Abstract
Laternula elliptica is a key bivalve species and widely distributed around the Antarctic continent. This bivalve has been the study subject in several studies centered on ecological, physiological, biochemical, and behavioral patterns. However, little is known about the chemistry and the biomechanical properties of the shells of this mollusk. Here, we present the first report of the intra-population variability in the organic composition and mechanical properties of L. elliptica shells. Further, we analyze different morphological traits and their association with the metabolism of a population of L. elliptica from King George Island, Western Antarctic Peninsula. The summer metabolic rates and the hepatosomatic index values indicate good health conditions of this clam’s population. Shell periostracum chemistry is quite similar to bivalves from temperate regions, but the relative amount of protein increased ca. five-fold in shells of L. elliptica. The microhardness is approximately 32% lower than in bivalves from temperate regions. Our characterization of the L. elliptica shells suggests that periostracum chemistry could be specially fitted to avoid shell carbon exposure to dissolution (e.g., in corrosive acidified seawater). In contrast, the reduction in shell hardness may result from prioritizing behavioral (burial) and shell repairing strategies to confront biological (predators) and physical disturbances (e.g., ice scouring). Similar studies in other Antarctic mollusks will help understand the role of shell structure and function in confronting projected climate changes in the Antarctic ocean.
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References
Ahn IY (1994) Ecology of the Antarctic bivalve Laternula elliptica (King and Broderip) in Collins Harbor, King George Island: benthic environment and an adaptive strategy. Mem Nat Inst Polar Res 50:1–10
Ahn IY, Shim JH (1998) Summer metabolism of the Antarctic clam Laternula elliptica in Maxwell Bay, King George Island and its implications. J Exp Mar Biol Ecol 224:253–264. https://doi.org/10.1016/S0022-0981(97)00201-3
Ahn IY, Cho KW, Choi K-S, Seo Y, Shin J (2000) Lipid content and composition of the Antarctic lamellibranch, Laternula elliptica (King & Broderip) (Anamalodesmata: Laternulidae), in King George Island during an austral summer. Polar Biol 23:24–33. https://doi.org/10.1007/s003000050004
Ahn IY, Kang J, Kim K-W (2001) The effect of body size on metal accumulations in the bivalve Laternula elliptica. Antarct Sci 13:355–362. https://doi.org/10.1017/S0954102001000505
Ahn IY, Surh J, Park YG, Kwon H, Choi KS, Kang SH, Choi HJ, Kim KW, Chung H (2003) Growth and seasonal energetics of the Antarctic bivalve Laternula elliptica from King George Island, Antarctica. Mar Ecol Prog Ser 257:99–110. https://doi.org/10.3354/meps257099
Aldana M, García-Huidobro MR, Pulgar VM, Pulgar J (2017) Upwelling promotes earlier onset and increased rate of gonadal development of four coastal herbivores. Bull Mar Sci 93:671–688. https://doi.org/10.5343/bms.2016.1063
Ansell AD, Harvey R (1997) Protected larval development in the Antarctic bivalve Laternula elliptica (King and Broderip) (Anomalodesmata: Laternulidae). J Moll Stud 63:109–111. https://doi.org/10.1093/mollus/63.2.285
Benítez S, Lagos NA, Osores S, Optiz T, Duarte C, Navarro JM, Lardies MA (2018) High pCO2 levels affect metabolic rate, but not feeding behavior and fitness, of farmed giant mussel Choromytilus chorus. Aquacult Environ Interact 10:267–278. https://doi.org/10.3354/aei00271
Brey T, Voigt M, Jenkins K, Ahn IY (2011) The bivalve Laternula elliptica at King George Island - a biological recorder of climate forcing in the West Antarctic Peninsula region. J Mar Syst 88:542–552. https://doi.org/10.1016/j.jmarsys.2011.07.004
Brockington S (2001) The seasonal energetics of the Antarctic bivalve Laternula elliptica (King and Broderip) at Rothera Point, Adelaide Island. Polar Biol 24:523–530. https://doi.org/10.1007/s003000100251
Bylenga CH, Cummings VJ, Ryan KG (2017) High resolution microscopy reveals significant impacts of ocean acidification and warming on larval shell development in Laternula elliptica. PLoS ONE 12:e0175706. https://doi.org/10.1371/journal.pone.0175706
Checa AG (2018) Physical and biological determinants of the fabrication of molluscan shell microstructures. Front Mar Sci 5:353. https://doi.org/10.3389/fmars.2018.00353
Checa AG, Salas C (2017) Periostracum and shell formation in the Bivalvia. Trea.tise online no 93, Part N, Volume 1, Chapter 3: 1-51. https://journals.ku.edu/treatiseonline/article/view/6650
Checa AG, Macías-Sánchez E, Harper EM, Cartwright JHE (2016) Organic membranes determine the pattern of the columnar prismatic layer of mollusc shells. Proc R Soc B. https://doi.org/10.1098/rspb.2016.0032
Checa AG, Salas C, Rodríguez-Navarro AB, Grenier C, Lagos NA (2019) Articulation and growth of skeletal elements in balanid bernacles (Belanidae, Balanomorpha, Cirripedia). R Soc Open Sci 6:e190458. https://doi.org/10.1098/rsos.190458
Chen PY, Lin AYM, Lin YS, Seki Y, Stokes AG, Peyras J, Olevsky EA, Meyers MA, McKittrick J (2008) Structure and mechanical properties of selected biological materials. J Mech Behav Biomed 1:208–226. https://doi.org/10.1016/j.jmbbm.2008.02.003
Clark MS, Fraser K, Peck L (2008) Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperones 13:39–49. https://doi.org/10.1007/s12192-008-0014-8
Clark MS, Throne M, Vieira F, Cardoso J, Power D, Peck L (2010) Insights into shell deposition in the Antarctic bivalve Laternula elliptica: gene discovery in the mantle transcriptome using 454 pyrosequencing. BMC Genomics 11:362. https://doi.org/10.1186/1471-2164-11-362
Clarke A (1980) A reappraisal of the concept of metabolic cold adaptation in polar marine invertebrates. Biol J Linn Soc 14:77–92. https://doi.org/10.1111/j.1095-8312.1980.tb00099.x
Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol Annu Rev 21:341–453
Clarke A (1990) Temperature and evolution. Southern Ocean cooling and the Antarctic marine fauna. In: Kerry KR, Hempel G (eds) Antarctic Ecosystems. Springer, Berlin, pp 9–12
Clarke A (1991) What is cold adaptation and how should we measure it? Amer Zool 31:81–92
Cummings V, Hewitt J, Van Rooyen A, Currie K, Beard S, Thrush S, Norkko J, Barr N, Neath P, Halliday NJ, Sedcole R, Gomez A, McGraw C, Metcalf V (2011) Ocean acidification at high latitudes: potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS ONE 6:e16069. https://doi.org/10.1371/journal.pone.0016069
Eklöf J, Austin A, Bergström U, Donadi S, Erikson BDHK, Hansen J, Sundblad G (2017) Size matters: relationships between body size and body mass of common coastal aquatic invertebrates in the Baltic Sea. PeerJ 5:e2906. https://doi.org/10.7717/peerj.2906
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. https://doi.org/10.1093/icesjms/fsn048
Falini G, Albeck S, Weiner S, Addadi L (1996) Control of Aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271:67–69. https://doi.org/10.1126/science.271.5245.67
García-Huidobro MR, Aldana M, Vargas O, Pulgar J, García-Herrera C, Abarca-Ortega A, Grenier C, Rodríguez-Navarro AB, Lagos NA (2020) Geographical variability and parasitism on body size, reproduction and shell characteristics of the keyhole limpet Fissurella crassa (Mollusca: vetigastropoda). Mar Environ Res 161:e105060. https://doi.org/10.1016/j.marenvres.2020.105060
Gunderson AR, Armstrong EJ, Stillman JH (2016) Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Ann Rev Mar Sci 8:357–378. https://doi.org/10.1146/annurev-marine-122414-033953
Harper EM, Palmer TJ, Alphey JR (1997) Evolutionary response by bivalves to changing Phanerozoic sea-water chemistry. Geol Mag 134:403–407
Harper EM, Checa AG, Rodríguez-Navarro AB (2009) Organization and model of secretion of the granular prismatic microstructure of Entodesma navicular (Bivalvia: Mollusca). Acta Zool 90:132–141. https://doi.org/10.1111/j.1463-6395.2008.00338.x
Harper EM, Melody SC, Hoffman JI, Philipp ER, Peck LS, Morley SA (2012) Iceberg scour and shell damage in the Antarctic bivalve Laternula elliptica. PLoS ONE 7:e46341–e46412. https://doi.org/10.1371/journal.pone.0046341
Husmann G, Philipp E, Abele D (2016) Seasonal proliferation rates and the capacity to express genes involved in cell cycling and maintenance in response to seasonal and experimental food shortage in Laternula elliptica form King George Island. Mar Environ Res 118:57–68. https://doi.org/10.1016/j.marenvres.2016.05.003
Lagos NA, Benítez S, Duarte C, Lardies MA, Broitman BR, Tapia C, Tapia P, Widdicombe S, Vargas CA (2016) Effects of temperature and ocean acidification on shell characteristics of Argopecten purpuratus: implications for scallop aquaculture in an upwelling-influenced area. Aquacult Environ Interact 8:357–370. https://doi.org/10.3354/aei00183
Marin F, Luquet G, Marie B, Medakovic D (2008) Molluscan shell proteins: primary structure, origin, and evolution. Curr Topics Dev Biol 80:209–276. https://doi.org/10.1016/S0070-2153(07)80006-8
Marin F, Le Roy N, Marie B (2012) The formation and mineralization of mollusk shell. Front Biosci S4:1099–1125
Marin F, Bundeleva I, Takeuchi T, Immel F, Medakovic D (2016) Organic matrices in metazoan calcium carbonate skeletons: composition, functions, evolution. J Struct Biol 196:98–106. https://doi.org/10.1016/j.jsb.2016.04.006
McClintock JB, Angus RB, McDonald MR, Amsler CD, Catledge SA, Vohra YK (2009) Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification. Antart Sci 21:449–456. https://doi.org/10.1017/S0954102009990198
Meyers MA, Lin AYM, Chen PY, Muyco J (2008) Mechanical strength of abalone nacre: role of the soft organic layer. J Mech Behav Biomed 1:76–85. https://doi.org/10.1016/j.jmbbm.2007.03.001
Morley SA, Peck LS, Tan KS, Martin SM, Pörtner H-O (2007) Slowest of the slow: latitudinal insensitivity of borrowing capacity in the bivalve Laternula. Mar Biol 151:1823–1830. https://doi.org/10.1007/s00227-007-0610-7
Morley SA, Tan KS, Day RW, Martin SM, Pörtner H-O, Peck LS (2009) Thermal dependency of burrowing in three species within the bivalve genus Laternula: a latitudinal comparison. Mar Biol 156:1977–1984. https://doi.org/10.1007/s00227-009-1228-8
Nehrke G, Poigner H, Wilhelms-Dick D, Brey T, Abele D (2012) Coexistence of three calcium carbonate polymorphs in the shell of the Antarctic calm Laternula elliptica. Geochem Geophys Geosyst 13:1–8. https://doi.org/10.1029/2011GC003996
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G-K, Rodgers KB, Sabine CL, Sarmiento L, Schlitzer R, Slater RD, Totterdell IJ, Weirig M-F, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. https://doi.org/10.1038/nature04095
Palmer AR (1992) Calcification in marine molluscs: how costly is it? Proc Natl Acad Sci USA 89:1379–1382. https://doi.org/10.1073/pnas.89.4.1379
Peck LS, Pörtner H-O, Hardewing I (2002) Metabolic demand, oxygen supply, and critical temperatures in the Antarctic bivalve Laternula Elliptica. Physiol Biochem Zool 75:123–133. https://doi.org/10.1086/340990
Peck LS, Webb KE, Bailey DM (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630. https://doi.org/10.1111/j.0269-8463.2004.00903.x
Peck LS, Thorne MAS, Hoffman JI, Morley SA, Clark MS (2015) Variability among individuals is generated at the gene expression level. Ecology 96:2004–2014. https://doi.org/10.1890/14-0726.1
Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and sperm ageing on fertilization success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpets Nacella concinna. Mar Ecol Prog Ser 215:191–200. https://doi.org/10.3354/meps215191
Pulgar J, Alvarez M, Morales J, García-Huidobro M, Aldana M, Ojeda FP, Pulgar VM (2011) Impact of oceanic upwelling on morphometric and molecular indices of an intertidal fish Scartichthys viridis (Blenniidae). Mar Freshw Behav Phy 44:33–42. https://doi.org/10.1080/10236244.2010.533512
Pulgar J, Aldana M, Alvarez G-H, Molina P, Morales JP, Pulgar VM (2012) Upwelling affects food availability, impacting the morphological and molecular conditions of the herbivorous limpet Fissurella crassa (Mollusca: Archeogastropoda). J Mar Biol Ass 93:797–802. https://doi.org/10.1017/S0025315412001415
Ramajo L, Rodríguez-Navarro AB, Duarte CM, Lardies MA, Lagos NA (2015) Shifts in shell mineralogy and metabolism of Concholepas concholepas juveniles along the Chilean coast. Mar Freshwater Res 66:1147–1157. https://doi.org/10.1071/MF14232
Ramajo L, Marbá N, Prado L, Person S, Lardies MA, Rodríguez-Navarro AB, Vargas CA, Lagos NA, Duarte CM (2016) Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification. Glob Chang Biol 22:2025–2037. https://doi.org/10.1111/gcb.13179
Ramajo L, Valladares M, Astudillo O, Fernández C, Rodríguez-Navarro AB, Watt-Arévalo P, Núñez M, Grenier C, Román R, Aguayo P, Lardies MA, Broitman BR, Tapia P, Tapia C (2020) Upwelling intensity modulates the fitness and physiological performance of coastal species: implications for the aquaculture of the scallop Argopecten purpuratus in the humboldt current system. Sci Total Environ 745:e140949. https://doi.org/10.1016/j.scitotenv.2020.140949
Rodríguez-Navarro AB, Domínguez-Gasca N, Muñoz A, Ortega-Huertas M (2013) Change in the chicken addshell cuticule with then age and egg freshness. Poult Sci 92:3026–3035. https://doi.org/10.3382/ps.2013-03230
Saborowski R, Buchholz F (1996) Annual changes in the nutritive state of North Sea dab. J Fish Biol 49:173–194. https://doi.org/10.1111/j.1095-8649.1996.tb00015.x
Sato-Okoshi W, Okoshi K (2008) Characteristics of shell microstructure and growth analysis of the Antarctic bivalve Laternula elliptica from Lützow-Holm Bay, Antarctica. Polar Biol 31:131–138. https://doi.org/10.1007/s00300-007-0340-9
Savazzi E (1990) Shell biomechanics in the bivalve Laternula. Lethaia 23:93–101. https://doi.org/10.1111/j.1502-3931.1990.tb01784.x
Schmahl WW, Greisshaber E, Kelm K, Goetz A, Jordan G, Ball A, Xu D, Merkel C, Brand U (2012) Hierarchical structure of marine shell biomaterials: biomechanical functionalization of calcite by brachiopods. Z Kristallogr 227:793–804. https://doi.org/10.1524/zkri.2012.1542
Taylor JD, Glover EA, Harper EM, Crame JA, Ikebe C, Williams ST (2018) Left in the cold? Evolutionary origin of Laternula elliptica, a keystone bivalve species of Antarctic benthos. Biol J Linn Soc 123:360–376. https://doi.org/10.1093/biolinnean/blx144
West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592. https://doi.org/10.1242/jeb.01589
West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126. https://doi.org/10.1126/science.276.5309.122
Acknowledgements
We thank the members of the Chilean Antarctic Institute (INACH) station at Professor Escudero for support during the practical aspects of the work. We are also thankful to the editor, Elizabeth Harper, Roger Mann, and an anonymous review for very constructive comments on the manuscript. This work was supported by project INACH RT_ 08-16 to MAL, NAL and MJP. MAL, NAL, RGH, JFV and ARN also acknowledge the support of PIA ANID ACT-172037 for international collaborative studies. RGH acknowledges the support of ANID Grant No. PAI77190031. Further support by the ANID – Millennium Science Initiative Program – Code ICN2019_015 to MAL and NAL is greatly appreciated.
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MAL, RGH, NAL, MJP, and LR conceived and designed research. RGH, MAL, IB, CU, and CG conducted experiment and analyses. JFV, ARN contributed with analytical tools. RGH, NAL, MAL, and MJP analyzed data. RGH, MAL, NAL, and MJP wrote the manuscript. All authors read and approved the manuscript.
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Supplementary file1 (PNG 45 KB) Relation between body mass (wet tissue weight) and metabolic rate in Laternula elliptica from Fildes Bay, King George Island, Antarctic region.
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García-Huidobro, M.R., Poupin, M.J., Urrutia, C. et al. An intrapopulational study of organic compounds and biomechanical properties of the shell of the Antarctic bivalve Laternula elliptica (P. P. King, 1832) at King George Island. Polar Biol 44, 1343–1352 (2021). https://doi.org/10.1007/s00300-021-02882-9
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DOI: https://doi.org/10.1007/s00300-021-02882-9