cold-water corals: the good, the bad and the ugly. Deep Sea Research Part I: Oceanographic Research Papers 121, 70-78.
| Crossref | Google Scholar |

Laverick JH, Green TK, Burdett HL, Newton J, Rogers AD (2019) Depth alone is an inappropriate proxy for physiological change in the mesophotic coral Agaricia lamarcki. Journal of the Marine Biological Association of the United Kingdom 99(7), 1535-1546.
| Crossref | Google Scholar |

Li S, Liu C, Huang J, Liu Y, Zheng G, Xie L, Zhang R (2015) Interactive effects of seawater acidification and elevated temperature on biomineralization and amino acid metabolism in the mussel Mytilus edulis. Journal of Experimental Biology 218(22), 3623-3631.
| Crossref | Google Scholar |

Lombardi C, Cocito S, Occhipinti-Ambrogi A, Hiscock K (2006) The influence of seawater temperature on zooid size and growth rate in Pentapora fascialis (Bryozoa: Cheilostomata). Marine Biology 149(5), 1103-1109.
| Crossref | Google Scholar |

Lombardi C, Rodolfo-Metalpa R, Cocito S, Gambi MC, Taylor PD (2011) Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO₂ simulating ocean acidification. Marine Ecology 32(2), 211-221.
| Crossref | Google Scholar |

Lonhart SI (2012) Growth and distribution of the invasive bryozoan Watersipora in Monterey Harbor, California. In ‘Diving For Science 2012. Proceedings of the American Academy of Underwater Sciences 31st Scientific Symposium’. (Eds DL Steller, LK Lobel) pp. 89–98. (American Academy of Underwater Sciences: Dauphin Island, AL, USA)

Lukasik JJ, James NP, McGowran B, Bone Y (2000) An epeiric ramp: low-energy, cool-water carbonate facies in a Tertiary inland sea, Murray Basin, South Australia. Sedimentology 47(4), 851-881.
| Crossref | Google Scholar |

Magnabosco G, Polishchuk I, Erez J, Fermani S, Pokroy B, Falini G (2018) Insights on the interaction of calcein with calcium carbonate and its implications in biomineralization studies. CrystEngComm 20(30), 4221-4224.
| Crossref | Google Scholar |

Mahé K, Bellamy E, Lartaud F, de Rafélis M (2010) Calcein and manganese experiments for marking the shell of the common cockle (Cerastoderma edule): tidal rhythm validation of increments formation. Aquatic Living Resources 23(3), 239-245.
| Crossref | Google Scholar |

McKinney FK, Jaklin A (2000) Spatial niche partitioning in the Cellaria meadow epibiont association, northern Adriatic Sea. Cahiers de Biologie Marine 41(1), 1-17.
| Google Scholar |

McKinney FK, Jaklin A (2001) Sediment accumulation in a shallow-water meadow carpeted by a small erect bryozoan. Sedimentary Geology 145, 397-410.
| Crossref | Google Scholar |

Mello HL, Gordon DP, Ryland JS, Smith AM (2023) Protecting the small: preliminary investigation of bryozoan community change in New Zealand’s oldest marine reserve. New Zealand Journal of Marine and Freshwater Research 57, 425-437.
| Crossref | Google Scholar |

Ostrovsky AN (2013a) From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates. Evolution 67(5), 1368-1382.
| Crossref | Google Scholar | PubMed |

Ostrovsky AN (2013b) ‘Evolution of sexual reproduction in marine invertebrates. Example of gymnolaemate bryozoans.’ (Springer: Dordrecht, Netherlands)

Pätzold J, Ristedt H, Wefer G (1987) Rate of growth and longevity of a large colony of Pentapora foliacea (Bryozoa) recorded in their oxygen isotope profiles. Marine Biology 96(4), 535-538.
| Crossref | Google Scholar |

Riisgård HU, Manríquez P (1997) Filter-feeding in fifteen marine ectoprocts (Bryozoa): particle capture and water pumping. Marine Ecology Progress Series 154, 223-239.
| Crossref | 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. Marine Ecology 31(3), 447-456.
| Crossref | Google Scholar |

Schack CR, Gordon DP, Ryan KG (2018) Classification of cheilostome polymorphs. In ‘Annals of bryozoology 6: aspects of the history of research on bryozoans’. (Eds PNW Jackson, MES Jones) pp. 85–134. (International Bryozoology Association: Dublin, Republic of Ireland)

Schafer P, Bader B, Blaschek H (2006) Morphology and function of the flexible nodes in the cheilostome bryozoan Cellaria sinuosa (Hassall). Courier Forschungsinstitut Senckenberg 257, 119-131.
| Google Scholar |

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9(7), 676-682.
| Crossref | Google Scholar | PubMed |

Smith AM (1995) Palaeoenvironmental interpretation using bryozoans: a review. Geological Society, London, Special Publications 83(1), 231-243.
| Crossref | Google Scholar |

Smith AM (2007) Age, growth and carbonate production by erect rigid bryozoans in Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 256(1–2), 86-98.
| Crossref | Google Scholar |

Smith AM (2014) Growth and calcification of marine bryozoans in a changing ocean. The Biological Bulletin 226(3), 203-210.
| Crossref | Google Scholar | PubMed |

Smith AM, Key MM, Jr. (2004) Controls, variation, and a record of climate change in detailed stable isotope record in a single bryozoan skeleton. Quaternary Research 61(2), 123-133.
| Crossref | Google Scholar |

Smith AM, Key JM Jr. (2020) Growth geometry and measurement of growth rates in marine bryozoans: a review. In ‘Bryozoan Studies 2019’. (Eds PW Jackson, K Zágoršek) pp. 139–156. (Czech Geological Society: Prague, Czech Republic)

Smith AM, Lawton EI (2010) Growing up in the temperate zone: age, growth, calcification and carbonate mineralogy of Melicerita chathamensis (Bryozoa) in southern New Zealand. Palaeogeography, Palaeoclimatology, Palaeoecology 298(3–4), 271-277.
| Crossref | Google Scholar |

Smith AM, Stewart B, Key MM, Jr., Jamet CM (2001) Growth and carbonate production by Adeonellopsis (Bryozoa: Cheilostomata) in Doubtful Sound, New Zealand. Palaeogeography, Palaeoclimatology, Palaeoecology 175(1–4), 201-210.
| Crossref | Google Scholar |

Smith AM, Key MM, Wood ACL (2019) Culturing large erect shelf bryozoans: skeletal growth measured using calcein staining in culture. Australasian Palaeontological Memoirs 52, 131-138.
| Google Scholar |

Smith AM, Batson PB, Achilleos K, Tamberg Y (2022) Collecting and culturing bryozoans for regenerative studies. In ‘Whole-body regeneration: methods and protocols’. (Eds S Blanchoud, B Galliot) pp. 151–177. (Humana: New York, NY, USA) 10.1007/978-1-0716-2172-1_8

Spires JE, North EW (2022) Marking the shells of juvenile and adult eastern oysters, Crassostrea virginica, with the fluorochrome dye calcein and measuring growth and mortality after marking. Journal of Molluscan Studies 88(1), eyac004.
| Crossref | Google Scholar |

Suggett DJ, Dong LF, Lawson T, Lawrenz E, Torres L, Smith DJ (2013) Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32(2), 327-337.
| Crossref | Google Scholar |

Swezey DS, Bean JR, Ninokawa AT, Hill TM, Gaylord B, Sanford E (2017a) Interactive effects of temperature, food and skeletal mineralogy mediate biological responses to ocean acidification in a widely distributed bryozoan. Proceedings of the Royal Society B: Biological Sciences 284(1853), 20162349.
| Crossref | Google Scholar |

Swezey DS, Bean JR, Hill TM, Gaylord B, Ninokawa AT, Sanford E (2017b) Plastic responses of bryozoans to ocean acidification. Journal of Experimental Biology 220(23), 4399-4409.
| Crossref | Google Scholar |

Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D (2012) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proceedings of the Royal Society B: Biological Sciences 279(1726), 19-27.
| Crossref | 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 Conservation: Marine and Freshwater Ecosystems 22(4), 547-563.
| Crossref | Google Scholar |

Wood ACL, Rowden AA, Compton TJ, Gordon DP, Probert PK (2013) Habitat forming bryozoans in New Zealand: their known and predicted distribution in relation to broad-scale environmental variables and fishing effort. PLoS ONE 8(9), e75160.
| Crossref | Google Scholar | PubMed |