Abstract
Pelagic biofoulers such as barnacles or bryozoans settle and raft on natural debris like pumice or seeds. Recent influxes of marine debris into the world’s oceans, especially plastic, have increased habitat availability for these biofoulers. Goose barnacles in the genus Lepas are some of the most common biofouling taxa globally, and play an important role in biofouling communities as foundation species. We examined community succession, growth rates and isotopic composition in Lepas and their associated biofouling communities in coastal waters of eastern Australia. Community succession on a fixed surface mooring showed an increase in species diversity over 25 weeks. Using the abundances of L. anserifera, L. anatifera, and the amphipods Caprella danilevskii and Jassa slatteryi, we created an equation to estimate minimum duration at sea. Predators such as the polychaete Amphinome rostrata may influence the biofouling community, as can beach scavengers once floating debris is cast ashore. We report a new maximum growth rate for L. anserifera of 1.45 mm−1, and our study is the first to report growth rates for any species of Lepas faster than 1 mm day−1. Lepas were larger on moored floats than on smaller, free-floating drifters. δ18O content of Lepas shells was a robust predictor of sea surface temperatures during formation for L. anatifera and L. anserifera. Our findings have important applications for estimating drift duration and trajectories of marine debris.
Graphic abstract
Similar content being viewed by others
Availability of data and material
The datasets generated during and/or analysed during the current study are available at https://github.com/tmesaglio/Lepas-Marine-Forensic-Tool
Code availability
All code is available at https://github.com/tmesaglio/Lepas-Marine-Forensic-Tool
References
Ahyong ST, Wilkens SL (2011) Aliens in the Antipodes: non-indigenous Crustacea in New Zealand and Australia. In: Galil BS, Clark PF, Carlton JT (eds) In the Wrong Place: Alien Marine Crustaceans – Distribution, Biology and Impacts. Springer Verlag, Heidelberg, pp 451–485
Anderson GS (2009) Decomposition and invertebrate colonization of cadavers in coastal marine environments. In: Amendt J, Lee Goff M, Campobasso CP, Grassberger M (eds) Current Concepts in Forensic Entomology. Springer, Dordrecht, pp 223–272
Astudillo JC, Bravo M, Dumont CP, Thiel M (2009) Detached aquaculture buoys in the SE Pacific: potential dispersal vehicles for associated organisms. Aquat Biol 5:219–231
Barnes DK, Sanderson WG (2000) Latitudinal patterns of colonization of marine debris. In Proceedings of the 11th international Bryozoology Association conference. Smithsonian Tropical Research Institute, Chicago, pp 154–160
Barnes DK (2002) Invasions by marine life on plastic debris. Nature 416:808–809
Barnes DK (2014) Marine plastic debris and colonization by bryozoans in the south Atlantic. CIESM Workshop Monographs 46:69–78
Barreiros JP, Teves M (2005) The sunfish Mola mola as an attachment surface for the lepadid cirriped Lepas anatifera: a previously unreported association. Aqua-Int J Ichthyol 10:1–4
Bieri R (1966) Feeding preferences and rates of the snail, Ianthina prolongata, the barnacle, Lepas anserifera, the nudibranchs, Glaucus atlanticus and Fiona pinnata, and the food web in the marine neuston. P Seto Mar Biol Lab 14:161–170
Blamart D, Bassinot F (2016) Rapport d’expertise: Estimation des températures de croissance des valves de cirripèdes fixes sur le flaperon du vol MH370 à partir de l’analyse de leur composition isotopique 18O/16O. Report to the ‘Tribunal de Grande Instance de Paris’
Bravo M, Astudillo JC, Lancellotti D, Luna-Jorquera G, Valdivia N, Thiel M (2011) Rafting on abiotic substrata: properties of floating items and their influence on community succession. Mar Ecol Prog 439:1–17
Bureau of Meteorology (BOM) (2019). Greater Sydney in February 2019: warm days, mild nights and dry. Australian Government. http://www.bom.gov.au/climate/current/month/nsw/archive/201902.sydney.shtml. Accessed 18 April 2020
Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer-Verlga, New York
Carlton JT, Fowler AE (2018) Ocean rafting and marine debris: a broader vector menu requires a greater appetite for invasion biology research support. Aquat Invasions 13:11–15
Carlton JT, Chapman JW, Geller JB, Miller JA, Carlton DA, McCuller MI, Treneman NC, Steves BP, Ruiz GM (2017) Tsunami-driven rafting: Transoceanic species dispersal and implications for marine biogeography. Science 357:1402–1406
Carlton JT, Chapman JW, Geller JB, Miller JA, Ruiz GM, Carlton DA, McCuller MI, Treneman NC, Steves BP, Breitenstein RA, Lewis R (2018) Ecological and biological studies of ocean rafting: Japanese tsunami marine debris in North America and the Hawaiian Islands. Aquat Invasions 13:1–9
Christensen RHB (2019) ordinal - Regression Models for Ordinal Data. R package version 2019.4–25. http://www.cran.r-project.org/package=ordinal/
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Earlbaum Associates, Hillsdale
de Graaf F (1952) Some Notes on the Genus Lepas Linné, 1767. (Subphylum Crustacea; Classis Cirripedia; Ordo Thoracica; Fam. Lepadidae.). Beaufortia 1:1–6
Dellinger T, Davenport J, Wirtz P (1997) Comparisons of social structure of Columbus crabs living on loggerhead sea turtles and inanimate flotsam. J Mar Biolog Assoc 77:185–194
DeLong KL, Quinn TM, Taylor FW (2007) Reconstructing twentieth‐century sea surface temperature variability in the southwest Pacific: A replication study using multiple coral Sr/Ca records from New Caledonia. Paleoceanography, 22:PA4212
Dickson GC, Poulter RT, Maas EW, Probert PK, Kieser JA (2011) Marine bacterial succession as a potential indicator of postmortem submersion interval. Forensic Sci Int 209:1–10
Dushoff J, Kain MP, Bolker BM (2019) I can see clearly now: reinterpreting statistical significance. Methods Ecol Evol 10:756–759
Evans F (1958) Growth and maturity of the barnacles Lepas hillii and Lepas anatifera. Nature 182:1245
Fitzgibbon QP, Simon CJ, Smith GG, Carter CG, Battaglene SC (2017) Temperature dependent growth, feeding, nutritional condition and aerobic metabolism of juvenile spiny lobster, Sagmariasus verreauxi. Comp Biochem Physiol Part A Mol Integr Physiol 207:13–20
Forrester GE, Macfarlan RJ, Holevoet AJ, Merolla S (2016) Dislodgement force and shell morphology vary according to wave exposure in a tropical gastropod (Cittarium pica). Mar Biol Res 12:986–992
Gil MA, Pfaller JB (2016) Oceanic barnacles act as foundation species on plastic debris: implications for marine dispersal. Sci Rep 6:1–7
Goldberg H (1985) An Investigation of the Feasibility of Gooseneck Barnacle Mariculture (Lepas anatifera), Master’s thesis, University of British Columbia
Goldstein MC, Carson HS, Eriksen M (2014) Relationship of diversity and habitat area in North Pacific plastic-associated rafting communities. Mar Biol 161:1441–1453
Gregg WW, Rousseaux CS (2019) Global ocean primary production trends in the modern ocean color satellite record (1998–2015). Environ Res Lett 14:124011
Gregory MR (2009) Environmental implications of plastic debris in marine settings—entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos Trans R Soc Lond B Biol Sci 364:2013–2025
Guilhem IF, Masi BP, Creed JC (2020) Impact of invasive Tubastraea spp. (Cnidaria: Anthozoa) on the growth of the space dominating tropical rocky-shore zoantharian Palythoa caribaeorum (Duchassaing and Michelotti, 1860). Aquat Invasions 15:98–113
Higuchi T, Ito SI, Ishimura T, Kamimura Y, Shirai K, Shindo H, Nishida K, Komatsu K (2019) Otolith oxygen isotope analysis and temperature history in early life stages of the chub mackerel Scomber japonicus in the Kuroshio-Oyashio transition region. Deep Sea Res Part II Top Stud Oceanogr 169:104660
Hoek PPC (1907) The Cirripedia of the Siboga Expedition: A. Cirripedia Pedunculata (Vol. 31). Brill Publishers, Leiden, pp 1–2
Iljin IN (1992) Pelagic fouling in tropic and subtropic oceanic waters. Fouling and Biological Damages: Environmental Problems. Nauka, Moscow, pp 77–111
Iljin IN, Makarov RR, Mileikovsky SA (1977) Fouling of experimental surfaces by goose barnacles and distribution of their larvae in plankton far from shores. Russ J Mar Biol 3:154–156
Iljin IN, Petrosyan VG, Bessonov SA, Dergunova NN (2013) Modeling of the invasion and development of the pelagic communities of fouling organisms in the ocean. Russ J Biol Invasions 4:225–233
Inatsuchi A, Yamato S, Yusa Y (2010) Effects of temperature and food availability on growth and reproduction in the neustonic pedunculate barnacle Lepas anserifera. Mar Biol 157:899–905
Ingólfsson A (1998) Dynamics of macrofaunal communities of floating seaweed clumps off western Iceland: a study of patches on the surface of the sea. J Exp Mar Biol Ecol 231:119–137
Jones DS, Hosie AM (2016) A checklist of the barnacles (Cirripedia: Thoracica) of Singapore and neighbouring waters. Raffles Bull Zool 34:241–311
Kennedy AB, Thomas D (2004) Drifter measurements in a laboratory rip current. J Geophys Res Oceans 109:1–16
Lavajoo F (2019) Influence of different algal diets on larval growth rates in the marine Serpulidae polychaete worm Spirobranchus kraussii. Ribarstvo 77:93–98
LeGrande AN, Schmidt GA (2006) Global gridded data set of the oxygen isotopic composition in seawater. Geophys Res Lett 33:L12604
Magni PA, Venn C, Aquila I, Pepe F, Ricci P, Di Nunzio C, Ausania F, Dadour IR (2015) Evaluation of the floating time of a corpse found in a marine environment using the barnacle Lepas anatifera L. (Crustacea: Cirripedia: Pedunculata). Forensic Sci Int 247:e6–e10
Mateus M, Pinto L, Chambel-Leitão P (2015) Evaluating the predictive skills of ocean circulation models in tracking the drift of a human body: a case study. Aust J Forensic Sci 47:322–331
Mazerolle MJ (2019) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 2.2–2. https://cran.r-project.org/package=AICcmodavg
McCuller MI, Carlton JT (2018) Transoceanic rafting of Bryozoa (Cyclostomata, Cheilostomata, and Ctenostomata) across the North Pacific Ocean on Japanese tsunami marine debris. Aquat Invasions 13:137–162
McIntosh WC (1885) Report on the Annelida Polychaeta collected by H.M.S. Challenger during the years 1873–1876, in Report on the Scientific Results of the Voyage of H.M.S. Challenger during the years 1873–76. Zoology 12:1–554
Memmi M (1982) Revision of the species Lepas anatifera (Crustacea, Cirripedia). Zool Zh 61:1165–1170
Michaelis R, Hass HC, Mielck F, Papenmeier S, Sander L, Ebbe B, Gutow L, Wiltshire KH (2019) Hard-substrate habitats in the German Bight (South-Eastern North Sea) observed using drift videos. J Sea Res 144:78–84
Murtaugh PA (2014) In defense of P values. Ecology 95:611–617
Nishizaki MT, Carrington E (2015) The effect of water temperature and velocity on barnacle growth: Quantifying the impact of multiple environmental stressors. J Therm Biol 54:37–46
Okamura B, Partridge JC (1999) Suspension feeding adaptations to extreme flow environments in a marine bryozoan. Biol Bull-US 196:205–215
Ortega-Cisneros K, de Lecea AM, Smit AJ, Schoeman DS (2017) Resource utilization and trophic niche width in sandy beach macrobenthos from an oligotrophic coast. Estuar Coast Mar Sci 184:115–125
Ostle C, Thompson RC, Broughton D, Gregory L, Wootton M, Johns DG (2019) The rise in ocean plastics evidenced from a 60-year time series. Nature Commun 10:1–6
Palmer J, Turney C, Hogg A, Hilliam N, Watson M, van Sebille E, Cowie W, Jones R, Petchey F (2014) The discovery of New Zealand’s oldest shipwreck–possible evidence of further Dutch exploration of the South Pacific. J Archaeol Sci 42:435–441
Pirtle D, Magni PA, Reinecke GW, Dadour IR (2019) Barnacle colonization of shoes: Evaluation of a novel approach to estimate the time spent in water of human remains. Forensic Sci Int 294:1–9
Popovic GC, Warton DI, Thomson FJ, Hui FK, Moles AT (2019) Untangling direct species associations from indirect mediator species effects with graphical models. Methods Ecol Evol 10:1571–1583
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reisser J, Shaw J, Hallegraeff G, Proietti M, Barnes DK, Thums M, Wilcox C, Hardesty BD, Pattiaratchi C (2014) Millimeter-sized marine plastics: a new pelagic habitat for microorganisms and invertebrates. PLoS ONE 9:e100289
Richardson AJ, Poloczanska ES (2008) Under-resourced, under threat. Science 320:1294
Sano M, Omori M, Taniguchi K (2003) Predator-prey systems of drifting seaweed communities off the Tohoku coast, northern Japan, as determined by feeding habit analysis of phytal animals. Fish Res 69:260–268
Schiffer PH, Herbig HG (2016) Endorsing Darwin: global biogeography of the epipelagic goose barnacles Lepas spp. (Cirripedia, Lepadomorpha) proves cryptic speciation. Zool J Linnean Soc 177:507–525
Schilling HT, Reis-Santos P, Hughes JM, Smith JA, Everett JD, Stewart J, Gillanders BM, Suthers IM (2018) Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia. Mar Ecol Prog 598:187–199
Schlacher TA, Strydom S, Connolly RM (2013) Multiple scavengers respond rapidly to pulsed carrion resources at the land–ocean interface. Acta Oecol (Montrouge) 48:7–12
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Setsaas TH, Bester MN (2006) Goose barnacle (Lepas australis) infestation of the Subantarctic fur seal (Arctocephalus tropicalis). Afr Zool 41:305–307
Stoner AW, Greening HS (1984) Geographic variation in the macrofaunal associates of pelagic Sargassum and some biogeographic implications. Mar Ecol Prog 20:185–192
Tao Y, Wen-xia Y, Guan-he L, Yu D, Hua-jie W, Yan Y (2000) Marine biofouling in offshore areas south of Hainan Island, northern South China Sea. Chin J Oceanol Limnol 18:132–139
Tao Y, Wen-xia Y, Yu D, Guan-he L, Yan Y (2003) Fouling in offshore areas southeast of the Zhujiang (Pearl) River Delta, the northern South China Sea. Hai Yang Xue Bao 22:201–211
Thiel M, Gutow L (2005a) The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr Mar Biol Annu Rev 42:181–264
Thiel M, Gutow L (2005b) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr Mar Biol Annu Rev 43:279–418
Tsikhon-Lukanina EA, Reznichenko OG, Nikolaeva GG (2001) Ecology of invertebrates on the oceanic floating substrata in the Northwest Pacific Ocean. Oceanology 41:525–530
Tsikhon-Lukanina EA, Soldatova IN, Kuznetsova IA, Iljin IN (1976) Makroepiboly in the Strait of Tunis. Okeanologiya 16:907–911
Ullmann CV, Gale AS, Huggett J, Wray D, Frei R, Korte C, Broom-Fendley S, Littler K, Hesselbo SP (2018) The geochemistry of modern calcareous barnacle shells and applications for palaeoenvironmental studies. Geochim Cosmochim Acta 243:149–168
Van Sebille E, Wilcox C, Lebreton L, Maximenko N, Hardesty BD, Van Franeker JA, Eriksen M, Siegel D, Galgani F, Law KL (2015) A global inventory of small floating plastic debris. Environ Res Let 10:124006
Vaughn CC (2018) Ecosystem services provided by freshwater mussels. Hydrobiologia 810:15–27
Velasquez E, Bryan SE, Ekins M, Cook AG, Hurrey L, Firn J (2018) Age and area predict patterns of species richness in pumice rafts contingent on oceanic climatic zone encountered. Ecol Evol 8:5034–5046
Wang Y, Naumann U, Eddelbuettel D, Wilshire J, Warton D (2019) mvabund: Statistical Methods for Analysing Multivariate Abundance Data. R package version 4.0.1. https://CRAN.R-project.org/package=mvabund
Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101
Wasson K, Von Holle B, Toft J, Ruiz G (2000) Detecting invasions of marine organisms: kamptozoan case histories. Biol Invasions 2:59–74
Winston JE (1982) Drift plastic—an expanding niche for a marine invertebrate? Mar Pollut Bull 13:348–351
Wright JP, Jones CG, Flecker AS (2002) An ecosystem engineer, the beaver, increases species richness at the landscape scale. Oecologia 132:96–101
Yan T, Yan W, Dong Y, Wang H, Yan Y, Liang G (2006) Marine fouling of offshore installations in the northern Beibu Gulf of China. Int Biodeterior Biodegradation 58:99–105
Ye S, Andrady AL (1991) Fouling of floating plastic debris under Biscayne Bay exposure conditions. Mar Pollut Bull 22:608–613
Zhang H (2017) Transport of microplastics in coastal seas. Estuar Coast Shelf Sci 199:74–86
Zvyagintsev AY, Ivin VV (1992) Fouling communities of the Seychelles Islands. Atoll Res Bull 370:1–18
Acknowledgements
We thank Clive Holden from Oceanographic Field Services, who installed and serviced the Bondi mooring; Di Jones for confirming identifications and for her translation of Blamart and Bassinot’s paper from French; David Griffin for providing valuable insights; and, Geoff Liggins, Gilles Ballinger and Marcus Miller from the New South Wales Department of Primary Industries for sampling Lepas from their puerulus floats. Thanks to Andrew Niccum, Sergio Torres Gabarda, Nigel Coombes, James Mercer, Aaron Puckeridge, Alex Milne-Muller, Gary Truong, Craig Steinberg, Felicity McAllister, Edward Buttler, Virginie van Dongen-Vogels, Ian Puckeridge and Nick Lambert for help with specimen and field data collection. Thanks to Di Jones, Janine Ledet, Barry Hutchins, Romain Sabroux, Chris Glasby, Adam Yates, Megan McCuller, Richard Willan, Peter Poortman, Brendan Lanham, Pat Hutchings, Sabine Rech, Mark McGrouther, Andrew Hosie, and Nick Lambert for their identifications. Thanks to Andrew Hosie, Jerry Kudenov and Andy Baker for help with data analysis and preparation of the manuscript, and to our reviewers for providing thoughtful comments that substantially improved the manuscript. This is contribution no. 266 of the Sydney Institute of Marine Science.
Funding
Mass spectrometry sample preparation and analysis was carried out at the UNSW Bioanalytical Mass Spectrometry Facility, part of the Mark Wainwright Analytical Centre, and was in part enabled by the granting of an in-kind honours scholarship by A/Prof. Mark Raftery. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Thomas Mesaglio: Conceptualisation, Methodology, Software, Formal Analysis, Investigation, Writing – Original Draft, Visualisation. Hayden Schilling: Conceptualisation, Methodology, Software, Formal Analysis, Writing – Review & Editing, Supervision. Lewis Adler: Methodology, Formal Analysis, Investigation, Writing – Review & Editing. Shane Ahyong: Conceptualisation, Methodology, Writing – Review & Editing, Supervision. Ben Maslen: Software, Formal Analysis, Writing – Review & Editing. Iain Suthers: Conceptualisation, Methodology, Formal Analysis, Writing – Review & Editing, Supervision.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no conflicts of interest to declare.
Consent for publication
All authors consent to the publication of this manuscript.
Additional information
Responsible Editor: E. Briski.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by F. Bettini Pitombo and F. Sylvester.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mesaglio, T.P., Schilling, H.T., Adler, L. et al. The ecology of Lepas-based biofouling communities on moored and drifting objects, with applications for marine forensic science. Mar Biol 168, 21 (2021). https://doi.org/10.1007/s00227-021-03822-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03822-1