Abstract
Fish skeletal remains recovered from two archaeological sites dated in the Middle Holocene of Tierra del Fuego (Argentina) were analysed to describe habitat use patterns by hake in the past and predict changes in a warmer world. Mitochondrial DNA was successfully extracted and amplified from 42 out of 45 first vertebra from ancient hake and phylogenetic analysis assigned all haplotypes to Argentine hake (Merluccius hubbsi). According to osteometry, the Argentine hake recovered from the archaeological site were likely adults ranging 37.2–58.1 cm in standard length. C and N stable isotope analysis showed that currently Argentine hake use foraging grounds deeper than those of Patagonian blenny and pink cusk-eel. Argentine hake, however, had a much broader isotopic niche during the Middle Holocene, when a large part of the population foraged much shallower than contemporary pink cusk-eel. The overall evidence suggests the presence of large numbers of Argentine hake onshore Tierra del Fuego during the Middle Holocene, which allowed exploitation by hunter-gatherer-fisher groups devoid of fishing technology. Interestingly, average SST off Tierra del Fuego during the Middle Holocene was higher than currently (11 °C vs 7 °C) and matched SST in the current southernmost onshore spawning aggregations, at latitude 47 °S. This indicates that increasing SST resulting from global warming will likely result into an increased abundance of adult Argentine hake onshore Tierra del Fuego, as during the Middle Holocene. Furthermore, stable isotope ratios from mollusc shells confirmed a much higher marine primary productivity during the Middle Holocene off Tierra del Fuego.
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References
Angelescu V, Prenski I (1987) Ecología trófica de la merluza común en el mar Argentino (Merluccidae, Merluccius hubbsi). Parte 2. Dinámica de la alimentación analizada sobre la base de las condiciones ambientales, la estructura y las evaluaciones de los efectivos en su área de distribución. INIDEP 561:205
Bakun A (1990) Global climate change and intensification of coastal ocean upwelling. Science 247:198–201. https://doi.org/10.1126/science.247.4939.198
Bas M, Cardona L (2018) Effects of skeletal element identity, delipidation and demineralization on the analysis of stable isotope ratios of C and N in fish bone. J Fish Biol 92:420–437. https://doi.org/10.1111/jfb.13521
Bas M, Godino IB, Álvarez M, Vales DG, Crespo EA, Cardona L (2019) Back to the future? Late Holocene marine food web structure in a warm climatic phase as a predictor of trophodynamics in a warmer South-Western Atlantic Ocean. Global Change Biol 25:404–419. https://doi.org/10.1111/gcb.14523
Belleggia M, Figueroa D, Irusta G, Bremec C (2014) Spatio-temporal and ontogenetic changes in the diet of the Argentine hake Merluccius hubbsi. J Mar Biol Assoc 94:1701–1710. https://doi.org/10.1017/S0025315414000629
Bentley MJ, Hodgson DA, Smith JA, Cofaigh CO, Domack EW, Larter RD, Roberts SJ, Brachfeld S, Lebenter A, Hjort C, Hillenbrand C-D, Evans J (2009) Mechanisms of Holocene paleoenvironmental change in the Antarctic Peninsula region. Holocene 19:51–69. https://doi.org/10.1177/0959683608096603
Bertolotti MI, Verazay GA, Errazti E, Pagani AN, Buono JJ (2001) Flota pesquera Argentina: Evolución durante el período 1960–1998, con una actualización al 2000. In: Bertolotti MI, Verazay GA, Akselman R (eds) El mar Argentino y sus recursos pesqueros. INIDEP, Mar del Plata, pp 9–53
Bezzi SI, Verazay GA, Dato CV (1995) Biology and fisheries of Argentine hakes (M. hubbsi and M. australis). In: Alheit J, Pitcher TJ (eds) Hake. Springer, Dordrecht, pp 239–267
Bolle LJ, Rijnsdorp AD, van Neer W, Millner RS, van Leeuwen PI, Ervynck A, Ayers R, Ongenae E (2004) Growth changes in plaice, cod, haddock and saithe in the North Sea: a comparison of (post-) medieval and present-day growth rates based on otolith measurements. J Sea Res 51:313–328. https://doi.org/10.1016/j.seares.2004.01.001
Boltovskoy E (1981) Masas de agua en el Atlántico Sudoccidental. In: Boltovskoy E (ed) Atlas del Zooplancton del Atlántico Sudoccidental y Métodos de Trabajo con el Zooplancton Marino. INIDEP, Mar del Plata, pp 227–237
Botto F, Gaitán E, Iribarne OO, Acha EM (2019) Trophic niche changes during settlement in the Argentine hake Merluccius hubbsi reveal the importance of pelagic food post metamorphosis. Mar Ecol Prog Ser 619:125–136. https://doi.org/10.3354/meps12947
Braje TJ, Rick TC, Szpak P, Newsome SD, McCain JM, Elliott Smith EA, Glassow M, Hamilton SL (2017) Historical ecology and the conservation of large, hermaphroditic fishes in Pacific Coast kelp forest ecosystems. Sci Adv 3:e1601759. https://doi.org/10.1126/sciadv.1601759
Bujalesky GG (2007) Coastal geomorphology and evolution of Tierra del Fuego (Southern Argentina). Geol Acta 5:337–362
Campo D, Machado-Schiaffino G, Perez J, Garcia-Vazquez E (2007) Phylogeny of the genus Merluccius based on mitochondrial and nuclear genes. Gene 406:171–179. https://doi.org/10.1016/j.gene.2007.09.008
Caniupán M, Lamy F, Lange CB, Kaiser J, Kilian R, Arz HW, León T, Mollenhauer G, Sandoval S, De Pol-Holz R, Pantoja S, Wellner J, Tiedemann R (2014) Holocene sea-surface temperature variability in the Chilean fjord region. Quat Res 82:342–353. https://doi.org/10.1016/j.yqres.2014.07.009
Cannon A (1988) Radiographic age determination of Pacific salmon: species and seasonal inferences. J Field Archaeol 15:103–108. https://doi.org/10.1179/009346988791974583
Casey MM, Post DM (2011) The problem of isotopic baseline: reconstructing the diet and trophic position of fossil animals. Earth Sci Rev 106:131–148. https://doi.org/10.1016/j.earscirev.2011.02.001
Casteel RW (1976) Fish remains in archaeology and paleo-environmental studies. Academic Press, New York
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453. https://doi.org/10.1111/j.1365-2664.2009.01620.x
Ciancio JE, Pascual MA, Botto F, Frere E, Iribarne O (2008) Trophic relationships of exotic anadromous salmonids in Southern Patagonian Shelf as inferred from stable isotopes. Limnol Oceanogr 53:788–798
Cousseau MB, Perrotta R (1998) Peces marinos de Argentina. Biología, distribución, pesca. INIDEP, Mar del Plata
DeNiro MJ (1985) Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317:806–809
Díaz de Astarloa JM, Bezzi SI, González Castro M, Mabragaña E, Hernández D, Delpiani SM, Figueroa DE, Cousseau MB, Deli Antoni MY, Tringali L (2011) Morphological, morphometric, meristic and osteological evidence for two species of hake (Actinopterygii: Gadiformes: Merluccius) in Argentinean waters. J Fish Biol 78:1336–1358. https://doi.org/10.1111/j.1095-8649.2011.02937.x
Drago M, Cardona L, Franco-Trecu V, Crespo EA, Vales D, Borella F, Zenteno L, Gonzáles EM, Inchausti P (2017) Isotopic niche partitioning between two apex predators over time. J Anim Ecol 86:766–780. https://doi.org/10.1111/1365-2656.12666
Eide M, Olsen A, Ninnemann US, Eldevik T (2017) A global estimate of the full oceanic 13C Suess effect since the preindustrial. Global Biogeochem Cycles 31:492–514. https://doi.org/10.1002/2016GB005472
Enghoff IB, MacKenzie BR, Nielsen EE (2007) The Danish fish fauna during the warm Atlantic period (ca. 7000–3900 bc): forerunner of future changes? Fish Res 87:167–180. https://doi.org/10.1016/j.fishres.2007.03.004
Evans S, Godino IB, Álvarez M, Rowsell K, Collier P, Goodall RNP, Mulville J, Lacrouts A, Collins MJ, Speller C (2016) Using combined biomolecular methods to explore whale exploitation and social aggregation in hunter-gatherer-fisher society in Tierra del Fuego. J Archaeol Sci: Rep 6:757–767. https://doi.org/10.1016/j.jasrep.2015.10.025
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509
Friedlander AM, Nowlis J, Koike H (2014) Improving fisheries assessments using historical data. In: Kittinger JN, McClenachan L, Gedan KB, Blight LK (eds) Marine historical ecology in conservation: applying the past to manage for the future. University of California Press, Berkeley, pp 91–118
Furuhashi T, Schwarzinger C, Miksik I, Smrz M, Beran A (2009) Molluscan shell evolution with review of shell calcification hypothesis. Com Biochem Physiol Part B 154:351–371. https://doi.org/10.1016/j.cbpb.2009.07.011
Gabriel S, Prista N, Costa MJ (2012) Estimating meagre (Argyrosomus regius) size from otoliths and vertebrae. J Archaeol Sci 39:2859–2865. https://doi.org/10.1016/j.jas.2012.04.046
Guiry EJ, Szpak P, Richards MP (2016) Effects of lipid extraction and ultrafiltration on stable carbon and nitrogen isotopic compositions of fish bone collagen. Rapid Commun Mass Spectrom 30:1591–1600. https://doi.org/10.1002/rcm.7590
Hall TA (2001) BioEdit: a user-friendly biological sequence alignment editor and analysis, version 5.09. North Carolina University, Chapel Hill
Hiddink JG, Ter Hofstede R (2008) Climate induced increases in species richness of marine fishes. Global Change Biol 14:453–460. https://doi.org/10.1111/j.1365-2486.2007.01518.x
Hill JM, McQuaid CD, Kaehler S (2006) Biogeographic and near-shore-offshore trends in isotope ratios of intertidal mussel beds and their food sources around the coast of southern Africa. Mar Ecol Prog Ser 318:63–73. https://doi.org/10.3354/meps318063
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528. https://doi.org/10.1126/science.1189930
Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Leniham HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. https://doi.org/10.1126/science.1059199
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
Leach F, Davidson J (2001) The use of size-frequency diagrams to characterize prehistoric fish catches and to assess human impact on inshore fisheries. Int J Osteoarchaeol 11:150–162. https://doi.org/10.1002/oa.553
Lernau O, Ben-Horin M (2016) Estimations of sizes of fish from subfossil bones with a logarithmic regression model. Environ Archaeol 21:133–136. https://doi.org/10.1080/14614103.2016.1157676
Licandeo RR, Barrientos CA, González MT (2006) Age, growth rates, sex change and feeding habits of notothenoid fish Eleginops maclovinus from the central-southern Chilean coast. Environ Biol Fishes 77:51–61. https://doi.org/10.1007/s10641-006-9054-z
Lloris D, Rucabado J (1991) Ictiofauna del Canal Beagle (Tierra del Fuego): Aspectos ecológicos y análisis biogeográfico. Publicación Especial 8. IEO, Madrid
Lloris D, Matallanas J, Oliver P (2005) Hakes of the World (Family Merlucciidae): an annotated and illustrated catalogue of hake species known to date (No. 2). FAO, Rome
Lotze HK, Erlandson JM, Hardt MJ, Norris RD, Roy K, Smith TD, Whitcraft CR (2011) Uncovering the ocean’s past. In: Jackson JBC, Alexander KE, Sala E (eds) Shifting baselines. Island Press, Washington, pp 137–161
Martin JP, Bastida R (2008) Contribución de las comunidades bentónicas en la dieta del róbalo (Eleginops maclovinus) en la ría Deseado (Santa Cruz, Argentina). Lat Am J Aquat Res 36:1–13. https://doi.org/10.4067/S0718-560X2008000100001
Misarti N, Gier E, Finney B, Barnes K, McCarthy M (2017) Compound-specific amino acid δ15N values in archaeological shell: assessing diagenetic integrity and potential for isotopic baseline reconstruction. Rapid Commun Mass Spectrom 31:1881–1891. https://doi.org/10.1002/rcm.7963
Morales A, Rosenlund K (1979) Fish bone measurements. Steenstrupia. Zoological Museum, Copenhagen
Newsome SD, Koch PL, Etnier MA, Aurioles-Gamboa D (2006) Using carbon and nitrogen isotope values to investigate maternal strategies in Northeast Pacific otariids. Mar Mammal Sci 22:556–572. https://doi.org/10.1111/j.1748-7692.2006.00043.x
Nielsen SH, Koç N, Crosta X (2004) Holocene climate in the Atlantic sector of the Southern Ocean: controlled by insolation or oceanic circulation? Geology 32:317–320. https://doi.org/10.1130/G20334.1
Pequeño G, Lamilla J, Lloris D, Rucabado J (1995) Comparación entre las ictiofaunas intermareales de los extremos austral y boreal de los canales patagónicos. Rev Biol Mar 30:155–177
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915. https://doi.org/10.1126/science.1111322
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. https://doi.org/10.1093/bioinformatics/14.9.817
Quiñones RA, Montes RM (2001) Relationship between freshwater input to the coastal zone and the historical landings of the benthic/demersal fish Eleginops maclovinus in central-south Chile. Fish Oceanogr 10:311–328
Rambaut A (2007) FigTree, a graphical viewer of phylogenetic trees. https://tree.bio.ed.ac.uk/software/figtree. Accessed 3 Dec 2018
Riccialdelli L, Newsome SD, Fogel ML, Fernández DA (2017) Trophic interactions and food web structure of a subantarctic marine food web in the Beagle Channel: Bahía Lapataia, Argentina. Polar Biol 40:807–821. https://doi.org/10.1007/s00300-016-2007-x
Rivas AL (2010) Spatial and temporal variability of satellite-derived sea surface temperature in the southwestern Atlantic Ocean. Cont Shelf Res 30:752–760. https://doi.org/10.1016/j.csr.2010.01.009
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Salemme M, Bujalesky G, Santiago F (2007) La Arcillosa 2: la ocupación humana durante el Holoceno medio en el Rió Chico, Tierra del Fuego, Argentina. In: Morello F, Martinic M, Prieto A, Bahamonde G (eds) Arqueologiá de Fuego-Patagonia: levantando Piedras, Desenterrando huesos... y Develando Arcanos. Ediciones CEQUA, Punta Arenas, pp 723–736
Salemme MC, Santiago FC, Oria J (2014) La Arcillosa 2: Registro Zooarqueológico de la Ocupación Humana durante el Holoceno Medio, Tierra del Fuego, Argentina. Rev Chil Antrop 29:19–25. https://doi.org/10.5354/0719-1472.2015.36201
Santiago FC (2013) La ocupación humana del norte de Tierra del Fuego durante el Holoceno medio y tardío: su vinculación con el paisaje. Editora Cultural Tierra del Fuego, Ushuaia
Santiago F, Gordillo S, Salemme M (2014) Moluscos en contextos arqueológicos de la costa Atlántica de Tierra del Fuego: Consumo prehistórico e implicancias de su distribución actual. Rev Chil Antrop 29:40–48. https://doi.org/10.5354/0719-1472.2015.36204
Saporiti F, Bala LO, Gómez Otero J, Crespo EA, Piana EL, Aguilar A, Cardona L (2014b) Paleoindian pinniped exploitation in South America was driven by oceanic productivity. Quat Int 352:85–91. https://doi.org/10.1016/j.quaint.2014.05.015
Saporiti F, Bearhop S, Silva L, Vales DG, Zenteno L, Crespo EA, Aguilar A, Cardona L (2014a) Longer and less overlapping food webs in anthropogenically disturbed marine ecosystems: confirmations from the past. PLoS ONE 9:e103132. https://doi.org/10.1371/journal.pone.0103132
Scartascini FL, Volpedo AV (2013) White croaker (Micropogonias furnieri) paleodistribution in the Southwestern Atlantic Ocean. An archaeological perspective. J Archaeol Sci 40:1059–1066. https://doi.org/10.1016/j.jas.2012.08.032
Shevenell AE, Ingalls AE, Domack EW, Kelly C (2011) Holocene Southern Ocean surface temperature variability west of the Antarctic Peninsula. Nature 470:250–254
Simpson SD, Jennings S, Johnson MP, Blanchard JL, Schön PJ, Sims DW, Genner MJ (2011) Continental shelf-wide response of a fish assemblage to rapid warming of the sea. Curr Biol 21:1565–1570. https://doi.org/10.1016/j.cub.2011.08.016
Skrzypek G (2013) Normalization procedures and reference material selection in stable HCNOS isotope analyses: an overview. Anal Bioanal Chem 405:2815–2823
Smith P (1995) A regression equation to determine the total length of hake (Merluccius merluccius) from selected measurements of the bones. Int J Osteoarchaeol 5:93–95. https://doi.org/10.1002/oa.1390050110
Speller CF, Hauser L, Lepofsky D, Moore J, Rodrigues AT, Moss ML, McKechnie I, Yang DY (2012) High potential for using DNA from ancient herring bones to inform modern fisheries management and conservation. PLoS ONE 7:e51122. https://doi.org/10.1371/journal.pone.0051122
Swetnam TW, Allen CD, Betancourt JL (1999) Applied historical ecology: using the past to manage for the future. Ecol Appl 9:1189–1206. https://doi.org/10.1890/1051-0761(1999)009[1189:AHEUTP]2.0.CO;2
Sydeman WJ, García-Reyes M, Schoeman DS, Rykaczewski RR, Thompson SA, Black BA, Bograd SJ (2014) Climate change and wind intensification in coastal upwelling ecosystems. Science 345:77–80. https://doi.org/10.1126/science.1251635
Szpak P, Buckley M, Darwent CM, Richards MP (2018) Long-term ecological changes in marine mammals driven by recent warming in northwestern Alaska. Global Change Biol 24:490–503. https://doi.org/10.1111/gcb.13880
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Torres J (2009) La pesca entre los cazadores recolectores terrestres de la Isla Grande de Tierra del Fuego, desde la prehistoria a tiempos etnográficos. Magallania 37:109–138. https://doi.org/10.4067/S0718-22442009000200007
Vales DG, Cardona L, Zangrando AF, Borella F, Saporiti F, Goodall RNP, de Oliveira LR, Crespo EA (2017) Holocene changes in the trophic ecology of an apex marine predator in the South Atlantic Ocean. Oecologia 183:555–570. https://doi.org/10.1007/s00442-016-3781-4
Villarino MF (1998) Distribución estacional y estructura de tallas del abadejo (Genypterus blacodes) en el Mar Argentino. INIDEP, Mar del Plata, pp 1–25
Yang DY, Eng B, Waye JS, Dudar JC, Saunders SR (1998) Improved DNA extraction from ancient bones using silica-based spin columns. Am J Phys Anthropol 105:539–543. https://doi.org/10.1002/(SICI)1096-8644(199804)105:4%3C539:AID-AJPA10%3E3.0.CO;2-1
Yang DY, Cannon A, Saunders SR (2004) DNA species identification of archaeological salmon bone from the Pacific Northwest Coast of North America. J Archaeol Sci 31:619–631. https://doi.org/10.1016/j.jas.2003.10.008
Yang DY, Liu L, Chen X, Speller CF (2008) Wild or domesticated: DNA analysis of ancient water buffalo remains from north China. J Archaeol Sci 35:2778–2785. https://doi.org/10.1016/j.jas.2008.05.010
Zangrando AF, Riccialdelli L, Kochi S, Nye JW, Tessone A (2016) Stable isotope evidence supports pelagic fishing by hunter-gatherers in southern South America during the Late Holocene. J Archaeol Sci Rep 8:486–491. https://doi.org/10.1016/j.jasrep.2016.05.015
Zenteno L, Borella F, Gómez Otero J, Piana E, Belardi JB, Borrero LA, Saporiti F, Cardona L, Crespo EA (2015) Shifting niches of marine predators due to human exploitation: the diet of the South American sea lion (Otaria flavescens) since the late Holocene as a case study. Paleobiology 41:387–401. https://doi.org/10.1017/pab.2015.9
Acknowledgements
Special thanks are due to Matias Pardo from San Arawa fishing company for his help in obtaining modern Southern hake samples. We acknowledge Dr. Begoña López Arias, Universidad Autónoma de Madrid, for her assistance in designing and testing the genetic primers. We are very grateful to Pilar Rubio who helped us with isotopic analyses at Centres Científics i Tecnològics de la Universitat de Barcelona (Barcelona, Spain). Two anonymous reviewers and the handling editor highly improved a previous version of the manuscript with their suggestions. The ancient genetic analysis was supported by the UK Arts and Humanities Research Council (Grant number AH/N005015/1) and the Leverhulme Trust (through a Philip Leverhulme Prize to CS). This paper was also supported by the following projects: PIP CONICET 0409-13 and PICT 2012-1944 to MS. MB has participated in this work with the support of a doctoral fellowship funded by CONICET for the completion of a PhD in Biological Sciences at Universidad Nacional de Mar del Plata. All the biological samples included on this paper are obtained, transported and analysed following the legal terms and conditions of the Argentine Government (MTA 19/10/2017).
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MB, MA, IBG and LC conceived and designed the study. MS and FS conducted the field work. MB, EG, CS and LC conducted laboratory analysis and data analysis. MB and LC wrote the first draft of the manuscript. Other authors provided editorial advice and contributed to revisions.
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Bas, M., Salemme, M., Green, E.J. et al. Predicting habitat use by the Argentine hake Merluccius hubbsi in a warmer world: inferences from the Middle Holocene. Oecologia 193, 461–474 (2020). https://doi.org/10.1007/s00442-020-04667-z
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DOI: https://doi.org/10.1007/s00442-020-04667-z