Spatial resolution of shell microchemistry for tracking dispersing pelagic mussels in a large open embayment in northern New Zealand
Wenjie Wu A * , Carolyn J. Lundquist B C and Andrew G. Jeffs A DA
B
C
D
Abstract
The effectiveness of using shell microchemistry methods for reconstructing the pelagic dispersal of shell-forming marine organisms relies on the existence of sufficient spatial variability and temporal stability in the microchemical composition of coastal waters.
This study aimed to determine whether shell microchemistry methods can reliably infer pelagic dispersal of green-lipped mussel (Perna canaliculus) across a large and well-mixed embayment in New Zealand.
Isotopes of 12 chemical elements (7Li, 27Al, 59Co, 60Ni, 63Cu, 66Zn, 88Sr, 138Ba, 139La, 140Ce, 208Pb and 238U) were assessed from juvenile mussel shells grown in situ from 22 sites for two consecutive periods of ~5 weeks.
There was sufficient spatial variability in measured shell element concentrations to support microchemical atlases that are capable of distinguishing among regions within this large embayment, with 73% assignment accuracy. However, the temporal variability in the microchemical signatures is such that they would need to be sampled contemporaneously with animal samples to be effective for distinguishing pelagic dispersal of mussels in the embayment.
The shell microchemistry shows sufficient spatio-temporal resolution for reliably inferring pelagic dispersal of this economically and ecologically important mussel species over a large embayment. Sufficient resolution at such large scale may come from unique hydro-geological inputs.
This study confirms the feasibility of shell microchemistry method in tracking pelagic dispersal of marine organisms across a large well-mixed embayment, offering insights to improve accuracy and reduce costs for future research.
Keywords: coastal-water chemistry, estuaries, freshwater inflows, green-lipped mussel, LA-ICP-MS, larval mussel dispersal, Perna canaliculus, shell microchemistry.
References
Adler D, Nenadic O, Zucchini W (2003) RGL: a R-library for 3D visualization with OpenGL. In ‘35th Symposium of the Interface: Computing Science and Statistics 2003: Security and Infrastructure Protection. Computing Science and Statistics, Vol. 35’, 12–15 March 2003, Salt Lake City, UT, USA. pp. 419–429. (Curran Associates, Inc.: Red Hook, NY, USA) Available at https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=c20764ebb8f384cfe76042c41af1ca0bd9695f7c
Alfaro AC, Jeffs AG, Hooker SH (2003) Spatial variability in reproductive behaviour of green-lipped mussel populations of northern New Zealand. Molluscan Research 23, 223-238.
| Crossref | Google Scholar |
Alfaro AC, Jeffs AG, Creese RG (2004) Bottom-drifting algal/mussel spat associations along a sandy coastal region in northern New Zealand. Aquaculture 241, 269-290.
| Crossref | Google Scholar |
Alfaro AC, McArdle B, Jeffs AG (2010) Temporal patterns of arrival of beachcast green-lipped mussel (Perna canaliculus) spat harvested for aquaculture in New Zealand and its relationship with hydrodynamic and meteorological conditions. Aquaculture 302, 208-218.
| Crossref | Google Scholar |
Apte S, Gardner JPA (2002) Population genetic subdivision in the New Zealand greenshell mussel (Perna canaliculus) inferred from single-strand conformation polymorphism analysis of mitochondrial DNA. Molecular Ecology 11, 1617-1628.
| Crossref | Google Scholar | PubMed |
Avdelas L, Avdic-Mravlje E, Borges Marques AC, Cano S, Capelle JJ, Carvalho N, Cozzolino M, Dennis J, Ellis T, Fernández Polanco JM, Guillen J, Lasner T, Le Bihan V, Llorente I, Mol A, Nicheva S, Nielsen R, van Oostenbrugge H, Villasante S, Visnic S, Zhelev K, Asche F (2021) The decline of mussel aquaculture in the European Union: causes, economic impacts and opportunities. Reviews in Aquaculture 13, 91-118.
| Crossref | Google Scholar |
Becker BJ, Fodrie FJ, McMillan PA, Levin LA (2005) Spatial and temporal variation in trace elemental fingerprints of mytilid mussel shells: a precursor to invertebrate larval tracking. Limnology and Oceanography 50, 48-61.
| Crossref | Google Scholar |
Becker BJ, Levin LA, Fodrie FJ, McMillan PA (2007) Complex larval connectivity patterns among marine invertebrate populations. Proceedings of the National Academy of Sciences 104, 3267-3272.
| Crossref | Google Scholar |
Beer NA, Wing SR, Hu Y (2011) Physical versus biological control of element incorporation into biogenic carbonate: an in situ experiment in a New Zealand fjord. Marine Ecology Progress Series 433, 289-301.
| Crossref | Google Scholar |
Bennion M, Morrison L, Brophy D, Carlsson J, Abrahantes JC, Graham CT (2019) Trace element fingerprinting of blue mussel (Mytilus edulis) shells and soft tissues successfully reveals harvesting locations. Science of The Total Environment 685, 50-58.
| Crossref | Google Scholar | PubMed |
Brenner M, Buck BH (2010) Attachment properties of blue mussel (Mytilus edulis L.) byssus threads on culture-based artificial collector substrates. Aquacultural Engineering 42, 128-139.
| Crossref | Google Scholar |
Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annual Review of Ecology and Systematics 27, 477-500.
| Crossref | Google Scholar |
Carrasco AV, Astorga M, Cisterna A, Farias A, Espinoza V, Uriarte I (2014) Pre-feasibility study for the installation of a Chilean mussel Mytilus chilensis (Hupe, 1854) seed hatchery in the lakes region, Chiles. Fisheries and Aquaculture Journal 5(3), 102.
| Crossref | Google Scholar |
Carré M, Bentaleb I, Bruguier O, Ordinola E, Barrett NT, Fontugne M (2006) Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochimica et Cosmochimica Acta 70, 4906-4920.
| Crossref | Google Scholar |
Carson HS (2010) Population connectivity of the Olympia oyster in southern California. Limnology and Oceanography 55, 134-148.
| Crossref | Google Scholar |
Carson HS, López-Duarte PC, Cook GS, Fodrie FJ, Becker BJ, DiBacco C, Levin LA (2013) Temporal, spatial, and interspecific variation in geochemical signatures within fish otoliths, bivalve larval shells, and crustacean larvae. Marine Ecology Progress Series 473, 133-148.
| Crossref | Google Scholar |
Cathey AM, Miller NR, Kimmel DG (2014) Spatiotemporal stability of trace and minor elemental signatures in early larval shell of the northern quahog (hard clam) Mercenaria mercenaria. Journal of Shellfish Research 33, 247-255.
| Crossref | Google Scholar |
Chipperfield PNJ (1953) Observations on the breeding and settlement of Mytilus edulis (L.) in British waters. Journal of the Marine Biological Association of the United Kingdom 32, 449-476.
| Crossref | Google Scholar |
Cook GS (2011) Changes in otolith microchemistry over a protracted spawning season influence assignment of natal origin. Marine Ecology Progress Series 423, 197-209.
| Crossref | Google Scholar |
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443-466.
| Crossref | Google Scholar | PubMed |
Crowder LB, Lyman SJ, Figueira WF, Priddy J (2000) Source–sink population dynamics and the problem of siting marine reserves. Bulletin of Marine Science 66, 799-820 https://www.ingentaconnect.com/content/umrsmas/bullmar/2000/00000066/00000003/art00021.
| Google Scholar |
Darroch JN, Mosimann JE (1985) Canonical and principal components of shape. Biometrika 72(2), 241-252.
| Crossref | Google Scholar |
de Montaudouin X, Bachelet G, Sauriau P-G (2003) Secondary settlement of cockles Cerastoderma edule as a function of current velocity and substratum: a flume study with benthic juveniles. Hydrobiologia 503, 103-116.
| Crossref | Google Scholar |
Dechaume-Moncharmont F-X, Monceau K, Cezilly F (2011) Sexing birds using discriminant function analysis: a critical appraisal. The Auk 128, 78-86.
| Crossref | Google Scholar |
Dixon P (2003) VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14(6), 927-930.
| Crossref | Google Scholar |
Dodd JR, Crisp EL (1982) Non-linear variation with salinity of Sr/Ca and Mg/Ca ratios in water and aragonitic bivalve shells and implications for paleosalinity studies. Palaeogeography, Palaeoclimatology, Palaeoecology 38, 45-56.
| Crossref | Google Scholar |
Dunphy BJ, Millet M-A, Jeffs AG (2011) Elemental signatures in the shells of early juvenile green-lipped mussels (Perna canaliculus) and their potential use for larval tracking. Aquaculture 311, 187-192.
| Crossref | Google Scholar |
Fodrie FJ, Becker BJ, Levin LA, Gruenthal K, McMillan PA (2011) Connectivity clues from short-term variability in settlement and geochemical tags of mytilid mussels. Journal of Sea Research 65, 141-150.
| Crossref | Google Scholar |
Forrester GE, Swearer SE (2002) Trace elements in otoliths indicate the use of open-coast versus bay nursery habitats by juvenile California halibut. Marine Ecology Progress Series 241, 201-213.
| Crossref | Google Scholar |
Gillanders BM (2002) Connectivity between juvenile and adult fish populations: do adults remain near their recruitment estuaries? Marine Ecology Progress Series 240, 215-223.
| Crossref | Google Scholar |
Gillanders BM, Sanchez-Jerez P, Bayle-Sempere J, Ramos-Espla A (2001) Trace elements in otoliths of the two-banded bream from a coastal region in the south-west Mediterranean: are there differences among locations? Journal of Fish Biology 59, 350-363.
| Crossref | Google Scholar |
Gillikin DP, Lorrain A, Navez J, Taylor JW, André L, Keppens E, Baeyens W, Dehairs F (2005) Strong biological controls on Sr/Ca ratios in aragonitic marine bivalve shells. Geochemistry, Geophysics, Geosystems 6, Q05009.
| Crossref | Google Scholar |
Gräler B, Pebesma EJ, Heuvelink GB (2016) Spatio-temporal interpolation using gstat. The R Journal 8(1), 204-218 https://journal.r-project.org/archive/2016/RJ-2016-014/index.html.
| Google Scholar |
Hayden BJ (1994) What do we know about greenshell mussel spat? Seafood New Zealand. Part I 2, 45-47.
| Google Scholar |
Hocking MWA, Hannington MD, Percival JB, Stoffers P, Schwarz-Schampera U, de Ronde CEJ (2010) Clay alteration of volcaniclastic material in a submarine geothermal system, Bay of Plenty, New Zealand. Journal of Volcanology and Geothermal Research 191, 180-192.
| Crossref | Google Scholar |
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5(3), 299-314.
| Crossref | Google Scholar |
Jeffs AG, Holland RC, Hooker SH, Hayden BJ (1999) Overview and bibliography of research on the greenshell mussel, Perna canaliculus, from New Zealand waters. Journal of Shellfish Research 18, 347-360.
| Google Scholar |
Jeffs AG, Delorme NJ, Stanley J, Zamora LN, Sim-Smith C (2018) Composition of beachcast material containing green-lipped mussel (Perna canaliculus) seed harvested for aquaculture in New Zealand. Aquaculture 488, 30-38.
| Crossref | Google Scholar |
Kilgour G, Kennedy B, Scott B, Christenson B, Jolly A, Asher C, Rosenberg M, Saunders K (2021) Whakaari/White Island: a review of New Zealand’s most active volcano. New Zealand Journal of Geology and Geophysics 64, 273-295.
| Crossref | Google Scholar |
Kroll IR, Poray AK, Puckett BJ, Eggleston DB, Fodrie FJ (2016) Environmental effects on elemental signatures in eastern oyster Crassostrea virginica shells: using geochemical tagging to assess population connectivity. Marine Ecology Progress Series 543, 173-186.
| Crossref | Google Scholar |
Lea DW, Shen GT, Boyle EA (1989) Coralline barium records temporal variability in equatorial Pacific upwelling. Nature 340, 373-376.
| Crossref | Google Scholar |
Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46, 282-297.
| Crossref | Google Scholar | PubMed |
Lopes RM (2007) Marine zooplankton studies in Brazil: a brief evaluation and perspectives. Anais da Academia Brasileira de Ciências 79, 369-379.
| Crossref | Google Scholar | PubMed |
Lyons GL, Giggenbach WF, Singleton RJ, Glasby GP (1977) Isotopic and chemical composition of submarine geothermal gases from the Bay of Plenty, New Zealand. New Zealand Department of Scientific and Industrial Research Bulletin 218, 65-67.
| Google Scholar |
Miller SH, Morgan SG, White JW, Green PG (2013) Interannual variability in an atlas of trace element signatures for determining population connectivity. Marine Ecology Progress Series 474, 179-190.
| Crossref | Google Scholar |
Mischler CP, Bell EA, Landers TJ, Dennis TE (2015) Sex determination of black petrels (Procellaria parkinsoni) using morphometric measurements and discriminant function analysis. Notornis 62, 57-62.
| Google Scholar |
Montaño MM, Suanda SH, Souza JMAC (2023) Modelled coastal circulation and Lagrangian statistics from a large coastal embayment: the case of Bay of Plenty, Aotearoa New Zealand. Estuarine, Coastal and Shelf Science 281, 108212.
| Crossref | Google Scholar |
Mundry R, Sommer C (2007) Discriminant function analysis with nonindependent data: consequences and an alternative. Animal Behaviour 74, 965-976.
| Crossref | Google Scholar |
Norrie CR, Dunphy BJ, Ragg NLC, Lundquist CJ (2018) Ocean acidification can interact with ontogeny to determine the trace element composition of bivalve shell. Limnology and Oceanography Letters 3, 393-400.
| Crossref | Google Scholar |
Norrie CR, Dunphy BJ, Ragg NLC, Lundquist CJ (2019) Comparative influence of genetics, ontogeny and the environment on elemental fingerprints in the shell of Perna canaliculus. Scientific Reports 9, 8533.
| Crossref | Google Scholar |
Norrie C, Dunphy B, Roughan M, Weppe S, Lundquist C (2020) Spill-over from aquaculture may provide a larval subsidy for the restoration of mussel reefs. Aquaculture Environment Interactions 12, 231-249.
| Crossref | Google Scholar |
Pantin HM, Wright IC (1994) Submarine hydrothermal activity within the offshore Taupo Volcanic Zone, Bay of Plenty continental shelf, New Zealand. Continental Shelf Research 14, 1411-1438.
| Crossref | Google Scholar |
Paton C, Hellstrom J, Paul B (2011) Iolite: freeware for the visualisation and processing of mass spectrometric data. Journal of Analytical Atomic Spectrometry 26(12), 2508-2518.
| Crossref | Google Scholar |
Patterson HM, Thorrold SR, Shenker JM (1999) Analysis of otolith chemistry in Nassau grouper (Epinephelus striatus) from the Bahamas and Belize using solution-based ICP-MS. Coral Reefs 18, 171-178.
| Crossref | Google Scholar |
Peacock E, Neff H, Rafferty J, Meaker T (2007) Using laser ablation–inductively coupled plasma–mass spectrometry (LA-ICP-MS) to source shell in shell-tempered pottery: a pilot study from North Mississippi. Southeastern Archaeology 26, 319-329.
| Google Scholar |
Pebesma EJ (2004) Multivariable geostatistics in S: the gstat package. Computers and Geoscience 30, 683-691.
| Crossref | Google Scholar |
Poulain C, Gillikin DP, Thébault J, Munaron JM, Bohn M, Robert R, Paulet Y-M, Lorrain A (2015) An evaluation of Mg/Ca, Sr/Ca, and Ba/Ca ratios as environmental proxies in aragonite bivalve shells. Chemical Geology 396, 42-50.
| Crossref | Google Scholar |
Putten EV, Dehairs F, Keppens E, Baeyens W (2000) High resolution distribution of trace elements in the calcite shell layer of modern Mytilus edulis: environmental and biological controls. Geochimica et Cosmochimica Acta 64, 997-1011.
| Crossref | Google Scholar |
Racine JS (2012) RStudio: a platform-independent IDE for R and Sweave. Journal of Applied Econometrics 27(1), 167-172.
| Crossref | Google Scholar |
Rand WM (1971) Objective criteria for the evaluation of clustering methods. Journal of the American Statistical Association 66, 846-850.
| Crossref | Google Scholar |
Ridgway NM, Greig MJN (1986) Water movements in Bay of Plenty, New Zealand. New Zealand Journal of Marine and Freshwater Research 20, 447-453.
| Crossref | Google Scholar |
Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Müller M (2011) pROC: an open-source package for R and S to analyze and compare ROC curves. BMC Bioinformatics 12, 77.
| Crossref | Google Scholar |
Secor DH, Henderson-Arzapalo A, Piccoli PM (1995) Can otolith microchemistry chart patterns of migration and habitat utilization in anadromous fishes? Journal of Experimental Marine Biology and Ecology 192, 15-33.
| Crossref | Google Scholar |
Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores – I. Breeding and settlement. Oecologia 3, 277-316.
| Crossref | Google Scholar | PubMed |
Skelton B, South PM, Jeffs AG (2021) Inefficiency of conversion of seed into marketready mussels in New Zealand’s GreenshellTM mussel (Perna canaliculus) industry. Aquaculture 560, 738584.
| Crossref | Google Scholar |
Sorte CJB, Etter RJ, Spackman R, Boyle EE, Hannigan RE (2013) Elemental fingerprinting of mussel shells to predict population sources and redistribution potential in the gulf of maine. PLoS ONE 8, e80868.
| Crossref | Google Scholar |
South PM, Delorme NJ, Skelton BM, Floerl O, Jeffs AG (2021) The loss of seed mussels in longline aquaculture. Reviews in Aquaculture 14(1), 440-455.
| Crossref | Google Scholar |
Stoffers P, Hannington M, Wright I, Herzig P, de Ronde C, Shipboard Scientific Party (1999) Elemental mercury at submarine hydrothermal vents in the Bay of Plenty, Taupo volcanic zone, New Zealand. Geology 27(10), 931-934.
| Crossref | Google Scholar |
Strasser CAA, Thorrold SRR, Starczak VRR, Mullineaux LSS, Adams D, Walther B, Elsdon T, Cohen A, Leavitt D (2007) Laser ablation ICP-MS analysis of larval shell in softshell clams (Mya arenaria) poses challenges for natural tag studies. Limnology and Oceanography: Methods 5, 241-249.
| Crossref | Google Scholar |
Suchley A, Alvarez-Filip L (2018) Local human activities limit marine protection efficacy on Caribbean coral reefs. Conservation Letters 11(5), e12571.
| Crossref | Google Scholar |
Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402, 799-802.
| Crossref | Google Scholar |
Thébault J, Chauvaud L, L’Helguen S, Clavier J, Barats A, Jacquet S, Pécheyran C, Amouroux D (2009) Barium and molybdenum records in bivalve shells: geochemical proxies for phytoplankton dynamics in coastal environments? Limnology and Oceanography 54, 1002-1014.
| Crossref | Google Scholar |
Thorrold S, Zacherl D, Levin L (2007) Population connectivity and larval dispersal using geochemical signatures in calcified structures. Oceanography 20, 80-89.
| Crossref | Google Scholar |
Toone TA, Benjamin ED, Hillman JR, Handley S, Jeffs A (2023) Multidisciplinary baselines quantify a drastic decline of mussel reefs and reveal an absence of natural recovery. Ecosphere 14(3), e4390.
| Crossref | Google Scholar |
Vavrek MJ (2011) fossil: palaeoecological and palaeogeographical analysis tools. Palaeontologia Electronica 14, 1T Available at http://palaeo-electronica.org/2011_1/238/index.html.
| Google Scholar |
Venables WN, Ripley BD (2002) ‘Modern applied statistics with S’, 4th edn. (Springer: New York, NY, USA) 10.1007/978-0-387-21706-2
Walters LJ, Wethey DS (1996) Settlement and early post-settlement survival of sessile marine invertebrates on topographically complex surfaces:the importance of refuge dimensions and adult morphology. Marine Ecology Progress Series 137, 161-171.
| Crossref | Google Scholar |
Watson JR, Siegel DA, Kendall BE, Mitarai S, Rassweiller A, Gaines SD (2011) Identifying critical regions in small-world marine metapopulations. Proceedings of the National Academy of Sciences of the USA 108(43), E907-E913.
| Crossref | Google Scholar |
Wei K, Wood AR, Gardner JPA (2013) Population genetic variation in the New Zealand greenshell mussel: locus-dependent conflicting signals of weak structure and high gene flow balanced against pronounced structure and high self-recruitment. Marine Biology 160, 931-949.
| Crossref | Google Scholar |
White JW, Ruttenberg BI (2007) Discriminant function analysis in marine ecology:some oversights and their solutions. Marine Ecology Progress Series 329, 301-305.
| Crossref | Google Scholar |
Wilson CJN, Rowland JV (2016) The volcanic, magmatic and tectonic setting of the Taupo Volcanic Zone, New Zealand, reviewed from a geothermal perspective. Geothermics 59, 168-187.
| Crossref | Google Scholar |
Wu W, Chaput R, Lundquist CJ, Montaño Orozco MM, Jeffs AG (2024) Tracking the source of wild mussel spat for aquaculture using shell microchemistry and biophysical models. Aquaculture 578, 740025.
| Crossref | Google Scholar |
Zacherl DC (2005) Spatial and temporal variation in statolith and protoconch trace elements as natural tags to track larval dispersal. Marine Ecology Progress Series 290, 145-163.
| Crossref | Google Scholar |
Zacherl DC, Manríquez PH, Paradis G, Day RW, Castilla JC, Warner RR, Lea DW, Gaines SD (2003) Trace elemental fingerprinting of gastropod statoliths to study larval dispersal trajectories. Marine Ecology Progress Series 248, 297-303.
| Crossref | Google Scholar |